Cancer drug pan-resistance: Pumps, cancer stem cells, quiescence, epithelial to mesenchymal transition, blocked cell death pathways, persisters or what?

Open Biology

Volumn 2, Issue MAY, 2012, Pages

  Borst, Piet ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

Drug resistance; Epithelial to mesenchymal transition; Multi drug resistance; Pan resistance; Persisters; Residual disease

Indexed keywords

ABC TRANSPORTER; ANTINEOPLASTIC AGENT; DNA; MULTIDRUG RESISTANCE PROTEIN; TUMOR PROTEIN;

ANIMAL; BIOAVAILABILITY; BIOLOGICAL MODEL; BLOOD BRAIN BARRIER; CANCER STEM CELL; CELL CYCLE; CELL DEATH; CHEMISTRY; CHROMATIN ASSEMBLY AND DISASSEMBLY; CLONAL EVOLUTION; CYTOLOGY; DNA REPAIR; DRUG ANTAGONISM; DRUG EFFECT; DRUG RESISTANCE; EPITHELIAL MESENCHYMAL TRANSITION; EXPERIMENTAL NEOPLASM; GENETIC EPIGENESIS; GENETICS; HUMAN; METABOLISM; MINIMAL RESIDUAL DISEASE; MOUSE; MULTI-DRUG RESISTANCE; PAN-RESISTANCE; PERSISTERS; PHYSIOLOGY; REVIEW;

DRUG RESISTANCE; EPITHELIAL TO MESENCHYMAL TRANSITION; MULTI-DRUG RESISTANCE; PAN-RESISTANCE; PERSISTERS; RESIDUAL DISEASE;

ANIMALS; ANTINEOPLASTIC AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL AVAILABILITY; BLOOD-BRAIN BARRIER; CELL CYCLE; CELL DEATH; CHROMATIN ASSEMBLY AND DISASSEMBLY; CLONAL EVOLUTION; DNA REPAIR; DNA, NEOPLASM; DRUG RESISTANCE, NEOPLASM; EPIGENESIS, GENETIC; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; MICE; MODELS, BIOLOGICAL; NEOPLASM PROTEINS; NEOPLASM, RESIDUAL; NEOPLASMS, EXPERIMENTAL; NEOPLASTIC STEM CELLS; P-GLYCOPROTEIN;

EID: 84864256047     PISSN: None     EISSN: 20462441     Source Type: Journal    
DOI: 10.1098/rsob.120066     Document Type: Article

References (90)

