Plant-Based Products Originating from Serbia That Affect P-glycoprotein Activity
Abstract
:1. Drug Resistance in Cancer Therapy
1.1. P-gp Role and Regulation in Cellular Physiology
1.2. P-gp Role in Cancer Therapy and Efforts to Overcome Multidrug Resistance
2. Modulation of P-gp Activity by Natural Product Drugs
2.1. Sesquiterpenoids
2.1.1. Genus Artemisia
2.1.2. Genus Curcuma
2.1.3. Genus Ferula
2.1.4. Genus Inula
2.1.5. Genus Petasites
2.1.6. Genus Celastrus
2.2. Diterpenoids
2.2.1. Genus Salvia
2.2.2. Genus Euphorbia
E. nicaeensis All.
E. dendroides L.
E. esula L.
E. helioscopia L.
E. sororia A. Schrenk
E. glomerulans Prokh.
2.3. Chalcones
2.3.1. Genus Piper
2.3.2. Genus Helichrysum
2.3.3. Genus Glycyrrhiza
2.3.4. Genus Cullen
2.3.5. Genus Artemisia
2.3.6. Genus Humulus
2.4. Riccardins
2.5. Diarylheptanoids
2.5.1. Genus Alnus
2.5.2. Genus Curcuma
Classes of Natural Products | P-gp Inhibitors and MDR Modulators | Derivatives | Additional Biological Activities * | Origin |
---|---|---|---|---|
sesquiterpenoids |
| Genus Artemisia | ||
|
|
| ||
Genus Curcuma | ||||
Genus Ferula | ||||
Genus Inula | ||||
Genus Petasites | ||||
| Genus Celastrus | |||
diterpenoids |
| Genus Salvia | ||
| Genus Euphorbia | |||
chalcones | Genus Piper | |||
Genus Helichrysum | ||||
| Genus Glycyrrhiza | |||
| Genus Cullen | |||
| Genus Artemisia | |||
| Genus Humulus | |||
riccardins | Genera Lunularia, Monoclea, Dumortiera, Plagiochila, and Primula | |||
diarylheptanoids |
| Genus Alnus | ||
Genus Curcuma |
3. Novel Perspectives with Naturally Derived P-Glycoprotein Inhibitors
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Gottesman, M.M.; Lavi, O.; Hall, M.D.; Gillet, J.P. Toward a Better Understanding of the Complexity of Cancer Drug Resistance. Annu. Rev. Pharmacol. Toxicol. 2016, 56, 85–102. [Google Scholar] [CrossRef] [PubMed]
- Zhitomirsky, B.; Assaraf, Y.G. Lysosomes as mediators of drug resistance in cancer. Drug Resist. Updat. 2016, 24, 23–33. [Google Scholar] [CrossRef] [PubMed]
- Gottesman, M.M. Mechanisms of cancer drug resistance. Annu. Rev. Med. 2002, 53, 615–627. [Google Scholar] [CrossRef] [PubMed]
- Ikediobi, O.N. Somatic pharmacogenomics in cancer. Pharmacogenom. J. 2008, 8, 305–314. [Google Scholar] [CrossRef]
- Valente, A.; Podolski-Renic, A.; Poetsch, I.; Filipovic, N.; Lopez, O.; Turel, I.; Heffeter, P. Metal- and metalloid-based compounds to target and reverse cancer multidrug resistance. Drug Resist. Updat. 2021, 58, 100778. [Google Scholar] [CrossRef]
- Assaraf, Y.G.; Brozovic, A.; Goncalves, A.C.; Jurkovicova, D.; Line, A.; Machuqueiro, M.; Saponara, S.; Sarmento-Ribeiro, A.B.; Xavier, C.P.R.; Vasconcelos, M.H. The multi-factorial nature of clinical multidrug resistance in cancer. Drug Resist. Updat. 2019, 46, 100645. [Google Scholar] [CrossRef]
- Cui, Q.; Wang, J.Q.; Assaraf, Y.G.; Ren, L.; Gupta, P.; Wei, L.; Ashby, C.R., Jr.; Yang, D.H.; Chen, Z.S. Modulating ROS to overcome multidrug resistance in cancer. Drug Resist. Updat. 2018, 41, 1–25. [Google Scholar] [CrossRef]
- Juvale, I.I.A.; Abdul Hamid, A.A.; Abd Halim, K.B.; Che Has, A.T. P-glycoprotein: New insights into structure, physiological function, regulation and alterations in disease. Heliyon 2022, 8, e09777. [Google Scholar] [CrossRef]
- Prachayasittikul, V.; Prachayasittikul, V. P-glycoprotein transporter in drug development. EXCLI J. 2016, 15, 113–118. [Google Scholar] [CrossRef]
- Borst, P.; Elferink, R.O. Mammalian ABC transporters in health and disease. Annu. Rev. Biochem. 2002, 71, 537–592. [Google Scholar] [CrossRef]
- Bottova, I.; Hehl, A.B.; Stefanic, S.; Fabrias, G.; Casas, J.; Schraner, E.; Pieters, J.; Sonda, S. Host cell P-glycoprotein is essential for cholesterol uptake and replication of Toxoplasma gondii. J. Biol. Chem. 2009, 284, 17438–17448. [Google Scholar] [CrossRef]
- Foucaud-Vignault, M.; Soayfane, Z.; Menez, C.; Bertrand-Michel, J.; Martin, P.G.; Guillou, H.; Collet, X.; Lespine, A. P-glycoprotein dysfunction contributes to hepatic steatosis and obesity in mice. PLoS ONE 2011, 6, e23614. [Google Scholar] [CrossRef]
- Hartmann, G.; Vassileva, V.; Piquette-Miller, M. Impact of endotoxin-induced changes in P-glycoprotein expression on disposition of doxorubicin in mice. Drug Metab. Dispos. 2005, 33, 820–828. [Google Scholar] [CrossRef]
- Heemskerk, S.; Wouterse, A.C.; Russel, F.G.; Masereeuw, R. Nitric oxide down-regulates the expression of organic cation transporters (OCT) 1 and 2 in rat kidney during endotoxemia. Eur. J. Pharmacol. 2008, 584, 390–397. [Google Scholar] [CrossRef] [PubMed]
- Noack, A.; Gericke, B.; von Kockritz-Blickwede, M.; Menze, A.; Noack, S.; Gerhauser, I.; Osten, F.; Naim, H.Y.; Loscher, W. Mechanism of drug extrusion by brain endothelial cells via lysosomal drug trapping and disposal by neutrophils. Proc. Natl. Acad. Sci. USA 2018, 115, E9590–E9599. [Google Scholar] [CrossRef] [PubMed]
- Su, L.; Mruk, D.D.; Lui, W.Y.; Lee, W.M.; Cheng, C.Y. P-glycoprotein regulates blood-testis barrier dynamics via its effects on the occludin/zonula occludens 1 (ZO-1) protein complex mediated by focal adhesion kinase (FAK). Proc. Natl. Acad. Sci. USA 2011, 108, 19623–19628. [Google Scholar] [CrossRef]
- Dunk, C.E.; Pappas, J.J.; Lye, P.; Kibschull, M.; Javam, M.; Bloise, E.; Lye, S.J.; Szyf, M.; Matthews, S.G. P-Glycoprotein (P-gp)/ABCB1 plays a functional role in extravillous trophoblast (EVT) invasion and is decreased in the pre-eclamptic placenta. J. Cell Mol. Med. 2018, 22, 5378–5393. [Google Scholar] [CrossRef]
- Kim, Y.; Chen, J. Molecular structure of human P-glycoprotein in the ATP-bound, outward-facing conformation. Science 2018, 359, 915–919. [Google Scholar] [CrossRef]
