Minimal residual disease in cancer therapy - Small things make all the difference

Drug Resistance Updates

Volumn 21-22, Issue , 2015, Pages 1-10

  Blatter, Sohvi ^a   Rottenberg, Sven ^a,b  

^a UNIVERSITY OF BERN   (Switzerland)

^b NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

Autophagy; BRCA1; Cancer dormancy; Cancer stem cells; Drug resistance; Drug tolerance; Genetically engineered mouse models; Microenvironment; Minimal residual disease

Indexed keywords

ARTICLE; AUTOPHAGY; BREAST CANCER; CANCER CHEMOTHERAPY; CANCER GROWTH; CANCER IMMUNOTHERAPY; CANCER RADIOTHERAPY; CANCER RECURRENCE; CANCER RESISTANCE; CANCER STEM CELL; CELL CYCLE ARREST; CELL PROLIFERATION; CELL SURVIVAL; DNA MODIFICATION; DNA REPAIR; DRUG TOLERANCE; EPITHELIAL MESENCHYMAL TRANSITION; GENETICALLY ENGINEERED MOUSE STRAIN; HUMAN; IMMUNOCOMPETENT CELL; MINIMAL RESIDUAL DISEASE; MITOSIS RATE; NONHUMAN; PATHOPHYSIOLOGY; PHENOTYPE; POLYPLOIDY; PRIORITY JOURNAL; STEM CELL TRANSPLANTATION; TREATMENT RESPONSE; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION; ANIMAL; DRUG EFFECTS; DRUG RESISTANCE; METABOLISM; MOUSE; NEOPLASM, RESIDUAL; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; PATHOLOGY; TRANSGENIC MOUSE;

ANTINEOPLASTIC AGENT;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL SURVIVAL; DRUG RESISTANCE, NEOPLASM; HUMANS; MICE; MICE, TRANSGENIC; NEOPLASM, RESIDUAL; NEOPLASMS; NEOPLASTIC STEM CELLS; NEOVASCULARIZATION, PATHOLOGIC;

EID: 84941182308     PISSN: 13687646     EISSN: 15322084     Source Type: Journal    
DOI: 10.1016/j.drup.2015.08.003     Document Type: Article

References (97)

1. J.A. Aguirre-Ghiso Models, mechanisms and clinical evidence for cancer dormancy Nat. Rev. Cancer 7 2007 834 846 10.1038/nrc2256
2. N. André, M. Carré, and E. Pasquier Metronomics: towards personalized chemotherapy? Nat. Rev. Clin. Oncol. 11 2014 413 431 10.1038/nrclinonc.2014.89
3. C. Bellodi, M.R. Lidonnici, A. Hamilton, G.V. Helgason, A.R. Soliera, M. Ronchetti, S. Galavotti, K.W. Young, T. Selmi, R. Yacobi, R.A. Van Etten, N. Donato, A. Hunter, D. Dinsdale, E. Tirrò, P. Vigneri, P. Nicotera, M.J. Dyer, T. Holyoake, P. Salomoni, and B. Calabretta Targeting autophagy potentiates tyrosine kinase inhibitor-induced cell death in Philadelphia chromosome-positive cells, including primary CML stem cells J. Clin. Invest. 119 2009 1109 1123 10.1172/JCI35660
4. P. Borst Cancer drug pan-resistance: pumps, cancer stem cells, quiescence, epithelial to mesenchymal transition, blocked cell death pathways, persisters or what? Open Biol. 2 2012 120066 10.1098/rsob.120066
5. J.M. Brown, and L.D. Attardi The role of apoptosis in cancer development and treatment response Nat. Rev. Cancer 5 2005 231 237 10.1038/nrc1560
6. R.A. Burrell, and C. Swanton Tumour heterogeneity and the evolution of polyclonal drug resistance Mol. Oncol. 8 2014 1095 1111 10.1016/j.molonc.2014.06.005
7. A.R. Cardones, and L.L. Banez VEGF inhibitors in cancer therapy Curr. Pharm. Des. 12 2006 387 394
8. J. Chen, Y. Li, T.-S. Yu, R.M. McKay, D.K. Burns, S.G. Kernie, and L.F. Parada A restricted cell population propagates glioblastoma growth after chemotherapy Nature 488 2012 522 526 10.1038/nature11287
9. H. Clevers The cancer stem cell: premises, promises and challenges Nat. Med. 2011 313 319 10.1038/nm.2304
