Phosphorylation of Thellungiella salsuginea dehydrins TsDHN-1 and TsDHN-2 facilitates cation-induced conformational changes and actin assembly

Biochemistry

Volumn 50, Issue 44, 2011, Pages 9587-9604

  Rahman, Luna N ^a   Smith, Graham S T ^a   Bamm, Vladimir V ^a   Voyer Grant, Janine A M ^a   Moffatt, Barbara A ^b   Dutcher, John R ^a   Harauz, George ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b UNIVERSITY OF WATERLOO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN FILAMENT; CASEIN KINASE; CONFORMATIONAL CHANGE; CYTOSKELETONS; DEHYDRINS; DISORDERED PROTEINS; DIVALENT CATION; ENVIRONMENTAL CONDITIONS; ENVIRONMENTAL STRESS; FUSION PROTEINS; IN-VITRO; LATE EMBRYOGENESIS ABUNDANT PROTEINS; LOW TEMPERATURES; POLYPROLINE II; STRESS CONDITION; TRANSFORM INFRARED SPECTROSCOPY; TRANSMISSION ELECTRON;

AMINO ACIDS; ATOMIC FORCE MICROSCOPY; CIRCULAR DICHROISM SPECTROSCOPY; CONFORMATIONS; CYTOLOGY; DICHROISM; FLEXIBLE STRUCTURES; FOURIER TRANSFORM INFRARED SPECTROSCOPY; METAL IONS; PHOSPHORYLATION; POSITIVE IONS; STRUCTURAL ANALYSIS;

PROTEINS;

ACTIN; CASEIN KINASE II; DEHYDRIN; DIVALENT CATION; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ARTICLE; ATOMIC FORCE MICROSCOPY; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CYTOSKELETON; HIGHER PLANT; IN VITRO STUDY; INFRARED SPECTROSCOPY; MEMBRANE; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN POLYMERIZATION; PROTEIN SECONDARY STRUCTURE; SEDIMENTATION; STRUCTURE ANALYSIS; TEMPERATURE; THELLUNGIELLA SALSUGINEA; TRANSMISSION ELECTRON MICROSCOPY;

ACTINS; BRASSICACEAE; CALCIUM; CATIONS, DIVALENT; HYDROGEN-ION CONCENTRATION; PHOSPHORYLATION; PLANT PROTEINS; PROTEIN CONFORMATION; PROTEIN ISOFORMS; ZINC;

THELLUNGIELLA SALSUGINEA;

EID: 80155138588     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi201205m     Document Type: Article

References (84)

