Heterogeneity of functional properties of clone 66 murine breast cancer cells expressing various stem cell phenotypes

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Mukhopadhyay, Partha ^a   Farrell, Tracy ^a   Sharma, Gayatri ^a   McGuire, Timothy R ^a   O'Kane, Barbara ^b   Sharp, J Graham ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b CREIGHTON UNIVERSITY SCHOOL OF DENTISTRY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE; CD24 ANTIGEN; CHEMOKINE; CYTOKINE; HERMES ANTIGEN; PROTEIN ALDH1; RANTES; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; BREAST CANCER; CANCER STEM CELL; CARCINOGENESIS; CELL ASSAY; CELL CLONE; CELL CULTURE; CELL EXPANSION; CELL FUNCTION; CELL GROWTH; CELL HETEROGENEITY; CELL ISOLATION; CELL POPULATION; CELL PROLIFERATION; CELL SELECTION; COLONY FORMATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PHENOTYPE;

ANIMALS; CARCINOGENESIS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSPLANTATION; CHEMOKINES; CLONE CELLS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; NEOPLASTIC STEM CELLS; PHENOTYPE; STROMAL CELLS; TUMOR MARKERS, BIOLOGICAL;

EID: 84893181707     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0078725     Document Type: Article

References (83)

1. Sharp JG., Jackson JD. (2008) Hematopoietic stem cells and cytokines. In: Current Medicine Philadelphia 2nd Ed., JO Armitage Ed, editors. Atlas of Clinical Hematology. 201-222.
2. Pierce GB (1974) The benign cells of malignant tumors. Developmental Aspects of Carcinogenesis and Immunity 3-22.
3. Thorup J, McLachlan R, Cortes D, Nation TR, Balic A, et al. (2010) What is new in cryptorchidism and hypospadias-a critical review on the testicular dysgenesis hypothesis. J Pediatr Surg 45: 2074-2086.
4. Dick JE (2008) Stem cell concepts renew cancer research. Blood 112: 4793-4807.
5. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 100: 3983-3988. (Pubitemid 36418143)
6. Britton KM, Eyre R, Harvey IJ, Stemke-Hale K, Browell D, et al. (2012) Breast cancer, side population cells and ABCG2 expression. Cancer Lett 323: 97-105.
7. Nakshatri H, Srour EF, Badve S (2009) Breast cancer stem cells and intrinsic subtypes: controversies rage on. Curr Stem Cell Res Ther 4: 50-60.
8. Ricardo S, Vieira AF, Gerhard R, Leitao D, Pinto R, et al. (2011) Breast cancer stem cell markers CD44, CD24 and ALDH1: expression distribution within intrinsic molecular subtype. J Clin Pathol 64: 937-946.
9. Wright MH, Calcagno AM, Salcido CD, Carlson MD, Ambudkar SV, et al. (2008) Brca1 breast tumors contain distinct CD44+/. Breast Cancer Res 10: R10.
10. Chiba T, Kita K, Zheng YW, Yokosuka O, Saisho H, et al. (2006) Side population purified from hepatocellular carcinoma cells harbors cancer stem cell-like properties. Hepatology 44: 240-251. (Pubitemid 44049156)
11. Lindeman GJ, Visvader JE (2010) Insights into the cell of origin in breast cancer and breast cancer stem cells. Asia Pac J Clin Oncol 6: 89-97.
12. Nguyen LV, Vanner R, Dirks P, Eaves CJ (2012) Cancer stem cells: an evolving concept. Nat Rev Cancer 12: 133-143.
13. Visvader JE, Lindeman GJ (2008) Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 8: 755-768.
14. Wu C, Alman BA (2008) Side population cells in human cancers. Cancer Lett 268: 1-9.
15. Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH, et al. (2006) Cancer stem cells-perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res 66: 9339-9344.
