Amplification of diacylglycerol activation of protein kinase C by cholesterol

Biophysical Journal

Volumn 94, Issue 12, 2008, Pages 4700-4710

  Armstrong, Don ^a   Zidovetzki, Raphael ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; DIACYLGLYCEROL; PROTEIN KINASE C;

ARTICLE; CHEMICAL MODEL; CHEMISTRY; COMPUTER SIMULATION; ENZYME ACTIVATION;

CHOLESTEROL; COMPUTER SIMULATION; DIGLYCERIDES; ENZYME ACTIVATION; MODELS, CHEMICAL; PROTEIN KINASE C;

EID: 45849109582     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.107.121426     Document Type: Article

References (91)

1. Pike, L. J. 2003. Lipid rafts: bringing order to chaos. J. Lipid Res. 44:655-667.
2. Zeyda, M., and T. M. Stulnig. 2006. Lipid Rafts & Co.: an integrated model of membrane organization in T cell activation. Prog. Lipid Res. 45:187-202.
3. Vereb, G., J. Szölläsi, J. Matkó, P. Nagy, T. Farkas, L. Vigh, L. Mátyus, T. A. Waldmann, and S. Damjanovich. 2003. Dynamic, yet structured: the cell membrane three decades after the Singer-Nicolson model. Proc. Natl. Acad. Sci. USA. 100:8053-8058.
4. 2+-ATPase isoform 4 is localized in lipid rafts of cerebellum synaptic plasma membranes. J. Biol. Chem. 281:447-453.
5. Floto, R. A., M. R. Clatworthy, K. R. Heilbronn, D. R. Rosner, P. A. MacAry, A. Rankin, P. J. Lehner, W. H. Ouwehand, J. M. Allen, N. A. Watkins, and K. G. C. Smith. 2005. Loss of function of a lupus-associated FcγRIIb polymorphism through exclusion from lipid rafts. Nat. Med. 11:1056-1058.
6. Kim, B.-W., H.-J. Choo, J.-W. Lee, J.-H. Kim, and Y.-G. Ko. 2004. Extracellular ATP is generated by ATP synthase complex in adipocyte lipid rafts. Exp. Mol. Med. 36:476-485.
7. Wisniewska, A., J. Draus, and W. K. Subczynski. 2003. Is a fluid-mosaic model of biological membranes fully relevant? Studies on lipid organization in model and biological membranes. Cell. Mol. Biol. Lett. 8:147-159.
8. Edidin, M. 2003. The state of lipid rafts: from model membranes to cells. Annu. Rev. Biophys. Biomol. Struct. 32:257-283.
9. London, E. 2005. How principles of domain formation in model membranes may explain ambiguities concerning lipid raft formation in cells. Biochim. Biophys. Acta. 1746:203-220.
10. Gómez-Moutón, C., E. M. Jose Luis Abad, R. A. Lacalle, E. Gallardo, I. I. Sonia Jiménez-Baranda, A. Bernad, S. M. Nes, and C. Martínez. 2001. Segregation of leading-edge and uropod components into specific lipid rafts during T cell polarization. Proc. Natl. Acad. Sci. USA. 98:9642-9647.
11. Selvaraj, V., A. Asano, D. E. Buttke, J. L. McElwee, J. L. Nelson, C. A. Wolff, T. Merdiushev, M. W. Fornés, A.W. Cohen, M. P. Lisanti, G. H. Rothblat, G. S. Kopf, and A. J. Travis. 2006. Segregation of micron-scale membrane sub-domains in live murine sperm. J. Cell. Physiol. 206:636-646.
12. Vigh, L., P. V. Escribá, A. Sonnleitner, M. Sonnleitner, S. Piotto, B. Maresca, I. Horváth, and J. L. Harwood. 2005. The significance of lipid composition for membrane activity: new concepts and ways of assessing function. Prog. Lipid Res. 44:303-344.
