Proteomic Profiling and Functional Characterization of Multiple Post-Translational Modifications of Tubulin

Journal of Proteome Research

Volumn 14, Issue 8, 2015, Pages 3292-3304

  Liu, Ningning ^a   Xiong, Yun ^b   Ren, Yiran ^a   Zhang, Linlin ^a   He, Xianfei ^a   Wang, Xincheng ^a   Liu, Min ^a   Li, Dengwen ^a   Shui, Wenqing ^b   Zhou, Jun ^a  

^a NANKAI UNIVERSITY   (China)

^b Chinese Academy of Sciences   (China)

Author keywords

intracellular transport; microtubule assembly; microtubule stability; post translational modification; tubulin

Indexed keywords

MUTANT PROTEIN; TUBULIN; GREEN FLUORESCENT PROTEIN;

ACETYLATION; ACYLATION; ADENOVIRIDAE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; FEMALE; FUNCTIONAL PROTEOMICS; HELA CELL LINE; HUMAN; HUMAN CELL; MICROTUBULE ASSEMBLY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ACETYLATION; PROTEIN ANALYSIS; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN STABILITY; PROTEIN TARGETING; STRUCTURAL PROTEOMICS; UBIQUITINATION; AMINO ACID SEQUENCE; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; FLUORESCENCE MICROSCOPY; GENETICS; GLYCOSYLATION; IMMUNOBLOTTING; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLISM; MICROTUBULE; MOLECULAR GENETICS; PHOSPHORYLATION; PROCEDURES; PROTEIN TERTIARY STRUCTURE; PROTEOMICS; SEQUENCE HOMOLOGY;

ACETYLATION; AMINO ACID SEQUENCE; BINDING SITES; CHROMATOGRAPHY, LIQUID; GLYCOSYLATION; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; IMMUNOBLOTTING; MASS SPECTROMETRY; MICROSCOPY, FLUORESCENCE; MICROTUBULES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; PROTEOMICS; SEQUENCE HOMOLOGY, AMINO ACID; TUBULIN; UBIQUITINATION;

EID: 84938791590     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/acs.jproteome.5b00308     Document Type: Article

References (51)

