14-3-3τ promotes breast cancer invasion and metastasis by inhibiting RhoGDIα

Molecular and Cellular Biology

Volumn 34, Issue 14, 2014, Pages 2635-2649

  Xiao, Yang ^a   Lin, Vivian Y ^a,c   Ke, Shi ^a   Lin, Gregory E ^b   Lin, Fang Tsyr ^a   Lin, Weei Chin ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b Rice University   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR; PHOSPHOPROTEIN; PROTEIN CDC42; RAC1 PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHO GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR 1; RHO KINASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SERINE; STRATIFIN; PROTEIN 14 3 3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST CANCER CELL LINE; CANCER INHIBITION; CANCER SURVIVAL; CARCINOGENESIS; CELL ADHESION; CELL MOTILITY; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME ACTIVATION; ENZYME INHIBITION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; MCF 7 CELL LINE; METASTASIS; METASTASIS INHIBITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN FUNCTION; TUMOR INVASION; ANIMAL; BREAST TUMOR; EXPERIMENTAL MAMMARY NEOPLASM; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; METABOLISM; NUDE MOUSE; PATHOLOGY; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

14-3-3 PROTEINS; ANIMALS; BREAST NEOPLASMS; CELL ADHESION; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HUMANS; MAMMARY NEOPLASMS, EXPERIMENTAL; MCF-7 CELLS; MICE; MICE, NUDE; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; PHOSPHORYLATION; RHO GTP-BINDING PROTEINS; RHO GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR ALPHA; SIGNAL TRANSDUCTION;

EID: 84902668709     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00076-14     Document Type: Article

References (48)