1. Swanton C, Nicke B, Marani M, Kelly G, Downward J. 2007 Initiation of high frequency multi-drug resistance following kinase targeting by siRNAs. Cell Cycle 6, 2001-2004. (doi:10.4161/cc.6.16.4538) (Pubitemid 47327887)
2. Falagas ME, Karageorgopoulos DE. 2008 Pandrug resistance (PDR), extensive drug resistance (XDR), and multidrug resistance (MDR) among Gram-negative bacilli: need for international harmonization in terminology. Clin. Infect Dis. 46, 1121-1122. (doi:10.1086/528867) (Pubitemid 351589881)
3. Harris AL. 1985 DNA repair and resistance to chemotherapy. Cancer Surv. 4, 601-624.
4. Kaelin Jr WG. 2005 The concept of synthetic lethality in the context of anticancer therapy. Nat. Rev. Cancer 5, 689-698. (doi:10.1038/nrc1691) (Pubitemid 41486362)
5. Chan DA, Giaccia AJ. 2011 Harnessing synthetic lethal interactions in anticancer drug discovery. Nat. Rev. Drug Discov. 10, 351-364. (doi:10.1038/nrd3374)
6. Tsukamoto S, Akashi-Tanaka S, Shien T, Terada K, Kinoshita T. 2007 Brain metastases after achieving local pathological complete responses with neoadjuvant chemotherapy. Breast Cancer 14, 420-424. (doi:10.2325/jbcs.14.420)
7. Bendell JC et al. 2003 Central nervous system metastases in women who receive trastuzumabbased therapy for metastatic breast carcinoma. Cancer 97, 2972-2977. (doi:10.1002/cncr.11436) (Pubitemid 36676250)
8. Olive KP et al. 2009 Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science 324, 1457-1461. (doi:10.1126/science.1171362)
9. Tuveson D, Hanahan D. 2011 Translational medicine: cancer lessons from mice to humans. Nature 471, 316-317. (doi:10.1038/471316a)
10. Michaud M et al. 2011 Autophagy-dependent anticancer immune responses induced by chemotherapeutic agents in mice. Science 334, 1573-1577. (doi:10.1126/science.1208347)
11. Ciampricotti M, Hau CS, Doornebal CW, Jonkers J, de Visser KE. 2012 Chemotherapy response of spontaneous mammary tumors is independent of the adaptive immune system. Nat. Med. 18, 344-346.
12. Juliano RL, Ling V. 1976 A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants. Biochim. Biophys. Acta 455, 152-162. (doi:10.1016/0005-2736(76)90160-7)
13. Szakacs G, Paterson JK, Ludwig JA, Booth-Genthe C, Gottesman MM. 2006 Targeting multidrug resistance in cancer. Nat. Rev. Drug Discov. 5, 219-234. (doi:10.1038/nrd1984) (Pubitemid 43336035)
14. Borst P, Oude Elferink R. 2002 Mammalian ABC transporters in health and disease. Annu. Rev. Biochem. 71, 537-592. (Pubitemid 34800230)
15. Deeley RG, Westlake C, Cole SP. 2006 Transmembrane transport of endo-and xenobiotics by mammalian ATP-binding cassette multidrug resistance proteins. Physiol. Rev. 86, 849-899. (doi:10.1152/physrev.00035.2005) (Pubitemid 44033384)
16. Sarkadi B, Ozvegy-Laczka C, Nemet K, Varadi A. 2004 ABCG2-a transporter for all seasons. FEBS Lett. 567, 116-120. (doi:10.1016/j.febslet.2004. 03.123) (Pubitemid 38686433)
17. Haimeur A, Conseil G, Deeley RG, Cole SP. 2004 The MRP-related and BCRP/ABCG2 multidrug resistance proteins: biology, substrate specificity and regulation. Curr. Drug Metab. 5, 21-53. (doi:10. 2174/1389200043489199) (Pubitemid 38294344)
18. Chen ZS, Tiwari AK. 2011 Multidrug resistance proteins (MRPs/ABCCs) in cancer chemotherapy and genetic diseases. FEBS J. 278, 3226-3245. (doi:10. 1111/j.1742-4658.2011.08235.x)
