Phosphorylation of High-Mobility Group Protein A2 by Nek2 Kinase during the First Meiotic Division in Mouse Spermatocytes

Molecular Biology of the Cell

Volumn 15, Issue 3, 2004, Pages 1224-1232

  Di Agostino, Silvia ^a   Fedele, Monica ^b   Chieffi, Paolo ^b   Fusco, Alfredo ^b   Rossi, Pellegrino ^a   Geremia, Raffaele ^a   Sette, Claudio ^a  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

HIGH MOBILITY GROUP A2 PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; NEK2 KINASE; PROTEIN SERINE THREONINE KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CELL CYCLE G2 PHASE; CHROMATIN CONDENSATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; IN VITRO STUDY; MALE; MEIOSIS; METAPHASE; MOUSE; NONHUMAN; PACHYTENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; SIGNAL TRANSDUCTION; SPERMATOCYTE;

ANIMALS; CELLS, CULTURED; CHROMATIN; CLONING, MOLECULAR; DNA-BINDING PROTEINS; HMGA2 PROTEIN; MALE; MEIOSIS; MICE; MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; SPERMATOCYTES;

ANIMALIA;

EID: 1542283801     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E03-09-0638     Document Type: Article

References (42)

1. Arama, E., Yanai, A., Kilfin, G., Bernstein, A., and Motro, B. (1998). Murine NIMA-related kinases are expressed in patterns suggesting distinct functions in gametogenesis and a role in the nervous system. Oncogene 16, 1813-1823.
2. Baldassarre, G., Fedele, M., Battista, S., Vecchione, A., Klein-Szanto, A.J.P., Waldmann, T.A., Azimi, N., Croce, C.M., and Fusco, A. (2001). Onset of Natural Killer Cell Lymphomas in transgenic mice carrying a truncated HMGI-C gene by the chronic stimulation of the IL-2 and IL-15 pathway. Proc. Natl. Acad. Sci. USA 98, 7970-7975,
3. Bustin, M. (1999). Regulation of DNA-dependent activities by the functional motifs of the high-mobility-group chromosomal proteins. Mol. Cell. Biol. 29, 5237-5246.
4. Cobb, J., Cargile, B., and Handel, M.A. (1999). Acquisition of competence to condense metaphase I chromosomes during spermatogenesis. Dev. Biol. 205, 49-64.
5. Chieffi, P., Battista, S., Barchi, M., Di Agostino, S., Pierantoni, G.M., Fedele, M., Chiariotti, L., Tramontano, D., and Fusco, A. (2002). HMGA1 and HMGA2 protein expression in mouse spermatogenesis. Oncogene 21, 3644-3650.
6. Chen, Y., Riley, D.J., Zheng, L., Chen, P.L., and Lee, W.H. (2002). Phosphorylation of the mitotic regulator protein Hecl by Nek2 kinase is essential for faithful chromosome segregation. J. Biol. Chem. 277, 49408-49416.
7. Choi, T., Fukasawa, K., Zhou, R., Tessarollo, L., Borror, K., Resau, J., and Vande Woude, G.F. (1996). The Mos/mitogen-activated protein kinase (MAPK) pathway regulates the size and degradation of the first polar body in maturing mouse oocytes. Proc. Natl. Acad. Sci. USA 93, 7032-7035.
8. Colledge, W.H., Carlton, M.B., Udy, G.B., and Evans, M.J. (1994). Disruption of c-mos causes parthenogenetic development of unfertilized mouse eggs. Nature 370, 65-68.
9. Di Agostino, S., Rossi, P., Geremia, R., and Sette, C. (2002). The MAPK pathway triggers activation of Nek2 during chromosome condensation in mouse spermatocytes. Development 129, 1715-1727.
