Mechanism of specific membrane targeting by C2 domains: Localized pools of target lipids enhance Ca2+ affinity

Biochemistry

Volumn 46, Issue 14, 2007, Pages 4322-4336

  Corbin, John A ^a,b   Evans, John H ^a   Landgraf, Kyle E ^a   Falke, Joseph J ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b Xoma LLC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM COMPOUNDS; CHEMICAL BONDS; LIGANDS; LIPIDS; MOLECULAR DYNAMICS; PROTEINS;

EUKARYOTIC SIGNALING PROTEINS; FUNCTIONAL DIVERSITY; PROTEIN KINASE; PROTEIN SIGNALING MOTIFS;

BIOLOGICAL MEMBRANES;

CALCIUM ION; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLSERINE; PHOSPHOLIPASE A2; TRIPHOSPHOINOSITIDE;

ARTICLE; CALCIUM BINDING; CELL KINETICS; CELL MEMBRANE; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN TARGETING; REGULATORY MECHANISM; SECOND MESSENGER; SIGNAL TRANSDUCTION;

ANIMALS; CALCIUM; CALCIUM SIGNALING; CELL LINE; CELL MEMBRANE; CYTOSOL; FLUORESCENT DYES; GLUTATHIONE TRANSFERASE; KINETICS; LIPID METABOLISM; MACROPHAGES; MICE; PHOSPHATIDYLCHOLINES; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PHOSPHATIDYLSERINES; PHOSPHOLIPASES A; PROTEIN KINASE C-ALPHA; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; SPECTROMETRY, FLUORESCENCE;

EUKARYOTA; RUMEX;

EID: 34147167641     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi062140c     Document Type: Article

References (70)

