The Abscopal Effect in the Era of Checkpoint Inhibitors
Abstract
:1. Introduction
- insufficient tumour infiltration by tumour infiltrating lymphocytes (TILs) resulting in immunologically “cold” or “deserted” tumours [5];
- absence of PD-1-expressing T cells and only transient infiltration of PD-L1-expressing tumour-associated macrophages (TAMs) in metastasis, which might be documented in biopsies at the beginning of therapy [6];
- presence of an innate transcriptional “signature” of anti-PD-1 resistance (IPRES, innate PD-1 RESistance) [7];
2. Case Report
2.1. Patient
2.2. Patient Follow Up
2.3. Skin Biopsy and Immunohistochemistry
2.4. Blood Test, Tumour Markers
3. Discussion
4. Methods and Materials
4.1. Cryotherapy and Sample Collection
4.2. Immunohistochemistry
4.3. Serological Analysis and Blood Count
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
APCs | Antigen-presenting cells |
ATP | Adenosine triphosphate |
CD4 | Cluster of differentiation 4 |
CD8 | Cluster of differentiation 8 |
CD28 | Cluster of Differentiation 28 |
CD 40 | Cluster of differentiation 40 |
CD48 | Cluster of Differentiation 48 (B-lymphocyte activation marker) |
CD68 | Cluster of Differentiation 68 |
CD 80 | Cluster of differentiation 80 |
CRP | C-reactive protein |
CT | Computed Tomography |
CTLA-4 | Cytotoxic T-lymphocyte antigen 4, CD152 |
DAMPs | Damage-associated molecular patterns |
DAB | 3:3′-Diaminobenzidine |
DCs | Dendritic Cells |
Gy | Gray (unit) |
H&E | Hematoxylin eosin staining |
HMGB1 | HMGB1 |
HRP | horseradish peroxidase |
ICAM1 | Intercellular Adhesion Molecule 1 |
ICD | Immunogenic cell death |
IFNs | Interferons |
IFN-γ: | Interferon gamma |
IL | Interleukin |
IL-1β | Interleukin 1 beta |
IL-18 | Interleukin 18 |
IL-2: | Interleukin 2 |
IL-6: | Interleukin 6 |
IL-12β: | Interleukin 12 beta |
IPRES | Innate PD-1 RESistance |
LDH | Lactate dehydrogenase |
MHC | Major histocompatibility complex |
NK | Natural killer cell |
NRL | Neutrophil to lymphocyte ratio |
ORR | Objective response rate |
OS | Overall survival |
P2 × 7 | P2X purinoceptor 7 |
PBS | Phosphate-buffered saline |
PD-1 | Programed cell death 1, CD279 |
PFS | Progression free survival |
SD | Stable disease |
S100B | S100 calcium-binding protein B |
TAMs | Tumor-associated macrophages |
TILs | Tumor-infiltrating lymphocytes |
TNF-α. | Tumor necrosis factor alfa |
VCAM1 | Vascular cell adhesion protein 1 |
References
- Hodi, F.S.; O’Day, S.J.; McDermott, D.F.; Weber, R.W.; Sosman, J.A.; Haanen, J.B.; Gonzalez, R.; Robert, C.; Schadendorf, D.; Hassel, J.C.; et al. Improved Survival with Ipilimumab in Patients with Metastatic Melanoma. N. Engl. J. Med. 2010, 363, 711–723. [Google Scholar] [CrossRef]
- Larkin, J.; Chiarion-Sileni, V.; Gonzalez, R.; Grob, J.J.; Rutkowski, P.; Lao, C.D.; Cowey, C.L.; Schadendorf, D.; Wagstaff, J.; Dummer, R.; et al. Five-Year Survival with Combined Nivolumab and Ipilimumab in Advanced Melanoma. N. Engl. J. Med. 2019, 381, 1535–1546. [Google Scholar] [CrossRef] [Green Version]
