Identification of Yin-Yang regulators and a phosphorylation consensus for male germ cell-associated kinase (MAK)-related kinase

Molecular and Cellular Biology

Volumn 26, Issue 22, 2006, Pages 8639-8654

  Fu, Zheng ^a   Larson, Katherine A ^a   Chitta, Raghu K ^b   Parker, Sirlester A ^c   Turk, Benjamin E ^c   Lawrence, Matthew W ^a   Kaldis, Philipp ^d   Galaktionov, Konstantin ^e   Cohn, Steven M ^b   Shabanowitz, Jeffrey ^b   Hunt, Donald F ^a,b   Sturgill, Thomas W ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

^e BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE 7; MAK RELATED KINASE; MALE GERM CELL ASSOCIATED KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; PEPTIDE LIBRARY; PHOSPHATASE; PROLINE; PROTEIN IME2P; PROTEIN KINASE; PROTEIN MDE3; PROTEIN PHOSPHATASE 5; PROTEIN SCYTHE; THREONINE; THREONINE KINASE; TRANSCRIPTION FACTOR PIT 1; TYROSINE; UNCLASSIFIED DRUG;

ARTICLE; AUTOPHOSPHORYLATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; MASS SPECTROMETRY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE; SITE DIRECTED MUTAGENESIS;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CELL LINE; CONSENSUS SEQUENCE; CYCLIN-DEPENDENT KINASES; DOWN-REGULATION; GENE EXPRESSION REGULATION; HUMANS; HYDROGEN PEROXIDE; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; PROTEINS; TRANSFECTION;

SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE;

EID: 33751017086     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00816-06     Document Type: Article

References (69)