1. Gardino AK, Yaffe MB. 2011. 14-3-3 proteins as signaling integration points for cell cycle control and apoptosis. Semin. Cell Dev. Biol. 22:688-695. http://dx.doi.org/10.1016/j.semcdb.2011.09.008.
2. Fu H, Subramanian RR, Masters SC. 2000. 14-3-3 proteins: structure, function, and regulation. Annu. Rev. Pharmacol. Toxicol. 40:617-647. http://dx.doi.org/10.1146/annurev.pharmtox.40.1.617.
3. Wang B, Liu K, Lin HY, Bellam N, Ling S, Lin WC. 2010. 14-3-3ß regulates ubiquitin-independent proteasomal degradation of p21, a novel mechanism of p21 downregulation in breast cancer. Mol. Cell. Biol. 30:1508-1527. http://dx.doi.org/10.1128/MCB.01335-09.
4. Martin D, Brown-Luedi M, Chiquet-Ehrismann R. 2003. Tenascin-C signaling through induction of 14-3-3 tau. J. Cell Biol. 160:171-175. http://dx.doi.org/10.1083/jcb.200206109.
5. Jahkola T, Toivonen T, Virtanen I, von Smitten K, Nordling S, von Boguslawski K, Haglund C, Nevanlinna H, Blomqvist C. 1998. Tenascin-C expression in invasion border of early breast cancer: a predictor of local and distant recurrence. Br. J. Cancer 78:1507-1513. http://dx.doi.org/10.1038/bjc.1998.714.
6. Siegel R, Naishadham D, Jemal A. 2013. Cancer statistics, 2013. CA Cancer J. Clin. 63:11-30. http://dx.doi.org/10.3322/caac.21166.
7. DeSantis C, Ma J, Bryan L, Jemal A. 2013. Breast cancer statistics, 2013. CA Cancer J. Clin. 64:52-62. http://dx.doi.org/10.3322/caac.21203.
8. O'Shaughnessy J. 2005. Extending survival with chemotherapy in metastatic breast cancer. Oncologist 10(Suppl 3):S20-S29. http://dx.doi.org/10.1634/theoncologist.10-90003-20.
9. Vanharanta S, Massague J. 2013. Origins of metastatic traits. Cancer Cell 24:410-421. http://dx.doi.org/10.1016/j.ccr.2013.09.007.
10. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, Savagner P, Gitelman I, Richardson A, Weinberg RA. 2004. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117:927-939. http://dx.doi.org/10.1016/j.cell.2004.06.006.
11. Alan JK, Lundquist EA. 2013. Mutationally activated Rho GTPases in cancer. Small GTPases 4:159-163. http://dx.doi.org/10.4161/sgtp.26530.
12. Wertheimer E, Gutierrez-Uzquiza A, Rosemblit C, Lopez-Haber C, Sosa MS, Kazanietz MG. 2012. Rac signaling in breast cancer: a tale of GEFs and GAPs. Cell Signal. 24:353-362. http://dx.doi.org/10.1016/j.cellsig.2011.08.011.
13. Burridge K, Wennerberg K. 2004. Rho and Rac take center stage. Cell 116:167-179. http://dx.doi.org/10.1016/S0092-8674(04)00003-0.
14. Parri M, Chiarugi P. 2010. Rac and Rho GTPases in cancer cell motility control. Cell Commun. Signal. 8:23. http://dx.doi.org/10.1186/1478-811X-8-23.
15. Olofsson B. 1999. Rho guanine dissociation inhibitors: pivotal molecules in cellular signalling. Cell Signal. 11:545-554. http://dx.doi.org/10.1016/S0898-6568(98)00063-1.
16. DerMardirossian C, Bokoch GM. 2005. GDIs: central regulatory molecules in Rho GTPase activation. Trends Cell Biol. 15:356-363. http://dx.doi.org/10.1016/j.tcb.2005.05.001.
17. Barone I, Brusco L, Gu G, Selever J, Beyer A, Covington KR, Tsimelzon A, Wang T, Hilsenbeck SG, Chamness GC, Ando S, Fuqua SA. 2011. Loss of Rho GDIalpha and resistance to tamoxifen via effects on estrogen receptor alpha. J. Natl. Cancer Inst. 103:538-552. http://dx.doi.org/10.1093/jnci/djr058.
18. Gildea JJ, Seraj MJ, Oxford G, Harding MA, Hampton GM, Moskaluk CA, Frierson HF, Conaway MR, Theodorescu D. 2002. RhoGDI2 is an invasion and metastasis suppressor gene in human cancer. Cancer Res. 62:6418-6423. http://cancerres.aacrjournals.org/content/62/22/6418.
19. Harding MA, Theodorescu D. 2007. RhoGDI2: a new metastasis suppressor gene: discovery and clinical translation. Urol. Oncol. 25:401-406. http://dx.doi.org/10.1016/j.urolonc.2007.05.006.
20. Wang B, Liu K, Lin FT, Lin WC. 2004. A role for 14-3-3 tau in E2F1 stabilization and DNA damage-induced apoptosis. J. Biol. Chem. 279:54140-54152. http://dx.doi.org/10.1074/jbc. M410493200.
