J Breast Cancer.  2015 Dec;18(4):303-312. 10.4048/jbc.2015.18.4.303.

New Findings on Breast Cancer Stem Cells: A Review

Affiliations
  • 1Fertility and Infertility Research Center, Kermanshah University of Medical Sciences, Kermanshah, Iran. Mkhazaei1345@yahoo.com

Abstract

Since the introduction of the "cancer stem cell" theory, significant developments have been made in the understanding of cancer and the heterogenic structure of tumors. In 2003, with the isolation of cancer stem cells from the first solid tumor, breast cancer, and recognition of the tumorigenicity of these cells, this theory suggested that the main reason for therapy failure might be the presence of cancer stem cells. This review article describes breast cancer stem cell origin, the related cellular and molecular characteristics, signaling pathways, and therapy resistance mechanisms. The databases PubMed, SCOPUS, and Embase were explored, and articles published on these topics between 1992 and 2015 were investigated. It appears that this small subpopulation of cells, with the capacity for self-renewal and a high proliferation rate, originate from normal stem cells, are identified by specific markers such as CD44+/CD24-/low, and enhance a tumor's capacity for metastasis, invasion, and therapy resistance. Cancer stem cell characteristics depend on their interactions with their microenvironment as well as on the inducing factors and elements. Although uncertainties about breast cancer stem cells exist, many of researchers believe that cancer stem cells should be considered as possible therapeutic targets.

Keyword

Biological markers; Breast neoplasms; Neoplastic stem cells

MeSH Terms

Biomarkers
Breast Neoplasms*
Breast*
Neoplasm Metastasis
Neoplastic Stem Cells
Stem Cells*

Figure

  • Figure 1 The most possible mechanisms of therapy resistance in breast cancer stem cells. MDR1=multidrug resistance protein 1; P-gp =glycoprotein P; BCRP=breast cancer resistance protein; ABC=ATP-binding cassette; ALDH1=aldehyde dehydrogenase 1; ROS=reactive oxygen species.


Cited by  1 articles

Molecular Portrait of the Normal Human Breast Tissue and Its Influence on Breast Carcinogenesis
Madalin Marius Margan, Andreea Adriana Jitariu, Anca Maria Cimpean, Cristian Nica, Marius Raica
J Breast Cancer. 2016;19(2):99-111.    doi: 10.4048/jbc.2016.19.2.99.


Reference

1. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin. 2015; 65:87–108.
Article
2. Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA Cancer J Clin. 2014; 64:9–29.
Article
3. Early Breast Cancer Trialists' Collaborative Group (EBCTCG). Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: an overview of the randomised trials. Lancet. 2005; 365:1687–1717.
4. Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH, Jones DL, et al. Cancer stem cells: perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res. 2006; 66:9339–9344.
Article
5. Hartwig FP, Nedel F, Collares T, Tarquinio SB, Nör JE, Demarco FF. Oncogenic somatic events in tissue-specific stem cells: a role in cancer recurrence? Ageing Res Rev. 2014; 13:100–106.
Article
6. Wang RA, Li ZS, Zhang HZ, Zheng PJ, Li QL, Shi JG, et al. Invasive cancers are not necessarily from preformed in situ tumours: an alternative way of carcinogenesis from misplaced stem cells. J Cell Mol Med. 2013; 17:921–926.
Article
7. Mintz B, Cronmiller C, Custer RP. Somatic cell origin of teratocarcinomas. Proc Natl Acad Sci U S A. 1978; 75:2834–2838.
Article
8. Gorden BH, Kim JH, Sarver AL, Frantz AM, Breen M, Lindblad-Toh K, et al. Identification of three molecular and functional subtypes in canine hemangiosarcoma through gene expression profiling and progenitor cell characterization. Am J Pathol. 2014; 184:985–995.
Article
9. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A. 2003; 100:3983–3988.
