Regulation of calcium channel activity by lipid domain formation in planar lipid bilayers

Biophysical Journal

Volumn 85, Issue 2, 2003, Pages 933-942

  Cannon, Brian ^a   Hermansson, Martin ^c   Györke, Sandor ^b   Somerharju, Pentti ^c   Virtanen, Jorma A ^c   Cheng, Kwan Hon ^a  

^a TEXAS TECH UNIVERSITY   (United States)

^b TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER SCHOOL OF MEDICINE   (United States)

^c NONE

Author keywords

[No Author keywords available]

Indexed keywords

1 PALMITOYL 2 OLEOYLPHOSPHATIDYLETHANOLAMINE; 2 OLEOYL 1 PALMITOYLPHOSPHATIDYLCHOLINE; CALCIUM CHANNEL; CALCIUM ION; LIPID; LIPOSOME; RYANODINE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CHANNEL GATING; CHEMICAL COMPOSITION; CONCENTRATION (PARAMETERS); CRYSTAL STRUCTURE; ENTROPY; HEART MUSCLE CELL; IN VIVO STUDY; LIPID BILAYER; LIQUID CRYSTAL; NONHUMAN; PHASE TRANSITION; PROTEIN FUNCTION; RAT; SARCOPLASMIC RETICULUM; TEMPERATURE DEPENDENCE;

ANIMALIA;

EID: 0041343071     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(03)74532-9     Document Type: Article

References (61)

