An outline of main factors of drug resistance influencing cancer therapy

References

• Trédan O, Galmarini CM, Patel K, Tannock IF. Drug resistance and the solid tumor microenvironment. J Natl Canc Inst. 2007;99:1441–54.10.1093/jnci/djm135
   PubMed Web of Science ®Google Scholar
• Carmeliet P, Jain RK. Angiogenesis in cancer and other diseases. Nature. 2000;407:249–57.10.1038/35025220
   PubMed Web of Science ®Google Scholar
• Mitrus I, Szala S. Chemioterapia – główne przyczyny niepowodzeń [Chemotherapy - the main cause of failure]. J Oncol. 2009;59:368–76.
   Google Scholar
• Rohwer N, Cramer T. Hypoxia-mediated drug resistance: novel insights on the functional interaction of HIFs and cell death pathways. Drug Resist Update. 2011;14:191–201.10.1016/j.drup.2011.03.001
   PubMed Web of Science ®Google Scholar
• Bristow RG, Hill RP. Hypoxia and metabolism: hypoxia, DNA repair and genetic instability. Nat Rev Canc. 2008;8:180–92.10.1038/nrc2344
   PubMed Web of Science ®Google Scholar
• Semenza GL. Hypoxia-inducible factors: mediators of cancer progression and targets for cancer therapy. Trends Pharmacol Sci. 2012;33:207–14.10.1016/j.tips.2012.01.005
   PubMed Web of Science ®Google Scholar
• Webb BA, Chimenti M, Jacobson M. Dysregulated pH: a perfect storm for cancer progression. Nat Rev Canc. 2011;11:671–7.10.1038/nrc3110
   PubMed Web of Science ®Google Scholar
• Halestrap AP, Wilson MC. The monocarboxylate transporter family. Role and regulation. IUBMB Life. 2012;64:109–19.10.1002/iub.572
   PubMed Web of Science ®Google Scholar
• Mahoney BP, Raghunand N, Baggett B. Tumor acidity, ion trapping and chemotherapeutics I. Acid pH affects the distribution of chemotherapeutic agents in vitro. Biochem Pharmacol. 2003;66:1207–18.10.1016/S0006-2952(03)00467-2
   PubMed Web of Science ®Google Scholar
• Raghunand N, Mahoney BP, Gillies RJ. Tumor acidity, ion trapping and chemotherapeutics II. pH-dependent partition coefficients predict importance of ion trapping on pharmacokinetics of weakly basic chemotherapeutic agents. Biochem Pharmacol. 2003;66:1219–29.10.1016/S0006-2952(03)00468-4
   PubMed Web of Science ®Google Scholar
• Wojtkowiak JW, Verduzco D, Schramm kJ. Drug resistance and cellular adaptation to tumor acidic pH microenvironment. Mol Pharm. 2011;8:2032–8.10.1021/mp200292c
   PubMed Web of Science ®Google Scholar
• Palazón A, Aragonés J, Morales-Kastresana A, de Landazuri MO, Melero I. Molecular pathways: hypoxia response in immune cells fighting or promoting cancer. Clin Canc Res. 2012;18:1207–13.10.1158/1078-0432.CCR-11-1591
   PubMed Web of Science ®Google Scholar
• Senn HJ, Drings P, Glaus A. Kompedium onkologii [A compendium of oncology]. Wyd Lek PZWL. 1995.
   Google Scholar
• Gray LH, Conger AD, Ebert M, Hornsey S, Scott OCA. The concentration of oxygen dissolved in tissues at the time of irradiation as a factor in radiotherapy. Brit J Radiol. 1953;26:638–48.10.1259/0007-1285-26-312-638
   PubMed Web of Science ®Google Scholar
• Zhou SF, Wang LL, Di YM, Xue CC, Duan W, Li CG. Substrates and inhibitors of human multidrug resistance associated proteins and implications in drug development. Curr Med Chem. 2008;15:1981–2039.10.2174/092986708785132870
   PubMed Web of Science ®Google Scholar
• Wu CP, Hsieh CH, Wu YS. The emergence of drug transporter-mediated multidrug resistance to cancer chemotherapy. Mol Pharm. 2011;8:1996–2011.10.1021/mp200261n
   PubMed Web of Science ®Google Scholar
• Roy U, Bulot C, Bentrup KH, Mondal D. Specific increase in MDR1 mediated drug-efflux in human brain endothelial cells following co-exposure to HIV-1 and saquinavir. Plos One. 2013;8(10):e75374.
