Volume 6 Issue 4
Mar.  2021
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Kai He, Kun Ling, Jinghua Hu. The emerging role of tubulin posttranslational modifications in cilia and ciliopathies. Biophysics Reports, 2020, 6(4): 89-104. doi: 10.1007/s41048-020-00111-0
Citation: Kai He, Kun Ling, Jinghua Hu. The emerging role of tubulin posttranslational modifications in cilia and ciliopathies. Biophysics Reports, 2020, 6(4): 89-104. doi: 10.1007/s41048-020-00111-0

The emerging role of tubulin posttranslational modifications in cilia and ciliopathies

doi: 10.1007/s41048-020-00111-0
Funds:  Jinghua Hu
  • Received Date: 08 May 2020
  • Rev Recd Date: 28 June 2020
  • Publish Date: 31 August 2020
  • Tubulin posttranslational modifications (PTMs) add “tubulin code” to generate functional diversities of microtubules. Several types of tubulin PTMs accumulate on axonemes and basal bodies of cilia, including acetylation, glutamylation, glycylation and detyrosination. Among them, glutamylation, glycylation and detyrosination are mostly enriched in the B-tubules, whereas acetylation occurs on both Aand B-tubule of the microtubule doublets in a similar level. Recent studies indicate that tubulin PTMs are critical for the fine tuning of assembly/disassembly, maintenance, motility, and signaling of cilia. Dysregulated tubulin PTMs are strongly implicated in human disorders including ciliopathies and neuron degeneration. Here, we review the current understanding how tubulin PTMs regulate cilia formation and function, and their relevance to human health.
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  • Adams M, Smith UM, Logan CV, Johnson CA (2008) Recent advances in the molecular pathology, cell biology and genetics of ciliopathies. J Med Genet 45:257-267
    Aillaud C, Bosc C, Peris L, Bosson A, Heemeryck P, Van Dijk J, Le Friec J, Boulan B, Vossier F, Sanman LE, Syed S, Amara N, Couté Y, Lafanechère L, Denarier E, Delphin C, Pelletier L, Humbert S, Bogyo M, Andrieux A, Rogowski K, Moutin M-J (2017) Vasohibins/SVBP are tubulin carboxypeptidases(TCPs) that regulate neuron differentiation. Science 358:1448-1452
    Aillaud C, Bosc C, Saoudi Y, Denarier E, Peris L, Sago L, Taulet N, Cieren A, Tort O, Magiera MM, Janke C, Redeker V, Andrieux A, Moutin M-J (2016) Evidence for new C-terminally truncated variants of alpha- and beta-tubulins. Mol Biol Cell 27:640-653
    Akella JS, Wloga D, Kim J, Starostina NG, Lyons-Abbott S, Morrissette NS, Dougan ST, Kipreos ET, Gaertig J (2010)MEC-17 is an alpha-tubulin acetyltransferase. Nature 467:218-222
    Akera T, Chmátal L, Trimm E, Yang K, Aonbangkhen C, Chenoweth DM, Janke C, Schultz RM, Lampson MA (2017) Spindle asymmetry drives non-Mendelian chromosome segregation.Science 358:668-672
    Alexander JE, Hunt DF, Lee MK, Shabanowitz J, Michel H, Berlin SC, MacDonald TL, Sundberg RJ, Rebhun LI, Frankfurter A (1991)Characterization of posttranslational modifications in neuron-specific class Ⅲ beta-tubulin by mass spectrometry.Proc Natl Acad Sci USA 88:4685-4689
    Alper JD, Decker F, Agana B, Howard J (2014) The motility of axonemal dynein is regulated by the tubulin code. Biophys J 107:2872-2880
    Arce CA, Barra HS (1983) Association of tubulinyl-tyrosine carboxypeptidase with microtubules. FEBS Lett 157:75-78
    Astuti GD, Arno G, Hull S, Pierrache L, Venselaar H, Carss K, Raymond FL, Collin RW, Faradz SM, van den Born LI, Webster AR, Cremers FPM (2016) Mutations in AGBL5, encoding alpha-tubulin deglutamylase, are associated with autosomal recessive retinitis pigmentosa. Invest Ophthalmol Vis Sci 57:6180-6187
    Audebert S, Koulakoff A, Berwald-Netter Y, Gros F, Denoulet P, Edde B (1994) Developmental regulation of polyglutamylated alpha- and beta-tubulin in mouse brain neurons. J Cell Sci 107(Pt 8):2313-2322
    Backer CB, Gutzman JH, Pearson CG, Cheeseman IM (2012) CSAP localizes to polyglutamylated microtubules and promotes proper cilia function and zebrafish development. Mol Biol Cell 23:2122-2130
    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
    Bangs F, Anderson KV (2017) Primary cilia and mammalian hedgehog signaling. Cold Spring Harb Perspect Biol 9:a028175
