A context-specific role for retinoblastoma protein-dependent negative growth control in suppressing mammary tumorigenesis

PLoS ONE

Volumn 6, Issue 2, 2011, Pages

  Francis, Sarah M ^a,b   Chakrabarti, Subrata ^b   Dick, Frederick A ^a,b,c  

^a LONDON REGIONAL CANCER PROGRAM   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

^c CHILDREN S HEALTH RESEARCH INSTITUTE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; DNA; PROTEIN LXCXE; PROTEIN P53; PROTEIN WAP; RETINOBLASTOMA PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; TUMOR SUPPRESSOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; BREAST EPITHELIUM; CANCER GROWTH; CANCER INHIBITION; CELL CYCLE REGULATION; CONTROLLED STUDY; DNA DAMAGE; FEMALE; GENE; MALIGNANT TRANSFORMATION; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN FUNCTION; RETINOBLASTOMA 1 GENE; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; ADENOCARCINOMA; ANIMAL; BREAST TUMOR; C57BL MOUSE; CELL CULTURE; CELL PROLIFERATION; CELL TRANSFORMATION; DOWN REGULATION; GENETICS; METABOLISM; PATHOLOGY; PHYSIOLOGY; UDDER;

MUS;

ADENOCARCINOMA; ANIMALS; BREAST NEOPLASMS; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; DOWN-REGULATION; FEMALE; MAMMARY GLANDS, ANIMAL; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; RETINOBLASTOMA PROTEIN; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS;

EID: 79952053379     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0016434     Document Type: Article

References (44)

