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PMID: 11891256 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S.

An Arabidopsis calcium-dependent protein kinase is associated with the endoplasmic reticulum.

Plant physiology ·Vol. 128 ·No. 3 ·2002-03-00 ·Pages 1008-21

Lu SX, Hrabak EM

Abstract

Arabidopsis contains 34 genes that are predicted to encode calcium-dependent protein kinases (CDPKs). CDPK enzymatic activity previously has been detected in many locations in plant cells, including the cytosol, the cytoskeleton, and the membrane fraction. However, little is known about the subcellular locations of individual CDPKs or the mechanisms involved in targeting them to those locations. We investigated the subcellular location of one Arabidopsis CDPK, AtCPK2, in detail. Membrane-associated AtCPK2 did not partition with the plasma membrane in a two-phase system. Sucrose gradient fractionation of microsomes demonstrated that AtCPK2 was associated with the endoplasmic reticulum (ER). AtCPK2 does not contain transmembrane domains or known ER-targeting signals, but does have predicted amino-terminal acylation sites. AtCPK2 was myristoylated in a cell-free extract and myristoylation was prevented by converting the glycine at the proposed site of myristate attachment to alanine (G2A). In plants, the G2A mutation decreased AtCPK2 membrane association by approximately 50%. A recombinant protein, consisting of the first 10 amino acids of AtCPK2 fused to the amino-terminus of beta-glucuronidase, was also targeted to the ER, indicating that the amino terminus of AtCPK2 can specify ER localization of a soluble protein. These results indicate that AtCPK2 is localized to the ER, that myristoylation is likely to be involved in the membrane association of AtCPK2, and that the amino terminal region of AtCPK2 is sufficient for correct membrane targeting.

MeSH Terms
Animals Arabidopsis/enzymology,genetics Arabidopsis Proteins/genetics,metabolism Calcium/metabolism Calcium-Binding Proteins/genetics,metabolism Cloning, Molecular DNA, Plant/chemistry,genetics Endoplasmic Reticulum/enzymology Female Gene Expression Regulation, Enzymologic Gene Expression Regulation, Plant Glucuronidase/genetics,metabolism Membrane Proteins/genetics,metabolism Molecular Sequence Data Mutation Myristic Acid/metabolism Plant Proteins Plants, Genetically Modified Protein Kinases/genetics,metabolism Rabbits Recombinant Fusion Proteins/genetics,metabolism Sequence Analysis, DNA
Chemicals
ATCDPK2 protein, Arabidopsis Arabidopsis Proteins Calcium-Binding Proteins DNA, Plant Membrane Proteins Plant Proteins Recombinant Fusion Proteins Myristic Acid Protein Kinases Glucuronidase Calcium
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Lu Sheen X
Department of Plant Biology, University of New Hampshire, 46 College Road, Durham, New Hampshire 03824, USA.
Hrabak Estelle M
References (69)
69 references, click to expand
  1. Protein kinase activities in ripening mango, Mangifera indica L., fruit tissue. III. Purification and characterisation of a calcium-regulated protein kinase.