19. Pajic M, Iyer JK, Kersbergen A, Van der Burg E, Nygren AO, Jonkers J, Borst P, Rottenberg S. 2009 Moderate increase in Mdr1a/1b expression causes in vivo resistance to doxorubicin in a mouse model for hereditary breast cancer. Cancer Res. 69, 6396-6404. (doi:10.1158/0008-5472.CAN-09-0041)
20. Zander S et al. 2010 Sensitivity and acquired resistance of BRCA1; -53-deficient mouse mammary tumors to the topoisomerase I inhibitor topotecan. Cancer Res. 70, 1700-1710. (doi:10.1158/0008-5472.CAN-09-3367)
21. Fojo T, Bates S. 2003 Strategies for reversing drug resistance. Oncogene 22, 7512-7523. (doi:10.1038/ sj.onc.1206951) (Pubitemid 37487173)
22. Bates SF, Chen C, Robey R, Kang M, Figg WD, Fojo T. 2002 Reversal of multidrug resistance: lessons from clinical oncology. Novartis Found Symp. 243, 83-9+ (doi:10.1002/0470846356.ch7)
23. Huff LM, Lee JS, Robey RW, Fojo T. 2006 Characterization of gene rearrangements leading to activation of MDR-1. J. Biol. Chem. 281, 36 501-36 509. (doi:10.1074/jbc.M602998200) (Pubitemid 46042117)
24. Hannemann J, Oosterkamp HM, Bosch CA, Velds A, Wessels LF, Loo C, Rutgers EJ, Rodenhuis S, van de Vijver MJ. 2005 Changes in gene expression associated with response to neoadjuvant chemotherapy in breast cancer. J. Clin. Oncol. 23, 3331-3342. (doi:10.1200/JCO.2005.09.077)
25. Lee JK, Coutant C, Kim YC, Qi Y, Theodorescu D, Symmans WF, Baggerly K, Rouzier R, Pusztai L. 2010 Prospective comparison of clinical and genomic multivariate predictors of response to neoadjuvant chemotherapy in breast cancer. Clin. Cancer Res. 16, 711-718. (doi:10.1158/1078-0432.CCR-09-2247)
26. Desmedt C et al. 2011 Multifactorial approach to predicting resistance to anthracyclines. J. Clin. Oncol. 29, 1578-1586. (doi:10.1200/JCO.2010.31.2231)
27. Rottenberg S et al. 2007 Selective induction of chemotherapy resistance of mammary tumors in a conditional mouse model for hereditary breast cancer. Proc. Natl Acad. Sci. USA 104, 12 117-12 122. (doi:10.1073/pnas.0702955104) (Pubitemid 47185639)
28. Stewart DJ, Chiritescu G, Dahrouge S, Banerjee S, Tomiak EM. 2007 Chemotherapy dose-response relationships in non-small cell lung cancer and implied resistance mechanisms. Cancer Treat Rev. 33, 101-137. (doi:10.1016/j.ctrv.2006.12.002) (Pubitemid 46343105)
29. Sijbers AM, van der Spek PJ, Odijk H, van den Berg J, van Duin M, Westerveld A, Jaspers NGJ, Bootsma D, Hoeijmakers JHJ. 1996 Mutational analysis of the human nucleotide excision repair gene ERCC1. Nucleic Acids Res. 24, 3370-3380. (doi:10.1093/ nar/24.17.3370) (Pubitemid 26294449)
30. Gorre ME, Mohammed M, Ellwood K, Hsu N, Paquette R, Rao PN, Sawyers CL. 2001 Clinical resistance to STI-571 cancer therapy caused by BCR-ABL gene mutation or amplification. Science 293, 876-880. (doi:10.1126/science.1062538) (Pubitemid 32743979)
31. Carter TA et al. 2005 Inhibition of drug-resistant mutants of ABL, KIT, and EGF receptor kinases. Proc. Natl Acad. Sci. USA 102, 11 011-11 016. (doi:10. 1073/pnas.0504952102) (Pubitemid 41105984)
32. Shah NP, Skaggs BJ, Branford S, Hughes TP, Nicoll JM, Paquette RL, Sawyers CL. 2007 Sequential ABL kinase inhibitor therapy selects for compound drugresistant BCR-ABL mutations with altered oncogenic potency. J. Clin. Invest. 117, 2562-2569. (doi:10. 1172/JCI30890) (Pubitemid 47494357)
33. Kaiser J. 2011 Combining targeted drugs to stop resistant tumors. Science 331, 1542-1545. (doi:10. 1126/science.331.6024.1542)