10. S. Colak, and J.P. Medema Cancer stem cells - important players in tumor therapy resistance FEBS J. 281 2014 4779 4791 10.1111/febs.13023
11. K.M. Comerford, T.J. Wallace, J. Karhausen, N.A. Louis, M.C. Montalto, and S.P. Colgan Hypoxia-inducible factor-1-dependent regulation of the multidrug resistance (MDR1) gene Cancer Res. 62 2002 3387 3394
12. S.M. Cross, C.A. Sanchez, C.A. Morgan, M.K. Schimke, S. Ramel, R.L. Idzerda, W.H. Raskind, and B.J. Reid A p53-dependent mouse spindle checkpoint Science 267 1995 1353 1356
13. I. Dey-Guha, A. Wolfer, A.C. Yeh, G.J. Albeck, R. Darp, E. Leon, J. Wulfkuhle, E.F. Petricoin, B.S. Wittner, and S. Ramaswamy Asymmetric cancer cell division regulated by AKT Proc. Natl. Acad. Sci. U. S. A. 108 2011 12845 12850 10.1073/pnas.1109632108
14. K.K. Dhillon, E.M. Swisher, and T. Taniguchi Secondary mutations of BRCA1/2 and drug resistance Cancer Sci. 102 2011 663 669 10.1111/j.1349-7006.2010.01840.x
15. G. Driessens, B. Beck, A. Caauwe, B.D. Simons, and C. Blanpain Defining the mode of tumour growth by clonal analysis Nature 488 2012 527 530 10.1038/nature11344
16. J.A. Ewald, J.A. Desotelle, G. Wilding, and D.F. Jarrard Therapy-induced senescence in cancer J. Natl. Cancer Inst. 102 2010 1536 1546 10.1093/jnci/djq364
17. O.J. Finn Human tumor antigens, immunosurveillance, and cancer vaccines Immunol. Res. 36 2006 73 82 10.1385/IR:36:1:73
18. L.E. Gerweck, S. Vijayappa, and S. Kozin Tumor pH controls the in vivo efficacy of weak acid and base chemotherapeutics Mol. Cancer Ther. 5 2006 1275 1279 10.1158/1535-7163.MCT-06-0024
19. J.-P. Gillet, T. Efferth, and J. Remacle Chemotherapy-induced resistance by ATP-binding cassette transporter genes Biochim. Biophys. Acta 1775 2007 237 262 10.1016/j.bbcan.2007.05.002
20. N. Gonen, and Y.G. Assaraf Antifolates in cancer therapy: structure, activity and mechanisms of drug resistance Drug Resist. Updates 15 2012 183 210 10.1016/j.drup.2012.07.002
21. Y.-S. Guo, G.-F. Jin, C.W. Houston, J.C. Thompson, and C.M. Townsend Insulin-like growth factor-I promotes multidrug resistance in MCLM colon cancer cells J. Cell. Physiol. 175 1998 141 148 10.1002/(SICI)1097-4652(199805)175:2<141::AID-JCP3>3.0.CO;2-O
22. G.V. Hegde, C. de la Cruz, J. Eastham-Anderson, Y. Zheng, E.A. Sweet-Cordero, and E.L. Jackson Residual tumor cells that drive disease relapse after chemotherapy do not have enhanced tumor initiating capacity PLoS ONE 7 2012 e45647 10.1371/journal.pone.0045647
23. T. Hennet, G. Bertoni, C. Richter, and E. Peterhans Expression of BCL-2 protein enhances the survival of mouse fibrosarcoid cells in tumor necrosis factor-mediated cytotoxicity Cancer Res. 53 1993 1456 1460
24. E. Ikeda, M.G. Achen, G. Breier, and W. Risau Hypoxia-induced transcriptional activation and increased mRNA stability of vascular endothelial growth factor in C6 glioma cells J. Biol. Chem. 270 1995 19761 19766
25. T.M. Illidge, M.S. Cragg, B. Fringes, P. Olive, and J.A. Erenpreisa Polyploid giant cells provide a survival mechanism for p53 mutant cells after DNA damage Cell Biol. Int. 24 2000 621 633 10.1006/cbir.2000.0557
