Inhibition of CCN6 (Wnt-1-induced signaling protein 3) down-regulates E-cadherin in the breast epithelium through induction of snail and ZEB1

American Journal of Pathology

Volumn 172, Issue 4, 2008, Pages 893-904

  Huang, Wei ^a   Zhang, Yanhong ^a   Varambally, Sooryanarayana ^a   Chinnaiyan, Arul M ^a   Banerjee, Mousumi ^a   Merajver, Sofia D ^a,b   Kleer, Celina G ^a,b  

^a UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE RICH PROTEIN 6; MESSENGER RNA; PROTEIN ZEB1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SNAIL; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; UVOMORULIN;

ADULT; AGED; ARTICLE; AXILLARY LYMPH NODE; BREAST CARCINOMA; BREAST EPITHELIUM; CANCER INVASION; CELL CULTURE; CELL DIFFERENTIATION; CELL LINE; CELL STRAIN HEK293; CHROMATIN IMMUNOPRECIPITATION; CULTURE MEDIUM; DISEASE ASSOCIATION; DOWN REGULATION; E BOX ELEMENT; HUMAN; HUMAN CELL; HUMAN TISSUE; LYMPH NODE METASTASIS; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; RNA INTERFERENCE; UPREGULATION;

EID: 42049085877     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.2353/ajpath.2008.070899     Document Type: Article

References (39)