- Jiang, T.; Shi, T.; Zhang, H.; Hu, J.; Song, Y.; Wei, J.; Ren, S.; Zhou, C. Tumor Neoantigens: From Basic Research to Clinical Applications. J. Hematol. Oncol. 2019, 12, 1–13. [Google Scholar] [CrossRef] [Green Version]
- Huang, J.; El-Gamil, M.; Dudley, M.E.; Li, Y.F.; Rosenberg, S.A.; Robbins, P.F. T Cells Associated with Tumor Regression Recognize Frameshifted Products of the CDKN2A Tumor Suppressor Gene Locus and a Mutated HLA Class I Gene Product. J. Immunol. 2004, 172, 6057–6064. [Google Scholar] [CrossRef] [Green Version]
- Bonaventura, P.; Shekarian, T.; Alcazer, V.; Valladeau-Guilemond, J.; Valsesia-Wittmann, S.; Amigorena, S.; Caux, C.; Depil, S. Cold Tumors: A Therapeutic Challenge for Immunotherapy. Front. Immunol. 2019, 10, 168. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nowicki, T.S.; Hu-Lieskovan, S.; Ribas, A. Mechanisms of Resistance to PD-1 and PD-L1 Blockade. Cancer J. 2018, 24, 47–53. [Google Scholar] [CrossRef] [PubMed]
- Hugo, W.; Zaretsky, J.M.; Sun, L.; Song, C.; Moreno, B.H.; Hu-Lieskovan, S.; Berent-Maoz, B.; Pang, J.; Chmielowski, B.; Cherry, G.; et al. Genomic and Transcriptomic Features of Response to Anti-PD-1 Therapy in Metastatic Melanoma. Cell 2016, 165, 35–44. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ayers, M.; Lunceford, J.; Nebozhyn, M.; Murphy, E.; Loboda, A.; Kaufman, D.R.; Albright, A.; Cheng, J.D.; Kang, S.P.; Shankaran, V.; et al. IFN-γ-Related MRNA Profile Predicts Clinical Response to PD-1 Blockade. J. Clin. Investig. 2017, 127, 2930–2940. [Google Scholar] [CrossRef]
- Vilain, R.E.; Menzies, A.M.; Wilmott, J.S.; Kakavand, H.; Madore, J.; Guminski, A.; Liniker, E.; Kong, B.Y.; Cooper, A.J.; Howle, J.R.; et al. Dynamic Changes in PD-L1 Expression and Immune Infiltrates Early during Treatment Predict Response to PD-1 Blockade in Melanoma. Clin. Cancer Res. 2017, 23, 5024–5033. [Google Scholar] [CrossRef] [Green Version]
- Snyder, A.; Makarov, V.; Merghoub, T.; Yuan, J.; Zaretsky, J.M.; Desrichard, A.; Walsh, L.A.; Postow, M.A.; Wong, P.; Ho, T.S.; et al. Genetic Basis for Clinical Response to CTLA-4 Blockade in Melanoma. N. Engl. J. Med. 2014, 371, 2189–2199. [Google Scholar] [CrossRef] [PubMed]
- Gao, J.; Shi, L.Z.; Zhao, H.; Chen, J.; Xiong, L.; He, Q.; Chen, T.; Roszik, J.; Bernatchez, C.; Woodman, S.E.; et al. Loss of IFN-γ Pathway Genes in Tumor Cells as a Mechanism of Resistance to Anti-CTLA-4 Therapy. Cell 2016, 167, 397–404. [Google Scholar] [CrossRef] [Green Version]
- McGranahan, N.; Furness, A.J.S.; Rosenthal, R.; Ramskov, S.; Lyngaa, R.; Saini, S.K.; Jamal-Hanjani, M.; Wilson, G.A.; Birkbak, N.J.; Hiley, C.T.; et al. Clonal Neoantigens Elicit T Cell Immunoreactivity and Sensitivity to Immune Checkpoint Blockade. Science 2016, 351, 1463–1469. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Greenman, C.; Stephens, P.; Smith, R.; Dalgliesh, G.L.; Hunter, C.; Bignell, G.; Davies, H.; Teague, J.; Butler, A.; Stevens, C.; et al. Patterns of Somatic Mutation in Human Cancer Genomes. Nature 2007, 446, 153–158. [Google Scholar] [CrossRef] [Green Version]
