Probing the determinants of diacylglycerol binding affinity in the C1B domain of protein kinase Cα

Journal of Molecular Biology

Volumn 408, Issue 5, 2011, Pages 949-970

  Stewart, Mikaela D ^a   Morgan, Brittany ^b   Massi, Francesca ^b   Igumenova, Tatyana I ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

conformational exchange; NMR spectroscopy; peripheral membrane protein; protein dynamics; protein lipid interactions

Indexed keywords

DIACYLGLYCEROL; PROTEIN KINASE C ALPHA;

ARTICLE; BINDING AFFINITY; BINDING SITE; GEOMETRY; MOLECULAR DYNAMICS; MUTATION; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; WILD TYPE;

EID: 79955473607     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.03.020     Document Type: Article

References (78)

1. Hurley J.H., Newton A.C., Parker P.J., Blumberg P.M., and Nishizuka Y. Taxonomy and function of C1 protein kinase C homology domains Protein Sci. 6 1997 477 480 (Pubitemid 27079944)
2. Brose N., and Rosenmund C. Move over protein kinase C, you've got company: alternative cellular effectors of diacylglycerol and phorbol esters J. Cell Sci. 115 2002 4399 4411 (Pubitemid 36004402)
3. Kazanietz M.G. Targeting protein kinase C and "non-kinase" phorbol ester receptors: emerging concepts and therapeutic implications Biochim. Biophys. Acta 1754 2005 296 304 (Pubitemid 41797711)
4. Blumberg P.M., Kedei N., Lewin N.E., Yang D., Czifra G., and Pu Y. Wealth of opportunity-the C1 domain as a target for drug development Curr. Drug Targets 9 2008 641 652
5. Goel G., Makkar H.P., Francis G., and Becker K. Phorbol esters: structure, biological activity, and toxicity in animals Int. J. Toxicol. 26 2007 279 288 (Pubitemid 47174587)
6. Kazanietz M.G., and Lorenzo P.S. Phorbol esters as probes for the study of protein kinase C function A.C. Newton, Protein Kinase C Protocols vol. 233 2003 Humana Press, Inc. Totowa, NJ 423 429
7. Griner E.M., and Kazanietz M.G. Protein kinase C and other diacylglycerol effectors in cancer Nat. Rev. Cancer 7 2007 281 294 (Pubitemid 46480971)
8. Castagna M., Takai Y., Kaibuchi K., Sano K., Kikkawa U., and Nishizuka Y. Direct activation of calcium-activated, phospholipid-dependent protein kinase by tumor-promoting phorbol esters J. Biol. Chem. 257 1982 7847 7851 (Pubitemid 12043279)
9. Newton A.C. Protein kinase C: structural and spatial regulation by phosphorylation, cofactors, and macromolecular interactions Chem. Rev. 101 2001 2353 2364 (Pubitemid 35373023)
10. Steinberg S.F. Structural basis of protein kinase C isoform function Physiol. Rev. 88 2008 1341 1378
11. House C., and Kemp B.E. Protein kinase C contains a pseudosubstrate prototype in its regulatory domain Science 238 1987 1726 1728 (Pubitemid 18046276)
12. 2+-binding motif in C2 domains of synaptotagmin and protein kinase C Science 273 1996 248 251 (Pubitemid 26285893)
13. Cho W., and Stahelin R.V. Membrane binding and subcellular targeting of C2 domains Biochim. Biophys. Acta 1761 2006 838 849 (Pubitemid 44332329)
14. Irie K., Oie K., Nakahara A., Yanai Y., Ohigashi H., and Wender P.A. Molecular basis for protein kinase C isozyme-selective binding: the synthesis, folding, and phorbol ester binding of the cysteine-rich domains of all protein kinase C isozymes J. Am. Chem. Soc. 120 1998 9159 9167 (Pubitemid 28452689)
15. Ananthanarayanan B., Stahelin R.V., Digman M.A., and Cho W.H. Activation mechanisms of conventional protein kinase C isoforms are determined by the ligand affinity and conformational flexibility of their C1 domains J. Biol. Chem. 278 2003 46886 46894 (Pubitemid 37452270)
16. Slater S.J., Ho C., Kelly M.B., Larkin J.D., Taddeo F.J., Yeager M.D., and Stubbs C.D. Protein kinase C α contains two activator binding sites that bind phorbol esters and diacylglycerols with opposite affinities J. Biol. Chem. 271 1996 4627 4631