34. Schmitt CA. 2033 Senescence, apoptosis and therapy: cutting the lifelines of cancer. Nat. Rev. Cancer 3, 286-295. (doi:10.1038/nrc1044)
35. Duy C et al. 2011 BCL6 enables Ph+ acute lymphoblastic leukaemia cells to survive BCR-ABL1 kinase inhibition. Nature 473, 384-388. (doi:10. 1038/nature09883)
36. Essers MA, Offner S, Blanco-Bose WE, Waibler Z, Kalinke U, Duchosal MA, Trumpp A. 2009 IFNalpha activates dormant haematopoietic stem cells in vivo. Nature 458, 904-908. (doi:10.1038/nature07815)
37. Essers MA, Trumpp A. 2010 Targeting leukemic stem cells by breaking their dormancy. Mol. Oncol. 4, 443-450. (doi:10.1016/j.molonc.2010.06.001)
38. Saito Y et al. 2010 Induction of cell cycle entry eliminates human leukemia stem cells in a mouse model of AML. Nat. Biotechnol. 28, 275-280. (doi:10.1038/nbt.1607)
39. Goff D, Jamieson C. 2010 Cycling toward elimination of leukemic stem cells. Cell Stem Cell 6, 296-297. (doi:10.1016/j.stem.2010.03.008)
40. Jiang X, Zhao Y, Smith C, Gasparetto M, Turhan A, Eaves A, Eaves C. 2007 Chronic myeloid leukemia stem cells possess multiple unique features of resistance to BCR-ABL targeted therapies. Leukemia 21, 926-935. (Pubitemid 46672068)
41. Roesch A et al. 2010 A temporarily distinct subpopulation of slow-cycling melanoma cells is required for continuous tumor growth. Cell 141, 583-594. (doi:10.1016/j.cell.2010.04.020)
42. Sharma SV et al. 2010 A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell 141, 69-80. (doi:10.1016/j. cell.2010.02.027)
43. Dey-Guha I et al. 2011 Asymmetric cancer cell division regulated by AKT. Proc. Natl Acad. Sci. USA 108, 12 845-12 850. (doi:10.1073/pnas.110963 2108)
44. Schewe DM, Aguirre-Ghiso JA. 2008 ATF6alpha-Rheb-mTOR signaling promotes survival of dormant tumor cells in vivo. Proc. Natl Acad. Sci. USA 105, 10 519-10 524. (doi:10.1073/pnas.0800939105)
45. Esteller M. 2008 Epigenetics in cancer. N. Engl. J. Med. 358, 1148-1159. (doi:10.1056/ NEJMra072067)
46. Tsai HC et al. 2012 Transient low doses of DNAdemethylating agents exert durable antitumor effects on hematological and epithelial tumor cells. Cancer Cell 21, 430-446. (doi:10.1016/j.ccr.2011.12.029)
47. Hauswald S, Duque-Afonso J, Wagner MM, Schertl FM, Lubbert M, Peschel C, Keller U, Licht T. 2009 Histone deacetylase inhibitors induce a very broad, pleiotropic anticancer drug resistance phenotype in acute myeloid leukemia cells by modulation of multiple ABC transporter genes. Clin. Cancer Res. 15, 3705-3715. (doi:10.1158/ 1078-0432.CCR-08-2048)
48. Clevers H. 2011 The cancer stem cell: premises, promises and challenges. Nat. Med. 17, 313-319. (doi:10.1038/nm.2304)
49. Dean M. 2009 ABC transporters, drug resistance, and cancer stem cells. J. Mammary Gland Biol. Neoplasia 14, 3-9. (doi:10.1007/s10911-009-9109-9)
50. Curtin JC, Lorenzi MV. 2010 Drug discovery approaches to target Wnt signaling in cancer stem cells. Oncotarget 1, 563-577.
51. Zhou BB, Zhang H, Damelin M, Geles KG, Grindley JC, Dirks PB. 2009 Tumour-initiating cells: challenges and opportunities for anticancer drug discovery. Nat. Rev. Drug Discov. 8, 806-823. (doi:10.1038/nrd2137)
52. Jordan CT. 2009 Cancer stem cells: controversial or just misunderstood? Cell Stem Cell 4, 203-205. (doi:10.1016/j.stem.2009.02.003)
53. Medema JP, Vermeulen L. 2011 Microenvironmental regulation of stem cells in intestinal homeostasis and cancer. Nature 474, 318-326. (doi:10.1038/ nature10212)