   PubMed Web of Science ®Google Scholar
• Donmez CY, Kuhnweeraphong N, Parveen Z, Schmid D, Artaker M, Ecker GF. Pore-exposed tyrosine residues of P-glycoprotein are important hydrogen-bonding partners for drugs. Mol Pharm. 2014;85:420–8.10.1124/mol.113.088526
   Web of Science ®Google Scholar
• Dębska S, Owecka A, Czernek U, Szydłowska-Pazera K, Habib M, Potemski P. Transportery błonowe ABCC – budowa, funkcja i znaczenie w mechanizmach wytwarzania oporności wielolekowej w komórkach nowotworów złośliwych [Transmembrane transporters ABCC - structure, function and role in multidrug resistance of cancer cells]. PHiMD. 2011;65:552–61.
   Google Scholar
• Kovalev AA, Tsvetaeva DA, Grudinskaja TV. Role of ABC-cassette transporters (MDR1, MRP1, BCRP) in the development of primary and acquired multipledrug resistance in patients with early and metastatic breast cancer. Exp Oncol. 2013;35:287–90.
   PubMedGoogle Scholar
• Doyle LA, Yang W, Abruzzo LV, Krogmann T, Gao Y, Rishi AK, et al. A multidrug resistance transporter from human MCF-7 breast cancer cells. Proc Natl Acad Sci. 1998;95(26):15665–70.10.1073/pnas.95.26.15665
   PubMed Web of Science ®Google Scholar
• Miyake K, Mickley L, Litman T, Zhan Z, Robey R, Cristensen B, et al. Molecular cloning of cDNAs which are highly overexpressed in mitoxantroneresistant cells: demonstration of homology to ABC transport genes. Canc Res. Advances in Brief. 1999;59:8–13.
   PubMed Web of Science ®Google Scholar
• Gutmann H, Fricker G, Török M, Michael S, Beglinger Ch, Drewe J. Evidence for different ABC-transporters in caco-2 cells modulating drug uptake. Pharm Res. 1999;16(3):402–7.10.1023/A:1018825819249
   PubMed Web of Science ®Google Scholar
• Tobe SW, Noble-Topham SE, Andrulis IL, Hartwick RW, Skorecki KL, Warner E. Expression of the multiple drug resistance gene in human renal cell carcinoma depends on tumor histology, grade, and stage. Clin Canc Res. 1995;1(12):1611–5.
   PubMed Web of Science ®Google Scholar
• Lemos C, Jansen G, Peters GJ. Drug transporters: recent advances concerning BCRP and tyrosine kinase inhibitors. Br J Canc. 2008;98:857–62.10.1038/sj.bjc.6604213
   PubMed Web of Science ®Google Scholar
• Nooter K, Westerman AM, Flens MJ, Zaman GJ, Scheper RJ, van Wingerden KE, et al. Expression of the multidrug resistance-associated protein (MRP) gene in human cancers. Clin Canc Res. 1995;1(11):1301–10.
   PubMed Web of Science ®Google Scholar
• Seebacher N, Lane DJR, Richardson DR, Jansson PJ. Turning the gun on cancer: utilizing lysosomal P-glycoprotein as a new strategy to overcome multi-drug resistance. Free Radic Biol Med. 2016;96:432–45.10.1016/j.freeradbiomed.2016.04.201
   PubMed Web of Science ®Google Scholar
• Silva KL, Silva de Souza P, Nestal de Moraes G, Moellmann-Coelho A, Vasconcelos F, Ciuvalschi Maia R. XIAP and P-glycoprotein co-expression is related to imatinib resistance in chronic myeloid leukemia cells. Leukemia Res. 2013;37:1350–8.10.1016/j.leukres.2013.06.014
   PubMed Web of Science ®Google Scholar
• Harmsen S, Meijerman I, Maas-Bakker RF, Beijnen JH, Schellens JHM. PXR-mediated P-glycoprotein induction by small molecule tyrosine kinase inhibitors. Eur J Pharm Sci. 2013;48:644–9.10.1016/j.ejps.2012.12.019
   PubMed Web of Science ®Google Scholar
• Lemos C, Kathmann I, Giovannetti E, Calhau C, Jansen C, Peters GJ. Impact of cellular folate status and epidermal growth factor receptor expression on BCRP/ABCG2-mediated resistance to gefitinib and erlotinib. Br J Canc. 2009;100:1120–7.10.1038/sj.bjc.6604980
   PubMed Web of Science ®Google Scholar
• Navarro G, Sawant RR, Biswas S, Essex S, Tros de Ilarduya C, Torchilin VP. P-glycoprotein silencing with siRNA delivered by DOPE-modified PEI overcomes doxorubicin resistance in breast cancer cells. Nanomedicine. 2012;7:65–78.10.2217/nnm.11.93
   PubMed Web of Science ®Google Scholar
• Bradshaw-Pierce EL, Pitts TM, Tan AC, McPhillips K, West M, Gustafson DL. Tumor P-glycoprotein correlates with efficacy of PF-3758309 in in vitro and in vivo models of colorectal cancer. Front Pharmacol. 2013;4:22.doi: 10.3389/fphar.2013.00022.