- Kodan, A.; Yamaguchi, T.; Nakatsu, T.; Sakiyama, K.; Hipolito, C.J.; Fujioka, A.; Hirokane, R.; Ikeguchi, K.; Watanabe, B.; Hiratake, J.; et al. Structural basis for gating mechanisms of a eukaryotic P-glycoprotein homolog. Proc. Natl. Acad. Sci. USA 2014, 111, 4049–4054. [Google Scholar] [CrossRef] [PubMed]
- Pluchino, K.M.; Hall, M.D.; Moen, J.K.; Chufan, E.E.; Fetsch, P.A.; Shukla, S.; Gill, D.R.; Hyde, S.C.; Xia, D.; Ambudkar, S.V.; et al. Human-Mouse Chimeras with Normal Expression and Function Reveal That Major Domain Swapping Is Tolerated by P-Glycoprotein (ABCB1). Biochemistry 2016, 55, 1010–1023. [Google Scholar] [CrossRef]
- Kodan, A.; Yamaguchi, T.; Nakatsu, T.; Matsuoka, K.; Kimura, Y.; Ueda, K.; Kato, H. Inward- and outward-facing X-ray crystal structures of homodimeric P-glycoprotein CmABCB1. Nat. Commun. 2019, 10, 88. [Google Scholar] [CrossRef] [PubMed]
- Scotto, K.W. Transcriptional regulation of ABC drug transporters. Oncogene 2003, 22, 7496–7511. [Google Scholar] [CrossRef] [PubMed]
- Shen, H.; Xu, W.; Luo, W.; Zhou, L.; Yong, W.; Chen, F.; Wu, C.; Chen, Q.; Han, X. Upregulation of mdr1 gene is related to activation of the MAPK/ERK signal transduction pathway and YB-1 nuclear translocation in B-cell lymphoma. Exp. Hematol. 2011, 39, 558–569. [Google Scholar] [CrossRef]
- Chen, Q.; Bian, Y.; Zeng, S. Involvement of AP-1 and NF-kappaB in the up-regulation of P-gp in vinblastine resistant Caco-2 cells. Drug Metab. Pharmacokinet. 2014, 29, 223–226. [Google Scholar] [CrossRef] [PubMed]
- Li, X.; Mu, P.; Qiao, H.; Wen, J.; Deng, Y. JNK-AKT-NF-kappaB controls P-glycoprotein expression to attenuate the cytotoxicity of deoxynivalenol in mammalian cells. Biochem. Pharmacol. 2018, 156, 120–134. [Google Scholar] [CrossRef]
- Feng, D.D.; Zhang, H.; Zhang, P.; Zheng, Y.S.; Zhang, X.J.; Han, B.W.; Luo, X.Q.; Xu, L.; Zhou, H.; Qu, L.H.; et al. Down-regulated miR-331-5p and miR-27a are associated with chemotherapy resistance and relapse in leukaemia. J. Cell Mol. Med. 2011, 15, 2164–2175. [Google Scholar] [CrossRef]
- Ikemura, K.; Yamamoto, M.; Miyazaki, S.; Mizutani, H.; Iwamoto, T.; Okuda, M. MicroRNA-145 post-transcriptionally regulates the expression and function of P-glycoprotein in intestinal epithelial cells. Mol. Pharmacol. 2013, 83, 399–405. [Google Scholar] [CrossRef]
- Zhu, X.; Li, Y.; Shen, H.; Li, H.; Long, L.; Hui, L.; Xu, W. miR-137 restoration sensitizes multidrug-resistant MCF-7/ADM cells to anticancer agents by targeting YB-1. Acta Biochim. Biophys. Sin. 2013, 45, 80–86. [Google Scholar] [CrossRef]
- Stankovic, T.; Dinic, J.; Podolski-Renic, A.; Musso, L.; Buric, S.S.; Dallavalle, S.; Pesic, M. Dual Inhibitors as a New Challenge for Cancer Multidrug Resistance Treatment. Curr. Med. Chem. 2019, 26, 6074–6106. [Google Scholar] [CrossRef]
- Dinic, J.; Podolski-Renic, A.; Jeremic, M.; Pesic, M. Potential of Natural-Based Anticancer Compounds for P-Glycoprotein Inhibition. Curr. Pharm. Des. 2018, 24, 4334–4354. [Google Scholar] [CrossRef]
- Begicevic, R.R.; Falasca, M. ABC Transporters in Cancer Stem Cells: Beyond Chemoresistance. Int. J. Mol. Sci. 2017, 18, 2362. [Google Scholar] [CrossRef] [PubMed]
- Ambudkar, S.V.; Kimchi-Sarfaty, C.; Sauna, Z.E.; Gottesman, M.M. P-glycoprotein: From genomics to mechanism. Oncogene 2003, 22, 7468–7485. [Google Scholar] [CrossRef] [PubMed]
- Leith, C.P.; Kopecky, K.J.; Chen, I.M.; Eijdems, L.; Slovak, M.L.; McConnell, T.S.; Head, D.R.; Weick, J.; Grever, M.R.; Appelbaum, F.R.; et al. Frequency and clinical significance of the expression of the multidrug resistance proteins MDR1/P-glycoprotein, MRP1, and LRP in acute myeloid leukemia: A Southwest Oncology Group Study. Blood 1999, 94, 1086–1099. [Google Scholar]
- Berger, W.; Setinek, U.; Hollaus, P.; Zidek, T.; Steiner, E.; Elbling, L.; Cantonati, H.; Attems, J.; Gsur, A.; Micksche, M. Multidrug resistance markers P-glycoprotein, multidrug resistance protein 1, and lung resistance protein in non-small cell lung cancer: Prognostic implications. J. Cancer Res. Clin. Oncol. 2005, 131, 355–363. [Google Scholar] [CrossRef] [PubMed]
- Yokoyama, H.; Ishida, T.; Sugio, K.; Inoue, T.; Sugimachi, K. Immunohistochemical evidence that P-glycoprotein in non-small cell lung cancers is associated with shorter survival. Surg. Today 1999, 29, 1141–1147. [Google Scholar] [CrossRef]
- Toth, K.; Vaughan, M.M.; Peress, N.S.; Slocum, H.K.; Rustum, Y.M. MDR1 P-glycoprotein is expressed by endothelial cells of newly formed capillaries in human gliomas but is not expressed in the neovasculature of other primary tumors. Am. J. Pathol. 1996, 149, 853–858. [Google Scholar]
- Henson, J.W.; Cordon-Cardo, C.; Posner, J.B. P-glycoprotein expression in brain tumors. J. Neurooncol. 1992, 14, 37–43. [Google Scholar] [CrossRef] [PubMed]
- Demeule, M.; Shedid, D.; Beaulieu, E.; Del Maestro, R.F.; Moghrabi, A.; Ghosn, P.B.; Moumdjian, R.; Berthelet, F.; Beliveau, R. Expression of multidrug-resistance P-glycoprotein (MDR1) in human brain tumors. Int. J. Cancer 2001, 93, 62–66. [Google Scholar] [CrossRef]
- Nanayakkara, A.K.; Follit, C.A.; Chen, G.; Williams, N.S.; Vogel, P.D.; Wise, J.G. Targeted inhibitors of P-glycoprotein increase chemotherapeutic-induced mortality of multidrug resistant tumor cells. Sci. Rep. 2018, 8, 967. [Google Scholar] [CrossRef]
- Saitoh, H.; Saikachi, Y.; Kobayashi, M.; Yamaguchi, M.; Oda, M.; Yuhki, Y.; Achiwa, K.; Tadano, K.; Takahashi, Y.; Aungst, B.J. Limited interaction between tacrolimus and P-glycoprotein in the rat small intestine. Eur. J. Pharm. Sci. 2006, 28, 34–42. [Google Scholar] [CrossRef]
