Autophosphorylation profiling of Arabidopsis protein kinases using the cell-free system

Phytochemistry

Volumn 72, Issue 10, 2011, Pages 1136-1144

  Nemoto, Keiichirou ^a   Seto, Takuya ^a   Takahashi, Hirotaka ^a,b   Nozawa, Akira ^a   Seki, Motoaki ^c   Shinozaki, Kazuo ^d   Endo, Yaeta ^a,d   Sawasaki, Tatsuya ^a,d  

^a EHIME UNIVERSITY   (Japan)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c Plant Functional Genomics Research Group   (Japan)

^d RIKEN   (Japan)

Author keywords

Arabidopsis cDNA library; Autophosphorylation; Profiling; Protein kinase; Wheat germ cell free protein synthesis system

Indexed keywords

ARABIDOPSIS PROTEIN; PROTEIN KINASE; SERINE; THREONINE;

ARABIDOPSIS; ARTICLE; CELL FREE SYSTEM; ENZYMOLOGY; GENETICS; METABOLISM; PHOSPHORYLATION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL-FREE SYSTEM; PHOSPHORYLATION; PROTEIN KINASES; SERINE; THREONINE;

ARABIDOPSIS; TRITICUM AESTIVUM; UNIDENTIFIED PLANT;

EID: 79958147364     PISSN: 00319422     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.phytochem.2011.02.029     Document Type: Article

References (77)

