A Mec17-Myosin II effector axis coordinates microtubule acetylation and actin dynamics to control primary cilium biogenesis

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Rao, Yanhua ^a   Hao, Rui ^a   Wang, Bin ^a   Yao, Tso Pang ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CEP290 PROTEIN; HISTONE DEACETYLASE 6; MYOSIN IIA; MYOSIN IIB; PCM 1 PROTEIN; PEPTIDES AND PROTEINS; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG; ACTIN; ACYLTRANSFERASE; MEC17 PROTEIN, HUMAN; MYOSIN HEAVY CHAIN; MYOSIN II; NONMUSCLE MYOSIN TYPE IIB HEAVY CHAIN;

ACETYLATION; ARTICLE; BIOGENESIS; CELL ELONGATION; CELL GROWTH; CELL PROLIFERATION; CILIOGENESIS; CONTROLLED STUDY; ENZYME INHIBITION; EUKARYOTIC FLAGELLUM; GENE; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE INDUCTION; HUMAN; HUMAN CELL; MEC17 GENE; MYH10 GENE; MYH9 GENE; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; CELL LINE; CILIUM; GENETICS; METABOLISM; MICROTUBULE;

ACETYLATION; ACETYLTRANSFERASES; ACTINS; CELL LINE; CILIA; HUMANS; MICROTUBULES; MYOSIN HEAVY CHAINS; MYOSIN TYPE II; NONMUSCLE MYOSIN TYPE IIB;

EID: 84918572088     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0114087     Document Type: Article

References (30)

