Arrest and Attack: Microtubule-Targeting Agents and Oncolytic Viruses Employ Complementary Mechanisms to Enhance Anti-Tumor Therapy Efficacy
Abstract
:1. Introduction
2. The Combination Factors: Oncolytic Viruses and Microtubule-Targeting Agents
2.1. Oncolytic Viruses and Their Exploitation of the Cancer-Cell Context
2.2. Microtubule Targeting Agents as Modifiers in the Cancer-Cell Context
3. Testing of OV–MTA Combinations
4. Concluding Remarks
Author Contributions
Funding
Conflicts of Interest
References
- Jin, H.; Wang, L.; Bernards, R. Rational combinations of targeted cancer therapies: Background, advances and challenges. Nat. Rev. Drug Discov. 2023, 22, 213–234. [Google Scholar] [CrossRef] [PubMed]
- Hanahan, D.; Weinberg, R.A. Hallmarks of cancer: The next generation. Cell 2011, 144, 646–674. [Google Scholar] [CrossRef] [PubMed]
- Aaltonen, L.A.; Abascal, F.; Abeshouse, A.; Aburatani, H.; Adams, D.J.; Agrawal, N.; Ahn, K.S.; Ahn, S.-M.; Aikata, H.; Akbani, R.; et al. Pan-cancer analysis of whole genomes. Nature 2020, 578, 82–93. [Google Scholar] [CrossRef]
- Dentro, S.C.; Leshchiner, I.; Haase, K.; Tarabichi, M.; Wintersinger, J.; Deshwar, A.G.; Yu, K.; Rubanova, Y.; Macintyre, G.; Demeulemeester, J.; et al. Characterizing genetic intra-tumor heterogeneity across 2,658 human cancer genomes. Cell 2021, 184, 2239–2254.e2239. [Google Scholar] [CrossRef] [PubMed]
- Flaherty, K.T.; Gray, R.; Chen, A.; Li, S.; Patton, D.; Hamilton, S.R.; Williams, P.M.; Mitchell, E.P.; Iafrate, A.J.; Sklar, J.; et al. The Molecular Analysis for Therapy Choice (NCI-MATCH) Trial: Lessons for Genomic Trial Design. J. Natl. Cancer Inst. 2020, 112, 1021–1029. [Google Scholar] [CrossRef]
- Hainsworth, J.D.; Meric-Bernstam, F.; Swanton, C.; Hurwitz, H.; Spigel, D.R.; Sweeney, C.; Burris, H.; Bose, R.; Yoo, B.; Stein, A.; et al. Targeted Therapy for Advanced Solid Tumors on the Basis of Molecular Profiles: Results From MyPathway, an Open-Label, Phase IIa Multiple Basket Study. J. Clin. Oncol. 2018, 36, 536–542. [Google Scholar] [CrossRef]
- Ehrlich, M.; Bacharach, E. Oncolytic Virotherapy: The Cancer Cell Side. Cancers 2021, 13, 939. [Google Scholar] [CrossRef]
- Li, K.; Zhao, Y.; Hu, X.; Jiao, J.; Wang, W.; Yao, H. Advances in the clinical development of oncolytic viruses. Am. J. Transl. Res. 2022, 14, 4192–4206. [Google Scholar]
- Duan, S.; Wang, S.; Qiao, L.; Yu, X.; Wang, N.; Chen, L.; Zhang, X.; Zhao, X.; Liu, H.; Wang, T.; et al. Oncolytic Virus-Driven Biotherapies from Bench to Bedside. Small 2023, 19, e2206948. [Google Scholar] [CrossRef]
- Shalhout, S.Z.; Miller, D.M.; Emerick, K.S.; Kaufman, H.L. Therapy with oncolytic viruses: Progress and challenges. Nat. Rev. Clin. Oncol. 2023, 20, 160–177. [Google Scholar] [CrossRef]
- Hardcastle, J.; Kurozumi, K.; Chiocca, E.A.; Kaur, B. Oncolytic viruses driven by tumor-specific promoters. Curr. Cancer Drug Targets 2007, 7, 181–189. [Google Scholar] [CrossRef] [PubMed]
- Cafferata, E.G.; Macció, D.R.; Lopez, M.V.; Viale, D.L.; Carbone, C.; Mazzolini, G.; Podhajcer, O.L. A novel A33 promoter-based conditionally replicative adenovirus suppresses tumor growth and eradicates hepatic metastases in human colon cancer models. Clin. Cancer Res. 2009, 15, 3037–3049. [Google Scholar] [CrossRef] [PubMed]
- Weber, H.L.; Gidekel, M.; Werbajh, S.; Salvatierra, E.; Rotondaro, C.; Sganga, L.; Haab, G.A.; Curiel, D.T.; Cafferata, E.G.; Podhajcer, O.L. A Novel CDC25B Promoter-Based Oncolytic Adenovirus Inhibited Growth of Orthotopic Human Pancreatic Tumors in Different Preclinical Models. Clin. Cancer Res. 2015, 21, 1665–1674. [Google Scholar] [CrossRef] [PubMed]
- Danziger, O.; Shai, B.; Sabo, Y.; Bacharach, E.; Ehrlich, M. Combined genetic and epigenetic interferences with interferon signaling expose prostate cancer cells to viral infection. Oncotarget 2016, 7, 52115–52134. [Google Scholar] [CrossRef]
- Danziger, O.; Pupko, T.; Bacharach, E.; Ehrlich, M. Interleukin-6 and Interferon-alpha Signaling via JAK1-STAT Differentially Regulate Oncolytic versus Cytoprotective Antiviral States. Front. Immunol. 2018, 9, 94. [Google Scholar] [CrossRef]
- Dellac, S.; Ben-Dov, H.; Raanan, A.; Saleem, H.; Zamostiano, R.; Semyatich, R.; Lavi, S.; Witz, I.P.; Bacharach, E.; Ehrlich, M. Constitutive low expression of antiviral effectors sensitizes melanoma cells to a novel oncolytic virus. Int. J. Cancer 2021, 148, 2321–2334. [Google Scholar] [CrossRef]
- Stojdl, D.F.; Lichty, B.; Knowles, S.; Marius, R.; Atkins, H.; Sonenberg, N.; Bell, J.C. Exploiting tumor-specific defects in the interferon pathway with a previously unknown oncolytic virus. Nat. Med. 2000, 6, 821–825. [Google Scholar] [CrossRef]
- Dunn, G.P.; Sheehan, K.C.; Old, L.J.; Schreiber, R.D. IFN unresponsiveness in LNCaP cells due to the lack of JAK1 gene expression. Cancer Res. 2005, 65, 3447–3453. [Google Scholar] [CrossRef]
- Noser, J.A.; Mael, A.A.; Sakuma, R.; Ohmine, S.; Marcato, P.; Lee, P.W.; Ikeda, Y. The RAS/Raf1/MEK/ERK signaling pathway facilitates VSV-mediated oncolysis: Implication for the defective interferon response in cancer cells. Mol. Ther. 2007, 15, 1531–1536. [Google Scholar] [CrossRef]
- Zhang, K.X.; Matsui, Y.; Hadaschik, B.A.; Lee, C.; Jia, W.; Bell, J.C.; Fazli, L.; So, A.I.; Rennie, P.S. Down-regulation of type I interferon receptor sensitizes bladder cancer cells to vesicular stomatitis virus-induced cell death. Int. J. Cancer 2010, 127, 830–838. [Google Scholar] [CrossRef]
- Komatsu, Y.; Christian, S.L.; Ho, N.; Pongnopparat, T.; Licursi, M.; Hirasawa, K. Oncogenic Ras inhibits IRF1 to promote viral oncolysis. Oncogene 2015, 34, 3985–3993. [Google Scholar] [CrossRef] [PubMed]
- Pikor, L.A.; Bell, J.C.; Diallo, J.S. Oncolytic Viruses: Exploiting Cancer’s Deal with the Devil. Trends Cancer 2015, 1, 266–277. [Google Scholar] [CrossRef] [PubMed]
- Huang, P.Y.; Guo, J.H.; Hwang, L.H. Oncolytic Sindbis virus targets tumors defective in the interferon response and induces significant bystander antitumor immunity in vivo. Mol. Ther. 2012, 20, 298–305. [Google Scholar] [CrossRef] [PubMed]
- Allagui, F.; Achard, C.; Panterne, C.; Combredet, C.; Labarrière, N.; Dréno, B.; Elgaaied, A.B.; Pouliquen, D.; Tangy, F.; Fonteneau, J.F.; et al. Modulation of the Type I Interferon Response Defines the Sensitivity of Human Melanoma Cells to Oncolytic Measles Virus. Curr. Gene Ther. 2017, 16, 419–428. [Google Scholar] [CrossRef] [PubMed]
- Delaunay, T.; Achard, C.; Boisgerault, N.; Grard, M.; Petithomme, T.; Chatelain, C.; Dutoit, S.; Blanquart, C.; Royer, P.J.; Minvielle, S.; et al. Frequent Homozygous Deletions of Type I Interferon Genes in Pleural Mesothelioma Confer Sensitivity to Oncolytic Measles Virus. J. Thorac. Oncol. 2020, 15, 827–842. [Google Scholar] [CrossRef]
- Barer, L.; Schröder, S.K.; Weiskirchen, R.; Bacharach, E.; Ehrlich, M. Lipocalin-2 regulates the expression of interferon-stimulated genes and the susceptibility of prostate cancer cells to oncolytic virus infection. Eur. J. Cell Biol. 2023, 102, 151328. [Google Scholar] [CrossRef]
- Dunn, G.P.; Koebel, C.M.; Schreiber, R.D. Interferons, immunity and cancer immunoediting. Nat. Rev. Immunol. 2006, 6, 836–848. [Google Scholar] [CrossRef]
- Tshering, L.F.; Luo, F.; Russ, S.; Szenk, M.; Rubel, D.; Tutuska, K.; Rail, J.G.; Balázsi, G.; Shen, M.M.; Talos, F. Immune mechanisms shape the clonal landscape during early progression of prostate cancer. Dev. Cell 2023, 58, 1071–1086.e1078. [Google Scholar] [CrossRef]
