Tubulin tyrosine nitration regulates microtubule organization in plant cells

Frontiers in Plant Science

Volumn 4, Issue DEC, 2013, Pages

  Blume, Yaroslav B ^a   Krasylenko, Yuliya A ^a   Demchuk, Oleh M ^a   Yemets, Alla I ^a  

^a INSTITUTE OF FOOD BIOTECHNOLOGY AND GENOMICS   (Ukraine)

Author keywords

3 nitrotyrosine; Arabidopsis; Detyrosination tyrosination cycle; Kinesin 8; Microtubules; Nitric oxide signaling; Tyrosine nitration; tubulin

Indexed keywords

EID: 84900865844     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00530     Document Type: Article

References (81)

1. Abello, N., Kerstjens, H. A., Postma, D. S., and Bischoff, R. (2009). Protein tyrosine nitration: selectivity, physicochemical and biological consequences, denitration, and proteomics methods for the identification of tyrosine-nitrated proteins. J. ProteomeRes. 8, 3222-3238. doi: 10.1021/pr900039c
2. Arnold, K., Bordoli, L., Kopp, J., and Schwede, T. (2006). The SWISS-MODEL Workspace: a web-based environment for protein structure homology modeling. Bioinformatics 22, 195-201. doi: 10.1093/bioinformatics/ bti770
3. Aslan, M., Ryan, T. M., Townes, T. M., Coward, L., Kirk, M. C., Barnes, S., et al. (2003). Nitric-oxide dependent generation of reactive species in sickle cell disease. Actin tyrosine nitration induces defective cytoskeletal polymerization. J. Biol. Chem. 278, 4194-4204. doi: 10.1074/jbc.M208916200.
4. Aulak, K. S., Koeck, T., Crabb, J. W., and Stuehr, D. J. (2001). Proteomic method for identification of tyrosine-nitrated proteins. Proc. Natl. Acad. Sci. U.S.A. 98, 12056-12061. doi: 10.1073/pnas.221269198.
5. Aulak, K. S., Koeck, T., Crabb, J. W., and Stuehr, D. J. (2004). Dynamics of protein nitration in cells and mitochondria. Am. J. Physiol. 286, 30-38. doi: 10.1152/ajpheart.00743.2003.
6. Bai, S., Li, M., Yao, T., Wang, H., Zhang, Y., Xiao, L., et al. (2012). Nitric oxide restrain root growth by DNA damage induced cell cycle arrest in Arabidopsis thaliana. Nitric Oxide 26, 54-60. doi: 10.1016/j.niox.2011.12.001.
7. Baluska, F., and Mancuso, S. (2013). Root apex transition zone as oscillatory zone. Front. PlantSci. 4:354. doi: 10.3389/fpls.2013.00354.
8. Banan, A., Fields, J. Z., Deckern, H., Zhang, Y., and Keshavarzian, A. (2000). Nitric oxide and its metabolites mediate ethanol-induced microtubule disruption and intestinal barrier dysfunction. J. Pharmacol. Exp. Ther. 294, 997-1008.
9. Baudouin, E. (2011). The language of nitric oxide signalling. Plant Biol. 13, 233-242. doi: 10.1111/j.1438-8677.2010.00403.x
10. Begara-Morales, J., Chaki, M., Sânchez-Calvo, B., Mata-Pérez, C., Leterrier, M., Palma, J. M., et al. (2013). Protein tyrosine nitration in pea roots during development and senescence. J. Exp. Bot. 64, 1121-1134. doi: 10.1093/jxb/ ert006
11. Besson-Bard, A., Pugin, A., and Wendehenne, D. (2008). New insights into nitric oxide signalling in plants. Annu. Rev. Plant Biol. 59, 21-39. doi: 10.1146/annurev.arplant.59.032607.092830.
