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Detection, Distribution and Amount of Posttranslational α-Tubulin Modifications in Immortalized Rat Schwann Cells

S. D. Gadau

Abstract


Microtubules (MTs), heterodimers of α- and β-tubulin, are involved in different cellular processes including mitosis, cell motility, intracellular transport, cell shape and polarization. In most eukaryotes tubulins, especially the α, are subjected to several post-translational modifications (PTMs) which include acetylation, tyrosination, detyrosination, Δ2 modification, polyglutamylation, that characterize different type of MTs and regulate the interactions between MTs and certain MAPs or motor proteins. Despite neurons, in which presence and distributions of tubulin PTMs are well evaluated, in glial cells like Schwann cells, little is known about the diverse tubulin PTMs amount, distribution and their functional role. So that, the purpose of the present work was to deepen the knowledge about the diverse tubulin PTMs in a commonly used immortalized Schwann cell line. By Western blot analysis we found a higher amount of   polyglutamylated and tyrosinated α-tubulin, whereas acetylated, Δ2 and detyrosinated α-tubulin were less expressed.  Immunofluorescence staining, highlighted the distribution of acetylated and detyrosinated α-tubulin along the Schwann cells prolongations. In contrast, polyglutamylated α-tubulin was more detectable close to the cell body of Schwann cells, whereas the Δ2-modification was mainly distributed round the nuclear profile. Summing up, our investigation offers insight on several tubulin PTMs amount and distribution in Schwann cells. This could be a further contribution to better understand the role played by different MTs in Schwann cells biology and during the onset of certain disorders of peripheral nervous system.

Keywords


Schwann cells; microtubules; tubulin posttranslational modifications

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Abal M., Keryer G., Bornens M. Centrioles resist forces applied on centrosomes during G2/M transition. Biol. Cell. 97: 425-434, 2005.

Ahmad F.J., Pienkowsky T.P., Baas P.W. Regional differences in microtubule dynamics in the axon. J. Neurosci. 13: 856-866, 1993.

Audebert S., Koulakoff A., Berwald-Netter Y., Gros F., Denoulet P., Eddè B. Developmental regulation of polyglutamylated alpha- and beta-tubulin im mouse brain neurons. J. Cell Sci. 107: 2313-2322, 1994.

Audebert S., Desbruyères E., Gruszczynski C., Koulakoff A., Gros F., Denoulet P. et al. Reversible polyglutamylation of alpha- and beta-tubulin and microtubule dynamics in mouse brain neurons. Mol. Biol. Cell. 4: 615-626, 1993.

Bhatheja K., Field J. Schwann cells: origins and role in axonal maintenance and regeneration. Int. J. Biochem. Cell Biol. 38: 1995-1999, 2006

Bauer N.G., Richter-Landsberg C., Ffrench-Constant C. Role of the oligodendroglial cytoskeleton in differentiation and myelination. Glia. 57: 1691-1705, 2009.

Bonnet C., Boucher D., Lazereg S., Pedrotti B., Islam K., Denoulet P., Larcher J.C. Differential binding regulation of microtubule-associated proteins MAP1A, MAP1B, and MAP2 by tubulin

polyglutamylation. J. Biol. Chem. 276: 12839–12848, 2001.

Cambray-Deakin M.A. and Burgoyne R.D. Acetylated and detyrosinated alpha-tubulins are co-localized in stable microtubules in rat meningeal fibroblasts. Cell Motil Cytoskeleton. 8: 284-291, 1987.(a)

Cambray-Deakin M.A. and Burgoyne R.D J. Posttranslational modifications of alpha-tubulin: acetylated and detyrosinated forms in axons of rat cerebellum. J. Cell Biol. 104: 1569-1574, 1987.(b).

Dunn S., Morrison E.E., Liverpool T.B., Molina-Paris C., Cross R.A., Alonso M.C., Peckham M. Differential traffiking of Kif5c on tyrosinated and detyrosinated microtubules in live cells. J. Cell Sci.121: 1085-1095, 2007.

Fukushima N., Furuta D., Hidaka Y., Moriyama R., Tsujiuchi T. Post-translational modifications of tubulin in the nervous system. J. Neurochem. 109: 683-693, 2009.

Gaertig J. and Wloga D. Ciliary tubulin and its post-translational modifications. Curr. Top Dev. Biol. 85: 83-113, 2008.

Galjart N. Plus-end-tracking proteins and their interactions at microtubule ends. Curr. Biol. 20: 528-37, 2010.