16. Kelly PN, Dakic A, Adams JM, Nutt SL, Strasser A (2007) Tumor growth need not be driven by rare cancer stem cells. Science 317: 337. (Pubitemid 47106366)
17. Kola I, Landis J (2004) Can the pharmaceutical industry reduce attrition rates? Nat Rev Drug Discov 3: 711-715. (Pubitemid 39173511)
18. Qin W, Stock JL, Sacca R (2012) Humanized Mouse Models in Drug Discovery Research. New American Pharmaceutical Review website.
19. Willyard C (2013) Stem cells: bad seeds. Nature 498: S12-S13.
20. Robinson SN, Seina SM, Gohr JC, Kuszynski CA, Sharp JG (2005) Evidence for a qualitative hierarchy within the Hoechst-33342 'side population' (SP) of murine bone marrow cells. Bone Marrow Transplant 35: 807-818. (Pubitemid 40613789)
21. Badve S, Nakshatri H (2012) Breast-cancer stem cells-beyond semantics. Lancet Oncol 13: e43-e48.
22. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, et al. (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. (Pubitemid 350056407)
23. Smalley MJ, Clarke RB (2005) The mammary gland "side population": a putative stem/progenitor cell marker? J Mammary Gland Biol Neoplasia 10: 37-47. (Pubitemid 40724021)
24. Dexter DL, Kowalski HM, Blazar BA, Fligiel Z, Vogel R, et al. (1978) Heterogeneity of tumor cells from a single mouse mammary tumor. Cancer Res 38: 3174-3181. (Pubitemid 9031291)
25. Murphy BO, Joshi S, Kessinger A, Reed E, Sharp JG (2002) A murine model of bone marrow micrometastasis in breast cancer. Clin Exp Metastasis 19: 561-569. (Pubitemid 36001998)
26. Cariati M, Naderi A, Brown JP, Smalley MJ, Pinder SE, et al. (2008) Alpha-6 integrin is necessary for the tumourigenicity of a stem cell-like subpopulation within the MCF7 breast cancer cell line. Int J Cancer 122: 298-304. (Pubitemid 350234715)
27. Masuda A, Kondo M, Saito T, Yatabe Y, Kobayashi T, et al. (1997) Establishment of human peripheral lung epithelial cell lines (HPL1) retaining differentiated characteristics and responsiveness to epidermal growth factor, hepatocyte growth factor, and transforming growth factor beta1. Cancer Res 57: 4898-4904. (Pubitemid 27469000)
28. Mukhopadhyay P, Lakshmanan I, Ponnusamy MP, Chakraborty S, Jain M, et al. (2013) MUC4 overexpression augments cell migration and metastasis through EGFR family proteins in triple negative breast cancer cells. PLoS One 8: e54455.
29. Dixit M, Yang JL, Poirier MC, Price JO, Andrews PA, et al. (1997) Abrogation of cisplatin-induced programmed cell death in human breast cancer cells by epidermal growth factor antisense RNA. J Natl Cancer Inst 89: 365-373. (Pubitemid 27102601)
30. Avwioro G (2011) Histochemical uses of haematoxylinGÇöa review. J Pharm Clin Sci (JPCS) 1: 24-34.
31. Moraes RC, Zhang X, Harrington N, Fung JY, Wu MF, et al. (2007) Constitutive activation of smoothened (SMO) in mammary glands of transgenic mice leads to increased proliferation, altered differentiation and ductal dysplasia. Development 134: 1231-1242. (Pubitemid 46630090)
32. Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, et al. (2003) In vitro propagation and transcriptional profiling of human mammary stem/ progenitor cells. Genes Dev 17: 1253-1270. (Pubitemid 36583168)
33. Dontu G, Wicha MS (2005) Survival of mammary stem cells in suspension culture: implications for stem cell biology and neoplasia. J Mammary Gland Biol Neoplasia 10: 75-86. (Pubitemid 40724024)
34. Grimshaw MJ, Cooper L, Papazisis K, Coleman JA, Bohnenkamp HR, et al. (2008) Mammosphere culture of metastatic breast cancer cells enriches for tumorigenic breast cancer cells. Breast Cancer Res 10: R52.
