GSK-3 kinases enhance calcineurin signaling by phosphorylation of RCNs

Genes and Development

Volumn 18, Issue 1, 2004, Pages 35-47

  Hilioti, Zoe ^a   Gallagher, Deirdre A ^a   Low Nam, Shalini T ^a   Ramaswamy, Priya ^a   Gajer, Pawel ^a   Kingsbury, Tami J ^a   Birchwood, Christine J ^a   Levchenko, Andre ^a   Cunningham, Kyle W ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Calcineurin; Calcium signaling; DSCR1; GSK 3; MCIP; Rcn1p

Indexed keywords

CALCINEURIN; CALCIUM ION; CALPAIN; DSCR1 PROTEIN; GLYCOGEN SYNTHASE KINASE 3; INHIBITOR 2 REGULATOR OF TYPE 1 PROTEIN PHOSPHATASE; INHIBITOR PROTEIN; MCIP1 PROTEIN; MCK1 PROTEIN; PHOSPHOPROTEIN PHOSPHATASE 1; PROTEIN; PROTEIN KINASE; RCN PROTEIN; RCN1 PROTEIN; SERINE; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CALCIUM SIGNALING; COMPUTER MODEL; CONSENSUS SEQUENCE; DOWN SYNDROME; NONHUMAN; OSCILLATION; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; YEAST CELL;

CALCINEURIN; CONSERVED SEQUENCE; GENE EXPRESSION REGULATION, FUNGAL; GLYCOGEN SYNTHASE KINASE 3; MODELS, BIOLOGICAL; MUTAGENESIS, SITE-DIRECTED; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHORYLATION; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 0347758480     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.1159204     Document Type: Article

References (52)