- Palmeira, A.; Sousa, E.; Vasconcelos, M.H.; Pinto, M.M. Three decades of P-gp inhibitors: Skimming through several generations and scaffolds. Curr. Med. Chem. 2012, 19, 1946–2025. [Google Scholar] [CrossRef] [PubMed]
- Varma, M.V.; Ashokraj, Y.; Dey, C.S.; Panchagnula, R. P-glycoprotein inhibitors and their screening: A perspective from bioavailability enhancement. Pharmacol. Res. 2003, 48, 347–359. [Google Scholar] [CrossRef] [PubMed]
- Tamaki, A.; Ierano, C.; Szakacs, G.; Robey, R.W.; Bates, S.E. The controversial role of ABC transporters in clinical oncology. Essays Biochem. 2011, 50, 209–232. [Google Scholar] [CrossRef]
- Cripe, L.D.; Uno, H.; Paietta, E.M.; Litzow, M.R.; Ketterling, R.P.; Bennett, J.M.; Rowe, J.M.; Lazarus, H.M.; Luger, S.; Tallman, M.S. Zosuquidar, a novel modulator of P-glycoprotein, does not improve the outcome of older patients with newly diagnosed acute myeloid leukemia: A randomized, placebo-controlled trial of the Eastern Cooperative Oncology Group 3999. Blood 2010, 116, 4077–4085. [Google Scholar] [CrossRef]
- Rolnik, A.; Olas, B. The Plants of the Asteraceae Family as Agents in the Protection of Human Health. Int. J. Mol. Sci. 2021, 22, 3009. [Google Scholar] [CrossRef] [PubMed]
- Crawford, D.; Kelly, J.; Anderson, G. Reproductive Biology of Asteraceae on Oceanic Islands. Bot. Rev. 2023, 90, 67–108. [Google Scholar] [CrossRef]
- Septembre-Malaterre, A.; Lalarizo Rakoto, M.; Marodon, C.; Bedoui, Y.; Nakab, J.; Simon, E.; Hoarau, L.; Savriama, S.; Strasberg, D.; Guiraud, P.; et al. Artemisia annua, a Traditional Plant Brought to Light. Int. J. Mol. Sci. 2020, 21, 4986. [Google Scholar] [CrossRef]
- Tu, Y. Artemisinin-A Gift from Traditional Chinese Medicine to the World (Nobel Lecture). Angew. Chem. Int. Ed. Engl. 2016, 55, 10210–10226. [Google Scholar] [CrossRef]
- Wong, Y.K.; Xu, C.; Kalesh, K.A.; He, Y.; Lin, Q.; Wong, W.S.F.; Shen, H.M.; Wang, J. Artemisinin as an anticancer drug: Recent advances in target profiling and mechanisms of action. Med. Res. Rev. 2017, 37, 1492–1517. [Google Scholar] [CrossRef]
- Xu, C.; Zhang, H.; Mu, L.; Yang, X. Artemisinins as Anticancer Drugs: Novel Therapeutic Approaches, Molecular Mechanisms, and Clinical Trials. Front. Pharmacol. 2020, 11, 529881. [Google Scholar] [CrossRef]
- Wang, Y.; Li, Y.; Shang, D.; Efferth, T. Interactions between artemisinin derivatives and P-glycoprotein. Phytomedicine 2019, 60, 152998. [Google Scholar] [CrossRef]
- Chen, L.; Wang, C.; Hu, N.; Zhao, H. Artesunate enhances adriamycin cytotoxicity by inhibiting glycolysis in adriamycin-resistant chronic myeloid leukemia K562/ADR cells. RSC Adv. 2019, 9, 1004–1014. [Google Scholar] [CrossRef] [PubMed]
- Koračak, L.; Lupšić, E.; Jovanović, N.T.; Jovanović, M.; Novakovic, M.; Nedialkov, P.; Trendafilova, A.; Zlatović, M.; Pešić, M.; Opsenica, I.M. Novel artesunate–pyrimidine-based hybrids with anticancer potential against multidrug-resistant cancer cells. New J. Chem. 2023, 47, 6844–6855. [Google Scholar] [CrossRef]
- Oga, E.F.; Sekine, S.; Shitara, Y.; Horie, T. Potential P-glycoprotein-mediated drug-drug interactions of antimalarial agents in Caco-2 cells. Am. J. Trop. Med. Hyg. 2012, 87, 64–69. [Google Scholar] [CrossRef] [PubMed]
- Zhang, L.; Chen, F.; Zhang, Z.; Chen, Y.; Wang, J. Synthesis and biological evaluation of a novel artesunate-podophyllotoxin conjugate as anticancer agent. Bioorg Med. Chem. Lett. 2016, 26, 38–42. [Google Scholar] [CrossRef]
- Di Sotto, A.; Irannejad, H.; Eufemi, M.; Mancinelli, R.; Abete, L.; Mammola, C.L.; Altieri, F.; Mazzanti, G.; Di Giacomo, S. Potentiation of Low-Dose Doxorubicin Cytotoxicity by Affecting P-Glycoprotein through Caryophyllane Sesquiterpenes in HepG2 Cells: An in Vitro and in Silico Study. Int. J. Mol. Sci. 2020, 21, 633. [Google Scholar] [CrossRef]
- Fuloria, S.; Mehta, J.; Chandel, A.; Sekar, M.; Rani, N.; Begum, M.Y.; Subramaniyan, V.; Chidambaram, K.; Thangavelu, L.; Nordin, R.; et al. A Comprehensive Review on the Therapeutic Potential of Curcuma longa Linn. in Relation to its Major Active Constituent Curcumin. Front. Pharmacol. 2022, 13, 820806. [Google Scholar] [CrossRef] [PubMed]
- Yue, G.G.; Cheng, S.W.; Yu, H.; Xu, Z.S.; Lee, J.K.; Hon, P.M.; Lee, M.Y.; Kennelly, E.J.; Deng, G.; Yeung, S.K.; et al. The role of turmerones on curcumin transportation and P-glycoprotein activities in intestinal Caco-2 cells. J. Med. Food 2012, 15, 242–252. [Google Scholar] [CrossRef]
- Zhu, X.Y.; Guo, D.W.; Lao, Q.C.; Xu, Y.Q.; Meng, Z.K.; Xia, B.; Yang, H.; Li, C.Q.; Li, P. Sensitization and synergistic anti-cancer effects of Furanodiene identified in zebrafish models. Sci. Rep. 2019, 9, 4541. [Google Scholar] [CrossRef]
- Zhang, Y.; Mu, X.D.; Li, E.Z.; Luo, Y.; Song, N.; Qu, X.J.; Hu, X.J.; Liu, Y.P. The role of E3 ubiquitin ligase Cbl proteins in beta-elemene reversing multi-drug resistance of human gastric adenocarcinoma cells. Int. J. Mol. Sci. 2013, 14, 10075–10089. [Google Scholar] [CrossRef]
- Deng, M.; Liu, B.; Song, H.; Yu, R.; Zou, D.; Chen, Y.; Ma, Y.; Lv, F.; Xu, L.; Zhang, Z.; et al. beta-Elemene inhibits the metastasis of multidrug-resistant gastric cancer cells through miR-1323/Cbl-b/EGFR pathway. Phytomedicine 2020, 69, 153184. [Google Scholar] [CrossRef] [PubMed]
- Tang, C.Y.; Zhu, L.X.; Yu, J.D.; Chen, Z.; Gu, M.C.; Mu, C.F.; Liu, Q.; Xiong, Y. Effect of beta-elemene on the kinetics of intracellular transport of d-luciferin potassium salt (ABC substrate) in doxorubicin-resistant breast cancer cells and the associated molecular mechanism. Eur. J. Pharm. Sci. 2018, 120, 20–29. [Google Scholar] [CrossRef] [PubMed]
