The microtubule affinity regulating kinase MARK4 promotes axoneme extension during early ciliogenesis

Journal of Cell Biology

Volumn 200, Issue 4, 2013, Pages 505-522

  Kuhns, Stefanie ^a   Schmidt, Kerstin N ^a   Reymann, Jürgen ^a   Gilbert, Daniel F ^a,d   Neuner, Annett ^a   Hub, Birgit ^b   Carvalho, Ricardo ^a,c   Wiedemann, Philipp ^c   Zentgraf, Hanswalter ^b   Erfle, Holger ^a   Klingmüller, Ursula ^a   Boutros, Michael ^a   Pereira, Gislene ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c UNIVERSITY OF APPLIED SCIENCES   (Germany)

^d UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; MICROTUBULE AFFINITY REGULATING KINASE 4; PHOSPHOTRANSFERASE; PROTEIN CEP97; PROTEIN CP110; PROTEIN ODF2; UNCLASSIFIED DRUG;

ARTICLE; AXONEME; CATALYSIS; CENTRIOLE; CONTROLLED STUDY; ENZYME ACTIVITY; EUKARYOTIC FLAGELLUM; HUMAN; HUMAN CELL; KINETOSOME; MOLECULAR INTERACTION; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RNA INTERFERENCE;

ANIMALS; AXONEME; CELL CYCLE PROTEINS; CELL LINE; CILIA; HEAT-SHOCK PROTEINS; HEK293 CELLS; HUMANS; MICE; MICROTUBULE-ASSOCIATED PROTEINS; MODELS, BIOLOGICAL; NIH 3T3 CELLS; PHOSPHOPROTEINS; PROTEIN-SERINE-THREONINE KINASES; RNA INTERFERENCE;

EID: 84874364274     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201206013     Document Type: Article

References (61)