Article
10. Ponti D, Costa A, Zaffaroni N, Pratesi G, Petrangolini G, Coradini D, et al. Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res. 2005; 65:5506–5511.
Article
11. Wright MH, Calcagno AM, Salcido CD, Carlson MD, Ambudkar SV, Varticovski L. BRCA1 breast tumors contain distinct CD44+/CD24- and CD133+ cells with cancer stem cell characteristics. Breast Cancer Res. 2008; 10:R10.
12. Perrone G, Gaeta LM, Zagami M, Nasorri F, Coppola R, Borzomati D, et al. In situ identification of CD44+/CD24- cancer cells in primary human breast carcinomas. PLoS One. 2012; 7:e43110.
Article
13. Wang LB, He YQ, Wu LG, Chen DM, Fan H, Jia W. Isolation and characterization of human breast tumor stem cells. Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi. 2012; 28:1261–1264.
14. Herrera-Gayol A, Jothy S. Adhesion proteins in the biology of breast cancer: contribution of CD44. Exp Mol Pathol. 1999; 66:149–156.
Article
15. Rangaswami H, Bulbule A, Kundu GC. Osteopontin: role in cell signaling and cancer progression. Trends Cell Biol. 2006; 16:79–87.
Article
16. Götte M, Yip GW. Heparanase, hyaluronan, and CD44 in cancers: a breast carcinoma perspective. Cancer Res. 2006; 66:10233–10237.
Article
17. Schabath H, Runz S, Joumaa S, Altevogt P. CD24 affects CXCR4 function in pre-B lymphocytes and breast carcinoma cells. J Cell Sci. 2006; 119(Pt 2):314–325.
Article
18. Pattabiraman DR, Weinberg RA. Tackling the cancer stem cells: what challenges do they pose? Nat Rev Drug Discov. 2014; 13:497–512.
Article
19. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell. 2007; 1:555–567.
Article
20. Balicki D. Moving forward in human mammary stem cell biology and breast cancer prognostication using ALDH1. Cell Stem Cell. 2007; 1:485–487.
Article
21. Chute JP, Muramoto GG, Whitesides J, Colvin M, Safi R, Chao NJ, et al. Inhibition of aldehyde dehydrogenase and retinoid signaling induces the expansion of human hematopoietic stem cells. Proc Natl Acad Sci U S A. 2006; 103:11707–11712.
Article
22. Meyer MJ, Fleming JM, Lin AF, Hussnain SA, Ginsburg E, Vonderhaar BK. CD44posCD49fhiCD133/2hi defines xenograft-initiating cells in estrogen receptor-negative breast cancer. Cancer Res. 2010; 70:4624–4633.
Article
23. Cariati M, Naderi A, Brown JP, Smalley MJ, Pinder SE, Caldas C, et al. Alpha-6 integrin is necessary for the tumourigenicity of a stem celllike subpopulation within the MCF7 breast cancer cell line. Int J Cancer. 2008; 122:298–304.
Article
24. Vaillant F, Asselin-Labat ML, Shackleton M, Forrest NC, Lindeman GJ, Visvader JE. The mammary progenitor marker CD61/beta3 integrin identifies cancer stem cells in mouse models of mammary tumorigenesis. Cancer Res. 2008; 68:7711–7717.
Article
25. Peitzsch C, Kurth I, Kunz-Schughart L, Baumann M, Dubrovska A. Discovery of the cancer stem cell related determinants of radioresistance. Radiother Oncol. 2013; 108:378–387.
Article
26. Karamboulas C, Ailles L. Developmental signaling pathways in cancer stem cells of solid tumors. Biochim Biophys Acta. 2013; 1830:2481–2495.
Article
27. Muñoz P, Iliou MS, Esteller M. Epigenetic alterations involved in cancer stem cell reprogramming. Mol Oncol. 2012; 6:620–636.