- Martínez-Sabadell, A.; Arenas, E.J.; Arribas, J. IFNγ Signaling in Natural and Therapy-Induced Antitumor Responses. Clin. Cancer Res. 2022, 28, 1243–1249. [Google Scholar] [CrossRef]
- von Locquenghien, M.; Rozalén, C.; Celià-Terrassa, T. Interferons in cancer immunoediting: Sculpting metastasis and immunotherapy response. J. Clin. Investig. 2021, 131. [Google Scholar] [CrossRef]
- Lawson, K.A.; Sousa, C.M.; Zhang, X.; Kim, E.; Akthar, R.; Caumanns, J.J.; Yao, Y.; Mikolajewicz, N.; Ross, C.; Brown, K.R.; et al. Functional genomic landscape of cancer-intrinsic evasion of killing by T cells. Nature 2020, 586, 120–126. [Google Scholar] [CrossRef] [PubMed]
- Katlinski, K.V.; Gui, J.; Katlinskaya, Y.V.; Ortiz, A.; Chakraborty, R.; Bhattacharya, S.; Carbone, C.J.; Beiting, D.P.; Girondo, M.A.; Peck, A.R.; et al. Inactivation of Interferon Receptor Promotes the Establishment of Immune Privileged Tumor Microenvironment. Cancer Cell 2017, 31, 194–207. [Google Scholar] [CrossRef] [PubMed]
- Katlinskaya, Y.V.; Katlinski, K.V.; Yu, Q.; Ortiz, A.; Beiting, D.P.; Brice, A.; Davar, D.; Sanders, C.; Kirkwood, J.M.; Rui, H.; et al. Suppression of Type I Interferon Signaling Overcomes Oncogene-Induced Senescence and Mediates Melanoma Development and Progression. Cell Rep. 2016, 15, 171–180. [Google Scholar] [CrossRef] [PubMed]
- Klampfer, L.; Huang, J.; Corner, G.; Mariadason, J.; Arango, D.; Sasazuki, T.; Shirasawa, S.; Augenlicht, L. Oncogenic Ki-ras inhibits the expression of interferon-responsive genes through inhibition of STAT1 and STAT2 expression. J. Biol. Chem. 2003, 278, 46278–46287. [Google Scholar] [CrossRef]
- Kriegsman, B.A.; Vangala, P.; Chen, B.J.; Meraner, P.; Brass, A.L.; Garber, M.; Rock, K.L. Frequent Loss of IRF2 in Cancers Leads to Immune Evasion through Decreased MHC Class I Antigen Presentation and Increased PD-L1 Expression. J. Immunol. 2019, 203, 1999–2010. [Google Scholar] [CrossRef]
- Kulaeva, O.I.; Draghici, S.; Tang, L.; Kraniak, J.M.; Land, S.J.; Tainsky, M.A. Epigenetic silencing of multiple interferon pathway genes after cellular immortalization. Oncogene 2003, 22, 4118–4127. [Google Scholar] [CrossRef]
- Lee, K.Y.; Geng, H.; Ng, K.M.; Yu, J.; van Hasselt, A.; Cao, Y.; Zeng, Y.X.; Wong, A.H.Y.; Wang, X.; Ying, J.; et al. Epigenetic disruption of interferon-γ response through silencing the tumor suppressor interferon regulatory factor 8 in nasopharyngeal, esophageal and multiple other carcinomas. Oncogene 2008, 27, 5267–5276. [Google Scholar] [CrossRef]
- Li, Q.; Tainsky, M.A. Epigenetic silencing of IRF7 and/or IRF5 in lung cancer cells leads to increased sensitivity to oncolytic viruses. PLoS ONE 2011, 6, e28683. [Google Scholar] [CrossRef]
- Li, S.; Zhu, M.; Pan, R.; Fang, T.; Cao, Y.Y.; Chen, S.; Zhao, X.; Lei, C.Q.; Guo, L.; Chen, Y.; et al. The tumor suppressor PTEN has a critical role in antiviral innate immunity. Nat. Immunol. 2016, 17, 241–249. [Google Scholar] [CrossRef]
- Lin, L.; Su, Z.; Lebedeva, I.V.; Gupta, P.; Boukerche, H.; Rai, T.; Barber, G.N.; Dent, P.; Sarkar, D.; Fisher, P.B. Activation of Ras/Raf protects cells from melanoma differentiation-associated gene-5-induced apoptosis. Cell Death Differ. 2006, 13, 1982–1993. [Google Scholar] [CrossRef]
- Luo, N.; Nixon, M.J.; Gonzalez-Ericsson, P.I.; Sanchez, V.; Opalenik, S.R.; Li, H.; Zahnow, C.A.; Nickels, M.L.; Liu, F.; Tantawy, M.N.; et al. DNA methyltransferase inhibition upregulates MHC-I to potentiate cytotoxic T lymphocyte responses in breast cancer. Nat. Commun. 2018, 9, 248. [Google Scholar] [CrossRef] [PubMed]
- Stone, M.L.; Chiappinelli, K.B.; Li, H.; Murphy, L.M.; Travers, M.E.; Topper, M.J.; Mathios, D.; Lim, M.; Shih, I.M.; Wang, T.L.; et al. Epigenetic therapy activates type I interferon signaling in murine ovarian cancer to reduce immunosuppression and tumor burden. Proc. Natl. Acad. Sci. USA 2017, 114, E10981–E10990. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Q.; Gong, R.; Qu, J.; Zhou, Y.; Liu, W.; Chen, M.; Liu, Y.; Zhu, Y.; Wu, J. Activation of the Ras/Raf/MEK Pathway Facilitates Hepatitis C Virus Replication via Attenuation of the Interferon-JAK-STAT Pathway. J. Virol. 2012, 86, 1544–1554. [Google Scholar] [CrossRef] [PubMed]
- Pol, J.G.; Workenhe, S.T.; Konda, P.; Gujar, S.; Kroemer, G. Cytokines in oncolytic virotherapy. Cytokine Growth Factor Rev. 2020, 56, 4–27. [Google Scholar] [CrossRef]
- LaRocca, C.J.; Warner, S.G. Oncolytic viruses and checkpoint inhibitors: Combination therapy in clinical trials. Clin. Transl. Med. 2018, 7, 35. [Google Scholar] [CrossRef]
- Puzanov, I.; Milhem, M.M.; Minor, D.; Hamid, O.; Li, A.; Chen, L.; Chastain, M.; Gorski, K.S.; Anderson, A.; Chou, J.; et al. Talimogene Laherparepvec in Combination With Ipilimumab in Previously Untreated, Unresectable Stage IIIB-IV Melanoma. J. Clin. Oncol. 2016, 34, 2619–2626. [Google Scholar] [CrossRef]
- Samson, A.; Scott, K.J.; Taggart, D.; West, E.J.; Wilson, E.; Nuovo, G.J.; Thomson, S.; Corns, R.; Mathew, R.K.; Fuller, M.J.; et al. Intravenous delivery of oncolytic reovirus to brain tumor patients immunologically primes for subsequent checkpoint blockade. Sci. Transl. Med. 2018, 10, eaam7577. [Google Scholar] [CrossRef]
- Shen, Y.; Song, W.; Lin, D.; Zhang, X.; Wang, M.; Li, Y.; Yang, Z.; Guo, S.; Wang, Z.; Sheng, J.; et al. VG161 activates systemic antitumor immunity in pancreatic cancer models as a novel oncolytic herpesvirus expressing multiple immunomodulatory transgenes. J. Med. Virol. 2023, 95, e28108. [Google Scholar] [CrossRef]
- Kim, S.I.; Park, A.K.; Chaurasiya, S.; Kang, S.; Lu, J.; Yang, A.; Sivanandam, V.; Zhang, Z.; Woo, Y.; Priceman, S.J.; et al. Recombinant Orthopoxvirus Primes Colon Cancer for Checkpoint Inhibitor and Cross-Primes T Cells for Antitumor and Antiviral Immunity. Mol. Cancer Ther. 2021, 20, 173–182. [Google Scholar] [CrossRef]
- Zuo, S.; Wei, M.; Xu, T.; Kong, L.; He, B.; Wang, S.; Wang, S.; Wu, J.; Dong, J.; Wei, J. An engineered oncolytic vaccinia virus encoding a single-chain variable fragment against TIGIT induces effective antitumor immunity and synergizes with PD-1 or LAG-3 blockade. J. Immunother. Cancer 2021, 9, e002843. [Google Scholar] [CrossRef]
- Chesney, J.A.; Ribas, A.; Long, G.V.; Kirkwood, J.M.; Dummer, R.; Puzanov, I.; Hoeller, C.; Gajewski, T.F.; Gutzmer, R.; Rutkowski, P.; et al. Randomized, Double-Blind, Placebo-Controlled, Global Phase III Trial of Talimogene Laherparepvec Combined With Pembrolizumab for Advanced Melanoma. J. Clin. Oncol. 2023, 41, 528–540. [Google Scholar] [CrossRef] [PubMed]
- Kelly, C.M.; Antonescu, C.R.; Bowler, T.; Munhoz, R.; Chi, P.; Dickson, M.A.; Gounder, M.M.; Keohan, M.L.; Movva, S.; Dholakia, R.; et al. Objective Response Rate Among Patients With Locally Advanced or Metastatic Sarcoma Treated With Talimogene Laherparepvec in Combination With Pembrolizumab: A Phase 2 Clinical Trial. JAMA Oncol. 2020, 6, 402–408. [Google Scholar] [CrossRef]
- Gilchrist, V.H.; Jémus-Gonzalez, E.; Said, A.; Alain, T. Kinase inhibitors with viral oncolysis: Unmasking pharmacoviral approaches for cancer therapy. Cytokine Growth Factor Rev. 2020, 56, 83–93. [Google Scholar] [CrossRef] [PubMed]
- Liang, M. Oncorine, the World First Oncolytic Virus Medicine and its Update in China. Curr. Cancer Drug Targets 2018, 18, 171–176. [Google Scholar] [CrossRef] [PubMed]
- Poh, A. First Oncolytic Viral Therapy for Melanoma. Cancer Discov. 2016, 6, 6. [Google Scholar] [CrossRef]