1. Luduena, R. F.; Shooter, E. M.; Wilson, L. Structure of the tubulin dimer J. Biol. Chem. 1977, 252 (20) 7006-7014
2. Cleveland, D. W.; Lopata, M. A.; MacDonald, R. J.; Cowan, N. J.; Rutter, W. J.; Kirschner, M. W. Number and evolutionary conservation of alpha- and beta-tubulin and cytoplasmic beta- and gamma-actin genes using specific cloned cDNA probes Cell 1980, 20 (1) 95-105 10.1016/0092-8674(80)90238-X
3. Luduena, R. F. Multiple forms of tubulin: different gene products and covalent modifications Int. Rev. Cytol. 1998, 178, 207-275
4. Nogales, E. Structural insight into microtubule function Annu. Rev. Biophys. Biomol. Struct. 2001, 30, 397-420 10.1146/annurev.biophys.30.1.397
5. Peris, L.; Thery, M.; Faure, J.; Saoudi, Y.; Lafanechere, L.; Chilton, J. K.; Gordon-Weeks, P.; Galjart, N.; Bornens, M.; Wordeman, L.; Wehland, J.; Andrieux, A.; Job, D. Tubulin tyrosination is a major factor affecting the recruitment of CAP-Gly proteins at microtubule plus ends J. Cell Biol. 2006, 174 (6) 839-849 10.1083/jcb.200512058
6. Regnard, C.; Desbruyeres, E.; Denoulet, P.; Edde, B. Tubulin polyglutamylase: isozymic variants and regulation during the cell cycle in HeLa cells J. Cell Sci. 1999, 112 (Pt 23) 4281-4289
7. Xia, L.; Hai, B.; Gao, Y.; Burnette, D.; Thazhath, R.; Duan, J.; Bre, M. H.; Levilliers, N.; Gorovsky, M. A.; Gaertig, J. Polyglycylation of tubulin is essential and affects cell motility and division in Tetrahymena thermophila J. Cell Biol. 2000, 149 (5) 1097-1106 10.1083/jcb.149.5.1097
8. Reed, N. A.; Cai, D.; Blasius, T. L.; Jih, G. T.; Meyhofer, E.; Gaertig, J.; Verhey, K. J. Microtubule acetylation promotes kinesin-1 binding and transport Curr. Biol. 2006, 16 (21) 2166-2172 10.1016/j.cub.2006.09.014
9. Xiao, H.; El Bissati, K.; Verdier-Pinard, P.; Burd, B.; Zhang, H.; Kim, K.; Fiser, A.; Angeletti, R. H.; Weiss, L. M. Post-translational modifications to Toxoplasma gondii alpha- and beta-tubulins include novel C-terminal methylation J. Proteome Res. 2010, 9 (1) 359-372 10.1021/pr900699a
10. Sahab, Z. J.; Kirilyuk, A.; Zhang, L.; Khamis, Z. I.; Pompach, P.; Sung, Y.; Byers, S. W. Analysis of tubulin alpha-1A/1B C-terminal tail post-translational poly-glutamylation reveals novel modification sites J. Proteome Res. 2012, 11 (3) 1913-1923 10.1021/pr2011044
11. Choudhary, C.; Kumar, C.; Gnad, F.; Nielsen, M. L.; Rehman, M.; Walther, T. C.; Olsen, J. V.; Mann, M. Lysine acetylation targets protein complexes and co-regulates major cellular functions Science 2009, 325 (5942) 834-840 10.1126/science.1175371
12. Sol, E. M.; Wagner, S. A.; Weinert, B. T.; Kumar, A.; Kim, H. S.; Deng, C. X.; Choudhary, C. Proteomic investigations of lysine acetylation identify diverse substrates of mitochondrial deacetylase sirt3 PLoS One 2012, 7 (12) e50545 10.1371/journal.pone.0050545
13. Zhang, L.; Liu, S.; Liu, N.; Zhang, Y.; Liu, M.; Li, D.; Seto, E.; Yao, T. P.; Shui, W.; Zhou, J. Proteomic identification and functional characterization of MYH9, Hsc70, and DNAJA1 as novel substrates of HDAC6 deacetylase activity Protein Cell 2015, 6 (1) 42-54 10.1007/s13238-014-0102-8
14. Daub, H.; Olsen, J. V.; Bairlein, M.; Gnad, F.; Oppermann, F. S.; Korner, R.; Greff, Z.; Keri, G.; Stemmann, O.; Mann, M. Kinase-selective enrichment enables quantitative phosphoproteomics of the kinome across the cell cycle Mol. Cell 2008, 31 (3) 438-448 10.1016/j.molcel.2008.07.007
15. Oppermann, F. S.; Gnad, F.; Olsen, J. V.; Hornberger, R.; Greff, Z.; Keri, G.; Mann, M.; Daub, H. Large-scale proteomics analysis of the human kinome Mol. Cell. Proteomics 2009, 8 (7) 1751-1764 10.1074/mcp.M800588-MCP200
16. Olsen, J. V.; Vermeulen, M.; Santamaria, A.; Kumar, C.; Miller, M. L.; Jensen, L. J.; Gnad, F.; Cox, J.; Jensen, T. S.; Nigg, E. A.; Brunak, S.; Mann, M. Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis Sci. Signaling 2010, 3 (104) ra3 10.1126/scisignal.2000475