1. Letunic, I., Copley, R. R., Schmidt, S., Ciccarelli, F. D., Doerks, T., Schultz, J., Ponting, C. P., and Bork, P. (2004) SMART 4.0: towards genomic data integration, Nucleic Acids Res. 32, D142-D144.
2. Nalefski, E. A., and Falke, J. J. (1996) The C2 domain calcium-binding motif: structural and functional diversity, Protein Sci. 5, 2375-2390.
3. Hurley, J. H. (2006) Membrane binding domains, Biochim. Biophys. Acta 1761, 805-811.
4. Cho, W., and Stahelin, R. V. (2006) Membrane binding and subcellular targeting of C2 domains, Biochim. Biophys. Acta 1761, 838-849.
5. Corbalan-Garcia, S., and Gomez-Fernandez, J. C. (2006) Protein kinase C regulatory domains: the art of decoding many different signals in membranes, Biochim. Biophys. Acta 1761, 633-654.
6. Benes, C. H., Wu, N., Elia, A. E., Dharia, T., Cantley, L. C., and Soltoff, S. P. (2005) The C2 domain of PKCdelta is a phosphotyrosine binding domain, Cell 121, 271-280.
7. Murray, D., and Honig, B. (2002) Electrostatic control of the membrane targeting of C2 domains, Mol. Cell 9, 145-154.
8. Hui, E., Bai, J., and Chapman, E. R. (2006) Ca2+-triggered simultaneous membrane penetration of the tandem C2-domains of synaptotagmin I, Biophys. J. 91, 1767-1777.
9. Davis, A. F., Bai, J., Fasshauer, D., Wolowick, M. J., Lewis, J. L., and Chapman, E. R. (1999) Kinetics of synaptotagmin responses to Ca2+ and assembly with the core SNARE complex onto membranes, Neuron 24, 363-376.
10. Nalefski, E. A., Wisner, M. A., Chen, J. Z., Sprang, S. R., Fukuda, M., Mikoshiba, K., and Falke, J. J. (2001) C2 domains from different Ca2+ signaling pathways display functional and mechanistic diversity, Biochemistry 40, 3089-3100.
11. Torrecillas, A., Corbalan-Garcia, S., and Gomez-Fernandez, J. C. (2003) Structural study of the C2 domains of the classical PKC isoenzymes using infrared spectroscopy and two-dimensional infrared correlation spectroscopy, Biochemistry 42, 11669-16681.
12. Stahelin, R. V., Rafter, J. D., Das, S., and Cho, W. (2003) The molecular basis of differential subcellular localization of C2 domains of protein kinase C-alpha and group IVa cytosolic phospholipase A2, J. Biol. Chem. 278, 12452-12460.
13. Evans, J. H., Gerber, S. H., Murray, D., and Leslie, C. C. (2004) The calcium binding loops of the cytosolic phospholipase A2 C2 domain specify targeting to Golgi and ER in live cells, Mol. Biol. Cell 15, 371-383.
14. Torrecillas, A., Laynez, J., Menendez, M., Corbalan-Garcia, S., and Gomez-Fernandez, J. C. (2004) Calorimetric study of the interaction of the C2 domains of classical protein kinase C isoenzymes with Ca2+ and phospholipids, Biochemistry 43, 11727-11739.
15. 2, J. Biol. Chem. 273, 1596-1604.
16. Sutton, R. B., and Sprang, S. R. (1998) Structure of the protein kinase Cbeta phospholipid-binding C2 domain complexed with Ca2+, Structure 6, 1395-13405.
17. 2, J. Mol. Biol. 280, 485-500.
18. 2 reveals a novel topology and catalytic mechanism, Cell 97, 349-360.
19. Verdaguer, N., Corbalan-Garcia, S., Ochoa, W. F., Fita, I., and Gomez-Fernandez, J. C. (1999) Ca(2+) bridges the C2 membrane-binding domain of protein kinase Calpha directly to phosphatidylserine, EMBO J. 18, 6329-6338.
20. 2+-independent catalytic domain, J. Biol. Chem. 269, 18239-18249.
21. Edwards, A. S., and Newton, A. C. (1997) Regulation of protein kinase C βII by its C2 domain, Biochemistry 36, 15615-15623.
22. Newton, A. C. (2001) Protein kinase C: structural and spatial regulation by phosphorylation, cofactors, and macromolecular interactions, Chem. Rev. 101, 2353-2364.
23. Kohout, S. C., Corbalan-Garcia, S., Torrecillas, A., Gomez-Fernandez, J. C., and Falke, J. J. (2002) C2 domains of protein kinase C isoforms alpha, beta, and gamma: activation parameters and calcium stoichiometries of the membrane-bound state, Biochemistry 41, 11411-11424.
