Advertisement

Planta

, 229:143 | Cite as

Tyrosine phosphorylation of plant tubulin

  • Yaroslav BlumeEmail author
  • Alla Yemets
  • Vadym Sulimenko
  • Tetyana Sulimenko
  • Jordi Chan
  • Clive Lloyd
  • Pavel Dráber
Original Article

Abstract

Phosphorylation of αβ-tubulins dimers by protein tyrosine kinases plays an important role in the regulation of cellular growth and differentiation in animal cells. In plants, however, the role of tubulin tyrosine phosphorylation is unknown and data on this tubulin modification are limited. In this study, we used an immunochemical approach to demonstrate that tubulin isolated by both immunoprecipitation and DEAE-chromatography is phosphorylated on tyrosine residues in cultured cells of Nicotiana tabacum. This opens up the possibility that tyrosine phosphorylation of tubulin could be involved in modulating the properties of plant microtubules.

Keywords

Plant microtubules Post-translational modifications Phosphorylation Tubulin Tyrosine residues 

Notes

Acknowledgments

The work was funded partially by NATO LST.CLG 979212 for Alla Yemets and Clive Lloyd, and by INTAS Grant 03-51-6459 for Alla Yemets, Yaroslav Blume, Pavel Dráber and Vadym Sulimenko. The work of Tetyana Sulimenko, Vadym Sulimenko and Pavel Dráber was also supported from project LC545 (Ministry of Education, Youth and Sport of Czech Republic) Grant No. 204/05/2375 from GACR and by Institutional Research support AVOZ 50520514. Alla Yemets was supported from INTAS Experienced Postdoctoral Fellowship for Young Scientists YSF 00-184. Clive Lloyd and Jordi Chan were funded by the BBSRC.

