Abstract
The microtubule (MT) cytoskeleton is essential for a variety of cellular processes. MTs are finely regulated by distinct classes of MT-associated proteins (MAPs), which themselves bind to and are regulated by a large number of additional proteins. We have carried out proteome analyses of tubulin-rich and tubulin-depleted MAPs and their interacting partners isolated from bovine brain. In total, 573 proteins were identified giving us unprecedented access to brain-specific MT-associated proteins from mammalian brain. Most of the standard MAPs were identified and at least 500 proteins have been reported as being associated with MTs. We identified protein complexes with a large number of subunits such as brain-specific motor/adaptor/cargo complexes for kinesins, dynein, and dynactin, and proteins of an RNA-transporting granule. About 25% of the identified proteins were also found in the synaptic vesicle proteome. Analysis of the MS/MS data revealed many posttranslational modifications, amino acid changes, and alternative splice variants, particularly in tau, a key protein implicated in Alzheimer’s disease. Bioinformatic analysis of known protein–protein interactions of the identified proteins indicated that the number of MAPs and their associated proteins is larger than previously anticipated and that our database will be a useful resource to identify novel binding partners.
Similar content being viewed by others
Abbreviations
- AMPPCP:
-
Adenylyl 5′-(β,γ-methylene)diphosphonate
- ATP:
-
Adenosine triphosphate
- EDTA:
-
Ethylenediaminetetraacetic acid
- GTP:
-
Guanosine triphosphate
- KLC:
-
Kinesin light chain
- MAPs:
-
Microtubule-associated proteins
- MgcRacGAP:
-
Rac GTPase-activating protein 1
- MKLP-1:
-
Mitotic kinesin-like protein 1
- MTs:
-
Microtubules
- PIPES:
-
1,4-Piperazinediethanesulfonic acid
- PMSF:
-
Phenylmethanesulfonylfluoride
- SVP:
-
Synaptic vesicle protein
- TAME:
-
N α -p-Tosyl-l-arginine methyl ester
References
Alfarano C, Andrade CE, Anthony K, Bahroos N, Bajec M, Bantoft K, Betel D, Bobechko B, Boutilier K, Burgess E, Buzadzija K, Cavero R, D’Abreo C, Donaldson I, Dorairajoo D, Dumontier MJ, Dumontier MR, Earles V, Farrall R, Feldman H, Garderman E, Gong Y, Gonzaga R, Grytsan V, Gryz E, Gu V, Haldorsen E, Halupa A, Haw R, Hrvojic A, Hurrell L, Isserlin R, Jack F, Juma F, Khan A, Kon T, Konopinsky S, Le V, Lee E, Ling S, Magidin M, Moniakis J, Montojo J, Moore S, Muskat B, Ng I, Paraiso JP, Parker B, Pintilie G, Pirone R, Salama JJ, Sgro S, Shan T, Shu Y, Siew J, Skinner D, Snyder K, Stasiuk R, Strumpf D, Tuekam B, Tao S, Wang Z, White M, Willis R, Wolting C, Wong S, Wrong A, Xin C, Yao R, Yates B, Zhang S, Zheng K, Pawson T, Ouellette BF, Hogue CW (2005) The Biomolecular Interaction Network Database and related tools 2005 update. Nucleic Acids Res 33:D418–D424
Ambudkar SV, Kimchi-Sarfaty C, Sauna ZE, Gottesman MM (2003) P-glycoprotein: from genomics to mechanism. Oncogene 22:7468–7485
Amos LA, Schlieper D (2005) Microtubules and maps. Adv Protein Chem 71:257–298
Aubert-Foucher E, Deleage G, Font B (1990) Do synapsin I and microtubule-associated proteins bind to a common site on polymerized tubulin? Biochem Int 22:821–827
Bader GD, Betel D, Hogue CW (2003) BIND: the Biomolecular Interaction Network Database. Nucleic Acids Res 31:248–250
Baines AJ, Bennett V (1986) Synapsin I is a microtubule-bundling protein. Nature 319:145–147
Barsnes H, Vizcaino JA, Eidhammer I, Martens L (2009) PRIDE Converter: making proteomics data-sharing easy. Nat Biotechnol 27:598–599
