Cloning, expression and functional characterization of the C2 domain from tomato phospholipase Dα

Plant Physiology and Biochemistry

Volumn 49, Issue 1, 2011, Pages 18-32

  Tiwari, Krishnaraj ^a   Paliyath, Gopinadhan ^a  

^a UNIVERSITY OF GUELPH   (Canada)

Author keywords

Calcium; Fluorescence resonance energy transfer; Fruit ripening; Immunohistochemistry; Lipid; Membrane; Phosphatidylinositol phosphate; Senescence

Indexed keywords

CALCIUM; COMPLEMENTARY DNA; PHOSPHOLIPASE D; PHOSPHOLIPID; PROTEIN KINASE C ALPHA; RECOMBINANT PROTEIN; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CELL ORGANELLE; CHEMISTRY; ENZYME ACTIVE SITE; ENZYMOLOGY; ESCHERICHIA COLI; FRUIT; GENE EXPRESSION; GENE VECTOR; GENETICS; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; PHOSPHORYLATION; PROTEIN TERTIARY STRUCTURE; SIGNAL TRANSDUCTION; STATIC ELECTRICITY; TOMATO;

AMINO ACID SEQUENCE; BINDING SITES; CALCIUM; CATALYTIC DOMAIN; CLONING, MOLECULAR; DNA, COMPLEMENTARY; ESCHERICHIA COLI; FRUIT; GENE EXPRESSION; GENETIC VECTORS; LYCOPERSICON ESCULENTUM; MOLECULAR SEQUENCE DATA; ORGANELLES; PHOSPHOLIPASE D; PHOSPHOLIPIDS; PHOSPHORYLATION; PLANT PROTEINS; PROTEIN KINASE C-ALPHA; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; STATIC ELECTRICITY;

ESCHERICHIA COLI; LYCOPERSICON ESCULENTUM;

EID: 78650290748     PISSN: 09819428     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plaphy.2010.09.015     Document Type: Article

References (57)

