Dlk/ZIP kinase, a novel Ser/Thr-specific protein kinase with multiple functions

Signal Transduction

Volumn 7, Issue 3, 2007, Pages 248-259

  Scheidtmann, Karl Heinz ^a  

^a UNIVERSITY OF BONN   (Germany)

Author keywords

Apoptosis; Cytokinesis; DAP kinase; Dlk ZIP kinase; Histones; Mitosis; Myosin light chain; Transcription

Indexed keywords

DEATH ASSOCIATED PROTEIN KINASE; PROTEIN KINASE; PROTEIN SERINE KINASE; THREONINE PROTEINASE; UNCLASSIFIED DRUG; ZIPPER INTERACTING PROTEIN KINASE;

AMINO TERMINAL SEQUENCE; APOPTOSIS; CARBOXY TERMINAL SEQUENCE; CELL MOTILITY; CELL POLARITY; CHROMATIN STRUCTURE; CYTOKINESIS; ENZYME ACTIVATION; ENZYME STRUCTURE; GENE STRUCTURE; MITOSIS; MULTINUCLEAR CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SMOOTH MUSCLE CONTRACTION; SMOOTH MUSCLE FIBER;

EID: 34250022495     PISSN: 16154053     EISSN: 16154061     Source Type: Journal    
DOI: 10.1002/sita.200600112     Document Type: Review

References (70)