54. Quintana E, Shackleton M, Foster HR, Fullen DR, Sabel MS, Johnson TM, Morrison SJ. 2010 Phenotypic heterogeneity among tumorigenic melanoma cells from patients that is reversible and not hierarchically organized. Cancer Cell 18, 510-523. (doi:10.1016/j.ccr.2010.10.012)
55. Shackleton M, Vaillant F, Simpson KJ, Stingl J, Smyth GK, Asselin-Labat ML, Wu L, Lindeman GJ, Visvader JE. 2006 Generation of a functional mammary gland from a single stem cell. Nature 439, 84-88. (doi:10.1038/nature04372) (Pubitemid 43053633)
56. Visvader JE, Lindeman GJ. 2008 Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat. Rev. Cancer 8, 755-768. (doi:10. 1038/nrc2499)
57. Emmink BL et al. 2011 Differentiated human colorectal cancer cells protect tumor-initiating cells from irinotecan. Gastroenterology 141, 269-278. (doi:10.1053/j.gastro.2011.03.052)
58. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN. 2006 Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444, 756-760. (doi:10.1038/ nature05236) (Pubitemid 44949604)
59. Diehn M et al. 2009 Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 458, 780-783. (doi:10.1038/ nature07733)
60. Yan KS et al. 2012 The intestinal stem cell markers Bmi1 and Lgr5 identify two functionally distinct populations. Proc. Natl Acad. Sci. USA 109, 466-471. (doi:10.1073/pnas.1118857109)
61. Sotiropoulou PA et al. 2010 Bcl-2 and accelerated DNA repair mediates resistance of hair follicle bulge stem cells to DNA-damage-induced cell death. Nat. Cell Biol. 12, 572-582. (doi:10.1038/ ncb2059)
62. Begg AC, Stewart FA, Vens C. 2011 Strategies to improve radiotherapy with targeted drugs. Nat. Rev. Cancer 11, 239-253. (doi:10.1038/nrc3007)
63. Aguirre-Ghiso JA. 2007 Models, mechanisms and clinical evidence for cancer dormancy. Nat. Rev. Cancer 7, 834-846. (doi:10.1038/nrc2256) (Pubitemid 350006258)
64. Baguley BC. 2010 Multiple drug resistance mechanisms in cancer. Mol. Biotechnol. 46, 308-316. (doi:10.1007/s12033-010-9321-2)
65. Singh A, Settleman J. 2010 EMT cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene 29, 4741-4751. (doi:10. 1038/onc.2010.215)
66. Pajic M, Kersbergen A, van Diepen F, Pfauth A, Jonkers J, Borst P, Rottenberg S. 2010 Tumorinitiating cells are not enriched in cisplatinsurviving Brca12/2;p532/2 mammary tumor cells in vivo. Cell Cycle 9, 3780-3791. (doi:10. 4161/cc.9.18.13002)
67. Gupta PB, Onder TT, Jiang G, Tao K, Kuperwasser C, Weinberg RA, Lander ES. 2009 Identification of selective inhibitors of cancer stem cells by highthroughput screening. Cell 138, 645-659. (doi:10. 1016/j.cell.2009.06.034)
68. Frank NY, Schatton T, Frank MH. 2010 The therapeutic promise of the cancer stem cell concept. J. Clin. Invest. 120, 41-50. (doi:10.1172/JCI41004)
69. Low JA, de Sauvage FJ. 2010 Clinical experience with Hedgehog pathway inhibitors. J. Clin. Oncol. 28, 5321-5326. (doi:10.1200/JCO.2010.27.9943)
70. Borst P, Rottenberg S, Jonkers J. 2008 How do real tumors become resistant to cisplatin? Cell Cycle 7, 1353-1359. (doi:10.4161/cc.7.10.5930) (Pubitemid 351872573)
71. Turk D, Hall MD, Chu BF, Ludwig JA, Fales HM, Gottesman MM, Szakacs G. 2009 Identification of compounds selectively killing multidrug-resistant cancer cells. Cancer Res. 69, 8293-8301. (doi:10. 1158/0008-5472.CAN-09-2422)