   PubMed Web of Science ®Google Scholar
• Ahn M, Ghaemmagami S, Huang Y, Phuan PW, May BCH, Giles K. Pharmackokinetics of quinacrine efflux from mouse brain via the P-glycoprotein efflux transporter. Plos One. 2012;7(7):e39112.
   PubMed Web of Science ®Google Scholar
• Beck WT. Mechanisms of multidrug resistance in human tumor cells. The roles of P-glycoprotein, DNA topoisomerase II, and other factors. Cancer Treat Rev. 1990;17:11–20.10.1016/0305-7372(90)90011-4
   PubMed Web of Science ®Google Scholar
• Li X, Hu J, Wang B, Sheng L, Liu Z, Yang S. Inhibitory effects of herbal constituents on P-glycoprotein in vitro and in vivo: herb-drug interactions mediated via p-gp. Toxicol Appl Pharm. 2013;275:163–75.
   PubMed Web of Science ®Google Scholar
• Meng H, Liong M, Xia T, Li Z, Ji Z, Zink JI. Engineered design of mesopourous silica nanoparticles to deliver doxorubicin and P-glycoprotein siRNA to overcome drug resistance in a cancer cell line. Am Chem Soc. 2010;4:4539–50.
   Google Scholar
• Malmo J, Sandvig A, Varum KM, Strand SP. Nanoparticle mediated P-glycoprotein silencing for improved drug delivery across the blood brain barrier: a siRNA chitosan approach. Plos One. 2013;8(1):e54182.
   PubMed Web of Science ®Google Scholar
• Kaczorowski S, Ochocka M, Kaczorowska M, Aleksandrowicz R, Matysiakl M, Karwacki M. Is P-glycoprotein a sufficient marker for multidrug resistance in vivo? immunohistochemical staining for P-glycoprotein in children and adult leukemia: correlation with clinical outcome. Lymphoma. 1995;20(1–2):143–52.10.3109/10428199509054766
   PubMed Web of Science ®Google Scholar
• Angelini A, Di Pietro R, Centurione L, Castellani ML, Conti P, Porreca E, et al. Inhibition of P-glycoprotein-mediated transport by s-adenosylmethionine and cynarin in multidrug-resistant human uterine sarcoma MES-SA/Dx5 cells. J Biol Regul Homeost Agents. 2011;26:495–504.
   Web of Science ®Google Scholar
• Visvader JE, Lindeman GJ. Cancer stem cells in solid tumors: accumulating evidences and unresolved questions. Nat Rev Canc. 2008;8:755–68.10.1038/nrc2499
   PubMed Web of Science ®Google Scholar
• Wieczorek K, Niewiarowska J. Nowotworowe komórki macierzyste. PH iMD. 2012;66:629–36.
   Google Scholar
• Fang A, Nguyen TK, Leisheat K, Finko R, Kulp AN, Hotz S, et al. A tumorogenic subpopulation with stem cell properties in melanomas. J Canc Res. 2005;65:9328–9337.