1. Paliyath G., Droillard M.J. The mechanisms of membrane deterioration and disassembly during senescence. Plant Physiol. Biochem. 1992, 30:789-812.
2. Wang X. Phospholipase D in hormonal and stress signaling. Curr. Opin. Plant Biol. 2002, 5:408-414.
3. Paliyath G., Tiwari K., Yuan H., Whitaker B.D. Structural deterioration in produce: phospholipase D, membrane deterioration, and senescence. Postharvest Biology and Technology of Fruits, Vegetables, and Flowers 2008, 195-239. Wiley-Blackwell, USA. first ed. G. Paliyath, D.P. Murr, A.K. Handa, S. Lurie (Eds.).
4. Pinhero R.G., Almquist K.C., Novotna Z., Paliyath G. Developmental regulation of phospholipase D in tomato fruits. Plant Physiol. Biochem. 2003, 41:223-240. 10.1016/S0981-9428(03)00014-7.
5. Ponting C.P., Parker P.J. Extending the C2 domain family: C2s in PKCs delta, epsilon, eta, theta, phospholipases, GAPs, and perforin. Protein Sci. 1996, 5:162-166.
6. Sutton R.B., Davletov B.A., Berghuis A.M., Sudhof T.C., Sprang S.R. Structure of the first C2 domain of synaptotagmin I: a novel Ca2+/phospholipid-binding fold. Cell 1995, 80:929-938.
7. Perisic O., Fong S., Lynch D.E., Bycroft M., Williams R.L. Crystal structure of a calcium-phospholipid binding domain from cytosolic phospholipase A2. J. Biol. Chem. 1998, 273:1596-1604.
8. Xu G.Y., McDonagh T., Yu H.A., Nalefski E.A., Clark J.D., Cumming D.A. Solution structure and membrane interactions of the C2 domain of cytosolic phospholipase A2. J. Mol. Biol. 1998, 280:485-500. 10.1006/jmbi.1998.1874.
9. Verdaguer N., Corbalan-Garcia S., Ochoa W.F., Fita I., Gomez-Fernandez J.C. Ca(2+) bridges the C2 membrane-binding domain of protein kinase Calpha directly to phosphatidylserine. EMBO J 1999, 18:6329-6338. 10.1093/emboj/18.22.6329.
10. Ochoa W.F., Garcia-Garcia J., Fita I., Corbalan-Garcia S., Verdaguer N., Gomez-Fernandez J.C. Structure of the C2 domain from novel protein kinase C epsilon. A membrane binding model for Ca(2+)-independent C2 domains. J. Mol. Biol. 2001, 311:837-849. 10.1006/jmbi.2001.4910.
11. Nalefski E.A., Falke J.J. The C2 domain calcium-binding motif: structural and functional diversity. Protein Sci. 1996, 5:2375-2390.
12. Medkova M., Cho W. Differential membrane-binding and activation mechanisms of protein kinase C-alpha and -epsilon. Biochemistry 1998, 37:4892-4900. 10.1021/bi972495j.
13. Bittova L., Sumandea M., Cho W. A structure-function study of the C2 domain of cytosolic phospholipase A2. Identification of essential calcium ligands and hydrophobic membrane binding residues. J. Biol. Chem. 1999, 274:9665-9672.
14. Cho W., Stahelin R.V. Membrane binding and subcellular targeting of C2 domains. Biochim. Biophys. Acta 2006, 1761:838-849. 10.1016/j.bbalip.2006.06.014.
15. Pappan K., Zheng S., Wang X. Identification and characterization of a novel plant phospholipase D that requires polyphosphoinositides and submicromolar calcium for activity in Arabidopsis. J. Biol. Chem. 1997, 272:7048-7054.
16. Pappan K., Qin W., Dyer J.H., Zheng L., Wang X. Molecular cloning and functional analysis of polyphosphoinositide-dependent phospholipase D, PLDbeta, from Arabidopsis. J. Biol. Chem. 1997, 272:7055-7061.
17. Zheng L., Krishnamoorthi R., Zolkiewski M., Wang X. Distinct Ca2+ binding properties of novel C2 domains of plant phospholipase D alpha and beta. J. Biol. Chem. 2000, 275:19700-19706. 10.1074/jbc.M001945200.
18. Whitaker B.D., Smith D.L., Green K.C. Cloning, characterization and functional expression of a phospholipase D alpha cDNA from tomato fruit. Physiol. Plant 2001, 112:87-94.