Article
28. Ling L, Nurcombe V, Cool SM. Wnt signaling controls the fate of mesenchymal stem cells. Gene. 2009; 433:1–7.
Article
29. Liu S, Dontu G, Mantle ID, Patel S, Ahn NS, Jackson KW, et al. Hedgehog signaling and Bmi-1 regulate self-renewal of normal and malignant human mammary stem cells. Cancer Res. 2006; 66:6063–6071.
Article
30. Rizzo P, Osipo C, Foreman K, Golde T, Osborne B, Miele L. Rational targeting of Notch signaling in cancer. Oncogene. 2008; 27:5124–5131.
Article
31. Farnie G, Clarke RB. Mammary stem cells and breast cancer: role of Notch signalling. Stem Cell Rev. 2007; 3:169–175.
Article
32. Yamanaka S. Induction of pluripotent stem cells from mouse fibroblasts by four transcription factors. Cell Prolif. 2008; 41:Suppl 1. 51–56.
Article
33. Rodriguez-Pinilla SM, Sarrio D, Moreno-Bueno G, Rodriguez-Gil Y, Martinez MA, Hernandez L, et al. Sox2: a possible driver of the basal-like phenotype in sporadic breast cancer. Mod Pathol. 2007; 20:474–481.
Article
34. Leis O, Eguiara A, Lopez-Arribillaga E, Alberdi MJ, Hernandez-Garcia S, Elorriaga K, et al. Sox2 expression in breast tumours and activation in breast cancer stem cells. Oncogene. 2012; 31:1354–1365.
Article
35. Zhang J, Liang Q, Lei Y, Yao M, Li L, Gao X, et al. SOX4 induces epithelial-mesenchymal transition and contributes to breast cancer progression. Cancer Res. 2012; 72:4597–4608.
Article
36. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 2007; 131:861–872.
Article
37. Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, Regev A, et al. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet. 2008; 40:499–507.
Article
38. Stolzenburg S, Rots MG, Beltran AS, Rivenbark AG, Yuan X, Qian H, et al. Targeted silencing of the oncogenic transcription factor SOX2 in breast cancer. Nucleic Acids Res. 2012; 40:6725–6740.
Article
39. Lu X, Mazur SJ, Lin T, Appella E, Xu Y. The pluripotency factor nanog promotes breast cancer tumorigenesis and metastasis. Oncogene. 2014; 33:2655–2664.
Article
40. Luo W, Li S, Peng B, Ye Y, Deng X, Yao K. Embryonic stem cells markers SOX2, OCT4 and Nanog expression and their correlations with epithelial-mesenchymal transition in nasopharyngeal carcinoma. PLoS One. 2013; 8:e56324.
Article
41. Singh A, Settleman J. EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene. 2010; 29:4741–4751.
Article
42. Creighton CJ, Li X, Landis M, Dixon JM, Neumeister VM, Sjolund A, et al. Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features. Proc Natl Acad Sci USA. 2009; 106:13820–13825.
Article
43. Creighton CJ, Chang JC, Rosen JM. Epithelial-mesenchymal transition (EMT) in tumor-initiating cells and its clinical implications in breast cancer. J Mammary Gland Biol Neoplasia. 2010; 15:253–260.
Article
44. Li QQ, Xu JD, Wang WJ, Cao XX, Chen Q, Tang F, et al. Twist1-mediated adriamycin-induced epithelial-mesenchymal transition relates to multidrug resistance and invasive potential in breast cancer cells. Clin Cancer Res. 2009; 15:2657–2665.
Article
45. Farmer P, Bonnefoi H, Anderle P, Cameron D, Wirapati P, Becette V, et al. A stroma-related gene signature predicts resistance to neoadjuvant chemotherapy in breast cancer. Nat Med. 2009; 15:68–74.
Article
46. Thiery JP, Sleeman JP. Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol. 2006; 7:131–142.
Article
47. Hugo H, Ackland ML, Blick T, Lawrence MG, Clements JA, Williams ED, et al. Epithelial--mesenchymal and mesenchymal--epithelial transitions in carcinoma progression. J Cell Physiol. 2007; 213:374–383.