1. Deiss, L. P., Feinstein, E., Berissi, H., Cohen, O., and Kimchi, A. (1995) Identification of a novel serine/threonine kinase and a novel 15-kD protein as potential mediators of the gamma interferon-induced cell death. Genes Dev. 9: 15-30.
2. Cohen, O., Feinstein, E., and Kimchi, A. (1997) DAP-kinase is a Ca2+/calmodulin-dependent, cytoskeletal-associated protein kinase, with cell death-inducing functions that depend on its catalytic activity. EMBO J. 16: 998-1008.
3. Inbal, B., Cohen, O., Polak-Charcon, S., Kopolovic, J., Vadai, E., Eisenbach, L., and Kimchi, A. (1997) DAP kinase links the control of apoptosis to metastasis. Nature 390: 180-184.
4. Schneider-Stock, R., Roesner, A., and Ullrich, O. (2005) DAP-kinase-Protector or enemy in apoptotic cell death. Int. J. Biochem. Cell Biol. 37: 1763-1767.
5. Kawai, T., Nomura, F., Hoshino, K., Copeland, N. G., Gilbert, D. J., Jenkins, N. A., and Akira, S. (1999) Death-associated protein kinase 2 is a new calcium/calmodulin-dependent protein kinase that signals apoptosis through its catalytic activity. Oncogene 18: 3471-3480.
6. Inbal, B., Shani, G., Cohen, O., Kissil, J. L., and Kimchi, A. (2000) Death-associated protein kinase-related protein 1, a novel serine/threonine kinase involved in apoptosis. Mol. Cell Biol. 20: 1044-1054.
7. Kogel, D., Plottner, O., Landsberg, G., Christian, S., and Scheidtmann, K. H. (1998) Cloning and characterization of Dlk, a novel serine/threonine kinase that is tightly associated with chromatin and phosphorylates core histones. Oncogene 17: 2645-2654.
8. Kawai, T., Matsumoto, M., Takeda, K., Sanjo, H., and Akira, S. (1998) ZIP kinase, a novel serine/threonine kinase which mediates apoptosis. Mol. Cell Biol. 18: 1642-1651.
9. Manning, G., Whyte, D. B., Martinez, R., Hunter, T., and Sudarsanam, S. (2002) The protein kinase complement of the human genome. Science 298: 1912-1934.
10. Sanjo, H., Kawai, T., and Akira, S. (1998) DRAKs, novel serine/threonine kinases related to death-associated protein kinase that trigger apoptosis. J. Biol. Chem. 273: 29066-29071.
11. Kogel, D., Prehn, J. H., and Scheidtmann, K. H. (2001) The DAP kinase family of pro-apoptotic proteins: novel players in the apoptotic game. Bioessays 23: 352-358.
12. Cohen, O. and Kimchi, A. (2001) DAP-kinase: from functional gene cloning to establishment of its role in apoptosis and cancer. Cell Death Differ. 8: 6-15.
13. Shani, G., Marash, L., Gozuacik, D., Bialik, S., Teitelbaum, L., Shohat, G., and Kimchi, A. (2004) Death-associated protein kinase phosphorylates ZIP kinase, forming a unique kinase hierarchy to activate its cell death functions. Mol. Cell. Biol. 24: 8611-8626.
14. Jin, Y., Blue, E. K., Dixon, S., Hou, L., Wysolmerski, R. B., and Gallagher, P. J. (2001) Identification of a new form of death-associated protein kinase that promotes cell survival. J. Biol. Chem. 276: 39667-39678.
15. Jin, Y. and Gallagher, P. J. (2003) Antisense depletion of death-associated protein kinase promotes apoptosis. J. Biol. Chem. 278: 51587-51593.
16. Kojima, H., Nemoto, A., Uemura, T., Honma, R., Ogura, M., and Liu, Y. (2001) rDrak1, a novel kinase related to apoptosis, is strongly expressed in active osteoclasts and induces apoptosis. J. Biol. Chem. 276: 19238-19243.
17. Friedrich, M. L., Wen, B. G., Bain, G., Kee, B. L., Katayama, C., Murre, C., Hedrick, S. M., and Walsh, C. M. (2005) DRAK2, a lymphoid-enriched DAP kinase, regulates the TCR activation threshold during thymocyte selection. Int. Immunol. 17: 1379-1390.
18. MacDonald, J. A., Borman, M. A., Muranyi, A., Somlyo, A. V., Hartshorne, D. J., and Haystead, T. A. (2001) Identification of the endogenous smooth muscle myosin phosphatase- associated kinase. Proc. Natl. Acad. Sci. U. S. A. 98: 2419-2424.