    Barisic M, e Sousa RS, Tripathy SK, Magiera MM, Zaytsev AV, Pereira AL, Janke C, Grishchuk EL, Maiato H (2015) Microtubule detyrosination guides chromosomes during mitosis.Science 348:799-803
    Benoy V, Vanden Berghe P, Jarpe M, Van Damme P, Robberecht W, Van Den Bosch L (2017) Development of improved HDAC6 inhibitors as pharmacological therapy for xonal CharcotMarie-Tooth disease. Neurotherapeutics 14:417-428
    Berbari NF, O'Connor AK, Haycraft CJ, Yoder BK (2009) The primary cilium as a complex signaling center. Curr Biol 19:R526-535
    Berbari NF, Sharma N, Malarkey EB, Pieczynski JN, Boddu R, Gaertig J, Guay-Woodford L, Yoder BK (2013) Microtubule modifications and stability are altered by cilia perturbation and in cystic kidney disease. Cytoskeleton (Hoboken) 70:24-31
    Berezniuk I, Lyons PJ, Sironi JJ, Xiao H, Setou M, Angeletti RH, Ikegami K, Fricker LD (2013) Cytosolic carboxypeptidase 5 removes alpha- and gamma-linked glutamates from tubulin.J Biol Chem 288:30445-30453
    Berezniuk I, Vu HT, Lyons PJ, Sironi JJ, Xiao H, Burd B, Setou M, Angeletti RH, Ikegami K, Fricker LD (2012) Cytosolic carboxypeptidase 1 is involved in processing alpha- and beta-tubulin. J Biol Chem 287:6503-6517
    Bobinnec Y, Moudjou M, Fouquet JP, Desbruyeres E, Edde B, Bornens M (1998) Glutamylation of centriole and cytoplasmic tubulin in proliferating non-neuronal cells. Cell Motil Cytoskeleton 39:223-232
    Branham K, Matsui H, Biswas P, Guru AA, Hicks M, Suk JJ, Li H, Jakubosky D, Long T, Telenti A, Nariai N, Heckenlively JR, Frazer KA, Sieving PA, Ayyagari R (2016) Establishing the involvement of the novel gene AGBL5 in retinitis pigmentosa by whole genome sequencing. Physiol Genomics 48:922-927
    Bre MH, Redeker V, Quibell M, Darmanaden-Delorme J, Bressac C, Cosson J, Huitorel P, Schmitter JM, Rossler J, Johnson T, Adoutte A, Levilliers N (1996) Axonemal tubulin polyglycylation probed with two monoclonal antibodies:widespread evolutionary distribution, appearance during spermatozoan maturation and possible function in motility. J Cell Sci 109(Pt 4):727-738
    Bre MH, Redeker V, Vinh J, Rossier J, Levilliers N (1998) Tubulin polyglycylation:differential posttranslational modification of dynamic cytoplasmic and stable axonemal microtubules in paramecium. Mol Biol Cell 9:2655-2665
    Bulinski JC, Richards JE, Piperno G (1988) Posttranslational modifications of alpha tubulin:detyrosination and acetylation differentiate populations of interphase microtubules in cultured cells. J Cell Biol 106:1213-1220
    Campbell PK, Waymire KG, Heier RL, Sharer C, Day DE, Reimann H, Jaje JM, Friedrich GA, Burmeister M, Bartness TJ, Russell LD, Young LJ, Zimmer M, Jenne DE, MacGregor GR (2002)
    Mutation of a novel gene results in abnormal development of spermatid flagella, loss of intermale aggression and reduced body fat in mice. Genetics 162:307-320
    Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, Walther TC, Olsen JV, Mann M (2009) Lysine acetylation targets protein complexes and co-regulates major cellular functions.Science 325:834-840
    Chretien D, Metoz F, Verde F, Karsenti E, Wade RH (1992) Latticedefects in microtubules - protofilament numbers vary within individual microtubules. J Cell Biol 117:1031-1040
    Chu CW, Hou F, Zhang J, Phu L, Loktev AV, Kirkpatrick DS, Jackson PK, Zhao Y, Zou H (2011) A novel acetylation of beta-tubulin by San modulates microtubule polymerization via downregulating tubulin incorporation. Mol Biol Cell 22:448-456
    Coombes C, Yamamoto A, McClellan M, Reid TA, Plooster M, Luxton GW, Alper J, Howard J, Gardner MK (2016) Mechanism of microtubule lumen entry for the alpha-tubulin acetyltransferase enzyme alphaTAT1. Proc Natl Acad Sci USA 113:E7176-E7184
    d'Ydewalle C, Krishnan J, Chiheb DM, Van Damme P, Irobi J, Kozikowski AP, Berghe PV, Timmerman V, Robberecht W, Van Den Bosch L (2011) HDAC6 inhibitors reverse axonal loss in a mouse model of mutant HSPB1-induced Charcot-Marie-Tooth disease. Nat Med 17:968-974