26. J.E. Jaspers, A. Kersbergen, U. Boon, W. Sol, L. van Deemter, S.A. Zander, R. Drost, E. Wientjens, J. Ji, A. Aly, J.H. Doroshow, A. Cranston, N.M.B. Martin, A. Lau, M.J. O'Connor, S. Ganesan, P. Borst, J. Jonkers, and S. Rottenberg Loss of 53BP1 causes PARP inhibitor resistance in Brca1-mutated mouse mammary tumors Cancer Discov. 3 2013 68 81 10.1158/2159-8290.CD-12-0049
27. C.H. June, S.R. Riddell, and T.N. Schumacher Adoptive cellular therapy: a race to the finish line Sci. Transl. Med. 7 2015 280ps7 10.1126/scitranslmed.aaa3643
28. K. Kakimi, H. Matsushita, A. Hosoi, M. Miyai, and O. Ohara CTLs regulate tumor growth via cytostatic effects rather than cytotoxicity: a few T cells can influence the growth of many times more tumor cells Oncoimmunology 4 2015 e970464 10.4161/21624011.2014.970464
29. H.T. Khong, and N.P. Restifo Natural selection of tumor variants in the generation of "tumor escape" phenotypes Nat. Immunol. 3 2002 999 1005 10.1038/ni1102-999
30. E.J. Kim, V. Sahai, E.V. Abel, K.A. Griffith, J.K. Greenson, N. Takebe, G.N. Khan, J.L. Blau, R. Craig, U.G. Balis, M.M. Zalupski, and D.M. Simeone Pilot clinical trial of hedgehog pathway inhibitor GDC-0449 (vismodegib) in combination with gemcitabine in patients with metastatic pancreatic adenocarcinoma Clin. Cancer Res. 20 2014 5937 5945 10.1158/1078-0432.CCR-14-1269
31. J.J. Kim, and I.F. Tannock Repopulation of cancer cells during therapy: an important cause of treatment failure Nat. Rev. Cancer 5 2005 516 525 10.1038/nrc1650
32. M. Konopleva, S. Zhao, W. Hu, S. Jiang, V. Snell, D. Weidner, C.E. Jackson, X. Zhang, R. Champlin, E. Estey, J.C. Reed, and M. Andreeff The anti-apoptotic genes Bcl-X(L) and Bcl-2 are over-expressed and contribute to chemoresistance of non-proliferating leukaemic CD34+ cells Br. J. Haematol. 118 2002 521 534
33. B.-K. Koo, and H. Clevers Stem cells marked by the R-spondin receptor LGR5 Gastroenterology 147 2014 289 302 10.1053/j.gastro.2014.05.007
34. E.J. Kort, N. Paneth, and G.F.V. Woude The decline in US cancer mortality in people born since 1925 Cancer Res. 69 2009 6500 6505 10.1158/0008-5472.CAN-09-0357
35. A. Kreso, C.A. O'Brien, P. van Galen, O.I. Gan, F. Notta, A.M.K. Brown, K. Ng, J. Ma, E. Wienholds, C. Dunant, A. Pollett, S. Gallinger, J. McPherson, C.G. Mullighan, D. Shibata, and J.E. Dick Variable clonal repopulation dynamics influence chemotherapy response in colorectal cancer Science 339 2013 543 548 10.1126/science.1227670
36. A.V. Kurtova, J. Xiao, Q. Mo, S. Pazhanisamy, R. Krasnow, S.P. Lerner, F. Chen, T.T. Roh, E. Lay, P.L. Ho, and K.S. Chan Blocking PGE2-induced tumour repopulation abrogates bladder cancer chemoresistance Nature 517 2015 209 213 10.1038/nature14034
37. R.J. Leary, M. Sausen, I. Kinde, N. Papadopoulos, J.D. Carpten, D. Craig, J. O'Shaughnessy, K.W. Kinzler, G. Parmigiani, B. Vogelstein, L.A. Diaz, and V.E. Velculescu Detection of chromosomal alterations in the circulation of cancer patients with whole-genome sequencing Sci. Transl. Med. 4 2012 10.1126/scitranslmed.3004742 162ra154-162ra154
38. W. Lin, N. Rajbhandari, C. Liu, K. Sakamoto, Q. Zhang, A.A. Triplett, S.K. Batra, R. Opavsky, D.W. Felsher, D.J. DiMaio, M.A. Hollingsworth, J.P. Morris, M. Hebrok, A.K. Witkiewicz, J.R. Brody, H. Rui, and K.-U. Wagner Dormant cancer cells contribute to residual disease in a model of reversible pancreatic cancer Cancer Res. 73 2013 1821 1830 10.1158/0008-5472.CAN-12-2067