    Biochim Biophys Acta. 1998 Sep 8;1387(1-2):342-54 PMID: 9748649
  2. Fatty acylation of alpha z. Effects of palmitoylation and myristoylation on alpha z signaling.
    J Biol Chem. 1995 Apr 21;270(16):9667-75 PMID: 7536745
  3. Protein Kinases in Zucchini (Characterization of Calcium-Requiring Plasma Membrane Kinases).
    Plant Physiol. 1993 Oct;103(2):413-419 PMID: 12231949
  4. Lipid-dependent targeting of G proteins into rafts.
    J Biol Chem. 2000 Jan 21;275(3):2191-8 PMID: 10636925
  5. Specific and saturable binding of pp60v-src to plasma membranes: evidence for a myristyl-src receptor.
    Cell. 1989 Jul 28;58(2):281-6 PMID: 2546680
  6. Identification of a 32K plasma membrane protein that binds to the myristylated amino-terminal sequence of p60v-src.
    Nature. 1990 Jul 5;346(6279):84-6 PMID: 2164157
  7. Regulation of cellular signalling by fatty acid acylation and prenylation of signal transduction proteins.
    Cell Signal. 1996 Sep;8(6):403-12 PMID: 8958442
  8. N-myristylation of the catalytic subunit of cAMP-dependent protein kinase conveys structural stability.
    J Biol Chem. 1993 Feb 5;268(4):2348-52 PMID: 8428909
  9. Guard cells possess a calcium-dependent protein kinase that phosphorylates the KAT1 potassium channel.
    Plant Physiol. 1998 Feb;116(2):785-95 PMID: 9489023
  10. Characterization of the major integral protein of vacuolar membrane.
    Plant Physiol. 1992 Apr;98(4):1248-54 PMID: 16668783
  11. The biology and enzymology of eukaryotic protein acylation.
    Annu Rev Biochem. 1988;57:69-99 PMID: 3052287
  12. The plasma-membrane H(+)-ATPase from beet root is inhibited by a calcium-dependent phosphorylation.
    Planta. 1998 Mar;204(3):352-9 PMID: 9530879
  13. Purification of a nitrate reductase kinase from Spinacea oleracea leaves, and its identification as a calmodulin-domain protein kinase.
    Planta. 1998 Oct;206(3):435-42 PMID: 9763711
  14. Calcium and lipid regulation of an Arabidopsis protein kinase expressed in Escherichia coli.
    Biochemistry. 1993 Apr 6;32(13):3282-90 PMID: 7916621
  15. Relocation of a Ca2+-dependent protein kinase activity during pollen tube reorientation
    Plant Cell. 1998 Sep;10(9):1499-510 PMID: 9724696
  16. Phosphorylation of serine-15 of maize leaf sucrose synthase. Occurrence in vivo and possible regulatory significance.
    Plant Physiol. 1996 Oct;112(2):793-802 PMID: 8883390
  17. Use of a gene expression system based on potato virus X to rapidly identify and characterize a tomato Pto homolog that controls fenthion sensitivity.
    Plant Cell. 1995 Mar;7(3):249-57 PMID: 7734960
  18. Analysis of the H(+)-ATPase and other proteins of the Arabidopsis plasma membrane.
    Methods Cell Biol. 1995;50:129-48 PMID: 8531789
  19. Characterization of a calcium- and lipid-dependent protein kinase associated with the plasma membrane of oat.
    Biochemistry. 1992 Feb 18;31(6):1721-7 PMID: 1737026
  20. Doubly-lipid-modified protein sequence motifs exhibit long-lived anchorage to lipid bilayer membranes.
    Biochemistry. 1995 Mar 21;34(11):3813-22 PMID: 7893678
  21. Identification of a calmodulin-regulated Ca2+-ATPase in the endoplasmic reticulum.
    Plant Physiol. 1999 Apr;119(4):1165-76 PMID: 10198075
  22. Identification of the calmodulin-binding domain of neuron-specific protein kinase C substrate protein CAP-22/NAP-22. Direct involvement of protein myristoylation in calmodulin-target protein interaction.
    J Biol Chem. 1999 Apr 23;274(17):11848-53 PMID: 10207003
  23. Partial purification and characterization of a Ca(2+)-dependent protein kinase from pea nuclei.
    Plant Physiol. 1991;96:720-7 PMID: 11538005
  24. Alkali treatment for rapid preparation of plant material for reliable PCR analysis.
    Plant J. 1993 Mar;3(3):493-4 PMID: 8220456
  25. Cloning, expression and N-terminal myristoylation of CpCPK1, a calcium-dependent protein kinase from zucchini (Cucurbita pepo L.).
    Plant Mol Biol. 1999 Jan;39(2):199-208 PMID: 10080688
  26. Lipid-linked proteins of plants.
    Prog Lipid Res. 2000 Jan;39(1):19-39 PMID: 10729606
  27. Understanding covalent modifications of proteins by lipids: where cell biology and biophysics mingle.
    Trends Cell Biol. 1997 Jan;7(1):14-20 PMID: 17708893
  28. The amino-terminal nine amino acid sequence of poliovirus capsid VP4 protein is sufficient to confer N-myristoylation and targeting to detergent-insoluble membranes.