21. Xu J, Lai YJ, Lin WC, Lin FT. 2004. TRIP6 enhances lysophosphatidic acid-induced cell migration by interacting with the lysophosphatidic acid 2 receptor. J. Biol. Chem. 279:10459-10468. http://dx.doi.org/10.1074/jbc. M311891200.
22. Ke S, Wang W, Qiu X, Zhang F, Yustein JT, Cameron AG, Zhang S, Yu D, Zou C, Gao X, Lin J, Yallampalli S, Li M. 2013. Multiple targetspecific molecular agents for detection and image analysis of breast cancer characteristics in mice. Curr. Mol. Med. 13:446-458. http://dx.doi.org/10.2174/1566524011313030014.
23. Liu K, Bellam N, Lin HY, Wang B, Stockard CR, Grizzle WE, Lin WC. 2009. Regulation of p53 by TopBP1: a potential mechanism for p53 inactivation in cancer. Mol. Cell. Biol. 29:2673-2693. http://dx.doi.org/10.1128/MCB.01140-08.
24. Schofield AV, Bernard O. 2013. Rho-associated coiled-coil kinase (ROCK) signaling and disease. Crit. Rev. Biochem. Mol. Biol. 48:301-316. http://dx.doi.org/10.3109/10409238.2013.786671.
25. Chuang HH, Yang CH, Tsay YG, Hsu CY, Tseng LM, Chang ZF, Lee HH. 2012. ROCKII Ser1366 phosphorylation reflects the activation status. Biochem. J. 443:145-151. http://dx.doi.org/10.1042/BJ20111839.
26. DerMardirossian C, Schnelzer A, Bokoch GM. 2004. Phosphorylation of RhoGDI by Pak1 mediates dissociation of Rac GTPase. Mol. Cell 15:117-127. http://dx.doi.org/10.1016/j.molcel.2004.05.019.
27. Qiao J, Holian O, Lee BS, Huang F, Zhang J, Lum H. 2008. Phosphor-ylation of GTP dissociation inhibitor by PKA negatively regulates RhoA. Am. J. Physiol. Cell Physiol. 295:C1161-C1168. http://dx.doi.org/10.1152/ajpcell.00139.2008.
28. Liu P, Morrison C, Wang L, Xiong D, Vedell P, Cui P, Hua X, Ding F, Lu Y, James M, Ebben JD, Xu H, Adjei AA, Head K, Andrae JW, Tschannen MR, Jacob H, Pan J, Zhang Q, Van den Bergh F, Xiao H, Lo KC, Patel J, Richmond T, Watt MA, Albert T, Selzer R, Anderson M, Wang J, Wang Y, Starnes S, Yang P, You M. 2012. Identification of somatic mutations in non-small cell lung carcinomas using whole-exome sequencing. Carcinogenesis 33:1270-1276. http://dx.doi.org/10.1093/carcin/bgs148.
29. Lochhead PA, Wickman G, Mezna M, Olson MF. 2010. Activating ROCK1 somatic mutations in human cancer. Oncogene 29:2591-2598. http://dx.doi.org/10.1038/onc.2010.3.
30. Kamai T, Tsujii T, Arai K, Takagi K, Asami H, Ito Y, Oshima H. 2003. Significant association of Rho/ROCK pathway with invasion and metastasis of bladder cancer. Clin. Cancer Res. 9:2632-2641. http://clincancerres.aacrjournals.org/content/9/7/2632.
31. Kamai T, Yamanishi T, Shirataki H, Takagi K, Asami H, Ito Y, Yoshida K. 2004. Overexpression of RhoA, Rac1, and Cdc42 GTPases is associated with progression in testicular cancer. Clin. Cancer Res. 10:4799-4805. http://dx.doi.org/10.1158/1078-0432.CCR-0436-03.
32. Qi W, Liu X, Qiao D, Martinez JD. 2005. Isoform-specific expression of 14-3-3 proteins in human lung cancer tissues. Int. J. Cancer 113:359-363. http://dx.doi.org/10.1002/ijc.20492.
33. Desmedt C, Piette F, Loi S, Wang Y, Lallemand F, Haibe-Kains B, Viale G, Delorenzi M, Zhang Y, d'Assignies MS, Bergh J, Lidereau R, Ellis P, Harris AL, Klijn JG, Foekens JA, Cardoso F, Piccart MJ, Buyse M, Sotiriou C. 2007. Strong time dependence of the 76-gene prognostic signature for node-negative breast cancer patients in the TRANSBIG multicenter independent validation series. Clin. Cancer Res. 13:3207-3214. http://dx.doi.org/10.1158/1078-0432.CCR-06-2765.
34. Loi S, Haibe-Kains B, Desmedt C, Lallemand F, Tutt AM, Gillet C, Ellis P, Harris A, Bergh J, Foekens JA, Klijn JG, Larsimont D, Buyse M, Bontempi G, Delorenzi M, Piccart MJ, Sotiriou C. 2007. Definition of clinically distinct molecular subtypes in estrogen receptor-positive breast carcinomas through genomic grade. J. Clin. Oncol. 25:1239-1246. http://dx.doi.org/10.1200/JCO.2006.07.1522.
35. Minn AJ, Gupta GP, Siegel PM, Bos PD, Shu W, Giri DD, Viale A, Olshen AB, Gerald WL, Massague J. 2005. Genes that mediate breast cancer metastasis to lung. Nature 436:518-524. http://dx.doi.org/10.1038/nature03799.