- Gros, A.; Parkhurst, M.R.; Tran, E.; Pasetto, A.; Robbins, P.F.; Ilyas, S.; Prickett, T.D.; Gartner, J.J.; Crystal, J.S.; Roberts, I.M.; et al. Prospective Identification of Neoantigen-Specific Lymphocytes in the Peripheral Blood of Melanoma Patients. Nat. Med. 2016, 22, 433–438. [Google Scholar] [CrossRef] [PubMed]
- Zhao, X.; Shao, C. Radiotherapy-Mediated Immunomodulation and Anti-Tumor Abscopal Effect Combining Immune Checkpoint Blockade. Cancers 2020, 12, 2762. [Google Scholar] [CrossRef]
- MOLE, R.H. Whole Body Irradiation; Radiobiology or Medicine? Br. J. Radiol. 1953, 26, 234–241. [Google Scholar] [CrossRef]
- Golden, E.B.; Demaria, S.; Schiff, P.B.; Chachoua, A.; Formenti, S.C. An Abscopal Response to Radiation and Ipilimumab in a Patient with Metastatic Non-Small Cell Lung Cancer. Cancer Immunol. Res. 2013, 1, 365–372. [Google Scholar] [CrossRef] [Green Version]
- Liu, Y.; Dong, Y.; Kong, L.; Shi, F.; Zhu, H.; Yu, J. Abscopal Effect of Radiotherapy Combined with Immune Checkpoint Inhibitors. J. Hematol. Oncol. 2018, 11, 1–15. [Google Scholar] [CrossRef] [Green Version]
- Chandra, R.A.; Wilhite, T.J.; Balboni, T.A.; Alexander, B.M.; Spektor, A.; Ott, P.A.; Ng, A.K.; Hodi, F.S.; Schoenfeld, J.D. A Systematic Evaluation of Abscopal Responses Following Radiotherapy in Patients with Metastatic Melanoma Treated with Ipilimumab. Oncoimmunology 2015, 4, 1–7. [Google Scholar] [CrossRef] [Green Version]
- Mukhopadhyay, A.; Wright, J.; Shirley, S.; Canton, D.A.; Burkart, C.; Connolly, R.J.; Campbell, J.S.; Pierce, R.H. Characterization of Abscopal Effects of Intratumoral Electroporation-Mediated IL-12 Gene Therapy. Gene Ther. 2019, 26, 1–15. [Google Scholar] [CrossRef] [PubMed]
- Iwai, T.; Oebisu, N.; Hoshi, M.; Orita, K.; Yamamoto, A.; Hamamoto, S.; Kageyama, K.; Nakamura, H. Promising Abscopal Effect of Combination Therapy with Thermal Tumour Ablation and Intratumoural OK-432 Injection in the Rat Osteosarcoma Model. Sci. Rep. 2020, 10, 9679. [Google Scholar] [CrossRef] [PubMed]
- Abdo, J.; Cornell, D.L.; Mittal, S.K.; Agrawal, D.K. Immunotherapy plus Cryotherapy: Potential Augmented Abscopal Effect for Advanced Cancers. Front. Oncol. 2018, 8, 85. [Google Scholar] [CrossRef] [PubMed]
- Tel, J.; Anguille, S.; Waterborg, C.E.J.; Smits, E.L.; Figdor, C.G.; de Vries, I.J.M. Tumoricidal Activity of Human Dendritic Cells. Trends Immunol. 2014, 35, 38–46. [Google Scholar] [CrossRef] [PubMed]
- Gerlinger, M.; Rowan, A.J.; Horswell, S.; Larkin, J.; Endesfelder, D.; Gronroos, E.; Martinez, P.; Matthews, N.; Stewart, A.; Tarpey, P.; et al. Intratumor Heterogeneity and Branched Evolution Revealed by Multiregion Sequencing. N. Engl. J. Med. 2012, 366, 883–892. [Google Scholar] [CrossRef] [Green Version]
- Mukherji, B. Immunology of Melanoma. Clin. Dermatol. 2013, 31, 156–165. [Google Scholar] [CrossRef]
