Breast cancer stem cells: Responsible for therapeutic resistance and relapse?

Breast Cancer Metastasis and Drug Resistance: Progress and Prospects

Volumn , Issue , 2013, Pages 385-398

  Korkaya, Hasan ^a   Malik, Fayaz ^a  

^a UNIVERSITY OF MICHIGAN COMPREHENSIVE CANCER CENTER   (United States)

Author keywords

Aldehyde dehydrogenase (ALDH); Biomarkers; Breast cancer stem cell self renewal; Cancer stem cell (CSC) targeted therapies; Cancer stem cells (CSCs); Cyclopamine; Cytokines; Metastasis; Relapse; Therapeutic resistance; Trastuzumab resistance; Xenografts

Indexed keywords

EID: 84949180230     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-4614-5647-6_21     Document Type: Chapter

References (83)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ (2009) Cancer statistics 2009. CA Cancer J Clin 59: 225-249
2. Siegel R, Naishadham D, Jemal A (2012) Cancer statistics 2012. CA Cancer J Clin 62: 10-29
3. O'Brien CA, Kreso A, Jamieson CH (2010) Cancer stem cells and self-renewal. Clin Cancer Res 16: 3113-3120
4. Shipitsin M, Polyak K (2008) The cancer stem cell hypothesis: in search of definitions markers and relevance Laboratory investigation. J Tech Meth Pathol 88: 459-463
5. Kordon EC, Smith GH (1998) An entire functional mammary gland may comprise the progeny from a single cell. Development 125: 1921-1930
6. Shackleton M, Vaillant F, Simpson KJ, Sting LJ, 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
7. Wang X, Willenbring H, Akkari Y, Torimaru Y, Foster M, Al-Dhalimy M, Lagasse E, Finegold M, Olson S, Grompe M (2003) Cell fusion is the principal source of bone-marrowderived hepatocytes. Nature 422: 897-901
8. Wagers AJ, Sherwood RI, Christensen JL, Weissman IL (2002) Little evidence for developmental plasticity of adult hematopoietic stem cells. Science 297: 2256-2259
9. Krause DS, Theise ND, Collector MI, Henegariu O, Hwang S, Gardner R, Neutzel S, Sharkis SJ (2001) Multi-organ multi-lineage engraftment by a single bone marrow-derived stem cell. Cell 105: 369-377
10. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 100: 3983-3988
11. Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ, Wicha MS (2003) In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev 17: 1253-1270
12. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, Dirks PB (2003) Identification of a cancer stem cell in human brain tumors. Cancer Res 63: 5821-5828
13. Korkaya H, Paulson A, Charafe-Jauffret E, Ginestier C, Brown M, Dutcher J, Clouthier SG, Wicha MS (2009) Regulation of mammary stem/progenitor cells by PTEN/Akt/beta-catenin signaling. PLoS Biol 7: e1000121
14. Gupta PB, Onder TT, Jiang G, Tao K, Kuperwasser C, Weinberg RA, Lander ES (2009) Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 138: 645-659
15. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, Campbell LL, Polyak K, Brisken C, Yang J, Weinberg RA (2008) The epithelialmesenchymal transition generates cells with properties of stem cells. Cell 133: 704-715
16. Goodell MA, Brose K, Paradis G, Conner AS, Mulligan RC (1996) Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med 183: 1797-1806
17. Zhou J, Wulfkuhle J, Zhang H, Gu P, Yang Y, Deng J, Margolick JB, Liotta LA, Petricoin E 3rd, Zhang Y (2007) Activation of the PTEN/mTOR/STAT3 pathway in breast cancer stem-like cells is required for viability and maintenance. Proc Natl Acad Sci USA 104: 16158-16163
18. Kondo T, Setoguchi T, Taga T (2004) Persistence of a small subpopulation of cancer stemlike cells in the C6 glioma cell line. Proc Natl Acad Sci USA 101: 781-786