1. Ansley SJ, Badano JL, Blacque OE, Hill J, Hoskins BE, et al. (2003) Basal body dysfunction is a likely cause of pleiotropic Bardet-Biedl syndrome. Nature 425: 628-633.
2. Louie CM, Gleeson JG (2005) Genetic basis of Joubert syndrome and related disorders of cerebellar development. Hum Mol Genet 14 Spec No. 2: R235-242.
3. Badano JL, Mitsuma N, Beales PL, Katsanis N (2006) The ciliopathies: An emerging class of human genetic disorders. Annu Rev Genomics Hum Genet 7: 125-148.
4. Garcia-Gonzalo FR, Reiter JF (2012) Scoring a backstage pass: Mechanisms of ciliogenesis and ciliary access. J Cell Biol 197: 697-709.
5. Zaghloul NA, Katsanis N (2009) Mechanistic insights into Bardet-Biedl syndrome, a model ciliopathy. J Clin Invest 119: 428-437.
6. Westlake CJ, Baye LM, Nachury MV, Wright KJ, Ervin KE, 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 U S A 108: 2759-2764.
7. Kim J, Lee JE, Heynen-Genel S, Suyama E, Ono K, et al. (2010) Functional genomic screen for modulators of ciliogenesis and cilium length. Nature 464: 1048-1051.
8. Kim J, Krishnaswami SR, Gleeson JG (2008) CEP290 interacts with the centriolar satellite component PCM-1 and is required for Rab8 localization to the primary cilium. Hum Mol Genet 17: 3796-3805.
9. Gerdes JM, Davis EE, Katsanis N (2009) The vertebrate primary cilium in development, homeostasis, and disease. Cell 137: 32-45.
10. L'Hernault SW, Rosenbaum JL (1985) Chlamydomonas alpha-tubulin is posttranslationally modified by acetylation on the epsilon-amino group of a lysine. Biochemistry 24: 473-478.
11. Akella JS, Wloga D, Kim J, Starostina NG, Lyons-Abbott S, et al. (2010) MEC-17 is an alpha-tubulin acetyltransferase. Nature 467: 218-222.
12. Shida T, Cueva JG, Xu Z, Goodman MB, Nachury MV (2010) The major alpha-tubulin K40 acetyltransferase alphaTAT1 promotes rapid ciliogenesis and efficient mechanosensation. Proc Natl Acad Sci U S A 107: 21517-21522.
13. Hubbert C, Guardiola A, Shao R, Kawaguchi Y, Ito A, et al. (2002) HDAC6 is a microtubuleassociated deacetylase. Nature 417: 455-458.
14. Kim GW, Li L, Gorbani M, You L, Yang XJ (2013) Mice lacking alpha-tubulin acetyltransferase 1 are viable but display alpha-tubulin acetylation deficiency and dentate gyrus distortion. J Biol Chem 288: 20334-20350.
15. Kalebic N, Sorrentino S, Perlas E, Bolasco G, Martinez C, et al. (2013) alphaTAT1 is the major alphatubulin acetyltransferase in mice. Nat Commun 4: 1962.
16. Pugacheva EN, Jablonski SA, Hartman TR, Henske EP, Golemis EA (2007) HEF1-dependent Aurora A activation induces disassembly of the primary cilium. Cell 129: 1351-1363.
17. Cao J, Shen Y, Zhu L, Xu Y, Zhou Y, et al. (2012) miR-129-3p controls cilia assembly by regulating CP110 and actin dynamics. Nat Cell Biol 14: 697-706.
18. Even-Ram S, Doyle AD, Conti MA, Matsumoto K, Adelstein RS, et al. (2007) Myosin IIA regulates cell motility and actomyosin-microtubule crosstalk. Nat Cell Biol 9: 299-309.
19. Lecuit T, Lenne PF, Munro E (2011) Force generation, transmission, and integration during cell and tissue morphogenesis. Annu Rev Cell Dev Biol 27: 157-184.
20. Mukhopadhyay S, Wen X, Chih B, Nelson CD, Lane WS, et al. (2010) TULP3 bridges the IFT-A complex and membrane phosphoinositides to promote trafficking of G protein-coupled receptors into primary cilia. Genes Dev 24: 2180-2193.
21. Corbit KC, Aanstad P, Singla V, Norman AR, Stainier DY, et al. (2005) Vertebrate Smoothened functions at the primary cilium. Nature 437: 1018-1021.
22. Wei Q, Adelstein RS (2000) Conditional expression of a truncated fragment of nonmuscle myosin II-A alters cell shape but not cytokinesis in HeLa cells. Mol Biol Cell 11: 3617-3627.
23. Topalidou I, Keller C, Kalebic N, Nguyen KC, Somhegyi H, et al. (2012) Genetically separable functions of the MEC-17 tubulin acetyltransferase affect microtubule organization. Curr Biol 22: 1057-1065.
24. Friedmann DR, Aguilar A, Fan JY, Nachury MV, Marmorstein R (2012) Structure of the alpha-tubulin acetyltransferase, alpha TAT1, and implications for tubulin-specific acetylation. Proceedings of the National Academy of Sciences of the United States of America 109: 19655-19660.
25. Butler KV, Kalin J, Brochier C, Vistoli G, Langley B, et al. (2010) Rational Design and Simple Chemistry Yield a Superior, Neuroprotective HDAC6 Inhibitor, Tubastatin A. Journal of the American Chemical Society 132: 10842-10846.
26. Nachury MV, Seeley ES, Jin H (2010) Trafficking to the ciliary membrane: How to get across the periciliary diffusion barrier? Annu Rev Cell Dev Biol 26: 59-87.
27. Liu X, Hong MS, Shu S, Yu S, Korn ED (2013) Regulation of the filament structure and assembly of Acanthamoeba myosin II by phosphorylation of serines in the heavy-chain nonhelical tailpiece. Proc Natl Acad Sci U S A 110: E33-40.
28. Smutny M, Cox HL, Leerberg JM, Kovacs EM, Conti MA, et al. (2010) Myosin II isoforms identify distinct functional modules that support integrity of the epithelial zonula adherens. Nat Cell Biol 12: 696-702.
29. Murakami N, Kotula L, Hwang YW (2000) Two distinct mechanisms for regulation of nonmuscle myosin assembly via the heavy chain: Phosphorylation for MIIB and mts 1 binding for MIIA. Biochemistry 39: 11441-11451.
30. Wang B, Rao YH, Inoue M, Hao R, Lai CH, et al. (2014) Microtubule acetylation amplifies p38 kinase signalling and anti-inflammatory IL-10 production. Nat Commun 5: 3479.