References

  1. Akiyama T, Kadowaki T, Nishida E, Kadooka T, Ogawara H, Fukami Y, Sakai H, Takaku F, Kasuga M (1986) Substrate specificities of tyrosine-specific protein kinases toward cytoskeletal proteins in vitro. J Biol Chem 261:14797–14803PubMedGoogle Scholar
  2. Ali N, Halfter U, Chua N-H (1994) Cloning and biochemical characterization of a plant protein kinase that phosphorylates serine, threonine, and tyrosine. J Biol Chem 269:31626–31629PubMedGoogle Scholar
  3. Barizza E, Schiavo FL, Terzi M, Filippini F (1999) Evidence suggesting protein tyrosine phosphorylation in plants depends on the developmental conditions. FEBS Lett 447:191–194PubMedCrossRefGoogle Scholar
  4. Barroso C, Chan J, Allan V, Doonan J, Hussey P, Lloyd C (2000) Two kinesin-related proteins associated with the cold-stable cytoskeleton of carrot cells: characterization of a novel kinesin, DcKRP120-2. Plant J 24:859–868PubMedCrossRefGoogle Scholar
  5. Blume YB, Smertenko A, Ostapets NN, Viklický V, Dráber P (1997) Post-translational modifications of plant tubulin. Cell Biol Int 21:918–920Google Scholar
  6. Breviario D (2000) Tubulin genes and promotors. In: Nick P (ed) Plant microtubules. Springer, Berlin, pp 137–157Google Scholar
  7. De la Fuente van Bentem S, Anrather D, Dohnal I, Roitinger E, Csaszar E, Joore J, Buijnink J, Carreri A, Forzani C, Lorkovic ZJ, Barta A, Lecourieux D, Verhouning A, Jonak C, Hirt H (2008) Site-specific phosphorylation profiling of Arabidopsis proteins by mass spectrometry and peptide chip analysis. J Proteome Res 7:2458–2470PubMedCrossRefGoogle Scholar
  8. Dráber P, Lagunowich LA, Dráberová E, Viklický V, Damjanov I (1988) Heterogeneity of tubulin epitopes in mouse fetal tissues. Histochemistry 89:485–492PubMedCrossRefGoogle Scholar
  9. Dráberová E, Dráber P (1993) A microtubule-interacting protein involved in coalignment of vimentin intermediate filaments with microtubules. J Cell Sci 106:1263–1273PubMedGoogle Scholar
  10. Dráberová E, Dráber P (1998) Novel monoclonal antibodies TU-08 and TU-16 specific for tubulin subunits. Folia Biol (Praha) 44:35–36Google Scholar
  11. Dráberová E, Zíková M, Dráber P (1999) Monoclonal antibody VI-10 specific for vimentin. Folia Biol (Praha) 45:35–36Google Scholar
  12. Dryková D, Sulimenko V, Cenklová V, Volc J, Dráber P, Binarová P (2003) Plant γ-tubulin interacts with αβ-tubulin dimers and forms membrane-associated complexes. Plant Cell 15:465–480PubMedCrossRefGoogle Scholar
  13. Duckett CM, Lloyd CW (1994) Gibberellic acid-induced microtubule reorientation in drawf peas is accompanied by rapid modification of an α-tubulin isotypes. Plant J 5:363–372CrossRefGoogle Scholar
  14. Fordham-Skelton AP, Skipsey M, Evans IM, Edwards R, Gatehouse JA (1999) Higher plant tyrosine-specific protein phosphatases (PTPs) contain novel amino-terminal domains: expression during embryogenesis. Plant Mol Biol 39:593–605PubMedCrossRefGoogle Scholar
  15. Gilmer S, Clay P, MacRae TH, Fowke LC (1999a) Acetylated tubulin is found in all microtubule arrays of two species of pine. Protoplasma 207:174–185CrossRefGoogle Scholar
  16. Gilmer S, Clay P, MacRae TH, Fowke LC (1999b) Tyrosinated, but not detyrosinated, α-tubulin is present in root tip cells. Protoplasma 210:92–98CrossRefGoogle Scholar
  17. Görg A, Obermaier C, Boguth G, Weiss W (1999) Recent developments in two-dimensional gel electrophoresis with immobilized pH gradients: wide pH gradients up to pH 12, longer separation distances and simplified procedures. Electrophoresis 20:712–717PubMedCrossRefGoogle Scholar
  18. Guo A, Villén J, Kornhauser J, Lee KA, Stokes MP, Rikova K, Possemato A, Nardone J, Innocenti G, Wetzel R, Wang Y, MacNeill J, Mitchell J, Gygi SP, Rush J, Polakiewicz RD, Comb MJ (2008) Signaling networks assembled by oncogenic EGFR and c-Met. Proc Natl Acad Sci USA 105:692–697PubMedCrossRefGoogle Scholar