Garnham C.P., Roll-Mecak A. The chemical complexity of cellular microtubules: tubulin post-translational modification enzymes and their roles in tuning microtubule functions. Cytoskeleton (Hoboken). 69: 442-463, 2012.

Glenn T.D. and Talbot W.S. Signals regulating myelination in peripheral nerves and the Schwann cell response to injury. Curr. Opin. Neurobiol. 23: 1041-1048, 2013.

Gonzalez-Martinez T., Perez-Piñera P., Díaz-Esnal B., Vega JA. S-100 proteins in the human peripheral nervous system. Microsc. Res. Tech. 60: 633-638, 2003.

Guillaud L., Bosc C., Fourest-Lieuvin A., Denarier E., Pirollet F., Lafanechere L., Job D. STOP proteins are responsible for the high degree of microtubule stabilization observed in neuronal cells. J. Cell Biol. 142: 167-179, 1998.

Hagiwara N., Imada S., Sueoka N. Cell-type specific segregationof transcriptional expression of glial genes in the rat peripheral neurotumor RT4 cell lines. J. Neurosci. Res. 36: 646-656, 1993.

Hai M., Muja N., DeVries G.H., Quarles R.H., Patel P.I. Comparative analysis of Schwann cell lines as model system for myelin gene transcription studies. J. Neurosci. Res.69: 497-508, 2002.

Hammond J.W., Cai D., Verhey K.J. Tubulin modifications and their cellular functions. Curr. Opin. Cell Biol. 20: 71-76, 2008.

Hattangady N.G., Rajsdhyaksha M.S. A brief review of in vitro models of diabetic neuropathy. Int. J Diabetes Dev. Ctries. 29: 143-149, 2009.

Ikegami K, Heier RL, Taruishi M, Takagi H, Mukai M, Shimma S., Taira S., Hatanaka K., Morone N., Yao I., Campbell P.K., Yuasa S., Janke C., Macgregor G.R., Setou M. Loss of alpha-tubulin polyglutamylation in ROSA22 mice is associated with abnormal targeting of KIF1A and modulated synaptic function. Proc. Natl. Acad. Sci. U S A. 104: 3213-3218, 2007.

Ikegami K., Mukai M., Tsuchida J., Heier R.L., Macgregor G.R., Setou M. TTLL7 is a mammalian bet-tubulin polyglutamylase required for growth of MAP2-positive neuritis. J. Biol. Chem. 281: 30707-30716, 2006.

Janke C. The tubulin code: molecular components, readout mechanisms and functions. J. Cell Biol. 206: 461-472, 2014.

Janke C., Bulinski J.C. Post-translational regulation of the microtubule cytoskeleton: mechanisms and functions. Nat. Rev. Mol. Cell. Biol. 12: 773-786, 2011.

Janke C., Kneussel M. Tubulin post-translational modifications: encoding functions on the neuronal microtubule cytoskeleton. Trends Neurosci. 33: 362-372, 2010.

Jaworski J., Hoogenraad C.C., Akhmanova A. Microtubule plus-end tracking proteins in differentiated mammalian cells. Int. J. Biochem. Cell Biol. 40: 619-37, 2008.

Mar 15;2. pii: 19. doi: 10.3410/B2-19.

Jessen K.R., Mirsky R. Control of Schwann cell myelination. F1000 Biol. Rep. 19:1-4, 2010

Jessen K.R. Glial cells. Int. J. Biochem. Cell Biol. 36: 1861-1867, 2004.

Konishi Y., Setou M. Tubulin tyrosination navigates the kinesin-1 motor domain to axons. Nat. Neurosci. 12: 559-567, 2009.

Kidd G.J., Andrews S.B., Trapp B.D. Organization of microtubules in myelinating Schwann cells. J. Neurocytol. 23: 801-810, 1994.

Kim H.A., Mindos T., Parkinson D.B. Plastic fantastic: Schwann cells and repair of the peripheral nervous system. Stem Cells Transl. Med. 2: 553-557, 2013.

Maas C., Belgardt D., Lee H.K., Heisler F.F., Lappe-Siefke C., Magiera M.M., van Dijk J., Hausrat T.J., Janke C., Kneussel M. Synaptic activation modifies microtubules underlying transport of postsynaptic cargo. Proc. Natl. Acad. Sci. U S A. 106: 8731-8736, 2009.