19. Hirschmann-Jax C, Foster AE, Wulf GG, Nuchtern JG, Jax TW, Gobel U, Goodell MA, Brenner MK (2004) A distinct ''side population'' of cells with high drug efflux capacity in human tumor cells. Proc Natl Acad Sci USA 101: 14228-14233
20. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, Jacquemier J, Viens P, Kleer CG, Liu S, Schott A, Hayes D, Birnbaum D, Wicha MS, Dontu G (2007) ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 1: 555-567
21. Charafe-Jauffret E, Ginestier C, Iovino F, Wicinski J, Cervera N, Finetti P, Hur MH, Diebel ME, Monville F, Dutcher J, Brown M, Viens P, Xerri L, Bertucci F, Stassi G, Dontu G, Birnbaum D, Wicha MS (2009) Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature. Cancer Res 69: 1302-1313
22. Ginestier C, Hur M, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, Jacquemier J, Viens P, Kleer CG, Schott A, Hayes DF, Birnbaum D, Wicha MS, Dontu G (2007) ALDH1 is a marker of normal and malignant breast stem cells and a predictor of poor clinical outcome. Cell Stem Cell 1: 555-567
23. Giatromanolaki A, Sivridis E, Fiska A, Koukourakis MI (2011) The CD44 +/CD24-phenotype relates to 'triple-negative' state and unfavorable prognosis in breast cancer patients. Med Oncol 28: 745-752
24. Pece S, Tosoni D, Confalonieri S, Mazzarol G, Vecchi M, Ronzoni S, Bernard L, Viale G, Pelicci PG, Di Fiore PP (2010) Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell 140: 62-73
25. Keller PJ, Lin AF, Arendt LM, Klebba I, Jones AD, Rudnick JA, Dimeo TA, Gilmore H, Jefferson DM, Graham RA, Naber SP, Schnitt S, Kuperwasser C (2010) Mapping the cellular and molecular heterogeneity of normal and malignant breast tissues and cultured cell lines. Breast Cancer Res 12: R87
26. Li X, Lewis MT, Huang J, Gutierrez C, Osborne CK, Wu MF, Hilsenbeck SG, Pavlick A, Zhang X, Chamness GC, Wong H, Rosen J, Chang JC (2008) Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J Natl Cancer Inst 100: 672-679
27. Phillips TM, McBride WH, Pajonk F (2006) The response of CD24(-/low)/CD44 ? breast cancer-initiating cells to radiation. J Natl Cancer Inst 98: 1777-1785
28. Diehn M, Cho RW, Lobo NA, Kalisky T, Dorie MJ, Kulp AN, Qian D, Lam JS, Ailles LE, Wong M, Joshua B, Kaplan MJ, Wapnir I, Dirbas FM, Somlo G, Garberoglio C, Paz B, Shen J, Lau SK, Quake SR, Brown JM, Weissman IL, Clarke MF(2009) Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 458: 780-783
29. Rich JN (2007) Cancer stem cells in radiation resistance. Cancer Res 67: 8980-8984
30. Dean M (2009) ABC transporters drug resistance and cancer stem cells. J Mammary Gland Biol Neoplasia 14: 3-9
31. Keshet GI, Goldstein I, Itzhaki O, Cesarkas K, Shenhav L, Yakirevitch A, Treves AJ, Schachter J, Amariglio N, Rechavi G (2008) MDR1 expression identifies human melanoma stem cells. Biochem Biophys Res Commun 368: 930-936
32. Lee JH, Jung C, Javadian-Elyaderani P, Schweyer S, Schutte D, Shoukier M, Karimi-Busheri F, Weinfeld M, Rasouli-Nia A, Hengstler JG, Mantilla A, Soleimanpour-Lichaei HR, Engel W, Robson CN, Nayernia K (2010) Pathways of proliferation and antiapoptosis driven in breast cancer stem cells by stem cell protein piwil2. Cancer Res 70: 4569-4579
33. Yule SM, Boddy AV, Cole M, Price L, Wyllie R, Tasso MJ, Pearson AD, Idle JR (1995) Cyclophosphamide metabolism in children. Cancer Res 55: 803-809
34. Lan KH, Lu CH, Yu D (2005) Mechanisms of trastuzumab resistance and their clinical implications. Ann NY Acad Sci 1059: 70-75