    Dafinger C, Liebau MC, Elsayed SM, Hellenbroich Y, Boltshauser E, Korenke GC, Fabretti F, Janecke AR, Ebermann I, Nurnberg G, Nürnberg P, Zentgraf H, Koerber F, Addicks K, Elsobky E, Benzing T, Schermer B, Bolz HJ (2011) Mutations in KIF7 link Joubert syndrome with Sonic Hedgehog signaling and microtubule dynamics. J Clin Invest 121:2662-2667
    Dan W, Gao N, Li L, Zhu JX, Diao L, Huang J, Han QJ, Wang S, Xue H, Wang Q, Wu Q-F, Zhang X, Bao L (2018) alpha-tubulin acetylation restricts axon overbranching by dampening microtubule plus-end dynamics in neurons. Cereb Cortex 28:3332-3346
    de Diego AS, Alonso Guerrero A, Martínez-A C, van Wely KHM (2014) Dido3-dependent HDAC6 targeting controls cilium size. Nature Commun 5:1-11
    de la Vega MR, Sevilla RG, Hermoso A, Lorenzo J, Tanco S, Diez A, Fricker LD, Bautista JM, Avilés FX (2007) Nna1-like proteins are active metallocarboxypeptidases of a new and diverse M14 subfamily. FASEB J 21:851-865
    Diagouraga B, Grichine A, Fertin A, Wang J, Khochbin S, Sadoul K (2014) Motor-driven marginal band coiling promotes cell shape change during platelet activation. J Cell Biol 204:177-185
    Dompierre JP, Godin JD, Charrin BC, Cordelieres FP, King SJ, Humbert S, Saudou F (2007) Histone deacetylase 6 inhibition compensates for the transport deficit in Huntington's disease by increasing tubulin acetylation. J Neurosci 27:3571-3583
    Drazic A, Myklebust LM, Ree R, Arnesen T (2016) The world of protein acetylation. Biochim Biophys Acta 1864:1372-1401
    Du H, Zhao J, Hai L, Wu J, Yi H, Shi Y (2017) The roles of vasohibin and its family members:beyond angiogenesis modulators.Cancer Biol Ther 18:827-832
    Dymek EE, Lefebvre PA, Smith EF (2004) PF15p is the chlamydomonas homologue of the Katanin p80 subunit and is required for assembly of flagellar central microtubules.Eukaryot Cell 3:870-879
    Edde B, Rossier J, Le Caer JP, Desbruyeres E, Gros F, Denoulet P (1990) Posttranslational glutamylation of alpha-tubulin.Science 247:83-85
    Erck C, Peris L, Andrieux A, Meissirel C, Gruber AD, Vernet M, Schweitzer A, Saoudi Y, Pointu H, Bosc C, Salin PA, Job D, Wehland J (2005) A vital role of tubulin-tyrosine-ligase for neuronal organization. Proc Natl Acad Sci USA 102:7853-7858
    Ersfeld K, Wehland J, Plessmann U, Dodemont H, Gerke V, Weber K (1993) Characterization of the tubulin-tyrosine ligase. J Cell Biol 120:725-732
    Fernandez-Gonzalez A, La Spada AR, Treadaway J, Higdon JC, Harris BS, Sidman RL, Morgan JI, Zuo J (2002) Purkinje cell degeneration (pcd) phenotypes caused by mutations in the axotomy-induced gene, Nna1. Science 295:1904-1906
    Fouquet JP, Edde B, Kann ML, Wolff A, Desbruyeres E, Denoulet P (1994) Differential distribution of glutamylated tubulin during spermatogenesis in mammalian testis. Cell Motil Cytoskeleton 27:49-58
    Gadadhar S, Bodakuntla S, Natarajan K, Janke C (2017a) The tubulin code at a glance. J Cell Sci 130:1347-1353
    Gadadhar S, Dadi H, Bodakuntla S, Schnitzler A, Bieche I, Rusconi F, Janke C (2017b) Tubulin glycylation controls primary cilia length. J Cell Biol 216:2701-2713
    Gagnon C, White D, Cosson J, Huitorel P, Edde B, Desbruyeres E, Paturle-Lafanechere L, Multigner L, Job D, Cibert C (1996)The polyglutamylated lateral chain of alpha-tubulin plays a key role in flagellar motility. J Cell Sci 109(Pt 6):1545-1553
    Garnham CP, Vemu A, Wilson-Kubalek EM, Yu I, Szyk A, Lander GC, Milligan RA, Roll-Mecak A (2015) Multivalent microtubule recognition by tubulin tyrosine ligase-like family glutamylases. Cell 161:1112-1123
    Giordano T, Gadadhar S, Bodakuntla S, Straub J, Leboucher S, Martinez G, Chemlali W, Bosc C, Andrieux A, Bieche I, Arnoult C, Geimer S, Janke C (2019) Loss of the deglutamylase CCP5 perturbs multiple steps of spermatogenesis and leads to male infertility. J Cell Sci 132:226951
    Godena VK, Brookes-Hocking N, Moller A, Shaw G, Oswald M, Sancho RM, Miller CCJ, Whitworth AJ, De Vos KJ (2014)Increasing microtubule acetylation rescues axonal transport and locomotor deficits caused by LRRK2 Roc-COR domain mutations. Nat Commun 5:1-11
    Goetz SC, Anderson KV (2010) The primary cilium:a signalling centre during vertebrate development. Nat Rev Genet 11:331-344