- Mohammadhosseini, M.; Venditti, A.; Sarker, S.D.; Nahar, L.; Akbarzadeh, A. The genus Ferula: Ethnobotany, phytochemistry and bioactivities—A review. Ind. Crops Prod. 2019, 129, 350–394. [Google Scholar] [CrossRef]
- Kasaian, J.; Mosaffa, F.; Behravan, J.; Masullo, M.; Piacente, S.; Ghandadi, M.; Iranshahi, M. Reversal of P-glycoprotein-mediated multidrug resistance in MCF-7/Adr cancer cells by sesquiterpene coumarins. Fitoterapia 2015, 103, 149–154. [Google Scholar] [CrossRef]
- Fischedick, J.T.; Pesic, M.; Podolski-Renic, A.; Bankovic, J.; de Vos, R.C.H.; Perić, M.; Todorović, S.; Tanic, N. Cytotoxic activity of sesquiterpene lactones from Inula britannica on human cancer cell lines. Phytochem. Lett. 2013, 6, 246–252. [Google Scholar] [CrossRef]
- Peng, Z.; Wang, Y.; Fan, J.; Lin, X.; Liu, C.; Xu, Y.; Ji, W.; Yan, C.; Su, C. Costunolide and dehydrocostuslactone combination treatment inhibit breast cancer by inducing cell cycle arrest and apoptosis through c-Myc/p53 and AKT/14-3-3 pathway. Sci. Rep. 2017, 7, 41254. [Google Scholar] [CrossRef]
- Cai, H.; Li, L.; Jiang, J.; Zhao, C.; Yang, C. Costunolide enhances sensitivity of K562/ADR chronic myeloid leukemia cells to doxorubicin through PI3K/Akt pathway. Phytother. Res. 2019, 33, 1683–1688. [Google Scholar] [CrossRef]
- Yami, A.; Hamzeloo-Moghadam, M.; Darbandi, A.; Karami, A.; Mashati, P.; Takhviji, V.; Gharehbaghian, A. Ergolide, a potent sesquiterpene lactone induces cell cycle arrest along with ROS-dependent apoptosis and potentiates vincristine cytotoxicity in ALL cell lines. J. Ethnopharmacol. 2020, 253, 112504. [Google Scholar] [CrossRef]
- Ding, Y.; Wang, T.; Chen, T.; Xie, C.; Zhang, Q. Sesquiterpenoids isolated from the flower of Inula japonica as potential antitumor leads for intervention of paclitaxel-resistant non-small-cell lung cancer. Bioorg Chem. 2020, 101, 103973. [Google Scholar] [CrossRef]
- Kulinowski, L.; Luca, S.V.; Minceva, M.; Skalicka-Wozniak, K. A review on the ethnobotany, phytochemistry, pharmacology and toxicology of butterbur species (Petasites L.). J. Ethnopharmacol. 2022, 293, 115263. [Google Scholar] [CrossRef]
- Lin, Y.L.; Mei, C.H.; Huang, S.L.; Kuo, Y.H. Four new sesquiterpenes from Petasites formosanus. J. Nat. Prod. 1998, 61, 887–890. [Google Scholar] [CrossRef] [PubMed]
- Abdelfatah, S.; Bockers, M.; Asensio, M.; Kadioglu, O.; Klinger, A.; Fleischer, E.; Efferth, T. Isopetasin and S-isopetasin as novel P-glycoprotein inhibitors against multidrug-resistant cancer cells. Phytomedicine 2021, 86, 153196. [Google Scholar] [CrossRef] [PubMed]
- Shen, Y.; Chen, B.L.; Zhang, Q.X.; Zheng, Y.Z.; Fu, Q. Traditional uses, secondary metabolites, and pharmacology of Celastrus species—A review. J. Ethnopharmacol. 2019, 241, 111934. [Google Scholar] [CrossRef]
- Callies, O.; Sanchez-Canete, M.P.; Gamarro, F.; Jimenez, I.A.; Castanys, S.; Bazzocchi, I.L. Optimization by Molecular Fine Tuning of Dihydro-beta-agarofuran Sesquiterpenoids as Reversers of P-Glycoprotein-Mediated Multidrug Resistance. J. Med. Chem. 2016, 59, 1880–1890. [Google Scholar] [CrossRef]
- Randjelovic, M.; Zlatković, B.; Jovanovic, M.; Miladinovic, B.; Milutinović, M.; Pavlovic, D.; Branković, S.; Kitic, D. Morphological and anatomical analysis of the clary sage herbal drug (Salviae sclareae herba). Lekovite Sirovine 2022, 42, 24–33. [Google Scholar] [CrossRef]
- Jaric, S.; Macukanovic-Jocic, M.; Djurdjevic, L.; Mitrovic, M.; Kostic, O.; Karadzic, B.; Pavlovic, P. An ethnobotanical survey of traditionally used plants on Suva planina mountain (south-eastern Serbia). J. Ethnopharmacol. 2015, 175, 93–108. [Google Scholar] [CrossRef]
- Afshari, H.; Nourbakhsh, M.; Salehi, N.; Mahboubi-Rabbani, M.; Zarghi, A.; Noori, S. STAT3-mediated Apoptotic-enhancing Function of Sclareol Against Breast Cancer Cells and Cell Sensitization to Cyclophosphamide. Iran. J. Pharm. Res. 2020, 19, 398–412. [Google Scholar] [CrossRef]
- Bordbar-Bonab, S.; Mahbob, S.; Vahed-Jabari, M.; Dolatkhah, H. The effect of Sclareol on the expression of MDR-1 gene and Glycoprotein-P Level in MKN-45 human gastric cancer cells. J. Res. Appl. Basic Med. Sci. 2021, 7, 1–10. [Google Scholar] [CrossRef]
- Chen, H.L.; Gong, J.Y.; Lin, S.C.; Li, S.; Chiang, Y.C.; Hung, J.H.; Yen, C.C.; Lin, C.C. Effects of Sclareol Against Small Cell Lung Carcinoma and the Related Mechanism: In Vitro and In Vivo Studies. Anticancer Res. 2020, 40, 4947–4960. [Google Scholar] [CrossRef]
- Pan, C.H.; Chen, S.Y.; Wang, J.Y.; Tsao, S.P.; Huang, H.Y.; Wei-Chen Chiu, P.; Wu, C.H. Sclareol ameliorated ERCC1-mediated cisplatin resistance in A549 human lung adenocarcinoma cells and a murine xenograft tumor model by suppressing AKT-GSK3beta-AP1/Snail and JNK-AP1 pathways. Chem. Biol. Interact. 2020, 332, 109304. [Google Scholar] [CrossRef]
- Zhang, T.; Wang, T.; Cai, P. Sclareol inhibits cell proliferation and sensitizes cells to the antiproliferative effect of bortezomib via upregulating the tumor suppressor caveolin-1 in cervical cancer cells. Mol. Med. Rep. 2017, 15, 3566–3574. [Google Scholar] [CrossRef] [PubMed]
- Borges, G.S.M.; Silva, J.O.; Fernandes, R.S.; de Souza, A.M.; Cassali, G.D.; Yoshida, M.I.; Leite, E.A.; de Barros, A.L.B.; Ferreira, L.A.M. Sclareol is a potent enhancer of doxorubicin: Evaluation of the free combination and co-loaded nanostructured lipid carriers against breast cancer. Life Sci. 2019, 232, 116678. [Google Scholar] [CrossRef] [PubMed]
- Stepanovic, A.; Terzic Jovanovic, N.; Korac, A.; Zlatovic, M.; Nikolic, I.; Opsenica, I.; Pesic, M. Novel hybrid compounds of sclareol and doxorubicin as potential anticancer nanotherapy for glioblastoma. Biomed. Pharmacother. 2024, 174, 116496. [Google Scholar] [CrossRef]
