LMO4 is an essential mediator of ErbB2/HER2/Neu-induced breast cancer cell cycle progression

Oncogene

Volumn 28, Issue 41, 2009, Pages 3608-3618

  Montaez Wiscovich M E ^a   Seachrist, D D ^a   Landis, M D ^a   Visvader, J ^b   Andersen, B ^c   Keri, R A ^a,d  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Victorian Breast Cancer Research   (Australia)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

Breast cancer; Cullin 3; ErbB2; HER2; LMO4

Indexed keywords

CULLIN; CULLIN 3; CYCLIN D1; CYCLIN E; EPIDERMAL GROWTH FACTOR RECEPTOR 2; LIM PROTEIN; LIM PROTEIN 4; PHOSPHATIDYLINOSITOL 3 KINASE; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BREAST CANCER; CANCER CELL; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE PROGRESSION; CELL PROLIFERATION; CONTROLLED STUDY; EPITHELIUM TUMOR; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MAMMARY GLAND; METASTASIS; MITOSIS; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; UPREGULATION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; BREAST NEOPLASMS; CELL CYCLE; CELL DIVISION; CELL LINE, TUMOR; CELL PROLIFERATION; CULLIN PROTEINS; CYCLIN D1; G2 PHASE; GENE EXPRESSION REGULATION, NEOPLASTIC; HOMEODOMAIN PROTEINS; HUMANS; MICE; NEUREGULIN-1; RECEPTOR, ERBB-2; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; UP-REGULATION;

MUS;

EID: 70350075690     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2009.221     Document Type: Article

References (53)

