Ras activation contributes to the maintenance and expansion of Sca-1pos cells in a mouse model of breast cancer

Cancer Letters

Volumn 287, Issue 2, 2010, Pages 172-181

  Kim, Ran Ju ^a   Kim, Soo Rim ^a   Roh, Kyung Jin ^a   Park, Sang Bum ^b   Park, Jeong Ran ^a   Kang, Kyung Sun ^b   Kong, Gu ^c   Tang, Binwu ^d   Yang, Yu an ^d   Kohn, Ethan A ^d   Wakefield, Lalage M ^d   Nam, Jeong Seok ^a  

^a Gachon University College of Medicine   (South Korea)

^b Konkuk University   (South Korea)

^c Hanyang University   (South Korea)

^d NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Cancer stem cell; Ras; Stem cell antigen 1

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE KINASE; N [[5 [(2 AMINO 3 MERCAPTOPROPYL)AMINO][1,1' BIPHENYL] 2 YL]CARBONYL]METHIONINE METHYL ESTER; RAS PROTEIN; STEM CELL ANTIGEN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; CANCER GROWTH; CANCER STEM CELL; CANCER THERAPY; CELL EXPANSION; CELL POPULATION; CONTROLLED STUDY; DOSE RESPONSE; DRUG MECHANISM; FEMALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; STEM CELL TRANSPLANTATION;

ALDEHYDE DEHYDROGENASE; ANIMALS; ANTIGENS, LY; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; ENZYME INHIBITORS; FARNESYLTRANSTRANSFERASE; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MAP KINASE KINASE KINASES; MEMBRANE PROTEINS; METHIONINE; MICE; MICE, INBRED BALB C; NEOPLASM INVASIVENESS; NEOPLASTIC STEM CELLS; PHOSPHORYLATION; PROTEIN PRENYLATION; RAS PROTEINS; SIGNAL TRANSDUCTION; SPHEROIDS, CELLULAR;

EID: 72949106003     PISSN: 03043835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.canlet.2009.06.010     Document Type: Article

References (45)