39. X. Liu, H. Holstege, H. van der Gulden, M. Treur-Mulder, J. Zevenhoven, A. Velds, R.M. Kerkhoven, M.H. van Vliet, L.F.A. Wessels, J.L. Peterse, A. Berns, and J. Jonkers Somatic loss of BRCA1 and p53 in mice induces mammary tumors with features of human BRCA1-mutated basal-like breast cancer Proc. Natl. Acad. Sci. U. S. A. 104 2007 12111 12116 10.1073/pnas.0702969104
40. Y.D. Livney, and Y.G. Assaraf Rationally designed nanovehicles to overcome cancer chemoresistance Adv. Drug Deliv. Rev. 65 2013 1716 1730 10.1016/j.addr.2013.08.006
41. C.J. Lord, A.N.J. Tutt, and A. Ashworth Synthetic lethality and cancer therapy: lessons learned from the development of PARP inhibitors Annu. Rev. Med. 66 2015 455 470 10.1146/annurev-med-050913-022545
42. H. Lu, K.R. Clauser, W.L. Tam, J. Fröse, X. Ye, E.N. Eaton, F. Reinhardt, V.S. Donnenberg, R. Bhargava, S.A. Carr, and R.A. Weinberg A breast cancer stem cell niche supported by juxtacrine signalling from monocytes and macrophages Nat. Cell Biol. 16 2014 1105 1117 10.1038/ncb3041
43. S.J. Mandriota, and M.S. Pepper Regulation of angiopoietin-2 mRNA levels in bovine microvascular endothelial cells by cytokines and hypoxia Circ. Res. 83 1998 852 859
44. J.R.W. Masters, and B. Köberle Curing metastatic cancer: lessons from testicular germ-cell tumours Nat. Rev. Cancer 3 2003 517 525 10.1038/nrc1120
45. C.E. Meacham, and S.J. Morrison Tumour heterogeneity and cancer cell plasticity Nature 501 2013 328 337 10.1038/nature12624
46. P. Mordant, Y. Loriot, B. Lahon, Y. Castier, G. Lesèche, J.-C. Soria, C. Massard, and E. Deutsch Minimal residual disease in solid neoplasia: new frontier or red-herring? Cancer Treat. Rev. 38 2012 101 110 10.1016/j.ctrv.2011.04.014
47. C.K.Y. Ng, B. Weigelt, R. A'Hern, F.-C. Bidard, C. Lemetre, C. Swanton, R. Shen, and J.S. Reis-Filho Predictive performance of microarray gene signatures: impact of tumor heterogeneity and multiple mechanisms of drug resistance Cancer Res. 74 2014 2946 2961 10.1158/0008-5472.CAN-13-3375
48. T. Ni Chonghaile, K.A. Sarosiek, T.-T. Vo, J.A. Ryan, A. Tammareddi, V.D.G. Moore, J. Deng, K.C. Anderson, P. Richardson, Y.-T. Tai, C.S. Mitsiades, U.A. Matulonis, R. Drapkin, R. Stone, D.J. Deangelo, D.J. McConkey, S.E. Sallan, L. Silverman, M.S. Hirsch, D.R. Carrasco, and A. Letai Pretreatment mitochondrial priming correlates with clinical response to cytotoxic chemotherapy Science 334 2011 1129 1133 10.1126/science.1206727
49. M.J. Niederst, and J.A. Engelman Bypass mechanisms of resistance to receptor tyrosine kinase inhibition in lung cancer Sci. Signal. 6 2013 re6 10.1126/scisignal.2004652
50. B. Norquist, K.A. Wurz, C.C. Pennil, R. Garcia, J. Gross, W. Sakai, B.Y. Karlan, T. Taniguchi, and E.M. Swisher Secondary somatic mutations restoring BRCA1/2 predict chemotherapy resistance in hereditary ovarian carcinomas J. Clin. Oncol. 29 2011 3008 3015 10.1200/JCO. 2010.34.2980
51. K.P. Olive, M.A. Jacobetz, C.J. Davidson, A. Gopinathan, D. McIntyre, D. Honess, B. Madhu, M.A. Goldgraben, M.E. Caldwell, D. Allard, K.K. Frese, G. Denicola, C. Feig, C. Combs, S.P. Winter, H. Ireland-Zecchini, S. Reichelt, W.J. Howat, A. Chang, M. Dhara, L. Wang, F. Rückert, R. Grützmann, C. Pilarsky, K. Izeradjene, S.R. Hingorani, P. Huang, S.E. Davies, W. Plunkett, M. Egorin, R.H. Hruban, N. Whitebread, K. McGovern, J. Adams, C. Iacobuzio-Donahue, J. Griffiths, and D.A. Tuveson Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer Science 324 2009 1457 1461 10.1126/science.1171362