35. Miller KD (2004) The role of ErbB inhibitors in trastuzumab resistance. Oncologist 9(3): 16-19
36. SlamonDJ, Leyland-Jones B, Shak S, FuchsH, PatonV, BajamondeA, Fleming T, Eiermann W, Wolter J, PegramM, Baselga J, NortonL(2001)Use of chemotherapy plus amonoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. N Engl JMed 344: 783-792
37. Nahta R, Esteva FJ (2006) HER2 therapy: molecular mechanisms of trastuzumab resistance. Breast Cancer Res 8: 215
38. Nagata Y, Lan KH, Zhou X, Tan M, Esteva FJ, Sahin AA, Klos KS, Li P, Monia BP, Nguyen NT, Hortobagyi GN, Hung MC, Yu D (2004) PTEN activation contributes to tumor inhibition by trastuzumab and loss of PTEN predicts trastuzumab resistance in patients. Cancer Cell 6: 117-127
39. Berns K, Horlings HM, Hennessy BT, Madiredjo M, Hijmans EM, Beelen K, Linn SC, Gonzalez-Angulo AM, Stemke-Hale K, Hauptmann M, Beijersbergen RL, Mills GB, van de Vijver MJ, Bernards R (2007) A functional genetic approach identifies the PI3 K pathway as a major determinant of trastuzumab resistance in breast cancer. Cancer Cell 12: 395-402
40. Cicalese A, Bonizzi G, Pasi CE, Faretta M, Ronzoni S, Giulini B, Brisken C, Minucci S, Di Fiore PP, Pelicci PG (2009) The tumor suppressor p53 regulates polarity of self-renewing divisions in mammary stem cells. Cell 138: 1083-1095
41. Korkaya H, Kim G, Davis A, Malik F, Henry NL, Ithimakin S, Quraishi AA, Tawakkol N, D'Angelo R, Paulson A, Chung S, Luther T, Paholak HS, Liu S, Hassan K, Zen Q, Clouthier SG, Wicha MS (2012) Activation of an IL-6 inflammatory loop mediates trastuzumab resistance in HER2 overexpressing breast cancers by expanding the cancer stem cell population. Molecular Cell (In print)
42. Iliopoulos D, Hirsch HA, Wang G, Struhl K (2011) Inducible formation of breast cancer stem cells and their dynamic equilibrium with non-stem cancer cells via IL6 secretion. Proc Natl Acad Sci USA 108: 1397-1402
43. Ginestier C, Liu S, Diebel ME, Korkaya H, Luo M, Brown M, Wicinski J, Cabaud O, Charafe-Jauffret E, Birnbaum D, Guan JL, Dontu G, Wicha MS (2010) CXCR1 blockade selectively targets human breast cancer stem cells in vitro and in xenografts. J Clin Invest 120: 485-497
44. Hartman ZC, Yang XY, Glass O, Lei G, Osada T, Dave SS, Morse MA, Clay TM, Lyerly HK (2011) HER2 overexpression elicits a proinflammatory IL-6 autocrine signaling loop that is critical for tumorigenesis. Cancer Res 71: 4380-4391
45. Sullivan NJ, Sasser AK, Axel AE, Vesuna F, Raman V, Ramirez N, Oberyszyn TM, Hall BM (2009) Interleukin-6 induces an epithelial-mesenchymal transition phenotype in human breast cancer cells. Oncogene 28: 2940-2947
46. Salgado R, Junius S, Benoy I, Van Dam P, Vermeulen P, Van Marck E, Huget P, Dirix LY (2003) Circulating interleukin-6 predicts survival in patients with metastatic breast cancer. Int J Cancer 103: 642-646
47. Bachelot T, Ray-Coquard I, Menetrier-Caux C, Rastkha M, Duc A, Blay JY (2003) Prognostic value of serum levels of interleukin 6 and of serum and plasma levels of vascular endothelial growth factor in hormone-refractory metastatic breast cancer patients. Br J Cancer 88: 1721-1726
48. Korkaya H, Liu S, Wicha MS (2011) Regulation of cancer stem cells by cytokine networks: attacking cancer's inflammatory roots. Clin Cancer Res 17: 6125-6129
49. Korkaya H, Liu S, Wicha MS (2011) Breast cancer stem cells cytokine networks and the tumor microenvironment. J Clin Invest 121: 3804-3809