35. Kakarala M, Wicha MS (2008) Implications of the cancer stem-cell hypothesis for breast cancer prevention and therapy. J Clin Oncol 26: 2813-2820.
36. Liu S, Dontu G, Mantle ID, Patel S, Ahn NS, et al. (2006) Hedgehog signaling and Bmi-1 regulate self-renewal of normal and malignant human mammary stem cells. Cancer Res 66: 6063-6071.
37. Ponti D, Costa A, Zaffaroni N, Pratesi G, Petrangolini G, et al. (2005) Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res 65: 5506-5511. (Pubitemid 40911148)
38. Pichiorri F, Suh SS, Ladetto M, Kuehl M, Palumbo T, et al. (2008) MicroRNAs regulate critical genes associated with multiple myeloma pathogenesis. Proc Natl Acad Sci U S A 105: 12885-12890.
39. Sun CY, She XM, Qin Y, Chu ZB, Chen L, et al. (2013) miR-15a and miR-16 affect the angiogenesis of multiple myeloma by targeting VEGF. Carcinogenesis 34: 426-435.
40. Liu S, Ginestier C, Ou SJ, Clouthier SG, Patel SH, et al. (2011) Breast cancer stem cells are regulated by mesenchymal stem cells through cytokine networks. Cancer Res 71: 614-624.
41. Benoy IH, Salgado R, Elst H, Van DP, Weyler J, et al. (2005) Relative microvessel area of the primary tumour, and not lymph node status, predicts the presence of bone marrow micrometastases detected by reverse transcriptase polymerase chain reaction in patients with clinically non-metastatic breast cancer. Breast Cancer Res 7: R210-R219.
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 U S A 108: 1397-1402.
43. Wang Y, Liu Y, Malek SN, Zheng P, Liu Y (2011) Targeting HIF1alpha eliminates cancer stem cells in hematological malignancies. Cell Stem Cell 8: 399-411.
44. Berezov TT, Ovchinnikova LK, Kuznetsova OM, Karabekova ZK, Vorotnikov IK, et al. (2009) Vascular endothelial growth factor in the serum of breast cancer patients. Bull Exp Biol Med 148: 419-424.
45. Gelmini S, Mangoni M, Serio M, Romagnani P, Lazzeri E (2008) The critical role of SDF-1/CXCR4 axis in cancer and cancer stem cells metastasis. J Endocrinol Invest 31: 809-819.
46. Kryczek I, Lange A, Mottram P, Alvarez X, Cheng P, et al. (2005) CXCL12 and vascular endothelial growth factor synergistically induce neoangiogenesis in human ovarian cancers. Cancer Res 65: 465-472.
47. Waugh DJ, Wilson C (2008) The interleukin-8 pathway in cancer. Clin Cancer Res 14: 6735-6741.
48. Doyle LA, Yang W, Abruzzo LV, Krogmann T, Gao Y, et al. (1998) A multidrug resistance transporter from human MCF-7 breast cancer cells. Proc Natl Acad Sci U S A 95: 15665-15670. (Pubitemid 29018757)
49. Houghton PJ, Germain GS, Harwood FC, Schuetz JD, Stewart CF, et al. (2004) Imatinib mesylate is a potent inhibitor of the ABCG2 (BCRP) transporter and reverses resistance to topotecan and SN-38 in vitro. Cancer Res 64: 2333-2337. (Pubitemid 38523883)
50. Hirschmann-Jax C, Foster AE, Wulf GG, Nuchtern JG, Jax TW, et al. (2004) A distinct "side population" of cells with high drug efflux capacity in human tumor cells. Proc Natl Acad Sci U S A 101: 14228-14233. (Pubitemid 39305058)
51. Liu R, Wang X, Chen GY, Dalerba P, Gurney A, et al. (2007) The prognostic role of a gene signature from tumorigenic breast-cancer cells. N Engl J Med 356: 217-226. (Pubitemid 46143225)
52. Sheridan C, Kishimoto H, Fuchs RK, Mehrotra S, Bhat-Nakshatri P, et al. (2006) CD44+/CD242 breast cancer cells exhibit enhanced invasive properties: an early step necessary for metastasis. Breast Cancer Res 8: R59.