19. Endo, A., Surks, H. K., Mochizuki, S., Mochizuki, N., and Mendelsohn, M. E. (2004) Identification and characterization of zipper-interacting protein kinase as the unique vascular smooth muscle myosin phosphatase-associated kinase. J. Biol. Chem. 279: 42055-42061.
20. Tereshko, V., Teplova, M., Brunzelle, J., Watterson, D. M., and Egli, M. (2001) Crystal structures of the catalytic domain of human protein kinase associated with apoptosis and tumor suppression. Nat. Struct. Biol. 8: 899-907.
21. Kogel, D., Bierbaum, H., Preuss, U., and Scheidtmann, K. H. (1999) C-terminal truncation of Dlk/ZIP kinase leads to abrogation of nuclear transport and high apoptotic activity. Oncogene 18: 7212-7218.
22. Saito, T., Seki, N., Ohira, M., Hayashi, A., Kozuma, S., Hattori, A., and Hori, T. (1998) Assignment of the ZIP kinase gene to human chromosome 19p13.3 by somatic hybrid analysis and fluorescence in-situ hybridization. J. Hum. Genet. 43: 209-211.
23. Engemann, H., Kögel, D., Manderscheid, S., Preuss, U., and Scheidtmann, K. H. (2002) Elucidation of transcriptional elements and the genomic structure of DAP-like kinase. Ann. N. Y. Acad. Sci. 973: 363-367.
24. Preuss, U., Bierbaum, H., Buchenau, P., and Scheidtmann, K. H. (2003) Dlk/ZIP kinase, a member of the proapoptotic DAP-kinase family, associates with Centrosomes, Centromers, and the Contractile Ring during Mitosis. Eur. J. Cell Biol. 82: 447-459.
25. Graves, P. R., Winkfield, K. M., and Haystead, T. A. (2005) Regulation of zipper-interacting protein kinase activity in vitro and in vivo by multisite phosphorylation. J. Biol. Chem. 280: 9363-9374.
26. Hagerty, L., Weitzel, D. H., Chambers, J., Fortner, C. N., Brush, M. H., Loiselle, D., Hosoya, H., and Haystead, T. A. (2007) ROCK1 phosphorylates and activates ZIP kinase. J. Biol. Chem. 282: 4884-4893.
27. Shohat, G., Spivak-Kroizman, T., Cohen, O., Bialik, S., Shani, G., Berrisi, H., Eisenstein, M., and Kimchi, A. (2001) The pro-apoptotic function of death-associated protein kinase is controlled by a unique inhibitory autophosphorylation-based mechanism. J. Biol.Chem. 276: 47460-47467.
28. Velentza, A. V., Schumacher, A. M., Weiss, C., Egli, M., and Watterson, D. M. (2001) A protein kinase associated with apoptosis and tumor suppression: structure, activity, and discovery of peptide substrates. J. Biol. Chem. 276: 38956-38965.
29. Murata-Hori, M., Suizu, F., Iwasaki, T., Kikuchi, A., and Hosoya, H. (1999) ZIP kinase identified as a novel myosin regulatory light chain kinase in HeLa cells. FEBS Lett. 451: 81-84.
30. Preuss, U., Landsberg, G., and Scheidtmann, K. H. (2003) Novel mitosis-specific phosphorylation of histone H3 at Thr11 mediated by Dlk/ZIP kinase. Nucleic Acids Res. 31: 878-885.
31. Page, G., Kögel, D., Rangnekar, V., and Scheidtmann, K. H. (1999) Interaction partners of Dlk/ZIP kinase: coexpression of Dlk/ZIP kinase and Par-4 results in cytoplasmic retention and apoptosis. Oncogene 18: 7265-7273.
32. Kawai, T., Akira, S., and Reed, J. C. (2003) ZIP kinase triggers apoptosis from nuclear PML oncogenic domains. Mol. Cell. Biol. 23: 6174-6186.
33. Burch, L. R., Scott, M., Pohler, E., Meek, D., and Hupp, T. (2004) Phage-peptide display identifies the interferon-responsive, death-activated protein kinase family as a novel modifier of MDM2 and p21WAF1. J. Mol. Biol. 337: 115-128.
34. Haystead TA. (2005) ZIP kinase, a key regulator of myosin protein phosphatase 1. Cell Signal. 17: 1313-1322.
35. MacDonald, J. A., Eto, M., Borman, M. A., Brautigan, D. L., and Haystead, T. A. (2001) Dual Ser and Thr phosphorylation of CPI-17, an inhibitor of myosin phosphatase, by MYPT-associated kinase. FEBS Lett. 493: 91-94.
36. Sato, N., Kawai, T., Sugiyama, K., Muromoto, R., Imoto, S., Sekine, Y., Ishida, M., Akira, S., and Matsuda, T. (2005) Physical and functional interactions between STAT3 and ZIP kinase. Int. Immunol. 17: 1543-1552.
