Elongator Controls the Migration and Differentiation of Cortical Neurons through Acetylation of α-Tubulin

Cell

Volumn 136, Issue 3, 2009, Pages 551-564

  Creppe, Catherine ^a   Malinouskaya, Lina ^a   Volvert, Marie Laure ^a   Gillard, Magali ^a   Close, Pierre ^a   Malaise, Olivier ^a   Laguesse, Sophie ^a   Cornez, Isabelle ^a   Rahmouni, Souad ^b   Ormenese, Sandra ^a   Belachew, Shibeshih ^a   Malgrange, Brigitte ^a   Chapelle, Jean Paul ^a   Siebenlist, Ulrich ^c   Moonen, Gustave ^a   Chariot, Alain ^a   Nguyen, Laurent ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b UNIVERSITY OF LIÈGE   (Belgium)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

CELLBIO; DEVBIO; MOLNEURO

Indexed keywords

ALPHA TUBULIN;

ACETYLATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CELL MIGRATION; CONTROLLED STUDY; FEMALE; GENE SILENCING; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

EID: 59349089711     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2008.11.043     Document Type: Article

References (50)

1. Anderson S.L., Coli R., Daly I.W., Kichula E.A., Rork M.J., Volpi S.A., Ekstein J., and Rubin B.Y. Familial dysautonomia is caused by mutations of the IKAP gene. Am. J. Hum. Genet. 68 (2001) 753-758
2. Axelrod F.B. Familial dysautonomia. Muscle Nerve 29 (2004) 352-363
3. Cau E., Gradwohl G., Fode C., and Guillemot F. Mash1 activates a cascade of bHLH regulators in olfactory neuron progenitors. Development 124 (1997) 1611-1621
4. Close P., Hawkes N., Cornez I., Creppe C., Lambert C.A., Rogister B., Siebenlist U., Merville M.P., Slaugenhaupt S.A., Bours V., et al. Transcription impairment and cell migration defects in elongator-depleted cells: implication for familial dysautonomia. Mol. Cell 22 (2006) 521-531
5. da Silva J.S., and Dotti C.G. Breaking the neuronal sphere: regulation of the actin cytoskeleton in neuritogenesis. Nat. Rev. Neurosci. 3 (2002) 694-704
6. Dajas-Bailador F., Jones E.V., and Whitmarsh A.J. The JIP1 scaffold protein regulates axonal development in cortical neurons. Curr. Biol. 18 (2008) 221-226
7. Dompierre J.P., Godin J.D., Charrin B.C., Cordelieres F.P., King S.J., Humbert S., and Saudou F. Histone deacetylase 6 inhibition compensates for the transport deficit in Huntington's disease by increasing tubulin acetylation. J. Neurosci. 27 (2007) 3571-3583
8. Esberg A., Huang B., Johansson M.J., and Bystrom A.S. Elevated levels of two tRNA species bypass the requirement for elongator complex in transcription and exocytosis. Mol. Cell 24 (2006) 139-148
9. Fox J.W., Lamperti E.D., Eksioglu Y.Z., Hong S.E., Feng Y., Graham D.A., Scheffer I.E., Dobyns W.B., Hirsch B.A., Radtke R.A., et al. Mutations in filamin 1 prevent migration of cerebral cortical neurons in human periventricular heterotopia. Neuron 21 (1998) 1315-1325
10. Fujita T., Maturana A.D., Ikuta J., Hamada J., Walchli S., Suzuki T., Sawa H., Wooten M.W., Okajima T., Tatematsu K., et al. Axonal guidance protein FEZ1 associates with tubulin and kinesin motor protein to transport mitochondria in neurites of NGF-stimulated PC12 cells. Biochem. Biophys. Res. Commun. 361 (2007) 605-610
11. Gaertig J., Cruz M.A., Bowen J., Gu L., Pennock D.G., and Gorovsky M.A. Acetylation of lysine 40 in alpha-tubulin is not essential in Tetrahymena thermophila. J. Cell Biol. 129 (1995) 1301-1310
12. Gardiner J., Barton D., Marc J., and Overall R. Potential role of tubulin acetylation and microtubule-based protein trafficking in familial dysautonomia. Traffic 8 (2007) 1145-1149
13. Gleeson J.G., Allen K.M., Fox J.W., Lamperti E.D., Berkovic S., Scheffer I., Cooper E.C., Dobyns W.B., Minnerath S.R., Ross M.E., et al. Doublecortin, a brain-specific gene mutated in human X-linked lissencephaly and double cortex syndrome, encodes a putative signaling protein. Cell 92 (1998) 63-72