- Dimas, K.; Kokkinopoulos, D.; Demetzos, C.; Vaos, B.; Marselos, M.; Malamas, M.; Tzavaras, T. The effect of sclareol on growth and cell cycle progression of human leukemic cell lines. Leuk. Res. 1999, 23, 217–234. [Google Scholar] [CrossRef]
- Dimas, K.; Demetzos, C.; Vaos, V.; Ioannidis, P.; Trangas, T. Labdane type diterpenes down-regulate the expression of c-Myc protein, but not of Bcl-2, in human leukemia T-cells undergoing apoptosis. Leuk. Res. 2001, 25, 449–454. [Google Scholar] [CrossRef]
- Dimas, K.; Hatziantoniou, S.; Tseleni, S.; Khan, H.; Georgopoulos, A.; Alevizopoulos, K.; Wyche, J.H.; Pantazis, P.; Demetzos, C. Sclareol induces apoptosis in human HCT116 colon cancer cells in vitro and suppression of HCT116 tumor growth in immunodeficient mice. Apoptosis 2007, 12, 685–694. [Google Scholar] [CrossRef]
- Dimas, K.; Papadaki, M.; Tsimplouli, C.; Hatziantoniou, S.; Alevizopoulos, K.; Pantazis, P.; Demetzos, C. Labd-14-ene-8,13-diol (sclareol) induces cell cycle arrest and apoptosis in human breast cancer cells and enhances the activity of anticancer drugs. Biomed. Pharmacother. 2006, 60, 127–133. [Google Scholar] [CrossRef]
- Mahaira, L.G.; Tsimplouli, C.; Sakellaridis, N.; Alevizopoulos, K.; Demetzos, C.; Han, Z.; Pantazis, P.; Dimas, K. The labdane diterpene sclareol (labd-14-ene-8, 13-diol) induces apoptosis in human tumor cell lines and suppression of tumor growth in vivo via a p53-independent mechanism of action. Eur. J. Pharmacol. 2011, 666, 173–182. [Google Scholar] [CrossRef]
- Stojkovic, P.; Kostic, A.; Lupsic, E.; Jovanovic, N.T.; Novakovic, M.; Nedialkov, P.; Trendafilova, A.; Pesic, M.; Opsenica, I.M. Novel hybrids of sclareol and 1,2,4-triazolo[1,5-a]pyrimidine show collateral sensitivity in multidrug-resistant glioblastoma cells. Bioorg Chem. 2023, 138, 106605. [Google Scholar] [CrossRef]
- Shi, Q.W.; Su, X.H.; Kiyota, H. Chemical and pharmacological research of the plants in genus Euphorbia. Chem. Rev. 2008, 108, 4295–4327. [Google Scholar] [CrossRef]
- Vasas, A.; Hohmann, J. Euphorbia diterpenes: Isolation, structure, biological activity, and synthesis (2008–2012). Chem. Rev. 2014, 114, 8579–8612. [Google Scholar] [CrossRef] [PubMed]
- Krstic, G.; Jadranin, M.; Todorovic, N.M.; Pesic, M.; Stankovic, T.; Aljancic, I.S.; Tesevic, V.V. Jatrophane diterpenoids with multidrug-resistance modulating activity from the latex of Euphorbia nicaeensis. Phytochemistry 2018, 148, 104–112. [Google Scholar] [CrossRef] [PubMed]
- Krstić, G.B.; Kostić, A.; Jadranin, M.B.; Pešić, M.; Novaković, M.M.; Aljančić, I.S.; Vajs, V.V. Two new jatrophane diterpenes from the roots of Euphorbia nicaeensis. J. Serbian Chem. Soc. 2021, 86, 1219–1228. [Google Scholar] [CrossRef]
- Dinić, J.; Novaković, M.; Pešić, M. Chapter 9—Potential for cancer treatment: Natural products from the Balkans. In Biodiversity and Biomedicine; Ozturk, M., Egamberdieva, D., Pešić, M., Eds.; Academic Press: Cambridge, MA, USA, 2020; pp. 137–159. [Google Scholar]
- Sharma, D.K.; Tiwari, M.; Behera, B.K. A review of integrated processes to get value-added chemicals and fuels from petrocrops. Bioresour. Technol. 1994, 49, 1–6. [Google Scholar] [CrossRef]
- Aljancic, I.S.; Pesic, M.; Milosavljevic, S.M.; Todorovic, N.M.; Jadranin, M.; Milosavljevic, G.; Povrenovic, D.; Bankovic, J.; Tanic, N.; Markovic, I.D.; et al. Isolation and biological evaluation of jatrophane diterpenoids from Euphorbia dendroides. J. Nat. Prod. 2011, 74, 1613–1620. [Google Scholar] [CrossRef]
- Jadranin, M.; Pesic, M.; Aljancic, I.S.; Milosavljevic, S.M.; Todorovic, N.M.; Podolski-Renic, A.; Bankovic, J.; Tanic, N.; Markovic, I.; Vajs, V.E.; et al. Jatrophane diterpenoids from the latex of Euphorbia dendroides and their anti-P-glycoprotein activity in human multi-drug resistant cancer cell lines. Phytochemistry 2013, 86, 208–217. [Google Scholar] [CrossRef]
- Xie, X.L.; Fan, R.Z.; Hu, R.; Luo, S.Y.; Tang, G.H.; Yin, S. Euphoresulanes A-M, structurally diverse jatrophane diterpenoids from Euphorbia esula. Bioorg Chem. 2020, 98, 103763. [Google Scholar] [CrossRef]
- Đurović, S.; Ranimirović, M.; Tomović, G.; Petkovski, G.; Niketic, M. Genus Euphorbia L. (Euphorbiaceae juss.) in Serbia based on herbarium data from the collections BEO and BEOU. Bull. Nat. Hist. Mus. Belgrade 2022, 15, 97–120. [Google Scholar] [CrossRef]
- Mai, Z.P.; Ni, G.; Liu, Y.F.; Li, L.; Shi, G.R.; Wang, X.; Li, J.Y.; Yu, D.Q. Heliosterpenoids A and B, two Novel Jatrophane-Derived Diterpenoids with a 5/6/4/6 Ring System from Euphorbia helioscopia. Sci. Rep. 2017, 7, 4922. [Google Scholar] [CrossRef]
- Fang, Y.; Sun, J.; Zhong, X.; Hu, R.; Gao, J.; Duan, G.; Ji, C.; Chen, L.; Zhang, W.; Miao, C.; et al. ES2 enhances the efficacy of chemotherapeutic agents in ABCB1-overexpressing cancer cells in vitro and in vivo. Pharmacol. Res. 2018, 129, 388–399. [Google Scholar] [CrossRef]
- Yang, H.; Mamatjan, A.; Tang, D.; Aisa, H.A. Jatrophane diterpenoids as multidrug resistance modulators from Euphorbia sororia. Bioorg Chem. 2021, 112, 104989. [Google Scholar] [CrossRef] [PubMed]
- Maimaitijiang, A.; Wang, B.; Yang, H.; Tang, D.; Liu, Y.; Aisa, H.A. Discovery of a novel highly potent and low-toxic jatrophane derivative enhancing the P-glycoprotein-mediated doxorubicin sensitivity of MCF-7/ADR cells. Eur. J. Med. Chem. 2022, 244, 114822. [Google Scholar] [CrossRef] [PubMed]
- Hasan, A.; Liu, G.Y.; Hu, R.; Aisa, H.A. Jatrophane Diterpenoids from Euphorbia glomerulans. J. Nat. Prod. 2019, 82, 724–734. [Google Scholar] [CrossRef] [PubMed]