12. Bibikova, T. N., Blancaflor, E. B., and Gilroy S. (1999). Microtubules regulate tip growth and orientation in root hairs of Arabidopsis thaliana L. Plant J. 17, 657-665. doi: 10.1046/j.1365-313X.1999.00415.x
13. Bisig, C. G., Purro, S. A., Conti n, M. A., Barra, H. S., and Arce, C. A. (2002). Incorporation of 3-nitrotyrosine into the C-terminus of a-tubulin is reversible and not detrimental to dividing cells. Eur. J. Biochem. 269, 5037-5045. doi: 10.1046/j.1432-1033.2002.03220.x
14. Blume, Y., Yemets, A., Sulimenko, V., Sulimenko, T., Chan, J., Lloyd, C., et al. (2008). Tyrosine phosphorylation of plant tubulin. Planta 229, 143-150. doi: 10.1007/s00425-008-0816-z
15. Blume, Y. B., Krasylenko, Y. A., and Yemets, A. I. (2009). Tyrosine nitration as regulatory protein post-translational modification. Ukr. Biochem. J. 81, 5-15.
16. Blume, Y. B., Nyporko, A., and Demchuk, O. (2005). Nitrotyrosination of plant a-tubulin: potential mechanisms of influence on cellular processes. BMC Plant Biol. 5:26. doi: 10.1186/1471-2229-5-S1-S26.
17. Blume, Y. B., Yemets, A. I., Sheremet, Y., Nyporko, A., Sulimenko, V., Sulimenko, T., et al. (2010). Exposure of beta-tubulin regions defined by antibodies on an Arabidopsis thaliana microtubule protofilament model and in the cells. BMC PlantBiol. 10:29. doi: 10.1186/1471-2229-10-29.
18. Capeletti, G., Maggioni, M. G., Ronchi, C., Maci, R., and Tedeschi, G. (2006). Protein tyrosine nitration is associated with cold- and drug-resistant microtubules in neuronal-like PC12 cells. Neurosci. Lett. 401, 159-164. doi: 10.1016/j.neulet.2006.03.009.
19. Cappelletti, G., Tedeschi, G., Maggioni, M. G., Negri, A., Nonnis, S., and Maci, R. (2004). The nitration of tau protein in neuron-like PC12 cells. FEBS Lett. 562, 35-39. doi: 10.1016/S0014-5793(04)00173-5.
20. Chaki, M., Valderrama, R., Fernândez-Ocana, M. F., Carreras, A., Lopez-Jaramillo, J., Luque, F., et al. (2009). Protein targets of tyrosine nitration in sunflower (Helianthus annuus L.) hypocotyls. J. Exp. Bot. 60, 422-424. doi: 10.1093/jxb/erp263
21. Chang, W., Webster, D. R., Salam, A. A., Gruber, D., Prasad, A., Eiserich, J. P., et al. (2002). Alteration of the C-terminal amino acid of tubulin specifically inhibits myogenic differentiation. J. Biol. Chem. 277, 30690-30698. doi: 10.1074/jbc.M204930200.
22. Chen, V. B., Arendall, III W. B., Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., et al. (2010). MolProbity: all-atom structure validation for macro-molecular crystallography. Acta Crystallogr. DBiol. Crystallogr. D66, 12-21. doi: 10.1107/S0907444909042073.
23. Clarke, A., Desikan, R., Hurst, R. D., Hancock, J. T., and Neill, S. J. (2000). NO way back: nitric oxide and programmed cell death in Arabidopsis thaliana suspension cultures. PlantJ. 24, 667-677. doi: 10.1046/j.1365-313x.2000.00911.x
24. Corpas, F. J., Chaki, M., Fernândez-Ocana, A., Valderrama, R., Palma, J. M., Carreras, A., et al. (2008). Metabolism of reactive nitrogen species in pea plants under abiotic stress conditions. Plant Cell Physiol. 49, 1711-1722. doi: 10.1093/pcp/pcn144
25. Corpas, F. J., Palma, J. M., del Rio, L. A., and Barroso, J. B. (2013). Protein tyrosine nitration in higher plants grown under natural and stress conditions. Front. PlantSci. 4:29. doi: 10.3389/fpls.2013.00029.