1. Bers, D. M., and E. Perez-Reyes. 1999. Ca channels in cardiac myocytes: structure and function in Ca influx and intracellular Ca release. Cardiovasc. Res. 42:339-360.
2. Boheim, G., W. Hanke, and E. Eibl. 1980. Lipid phase transition in planar bilayer and its effects on carrier and pore-mediated ion transport. Proc. Natl. Acad. Sci. USA. 77:3403-3407.
3. Burack, W. R., A. R. Dibble, M. M. Allietta, and R. L. Biltonen. 1997. Changes in vesicle morphology induced by lateral phase separation modulate phospholipase A2 activity. Biochemistry. 36:10551-10557.
4. Chang, H., R. Reitstetter, and R. Gruener. 1995a. Lipid-ion channel interactions: increasing phospholipid headgroup size but not ordering acyl chains alters reconstituted channel behavior. J. Membr. Biol. 145:13-19.
5. Chang, H., R. Reitstetter, R. Mason, and R. Gruener. 1995b. Attenuation of channel kinetics and conductance by cholesterol: an interpretation using structural stress as a unifying concept. J. Membr. Biol. 143:51-63.
6. Cheng, K. H., and S. W. Hui. 1986. Correlation between the bilayer destabilization and activity enhancement by diacylglycerols in reconstituted Ca-ATPase vesicles. Arch. Biochem. Biophys. 24:382-386.
7. Cheng, K., J. Lepock, S. Hui, and P. Yeagle. 1986. The role of cholesterol in the activity of reconstituted Ca-ATPase vesicles containing unsaturated PE. J. Biol. Chem. 261:5081-5087.
8. Cheng, K. H., T. Weidmer, and P. J. Sims. 1985. Fluorescence resonance energy transfer study of the membrane bound complexes of complement protein C5b-8. J. Immunol. 135:459-464.
9. Cullis, P. R., M. J. Hope, and C. P. Tilcock. 1986. Lipid polymorphism and the roles of lipids in membranes. Chem. Phys. Lipids. 40:127-144.
10. Davis, P., B. Fleming, B. K. Coolbear, and K. Keough. 1981. Gel to liquid-crystalline transition temperatures of water dispersions of two pairs of positional isomers of unsaturated mixed-acid phosphatidylcholines. Biochemistry. 20:3633-3636.
11. Dong, L. W., L.-L. Wu, Y. Ji, and M.-S. Liu. 2001. Impairment of the ryanodine-sensitive calcium release channels in the cardiac sarcoplasmic reticulum and its underlying mechanism during the hypodynamic phase of sepsis. Shock. 16:33-39.
12. Elliott, J. R., D. Needham, J. P. Dilger, and D. A. Haydon. 1983. The effects of bilayer thickness and tension on gramicidin single-channel lifetime. Biochim. Biophys. Acta. 735:95-103.
13. Fabiato, A. 1983. Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum. Am. J. Physiol. Cell Physiol. 245:C1-C14.
14. Ferguson, G. A. 1971. Tests of significance: means. In Statistical Analysis in Psychology and Education, 3rd ed. McGraw-Hill, New York. 146-157.
15. Fettiplace, R., D. Andrews, and D. Haydon. 1971. The thickness, composition and structure of some lipid bilayers and natural membranes. J. Membr. Biol. 5:277-296.
16. Fill, M., R. Coronado, J. R. Mickelson, J. Vilven, J. Ma, B. A. Jacobson, and C. F. Louis. 1990. Abnormal ryanodine receptor channels in malignant hyperthermia. Biophys. J. 57:471-475.
17. 2+ release units and couplons in skeletal and cardiac muscles. Biophys. J. 77:1528-1539.
18. Gruner, S. 1985. Intrinsic curvature hypothesis for biomembrane lipid composition: a role for nonbilayer lipids. Proc. Natl. Acad. Sci. USA. 82:3665-3669.
19. Hamill, O. P., and B. Martinac. 2001. Molecular basis of mechanotransduction in living cells. Physiol. Rev. 81:685-740.
20. Harroun, T. A., W. T. Heller, T. M. Weiss, L. Yang, and H. W. Huang. 1999. Experimental evidence for hydrophobic matching and membrane-mediated interactions in lipid bilayers containing gramicidin. Biophys. J. 76:937-945.
21. Haverstick, D. M., and M. Glaser. 1988. Visualization of domain formation in the inner and outer leaflets of a phospholipid bilayer. J. Cell Biol. 106:1885-1892.
22. Heller, W., K. He, S. Ludtke, T. Harroun, and H. Huang. 1997. Effect of changing the size of lipid headgroup on peptide insertion into membranes. Biophys. J. 73:239-244.
23. Hinderliter, A. K., J. Huang, and G. W. Feigenson. 1994. Detection of phase separation in fluid phosphatidylserine/phosphatidylcholine mixtures. Biophys. J. 67:1906-1911.
24. Ho, C., and C. D. Stubbs. 1992. Hydration at the membrane protein-lipid interface. Biophys. J. 63:897-902.
25. Huang, H. W. 1986. Deformation free energy of bilayer membrane and its effects on gramicidin channel lifetime. Biophys. J. 54:527-533.
26. 62 with 1-palmitoyl-2-oleoylphosphatidylethanol-amine and 1-stearoyl-2-oleoyl-phosphatidyl-choline. Biochemistry. 24:3422-3428.
27. Keller, S., S. Bezrukov, S. Gruner, M. Tate, I. Vodyanoy, and V. Parsegian. 1993. Probability of alamethicin conductance states varies with non-lamellar tendency of bilayer phospholipids. Biophys. J. 65:23-27.
28. Litman, B. 1973. Lipid model membranes. Characterization of mixed phospholipid vesicles. Biochemistry. 12:2545-2554.
29. Liu, F., and P. Chong. 1999. Evidence for a regulatory role of cholesterol superlattices in the hydrolytic activity of secretory phospholipase A2 in lipid membranes. Biochemistry. 38:3867-3873.
30. Lundbaek, J. A., P. Birn, J. Girsham, A. Hansen, and O. Andersen. 1996. Membrane stiffness and channel function. Biochemistry. 35:3825-3830.
31. Marks, A. R. 2002. Ryanodine receptors, FKBP 12, and heart failure. Front. Biosci. 7:970-977.
32. McIntosh, T. J., S. A. Simon, and R. C. MacDonald. 1980. The organization of n-alkanes in lipid bilayers. Biochim. Biophys. Acta. 597:445-463.
