Defining the ATM-mediated barrier to tumorigenesis in somatic mammary cells following ErbB2 activation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 8, 2010, Pages 3728-3733

  Reddy, Jay P ^a   Peddibhotla, Sirisha ^a   Bu, Wen ^a   Zhao, Jing ^a   Haricharan, Svasti ^a   Dud, Yi Chieh Nancy ^b   Podsypanina, Katrina ^b   Rosen, Jeffrey M ^a   Donehower, Larry A ^a   Li, Yi ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Apoptosis; DNA damage response; Oncogene; p53; Senescence

Indexed keywords

ATM PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; PROTEIN P53;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BREAST CELL; CARCINOGENESIS; CELL AGING; CELL PROLIFERATION; DNA DAMAGE; DNA DAMAGE RESPONSE; DNA REPLICATION; ENZYME ACTIVATION; GENE ACTIVATION; GENE EXPRESSION; IN VIVO STUDY; MOUSE; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN STABILITY; SIGNAL TRANSDUCTION; SOMATIC CELL; TRANSGENIC MOUSE; TUMOR MODEL; UPREGULATION;

ANIMALS; APOPTOSIS; BREAST NEOPLASMS; CELL AGING; CELL CYCLE PROTEINS; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; DISEASE MODELS, ANIMAL; DNA DAMAGE; DNA-BINDING PROTEINS; FEMALE; MICE; MICE, TRANSGENIC; PROTEIN-SERINE-THREONINE KINASES; RECEPTOR, ERBB-2; TUMOR SUPPRESSOR PROTEINS;

MURINAE; MUS MUSCULUS;

EID: 77649247825     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0910665107     Document Type: Article

References (59)