Article
48. Hollier BG, Tinnirello AA, Werden SJ, Evans KW, Taube JH, Sarkar TR, et al. FOXC2 expression links epithelial-mesenchymal transition and stem cell properties in breast cancer. Cancer Res. 2013; 73:1981–1992.
Article
49. Cheng GZ, Chan J, Wang Q, Zhang W, Sun CD, Wang LH. Twist transcriptionally up-regulates AKT2 in breast cancer cells leading to increased migration, invasion, and resistance to paclitaxel. Cancer Res. 2007; 67:1979–1987.
Article
50. Hiscox S, Jiang WG, Obermeier K, Taylor K, Morgan L, Burmi R, et al. Tamoxifen resistance in MCF7 cells promotes EMT-like behaviour and involves modulation of beta-catenin phosphorylation. Int J Cancer. 2006; 118:290–301.
Article
51. Borovski T, De Sousa E Melo F, Vermeulen L, Medema JP. Cancer stem cell niche: the place to be. Cancer Res. 2011; 71:634–639.
52. Korkaya H, Liu S, Wicha MS. Regulation of cancer stem cells by cytokine networks: attacking cancer's inflammatory roots. Clin Cancer Res. 2011; 17:6125–6129.
Article
53. Brooks MD, Wicha MS. Tumor twitter: cellular communication in the breast cancer stem cell niche. Cancer Discov. 2015; 5:469–471.
Article
54. Korkaya H, Kim GI, Davis A, Malik F, Henry NL, Ithimakin S, et al. Activation of an IL6 inflammatory loop mediates trastuzumab resistance in HER2+ breast cancer by expanding the cancer stem cell population. Mol Cell. 2012; 47:570–584.
Article
55. Bhola NE, Balko JM, Dugger TC, Kuba MG, Sánchez V, Sanders M, et al. TGF-beta inhibition enhances chemotherapy action against triplenegative breast cancer. J Clin Invest. 2013; 123:1348–1358.
Article
56. Ginestier C, Liu S, Diebel ME, Korkaya H, Luo M, Brown M, et al. CXCR1 blockade selectively targets human breast cancer stem cells in vitro and in xenografts. J Clin Invest. 2010; 120:485–497.
Article
57. Azab AK, Runnels JM, Pitsillides C, Moreau AS, Azab F, Leleu X, et al. CXCR4 inhibitor AMD3100 disrupts the interaction of multiple myeloma cells with the bone marrow microenvironment and enhances their sensitivity to therapy. Blood. 2009; 113:4341–4351.
Article
58. Zeng Z, Samudio IJ, Munsell M, An J, Huang Z, Estey E, et al. Inhibition of CXCR4 with the novel RCP168 peptide overcomes stromamediated chemoresistance in chronic and acute leukemias. Mol Cancer Ther. 2006; 5:3113–3121.
Article
59. Dubrovska A, Elliott J, Salamone RJ, Telegeev GD, Stakhovsky AE, Schepotin IB, et al. CXCR4 expression in prostate cancer progenitor cells. PLoS One. 2012; 7:e31226.
Article
60. Kuonen F, Secondini C, Rüegg C. Molecular pathways: emerging pathways mediating growth, invasion, and metastasis of tumors progressing in an irradiated microenvironment. Clin Cancer Res. 2012; 18:5196–5202.
Article
61. Chung YL, Jian JJ, Cheng SH, Tsai SY, Chuang VP, Soong T, et al. Sublethal irradiation induces vascular endothelial growth factor and promotes growth of hepatoma cells: implications for radiotherapy of hepatocellular carcinoma. Clin Cancer Res. 2006; 12:2706–2715.
Article
62. Sofia Vala I, Martins LR, Imaizumi N, Nunes RJ, Rino J, Kuonen F, et al. Low doses of ionizing radiation promote tumor growth and metastasis by enhancing angiogenesis. PLoS One. 2010; 5:e11222.