1. Battaglia, M., Olvera-Carrillo, Y., Garciarrubio, A., Campos, F., and Covarrubias, A. A. (2008) The enigmatic LEA proteins and other hydrophilins Plant Physiol. 148, 6-24 (Pubitemid 352847571)
2. Hundertmark, M. and Hincha, D. K. (2008) LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana BMC Genomics 9, 118
3. Close, T. J. (1997) Dehydrins: A commonality in the response of plants to dehydration and low temperature Physiol. Plant. 100, 291-296 (Pubitemid 27274905)
4. Kosova, K., Vitamvas, P., and Prasil, I. T. (2007) The role of dehydrins in plant response to cold Biol. Plant. 51, 601-617 (Pubitemid 350163610)
5. Tommasini, L., Svensson, J. T., Rodriguez, E. M., Wahid, A., Malatrasi, M., Kato, K., Wanamaker, S., Resnik, J., and Close, T. J. (2008) Dehydrin gene expression provides an indicator of low temperature and drought stress: Transcriptome-based analysis of barley (Hordeum vulgare L.) Funct. Integr. Genomics 8, 387-405
6. Eriksson, S. K. and Harryson, P. (2011) Dehydrins: Molecular biology, structure, and function. In Plant Desiccation Tolerance (Lüttge, U., Ed.) pp 289-304, Springer-Verlag, Berlin.
7. Tunnacliffe, A. and Wise, M. J. (2007) The continuing conundrum of the LEA proteins Naturwissenschaften 94, 791-812 (Pubitemid 47367664)
8. Rahman, L. N., Chen, L., Nazim, S., Bamm, V. V., Yaish, M. W., Moffatt, B. A., Dutcher, J. R., and Harauz, G. (2010) Interactions of intrinsically disordered Thellungiella salsuginea dehydrins TsDHN-1 and TsDHN-2 with membranes: Synergistic effects of lipid composition and temperature on secondary structure Biochem. Cell Biol. 88, 791-807
9. Rahman, L. N., Bamm, V. V., Voyer, J. A. M., Smith, G. S., Chen, L., Yaish, M. W., Moffatt, B. A., Dutcher, J. R., and Harauz, G. (2011) Zinc induces disorder-to-order transitions in free and membrane-associated Thellungiella salsuginea dehydrins TsDHN-1 and TsDHN-2: A solution CD and solid-state ATR-FTIR study Amino Acids 40, 1485-1502
10. Haaning, S., Radutoiu, S., Hoffmann, S. V., Dittmer, J., Giehm, L., Otzen, D. E., and Stougaard, J. (2008) An unusual intrinsically disordered protein from the model legume Lotus japonicus stabilizes proteins in vitro J. Biol. Chem. 283, 31142-31152
11. Kovacs, D., Kalmar, E., Torok, Z., and Tompa, P. (2008) Chaperone activity of ERD10 and ERD14, two disordered stress-related plant proteins Plant Physiol. 147, 381-390 (Pubitemid 352844363)
12. Tompa, P. and Kovacs, D. (2010) Intrinsically disordered chaperones in plants and animals Biochem. Cell Biol. 88, 167-174
13. Hughes, S. and Graether, S. P. (2011) Cryoprotective mechanism of a small intrinsically disordered dehydrin protein Protein Sci. 20, 42-50
14. Hundertmark, M., Dimova, R., Lengefeld, J., Seckler, R., and Hincha, D. K. (2011) The intrinsically disordered late embryogenesis abundant protein LEA18 from Arabidopsis thaliana modulates membrane stability through binding and folding Biochim. Biophys. Acta 1808, 446-453
15. Eriksson, S. K., Kutzer, M., Procek, J., Grobner, G., and Harryson, P. (2011) Tunable membrane binding of the intrinsically disordered dehydrin lti30, a cold-induced plant stress protein Plant Cell 23, 2391-2404
16. Abu-Abied, M., Golomb, L., Belausov, E., Huang, S., Geiger, B., Kam, Z., Staiger, C. J., and Sadot, E. (2006) Identification of plant cytoskeleton-interacting proteins by screening for actin stress fiber association in mammalian fibroblasts Plant J. 48, 367-379 (Pubitemid 44571143)