33. Menashe, M., G. Romero, R. Biltonen, and D. Lichtenberg. 1986. Hydrolysis of DPPC small unilamellar vesicles by porcine pancreatic phospholipase A2. J. Biol. Chem. 261:5328-5333.
34. Micol, V., P. Sanchez-Pinera, J. Villaliain, A. de Godos, and J. C. Gomez-Fernandez. 1999. Correlation between protein kinase C α activity and membrane phase behavior. Biophys. J. 76:916-927.
35. Opdenkamp, J. A., M. T. Kauerz, and L. L. van Deenen. 1975. Action of pancreatic phospholipase A2 on phosphatidylcholine bilayers in different physical states. Biochim. Biophys. Acta. 406:169-177.
36. Orlova, E., I. Serysheva, S. Hamilton, W. Chiu, and M. van Heel. 1998. The skeletal muscle calcium-release channel visualized by electron microscopy. In The Structure and Function of Ryanodine Receptors. R. Sitsapesan, editor. Imperial College Press, London. 23-47.
37. Pagano, R., R. Cherry, and D. Chapman. 1973. Phase transitions and heterogeneity in lipid bilayers. Science. 181:557-558.
38. Pantoja, R., D. Sigg, R. Blunck, F. Bezanilla, and J. R. Heath. 2001. Bilayer reconstitution of voltage-dependent ion channels using a microfabricated silicon chip. Biophys. J. 81:2389-2394.
39. Papahadjopoulos, D., W. J. Vail, C. Newton, S. Nir, K. Jacobson, G. Poste, and R. Lazo. 1977. Studies on membrane fusion. III. The role of calcium-induced phase changes. Biochim. Biophys. Acta. 465:579-598.
40. Rand, R. P., N. Fuller, V. A. Parsegian, and D. C. Rau. 1998. Variation in hydration forces between neutral phospholipid bilayers: evidence for hydration attraction. Biochemistry. 27:7711-7722.
41. Romsicki, Y., and F. Sharom. 1998. The ATPase and ATP-binding function of P-glycoprotein modulation by interaction with defined phospholipids. Eur. J. Biochem. 256:170-178.
42. Roth, R., R. Evans, and S. Dietrich. 2000. Depletion potential in hardsphere mixtures: theory and applications. Phys. Rev. E Stat. Phys. Plasmas Fluids Relat. Interdiscip. Topics. 62:5360-5377.
43. Sackmann, E. 1995. Biological membranes: architecture and function. In Structure and Dynamics of Membranes: From Cells to Vesicles. Handbook of Biological Physics, Vol. 1. R. Lipowsky and E. Sackmann, editors. Elsevier Science, New York. 1-63.
44. Scarlata, S., and S. Gruner. 1997. Role of PE lipids in the stabilization of protein-lipid contacts. Biophys. Chem. 67:269-279.
45. Scriven, D. R. L., A. Klimek, K. L. Lee, and D. W. Moore. 2002. The molecular architecture of calcium microdomains in rat cardiomyocytes. Ann. N. Y. Acad. Sci. 976:488-499.
46. Shen, Y. M., O. I. Chertihin, R. L. Biltonen, and J. J. Sando. 1999. Lipid-dependent activation of protein kinase C-alpha by normal alcohols. J. Biol. Chem. 274:34036-34044.
47. Slater, S., M. Kelly, F. Taddeo, C. Ho, E. Rubin, and C. Stubbs. 1994. The modulation of protein kinase C activity by membrane lipid bilayer structure. J. Biol. Chem. 269:4866-4871.
48. Small, D. M. 1986. The physical chemistry of lipids. In Handbook of Lipid Research. D. K. Hanaham, editor. Plenum Press, New York. 97-143.
49. Somerharju, P., J. Virtanen, and K. H. Cheng. 1999. Lateral organization of membrane lipids: the superlattice view. Biochim. Biophys. Acta. 1440:32-48.
50. Sonnleitner, A., G. Schutz, and T. Schmidt. 1999. Free Brownian motion of individual lipid molecules in biomembranes. Biophys. J. 77:2638-2642.
51. Stoscheck, C. M. 1990. Quantitation of protein. Methods Enzymol. 182:50-69.
52. Takeshima, H., S. Komazaki, M. Nishi, M. Iino, and K. Kangawa. 2000. Junctophilins: a novel family of junctional membrane complex proteins. Mol. Cell. 6:11-22.
53. Tate, C. A., R. J. Bick, A. Chu, W. B. Van Winkle, and M. L. Entman. 1985. Nucleotide specificity of canine cardiac sarcoplasmic reticulum. GTP-induced calcium accumulation and GTPase activity. J. Biol. Chem. 260:9618-9623.
54. 2+-induced phase separation in phosphatidylserine, phosphatidylethanolamine and phosphatidylcholine mixed membranes. Biochim. Biophys. Acta. 643:276-282.
55. Trokhymchuk, A., D. Henderson, A. Nikolov, and D. T. Wasan. 2001. Entropically driven ordering in a binary colloidal suspension near a planar wall. Phys. Rev. E Stat. Nonlin. Soft Matter. Phys. 64:012401.
56. Upreti, G. C., and M. K. Jain. 1980. Action of phospholipase A2 on unmodified phosphatidylcholine bilayers: organizational defects are preferred sites of action. J. Membr. Biol. 55:113-121.
57. Virtanen, J. A., K. H. Cheng, and P. Somerharju. 1998. Phospholipid composition of the mammalian red cell membrane can be rationalized by a superlattice model. Proc. Natl. Acad. Sci. USA. 95:4964-4969.
58. 2+ channel/dihydropyridine receptor interactions in skeletal muscle. In The Structure and Function of Ryanodine Receptors. R. Sitsapesan, editor. Imperial College Press, London. 95-111.
59. Wilschut, J. C., J. Regts, H. Westenberg, and G. Scherphof. 1978. Action of phospholipases A2 on phosphatidylcholine bilayers. Effects of the phase transition, bilayer curvature and structural defects. Biochim. Biophys. Acta. 508:185-196.
60. Xu, Y. H., K. Gietzen, H. J. Galla, and E. Sackmann. 1983. Protein-mediated lipid transfer. The effects of lipid-phase transition and of charged lipids. Biochem. J. 213:21-24.
61. Zhang, W., and H. Kaback. 2000. Effect of the lipid phase transition on the lactose permease from Escherichia coli. Biochemistry. 39:14538-14542.