17. Medkova M., and Cho W.H. Interplay of C1 and C2 domains of protein kinase C-α in its membrane binding and activation J. Biol. Chem. 274 1999 19852 19861
18. Stahelin R.V., Digman M.A., Medkova M., Ananthanarayanan B., Rafter J.D., Melowic H.R., and Cho W.H. Mechanism of diacylglycerol-induced membrane targeting and activation of protein kinase C δ J. Biol. Chem. 279 2004 29501 29512 (Pubitemid 38915830)
19. Szallasi Z., Bogi K., Gohari S., Biro T., Acs P., and Blumberg P.M. Non-equivalent roles for the first and second zinc fingers of protein kinase C δ. Effect of their mutation on phorbol ester-induced translocation in NIH 3T3 cells J. Biol. Chem. 271 1996 18299 18301 (Pubitemid 26322676)
20. Grishin N.V. Treble clef finger-a functionally diverse zinc-binding structural motif Nucleic Acids Res. 29 2001 1703 1714 (Pubitemid 32427851)
21. Mott H.R., Carpenter J.W., Zhong S., Ghosh S., Bell R.M., and Campbell S.L. The solution structure of the Raf-1 cysteine-rich domain: a novel Ras and phospholipid binding site Proc. Natl Acad. Sci. USA 93 1996 8312 8317 (Pubitemid 26269554)
22. Zhou M., Horita D.A., Waugh D.S., Byrd R.A., and Morrison D.K. Solution structure and functional analysis of the cysteine-rich C1 domain of kinase suppressor of Ras (KSR) J. Mol. Biol. 315 2002 435 446 (Pubitemid 34729351)
23. Hommel U., Zurini M., and Luyten M. Solution structure of a cysteine-rich domain of rat protein kinase C Nat. Struct. Biol. 1 1994 383 387
24. Zhang G.G., Kazanietz M.G., Blumberg P.M., and Hurley J.H. Crystal-structure of the Cys2 activator-binding domain of protein kinase C-δ in complex with phorbol ester Cell 81 1995 917 924
25. Xu R.X., Pawelczyk T., Xia T.H., and Brown S.C. NMR structure of a protein kinase C-γ phorbol-binding domain and study of protein-lipid micelle interactions Biochemistry 36 1997 10709 10717 (Pubitemid 27382560)
26. Shen N., Guryev O., and Rizo J. Intramolecular occlusion of the diacylglycerol-binding site in the C1 domain of munc13-1 Biochemistry 44 2005 1089 1096 (Pubitemid 40208988)
27. Harjes E., Harjes S., Wohlgemuth S., Muller K.H., Krieger E., Herrmann C., and Bayer P. GTP-Ras disrupts the intramolecular complex of C1 and RA domains of Nore1 Structure 14 2006 881 888 (Pubitemid 43674096)
28. Dries D.R., Gallegos L.L., and Newton A.C. A single residue in the C1 domain sensitizes novel protein kinase C isoforms to cellular diacylglycerol production J. Biol. Chem. 282 2007 826 830 (Pubitemid 47076514)
29. Dries D.R., and Newton A.C. Kinetic analysis of the interaction of the C1 domain of protein kinase C with lipid membranes by stopped-flow spectroscopy J. Biol. Chem. 283 2008 7885 7893
30. Lemmon M.A. Membrane recognition by phospholipid-binding domains Nat. Rev. Mol. Cell Biol. 9 2008 99 111 (Pubitemid 351158910)
31. Vriend G. WHAT IF-a molecular modeling and drug design program J. Mol. Graphics 8 1990 52 56 (Pubitemid 20717037)
32. 2H NMR dynamics and scalar couplings J. Mol. Biol. 329 2003 551 563 (Pubitemid 36593211)
33. Oxenoid K., Rice A.J., and Chou J.J. Comparing the structure and dynamics of phospholamban pentamer in its unphosphorylated and pseudo-phosphorylated states Protein Sci. 16 2007 1977 1983 (Pubitemid 47367121)
34. Hritz J., Ulicny J., Laaksonen A., Jancura D., and Miskovsky P. Molecular interaction model for the C1B domain of protein kinase C-γ in the complex with its activator phorbol-12-myristate-13-acetate in water solution and lipid bilayer J. Med. Chem. 47 2004 6547 6555 (Pubitemid 39657317)
35. Gallegos L.L., and Newton A.C. Spatiotemporal dynamics of lipid signaling: protein kinase C as a paradigm IUBMB Life 60 2008 782 789