  19. Hardie DG (1999) Plant protein serine/threonine kinases: classification and functions. Annu Rev Plant Physiol Plant Mol Biol 50:97–131PubMedCrossRefGoogle Scholar
  20. Heazlewood JL, Durek P, Hummel J, Selbig J, Weckwerth W, Walther D, Schulze WX (2007) PhosPhat: a database of phosphorylation sites in Arabidopsis thaliana and plant-specific phosphorylation site predictor. Nucleic Acids Res 36:D1015–D1021 database issuePubMedCrossRefGoogle Scholar
  21. Heberle-Bors E (2001) Cyclin-dependent protein kinases, mitogen-activated protein kinases and the plant cell cycle. Curr Sci 80:225–232Google Scholar
  22. Hirt H (1997) Multiple roles of MAP kinases in plant signal transduction. Trends Plant Sci 2:11–15CrossRefGoogle Scholar
  23. Hirt H (2000) Connecting oxidative stress, auxin, and cell cycle regulation through a plant mitogen-activated protein kinase pathway. Proc Natl Acad Sci USA 97:2405–2407PubMedCrossRefGoogle Scholar
  24. Huang RF, Lloyd CW (1999) Gibberellic acid stabilizes microtubules in maize suspension cells to cold and stimulates acetylation of α-tubulin. FEBS Lett 443:317–320PubMedCrossRefGoogle Scholar
  25. Ingram GC, Waites R (2006) Keeping it together: co-ordinating plant growth. Curr Opin Plant Biol 9:12–20PubMedCrossRefGoogle Scholar
  26. Ishibashi K, Fujioka T, Ui M (1999) Decreases in cAMP phosphodiesterase activity in hepatocytes cultured with herbimycin A due to cellular microtubule polymerization related to inhibition of tyrosine phosphorylation of α-tubulin. Eur J Biochem 260:398–408PubMedCrossRefGoogle Scholar
  27. Kadowaki T, Fujita-Yamaguchi Y, Nishida E, Takaku F, Akiyama T, Kathuria S, Akanuma Y, Kasuga M (1985) Phosphorylation of tubulin and microtubule-associated proteins by the purified insulin receptor kinase. J Biol Chem 260:4016–4020PubMedGoogle Scholar
  28. Kameyama K, Kishi Y, Yoshimura M, Kanzawa N, Sameshima M, Tsuchiya T (2000) Tyrosine phosphorylation in plant bending. Nature 407:37PubMedCrossRefGoogle Scholar
  29. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685PubMedCrossRefGoogle Scholar
  30. Ley SC, Verbi W, Pappin DJ, Druker B, Davies AA, Crumpton MJ (1994) Tyrosine phosphorylation of alpha tubulin in human T lymphocytes. Eur J Immunol 24:99–106PubMedCrossRefGoogle Scholar
  31. Linhartová I, Dráber P, Dráberová E, Viklický V (1992) Immunological discrimination of β-tubulin isoforms in developing mouse brain. Biochem J 288:919–924PubMedGoogle Scholar
  32. Luan S (2002) Tyrosine phosphorylation in plant cell signaling. Proc Nat Acad Sci USA 99:11567–11569PubMedCrossRefGoogle Scholar
  33. Lukáš Z, Dráber P, Buček J, Dráberová E, Viklický V, Doležel S (1993) Expression of phosphorylated high molecular weight neurofilament protein (NF-H) and vimentin in human developing dorsal root ganglia and spinal cord. Histochemistry 100:495–502PubMedCrossRefGoogle Scholar
  34. Maness PF, Matten WT (1990) Tyrosine phosphorylation of membrane-associated tubulin in nerve growth cones enriched in pp60c-src. Ciba Found Symp 150:57–69PubMedGoogle Scholar
  35. Matten WT, Aubry M, West J, Maness PF (1990) Tubulin is phosphorylated at tyrosine by pp60c-src in nerve growth cone membranes. J Cell Biol 111:1959–1970PubMedCrossRefGoogle Scholar
  36. Morejohn LC, Bureau TE, Tocchi LP, Fosket DE (1984) Tubulins from different higher-plant species are immunologically nonidentical and bind colchicine differentially. Proc Natl Acad Sci USA 81:1440–1444PubMedCrossRefGoogle Scholar
  37. Nühse TS, Bottrill AR, Jones AME, Peck SC (2007) Quantitative phosphoproteomic analysis of plasma membrane proteins reveals regulatory mechanisms of plant innate immune responses. Plant J 51:931–940PubMedCrossRefGoogle Scholar