    Grau BM, Rochas C, Meunier A, Spassky N, Janke C (2012) Tubulin posttranslational modifications as regulators of microtubulebased functions in cells. Cilia 1:1
    Grau BM, Gonzalez Curto G, Rocha C, Magiera MM, Marques Sousa P, Giordano T, Spassky N, Janke C (2013) Tubulin glycylases and glutamylases have distinct functions in stabilization and motility of ependymal cilia. J Cell Biol 202:441-451
    Grau MB, Masson C, Gadadhar S, Rocha C, Tort O, Sousa PM, Vacher S, Bieche I, Janke C (2017) Alterations in the balance of tubulin glycylation and glutamylation in photoreceptors leads to retinal degeneration. J Cell Sci 130:938-949
    Greer CA, Shepherd GM (1982) Mitral cell degeneration and sensory function in the neurological mutant mouse Purkinje cell degeneration (PCD). Brain Res 235:156-161
    He K, Ma X, Xu T, Li Y, Hodge A, Zhang Q, Torline J, Huang Y, Zhao J, Ling K, Hu J (2018) Axoneme polyglutamylation regulated by Joubert syndrome protein ARL13B controls ciliary targeting of signaling molecules. Nat Commun 9:3310
    Hong SR, Wang CL, Huang YS, Chang YC, Chang YC, Pusapati GV, Lin CY, Hsu N, Cheng HC, Chiang YC, Huang WE, Shaner NC, Rohatgi R, Inoue T, Lin YC (2018) Spatiotemporal manipulation of ciliary glutamylation reveals its roles in intraciliary trafficking and Hedgehog signaling. Nat Commun 9:1732
    Hubbert C, Guardiola A, Shao R, Kawaguchi Y, Ito A, Nixon A, Yoshida M, Wang XF, Yao TP (2002) HDAC6 is a microtubuleassociated deacetylase. Nature 417:455-458
    Huq MDM, Wei L-N (2010) Protein posttranslational modification:a potential target in pharmaceutical development. Pharm Biotechnol. https://doi.org/10.1002/9780470571224.pse302
    Iancu-Rubin C, Gajzer D, Mosoyan G, Feller F, Mascarenhas J, Hoffman R (2012) Panobinostat (LBH589)-induced acetylation of tubulin impairs megakaryocyte maturation and platelet formation. Exp Hematol 40:564-574
    Ichikawa M, Liu D, Kastritis PL, Basu K, Hsu TC, Yang S, Bui KH (2017) Subnanometre-resolution structure of the doublet microtubule reveals new classes of microtubule-associated proteins. Nat Commun 8:1-22
    Ikegami K, Heier RL, Taruishi M, Takagi H, Mukai M, Shimma S, Taira S, Hatanaka K, Morone N, Yao I, Campbell PK, Yuasa S, Janke C, Macgregor GR, Setou M (2007) Loss of alpha-tubulin polyglutamylation in ROSA22 mice is associated with abnormal targeting of KIF1A and modulated synaptic function. Proc Natl Acad Sci USA 104:3213-3218
    Ikegami K, Mukai M, Tsuchida J, Heier RL, Macgregor GR, Setou M (2006) TTLL7 is a mammalian beta-tubulin polyglutamylase required for growth of MAP2-positive neurites. J Biol Chem 281:30707-30716
    Ikegami K, Sato S, Nakamura K, Ostrowski LE, Setou M (2010)Tubulin polyglutamylation is essential for airway ciliary function through the regulation of beating asymmetry. Proc Natl Acad Sci USA 107:10490-10495
    Ikegami K, Setou M (2009) TTLL10 can perform tubulin glycylation when co-expressed with TTLL8. FEBS Lett 583:1957-1963
    Janke C (2014) The tubulin code:molecular components, readout mechanisms, and functions. J Cell Biol 206:461-472
    Janke C, Bulinski JC (2011) Post-translational regulation of the microtubule cytoskeleton:mechanisms and functions. Nat Rev Mol Cell Biol 12:773-786
    Janke C, Rogowski K, van Dijk J (2008) Polyglutamylation:a fineregulator of protein function? ‘Protein Modifications:beyond the usual suspects’ review series. EMBO Rep 9:636-641
    Janke C, Rogowski K, Wloga D, Regnard C, Kajava AV, Strub JM, Temurak N, van Dijk J, Boucher D, van Dorsselaer A, Suryavanshi S, Gaertig J, Eddé B (2005) Tubulin polyglutamylase enzymes are members of the TTL domain protein family. Science 308:1758-1762
    Johnson GJ, Leis LA, Krumwiede MD, White JG (2007) The critical role of myosin ⅡA in platelet internal contraction. J Thromb Haemost 5:1516-1529
    Johnson KA (1998) The axonemal microtubules of the Chlamydomonas flagellum differ in tubulin isoform content. J Cell Sci 111(Pt 3):313-320
    Kalebic N, Martinez C, Perlas E, Hublitz P, Bilbao-Cortes D, Fiedorczuk K, Andolfo A, Heppenstall PA (2013a) Tubulin acetyltransferase aTAT1 destabilizes microtubules independently of its acetylation activity. Mol Cell Biol 33:1114-1123