1. Halazonetis TD, Gorgoulis VG, Bartek J (2008) An oncogene-induced DNA damage model for cancer development. Science 319:1352-1355.
2. Venkitaraman AR (2005) Medicine: aborting the birth of cancer. Nature 434:829-830.
3. Lowe SW, Cepero E, Evan G (2004) Intrinsic tumour suppression. Nature 432:307-315.
4. Bartek J, Bartkova J, Lukas J (2007) DNA damage signalling guards against activated oncogenes and tumour progression. Oncogene 26:7773-7779.
5. Kastan MB (2008) DNA damage responses: Mechanisms and roles in human disease: 2007 G.H.A. Clowes Memorial Award Lecture. Mol Cancer Res 6:517-524.
6. Harper JW, Elledge SJ (2007) The DNA damage response: Ten years after. Mol Cell 28: 739-745.
7. Kastan MB, Bartek J (2004) Cell-cycle checkpoints and cancer. Nature 432:316-323.
8. Bartkova J, et al. (2005) DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 434:864-870.
9. Gorgoulis VG, et al. (2005) Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 434:907-913.
10. Reimann M, et al. (2007) The Myc-evoked DNA damage response accounts for treatment resistance in primary lymphomas in vivo. Blood 110:2996-3004.
11. Pusapati RV, et al. (2006) ATM promotes apoptosis and suppresses tumorigenesis in response to Myc. Proc Natl Acad Sci USA 103:1446-1451.
12. Bartkova J, et al. (2006) Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 444:633-637.
13. Di Micco R, et al. (2006) Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication. Nature 444:638-642.
14. Mallette FA, Gaumont-Leclerc MF, Ferbeyre G (2007) The DNA damage signaling pathway is a critical mediator of oncogene-induced senescence. Genes Dev 21:43-48.
15. Liao MJ, Yin C, Barlow C, Wynshaw-Boris A, van Dyke T (1999) Atm is dispensable for p53 apoptosis and tumor suppression triggered by cell cycle dysfunction. Mol Cell Biol 19:3095-3102.
16. Efeyan A, et al. (2009) Limited role of murine ATM in oncogene-induced senescence and p53-dependent tumor suppression. PLoS One, 4:e5475, 1-11.
17. Woditschka S, Haag JD, Sullivan R, Gould MN (2009) A short-term rat mammary carcinogenesis model for the prevention of hormonally responsive and nonresponsive in situ carcinomas. Cancer Prev Res 2:153-160.
18. Sarkisian CJ, et al. (2007) Dose-dependent oncogene-induced senescence in vivo and its evasion during mammary tumorigenesis. Nat Cell Biol 9:493-505.
19. Ayyanan A, et al. (2006) Increased Wnt signaling triggers oncogenic conversion of human breast epithelial cells by a Notch-dependent mechanism. Proc Natl Acad Sci USA 103:3799-3804.
20. Umesako S, et al. (2005) Atm heterozygous deficiency enhances development of mammary carcinomas in p53 heterozygous knockout mice. Breast Cancer Res 7: R164-R170.
21. Lu S, et al. (2006) Atm-haploinsufficiency enhances susceptibility to carcinogeninduced mammary tumors. Carcinogenesis 27:848-855.
22. Du Z, et al. (2006) Introduction of oncogenes into mammary glands in vivo with an avian retroviral vector initiates and promotes carcinogenesis in mouse models. Proc Natl Acad Sci USA 103:17396-17401.
23. Marcotte R, Muller WJ (2008) Signal transduction in transgenic mouse models of human breast cancer-implications for human breast cancer. J Mammary Gland Biol Neoplasia 13:323-335.
24. Podsypanina K, et al. (2008) Seeding and propagation of untransformed mouse mammary cells in the lung. Science 321:1841-1844.
25. Du Z, Li Y (2007) RCAS-TVA in the mammary gland: An in vivo oncogene screen and a high fidelity model for breast transformation? Cell Cycle 6:823-826.
26. Reddy JP, Li Y (2009) The RCAS-TVA system for introduction of oncogenes into selected somatic mammary epithelial cells in vivo. J Mammary Gland Biol Neoplasia 14:405-409.
27. Hughes SH (2004) The RCAS vector system. Folia Biol (Praha) 50:107-119.
28. Ursini-Siegel J, Schade B, Cardiff RD, Muller WJ (2007) Insights from transgenic mouse models of ERBB2-induced breast cancer. Nat Rev Cancer 7:389-397.
29. Campisi J, d'Adda di Fagagna F (2007) Cellular senescence: When bad things happen to good cells. Nat Rev Mol Cell Biol 8:729-740.
30. Di Micco R, Fumagalli M, d'Adda di Fagagna F (2007) Breaking news: High-speed race ends in arrest-how oncogenes induce senescence. Trends Cell Biol 17:529-536.
31. Dimri GP, et al. (1995) A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci USA 92:9363-9367.
32. Collado M, et al. (2005) Tumour biology: Senescence in premalignant tumours. Nature 436:642.
33. Collado M, Serrano M (2006) The power and the promise of oncogene-induced senescence markers. Nat Rev Cancer 6:472-476.
34. Borghesani PR, et al. (2000) Abnormal development of Purkinje cells and lymphocytes in Atm mutant mice. Proc Natl Acad Sci USA 97:3336-3341.
35. Andrechek ER, Hardy WR, Laing MA, Muller WJ (2004) Germ-line expression of an oncogenic erbB2 allele confers resistance to erbB2-induced mammary tumorigenesis. Proc Natl Acad Sci USA 101:4984-4989.
36. Hynes NE, Lane HA (2005) ERBB receptors and cancer: The complexity of targeted inhibitors. Nat Rev Cancer 5:341-354.
37. Donehower LA (1996) The p53-deficient mouse: A model for basic and applied cancer studies. Semin Cancer Biol 7:269-278.
38. Langerød A, et al. (2007) TP53 mutation status and gene expression profiles are powerful prognostic markers of breast cancer. Breast Cancer Res, 9:R30, 1-16.
39. Deng CX, Wang RH (2003) Roles of BRCA1 in DNA damage repair: A link between development and cancer. Hum Mol Genet 12(Spec No 1, Spec No 1)R113-R123.
40. Palmero I, Pantoja C, Serrano M (1998) p19ARF links the tumour suppressor p53 to Ras. Nature 395:125-126.
41. Zindy F, et al. (1998) Myc signaling via the ARF tumor suppressor regulates p53-dependent apoptosis and immortalization. Genes Dev 12:2424-2433.
42. Swarbrick A, Roy E, Allen T, Bishop JM (2008) Id1 cooperates with oncogenic Ras to induce metastatic mammary carcinoma by subversion of the cellular senescence response. Proc Natl Acad Sci USA 105:5402-5407.
43. D'Amico M, et al. (2003) The role of Ink4a/Arf in ErbB2 mammary gland tumorigenesis. Cancer Res 63:3395-3402.
44. Debies MT, et al. (2008) Tumor escape in a Wnt1-dependent mouse breast cancer model is enabled by p19Arf/p53 pathway lesions but not p16 Ink4a loss. J Clin Invest 118:51-63.
45. Michaloglou C, et al. (2005) BRAFE600-associated senescence-like cell cycle arrest of human naevi. Nature 436:720-724.
46. Chen Z, et al. (2005) Crucial role of p53-dependent cellular senescence in suppression of Pten-deficient tumorigenesis. Nature 436:725-730.
47. Braig M, et al. (2005) Oncogene-induced senescence as an initial barrier in lymphoma development. Nature 436:660-665.
48. Trost TM, et al. (2005) Premature senescence is a primary fail-safe mechanism of ERBB2-driven tumorigenesis in breast carcinoma cells. Cancer Res 65:840-849.
49. Visvader JE, Lindeman GJ (2008) Cancer stem cells in solid tumours: Accumulating evidence and unresolved questions. Nat Rev Cancer 8:755-768.
50. Rosen JM, Jordan CT (2009) The increasing complexity of the cancer stem cell paradigm. Science 324:1670-1673.
51. Aliouat-Denis CM, et al. (2005) p53-independent regulation of p21Waf1/Cip1 expression and senescence by Chk2. Mol Cancer Res 3:627-634.
52. Chen CR, et al. (2005) Dual induction of apoptosis and senescence in cancer cells by Chk2 activation: Checkpoint activation as a strategy against cancer. Cancer Res 65: 6017-6021.
53. Serrano M, Lin AW, McCurrach ME, Beach D, Lowe SW (1997) Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 88:593-602.
54. Beauséjour CM, et al. (2003) Reversal of human cellular senescence: Roles of the p53 and p16 pathways. EMBO J 22:4212-4222.
55. Narita M, et al. (2003) Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell 113:703-716.
56. Guy CT, Cardiff RD, Muller WJ (1992) Induction of mammary tumors by expression of polyomavirus middle T oncogene: A transgenic mouse model for metastatic disease. Mol Cell Biol 12:954-961.
57. Guy CT, 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.
58. Leder A, Pattengale PK, Kuo A, Stewart TA, Leder P (1986) Consequences of widespread deregulation of the c-myc gene in transgenic mice: Multiple neoplasms and normal development. Cell 45:485-495.
59. Sinn E, et al. (1987) Coexpression of MMTV/v-Ha-ras and MMTV/c-myc genes in transgenic mice: Synergistic action of oncogenes in vivo. Cell 49:465-475.