- Zhu, J.; Wang, R.; Lou, L.; Li, W.; Tang, G.; Bu, X.; Yin, S. Jatrophane Diterpenoids as Modulators of P-Glycoprotein-Dependent Multidrug Resistance (MDR): Advances of Structure-Activity Relationships and Discovery of Promising MDR Reversal Agents. J. Med. Chem. 2016, 59, 6353–6369. [Google Scholar] [CrossRef]
- Martinez, C.; Carvalho, M.R.; Madrinan, S.; Jaramillo, C.A. A Late Cretaceous Piper (Piperaceae) from Colombia and diversification patterns for the genus. Am. J. Bot. 2015, 102, 273–289. [Google Scholar] [CrossRef]
- Dharmaratne, H.R.; Nanayakkara, N.P.; Khan, I.A. Kavalactones from Piper methysticum, and their 13C NMR spectroscopic analyses. Phytochemistry 2002, 59, 429–433. [Google Scholar] [CrossRef]
- Li, J.; Zheng, L.; Yan, M.; Wu, J.; Liu, Y.; Tian, X.; Jiang, W.; Zhang, L.; Wang, R. Activity and mechanism of flavokawain A in inhibiting P-glycoprotein expression in paclitaxel resistance of lung cancer. Oncol. Lett. 2020, 19, 379–387. [Google Scholar] [CrossRef]
- Palko-Labuz, A.; Kostrzewa-Suslow, E.; Janeczko, T.; Sroda-Pomianek, K.; Pola, A.; Uryga, A.; Michalak, K. Cyclization of flavokawain B reduces its activity against human colon cancer cells. Hum. Exp. Toxicol. 2020, 39, 262–275. [Google Scholar] [CrossRef]
- Akaberi, M.; Sahebkar, A.; Azizi, N.; Emami, S.A. Everlasting flowers: Phytochemistry and pharmacology of the genus Helichrysum. Ind. Crops Prod. 2019, 138, 111471. [Google Scholar] [CrossRef]
- Matić, I.; Aljančić, I.; Vajs, V.; Jadranin, M.; Gligorijevic, N.; Milosavljević, S.; Juranic, Z. Cancer-Suppressive Potential of Extracts of Endemic Plant Helichrysum Zivojinii: Effects on Cell Migration, Invasion and Angiogenesis. Nat. Prod. Commun. 2013, 8, 1291–1296. [Google Scholar] [CrossRef]
- Matic, I.Z.; Aljancic, I.; Zizak, Z.; Vajs, V.; Jadranin, M.; Milosavljevic, S.; Juranic, Z.D. In vitro antitumor actions of extracts from endemic plant Helichrysum zivojinii. BMC Complement. Altern. Med. 2013, 13, 36. [Google Scholar] [CrossRef] [PubMed]
- Aljancic, I.S.; Vuckovic, I.; Jadranin, M.; Pesic, M.; Dordevic, I.; Podolski-Renic, A.; Stojkovic, S.; Menkovic, N.; Vajs, V.E.; Milosavljevic, S.M. Two structurally distinct chalcone dimers from Helichrysum zivojinii and their activities in cancer cell lines. Phytochemistry 2014, 98, 190–196. [Google Scholar] [CrossRef] [PubMed]
- Wahab, S.; Annadurai, S.; Abullais, S.S.; Das, G.; Ahmad, W.; Ahmad, M.F.; Kandasamy, G.; Vasudevan, R.; Ali, M.S.; Amir, M. Glycyrrhiza glabra (Licorice): A Comprehensive Review on Its Phytochemistry, Biological Activities, Clinical Evidence and Toxicology. Plants 2021, 10, 2751. [Google Scholar] [CrossRef] [PubMed]
- Jakovljević, K.; Tomović, G.; Djordjević, V.; Niketić, M.; Stevanović, V. Steppe flora in Serbia—Distribution, ecology, centres of diversity and conservation status. Folia Geobot. 2020, 55, 1–14. [Google Scholar] [CrossRef]
- Nabekura, T.; Hiroi, T.; Kawasaki, T.; Uwai, Y. Effects of natural nuclear factor-kappa B inhibitors on anticancer drug efflux transporter human P-glycoprotein. Biomed. Pharmacother. 2015, 70, 140–145. [Google Scholar] [CrossRef] [PubMed]
- Toksoy Köseoğlu, S.; Öztürk, M.; Sağıroğlu, M. Phylogenetic and cladistic analyses of the enigmatic genera Bituminaria and Cullen (Fabaceae) in Turkey. Turk. J. Bot. 2015, 39, 60–69. [Google Scholar] [CrossRef]
- Alam, F.; Khan, G.N.; Asad, M. Psoralea corylifolia L: Ethnobotanical, biological, and chemical aspects: A review. Phytother. Res. 2018, 32, 597–615. [Google Scholar] [CrossRef]
- Xing, N.; Meng, X.; Wang, S. Isobavachalcone: A comprehensive review of its plant sources, pharmacokinetics, toxicity, pharmacological activities and related molecular mechanisms. Phytother. Res. 2022, 36, 3120–3142. [Google Scholar] [CrossRef]
- Palko-Labuz, A.; Blaszczyk, M.; Sroda-Pomianek, K.; Wesolowska, O. Isobavachalcone as an Active Membrane Perturbing Agent and Inhibitor of ABCB1 Multidrug Transporter. Molecules 2021, 26, 4637. [Google Scholar] [CrossRef]
- Konowalik, K.; Kreitschitz, A. Morphological and anatomical characteristics of Artemisia absinthium var. absinthium and its Polish endemic variety A. absinthium var. calcigena. Plant Syst. Evol. 2012, 298, 1325–1336. [Google Scholar] [CrossRef]
- Ivanov, M.; Gasic, U.; Stojkovic, D.; Kostic, M.; Misic, D.; Sokovic, M. New Evidence for Artemisia absinthium L. Application in Gastrointestinal Ailments: Ethnopharmacology, Antimicrobial Capacity, Cytotoxicity, and Phenolic Profile. Evid. Based Complement. Alternat Med. 2021, 2021, 9961089. [Google Scholar] [CrossRef] [PubMed]
- Hou, G.; Yuan, X.; Li, Y.; Hou, G.; Liu, X. Cardamonin, a natural chalcone, reduces 5-fluorouracil resistance of gastric cancer cells through targeting Wnt/beta-catenin signal pathway. Investig. New Drugs 2020, 38, 329–339. [Google Scholar] [CrossRef] [PubMed]
- Zanoli, P.; Zavatti, M. Pharmacognostic and pharmacological profile of Humulus lupulus L. J. Ethnopharmacol. 2008, 116, 383–396. [Google Scholar] [CrossRef] [PubMed]
- Liu, F.; Hoag, H.; Wu, C.; Liu, H.; Yin, H.; Dong, J.; Qian, Z.; Miao, F.; Liu, M.; Miao, J. Experimental and Simulation Identification of Xanthohumol as an Inhibitor and Substrate of ABCB1. Appl. Sci. 2018, 8, 681. [Google Scholar] [CrossRef]
- Novakovic, M.; Bukvicki, D.; Andjelkovic, B.; Ilic-Tomic, T.; Veljic, M.; Tesevic, V.; Asakawa, Y. Cytotoxic Activity of Riccardin and Perrottetin Derivatives from the Liverwort Lunularia cruciata. J. Nat. Prod. 2019, 82, 694–701. [Google Scholar] [CrossRef]
- Kosenkova, Y.S.; Polovinka, M.P.; Komarova, N.I.; Korchagina, D.V.; Kurochkina, N.Y.; Cheremushkina, V.A.; Salakhutdinov, N.F. Riccardin C, a bisbibenzyl compound from Primula macrocalyx. Chem. Nat. Compd. 2007, 43, 712–713. [Google Scholar] [CrossRef]