1. Anderson, C.T., and T. Stearns. 2009. Centriole age underlies asynchronous primary cilium growth in mammalian cells. Curr. Biol. 19:1498-1502. http://dx.doi.org/10.1016/j.cub.2009.07.034
2. Boehlke, C., F. Kotsis, V. Patel, S. Braeg, H. Voelker, S. Bredt, T. Beyer, H. Janusch, C. Hamann, M. Gödel, et al. 2010 Primary cilia regulate mTORC1 activity and cell size through Lkb1. Nat. Cell Biol. 12:1115- 1122. http://dx.doi.org/10.1038/ncb2117
3. Boesger, J., V. Wagner, W. Weisheit, and M. Mittag. 2009. Analysis of flagellar phosphoproteins from Chlamydomonas reinhardtii. Eukaryot. Cell. 8:922-932. http://dx.doi.org/10.1128/EC.00067-09
4. Brajenovic, M., G. Joberty, B. Küster, T. Bouwmeester, and G. Drewes. 2004. Comprehensive proteomic analysis of human Par protein complexes reveals an interconnected protein network. J. Biol. Chem. 279:12804- 12811. http://dx.doi.org/10.1074/jbc.M312171200
5. Cao, M., G. Li, and J. Pan. 2009. Regulation of cilia assembly, disassembly, and length by protein phosphorylation. Methods Cell Biol. 94:333-346. http://dx.doi.org/10.1016/S0091-679X(08)94017-6
6. Cheeseman, I.M., and A. Desai. 2005. A combined approach for the localization and tandem affinity purification of protein complexes from metazoans. Sci. STKE. 2005:pl1. http://dx.doi.org/10.1126/stke.2662005pl1
7. Dammermann, A., and A. Merdes. 2002. Assembly of centrosomal proteins and microtubule organization depends on PCM-1. J. Cell Biol. 159:255-266. http://dx.doi.org/10.1083/jcb.200204023
8. D'Angelo, A., and B. Franco. 2009. The dynamic cilium in human diseases. Pathogenetics. 2:3. http://dx.doi.org/10.1186/1755-8417-2-3 Drewes, G., A. Ebneth, and E.M. Mandelkow. 1998. MAPs, MARKs and microtubule dynamics. Trends Biochem. Sci. 23:307-311. http://dx.doi.org/ 10.1016/S0968-0004(98)01245-6
9. Drewes, G., A. Ebneth, and E.M. Mandelkow. 1998. MAPs, MARKs and microtubule dynamics. Trends Biochem. Sci. 23:307-311. http://dx.doi.org/10.1016/S0968-0004(98)01245-6
10. Fliegauf, M., T. Benzing, and H. Omran. 2007. When cilia go bad: cilia defects and ciliopathies. Nat. Rev. Mol. Cell Biol. 8:880-893. http://dx.doi.org/10.1038/nrm2278
11. Follit, J.A., R.A. Tuft, K.E. Fogarty, and G.J. Pazour. 2006. The intraflagellar transport protein IFT20 is associated with the Golgi complex and is required for cilia assembly. Mol. Biol. Cell. 17:3781-3792. http://dx.doi.org/10.1091/mbc.E06-02-0133
12. Ghossoub, R., A. Molla-Herman, P. Bastin, and A. Benmerah. 2011. The ciliary pocket: a once-forgotten membrane domain at the base of cilia. Biol. Cell. 193:131-144. http://dx.doi.org/10.1042/BC20100128
13. Gossen, M., and H. Bujard. 1992. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc. Natl. Acad. Sci. USA. 89:5547-5551. http://dx.doi.org/10.1073/pnas.89.12.5547
14. Graser, S., Y.D. Stierhof, S.B. Lavoie, O.S. Gassner, S. Lamla, M. Le Clech, and E.A. Nigg. 2007. Cep164, a novel centriole appendage protein required for primary cilium formation. J. Cell Biol. 179:321-330. http://dx.doi.org/10.1083/jcb.200707181
15. Guarguaglini, G., P.I. Duncan, Y.D. Stierhof, T. Holmström, S. Duensing, and E.A. Nigg. 2005. The forkhead-associated domain protein Cep170 interacts with Polo-like kinase 1 and serves as a marker for mature centrioles. Mol. Biol. Cell. 16:1095-1107. http://dx.doi.org/10.1091/mbc.E04-10-0939
16. Hurov, J., and H. Piwnica-Worms. 2007. The Par-1/MARK family of protein kinases: from polarity to metabolism. Cell Cycle. 6:1966-1969. http://dx.doi.org/10.4161/cc.6.16.4576