1. Abe, H., and C. Shimoda. 2000. Autoregulated expression of Schizosaccharomyces pombe meiosis-specific transcription factor Mei4 and a genome-wide search for its target genes. Genetics 154:1497-1508.
2. Abe, S., T. Yagi, S. Ishiyama, M. Hiroe, F. Marumo, and Y. Ikawa. 1995. Molecular cloning of a novel serine/threonine kinase, MRK, possibly involved in cardiac development. Oncogene 11:2187-2195.
3. Ali, A., J. Zhang, S. Bao, I. Liu, D. Otterness, N. M. Dean, R. T. Abraham, and X. F. Wang. 2004. Requirement of protein phosphatase 5 in DNA-damage-induced ATM activation. Genes Dev. 18:249-254.
4. Banerji, J., J. Sands, J. L. Strominger, and T. Spies. 1990. A gene pair from the human major histocompatibility complex encodes large proline-rich proteins with multiple repeated motifs and a single ubiquitin-like domain. Proc. Natl. Acad. Sci. USA 87:2374-2378.
5. Barzilai, A., and K. Yamamoto. 2004. DNA damage responses to oxidative stress. DNA Repair 3:1109-1115.
6. Caligiuri, M., F. Becker, K. Murthi, F. Kaplan, S. Dedier, C. Kaufmann, A. Machl, G. Zybarth, J. Richard, N. Bockovich, A. Kluge, and N. Kley. 2005. A proteome-wide CDK/CRK-specific kinase inhibitor promotes tumor cell death in the absence of cell cycle progression. Chem. Biol. 12:1103-1115.
7. 2 on cell cycle and survival in DNA mismatch repair-deficient and -proficient cell lines. Cancer Lett. 195:243-251.
8. Chen, M. X., and P. T. Cohen. 1997. Activation of protein phosphatase 5 by limited proteolysis or the binding of polyunsaturated fatty acids to the TPR domain. FEBS Lett. 400:136-140.
9. Chen, M. X., A. E. McPartlin, L. Brown, Y. H. Chen, H. M. Barker, and P. T. Cohen. 1994. A novel human protein serine/threonine phosphatase, which possesses four tetratricopeptide repeat motifs and localizes to the nucleus. EMBO J. 13:4278-4290.
10. Clifford, D. M., K. E. Stark, K. E. Gardner, S. Hoffmann-Benning, and G. S. Brush. 2005. Mechanistic insight into the Cdc28-related protein kinase Ime2 through analysis of replication protein A phosphorylation. Cell Cycle 4:1826-1833.
11. Conde, R., J. Xavier, C. McLoughlin, M. Chinkers, and N. C. Ovsenek. 2005. Protein phosphatase 5 is a negative modulator of heat shock factor 1. J. Biol. Chem. 280:28989-28996.
12. Daroui, P., S. D. Desai, T. K. Li, A. A. Liu, and L. F. Liu. 2004. Hydrogen peroxide induces topoisomerase I-mediated DNA damage and cell death. J. Biol. Chem. 279:14587-14594.
13. Desmots, F., H. R. Russell, Y. Lee, K. Boyd, and P. J. McKinnon. 2005. The Reaper-binding protein Scythe modulates apoptosis and proliferation during mammalian development. Mol. Cell. Biol. 25:10329-10337.
14. Doong, H., A. Vrailas, and E. C. Kohn. 2002. What's in the "BAG"?-a functional domain analysis of the BAG-family proteins. Cancer Lett. 188:25-32.
15. Espinoza, F. H., A. Farrell, H. Erdjument-Bromage, P. Tempst, and D. O. Morgan. 1996. A cyclin-dependent kinase-activating kinase (CAK) in budding yeast unrelated to vertebrate CAK. Science 273:1714-1717.
16. Foiani, M., E. Nadjar-Boger, R. Capone, S. Sagee, T. Hashimshoni, and Y. Kassir. 1996. A meiosis-specific protein kinase, Ime2, is required for the correct timing of DNA replication and for spore formation in yeast meiosis. Mol. Gen. Genet. 253:278-288.
17. Fu, Z., M. J. Schroeder, J. Shabanowitz, P. Kaldis, K. Togawa, A. K. Rustgi, D. F. Hunt, and T. W. Sturgill. 2005. Activation of a nuclear Cdc2-related kinase within a mitogen-activated protein kinase-like TDY motif by autophosphorylation and cyclin-dependent protein kinase-activating kinase. Mol. Cell. Biol. 25:6047-6064.
