Structure and function of polarity-inducing kinase family MARK/Par-1 within the branch of AMPK/Snf1-related kinases

FASEB Journal

Volumn 24, Issue 6, 2010, Pages 1637-1648

  Marx, A ^a   Nugoor, C ^a,b   Panneerselvam, S ^a,b   Mandelkow, E ^a  

^a MAX PLANCK UNIT FOR STRUCTURAL MOLECULAR BIOLOGY   (Germany)

^b DESY   (Germany)

Author keywords

Alzheimer disease; Autoinhibitory domain; KA1; Kinase structure; Neurodegeneration; UBA domain

Indexed keywords

ADENYLATE KINASE; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 2; PROTEINASE ACTIVATED RECEPTOR 3;

AUTOREGULATION; CATALYSIS; CELL COMMUNICATION; CRYSTAL STRUCTURE; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; ENZYME STRUCTURE; HUMAN; INTRACELLULAR TRANSPORT; MICROTUBULE; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MOTIF; REVIEW; STRUCTURE ANALYSIS; TAUOPATHY;

ANIMALS; HUMANS; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; RECEPTOR, PAR-1;

CAENORHABDITIS ELEGANS; MAMMALIA;

EID: 77953510471     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.09-148064     Document Type: Review

References (62)

1. Drewes, G., Ebneth, A., Preuss, U., Mandelkow, E. M., and Mandelkow, E. (1997) MARK, a novel family of protein kinases that phosphorylate microtubule-associated proteins and trigger microtubule disruption. Cell 89, 297-308 (Pubitemid 27199901)
2. Kemphues, K. (2000) PARsing embryonic polarity. Cell 101, 345-348
3. Goldstein, B., and Macara, I. G. (2007) The PAR proteins: fundamental players in animal cell polarization. Dev. Cell. 13, 609-622
4. Matenia, D., and Mandelkow, E. M. (2009) The tau of MARK: a polarized view of the cytoskeleton. Trends Biochem. Sci. 34, 332-342
5. Mocanu, M. M., Nissen, A., Eckermann, K., Khlistunova, I., Biernat, J., Drexler, D., Petrova, O., Schonig, K., Bujard, H., Mandelkow, E., Zhou, L., Rune, G., and Mandelkow, E. M. (2008) The potential for beta-structure in the repeat domain of tau protein determines aggregation, synaptic decay, neuronal loss, and coassembly with endogenous Tau in inducible mouse models of tauopathy. J. Neurosci. 28, 737-748
6. 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
7. Cohen, P., and Goedert, M. (2004) GSK3 inhibitors: development and therapeutic potential. Nat. Rev. 3, 479-487 (Pubitemid 38807530)
8. Zhou, G., Myers, R., Li, Y., Chen, Y., Shen, X., Fenyk-Melody, J., Wu, M., Ventre, J., Doebber, T., Fujii, N., Musi, N., Hirshman, M. F., Goodyear, L. J., and Moller, D. E. (2001) Role of AMP-activated protein kinase in mechanism of metformin action. J. Clin. Investig. 108, 1167-1174
9. Bright, N. J., Thornton, C., and Carling, D. (2009) The regulation and function of mammalian AMPK-related kinases. Acta Physiologica 196, 15-26
10. Timm, T., Marx, A., Panneerselvam, S., Mandelkow, E., and Mandelkow, E. M. (2008) Structure and regulation of MARK, a kinase involved in abnormal phosphorylation of Tau protein. BMC Neurosci. 9(Suppl. 2), S9
11. Dequiedt, F., Martin, M., Von Blume, J., Vertommen, D., Lecomte, E., Mari, N., Heinen, M. F., Bachmann, M., Twizere, J. C., Huang, M. C., Rider, M. H., Piwnica-Worms, H., Seufferlein, T., and Kettmann, R. (2006) New role for hPar-1 kinases EMK and C-TAK1 in regulating localization and activity of class IIa histone deacetylases. Mol. Cell. Biol. 26, 7086-7102
12. Muller, J., Ritt, D. A., Copeland, T. D., and Morrison, D. K. (2003) Functional analysis of C-TAK1 substrate binding and identification of PKP2 as a new C-TAK1 substrate. EMBO J. 22, 4431-4442
13. Zhang, S. H., Kobayashi, R., Graves, P. R., Piwnica-Worms, H., and Tonks, N. K. (1997) Serine phosphorylation-dependent association of the band 4.1-related protein-tyrosine phosphatase PTPH1 with 14-3-3beta protein. J. Biol. Chem. 272, 27281-27287