37. Engemann, H., Heinzel, V., Page, G., Preuss, U., and Scheidtmann, K. H. (2002) DAP-like kinase interacts with the rat homolog of Schizosaccharomyces pombe CDC5 protein, a factor involved in pre-mRNA splicing and required for G2/M phase transition. Nucleic Acids Res. 30: 1408-1417.
38. Wooldridge, A. A., MacDonald, J. A., Erdodi, F., Ma, C., Borman, M. A., Hartshorne, D. J., and Haystead, T. A. (2004) Smooth muscle phosphatase is regulated in vivo by exclusion of phosphorylation of threonine 696 of MYPT1 by phosphorylation of Serine 695 in response to cyclic nucleotides. J. Biol. Chem. 279: 34496-34504.
39. Page, G., Lödige, I., Kögel, D., and Scheidtmann, K. H. (1999) AATF, a novel transcription factor that interacts with Dlk/ZIP kinase and interferes with apoptosis. FEBS Lett. 462: 187-191.
40. Ito, M., Nakano, T., Erdodi, F., and Hartshorne, D. J. (2004) Myosin phosphatase: structure, regulation and function. Mol. Cell. Biochem. 259: 197-209.
41. El-Guendy, N. and Rangnekar, V. M. (2003) Apoptosis by Par-4 in cancer and neurodegenerative diseases. Exp. Cell Res. 283: 51-66.
42. Bieberich, E., MacKinnon, S., Silva, J., Noggle, S., and Condie, B. G. (2003) Regulation of cell death in mitotic neural progenitor cells by asymmetric distribution of prostate apoptosis response 4 (PAR-4) and simultaneous elevation of endogenous ceramide. J. Cell Biol. 162: 469-479.
43. Vetterkind, S., Illenberger, S., Kubicek, J., Boosen, M., Appel, S., Nairn, H. Y., Scheidtmann, K. H., and Preuss, U. (2005) Binding of Par-4 to the actin cytoskeleton is essential for Par-4/Dlk-mediated apoptosis. Exp. Cell Res. 305: 392-408.
44. Gurumurthy, S., Goswami, A., Vasudevan, K. M., and Rangnekar, V. M. (2005) Phosphorylation of Par-4 by protein kinase A is critical for apoptosis. Mol. Cell. Biol. 25: 1146-1161.
45. Goswami, A., Burikhanov, R., de Thonel, A., Fujita, N., Goswami, M., Zhao, Y., Eriksson, J. E., Tsuruo, T., and Rangnekar, V. M. (2005) Binding and phosphorylation of par-4 by akt is essential for cancer cell survival. Mol. Cell 20: 33-44.
46. Guo, Q., and Xie, J. (2004) AATF inhibits aberrant production of amyloid beta peptide 1-42 by interacting directly with Par-4. J. Biol. Chem. 279: 4596-4603.
47. Levy, D. E. and Darnell, J. E., Jr. (2002) Stats: transcriptional control and biological impact. Nat. Rev. Mol. Cell Biol. 3: 651-662.
48. Murata-Hori, M., Fukuta, Y., Ueda, K., Iwasaki, T., and Hosoya, H. (2001) HeLa ZIP kinase induces diphosphorylation of myosin II regulatory light chain and reorganization of actin filaments in nonmuscle cells. Oncogene 20: 8175-8183.
49. Komatsu, S. and Ikebe, M. (2004) ZIP kinase is responsible for the phosphorylation of myosin II and necessary for cell motility in mammalian fibroblasts. J. Cell Biol. 165: 243-254.
50. Kögel, D., Reimertz, C., Mech, P., Poppe, M., Fruhwald, M. C., Engemann, H., Scheidtmann, K. H., and Prehn, J. H. (2001) Dlk/ZIP kinase-induced apoptosis in human medulloblastoma cells: requirement of the mitochondrial apoptosis pathway. Br. J. Cancer 85: 1801-1808.
51. Fanciulli, M., Bruno, T., Di Padova, M., De Angelis, R., Iezzi, S., Iacobini, C., Floridi, A., and Passananti, C. (2000) Identification of a novel partner of RNA polymerase II subunit 11, Che- 1, which interacts with and affects the growth suppression function of Rb. FASEB J. 14: 904-912.
52. Bruno, T., De Angelis, R., De Nicola, F., Barbato, C., Di Padova, M., Corbi, N., Libri, V., Benassi, B., Mattei, E., Chersi, A., Soddu, S., Floridi, A., Passananti, C., and Fanciulli, M. (2002) Che-1 affects cell growth by interfering with the recruitment of HDAC1 by Rb. Cancer Cell. 2: 387-399.