17. Battaglia, M., Solorzano, R. M., Hernandez, M., Cuellar-Ortiz, S., Garcia-Gomez, B., Marquez, J., and Covarrubias, A. A. (2007) Proline-rich cell wall proteins accumulate in growing regions and phloem tissue in response to water deficit in common bean seedlings Planta 225, 1121-1133 (Pubitemid 46434730)
18. Hara, M., Shinoda, Y., Tanaka, Y., and Kuboi, T. (2009) DNA binding of Citrus dehydrin promoted by zinc ion Plant Cell Environ. 32, 532-541
19. Receveur-Bréchot, V., Bourhis, J. M., Uversky, V. N., Canard, B., and Longhi, S. (2006) Assessing protein disorder and induced folding Proteins 62, 24-45 (Pubitemid 43063003)
20. Mouillon, J. M., Eriksson, S. K., and Harryson, P. (2008) Mimicking the plant-cell interior under water stress by macromolecular crowding: Disordered dehydrin proteins are highly resistant to structural collapse Plant Physiol. 148, 1925-1937 (Pubitemid 352847470)
21. Tompa, P., Banki, P., Bokor, M., Kamasa, P., Kovacs, D., Lasanda, G., and Tompa, K. (2006) Protein-water and protein-buffer interactions in the aqueous solution of an intrinsically unstructured plant dehydrin: NMR intensity and DSC aspects Biophys. J. 91, 2243-2249 (Pubitemid 44354754)
22. Heyen, B. J., Alsheikh, M. K., Smith, E. A., Torvik, C. F., Seals, D. F., and Randall, S. K. (2002) The calcium-binding activity of a vacuole-associated, dehydrin-like protein is regulated by phosphorylation Plant Physiol. 130, 675-687 (Pubitemid 35224775)
23. Alsheikh, M. K., Heyen, B. J., and Randall, S. K. (2003) Ion binding properties of the dehydrin ERD14 are dependent upon phosphorylation J. Biol. Chem. 278, 40882-40889 (Pubitemid 37280907)
24. Hara, M., Fujinaga, M., and Kuboi, T. (2004) Radical scavenging activity and oxidative modification of Citrus dehydrin Plant Physiol. Biochem. 42, 657-662 (Pubitemid 39160979)
25. Hara, M., Fujinaga, M., and Kuboi, T. (2005) Metal binding by citrus dehydrin with histidine-rich domains J. Exp. Bot. 56, 2695-2703 (Pubitemid 41330535)
26. Rom, S., Gilad, A., Kalifa, Y., Konrad, Z., Karpasas, M. M., Goldgur, Y., and Bar-Zvi, D. (2006) Mapping the DNA- and zinc-binding domains of ASR1 (abscisic acid stress ripening), an abiotic-stress regulated plant specific protein Biochimie 88, 621-628 (Pubitemid 44062084)
27. Goldgur, Y., Rom, S., Ghirlando, R., Shkolnik, D., Shadrin, N., Konrad, Z., and Bar-Zvi, D. (2007) Desiccation and zinc binding induce transition of tomato abscisic acid stress ripening 1, a water stress- and salt stress-regulated plant-specific protein, from unfolded to folded state Plant Physiol. 143, 617-628 (Pubitemid 46940954)
28. Xu, J., Zhang, Y. X., Wei, W., Han, L., Guan, Z. Q., Wang, Z., and Chai, T. Y. (2008) BjDHNs confer heavy-metal tolerance in plants Mol. Biotechnol. 38, 91-98
29. 2+ triggers reversible aggregation of a disordered His-rich dehydrin MpDhn12 from Musa paradisiaca J. Biochem. doi: 10.1093/jb/mvr082
30. Mehta, P. A., Rebala, K. C., Venkataraman, G., and Parida, A. (2009) A diurnally regulated dehydrin from Avicennia marina that shows nucleo-cytoplasmic localization and is phosphorylated by casein kinase II in vitro Plant Physiol. Biochem. 47, 701-709
31. Jiang, X. and Wang, Y. (2004) β-Elimination coupled with tandem mass spectrometry for the identification of in vivo and in vitro phosphorylation sites in maize dehydrin DHN1 protein Biochemistry 43, 15567-15576 (Pubitemid 39647482)
32. Nardozzi, J. D., Lott, K., and Cingolani, G. (2010) Phosphorylation meets nuclear import: A review Cell Commun. Signaling 8, 32