36. Schmidt M, Bohm D, von Torne C, Steiner E, Puhl A, Pilch H, Lehr HA, Hengstler JG, Kolbl H, Gehrmann M. 2008. The humoral immune system has a key prognostic impact in node-negative breast cancer. Cancer Res. 68:5405-5413. http://dx.doi.org/10.1158/0008-5472.CAN-07-5206.
37. van't Veer LJ, Dai H, van de Vijver MJ, He YD, Hart AA, Mao M, Peterse HL, van der Kooy K, Marton MJ, Witteveen AT, Schreiber GJ, Kerkhoven RM, Roberts C, Linsley PS, Bernards R, Friend SH. 2002. Gene expression profiling predicts clinical outcome of breast cancer. Nature 415:530-536. http://dx.doi.org/10.1038/415530a.
38. van de Vijver MJ, He YD, van't Veer LJ, Dai H, Hart AA, Voskuil DW, Schreiber GJ, Peterse JL, Roberts C, Marton MJ, Parrish M, Atsma D, Witteveen A, Glas A, Delahaye L, van der Velde T, Bartelink H, Rodenhuis S, Rutgers ET, Friend SH, Bernards R. 2002. A geneexpression signature as a predictor of survival in breast cancer. N. Engl. J. Med. 347:1999-2009. http://dx.doi.org/10.1056/NEJMoa021967.
39. Hoffman GR, Nassar N, Cerione RA. 2000. Structure of the Rho family GTP-binding protein Cdc42 in complex with the multifunctional regulator RhoGDI. Cell 100:345-356. http://dx.doi.org/10.1016/S0092-8674(00)80670-4.
40. Garcia-Mata R, Boulter E, Burridge K. 2011. The 'invisible hand': regulation of RHO GTPases by RHOGDIs. Nat. Rev. Mol. Cell Biol. 12:493-504. http://dx.doi.org/10.1038/nrm3153.
41. Alonso SR, Tracey L, Ortiz P, Perez-Gomez B, Palacios J, Pollan M, Linares J, Serrano S, Saez-Castillo AI, Sanchez L, Pajares R, Sanchez-Aguilera A, Artiga MJ, Piris MA, Rodriguez-Peralto JL. 2007. A highthroughput study in melanoma identifies epithelial-mesenchymal transition as a major determinant of metastasis. Cancer Res. 67:3450-3460. http://dx.doi.org/10.1158/0008-5472.CAN-06-3481.
42. Bergamaschi A, Frasor J, Borgen K, Stanculescu A, Johnson P, Rowland K, Wiley EL, Katzenellenbogen BS. 2013. 14-3-3Δ as a predictor of early time to recurrence and distant metastasis in hormone receptor-positive and -negative breast cancers. Breast Cancer Res. Treat. 137:689-696. http://dx.doi.org/10.1007/s10549-012-2390-0.
43. Neal CL, Yao J, Yang W, Zhou X, Nguyen NT, Lu J, Danes CG, Guo H, Lan KH, Ensor J, Hittelman W, Hung MC, Yu D. 2009. 14-3-3Δ overexpression defines high risk for breast cancer recurrence and promotes cancer cell survival. Cancer Res. 69:3425-3432. http://dx.doi.org/10.1158/0008-5472.CAN-08-2765.
44. Lu J, Guo H, Treekitkarnmongkol W, Li P, Zhang J, Shi B, Ling C, Zhou X, Chen T, Chiao PJ, Feng X, Seewaldt VL, Muller WJ, Sahin A, Hung MC, Yu D. 2009. 14-3-3Δ cooperates with ErbB2 to promote ductal carcinoma in situ progression to invasive breast cancer by inducing epithelial-mesenchymal transition. Cancer Cell 16:195-207. http://dx.doi.org/10.1016/j.ccr.2009.08.010.
45. Song Y, Yang Z, Ke Z, Yao Y, Hu X, Sun Y, Li H, Yin J, Zeng C. 2012. Expression of 14-3-3gamma in patients with breast cancer: correlation with clinicopathological features and prognosis. Cancer Epidemiol. 36:533-536. http://dx.doi.org/10.1016/j.canep.2012.05.003.
46. Ferguson AT, Evron E, Umbricht CB, Pandita TK, Chan TA, Hermeking H, Marks JR, Lambers AR, Futreal PA, Stampfer MR, Sukumar S. 2000. High frequency of hypermethylation at the 14-3-3 sigma locus leads to gene silencing in breast cancer. Proc. Natl. Acad. Sci. U. S. A. 97:6049-6054. http://dx.doi.org/10.1073/pnas.100566997.
47. Umbricht CB, Evron E, Gabrielson E, Ferguson A, Marks J, Sukumar S. 2001. Hypermethylation of 14-3-3 sigma (stratifin) is an early event in breast cancer. Oncogene 20:3348-3353. http://dx.doi.org/10.1038/sj.onc.1204438.
48. Lai YJ, Chen CS, Lin WC, Lin FT. 2005. c-Src-mediated phosphorylation of TRIP6 regulates its function in lysophosphatidic acid-induced cell migration. Mol. Cell. Biol. 25:5859-5868. http://dx.doi.org/10.1128/MCB.25.14.5859-5868.2005.