10. Eto, M., Elliott, E., Prickett, T.D., and Brautigan, D.L. (2002). Inhibitor-2 regulates protein phosphatase-1 complexed with NimA-related kinase to induce centrosome separation. J. Biol. Chem. 277, 44013-44020.
11. Falvo, J.V., Thanos, D., and Maniatis, T. (1995). Reversal of intrinsic DNA bends in the IFN beta gene enhancer by transcription factors and the architectural protein HMG I(Y). Cell 83, 1101-1111.
12. Fedele, M., Battista, S., Manfioletti, G., Croce, C.M., Giancotti, V., and Fusco, A. (2001). Role of the high mobility group A proteins in human lipomas. Carcinogenesis 22, 1583-1591.
13. Foti, D., Iuliano, R., Chiefari, E., and Brunetti, A. (2003). A nucleoprotein complex containing Sp1, C/EBP beta, and HMGI-Y controls human insulin receptor gene transcription. Mol. Cell. Biol. 23, 2720-2732.
14. Fry, A.M., Schultz, S.J., Bartek, J., and Nigg, E.A. (1995). Substrate specificity and cell cycle regulation of the Nek2 protein kinase, a potential human homolog of the mitotic regulator NIMA of Aspergillus nidulans. J. Biol. Chem. 270, 12899-12905.
15. Fry, A.M., Meraldi, P., and Nigg, E.A. (1998a). A centrosomal function for the human Nek2 protein kinase, a member of the NIMA family of cell cycle regulators. EMBO J. 17, 470-481.
16. Fry, A.M., Mayor, T., Meraldi, P., Stierhof, Y.D., Tanaka, K., and Nigg, E.A. (1998b). C-Nap1, a novel centrosomal coiled-coil protein and candidate substrate of the cell cycle-regulated protein kinase Nek2. J. Cell Biol. 141, 1563-1574.
17. Fry, A.M. (2002). The Nek2 protein kinase: a novel regulator of centrosome structure. Oncogene 21, 6184-6194.
18. Gross, S.D., Schwab, M.S., Taieb, F.E., Lewellyn, A.L., Qian, Y.W., and Maller, J.L. (2000). The critical role of the MAP kinase pathway in meiosis II in Xenopus oocytes is mediated by p90Rsk. Curr. Biol. 10, 430-438.
19. Hames, R.S., Wattam, S.L., Yamano, H., Bacchieri, R., and Fry, A.M. (2001). APC/C-mediated destruction of the centrosomal kinase Nek2A occurs in early mitosis and depends upon a cyclin A-type D-box. EMBO J. 20, 7117-7127.
20. Handel, M.A., and Eppig, J.J. (1998). Sexual dimorphism in the regulation of mammalian meiosis. Curr. Top. Dev. Biol. 37, 333-358.
21. Hashimoto, N., et al. (1994). Parthenogenetic activation of oocytes in c-mos-deficient mice. Nature 370, 68-71.
22. Helps, N.R., Luo, X., Barker, H.M., and Cohen, P.T. (2000). NIMA-related kinase 2 (Nek2), a cell-cycle-regulated protein kinase localized to centrosomes, is complexed to protein phosphatase 1. Biochem. J. 349, 509-518.
23. Lu, K.P., and Means, A.R. (1994). Expression of the noncatalytic domain of the NIMA kinase causes a G2 arrest in Aspergillus nidulans. EMBO J. 13, 2103-2113.
24. Mayor, T., Hacker, U., Stierhof, Y.D., and Nigg, E.A. (2002). The mechanism regulating the dissociation of the centrosomal protein C-Nap1 from mitotic spindle poles. J. Cell Sci. 115, 3275-3284.
25. Osmani, A.H., McGuire, S.L., and Osmani, S.A. (1991). Parallel activation of the NIMA and p34cdc2 cell cycle-regulated protein kinases is required to initiate mitosis in A. nidulans. Cell 67, 283-291.
26. Petronczki, M., Siomos, M.F., and Nasmyth, K. (2003). Un menage a quatre: the molecular biology of chromosome segregation in meiosis. Cell 112, 423-440.
