Regulator of G-protein signaling 3 isoform 1 (PDZ-RGS3) enhances canonical Wnt signaling and promotes epithelial mesenchymal transition

Journal of Biological Chemistry

Volumn 287, Issue 40, 2012, Pages 33480-33487

  Shi, Chong Shan ^a   Huang, Ning Na ^a   Kehrl, John H ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOMATOUS POLYPOSIS COLI; BIOCHEMICAL CHANGES; CANONICAL WNT SIGNALING; CELL DIFFERENTIATION; CELL-FATE; CELLULAR PROCESS; DOMAIN-CONTAINING PROTEINS; EPITHELIAL-MESENCHYMAL TRANSITION; G PROTEIN; ISOFORMS; OVER-EXPRESSION; RECEPTOR COMPLEX; WNT SIGNALING;

CELL MEMBRANES; PROTEINS;

SIGNALING;

BETA CATENIN; GLYCOGEN SYNTHASE KINASE 3BETA; PROTEIN PDZ RGS3; RGS PROTEIN; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR SNAIL1; UNCLASSIFIED DRUG; WNT3A PROTEIN;

ANIMAL CELL; ARTICLE; CATALYSIS; CELL STRAIN; CELL STRAIN HEK293; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; IN VITRO STUDY; MORPHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

ACTINS; ANIMALS; BETA CATENIN; CATALYTIC DOMAIN; CELL LINE; DOGS; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; GTP-BINDING PROTEINS; GTPASE-ACTIVATING PROTEINS; HEK293 CELLS; HUMANS; MODELS, BIOLOGICAL; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS C-MYC; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; WNT PROTEINS;

EID: 84866913428     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.361873     Document Type: Article

References (34)