    Biochemistry. 2000 Feb 8;39(5):1083-90 PMID: 10653654
  29. Calcium-Dependent Protein Phosphorylation May Mediate the Gibberellic Acid Response in Barley Aleurone
    Plant Physiol. 1998 Feb 1;116(2):765-76 PMID: 9490770
  30. Gene Expression and Signal Transduction in Water-Stress Response.
    Plant Physiol. 1997 Oct;115(2):327-334 PMID: 12223810
  31. Changes in Calcium-Dependent Protein Kinase Activity during in Vitro Tuberization in Potato.
    Plant Physiol. 1996 Dec;112(4):1541-1550 PMID: 12226463
  32. Specialized binary vector for plant transformation: expression of the Arabidopsis thaliana AHAS gene in Nicotiana tabacum.
    Nucleic Acids Res. 1988 Nov 25;16(22):10765-82 PMID: 3060849
  33. Functional roles for fatty acylated amino-terminal domains in subcellular localization.
    Mol Biol Cell. 1999 Nov;10(11):3771-86 PMID: 10564270
  34. Kinetic and calcium-binding properties of three calcium-dependent protein kinase isoenzymes from soybean.
    Biochemistry. 1998 May 12;37(19):6801-9 PMID: 9578565
  35. Protein lipidation in cell signaling.
    Science. 1995 Apr 14;268(5208):221-5 PMID: 7716512
  36. Characterization of a calcium-dependent protein kinase from Arachis hypogea (groundnut) seeds.
    Plant Physiol. 1994 Mar;104(3):961-9 PMID: 8165262
  37. A calcium-dependent protein kinase can inhibit a calmodulin-stimulated Ca2+ pump (ACA2) located in the endoplasmic reticulum of Arabidopsis.
    Proc Natl Acad Sci U S A. 2000 May 23;97(11):6224-9 PMID: 10823962
  38. Immunocytological localization of an epitope-tagged plasma membrane proton pump (H(+)-ATPase) in phloem companion cells.
    Plant Cell. 1995 Dec;7(12):2053-67 PMID: 8718619
  39. 11-(Ethylthio)undecanoic acid. A myristic acid analogue of altered hydrophobicity which is functional for peptide N-myristoylation with wheat germ and yeast acyltransferase.
    J Biol Chem. 1988 Feb 15;263(5):2127-33 PMID: 3123489
  40. Contributions of myristoylation to calcineurin structure/function.
    J Biol Chem. 1996 Oct 25;271(43):26517-21 PMID: 8900120
  41. The Polyadenylation of RNA in Plants.
    Plant Physiol. 1997 Oct;115(2):321-325 PMID: 12223809
  42. Characterization of a calcium-dependent protein kinase of tobacco leaves that is associated with the plasma membrane and is inducible by sucrose.
    Plant Cell Physiol. 1998 Nov;39(11):1176-83 PMID: 9891416
  43. Protein myristoylation in protein-lipid and protein-protein interactions.
    Biophys Chem. 1999 Dec 13;82(2-3):129-37 PMID: 10631796
  44. Resistance gene-dependent activation of a calcium-dependent protein kinase in the plant defense response.
    Plant Cell. 2000 May;12(5):803-16 PMID: 10810151
  45. CDPKs - a kinase for every Ca2+ signal?
    Trends Plant Sci. 2000 Apr;5(4):154-9 PMID: 10740296
  46. Molecular cloning, genomic organization, and biochemical characterization of myristoyl-CoA:protein N-myristoyltransferase from Arabidopsis thaliana.
    J Biol Chem. 2000 Mar 31;275(13):9673-83 PMID: 10734119
  47. New vectors for high level expression of recombinant proteins in bacteria.
    Anal Biochem. 1992 May 1;202(2):293-8 PMID: 1519755
  48. The dynamic role of palmitoylation in signal transduction.
    Trends Biochem Sci. 1995 May;20(5):181-7 PMID: 7610481
  49. A rice membrane calcium-dependent protein kinase is induced by gibberellin.
    Plant Physiol. 1995 Jun;108(2):787-93 PMID: 7610167
  50. N-terminal fatty acylation of the alpha-subunit of the G-protein Gi1: only the myristoylated protein is a substrate for palmitoylation.