18. Gentile, S., T. Darden, C. Erxleben, C. Romeo, A. Russo, N. Martin, S. Rossie, and D. L. Armstrong. 2006. Rac GTPase signaling through the PPS protein phosphatase. Proc. Natl. Acad. Sci. USA 103:5202-5206.
19. Goldman, E. H., L. Chen, and H. Fu. 2004. Activation of apoptosis signal-regulating kinase 1 by reactive oxygen species through dephosphorylation at serine 967 and 14-3-3 dissociation. J. Biol. Chem. 279:10442-10449.
20. Rsk2-dependent pathways regulate the CCAAT/enhancer-binding protein-beta interaction with serum response factor. J. Biol. Chem. 276:38449-38456.
21. Himpel, S., W. Tegge, R. Frank, S. Leder, H. G. Joost, and W. Becker. 2000. Specificity determinants of substrate recognition by the protein kinase DYRK1A. J. Biol. Chem. 275:2431-2438.
22. Holmes, J. K., and M. J. Solomon. 1996. A predictive scale for evaluating cyclin-dependent kinase substrates. A comparison of p34cdc2 and p33cdk2. J. Biol. Chem. 271:25240-25246.
23. Honigberg, S. M. 2004. Ime2p and Cdc28p: co-pilots driving meiotic development. J. Cell. Biochem. 92:1025-1033.
24. - gene encodes a meiosis-specific transcription factor containing a forkhead DNA-binding domain. Mol. Cell. Biol. 18:2118-2129.
25. Hutti, J. E., E. T. Jarrell, J. D. Chang, D. W. Abbott, P. Storz, A. Toker, L. C. Cantley, and B. E. Turk. 2004. A rapid method for determining protein kinase specificity. Nat. Methods 1:27-29.
26. Jeong, J. Y., J. Johns, C. Sinclair, J. M. Park, and S. Rossie. 2003. Characterization of Saccharomyces cerevisiae protein Ser/Thr phosphatase T1 and comparison to its mammalian homolog PP5. BMC Cell Biol. 4:3.
27. Jha, M. N., J. R. Hamburg, B. W. Bernstein, and J. S. Bedford. 2002. Caffeine eliminates gamma-ray-induced G2-phase delay in human tumor cells but not in normal cells. Radiat. Res. 157:26-31.
28. Jinno, A., K. Tanaka, H. Matsushime, T. Haneji, and M. Shibuya. 1993. Testis-specific Mak protein kinase is expressed specifically in the meiotic phase in spermatogenesis and is associated with a 210-kilodalton cellular phosphoprotein. Mol. Cell. Biol. 13:4146-4156.
29. Johnson, S. A., and T. Hunter. 2005. Kinomics: methods for deciphering the kinome. Nat. Methods 2:17-25.
30. Kaldis, P., and M. J. Solomon. 2000. Analysis of CAK activities from human cells. Eur. J. Biochem. 267:4213-1221.
31. Kaldis, P., A. Sutton, and M. J. Solomon. 1996. The Cdk-activating kinase (CAK) from budding yeast. Cell 86:553-564.
32. Kaye, F. J., S. Modi, I. Ivanovska, E. V. Koonin, K. Thress, A. Kubo, S. Kornbluth, and M. D. Rose. 2000. A family of ubiquitin-like proteins binds the ATPase domain of Hsp70-like Stch. FEBS Lett. 467:348-355.
33. Kikukawa, Y., R. Minami, M. Shimada, M. Kobayashi, K. Tanaka, H. Yokosawa, and H. Kawahara. 2005. Unique proteasome subunit Xrpn10c is a specific receptor for the antiapoptotic ubiquitin-like protein Scythe. FEBS J. 272:6373-6386.
34. Koji, T., A. Jinno, H. Matsushime, M. Shibuya, and P. K. Nakane. 1992. In situ localization of male germ cell-associated kinase (mak) mRNA in adult mouse testis: specific expression in germ cells at stages around meiotic cell division. Cell Biochem. Funct. 10:273-279.
35. Liu, Y., C. Wu, and K. Galaktionov. 2004. p42, a novel cyclin-dependent kinase-activating kinase in mammalian cells. J. Biol. Chem. 279:4507-4514.
36. MacKeigan, J. P., L. O. Murphy, and J. Blenis. 2005. Sensitized RNAi screen of human kinases and phosphatases identifies new regulators of apoptosis and chemoresistance. Nat. Cell Biol. 7:591-600.