13. Simons, K., and D. Toomre. 2000. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1:31-39.
14. Huang, H. W., E. M. Goldberg, and R. Zidovetzki. 1999. Ceramides modulate protein kinase C activity and perturb the structure of phosphatidylcholine/ phosphatidylserine bilayers. Biophys. J. 77:1489-1497.
15. Goldberg, E. M., and R. Zidovetzki. 1998. Synergistic effects of diacylglycerols and fatty acids on membrane structure and protein kinase C activity. Biochemistry. 37:5623-5632.
16. Jiménez-Monreal, A. M., F. J. Aranda, V. Micol, P. S.-P. Nera, A. de Godos, and J. C. Gómez-Fernández. 1999. Influence of the physical state of the membrane on the enzymatic activity and energy of activation of protein kinase Cα. Biochemistry. 38:7747-7754.
17. Medkova, M., and W. Cho. 1998. Differential membrane-binding and activation mechanisms of protein kinase C-α and -ε. Biochemistry. 37:4892-4900.
18. 2. Biochem. Biophys. Res. Commun. 220:834-838.
19. Escribá, P. V., A. Ozaita, C. Ribas, A. Miralles, E. Fodor, T. Farkas, and J. A. García-Sevilla. 1997. Role of lipid polymorphism in G protein-membrane interactions: nonlamellar-prone phospholipids and peripheral protein binding to membranes. Proc. Natl. Acad. Sci. USA. 94:11375-11380.
20. Sugar, I. P., N. K. Mizuno, M. M. Momsen, and H. L. Brockman. 2001. Lipid lateral organization in fluid interfaces controls the rate of colipase association. Biophys. J. 81:3387-3397.
21. Ruiz-Argüello, M. B., F. M. Goñi, and A. Alonso. 1998. Phospholipase C hydrolysis of phospholipids in bilayers of mixed lipid compositions. Biochemistry. 37:11621-11628.
22. Nakashima, S. 2002. Protein kinase C alpha (PKC α): regulation and biological function. J. Biochem. (Tokyo). 132:669-675.
23. Griner, E. M., and M. G. Kazanietz. 2007. Protein kinase C and other diacylglycerol effectors in cancer. Nat. Rev. Cancer. 7:281-294.
24. Senisterra, G., and R. M. Epand. 1993. Role of membrane defects in the regulation of the activity of protein kinase C. Arch. Biochem. Biophys. 300:378-383.
25. 2+ on structure of phosphatidylcholine/ phosphatidylserine bilayers. Biophys. J. 66:382-393.
26. Goldberg, E. M., and R. Zidovetzki. 1997. Effects of dipalmitoylglycerol and fatty acids on membrane structure and protein kinase C activity. Biophys. J. 73:2603-2614.
27. Dibble, A. R., A. K. Hinderliter, J. J. Sando, and R. L. Biltonen. 1996. Lipid lateral heterogeneity in phosphatidylcholine/phosphatidylserine/ diacylglycerol vesicles and its influence on protein kinase C activation. Biophys. J. 71:1877-1890.
28. Wakelam, M. J. 1998. Diacylglycerol - when is it an intracellular messenger? Biochim. Biophys. Acta. 1436:117-126.
29. Rhee, S. G. 2001. Regulation of phosphoinositide-specific phospholipase C. Annu. Rev. Biochem. 70:281-312.
30. Exton, J. H. 1997. New developments in phospholipase D. J. Biol. Chem. 272:15579-15582.
31. Springett, G. M., H. Kawasaki, and D. R. Spriggs. 2004. Non-kinase second-messenger signaling: new pathways with new promise. Bioessays. 26:730-738.
32. Pessin, M. S., J. J. Baldassare, and D. M. Raben. 1990. Molecular species analysis of mitogen-stimulated 1,2-diglycerides in fibroblasts. Comparison of α-thrombin, epidermal growth factor, and platelet-derived growth factor. J. Biol. Chem. 265:7959-7966.