14. Gomes R.A., Hampton C., El-Sabeawy F., Sabo S.L., and McAllister A.K. The dynamic distribution of TrkB receptors before, during, and after synapse formation between cortical neurons. J. Neurosci. 26 (2006) 11487-11500
15. Haggarty S.J., Koeller K.M., Wong J.C., Grozinger C.M., and Schreiber S.L. Domain-selective small-molecule inhibitor of histone deacetylase 6 (HDAC6)-mediated tubulin deacetylation. Proc. Natl. Acad. Sci. USA 100 (2003) 4389-4394
16. Hawkes N.A., Otero G., Winkler G.S., Marshall N., Dahmus M.E., Krappmann D., Scheidereit C., Thomas C.L., Schiavo G., Erdjument-Bromage H., et al. Purification and characterization of the human elongator complex. J. Biol. Chem. 277 (2002) 3047-3052
17. Hayashi K., Ohshima T., and Mikoshiba K. Pak1 is involved in dendrite initiation as a downstream effector of Rac1 in cortical neurons. Mol. Cell. Neurosci. 20 (2002) 579-594
18. Huang B., Johansson M.J., and Bystrom A.S. An early step in wobble uridine tRNA modification requires the Elongator complex. RNA 11 (2005) 424-436
19. Hubbert C., Guardiola A., Shao R., Kawaguchi Y., Ito A., Nixon A., Yoshida M., Wang X.F., and Yao T.P. HDAC6 is a microtubule-associated deacetylase. Nature 417 (2002) 455-458
20. Johansen L.D., Naumanen T., Knudsen A., Westerlund N., Gromova I., Junttila M., Nielsen C., Bottzauw T., Tolkovsky A., Westermarck J., et al. IKAP localizes to membrane ruffles with filamin A and regulates actin cytoskeleton organization and cell migration. J. Cell Sci. 121 (2008) 854-864
21. Keays D.A., Tian G., Poirier K., Huang G.J., Siebold C., Cleak J., Oliver P.L., Fray M., Harvey R.J., Molnar Z., et al. Mutations in alpha-tubulin cause abnormal neuronal migration in mice and lissencephaly in humans. Cell 128 (2007) 45-57
22. Kim J.H., Lane W.S., and Reinberg D. Human Elongator facilitates RNA polymerase II transcription through chromatin. Proc. Natl. Acad. Sci. USA 99 (2002) 1241-1246
23. Kim S.C., Sprung R., Chen Y., Xu Y., Ball H., Pei J., Cheng T., Kho Y., Xiao H., Xiao L., et al. Substrate and functional diversity of lysine acetylation revealed by a proteomics survey. Mol. Cell 23 (2006) 607-618
24. Kouskouti A., and Talianidis I. Histone modifications defining active genes persist after transcriptional and mitotic inactivation. EMBO J. 24 (2005) 347-357
25. Kozminski K.G., Diener D.R., and Rosenbaum J.L. High level expression of nonacetylatable alpha-tubulin in Chlamydomonas reinhardtii. Cell Motil. Cytoskeleton 25 (1993) 158-170
26. Kristjuhan A., and Svejstrup J.Q. Evidence for distinct mechanisms facilitating transcript elongation through chromatin in vivo. EMBO J. 23 (2004) 4243-4252
27. Lom B., and Cohen-Cory S. Brain-derived neurotrophic factor differentially regulates retinal ganglion cell dendritic and axonal arborization in vivo. J. Neurosci. 19 (1999) 9928-9938
28. LoTurco J.J., and Bai J. The multipolar stage and disruptions in neuronal migration. Trends Neurosci. 29 (2006) 407-413
29. Marin O., and Rubenstein J.L. Cell migration in the forebrain. Annu. Rev. Neurosci. 26 (2003) 441-483
30. Mezey E., Parmalee A., Szalayova I., Gill S.P., Cuajungco M.P., Leyne M., Slaugenhaupt S.A., and Brownstein M.J. Of splice and men: what does the distribution of IKAP mRNA in the rat tell us about the pathogenesis of familial dysautonomia?. Brain Res. 983 (2003) 209-214
31. Nagano T., Morikubo S., and Sato M. Filamin A and FILIP (Filamin A-Interacting Protein) regulate cell polarity and motility in neocortical subventricular and intermediate zones during radial migration. J. Neurosci. 24 (2004) 9648-9657