50. Radtke F, Clevers H (2005) Self-renewal and cancer of the gut: two sides of a coin. Science 307: 1904-1909
51. Vermeulen L, De Sousa EMF, van der Heijden M, Cameron K, de Jong JH, Borovski T, Tuynman JB, Todaro M, Merz C, Rodermond H, Sprick MR, Kemper K, Richel DJ, Stassi G, Medema JP (2010) Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat Cell Biol 12: 468-476
52. Korkaya H, Wicha MS (2010) Cancer stem cells: nature versus nurture. Nat Cell Biol 12: 419-421
53. Sigurdsson V, Hilmarsdottir B, Sigmundsdottir H, Fridriksdottir AJ, Ringner M, Villadsen R, Borg A, Agnarsson BA, Petersen OW, Magnusson MK, Gudjonsson T (2011) Endothelial induced EMT in breast epithelial cells with stem cell properties. PLoS ONE 6: e23833
54. Pierce BL, Ballard-Barbash R, Bernstein L, Baumgartner RN, Neuhouser ML, Wener MH, Baumgartner KB, Gilliland FD, Sorensen BE, McTiernan A, Ulrich CM (2009) Elevated biomarkers of inflammation are associated with reduced survival among breast cancer patients. J Clin Oncol 27: 3437-3444
55. Mantovani A, Romero P, Palucka AK, Marincola FM (2008) Tumour immunity: effector response to tumour and role of the microenvironment. Lancet 371: 771-783
56. Mantovani A, Pierotti MA (2008) Cancer and inflammation: a complex relationship. Cancer Lett 267: 180-181
57. Mantovani A, Allavena P, Sica A, Balkwill F (2008) Cancer-related inflammation. Nature 454: 436-444
58. Balkwill F, Mantovani A (2001) Inflammation and cancer: back to Virchow? Lancet 357: 539-545
59. Michaud DS, Daugherty SE, Berndt SI, Platz EA, Yeager M, Crawford ED, Hsing A, Huang WY, Hayes RB (2006) Genetic polymorphisms of interleukin-1B (IL-1B) IL-6 IL-8 and IL-10 and risk of prostate cancer. Cancer Res 66: 4525-4530
60. Zou W (2005) Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat Rev Cancer 5: 263-274
61. Pardoll D (2003) Does the immune system see tumors as foreign or self? Annu Rev Immunol 21: 807-839
62. Dunn GP, Bruce AT, Ikeda H, Old LJ, Schreiber RD (2002) Cancer immunoediting: from immunosurveillance to tumor escape. Nat Immunol 3: 991-998
63. Iliopoulos D, Hirsch HA, Struhl K (2009) An epigenetic switch involving NF-kappaB Lin28 Let-7 MicroRNA and IL6 links inflammation to cell transformation. Cell 139: 693-706
64. Iliopoulos D, Jaeger SA, Hirsch HA, Bulyk ML, Struhl (2010) K STAT3 activation of miR-21 and miR-181b-1 via PTEN and CYLD are part of the epigenetic switch linking inflammation to cancer. Mol Cell 39: 493-506
65. Sansone P, Storci G, Tavolari S, Guarnieri T, Giovannini C, Taffurelli M, Ceccarelli C, Santini D, Paterini P, Marcu KB, Chieco P, Bonafe M (2007) IL-6 triggers malignant features in mammospheres from human ductal breast carcinoma and normal mammary gland. J Clin Invest 117: 3988-4002
66. Liu H, Patel MR, Prescher JA, Patsialou A, Qian D, Lin J, Wen S, Chang YF, Bachmann MH, Shimono Y, Dalerba P, Adorno M, Lobo N, Bueno J, Dirbas FM, Goswami S, Somlo G, Condeelis J, Contag CH, Gambhir SS, Clarke MF (2010) Cancer stem cells from human breast tumors are involved in spontaneous metastases in orthotopic mouse models. Proc Natl Acad Sci USA 107: 18115-18120
67. Magnifico A, Albano L, Campaner S, Delia D, Castiglioni F, Gasparini P, Sozzi G, Fontanella E, Menard S, Tagliabue E (2009) Tumor-initiating cells of HER2-positive carcinoma cell lines express the highest oncoprotein levels and are sensitive to trastuzumab. Clin Cancer Res 15: 2010-2021
68. Korkaya H, Wicha MS (2009) HER-2 notch and breast cancer stem cells: targeting an axis of evil. Clin Cancer Res 15: 1845-1847