   Web of Science ®Google Scholar
• Prabhu VV, Allen JE, Hong B, Zhang S, Cheng H, El-Deiry WS. Therapeutic targeting of the p53 pathway in cancer stem cells. Expert Opin Ther Targets. 2012;16:1161–74.10.1517/14728222.2012.726985
   PubMed Web of Science ®Google Scholar
• Blagosklonny MV. Target for cancer therapy: proliferating cells or stem cells. Leukemia. 2006;20:385–91.10.1038/sj.leu.2404075
   PubMed Web of Science ®Google Scholar
• Baccelli I, Trumpp A. The evolving concept of cancer and metastasis stem cell. J Cell Biol. 2012;198:281–93.10.1083/jcb.201202014
   PubMed Web of Science ®Google Scholar
• Schwarz-Cruz-y-Celis A, Mendelez-Zajgla J. Cancer stem cells. Revista de investigacion clinica. 2011;63:179–86.
   PubMedGoogle Scholar
• Malanchi I, Santamaria-Martinez A, Susanto E, Peng H, Lehr HA, Delaloye JF, et al. Interactions between cancer stem cells and their niche govern metastatic colonization. Nature. 2012;481:85–9.
   PubMed Web of Science ®Google Scholar
• Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144:646–74.10.1016/j.cell.2011.02.013
   PubMed Web of Science ®Google Scholar
• Happo L, Strasser A, Cory S. BH3-only proteins in apoptosis at a glance. J Cell Sci. 2012;125:1081–7.10.1242/jcs.090514
   PubMed Web of Science ®Google Scholar
• Longley DB, Johnston PG. Molecular mechanisms of drug resistance. J Pathol. 2005;205:275–92.10.1002/(ISSN)1096-9896
   PubMed Web of Science ®Google Scholar
• Chonghaile TN, Sarosiek KA, Vo TT, Ryan JA, Tammareddi A, Moore V. Pretreatment mitochondrial priming correlates with clinical response to cytotoxic chemotherapy. Science. 2011;334:1129–33.10.1126/science.1206727
   PubMed Web of Science ®Google Scholar
• Wong FY, Liem N, Xie C, Yan FL, Wong WC, Wang L, et al. Combination therapy with gossypol reveals synergism against gemcitabine resistance in cancer cells with highBCL-2 expression. Plos One. 2012;7(12):e50786.
   PubMed Web of Science ®Google Scholar
• Raffo AJ, Perlman H, Chen MW, Day ML, Streitman JS, Buttyan R. Overexpression of bcl-2 protects prostate cancer cells from apoptosis in vitro and confers resistance to androgen depletion in vivo. Canc Res. 1995;55:4438–45.
   PubMed Web of Science ®Google Scholar
• Geng M, Wang L, Li P. Correlation between chemosensitivity to anticancer drugs and Bcl-2 expression in gastric cancer. Int J Clin Exp Pathol. 2013;6:2554–9.
   PubMed Web of Science ®Google Scholar
• Myashita T, Reed JC. Bcl-2 gene transfer increases relative resistance of S49.1 and WEHI7.2 lymphoid cells to cell death and DNA fragmentation induced by glucocorticoids and multiple chemotherapeutic drugs. Cancer Res. 1992;52:5407–11.
   PubMed Web of Science ®Google Scholar
• Siegel RM, Katsumata M, Miyashita T, Louie DC, Greene MI, Reed J. Inhibition of thymocyte apoptosis and negative antigenic selection in bcl-2 transgenic. Proc Natl Acad Sci USA. 1992;89:7003–7.10.1073/pnas.89.15.7003
   PubMed Web of Science ®Google Scholar
• Campos L, Rouault JP, Sabido O, Oriol P, Roubi N, Vasselon CH, et al. High expression of bcl-2 protein in acute myeloid leukemia cells is associated with poor response to chemotherapy. Blood. 1993;81:3091–6.