52. P.A. Ott, F.S. Hodi, and C. Robert CTLA-4 and PD-1/PD-L1 blockade: new immunotherapeutic modalities with durable clinical benefit in melanoma patients Clin. Cancer Res. 19 2013 5300 5309 10.1158/1078-0432.CCR-13-0143
53. M. Pajic, A. Kersbergen, F. van Diepen, A. Pfauth, J. Jonkers, P. Borst, and S. Rottenberg Tumor-initiating cells are not enriched in cisplatin-surviving BRCA1;p53-deficient mammary tumor cells in vivo Cell Cycle 9 2010 3780 3791
54. W. Pao, V.A. Miller, K.A. Politi, G.J. Riely, R. Somwar, M.F. Zakowski, M.G. Kris, and H. Varmus Acquired resistance of lung adenocarcinomas to gefitinib or erlotinib is associated with a second mutation in the EGFR kinase domain PLoS Med. 2 2005 e73 10.1371/journal.pmed.0020073
55. A.-M. Patch, E.L. Christie, D. Etemadmoghadam, D.W. Garsed, J. George, S. Fereday, K. Nones, P. Cowin, K. Alsop, P.J. Bailey, K.S. Kassahn, F. Newell, M.C.J. Quinn, S. Kazakoff, K. Quek, C. Wilhelm-Benartzi, E. Curry, H.S. Leong, Australian Ovarian Cancer Study Group, A. Hamilton, L. Mileshkin, G. Au-Yeung, C. Kennedy, J. Hung, Y.-E. Chiew, P. Harnett, M. Friedlander, M. Quinn, J. Pyman, S. Cordner, P. O'Brien, J. Leditschke, G. Young, K. Strachan, P. Waring, W. Azar, C. Mitchell, N. Traficante, J. Hendley, H. Thorne, M. Shackleton, D.K. Miller, G.M. Arnau, R.W. Tothill, T.P. Holloway, T. Semple, I. Harliwong, C. Nourse, E. Nourbakhsh, S. Manning, S. Idrisoglu, T.J.C. Bruxner, A.N. Christ, B. Poudel, O. Holmes, M. Anderson, C. Leonard, A. Lonie, N. Hall, S. Wood, D.F. Taylor, Q. Xu, J.L. Fink, N. Waddell, R. Drapkin, E. Stronach, H. Gabra, R. Brown, A. Jewell, S.H. Nagaraj, E. Markham, P.J. Wilson, J. Ellul, O. McNally, M.A. Doyle, R. Vedururu, C. Stewart, E. Lengyel, J.V. Pearson, N. Waddell, A. deFazio, S.M. Grimmond, and D.D.L. Bowtell Whole-genome characterization of chemoresistant ovarian cancer Nature 521 2015 489 494 10.1038/nature14410
56. A.W. Payne, D.K. Pant, T.-C. Pan, and L.A. Chodosh Ceramide kinase promotes tumor cell survival and mammary tumor recurrence Cancer Res. 74 2014 6352 6363 10.1158/0008-5472.CAN-14-1292
57. N. Podergajs, N. Brekka, B. Radlwimmer, C. Herold-Mende, K.M. Talasila, K. Tiemann, U. Rajcevic, T.T. Lah, R. Bjerkvig, and H. Miletic Expansive growth of two glioblastoma stem-like cell lines is mediated by bFGF and not by EGF Radiol. Oncol. 47 2013 330 337 10.2478/raon-2013-0063
58. K. Politi, M.F. Zakowski, P.-D. Fan, E.A. Schonfeld, W. Pao, and H.E. Varmus Lung adenocarcinomas induced in mice by mutant EGF receptors found in human lung cancers respond to a tyrosine kinase inhibitor orto down-regulation of the receptors Genes Dev. 20 2006 1496 1510 10.1101/gad.1417406
59. P.-E. Puig, M.-N. Guilly, A. Bouchot, N. Droin, D. Cathelin, F. Bouyer, L. Favier, F. Ghiringhelli, G. Kroemer, E. Solary, F. Martin, and B. Chauffert Tumor cells can escape DNA-damaging cisplatin through DNA endoreduplication and reversible polyploidy Cell Biol. Int. 32 2008 1031 1043 10.1016/j.cellbi.2008.04.021