17. Inglis, P.N., K.A. Boroevich, and M.R. Leroux. 2006. Piecing together a ciliome. Trends Genet. 22:491-500. http://dx.doi.org/10.1016/j.tig.2006.07.006 Ishikawa, H., and W.F. Marshall. 2011. Ciliogenesis: building the cell's antenna. Nat. Rev. Mol. Cell Biol. 12:222-234. http://dx.doi.org/10.1038/nrm3085
18. Ishikawa, H., and W.F. Marshall. 2011. Ciliogenesis: building the cell's antenna. Nat. Rev. Mol. Cell Biol. 12:222-234. http://dx.doi.org/10.1038/nrm3085
19. Ishikawa, H., A. Kubo, S. Tsukita, and S. Tsukita. 2005. Odf2-deficient mother centrioles lack distal/subdistal appendages and the ability to generate primary cilia. Nat. Cell Biol. 7:517-524. http://dx.doi.org/10.1038/ncb1251
20. Jacob, L.S., X. Wu, M.E. Dodge, C.W. Fan, O. Kulak, B. Chen, W. Tang, B. Wang, J.F. Amatruda, and L. Lum. 2011. Genome-wide RNAi screen reveals disease-associated genes that are common to Hedgehog and Wnt signaling. Sci. Signal. 4:ra4. http://dx.doi.org/10.1126/scisignal.2001225
21. Janke, C., and J.C. Bulinski. 2011. Post-translational regulation of the microtubule cytoskeleton: mechanisms and functions. Nat. Rev. Mol. Cell Biol. 12:773-786. http://dx.doi.org/10.1038/nrm3227
22. Jurczyk, A., A. Gromley, S. Redick, J. San Agustin, G. Witman, G.J. Pazour, D.J. Peters, and S. Doxsey. 2004. Pericentrin forms a complex with intraflagellar transport proteins and polycystin-2 and is required for primary cilia assembly. J. Cell Biol. 166:637-643. http://dx.doi.org/10.1083/jcb.200405023
23. Kato, T., S. Satoh, H. Okabe, O. Kitahara, K. Ono, C. Kihara, T. Tanaka, T. Tsunoda, Y. Yamaoka, Y. Nakamura, and Y. Furukawa. 2001. Isolation of a novel human gene, MARKL1, homologous to MARK3 and its involvement in hepatocellular carcinogenesis. Neoplasia. 3:4-9. http://dx.doi.org/10.1038/sj.neo.7900132
24. Ketteler, R., S. Glaser, O. Sandra, U.M. Martens, and U. Klingmüller. 2002. Enhanced transgene expression in primitive hematopoietic progenitor cells and embryonic stem cells efficiently transduced by optimized retroviral hybrid vectors. Gene Ther. 9:477-487. http://dx.doi.org/10.1038/sj.gt.3301653
25. Kim, J., J.E. Lee, S. Heynen-Genel, E. Suyama, K. Ono, K. Lee, T. Ideker, P. Aza-Blanc, and J.G. Gleeson. 2010. Functional genomic screen for modulators of ciliogenesis and cilium length. Nature. 464:1048-1051. http://dx.doi.org/10.1038/nature08895
26. Knödler, A., S. Feng, J. Zhang, X. Zhang, A. Das, J. Peränen, and W. Guo. 2010. Coordination of Rab8 and Rab11 in primary ciliogenesis. Proc. Natl. Acad. Sci. USA. 197:6346-6351. http://dx.doi.org/10.1073/pnas.1002401107
27. Kunimoto, K., Y. Yamazaki, T. Nishida, K. Shinohara, H. Ishikawa, T. Hasegawa, T. Okanoue, H. Hamada, T. Noda, A. Tamura, et al. 2012. Coordinated ciliary beating requires Odf2-mediated polarization of basal bodies via basal feet. Cell. 148:189-200. http://dx.doi.org/10.1016/j.cell.2011.10.052
28. Lange, B.M., and K. Gull. 1995. A molecular marker for centriole maturation in the mammalian cell cycle. J. Cell Biol. 130:919-927. http://dx.doi.org/10.1083/jcb.130.4.919
29. Lizcano, J.M., O. Göransson, R. Toth, M. Deak, N.A. Morrice, J. Boudeau, S.A. Hawley, L. Udd, T.P. Mäkelä, D.G. Hardie, and D.R. Alessi. 2004. LKB1 is a master kinase that activates 13 kinases of the AMPK subfamily, including MARK/PAR-1. EMBO J. 23:833-843. http://dx.doi.org/10.1038/sj.emboj.7600110
30. Lopes, C.A., S.L. Prosser, L. Romio, R.A. Hirst, C. O'Callaghan, A.S. Woolf, and A.M. Fry. 2011. Centriolar satellites are assembly points for proteins implicated in human ciliopathies, including oral-facial-digital syndrome 1. J. Cell Sci. 124:600-612. http://dx.doi.org/10.1242/jcs.077156