33. Pettitt, T. R., and M. J. Wakelam. 1993. Bombesin stimulates distinct time-dependent changes in the sn-1,2-diradylglycerol molecular species profile from Swiss 3T3 fibroblasts as analyzed by 3,5-dinitrobenzoyl derivitization and HPLC separation. Biochem. J. 289:487-495.
34. Ipsen, J. H., O. G. Mouritsen, and M. Bloom. 1990. Relationships between lipid membrane area, hydrophobic thickness, and acyl-chain orientational order. The effects of cholesterol. Biophys. J. 57:405-412.
35. 2H nuclear magnetic resonance and differential scanning calorimetry. Biochemistry. 29:451-464.
36. Lindblom, G., G. Orädd, and A. Filippov. 2006. Lipid lateral diffusion in bilayers with phosphatidylcholine, sphingomyelin and cholesterol. An NMR study of dynamics and lateral phase separation. Chem. Phys. Lipids. 141:179-184.
37. Leathes, J. 1925. Rôle of fats in vital phenomena. Lancet. 208:853-856.
38. Pucadyil, T. J., and A. Chattopadhyay. 2006. Role of cholesterol in the function and organization of G-protein coupled receptors. Prog. Lipid Res. 45:295-333.
39. Arispe, N., and M. Doh. 2002. Plasma membrane cholesterol controls the cytotoxicity of Alzheimer's disease AβP (1-40) and (1-42) peptides. FASEB J. 16:1526-1536.
40. Zidovetzki, R., and I. Levitan. 2007. Use of cyclodextrins to manipulate plasma membrane cholesterol content: evidence, misconceptions and control strategies. Biochim. Biophys. Acta. 1768:1311-1324.
41. Sando, J. J., and O. I. Chertihin. 1996. Activation of protein kinase C by lysophosphatidic acid: dependence on composition of phospholipid vesicles. Biochem. J. 317:583-588.
42. Goldberg, E. M., D. B. Borchardt, and R. Zidovetzki. 1998. Effects of histone and diolein on the structure of phosphatidylcholine/phosphatidylserine or phosphatidylcholine/phosphatidylglycerol bilayers. Eur. J. Biochem. 258:722-728.
43. Bach, D., E. Wachtel, N. Borochov, G. Senisterra, and R. M. Epand. 1992. Phase behavior of heteroacid phosphatidylserines and cholesterol. Chem. Phys. Lipids. 63:105-113.
44. Ronemus, A. D., R. L. Vold, and R. R. Vold. 1986. Deuterium quadrupole echo NMR spectroscopy. II. Artifact suppression. J. Magn. Reson. 70:416-426.
45. Sternin, E., M. Bloom, and A. MacKay. 1983. De-Pakeing of NMR spectra. J. Magn. Reson. 55:274-282.
46. McCabe, M. A., and S. R. Wassal. 1995. Fast-Fourier-transform dePaking. J. Mag. Res. Ser. B. 106:80-82.
47. 31P NMR study. Biochemistry. 28:7439-7446.
48. Escribá, P. V., M. Sastre, and J. A. García-Sevilla. 1995. Disruption of cellular signaling pathways by daunomycin through destabilization of nonlamellar membrane structures. Proc. Natl. Acad. Sci. USA. 92:7595-7599.
49. Epand, R. M. 1997. Studies of membrane physical properties and their role in biological function. Biochem. Soc. Trans. 25:1073-1079.
50. Epand, R. M. 1987. The relationship between the effects of drugs on bilayer stability and on protein kinase C activity. Chem. Biol. Interact. 63:239-247.
51. Epand, R. M., A. R. Stafford, J. J. Cheetham, R. Bottega, and E. H. Ball. 1988. The relationship between the bilayer to hexagonal phase transition temperature in membranes and protein kinase C activity. Biosci. Rep. 8:49-54.
52. Epand, R. M., and D. S. Lester. 1990. The role of membrane biophysical properties in the regulation of protein kinase C activity. Trends Pharmacol. Sci. 11:317-320.
