The C2 Domains of Classical PKCs are Specific PtdIns(4,5)P2-sensing Domains with Different Affinities for Membrane Binding

Journal of Molecular Biology

Volumn 371, Issue 3, 2007, Pages 608-621

  Guerrero Valero, Marta ^a   Marín Vicente, Consuelo ^a   Gómez Fernández, Juan C ^a   Corbalán García, Senena ^a  

^a UNIVERSITY OF MURCIA   (Spain)

Author keywords

C2 domain; GFP; phosphatidylserine; PKC; PtdIns(4,5)P2

Indexed keywords

PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PROTEIN KINASE C ALPHA; PROTEIN KINASE C BETA; PROTEIN KINASE C GAMMA;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; IN VIVO STUDY; ISOTHERMAL TITRATION CALORIMETRY; MEMBRANE BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN;

EUKARYOTA;

EID: 34447647309     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.05.086     Document Type: Article

References (55)

1. Nishizuka Y. Protein kinase C and lipid signaling for sustained cellular responses. FASEB J. 9 (1995) 484-496
2. Newton A. Protein kinase C: Structural and spatial regulation by phosphorylation, cofactors, and macromolecular interactions. Chem. Rev. 101 (2001) 2353-2364
3. Ohno S., and Nishizuka Y. Protein kinase C isotypes and their specific functions: prologue. J. Biochem. (Tokyo) 132 (2002) 509-511
4. Hofmann J. The potential for isoenzyme-selective modulation of protein kinase C. FASEB J. 11 (1997) 649-669
5. Mellor H., and Parker P.J. The extended protein kinase C superfamily. Biochem. J. 332 (1998) 281-292
6. Newton A.C., and Johnson J.E. Protein kinase C: A paradigm for regulation of protein function by two membrane-targeting modules. Biochim. Biophys. Acta 1376 (1998) 155-172
7. Takai Y., Kishimoto A., Kikkawa U., Mori T., and Nishizuka Y. Unsaturated diacylglycerol as a possible messenger for the activation of calcium-activated, phospholipid-dependent protein kinase system. Biochem. Biophys. Res. Commun. 91 (1979) 1218-1224
8. Toker A. Signaling through protein kinase C. Front. Biosci. 3 (1998) 1134-1147
9. Martin T.F. Phosphoinositide lipids as signaling molecules: common themes for signal transduction, cytoskeletal regulation, and membrane trafficking. Annu. Rev. Cell Dev. Biol. 14 (1998) 231-264
10. Czech M.P. PIP2 and PIP3: complex roles at the cell surface. Cell 100 (2000) 603-606
11. Lemmon M.A. Phosphoinositide recognition domains. Traffic 4 (2003) 201-213
12. McLaughlin S., and Murray D. Plasma membrane phosphoinositide organization by protein electrostatics. Nature 438 (2005) 605-611
13. Di Paolo G., and De Camilli P. Phosphoinositides in cell regulation and membrane dynamics. Nature 443 (2006) 651-657
14. Nalefski E.A., and Falke J.J. The C2 domain calcium-binding motif: structural and functional diversity. Protein Sci. 5 (1996) 2375-2390
15. 2+-binding domain. J. Biol. Chem. 273 (1998) 15879-15882
16. Cho W., and Stahelin R.V. Membrane binding and subcellular targeting of C2 domains. Biochim. Biophys. Acta 1761 (2006) 838-849
17. Corbalan-Garcia S., and Gomez-Fernandez J.C. Protein kinase C regulatory domains: the art of decoding many different signals in membranes. Biochim. Biophys. Acta 1761 (2006) 633-654
18. Verdaguer N., Corbalan-Garcia S., Ochoa W., Gomez-Fernandez J., and Fita I. Membrane binding C2-like domains. In: Messerschmidt A., Bode W., and Cygler M. (Eds). Handbook of Metalloproteins (2004), John Wiley and Sons, New York 587-598
19. 2+. Structure 6 (1998) 1395-1405