Magiera M.M., Janke C. Post-translational modifications of tubulin. Curr. Biol. 24: 351-354, 2014.

Miller R.H. Unwrapping HDAC1 and HDAC2 functions in Schwann cell myelination. Nat. Neuroscience. 14: 401-403, 2011

Parker A.L., Kavallaris M., McCarroll J.A. Microtubules and their role in cellular stress in cancer. Front. Oncol. 4:1-19, 2014.

Paturle-Lafanechere L., Manier M., Trigault N., Pirollet F., Mazarguil H., Job D. Accumulation of delta 2-tubulin, a major tubulin variant that cannot be tyrosinated, in neuronal tissues and in stable microtubule assembles. J. Cell Sci. 107: 1529-1543, 1994.

Prota A.E., Bargsten K., Zurwerra D., Field J.J., Díaz J.F., Altmann K.H. et al. Molecular mechanism of action of microtubule-stabilizing anticancer agents. Science. 339:587-590, 2013.

Prokop A. The intricate relationship between microtubules and their associated motor proteins during axon growth and maintenance. Neural Dev. 8: 1-10, 2013.

Rosenbaum J. Cytoskeleton: functions for tubulin modifications at last. Curr. Biol. 10: 801-803, 2000.

Richter-Landsberg C. The cytoskeleton in oligodendrocytes. Microtubule dynamics in health and disease. J. Mol. Neurosci. 35: 55-63, 2008.

Richter-Landsberg C. Organization and functional roles of the cytoskeleton in oligodendrocytes. Microsc. Res. Tech. 52: 628-36, 2001.

Richter-Landsberg C. The oligodendroglia cytoskeleton in health and disease. J. Neurosci. Res. 59: 8-11, 2000.

Sakakibara A., Sato T., Ando R., Noguchi N., Masaoka M., Miyata T. Dynamics of centrosome translocation and microtubule organization in neocortical neurons during distinct modes of polarization. Cereb. Cortex. 24: 1301-1310, 2014.

Sango K., Yanagisawa H., Takaku S., Kawakami E., Watabe K. Immortalized adult rodent Schwann cells as in vitro models to study diabetic neuropathy. Exp. Diabetes Res., doi: 10.1155/2011/374943, 2011.a

Sango K., Yanagisawa H., Kawakami E., Takaku S., Ajiki K., Watabe K. Spontaneously immortalized Schwann cells from adult Fischer rat as a valuable tool for exploring neuron-Schwann cell interactions. J. Neurosci. Res. 89: 898-908, 2011.b

Shea T.B. Selective stabilization of microtubules within the proximal region of developing axonal neuritis. Brain Res. Bull. 43: 322-333, 1999.

Spiliotis E.T., Hunt S.J., Hu Q., Kinoshita M., Nelson W.J. Epithelial polarity requires septin coupling of vesicle transport to polyglutamylated microtubules. J. Cell Biol.; 180:295–303, 2008.

Toda K., Small J.A., Goda S., Quarles R.H. Biochemical and cellular properties of three immortalized Schwann cell lines expressing different levels of the myelin-associated glycoprotein. J. Neurochem. 63: 1646-1657, 1994.

Triolo D., Dina G., Lorenzetti I., Malaguti M., Morana P., Del Carro U., Comi G., Messing A., Quattrini A., Previtali SC. Loss of glial fibrillary acidic protein (GFAP) impairs Schwann cell proliferation and delays nerve regeneration after damage. J. Cell. Sci. 119: 3981-3993, 2006.

Vasiliev J.M., Samoylov V.I. Regulatory functions of microtubules. Biochemistry (Mosc).78: 37-40, 2013.

Verhey K.J., Gaertig J. The tubulin code. Cell Cycle. 6: 2152-2160, 2007.

Wade R.H. On and around microtubules: an overview. Mol. Biotechnol. 43: 177-191, 2009.

Watabe K., Fukuda T., Tanaka J., Honda H., Toyohara K., Sakai O. Spontaneously immortalized adult mouse Schwann cells secrete autocrine and paracrine growth-promoting activities. J. Neurosci. Res. 41:279-290, 1995.

Westermann S., Weber K. Post-translational modifications regulate microtubule function. Nat. Rev. Mol. Cell Biol. 4: 938-947, 2003.

Wloga D., Gaertig J. Post-translational modifications of microtubules. J. Cell. Sci. 123: 3447-3455, 2010.




DOI: https://doi.org/10.4449/aib.v153i4.3528

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