- Lee, Y.; Auh, S.L.; Wang, Y.; Burnette, B.; Wang, Y.; Meng, Y.; Beckett, M.; Sharma, R.; Chin, R.; Tu, T.; et al. Therapeutic Effects of Ablative Radiation on Local Tumor Require CD8 + T Cells: Changing Strategies for Cancer Treatment. Blood 2009, 114, 589–595. [Google Scholar] [CrossRef] [PubMed]
- Demaria, S.; Ng, B.; Devitt, M.L.; Babb, J.S.; Kawashima, N.; Liebes, L.; Formenti, S.C. Ionizing Radiation Inhibition of Distant Untreated Tumors (Abscopal Effect) Is Immune Mediated. Int. J. Radiat. Oncol. Biol. Phys. 2004, 58, 862–870. [Google Scholar] [CrossRef]
- Ribas, A.; Dummer, R.; Puzanov, I.; VanderWalde, A.; Andtbacka, R.H.I.; Michielin, O.; Olszanski, A.J.; Malvehy, J.; Cebon, J.; Fernandez, E.; et al. Oncolytic Virotherapy Promotes Intratumoral T Cell Infiltration and Improves Anti-PD-1 Immunotherapy. Cell 2017, 170, 1109–1119.e10. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Marchini, A.; Daeffler, L.; Pozdeev, V.I.; Angelova, A.; Rommelaere, J. Immune Conversion of Tumor Microenvironment by Oncolytic Viruses: The Protoparvovirus H-1PV Case Study. Front. Immunol. 2019, 10, 1848. [Google Scholar] [CrossRef] [PubMed]
- Capone, M.; Giannarelli, D.; Mallardo, D.; Madonna, G.; Festino, L.; Grimaldi, A.M.; Vanella, V.; Simeone, E.; Paone, M.; Palmieri, G.; et al. Baseline Neutrophil-to-Lymphocyte Ratio (NLR) and Derived NLR Could Predict Overall Survival in Patients with Advanced Melanoma Treated with Nivolumab. J. Immunother. Cancer 2018, 6, 1–7. [Google Scholar] [CrossRef] [Green Version]
- Robert, C.; Thomas, L.; Bondarenko, I.; O’Day, S.; Weber, J.; Garbe, C.; Lebbe, C.; Baurain, J.-F.; Testori, A.; Grob, J.-J.; et al. Ipilimumab plus Dacarbazine for Previously Untreated Metastatic Melanoma. N. Engl. J. Med. 2011, 364, 2517–2526. [Google Scholar] [CrossRef] [Green Version]
- Schadendorf, D.; Hodi, F.S.; Robert, C.; Weber, J.S.; Margolin, K.; Hamid, O.; Patt, D.; Chen, T.T.; Berman, D.M.; Wolchok, J.D. Pooled Analysis of Long-Term Survival Data from Phase II and Phase III Trials of Ipilimumab in Unresectable or Metastatic Melanoma. J. Clin. Oncol. 2015, 33, 1889–1894. [Google Scholar] [CrossRef] [Green Version]
- Grimaldi, A.M.; Simeone, E.; Giannarelli, D.; Muto, P.; Falivene, S.; Borzillo, V.; Giugliano, F.M.; Sandomenico, F.; Petrillo, A.; Curvietto, M.; et al. Abscopal Effects of Radiotherapy on Advanced Melanoma Patients Who Progressed after Ipilimumab Immunotherapy. Oncoimmunology 2014, 3, e28780. [Google Scholar] [CrossRef]
- Liang, H.; Deng, L.; Chmura, S.; Burnette, B.; Liadis, N.; Darga, T.; Beckett, M.A.; Lingen, M.W.; Witt, M.; Weichselbaum, R.R.; et al. Radiation-Induced Equilibrium Is a Balance between Tumor Cell Proliferation and T Cell–Mediated Killing. J. Immunol. 2013, 190, 5874–5881. [Google Scholar] [CrossRef] [Green Version]