- Kosenkova, Y.S.; Polovinka, M.P.; Komarova, N.I.; Korchagina, D.V.; Morozov, S.V.; Vyalkov, A.I.; Kurochkina, N.Y.; Cheremushkina, V.A.; Salakhutdinov, N.F. Fatty-acid composition and secondary metabolites from slightly polar extracts of the aerial part of Primula macrocalyx. Chem. Nat. Compd. 2008, 44, 564–568. [Google Scholar] [CrossRef]
- Novakovic, M.; Ilic-Tomic, T.; Djordjevic, I.; Andjelkovic, B.; Tesevic, V.; Milosavljevic, S.; Asakawa, Y. Bisbibenzyls from Serbian Primula veris subsp. Columnae (Ten.) Ludi and P. acaulis (L.) L. Phytochemistry 2023, 212, 113719. [Google Scholar] [CrossRef]
- Xue, X.; Qu, X.J.; Gao, Z.H.; Sun, C.C.; Liu, H.P.; Zhao, C.R.; Cheng, Y.N.; Lou, H.X. Riccardin D, a novel macrocyclic bisbibenzyl, induces apoptosis of human leukemia cells by targeting DNA topoisomerase II. Investig. New Drugs 2012, 30, 212–222. [Google Scholar] [CrossRef]
- Ji, M.; Shi, Y.; Lou, H. Overcoming of P-glycoprotein-mediated multidrug resistance in K562/A02 cells using riccardin F and pakyonol, bisbibenzyl derivatives from liverworts. Biosci. Trends 2011, 5, 192–197. [Google Scholar] [CrossRef]
- Brand, S.; Holscher, D.; Schierhorn, A.; Svatos, A.; Schroder, J.; Schneider, B. A type III polyketide synthase from Wachendorfia thyrsiflora and its role in diarylheptanoid and phenylphenalenone biosynthesis. Planta 2006, 224, 413–428. [Google Scholar] [CrossRef] [PubMed]
- Munde, T.; Brand, S.; Hidalgo, W.; Maddula, R.K.; Svatos, A.; Schneider, B. Biosynthesis of tetraoxygenated phenylphenalenones in Wachendorfia thyrsiflora. Phytochemistry 2013, 91, 165–176. [Google Scholar] [CrossRef] [PubMed]
- Matsuda, H.; Ishikado, A.; Nishida, N.; Ninomiya, K.; Fujiwara, H.; Kobayashi, Y.; Yoshikawa, M. Hepatoprotective, superoxide scavenging, and antioxidative activities of aromatic constituents from the bark of Betula platyphylla var. japonica. Bioorg. Med. Chem. Lett. 1998, 8, 2939–2944. [Google Scholar] [CrossRef]
- Tung, N.H.; Kim, S.K.; Ra, J.C.; Zhao, Y.Z.; Sohn, D.H.; Kim, Y.H. Antioxidative and hepatoprotective diarylheptanoids from the bark of Alnus japonica. Planta Med. 2010, 76, 626–629. [Google Scholar] [CrossRef]
- Lai, Y.C.; Chen, C.K.; Lin, W.W.; Lee, S.S. A comprehensive investigation of anti-inflammatory diarylheptanoids from the leaves of Alnus formosana. Phytochemistry 2012, 73, 84–94. [Google Scholar] [CrossRef]
- Tung, N.H.; Kwon, H.J.; Kim, J.H.; Ra, J.C.; Ding, Y.; Kim, J.A.; Kim, Y.H. Anti-influenza diarylheptanoids from the bark of Alnus japonica. Bioorg Med. Chem. Lett. 2010, 20, 1000–1003. [Google Scholar] [CrossRef]
- Choi, S.E.; Kim, K.H.; Kwon, J.H.; Kim, S.B.; Kim, H.W.; Lee, M.W. Cytotoxic activities of diarylheptanoids from Alnus japonica. Arch. Pharm. Res. 2008, 31, 1287–1289. [Google Scholar] [CrossRef] [PubMed]
- Mshvildadze, V.; Legault, J.; Lavoie, S.; Gauthier, C.; Pichette, A. Anticancer diarylheptanoid glycosides from the inner bark of Betula papyrifera. Phytochemistry 2007, 68, 2531–2536. [Google Scholar] [CrossRef]
- Sun, Y.; Tabata, K.; Matsubara, H.; Kitanaka, S.; Suzuki, T.; Yasukawa, K. New cytotoxic diarylheptanoids from the rhizomes of Alpinia officinarum. Planta Med. 2008, 74, 427–431. [Google Scholar] [CrossRef]
- Ren, B.Q.; Xiang, X.G.; Chen, Z.D. Species identification of Alnus (Betulaceae) using nrDNA and cpDNA genetic markers. Mol. Ecol. Resour. 2010, 10, 594–605. [Google Scholar] [CrossRef]
- Skoczowski, A.; Odrzywolska-Hasiec, M.; Oliwa, J.; Ciereszko, I.; Kornas, A. Ecophysiological Variability of Alnus viridis (Chaix) DC. Green Alder Leaves in the Bieszczady Mountains (Poland). Plants 2021, 10, 96. [Google Scholar] [CrossRef] [PubMed]
- Szokala, D. Alpine and subalpine acidophilous vegetation on the eastern side of the Chiprovska Planina Mts. Tuexenia 2023, 43, 109–158. [Google Scholar] [CrossRef]
- Vidaković, V.; Novaković, M.; Popović, Z.; Janković, M.; Matić, R.; Tešević, V.; Bojović, S. Significance of diarylheptanoids for chemotaxonomical distinguishing between Alnus glutinosa and Alnus incana. Holzforschung 2018, 72, 9–16. [Google Scholar] [CrossRef]
- Lee, H.-B.; Lee, H.-K.; Kim, J.-R.; Ahn, Y.-J. Anti-Helicobacter pylori diarylheptanoid identified in the rhizome of Alpinia officinarum. J. Korean Soc. Appl. Biol. Chem. 2009, 52, 367–370. [Google Scholar] [CrossRef]
- Martineau, L.C.; Herve, J.; Muhamad, A.; Saleem, A.; Harris, C.S.; Arnason, J.T.; Haddad, P.S. Anti-adipogenic activities of Alnus incana and Populus balsamifera bark extracts, part I: Sites and mechanisms of action. Planta Med. 2010, 76, 1439–1446. [Google Scholar] [CrossRef]
- Telysheva, G.; Dizhbite, T.; Bikovens, O.; Ponomarenko, J.; Janceva, S.; Krasilnikova, J. Structure and antioxidant activity of diarylheptanoids extracted from bark of grey alder (Alnus incana) and potential of biorefinery-based bark processing of European trees. In Proceedings of the 11th EWLP, Hamburg, Germany, 16–19 August 2010; Volume 65, pp. 623–629. [Google Scholar] [CrossRef]
- Lee, O.; Kim, J.; Choi, Y.W.; Lee, M.; Park, G.; Oh, C. Efficacy of oregonin investigated by non-invasive evaluation in a B16 mouse melanoma model. Exp. Dermatol. 2013, 22, 842–844. [Google Scholar] [CrossRef]
- Novakovic, M.; Stankovic, M.; Vuckovic, I.; Todorovic, N.; Trifunovic, S.; Apostolovic, D.; Mandic, B.; Veljic, M.; Marin, P.; Tesevic, V.; et al. Diarylheptanoids from green alder bark and their potential for DNA protection. Chem. Biodivers. 2014, 11, 872–885. [Google Scholar] [CrossRef] [PubMed]