60. E.B. Rankin, K.C. Fuh, L. Castellini, K. Viswanathan, E.C. Finger, A.N. Diep, E.L. LaGory, M.S. Kariolis, A. Chan, D. Lindgren, H. Axelson, Y.R. Miao, A.J. Krieg, and A.J. Giaccia Direct regulation of GAS6/AXL signaling by HIF promotes renal metastasis through SRC and MET Proc. Natl. Acad. Sci. U.S.A. 111 2014 13373 13378 10.1073/pnas.1404848111
61. S. Raz, D. Sheban, N. Gonen, M. Stark, B. Berman, and Y.G. Assaraf Severe hypoxia induces complete antifolate resistance in carcinoma cells due to cell cycle arrest Cell Death Dis. 5 2014 e1067 10.1038/cddis.2014.39
62. T. Reya, S.J. Morrison, M.F. Clarke, and I.L. Weissman Stem cells, cancer, and cancer stem cells Nature 414 2001 105 111 10.1038/35102167
63. S. Rottenberg, and P. Borst Drug resistance in the mouse cancer clinic Drug Resist. Updates 15 2012 81 89 10.1016/j.drup.2012.01.001
64. S. Rottenberg, J.E. Jaspers, A. Kersbergen, E. van der Burg, A.O.H. Nygren, S.A.L. Zander, P.W.B. Derksen, M. de Bruin, J. Zevenhoven, A. Lau, R. Boulter, A. Cranston, M.J. O'Connor, N.M.B. Martin, P. Borst, and J. Jonkers High sensitivity of BRCA1-deficient mammary tumors to the PARP inhibitor AZD2281 alone and in combination with platinum drugs Proc. Natl. Acad. Sci. U. S. A. 105 2008 17079 17084 10.1073/pnas.0806092105
65. S. Rottenberg, A.O.H. Nygren, M. Pajic, F.W.B. van Leeuwen, I. van der Heijden, K. van de Wetering, X. Liu, K.E. de Visser, K.G. Gilhuijs, O. van Tellingen, J.P. Schouten, J. Jonkers, and P. Borst Selective induction of chemotherapy resistance of mammary tumors in a conditional mouse model for hereditary breast cancer Proc. Natl. Acad. Sci. U. S. A. 104 2007 12117 12122 10.1073/pnas.0702955104
66. S. Rottenberg, M.A. Vollebergh, B. de Hoon, J. de Ronde, P.C. Schouten, A. Kersbergen, S.A.L. Zander, M. Pajic, J.E. Jaspers, M. Jonkers, M. Lodén, W. Sol, E. van der Burg, J. Wesseling, J.-P. Gillet, M.M. Gottesman, J. Gribnau, L. Wessels, S.C. Linn, J. Jonkers, and P. Borst Impact of intertumoral heterogeneity on predicting chemotherapy response of BRCA1-deficient mammary tumors Cancer Res. 72 2012 2350 2361 10.1158/0008-5472.CAN-11-4201
67. W. Sakai, E.M. Swisher, B.Y. Karlan, M.K. Agarwal, J. Higgins, C. Friedman, E. Villegas, C. Jacquemont, D.J. Farrugia, F.J. Couch, N. Urban, and T. Taniguchi Secondary mutations as a mechanism of cisplatin resistance in BRCA2-mutated cancers Nature 451 2008 1116 1120 10.1038/nature06633
68. D. Samanta, D.M. Gilkes, P. Chaturvedi, L. Xiang, and G.L. Semenza Hypoxia-inducible factors are required for chemotherapy resistance of breast cancer stem cells Proc. Natl. Acad. Sci. U. S. A. 111 2014 E5429 E5438 10.1073/pnas.1421438111
69. A.G. Schepers, H.J. Snippert, D.E. Stange, M. van den Born, J.H. van Es, M. van de Wetering, and H. Clevers Lineage tracing reveals Lgr5 + stem cell activity in mouse intestinal adenomas Science 337 2012 730 735 10.1126/science.1224676
70. M. Schrappe Minimal residual disease: optimal methods, timing, and clinical relevance for an individual patient Hematology 2012 2012 137 142 10.1182/asheducation-2012.1.137
71. R.D. Schreiber, L.J. Old, and M.J. Smyth Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion Science 331 2011 1565 1570 10.1126/science.1203486
72. T.N. Schumacher, C. Kesmir, and M.M. van Buuren Biomarkers in cancer immunotherapy Cancer Cell 27 2015 12 14 10.1016/j.ccell.2014.12.004