Article
63. Wardman P. Chemical radiosensitizers for use in radiotherapy. Clin Oncol (R Coll Radiol). 2007; 19:397–417.
Article
64. Batchelor TT, Gerstner ER, Emblem KE, Duda DG, Kalpathy-Cramer J, Snuderl M, et al. Improved tumor oxygenation and survival in glioblastoma patients who show increased blood perfusion after cediranib and chemoradiation. Proc Natl Acad Sci U S A. 2013; 110:19059–19064.
Article
65. Pece S, Tosoni D, Confalonieri S, Mazzarol G, Vecchi M, Ronzoni S, et al. Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell. 2010; 140:62–73.
Article
66. Cho KH, Choi MJ, Jeong KJ, Kim JJ, Hwang MH, Shin SC, et al. A ROS/STAT3/HIF-1alpha signaling cascade mediates EGF-induced TWIST1 expression and prostate cancer cell invasion. Prostate. 2014; 74:528–536.
Article
67. Cojoc M, Peitzsch C, Trautmann F, Polishchuk L, Telegeev GD, Dubrovska A. Emerging targets in cancer management: role of the CXCL12/CXCR4 axis. Onco Targets Ther. 2013; 6:1347–1361.
68. Qiang L, Wu T, Zhang HW, Lu N, Hu R, Wang YJ, et al. HIF-1alpha is critical for hypoxia-mediated maintenance of glioblastoma stem cells by activating Notch signaling pathway. Cell Death Differ. 2012; 19:284–294.
Article
69. Choi H, Chun YS, Kim TY, Park JW. HIF-2alpha enhances beta-catenin/TCF-driven transcription by interacting with beta-catenin. Cancer Res. 2010; 70:10101–10111.
Article
70. Semenza GL. Hypoxia-inducible factors: mediators of cancer progression and targets for cancer therapy. Trends Pharmacol Sci. 2012; 33:207–214.
Article
71. Generali D, Berruti A, Brizzi MP, Campo L, Bonardi S, Wigfield S, et al. Hypoxia-inducible factor-1alpha expression predicts a poor response to primary chemoendocrine therapy and disease-free survival in primary human breast cancer. Clin Cancer Res. 2006; 12:4562–4568.
Article
72. DeGorter MK, Xia CQ, Yang JJ, Kim RB. Drug transporters in drug efficacy and toxicity. Annu Rev Pharmacol Toxicol. 2012; 52:249–273.
Article
73. Gottesman MM, Fojo T, Bates SE. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer. 2002; 2:48–58.
Article
74. Vasiliou V, Vasiliou K, Nebert DW. Human ATP-binding cassette (ABC) transporter family. Hum Genomics. 2009; 3:281–290.
Article
75. Leonard GD, Fojo T, Bates SE. The role of ABC transporters in clinical practice. Oncologist. 2003; 8:411–424.
Article
76. Huang WC, Hsieh YL, Hung CM, Chien PH, Chien YF, Chen LC, et al. BCRP/ABCG2 inhibition sensitizes hepatocellular carcinoma cells to sorafenib. PLoS One. 2013; 8:e83627.
Article
77. Lecerf-Schmidt F, Peres B, Valdameri G, Gauthier C, Winter E, Payen L, et al. ABCG2: recent discovery of potent and highly selective inhibitors. Future Med Chem. 2013; 5:1037–1045.
Article
78. Stacy AE, Jansson PJ, Richardson DR. Molecular pharmacology of ABCG2 and its role in chemoresistance. Mol Pharmacol. 2013; 84:655–669.
Article
79. Ma I, Allan AL. The role of human aldehyde dehydrogenase in normal and cancer stem cells. Stem Cell Rev. 2011; 7:292–306.
Article
80. Young SZ, Bordey A. GABA's control of stem and cancer cell proliferation in adult neural and peripheral niches. Physiology (Bethesda). 2009; 24:171–185.