1. Reya T., Morrison S.J., Clarke M.F., and Weissman I.L. Stem cells, cancer, and cancer stem cells. Nature 414 (2001) 105-111
2. Al-Hajj M., Wicha M.S., Benito-Hernandez A., Morrison S.J., and Clarke M.F. Prospective identification of tumorigenic breast cancer cells. Proc. Natl. Acad. Sci. USA 100 (2003) 3983-3988
3. Jordan C.T., Guzman M.L., and Noble M. Cancer stem cells. New Engl. J. Med. 355 (2006) 1253-1261
4. Dean M., Fojo T., and Bates S. Tumour stem cells and drug resistance. Nat. Rev. Cancer 5 (2005) 275-284
5. Charafe-Jauffret E., Monville F., Ginestier C., Dontu G., Birnbaum D., and Wicha M.S. Cancer stem cells in breast: current opinion and future challenges. Pathobiology 75 (2008) 75-84
6. Vermeulen L., Sprick M.R., Kemper K., Stassi G., and Medema J.P. Cancer stem cells - old concepts, new insights. Cell Death Differ. 15 (2008) 947-958
7. Kuperwasser C., Chavarria T., Wu M., Magrane G., Gray J.W., Carey L., Richardson A., and Weinberg R.A. Reconstruction of functionally normal and malignant human breast tissues in mice. Proc. Natl. Acad. Sci. USA 101 (2004) 4966-4971
8. Kruger J.A., Kaplan C.D., Luo Y., Zhou H., Markowitz D., Xiang R., and Reisfeld R.A. Characterization of stem cell-like cancer cells in immune-competent mice. Blood 108 (2006) 3906-3912
9. Welm B.E., Tepera S.B., Venezia T., Graubert T.A., Rosen J.M., and Goodell M.A. Sca-1(pos) cells in the mouse mammary gland represent an enriched progenitor cell population. Dev. Biol. 245 (2002) 42-56
10. Li Y., and Rosen J.M. Stem/progenitor cells in mouse mammary gland development and breast cancer. J. Mammary Gland Biol. Neoplasia 10 (2005) 17-24
11. van de Rijn M., Heimfeld S., Spangrude G.J., and Weissman I.L. Mouse hematopoietic stem-cell antigen Sca-1 is a member of the Ly-6 antigen family. Proc. Natl. Acad. Sci. USA 86 (1989) 4634-4638
12. Spangrude G.J., Heimfeld S., and Weissman I.L. Purification and characterization of mouse hematopoietic stem cells. Science 241 (1988) 58-62
13. Matsuura K., Nagai T., Nishigaki N., Oyama T., Nishi J., Wada H., Sano M., Toko H., Akazawa H., Sato T., Nakaya H., Kasanuki H., and Komuro I. Adult cardiac Sca-1-positive cells differentiate into beating cardiomyocytes. J. Biol. Chem. 279 (2004) 11384-11391
14. Montanaro F., Liadaki K., Volinski J., Flint A., and Kunkel L.M. Skeletal muscle engraftment potential of adult mouse skin side population cells. Proc. Natl. Acad. Sci. USA 100 (2003) 9336-9341
15. Asakura A. Stem cells in adult skeletal muscle. Trends Cardiovas. Med. 13 (2003) 123-128
16. Falciatori I., Borsellino G., Haliassos N., Boitani C., Corallini S., Battistini L., Bernardi G., Stefanini M., and Vicini E. Identification and enrichment of spermatogonial stem cells displaying side-population phenotype in immature mouse testis. FASEB J. 18 (2004) 376-378
17. Burger P.E., Xiong X., Coetzee S., Salm S.N., Moscatelli D., Goto K., and Wilson E.L. Sca-1 expression identifies stem cells in the proximal region of prostatic ducts with high capacity to reconstitute prostatic tissue. Proc. Natl. Acad. Sci. USA 102 (2005) 7180-7185
18. Cohn M.A., Kramerov D., Hulgaard E.F., and Lukanidin E.M. The differentiation antigen Ly-6E.1 is expressed in mouse metastatic tumor cell lines. FEBS Lett. 403 (1997) 181-185
19. Katz B.Z., Eshel R., Sagi-Assif O., and Witz I.P. An association between high Ly-6A/E expression on tumor cells and a highly malignant phenotype. Int. J. Cancer 59 (1994) 684-691
20. Treister A., Sagi-Assif O., Meer M., Smorodinsky N.I., Anavi R., Golan I., Meshel T., Kahana O., Eshel R., Katz B.Z., Shevach E., and Witz I.P. Expression of Ly-6, a marker for highly malignant murine tumor cells, is regulated by growth conditions and stress. Int. J. Cancer 77 (1998) 306-313
21. Chakrabarty K., and Heumann R. Prospective of Ras signaling in stem cells. Biol. Chem. 389 (2008) 791-798
22. Scherl A., Li J.F., Cardiff R.D., and Schreiber-Agus N. Prostatic intraepithelial neoplasia and intestinal metaplasia in prostates of probasin-RAS transgenic mice. Prostate 59 (2004) 448-459
23. Pearson H.B., Phesse T.J., and Clarke A.R. K-ras and Wnt signaling synergize to accelerate prostate tumorigenesis in the mouse. Cancer Res. 69 (2009) 94-101
24. Lu C.W., Yabuuchi A., Chen L., Viswanathan S., Kim K., and Daley G.Q. Ras-MAPK signaling promotes trophectoderm formation from embryonic stem cells and mouse embryos. Nat. Genet. 40 (2008) 921-926