36. Yau W.M., Wimley W.C., Gawrisch K., and White S.H. The preference of tryptophan for membrane interfaces Biochemistry 37 1998 14713 14718 (Pubitemid 28487579)
37. Killian J.A., and von Heijne G. How proteins adapt to a membrane-water interface Trends Biochem. Sci. 25 2000 429 434 (Pubitemid 30662410)
38. Kazanietz M.G., Wang S., Milne G.W.A., Lewin N.E., Liu H.L., and Blumberg P.M. Residues in the second cysteine-rich region of protein kinase C-δ relevant to phorbol ester binding as revealed by site-directed mutagenesis J. Biol. Chem. 270 1995 21852 21859
39. Jarymowycz V.A., and Stone M.J. Fast time scale dynamics of protein backbones: NMR relaxation methods, applications, and functional consequences Chem. Rev. 106 2006 1624 1671 (Pubitemid 43792775)
40. James L.C., and Tawfik D.S. Conformational diversity and protein evolution-a 60-year-old hypothesis revisited Trends Biochem. Sci. 28 2003 361 368 (Pubitemid 36851617)
41. Filipp F.V., and Sattler M. Conformational plasticity of the lipid transfer protein SCP2 Biochemistry 46 2007 7980 7991 (Pubitemid 47051634)
42. 1H exchange Biochemistry 36 1997 2278 2290 (Pubitemid 27104722)
43. Hodsdon M.E., and Cistola D.P. Discrete backbone disorder in the nuclear magnetic resonance structure of apo intestinal fatty acid-binding protein: implications for the mechanism of ligand entry Biochemistry 36 1997 1450 1460 (Pubitemid 27074969)
44. Long D., and Yang D. Millisecond timescale dynamics of human liver fatty acid binding protein: testing of its relevance to the ligand entry process Biophys. J. 98 2010 3054 3061
45. Butt T.R., Edavettal S.C., Hall J.P., and Mattern M.R. SUMO fusion technology for difficult-to-express proteins Protein Expression Purif. 43 2005 1 9 (Pubitemid 41097378)
46. Muhandiram D.R., and Kay L.E. Gradient-enhanced triple-resonance three-dimensional NMR experiments with improved sensitivity J. Magn. Reson. Ser. B 103 1994 203 216
47. Delaglio F., Grzesiek S., Vuister G.W., Zhu G., Pfeifer J., and Bax A. NMRPipe-a multidimensional spectral processing system based on Unix pipes J. Biomol. NMR 6 1995 277 293
48. Goddard T.D., and Kneller D.G. SPARKY 3 2003 University of California San Francisco, CA
49. Wilcox C.S. Design, synthesis, and evaluation of an efficacious functional group dyad. Methods and limitations in the use of NMR for measuring host-guest interactions H.J. Schneider, H. Dürr, Frontiers in Supramolecular Organic Chemistry and Photochemistry 1991 Wiley-VCH Weinheim, Germany 123 143
50. 2H labeled proteins with high-sensitivity J. Am. Chem. Soc. 116 1994 11655 11666
51. Sass H.J., Musco G., Stahl S.J., Wingfield P.T., and Grzesiek S. Solution NMR of proteins within polyacrylamide gels: diffusional properties and residual alignment by mechanical stress or embedding of oriented purple membranes J. Biomol. NMR 18 2000 303 309 (Pubitemid 32065084)
52. Tycko R., Blanco F.J., and Ishii Y. Alignment of biopolymers in strained gels: a new way to create detectable dipole-dipole couplings in high-resolution biomolecular NMR J. Am. Chem. Soc. 22 2000 9340 9341
53. Chou J.J., Gaemers S., Howder B., Louis J.M., and Bax A. A simple apparatus for generating stretched polyacrylamide gels, yielding uniform alignment of proteins and detergent micelles J. Biomol. NMR 21 2001 377 382 (Pubitemid 34071393)
54. Ottiger M., Delaglio F., and Bax A. Measurement of J and dipolar couplings from simplified two-dimensional NMR spectra J. Magn. Reson. 131 1998 373 378 (Pubitemid 128450579)
55. 15N NMR relaxation Biochemistry 33 1994 5984 6003 (Pubitemid 24184605)
56. de la Torre J.G., Huertas M.L., and Carrasco B. HYDRONMR: prediction of NMR relaxation of globular proteins from atomic-level structures and hydrodynamic calculations J. Magn. Reson. 147 2000 138 146
57. 15N NMR relaxation J. Am. Chem. Soc. 117 1995 12562 12566