32. Nguyen L., Besson A., Heng J.I., Schuurmans C., Teboul L., Parras C., Philpott A., Roberts J.M., and Guillemot F. p27kip1 independently promotes neuronal differentiation and migration in the cerebral cortex. Genes Dev. 20 (2006) 1511-1524
33. North B.J., Marshall B.L., Borra M.T., Denu J.M., and Verdin E. The human Sir2 ortholog, SIRT2, is an NAD+-dependent tubulin deacetylase. Mol. Cell 11 (2003) 437-444
34. North B.J., and Verdin E. Mitotic regulation of SIRT2 by cyclin-dependent kinase 1-dependent phosphorylation. J. Biol. Chem. 282 (2007) 19546-19555
35. Petrakis T.G., Wittschieben B.O., and Svejstrup J.Q. Molecular architecture, structure-function relationship, and importance of the Elp3 subunit for the RNA binding of holo-elongator. J. Biol. Chem. 279 (2004) 32087-32092
36. Rahl P.B., Chen C.Z., and Collins R.N. Elp1p, the yeast homolog of the FD disease syndrome protein, negatively regulates exocytosis independently of transcriptional elongation. Mol. Cell 17 (2005) 841-853
37. Reed N.A., Cai D., Blasius T.L., Jih G.T., Meyhofer E., Gaertig J., and Verhey K.J. Microtubule acetylation promotes kinesin-1 binding and transport. Curr. Biol. 16 (2006) 2166-2172
38. Reiner O., Carrozzo R., Shen Y., Wehnert M., Faustinella F., Dobyns W.B., Caskey C.T., and Ledbetter D.H. Isolation of a Miller-Dieker lissencephaly gene containing G protein beta-subunit-like repeats. Nature 364 (1993) 717-721
39. Roy S., Coffee P., Smith G., Liem R.K., Brady S.T., and Black M.M. Neurofilaments are transported rapidly but intermittently in axons: implications for slow axonal transport. J. Neurosci. 20 (2000) 6849-6861
40. Shu T., Tseng H.C., Sapir T., Stern P., Zhou Y., Sanada K., Fischer A., Coquelle F.M., Reiner O., and Tsai L.H. Doublecortin-like kinase controls neurogenesis by regulating mitotic spindles and M phase progression. Neuron 49 (2006) 25-39
41. Slaugenhaupt S.A., Blumenfeld A., Gill S.P., Leyne M., Mull J., Cuajungco M.P., Liebert C.B., Chadwick B., Idelson M., Reznik L., et al. Tissue-specific expression of a splicing mutation in the IKBKAP gene causes familial dysautonomia. Am. J. Hum. Genet. 68 (2001) 598-605
42. Slaugenhaupt S.A., and Gusella J.F. Familial dysautonomia. Curr. Opin. Genet. Dev. 12 (2002) 307-311
43. Svejstrup J.Q. Elongator complex: how many roles does it play?. Curr. Opin. Cell Biol. 19 (2007) 331-336
44. Tabata H., and Nakajima K. Multipolar migration: the third mode of radial neuronal migration in the developing cerebral cortex. J. Neurosci. 23 (2003) 9996-10001
45. Vaquero A., Scher M.B., Lee D.H., Sutton A., Cheng H.L., Alt F.W., Serrano L., Sternglanz R., and Reinberg D. SirT2 is a histone deacetylase with preference for histone H4 Lys 16 during mitosis. Genes Dev. 20 (2006) 1256-1261
46. Winkler G.S., Kristjuhan A., Erdjument-Bromage H., Tempst P., and Svejstrup J.Q. Elongator is a histone H3 and H4 acetyltransferase important for normal histone acetylation levels in vivo. Proc. Natl. Acad. Sci. USA 99 (2002) 3517-3522
47. Wittschieben B.O., Otero G., de Bizemont T., Fellows J., Erdjument-Bromage H., Ohba R., Li Y., Allis C.D., Tempst P., and Svejstrup J.Q. A novel histone acetyltransferase is an integral subunit of elongating RNA polymerase II holoenzyme. Mol. Cell 4 (1999) 123-128
48. Wittschieben B.O., Fellows J., Du W., Stillman D.J., and Svejstrup J.Q. Overlapping roles for the histone acetyltransferase activities of SAGA and elongator in vivo. EMBO J. 19 (2000) 3060-3068
49. Yokota Y., Ring C., Cheung R., Pevny L., and Anton E.S. Nap1-regulated neuronal cytoskeletal dynamics is essential for the final differentiation of neurons in cerebral cortex. Neuron 54 (2007) 429-445
50. Zhang Y., Li N., Caron C., Matthias G., Hess D., Khochbin S., and Matthias P. HDAC-6 interacts with and deacetylates tubulin and microtubules in vivo. EMBO J. 22 (2003) 1168-1179