31. Marx, A., C. Nugoor, S. Panneerselvam, and E. Mandelkow. 2010. Structure and function of polarity-inducing kinase family MARK/Par-1 within the branch of AMPK/Snf1-related kinases. FASEB J. 24:1637-1648. http://dx.doi.org/10.1096/fj.09-148064
32. Matenia, D., and E.M. Mandelkow. 2009. The tau of MARK: a polarized view of the cytoskeleton. Trends Biochem. Sci. 34:332-342. http://dx.doi.org/10.1016/j.tibs.2009.03.008
33. Mikule, K., B. Delaval, P. Kaldis, A. Jurcyzk, P. Hergert, and S. Doxsey. 2007. Loss of centrosome integrity induces p38-p53-p21-dependent G1-S arrest. Nat. Cell Biol. 9:160-170. http://dx.doi.org/10.1038/ncb1529 Mitchison, T., and M. Kirschner. 1984. Microtubule assembly nucleated by isolated centrosomes. Nature. 312:232-237. http://dx.doi.org/10.1038/312232a0
34. Mitchison, T., and M. Kirschner. 1984. Microtubule assembly nucleated by isolated centrosomes. Nature. 312:232-237. http://dx.doi.org/10.1038/312232a0
35. Moroni, R.F., S. De Biasi, P. Colapietro, L. Larizza, and A. Beghini. 2006. Distinct expression pattern of microtubule-associated protein/microtubule affinity-regulating kinase 4 in differentiated neurons. Neuroscience. 143:83-94. http://dx.doi.org/10.1016/j.neuroscience.2006.07.052
36. Nakagawa, Y., Y. Yamane, T. Okanoue, S. Tsukita, and S. Tsukita. 2001. Outer dense fiber 2 is a widespread centrosome scaffold component preferentially associated with mother centrioles: its identification from isolated centrosomes. Mol. Biol. Cell. 12:1687-1697.
37. Nigg, E.A., and J.W. Raff. 2009. Centrioles, centrosomes, and cilia in health and disease. Cell. 139:663-678. http://dx.doi.org/10.1016/j.cell.2009.10.036
38. Pazour, G.J., B.L. Dickert, Y. Vucica, E.S. Seeley, J.L. Rosenbaum, G.B. Witman, and D.G. Cole. 2000. Chlamydomonas IFT88 and its mouse homologue, polycystic kidney disease gene tg737, are required for assembly of cilia and flagella. J. Cell Biol. 151:709-718. http://dx.doi.org/10.1083/jcb.151.3.709
39. Pazour, G.J., S.A. Baker, J.A. Deane, D.G. Cole, B.L. Dickert, J.L. Rosenbaum, G.B. Witman, and J.C. Besharse. 2002. The intraflagellar transport protein, IFT88, is essential for vertebrate photoreceptor assembly and maintenance. J. Cell Biol. 157:103-113. http://dx.doi.org/10.1083/jcb.200107108
40. Pedersen, L.B., and J.L. Rosenbaum. 2008. Intraflagellar transport (IFT) role in ciliary assembly, resorption and signalling. Curr. Top. Dev. Biol. 85:23- 61. http://dx.doi.org/10.1016/S0070-2153(08)00802-8
41. Pfeifer, A.C., D. Kaschek, J. Bachmann, U. Klingmüller, and J. Timmer. 2010. Model-based extension of high-throughput to high-content data. BMC Syst. Biol. 4:106. http://dx.doi.org/10.1186/1752-0509-4-106
42. Piehl, M., U.S. Tulu, P. Wadsworth, and L. Cassimeris. 2004. Centrosome maturation: measurement of microtubule nucleation throughout the cell cycle by using GFP-tagged EB1. Proc. Natl. Acad. Sci. USA. 191:1584-1588. http://dx.doi.org/10.1073/pnas.0308205100
43. Plotnikova, O.V., E.A. Golemis, and E.N. Pugacheva. 2008. Cell cycle-dependent ciliogenesis and cancer. Cancer Res. 68:2058-2061. http://dx.doi.org/10.1158/0008-5472.CAN-07-5838
44. Quarmby, L.M., and J.D. Parker. 2005. Cilia and the cell cycle? J. Cell Biol. 169:707-710. http://dx.doi.org/10.1083/jcb.200503053
45. Rosa, J., P. Canovas, A. Islam, D.C. Altieri, and S.J. Doxsey. 2006. Survivin modulates microtubule dynamics and nucleation throughout the cell cycle. Mol. Biol. Cell. 17:1483-1493. http://dx.doi.org/10.1091/mbc.E05-08-0723
46. Rothbauer, U., K. Zolghadr, S. Muyldermans, A. Schepers, M.C. Cardoso, and H. Leonhardt. 2008. A versatile nanotrap for biochemical and functional studies with fluorescent fusion proteins. Mol. Cell. Proteomics. 7:282-289.