Bennett AF, Baines AJ (1992) Bundling of microtubules by synapsin 1. Characterization of bundling and interaction of distinct sites in synapsin 1 head and tail domains with different sites in tubulin. Eur J Biochem 206:783–792
Berrueta L, Kraeft SK, Tirnauer JS, Schuyler SC, Chen LB, Hill DE, Pellman D, Bierer BE (1998) The adenomatous polyposis coli-binding protein EB1 is associated with cytoplasmic and spindle microtubules. Proc Natl Acad Sci USA 95:10596–10601
Berrueta L, Tirnauer JS, Schuyler SC, Pellman D, Bierer BE (1999) The APC-associated protein EB1 associates with components of the dynactin complex and cytoplasmic dynein intermediate chain. Curr Biol 9:425–428
Bhaskar K, Shareef MM, Sharma VM, Shetty AP, Ramamohan Y, Pant HC, Raju TR, Shetty KT (2004) Co-purification and localization of Munc18-1 (p67) and Cdk5 with neuronal cytoskeletal proteins. Neurochem Int 44:35–44
Bhat KM, Setaluri V (2007) Microtubule-associated proteins as targets in cancer chemotherapy. Clin Cancer Res 13:2849–2854
Brown KR, Jurisica I (2005) Online predicted human interaction database. Bioinformatics 21:2076–2082
Burre J, Volknandt W (2007) The synaptic vesicle proteome. J Neurochem 101:1448–1462
Burre J, Beckhaus T, Schagger H, Corvey C, Hofmann S, Karas M, Zimmermann H, Volknandt W (2006) Analysis of the synaptic vesicle proteome using three gel-based protein separation techniques. Proteomics 6:6250–6262
Cai Q, Pan PY, Sheng ZH (2007) Syntabulin-kinesin-1 family member 5B-mediated axonal transport contributes to activity-dependent presynaptic assembly. J Neurosci 27:7284–7296
Candiano G, Bruschi M, Musante L, Santucci L, Ghiggeri GM, Carnemolla B, Orecchia P, Zardi L, Righetti PG (2004) Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 25:1327–1333
Chatr-aryamontri A, Ceol A, Palazzi LM, Nardelli G, Schneider MV, Castagnoli L, Cesareni G (2007) MINT: the Molecular INTeraction database. Nucleic Acids Res 35:D572–D574
Chuong SD, Good AG, Taylor GJ, Freeman MC, Moorhead GB, Muench DG (2004) Large-scale identification of tubulin-binding proteins provides insight on subcellular trafficking, metabolic channeling, and signaling in plant cells. Mol Cell Proteomics 3:970–983
Correas I, Avila J (1988) Erythrocyte protein 4.1 associates with tubulin. Biochem J 255:217–221
Diefenbach RJ, Diefenbach E, Douglas MW, Cunningham AL (2002) The heavy chain of conventional kinesin interacts with the SNARE proteins SNAP25 and SNAP23. Biochemistry 41:14906–14915
Dutcher SK (2001) The tubulin fraternity: alpha to eta. Curr Opin Cell Biol 13:49–54
Echard A, Jollivet F, Martinez O, Lacapere JJ, Rousselet A, Janoueix-Lerosey I, Goud B (1998) Interaction of a golgi-associated kinesin-like protein with Rab6. Science 279:580–585
Eichenmuller B, Ahrens DP, Li Q, Suprenant KA (2001) Saturable binding of the echinoderm microtubule-associated protein (EMAP) on microtubules, but not filamentous actin or vimentin filaments. Cell Motil Cytoskeleton 50:161–172
Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4:1313–1317
Ferreira A, Niclas J, Vale RD, Banker G, Kosik KS (1992) Suppression of kinesin expression in cultured hippocampal neurons using antisense oligonucleotides. J Cell Biol 117:595–606
Gache V, Waridel P, Luche S, Shevchenko A, Popov AV (2007) Purification and mass spectrometry identification of microtubule-binding proteins from Xenopus egg extracts. Methods Mol Med 137:29–43
Gache V, Waridel P, Winter C, Juhem A, Schroeder M, Shevchenko A, Popov AV (2010) Xenopus meiotic microtubule-associated interactome. PLoS One 5:e9248
Galiano MR, Andrieux A, Deloulme JC, Bosc C, Schweitzer A, Job D, Hallak ME (2006) Myelin basic protein functions as a microtubule stabilizing protein in differentiated oligodendrocytes. J Neurosci Res 84:534–541