27. Piekielko, A., Drung, A., Rogalla, P., Schwanbeck, R., Heyduk, T., Gerharz, M., Bullerdiek, J., and Wisniewski, J.R. (2001). Distinct organization of DNA complexes of various HMGI/Y family proteins and their modulation upon mitotic phosphorylation. J. Biol. Chem. 276, 1984-1992.
28. Rhee, K., and Wolgemuth, D.J. (1997). The NIMA-related kinase 2, Nek2, is expressed in specific stages of the meiotic cell cycle and associates with meiotic chromosomes. Development 124, 2167-2177.
29. Roeder, G.S. (1997). Meiotic chromosomes: it takes two to tango. Genes Dev. 11, 2600-2621.
30. Ronfani, L., Ferraguti, M., Croci, L., Ovitt, C.E., Scholer, H.R., Consalez, G.G., and Bianchi, M. (2001). Reduced fertility and spermatogenesis defects in mice lacking chromosomal protein Hmgb2. Development 128, 1265-1273.
31. Rossi, P., Dolci, S., Albanesi, C., Grimaldi, P., Ricca, R., and Geremia, R. (1993). Follicle-stimulating hormone induction of steel factor (SLF) mRNA in mouse Sertoli cells and stimulation of DNA synthesis in spermatogonia by soluble SLF. Dev. Biol. 155, 68-74.
32. Sagata, N. (1997). What does Mos do in oocytes and somatic cells? Bioessays 19, 13-21.
33. Sette, C., Barchi, M., Bianchini, A., Conti, M., Rossi, P., and Geremia, R. (1999). Activation of the mitogen-activated protein kinase Erk1 during meiotic progression of mouse pachytene spermatocytes. J. Biol. Chem. 274, 33571-33579.
34. Sheflin, L.G., Fucile, N.W., and Spaulding, S.W. (1993). The specific interactions of HMG 1 and 2 with negatively supercoiled DNA are modulated by their acidic C-terminal domains and involve cysteine residues in their HMG 1/2 boxes. Biochemistry 32, 3238-3248.
35. Subramanian, D., and Griffith, J.D. (2002). Interactions between p53, hMSH2-hMSH6 and HMG I(Y) on Holliday junctions and bulged bases. Nucleic Acids Res. 30, 2427-2434.
36. Tanaka, K., Parvinen, M., and Nigg, E.A. (1997). The in vivo expression pattern of mouse Nek2, a NIMA-related kinase, indicates a role in both mitosis and meiosis. Exp. Cell Res. 237, 264-274.
37. Tunquist, B.J., and Maller, J.L. (2003). Under arrest: cytostatic factor (CSF)-mediated metaphase arrest in vertebrate eggs. Genes Dev. 17, 683-710.
38. Verlhac, M.H., Kubiak, J.Z., Weber, M., Geraud, G., Colledge, W.H., Evans, M.J., and Maro, B. (1996). Mos is required for MAP kinase activation and is involved in microtubule organization during meiotic maturation in the mouse. Development 122, 815-822.
39. Verlhac, M.H., Lefebvre, C., Guillaud, P., Rassinier, P., and Maro, B. (2000). Asymmetric division in mouse oocytes: with or without Mos. Curr. Biol. 10, 1303-1306.
40. Wiltshire, T., Park, C., Caldwell, K.A., and Handel, M.A. (1995). Induced premature G2/M-phase transition in pachytene spermatocytes includes events unique to meiosis. Dev. Biol. 169, 557-567.
41. Wisniewski, J.R., Szewczuk, Z., Petry, I., Schwanbeck, R., and Renner, U. (1999). Constitutive phosphorylation of the acidic tails of the high mobility group 1 proteins by casein kinase II alters their conformation, stability, and DNA binding specificity. J. Biol. Chem. 274, 20116-20122.
42. Zhou, X., Benson, K.F., Ashar, H.R., and Chada, K. (1995). Mutation responsible for the mouse pygmy phenotype in the developmentally regulated factor HMGI-C. Nature 376, 771-774.