37. Manchen, S. T., and A. V. Hubberstey. 2001. Human Scythe contains a functional nuclear localization sequence and remains in the nucleus during staurosporine-induced apoptosis. Biochem. Biophys. Res. Commun. 287:1075-1082.
38. Matsushime, H., A. Jinno, N. Takagi, and M. Shibuya. 1990. A novel mammalian protein kinase gene (mak) is highly expressed in testicular germ cells at and after meiosis. Mol. Cell. Biol. 10:2261-2268.
39. Miyata, Y., and E. Nishida. 2004. CK2 controls multiple protein kinases by phosphorylating a kinase-targeting molecular chaperone, Cdc37. Mol. Cell. Biol. 24:4065-4074.
40. Morita, K., M. Saitoh, K. Tobiume, H. Matsuura, S. Enomoto, H. Nishitoh, and H. Ichijo. 2001. Negative feedback regulation of ASK1 by protein phosphatase 5 (PP5) in response to oxidative stress. EMBO J. 20:6028-6036.
41. Obenauer, J. C., L. C. Cantley, and M. B. Yaffe. 2003. Scansite 2.0: proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res. 31:3635-3641.
42. Pearson, W. R. 1991. Searching protein sequence libraries: comparison of the sensitivity and selectivity of the Smith-Waterman and FASTA algorithms. Genomics 11:635-650.
43. Schaber, M., A. Lindgren, K. Schindler, D. Bungard, P. Kaldis, and E. Winter. 2002. CAK1 promotes meiosis and spore formation in Saccharomyces cerevisiae in a CDC28-independent fashion. Mol. Cell. Biol. 22:57-68.
44. Schindler, K., K. R. Benjamin, A. Martin, A. Boglioli, I. Herskowitz, and E. Winter. 2003. The Cdk-activating kinase Cak1p promotes meiotic S phase through Ime2p. Mol. Cell. Biol. 23:8718-8728.
45. Shevchenko, A., M. Wilm, O. Vorm, and M. Mann. 1996. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68:850-858.
46. Shinkai, Y., H. Satoh, N. Takeda, M. Fukuda, E. Chiba, T. Kato, T. Kuramochi, and Y. Araki. 2002. A testicular germ cell-associated serine-threonine kinase, MAK, is dispensable for sperm formation. Mol. Cell. Biol. 22:3276-3280.
47. Sinclair, C., C. Borchers, C. Parker, K. Tomer, H. Charbonneau, and S. Rossie. 1999. The tetratricopeptide repeat domain and a C-terminal region control the activity of Ser/Thr protein phosphatase 5. J. Biol. Chem. 274:23666-23672.
48. Skinner, J., C. Sinclair, C. Romeo, D. Armstrong, H. Charbonneau, and S. Rossie. 1997. Purification of a fatty acid-stimulated protein-serine/threonine phosphatase from bovine brain and its identification as a homolog of protein phosphatase 5. J. Biol. Chem. 272:22464-22471.
49. Songyang, Z., S. Blechner, N. Hoagland, M. F. Hoekstra, H. Piwnica-Worms, and L. C. Cantley. 1994. Use of an oriented peptide library to determine the optimal substrates of protein kinases. Curr. Biol. 4:973-982.
50. Songyang, Z., K. P. Lu, Y. T. Kwon, L. H. Tsai, O. Filhol, C. Cochet, D. A. Brickey, T. R. Soderling, C. Bartleson, D. J. Graves, A. J. DeMaggio, M. F. Hoekstra, J. Blenis, T. Hunter, and L. C. Cantley. 1996. A structural basis for substrate specificities of protein Ser/Thr kinases: primary sequence preference of casein kinases I and II, NIMA, phosphorylase kinase, calmodulin-dependent kinase II, CDK5, and Erk1. Mol. Cell. Biol. 16:6486-6493.
51. Swingle, M. R., R. E. Honkanen, and E. M. Ciszak. 2004. Structural basis for the catalytic activity of human serine/threonine protein phosphatase-5. J. Biol. Chem. 279:33992-33999.
52. Tanoue, T., R. Maeda, M. Adachi, and E. Nishida. 2001. Identification of a docking groove on ERK and p38 MAP kinases that regulates the specificity of docking interactions. EMBO J. 20:466-479.