Gendreau S, Schirmer J, Schmalzing G (2003) Identification of a tubulin binding motif on the P2X2 receptor. J Chromatogr B Analyt Technol Biomed Life Sci 786:311–318
Gleeson JG, Lin PT, Flanagan LA, Walsh CA (1999) Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 23:257–271
Goode BL, Wong JJ, Butty AC, Peter M, McCormack AL, Yates JR, Drubin DG, Barnes G (1999) Coronin promotes the rapid assembly and cross-linking of actin filaments and may link the actin and microtubule cytoskeletons in yeast. J Cell Biol 144:83–98
Green LA, Liem RK (1989) Beta-internexin is a microtubule-associated protein identical to the 70-kDa heat-shock cognate protein and the clathrin uncoating ATPase. J Biol Chem 264:15210–15215
Guldener U, Munsterkotter M, Oesterheld M, Pagel P, Ruepp A, Mewes HW, Stumpflen V (2006) MPact: the MIPS protein interaction resource on yeast. Nucleic Acids Res 34:D436–D441
Gundersen GG, Cook TA (1999) Microtubules and signal transduction. Curr Opin Cell Biol 11:81–94
Gyoeva FK, Sarkisov DV, Khodjakov AL, Minin AA (2004) The tetrameric molecule of conventional kinesin contains identical light chains. Biochemistry 43:13525–13531
Hermjakob H, Fleischmann W, Apweiler R (1999) Swissknife—‘lazy parsing’ of SWISS-PROT entries. Bioinformatics 15:771–772
Hermjakob H, Montecchi-Palazzi L, Lewington C, Mudali S, Kerrien S, Orchard S, Vingron M, Roechert B, Roepstorff P, Valencia A, Margalit H, Armstrong J, Bairoch A, Cesareni G, Sherman D, Apweiler R (2004) IntAct: an open source molecular interaction database. Nucleic Acids Res 32:D452–D455
Hill AM, Cassoly R, Chetrite G, Pantaloni D (1985) High molecular weight microtubule-associated proteins from pig brain are immunologically related to human erythrocyte membrane proteins spectrin, ankyrin, proteins 4.1 and 4.2. Biol Cell 53:141–147
Hirokawa N, Noda Y (2008) Intracellular transport and kinesin superfamily proteins, KIFs: structure, function, and dynamics. Physiol Rev 88:1089–1118
Homma N, Takei Y, Tanaka Y, Nakata T, Terada S, Kikkawa M, Noda Y, Hirokawa N (2003) Kinesin superfamily protein 2A (KIF2A) functions in suppression of collateral branch extension. Cell 114:229–239
Honda A, Yamada M, Saisu H, Takahashi H, Mori KJ, Abe T (2002) Direct, Ca2+-dependent interaction between tubulin and synaptotagmin I: a possible mechanism for attaching synaptic vesicles to microtubules. J Biol Chem 277:20234–20242
Hook P, Vallee RB (2006) The dynein family at a glance. J Cell Sci 119:4369–4371
Huang JD, Brady ST, Richards BW, Stenolen D, Resau JH, Copeland NG, Jenkins NA (1999) Direct interaction of microtubule- and actin-based transport motors. Nature 397:267–270
Huang DW, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4:44–57
Hughes JR, Meireles AM, Fisher KH, Garcia A, Antrobus PR, Wainman A, Zitzmann N, Deane C, Ohkura H, Wakefield JG (2008) A microtubule interactome: complexes with roles in cell cycle and mitosis. PLoS Biol 6:e98
Inoue E, Mochida S, Takagi H, Higa S, Deguchi-Tawarada M, Takao-Rikitsu E, Inoue M, Yao I, Takeuchi K, Kitajima I, Setou M, Ohtsuka T, Takai Y (2006) SAD: a presynaptic kinase associated with synaptic vesicles and the active zone cytomatrix that regulates neurotransmitter release. Neuron 50:261–275
Ishikawa M, Murofushi H, Sakai H (1983) Bundling of microtubules in vitro by fodrin. J Biochem 94:1209–1217
Itoh TJ, Fujiwara T, Shibuya T, Akagawa K, Hotani H (1999) Inhibition of microtubule assembly by HPC-1/syntaxin 1A, an exocytosis relating protein. Cell Struct Funct 24:359–364