19. Yuan H., Chen L., Paliyath G., Sullivan A., Murr D.P. Characterization of microsomal and mitochondrial phospholipase D activities and cloning of a phospholipase D alpha cDNA from strawberry fruits. Plant Physiol. Biochem. 2005, 43:535-547. 10.1016/j.plaphy.2005.04.003.
20. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
21. Nalefski E.A., Slazas M.M., Falke J.J. Ca2+-signaling cycle of a membrane-docking C2 domain. Biochemistry 1997, 36:12011-12018. 10.1021/bi9717340.
22. Davletov B., Perisic O., Williams R.L. Calcium-dependent membrane penetration is a hallmark of the C2 domain of cytosolic phospholipase A2 whereas the C2A domain of synaptotagmin binds membranes electrostatically. J. Biol. Chem. 1998, 273:19093-19096.
23. Nalefski E.A., McDonagh T., Somers W., Seehra J., Falke J.J., Clark J.D. Independent folding and ligand specificity of the C2 calcium-dependent lipid binding domain of cytosolic phospholipase A2. J. Biol. Chem. 1998, 273:1365-1372.
24. Paliyath G., Lynch D.V., Thompson J.E. Regulation of membrane phospholipid catabolism in senescing carnation flowers. Physiol. Plantarum 1987, 71:503-511.
25. Paliyath G., Thompson J.E. Calcium- and calmodulin-regulated breakdown of phospholipid by microsomal membranes from bean cotyledons. Plant Physiol. 1987, 83:63-68.
26. Murray D., Honig B. Electrostatic control of the membrane targeting of C2 domains. Mol. Cell 2002, 9:145-154.
27. Kohout S.C., Corbalan-Garcia S., Torrecillas A., Gomez-Fernandez J.C., Falke J.J. C2 domains of protein kinase C isoforms alpha, beta, and gamma: activation parameters and calcium stoichiometries of the membrane-bound state. Biochemistry 2002, 41:11411-11424.
28. Wang Y., Geer L.Y., Chappey C., Kans J.A., Bryant S.H. Cn3D: sequence and structure views for Entrez. Trends Biochem. Sci. 2000, 25:300-302.
29. Evans J.H., Gerber S.H., Murray D., Leslie C.C. The calcium binding loops of the cytosolic phospholipase A2 C2 domain specify targeting to golgi and ER in live cells. Mol. Biol. Cell 2004, 15:371-383. 10.1091/mbc.E03-05-0338.
30. Guerrero-Valero M., Ferrer-Orta C., Querol-Audi J., Marin-Vicente C., Fita I., Gomez-Fernandez J.C., Verdaguer N., Corbalan-Garcia S. Structural and mechanistic insights into the association of PKC alpha-C2 domain to PtdIns(4,5)P2. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:6603-6607. 10.1073/pnas.0813099106.
31. Kelley L.A., Sternberg M.J. Protein structure prediction on the web: a case study using the Phyre server. Nat. Protoc 2009, 4:363-371. 10.1038/nprot.2009.2.
32. Zhang Y. I-TASSER: fully automated protein structure prediction in CASP8. Proteins 2009, 77(Suppl. 9):100-113. 10.1002/prot.22588.
33. Hopp T.P., Woods K.R. Prediction of protein antigenic determinants from amino acid sequences. Proc. Natl. Acad. Sci. U.S.A. 1981, 78:3824-3828.
34. Jo S., Vargyas M., Vasko-Szedlar J., Roux B., Im W. PBEQ-Solver for online visualization of electrostatic potential of biomolecules. Nucleic Acids Res. 2008, 36:W270-W275. 10.1093/nar/gkn314.
35. Li M., Hong Y., Wang X. Phospholipase D- and phosphatidic acid-mediated signaling in plants. Biochim. Biophys. Acta 2009, 1791:927-935. 10.1016/j.bbalip.2009.02.017.
36. Kudla J., Batistic O., Hashimoto K. Calcium signals: the lead currency of plant information processing. Plant Cell 2010, 22:541-563. 10.1105/tpc.109.072686.
37. Laxalt A.M., ter Riet B., Verdonk J.C., Parigi L., Tameling W.I., Vossen J., Haring M., Musgrave A., Munnik T. Characterization of five tomato phospholipase D cDNAs: rapid and specific expression of LePLDbeta1 on elicitation with xylanase. Plant J 2001, 26:237-247.
38. Testerink C., Larsen P.B., van der Does D., van Himbergen J.A., Munnik T. Phosphatidic acid binds to and inhibits the activity of Arabidopsis CTR1. J. Exp. Bot. 2007, 58:3905-3914. 10.1093/jxb/erm243.