- Park, S.S.; Dong, H.; Liu, X.; Harrington, S.M.; Krco, C.J.; Grams, M.P.; Mansfield, A.S.; Furutani, K.M.; Olivier, K.R.; Kwon, E.D. PD-1 Restrains Radiotherapy-Induced Abscopal Effect. Cancer Immunol. Res. 2015, 3, 610–619. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pilones, K.A.; Kawashima, N.; Yang, A.M.; Babb, J.S.; Formenti, S.C.; Demaria, S. Invariant Natural Killer T Cells Regulate Breast Cancer Response to Radiation and CTLA-4 Blockade. Clin. Cancer Res. 2009, 15, 597–606. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Milano, M.T.; Katz, A.W.; Zhang, H.; Okunieff, P. Oligometastases Treated with Stereotactic Body Radiotherapy: Long-Term Follow-up of Prospective Study. Int. J. Radiat. Oncol. Biol. Phys. 2012, 83, 878–886. [Google Scholar] [CrossRef] [PubMed]
- Salama, J.K.; Hasselle, M.D.; Chmura, S.J.; Malik, R.; Mehta, N.; Yenice, K.M.; Villaflor, V.M.; Stadler, W.M.; Hoffman, P.C.; Cohen, E.E.W.; et al. Stereotactic Body Radiotherapy for Multisite Extracranial Oligometastases: Final Report of a Dose Escalation Trial in Patients with 1 to 5 Sites of Metastatic Disease. Cancer 2012, 118, 2962–2970. [Google Scholar] [CrossRef]
- Schreiber, R.D.; Old, L.J.; Smyth, M.J. Cancer Immunoediting: Integrating Immunity’s Roles in Cancer Suppression and Promotion. Science 2011, 331, 1565–1570. [Google Scholar] [CrossRef] [Green Version]
- Zhang, D.; Bi, J.; Liang, Q.; Wang, S.; Zhang, L.; Han, F.; Li, S.; Qiu, B.; Fan, X.; Chen, W.; et al. VCAM1 Promotes Tumor Cell Invasion and Metastasis by Inducing EMT and Transendothelial Migration in Colorectal Cancer. Front. Oncol. 2020, 10, 1066. [Google Scholar] [CrossRef]
- Johnson, J.P. Cell Adhesion Molecules in the Development and Progression of Malignant Melanoma. Cancer Metastasis Rev. 1999, 18, 345–357. [Google Scholar] [CrossRef]
- Reits, E.A.; Hodge, J.W.; Herberts, C.A.; Groothuis, T.A.; Chakraborty, M.; Wansley, E.K.; Camphausen, K.; Luiten, R.M.; De Ru, A.H.; Neijssen, J.; et al. Radiation Modulates the Peptide Repertoire, Enhances MHC Class I Expression, and Induces Successful Antitumor Immunotherapy. J. Exp. Med. 2006, 203, 1259–1271. [Google Scholar] [CrossRef] [PubMed]
- Chakraborty, M.; Abrams, S.I.; Camphausen, K.; Liu, K.; Scott, T.; Coleman, C.N.; Hodge, J.W. Irradiation of Tumor Cells Up-Regulates Fas and Enhances CTL Lytic Activity and CTL Adoptive Immunotherapy. J. Immunol. 2003, 170, 6338–6347. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fuertes, M.B.; Kacha, A.K.; Kline, J.; Woo, S.R.; Kranz, D.M.; Murphy, K.M.; Gajewski, T.F. Host Type I IFN Signals Are Required for Antitumor CD8+ T Cell Responses through CD8α+ Dendritic Cells. J. Exp. Med. 2011, 208, 2005–2016. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Grasso, C.S.; Tsoi, J.; Onyshchenko, M.; Abril-Rodriguez, G.; Ross-Macdonald, P.; Wind-Rotolo, M.; Champhekar, A.; Medina, E.; Torrejon, D.Y.; Shin, D.S.; et al. Conserved Interferon-γ Signaling Drives Clinical Response to Immune Checkpoint Blockade Therapy in Melanoma. Cancer Cell 2020, 38, 500–515.e3. [Google Scholar] [CrossRef] [PubMed]