- Dinic, J.; Randelovic, T.; Stankovic, T.; Dragoj, M.; Isakovic, A.; Novakovic, M.; Pesic, M. Chemo-protective and regenerative effects of diarylheptanoids from the bark of black alder (Alnus glutinosa) in human normal keratinocytes. Fitoterapia 2015, 105, 169–176. [Google Scholar] [CrossRef] [PubMed]
- Novakovic, M.; Stankovic, M.; Vuckovic, I.; Todorovic, N.; Trifunovic, S.; Tesevic, V.; Vajs, V.; Milosavljevic, S. Diarylheptanoids from Alnus glutinosa bark and their chemoprotective effect on human lymphocytes DNA. Planta Med. 2013, 79, 499–505. [Google Scholar] [CrossRef]
- Dinic, J.; Novakovic, M.; Podolski-Renic, A.; Vajs, V.; Tesevic, V.; Isakovic, A.; Pesic, M. Structural differences in diarylheptanoids analogues from Alnus viridis and Alnus glutinosa influence their activity and selectivity towards cancer cells. Chem. Biol. Interact. 2016, 249, 36–45. [Google Scholar] [CrossRef]
- Novakovic, M.; Nikodinovic-Runic, J.; Veselinovic, J.; Ilic-Tomic, T.; Vidakovic, V.; Tesevic, V.; Milosavljevic, S. Bioactive Pentacyclic Triterpene Ester Derivatives from Alnus viridis ssp. viridis Bark. J. Nat. Prod. 2017, 80, 1255–1263. [Google Scholar] [CrossRef] [PubMed]
- Dinic, J.; Novakovic, M.; Podolski-Renic, A.; Stojkovic, S.; Mandic, B.; Tesevic, V.; Vajs, V.; Isakovic, A.; Pesic, M. Antioxidative activity of diarylheptanoids from the bark of black alder (Alnus glutinosa) and their interaction with anticancer drugs. Planta Med. 2014, 80, 1088–1096. [Google Scholar] [CrossRef] [PubMed]
- Novakovic, M.; Pesic, M.; Trifunovic, S.; Vuckovic, I.; Todorovic, N.; Podolski-Renic, A.; Dinic, J.; Stojkovic, S.; Tesevic, V.; Vajs, V.; et al. Diarylheptanoids from the bark of black alder inhibit the growth of sensitive and multi-drug resistant non-small cell lung carcinoma cells. Phytochemistry 2014, 97, 46–54. [Google Scholar] [CrossRef]
- Islam, M.R.; Rauf, A.; Akash, S.; Trisha, S.I.; Nasim, A.H.; Akter, M.; Dhar, P.S.; Ogaly, H.A.; Hemeg, H.A.; Wilairatana, P.; et al. Targeted therapies of curcumin focus on its therapeutic benefits in cancers and human health: Molecular signaling pathway-based approaches and future perspectives. Biomed. Pharmacother. 2024, 170, 116034. [Google Scholar] [CrossRef]
- Andjelkovic, T.; Pesic, M.; Bankovic, J.; Tanic, N.; Markovic, I.D.; Ruzdijic, S. Synergistic effects of the purine analog sulfinosine and curcumin on the multidrug resistant human non-small cell lung carcinoma cell line (NCI-H460/R). Cancer Biol. Ther. 2008, 7, 1024–1032. [Google Scholar] [CrossRef]
- Amalraj, A.; Pius, A.; Gopi, S.; Gopi, S. Biological activities of curcuminoids, other biomolecules from turmeric and their derivatives—A review. J. Tradit. Complement. Med. 2017, 7, 205–233. [Google Scholar] [CrossRef] [PubMed]
- Limtrakul, P.; Chearwae, W.; Shukla, S.; Phisalphong, C.; Ambudkar, S.V. Modulation of function of three ABC drug transporters, P-glycoprotein (ABCB1), mitoxantrone resistance protein (ABCG2) and multidrug resistance protein 1 (ABCC1) by tetrahydrocurcumin, a major metabolite of curcumin. Mol. Cell Biochem. 2007, 296, 85–95. [Google Scholar] [CrossRef]
- Tang, X.Q.; Bi, H.; Feng, J.Q.; Cao, J.G. Effect of curcumin on multidrug resistance in resistant human gastric carcinoma cell line SGC7901/VCR. Acta Pharmacol. Sin. 2005, 26, 1009–1016. [Google Scholar] [CrossRef]
- Yu, S.; Shen, G.; Khor, T.O.; Kim, J.H.; Kong, A.N. Curcumin inhibits Akt/mammalian target of rapamycin signaling through protein phosphatase-dependent mechanism. Mol. Cancer Ther. 2008, 7, 2609–2620. [Google Scholar] [CrossRef]
- Lin, X.; Yang, X.; Yang, Y.; Zhang, H.; Huang, X. Research progress of traditional Chinese medicine as sensitizer in reversing chemoresistance of colorectal cancer. Front. Oncol. 2023, 13, 1132141. [Google Scholar] [CrossRef]
- Guo, S.; Lv, L.; Shen, Y.; Hu, Z.; He, Q.; Chen, X. A nanoparticulate pre-chemosensitizer for efficacious chemotherapy of multidrug resistant breast cancer. Sci. Rep. 2016, 6, 21459. [Google Scholar] [CrossRef] [PubMed]
- Lu, K.H.; Lu, P.W.; Lu, E.W.; Lin, C.W.; Yang, S.F. Curcumin and its Analogs and Carriers: Potential Therapeutic Strategies for Human Osteosarcoma. Int. J. Biol. Sci. 2023, 19, 1241–1265. [Google Scholar] [CrossRef] [PubMed]
- Viriyaadhammaa, N.; Duangmano, S.; Saiai, A.; Tungjai, M.; Dejkriengkraikul, P.; Tima, S.; Chiampanichayakul, S.; Krise, J.; Anuchapreeda, S. A Novel Drug Modulator Diarylheptanoid (trans-1,7-Diphenyl-5-hydroxy-1-heptene) from Curcuma comosa Rhizomes for P-glycoprotein Function and Apoptosis Induction in K652/ADR Leukemic Cells. Int. J. Mol. Sci. 2022, 23, 8989. [Google Scholar] [CrossRef]
- Danko, B.; Toth, S.; Martins, A.; Vagvolgyi, M.; Kusz, N.; Molnar, J.; Chang, F.R.; Wu, Y.C.; Szakacs, G.; Hunyadi, A. Synthesis and SAR Study of Anticancer Protoflavone Derivatives: Investigation of Cytotoxicity and Interaction with ABCB1 and ABCG2 Multidrug Efflux Transporters. ChemMedChem 2017, 12, 850–859. [Google Scholar] [CrossRef] [PubMed]
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Dinić, J.; Podolski-Renić, A.; Novaković, M.; Li, L.; Opsenica, I.; Pešić, M. Plant-Based Products Originating from Serbia That Affect P-glycoprotein Activity. Molecules 2024, 29, 4308. https://doi.org/10.3390/molecules29184308
Dinić J, Podolski-Renić A, Novaković M, Li L, Opsenica I, Pešić M. Plant-Based Products Originating from Serbia That Affect P-glycoprotein Activity. Molecules. 2024; 29(18):4308. https://doi.org/10.3390/molecules29184308
Chicago/Turabian StyleDinić, Jelena, Ana Podolski-Renić, Miroslav Novaković, Liang Li, Igor Opsenica, and Milica Pešić. 2024. "Plant-Based Products Originating from Serbia That Affect P-glycoprotein Activity" Molecules 29, no. 18: 4308. https://doi.org/10.3390/molecules29184308