20. Verdaguer N., Corbalan-Garcia S., Ochoa W., Fita I., and Gomez-Fernandez J. Ca(2+) bridges the C2 membrane-binding domain of protein kinase Calpha directly to phosphatidylserine. EMBO J. 18 (1999) 6329-6338
21. Ochoa W., Corbalan-Garcia S., Eritja R., Rodriguez-Alfaro J., Gomez-Fernandez J., Fita I., and Verdaguer N. Additional binding sites for anionic phospholipids and calcium ions in the crystal structures of complexes of the C2 domain of protein kinase calpha. J. Mol. Biol. 320 (2002) 277-291
22. Kohout S.C., Corbalan-Garcia S., Torrecillas A., Gomez-Fernandez J.C., and 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 41 (2002) 11411-11424
23. Kohout S.C., Corbalan-Garcia S., Gomez-Fernandez J.C., and Falke J.J. C2 domain of protein kinase C alpha: elucidation of the membrane docking surface by site-directed fluorescence and spin labeling. Biochemistry 42 (2003) 1254-1265
24. 2+ and phospholipids. Biochemistry 43 (2004) 11727-11739
25. Sanchez-Bautista S., Kazaks A., Beaulande M., Torrecillas A., Corbalan-Garcia S., and Gomez-Fernandez J.C. Structural study of the catalytic domain of PKCzeta using infrared spectroscopy and two-dimensional infrared correlation spectroscopy. FEBS J. 273 (2006) 3273-3286
26. Conesa-Zamora P., Gomez-Fernandez J., and Corbalan-Garcia S. The C2 domain of protein kinase calpha is directly involved in the diacylglycerol-dependent binding of the C1 domain to the membrane. Biochim. Biophys. Acta 1487 (2000) 246-254
27. Conesa-Zamora P., Lopez-Andreo M., Gomez-Fernandez J., and Corbalan-Garcia S. Identification of the phosphatidylserine binding site in the C2 domain that is important for PKC alpha activation and in vivo cell localization. Biochemistry 40 (2001) 13898-13905
28. Bolsover S., Gomez-Fernandez J., and Corbalan-Garcia S. 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 (2003) 10282-10290
29. Corbalan-Garcia S., Garcia-Garcia J., Rodriguez-Alfaro J., and Gomez-Fernandez J. A new phosphatidylinositol 4,5-bisphosphate-binding site located in the C2 domain of protein kinase Calpha. J. Biol. Chem. 278 (2003) 4972-4980
30. Rodriguez-Alfaro J., Gomez-Fernandez J., and Corbalan-Garcia S. Role of the lysine-rich cluster of the C2 domain in the phosphatidylserine-dependent activation of PKCalpha. J. Mol. Biol. 335 (2004) 1117-1129
31. Marin-Vicente C., Gomez-Fernandez J., and Corbalan-Garcia S. 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 (2005) 2848-2861
32. Evans J.H., Murray D., Leslie C.C., and Falke J.J. Specific translocation of protein kinase C{alpha} to the plasma membrane requires both Ca2+ and PIP2 recognition by its C2 domain. Mol. Biol. Cell 17 (2006) 56-66
33. Liu L., Song X., He D., Komma C., Kita A., Virbasius J., et al. Crystal structure of the C2 domain of class II phosphatidylinositide 3-kinase C2alpha. J. Biol. Chem. 281 (2005) 4254-4260
34. Schiavo G., Gu Q.M., Prestwich G.D., Sollner T.H., and Rothman J.E. Calcium-dependent switching of the specificity of phosphoinositide binding to synaptotagmin. Proc. Natl Acad. Sci. USA 93 (1996) 13327-13332
35. Bai J., Tucker W.C., and Chapman E.R. PIP2 increases the speed of response of synaptotagmin and steers its membrane-penetration activity toward the plasma membrane. Nature Struct. Mol. Biol. 11 (2004) 36-44
36. Li L., Shin O., Rhee J., Arac D., Rah J., Rizo J., et al. Phosphatidylinositolphosphates as coactivators of Ca2+-binding to C2-domains of synaptotagmin 1. J. Biol. Chem. 281 (2006) 15845-15852
37. 2+ affinity. Biochemistry 46 (2007) 4322-43236
38. 2+ signaling pathways display functional and mechanistic diversity. Biochemistry 40 (2001) 3089-3100