58. Hall J.B., and Fushman D. Characterization of the overall and local dynamics of a protein with intermediate rotational anisotropy: differentiating between conformational exchange and anisotropic diffusion in the B3 domain of protein G J. Biomol. NMR 27 2003 261 275 (Pubitemid 37185125)
59. Lipari G., and Szabo A. Model-free approach to the interpretation of nuclear magnetic-resonance relaxation in macromolecules: 1. Theory and range of validity J. Am. Chem. Soc. 104 1982 4546 4559
60. Mandel A.M., Akke M., and Palmer A.G. Backbone dynamics of Escherichia coli ribonuclease HI: correlations with structure and function in an active enzyme J. Mol. Biol. 246 1995 144 163
61. Cole R., and Loria J.P. FAST-Modelfree: a program for rapid automated analysis of solution NMR spin-relaxation data J. Biomol. NMR 26 2003 203 213 (Pubitemid 36758441)
62. 1 constant relaxation time NMR spectroscopy J. Am. Chem. Soc. 118 1996 911 912 (Pubitemid 126528353)
63. 15N spin relaxation-times J. Biomol. NMR 3 1993 151 164
64. Palmer A.G., and Massi F. Characterization of the dynamics of biomacromolecules using rotating-frame spin relaxation NMR spectroscopy Chem. Rev. 106 2006 1700 1719 (Pubitemid 43840531)
65. α carbons J. Am. Chem. Soc. 116 1994 8266 8278 (Pubitemid 24981535)
66. Mulder F.A.A., de Graaf R.A., Kaptein R., and Boelens R. An off-resonance rotating frame relaxation experiment for the investigation of macromolecular dynamics using adiabatic rotations J. Magn. Reson. 131 1998 351 357 (Pubitemid 128450575)
67. Palmer A.G., Kroenke C.D., and Loria J.P. Nuclear magnetic resonance methods for quantifying microsecond-to-millisecond motions in biological macromolecules Methods Enzymol. 339 2001 204 238 (Pubitemid 32666562)
68. 15N chemical shift anisotropy from quantitative measurement of relaxation interference effects J. Am. Chem. Soc. 118 1996 6986 6991 (Pubitemid 26252043)
69. 15N chemical shift anisotropy relaxation interference: unambiguous determination of rotational diffusion tensors and chemical exchange effects in biological macromolecules J. Am. Chem. Soc. 120 1998 7905 7915 (Pubitemid 28392074)
70. 15N chemical shift anisotropy from NMR relaxation data. Ubiquitin as a test example J. Am. Chem. Soc. 120 1998 7109 7110 (Pubitemid 28378372)
71. Wang C.Y., Rance M., and Palmer A.G. Mapping chemical exchange in proteins with MW > 50 kD J. Am. Chem. Soc. 125 2003 8968 8969 (Pubitemid 36903790)
72. Humphrey W., Dalke A., and Schulten K. VMD-Visual Molecular Dynamics J. Mol. Graphics 14 1996 33 38
73. Phillips J.C., Braun R., Wang W., Gumbart J., Tajkhorshid E., and Villa E. Scalable molecular dynamics with NAMD J. Comput. Chem. 26 2005 1781 1802 (Pubitemid 43078511)
74. MacKerell A.D., Bashford D., Bellott M., Dunbrack R.L., Evanseck J.D., and Field M.J. All-atom empirical potential for molecular modeling and dynamics studies of proteins J. Phys. Chem. B 102 1998 3586 3616 (Pubitemid 128576688)
75. Sakharov D.V., and Lim C. Zn protein simulations including charge transfer and local polarization effects J. Am. Chem. Soc. 127 2005 4921 4929 (Pubitemid 40489646)
76. Ryckaert J.P., Ciccotti G., and Berendsen H.J.C. Numerical-integration of Cartesian equations of motion of a system with constraints-molecular-dynamics of n-alkanes J. Comput. Phys. 23 1977 327 341
77. Simmerling C., Elber R., and Zhang J. MOIL-View-a program for visualization of structure and dynamics of biomolecules and STO-a program for computing stochastic paths Jerusalem Symposium Q: Modelling of Biomolecular Structures and Mechanisms vol. 27 1995 Kluwer Academic Publishers The Netherlands 241 265
78. Morgan B.R., and Massi F. A computational study of RNA binding and specificity in the tandem zinc finger domain of TIS11d Protein Sci. 19 2010 1222 1234