    Kalebic N, Sorrentino S, Perlas E, Bolasco G, Martinez C, Heppenstall PA (2013b) alphaTAT1 is the major alpha-tubulin acetyltransferase in mice. Nat Commun 4:1962
    Kalinina E, Biswas R, Berezniuk I, Hermoso A, Aviles FX, Fricker LD (2007) A novel subfamily of mouse cytosolic carboxypeptidases. FASEB J 21:836-850
    Kann ML, Soues S, Levilliers N, Fouquet JP (2003) Glutamylated tubulin:diversity of expression and distribution of isoforms.Cell Motil Cytoskeleton 55:14-25
    Kapitein LC, Hoogenraad CC (2015) Building the neuronal microtubule cytoskeleton. Neuron 87:492-506
    Kastner S, Thiemann IJ, Dekomien G, Petrasch-Parwez E, Schreiber S, Akkad DA, Gerding WM, Hoffjan S, Günes S, Günes S, Bagci H, Epplen JT (2015) Exome sequencing reveals AGBL5 as novel candidate gene and additional variants for retinitis pigmentosa in five Turkish families. Invest Ophthalmol Vis Sci 56:8045-8053
    Kato C, Miyazaki K, Nakagawa A, Ohira M, Nakamura Y, Ozaki T, Imai T, Nakagawara A (2004) Low expression of human tubulin tyrosine ligase and suppressed tubulin tyrosination/detyrosination cycle are associated with impaired neuronal differentiation in neuroblastomas with poor prognosis. Int J Cancer 112:365-375
    Kaul N, Soppina V, Verhey KJ (2014) Effects of alpha-tubulin K40 acetylation and detyrosination on kinesin-1 motility in a purified system. Biophys J 106:2636-2643
    Kerr JP, Robison P, Shi G, Bogush AI, Kempema AM, Hexum JK, Becerra N, Harki DA, Martin SS, Raiteri R, Prosser BL, Ward CW (2015) Detyrosinated microtubules modulate mechanotransduction in heart and skeletal muscle. Nat Commun 6:8526
    Kimura Y, Kurabe N, Ikegami K, Tsutsumi K, Konishi Y, Kaplan OI, Kunitomo H, Iino Y, Blacque OE, Setou M (2010) Identification of tubulin deglutamylase among Caenorhabditis elegans and mammalian cytosolic carboxypeptidases (CCPs). J Biol Chem 285:22936-22941
    Kimura Y, Tsutsumi K, Konno A, Ikegami K, Hameed S, Kaneko T, Kaplan OI, Teramoto T, Fujiwara M, Ishihara T, Blacque OE, Setou M (2018) Environmental responsiveness of tubulin glutamylation in sensory cilia is regulated by the p38 MAPK pathway. Sci Rep 8(1):3892
    Konno A, Ikegami K, Konishi Y, Yang HJ, Abe M, Yamazaki M, Sakimura K, Yao I, Shiba K, Inaba K, Setou M (2016) Ttll9-/-mice sperm flagella show shortening of doublet 7, reduction of doublet 5 polyglutamylation and a stall in beating. J Cell Sci 129:2757-2766
    Kozminski KG, Beech PL, Rosenbaum JL (1995) The Chlamydomonas kinesin-like protein FLA10 is involved in motility associated with the flagellar membrane. J Cell Biol 131:1517-1527
    Kubo T, Hirono M, Aikawa T, Kamiya R, Witman GB (2015)Reduced tubulin polyglutamylation suppresses flagellar shortness in Chlamydomonas. Mol Biol Cell 26:2810-2822
    Kubo T, Yanagisawa HA, Yagi T, Hirono M, Kamiya R (2010)Tubulin polyglutamylation regulates axonemal motility by modulating activities of inner-arm dyneins. Curr Biol 20:441-445
    Kumar N, Flavin M (1981) Preferential action of a brain detyrosinolating carboxypeptidase on polymerized tubulin.J Biol Chem 256:7678-7686
    Lacroix B, van Dijk J, Gold ND, Guizetti J, Aldrian-Herrada G, Rogowski K, Gerlich DW, Janke C (2010) Tubulin polyglutamylation stimulates spastin-mediated microtubule severing. J Cell Biol 189:945-954
    Latour BL, Van De Weghe JC, Rusterholz TDS, Letteboer SJF, Gomez A, Shaheen R, Gesemann M, Grout ME, van Reeuwijk J, Van Beersum SEC, Miller CV, Dempsey JC, Morsy H, Bamshad MJ, Nickerson DA, Neuhauss SCF, Boldt K, Ueffing M, Alkuraya FS, Bachmann-Gagescu R, Roepman R, Doherty D (2019) ARMC9 and TOGARAM1 define a Joubert syndrome-associated protein module that regulates axonemal post-translational modifications and cilium stability. bioRxiv. doi: 10.1101/817213
    Lazo-Gomez R, Ramirez-Jarquin UN, Tovar YRLB, Tapia R (2013)Histone deacetylases and their role in motor neuron degeneration. Front Cell Neurosci 7:243
    Lechtreck KF, Geimer S (2000) Distribution of polyglutamylated tubulin in the flagellar apparatus of green flagellates. Cell Motil Cytoskeleton 47:219-235