33. Plotnikov, A., Zehorai, E., Procaccia, S., and Seger, R. (2011) The MAPK cascades: Signaling components, nuclear roles and mechanisms of nuclear translocation Biochim. Biophys. Acta 1813, 1619-1633
34. Jensen, A. B., Goday, A., Figueras, M., Jessop, A. C., and Pages, M. (1998) Phosphorylation mediates the nuclear targeting of the maize Rab17 protein Plant J. 13, 691-697 (Pubitemid 28178495)
35. Vilardell, J., Goday, A., Freire, M. A., Torrent, M., Martinez, M. C., Torne, J. M., and Pages, M. (1990) Gene sequence, developmental expression, and protein phosphorylation of RAB-17 in maize Plant Mol. Biol. 14, 423-432
36. Wong, C. E., Li, Y., Whitty, B. R., Diaz-Camino, C., Akhter, S. R., Brandle, J. E., Golding, G. B., Weretilnyk, E. A., Moffatt, B. A., and Griffith, M. (2005) Expressed sequence tags from the Yukon ecotype of Thellungiella reveal that gene expression in response to cold, drought and salinity shows little overlap Plant Mol. Biol. 58, 561-574 (Pubitemid 41125985)
37. Griffith, M., Timonin, M., Wong, A. C., Gray, G. R., Akhter, S. R., Saldanha, M., Rogers, M. A., Weretilnyk, E. A., and Moffatt, B. (2007) Thellungiella: An Arabidopsis -related model plant adapted to cold temperatures Plant Cell Environ. 30, 529-538 (Pubitemid 46537712)
38. Amtmann, A. (2009) Learning from evolution: Thellungiella generates new knowledge on essential and critical components of abiotic stress tolerance in plants Mol. Plant 2, 3-12
39. Rath, A., Davidson, A. R., and Deber, C. M. (2005) The structure of "unstructured" regions in peptides and proteins: Role of the polyproline II helix in protein folding and recognition Biopolymers 80, 179-185 (Pubitemid 40791050)
40. Mossessova, E. and Lima, C. D. (2000) Ulp1-SUMO crystal structure and genetic analysis reveal conserved interactions and a regulatory element essential for cell growth in yeast Mol. Cell 5, 865-876
41. Jacob, A. M. and Turck, C. W. (2008) Detection of post-translational modifications by fluorescent staining of two-dimensional gels Methods Mol. Biol. 446, 21-32
42. Yan, J. X., Harry, R. A., Spibey, C., and Dunn, M. J. (2000) Postelectrophoretic staining of proteins separated by two-dimensional gel electrophoresis using SYPRO dyes Electrophoresis 21, 3657-3665
43. Bamm, V. V. and Harauz, G. (2008) Expression and purification of the active variant of recombinant murine Golli-interacting protein (GIP): Characterization of its phosphatase activity and interaction with Golli-BG21 Protein Expression Purif. 62, 36-43
44. 2+-dependent calmodulin interaction Biophys. J. 101, 1248-1256
45. Pardee, J. D. and Spudich, J. A. (1982) Purification of muscle actin Methods Cell Biol. 24, 271-289 (Pubitemid 12055905)
46. Bamm, V. V., Ahmed, M. A., and Harauz, G. (2010) Interaction of myelin basic protein with actin in the presence of dodecylphosphocholine micelles Biochemistry 49, 6903-6915
47. Ahmed, M. A. M., Bamm, V. V., Shi, L., Steiner-Mosonyi, M., Dawson, J. F., Brown, L., Harauz, G., and Ladizhansky, V. (2009) Induced secondary structure and polymorphism in an intrinsically disordered structural linker of the CNS: Solid-state NMR and FTIR spectroscopy of myelin basic protein bound to actin Biophys. J. 96, 180-191
48. Boggs, J. M., Rangaraj, G., Gao, W., and Heng, Y. M. (2006) Effect of phosphorylation of myelin basic protein by MAPK on its interactions with actin and actin binding to a lipid membrane in vitro Biochemistry 45, 391-401 (Pubitemid 43100406)
49. Malakhov, M. P., Mattern, M. R., Malakhova, O. A., Drinker, M., Weeks, S. D., and Butt, T. R. (2004) SUMO fusions and SUMO-specific protease for efficient expression and purification of proteins J. Struct. Funct. Genomics 5, 75-86 (Pubitemid 39030623)