14. Kato, T., Satoh, S., Okabe, H., Kitahara, O., Ono, K., Kihara, C., Tanaka, T., Tsunoda, T., Yamaoka, Y., Nakamura, Y., and Furukawa, Y. (2001) Isolation of a novel human gene, MARKL1, homologous to MARK3 and its involvement in hepatocellular carcinogenesis. Neoplasia 3, 4-9 (Pubitemid 32201604)
15. Moroni, R. F., De Biasi, S., Colapietro, P., Larizza, L., and Beghini, A. (2006) Distinct expression pattern of microtubule-associated protein/microtubule affinity-regulating kinase 4 in differentiated neurons. Neuroscience 143, 83-94
16. Beghini, A., Magnani, I., Roversi, G., Piepoli, T., Di Terlizzi, S., Moroni, R. F., Pollo, B., Fuhrman Conti, A. M., Cowell, J. K., Finocchiaro, G., and Larizza, L. (2003) The neural progenitor-restricted isoform of the MARK4 gene in 19q13.2 is upregulated in human gliomas and overexpressed in a subset of glioblastoma cell lines. Oncogene 22, 2581-2591 (Pubitemid 36605606)
17. Timm, T., Li, X. Y., Biernat, J., Jiao, J., Mandelkow, E., Vandekerckhove, J., and Mandelkow, E. M. (2003) MARKK, a Ste20-like kinase, activates the polarity-inducing kinase MARK/PAR-1. EMBO J. 22, 5090-5101
18. Lizcano, J. M., Goransson, O., Toth, R., Deak, M., Morrice, N. A., Boudeau, J., Hawley, S. A., Udd, L., Makela, T. P., Hardie, D. G., and Alessi, D. R. (2004) LKB1 is a master kinase that activates 13 kinases of the AMPK subfamily, including MARK/PAR-1. EMBO J. 23, 833-843
19. Timm, T., Balusamy, K., Li, X., Biernat, J., Mandelkow, E., and Mandelkow, E. M. (2008) Glycogen synthase kinase (GSK) 3beta directly phosphorylates Serine 212 in the regulatory loop and inhibits microtubule affinity-regulating kinase (MARK) 2. J. Biol. Chem. 283, 18873-18882
20. Uboha, N. V., Flajolet, M., Nairn, A. C., and Picciotto, M. R. (2007) A calcium- and calmodulin-dependent kinase Ialpha/microtubule affinity regulating kinase 2 signaling cascade mediates calcium-dependent neurite outgrowth. J. Neurosci. 27, 4413-4423
21. Bachmann, M., Hennemann, H., Xing, P. X., Hoffmann, I., and Moroy, T. (2004) The oncogenic serine/threonine kinase Pim-1 phosphorylates and inhibits the activity of Cdc25C-associated kinase 1 (C-TAK1): a novel role for Pim-1 at the G2/M cell cycle checkpoint. J. Biol. Chem. 279, 48319-48328
22. Hurov, J. B., Watkins, J. L., and Piwnica-Worms, H. (2004) Atypical PKC phosphorylates PAR-1 kinases to regulate localization and activity. Curr. Biol. 14, 736-741
23. Suzuki, A., Hirata, M., Kamimura, K., Maniwa, R., Yamanaka, T., Mizuno, K., Kishikawa, M., Hirose, H., Amano, Y., Izumi, N., Miwa, Y., and Ohno, S. (2004) aPKC acts upstream of PAR-1b in both the establishment and maintenance of mammalian epithelial polarity. Curr. Biol. 14, 1425-1435
24. Watkins, J. L., Lewandowski, K. T., Meek, S. E., Storz, P., Toker, A., and Piwnica-Worms, H. (2008) Phosphorylation of the Par-1 polarity kinase by protein kinase D regulates 14-3-3 binding and membrane association. Proc. Natl. Acad. Sci. U. S. A. 105, 18378-18383
25. Matenia, D., Griesshaber, B., Li, X. Y., Thiessen, A., Johne, C., Jiao, J., Mandelkow, E., and Mandelkow, E. M. (2005) PAK5 kinase is an inhibitor of MARK/Par-1, which leads to stable microtubules and dynamic actin. Mol. Biol. Cell 16, 4410-4422
26. Lu, H., Murata-Kamiya, N., Saito, Y., and Hatakeyama, M. (2009) Role of partitioning-defective 1/microtubule affinity-regulating kinases in the morphogenetic activity of Helicobacter pylori CagA. J. Biol. Chem. 284, 23024-23036
27. Jaleel, M., Villa, F., Deak, M., Toth, R., Prescott, A. R., Van Aalten, D. M., and Alessi, D. R. (2006) The ubiquitin-associated domain of AMPK-related kinases regulates conformation and LKB1-mediated phosphorylation and activation. Biochem. J. 394, 545-555