Article
81. Singh S, Brocker C, Koppaka V, Chen Y, Jackson BC, Matsumoto A, et al. Aldehyde dehydrogenases in cellular responses to oxidative/electrophilic stress. Free Radic Biol Med. 2013; 56:89–101.
Article
82. Croker AK, Goodale D, Chu J, Postenka C, Hedley BD, Hess DA, et al. High aldehyde dehydrogenase and expression of cancer stem cell markers selects for breast cancer cells with enhanced malignant and metastatic ability. J Cell Mol Med. 2009; 13:2236–2252.
Article
83. Magni M, Shammah S, Schiró R, Mellado W, Dalla-Favera R, Gianni AM. Induction of cyclophosphamide-resistance by aldehyde-dehydrogenase gene transfer. Blood. 1996; 87:1097–1103.
Article
84. Parajuli B, Fishel ML, Hurley TD. Selective ALDH3A1 inhibition by benzimidazole analogues increase mafosfamide sensitivity in cancer cells. J Med Chem. 2014; 57:449–461.
Article
85. Tanei T, Morimoto K, Shimazu K, Kim SJ, Tanji Y, Taguchi T, et al. Association of breast cancer stem cells identified by aldehyde dehydrogenase 1 expression with resistance to sequential paclitaxel and epirubicin-based chemotherapy for breast cancers. Clin Cancer Res. 2009; 15:4234–4241.
Article
86. Cheung-Ong K, Giaever G, Nislow C. DNA-damaging agents in cancer chemotherapy: serendipity and chemical biology. Chem Biol. 2013; 20:648–659.
Article
87. Al-Assar O, Mantoni T, Lunardi S, Kingham G, Helleday T, Brunner TB. Breast cancer stem-like cells show dominant homologous recombination due to a larger S-G2 fraction. Cancer Biol Ther. 2011; 11:1028–1035.
Article
88. Kim SY, Rhee JG, Song X, Prochownik EV, Spitz DR, Lee YJ. Breast cancer stem cell-like cells are more sensitive to ionizing radiation than non-stem cells: role of ATM. PLoS One. 2012; 7:e50423.
Article
89. Brandsma I, Gent DC. Pathway choice in DNA double strand break repair: observations of a balancing act. Genome Integr. 2012; 3:9.
Article
90. Jasin M, Rothstein R. Repair of strand breaks by homologous recombination. Cold Spring Harb Perspect Biol. 2013; 5:a012740.
Article
91. Jackson SP. Sensing and repairing DNA double-strand breaks. Carcinogenesis. 2002; 23:687–696.
Article
92. Niida H, Nakanishi M. DNA damage checkpoints in mammals. Mutagenesis. 2006; 21:3–9.
Article
93. Yin H, Glass J. The phenotypic radiation resistance of CD44+/CD24(- or low) breast cancer cells is mediated through the enhanced activation of ATM signaling. PLoS One. 2011; 6:e24080.
94. Sena LA, Chandel NS. Physiological roles of mitochondrial reactive oxygen species. Mol Cell. 2012; 48:158–167.
Article
95. Cook JA, Gius D, Wink DA, Krishna MC, Russo A, Mitchell JB. Oxidative stress, redox, and the tumor microenvironment. Semin Radiat Oncol. 2004; 14:259–266.
Article
96. Trachootham D, Alexandre J, Huang P. Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat Rev Drug Discov. 2009; 8:579–591.
Article
97. Diehn M, Cho RW, Lobo NA, Kalisky T, Dorie MJ, Kulp AN, et al. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature. 2009; 458:780–783.
Article
98. Vanharanta S, Massagué J. Origins of metastatic traits. Cancer Cell. 2013; 24:410–421.
Article
99. Del Mastro L, Clavarezza M, Venturini M. Reducing the risk of distant metastases in breast cancer patients: role of aromatase inhibitors. Cancer Treat Rev. 2007; 33:681–687.