53. Leister, P., Burgdorf, S., and Scheidtmann, K. H. (2003) Apoptosis Antagonizing Transcription Factor AATF is a novel co-activator of nuclear hormone receptors. Signal Transduction 3: 17-25.
54. Burgdorf, S., Leister, P., and Scheidtmann, K. H. (2004) TSG101 interacts with apoptosis-antagonizing transcription factor and enhances androgen receptor-mediated transcription by promoting its monoubiquitination. J. Biol. Chem. 279: 17524-17534.
55. Burns, C. G., Ohi, R., Krainer, A. R., and Gould, K. L. (1999) Evidence that Myb-related CDC5 proteins are required for pre-mRNA splicing. Proc. Natl. Acad. Sci. U. S. A. 96: 13789-13794.
56. Fawcett, T. W., Martindale, J. L., Guyton, K. Z., Hai, T., and Holbrook, N. J. (1999) Complexes containing activating transcription factor (ATF)/cAMP-responsive-element-binding protein (CREB) interact with the CCAAT/enhancer-binding protein (C/EBP)-ATF composite site to regulate Gadd153 expression during the stress response. Biochem. J. 339: 135-141.
57. Page, G. (2000) Interaction Partners of DAP like Kinase. Dissertation, University of Bonn.
58. Rutkowski, D. T. and Kaufman, R. J. (2004) A trip to the ER: coping with stress. Trends Cell Biol. 14: 20-28.
59. Nowak, S. J. and Corces, V. G. (2004) Phosphorylation of histone H3: a balancing act between chromosome condensation and transcriptional activation. Trends Genet. 20: 214-220.
60. Gao, S., Wang, H., Lee, P., Melamed, J., Li, C. X., Zhang, F., Wu, H., Zhou, L., and Wang, Z. (2006) Androgen receptor and prostate apoptosis response factor-4 target the c-FLIP gene to determine survival and apoptosis in the prostate gland. J. Mol. Endocrinol. 36: 463-483.
61. Bernstein, H. S. and Coughlin, S. R. (1997) Pombe Cdc5-related protein. A putative human transcription factor implicated in mitogen-activated signaling. J. Biol. Chem. 272: 5833-5837.
62. Lei, X. H., Shen, X., Xu, X. Q.., and Bernstein, H. S. (2000) Human Cdc5, a regulator of mitotic entry, can act as a site-specific DNA binding protein. J. Cell Sci. 113: 4523-4531.
63. Burns, C. G., Ohi, R., Mehta, S., O'Toole, E. T., Winey, M., Clark, T. A., Sugnet, C. W., Ares, M., Jr., and Gould, K. L. (2002) Removal of a single alpha-tubulin gene intron suppresses cell cycle arrest phenotypes of splicing factor mutations in Saccharomyces cerevisiae. Mol. Cell Biol. 22: 801-815.
64. Niiro, N. and Ikebe, M. (2001) Zipper-interacting protein kinase induces Ca(2+)-free smooth muscle contraction via myosin light chain phosphorylation. J. Biol. Chem. 276: 29567-29574.
65. Ng, D. C., Lin, B. H., Lim, C. P., Huang, G., Zhang, T., Poli, V., and Cao, X. (2006) Stat3 regulates microtubules by antagonizing the depolymerization activity of stathmin. J. Cell Biol. 172: 245-257.
66. Van Hooser, A. A., Ouspenski, I. I., Gregson, H. C., Starr, D. A., Yen, T. J., Goldberg, M. L., Yokomori, K., Earnshaw, W. C., Sullivan, K. F., and Brinkley, B. R. (2001) Specification of kinetochore-forming chromatin by the histone H3 variant CENP-A. J Cell Sci. 114: 3529-3542.
67. Zeitlin, S. G., Barber, C. M., Allis, C. D., Sullivan, K. F., and Sullivan, K. (2001) Differential regulation of CENP-A and histone H3 phosphorylation in G2/M. J. Cell Sci. 114: 653-661.
68. Kunitoku, N., Sasayama, T., Marumoto, T., Zhang, D., Honda, S., Kobayashi, O., Hatakeyama, K., Ushio, Y., Saya, H., and Hirota, T. (2003) CENP-A phosphorylation by Aurora-A in prophase is required for enrichment of Aurora-B at inner centromeres and for kinetochore function. Dev Cell. 5: 853-864.
69. Matsumura, F. (2005) Regulation of myosin II during cytokinesis in higher eukaryotes. Trends Cell Biol. 15: 371-377.
70. Murata-Hori, M., Fumoto, K., Fukuta, Y., Iwasaki, T., Kikuchi, A., Tatsuka, M., and Hosoya, H. (2000) Myosin II regulatory light chain as a novel substrate for AIM-1, an aurora/Ip11p-related kinase from rat. J. Biochem. (Tokyo) 128: 903-907.