47. Santos, N., and J.F. Reiter. 2008. Building it up and taking it down: the regulation of vertebrate ciliogenesis. Dev. Dyn. 237:1972-1981. http://dx.doi.org/10.1002/dvdy.21540
48. Schmidt, T.I., J. Kleylein-Sohn, J. Westendorf, M. Le Clech, S.B. Lavoie, Y.D. Stierhof, and E.A. Nigg. 2009. Control of centriole length by CPAP and CP110. Curr. Biol. 19:1005-1011. http://dx.doi.org/10.1016/j.cub.2009.05.016
49. Schmidt, K.N., S. Kuhns, A. Neuner, B. Hub, H. Zentgraf, and G. Pereira. 2012. Cep164 mediates vesicular docking to the mother centriole during early steps of ciliogenesis. J. Cell Biol. 199:1083-1101. http://dx.doi.org/10.1083/jcb.201202126
50. Sironi, L., J. Solon, C. Conrad, T.U. Mayer, D. Brunner, and J. Ellenberg. 2011. Automatic quantification of microtubule dynamics enables RNAi-screening of new mitotic spindle regulators. Cytoskeleton (Hoboken). 68:266-278. http://dx.doi.org/10.1002/cm.20510
51. Sorokin, S. 1962. Centrioles and the formation of rudimentary cilia by fibroblasts and smooth muscle cells. J. Cell Biol. 15:363-377. http://dx.doi.org/10.1083/jcb.15.2.363
52. Sorokin, S.P. 1968. Reconstructions of centriole formation and ciliogenesis in mammalian lungs. J. Cell Sci. 3:207-230.
53. Soung, N.K., J.E. Park, L.R. Yu, K.H. Lee, J.M. Lee, J.K. Bang, T.D. Veenstra, K. Rhee, and K.S. Lee. 2009. Plk1-dependent and -independent roles of an ODF2 splice variant, hCenexin1, at the centrosome of somatic cells. Dev. Cell. 16:539-550. http://dx.doi.org/10.1016/j.devcel.2009.02.004
54. Spektor, A., W.Y. Tsang, D. Khoo, and B.D. Dynlacht. 2007. Cep97 and CP110 suppress a cilia assembly program. Cell. 130:678-690. http://dx.doi.org/10.1016/j.cell.2007.06.027
55. Tassan, J.P., and X. Le Goff. 2004. An overview of the KIN1/PAR-1/MARK kinase family. Biol. Cell. 96:193-199. http://dx.doi.org/10.1016/j.biolcel.2003.10.009
56. Timm, T., A. Marx, S. Panneerselvam, E. Mandelkow, and E.M. Mandelkow. 2008. Structure and regulation of MARK, a kinase involved in abnormal phosphorylation of Tau protein. BMC Neurosci. 9(Suppl. 2):S9. http://dx.doi.org/10.1186/1471-2202-9-S2-S9
57. Trinczek, B., M. Brajenovic, A. Ebneth, and G. Drewes. 2004. MARK4 is a novel microtubule-associated proteins/microtubule affinity-regulating kinase that binds to the cellular microtubule network and to centrosomes. J. Biol. Chem. 279:5915-5923. http://dx.doi.org/10.1074/jbc.M304528200
58. Westlake, C.J., L.M. Baye, M.V. Nachury, K.J. Wright, K.E. Ervin, L. Phu, C. Chalouni, J.S. Beck, D.S. Kirkpatrick, D.C. Slusarski, et al. 2011. Primary cilia membrane assembly is initiated by Rab11 and transport protein particle II (TRAPPII) complex-dependent trafficking of Rabin8 to the centrosome. Proc. Natl. Acad. Sci. USA. 198:2759-2764. http://dx.doi.org/10.1073/pnas.1018823108
59. Wissing, J., L. Jänsch, M. Nimtz, G. Dieterich, R. Hornberger, G. Kéri, J. Wehland, and H. Daub. 2007. Proteomics analysis of protein kinases by target class-selective prefractionation and tandem mass spectrometry. Mol. Cell. Proteomics. 6:537-547.
60. Wolff, A., M. Houdayer, D. Chillet, B. de Néchaud, and P. Denoulet. 1994. Structure of the polyglutamyl chain of tubulin: occurrence of alpha and gamma linkages between glutamyl units revealed by monoreactive polyclonal antibodies. Biol. Cell. 81:11-16. http://dx.doi.org/10.1016/0248-4900(94)90049-3
61. Yoshimura, S., J. Egerer, E. Fuchs, A.K. Haas, and F.A. Barr. 2007. Functional dissection of Rab GTPases involved in primary cilium formation. J. Cell Biol. 178:363-369. http://dx.doi.org/10.1083/jcb.200703047