1. Hanahan D, Weinberg RA, (2000) The hallmarks of cancer. Cell 100: 57-70.
2. Hennighausen L, Robinson GW, (2001) Signaling pathways in mammary gland development. Dev Cell 1: 467-475.
3. Massague J, (2004) G1 cell-cycle control and cancer. Nature 432: 298-306.
4. Sherr CJ, (1996) Cancer cell cycles. Science 274: 1672-1677.
5. Sherr CJ, Roberts JM, (1995) Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev 9: 1149-1163.
6. Brugarolas J, Chandrasekaran C, Gordon JI, Beach D, Jacks T, et al. (1995) Radiation-induced cell cycle arrest compromised by p21 deficiency. Nature 377: 552-557.
7. Brugarolas J, Moberg K, Boyd S, Taya Y, Jacks T, et al. (1999) Inhibition of cyclin-dependent kinase 2 by p21 is necessary for retinoblastoma protein-mediated G1 arrest after gamma-irradiation. Proc Natl Acad Sci USA 96: 1002-1007.
8. Florenes VA, Bhattacharya N, Bani MR, Ben-David Y, Kerbel RS, et al. (1996) TGF-beta mediated G1 arrest in a human melanoma cell line lacking p15INK4B: evidence for cooperation between p21Cip1/WAF1 and p27Kip1. Oncogene 13: 2447-2457.
9. Iavarone A, Massague J, (1997) Repression of the CDK activator Cdc25A and cell-cycle arrest by cytokine TGF-beta in cells lacking the CDK inhibitor p15. Nature 387: 417-422.
10. Missero C, di Cunto F, Kiyokawa H, Koff A, Dotto G, (1996) The abscence of p21 Cip1/WAF1 alters keratinocyte growth and differentiation and promotes ras tumor progression. Genes Dev 10: 3065-3075.
11. Nakayama K, Ishida N, Shirane M, Inomata A, Inoue T, et al. (1996) Mice lacking p27(Kip1) display increased body size, multiple organ hyperplasia, retinal dysplasia, and pituitary tumors. Cell 85: 707-720.
12. Sharpless NE, Bardeesy N, Lee KH, Carrasco D, Castrillon DH, et al. (2001) Loss of p16Ink4a with retention of p19Arf predisposes mice to tumorigenesis. Nature 413: 86-91.
13. Krimpenfort P, Quon KC, Mooi WJ, Loonstra A, Berns A, (2001) Loss of p16Ink4a confers susceptibility to metastatic melanoma in mice. Nature 413: 83-86.
14. Fero ML, Rivkin M, Tasch M, Porter P, Carow CE, et al. (1996) A syndrome of multiorgan hyperplasia with features of gigantism, tumorigenesis, and female sterility in p27(Kip1)-deficient mice. Cell 85: 733-744.
15. Kiyokawa H, Kineman RD, Manova-Todorova KO, Soares VC, Hoffman ES, et al. (1996) Enhanced growth of mice lacking the cyclin-dependent kinase inhibitor function of p27(Kip1). Cell 85: 721-732.
16. Deng C, Zhang P, Harper JW, Elledge SJ, Leder P, (1995) Mice lacking p21CIP1/WAF1 undergo normal development, but are defective in G1 checkpoint control. Cell 82: 675-684.
17. Krimpenfort P, Ijpenberg A, Song JY, van der Valk M, Nawijn M, et al. (2007) p15Ink4b is a critical tumour suppressor in the absence of p16Ink4a. Nature 448: 943-946.
18. Latres E, Malumbres M, Sotillo R, Martin J, Ortega S, et al. (2000) Limited overlapping roles of P15(INK4b) and P18(INK4c) cell cycle inhibitors in proliferation and tumorigenesis. Embo J 19: 3496-3506.
19. Robinson GW, Wagner KU, Hennighausen L, (2001) Functional mammary gland development and oncogene-induced tumor formation are not affected by the absence of the retinoblastoma gene. Oncogene 20: 7115-7119.
20. Fernandez PL, Jares P, Rey MJ, Campo E, Cardesa A, (1998) Cell cycle regulators and their abnormalities in breast cancer. Mol Pathol 51: 305-309.
21. Bosco EE, Knudsen ES, (2007) RB in breast cancer: at the crossroads of tumorigenesis and treatment. Cell Cycle 6: 667-671.
22. Pietilainen T, Lipponen P, Aaltomaa S, Eskelinen M, Kosma VM, et al. (1995) Expression of retinoblastoma gene protein (Rb) in breast cancer as related to established prognostic factors and survival. Eur J Cancer 31A: 329-333.
23. Borg A, Zhang QX, Alm P, Olsson H, Sellberg GE, (1992) The retinoblastoma gene in breast cancer: allele loss is not correlated with loss of gene protein expression. Cancer Res 52: 2991-2994.
24. Nielsen NH, Emdin SO, Cajander J, Landberg G, (1997) Deregulation of cyclin E and D1 in breast cancer is associated with inactivation of the retinoblastoma protein. Oncogene 14: 295-304.
25. Weinberg RA, (1995) The retinoblastoma protein and cell cycle control. Cell 81: 323-330.
26. Francis SM, Bergsied J, Isaac CE, Coschi CH, Martens AL, et al. (2009) A functional connection between pRB and transforming growth factor beta in growth inhibition and mammary gland development. Mol Cell Biol 29: 4455-4466.
27. Talluri S, Isaac CE, Ahmad M, Henley SA, Francis SM, et al. (2010) A G1 checkpoint mediated by the retinoblastoma protein that is dispensable in terminal differentiation but essential for senescence. Mol Cell Biol 30: 948-960.
28. Isaac CE, Francis SM, Martens AL, Julian LM, Seifried LA, et al. (2006) The retinoblastoma protein regulates pericentric heterochromatin. Mol Cell Biol 26: 3659-3671.
29. Coschi CH, Martens AL, Ritchie K, Francis SM, Chakrabarti S, et al. (2010) Mitotic chromosome condensation mediated by the retinoblastoma protein is tumor-suppressive. Genes Dev 24: 1351-1363.
30. Page DL, Dupont WD, Rogers LW, Rados MS, (1985) Atypical hyperplastic lesions of the female breast. A long-term follow-up study. Cancer 55: 2698-2708.
31. Dupont WD, Page DL, (1985) Risk factors for breast cancer in women with proliferative breast disease. N Engl J Med 312: 146-151.
32. Ossovskaya VS, Mazo IA, Chernov MV, Chernova OB, Strezoska Z, et al. (1996) Use of genetic suppressor elements to dissect distinct biological effects of separate p53 domains. Proc Natl Acad Sci USA 93: 10309-10314.
33. Li B, Murphy KL, Laucirica R, Kittrell F, Medina D, et al. (1998) A transgenic mouse model for mammary carcinogenesis. Oncogene 16: 997-1007.
34. Li B, Rosen JM, McMenamin-Balano J, Muller WJ, Perkins AS, (1997) neu/ERBB2 cooperates with p53-172H during mammary tumorigenesis in transgenic mice. Mol Cell Biol 17: 3155-3163.
35. Guy CT, Webster MA, Schaller M, Parsons TJ, Cardiff RD, et al. (1992) Expression of the neu protooncogene in the mammary epithelium of transgenic mice induces metastatic disease. Proc Natl Acad Sci USA 89: 10578-10582.
36. Dankort DL, Wang Z, Blackmore V, Moran MF, Muller WJ, (1997) Distinct tyrosine autophosphorylation sites negatively and positively modulate neu-mediated transformation. Mol Cell Biol 17: 5410-5425.
37. Siegel PM, Shu W, Cardiff RD, Muller WJ, Massague J, (2003) Transforming growth factor beta signaling impairs Neu-induced mammary tumorigenesis while promoting pulmonary metastasis. Proc Natl Acad Sci USA 100: 8430-8435.
38. Muraoka RS, Koh Y, Roebuck LR, Sanders ME, Brantley-Sieders D, et al. (2003) Increased malignancy of Neu-induced mammary tumors overexpressing active transforming growth factor beta1. Mol Cell Biol 23: 8691-8703.
39. Siegel PM, Dankort DL, Hardy WR, Muller WJ, (1994) Novel activating mutations in the neu proto-oncogene involved in induction of mammary tumors. Mol Cell Biol 14: 7068-7077.
40. Cardiff RD, Anver MR, Gusterson BA, Hennighausen L, Jensen RA, et al. (2000) The mammary pathology of genetically engineered mice: the consensus report and recommendations from the Annapolis meeting. Oncogene 19: 968-988.
41. Ewan KB, Oketch-Rabah HA, Ravani SA, Shyamala G, Moses HL, et al. (2005) Proliferation of estrogen receptor-alpha-positive mammary epithelial cells is restrained by transforming growth factor-beta1 in adult mice. Am J Pathol 167: 409-417.
42. Hojilla CV, Kim I, Kassiri Z, Fata JE, Fang H, et al. (2007) Metalloproteinase axes increase beta-catenin signaling in primary mouse mammary epithelial cells lacking TIMP3. J Cell Sci 120: 1050-1060.
43. Pear WS, Nolan GP, Scott ML, Baltimore D, (1993) Production of high-titre helper-free retroviuses by transient transfection. Proc Natl Acad Sci USA 90: 8392-8396.
44. Dannenberg J-H, van Rossum A, Schuijff L, te Riele H, (2000) Ablation of the Retinoblastoma gene family deregulates G1 control causing immortalization and increased cell turnover under growth-restricting conditions. Genes Dev 14: 3051-3064.