26. Deeb, R. S., Nuriel, T., Cheung, C., Summers, B., Lamon, B. D., Gross, S. S., et al. (2013). Characterization of a cellular denitrase activity that reverses nitration of cyclooxygenase. Am. J. Physiol. Heart Circ. Physiol. 305, H687-H698. doi: 10.1152/ajpheart.00876.2012.
27. Eiserich, J. P., Estévez, A. G., Bamberg, T. V., Ye, Y. Z., Chumley, P. H., Beckman, J. S., et al. (1999). Microtubule dysfunction by posttranslational nitroty-rosination of alpha-tubulin: a nitric oxide-dependent mechanism of cellular injury. Proc. Natl. Acad. Sci. U.S.A. 96, 6365-6370. doi: 10.1073/pnas. 96.11.6365
28. Essmann, U., Perera, L., Berkowitz, M. L., Darden, T., Lee, H., and Pedersen, L. G. (1995). A smooth particle-meshEwald potential. J. Chem. Phys. 103, 8577-8592. doi: 10.1063/1.470117.
29. Fernândez-Marcos, M., Sanza, L., Lewis, D. R., Muday, G. K., and Lorenzo, O. K. (2011). Nitric oxide causes root apical meristem defects and growth inhibition while reducing PIN-FORMED 1 (PIN1)-dependent acropetal auxin transport. Proc. Natl. Acad. Sci. U.S.A. 108, 18506-18511. doi: 10.1073/pnas.1108644108.
30. Gardiner, J., and Marc, J. (2003). Putative microtubule-associated proteins from the Arabidopsis genome. Protoplasma 222, 61-74. doi: 10.1007/s00709-003-0009-3.
31. Gfeller, D., Michielin, O., and Zoete, V. (2013). SwissSidechain: a molecular and structural database of non-natural sidechains. Nucleic Acids Res. 41, D327-D332. doi: 10.1093/nar/gks991.
32. Giannopoulou, E., Katsoris, P., Polytarchou, C., and Papadimitriou, E. (2002). Nitration of cytoskeletal proteins in the chicken embryo chorioallantoic membrane. Arch. Biochem. Biophys. 400, 188-198. doi: 10.1016/S0003-9861(02)00023-1
33. Granger, C. L., and Cyr, R. J. (2001). Spatiotemporal relationships between growth and microtubule orientation as revealed in living root cells of Arabidopsis thaliana transformedwith green-fluorescent-protein gene construct GFP-MBD. Protoplasma 216, 201-214. doi: 10.1007/BF02673872.
34. Greenacre, S. A., and Ischiropoulos, H. (2001). Tyrosine nitration: localisation, quantification, consequences for protein function and signal transduction. Free RadicRes. 34, 541-581. doi: 10.1080/10715760100300471.
35. Hess, B., Bekker, H., Berendsen, H. J. C., and Fraaije, J. G. E. M. (1997). LINCS: a linear constraint solver for molecular simulations. J. Comput. Phys. 18, 1463-1472.
36. Hess, B., Kutzner, C., van der Spoel, D., and Lindahl, E. (2008). GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. J. Chem. Theory Comput. 4, 435-447. doi: 10.1021/ct700301q
37. Jovanovic, A. M., Durst, S., and Nick, P. (2010). Plant cell division is specifically affected bynitrotyrosine. J. Exp. Bot. 61, 901-909. doi: 10.1093/jxb/erp369.