1. A.J. Afzal, A.J. Wood, and D.A. Lightfoot Plant receptor-like serine threonine kinases: roles in signaling and plant defense Mol. Plant Microbe Interact. 21 2008 507 517 (Pubitemid 351679729)
2. V.S. Anil, A.C. Harmon, and K.S. Rao Spatio-temporal accumulation and activity of calcium-dependent protein kinases during embryogenesis, seed development, and germination in sandalwood Plant Physiol. 122 2000 1035 1043 (Pubitemid 30221383)
3. M. Ashburner, C.A. Ball, J.A. Blake, D. Botstein, H. Butler, J.M. Cherry, A.P. Davis, K. Dolinski, S.S. Dwight, J.T. Eppig, M.A. Harris, D.P. Hill, L. Issel-Tarver, A. Kasarskis, S. Lewis, J.C. Matese, J.E. Richardson, M. Ringwald, G.M. Rubin, and G. Sherlock Gene ontology: tool for the unification of biology. The gene ontology consortium Nat. Genet. 25 2000 25 29 (Pubitemid 30257031)
4. L. Bai, G. Zhang, Y. Zhou, Z. Zhang, W. Wang, Y. Du, Z. Wu, and C.P. Song Plasma membrane-associated proline-rich extensin-like receptor kinase 4, a novel regulator of Ca signalling, is required for abscisic acid responses in Arabidopsis thaliana Plant J. 60 2009 314 327
5. Y. Belkhadir, and J. Chory Brassinosteroid signaling: a paradigm for steroid hormone signaling from the cell surface Science 314 2006 1410 1411 (Pubitemid 44871937)
6. J.J. Benschop, S. Mohammed, M. O'Flaherty, A.J. Heck, M. Slijper, and F.L. Menke Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis Mol. Cell Proteomics 6 2007 1198 1214 (Pubitemid 47099230)
7. T.Z. Berardini, S. Mundodi, L. Reiser, E. Huala, M. Garcia-Hernandez, P. Zhang, L.A. Mueller, J. Yoon, A. Doyle, G. Lander, N. Moseyko, D. Yoo, I. Xu, B. Zoeckler, M. Montoya, N. Miller, D. Weems, and S.Y. Rhee Functional annotation of the Arabidopsis genome using controlled vocabularies Plant Physiol. 135 2004 745 755 (Pubitemid 38819021)
8. M.W. Bianchi, D. Guivarc'h, M. Thomas, J.R. Woodgett, and M. Kreis Arabidopsis homologs of the shaggy and GSK-3 protein kinases: molecular cloning and functional expression in Escherichia coli Mol. Gen. Genet. 242 1994 337 345 (Pubitemid 24061215)
9. B.M. Binder, J.F. Harper, and M.R. Sussman Characterization of an Arabidopsis calmodulin-like domain protein kinase purified from Escherichia coli using an affinity sandwich technique Biochemistry 33 1994 2033 2041 (Pubitemid 24099597)
10. J.R. Botella, J.M. Arteca, M. Somodevilla, and R.N. Arteca Calcium-dependent protein kinase gene expression in response to physical and chemical stimuli in mung bean (Vigna radiata) Plant Mol. Biol. 30 1996 1129 1137 (Pubitemid 26310786)
11. D.S. Bush Calcium regulation in plant cells and its role in signaling Annu. Rev. Plant Physiol. Plant Mol. Biol. 46 1995 95 122
12. S. Chaudhuri, A. Seal, and M.D. Gupta Autophosphorylation-dependent activation of a calcium-dependent protein kinase from groundnut Plant Physiol. 120 1999 859 866 (Pubitemid 29384516)
13. E.W. Chehab, O.R. Patharkar, A.D. Hegeman, T. Taybi, and J.C. Cushman Autophosphorylation and subcellular localization dynamics of a salt- and water deficit-induced calcium-dependent protein kinase from ice plant Plant Physiol. 135 2004 1430 1446 (Pubitemid 39009390)
14. J.M. Chico, M. Raíces, M.T. Téllez-Iñón, and R.M. Ulloa A calcium-dependent protein kinase is systemically induced upon wounding in tomato plants Plant Physiol. 128 2002 256 270 (Pubitemid 34115327)
15. S.E. Clark Cell signalling at the shoot meristem Nat. Rev. Mol. Cell Biol. 2 2001 276 284 (Pubitemid 33676970)
16. D.A. Cross, D.R. Alessi, P. Cohen, M. Andjelkovich, and B.A. Hemmings Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B Nature 378 1995 785 789 (Pubitemid 26004411)
17. Y. Endo, and T. Sawasaki High-throughput, genome-scale protein production method based on the wheat germ cell-free expression system J. Struct. Funct. Genomics 5 2004 45 57 (Pubitemid 39030619)
18. Y. Endo, and T. Sawasaki Cell-free expression systems for eukaryotic protein production Curr. Opin. Biotechnol. 17 2006 373 380 (Pubitemid 44163458)