1. Andrechek ER, White D, Muller WJ. (2005). Targeted disruption of ErbB2/Neu in the mammary epithelium results in impaired ductal outgrowth. Oncogene 24: 932-937.
2. Beerli RR, Hynes NE. (1996). Epidermal growth factor-related peptides activate distinct subsets of ErbB receptors and differ in their biological activities. J Biol Chem 271: 6071-6076.
3. Ben Levy R, Paterson HF, Marshall CJ, Yarden Y. (1994). A single autophosphorylation site confers oncogenicity to the Neu/ErbB-2 receptor and enables coupling to the MAP kinase pathway. EMBO J 13: 3302-3311.
4. Caporossi D, Vernole P, Nicoletti B, Tedeschi B. (1995). Characteristic chromosomal fragility of human embryonic cells exposed in vitro to aphidicolin. Hum Genet 96: 269-274.
5. Chen HH, Xu J, Safarpour F, Stewart AF. (2007). LMO4 mRNA stability is regulated by extracellular ATP in F11 cells. Biochem Biophys Res Commun 357: 56-61.
6. Dankort DL, Muller WJ. (2000). Signal transduction in mammary tumorigenesis: a transgenic perspective. Oncogene 19: 1038-1044.
7. Desai KV, Xiao N, Wang W, Gangi L, Greene J, Powell JI et al. (2002). Initiating oncogenic event determines gene-expression patterns of human breast cancer models. Proc Natl Acad Sci USA 99: 6967-6972.
8. Desmedt C, Piette F, Loi S, Wang Y, Lallemand F, Haibe-Kains B et al. (2007). Strong time dependence of the 76-gene prognostic signature for node-negative breast cancer patients in the TRANS-BIG multicenter independent validation series. Clin Cancer Res 13: 3207-3214.
9. Graus-Porta D, Beerli RR, Daly JM, Hynes NE. (1997). ErbB-2, the preferred heterodimerization partner of all ErbB receptors, is a mediator of lateral signaling. EMBO J 16: 1647-1655.
10. Guy CT, Webster MA, Schaller M, Parsons TJ, Cardiff RD, Muller WJ. (1992). Expression of the neu protooncogene in the mammary epithelium of transgenic mice induces metastatic disease. Proc Natl Acad Sci USA 89: 10578-10582.
11. Ismail IA, Kang KS, Lee HA, Kim JW, Sohn YK. (2007). Genistein-induced neuronal apoptosis and G2/M cell cycle arrest is associated with MDC1 up-regulation and PLK1 down-regulation. Eur J Pharmacol 575: 12-20.
12. Ivshina AV, George J, Senko O, Mow B, Putti TC, Smeds J et al. (2006). Genetic reclassification of histologic grade delineates new clinical subtypes of breast cancer. Cancer Res 66: 10292-10301.
13. Junaid A, Moon MC, Harding GE, Zahradka P. (2007). Osteopontin localizes to the nucleus of 293 cells and associates with polo-like kinase-1. Am J Physiol Cell Physiol 292: C919-C926.
14. Kraus MH, Popescu NC, Amsbaugh SC, King CR. (1987). Over-expression of the EGF receptor-related proto-oncogene erbB-2 in human mammary tumor cell lines by different molecular mechanisms. EMBO J 6: 605-610.
15. Kuraguchi M, Ohene-Baah NY, Sonkin D, Bronson RT, Kucherlapati R. (2009). Genetic mechanisms in apc-mediated mammary tumor-igenesis. PLoS Genet 5: e1000367.
16. Lal A, Mazan-Mamczarz K, Kawai T, Yang X, Martindale JL, Gorospe M. (2004). Concurrent versus individual binding of HuR and AUF1 to common labile target mRNAs. EMBO J 23: 3092-3102.
17. Landis MD, Seachrist DD, Montanez-Wiscovich ME, Danielpour D, Keri RA. (2005). Gene expression profiling of cancer progression reveals intrinsic regulation of transforming growth factor-beta signaling in ErbB2/Neu-induced tumors from transgenic mice. Oncogene 24: 5173-5190.
18. Lee RJ, Albanese C, Fu M, D'Amico M, Lin B, Watanabe G et al. (2000). Cyclin D1 is required for transformation by activated Neu and is induced through an E2F-dependent signaling pathway. Mol Cell Biol 20: 672-683.
19. Lenferink AE, Busse D, Flanagan WM, Yakes FM, Arteaga CL. (2001). ErbB2/neu kinase modulates cellular p27(Kip1) and cyclin D1 through multiple signaling pathways. Cancer Res 61: 6583-6591.
20. Lewis GD, Lofgren JA, McMurtrey AE, Nuijens A, Fendly BM, Bauer KD et al. (1996). Growth regulation of human breast and ovarian tumor cells by heregulin: Evidence for the requirement of ErbB2 as a critical component in mediating heregulin responsiveness. Cancer Res 56: 1457-1465.
21. Moody SE, Perez D, Pan TC, Sarkisian CJ, Portocarrero CP, Sterner CJ et al. (2005). The transcriptional repressor Snail promotes mammary tumor recurrence. Cancer Cell 8: 197-209.
22. Mosley JD, Keri RA. (2008). Cell cycle correlated genes dictate the prognostic power of breast cancer gene lists. BMC Med Genomics 1: 11.
23. Mousses S, Bubendorf L, Wagner U, Hostetter G, Kononen J, Cornelison R et al. (2002). Clinical validation of candidate genes associated with prostate cancer progression in the CWR22 model system using tissue microarrays. Cancer Res 62: 1256-1260.
24. Peles E, Lamprecht R, Ben Levy R, Tzahar E, Yarden Y. (1992). Regulated coupling of the Neu receptor to phosphatidylinositol 30-kinase and its release by oncogenic activation. J Biol Chem 267: 12266-12274.
25. Peles E, Levy RB, Or E, Ullrich A, Yarden Y. (1991). Oncogenic forms of the neu/HER2 tyrosine kinase are permanently coupled to phospholipase C gamma. EMBO J 10: 2077-2086.
26. Piccart-Gebhart MJ, Procter M, Leyland-Jones B, Goldhirsch A, Untch M, Smith I et al. (2005). Trastuzumab after adjuvant chemotherapy in HER2-positive breast cancer. N Engl J Med 353: 1659-1672. (Pubitemid 41464705)