Ivings L, Pennington SR, Jenkins R, Weiss JL, Burgoyne RD (2002) Identification of Ca2+-dependent binding partners for the neuronal calcium sensor protein neurocalcin delta: interaction with actin, clathrin and tubulin. Biochem J 363:599–608
Jacob C, Giles GI, Giles NM, Sies H (2003) Sulfur and selenium: the role of oxidation state in protein structure and function. Angew Chem Int Ed Engl 42:4742–4758
Jordan MA, Wilson L (2004) Microtubules as a target for anticancer drugs. Nat Rev Cancer 4:253–265
Jungblut P, Thiede B, Zimny-Arndt U, Muller EC, Scheler C, Wittmann-Liebold B, Otto A (1996) Resolution power of two-dimensional electrophoresis and identification of proteins from gels. Electrophoresis 17:839–847
Jungblut PR, Holzhutter HG, Apweiler R, Schluter H (2008) The speciation of the proteome. Chem Cent J 2:16
Juwana JP, Henderikx P, Mischo A, Wadle A, Fadle N, Gerlach K, Arends JW, Hoogenboom H, Pfreundschuh M, Renner C (1999) EB/RP gene family encodes tubulin binding proteins. Int J Cancer 81:275–284
Kanai Y, Dohmae N, Hirokawa N (2004) Kinesin transports RNA: isolation and characterization of an RNA-transporting granule. Neuron 43:513–525
Kann ML, Fouquet JP (1993) Association of spectrin with manchette microtubules in mammalian spermatids. Biol Cell 77:311–313
Kavallaris M, Tait AS, Walsh BJ, He L, Horwitz SB, Norris MD, Haber M (2001) Multiple microtubule alterations are associated with Vinca alkaloid resistance in human leukemia cells. Cancer Res 61:5803–5809
Kerrien S, Alam-Faruque Y, Aranda B, Bancarz I, Bridge A, Derow C, Dimmer E, Feuermann M, Friedrichsen A, Huntley R, Kohler C, Khadake J, Leroy C, Liban A, Lieftink C, Montecchi-Palazzi L, Orchard S, Risse J, Robbe K, Roechert B, Thorneycroft D, Zhang Y, Apweiler R, Hermjakob H (2007) IntAct—open source resource for molecular interaction data. Nucleic Acids Res 35:D561–D565
Kimura T, Watanabe H, Iwamatsu A, Kaibuchi K (2005) Tubulin and CRMP-2 complex is transported via Kinesin-1. J Neurochem 93:1371–1382
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
Liska AJ, Popov AV, Sunyaev S, Coughlin P, Habermann B, Shevchenko A, Bork P, Karsenti E, Shevchenko A (2004) Homology-based functional proteomics by mass spectrometry: application to the Xenopus microtubule-associated proteome. Proteomics 4:2707–2721
Luton F (2005) The role of EFA6, exchange factor for Arf6, for tight junction assembly, functions, and interaction with the actin cytoskeleton. Methods Enzymol 404:332–345
Maiato H, Sampaio P, Sunkel CE (2004) Microtubule-associated proteins and their essential roles during mitosis. Int Rev Cytol 241:53–153
Mannan AU, Boehm J, Sauter SM, Rauber A, Byrne PC, Neesen J, Engel W (2006) Spastin, the most commonly mutated protein in hereditary spastic paraplegia interacts with Reticulon 1 an endoplasmic reticulum protein. Neurogenetics 7:93–103
McKean PG, Vaughan S, Gull K (2001) The extended tubulin superfamily. J Cell Sci 114:2723–2733
Mishima M, Kaitna S, Glotzer M (2002) Central spindle assembly and cytokinesis require a kinesin-like protein/RhoGAP complex with microtubule bundling activity. Dev Cell 2:41–54
Mishra GR, Suresh M, Kumaran K, Kannabiran N, Suresh S, Bala P, Shivakumar K, Anuradha N, Reddy R, Raghavan TM, Menon S, Hanumanthu G, Gupta M, Upendran S, Gupta S, Mahesh M, Jacob B, Mathew P, Chatterjee P, Arun KS, Sharma S, Chandrika KN, Deshpande N, Palvankar K, Raghavnath R, Krishnakanth R, Karathia H, Rekha B, Nayak R, Vishnupriya G, Kumar HG, Nagini M, Kumar GS, Jose R, Deepthi P, Mohan SS, Gandhi TK, Harsha HC, Deshpande KS, Sarker M, Prasad TS, Pandey A (2006) Human protein reference database—2006 update. Nucleic Acids Res 34:D411–D414
Mollinedo F, Gajate C (2003) Microtubules, microtubule-interfering agents and apoptosis. Apoptosis 8:413–450