19. Y.X. Fan, L. Wong, T.B. Deb, and G.R. Johnson Ligand regulates epidermal growth factor receptor kinase specificity: activation increases preference for GAB1 and SHC versus autophosphorylation sites J. Biol. Chem. 279 2004 38143 38150 (Pubitemid 39295960)
20. L. Frylinck, and I.A. Dubery Protein kinase activities in ripening mango Mangifera indica L., fruit tissue. III. Purification and characterisation of a calcium-regulated protein kinase Biochim. Biophys. Acta 1387 1998 342 354 (Pubitemid 28529235)
21. M. Gribskov, F. Fana, J. Harper, D.A. Hope, A.C. Harmon, D.W. Smith, F.E. Tax, and G. Zhang PlantsP: a functional genomics database for plant phosphorylation Nucleic Acids Res. 29 2001 111 113 (Pubitemid 32054420)
22. A.C. Harmon, C. Putnam-Evans, and M.J. Cormier A calcium-dependent but calmodulin-independent protein kinase from soybean Plant Physiol. 83 1987 830 837
23. T.A. Haystead, P. Dent, J. Wu, C.M. Haystead, and T.W. Sturgill Ordered phosphorylation of p42mapk by MAP kinase FEBS Lett. 306 1992 17 22
24. J.X. He, J.M. Gendron, Y. Yang, J. Li, and Z.Y. Wang The GSK3-like kinase BIN2 phosphorylates and destabilizes BZR1, a positive regulator of the brassinosteroid signaling pathway in Arabidopsis Proc. Natl. Acad. Sci. USA 99 2002 10185 10190 (Pubitemid 34831193)
25. A.D. Hegeman, M. Rodriguez, B.W. Han, Y. Uno, G.N. Phillips Jr., E.M. Hrabak, J.C. Cushman, J.F. Harper, A.C. Harmon, and M.R. Sussman A phyloproteomic characterization of in vitro autophosphorylation in calcium-dependent protein kinases Proteomics 6 2006 3649 3664 (Pubitemid 44000192)
26. K. Hematy, and H. Hofte Novel receptor kinases involved in growth regulation Curr. Opin. Plant Biol. 11 2008 321 328
27. M. Huse, and J. Kuriyan The conformational plasticity of protein kinases Cell 109 2002 275 282 (Pubitemid 34606870)
28. Y. Ikeda, N. Koizumi, T. Kusano, and H. Sano Specific binding of a 14-3-3 protein to autophosphorylated WPK4, an SNF1-related wheat protein kinase, and to WPK4-phosphorylated nitrate reductase J. Biol. Chem. 275 2000 31695 31700
29. C. Jonak, E. Heberle-Bors, and H. Hirt Inflorescence-specific expression of AtK-1, a novel Arabidopsis thaliana homologue of shaggy/glycogen synthase kinase-3 Plant Mol. Biol. 27 1995 217 221
30. C.N. Kanchiswamy, H. Takahashi, S. Quadro, M.E. Maffei, S. Bossi, C. Bertea, S.A. Zebelo, A. Muroi, N. Ishihama, H. Yoshioka, W. Boland, J. Takabayashi, Y. Endo, T. Sawasaki, and G. Arimura Regulation of Arabidopsis defense responses against Spodoptera littoralis by CPK-mediated calcium signaling BMC Plant Biol. 10 2010 97
31. T.W. Kim, S. Guan, Y. Sun, Z. Deng, W. Tang, J.X. Shang, Y. Sun, A.L. Burlingame, and Z.Y. Wang Brassinosteroid signal transduction from cell-surface receptor kinases to nuclear transcription factors Nat. Cell Biol. 11 2009 1254 1260
32. H. Knight, and M.R. Knight Abiotic stress signaling pathways: specificity and cross-talk Trends Plant Sci. 6 2001 262 267
33. C.G. Kurland Translational accuracy in vitro Cell 28 1982 201 202 (Pubitemid 12100381)
34. J. Li, and K.H. Nam Regulation of brassinosteroid signaling by a GSK3/SHAGGY-like kinase Science 295 2002 1299 1301 (Pubitemid 34157622)
35. J. Li, J. Wen, K.A. Lease, J.T. Doke, F.E. Tax, and J.C. Walker BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling Cell 110 2002 213 222 (Pubitemid 34876549)
36. K. Madin, T. Sawasaki, T. Ogasawara, and Y. Endo A highly efficient and robust cell-free protein synthesis system prepared from wheat embryos: plants apparently contain a suicide system directed at ribosomes Proc. Natl. Acad. Sci. USA 97 2000 559 564 (Pubitemid 30070348)
37. K. Matsuoka, H. Komori, M. Nose, Y. Endo, and T. Sawasaki Simple screening method for autoantigen proteins using the N-terminal biotinylated protein library produced by wheat cell-free synthesis J. Proteome Res. 9 2010 4264 4273
38. D. Merkle, P. Douglas, G.B. Moorhead, Z. Leonenko, Y. Yu, D. Cramb, D.P. Bazett-Jones, and S.P. Lees-Miller The DNA-dependent protein kinase interacts with DNA to form a protein-DNA complex that is disrupted by phosphorylation Biochemistry 41 2002 12706 12714 (Pubitemid 35192499)