69. Pece S, Serresi M, Santolini E, Capra M, Hulleman E, Galimberti V, Zurrida S, Maisonneuve P, Viale G, Di Fiore PP (2004) Loss of negative regulation by Numb over Notch is relevant to human breast carcinogenesis. J Cell Biol 167: 215-221
70. Chen JK, Taipale J, Cooper MK, Beachy PA (2002) Inhibition of Hedgehog signaling by direct binding of cyclopamine to smoothened genes. Dev 16: 2743-2748
71. Clement V, Sanchez P, de Tribolet N, Radovanovic I, Altaba A Ruiz i (2007) HEDGEHOGGLI1 signaling regulates human glioma growth cancer stem cell self-renewal and tumorigenicity. Curr Biol 17: 165-172
72. Karhadkar SS, Bova GS, Abdallah N, Dhara S, Gardner D, Maitra A, Isaacs JT, Berman DM, Beachy PA (2004) Hedgehog signalling in prostate regeneration neoplasia and metastasis. Nature 431: 707-712
73. Thayer SP, di Magliano MP, Heiser PW, Nielsen CM, Roberts DJ, Lauwers GY, Qi YP, Gysin S, Fernandez-del Castillo C, Yajnik V, Antoniu B, McMahon M, Warshaw AL, Hebrok M (2003) Hedgehog is an early and late mediator of pancreatic cancer tumorigenesis. Nature 425: 851-856
74. Berman DM, Karhadkar SS, Maitra A, Montes De Oca R, Gerstenblith MR, Briggs K, Parker AR, Shimada Y, Eshleman JR, Watkins DN, Beachy PA (2003) Widespread requirement for Hedgehog ligand stimulation in growth of digestive tract tumours. Nature 425: 846-851
75. Rudin CM, Hann CL, Laterra J, Yauch RL, Callahan CA, Fu L, Holcomb T, Stinson J, Gould SE, Coleman B, LoRusso PM, Von Hoff DD, de Sauvage FJ, Low JA (2009) Treatment of medulloblastoma with hedgehog pathway inhibitor GDC-0449. N Engl J Med 361: 1173-1178
76. Kelly OG, Pinson KI, Skarnes WC (2004) The Wnt co-receptors Lrp5 and Lrp6 are essential for gastrulation in mice. Development 131: 2803-2815
77. Huelsken J, Vogel R, Brinkmann V, Erdmann B, Birchmeier C, Birchmeier W (2000) Requirement for beta-catenin in anterior-posterior axis formation in mice. J Cell Biol 148: 567-578
78. Li Y, Welm B, Podsypanina K, Huang S, Chamorro M, Zhang X, Rowlands T, Egeblad M, Cowin P, Werb Z, Tan LK, Rosen JM, Varmus HE (2003) Evidence that transgenes encoding components of the Wnt signaling pathway preferentially induce mammary cancers from progenitor cells. Proc Natl Acad Sci USA 100: 15853-15858
79. Lepourcelet M, Chen YN, France DS, Wang H, Crews P, Petersen F, Bruseo C, Wood AW, Shivdasani RA (2004) Small-molecule antagonists of the oncogenic Tcf/beta-catenin protein complex. Cancer Cell 5: 91-102
80. Liu M, Sakamaki T, Casimiro MC, Willmarth NE, Quong AA, Ju X, Ojeifo J, Jiao X, Yeow WS, Katiyar S, Shirley LA, Joyce D, Lisanti MP, Albanese C, Pestell RG (2010) The canonical NF-kappaB pathway governs mammary tumorigenesis in transgenic mice and tumor stem cell expansion. Cancer Res 70: 10464-10473
81. Joshi PA, Jackson HW, Beristain AG, Di Grappa MA, Mote PA, Clarke CL, Sting LJ, Waterhouse PD, Khokha R (2010) Progesterone induces adult mammary stem cell expansion. Nature 465: 803-807
82. Asselin-Labat ML, Vaillant F, Sheridan JM, Pal B, Wu D, Simpson ER, Yasuda H, Smyth GK, Martin TJ, Lindeman GJ, Visvader JE (2010) Control of mammary stem cell function by steroid hormone signalling. Nature 465: 798-802
83. Hassane DC, Sen S, Minhajuddin M, Rossi RM, Corbett CA, Balys M, Wei L, Crooks PA, Guzman ML, Jordan CT (2010) Chemical genomic screening reveals synergism between parthenolide and inhibitors of the PI-3 kinase and mTOR pathways. Blood 116: 5983-5990