50. Satakarni, M. and Curtis, R. (2011) Production of recombinant peptides as fusions with SUMO Protein Expression Purif. 78, 113-119
51. Kader, M. A. and Lindberg, S. (2010) Cytosolic calcium and pH signaling in plants under salinity stress Plant Signaling Behav. 5, 233-238
52. Koyama, H., Toda, T., and Hara, T. (2001) Brief exposure to low-pH stress causes irreversible damage to the growing root in Arabidopsis thaliana: Pectin-Ca interaction may play an important role in proton rhizotoxicity J. Exp. Bot. 52, 361-368 (Pubitemid 32337474)
53. Mathieu, Y., Jouanneau, J. P., Thomine, S., Lapous, D., and Guern, J. (1994) Cytosolic protons as secondary messengers in elicitor-induced defence responses Biochem. Soc. Symp. 60, 113-130
54. Roos, W., Viehweger, K., Dordschbal, B., Schumann, B., Evers, S., Steighardt, J., and Schwartze, W. (2006) Intracellular pH signals in the induction of secondary pathways: The case of Eschscholzia californica J. Plant Physiol. 163, 369-381 (Pubitemid 43112090)
55. Polverini, E., Rangaraj, G., Libich, D. S., Boggs, J. M., and Harauz, G. (2008) Binding of the proline-rich segment of myelin basic protein to SH3-domains: Spectroscopic, microarray, and modelling studies of ligand conformation and effects of post-translational modifications Biochemistry 47, 267-282
56. Harauz, G. and Libich, D. S. (2009) The classic basic protein of myelin: Conserved structural motifs and the dynamic molecular barcode involved in membrane adhesion and protein-protein interactions Curr. Protein Pept. Sci. 10, 196-215
57. Soulages, J. L., Kim, K., Arrese, E. L., Walters, C., and Cushman, J. C. (2003) Conformation of a group 2 late embryogenesis abundant protein from soybean. Evidence of poly(l -proline)-type II structure Plant Physiol. 131, 963-975 (Pubitemid 36400336)
58. Mazars, C., Bourque, S., Mithofer, A., Pugin, A., and Ranjeva, R. (2009) Calcium homeostasis in plant cell nuclei New Phytol. 181, 261-274 (Pubitemid 352840371)
59. Reddy, V. S. and Reddy, A. S. (2004) Proteomics of calcium-signaling components in plants Phytochemistry 65, 1745-1776 (Pubitemid 38969920)
60. Jung, C. (2000) Insight into protein structure and protein-ligand recognition by Fourier transform infrared spectroscopy J. Mol. Recognit. 13, 325-351
61. Goormaghtigh, E., Gasper, R., Benard, A., Goldsztein, A., and Raussens, V. (2009) Protein secondary structure content in solution, films and tissues: Redundancy and complementarity of the information content in circular dichroism, transmission and ATR FTIR spectra Biochim. Biophys. Acta 1794, 1332-1343
62. Harauz, G., Ladizhansky, V., and Boggs, J. M. (2009) Structural polymorphism and multifunctionality of myelin basic protein Biochemistry 48, 8094-8104
63. Iakoucheva, L. M., Radivojac, P., Brown, C. J., OConnor, T. R., Sikes, J. G., Obradovic, Z., and Dunker, A. K. (2004) The importance of intrinsic disorder for protein phosphorylation Nucleic Acids Res. 32, 1037-1049 (Pubitemid 38854704)
64. Vacic, V., Oldfield, C. J., Mohan, A., Radivojac, P., Cortese, M. S., Uversky, V. N., and Dunker, A. K. (2007) Characterization of molecular recognition features, MoRFs, and their binding partners J. Proteome Res. 6, 2351-2366 (Pubitemid 46985123)
65. Tompa, P. and Fuxreiter, M. (2008) Fuzzy complexes: Polymorphism and structural disorder in protein-protein interactions Trends Biochem. Sci. 33, 2-8