- Zhou, J.; Wang, G.; Chen, Y.; Wang, H.; Hua, Y.; Cai, Z. Immunogenic Cell Death in Cancer Therapy: Present and Emerging Inducers. J. Cell. Mol. Med. 2019, 23, 4854–4865. [Google Scholar] [CrossRef] [PubMed]
- Gardai, S.J.; McPhillips, K.A.; Frasch, S.C.; Janssen, W.J.; Starefeldt, A.; Murphy-Ullrich, J.E.; Bratton, D.L.; Oldenborg, P.A.; Michalak, M.; Henson, P.M. Cell-Surface Calreticulin Initiates Clearance of Viable or Apoptotic Cells through Trans-Activation of LRP on the Phagocyte. Cell 2005, 123, 321–334. [Google Scholar] [CrossRef] [Green Version]
- Perregaux, D.G.; McNiff, P.; Laliberte, R.; Conklyn, M.; Gabel, C.A. ATP Acts as an Agonist to Promote Stimulus-Induced Secretion of IL-1β and IL-18 in Human Blood. J. Immunol. 2000, 165, 4615–4623. [Google Scholar] [CrossRef] [Green Version]
- Vijay, K. Toll-like Receptors in Immunity and Inflammatory Diseases: Past, Present, and Future. Int. Immunopharmacol. 2018, 59, 391–412. [Google Scholar] [CrossRef] [PubMed]
- Herrera, F.G.; Bourhis, J.; Coukos, G. Radiotherapy Combination Opportunities Leveraging Immunity for the next Oncology Practice. CA. Cancer J. Clin. 2017, 67, 65–85. [Google Scholar] [CrossRef]
- Pedicord, V.A.; Montalvo, W.; Leiner, I.M.; Allison, J.P. Single Dose of Anti-CTLA-4 Enhances CD8+ T-Cell Memory Formation, Function, and Maintenance. Proc. Natl. Acad. Sci. USA 2011, 108, 266–271. [Google Scholar] [CrossRef] [Green Version]
- Herbst, R.S.; Baas, P.; Kim, D.W.; Felip, E.; Pérez-Gracia, J.L.; Han, J.Y.; Molina, J.; Kim, J.H.; Arvis, C.D.; Ahn, M.J.; et al. Pembrolizumab versus Docetaxel for Previously Treated, PD-L1-Positive, Advanced Non-Small-Cell Lung Cancer (KEYNOTE-010): A Randomised Controlled Trial. Lancet 2016, 387, 1540–1550. [Google Scholar] [CrossRef]
- Long, G.V.; Larkin, J.; Ascierto, P.A.; Hodi, F.S.; Rutkowski, P.; Sileni, V.; Hassel, J.; Lebbe, C.; Pavlick, A.C.; Wagstaff, J.; et al. Melanoma and Other Skin Tumours 1112PD PD-L1 Expression as a Biomarker for Nivolumab (NIVO) plus Ipilimumab (IPI) and NIVO Alone in Advanced Melanoma (MEL): A Pooled Analysis. Ann. Oncol. 2016, 27, 379–400. [Google Scholar] [CrossRef]
- Deng, L.; Liang, H.; Burnette, B.; Beckett, M.; Darga, T.; Weichselbaum, R.R.; Fu, Y.X. Irradiation and Anti-PD-L1 Treatment Synergistically Promote Antitumor Immunity in Mice. J. Clin. Investig. 2014, 124, 687–695. [Google Scholar] [CrossRef] [PubMed]
- Tsui, J.M.; Mihalcioiu, C.; Cury, F.L. Abscopal Effect in a Stage IV Melanoma Patient Who Progressed on Pembrolizumab. Cureus 2018, 10, e2238. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tchanque-Fossuo, C.N.; Eisen, D.B. A Systematic Review on the Use of Cryotherapy versus Other Treatments for Basal Cell Carcinoma. Dermatol. Online J. 2018, 24. [Google Scholar] [CrossRef] [Green Version]
- Zeng, Y.; Hu, C.; Shu, L.; Pan, Y.; Zhao, L.; Pu, X.; Wu, F. Clinical Treatment Options for Early-Stage and Advanced Conjunctival Melanoma. Surv. Ophthalmol. 2020, 66, 461–470. [Google Scholar] [CrossRef]
- John, H.E.; Mahaffey, P.J. Laser Ablation and Cryotherapy of Melanoma Metastases. J. Surg. Oncol. 2014, 109, 296–300. [Google Scholar] [CrossRef]
