Slug regulates E-cadherin repression via p19Arf in prostate tumorigenesis

Molecular Oncology

Volumn 8, Issue 7, 2014, Pages 1355-1364

  Xie, Yingqiu ^a   Liu, Shenji ^a   Lu, Wenfu ^a   Yang, Qing ^a   Williams, Kieosha D ^a   Binhazim, Awadh A ^a   Carver, Brett S ^b   Matusik, Robert J ^c   Chen, Zhenbang ^a  

^a MEHARRY MEDICAL COLLEGE   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Mouse model; Prostate cancer; SLUG; SUMO1

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN P53; SHORT HAIRPIN RNA; SUMO 1 PROTEIN; TRANSCRIPTION FACTOR SLUG; UVOMORULIN; CADHERIN; CDKN2A PROTEIN, MOUSE; CYCLIN DEPENDENT KINASE INHIBITOR 2A; SNAIL FAMILY TRANSCRIPTION FACTORS; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL; CANCER MODEL; CARCINOGENESIS; EPITHELIAL MESENCHYMAL TRANSITION; GENOTYPE; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; PROSTATE CANCER; TISSUE MICROARRAY; WESTERN BLOTTING; ANIMAL; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENETICS; HUMAN; METABOLISM; PATHOLOGY; PROSTATE; PROSTATE TUMOR;

ANIMALS; CADHERINS; CYCLIN-DEPENDENT KINASE INHIBITOR P16; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKOUT TECHNIQUES; HUMANS; MALE; MICE; PROSTATE; PROSTATIC NEOPLASMS; SUMO-1 PROTEIN; TRANSCRIPTION FACTORS;

EID: 84908508684     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2014.05.006     Document Type: Article

References (38)