38. Kalisz, H. M., Erck, C., Plessmann, U., and Wehland, J. (2000). Incorporation of nitrotyrosine into alpha-tubulin by recombinant mammalian tubulin-tyrosine ligase. Biochim. Biophys. Acta 1481, 131-138. doi: 10.1016/S0167-4838(00)00110-2
39. Kasprowicz, A., Szuba, A., Volkmann, D., Baluska, F., and Wojtaszek, P. (2009). Nitric oxide modulates dynamic actin cytoskeleton and vesicle trafficking in a cell type-specific manner in root apices. J. Exp. Bot. 60, 1605-1617. doi: 10.1093/jxb/erp033
40. Koeck, T., Fu, X., Hazen, S. L., Crabb, J. W., Stuehr, D. J., and Aulak, K. S. (2004). Rapid and selective oxygen-regulated protein tyrosine denitration and nitration in mitochondria. J. Biol. Chem. 279, 27257-27262. doi: 10.1074/jbc.M401586200.
41. Kikkawa, M., Sablin, E. P., Okada, Y., Yajima, H., Fletterick, R. J., and Hirokawa, N. (2001). Switch-based mechanism of kinesin motors. Nature 411, 439-445. doi: 10.1038/35078000
42. Landino, L. M., Koumas, M. T., Mason, C. E., and Alston, J. A. (2007). Modification of tubulin cysteines by nitric oxide and nitroxyl donors alters tubulin polymerization activity. Chem. Res. Toxicol. 20, 1693-1700. doi: 10.1021/ tx7001492
43. Leon, L., Jeannin, J. F., and Bettaieb, A. (2008). Post-translational modification inducedbynitric oxide. Nitric Oxide 19, 77-83. doi: 10.1016/j.niox.2008.04.014.
44. Lindermayr, C., Saalbach, G., and Durner, J. (2005). Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiol. 137, 921-930. doi: 10.1104/pp.104.058719.
45. Livanos, P., Apostolakos, P., and Galatis, B. (2012). Plant cell division: ROS homeostasis is required. Plant Signal Behav. 7, 771-778. doi: 10.4161/psb.20530.
46. Lozano-Juste, J., Colom-Moreno, R., and Leon, J. (2011). In vivo protein tyrosine nitration in Arabidopsis thaliana. J. Exp. Bot. 62, 3501-3517. doi: 10.1093/jxb/err042
47. Mathur, J., and Chua, N. H. (2001). Microtubule stabilization leads to growthreori-entationin Arabidopsistrichomes. PlantCell. 12,465-477. doi: 10.2307/3871062.
48. Monteiro, H. P., Arai, R. A., and Travassos, L. R. (2008). Protein tyrosine phosphorylation and protein tyrosine nitration in redox signalling. Antioxid. Redox. Signal. 10, 843-889. doi: 10.1089/ars.2007.1853.
49. Murashige, T. A., and Skoog, F. (1962). A revisied medium for rapid growth and bioassays with tobacco tissue culture. Physiol. Plant. 15, 473-497. doi: 10.1111/j.1399-3054.1962.tb08052.x
50. Nagata, T., Nemoto, T., and Hasezawa, S. (1992). Tobacco BY-2 cell line as the "HeLa" cell in the cell biology of higher plants. Int. Rev. Cytol. 132, 1-30. doi: 10.1016/S0074-7696(08)62452-3.
51. Neill, S. J., Bright, J., Desikan, R., Hancock, J., Harrison, J., and Wilson, I. (2008). Nitric oxide evolution and perception. J. Exp. Bot. 59, 25-35. doi: 10.1093/jxb/erm218
52. Otvos, K., Pasternak, T. P., Dudits, D., andFehér, A. (2005). Nitric oxide, asignalling molecule in plant cell reactivation. BMC Plant Biol. 5:S27. doi: 10.1186/1471-2229-5-S1-S27
53. Palumbo, A., Fiore, G., Di Cristo, C., Di Cosmo, A., and d'Ischia, M. (2002). NMDA receptor stimulation induces temporary alpha-tubulin degradation signaled by nitric oxide-mediated tyrosine nitration in the nervous system of Sepia officinalis. Biochem. Biophys. Res. Commun. 293, 1536-1543. doi: 10.1016/S0006-291X(02)00392-3.
54. Parrotta, L., Cresti, M., and Cai, G. (2013). Accumulation and post-translational modifications ofplanttubulins. Plant Biol. doi: 10.1111/plb.12104. [Epub ahead of print].