53. Shipitsin M, Campbell LL, Argani P, Weremowicz S, Bloushtain-Qimron N, et al. (2007) Molecular definition of breast tumor heterogeneity. Cancer Cell 11: 259-273. (Pubitemid 46349843)
54. Bonnet D, Dick JE (1997) Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 3: 730-737. (Pubitemid 27298715)
55. O'Brien CA, Pollett A, Gallinger S, Dick JE (2007) A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445: 106-110. (Pubitemid 46067310)
56. Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, et al. (2007) Identification and expansion of human colon-cancer-initiating cells. Nature 445: 111-115. (Pubitemid 46067311)
57. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, et al. (2004) Identification of human brain tumour initiating cells. Nature 432: 396-401. (Pubitemid 39551674)
58. Visvader JE (2009) Keeping abreast of the mammary epithelial hierarchy and breast tumorigenesis. Genes Dev 23: 2563-2577.
59. Pereira C, Clarke E, Damen J (2007) Hematopoietic colony-forming cell assays. Methods Mol Biol 407: 177-208.
60. Freedman VH, Shin SI (1974) Cellular tumorigenicity in nude mice: correlation with cell growth in semi-solid medium. Cell 3: 355-359.
61. Vincent A, Van S, I (2012) On the epigenetic origin of cancer stem cells. Biochim Biophys Acta 1826: 83-88.
62. Donjacour AA, Cunha GR (1991) Stromal regulation of epithelial function. Cancer Treat Res 53: 335-364.
63. Chang CP, Chio CC, Cheong CU, Chao CM, Cheng BC, et al. (2013) Hypoxic preconditioning enhances the therapeutic potential of the secretome from cultured human mesenchymal stem cells in experimental traumatic brain injury. Clin Sci (Lond) 124: 165-176.
64. Ling-Ling Z, Li-Ying W, Kui-Wu W, Ming F (2012) Mild hypoxia regulates the properties and functions of neural stem cells in vitro. Science 338: 1485.
65. Azenshtein E, Luboshits G, Shina S, Neumark E, Shahbazian D, et al. (2002) The CC chemokine RANTES in breast carcinoma progression: regulation of expression and potential mechanisms of promalignant activity. Cancer Res 62: 1093-1102. (Pubitemid 34160293)
66. Azenshtein E, Meshel T, Shina S, Barak N, Keydar I, et al. (2005) The angiogenic factors CXCL8 and VEGF in breast cancer: regulation by an array of pro-malignancy factors. Cancer Lett 217: 73-86. (Pubitemid 39642868)
67. Khodarev NN, Yu J, Labay E, Darga T, Brown CK, et al. (2003) Tumour-endothelium interactions in co-culture: coordinated changes of gene expression profiles and phenotypic properties of endothelial cells. J Cell Sci 116: 1013-1022. (Pubitemid 36395612)
68. Sun XT, Zhang MY, Shu C, Li Q, Yan XG, et al. (2005) Differential gene expression during capillary morphogenesis in a microcarrier-based three-dimensional in vitro model of angiogenesis with focus on chemokines and chemokine receptors. World J Gastroenterol 11: 2283-2290. (Pubitemid 40691338)
69. Gazzaniga S, Bravo AI, Guglielmotti A, van RN, Maschi F, et al. (2007) Targeting tumor-associated macrophages and inhibition of MCP-1 reduce angiogenesis and tumor growth in a human melanoma xenograft. J Invest Dermatol 127: 2031-2041. (Pubitemid 47075380)