1. Jemal A, Murray T, Samuels A, Ghafoor A, Ward E, Thun MJ: Cancer statistics, 2003. CA Cancer J Clin 2003, 53:5-26
2. Battaglia C, Salani G, Consolandi C, Bernardi LR, De Bellis G: Analysis of DNA microarrays by non-destructive fluorescent staining using SYBR green II [In Process Citation]. Biotechniques 2000, 29:78-81
3. Batlle E, Sancho E, Franci C, Dominguez D, Monfar M, Baulida J, Garcia De Herreros A: The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat Cell Biol 2000, 2:84-89
4. Cano A, Perez-Moreno MA, Rodrigo I, Locascio A, Blanco MJ, del Barrio MG, Portillo F, Nieto MA: The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol 2000, 2:76-83
5. Hajra KM, Chen DY, Fearon ER: The SLUG zinc-finger protein represses E-cadherin in breast cancer. Cancer Res 2002, 62:1613-1618
6. Yook JI, Li XY, Ota I, Fearon ER, Weiss SJ: Wnt-dependent regulation of the E-cadherin repressor snail. J Biol Chem 2005, 280:11740-11748
7. Zhou BP, Deng J, Xia W, Xu J, Li YM, Gunduz M, Hung MC: Dual regulation of Snail by GSK-3beta-mediated phosphorylation in control of epithelial-mesenchymal transition. Nat Cell Biol 2004, 6:931-940
8. van Golen KL, Davies S, Wu ZF, Wang Y, Bucana CD, Root H, Chandrasekharappa S, Strawderman M, Ethier SP, Merajver SD: A novel putative low-affinity insulin-like growth factor-binding protein, LIBC (lost in inflammatory breast cancer), and RhoC GTPase correlate with the inflammatory breast cancer phenotype. Clin Cancer Res 1999, 5:2511-2519
9. Kleer CG, Zhang Y, Pan Q, Merajver SD: WISP3 (CCN6) is a secreted tumor-suppressor protein that modulates IGF signaling in inflammatory breast cancer. Neoplasia 2004, 6:179-185
10. Kleer CG, Zhang Y, Pan Q, Gallagher G, Wu M, Wu ZF, Merajver SD: WISP3 and RhoC guanosine triphosphatase cooperate in the development of inflammatory breast cancer. Breast Cancer Res 2004, 6:R110-R115
11. Kleer CG, Zhang Y, Pan Q, van Golen KL, Wu ZF, Livant D, Merajver SD: WISP3 is a novel tumor suppressor gene of inflammatory breast cancer. Oncogene 2002, 21:3172-3180
12. Zhang Y, Pan Q, Zhong H, Merajver SD, Kleer CG: Inhibition of CCN6 (WISP3) expression promotes neoplastic progression and enhances the effects of insulin-like growth factor-1 on breast epithelial cells. Breast Cancer Res 2005, 7:R1080-R1089
13. Kleer CG, Cao Q, Varambally S, Shen R, Ota I, Tomlins SA, Ghosh D, Sewalt RG, Otte AP, Hayes DF, Sabel MS, Livant D, Weiss SJ, Rubin MA, Chinnaiyan AM: EZH2 is a marker of aggressive breast cancer and promotes neoplastic transformation of breast epithelial cells. Proc Natl Acad Sci USA 2003, 100:11606-11611
14. Elston EW, Ellis IO: Method for grading breast cancer. J Clin Pathol 1993, 46:189-190
15. Kowalski PJ, Rubin MA, Kleer CG: E-cadherin expression in primary carcinomas of the breast and its distant metastases. Breast Cancer Res 2003, 5:R217-R222
16. Kleer CG, Griffith KA, Sabel MS, Gallagher G, van Golen KL, Wu ZF, Merajver SD: RhoC-GTPase is a novel tissue biomarker associated with biologically aggressive carcinomas of the breast. Breast Cancer Res Treat 2005, 93:101-110
17. Witkiewicz AK, Varambally S, Shen R, Mehra R, Sabel MS, Ghosh D, Chinnaiyan AM, Rubin MA, Kleer CG: Alpha-methylacyl-CoA race-mase protein expression is associated with the degree of differentiation in breast cancer using quantitative image analysis. Cancer Epidemiol Biomarkers Prev 2005, 14:1418-1423
18. Camp RL, Dolled-Filhart M, King BL, Rimm DL: Quantitative analysis of breast cancer tissue microarrays shows that both high and normal levels of HER2 expression are associated with poor outcome. Cancer Res 2003, 63:1445-1448
19. Hajra KM, Ji X, Fearon ER: Extinction of E-cadherin expression in breast cancer via a dominant repression pathway acting on proximal promoter elements. Oncogene 1999, 18:7274-7279
20. Perbal B: NOV (nephroblastoma overexpressed) and the CCN family of genes: structural and functional issues. Mol Pathol 2001, 54:57-79
21. Brigstock DR, Goldschmeding R, Katsube KI, Lam SC, Lau LF, Lyons K, Naus C, Perbal B, Riser B, Takigawa M, Yeger H: Proposal for a unified CCN nomenclature. Mol Pathol 2003, 56:127-128
22. Lin CG, Chen CC, Leu SJ, Grzeszkiewicz TM, Lau LF: Integrin-dependent Functions of the angiogenic inducer NOV (CCN3): implication in wound healing. J Biol Chem 2005, 280:8229-8237
23. Lin CG, Leu SJ, Chen N, Tebeau CM, Lin SX, Yeung CY, Lau LF: CCN3 (NOV) is a novel angiogenic regulator of the CCN protein family. J Biol Chem 2003, 278:24200-24208
24. Lau LF, Lam SC: The CCN family of angiogenic regulators: the integrin connection. Exp Cell Res 1999, 248:44-57
25. Sakamoto K, Yamaguchi S, Ando R, Miyawaki A, Kabasawa Y, Takagi M, Li CL, Perbal B, Katsube K: The nephroblastoma overexpressed gene (NOV/ccn3) protein associates with Notch1 extracellular domain and inhibits myoblast differentiation via Notch signaling pathway. J Biol Chem 2002, 277:29399-29405
26. Li CL, Martinez V, He B, Lombet A, Perbal B: A role for CCN3 (NOV) in calcium signalling. Mol Pathol 2002, 55:250-261
27. Perbal B, Martinerie C, Sainson R, Werner M, He B, Roizman B: The C-terminal domain of the regulatory protein NOVH is sufficient to promote interaction with fibulin 1C: a clue for a role of NOVH in cell-adhesion signaling. Proc Natl Acad Sci USA 1999, 96:869-874
28. Benini S, Perbal B, Zambelli D, Colombo MP, Manara MC, Serra M, Parenza M, Martinez V, Picci P, Scotlandi K: In Ewing's sarcoma CCN3(NOV) inhibits proliferation while promoting migration and invasion of the same cell type. Oncogene 2005, 24:4349-4361
29. Manara MC, Perbal B, Benini S, Strammiello R, Cerisano V, Perdichizzi S, Serra M, Astolfi A, Bertoni F, Alami J, Yeger H, Picci P, Scotlandi K: The expression of ccn3(nov) gene in musculoskeletal tumors. Am J Pathol 2002, 160:849-859
30. Cowin P, Rowlands TM, Hatsell SJ: Cadherins and catenins in breast cancer. Curr Opin Cell Biol 2005, 17:499-508
31. Eger A, Aigner K, Sonderegger S, Dampier B, Oehler S, Schreiber M, Berx G, Cano A, Beug H, Foisner R: DeltaEF1 is a transcriptional repressor of E-cadherin and regulates epithelial plasticity in breast cancer cells. Oncogene 2005, 24:2375-2385
32. Moody SE, Perez D, Pan TC, Sarkisian CJ, Portocarrero CP, Sterner CJ, Notorfrancesco KL, Cardiff RD, Chodosh LA: The transcriptional repressor Snail promotes mammary tumor recurrence. Cancer Cell 2005, 8:197-209
33. Aigner K, Descovich L, Mikula M, Sultan A, Dampier B, Bonne S, van Roy F, Mikulits W, Schreiber M, Brabletz T, Sommergruber W, Schweifer N, Wernitznig A, Beug H, Foisner R, Eger A: The transcription factor ZEB1 (deltaEF1) represses Plakophilin 3 during human cancer progression. FEBS Lett 2007, 581:1617-1624
34. Peinado H, Olmeda D, Cano A: Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat Rev Cancer 2007, 7:415-428
35. Bachelder RE, Yoon SO, Franci C, de Herreros AG, Mercurio AM: Glycogen synthase kinase-3 is an endogenous inhibitor of Snail transcription: implications for the epithelial-mesenchymal transition. J Cell Biol 2005, 168:29-33
36. Yang Z, Rayala S, Nguyen D, Vadlamudi RK, Chen S, Kumar R: Pak1 phosphorylation of snail, a master regulator of epithelial-to-mesenchyme transition, modulates snail's subcellular localization and functions. Cancer Res 2005, 65:3179-3184
37. Yook JI, Li XY, Ota I, Hu C, Kim HS, Kim NH, Cha SY, Ryu JK, Choi YJ, Kim J, Fearon ER, Weiss SJ: A Wnt-Axin2-GSK3beta cascade regulates Snail1 activity in breast cancer cells. Nat Cell Biol 2006, 8:1398-1406
38. Pennica D, Swanson TA, Welsh JW, Roy MA, Lawrence DA, Lee J, Brush J, Taneyhill LA, Deuel B, Lew M, Watanabe C, Cohen RL, Melhem MF, Finley GG, Quirke P, Goddard AD, Hillan KJ, Gurney AL, Botstein D, Levine AJ: WISP genes are members of the connective tissue growth factor family that are up-regulated in wnt-1-transformed cells and aberrantly expressed in human colon tumors. Proc Natl Acad Sci USA 1998, 95:14717-14722
39. Strathdee G: Epigenetic versus genetic alterations in the inactivation of E-cadherin. Semin Cancer Biol 2002, 12:373-379