72. Schmitt CA, Lowe SW. 2001 Apoptosis is critical for drug response in vivo. Drug Resist. Updat. 4, 132-134. (doi:10.1054/drup.2001.0188) (Pubitemid 32619571)
73. Borst P, Borst J, Smets LA. 2001 Does resistance to apoptosis affect clinical response to antitumor drugs? Drug Resist. Updat. 4, 129-131. (doi:10. 1054/drup.2001.0187) (Pubitemid 32619570)
74. Brown JM, Attardi LD. 2005 The role of apoptosis in cancer development and treatment response. Nat. Rev. Cancer 5, 231-237. (doi:10.1038/nrc1560) (Pubitemid 40314954)
75. Blagosklonny MV. 2005 Why therapeutic response may not prolong the life of a cancer patient: selection for oncogenic resistance. Cell Cycle 4, 1693-1698. (doi:10.4161/cc.4.12.2259) (Pubitemid 41827304)
76. Burgess DJ, Doles J, Zender L, Xue W, Ma B, McCombie WR, Hannon GJ, Lowe SW, Hemann MT. 2008 Topoisomerase levels determine chemotherapy response in vitro and in vivo. Proc. Natl Acad. Sci. USA 105, 9053-9058. (doi:10.1073/pnas. 0803513105)
77. Borst P, Jonkers J, Rottenberg S. 2007 What makes tumors multidrug resistant? Cell Cycle 6, 2782-2787. (doi:10.4161/cc.6.22.4936) (Pubitemid 350277170)
78. Han J, Zhong CQ, Zhang DW. 2011 Programmed necrosis: backup to and competitor with apoptosis in the immune system. Nat. Immunol. 12, 1143-1149. (doi:10.1038/ni.2159)
79. Vanlangenakker N, Vanden Berghe T, Vandenabeele P. 2012 Many stimuli pull the necrotic trigger, an overview. Cell Death Differ. 19, 75-86. (doi:10. 1038/cdd.2011.164)
80. Speirs CK, Hwang M, Kim S, Li W, Chang S, Varki V, Mitchell L, Schleicher S, Lu B. 2011 Harnessing the cell death pathway for targeted cancer treatment. Am. J. Cancer Res. 1, 43-61.
81. Chiba N, Comaills V, Shiotani B, Takahashi F, Shimada T, Tajima K et al. 2012 Homeobox B9 induces epithelial-to-mesenchymal transitionassociated radioresistance by accelerating DNA damage responses. Proc. Natl Acad. Sci. USA 109, 2760-2765. (doi:10.1073/pnas.1018867108)
82. Drasin DJ, Robin TP, Ford HL. 2011 Breast cancer epithelial-to- mesenchymal transition: examining the functional consequences of plasticity. Breast Cancer Res. 13, 226. (doi:10.1186/bcr3037)
83. Evers B, Jonkers J. 2006 Mouse models of BRCA1 and BRCA2 deficiency: past lessons, current understanding and future prospects. Oncogene 25, 5885-5897. (doi:10.1038/sj.onc.1209871) (Pubitemid 44453444)
84. Gillet JP et al. 2011 Redefining the relevance of established cancer cell lines to the study of mechanisms of clinical anti-cancer drug resistance. Proc. Natl Acad. Sci. USA 108, 18 708-18 713. (doi:10.1073/pnas.1111840108)
85. Goldie JH, Coldman AJ. 1979 A mathematic model for relating the drug sensitivity of tumors to their spontaneous mutation rate. Cancer Treat Rep. 63, 1727-1733. (Pubitemid 10138923)
86. Goldie JH, Coldman AJ. 1984 The genetic origin of drug resistance in neoplasms: implications for systemic therapy. Cancer Res. 44, 3643-3653. (Pubitemid 14041569)
87. Weinstein J. 2012 Drug discovery: cell lines battle cancer. Nature 483, 544-545. (doi:10.1038/ 483544a)
88. Michalak EM, Jonkers J. 2011 Studying therapy response and resistance in mouse models for BRCA1-deficient breast cancer. J. Mammary Gland Biol. Neoplasia 16, 41-50. (doi:10.1007/s10911-011-9199-z)
89. Rottenberg S, Borst P. 2012 Drug resistance in the mouse cancer clinic. Drug Resist. Updat. 15, 81-89.
90. Johnson L. 2012 Cancer: clinical trials unite mice and humans. Nature 483, 546-548. (doi:10.1038/ 483546a)