70. Koga M, Kai H, Egami K, Murohara T, Ikeda A, et al. (2008) Mutant MCP-1 therapy inhibits tumor angiogenesis and growth of malignant melanoma in mice. Biochem Biophys Res Commun 365: 279-284. (Pubitemid 350137285)
71. Kuroda T, Kitadai Y, Tanaka S, Yang X, Mukaida N, et al. (2005) Monocyte chemoattractant protein-1 transfection induces angiogenesis and tumorigenesis of gastric carcinoma in nude mice via macrophage recruitment. Clin Cancer Res 11: 7629-7636. (Pubitemid 41611603)
72. Weber KS, Nelson PJ, Grone HJ, Weber C (1999) Expression of CCR2 by endothelial cells : implications for MCP-1 mediated wound injury repair and In vivo inflammatory activation of endothelium. Arterioscler Thromb Vasc Biol 19: 2085-2093. (Pubitemid 29422239)
73. Yamada M, Kim S, Egashira K, Takeya M, Ikeda T, et al. (2003) Molecular mechanism and role of endothelial monocyte chemoattractant protein-1 induction by vascular endothelial growth factor. Arterioscler Thromb Vasc Biol 23: 1996-2001. (Pubitemid 37433191)
74. Raman D, Baugher PJ, Thu YM, Richmond A (2007) Role of chemokines in tumor growth. Cancer Lett 256: 137-165. (Pubitemid 47418345)
75. Yaal-Hahoshen N, Shina S, Leider-Trejo L, Barnea I, Shabtai EL, et al. (2006) The chemokine CCL5 as a potential prognostic factor predicting disease progression in stage II breast cancer patients. Clin Cancer Res 12: 4474-4480. (Pubitemid 44297794)
76. Soria G, Yaal-Hahoshen N, Azenshtein E, Shina S, Leider-Trejo L, et al. (2008) Concomitant expression of the chemokines RANTES and MCP-1 in human breast cancer: a basis for tumor-promoting interactions. Cytokine 44: 191-200.
77. Velasco-Velazquez M, Jiao X, De La Fuente M, Pestell TG, Ertel A, et al. (2012) CCR5 antagonist blocks metastasis of basal breast cancer cells. Cancer Res 72: 3839-3850.
78. Lv D, Zhang Y, Kim HJ, Zhang L, Ma X (2013) CCL5 as a potential immunotherapeutic target in triple-negative breast cancer. Cell Mol Immunol 10(4) 303-310.
79. Lin S, Wan S, Sun L, Hu J, Fang D, et al. (2012) Chemokine C-C motif receptor 5 and C-C motif ligand 5 promote cancer cell migration under hypoxia. Cancer Sci 103: 904-912.
80. Mulligan AM, Raitman I, Feeley L, Pinnaduwage D, Nguyen LT, et al. (2013) Tumoral lymphocytic infiltration and expression of the chemokine CXCL10 in breast cancers from the Ontario Familial Breast Cancer Registry. Clin Cancer Res 19: 336-346.
81. Bigelow RL, Williams BJ, Carroll JL, Daves LK, Cardelli JA (2009) TIMP-1 overexpression promotes tumorigenesis of MDA-MB-231 breast cancer cells and alters expression of a subset of cancer promoting genes in vivo distinct from those observed in vitro. Breast Cancer Res Treat 117: 31-44.
82. Acharyya S, Oskarsson T, Vanharanta S, Malladi S, Kim J, et al. (2012) A CXCL1 paracrine network links cancer chemoresistance and metastasis. Cell 150: 165-178.
83. Laoui D, Movahedi K, Van OE, Van den Bossche J, Schouppe E, et al. (2011) Tumor-associated macrophages in breast cancer: distinct subsets, distinct functions. Int J Dev Biol 55: 861-867.