1. Antos, C.L., McKinsey, T.A., Frey, N., Kutschke, W., McAnally, J., Shelton, J.M., Richardson, J.A., Hill, J.A., and Olson, E.N. 2002. Activated glycogen synthase-3 β suppresses cardiac hypertrophy in vivo. Proc. Natl. Acad. Sci. 99: 907-912.
2. Beals, C.R., Sheridan, C.M., Turck, C.W., Gardner, P., and Crabtree, G.R. 1997. Nuclear export of NF-ATc enhanced by glycogen synthase kinase-3. Science 275: 1930-1934.
3. 2+ signaling is required for survival of endoplasmic reticulum stress in yeast. Mol. Biol. Cell 14: 4296-4305.
4. Causton, H.C., Ren, B., Koh, S.S., Harbison, C.T., Kanin, E., Jennings, E.G., Lee, T.I., True, H.L., Lander, E.S., and Young, R.A. 2001. Remodeling of yeast genome expression in response to environmental changes. Mol. Biol. Cell 12: 323-337.
5. Cohen, P.T. 2002. Protein phosphatase 1 - Targeted in many directions. J. Cell Sci. 115: 241-256.
6. Crabtree, G.R. and Olson, E.N. 2002. NFAT signaling: Choreographing the social lives of cells. Cell 109 Suppl: S67-S79.
7. 2+ ATPases. J. Cell Biol. 124: 351-363.
8. 2+ ATPases in yeast. Mol. Cell. Biol. 16: 2226-2237.
9. Eisen, M.B., Spellman, P.T., Brown, P.O., and Botstein, D. 1998. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. 95: 14863-14868.
10. Ermak, G., Morgan, T.E., and Davies, K.J. 2001. Chronic overexpression of the calcineurin inhibitory gene DSCR1 (Adapt78) is associated with Alzheimer's disease. J. Biol. Chem. 276: 38787-38794.
11. Fox, D.S. and Heitman, J. 2002. Good fungi gone bad: The corruption of calcineurin. Bioessays 24: 894-903.
12. Fuentes, J.J., Genescà, L., Kingsbury, T.J., Cunningham, K.W., Pérez-Riba, M., Estivill, X., and De La Luna, S. 2000. DSCR1, overexpressed in Down syndrome, is an inhibitor of calcineurin-mediated signaling pathways. Hum. Mol. Gen. 9: 1681-1690.
13. Gasch, A.P., Spellman, P.T., Kao, C.M., Carmel-Harel, O., Eisen, M.B., Storz, G., Botstein, D., and Brown, P.O. 2000. Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell 11: 4241-4257.
14. Genesca, L., Aubareda, A., Fuentes, J.J., Estivill, X., De La Luna, S., and Perez-Riba, M. 2003. Phosphorylation of calcipressin 1 increases its ability to inhibit calcineurin and decreases-calcipressin half-life. Biochem. J. 374: 567-575.
15. Giaever, G., Chu, A.M., Ni, L., Connelly, C., Riles, L., Veronneau, S., Dow, S., Lucau-Danila, A., Anderson, K., Andre, B., et al. 2002. Functional profiling of the Saccharomyces cerevisiae genome. Nature 418: 387-391.
16. Gorlach, J., Fox, D.S., Cutler, N.S., Cox, G.M., Perfect, J.R., and Heitman, J. 2000. Identification and characterization of a highly conserved calcineurin binding protein, CBP1/calcipressin, in Cryptococcus neoformans. EMBO J. 19: 3618-3629.
17. Graef, I.A., Mermelstein, P.G., Stankunas, K., Neilson, J.R., Deisseroth, K., Tsien, R.W., and Crabtree, G.R. 1999. L-type calcium channels and GSK-3 regulate the activity of NFATc4 in hippocampal neurons. Nature 401: 703-708.
18. 2+/calmodulin-dependent protein phosphatase in diverse eukaryotes. Topics Curr. Genet. 5: 73-90.
19. - . 2003b. The RCN family of calcineurin regulators. Biochem. Biophys. Res. Commun. 311: 1089-1093.
20. Hill, J.A., Rothermel, B., Yoo, K.D., Cabuay, B., Demetroulis, E., Weiss, R.M., Kutschke, W., Bassel-Duby, R., and Williams, R.S. 2002. Targeted inhibition of calcineurin in pressure-overload cardiac hypertrophy. Preservation of systolic function. J. Biol. Chem. 277: 10251-10255.
21. Hirata, Y., Andoh, T., Asahara, T., and Kikuchi, A. 2003. Yeast glycogen synthase kinase-3 activates Msn2p-dependent transcription of stress responsive genes. Mol. Biol. Cell 14: 302-312.
22. Jung, U.S. and Levin, D.E. 1999. Genome-wide analysis of gene expression regulated by the yeast cell wall integrity signalling pathway. Mol. Microbiol. 34: 1049-1057.
23. Kingsbury, T.J. and Cunningham, K.W. 2000. A conserved family of calcineurin regulators. Genes & Dev. 13: 1595-1604.
24. Klee, C.B., Ren, H., and Wang, X. 1998. Regulation of the calmodulin-stimulated protein phosphatase, calcineurin. J. Biol. Chem. 273: 13367-13370.
25. Lee, J.I., Dhakal, B.K., Lee, J., Bandyopadhyay, J., Jeong, S.Y., Eom, S.H., Kim, D.H., and Ahnn, J. 2003. The Caenorhabditis elegans homologue of Down Syndrome Critical Region 1, RCN-1, inhibits multiple functions of the phosphatase calcineurin. J. Mol. Biol. 328: 147-156.
26. Levchenko, A., Bruck, J., and Sternberg, P.W. 2000. Scaffold proteins may biphasically affect the levels of mitogen-activated protein kinase signaling and reduce its threshold properties. Proc. Natl. Acad. Sci. 97: 5818-5823.
27. Lohse, D.L., Denu, J.M., and Dixon, J.E. 1995. Insights derived from the structures of the Ser/Thr phosphatases calcineurin and protein phosphatase 1. Structure 3: 987-990.