66. Uversky, V. N. (2009) Intrinsically disordered proteins and their environment: Effects of strong denaturants, temperature, pH, counter ions, membranes, binding partners, osmolytes, and macromolecular crowding Protein J. 28, 305-325
67. Wang, H., Wu, Z., Chen, Y., Yang, C., and Shi, D. (2011) Effects of salt and alkali stresses on growth and ion balance in rice (Oryza sativa L.) Plant Soil Environ. 57, 286-294
68. Szalaine, A. B., Kovacs, D., Tompa, P., and Perczel, A. (2011) Full backbone assignment and dynamics of the intrinsically disordered dehydrin ERD14 Biomol. NMR Assignments 5, 189-193
69. He, H. J., Wang, X. S., Pan, R., Wang, D. L., Liu, M. N., and He, R. Q. (2009) The proline-rich domain of tau plays a role in interactions with actin BMC Cell Biol. 10, 81
70. Volkmann, D. and Baluska, F. (1999) Actin cytoskeleton in plants: From transport networks to signaling networks Microsc. Res. Tech. 47, 135-154 (Pubitemid 29519822)
71. Chen, C. Y., Cheung, A. Y., and Wu, H. M. (2003) Actin-depolymerizing factor mediates Rac/Rop GTPase-regulated pollen tube growth Plant Cell 15, 237-249 (Pubitemid 36137673)
72. Chen, C. W., Yang, Y. W., Lur, H. S., Tsai, Y. G., and Chang, M. C. (2006) A novel function of abscisic acid in the regulation of rice (Oryza sativa L.) root growth and development Plant Cell Physiol. 47, 1-13
73. Ouellet, F., Carpentier, E., Cope, M. J., Monroy, A. F., and Sarhan, F. (2001) Regulation of a wheat actin-depolymerizing factor during cold acclimation Plant Physiol. 125, 360-368 (Pubitemid 32116773)
74. Hohenberger, P., Eing, C., Straessner, R., Durst, S., Frey, W., and Nick, P. (2011) Plant actin controls membrane permeability Biochim. Biophys. Acta 1808, 2304-2312
75. Wang, H. J., Wan, A. R., and Jauh, G. Y. (2008) An actin-binding protein, LlLIM1, mediates calcium and hydrogen regulation of actin dynamics in pollen tubes Plant Physiol. 147, 1619-1636
76. Papuga, J., Hoffmann, C., Dieterle, M., Moes, D., Moreau, F., Tholl, S., Steinmetz, A., and Thomas, C. (2010) Arabidopsis LIM proteins: A family of actin bundlers with distinct expression patterns and modes of regulation Plant Cell 22, 3034-3052
77. Chen, C. Y., Wong, E. I., Vidali, L., Estavillo, A., Hepler, P. K., Wu, H. M., and Cheung, A. Y. (2002) The regulation of actin organization by actin-depolymerizing factor in elongating pollen tubes Plant Cell 14, 2175-2190
78. Dunn, M. A., Morris, A., Jack, P. L., and Hughes, M. A. (1993) A low-temperature-responsive translation elongation factor 1α from barley (Hordeum vulgare L.) Plant Mol. Biol. 23, 221-225 (Pubitemid 2005204)
79. Thomashow, M. F. (1999) Plant Cold Acclimation: Freezing Tolerance Genes and Regulatory Mechanisms Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 571-599 (Pubitemid 129491974)
80. Reape, T. J. and McCabe, P. F. (2010) Apoptotic-like regulation of programmed cell death in plants Apoptosis 15, 249-256
81. Gourlay, C. W. and Ayscough, K. R. (2005) The actin cytoskeleton: A key regulator of apoptosis and ageing? Nat. Rev. Mol. Cell Biol. 6, 583-589 (Pubitemid 40943049)
82. Franklin-Tong, V. E. and Gourlay, C. W. (2008) A role for actin in regulating apoptosis/programmed cell death: Evidence spanning yeast, plants and animals Biochem. J. 413, 389-404
83. Smertenko, A. and Franklin-Tong, V. E. (2011) Organisation and regulation of the cytoskeleton in plant programmed cell death Cell Death Differ. 18, 1263-1270
84. DAngeli, S., Malho, R., and Altamura, M. M. (2003) Low-temperature sensing in olive tree: Calcium signalling and cold acclimation Plant Sci. 165, 1303-1313 (Pubitemid 37481362)