28. Marx, A., Nugoor, C., Muller, J., Panneerselvam, S., Timm, T., Bilang, M., Mylonas, E., Svergun, D. I., Mandelkow, E. M., and Mandelkow, E. (2006) Structural variations in the catalytic and ubiquitin-associated domains of microtubule-associated protein/microtubule affinity regulating kinase (MARK) 1 and MARK2. J. Biol. Chem. 281, 27586-27599
29. Panneerselvam, S., Marx, A., Mandelkow, E. M., and Mandelkow, E. (2006) Structure of the catalytic and ubiquitin-associated domains of the protein kinase MARK/Par-1. Structure 14, 173-183
30. Elbert, M., Rossi, G., and Brennwald, P. (2005) The yeast par-1 homologs kin1 and kin2 show genetic and physical interactions with components of the exocytic machinery. Mol. Biol. Cell 16, 532-549
31. Chen, L., Jiao, Z. H., Zheng, L. S., Zhang, Y. Y., Xie, S. T., Wang, Z. X., and Wu, J. W. (2009) Structural insight into the autoinhibition mechanism of AMP-activated protein kinase. Nature 459, 1146-1149
32. Nayak, V., Zhao, K., Wyce, A., Schwartz, M. F., Lo, W. S., Berger, S. L., and Marmorstein, R. (2006) Structure and dimerization of the kinase domain from yeast Snf1, a member of the Snf1/AMPK protein family. Structure 14, 477-485
33. Scholz, R., Suter, M., Weimann, T., Polge, C., Konarev, P. V., Thali, R. F., Tuerk, R. D., Viollet, B., Wallimann, T., Schlattner, U., and Neumann, D. (2009) Homooligomerization and activation of AMP-activated protein kinase is mediated by the kinase domain αG-helix. J. Biol. Chem. 284, 27425-27437
34. Raasi, S., Varadan, R., Fushman, D., and Pickart, C. M. (2005) Diverse polyubiquitin interaction properties of ubiquitin-associated domains. Nat. Struct. Mol. Biol. 12, 708-714
35. Varadan, R., Assfalg, M., Raasi, S., Pickart, C., and Fushman, D. (2005) Structural determinants for selective recognition of a Lys48-linked polyubiquitin chain by a UBA domain. Mol. Cell. 18, 687-698
36. Finn, R. D., Tate, J., Mistry, J., Coggill, P. C., Sammut, S. J., Hotz, H. R., Ceric, G., Forslund, K., Eddy, S. R., Sonnhammer, E. L., and Bateman, A. (2008) The Pfam protein families database. Nucleic Acids Res. 36, D281-D288
37. Hulo, N., Bairoch, A., Bulliard, V., Cerutti, L., Cuche, B. A., de Castro, E., Lachaize, C., Langendijk-Genevaux, P. S., and Sigrist, C. J. (2008) The 20 years of PROSITE. Nucleic Acids Res. 36, D245-D249
38. Tochio, N., Koshiba, S., Kobayashi, N., Inoue, M., Yabuki, T., Aoki, M., Seki, E., Matsuda, T., Tomo, Y., Motoda, Y., Kobayashi, A., Tanaka, A., Hayashizaki, Y., Terada, T., Shirouzu, M., Kigawa, T., and Yokoyama, S. (2006) Solution structure of the kinase-associated domain 1 of mouse microtubule-associated protein/microtubule affinity-regulating kinase 3. Protein Sci. 15, 2534-2543
39. Murphy, J. M., Korzhnev, D. M., Ceccarelli, D. F., Briant, D. J., Zarrine-Afsar, A., Sicheri, F., Kay, L. E., and Pawson, T. (2007) Conformational instability of the MARK3 UBA domain compromises ubiquitin recognition and promotes interaction with the adjacent kinase domain. Proc. Natl. Acad. Sci. U. S. A. 104, 14336-14341
40. Pellicena, P., and Kuriyan, J. (2006) Protein-protein interactions in the allosteric regulation of protein kinases. Curr. Opin. Struct. Biol. 16, 702-709
41. Tanoue, T., Adachi, M., Moriguchi, T., and Nishida, E. (2000) A conserved docking motif in MAP kinases common to substrates, activators and regulators. Nat. Cell Biol. 2, 110-116
42. Nolen, B., Taylor, S., and Ghosh, G. (2004) Regulation of protein kinases: controlling activity through activation segment conformation. Mol. Cell 15, 661-675