- Hanahan, D.; Weinberg, R.A. The hallmarks of cancer. Cell 2000, 100, 57–70. [Google Scholar] [CrossRef]
- Hanahan, D. Hallmarks of Cancer: New Dimensions. Cancer Discov. 2022, 12, 31–46. [Google Scholar] [CrossRef]
- Schiff, P.B.; Fant, J.; Horwitz, S.B. Promotion of microtubule assembly in vitro by taxol. Nature 1979, 277, 665–667. [Google Scholar] [CrossRef]
- Noble, R.L.; Beer, C.T.; Cutts, J.H. Role of chance observations in chemotherapy: Vinca rosea. Ann. N. Y. Acad. Sci. 1958, 76, 882–894. [Google Scholar] [CrossRef]
- Dumontet, C.; Jordan, M.A. Microtubule-binding agents: A dynamic field of cancer therapeutics. Nat. Rev. Drug Discov. 2010, 9, 790–803. [Google Scholar] [CrossRef]
- Lao, K.; Wang, Y.; Chen, M.; Zhang, J.; You, Q.; Xiang, H. Design, synthesis and biological evaluation of novel 2-methoxyestradiol analogs as dual selective estrogen receptor modulators (SERMs) and antiangiogenic agents. Eur. J. Med. Chem. 2017, 139, 390–400. [Google Scholar] [CrossRef] [PubMed]
- D’Amato, R.J.; Lin, C.M.; Flynn, E.; Folkman, J.; Hamel, E. 2-Methoxyestradiol, an endogenous mammalian metabolite, inhibits tubulin polymerization by interacting at the colchicine site. Proc. Natl. Acad. Sci. USA 1994, 91, 3964–3968. [Google Scholar] [CrossRef] [PubMed]
- Steinmetz, M.O.; Prota, A.E. Microtubule-Targeting Agents: Strategies To Hijack the Cytoskeleton. Trends Cell Biol. 2018, 28, 776–792. [Google Scholar] [CrossRef] [PubMed]
- Yvon, A.M.; Wadsworth, P.; Jordan, M.A. Taxol suppresses dynamics of individual microtubules in living human tumor cells. Mol. Biol. Cell 1999, 10, 947–959. [Google Scholar] [CrossRef]
- Gascoigne, K.E.; Taylor, S.S. How do anti-mitotic drugs kill cancer cells? J. Cell Sci. 2009, 122, 2579–2585. [Google Scholar] [CrossRef]
- Ireson, C.R.; Chander, S.K.; Purohit, A.; Perera, S.; Newman, S.P.; Parish, D.; Leese, M.P.; Smith, A.C.; Potter, B.V.; Reed, M.J. Pharmacokinetics and efficacy of 2-methoxyoestradiol and 2-methoxyoestradiol-bis-sulphamate in vivo in rodents. Br. J. Cancer 2004, 90, 932–937. [Google Scholar] [CrossRef]
- Bruggemann, E.P.; Currier, S.J.; Gottesman, M.M.; Pastan, I. Characterization of the azidopine and vinblastine binding site of P-glycoprotein. J. Biol. Chem. 1992, 267, 21020–21026. [Google Scholar] [CrossRef]
- Breuninger, L.M.; Paul, S.; Gaughan, K.; Miki, T.; Chan, A.; Aaronson, S.A.; Kruh, G.D. Expression of multidrug resistance-associated protein in NIH/3T3 cells confers multidrug resistance associated with increased drug efflux and altered intracellular drug distribution. Cancer Res. 1995, 55, 5342–5347. [Google Scholar]
- Hopper-Borge, E.; Chen, Z.S.; Shchaveleva, I.; Belinsky, M.G.; Kruh, G.D. Analysis of the drug resistance profile of multidrug resistance protein 7 (ABCC10): Resistance to docetaxel. Cancer Res. 2004, 64, 4927–4930. [Google Scholar] [CrossRef]
- Huisman, M.T.; Chhatta, A.A.; van Tellingen, O.; Beijnen, J.H.; Schinkel, A.H. MRP2 (ABCC2) transports taxanes and confers paclitaxel resistance and both processes are stimulated by probenecid. Int. J. Cancer 2005, 116, 824–829. [Google Scholar] [CrossRef]
- Schumacher, G.; Hoffmann, J.; Cramer, T.; Spinelli, A.; Jacob, D.; Bahra, M.; Pratschke, J.; Pfitzmann, R.; Schmidt, S.; Lage, H. Antineoplastic activity of 2-methoxyestradiol in human pancreatic and gastric cancer cells with different multidrug-resistant phenotypes. J. Gastroenterol. Hepatol. 2007, 22, 1469–1473. [Google Scholar] [CrossRef] [PubMed]
- Crombag, M.-R.B.S.; Koolen, S.L.W.; Wijngaard, S.; Joerger, M.; Dorlo, T.P.C.; van Erp, N.P.; Mathijssen, R.H.J.; Beijnen, J.H.; Huitema, A.D.R. Does Older Age Lead to Higher Risk for Neutropenia in Patients Treated with Paclitaxel? Pharm. Res. 2019, 36, 163. [Google Scholar] [CrossRef] [PubMed]
- Escuin, D.; Burke, P.A.; McMahon-Tobin, G.; Hembrough, T.; Wang, Y.; Alcaraz, A.A.; Leandro-García, L.J.; Rodríguez-Antona, C.; Snyder, J.P.; Lavallee, T.M.; et al. The hematopoietic-specific beta1-tubulin is naturally resistant to 2-methoxyestradiol and protects patients from drug-induced myelosuppression. Cell Cycle 2009, 8, 3914–3924. [Google Scholar] [CrossRef] [PubMed]
- Strieth, S.; Eichhorn, M.E.; Sauer, B.; Schulze, B.; Teifel, M.; Michaelis, U.; Dellian, M. Neovascular targeting chemotherapy: Encapsulation of paclitaxel in cationic liposomes impairs functional tumor microvasculature. Int. J. Cancer 2004, 110, 117–124. [Google Scholar] [CrossRef]
- Mabjeesh, N.J.; Escuin, D.; LaVallee, T.M.; Pribluda, V.S.; Swartz, G.M.; Johnson, M.S.; Willard, M.T.; Zhong, H.; Simons, J.W.; Giannakakou, P. 2ME2 inhibits tumor growth and angiogenesis by disrupting microtubules and dysregulating HIF. Cancer Cell 2003, 3, 363–375. [Google Scholar] [CrossRef]
- Vennin, C.; Cattaneo, C.M.; Bosch, L.; Vegna, S.; Ma, X.; Damstra, H.G.J.; Martinovic, M.; Tsouri, E.; Ilic, M.; Azarang, L.; et al. Taxanes trigger cancer cell killing in vivo by inducing non-canonical T cell cytotoxicity. Cancer Cell 2023, 41, 1170–1185.e1112. [Google Scholar] [CrossRef]
- Shand, F.H.; Langenbach, S.Y.; Keenan, C.R.; Ma, S.P.; Wheaton, B.J.; Schuliga, M.J.; Ziogas, J.; Stewart, A.G. In vitro and in vivo evidence for anti-inflammatory properties of 2-methoxyestradiol. J. Pharmacol. Exp. Ther. 2011, 336, 962–972. [Google Scholar] [CrossRef]
- Huerta-Yepez, S.; Baay-Guzman, G.J.; Garcia-Zepeda, R.; Hernandez-Pando, R.; Vega, M.I.; Gonzalez-Bonilla, C.; Bonavida, B. 2-Methoxyestradiol (2-ME) reduces the airway inflammation and remodeling in an experimental mouse model. Clin. Immunol. 2008, 129, 313–324. [Google Scholar] [CrossRef]
- Plum, S.M.; Park, E.J.; Strawn, S.J.; Moore, E.G.; Sidor, C.F.; Fogler, W.E. Disease modifying and antiangiogenic activity of 2-methoxyestradiol in a murine model of rheumatoid arthritis. BMC Musculoskelet. Disord. 2009, 10, 46. [Google Scholar] [CrossRef]
- Hirschhorn, T.; Barizilay, L.; Smorodinsky, N.I.; Ehrlich, M. Differential regulation of Smad3 and of the type II transforming growth factor-beta receptor in mitosis: Implications for signaling. PLoS ONE 2012, 7, e43459. [Google Scholar] [CrossRef]
- Chetrit, D.; Barzilay, L.; Horn, G.; Bielik, T.; Smorodinsky, N.I.; Ehrlich, M. Negative regulation of the endocytic adaptor disabled-2 (Dab2) in mitosis. J. Biol. Chem. 2011, 286, 5392–5403. [Google Scholar] [CrossRef] [PubMed]
- Boucrot, E.; Howes, M.T.; Kirchhausen, T.; Parton, R.G. Redistribution of caveolae during mitosis. J. Cell Sci. 2011, 124, 1965–1972. [Google Scholar] [CrossRef] [PubMed]
- Fürthauer, M.; González-Gaitán, M. Endocytosis and mitosis: A two-way relationship. Cell Cycle 2009, 8, 3311–3318. [Google Scholar] [CrossRef] [PubMed]
- Fielding, A.B.; Willox, A.K.; Okeke, E.; Royle, S.J. Clathrin-mediated endocytosis is inhibited during mitosis. Proc. Natl. Acad. Sci. USA 2012, 109, 6572–6577. [Google Scholar] [CrossRef]
- Palozola, K.C.; Donahue, G.; Liu, H.; Grant, G.R.; Becker, J.S.; Cote, A.; Yu, H.; Raj, A.; Zaret, K.S. Mitotic transcription and waves of gene reactivation during mitotic exit. Science 2017, 358, 119–122. [Google Scholar] [CrossRef]
- Sivan, G.; Kedersha, N.; Elroy-Stein, O. Ribosomal slowdown mediates translational arrest during cellular division. Mol. Cell Biol. 2007, 27, 6639–6646. [Google Scholar] [CrossRef]
- Aviner, R.; Hofmann, S.; Elman, T.; Shenoy, A.; Geiger, T.; Elkon, R.; Ehrlich, M.; Elroy-Stein, O. Proteomic analysis of polyribosomes identifies splicing factors as potential regulators of translation during mitosis. Nucleic Acids Res. 2017, 45, 5945–5957. [Google Scholar] [CrossRef]