Article
100. Brown LF, Berse B, Van de Water L, Papadopoulos-Sergiou A, Perruzzi CA, Manseau EJ, et al. Expression and distribution of osteopontin in human tissues: widespread association with luminal epithelial surfaces. Mol Biol Cell. 1992; 3:1169–1180.
Article
101. Wai PY, Kuo PC. The role of osteopontin in tumor metastasis. J Surg Res. 2004; 121:228–241.
Article
102. Chakraborty G, Jain S, Kundu GC. Osteopontin promotes vascular endothelial growth factor-dependent breast tumor growth and angiogenesis via autocrine and paracrine mechanisms. Cancer Res. 2008; 68:152–161.
Article
103. Draffin JE, McFarlane S, Hill A, Johnston PG, Waugh DJ. CD44 potentiates the adherence of metastatic prostate and breast cancer cells to bone marrow endothelial cells. Cancer Res. 2004; 64:5702–5711.
Article
104. Tuck AB, Arsenault DM, O'Malley FP, Hota C, Ling MC, Wilson SM, et al. Osteopontin induces increased invasiveness and plasminogen activator expression of human mammary epithelial cells. Oncogene. 1999; 18:4237–4246.
Article
105. Kang Y, Siegel PM, Shu W, Drobnjak M, Kakonen SM, Cordón-Cardo C, et al. A multigenic program mediating breast cancer metastasis to bone. Cancer Cell. 2003; 3:537–549.
Article
106. Oskarsson T, Acharyya S, Zhang XH, Vanharanta S, Tavazoie SF, Morris PG, et al. Breast cancer cells produce tenascin C as a metastatic niche component to colonize the lungs. Nat Med. 2011; 17:867–874.
Article
107. Zhang XH, Wang Q, Gerald W, Hudis CA, Norton L, Smid M, et al. Latent bone metastasis in breast cancer tied to Src-dependent survival signals. Cancer Cell. 2009; 16:67–78.
Article
108. Chen Q, Zhang XH, Massagué J. Macrophage binding to receptor VCAM-1 transmits survival signals in breast cancer cells that invade the lungs. Cancer Cell. 2011; 20:538–549.
Article
109. Wu K, Fukuda K, Xing F, Zhang Y, Sharma S, Liu Y, et al. Roles of the cyclooxygenase 2 matrix metalloproteinase 1 pathway in brain metastasis of breast cancer. J Biol Chem. 2015; 290:9842–9854.
Article
110. Cojoc M, Mäbert K, Muders MH, Dubrovska A. A role for cancer stem cells in therapy resistance: cellular and molecular mechanisms. Semin Cancer Biol. 2015; 31:16–27.
Article
111. Kroemer G, Mariño G, Levine B. Autophagy and the integrated stress response. Mol Cell. 2010; 40:280–293.
Article
112. Parzych KR, Klionsky DJ. An overview of autophagy: morphology, mechanism, and regulation. Antioxid Redox Signal. 2014; 20:460–473.
Article
113. McCarthy N. Autophagy: directed development. Nat Rev Cancer. 2014; 14:74–75.
114. Paglin S, Hollister T, Delohery T, Hackett N, McMahill M, Sphicas E, et al. A novel response of cancer cells to radiation involves autophagy and formation of acidic vesicles. Cancer Res. 2001; 61:439–444.
115. Yao KC, Komata T, Kondo Y, Kanzawa T, Kondo S, Germano IM. Molecular response of human glioblastoma multiforme cells to ionizing radiation: cell cycle arrest, modulation of the expression of cyclindependent kinase inhibitors, and autophagy. J Neurosurg. 2003; 98:378–384.
Article
116. Lu J, Sun D, Gao S, Gao Y, Ye J, Liu P. Cyclovirobuxine D induces autophagy-associated cell death via the Akt/mTOR pathway in MCF-7 human breast cancer cells. J Pharmacol Sci. 2014; 125:74–82.