    LeDizet M, Piperno G (1987) Identification of an acetylation site of Chlamydomonas alpha-tubulin. Proc Natl Acad Sci USA 84:5720-5724
    Lee GS, He Y, Dougherty EJ, Jimenez-Movilla M, Avella M, Grullon S, Sharlin DS, Guo C, Blackford JA Jr, Awasthi S, Zhang Z, Armstrong SP, London EC, Chen W, Dean J, Simons SS Jr(2013) Disruption of Ttll5/stamp gene (tubulin tyrosine ligase-like protein 5/SRC-1 and TIF2-associated modulatory protein gene) in male mice causes sperm malformation and infertility. J Biol Chem 288:15167-15180
    Lee JE, Silhavy JL, Zaki MS, Schroth J, Bielas SL, Marsh SE, Olvera J, Brancati F, Iannicelli M, Ikegami K, Schlossman AM, Merriman B, Attié-Bitach T, Logan CV, Glass IA, Cluckey A, Louie CM, Lee JH, Raynes HR, Rapin I, Castroviejo IP, Setou M, Barbot C, Boltshauser E, Nelson SF, Hildebrandt F, Johnson CA, Doherty DA, Valente EM, Gleeson JG (2012) CEP41 is mutated in Joubert syndrome and is required for tubulin glutamylation at the cilium. Nat Genet 44:193-199
    Lee SH, Somlo S (2014) Cyst growth, polycystins, and primary cilia in autosomal dominant polycystic kidney disease. Kidney Res Clin Pract 33:73-78
    Levilliers N, Fleury A, Hill AM (1995) Monoclonal and polyclonal antibodies detect a new type of post-translational modification of axonemal tubulin. J Cell Sci 108(Pt 9):3013-3028
    Lhernault SW, Rosenbaum JL (1983) Chlamydomonas alphatubulin Is posttranslationally modified in the Flagella during flagellar assembly. J Cell Biol 97:258-263
    Lhernault SW, Rosenbaum JL (1985) Chlamydomonas alphatubulin is posttranslationally modified by acetylation on the epsilon-amino group of a lysine. Biochemistry-US 24:473-478
    Li L, Wei D, Wang Q, Pan J, Liu R, Zhang X, Bao L (2012) MEC-17 deficiency leads to reduced-tubulin acetylation and impaired migration of cortical neurons. J Neurosci 32:12673-12683
    Liu N, Xiong Y, Ren Y, Zhang L, He X, Wang X, Liu M, Li D, Shui W, Zhou J (2015) Proteomic profiling and functional characterization of multiple post-translational modifications of tubulin.J Proteome Res 14:3292-3304
    Loktev AV, Zhang Q, Beck JS, Searby CC, Scheetz TE, Bazan JF, Slusarski DC, Sheffield VC, Jackson PK, Nachury MV (2008) A BBSome subunit links ciliogenesis, microtubule stability, and acetylation. Dev Cell 15:854-865
    Lu C, Srayko M, Mains PE (2004) The Caenorhabditis elegans microtubule-severing complex MEI-1/MEI-2 katanin interacts differently with two superficially redundant beta-tubulin isotypes. Mol Biol Cell 15:142-150
    Ly N, Elkhatib N, Bresteau E, Pietrement O, Khaled M, Magiera MM, Janke C, Le Cam E, Rutenberg AD, Montagnac G (2016)alphaTAT1 controls longitudinal spreading of acetylation marks from open microtubules extremities. Sci Rep 6:35624
    Ma M, Stoyanova M, Rademacher G, Dutcher SK, Brown A, Zhang R (2019) Structure of the decorated ciliary doublet microtubule. Cell 179:909-922.e912
    Magiera MM, Singh P, Gadadhar S, Janke C (2018a) Tubulin posttranslational modifications and emerging links to human disease. Cell 173:1323-1327
    Magiera MM, Singh P, Janke C (2018b) SnapShot:functions of tubulin posttranslational modifications. Cell 173(1552-1552):e1551
    Marchena M, Lara J, Aijon J, Germain F, de la Villa P, Velasco A (2011) The retina of the PCD/PCD mouse as a model of photoreceptor degeneration. A structural and functional study. Exp Eye Res 93:607-617
    Maruta H, Greer K, Rosenbaum JL (1986) The acetylation of alphatubulin and its relationship to the assembly and disassembly of microtubules. J Cell Biol 103:571-579
    Mary J, Redeker V, Le Caer JP, Rossier J, Schmitter JM (1996)Posttranslational modifications in the C-terminal tail of axonemal tubulin from sea urchin sperm. J Biol Chem 271:9928-9933
    Matsuyama A, Shimazu T, Sumida Y, Saito A, Yoshimatsu Y, Seigneurin-Berny D, Osada H, Komatsu Y, Nishino N, Khochbin S, Horinouchi S, Yoshida M (2002) In vivo destabilization of dynamic microtubules by HDAC6-mediated deacetylation. EMBO J 21:6820-6831