55. Peluffo, H., Shacka, J. J., Ricart, K., Bisig, C. G., Martinez-Palma, L., Pritsch, O., et al. (2004). Induction of motor neuron apoptosis by free 3-nitro-L-tyrosine. J. Neurochem. 89, 602-612. doi: 10.1046/j.1471-4159.2004.02363.
56. Peris, L., Wagenbach, M., Lafanechère, L., Brocard, J., Moore, A. T., Kozielski F., et al. (2009). Motor-dependent microtubule disassembly driven by tubulin tyrosination. J. CellBiol. 185, 1159-1166. doi: 10.1083/jcb.200902142.
57. Peters, C., Brejc, K., Belmont, L., Bodey, A. J., Lee, Y., Yu, M., et al. (2010). Insight into the molecular mechanism of the multitasking kinesin-8 motor. EMBO J. 29, 3437-3447. doi: 10.1038/emboj.2010.220.
58. Phung, A. D., Soucek, K., Kubala, L., Harpera, R. W., Bulinski, J. C., and Eiserich, J. P. (2006). Posttranslational nitrotyrosination of a-tubulin induces cell cycle arrest and inhibits proliferation ofvascular smooth muscle cells. Eur. J. CellBiol. 85, 1241-1252. doi: 10.1016/j.ejcb.2006.05.016.
59. Pronk, S., Pâll, S., Schulz, R., Larsson, P., Bjelkmar, P., Apostolov, R., et al. (2013). GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics 29, 845-854. doi: 10.1093/bioin-formatics/btt055
60. Prota, A. E., Magiera, M. M., Kuijpers, M., Bargsten, K., Frey, D., Wieser, M., et al. (2013). Structural basis of tubulin tyrosination by tubulin tyrosine ligase. J. Cell Biol. 200, 259-270. doi: 10.1083/jcb.201211017.
61. Roostalu, J., and Surrey, T. (2013). The multiple talents of kinesin-8. Nat. Cell Biol. 15, 889-891. doi: 10.1038/ncb2820.
62. Rounds, C. M., andBezanilla, M. (2013). Growth mechanisms in tip-growingplant cells. Annu. Rev. PlantBiol. 64, 243-265. doi: 10.1146/annurev-arplant-050312-120150
63. Sheremet, Y.A., Yemets, A. I., and Blume, Y. B. (2012). Inhibitors oftyrosine kinases and phosphatases as a tool for the investigation of microtubule role in plant cold response. Tsitol Genet. 46, 3-9. doi: 10.3103/S0095452712010112.
64. Shi, F. M., Yao, L. L., Pei, B. L., Zhou, Q., Li, X. L., Li, Y., et al. (2009). Cortical microtubule as a sensor and target of nitric oxide signal during the defence responses to Verticillium dahliae toxins in Arabidopsis. PlantCellEnviron. 32, 428-438. doi: 10.1111/j.1365-3040.2009.01939.x
65. Smertenko, A., Blume, Y. B., Viklick, V., and Drâber, P. (1997). Posttranslational modifications and multiple isoforms of tubulin in Nicotiana tabacum L. cells. Planta 201, 349-358. doi: 10.1007/s004250050077.
66. Su, X., Arellano-Santoyo, H., Portran, D., Gaillard, J., Vantard, M., Thery, M., et al. (2013). Microtubule-sliding activity of a kinesin-8 promotes spindle assembly andspindle-lengthcontrol. Nat. CellBiol. 15, 948-958. doi: 10.1038/ncb2801.
67. Szechynska-Hebda, M., Wedzony, M., and Dubas, E. (2005). Visualisation of microtubules and actin filaments in fixed BY-2 suspension cells using an optimised whole mount immunolabelling protocol. PlantCellRep. 25, 758-766. doi: 10.1007/s00299-005-0089-y
68. Takahashi, H., Kawahara, A., and Inoe, Y. (2003). Ethylene promotes the induction by auxin of the corticsl microtubules rendomisation required for low-Ph-induced root hair initiation in lettuce (Lactuca sativa L.) seedlings. Plant Cell Physiol. 44, 932-940. doi: 10.1093/pcp/pcg119.