Article
117. Karantza-Wadsworth V, Patel S, Kravchuk O, Chen G, Mathew R, Jin S, et al. Autophagy mitigates metabolic stress and genome damage in mammary tumorigenesis. Genes Dev. 2007; 21:1621–1635.
Article
118. Mathew R, Kongara S, Beaudoin B, Karp CM, Bray K, Degenhardt K, et al. Autophagy suppresses tumor progression by limiting chromosomal instability. Genes Dev. 2007; 21:1367–1381.
Article
119. Ito H, Daido S, Kanzawa T, Kondo S, Kondo Y. Radiation-induced autophagy is associated with LC3 and its inhibition sensitizes malignant glioma cells. Int J Oncol. 2005; 26:1401–1410.
Article
120. Chaterjee M, van Golen KL. Breast cancer stem cells survive periods of farnesyl-transferase inhibitor-induced dormancy by undergoing autophagy. Bone Marrow Res. 2011; 2011:362938.
Article
121. Rao R, Balusu R, Fiskus W, Mudunuru U, Venkannagari S, Chauhan L, et al. Combination of pan-histone deacetylase inhibitor and autophagy inhibitor exerts superior efficacy against triple-negative human breast cancer cells. Mol Cancer Ther. 2012; 11:973–983.
Article
122. Gong C, Bauvy C, Tonelli G, Yue W, Deloménie C, Nicolas V, et al. Beclin 1 and autophagy are required for the tumorigenicity of breast cancer stem-like/progenitor cells. Oncogene. 2013; 32:2261–2272.
Article
123. Palacios F, Tushir JS, Fujita Y, D'Souza-Schorey C. Lysosomal targeting of E-cadherin: a unique mechanism for the down-regulation of cell-cell adhesion during epithelial to mesenchymal transitions. Mol Cell Biol. 2005; 25:389–402.
Article
124. Sharif J, Muto M, Takebayashi S, Suetake I, Iwamatsu A, Endo TA, et al. The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature. 2007; 450:908–912.
Article
125. van Vlerken LE, Hurt EM, Hollingsworth RE. The role of epigenetic regulation in stem cell and cancer biology. J Mol Med (Berl). 2012; 90:791–801.
Article
126. Jin B, Ernst J, Tiedemann RL, Xu H, Sureshchandra S, Kellis M, et al. Linking DNA methyltransferases to epigenetic marks and nucleosome structure genome-wide in human tumor cells. Cell Rep. 2012; 2:1411–1424.
Article
127. El Helou R, Wicinski J, Guille A, Adélaïde J, Finetti P, Bertucci F, et al. Brief reports: a distinct DNA methylation signature defines breast cancer stem cells and predicts cancer outcome. Stem Cells. 2014; 32:3031–3036.
Article
128. Shukla S, Meeran SM. Epigenetics of cancer stem cells: pathways and therapeutics. Biochim Biophys Acta. 2014; 1840:3494–3502.
Article
129. Han M, Liu M, Wang Y, Chen X, Xu J, Sun Y, et al. Antagonism of miR-21 reverses epithelial-mesenchymal transition and cancer stem cell phenotype through AKT/ERK1/2 inactivation by targeting PTEN. PLoS One. 2012; 7:e39520.
Article
130. Shimono Y, Zabala M, Cho RW, Lobo N, Dalerba P, Qian D, et al. Downregulation of miRNA-200c links breast cancer stem cells with normal stem cells. Cell. 2009; 138:592–603.
Article
131. Gwak JM, Kim HJ, Kim EJ, Chung YR, Yun S, Seo AN, et al. MicroRNA-9 is associated with epithelial-mesenchymal transition, breast cancer stem cell phenotype, and tumor progression in breast cancer. Breast Cancer Res Treat. 2014; 147:39–49.
Article
132. Taube JH, Malouf GG, Lu E, Sphyris N, Vijay V, Ramachandran PP, et al. Epigenetic silencing of microRNA-203 is required for EMT and cancer stem cell properties. Sci Rep. 2013; 3:2687.
Article
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