17. Peters, J. D.; Furlong, M. T.; Asai, D. J.; Harrison, M. L.; Geahlen, R. L. Syk, activated by cross-linking the B-cell antigen receptor, localizes to the cytosol where it interacts with and phosphorylates alpha-tubulin on tyrosine J. Biol. Chem. 1996, 271 (9) 4755-4762 10.1074/jbc.271.9.4755
18. Laurent, C. E.; Delfino, F. J.; Cheng, H. Y.; Smithgall, T. E. The human c-Fes tyrosine kinase binds tubulin and microtubules through separate domains and promotes microtubule assembly Mol. Cell. Biol. 2004, 24 (21) 9351-9358 10.1128/MCB.24.21.9351-9358.2004
19. Ma, X.; Sayeski, P. P. Identification of tubulin as a substrate of Jak2 tyrosine kinase and its role in Jak2-dependent signaling Biochemistry 2007, 46 (24) 7153-7162 10.1021/bi700101n
20. Wandosell, F.; Serrano, L.; Avila, J. Phosphorylation of alpha-tubulin carboxyl-terminal tyrosine prevents its incorporation into microtubules J. Biol. Chem. 1987, 262 (17) 8268-8273
21. Piperno, G.; LeDizet, M.; Chang, X. J. Microtubules containing acetylated alpha-tubulin in mammalian cells in culture J. Cell Biol. 1987, 104 (2) 289-302
22. Webster, D. R.; Borisy, G. G. Microtubules are acetylated in domains that turn over slowly J. Cell Sci. 1989, 92 (Pt 1) 57-65
23. Chu, C. W.; Hou, F.; Zhang, J.; Phu, L.; Loktev, A. V.; Kirkpatrick, D. S.; Jackson, P. K.; Zhao, Y.; Zou, H. A novel acetylation of beta-tubulin by San modulates microtubule polymerization via down-regulating tubulin incorporation Mol. Biol. Cell 2011, 22 (4) 448-456 10.1091/mbc.E10-03-0203
24. Fourest-Lieuvin, A.; Peris, L.; Gache, V.; Garcia-Saez, I.; Juillan-Binard, C.; Lantez, V.; Job, D. Microtubule regulation in mitosis: tubulin phosphorylation by the cyclin-dependent kinase Cdk1 Mol. Biol. Cell 2006, 17 (3) 1041-1050 10.1091/mbc.E05-07-0621
25. Dompierre, J. P.; Godin, J. D.; Charrin, B. C.; Cordelieres, F. P.; King, S. J.; Humbert, S.; Saudou, F. Histone deacetylase 6 inhibition compensates for the transport deficit in Huntingtons disease by increasing tubulin acetylation J. Neurosci. 2007, 27 (13) 3571-3583 10.1523/JNEUROSCI.0037-07.2007
26. Ikegami, K.; Heier, R. L.; 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. 2007, 104 (9) 3213-3218 10.1073/pnas.0611547104
27. Dunn, S.; Morrison, E. E.; Liverpool, T. B.; Molina-Paris, C.; Cross, R. A.; Alonso, M. C.; Peckham, M. Differential trafficking of Kif5c on tyrosinated and detyrosinated microtubules in live cells J. Cell Sci. 2008, 121 (Pt 7) 1085-1095 10.1242/jcs.026492
28. Xuan, C.; Qiao, W.; Li, J.; Peng, G.; Liu, M.; Chen, Q.; Zhou, J.; Geng, Y. BTat, a trans-acting regulatory protein, contributes to bovine immunodeficiency virus-induced apoptosis Cell. Microbiol. 2008, 10 (1) 31-40 10.1111/j.1462-5822.2007.01011.x
29. Su, Y.; Qiao, W.; Guo, T.; Tan, J.; Li, Z.; Chen, Y.; Li, X.; Li, Y.; Zhou, J.; Chen, Q. Microtubule-dependent retrograde transport of bovine immunodeficiency virus Cell. Microbiol. 2010, 12 (8) 1098-1107 10.1111/j.1462-5822.2010.01453.x
30. Sabo, Y.; Walsh, D.; Barry, D. S.; Tinaztepe, S.; de Los Santos, K.; Goff, S. P.; Gundersen, G. G.; Naghavi, M. H. HIV-1 induces the formation of stable microtubules to enhance early infection Cell Host Microbe 2013, 14 (5) 535-546 10.1016/j.chom.2013.10.012
31. Miller, L. M.; Xiao, H.; Burd, B.; Horwitz, S. B.; Angeletti, R. H.; Verdier-Pinard, P. Methods in tubulin proteomics Methods Cell Biol. 2010, 95, 105-126 10.1016/S0091-679X(10)95007-3
32. Weinert, B. T.; Wagner, S. A.; Horn, H.; Henriksen, P.; Liu, W. R.; Olsen, J. V.; Jensen, L. J.; Choudhary, C. Proteome-wide mapping of the Drosophila acetylome demonstrates a high degree of conservation of lysine acetylation Sci. Signaling 2011, 4 (183) ra48 10.1126/scisignal.2001902
33. Lundby, A.; Lage, K.; Weinert, B. T.; Bekker-Jensen, D. B.; Secher, A.; Skovgaard, T.; Kelstrup, C. D.; Dmytriyev, A.; Choudhary, C.; Lundby, C.; Olsen, J. V. Proteomic analysis of lysine acetylation sites in rat tissues reveals organ specificity and subcellular patterns Cell Rep. 2012, 2 (2) 419-431 10.1016/j.celrep.2012.07.006