Moss DK, Lane JD (2006) Microtubules: forgotten players in the apoptotic execution phase. Trends Cell Biol 16:330–338
Nakata T, Hirokawa N (2003) Microtubules provide directional cues for polarized axonal transport through interaction with kinesin motor head. J Cell Biol 162:1045–1055
Nakayama M, Kikuno R, Ohara O (2002) Protein-protein interactions between large proteins: two-hybrid screening using a functionally classified library composed of long cDNAs. Genome Res 12:1773–1784
Okajima T, Kawata Y, Hamaguchi K (1990) Chemical modification of tryptophan residues and stability changes in proteins. Biochemistry 29:9168–9175
Orban-Nemeth Z, Simader H, Badurek S, Trancikova A, Propst F (2005) Microtubule-associated protein 1S, a short and ubiquitously expressed member of the microtubule-associated protein 1 family. J Biol Chem 280:2257–2265
Pagel P, Kovac S, Oesterheld M, Brauner B, Dunger-Kaltenbach I, Frishman G, Montrone C, Mark P, Stumpflen V, Mewes HW, Ruepp A, Frishman D (2005) The MIPS mammalian protein-protein interaction database. Bioinformatics 21:832–834
Peri S, Navarro JD, Amanchy R, Kristiansen TZ, Jonnalagadda CK, Surendranath V, Niranjan V, Muthusamy B, Gandhi TK, Gronborg M, Ibarrola N, Deshpande N, Shanker K, Shivashankar HN, Rashmi BP, Ramya MA, Zhao Z, Chandrika KN, Padma N, Harsha HC, Yatish AJ, Kavitha MP, Menezes M, Choudhury DR, Suresh S, Ghosh N, Saravana R, Chandran S, Krishna S, Joy M, Anand SK, Madavan V, Joseph A, Wong GW, Schiemann WP, Constantinescu SN, Huang L, Khosravi-Far R, Steen H, Tewari M, Ghaffari S, Blobe GC, Dang CV, Garcia JG, Pevsner J, Jensen ON, Roepstorff P, Deshpande KS, Chinnaiyan AM, Hamosh A, Chakravarti A, Pandey A (2003) Development of human protein reference database as an initial platform for approaching systems biology in humans. Genome Res 13:2363–2371
Perkins DN, Pappin DJ, Creasy DM, Cottrell JS (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20:3551–3567
Peter F, Nuoffer C, Pind SN, Balch WE (1994) Guanine nucleotide dissociation inhibitor is essential for Rab1 function in budding from the endoplasmic reticulum and transport through the Golgi stack. J Cell Biol 126:1393–1406
Pollard TD, Earnshaw WC (2004) Cell biology. Elsevier, pp 589–593
Razick S, Magklaras G, Donaldson IM (2008) iRefIndex: a consolidated protein interaction database with provenance. BMC Bioinformatics 9:405
Rodriguez OC, Schaefer AW, Mandato CA, Forscher P, Bement WM, Waterman-Storer CM (2003) Conserved microtubule-actin interactions in cell movement and morphogenesis. Nat Cell Biol 5:599–609
Roger B, Al-Bassam J, Dehmelt L, Milligan RA, Halpain S (2004) MAP2c, but not tau, binds and bundles F-actin via its microtubule binding domain. Curr Biol 14:363–371
Salwinski L, Miller CS, Smith AJ, Pettit FK, Bowie JU, Eisenberg D (2004) The Database of Interacting Proteins: 2004 update. Nucleic Acids Res 32:D449–D451
Saoudi Y, Paintrand I, Multigner L, Job D (1995) Stabilization and bundling of subtilisin-treated microtubules induced by microtubule associated proteins. J Cell Sci 108(Pt 1):357–367
Scales SJ, Hesser BA, Masuda ES, Scheller RH (2002) Amisyn, a novel syntaxin-binding protein that may regulate SNARE complex assembly. J Biol Chem 277:28271–28279
Schluter H, Apweiler R, Holzhutter HG, Jungblut PR (2009) Finding one’s way in proteomics: a protein species nomenclature. Chem Cent J 3:11
Schroer TA (2004) Dynactin. Annu Rev Cell Dev Biol 20:759–779
Setou M, Nakagawa T, Seog DH, Hirokawa N (2000) Kinesin superfamily motor protein KIF17 and mLin-10 in NMDA receptor-containing vesicle transport. Science 288:1796–1802