1. Huelsken, J., and Behrens, J. (2002) The Wnt signaling pathway. J. Cell Sci. 115, 3977-3988
2. Miller, J. R., Hocking, A. M., Brown, J. D., and Moon, R. T. (1999) Mechanism and function of signal transduction by the Wnt/β-catenin and Wnt/Ca2+ pathways. Oncogene 18, 7860-7872 (Pubitemid 30066232)
3. Veeman, M. T., Axelrod, J. D., and Moon, R. T. (2003) A second canon: functions and mechanisms of β-catenin-independent Wnt signaling. Dev. Cell 5, 367-377 (Pubitemid 37107667)
4. Li, V. S., Ng, S. S., Boersema, P. J., Low, T. Y., Karthaus, W. R., Gerlach, J. P., Mohammed, S., Heck, A. J., Maurice, M. M., Mahmoudi, T., and Clevers, H. (2012) Wnt signaling through inhibition of β-catenin degradation in an intact axin1 complex. Cell 149, 1245-1256
5. Gordon, M. D., and Nusse, R. (2006) Wnt signaling: multiple pathways, multiple receptors, and multiple transcription factors. J. Biol. Chem. 281, 22429-22433
6. Zhou, B. P., Deng, J., Xia, W., Xu, J., Li, Y. M., Gunduz, M., and Hung, M. C. (2004) Dual regulation of snail by GSK3β-mediated phosphorylation in control of epithelial-mesenchymal transition. Nat. Cell Biol. 6, 931-940 (Pubitemid 39359846)
7. Yook, J. I., Li, X. Y., Ota, I., Fearon, E. R., and Weiss, S. J. (2005) Wnt-dependent regulation of the E-cadherin repressor snail. J. Biol. Chem. 280, 11740-11748 (Pubitemid 40418488)
8. Yook, J. I., Li, X. Y., Ota, I., Hu, C., Kim, H. S., Kim, N. H., Cha, S. Y., Ryu, J. K., Choi, Y. J., Kim, J., Fearon, E. R., and Weiss, S. J. (2006) A Wnt-axin2- GSK3β cascade regulates snail1 activity in breast cancer cells. Nat. Cell Biol. 8, 1398-1406 (Pubitemid 44835115)
9. Lee, J. M., Dedhar, S., Kalluri, R., and Thompson, E. W. (2006) The epi-thelial- mesenchymal transition: new insights in signaling, development, and disease. J. Cell Biol. 172, 973-981
10. Zhou, B. P., and Hung, M. C. (2005) Wnt, hedgehog and snail: sister pathways that control by GSK3β and βTrCP in the regulation of metastasis. Cell Cycle 4, 772-776 (Pubitemid 41353827)
11. Scheel, C., and Weinberg, R. A. (2011) Phenotypic plasticity and epithelial-mesenchymal transitions in cancer and normal stem cells? Int. J. Cancer 129, 2310-2314
12. s-axin-β-catenin signaling axis. Science 310, 1504-1510
13. 13. Mol. Pharmacol. 70, 1461-1468
14. Kehrl, J. H. (1998) Heterotrimeric G-protein signaling: roles in immune function and fine-tuning by RGS proteins. Immunity 8, 1-10
15. Cho, H., and Kehrl, J. H. (2009) Regulation of immune function by G-protein- coupled receptors, trimeric G-proteins, and RGS proteins. Prog. Mol. Biol. Transl. Sci. 86, 249-298
16. Kehrl, J. H., Srikumar, D., Harrison, K., Wilson, G. L., and Shi, C. S. (2002) Additional 5′ exons in the RGS3 locus generate multiple mRNA transcripts, one of which accounts for the origin of human PDZ-RGS3. Genomics 79, 860-868 (Pubitemid 34595321)
17. Lu, Q., Sun, E. E., Klein, R. S., and Flanagan, J. G. (2001) Ephrin-B reverse signaling is mediated by a novel PDZ-RGS protein and selectively inhibits G-protein-coupled chemoattraction. Cell 105, 69-79 (Pubitemid 32323917)
18. Qiu, R., Wang, J., Tsark, W., and Lu, Q. (2010) Essential role of PDZ-RGS3 in the maintenance of neural progenitor cells. Stem Cells 28, 1602-1610
19. He, T. C., Sparks, A. B., Rago, C., Hermeking, H., Zawel, L., da Costa, L. T., Morin, P. J., Vogelstein, B., and Kinzler, K. W. (1998) Identification of c-Myc as a target of the APC pathway. Science 281, 1509-1512 (Pubitemid 28425575)
20. Yan, D., Wiesmann, M., Rohan, M., Chan, V., Jefferson, A. B., Guo, L., Sakamoto, D., Caothien, R. H., Fuller, J. H., Reinhard, C., Garcia, P. D., Randazzo, F. M., Escobedo, J., Fantl, W. J., and Williams, L. T. (2001) Elevated expression of axin2 and hnkd mRNA provides evidence that Wnt/β-catenin signaling is activated in human colon tumors. Proc. Natl. Acad. Sci. U.S.A. 98, 14973-14978 (Pubitemid 34013954)
21. Lustig, B., Jerchow, B., Sachs, M., Weiler, S., Pietsch, T., Karsten, U., van de Wetering, M., Clevers, H., Schlag, P. M., Birchmeier, W., and Behrens, J. (2002) Negative feedback loop of Wnt signaling through upregulation of conductin/axin2 in colorectal and liver tumors. Mol. Cell. Biol. 22, 1184-1193 (Pubitemid 34094854)
22. Jho, E. H., Zhang, T., Domon, C., Joo, C. K., Freund, J. N., and Costantini, F. (2002) Wnt/β-catenin/TCF signaling induces the transcription of axin2, a negative regulator of the signaling pathway. Mol. Cell Biol. 22, 1172-1183 (Pubitemid 34094853)
23. Tetsu, O., and McCormick, F. (1999) β-Catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398, 422-426 (Pubitemid 29180374)
24. Ikeda, S., Kishida, S., Yamamoto, H., Murai, H., Koyama, S., and Kikuchi, A. (1998) Axin, a negative regulator of the Wnt signaling pathway, forms a complex with GSK3β and β-catenin and promotes GSK3β-dependent phosphorylation of β-catenin. EMBO J. 17, 1371-1384 (Pubitemid 28105516)
25. Sakanaka, C., Weiss, J. B., and Williams, L. T. (1998) Bridging of β-catenin and glycogen synthase kinase 3β by axin and inhibition of β-catenin-mediated transcription. Proc. Natl. Acad. Sci. U.S.A. 95, 3020-3023 (Pubitemid 28135847)
26. Egger-Adam, D., and Katanaev, V. L. (2010) The trimeric G-protein Go inflicts a double impact on axin in the Wnt/Frizzled signaling pathway. Dev. Dyn. 239, 168-183
27. Koval, A., Purvanov, V., Egger-Adam, D., and Katanaev, V. L. (2011) Yellow submarine of the Wnt/Frizzled signaling: submerging from the Gprotein harbor to the targets. Biochem. Pharmacol. 82, 1311-1319
28. Deleted in proof
29. Deleted in proof
30. Deleted in proof
31. van Amerongen, R., Nawijn, M., Franca-Koh, J., Zevenhoven, J., van der Gulden, H., Jonkers, J., and Berns, A. (2005) FRAT is dispensable for canonical Wnt signaling in mammals. Genes Dev. 19, 425-430 (Pubitemid 40256273)
32. Freisinger, C. M., Fisher, R. A., and Slusarski, D. C. (2010) Regulator of G-protein signaling 3 modulates Wnt5b calcium dynamics and somite patterning. PLoS Genet. (2010) 6, e1001020
33. Louwette, S., Labarque, V., Wittevrongel, C., Thys, C., Metz, J., Gijsbers, R., Debyser, Z., Arnout, J., Van Geet, C., and Freson. K. (2012) Regulator of G-protein signaling 18 controls megakaryopoiesis and the cilia-mediated vertebrate mechanosensory system. FASEB J. 5, 2121-2136
34. Ooe, A., Kato, K., and Noguchi, S. (2007) Possible involvement of CCT5, RGS3, and YKT6 genes up-regulated in p53-mutated tumors in resistance to docetaxel in human breast cancers. Breast Cancer Res. Treat. 101, 305-315 (Pubitemid 46169885)