- Aviner, R.; Shenoy, A.; Elroy-Stein, O.; Geiger, T. Uncovering Hidden Layers of Cell Cycle Regulation through Integrative Multi-omic Analysis. PLoS Genet. 2015, 11, e1005554. [Google Scholar] [CrossRef]
- Blagosklonny, M.V. Mitotic arrest and cell fate: Why and how mitotic inhibition of transcription drives mutually exclusive events. Cell Cycle 2007, 6, 70–74. [Google Scholar] [CrossRef]
- Petrone, A.; Adamo, M.E.; Cheng, C.; Kettenbach, A.N. Identification of Candidate Cyclin-dependent kinase 1 (Cdk1) Substrates in Mitosis by Quantitative Phosphoproteomics. Mol. Cell. Proteom. 2016, 15, 2448–2461. [Google Scholar] [CrossRef]
- Olsen, J.V.; Vermeulen, M.; Santamaria, A.; Kumar, C.; Miller, M.L.; Jensen, L.J.; Gnad, F.; Cox, J.; Jensen, T.S.; Nigg, E.A.; et al. Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci. Signal 2010, 3, ra3. [Google Scholar] [CrossRef] [PubMed]
- Dephoure, N.; Zhou, C.; Villén, J.; Beausoleil, S.A.; Bakalarski, C.E.; Elledge, S.J.; Gygi, S.P. A quantitative atlas of mitotic phosphorylation. Proc. Natl. Acad. Sci. USA 2008, 105, 10762–10767. [Google Scholar] [CrossRef] [PubMed]
- Fan, M.; Goodwin, M.; Vu, T.; Brantley-Finley, C.; Gaarde, W.A.; Chambers, T.C. Vinblastine-induced phosphorylation of Bcl-2 and Bcl-XL is mediated by JNK and occurs in parallel with inactivation of the Raf-1/MEK/ERK cascade. J. Biol. Chem. 2000, 275, 29980–29985. [Google Scholar] [CrossRef] [PubMed]
- Chu, R.; Upreti, M.; Ding, W.X.; Yin, X.M.; Chambers, T.C. Regulation of Bax by c-Jun NH2-terminal kinase and Bcl-xL in vinblastine-induced apoptosis. Biochem. Pharmacol. 2009, 78, 241–248. [Google Scholar] [CrossRef]
- Chiu, W.H.; Luo, S.J.; Chen, C.L.; Cheng, J.H.; Hsieh, C.Y.; Wang, C.Y.; Huang, W.C.; Su, W.C.; Lin, C.F. Vinca alkaloids cause aberrant ROS-mediated JNK activation, Mcl-1 downregulation, DNA damage, mitochondrial dysfunction, and apoptosis in lung adenocarcinoma cells. Biochem. Pharmacol. 2012, 83, 1159–1171. [Google Scholar] [CrossRef]
- Zhang, L.; Yang, Z.; Granieri, L.; Pasculescu, A.; Datti, A.; Asa, S.L.; Xu, Z.; Ezzat, S. High-throughput drug library screening identifies colchicine as a thyroid cancer inhibitor. Oncotarget 2016, 7, 19948–19959. [Google Scholar] [CrossRef]
- Huang, Z.; Xu, Y.; Peng, W. Colchicine induces apoptosis in HT-29 human colon cancer cells via the AKT and c-Jun N-terminal kinase signaling pathways. Mol. Med. Rep. 2015, 12, 5939–5944. [Google Scholar] [CrossRef]
- Feng, R.; Li, S.; Lu, C.; Andreas, C.; Stolz, D.B.; Mapara, M.Y.; Lentzsch, S. Targeting the microtubular network as a new antimyeloma strategy. Mol. Cancer Ther. 2011, 10, 1886–1896. [Google Scholar] [CrossRef]
- Sánchez-Pérez, T.; Ortiz-Ferrón, G.; López-Rivas, A. Mitotic arrest and JNK-induced proteasomal degradation of FLIP and Mcl-1 are key events in the sensitization of breast tumor cells to TRAIL by antimicrotubule agents. Cell Death Differ. 2010, 17, 883–894. [Google Scholar] [CrossRef]
- Yu-Wei, D.; Li, Z.S.; Xiong, S.M.; Huang, G.; Luo, Y.F.; Huo, T.Y.; Zhou, M.H.; Zheng, Y.W. Paclitaxel induces apoptosis through the TAK1-JNK activation pathway. FEBS Open Bio 2020, 10, 1655–1667. [Google Scholar] [CrossRef]
- Selimovic, D.; Hassan, M.; Haikel, Y.; Hengge, U.R. Taxol-induced mitochondrial stress in melanoma cells is mediated by activation of c-Jun N-terminal kinase (JNK) and p38 pathways via uncoupling protein 2. Cell. Signal 2008, 20, 311–322. [Google Scholar] [CrossRef] [PubMed]
- Zhang, X.; Ling, M.T.; Wang, X.; Wong, Y.C. Inactivation of Id-1 in prostate cancer cells: A potential therapeutic target in inducing chemosensitization to taxol through activation of JNK pathway. Int. J. Cancer 2006, 118, 2072–2081. [Google Scholar] [CrossRef] [PubMed]
- Lan, Y.Y.; Chen, Y.H.; Liu, C.; Tung, K.L.; Wu, Y.T.; Lin, S.C.; Wu, C.H.; Chang, H.Y.; Chen, Y.C.; Huang, B.M. Role of JNK activation in paclitaxel-induced apoptosis in human head and neck squamous cell carcinoma. Oncol. Lett. 2021, 22, 705. [Google Scholar] [CrossRef] [PubMed]
- Su, C.C.; Lin, J.W.; Chang, K.Y.; Wu, C.T.; Liu, S.H.; Chang, K.C.; Liu, J.M.; Lee, K.I.; Fang, K.M.; Chen, Y.W. Involvement of AMPKα and MAPK-ERK/-JNK Signals in Docetaxel-Induced Human Tongue Squamous Cell Carcinoma Cell Apoptosis. Int. J. Mol. Sci. 2022, 23, 13857. [Google Scholar] [CrossRef]
- Mingo-Sion, A.M.; Marietta, P.M.; Koller, E.; Wolf, D.M.; Van Den Berg, C.L. Inhibition of JNK reduces G2/M transit independent of p53, leading to endoreduplication, decreased proliferation, and apoptosis in breast cancer cells. Oncogene 2004, 23, 596–604. [Google Scholar] [CrossRef]
- Huang, Y.; Sheikh, M.S.; Fornace, A.J., Jr.; Holbrook, N.J. Serine protease inhibitor TPCK prevents Taxol-induced cell death and blocks c-Raf-1 and Bcl-2 phosphorylation in human breast carcinoma cells. Oncogene 1999, 18, 3431–3439. [Google Scholar] [CrossRef]
- Kolomeichuk, S.N.; Terrano, D.T.; Lyle, C.S.; Sabapathy, K.; Chambers, T.C. Distinct signaling pathways of microtubule inhibitors--vinblastine and Taxol induce JNK-dependent cell death but through AP-1-dependent and AP-1-independent mechanisms, respectively. FEBS J. 2008, 275, 1889–1899. [Google Scholar] [CrossRef]
- Notte, A.; Ninane, N.; Arnould, T.; Michiels, C. Hypoxia counteracts taxol-induced apoptosis in MDA-MB-231 breast cancer cells: Role of autophagy and JNK activation. Cell Death Dis. 2013, 4, e638. [Google Scholar] [CrossRef]
- Wang, T.-H.; Wang, H.-S.; Ichijo, H.; Giannakakou, P.; Foster, J.S.; Fojo, T.; Wimalasena, J. Microtubule-interfering Agents Activate c-Jun N-terminal Kinase/Stress-activated Protein Kinase through Both Ras and Apoptosis Signal-regulating Kinase Pathways*. J. Biol. Chem. 1998, 273, 4928–4936. [Google Scholar] [CrossRef]
- Stone, A.A.; Chambers, T.C. Microtubule Inhibitors Elicit Differential Effects on MAP Kinase (JNK, ERK, and p38) Signaling Pathways in Human KB-3 Carcinoma Cells. Exp. Cell Res. 2000, 254, 110–119. [Google Scholar] [CrossRef]
- Matthews, H.K.; Bertoli, C.; de Bruin, R.A.M. Cell cycle control in cancer. Nat. Rev. Mol. Cell Biol. 2022, 23, 74–88. [Google Scholar] [CrossRef] [PubMed]
- Yuan, J.; Ofengeim, D. A guide to cell death pathways. Nat. Rev. Mol. Cell Biol. 2024, 25, 379–395. [Google Scholar] [CrossRef] [PubMed]
- Sorokina, I.V.; Denisenko, T.V.; Imreh, G.; Tyurin-Kuzmin, P.A.; Kaminskyy, V.O.; Gogvadze, V.; Zhivotovsky, B. Involvement of autophagy in the outcome of mitotic catastrophe. Sci. Rep. 2017, 7, 14571. [Google Scholar] [CrossRef] [PubMed]
- Denisenko, T.V.; Sorokina, I.V.; Gogvadze, V.; Zhivotovsky, B. Mitotic catastrophe and cancer drug resistance: A link that must to be broken. Drug Resist. Updates 2016, 24, 1–12. [Google Scholar] [CrossRef]
- Roninson, I.B.; Broude, E.V.; Chang, B.-D. If not apoptosis, then what? Treatment-induced senescence and mitotic catastrophe in tumor cells. Drug Resist. Updates 2001, 4, 303–313. [Google Scholar] [CrossRef]
- Kimura, M.; Yoshioka, T.; Saio, M.; Banno, Y.; Nagaoka, H.; Okano, Y. Mitotic catastrophe and cell death induced by depletion of centrosomal proteins. Cell Death Dis. 2013, 4, e603. [Google Scholar] [CrossRef]
- Vitale, I.; Galluzzi, L.; Castedo, M.; Kroemer, G. Mitotic catastrophe: A mechanism for avoiding genomic instability. Nat. Rev. Mol. Cell Biol. 2011, 12, 385–392. [Google Scholar] [CrossRef]
- Castedo, M.; Perfettini, J.-L.; Roumier, T.; Andreau, K.; Medema, R.; Kroemer, G. Cell death by mitotic catastrophe: A molecular definition. Oncogene 2004, 23, 2825–2837. [Google Scholar] [CrossRef]