43. Xu, W., Doshi, A., Lei, M., Eck, M. J., and Harrison, S. C. (1999) Crystal structures of c-Src reveal features of its autoinhibitory mechanism. Mol. Cell 3, 629-638
44. Winder, W. W., and Hardie, D. G. (1999) AMP-activated protein kinase, a metabolic master switch: possible roles in type 2 diabetes. Am. J. Physiol. 277, E1-E10
45. Hawley, S. A., Davison, M., Woods, A., Davies, S. P., Beri, R. K., Carling, D., and Hardie, D. G. (1996) Characterization of the AMP-activated protein kinase kinase from rat liver and identification of threonine 172 as the major site at which it phosphorylates AMP-activated protein kinase. J. Biol. Chem. 271, 27879-27887
46. Crute, B. E., Seefeld, K., Gamble, J., Kemp, B. E., and Witters, L. A. (1998) Functional domains of the alpha1 catalytic subunit of the AMP-activated protein kinase. J. Biol. Chem. 273, 35347-35354
47. Terabayashi, T., Funato, Y., and Miki, H. (2008) Dishevelled-induced phosphorylation regulates membrane localization of Par1b. Biochem. Biophys. Res. Commun. 375, 660-665
48. Al-Hakim, A. K., Zagorska, A., Chapman, L., Deak, M., Peggie, M., and Alessi, D. R. (2008) Control of AMPK-related kinases by USP9X and atypical Lys(29)/Lys(33)-linked polyubiquitin chains. Biochem. J. 411, 249-260
49. Inglis, J. D., Lee, M., and Hill, R. E. (1993) Emk, a protein kinase with homologs in yeast maps to mouse chromosome 19. Mamm. Genome 4, 401-403
50. Espinosa, L., and Navarro, E. (1998) Human serine/threonine protein kinase EMK1: genomic structure and cDNA cloning of isoforms produced by alternative splicing. Cytogenet. Cell Genet. 81, 278-282 (Pubitemid 28431958)
51. Beullens, M., Vancauwenbergh, S., Morrice, N., Derua, R., Ceulemans, H., Waelkens, E., and Bollen, M. (2005) Substrate specificity and activity regulation of protein kinase MELK. J. Biol. Chem. 280, 40003-40011
52. Sapir, T., Sapoznik, S., Levy, T., Finkelshtein, D., Shmueli, A., Timm, T., Mandelkow, E. M., and Reiner, O. (2008) Accurate balance of the polarity kinase MARK2/Par-1 is required for proper cortical neuronal migration. J. Neurosci. 28, 5710-5720
53. Bryson, K., McGuffin, L. J., Marsden, R. L., Ward, J. J., Sodhi, J. S., and Jones, D. T. (2005) Protein structure prediction servers at University College London. Nucleic Acids Res. 33, W36-W38
54. Kabsch, W., and Sander, C. (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22, 2577-2637
55. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291
56. DeLano, W. L. (2002) PyMOL. DeLano Scientific, San Carlos, CA, USA
57. Mueller, T. D., and Feigon, J. (2002) Solution structures of UBA domains reveal a conserved hydrophobic surface for proteinprotein interactions. J. Mol. Biol. 319, 1243-1255
58. Tanoue, T., Maeda, R., Adachi, M., and Nishida, E. (2001) Identification of a docking groove on ERK and p38 MAP kinases that regulates the specificity of docking interactions. EMBO J. 20, 466-479
59. Townley, R., and Shapiro, L. (2007) Crystal structures of the adenylate sensor from fission yeast AMP-activated protein kinase. Science 315, 1726-1729
60. Amodeo, G. A., Rudolph, M. J., and Tong, L. (2007) Crystal structure of the heterotrimer core of Saccharomyces cerevisiae AMPK homologue SNF1. Nature 449, 492-495
61. Xiao, B., Heath, R., Saiu, P., Leiper, F. C., Leone, P., Jing, C., Walker, P. A., Haire, L., Eccleston, J. F., Davis, C. T., Martin, S. R., Carling, D., and Gamblin, S. J. (2007) Structural basis for AMP binding to mammalian AMP-activated protein kinase. Nature 449, 496-500 (Pubitemid 47509548)
62. Nešić, D., Miller, M. C., Quinkert, Z. T., Stein, M., Chait, B. T., and Stebbins, C. E. (2010) Helicobacter pylori CagA inhibits PAR1-MARK family kinases by mimicking host substrates. Nat. Struct. Mol. Biol. 17, 130-132