24. Corbalan-Garcia, S., Garcia-Garcia, J., Rodriguez-Alfaro, J. A., and Gomez-Fernandez, J. C. (2003) A new phosphatidylinositol 4,5-bisphosphate- binding site located in the C2 domain of protein kinase Calpha, J. Biol. Chem. 278, 4972-4980.
25. Rodriguez-Alfaro, J. A., Gomez-Fernandez, J. C., and Corbalan-Garcia, S. (2004) Role of the lysine-rich cluster of the C2 domain in the phosphatidylserine-dependent activation of PKCalpha, J. Mol. Biol. 335, 1117-1129.
26. Marin-Vicente, C., Gomez-Fernandez, J. C., and Corbalan-Garcia, S. (2005) The ATP-dependent membrane localization of protein kinase Calpha is regulated by Ca2+ influx and phosphatidylinositol 4,5-bisphosphate in differentiated PC12 cells, Mol. Biol. Cell 16, 2848-2861.
27. Evans, J. H., Murray, D., Leslie, C. C., and Falke, J. J. (2006) Specific translocation of protein kinase Calpha to the plasma membrane requires both Ca2+ and PIP2 recognition by its C2 domain, Mol. Biol. Cell 17, 56-66.
28. Sanchez-Bautista, S., Marin-Vicente, C., Gomez-Fernandez, J. C., and Corbalan-Garcia, S. (2006) The C2 Domain of PKCalpha is a Ca(2+)-dependent PtdIns(4,5)P(2) sensing domain: a new insight into an old pathway, J. Mol. Biol. 362, 901-914.
29. Kohout, S. C., Corbalan-Garcia, S., Gomez-Fernandez, J. C., and Falke, J. J. (2003) C2 domain of protein kinase calpha: elucidation of the membrane docking surface by site-directed fluorescence and spin labeling, Biochemistry 42, 1254-1265.
30. Malmberg, N. J., and Falke, J. J. (2005) Use of EPR power saturation to analyze the membrane-docking geometries of peripheral proteins: applications to C2 domains, Annu. Rev. Biophys. Biomol. Struct. 34, 71-90.
31. Oancea, E., and Meyer, T. (1998) Protein kinase C as a molecular machine for decoding calcium and diacylglycerol signals, Cell 95, 307-318.
32. Nalefski, E. A., and Newton, A. C. (2001) Membrane binding kinetics of protein kinase C betaII mediated by the C2 domain, Biochemistry 40, 13216-13229.
33. Allen, L. H., and Aderem, A. (1995) A role for MARCKS, the alpha isozyme of protein kinase C and myosin I in zymosan phagocytosis by macrophages, J. Exp. Med. 182, 829-840.
34. Mineo, C., Ying, Y. S., Chapline, C., Jaken, S., and Anderson, R. G. (1998) Targeting of protein kinase Calpha to caveolae, J. Cell Biol. 141, 601-610.
35. Rucei, N., Digiacinto, C., Orni, L., Millimaggi, D., Baron, R., and Teti, A. (2005) A novel protein kinase C {alpha}-dependent signal to ERK1/2 activated by {alpha}V{beta}3 integrin in osteoclasts and in Chinese hamster ovary (CHO) cells, J. Cell. Sci. 118, 3263-3275.
36. Cai, L., Holoweckyj, N., Schaller, M. D., and Bear, J. E. (2005) Phosphorylation of coronin 1B by protein kinase C regulates interaction with Arp2/3 and cell motility, J Biol. Chem. 280, 31913-31923.
37. McLaughlin, S., and Murray, D. (2005) Plasma membrane phosphoinositide organization by protein electrostatics, Nature 438, 605-611.
38. Levitan, I. B. (2006) Signaling protein complexes associated with neuronal ion channels, Nat. Neurosci. 9, 305-310.
39. Tao, J., Shumay, E., McLaughlin, S., Wang, H. Y., and Malbon, C. C. (2006) Regulation of AKAP-membrane interactions by calcium, J. Biol. Chem. 281, 23932-23944.
40. Newton, A. C. (1995) Protein kinase C. Seeing two domains, Curr. Biol. 5, 973-976.
41. Teruel, M. N., and Meyer, T. (2002) Parallel single-cell monitoring of receptor-triggered membrane translocation of a calcium-sensing protein module, Science 295, 1910-1912.
42. Bolsover, S. R., Gomez-Fernandez, J. C., and Corbalan-Garcia, S. (2003) Role of the Ca2+/phosphatidylserine binding region of the C2 domain in the translocation of protein kinase Calpha to the plasma membrane, J. Biol. Chem. 278, 10282-10290.
43. Alonso, F., Henson, P. M., and Leslie, C. C. (1986) A cytosolic phospholipase in human neutrophils that hydrolyzes arachidonoyl-containing phosphatidylcholine, Biochim. Biophys. Acta 878, 273-280.
44. 2, J. Lipid Mediators Cell Signalling 12, 83-117.
45. 2+-signaling cycle of a membrane-docking C2 domain, Biochemistry 36, 12011-12018.