- Bekier, M.E.; Fischbach, R.; Lee, J.; Taylor, W.R. Length of mitotic arrest induced by microtubule-stabilizing drugs determines cell death after mitotic exit. Mol. Cancer Ther. 2009, 8, 1646–1654. [Google Scholar] [CrossRef]
- Gangemi, R.M.; Tiso, M.; Marchetti, C.; Severi, A.B.; Fabbi, M. Taxol cytotoxicity on human leukemia cell lines is a function of their susceptibility to programmed cell death. Cancer Chemother. Pharmacol. 1995, 36, 385–392. [Google Scholar] [CrossRef]
- Jordan, M.A.; Wendell, K.; Gardiner, S.; Derry, W.B.; Copp, H.; Wilson, L. Mitotic block induced in HeLa cells by low concentrations of paclitaxel (Taxol) results in abnormal mitotic exit and apoptotic cell death. Cancer Res. 1996, 56, 816–825. [Google Scholar] [PubMed]
- Milross, C.G.; Mason, K.A.; Hunter, N.R.; Chung, W.K.; Peters, L.J.; Milas, L. Relationship of mitotic arrest and apoptosis to antitumor effect of paclitaxel. J. Natl. Cancer Inst. 1996, 88, 1308–1314. [Google Scholar] [CrossRef] [PubMed]
- Egorshina, A.Y.; Zamaraev, A.V.; Kaminskyy, V.O.; Radygina, T.V.; Zhivotovsky, B.; Kopeina, G.S. Necroptosis as a Novel Facet of Mitotic Catastrophe. Int. J. Mol. Sci. 2022, 23, 3733. [Google Scholar] [CrossRef] [PubMed]
- Frank, T.; Tuppi, M.; Hugle, M.; Dötsch, V.; van Wijk, S.J.L.; Fulda, S. Cell cycle arrest in mitosis promotes interferon-induced necroptosis. Cell Death Differ. 2019, 26, 2046–2060. [Google Scholar] [CrossRef] [PubMed]
- Wang, X.; Li, H.; Li, W.; Xie, J.; Wang, F.; Peng, X.; Song, Y.; Tan, G. The role of Caspase-1/GSDMD-mediated pyroptosis in Taxol-induced cell death and a Taxol-resistant phenotype in nasopharyngeal carcinoma regulated by autophagy. Cell Biol. Toxicol. 2020, 36, 437–457. [Google Scholar] [CrossRef] [PubMed]
- Mason, K.A.; Hunter, N.R.; Milas, M.; Abbruzzese, J.L.; Milas, L. Docetaxel enhances tumor radioresponse in vivo. Clin. Cancer Res. 1997, 3, 2431–2438. [Google Scholar]
- Schimming, R.; Mason, K.A.; Hunter, N.; Weil, M.; Kishi, K.; Milas, L. Lack of correlation between mitotic arrest or apoptosis and antitumor effect of docetaxel. Cancer Chemother. Pharmacol. 1999, 43, 165–172. [Google Scholar] [CrossRef]
- Nakayama, Y.; Inoue, T. Antiproliferative Fate of the Tetraploid Formed after Mitotic Slippage and Its Promotion; A Novel Target for Cancer Therapy Based on Microtubule Poisons. Molecules 2016, 21, 663. [Google Scholar] [CrossRef]
- Sinha, D.; Duijf, P.H.G.; Khanna, K.K. Mitotic slippage: An old tale with a new twist. Cell Cycle 2019, 18, 7–15. [Google Scholar] [CrossRef]
- Mosca, L.; Ilari, A.; Fazi, F.; Assaraf, Y.G.; Colotti, G. Taxanes in cancer treatment: Activity, chemoresistance and its overcoming. Drug Resist. Updates 2021, 54, 100742. [Google Scholar] [CrossRef]
- Haschka, M.; Karbon, G.; Fava, L.L.; Villunger, A. Perturbing mitosis for anti-cancer therapy: Is cell death the only answer? EMBO Rep. 2018, 19, e45440. [Google Scholar] [CrossRef]
- Sakurikar, N.; Eichhorn, J.M.; Chambers, T.C. Cyclin-dependent kinase-1 (Cdk1)/cyclin B1 dictates cell fate after mitotic arrest via phosphoregulation of antiapoptotic Bcl-2 proteins. J. Biol. Chem. 2012, 287, 39193–39204. [Google Scholar] [CrossRef] [PubMed]
- Huang, H.C.; Mitchison, T.J.; Shi, J. Stochastic competition between mechanistically independent slippage and death pathways determines cell fate during mitotic arrest. PLoS ONE 2010, 5, e15724. [Google Scholar] [CrossRef] [PubMed]
- Gascoigne, K.E.; Taylor, S.S. Cancer cells display profound intra- and interline variation following prolonged exposure to antimitotic drugs. Cancer Cell 2008, 14, 111–122. [Google Scholar] [CrossRef] [PubMed]
- Cheng, B.; Crasta, K. Consequences of mitotic slippage for antimicrotubule drug therapy. Endocr. Relat. Cancer 2017, 24, T97–T106. [Google Scholar] [CrossRef] [PubMed]
- Shimizu, S.; Konishi, A.; Nishida, Y.; Mizuta, T.; Nishina, H.; Yamamoto, A.; Tsujimoto, Y. Involvement of JNK in the regulation of autophagic cell death. Oncogene 2010, 29, 2070–2082. [Google Scholar] [CrossRef]
- Zhou, Y.-Y.; Li, Y.; Jiang, W.-Q.; Zhou, L.-F. MAPK/JNK signalling: A potential autophagy regulation pathway. Biosci. Rep. 2015, 35, e00199. [Google Scholar] [CrossRef]
- Lorin, S.; Borges, A.; Ribeiro Dos Santos, L.; Souquère, S.; Pierron, G.; Ryan, K.M.; Codogno, P.; Djavaheri-Mergny, M. c-Jun NH2-terminal kinase activation is essential for DRAM-dependent induction of autophagy and apoptosis in 2-methoxyestradiol-treated Ewing sarcoma cells. Cancer Res. 2009, 69, 6924–6931. [Google Scholar] [CrossRef]
- Lorin, S.; Pierron, G.; Ryan, K.M.; Codogno, P.; Djavaheri-Mergny, M. Evidence for the interplay between JNK and p53-DRAM signalling pathways in the regulation of autophagy. Autophagy 2010, 6, 153–154. [Google Scholar] [CrossRef]
- Dhanasekaran, D.N.; Reddy, E.P. JNK-signaling: A multiplexing hub in programmed cell death. Genes Cancer 2017, 8, 682–694. [Google Scholar] [CrossRef]
- Tournier, C.; Hess, P.; Yang, D.D.; Xu, J.; Turner, T.K.; Nimnual, A.; Bar-Sagi, D.; Jones, S.N.; Flavell, R.A.; Davis, R.J. Requirement of JNK for stress-induced activation of the cytochrome c-mediated death pathway. Science 2000, 288, 870–874. [Google Scholar] [CrossRef] [PubMed]
- Behrens, A.; Sibilia, M.; Wagner, E.F. Amino-terminal phosphorylation of c-Jun regulates stress-induced apoptosis and cellular proliferation. Nat. Genet. 1999, 21, 326–329. [Google Scholar] [CrossRef] [PubMed]
- Kamata, H.; Honda, S.; Maeda, S.; Chang, L.; Hirata, H.; Karin, M. Reactive oxygen species promote TNFalpha-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell 2005, 120, 649–661. [Google Scholar] [CrossRef] [PubMed]
- Sun, W.; Wu, X.; Gao, H.; Yu, J.; Zhao, W.; Lu, J.J.; Wang, J.; Du, G.; Chen, X. Cytosolic calcium mediates RIP1/RIP3 complex-dependent necroptosis through JNK activation and mitochondrial ROS production in human colon cancer cells. Free Radic. Biol. Med. 2017, 108, 433–444. [Google Scholar] [CrossRef]
- Lupfer, C.R.; Anand, P.K.; Liu, Z.; Stokes, K.L.; Vogel, P.; Lamkanfi, M.; Kanneganti, T.D. Reactive oxygen species regulate caspase-11 expression and activation of the non-canonical NLRP3 inflammasome during enteric pathogen infection. PLoS Pathog. 2014, 10, e1004410. [Google Scholar] [CrossRef]
- Gutierrez, G.J.; Tsuji, T.; Chen, M.; Jiang, W.; Ronai, Z.A. Interplay between Cdh1 and JNK activity during the cell cycle. Nat. Cell Biol. 2010, 12, 686–695. [Google Scholar] [CrossRef]
- Gutierrez, G.J.; Tsuji, T.; Cross, J.V.; Davis, R.J.; Templeton, D.J.; Jiang, W.; Ronai, Z.A. JNK-mediated phosphorylation of Cdc25C regulates cell cycle entry and G(2)/M DNA damage checkpoint. J. Biol. Chem. 2010, 285, 14217–14228. [Google Scholar] [CrossRef]
- Cosolo, A.; Jaiswal, J.; Csordás, G.; Grass, I.; Uhlirova, M.; Classen, A.K. JNK-dependent cell cycle stalling in G2 promotes survival and senescence-like phenotypes in tissue stress. Elife 2019, 8, e41036. [Google Scholar] [CrossRef]
- Pineda, J.J.; Miller, M.A.; Song, Y.; Kuhn, H.; Mikula, H.; Tallapragada, N.; Weissleder, R.; Mitchison, T.J. Site occupancy calibration of taxane pharmacology in live cells and tissues. Proc. Natl. Acad. Sci. USA 2018, 115, E11406–E11414. [Google Scholar] [CrossRef]
- Mitchison, T.J.; Pineda, J.; Shi, J.; Florian, S. Is inflammatory micronucleation the key to a successful anti-mitotic cancer drug? Open Biol. 2017, 7, 170182. [Google Scholar] [CrossRef]