69. Tanou, G., Filippou, P., Belghazi, M., Job, J., Diamantidis, G., Fotopoulos, V., et al. (2012). Oxidative and nitrosative-based signalling and associated post-translational modifications orchestrate the acclimation of citrus plants to salinitystress. PlantJ. 72,585-599. doi: 10.1111/j.1365-313X.2012.05100.x
70. Tedeschi, G., Cappelletti, G., Negri, A., Pagliato, L., Maggioni, M. G., Maci, R., et al. (2005). Characterisation of nitroproteome in neuron-like PC12 cells differentiated with nerve growth factor: identification of two nitration sites in alpha-tubulin. Proteomics 5, 2422-2432. doi: 10.1002/pmic.200401208.
71. Van Bruaene, N., Joss, G., and Oostveldt, P. V. (2004). Reorganization and in vivo dynamics of microtubules during Arabidopsis root hair development. Plant Physiol. 136, 3905-3919. doi: 10.1104/pp.103.031591.
72. Vassileva, V. N., Kouchi, H., and Ridge, R. W. (2005). Microtubule dynamics in living root hairs: transient slowing by lipochitin oligosaccharide nodulation signals. PlantCell 17, 1777-1787. doi: 10.1105/tpc.105.031641.
73. Westermann, S., and Weber, K. (2003). Post-translational modifications regulate microtubule function. Nat. Rev. Mol. Cell Biol. 4, 938-947. doi: 10.1038/nrm1260
74. Wiever, L. N., and Walczak, C. E. (2011). Kinesin-8s hang on by a tail.Bioarchitecture 1, 236-239. doi: 10.4161/bioa.18427.
75. Wilson, I. D., Neill, S. J., and Hancock, J. T. (2008). Nitric oxide synthesis and signalling in plants. Plant Cell Environ. 31, 622-631. doi: 10.1111/j.1365-3040.2007.01761.x
76. Yadav, S., David, A., Baluska, F., and Bhatla, S. (2013). Rapid auxin-induced nitric oxide accumulation and subsequent tyrosine nitration of protein during adventitious root formation in sunflower hypocotyls. Plant Signal. Behav. 8:e23196. doi: 10.4161/psb.23196.
77. Yemets, A. I., Krasylenko, Y. A., Lytvyn, D. I., Sheremet, Y. A., and Blume, Y. B. (2011). Nitric oxide signalling via cytoskeleton in plants. Plant Sci. 181, 545-554. doi: 10.1016/j.plantsci.2011.04.017.
78. Yemets, A. I., Krasylenko, Y. A., Sheremet, Y. A., and Blume, Y. B. (2009). Microtubule reorganization as a response to implementation of NO signals in plant cells. Cytol. Genet. 43, 73-79. doi: 10.3103/S009545270 9020017
79. Yemets, A., Sheremet, Y., Vissenberg, K., Van Orden, J., Verbelen, J.-P., and Blume, Y. B. (2008). Effects of tyrosine kinase and phosphatase inhibitors on microtubules in Arabidopsis root cells. Cell Biol. Int. 32, 630-637. doi: 10.1016/j.cellbi.2008.01.013.
80. Zachgo, S., Hanke, G. T., and Scheibe, R. (2013). Plant cell microcompartments: a redox-signaling perspective. Biol. Chem. 394, 203-216. doi: 10.1515/hsz-2012-0284
81. Zhang, Y. M., Wu, Z. Y., Wang, X. C., and Yu, R. (2008). Rearrangements of microtubule cytoskeleton in stomatal closure of Arabidopsis induced by nitric oxide. Chin. Sci. Bull. 53, 848-852. doi: 10.1007/s11434-008-0142-7