39. A.F. Monroy, and R.S. Dhindsa Low-temperature signal transduction: induction of cold acclimation-specific genes of alfalfa by calcium at 25 °C Plant Cell 7 1995 321 333
40. K.H. Nam, and J. Li BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling Cell 110 2002 203 212 (Pubitemid 34876548)
41. O. Nayler, F. Schnorrer, S. Stamm, and A. Ullrich The cellular localization of the murine serine/arginine-rich protein kinase CLK2 is regulated by serine 141 autophosphorylation J. Biol. Chem. 273 1998 34341 34348 (Pubitemid 29008912)
42. W.J. Netzer, and F.U. Hartl Recombination of protein domains facilitated by co-translational folding in eukaryotes Nature 388 1997 343 349 (Pubitemid 27334805)
43. R. Nishihama, T. Soyano, M. Ishikawa, S. Araki, H. Tanaka, T. Asada, K. Irie, M. Ito, M. Terada, H. Banno, Y. Yamazaki, and Y. Machida Expansion of the cell plate in plant cytokinesis requires a kinesin-like protein/MAPKKK complex Cell 109 2002 87 99 (Pubitemid 34327519)
44. A. Nozawa, Y. Matsubara, Y. Tanaka, H. Takahashi, T. Akagi, M. Seki, K. Shinozaki, Y. Endo, and T. Sawasaki Construction of a protein library of Arabidopsis transcription factors using a wheat cell-free protein production system and its application for DNA binding analysis Biosci. Biotechnol. Biochem. 73 2009 1661 1664
45. T. Ogasawara, T. Sawasaki, R. Morishita, A. Ozawa, K. Madin, and Y. Endo A new class of enzyme acting on damaged ribosomes: ribosomal RNA apurinic site specific lyase found in wheat germ EMBO J. 18 1999 6522 6531 (Pubitemid 29533256)
46. M.H. Oh, X. Wang, U. Kota, M.B. Goshe, S.D. Clouse, and S.C. Huber Tyrosine phosphorylation of the BRI1 receptor kinase emerges as a component of brassinosteroid signaling in Arabidopsis Proc. Natl. Acad. Sci. USA 106 2009 658 663
47. M. Parniske Arbuscular mycorrhiza: the mother of plant root endosymbioses Nat. Rev. Microbiol. 6 2008 763 775
48. O.R. Patharkar, and J.C. Cushman A stress-induced calcium-dependent protein kinase from Mesembryanthemum crystallinum phosphorylates a two-component pseudo-response regulator Plant Cell 24 2000 679 691 (Pubitemid 32040066)
49. M.Y. Pavlov, and M. Ehrenberg Rate of translation of natural mRNAs in an optimized in vitro system Arch. Biochem. Biophys. 328 1996 9 16 (Pubitemid 26108163)
50. G. Pimienta, and J. Pascual Canonical and alternative MAPK signaling Cell Cycle 6 2007 2628 2632 (Pubitemid 350224045)
51. D.M. Roberts, and A.C. Harmon Calcium modulated proteins: targets of intracellular calcium signals in higher plants Annu. Rev. Plant Physiol. Plant Mol. Biol. 43 1992 375 414
52. P.P. Roux, and J. Blenis ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions Microbiol. Mol. Biol. Rev. 68 2004 320 344 (Pubitemid 38756868)
53. A. Ryo, N. Tsurutani, K. Ohba, R. Kimura, J. Komano, M. Nishi, H. Soeda, S. Hattori, K. Perrem, M. Yamamoto, J. Chiba, J. Mimaya, K. Yoshimura, S. Matsushita, M. Honda, A. Yoshimura, T. Sawasaki, I. Aoki, Y. Morikawa, and N. Yamamoto SOCS1 is an inducible host factor during HIV-1 infection and regulates the intracellular trafficking and stability of HIV-1 Gag Proc. Natl. Acad. Sci. USA 105 2008 294 299
54. 2+-dependent protein kinase confers both cold and salt/drought tolerance on rice plants Plant J. 23 2000 319 327 (Pubitemid 30620839)
55. T. Sawasaki, T. Ogasawara, R. Morishita, and Y. Endo A cell-free protein synthesis system for high-throughput proteomics Proc. Natl. Acad. Sci. USA 99 2002 14652 14657 (Pubitemid 35334539)
56. T. Sawasaki, Y. Hasegawa, M. Tsuchimochi, N. Kamura, T. Ogasawara, and Y. Endo A bilayer cell-free protein synthesis system for high-throughput screening of gene products FEBS Lett. 514 2002 102 105 (Pubitemid 34251251)
57. T. Sawasaki, Y. Hasegawa, R. Morishita, M. Seki, K. Shinozaki, and Y. Endo Genome-scale, biochemical annotation method based on the wheat germ cell-free protein synthesis system Phytochemistry 65 2004 1549 1555 (Pubitemid 38969936)
58. T. Sawasaki, M.D. Gouda, T. Kawasaki, T. Tsuboi, Y. Tozawa, K. Takai, and Y. Endo The wheat germ cell-free expression system: methods for high-throughput materialization of genetic information Methods Mol. Biol. 310 2005 131 144