27. Pines J, Hunter T. (1989). Isolation of a human cyclin cDNA: evidence for cyclin mRNA and protein regulation in the cell cycle and for interaction with p34cdc2. Cell 58: 833-846.
28. Rabbitts TH. (1998). LMO T-cell translocation oncogenes typify genes activated by chromosomal translocations that alter transcription and developmental processes. Genes Dev 12: 2651-2657.
29. Resnitzky D, Gossen M, Bujard H, Reed SI. (1994). Acceleration of the G1/S phase transition by expression of cyclins D1 and E with an inducible system. Mol Cell Biol 14: 1669-1679.
30. Rhodes DR, Yu J, Shanker K, Deshpande N, Varambally R, Ghosh D et al. (2004). ONCOMINE: a cancer microarray database and integrated data-mining platform. Neoplasia 6: 1-6.
31. Ribar B, Prakash L, Prakash S. (2007). ELA1 and CUL3 are required along with ELC1 for RNA polymerase II polyubiquitylation and degradation in DNA-damaged yeast cells. Mol Cell Biol 27: 3211-3216.
32. Romond EH, Perez EA, Bryant J, Suman VJ, Geyer Jr CE, Davidson NE et al. (2005). Trastuzumab plus adjuvant chemotherapy for operable HER2-positive breast cancer. N Engl J Med 353: 1673-1684.
33. Sanchez-Margalet V, Goldfine ID, Vlahos CJ, Sung CK. (1994). Role of phosphatidylinositol-3-kinase in insulin receptor signaling: studies with inhibitor, LY294002. Biochem Biophys Res Commun 204: 446-452.
34. Seidman A, Hudis C, Pierri MK, Shak S, Paton V, Ashby M et al. (2002). Cardiac dysfunction in the trastuzumab clinical trials experience. J Clin Oncol 20: 1215-1221.
35. Slamon DJ, Godolphin W, Jones LA, Holt JA, Wong SG, Keith DE et al. (1989). Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. Science 244: 707-712.
36. Stern DF. (2003). ErbBs in mammary development. Exp Cell Res 284: 89-98.
37. Sugihara TM, Bach I, Kioussi C, Rosenfeld MG, Andersen B. (1998). Mouse deformed epidermal autoregulatory factor 1 recruits a LIM domain factor, LMO-4, and CLIM coregulators. Proc Natl Acad Sci USA 95: 15418-15423.
38. Sum EY, O'Reilly LA, Jonas N, Lindeman GJ, Visvader JE. (2005a). The LIM domain protein Lmo4 is highly expressed in proliferating mouse epithelial tissues. J Histochem Cytochem 53: 475-486.
39. Sum EY, Peng B, Yu X, Chen J, Byrne J, Lindeman GJ et al. (2002). The LIM domain protein LMO4 interacts with the cofactor CtIP and the tumor suppressor BRCA1 and inhibits BRCA1 activity. J Biol Chem 277: 7849-7856.
40. Sum EY, Segara D, Duscio B, Bath ML, Field AS, Sutherland RL et al. (2005b). Overexpression of LMO4 induces mammary hyperplasia, promotes cell invasion, and is a predictor of poor outcome in breast cancer. Proc Natl Acad Sci USA 102: 7659-7664.
41. Sum EY, Shackleton M, Hahm K, Thomas RM, O'Reilly LA, Wagner KU et al. (2005c). Loss of the LIM domain protein Lmo4 in the mammary gland during pregnancy impedes lobuloalveolar development. Oncogene 24: 4820-4828.
42. Sumara I, Quadroni M, Frei C, Olma MH, Sumara G, Ricci R et al. (2007). A Cul3-based E3 ligase removes Aurora B from mitotic chromosomes, regulating mitotic progression and completion of cytokinesis in human cells. Dev Cell 12: 887-900.
43. Sutherland KD, Visvader JE, Choong DY, Sum EY, Lindeman GJ, Campbell IG. (2003). Mutational analysis of the LMO4 gene, encoding a BRCA1-interacting protein, in breast carcinomas. Int J Cancer 107: 155-158.
44. Taniwaki M, Daigo Y, Ishikawa N, Takano A, Tsunoda T, Yasui W et al. (2006). Gene expression profiles of small-cell lung cancers: molecular signatures of lung cancer. Int J Oncol 29: 567-575.
45. Visvader JE, Venter D, Hahm K, Santamaria M, Sum EY, O'Reilly L et al. (2001). The LIM domain gene LMO4 inhibits differentiation of mammary epithelial cells in vitro and is overexpressed in breast cancer. Proc Natl Acad Sci USA 98: 14452-14457.
46. Wang N, Kudryavtseva E, Ch'en IL, McCormick J, Sugihara TM, Ruiz R et al. (2004). Expression of an engrailed-LMO4 fusion protein in mammary epithelial cells inhibits mammary gland development in mice. Oncogene 23: 1507-1513.
47. Wang N, Lin KK, Lu Z, Lam KS, Newton R, Xu X et al. (2007). The LIM-only factor LMO4 regulates expression of the BMP7 gene through an HDAC2-dependent mechanism, and controls cell proliferation and apoptosis of mammary epithelial cells. Oncogene 26: 6431-6441.
48. Wang W, Caldwell MC, Lin S, Furneaux H, Gorospe M. (2000). HuR regulates cyclin A and cyclin B1 mRNA stability during cell proliferation. EMBO J 19: 2340-2350.
49. Wittlin S, Sum EY, Jonas NK, Lindeman GJ, Visvader JE. (2003). Two promoters within the human LMO4 gene contribute to its overexpression in breast cancer cells. Genomics 82: 280-287.
50. Xu L, Wei Y, Reboul J, Vaglio P, Shin TH, Vidal M et al. (2003). BTB proteins are substrate-specific adaptors in an SCF-like modular ubiquitin ligase containing CUL-3. Nature 425: 316-321.
51. Yakes FM, Chinratanalab W, Ritter CA, King W, Seelig S, Arteaga CL. (2002). Herceptin-induced inhibition of phosphatidylinositol-3 kinase and Akt Is required for antibody-mediated effects on p27, cyclin D1, and antitumor action. Cancer Res 62: 4132-4141.
52. Yamamoto T, Ikawa S, Akiyama T, Semba K, Nomura N, Miyajima N et al. (1986). Similarity of protein encoded by the human c-erb-B-2 gene to epidermal growth factor receptor. Nature 319: 230-234. (Pubitemid 16128786)
53. Yu Q, Geng Y, Sicinski P. (2001). Specific protection against breast cancers by cyclin D1 ablation. Nature 411: 1017-1021.