- Flynn, P.J.; Koch, P.D.; Mitchison, T.J. Chromatin bridges, not micronuclei, activate cGAS after drug-induced mitotic errors in human cells. Proc. Natl. Acad. Sci. USA 2021, 118, e2103585118. [Google Scholar] [CrossRef] [PubMed]
- Randow, F.; MacMicking, J.D.; James, L.C. Cellular self-defense: How cell-autonomous immunity protects against pathogens. Science 2013, 340, 701–706. [Google Scholar] [CrossRef] [PubMed]
- Zhong, L.; Hu, M.M.; Bian, L.J.; Liu, Y.; Chen, Q.; Shu, H.B. Phosphorylation of cGAS by CDK1 impairs self-DNA sensing in mitosis. Cell Discov. 2020, 6, 26. [Google Scholar] [CrossRef] [PubMed]
- Li, T.; Huang, T.; Du, M.; Chen, X.; Du, F.; Ren, J.; Chen, Z.J. Phosphorylation and chromatin tethering prevent cGAS activation during mitosis. Science 2021, 371, eabc5386. [Google Scholar] [CrossRef] [PubMed]
- Uhlorn, B.L.; Gamez, E.R.; Li, S.; Campos, S.K. Attenuation of cGAS/STING activity during mitosis. Life Sci. Alliance 2020, 3, e201900636. [Google Scholar] [CrossRef]
- Zhong, L.; Shu, H.B. Mitotic inactivation of the cGAS–MITA/STING pathways. J. Mol. Cell Biol. 2021, 13, 721–727. [Google Scholar] [CrossRef]
- Zierhut, C.; Yamaguchi, N.; Paredes, M.; Luo, J.D.; Carroll, T.; Funabiki, H. The Cytoplasmic DNA Sensor cGAS Promotes Mitotic Cell Death. Cell 2019, 178, 302–315.e23. [Google Scholar] [CrossRef]
- Gal-Ben-Ari, S.; Barrera, I.; Ehrlich, M.; Rosenblum, K. PKR: A Kinase to Remember. Front. Mol. Neurosci. 2018, 11, 480. [Google Scholar] [CrossRef]
- Kim, Y.; Lee, J.H.; Park, J.E.; Cho, J.; Yi, H.; Kim, V.N. PKR is activated by cellular dsRNAs during mitosis and acts as a mitotic regulator. Genes Dev. 2014, 28, 1310–1322. [Google Scholar] [CrossRef]
- Yin, L.; Zeng, Y.; Zeng, R.; Chen, Y.; Wang, T.L.; Rodabaugh, K.J.; Yu, F.; Natarajan, A.; Karpf, A.R.; Dong, J. Protein kinase RNA-activated controls mitotic progression and determines paclitaxel chemosensitivity through B-cell lymphoma 2 in ovarian cancer. Oncogene 2021, 40, 6772–6785. [Google Scholar] [CrossRef]
- Lanni, J.S.; Lowe, S.W.; Licitra, E.J.; Liu, J.O.; Jacks, T. p53-independent apoptosis induced by paclitaxel through an indirect mechanism. Proc. Natl. Acad. Sci. USA 1997, 94, 9679–9683. [Google Scholar] [CrossRef] [PubMed]
- Herbst, R.S.; Khuri, F.R. Mode of action of docetaxel—A basis for combination with novel anticancer agents. Cancer Treat. Rev. 2003, 29, 407–415. [Google Scholar] [CrossRef] [PubMed]
- Jang, H.J.; Hwang, S.; Cho, K.Y.; Kim, D.K.; Chay, K.O.; Kim, J.K. Taxol induces oxidative neuronal cell death by enhancing the activity of NADPH oxidase in mouse cortical cultures. Neurosci. Lett. 2008, 443, 17–22. [Google Scholar] [CrossRef] [PubMed]
- Tran, T.A.; Gillet, L.; Roger, S.; Besson, P.; White, E.; Le Guennec, J.Y. Non-anti-mitotic concentrations of taxol reduce breast cancer cell invasiveness. Biochem. Biophys Res. Commun. 2009, 379, 304–308. [Google Scholar] [CrossRef]
- Dark, G.G.; Hill, S.A.; Prise, V.E.; Tozer, G.M.; Pettit, G.R.; Chaplin, D.J. Combretastatin A-4, an agent that displays potent and selective toxicity toward tumor vasculature. Cancer Res. 1997, 57, 1829–1834. [Google Scholar]
- Ganansia-Leymarie, V.; Bischoff, P.; Bergerat, J.P.; Holl, V. Signal transduction pathways of taxanes-induced apoptosis. Curr. Med. Chem. Anticancer Agents 2003, 3, 291–306. [Google Scholar] [CrossRef]
- Darshan, M.S.; Loftus, M.S.; Thadani-Mulero, M.; Levy, B.P.; Escuin, D.; Zhou, X.K.; Gjyrezi, A.; Chanel-Vos, C.; Shen, R.; Tagawa, S.T.; et al. Taxane-induced blockade to nuclear accumulation of the androgen receptor predicts clinical responses in metastatic prostate cancer. Cancer Res. 2011, 71, 6019–6029. [Google Scholar] [CrossRef]
- Lin, S.F.; Gao, S.P.; Price, D.L.; Li, S.; Chou, T.C.; Singh, P.; Huang, Y.Y.; Fong, Y.; Wong, R.J. Synergy of a herpes oncolytic virus and paclitaxel for anaplastic thyroid cancer. Clin. Cancer Res. 2008, 14, 1519–1528. [Google Scholar] [CrossRef]
- Mato-Berciano, A.; Raimondi, G.; Maliandi, M.V.; Alemany, R.; Montoliu, L.; Fillat, C. A NOTCH-sensitive uPAR-regulated oncolytic adenovirus effectively suppresses pancreatic tumor growth and triggers synergistic anticancer effects with gemcitabine and nab-paclitaxel. Oncotarget 2017, 8, 22700–22715. [Google Scholar] [CrossRef]
- Cao, L.; Zeng, Q.; Xu, C.; Shi, S.; Zhang, Z.; Sun, X. Enhanced antitumor response mediated by the codelivery of paclitaxel and adenoviral vector expressing IL-12. Mol. Pharm. 2013, 10, 1804–1814. [Google Scholar] [CrossRef]
- Kim, I.W.; Yoon, A.R.; Hong, J.; Kasala, D.; Yun, C.O. Synergistic antitumor immune response mediated by paclitaxel-conjugated nanohybrid oncolytic adenovirus with dendritic cell therapy. Front. Immunol. 2024, 15, 1355566. [Google Scholar] [CrossRef] [PubMed]
- Fang, L.; Cheng, Q.; Bai, J.; Qi, Y.D.; Liu, J.J.; Li, L.T.; Zheng, J.N. An oncolytic adenovirus expressing interleukin-24 enhances antitumor activities in combination with paclitaxel in breast cancer cells. Mol. Med. Rep. 2013, 8, 1416–1424. [Google Scholar] [CrossRef] [PubMed]
- Yu, D.C.; Chen, Y.; Dilley, J.; Li, Y.; Embry, M.; Zhang, H.; Nguyen, N.; Amin, P.; Oh, J.; Henderson, D.R. Antitumor synergy of CV787, a prostate cancer-specific adenovirus, and paclitaxel and docetaxel. Cancer Res. 2001, 61, 517–525. [Google Scholar] [PubMed]
- Chen, P.; Luo, S.; Wen, Y.J.; Li, Y.H.; Li, J.; Wang, Y.S.; Du, L.C.; Zhang, P.; Tang, J.; Yang, D.B.; et al. Low-dose paclitaxel improves the therapeutic efficacy of recombinant adenovirus encoding CCL21 chemokine against murine cancer. Cancer Sci. 2014, 105, 1393–1401. [Google Scholar] [CrossRef] [PubMed]
- Garofalo, M.; Villa, A.; Rizzi, N.; Kuryk, L.; Rinner, B.; Cerullo, V.; Yliperttula, M.; Mazzaferro, V.; Ciana, P. Extracellular vesicles enhance the targeted delivery of immunogenic oncolytic adenovirus and paclitaxel in immunocompetent mice. J. Control. Release 2019, 294, 165–175. [Google Scholar] [CrossRef]
- Wang, J.; Li, Y.; Li, S.; Yao, W.; Liu, X.; Zhu, Y.; Li, W.; Sun, L.; Jin, N.; Li, X. Anti-tumor Synergistic Effect of a Dual Cancer-Specific Recombinant Adenovirus and Paclitaxel on Breast Cancer. Front. Oncol. 2020, 10, 244. [Google Scholar] [CrossRef]
- Hossain, E.; Habiba, U.; Yanagawa-Matsuda, A.; Alam, A.; Ahmed, I.; Alam, M.T.; Yasuda, M.; Higashino, F. Advantages of Using Paclitaxel in Combination with Oncolytic Adenovirus Utilizing RNA Destabilization Mechanism. Cancers 2020, 12, 1210. [Google Scholar] [CrossRef]
- Mahalingam, D.; Fountzilas, C.; Moseley, J.; Noronha, N.; Tran, H.; Chakrabarty, R.; Selvaggi, G.; Coffey, M.; Thompson, B.; Sarantopoulos, J. A phase II study of REOLYSIN® (pelareorep) in combination with carboplatin and paclitaxel for patients with advanced malignant melanoma. Cancer Chemother. Pharmacol. 2017, 79, 697–703. [Google Scholar] [CrossRef]
- Bernstein, V.; Ellard, S.L.; Dent, S.F.; Tu, D.; Mates, M.; Dhesy-Thind, S.K.; Panasci, L.; Gelmon, K.A.; Salim, M.; Song, X.; et al. A randomized phase II study of weekly paclitaxel with or without pelareorep in patients with metastatic breast cancer: Final analysis of Canadian Cancer Trials Group IND.213. Breast Cancer Res. Treat. 2018, 167, 485–493. [Google Scholar] [CrossRef]
- Comins, C.; Spicer, J.; Protheroe, A.; Roulstone, V.; Twigger, K.; White, C.M.; Vile, R.; Melcher, A.; Coffey, M.C.; Mettinger, K.L.; et al. REO-10: A phase I study of intravenous reovirus and docetaxel in patients with advanced cancer. Clin. Cancer Res. 2010, 16, 5564–5572. [Google Scholar] [CrossRef]