73. C. Seidel, C. Florean, M. Schnekenburger, M. Dicato, and M. Diederich Chromatin-modifying agents in anti-cancer therapy Biochimie 94 2012 2264 2279 10.1016/j.biochi.2012.05.012 Special Section on Epigenetics
74. B.C. Shaffer, J.-P. Gillet, C. Patel, M.R. Baer, S.E. Bates, and M.M. Gottesman Drug resistance: still a daunting challenge to the successful treatment of AML Drug Resist. Updates 15 2012 62 69 10.1016/j.drup.2012.02.001
75. S.V. Sharma, D.Y. Lee, B. Li, M.P. Quinlan, F. Takahashi, S. Maheswaran, U. McDermott, N. Azizian, L. Zou, M.A. Fischbach, K.-K. Wong, K. Brandstetter, B. Wittner, S. Ramaswamy, M. Classon, and J. Settleman A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations Cell 141 2010 69 80 10.1016/j.cell.2010.02.027
76. T. Shimizu, E. Sugihara, S. Yamaguchi-Iwai, S. Tamaki, Y. Koyama, W. Kamel, A. Ueki, T. Ishikawa, T. Chiyoda, S. Osuka, N. Onishi, H. Ikeda, J. Kamei, K. Matsuo, Y. Fukuchi, T. Nagai, J. Toguchida, Y. Toyama, A. Muto, and H. Saya IGF2 preserves osteosarcoma cell survival by creating an autophagic state of dormancy that protects cells against chemotherapeutic stress Cancer Res. 74 2014 6531 6541 10.1158/0008-5472.CAN-14-0914
77. A.K. Singh, R.K. Arya, S. Maheshwari, A. Singh, S. Meena, P. Pandey, O. Dormond, and D. Datta Tumor heterogeneity and cancer stem cell paradigm: updates in concept, controversies and clinical relevance Int. J. Cancer 136 2015 1991 2000 10.1002/ijc.28804
78. M.S. Sosa, P. Bragado, and J.A. Aguirre-Ghiso Mechanisms of disseminated cancer cell dormancy: an awakening field Nat. Rev. Cancer 14 2014 611 622 10.1038/nrc3793
79. R. Straussman, T. Morikawa, K. Shee, M. Barzily-Rokni, Z.R. Qian, J. Du, A. Davis, M.M. Mongare, J. Gould, D.T. Frederick, Z.A. Cooper, P.B. Chapman, D.B. Solit, A. Ribas, R.S. Lo, K.T. Flaherty, S. Ogino, J.A. Wargo, and T.R. Golub Tumour micro-environment elicits innate resistance to RAF inhibitors through HGF secretion Nature 487 2012 500 504 10.1038/nature11183
80. E.M. Swisher, W. Sakai, B.Y. Karlan, K. Wurz, N. Urban, and T. Taniguchi Secondary BRCA1 mutations in BRCA1-mutated ovarian carcinomas with platinum resistance Cancer Res. 68 2008 2581 2586 10.1158/0008-5472.CAN-08-0088
81. N. Takebe, P.J. Harris, R.Q. Warren, and S.P. Ivy Targeting cancer stem cells by inhibiting Wnt Notch, and Hedgehog pathways Nat. Rev. Clin. Oncol. 8 2011 97 106 10.1038/nrclinonc.2010.196
82. I.F. Tannock, and D. Rotin Acid pH in tumors and its potential for therapeutic exploitation Cancer Res. 49 1989 4373 4384
83. O. Trédan, C.M. Galmarini, K. Patel, and I.F. Tannock Drug resistance and the solid tumor microenvironment J. Natl. Cancer Inst. 99 2007 1441 1454 10.1093/jnci/djm135
84. N.C. Turner, and A.N. Tutt Platinum chemotherapy for BRCA1-related breast cancer: do we need more evidence? Breast Cancer Res. 14 2012 115 10.1186/bcr3332
85. M.D. Vesely, M.H. Kershaw, R.D. Schreiber, and M.J. Smyth Natural innate and adaptive immunity to cancer Annu. Rev. Immunol. 29 2011 235 271 10.1146/annurev-immunol-031210-101324