Setou M, Seog DH, Tanaka Y, Kanai Y, Takei Y, Kawagishi M, Hirokawa N (2002) Glutamate-receptor-interacting protein GRIP1 directly steers kinesin to dendrites. Nature 417:83–87
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504
Sharp DJ, Yu W, Ferhat L, Kuriyama R, Rueger DC, Baas PW (1997) Identification of a microtubule-associated motor protein essential for dendritic differentiation. J Cell Biol 138:833–843
Sharp DJ, Rogers GC, Scholey JM (2000) Microtubule motors in mitosis. Nature 407:41–47
Stark C, Breitkreutz BJ, Reguly T, Boucher L, Breitkreutz A, Tyers M (2006) BioGRID: a general repository for interaction datasets. Nucleic Acids Res 34:D535–D539
Su Q, Cai Q, Gerwin C, Smith CL, Sheng ZH (2004) Syntabulin is a microtubule-associated protein implicated in syntaxin transport in neurons. Nat Cell Biol 6:941–953
Takamori S, Holt M, Stenius K, Lemke EA, Gronborg M, Riedel D, Urlaub H, Schenck S, Brugger B, Ringler P, Muller SA, Rammner B, Grater F, Hub JS, De Groot BL, Mieskes G, Moriyama Y, Klingauf J, Grubmuller H, Heuser J, Wieland F, Jahn R (2006) Molecular anatomy of a trafficking organelle. Cell 127:831–846
UniProt consortium (2008) The universal protein resource (UniProt). Nucleic Acids Res 36:D190–D195
Utton MA, Noble WJ, Hill JE, Anderton BH, Hanger DP (2005) Molecular motors implicated in the axonal transport of tau and alpha-synuclein. J Cell Sci 118:4645–4654
Vaughan L, Weber P, D’Alessandri L, Zisch AH, Winterhalter KH (1994) Tenascin-contactin/F11 interactions: a clue for a developmental role? Perspect Dev Neurobiol 2:43–52
Verhey KJ, Meyer D, Deehan R, Blenis J, Schnapp BJ, Rapoport TA, Margolis B (2001) Cargo of kinesin identified as JIP scaffolding proteins and associated signaling molecules. J Cell Biol 152:959–970
Wade RH (2007) Microtubules: an overview. Methods Mol Med 137:1–16
Wang JZ, Liu F (2008) Microtubule-associated protein tau in development, degeneration and protection of neurons. Prog Neurobiol 85:148–175
Wang JZ, Grundke-Iqbal I, Iqbal K (2007) Kinases and phosphatases and tau sites involved in Alzheimer neurofibrillary degeneration. Eur J Neurosci 25:59–68
Williams RC Jr, Lee JC (1982) Preparation of tubulin from brain. Methods Enzymol 85(Pt B):376–385
Xue J, Tsang CW, Gai WP, Malladi CS, Trimble WS, Rostas JA, Robinson PJ (2004) Septin 3 (G-septin) is a developmentally regulated phosphoprotein enriched in presynaptic nerve terminals. J Neurochem 91:579–590
Ye K, Compton DA, Lai MM, Walensky LD, Snyder SH (1999) Protein 4.1N binding to nuclear mitotic apparatus protein in PC12 cells mediates the antiproliferative actions of nerve growth factor. J Neurosci 19:10747–10756
Yoshida Y, Takei K (2005) Stimulation of dynamin GTPase activity by amphiphysin. Methods Enzymol 404:528–537
Yu JZ, Rasenick MM (2006) Tau associates with actin in differentiating PC12 cells. FASEB J 20:1452–1461
Yu LR, Zhu Z, Chan KC, Issaq HJ, Dimitrov DS, Veenstra TD (2007) Improved titanium dioxide enrichment of phosphopeptides from HeLa cells and high confident phosphopeptide identification by cross-validation of MS/MS and MS/MS/MS spectra. J Proteome Res 6:4150–4162
Yuan A, Mills RG, Chia CP, Bray JJ (2000) Tubulin and neurofilament proteins are transported differently in axons of chicken motoneurons. Cell Mol Neurobiol 20:623–632
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kozielski, F., Riaz, T., DeBonis, S. et al. Proteome analysis of microtubule-associated proteins and their interacting partners from mammalian brain. Amino Acids 41, 363–385 (2011). https://doi.org/10.1007/s00726-010-0649-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00726-010-0649-5