- Passer, B.J.; Cheema, T.; Wu, S.; Wu, C.L.; Rabkin, S.D.; Martuza, R.L. Combination of vinblastine and oncolytic herpes simplex virus vector expressing IL-12 therapy increases antitumor and antiangiogenic effects in prostate cancer models. Cancer Gene Ther. 2013, 20, 17–24. [Google Scholar] [CrossRef] [PubMed]
- Moreno, V.; Barretina-Ginesta, M.-P.; García-Donas, J.; Jayson, G.C.; Roxburgh, P.; Vázquez, R.M.; Michael, A.; Antón-Torres, A.; Brown, R.; Krige, D.; et al. Safety and efficacy of the tumor-selective adenovirus enadenotucirev with or without paclitaxel in platinum-resistant ovarian cancer: A phase 1 clinical trial. J. Immunother. Cancer 2021, 9, e003645. [Google Scholar] [CrossRef] [PubMed]
- Ishikawa, W.; Kikuchi, S.; Ogawa, T.; Tabuchi, M.; Tazawa, H.; Kuroda, S.; Noma, K.; Nishizaki, M.; Kagawa, S.; Urata, Y.; et al. Boosting Replication and Penetration of Oncolytic Adenovirus by Paclitaxel Eradicate Peritoneal Metastasis of Gastric Cancer. Mol. Ther. Oncolytics 2020, 18, 262–271. [Google Scholar] [CrossRef] [PubMed]
- Cohn, D.E.; Sill, M.W.; Walker, J.L.; O’Malley, D.; Nagel, C.I.; Rutledge, T.L.; Bradley, W.; Richardson, D.L.; Moxley, K.M.; Aghajanian, C. Randomized phase IIB evaluation of weekly paclitaxel versus weekly paclitaxel with oncolytic reovirus (Reolysin®) in recurrent ovarian, tubal, or peritoneal cancer: An NRG Oncology/Gynecologic Oncology Group study. Gynecol. Oncol. 2017, 146, 477–483. [Google Scholar] [CrossRef]
- Musher, B.L.; Rowinsky, E.K.; Smaglo, B.G.; Abidi, W.; Othman, M.; Patel, K.; Jawaid, S.; Jing, J.; Brisco, A.; Leen, A.M.; et al. LOAd703, an oncolytic virus-based immunostimulatory gene therapy, combined with chemotherapy for unresectable or metastatic pancreatic cancer (LOKON001): Results from arm 1 of a non-randomised, single-centre, phase 1/2 study. Lancet Oncol. 2024, 25, 488–500. [Google Scholar] [CrossRef]
- Ingemarsdotter, C.K.; Baird, S.K.; Connell, C.M.; Öberg, D.; Halldén, G.; McNeish, I.A. Low-dose paclitaxel synergizes with oncolytic adenoviruses via mitotic slippage and apoptosis in ovarian cancer. Oncogene 2010, 29, 6051–6063. [Google Scholar] [CrossRef]
- Garcia-Carbonero, R.; Bazan-Peregrino, M.; Gil-Martín, M.; Álvarez, R.; Macarulla, T.; Riesco-Martinez, M.C.; Verdaguer, H.; Guillén-Ponce, C.; Farrera-Sal, M.; Moreno, R.; et al. Phase I, multicenter, open-label study of intravenous VCN-01 oncolytic adenovirus with or without nab-paclitaxel plus gemcitabine in patients with advanced solid tumors. J. Immunother. Cancer 2022, 10, e003255. [Google Scholar] [CrossRef]
- Karapanagiotou, E.M.; Roulstone, V.; Twigger, K.; Ball, M.; Tanay, M.; Nutting, C.; Newbold, K.; Gore, M.E.; Larkin, J.; Syrigos, K.N.; et al. Phase I/II Trial of Carboplatin and Paclitaxel Chemotherapy in Combination with Intravenous Oncolytic Reovirus in Patients with Advanced Malignancies. Clin. Cancer Res. 2012, 18, 2080–2089. [Google Scholar] [CrossRef]
- Soliman, H.; Hogue, D.; Han, H.; Mooney, B.; Costa, R.; Lee, M.C.; Niell, B.; Williams, A.; Chau, A.; Falcon, S.; et al. Oncolytic T-VEC virotherapy plus neoadjuvant chemotherapy in nonmetastatic triple-negative breast cancer: A phase 2 trial. Nat. Med. 2023, 29, 450–457. [Google Scholar] [CrossRef]
- Passer, B.J.; Castelo-Branco, P.; Buhrman, J.S.; Varghese, S.; Rabkin, S.D.; Martuza, R.L. Oncolytic herpes simplex virus vectors and taxanes synergize to promote killing of prostate cancer cells. Cancer Gene Ther. 2009, 16, 551–560. [Google Scholar] [CrossRef]
- Heinemann, L.; Simpson, G.R.; Boxall, A.; Kottke, T.; Relph, K.L.; Vile, R.; Melcher, A.; Prestwich, R.; Harrington, K.J.; Morgan, R.; et al. Synergistic effects of oncolytic reovirus and docetaxel chemotherapy in prostate cancer. BMC Cancer 2011, 11, 221. [Google Scholar] [CrossRef] [PubMed]
- Pakola, S.; Quixabeira, D.C.A.; Kudling, T.V.; Clubb, J.H.A.; Grönberg-Vähä-Koskela, S.; Basnet, S.; Jirovec, E.; Arias, V.; Haybout, L.; Heiniö, C.; et al. An oncolytic adenovirus coding for a variant interleukin 2 cytokine improves response to chemotherapy through enhancement of effector lymphocyte cytotoxicity, fibroblast compartment modulation and mitotic slippage. Front. Immunol. 2023, 14, 1171083. [Google Scholar] [CrossRef] [PubMed]
- Huang, B.; Sikorski, R.; Kirn, D.H.; Thorne, S.H. Synergistic anti-tumor effects between oncolytic vaccinia virus and paclitaxel are mediated by the IFN response and HMGB1. Gene Ther. 2011, 18, 164–172. [Google Scholar] [CrossRef] [PubMed]
- Arulanandam, R.; Batenchuk, C.; Varette, O.; Zakaria, C.; Garcia, V.; Forbes, N.E.; Davis, C.; Krishnan, R.; Karmacharya, R.; Cox, J.; et al. Microtubule disruption synergizes with oncolytic virotherapy by inhibiting interferon translation and potentiating bystander killing. Nat. Commun. 2015, 6, 6410. [Google Scholar] [CrossRef] [PubMed]
- Bressy, C.; Droby, G.N.; Maldonado, B.D.; Steuerwald, N.; Grdzelishvili, V.Z. Cell Cycle Arrest in G(2)/M Phase Enhances Replication of Interferon-Sensitive Cytoplasmic RNA Viruses via Inhibition of Antiviral Gene Expression. J. Virol. 2019, 93, e01885-18. [Google Scholar] [CrossRef]
- Song, X.; Wang, H.; Jia, R.; Cun, B.; Zhao, X.; Zhou, Y.; Xu, X.; Qian, G.; Ge, S.; Fan, X. Combined treatment with an oncolytic adenovirus and antitumor activity of vincristine against retinoblastoma cells. Int. J. Mol. Sci. 2012, 13, 10736–10749. [Google Scholar] [CrossRef]
- AbouEl Hassan, M.A.; Braam, S.R.; Kruyt, F.A. Paclitaxel and vincristine potentiate adenoviral oncolysis that is associated with cell cycle and apoptosis modulation, whereas they differentially affect the viral life cycle in non-small-cell lung cancer cells. Cancer Gene Ther. 2006, 13, 1105–1114. [Google Scholar] [CrossRef]
- Fujiwara, T.; Kagawa, S.; Kishimoto, H.; Endo, Y.; Hioki, M.; Ikeda, Y.; Sakai, R.; Urata, Y.; Tanaka, N.; Fujiwara, T. Enhanced antitumor efficacy of telomerase-selective oncolytic adenoviral agent OBP-401 with docetaxel: Preclinical evaluation of chemovirotherapy. Int. J. Cancer 2006, 119, 432–440. [Google Scholar] [CrossRef]
- Garofalo, M.; Saari, H.; Somersalo, P.; Crescenti, D.; Kuryk, L.; Aksela, L.; Capasso, C.; Madetoja, M.; Koskinen, K.; Oksanen, T.; et al. Antitumor effect of oncolytic virus and paclitaxel encapsulated in extracellular vesicles for lung cancer treatment. J. Control. Release 2018, 283, 223–234. [Google Scholar] [CrossRef]
- Kuryk, L.; Mathlouthi, S.; Wieczorek, M.; Gad, B.; Rinner, B.; Malfanti, A.; Mastrotto, F.; Salmaso, S.; Caliceti, P.; Garofalo, M. Priming with oncolytic adenovirus followed by anti-PD-1 and paclitaxel treatment leads to improved anti-cancer efficacy in the 3D TNBC model. Eur. J. Pharm. Biopharm. 2024, 199, 114300. [Google Scholar] [CrossRef]
- Kasala, D.; Lee, S.H.; Hong, J.W.; Choi, J.W.; Nam, K.; Chung, Y.H.; Kim, S.W.; Yun, C.O. Synergistic antitumor effect mediated by a paclitaxel-conjugated polymeric micelle-coated oncolytic adenovirus. Biomaterials 2017, 145, 207–222. [Google Scholar] [CrossRef] [PubMed]
- Li, X.; Liu, Y.; Tang, Y.; Roger, P.; Jeng, M.H.; Kao, C. Docetaxel increases antitumor efficacy of oncolytic prostate-restricted replicative adenovirus by enhancing cell killing and virus distribution. J. Gene Med. 2010, 12, 516–527. [Google Scholar] [CrossRef] [PubMed]
- Mao, L.; Yu, H.; Ma, S.; Xu, Z.; Wei, F.; Yang, C.; Zheng, J. Combination of oncolytic adenovirus targeting SATB1 and docetaxel for the treatment of castration-resistant prostate cancer. J. Cancer 2021, 12, 1846–1852. [Google Scholar] [CrossRef] [PubMed]