53. Pike, L. J., X. Han, K.-N. Chung, and R. W. Gross. 2002. Lipid rafts are enriched in arachidonic acid and plasmenylethanolamine and their composition is independent of caveolin-1 expression: a quantitative electrospray ionization/mass spectrometric analysis. Biochemistry. 41:2075-2088.
54. Baron, C. B., and R. F. Coburn. 2004. Smooth muscle raft-like membranes. J. Lipid Res. 45:41-53.
55. Tewes, B., and H. Galla. 2001. Lipid polarity in brain capillary endothelial cells. Endothelium. 8:207-220.
56. Armstrong, D. L., D. B. Borchardt, and R. Zidovetzki. 2002. Synergistic perturbation of phosphatidylcholine/sphingomyelin bilayers by diacylglycerol and cholesterol. Biochem. Biophys. Res. Commun. 296:806-812.
57. 2H nuclear magnetic resonance spin-lattice relaxation in phospholipid and phospholipid:cholesterol systems. J. Chem. Phys. 101:749-763.
58. Davis, J., and K. Jeffrey. 1977. The temperature dependence of chain disorder in potassium palmitate-water. A deuterium NMR study. Chem. Phys. Lipids. 20:87-104.
59. 14. J. Chem. Phys. 55:5829-5831.
60. Leventis, R., and J. R. Silvius. 2001. Use of cyclodextrins to monitor transbilayer movement and differential lipid affinities of cholesterol. Biophys. J. 81:2257-2267.
61. 13C magic angle spinning nuclear magnetic resonance. Biophys. J. 83:2053-2063.
62. 2H NMR spectroscopy. Biophys. J. 79:3172-3192.
63. Greenwood, A. I., S. Tristram-Nagle, and J. F. Nagle. 2006. Partial molecular volumes of lipids and cholesterol. Chem. Phys. Lipids. 143:1-10.
64. Róg, T., and M. Pasenkiewicz-Gierula. 2006. Cholesterol effects on a mixed-chain phosphatidylcholine bilayer: a molecular dynamics simulation study. Biochimie. 88:449-460.
65. Smaby, J. M., M. M. Momsen, H. L. Brockman, and R. E. Brown. 1997. Phosphatidylcholine acyl unsaturation modulates the decrease in interfacial elasticity induced by cholesterol. Biophys. J. 73:1492-1505.
66. Bloom, M., E. Evans, and O. G. Mouritsen. 1991. Physical properties of the fluid lipid-bilayer component of cell membranes: a perspective. Q. Rev. Biophys. 24:293-397.
67. Clarke, J. A., A. J. Heron, J. M. Seddon, and R. V. Law. 2006. The diversity of the liquid ordered (Lo) phase of phosphatidylcholine/cholesterol membranes: a variable temperature multinuclear solid-state NMR and x-ray diffraction study. Biophys. J. 90:2383-2393.
68. 31P-NMR study. Biophys. J. 68:965-977.
69. Vogel, A., H. A. Scheidt, and D. Huster. 2003. The distribution of lipid attached spin probes in bilayers: application to membrane protein topology. Biophys. J. 85:1691-1701.
70. Wolf, C., K. Koumanov, B. Tenchov, and P. J. Quinn. 2001. Cholesterol favors phase separation of sphingomyelin. Biophys. Chem. 89:163-172.
71. Tenchov, B. G., R. C. MacDonald, and D. P. Siegel. 2006. Cubic phases in phosphatidylcholine-cholesterol mixtures: cholesterol as membrane "fusogen". Biophys. J. 91:2508-2516.
72. Filippov, A., G. Orädd, and G. Lindblom. 2003. The effect of cholesterol on the lateral diffusion of phospholipids in oriented bilayers. Biophys. J. 84:3079-3086.
73. 31P solid-state NMR. Biochemistry. 42:1383-1390.
74. Veatch, S. L., and S. L. Keller. 2005. Seeing spots: complex phase behavior in simple membranes. Biochim. Biophys. Acta. 1746:172-185.