28. Matheos, D.P., Kingsbury, T.J., Ahsan, U.S., and Cunningham, K.W. 1997. Tcn1p/Crz1p, a calcineurin-dependent transcription factor that differentially regulates gene expression in Saccharomyces cerevisiae. Genes & Dev. 11: 3445-3458.
29. 2+ in budding yeast. EMBO J. 20: 1074-1085.
30. Molkentin, J.D., Lu, J.R., Antos, C.L., Markham, B., Richardson, J., Robbins, J., Grant, S.R., and Olson, E.N. 1998. A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell 93: 215-228.
31. Mumberg, D., Muller, R., and Funk, M. 1994. Regulatable promoters of Saccharomyces cerevisiae: Comparison of transcriptional activity and their use for heterologous expression. Nucleic Acids Res. 22: 5767-5768.
32. Neigeborn, L. and Mitchell, A.P. 1991. The yeast MCK1 gene encodes a protein kinase homolog that activates early meiotic gene expression. Genes & Dev. 5: 533-548.
33. Ohteki, T., Parsons, M., Zakarian, A., Jones, R.G., Nguyen, L.T., Woodgett, J.R., and Ohashi, P.S. 2000. Negative regulation of T cell proliferation and interleukin 2 production by the serine threonine kinase GSK-3. J. Exp. Med. 192: 99-104.
34. Puziss, J.W., Hardy, T.A., Johnson, R.B., Roach, P.J., and Hieter, P. 1994. MDS1, a dosage suppressor of an mckl mutant, encodes a putative yeast homolog of glycogen synthase kinase 3. Mol. Cell. Biol. 14: 831-839.
35. Rayner, T.F., Gray, J.V., and Thomer, J.W. 2002. Direct and novel regulation of cAMP-dependent protein kinase by Mck1p, a yeast glycogen synthase kinase-3. J. Biol. Chem. 277: 16814-16822.
36. Rothermel, B., Vega, R.B., Yang, J., Wu, H., Bassel-Duby, R., and Williams, R.S. 2000. A protein encoded within the Down syndrome critical region is enriched in striated muscles and inhibits calcineurin signaling. J. Biol. Chem. 275: 8719-8725.
37. Rothermel, B.A., McKinsey, T.A., Vega, R.B., Nicol, R.L., Mammen, P., Yang, J., Antos, C.L., Shelton, J.M., Bassel-Duby, R., Olson, E.N., et al. 2001. Myocyte-enriched calcineurin-interacting protein, MCIP1, inhibits cardiac hypertrophy in vivo. Proc. Natl. Acad. Sci. 98: 3328-3333.
38. Rusnak, F. and Mertz, P. 2000. Calcineurin: form and function. Physiol. Rev. 80: 1483-1521.
39. Shapiro, B.E., Levchenko, A., and Mjolsness, E. 2001. Automatic model generation for signal transduction with applications to MAPK pathway. In Foundations of systems biology (ed. H. Kitano), pp. 145-161. MIT Press, Cambridge, MA.
40. Sherman, F., Hicks, J.B., and Fink, G.R. 1986. Methods in yeast genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
41. Shero, J.H. and Hieter, P. 1991. A suppressor of a centromere DNA mutation encodes a putative protein kinase (MCK1). Genes & Dev. 5: 549-560.
42. Sikorski, R.S. and Hieter, P. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122: 19-27.
43. Stathopoulos, A.M. and Cyert, M.S. 1997. Calcineurin acts through the CRZ1/TCN1 encoded transcription factor to regulate gene expression in yeast. Genes & Dev. 11: 3432-3444.
44. Stathopoulos-Gerontides, A., Guo, J.J., and Cyert, M.S. 1999. Yeast calcineurin regulates nuclear localization of the Crz1p transcription factor through dephosphorylation. Genes & Dev. 13: 798-803.
45. Tung, H.Y., Wang, W., and Chan, C.S. 1995. Regulation of chromosome segregation by Glc8p, a structural homolog of mammalian inhibitor 2 that functions as both an activator and an inhibitor of yeast protein phosphatase 1. Mol. Cell. Biol. 15: 6064-6074.
46. Vega, R.B., Yang, J., Rothermel, B.A., Bassel-Duby, R., and Williams, R.S. 2002. Multiple domains of MCIP1 contribute to inhibition of calcineurin activity. J. Biol. Chem. 277: 30401-30407.
47. Vega, R.B., Rothermel, B.A., Weinheimer, C.J., Kovacs, A., Naseem, R.H., Bassel-Duby, R., Williams, R.S., and Olson, E.N. 2003. Dual roles of modulatory calcineurin-interacting protein 1 in cardiac hypertrophy. Proc. Natl. Acad. Sci. 100: 669-674.
48. Vyas, D.R., Spangenburg, E.E., Abraha, T.W., Childs, T.E., and Booth, F.W. 2002. GSK-3β negatively regulates skeletal myotube hypertrophy. Am. J. Physiol. Cell Physiol. 283: C545-C551.
49. Wallis, J.W., Chrebet, G., Brodsky, G., Rolfe, M., and Rothstein, R. 1989. A hyper-recombination mutation in S. cerevisiae identifies a novel eukaryotic topoisomerase. Cell 58: 409-419.
50. Woodgett, J.R. 2001. Judging a protein by more than its name: GSK-3. Sci. STKE 2001: RE12.
51. Yang, J., Rothermel, B., Vega, R.B., Frey, N., McKinsey, T.A., Olson, E.N., Bassel-Duby, R., and Williams, R.S. 2000. Independent signals control expression of the calcineurin inhibitory proteins MCIP1 and MCIP2 in striated muscles. Circ. Res. 87: E61-E68.
52. Yoshimoto, H., Saltsman, K., Gasch, A.P., Li, H.X., Ogawa, N., Botstein, D., Brown, P.O., and Cyert, M.S. 2002. Genome-wide analysis of gene expression regulated by the calcineurin/Crz1p signaling pathway in Saccharomyces cerevisiae. J. Biol. Chem. 277: 31079-31088.