86. A. Viale, P. Pettazzoni, C.A. Lyssiotis, H. Ying, N. Sánchez, M. Marchesini, A. Carugo, T. Green, S. Seth, V. Giuliani, M. Kost-Alimova, F. Muller, S. Colla, L. Nezi, G. Genovese, A.K. Deem, A. Kapoor, W. Yao, E. Brunetto, Y. Kang, M. Yuan, J.M. Asara, Y.A. Wang, T.P. Heffernan, A.C. Kimmelman, H. Wang, J.B. Fleming, L.C. Cantley, R.A. DePinho, and G.F. Draetta Oncogene ablation-resistant pancreatic cancer cells depend on mitochondrial function Nature 514 2014 628 632 10.1038/nature13611
87. M.A. Vollebergh, E.H. Lips, P.M. Nederlof, L.F.A. Wessels, J. Wesseling, M.J. Vd Vijver, E.G.E. de Vries, H. van Tinteren, J. Jonkers, M. Hauptmann, S. Rodenhuis, and S.C. Linn Genomic patterns resembling BRCA1- and BRCA2-mutated breast cancers predict benefit of intensified carboplatin-based chemotherapy Breast Cancer Res. 16 2014 R47 10.1186/bcr3655
88. Q. Wang, P.C. Wu, D.Z. Dong, I. Ivanova, E. Chu, S. Zeliadt, H. Vesselle, and D.Y. Wu Polyploidy road to therapy-induced cellular senescence and escape Int. J. Cancer 132 2013 1505 1515 10.1002/ijc.27810
89. S. Wang, and S.-Y. Lin Tumor dormancy: potential therapeutic target in tumor recurrence and metastasis prevention Exp. Hematol. Oncol. 2 2013 29 10.1186/2162-3619-2-29
90. T.R. Wilson, J. Fridlyand, Y. Yan, E. Penuel, L. Burton, E. Chan, J. Peng, E. Lin, Y. Wang, J. Sosman, A. Ribas, J. Li, J. Moffat, D.P. Sutherlin, H. Koeppen, M. Merchant, R. Neve, and J. Settleman Widespread potential for growth-factor-driven resistance to anticancer kinase inhibitors Nature 487 2012 505 509 10.1038/nature11249
91. G. Xu, J.R. Chapman, I. Brandsma, J. Yuan, M. Mistrik, P. Bouwman, J. Bartkova, E. Gogola, D. Warmerdam, M. Barazas, J.E. Jaspers, K. Watanabe, M. Pieterse, A. Kersbergen, W. Sol, P.H.N. Celie, P.C. Schouten, B. van den Broek, A. Salman, M. Nieuwland, I. de Rink, J. de Ronde, K. Jalink, S.J. Boulton, J. Chen, D.C. van Gent, J. Bartek, J. Jonkers, P. Borst, and S. Rottenberg REV7 counteracts DNA double-strand break resection and affects PARP inhibition Nature 521 2015 541 544 10.1038/nature14328
92. H. Yu, M. Kortylewski, and D. Pardoll Crosstalk between cancer and immune cells: role of STAT3 in the tumour microenvironment Nat. Rev. Immunol. 7 2007 41 51 10.1038/nri1995
93. S.A.L. Zander, A. Kersbergen, E. van der Burg, N. de Water, O. van Tellingen, S. Gunnarsdottir, J.E. Jaspers, M. Pajic, A.O.H. Nygren, J. Jonkers, P. Borst, and S. Rottenberg Sensitivity and acquired resistance of BRCA1;p53-deficient mouse mammary tumors to the topoisomerase I inhibitor topotecan Cancer Res. 70 2010 1700 1710 10.1158/0008-5472.CAN-09-3367
94. H. Zhang, M. Bosch-Marce, L.A. Shimoda, Y.S. Tan, J.H. Baek, J.B. Wesley, F.J. Gonzalez, and G.L. Semenza Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia J. Biol. Chem. 283 2008 10892 10903 10.1074/jbc.M800102200
95. S. Zhang, I. Mercado-Uribe, Z. Xing, B. Sun, J. Kuang, and J. Liu Generation of cancer stem-like cells through the formation of polyploid giant cancer cells Oncogene 33 2014 116 128 10.1038/onc.2013.96
96. B. Zhitomirsky, and Y.G. Assaraf Lysosomal sequestration of hydrophobic weak base chemotherapeutics triggers lysosomal biogenesis and lysosome-dependent cancer multidrug resistance Oncotarget 6 2015 1143 1156
97. A. Zomer, S.I.J. Ellenbroek, L. Ritsma, E. Beerling, N. Vrisekoop, and J. Van Rheenen Intravital imaging of cancer stem cell plasticity in mammary tumors Stem Cells 31 2013 602 606 10.1002/stem.1296