1. Abida W.M., Gu W. p53-Dependent and p53-independent activation of autophagy by ARF. Cancer Res. 2008, 68:352-357.
2. Bardeesy N., Aguirre A.J., Chu G.C., Cheng K.H., Lopez L.V., Hezel A.F., et al. Both p16(Ink4a) and the p19(Arf)-p53 pathway constrain progression of pancreatic adenocarcinoma in the mouse. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:5947-5952.
3. Cano A., Perez-Moreno M.A., Rodrigo I., Locascio A., Blanco M.J., del Barrio M.G., et al. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat. Cell Biol. 2000, 2:76-83.
4. Cantley L.C., Neel B.G. New insights into tumor suppression: PTEN suppresses tumor formation by restraining the phosphoinositide 3-kinase/AKT pathway. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:4240-4245.
5. Chang C.J., Chao C.H., Xia W., Yang J.Y., Xiong Y., Li C.W., et al. p53 regulates epithelial-mesenchymal transition and stem cell properties through modulating miRNAs. Nat. Cell Biol. 2011, 13:317-323.
6. Chen D., Shan J., Zhu W.G., Qin J., Gu W. Transcription-independent ARF regulation in oncogenic stress-mediated p53 responses. Nature 2010, 464:624-627.
7. Chen Z., Carracedo A., Lin H.K., Koutcher J.A., Behrendt N., Egia A., et al. Differential p53-independent outcomes of p19(Arf) loss in oncogenesis. Sci. Signal. 2009, 2:ra44.
8. Chen Z., Trotman L.C., Shaffer D., Lin H.K., Dotan Z.A., Niki M., et al. Crucial role of p53-dependent cellular senescence in suppression of Pten-deficient tumorigenesis. Nature 2005, 436:725-730.
9. Churchman M.L., Roig I., Jasin M., Keeney S., Sherr C.J. Expression of Arf tumor suppressor in spermatogonia facilitates meiotic progression in male germ cells. PLoS Genet. 2011, 7:e1002157.
10. den Besten W., Kuo M.L., Tago K., Williams R.T., Sherr C.J. Ubiquitination of, and sumoylation by, the Arf tumor suppressor. Isr. Med. Assoc. J. 2006, 8:249-251.
11. Dubrovska A., Kim S., Salamone R.J., Walker J.R., Maira S.M., Garcia-Echeverria C., et al. The role of PTEN/Akt/PI3K signaling in the maintenance and viability of prostate cancer stem-like cell populations. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:268-273.
12. Geiss-Friedlander R., Melchior F. Concepts in sumoylation: a decade on. Nat. Rev. Mol. Cell Biol. 2007, 8:947-956.
13. Guo F., Gao Y., Wang L., Zheng Y. p19Arf-p53 tumor suppressor pathway regulates cell motility by suppression of phosphoinositide 3-kinase and Rac1 GTPase activities. J.Biol. Chem. 2003, 278:14414-14419.
14. Ha L., Ichikawa T., Anver M., Dickins R., Lowe S., Sharpless N.E., et al. ARF functions as a melanoma tumor suppressor by inducing p53-independent senescence. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:10968-10973.
15. Hajra K.M., Chen D.Y., Fearon E.R. The SLUG zinc-finger protein represses E-cadherin in breast cancer. Cancer Res. 2002, 62:1613-1618.
16. Humbey O., Pimkina J., Zilfou J.T., Jarnik M., Dominguez-Brauer C., Burgess D.J., et al. The ARF tumor suppressor can promote the progression of some tumors. Cancer Res. 2008, 68:9608-9613.
17. Ji H., Wang J., Nika H., Hawke D., Keezer S., Ge Q., et al. EGF-induced ERK activation promotes CK2-mediated disassociation of alpha-catenin from beta-catenin and transactivation of beta-catenin. Mol. Cell 2009, 36:547-559.
18. Kamijo T., Bodner S., van de Kamp E., Randle D.H., Sherr C.J. Tumor spectrum in ARF-deficient mice. Cancer Res. 1999, 59:2217-2222.
19. Kho C., Lee A., Jeong D., Oh J.G., Chaanine A.H., Kizana E., et al. SUMO1-dependent modulation of SERCA2a in heart failure. Nature 2011, 477:601-605.
20. Khoo C.M., Carrasco D.R., Bosenberg M.W., Paik J.H., Depinho R.A. Ink4a/Arf tumor suppressor does not modulate the degenerative conditions or tumor spectrum of the telomerase-deficient mouse. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:3931-3936.
21. Kuilman T., Michaloglou C., Mooi W.J., Peeper D.S. The essence of senescence. Genes Dev. 2010, 24:2463-2479.
22. Liu Y.N., Abou-Kheir W., Yin J.J., Fang L., Hynes P., Casey O., et al. Critical and reciprocal regulation of KLF4 and SLUG in transforming growth factor beta-initiated prostate cancer epithelial-mesenchymal transition. Mol. Cell. Biol. 2012, 32:941-953.
23. Liu Y.N., Liu Y., Lee H.J., Hsu Y.H., Chen J.H. Activated androgen receptor downregulates E-cadherin gene expression and promotes tumor metastasis. Mol. Cell. Biol. 2008, 28:7096-7108.
24. Lowe S.W., Sherr C.J. Tumor suppression by Ink4a-Arf: progress and puzzles. Curr. Opin. Genet. Dev. 2003, 13:77-83.
25. Lu W., Xie Y., Ma Y., Matusik R.J., Chen Z. ARF represses androgen receptor transactivation in prostate cancer. Mol. Endocrinol. 2013, 27:635-648.
26. Mulholland D.J., Kobayashi N., Ruscetti M., Zhi A., Tran L.M., Huang J., et al. Pten loss and RAS/MAPK activation cooperate to promote EMT and metastasis initiated from prostate cancer stem/progenitor cells. Cancer Res. 2012, 72:1878-1889.
27. Pourmand G., Ziaee A.A., Abedi A.R., Mehrsai A., Alavi H.A., Ahmadi A., et al. Role of PTEN gene in progression of prostate cancer. Urol. J. 2007, 4:95-100.
28. Rodriguez F.J., Lewis-Tuffin L.J., Anastasiadis P.Z. E-cadherin's dark side: possible role in tumor progression. Biochim. Biophys. Acta 2012, 1826:23-31.
29. Sharpless N.E., Ramsey M.R., Balasubramanian P., Castrillon D.H., DePinho R.A. The differential impact of p16(INK4a) or p19(ARF) deficiency on cell growth and tumorigenesis. Oncogene 2004, 23:379-385.
30. Shen M.M., Abate-Shen C. Molecular genetics of prostate cancer: new prospects for old challenges. Genes Dev. 2010, 24:1967-2000.
31. Shih J.Y., Yang P.C. The EMT regulator slug and lung carcinogenesis. Carcinogenesis 2011, 32:1299-1304.
32. Sun Y., Wang B.E., Leong K.G., Yue P., Li L., Jhunjhunwala S., et al. Androgen deprivation causes epithelial-mesenchymal transition in the prostate: implications for androgen-deprivation therapy. Cancer Res. 2012, 72:527-536.
33. Tago K., Chiocca S., Sherr C.J. Sumoylation induced by the Arf tumor suppressor: a p53-independent function. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:7689-7694.
34. Thomas G., Jacobs K.B., Yeager M., Kraft P., Wacholder S., Orr N., et al. Multiple loci identified in a genome-wide association study of prostate cancer. Nat. Genet. 2008, 40:310-315.
35. Whang Y.E., Wu X., Suzuki H., Reiter R.E., Tran C., Vessella R.L., et al. Inactivation of the tumor suppressor PTEN/MMAC1 in advanced human prostate cancer through loss of expression. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:5246-5250.
36. Yilmaz O.H., Valdez R., Theisen B.K., Guo W., Ferguson D.O., Wu H., et al. Pten dependence distinguishes haematopoietic stem cells from leukaemia-initiating cells. Nature 2006, 441:475-482.
37. Yu J., Zhang S.S., Saito K., Williams S., Arimura Y., Ma Y., et al. PTEN regulation by Akt-EGR1-ARF-PTEN axis. EMBO J. 2009, 28:21-33.
38. Zheng H., Ying H., Yan H., Kimmelman A.C., Hiller D.J., Chen A.J., et al. p53 and Pten control neural and glioma stem/progenitor cell renewal and differentiation. Nature 2008, 455:1129-1133.