    Biochem J. 1994 Nov 1;303 ( Pt 3):697-700 PMID: 7980434
  51. A knowledge base for predicting protein localization sites in eukaryotic cells.
    Genomics. 1992 Dec;14(4):897-911 PMID: 1478671
  52. Le calcium, C'est la vie: calcium makes waves
    Plant Physiol. 1999 May;120(1):1-6 PMID: 10318677
  53. Genetic and biochemical studies of protein N-myristoylation.
    Annu Rev Biochem. 1994;63:869-914 PMID: 7979256
  54. Plasma membrane localization of G alpha z requires two signals.
    Mol Biol Cell. 1998 Jan;9(1):1-14 PMID: 9436987
  55. Calcium-activated protein kinase from soluble and membrane fractions of maize coleoptiles.
    Biochem Biophys Res Commun. 1990 Jul 16;170(1):17-22 PMID: 2372285
  56. p59fyn tyrosine kinase associates with multiple T-cell receptor subunits through its unique amino-terminal domain.
    Mol Cell Biol. 1992 Dec;12(12):5438-46 PMID: 1448076
  57. Biochemical Similarities between Soluble and Membrane-Bound Calcium-Dependent Protein Kinases of Barley.
    Plant Physiol. 1990 Apr;92(4):919-23 PMID: 16667406
  58. Targeting of two Arabidopsis H(+)-ATPase isoforms to the plasma membrane.
    Plant Physiol. 1996 Oct;112(2):833-44 PMID: 8883393
  59. SOS3 function in plant salt tolerance requires N-myristoylation and calcium binding.
    Plant Cell. 2000 Sep;12(9):1667-78 PMID: 11006339
  60. Importance of the A-helix of the catalytic subunit of cAMP-dependent protein kinase for stability and for orienting subdomains at the cleft interface.
    Protein Sci. 1997 Mar;6(3):569-79 PMID: 9070439
  61. A novel chloride channel in Vicia faba guard cell vacuoles activated by the serine/threonine kinase, CDPK.
    EMBO J. 1996 Dec 2;15(23):6564-74 PMID: 8978683
  62. Purification and characterization of a novel calcium-dependent protein kinase from soybean.
    Biochemistry. 1990 Mar 13;29(10):2488-95 PMID: 2334677
  63. A novel calmodulin-regulated Ca2+-ATPase (ACA2) from Arabidopsis with an N-terminal autoinhibitory domain.
    J Biol Chem. 1998 Jan 9;273(2):1099-106 PMID: 9422775
  64. Failure to myristoylate the alpha subunit of Gz is correlated with an inhibition of palmitoylation and membrane attachment, but has no affect on phosphorylation by protein kinase C.
    J Biol Chem. 1994 Feb 11;269(6):4571-6 PMID: 8308028
  65. Agrobacterium tumefaciens-mediated transformation of Arabidopsis thaliana root explants by using kanamycin selection.
    Proc Natl Acad Sci U S A. 1988 Aug;85(15):5536-40 PMID: 16593964
  66. Phosphorylation of the plasma-membrane H(+)-ATPase of oat roots by a calcium-stimulated protein kinase.
    Planta. 1988 Dec;173(4):509-18 PMID: 24226688
  67. Heterodimerization between light-regulated and ubiquitously expressed Arabidopsis GBF bZIP proteins.
    EMBO J. 1992 Apr;11(4):1261-73 PMID: 1373374
  68. Membrane localization of a rice calcium-dependent protein kinase (CDPK) is mediated by myristoylation and palmitoylation.
    Plant J. 2000 Nov;24(4):429-35 PMID: 11115124
  69. Monoclonal Antibodies to the [alpha]- and [beta]-Subunits of the Plant Mitochondrial F1-ATPase.
    Plant Physiol. 1993 Mar;101(3):931-937 PMID: 12231744
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
0032-0889
Published
2002-03-00
Pages
1008-21
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC152213
Subset
IM
Databases
GENBANK
AF286222
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