- Bala, M.M.; Riemsma, R.P.; Wolff, R.; Kleijnen, J. Cryotherapy for Liver Metastases. Cochrane Database Syst. Rev. 2013, CD009058. [Google Scholar] [CrossRef] [Green Version]
- Slovak, R.; Ludwig, J.M.; Gettinger, S.N.; Herbst, R.S.; Kim, H.S. Immuno-Thermal Ablations–Boosting the Anticancer Immune Response. J. Immunother. Cancer 2017, 5, 1–15. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gazzaniga, S.; Bravo, A.; Goldszmid, S.R.; Maschi, F.; Martinelli, J.; Mordoh, J.; Wainstok, R. Inflammatory Changes after Cryosurgery-Induced Necrosis in Human Melanoma Xenografted in Nude Mice. J. Investig. Dermatol. 2001, 116, 664–671. [Google Scholar] [CrossRef] [Green Version]
- Liu, Y.C.; Zou, X.B.; Chai, Y.F.; Yao, Y.M. Macrophage Polarization in Inflammatory Diseases. Int. J. Biol. Sci. 2014, 10, 520–529. [Google Scholar] [CrossRef] [PubMed]
- Zhou, J.; Tang, Z.; Gao, S.; Li, C.; Feng, Y.; Zhou, X. Tumor-Associated Macrophages: Recent Insights and Therapies. Front. Oncol. 2020, 10, 188. [Google Scholar] [CrossRef]
- Gu, Y.; Srimathveeravalli, G.; Cai, L.; Ueshima, E.; Maybody, M.; Yarmohammadi, H.; Zhu, Y.S.; Durack, J.C.; Solomon, S.B.; Coleman, J.A.; et al. Pirfenidone Inhibits Cryoablation Induced Local Macrophage Infiltration along with Its Associated TGFb1 Expression and Serum Cytokine Level in a Mouse Model. Cryobiology 2018, 82, 106–111. [Google Scholar] [CrossRef]
- Takahashi, Y.; Izumi, Y.; Matsutani, N.; Dejima, H.; Nakayama, T.; Okamura, R.; Uehara, H.; Kawamura, M. Optimized Magnitude of Cryosurgery Facilitating Anti-Tumor Immunoreaction in a Mouse Model of Lewis Lung Cancer. Cancer Immunol. Immunother. 2016, 65, 973–982. [Google Scholar] [CrossRef] [PubMed]
- Den Brok, M.H.M.G.M.; Sutmuller, R.P.M.; Nierkens, S.; Bennink, E.J.; Toonen, L.W.J.; Figdor, C.G.; Ruers, T.J.M.; Adema, G.J. Synergy between in Situ Cryoablation and TLR9 Stimulation Results in a Highly Effective in Vivo Dendritic Cell Vaccine. Cancer Res. 2006, 66, 7285–7292. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lacina, L.; Kodet, O.; Dvořánková, B.; Szabo, P.; Smetana, K. Ecology of Melanoma Cell. Histol. Histopathol. 2018, 33, 247–254. [Google Scholar]
- Dvorak, H.F. Tumors: Wounds That Do Not Heal-Redux. Cancer Immunol. Res. 2015, 3, 1–11. [Google Scholar] [CrossRef] [Green Version]
- Jobe, N.P.; Živicová, V.; Mifková, A.; Rösel, D.; Dvořánková, B.; Kodet, O.; Strnad, H.; Kolář, M.; Šedo, A.; Smetana, K.; et al. Fibroblasts Potentiate Melanoma Cells in Vitro Invasiveness Induced by UV-Irradiated Keratinocytes. Histochem. Cell Biol. 2018, 149, 503–516. [Google Scholar] [CrossRef]
- Čoma, M.; Fröhlichová, L.; Urban, L.; Zajícĕk, R.; Urban, T.; Szabo, P.; Novák, Š.; Fetissov, V.; Dvořánková, B.; Smetana, K.; et al. Molecular Changes Underlying Hypertrophic Scarring Following Burns Involve Specific Deregulations at Allwound Healing Stages (Inflammation, Proliferation and Maturation). Int. J. Mol. Sci. 2021, 22, 897. [Google Scholar] [CrossRef]