  38. Opatrný Z, Opatrná J (1976) The specificity of the effect of 2, 4-D and NAA on the growth, micromorphology, and occurence of starch in long-term Nicotiana tabacum L. cell strains. Biol Plant (Praha) 18:359–365Google Scholar
  39. Peters JD, Furlong MT, Asai DJ, Harrison ML, Geahlen RL (1996) 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 271:4755–4762PubMedCrossRefGoogle Scholar
  40. Reddy MM, Rajasekharan R (2007) Serine/threonine/tyrosine protein kinase from Arabidopsis thaliana is dependent on serine residues for its activity. Arch Biochem Biophys 460:122–128PubMedCrossRefGoogle Scholar
  41. Rudrabhatla P, Reddy MM, Rajasekharan R (2006) Genome-wide analysis and experimentation of plant serine/threonine/tyrosine-specific protein kinases. Plant Mol Biol 60:293–319PubMedCrossRefGoogle Scholar
  42. Shimotohno A, Ohno R, Bisova K, Sakaguchi N, Huang J, Koncz C, Hirofumi U, Umeda M (2006) Diverse phosphoregulatory mechanisms controlling cyclin-dependent kinase-activating kinases in Arabidopsis. Plant J 47:701–710PubMedCrossRefGoogle Scholar
  43. Smertenko A, Blume YB, Viklický V, Opatrný Z, Dráber P (1997) Posttranslational modifications and multiple isoforms of tubulin in Nicotiana tabacum cells. Planta 201:349–358PubMedCrossRefGoogle Scholar
  44. Sugiyama N, Nakagami H, Mochida K, Daudi A, Tomita M, Shirasu K, Ishihama Y (2008) Large-scale phosphorylation mapping reveals the extent of tyrosine phosphorylation in Arabidopsis. Mol Syst Biol 4, article number 193Google Scholar
  45. Torruella M, Casano LM, Vallejos RH (1986) Evidence of the activity of tyrosine kinase(s) and of the presence of phosphotyrosine proteins in pea plantlets. J Biol Chem 261:6651–6653PubMedGoogle Scholar
  46. Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76:4350–4354PubMedCrossRefGoogle Scholar
  47. Trojanek J, Ek P, Scoble J, Muszynska G, Engström L (1996) Phosphorylation of plant proteins and the identification of protein-tyrosine kinase activity in maize seedlings. Eur J Biochem 235:338–344PubMedCrossRefGoogle Scholar
  48. Trojanek JB, Klimecka MM, Fraser A, Dobrowolska G, Muszyńska G (2004) Characterization of dual specificity protein kinase from maize seedlings. Acta Biochim Pol 51:635–647PubMedGoogle Scholar
  49. Viklický V, Dráber P, Hašek J, Bártek J (1982) Production and characterization of a monoclonal antitubulin antibody. Cell Biol Int Rep 6:725–731PubMedCrossRefGoogle Scholar
  50. Walker-Simmons MK (1998) Protein kinases in seeds. Seed Sci Res 8:193–200CrossRefGoogle Scholar
  51. Wandosell F, Serrano L, Avila J (1987) Phosphorylation of alpha-tubulin carboxy-terminal tyrosine prevents its incorporation into microtubules. J Biol Chem 262:8268–8273PubMedGoogle Scholar
  52. Wang W, Vignani R, Scali M, Sensi E, Cresti M (2004) Post-translational modifications of alpha-tubulin in Zea mays L. are highly tissue specific. Planta 218:460–465PubMedCrossRefGoogle Scholar
  53. Westermann S, Weber K (2003) Post-translational modifications regulate microtubule function. Nat Rev Mol Cell Biol 4:938–947PubMedCrossRefGoogle Scholar
  54. Xu Q, Fu HH, Gupta R, Luan S (1998) Molecular characterization of a tyrosine-specific protein phosphatase encoded by a stress-responsive gene in Arabidopsis. Plant Cell 10:849–857PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Yaroslav Blume
    • 1
    Email author
  • Alla Yemets
    • 1
  • Vadym Sulimenko
    • 2
  • Tetyana Sulimenko
    • 2
  • Jordi Chan
    • 3
  • Clive Lloyd
    • 3
  • Pavel Dráber
    • 2
  1. 1.Institute of Cell Biology and Genetic EngineeringNational Academy of Sciences of UkraineKievUkraine
  2. 2.Institute of Molecular GeneticsAcademy of Sciences of the Czech RepublicPrague 4Czech Republic
  3. 3.Department of Cell and Developmental BiologyJohn Innes CentreNorwichUK

Personalised recommendations