39. Medkova M., and Cho W. Interplay of C1 and C2 domains of protein kinase C-alpha in its membrane binding and activation. J. Biol. Chem. 274 (1999) 19852-19861
40. Torrecillas A., Corbalan-Garcia S., and Gomez-Fernandez J. Structural study of the C2 domains of the classical PKC isoenzymes using infrared spectroscopy and two-dimensional infrared correlation spectroscopy. Biochemistry 42 (2003) 11661-11668
41. Koreh K., and Monaco M.E. The relationship of hormone-sensitive and hormone-insensitive phosphatidylinositol to phosphatidylinositol 4,5-bisphosphate in the WRK-1 cell. J. Biol. Chem. 261 (1986) 88-91
42. Wang Y.J., Li W.H., Wang J., Xu K., Dong P., Luo X., and Yin H.L. Critical role of PIP5KI{gamma}87 in InsP3-mediated Ca(2+) signaling. J. Cell Biol. 167 (2004) 1005-1010
43. Matsu-ura T., Michikawa T., Inoue T., Miyawaki A., Yoshida M., and Mikoshiba K. Cytosolic inositol 1,4,5-trisphosphate dynamics during intracellular calcium oscillations in living cells. J. Cell Biol. 173 (2006) 755-765
44. Lopez-Andreo M., Gomez-Fernandez J., and Corbalan-Garcia S. The simultaneous production of phosphatidic acid and diacylglycerol is essential for the translocation of protein kinase Cepsilon to the plasma membrane in RBL-2H3 cells. Mol. Biol. Cell 14 (2003) 4885-4895
45. Stahelin R.V., Digman M.A., Medkova M., Ananthanarayanan B., Rafter J.D., Melowic H.R., and Cho W. Mechanism of diacylglycerol-induced membrane targeting and activation of protein kinase Cdelta. J. Biol. Chem. 279 (2004) 29501-29512
46. Stahelin R.V., Digman M.A., Medkova M., Ananthanarayanan B., Melowic H.R., Rafter J.D., and Cho W. Diacylglycerol-induced membrane targeting and activation of protein kinase Cepsilon: mechanistic differences between protein kinases Cdelta and Cepsilon. J. Biol. Chem. 280 (2005) 19784-19793
47. Giorgione J.R., Lin J.-H., McCammon J.A., and Newton A.C. Increased membrane affinity of the C1 domain of protein kinase C{delta} compensates for the lack of involvement of its C2 domain in membrane recruitment. J. Biol. Chem. 281 (2006) 1660-1669
48. Garcia-Garcia J., Corbalan-Garcia S., and Gomez-Fernandez J. Effect of calcium and phosphatidic acid binding on the C2 domain of PKC alpha as studied by Fourier transform infrared spectroscopy. Biochemistry 38 (1999) 9667-9675
49. Zacharias D.A., Violin J.D., Newton A.C., and Tsien R.Y. Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 296 (2002) 913-916
50. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
51. Ochoa W., Torrecillas A., Fita I., Verdaguer N., Corbalan-Garcia S., and Gomez-Fernandez J.C. Retinoic acid binds to the C2-domain of protein kinase C(alpha). Biochemistry 42 (2003) 8774-8779
52. Garcia-Garcia J., Gomez-Fernandez J., and Corbalan-Garcia S. Structural characterization of the C2 domain of novel protein kinase Cepsilon. Eur. J. Biochem. 268 (2001) 1107-1117
53. Fabiato A. Computer programs for calculating total from specified free or free from specified total ionic concentrations in aqueous solutions containing multiple metals and ligands. Methods Enzymol. 157 (1988) 378-417
54. Meyer T., and Oancea E. Studies of signal transduction events using chimeras to green fluorescent protein. Methods Enzymol. 327 (2000) 500-513
55. Hoff B., Strandberg E., Ulrich A.S., Tieleman D.P., and Posten C. 2H-NMR study and molecular dynamics simulation of the location, alignment, and mobility of pyrene in POPC bilayers. Biophys. J. 88 (2005) 1818-1827