- Ressler, J.M.; Karasek, M.; Koch, L.; Silmbrod, R.; Mangana, J.; Latifyan, S.; Aedo-Lopez, V.; Kehrer, H.; Weihsengruber, F.; Koelblinger, P.; et al. Real-Life Use of Talimogene Laherparepvec (T-VEC) in Melanoma Patients in Centers in Austria, Switzerland and Germany. J. Immunother. Cancer 2021, 9, e001701. [Google Scholar] [CrossRef] [PubMed]
- Kepp, O.; Marabelle, A.; Zitvogel, L.; Kroemer, G. Oncolysis without Viruses–Inducing Systemic Anticancer Immune Responses with Local Therapies. Nat. Rev. Clin. Oncol. 2020, 17, 49–64. [Google Scholar] [CrossRef] [PubMed]
Serological Analysis | Lower Value Limit | Uper Value Limit | Critical Value Limit | Units |
---|---|---|---|---|
S100B | 0.00 | 0.11 | 1 | g/L |
LDH | 2.20 | 3.80 | 15.00 | μkat/L |
CRP | 0.00 | 5.50 | 100.00 | mg/L |
Blood count | ||||
Neutrophils abs | 2.00 | 7.00 | 50.00 | 109/L |
Lymphocytes abs | 0.80 | 4.00 | 7.20 | 109/L |
Primary Antibody (Clone No.) | Supplier (Location) |
---|---|
MiTF (Clone D5), MoMoAb, 1:100 | Dako, Agilent Technologies, Inc. (Santa Clara, CA, USA) |
HMB45 (Clone HMB-45), MoMoAb, 1:100 | |
MiTF (Clone D5), MoMoAb, 1:100 | |
MELAN A (A103), MoMoAb, 1:100 | |
CD68 (M0814), MoMoAb, 1:100 | |
CD45 (SAB4502541) RaMoAb, 1:200 | Sigma-Aldrich, Prague, Czech Republic |
CD8 (Clone SP239), RaMoAb, 1:100 | |
Secondary Antibody (Clone No.) | Supplier (Location) |
N-Histofine Simple Stain MAX PO (414152F) | EXBIO Prague s.r.o. (Prague, Czech Republic) |
Chromogen | Supplier (Location) |
DAB (3,3′-Diaminobenzidine) | Dako, Agilent Technologies, Inc. (Santa Clara, CA, USA) |
MoMoAb, Mouse Monoclonal Antibody; RaMoAb, Rabbit Monoclonal Antibody; RaPoAb, Rabbit Polyclonal Antibody |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 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
Kodet, O.; Němejcova, K.; Strnadová, K.; Havlínová, A.; Dundr, P.; Krajsová, I.; Štork, J.; Smetana, K., Jr.; Lacina, L. The Abscopal Effect in the Era of Checkpoint Inhibitors. Int. J. Mol. Sci. 2021, 22, 7204. https://doi.org/10.3390/ijms22137204
Kodet O, Němejcova K, Strnadová K, Havlínová A, Dundr P, Krajsová I, Štork J, Smetana K Jr., Lacina L. The Abscopal Effect in the Era of Checkpoint Inhibitors. International Journal of Molecular Sciences. 2021; 22(13):7204. https://doi.org/10.3390/ijms22137204
Chicago/Turabian StyleKodet, Ondřej, Kristýna Němejcova, Karolína Strnadová, Andrea Havlínová, Pavel Dundr, Ivana Krajsová, Jiří Štork, Karel Smetana, Jr., and Lukáš Lacina. 2021. "The Abscopal Effect in the Era of Checkpoint Inhibitors" International Journal of Molecular Sciences 22, no. 13: 7204. https://doi.org/10.3390/ijms22137204
APA StyleKodet, O., Němejcova, K., Strnadová, K., Havlínová, A., Dundr, P., Krajsová, I., Štork, J., Smetana, K., Jr., & Lacina, L. (2021). The Abscopal Effect in the Era of Checkpoint Inhibitors. International Journal of Molecular Sciences, 22(13), 7204. https://doi.org/10.3390/ijms22137204