75. de Almeida, R. F. M., A. Fedorov, and M. Prieto. 2003. Sphingomyelin/ phosphatidylcholine/cholesterol phase diagram: boundaries and composition of lipid rafts. Biophys. J. 85:2406-2416.
76. Niggli, V., A. V. Meszaros, C. Oppliger, and S. Tornay. 2004. Impact of cholesterol depletion on shape changes, actin reorganization, and signal transduction in neutrophil-like HL-60 cells. Exp. Cell Res. 296:358-368.
77. Bolen, E. J., and J. J. Sando. 1992. Effect of phospholipid unsaturation on protein kinase C activation. Biochemistry. 31:5945-5951.
78. Slater, S. J., M. B. Kelly, F. J. Taddeo, C. Ho, E. Rubin, and C. D. Stubbs. 1994. The modulation of protein kinase C activity by membrane lipid bilayer structure. J. Biol. Chem. 269:4866-4871.
79. Kuroki, T., T. Ikuta, M. Kashiwagi, S. Kawabe, M. Ohba, N. Huh, K. Mizuno, S. Ohno, E. Yamada, and K. Chida. 2000. Cholesterol sulfate, an activator of protein kinase C mediating squamous cell differentiation: a review. Mutat. Res. 462:189-195.
80. Newton, A. C., and J. E. Johnson. 1998. Protein kinase C: a paradigm for regulation of protein function by two membrane-targeting modules. Biochim. Biophys. Acta. 1376:155-172.
81. Das, S., and R. P. Rand. 1986. Modification by diacylglycerol of the structure and interaction of various phospholipid bilayer membranes. Biochemistry. 25:2882-2889.
82. Kazanietz, M. G. 2002. Novel "nonkinase" phorbol ester receptors: the C1 domain connection. Mol. Pharmacol. 61:759-767.
83. Calderón, R. O., and G. H. DeVries. 1997. Lipid composition and phospholipid asymmetry of membranes from a Schwann cell line. J. Neurosci. Res. 49:372-380.
84. Verkleij, A., R. Zwaal, B. Roelofsen, P. Comfurius, D. Kastelijn, and L. van Deenen. 1973. The asymmetric distribution of phospholipids in the human red cell membrane. A combined study using phospholipases and freeze-etch electron microscopy. Biochim. Biophys. Acta. 323:178-193.
85. Boesze-Battaglia, K., and R. Schimmel. 1997. Cell membrane lipid composition and distribution: implications for cell function and lessons learned from photoreceptors and platelets. J. Exp. Biol. 200:2927-2936.
86. Pike, L. J. 2004. Lipid rafts: heterogeneity on the high seas. Biochem. J. 378:281-292.
87. Babiychuk, E. B., and A. Draeger. 2006. Biochemical characterization of detergent-resistant membranes: a systematic approach. Biochem. J. 397:407-416.
88. Veatch, S. L., and S. L. Keller. 2003. A closer look at the canonical "raft mixture" in model membrane studies. Biophys. J. 84:725-726.
89. Gaus, K., M. Rodriguez, K. R. Ruberu, I. Gelissen, T. M. Sloane, L. Kritharides, and W. Jessup. 2005. Domain-specific lipid distribution in macrophage plasma membranes. J. Lipid Res. 46:1526-1538.
90. Drobnik, W., H. Borsukova, A. Böttcher, A. Pfeiffer, G. Liebisch, G. J. Schötz, H. Schindler, and G. Schmitz. 2002. Apo AI/ABCA1-dependent and HDL3-mediated lipid efflux from compositionally distinct cholesterol-based microdomains. Traffic. 3:268-278.
91. Holowka, D., J. A. Gosse, A. T. Hammond, X. Han, P. Sengupta, N. L. Smith, A. Wagenknecht-Wiesner, M. Wu, R. M. Young, and B. Baird. 2005. Lipid segregation and IgE receptor signaling: a decade of progress. Biochim. Biophys. Acta. 1746:252-259.