25. Ventura J.J., Tenbaum S., Perdiguero E., Huth M., Guerra C., Barbacid M., Pasparakis M., and Nebreda A.R. p38alpha MAP kinase is essential in lung stem and progenitor cell proliferation and differentiation. Nat. Genet. 39 (2007) 750-758
26. Nam J.S., Kang M.J., Suchar A.M., Shimamura T., Kohn E.A., Michalowska A.M., Jordan V.C., Hirohashi S., and Wakefield L.M. Chemokine (C-C motif) ligand 2 mediates the prometastatic effect of dysadherin in human breast cancer cells. Cancer Res. 66 (2006) 7176-7184
27. Nam J.S., Suchar A.M., Kang M.J., Stuelten C.H., Tang B., Michalowska A.M., Fisher L.W., Fedarko N.S., Jain A., Pinkas J., Lonning S., and Wakefield L.M. Bone sialoprotein mediates the tumor cell-targeted prometastatic activity of transforming growth factor beta in a mouse model of breast cancer. Cancer Res. 66 (2006) 6327-6335
28. Nanni P., de Giovanni C., Lollini P.L., Nicoletti G., and Prodi G. TS/A: a new metastasizing cell line from a BALB/c spontaneous mammary adenocarcinoma. Clin. Exp. Metast. 1 (1983) 373-380
29. Rockwell S.C., Kallman R.F., and Fajardo L.F. Characteristics of a serially transplanted mouse mammary tumor and its tissue-culture-adapted derivative. J. Natl. Cancer Inst. 49 (1972) 735-749
30. Lerner W.A., Pearlstein E., Ambrogio C., and Karpatkin S. A new mechanism for tumor induced platelet aggregation. Comparison with mechanisms shared by other tumor with possible pharmacologic strategy toward prevention of metastases. Int. J. Cancer 31 (1983) 463-469
31. Stingl J., Eirew P., Ricketson I., Shackleton M., Vaillant F., Choi D., Li H.I., and Eaves C.J. Purification and unique properties of mammary epithelial stem cells. Nature 439 (2006) 993-997
32. Matsuda M., Imaoka T., Vomachka A.J., Gudelsky G.A., Hou Z., Mistry M., Bailey J.P., Nieport K.M., Walther D.J., Bader M., and Horseman N.D. Serotonin regulates mammary gland development via an autocrine-paracrine loop. Dev. Cell 6 (2004) 193-203
33. Nam J.S., Terabe M., Kang M.J., Chae H., Voong N., Yang Y.A., Laurence A., Michalowska A., Mamura M., Lonning S., Berzofsky J.A., and Wakefield L.M. Transforming growth factor beta subverts the immune system into directly promoting tumor growth through interleukin-17. Cancer Res. 68 (2008) 3915-3923
34. Dontu G., Abdallah W.M., Foley J.M., Jackson K.W., Clarke M.F., Kawamura M.J., and Wicha M.S. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev. 17 (2003) 1253-1270
35. Aslakson C.J., and Miller F.R. Selective events in the metastatic process defined by analysis of the sequential dissemination of subpopulations of a mouse mammary tumor. Cancer Res. 52 (1992) 1399-1405
36. Lelekakis M., Moseley J.M., Martin T.J., Hards D., Williams E., Ho P., Lowen D., Javni J., Miller F.R., Slavin J., and Anderson R.L. A novel orthotopic model of breast cancer metastasis to bone. Clin. Exp. Metast. 17 (1999) 163-170
37. Ginestier C., Hur M.H., Charafe-Jauffret E., Monville F., Dutcher J., Brown M., Jacquemier J., Viens P., Kleer C.G., Liu S., Schott A., Hayes D., Birnbaum D., Wicha M.S., and Dontu G. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 1 (2007) 555-567
38. Takahashi K., and Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126 (2006) 663-676
39. O'Brien C.A., Pollett A., Gallinger S., and Dick J.E. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445 (2007) 106-110
40. Morel A.P., Lievre M., Thomas C., Hinkal G., Ansieau S., and Puisieux A. Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS ONE 3 (2008) e2888
41. Shaw R.J., and Cantley L.C. Ras, PI(3)K and mTOR signalling controls tumour cell growth. Nature 441 (2006) 424-430
42. Yang Y., Iwanaga K., Raso M.G., Wislez M., Hanna A.E., Wieder E.D., Molldrem J.J., Wistuba I.I., Powis G., Demayo F.J., Kim C.F., and Kurie J.M. Phosphatidylinositol 3-kinase mediates bronchioalveolar stem cell expansion in mouse models of oncogenic K-ras-induced lung cancer. PLoS ONE 3 (2008) e2220
43. Hodkinson P.S., Elliott P.A., Lad Y., McHugh B.J., MacKinnon A.C., Haslett C., and Sethi T. Mammalian NOTCH-1 activates beta1 integrins via the small GTPase R-Ras. J. Biol. Chem. 282 (2007) 28991-29001
44. Downward J. Targeting RAS signalling pathways in cancer therapy. Nat. Rev. Cancer 3 (2003) 11-22
45. Nam J.S., Ino Y., Sakamoto M., and Hirohashi S. Ras farnesylation inhibitor FTI-277 restores the E-cadherin/catenin cell adhesion system in human cancer cells and reduces cancer metastasis. Jpn. J. Cancer Res. 93 (2002) 1020-1028