- Sei, S.; Mussio, J.K.; Yang, Q.E.; Nagashima, K.; Parchment, R.E.; Coffey, M.C.; Shoemaker, R.H.; Tomaszewski, J.E. Synergistic antitumor activity of oncolytic reovirus and chemotherapeutic agents in non-small cell lung cancer cells. Mol. Cancer 2009, 8, 47. [Google Scholar] [CrossRef] [PubMed]
- Cinatl, J., Jr.; Cinatl, J.; Michaelis, M.; Kabickova, H.; Kotchetkov, R.; Vogel, J.U.; Doerr, H.W.; Klingebiel, T.; Driever, P.H. Potent oncolytic activity of multimutated herpes simplex virus G207 in combination with vincristine against human rhabdomyosarcoma. Cancer Res. 2003, 63, 1508–1514. [Google Scholar]
- Zeng, W.G.; Li, J.J.; Hu, P.; Lei, L.; Wang, J.N.; Liu, R.B. An oncolytic herpes simplex virus vector, G47Δ, synergizes with paclitaxel in the treatment of breast cancer. Oncol. Rep. 2013, 29, 2355–2361. [Google Scholar] [CrossRef]
- Deng, X.; Shen, Y.; Yi, M.; Zhang, C.; Zhao, B.; Zhong, G.; Weiyang, L.; Xue, D.; Leng, Q.; Ding, J.; et al. Combination of novel oncolytic herpesvirus with paclitaxel as an efficient strategy for breast cancer therapy. J. Med. Virol. 2023, 95, e28768. [Google Scholar] [CrossRef]
- Binz, E.; Berchtold, S.; Beil, J.; Schell, M.; Geisler, C.; Smirnow, I.; Lauer, U.M. Chemovirotherapy of Pancreatic Adenocarcinoma by Combining Oncolytic Vaccinia Virus GLV-1h68 with nab-Paclitaxel Plus Gemcitabine. Mol. Ther. Oncolytics 2017, 6, 10–21. [Google Scholar] [CrossRef]
- Bourgeois-Daigneault, M.C.; St-Germain, L.E.; Roy, D.G.; Pelin, A.; Aitken, A.S.; Arulanandam, R.; Falls, T.; Garcia, V.; Diallo, J.S.; Bell, J.C. Combination of Paclitaxel and MG1 oncolytic virus as a successful strategy for breast cancer treatment. Breast Cancer Res. 2016, 18, 83. [Google Scholar] [CrossRef]
- Anjum, S.; Naseer, F.; Ahmad, T.; Liaquat, A.; Abduh, M.S.; Kousar, K. Co-delivery of oncolytic virus and chemotherapeutic modality: Vincristine against prostate cancer treatment: A potent viro-chemotherapeutic approach. J. Med. Virol. 2024, 96, e29748. [Google Scholar] [CrossRef]
- Moehler, M.; Sieben, M.; Roth, S.; Springsguth, F.; Leuchs, B.; Zeidler, M.; Dinsart, C.; Rommelaere, J.; Galle, P.R. Activation of the human immune system by chemotherapeutic or targeted agents combined with the oncolytic parvovirus H-1. BMC Cancer 2011, 11, 464. [Google Scholar] [CrossRef] [PubMed]
- Lal, G.; Rajala, M.S. Combination of Oncolytic Measles Virus Armed With BNiP3, a Pro-apoptotic Gene and Paclitaxel Induces Breast Cancer Cell Death. Front. Oncol. 2018, 8, 676. [Google Scholar] [CrossRef] [PubMed]
- Zhang, T.; Jou, T.H.; Hsin, J.; Wang, Z.; Huang, K.; Ye, J.; Yin, H.; Xing, Y. Talimogene Laherparepvec (T-VEC): A Review of the Recent Advances in Cancer Therapy. J. Clin. Med. 2023, 12, 1098. [Google Scholar] [CrossRef] [PubMed]
Oncolytic Virus | Compound | Cancer Type/Cell Line | Ref. |
---|---|---|---|
Oncolytic Measles Virus (OMV) | Vincristine | Human prostate cancer cells (PC3) | [210] |
Oncolytic Adenovirus SG600 | Vincristine | Human retinoblastoma cells (HXO-RB44) | [196] |
Oncolytic adenovirus Ad5 | Vincristine | Non-small-cell lung cancer (NSCLC) | [197] |
Oncolytic Herpes simplex virus (G207) | Vincristine | Human rhabdomyosarcoma cells (KFR, KF-RMS-1) | [205] |
Oncolytic parvovirus H-1PV | Vincristine | Human melanoma cells (Mz-Mel, SK29-Mel-1, SK29-Mel-1.22) | [211] |
Oncolytic adenovirus OBP-401 | Vinorelbine | Human non-small-cell lung cancer (H1299) and human colorectal carcinoma (SW620) cells | [198] |
Oncolytic Vesicular Stomatitis Virus VSV-Δ51 | Vinorelbine/colchicine | Human renal carcinoma cells (768-O), a mouse model of triple-negative breast cancer (4T1) | [194] |
Oncolytic Herpes Simplex Virus (NV1023) and human IL12 producing variant (NV1042) | Vinblastine | Human prostate cancer cell lines (CWR22, PC3), in vivo xenograft (CWR22) | [181] |
Oncolytic Reovirus Type 3 Dearing strain (ReoT3D) | Vinblastine | Non-small-cell lung cancer cells (EKVX, NCL-H322M, NCL-H226) | [204] |
Oncolytic Rhabdovirus Maraba MG-1 virus | Paclitaxel | Murine mammary carcinoma cells (4T1, EMT6, EO771), mouse tumor models (4T1, EMT6), human breast cancer cells (S578T, BT-549 and MDA-MB-231) | [209] |
Oncolytic adenovirus AD5D24-CpG | Paclitaxel | Human lung cancer cells (A549) | [199] |
Oncolytic Herpes simplex virus (G207), Oncolytic Herpes Simplex Virus (NV1023) | Paclitaxel | Human anaplastic thyroid cancer cells (KAT-4, DRO90-1) | [168] |
Oncolytic Herpes Simplex virus (G47∆) | Paclitaxel | Human breast cancer (MCF-7 and MDA-MB-468 cell lines) | [206] |
Oncolytic Vaccinia virus (vvDD) | Paclitaxel | Human colorectal carcinoma cells (HCT-116), human breast cancer cells (MCF-7), human ovarian cancer cells (UCI-101) | [193] |
Oncolytic Vaccinia virus (GLV-1h68) | Paclitaxel | Human pancreatic adenocarcinoma cells (AsPc-1, Panc-1) | [208] |
Oncolytic Herpes simplex virus type I (VG161) | Paclitaxel | Mouse breast cancer tumor model EMT6 | [207] |
Oncolytic adenovirus (dl922-947) | Paclitaxel | Human ovarian cancer cells (A2780CP, IGROV1) | [186] |
Oncolytic Herpes simplex virus (G47∆) | Paclitaxel | Human Prostate cancer cells (LNCaP, DU145) | [190] |
Oncolytic adenovirus (AdV5/3-D24-ICOSL-CD40L,) | Paclitaxel | Human breast cancer cells (MCF-7, MDA-MB-231, MDA-MB-468) | [200] |
Oncolytic adenovirus (OBP-401) | Paclitaxel | Human gastric cancer cells (GCIY, KATOIII) | [183] |
Oncolytic adenovirus (Ad-fosARE) | Paclitaxel | Human lung cancer cells (A549, H1299), human cervical carcinoma cells (HeLa, HeLa S3, C-33), human osteosarcoma cells (U-2-OS) human hepatoma cells (HepG2) | [177] |
Oncolytic adenovirus (oAd-vp53) | Paclitaxel | Human breast cancer cells (MCF-7, SKBR-3), human ovarian cancer cells (MDAH 2774), human lung cancer cells (H460) | [201] |
Oncolytic recombinant measles virus (rMV-BNiP3) | Paclitaxel | Human breast cancer cells (MCF-7, MDA-MB-231) | [212] |
Oncolytic adenovirus (PRRA) | Docetaxel | Human prostate cancer cells (CWR22rv, C4-2 cell), CWR22rv subcutaneous tumor xenograft mouse model | [202] |
Oncolytic adenovirus (OBP-401) | Docetaxel/vinorelbine | Human non-small cell lung cancer cells (A549, H1299, H226Br), human colorectal carcinoma cells (SW620, DLD-1), human gastric cancer cells (MKN28), human esophageal cancer cells (T.Tn, TE8), human prostate cancer cells (LNCaP) and human hepatic cancer cells (HepG2), human H1299 xenograft mouse model | [198] |
Oncolytic adenovirus (ZD55-SATB1) | Docetaxel | Human prostate cancer cells (PC3 and DU145), PC3 xenograft | [203] |
Oncolytic Reovirus Type 3 Dearing (ReoT3D) | Docetaxel | Human prostate cancer cells (PC3 and DU145), PC3 xenograft | [191] |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
De, S.; Ehrlich, M. Arrest and Attack: Microtubule-Targeting Agents and Oncolytic Viruses Employ Complementary Mechanisms to Enhance Anti-Tumor Therapy Efficacy. Genes 2024, 15, 1193. https://doi.org/10.3390/genes15091193
De S, Ehrlich M. Arrest and Attack: Microtubule-Targeting Agents and Oncolytic Viruses Employ Complementary Mechanisms to Enhance Anti-Tumor Therapy Efficacy. Genes. 2024; 15(9):1193. https://doi.org/10.3390/genes15091193
Chicago/Turabian StyleDe, Sucheta, and Marcelo Ehrlich. 2024. "Arrest and Attack: Microtubule-Targeting Agents and Oncolytic Viruses Employ Complementary Mechanisms to Enhance Anti-Tumor Therapy Efficacy" Genes 15, no. 9: 1193. https://doi.org/10.3390/genes15091193