46. 2 from cytosol to the nuclear envelope in rat basophilic leukemia cells stimulated with calcium ionophore or IgE/antigen, J. Biol. Chem. 270, 15359-15367.
47. 2, J. Biol. Chem. 274, 14979-14987.
48. 2, Biochemistry 37, 17642-17650.
49. Frazier, A. A., Wisner, M. A., Malmberg, N. J., Victor, K. G., Fanucci, G. E., Nalefski, E. A., Falke, J. J., and Cafiso, D. S. (2002) Membrane orientation and position of the C2 domain from cPLA2 by site-directed spin labeling. (The erratum appears in Biochemistry (2002) Jun 11, 41, 7528.), Biochemistry 41, 6282-6292.
50. Malmberg, N. J., Van Buskirk, D. R., and Falke, J. J. (2003) Membrane-docking loops of the cPLA2 C2 domain: detailed structural analysis of the protein-membrane interface via site-directed spin-labeling, Biochemistry 42, 13227-13240.
51. Evans, J. H., and Leslie, C. C. (2004) The cytosolic phospholipase A2 catalytic domain modulates association and residence time at Golgi membranes, J. Biol. Chem. 279, 6005-6016.
52. 2, J. Biol. Chem. 273, 1365-1372.
53. Berridge, M. J. (1993) Inositol trisphosphate and calcium signalling, Nature 361, 315-325.
54. Griffiths, G., Warren, G., Quinn, P., Mathieu-Costello, O., and Hoppeler, H. (1984) Density of newly synthesized plasma membrane proteins in intracellular membranes. I. Stereological studies, J. Cell Biol. 98, 2133-2141.
55. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature 227, 680-685.
56. Copeland, R. A. (1994) Methods for Protein Analysis: A Practical Guide to Laboratory Protocols, Chapman and Hall, New York.
57. Corbalan-Garcia, S., Rodríguez-Alfaro, J. A., and Gómez-Fernández, J. C. (1999) Determination of the calcium-binding sites of the C2 domain of protein kinase Cα that are critical for its translocation to the plasma membrane, Biochem. J. 337, 513-521.
58. Evans, J. H., Spencer, D. M., Zweifach, A., and Leslie, C. C. (2001) Intracellular calcium signals regulating cytosolic phospholipase A2 translocation to internal membranes, J. Biol. Chem. 276, 30150-30160.
59. 2, J. Biol. Chem. 274, 5163-5169.
60. van Meer, G. (1998) Lipids of the Golgi membrane, Trends Cell Biol. 8, 29-33.
61. Vance, D. E., and Vance, J. E. (2002), Biochemistry of Lipids, Lipoproteins, and Membranes, Elsevier Science, Burlington, MA.
62. Hope, H. R., and Pike, L. J. (1996) Phosphoinositides and phosphoinositide-utilizing enzymes in detergent-insoluble lipid domains, Mol. Biol. Cell 7, 843-51.
63. Laux, T., Fukami, K., Thelen, M., Golub, T., Frey, D., and Caroni, P. (2000) GAP43, MARCKS, and CAP23 modulate PI(4,5)P(2) at plasmalemmal rafts, and regulate cell cortex actin dynamics through a common mechanism, J. Cell Biol. 149, 1455-1472.
64. Caroni, P. (2001) New EMBO members' review: actin cytoskeleton regulation through modulation of PI(4,5)P(2) rafts, EMBO. J. 20, 4332-4336.
65. Golub, T., and Caroni, P. (2005) PI(4,5)P2-dependent microdomain assemblies capture microtubules to promote and control leading edge motility, J. Cell Biol. 169, 151-165.
66. VanScyoc, W. S., Sorensen, B. R., Rusinova, E., Laws, W. R., Ross, J. B., and Shea, M. A. (2002) Calcium binding to calmodulin mutants monitored by domain-specific intrinsic phenylalanine and tyrosine fluorescence, Biophys J. 83, 2767-2780.
67. Vetter, S. W., and Leclerc, E. (2003) Novel aspects of calmodulin target recognition and activation, Eur. J. Biochem. 270, 404-414.
68. Ishida, H., and Vogel, H. J. (2006) Protein-peptide interaction studies demonstrate the versatility of calmodulin target protein binding, Protein Pept. Lett. 13, 455-465.
69. Peersen, O. B., Madsen, T. S., and Falke, J. J. (1997) Intermolecular tuning of calmodulin by target peptides and proteins: differential effects on Ca2+ binding and implications for kinase activation, Protein Sci. 6, 794-807.
70. Ron, D., Luo, J., and Mochly-Rosen, D. (1995) C2 region-derived peptides inhibit translocation and function of β protein kinase C in vivo J. Biol. Chem. 270, 24180-24187.