   PubMed Web of Science ®Google Scholar
• Lomonosova E, Chinnadurai G. BH3-only proteins in apoptosis and beyond: an overview. Oncogene. 2008;27:2–19.10.1038/onc.2009.39
   PubMed Web of Science ®Google Scholar
• Tan TT, Degenhardt K, Nelson DA, Beaudoin B, Nieves-Neira W, Bouilet P, et al. Key roles of BIM-driven apoptosis in epithelial tumors and rational chemotherapy. Canc Cell. 2005;7:227–38.10.1016/j.ccr.2005.02.008
   PubMed Web of Science ®Google Scholar
• Jeffers JR, Parganas E, Lee Y, Yang CH, Wang JL, Brennan J. Puma is an essential mediator of p53-dependent and -independent apoptotic pathways. Canc Cell. 2003;4:321–8.10.1016/S1535-6108(03)00244-7
   PubMed Web of Science ®Google Scholar
• Moore VDG, Letai A. BH3 profiling – measuring integrated function of the mitochondrial apoptotic pathway to predict cell fate decisions. Canc Lett. 2013;332:202–5.10.1016/j.canlet.2011.12.021
   PubMed Web of Science ®Google Scholar
• Labi V, Grespi F, Baumgartner F, Villuger A. Targeting the Bcl-2-regulated apoptosis pathway by BH3 mimetics: a breakthrough in anticancer therapy? Cell death Differ. 2008;15:977–87.10.1038/cdd.2008.37
   PubMed Web of Science ®Google Scholar
• Zhang L, Yu J, Park BH, Kinzler KW, Vogelstein B. Role of BAX in the apoptotic response to anticancer agents. Science. 2000;290:989–92.10.1126/science.290.5493.989
   PubMed Web of Science ®Google Scholar
• Hong B, van den Heuvel AP, Prabhu VV, Zhang S, El-Deiry WS. Targeting tumor suppressor p53 for cancer therapy: strategies, challenges and opportunities. Curr Drug Targets. 2014;15:80–9.10.2174/1389450114666140106101412
   PubMed Web of Science ®Google Scholar
• Mathivanan S. Exosomes and shedding microvesicles are mediators of intracellular communications: how do they communicate with the target cells? Biotech Biomater. 2012;2:e110.
   Google Scholar
• Park JE, Tan HS, Datta A, Lai RC, Zhang H, Meng W, et al. Hypoxic tumor cell modulates its microenvironment to enhance angiogenic and metastatic potential by secretion of proteins and exosomes. Mol Cell Proteomics. 2010;9:1085–1099.10.1074/mcp.M900381-MCP200
   PubMed Web of Science ®Google Scholar
• Azmi AS, Bao B, Sarkar FH. Exosomes in cancer development, metastasis and drug resistance: a comprehensive review. Canc Metastasis Rev. 2013;32:623–42.10.1007/s10555-013-9441-9
   PubMed Web of Science ®Google Scholar
• Iero M, Valenti R, Huber V, Filipazzi P, Parmiani G, Fai S. Tumour-released exosomes and their implications in cancer immunity. Cell Death Differ. 2008;15:80–8.10.1038/sj.cdd.4402237
   PubMed Web of Science ®Google Scholar
• Cortez MA, Bueso-Ramos C, Ferdin J, Lopez-Berestein G, Sood AK, Calin GA. MicroRNAs in body fluids – the mix of hormones and biomarkers. Nature Reviews. Clin Oncol. 2011;8:467–77.
   Web of Science ®Google Scholar
• Gallo A, Tandon M, Alevizos I, Illei GG. The majority of microRNAs detectable in serum and saliva is concentrated in exosomes. Plos One. 2012;7:e30679.10.1371/journal.pone.0030679
   PubMed Web of Science ®Google Scholar
• Yang M, Chen J, Su F, Yu B, Su F, Lin L, et al. Microvesicles secreted by macrophages shuttle invasionpotentiating microRNAs into breast cancer cells. Mol Cancer. 2011;10:117.doi: 10.1186/1476-4598-10-117.10.1186/1476-4598-10-117
   PubMed Web of Science ®Google Scholar
• King HW, Michael MZ, Gleadle JM. Hypoxic enhancement of exosome release by breast cancer cells. BMC Cancer. 2012;12:421.doi: 10.1186/1471-2407-12-421.10.1186/1471-2407-12-421
   PubMed Web of Science ®Google Scholar
• Shedden K, Xie TX, Chandaroy P, Chang YT, Rosania GR. Expulsion of small molecules in vesicles shed by cancer cells: association with gene expression and chemosensitivity profiles. Canc Res. 2003;63:4331–7.
   PubMed Web of Science ®Google Scholar
• Corcoran C, Rani S, O’Brien K, O’Neill A, Prencipe M, Sheikh R. Docetaxel-resistance in prostate cancer: evaluating associated phenotypic changes and potential for resistance transfer via exosomes. Plos One. 2012;7(12):e50999.10.1371/journal.pone.0050999
   PubMed Web of Science ®Google Scholar