    Mialhe A, Lafanechere L, Treilleux I, Peloux N, Dumontet C, Bremond A, Panh MH, Payan R, Wehland J, Margolis RL, Job D (2001) Tubulin detyrosination is a frequent occurrence in breast cancers of poor prognosis. Cancer Res 61:5024-5027
    Mitchell DR (2010) Polyglutamylation:the GLU that makes microtubules sticky. Curr Biol 20:R234-236
    Miyake Y, Keusch JJ, Wang L, Saito M, Hess D, Wang X, Melancon BJ, Helquist P, Gut H, Matthias P (2016) Structural insights into HDAC6 tubulin deacetylation and its selective inhibition. Nat Chem Biol 12:748-754
    Morley SJ, Qi Y, Iovino L, Andolfi L, Guo D, Kalebic N, Castaldi L, Tischer C, Portulano C, Bolasco G, Shirlekar K, Fusco CM, Asaro A, Fermani F, Sundukova M, Matti U, Reymond L, Ninno AD, Businaro L, Johnsson K, Lazzarino M, Ries J, Schwab Y, Hu J, Heppenstall PA (2016) Acetylated tubulin is essential for touch sensation in mice. Elife 5:e20813. https://doi.org/10.7554/eLife.20813
    Mullen RJ, Eicher EM, Sidman RL (1976) Purkinje cell degeneration, a new neurological mutation in the mouse. Proc Natl Acad Sci USA 73:208-212
    Murofushi H (1980) Purification and characterization of tubulintyrosine ligase from porcine brain1. J Biochem 87:979-984
    Narita T, Weinert BT, Choudhary C (2019) Functions and mechanisms of non-histone protein acetylation. Nat Rev Mol Cell Biol 20:156-174
    Natarajan K, Gadadhar S, Souphron J, Magiera MM, Janke C (2017)Molecular interactions between tubulin tails and glutamylases reveal determinants of glutamylation patterns. EMBO Rep 18:1013-1026
    Nauli SM, Alenghat FJ, Luo Y, Williams E, Vassilev P, Li X, Elia AE, Lu W, Brown EM, Quinn SJ, Ingber DE, Zhou J (2003)Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat Genet 33:129-137
    Nieuwenhuis J, Adamopoulos A, Bleijerveld OB, Mazouzi A, Stickel E, Celie P, Altelaar M, Knipscheer P, Perrakis A, Blomen VA, Brummelkamp TR (2017) Vasohibins encode tubulin detyrosinating activity. Science 358:1453-1456
    Nishimura Y, Kasahara K, Shiromizu T, Watanabe M, Inagaki M (2019) Primary cilia as signaling hubs in health and disease.Adv Sci 6:1801138
    North BJ, Marshall BL, Borra MT, Denu JM, Verdin E (2003) The human Sir2 ortholog, SIRT2, is an NAD(+)-dependent tubulin deacetylase. Mol Cell 11:437-444
    O'Hagan R, Piasecki BP, Silva M, Phirke P, Nguyen KC, Hall DH, Swoboda P, Barr MM (2011) The tubulin deglutamylase CCPP-1 regulates the function and stability of sensory cilia in C. elegans. Curr Biol 21:1685-1694
    Ohta S, Hamada M, Sato N, Toramoto I (2015) Polyglutamylated tubulin binding protein C1orf96/CSAP is involved in microtubule stabilization in mitotic spindles. PLoS ONE 10:e0142798
    Orbach R, Howard J (2019) The dynamic and structural properties of axonemal tubulins support the high length stability of cilia.Nat Commun 10:1838
    Patel-Hett S, Richardson JL, Schulze H, Drabek K, Isaac NA, Hoffmeister K, Shivdasani RA, Bulinski JC, Galjart N, Hartwig JH, Italiano JE Jr (2008) Visualization of microtubule growth in living platelets reveals a dynamic marginal band with multiple microtubules. Blood 111:4605-4616
    Patel A, Honore E (2010) Polycystins and renovascular mechanosensory transduction. Nat Rev Nephrol 6:530-538
    Pathak N, Austin-Tse CA, Liu Y, Vasilyev A, Drummond IA (2014)Cytoplasmic carboxypeptidase 5 regulates tubulin glutamylation and zebrafish cilia formation and function. Mol Biol Cell 25:1836-1844
    Pathak N, Austin CA, Drummond IA (2011) Tubulin tyrosine ligase-like genes ttll3 and ttll6 maintain zebrafish cilia structure and motility. J Biol Chem 286:11685-11695
    Paturle-Lafanechere L, Edde B, Denoulet P, Van Dorsselaer A, Mazarguil H, Le Caer JP, Wehland J, Job D (1991) Characterization of a major brain tubulin variant which cannot be tyrosinated. Biochemistry-US 30:10523-10528
    Pazour GJ, Rosenbaum JL (2002) Intraflagellar transport and ciliadependent diseases. Trends Cell Biol 12:551-555
    Pedersen LB, Rosenbaum JL (2008) Intraflagellar transport (IFT)role in ciliary assembly, resorption and signalling. Curr Top Dev Biol 85:23-61
    Pigino G, Geimer S, Lanzavecchia S, Paccagnini E, Cantele F, Diener DR, Rosenbaum JL, Lupetti P (2009) Electron-tomographic analysis of intraflagellar transport particle trains in situ. J Cell Biol 187:135-148