53. Thress, K., J. Song, R. I. Morimoto, and S. Kornbluth. 2001. Reversible inhibition of Hsp70 chaperone function by Scythe and Reaper. EMBO J. 20:1033-1041.
54. Thuret, J. Y., J. G. Valay, G. Faye, and C. Mann. 1996. Civ1 (CAK in vivo), a novel Cdk-activating kinase. Cell 86:565-576.
55. Togawa, K., Y. X. Yan, T. Inomoto, S. Slaugenhaupt, and A. K. Rustgi. 2000. Intestinal cell kinase (ICK) localizes to the crypt region and requires a dual phosphorylation site found in map kinases. J. Cell. Physiol. 183:129-139.
56. Wang, I. C., Y. J. Chen, D. Hughes, V. Petrovic, M. L. Major, H. J. Park, Y. Tan, T. Ackerson, and R. H. Costa. 2005. Forkhead box M1 regulates the transcriptional network of genes essential for mitotic progression and genes encoding the SCF (Skp2-Cks1) ubiquitin ligase. Mol. Cell. Biol. 25:10875-10894.
57. Wang, R., and C. C. Liew. 1994. The human BAT3 ortholog in rodents is predominantly and developmentally expressed in testis. Mol. Cell. Biochem. 136:49-57.
58. Wechsler, T., B. P. Chen, R. Harper, K. Morotomi-Yano, B. C. Huang, K. Meek, J. E. Cleaver, D. J. Chen, and M. Wabl. 2004. DNA-PKcs function regulated specifically by protein phosphatase 5. Proc. Natl. Acad. Sci. USA 101:1247-1252.
59. Wohlbold, L., S. Larochelle, J. C. Liao, G. Livshits, J. Singer, K. M. Shokat, and R. P. Fisher. 2006. The cyclin-dependent kinase (CDK) family member PNQALRE/CCRK supports cell proliferation but has no intrinsic CDK-activating kinase (CAK) activity. Cell Cycle 5:546-554.
60. Woods, J. A., A. J. Young, I. T. Gilmore, A. Morris, and R. F. Bilton. 1997. Measurement of menadione-mediated DNA damage in human lymphocytes using the comet assay. Free Radic. Res. 26:113-124.
61. Xia, L., D. Robinson, A. H. Ma, H. C. Chen, F. Wu, Y. Qiu, and H. J. Kung. 2002. Identification of human male germ cell-associated kinase, a kinase transcriptionally activated by androgen in prostate cancer cells. J. Biol. Chem. 277:35422-35433.
62. Xu, L., M. Ajimura, R. Padmore, C. Klein, and N. Kleckner. 1995. NDT80, a meiosis-specific gene required for exit from pachytene in Saccharomyces cerevisiae. Mol. Cell. Biol. 15:6572-6581.
63. Yang, J., S. M. Roe, M. J. Cliff, M. A. Williams, J. E. Ladbury, P. T. Cohen, and D. Barford. 2005. Molecular basis for TPR domain-mediated regulation of protein phosphatase 5. EMBO J. 24:1-10.
64. Ye, H., T. F. Kelly, U. Samadani, L. Lim, S. Rubio, D. G. Overdier, K. A. Roebuck, and R. H. Costa. 1997. Hepatocyte nuclear factor 3/fork head homolog 11 is expressed in proliferating epithelial and mesenchymal cells of embryonic and adult tissues. Mol. Cell. Biol. 17:1626-1641.
65. Young, J. A., R. W. Hyppa, and G. R. Smith. 2004. Conserved and nonconserved proteins for meiotic DNA breakage and repair in yeasts. Genetics 167:593-605.
66. Zeke, T., N. Morrice, C. Vazquez-Martin, and P. T. Cohen. 2005. Human protein phosphatase 5 dissociates from heat-shock proteins and is proteolytically activated in response to arachidonic acid and the microtubule-depolymerizing drug nocodazole. Biochem. J. 385:45-56.
67. Zhang, J., S. Bao, R. Furumai, K. S. Kucera, A. Ali, N. M. Dean, and X. F. Wang. 2005. Protein phosphatase 5 is required for ATR-mediated checkpoint activation. Mol. Cell. Biol. 25:9910-9919.
68. Zhou, G., T. Golden, I. V. Aragon, and R. E. Honkanen. 2004. Ser/Thr protein phosphatase 5 inactivates hypoxia-induced activation of an apoptosis signal-regulating kinase 1/MKK-4/JNK signaling cascade. J. Biol. Chem. 279:46595-46605.
69. WAF1/CiP1 and mediate growth arrest. J. Biol. Chem. 273:12250-12258.