59. T. Sawasaki, R. Morishita, M.D. Gouda, and Y. Endo Methods for high-throughput materialization of genetic information based on wheat germ cell-free expression system Methods Mol. Biol. 375 2007 95 106 (Pubitemid 350183383)
60. T. Sawasaki, N. Kamura, S. Matsunaga, M. Saeki, M. Tsuchimochi, R. Morishita, and Y. Endo Arabidopsis HY5 protein functions as a DNA-binding tag for purification and functional immobilization of proteins on agarose/DNA microplate FEBS Lett. 582 2008 221 228
61. M. Seki, M. Narusaka, A. Kamiya, J. Ishida, M. Satou, T. Sakurai, M. Nakajima, A. Enju, K. Akiyama, Y. Oono, M. Muramatsu, Y. Hayashizaki, J. Kawai, P. Carninci, M. Itoh, Y. Ishii, T. Arakawa, K. Shibata, A. Shinagawa, and K. Shinozaki Functional annotation of a full-length Arabidopsis cDNA collection Science 296 2002 141 145 (Pubitemid 34280073)
62. S.H. Shiu, and A.B. Bleecker Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases Proc. Natl. Acad. Sci. USA 99 2001 10763 10768 (Pubitemid 32878695)
63. N.F. Silva, and D.R. Goring The proline-rich, extensin-like receptor kinase-1 (PERK1) gene is rapidly induced by wounding Plant Mol. Biol. 50 2002 667 685
64. Y. Stahl, and R. Simon Plant stem cell niches Int. J. Dev. Biol. 49 2005 479 489 (Pubitemid 41615603)
65. N. Sugiyama, H. Nakagami, K. Mochida, A. Daudi, M. Tomita, K. Shirasu, and Y. Ishihama Large-scale phosphorylation mapping reveals the extent of tyrosine phosphorylation in Arabidopsis Mol. Syst. Biol. 4 2008 193
66. D. Tadokoro, S. Shimizu, S.K. Takahama, S. Hayashi, y. Endo, and T. Sawasaki Characterization of a caspase-3-substrate kinome using an N- and C-terminally tagged protein kinase library produced by a cell-free system Cell Death Dis. 1 2010 e89
67. H. Takahashi, A. Nozawa, M. Seki, K. Shinozaki, Y. Endo, and T. Sawasaki A simple and high-sensitivity method for analysis of ubiquitination and polyubiquitination based on wheat cell-free protein synthesis BMC Plant Biol. 9 2009 39
68. S. Takayama, and A. Isogai Self-incompatibility in plants Annu. Rev. Plant Biol. 56 2005 467 489 (Pubitemid 40802418)
69. A. Trewavas Le calcium, C'est la vie: calcium makes waves Plant Physiol. 120 1999 1 6 (Pubitemid 29375402)
70. 2+-dependent protein kinases are induced by drought and high-salt stresses in Arabidopsis thaliana Mol. Gen. Genet. 244 1994 331 340
71. S. van Bentem, D. Anrather, I. Dohnal, E. Roitinger, E. Csaszar, J. Joore, J. Buijnink, A. Carreri, C. Forzani, Z.J. Lorkovic, A. Barta, D. Lecourieux, A. Verhounig, C. Jonak, and H. Hirt Site-specific phosphorylation profiling of Arabidopsis proteins by mass spectrometry and peptide chip analysis J. Proteome Res. 7 2008 2458 2470
72. Q.M. Wang, C.J. Fiol, A.A. DePaoli-Roach, and P.J. Roach Glycogen synthase kinase-3 beta is a dual specificity kinase differentially regulated by tyrosine and serine/threonine phosphorylation J. Biol. Chem. 269 1994 14566 14574
73. X. Wang, X. Li, J. Meisenhelder, T. Hunter, S. Yoshida, T. Asami, and J. Chory Autoregulation and homodimerization are involved in the activation of the plant steroid receptor BRI1 Dev. Cell 8 2005 855 865 (Pubitemid 40754057)
74. J. Wu, A.J. Rossomando, J.H. Her, R. Del Vecchio, M.J. Weber, and T.W. Sturgill Autophosphorylation in vitro of recombinant 42-kilodalton mitogen-activated protein kinase on tyrosine Proc. Natl. Acad. Sci. USA 88 1991 9508 9512 (Pubitemid 21915660)
75. J. Xu, Y.S. Tian, R.H. Peng, A.S. Xiong, B. Zhu, X.F. Jin, F. Gao, X.Y. Fu, X.L. Hou, and Q.H. Yao AtCPK6, a functionally redundant and positive regulator involved in salt/drought stress tolerance in Arabidopsis Planta 231 2010 1251 1260
76. K. Yano, K. Aoki, H. Suzuki, and D. Shibata DAGViz: a directed acyclic graph browser that supports analysis of Gene Ontology annotation Plant Biotechnol. 26 2009 9 13
77. G.M. Yoon, H.S. Cho, H.J. Ha, J.R. Liu, and H.P. Lee Characterization of NtCDPK1, a calcium-dependent protein kinase gene in Nicotiana tabacum, and the activity of its encoded protein Plant Mol. Biol. 39 1999 991 1001