    Piperno G, LeDizet M, Chang XJ (1987) Microtubules containing acetylated alpha-tubulin in mammalian cells in culture. J Cell Biol 104:289-302
    Portran D, Schaedel L, Xu Z, Théry M, Nachury MV (2017) Tubulin acetylation protects long-lived microtubules against mechanical ageing. Nat Cell Biol 19:391-398
    Praetorius HA, Spring KR (2001) Bending the MDCK cell primary cilium increases intracellular calcium. J Membr Biol 184:71-79
    Praetorius HA, Spring KR (2003a) Removal of the MDCK cell primary cilium abolishes flow sensing. J Membr Biol 191:69-76
    Praetorius HA, Spring KR (2003b) The renal cell primary cilium functions as a flow sensor. Curr Opin Nephrol Hypertens 12:517-520
    Prota AE, Magiera MM, Kuijpers M, Bargsten K, Frey D, Wieser M, Jaussi R, Hoogenraad CC, Kammerer RA, Janke C, Steinmetz MO (2013) Structural basis of tubulin tyrosination by tubulin tyrosine ligase. J Cell Biol 200:259-270
    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
    Ran J, Yang Y, Li D, Liu M, Zhou J (2015) Deacetylation of alphatubulin and cortactin is required for HDAC6 to trigger ciliary disassembly. Sci Rep 5:12917
    Rao KN, Anand M, Khanna H (2016) The carboxyl terminal mutational hotspot of the ciliary disease protein RPGRORF15(retinitis pigmentosa GTPase regulator) is glutamylated in vivo. Biol Open 5:424-428
    Redeker V, Levilliers N, Schmitter J, Le Caer J, Rossier J, Adoutte A, Bre M (1994) Polyglycylation of tubulin:a posttranslational modification in axonemal microtubules. Science 266:1688-1691
    Redeker V, Levilliers N, Vinolo E, Rossier J, Jaillard D, Burnette D, Gaertig J, Bre MH (2005) Mutations of tubulin glycylation sites reveal cross-talk between the C termini of alpha- and beta-tubulin and affect the ciliary matrix in Tetrahymena.J Biol Chem 280:596-606
    Reed NA, Cai D, Blasius TL, Jih GT, Meyhofer E, Gaertig J, Verhey KJ (2006) Microtubule acetylation promotes kinesin-1 binding and transport. Curr Biol 16:2166-2172
    Regnard C, Audebert S, Desbruyères É, Denoulet P, Eddé B (1998)Tubulin polyglutamylase:partial purification and enzymatic properties. Biochemistry-US 37:8395-8404
    Regnard C, Desbruyeres E, Denoulet P, Edde B (1999) Tubulin polyglutamylase:isozymic variants and regulation during the cell cycle in HeLa cells. J Cell Sci 112(Pt 23):4281-4289
    Regnard C, Desbruyeres E, Huet JC, Beauvallet C, Pernollet JC, Edde B (2000) Polyglutamylation of nucleosome assembly proteins. J Biol Chem 275:15969-15976
    Regnard C, Fesquet D, Janke C, Boucher D, Desbruyeres E, Koulakoff A, Insina C, Travo P, Edde B (2003) Characterisation of PGs1, a subunit of a protein complex co-purifying with tubulin polyglutamylase. J Cell Sci 116:4181-4190
    Robison P, Caporizzo MA, Ahmadzadeh H, Bogush AI, Chen CY, Margulies KB, Shenoy VB, Prosser BL (2016) Detyrosinated microtubules buckle and bear load in contracting cardiomyocytes. Science 352:0659
    Rocha C, Papon L, Cacheux W, Marques Sousa P, Lascano V, Tort O, Giordano T, Vacher S, Lemmers B, Mariani P, Meseure D, Medema JP, Bièche I, Hahne M, Janke C (2014) Tubulin glycylases are required for primary cilia, control of cell proliferation and tumor development in colon. EMBO J 33:2247-2260
    Rogowski K, Juge F, van Dijk J, Wloga D, Strub JM, Levilliers N, Thomas D, Bre MH, Van Dorsselaer A, Gaertig J, Janke C (2009) Evolutionary divergence of enzymatic mechanisms for posttranslational polyglycylation. Cell 137:1076-1087
    Rogowski K, van Dijk J, Magiera MM, Bosc C, Deloulme JC, Bosson A, Peris L, Gold ND, Lacroix B, Grau MB, Bec N, Larroque C, Desagher S, Holzer M, Andrieux A, Moutin M-J, Janke C (2010)A family of protein-deglutamylating enzymes associated with neurodegeneration. Cell 143:564-578
    Rosenbaum JL, Witman GB (2002) Intraflagellar transport. Nat Rev Mol Cell Biol 3:813-825
    Rüdiger M, Plessman U, Klöppel K-D, Wehland J, Weber K (1992)Class Ⅱ tubulin, the major brain b tubulin isotype is polyglutamylated on glutamic acid residue 435. FEBS Lett 308:101-105
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