39. Wang X., Xu L., Zheng L. Cloning and expression of phosphatidylcholine-hydrolyzing phospholipase D from Ricinus communis L. J. Biol. Chem. 1994, 269:20312-20317.
40. Hénaut A., Danchin A. Analysis and predictions from Escherichia coli sequences in: Escherichia coli and Salmonella. Escherichia coli and Salmonella, Cellular and Molecular Biology 1996, 2047. ASM Press, Washington, D.C. F.C. Neidhardt (Ed.).
41. Stahelin R.V., Digman M.A., Medkova M., Ananthanarayanan B., Melowic H.R., Rafter J.D., Cho W. Diacylglycerol-induced membrane targeting and activation of protein kinase C epsilon: mechanistic differences between protein kinases C delta and epsilon. J. Biol. Chem. 2005, 280:19784-19793. 10.1074/jbc.M411285200.
42. DeLano W.L. The PyMOL molecular graphics system on world wide web http://www.pymol.org.
43. Zhang X., Rizo J., Sudhof T.C. Mechanism of phospholipid binding by the C2A-domain of synaptotagmin I. Biochemistry 1998, 37:12395-12403. 10.1021/bi9807512.
44. Nalefski E.A., Wisner M.A., Chen J.Z., Sprang S.R., Fukuda M., Mikoshiba K., Falke J.J. C2 domains from different Ca2+ signaling pathways display functional and mechanistic diversity. Biochemistry 2001, 40:3089-3100.
45. Stahelin R.V., Rafter J.D., Das S., Cho W. The molecular basis of differential subcellular localization of C2 domains of protein kinase C-alpha and group IV a cytosolic phospholipase A2. J. Biol. Chem. 2003, 278:12452-12460. 10.1074/jbc.M212864200.
46. Ananthanarayanan B., Das S., Rhee S.G., Murray D., Cho W. Membrane targeting of C2 domains of phospholipase C-delta isoforms. J. Biol. Chem. 2002, 277:3568-3575. 10.1074/jbc.M109705200.
47. Guerrero-Valero M., Marin-Vicente C., Gomez-Fernandez J.C., Corbalan-Garcia S. The C2 domains of classical PKCs are specific PtdIns(4,5)P2-sensing domains with different affinities for membrane binding. J. Mol. Biol. 2007, 371:608-621. 10.1016/j.jmb.2007.05.086.
48. Corbalan-Garcia S., Garcia-Garcia J., Rodriguez-Alfaro J.A., Gomez-Fernandez J.C. A new phosphatidylinositol 4,5-bisphosphate-binding site located in the C2 domain of protein kinase C alpha. J. Biol. Chem. 2003, 278:4972-4980. 10.1074/jbc.M209385200.
49. Liu L., Song X., He D., Komma C., Kita A., Virbasius J.V., Huang G., Bellamy H.D., Miki K., Czech M.P., Zhou G.W. Crystal structure of the C2 domain of class II phosphatidylinositide 3-kinase C2 alpha. J. Biol. Chem. 2006, 281:4254-4260. 10.1074/jbc.M510791200.
50. Li L., Shin O.H., Rhee J.S., Arac D., Rah J.C., Rizo J., Sudhof T., Rosenmund C. Phosphatidylinositol phosphates as co-activators of Ca2+ binding to C2 domains of synaptotagmin 1. J. Biol. Chem. 2006, 281:15845-15852. 10.1074/jbc.M600888200.
51. Bradshaw J.P., Bushby R.J., Giles C.C., Saunders M.R. Orientation of the headgroup of phosphatidylinositol in a model biomembrane as determined by neutron diffraction. Biochemistry 1999, 38:8393-8401. 10.1021/bi990338.
52. White P.J., Broadley M.R. Calcium in plants. Ann. Bot. 2003, 92:487-511.
53. Paliyath G., Thompson J.E. Senescence-related changes in ATP-dependent uptake of calcium into microsomal vesicles from carnation petals. Plant Physiol. 1988, 88:295-302.
54. Kuppe K., Kerth A., Blume A., Ulbrich-Hofmann R. Calcium-induced membrane microdomains trigger plant phospholipase D activity. Chembiochem 2008, 9:2853-2859. 10.1002/cbic.200800431.
55. Lakowicz J.R. Principles of Fluorescence Spectroscopy 1983, Plenum Press, New York.
56. Haseloff J., Siemering K.R., Prasher D.C., Hodge S. Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:2122-2127.
57. Weigel D., Glazebrook J. Arabidopsis: A Laboratory Manual 2002, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.