34. Casale, C. H.; Alonso, A. D.; Barra, H. S. Brain plasma membrane Na+,K+-ATPase is inhibited by acetylated tubulin Mol. Cell. Biochem. 2001, 216 (1-2) 85-92
35. Friedman, J. R.; Webster, B. M.; Mastronarde, D. N.; Verhey, K. J.; Voeltz, G. K. ER sliding dynamics and ER-mitochondrial contacts occur on acetylated microtubules J. Cell Biol. 2010, 190 (3) 363-375 10.1083/jcb.200911024
36. Friedman, J. R.; Lackner, L. L.; West, M.; DiBenedetto, J. R.; Nunnari, J.; Voeltz, G. K. ER tubules mark sites of mitochondrial division Science 2011, 334 (6054) 358-362 10.1126/science.1207385
37. LHernault, S. W.; Rosenbaum, J. L. Chlamydomonas alpha-tubulin is posttranslationally modified by acetylation on the epsilon-amino group of a lysine Biochemistry 1985, 24 (2) 473-478 10.1021/bi00323a034
38. Edde, B.; Rossier, J.; Le Caer, J. P.; Berwald-Netter, Y.; Koulakoff, A.; Gros, F.; Denoulet, P. A combination of posttranslational modifications is responsible for the production of neuronal alpha-tubulin heterogeneity J. Cell. Biochem. 1991, 46 (2) 134-142 10.1002/jcb.240460207
39. LeDizet, M.; Piperno, G. Identification of an acetylation site of Chlamydomonas alpha-tubulin Proc. Natl. Acad. Sci. U. S. A. 1987, 84 (16) 5720-5724 10.1073/pnas.84.16.5720
40. Draberova, E.; Viklicky, V.; Draber, P. Exposure of lumenal microtubule sites after mild fixation Eur. J. Cell Biol. 2000, 79 (12) 982-985 10.1078/0171-9335-00129
41. Nogales, E. A structural view of microtubule dynamics Cell. Mol. Life Sci. 1999, 56 (1-2) 133-142 10.1007/s000180050012
42. Waterman-Storer, C. M.; Salmon, E. D. Endoplasmic reticulum membrane tubules are distributed by microtubules in living cells using three distinct mechanisms Curr. Biol. 1998, 8 (14) 798-806 10.1016/S0960-9822(98)70321-5
43. Cambray-Deakin, M. A.; Robson, S. J.; Burgoyne, R. D. Colocalisation of acetylated microtubules, glial filaments, and mitochondria in astrocytes in vitro Cell Motil. Cytoskeleton 1988, 10 (3) 438-449 10.1002/cm.970100311
44. Sodeik, B.; Ebersold, M. W.; Helenius, A. Microtubule-mediated transport of incoming herpes simplex virus 1 capsids to the nucleus J. Cell Biol. 1997, 136 (5) 1007-1021 10.1083/jcb.136.5.1007
45. Greber, U. F.; Willetts, M.; Webster, P.; Helenius, A. Stepwise dismantling of adenovirus 2 during entry into cells Cell 1993, 75 (3) 477-486 10.1016/0092-8674(93)90382-Z
46. Liu, C.; Liu, M.; Zhou, J. Analysis of microtubule-mediated intracellular viral transport Methods Mol. Med. 2007, 137, 175-180
47. Leopold, P. L.; Kreitzer, G.; Miyazawa, N.; Rempel, S.; Pfister, K. K.; Rodriguez-Boulan, E.; Crystal, R. G. Dynein- and microtubule-mediated translocation of adenovirus serotype 5 occurs after endosomal lysis Hum. Gene Ther. 2000, 11 (1) 151-165 10.1089/10430340050016238
48. Alonso, C.; Miskin, J.; Hernaez, B.; Fernandez-Zapatero, P.; Soto, L.; Canto, C.; Rodriguez-Crespo, I.; Dixon, L.; Escribano, J. M. African swine fever virus protein p54 interacts with the microtubular motor complex through direct binding to light-chain dynein J. Virol. 2001, 75 (20) 9819-9827 10.1128/JVI.75.20.9819-9827.2001
49. Shevchenko, A.; Tomas, H.; Havlis, J.; Olsen, J. V.; Mann, M. In-gel digestion for mass spectrometric characterization of proteins and proteomes Nat. Protoc. 2006, 1 (6) 2856-2860 10.1038/nprot.2006.468
50. Hummel, M.; Cordewener, J. H.; de Groot, J. C.; Smeekens, S.; America, A. H.; Hanson, J. Dynamic protein composition of Arabidopsis thaliana cytosolic ribosomes in response to sucrose feeding as revealed by label free MSE proteomics Proteomics 2012, 12 (7) 1024-1038 10.1002/pmic.201100413
51. Nogales, E.; Wolf, S. G.; Downing, K. H. Structure of the alpha beta tubulin dimer by electron crystallography Nature 1998, 391 (6663) 199-203 10.1038/34465