Home LiteratureArticle Details
PMID: 12885640 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

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

Biophysical journal ·Vol. 85 ·No. 2 ·2003-08-00 ·Pages 933-42

Cannon B, Hermansson M, Györke S, Somerharju P, Virtanen JA, Cheng KH

Abstract

The sarcoplasmic reticulum channel (ryanodine receptor) from cardiac myocytes was reconstituted into planar lipid bilayers consisting of 1-palmitoyl-2-oleoyl-phosphatidylethanolamine (POPE) and 1-palmitoyl-2-oleoyl-phosphatidylcholine (POPC) in varying ratios. The channel activity parameters, i.e., open probability and average open time and its resolved short and long components, were determined as a function of POPE mole fraction (X(PE)) at 22.4 degrees C. Interestingly, all of these parameters exhibited a narrow and pronounced peak at X(PE) approximately 0.80. Differential scanning calorimetric measurements on POPE/POPC liposomes with increasing X(PE) indicated that the lipid bilayer enters a composition-driven transition from the liquid-crystalline state to the gel state at 22.4 degrees C when X(PE) approaches 0.80. Thus, the peaking of the reconstituted channel activity at X(PE) approximately 0.80 in the planar bilayer could result from the appearance of gel/liquid-crystalline domain boundaries at this POPE content. Lipid packing at domain boundaries is known to be looser as compared to the homogenous gel or liquid-crystalline state. We propose that the attractive potential of packing defects at lipid domain boundaries and entropic excluded-volume effects could result in the direct interactions of the transmembrane region of the channel protein with the lipid-packing defects at the lipid/protein interface, which could thus provide a favorable environment for the open state of the protein. The present findings indicate that the activity of the sarcoplasmic reticulum calcium channel could be modulated by lipid domain formation upon slight changes in membrane lipid composition in vivo.

MeSH Terms
Calcium Channels/chemistry Electric Capacitance Ion Channel Gating Lipid Bilayers/chemistry Membrane Fluidity Membrane Microdomains/chemistry Membrane Potentials Membranes, Artificial Molecular Conformation Phosphatidylcholines/chemistry Phosphatidylethanolamines/chemistry Protein Conformation Ryanodine Receptor Calcium Release Channel/chemistry Structure-Activity Relationship
Chemicals
Calcium Channels Lipid Bilayers Membranes, Artificial Phosphatidylcholines Phosphatidylethanolamines Ryanodine Receptor Calcium Release Channel 1-palmitoyl-2-oleoylphosphatidylethanolamine 1-palmitoyl-2-oleoylphosphatidylcholine
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Cannon Brian
Department of Physics, Texas Tech University, Lubbock, Texas 79409, USA.
Hermansson Martin
Györke Sandor
Somerharju Pentti
Virtanen Jorma A
Cheng Kwan Hon
References (56)
56 references, click to expand
  1. The thickness, composition and structure of some lipid bilayers and natural membranes.
    J Membr Biol. 1971 Sep;5(3):277-96 PMID: 24173132
  2. Abnormal ryanodine receptor channels in malignant hyperthermia.
    Biophys J. 1990 Mar;57(3):471-5 PMID: 2306496
  3. Ca channels in cardiac myocytes: structure and function in Ca influx and intracellular Ca release.
    Cardiovasc Res. 1999 May;42(2):339-60 PMID: 10533572
  4. Lateral organisation of membrane lipids. The superlattice view.
    Biochim Biophys Acta. 1999 Aug 25;1440(1):32-48 PMID: 10477823
  5. Lipid-ion channel interactions: increasing phospholipid headgroup size but not ordering acyl chains alters reconstituted channel behavior.
    J Membr Biol. 1995 May;145(1):13-9 PMID: 7636882
  6. Lipid phase transition in planar bilayer membrane and its effect on carrier- and pore-mediated ion transport.
    Proc Natl Acad Sci U S A. 1980 Jun;77(6):3403-7 PMID: 6158046
  7. Membrane stiffness and channel function.
    Biochemistry. 1996 Mar 26;35(12):3825-30 PMID: 8620005
  8. Variation in hydration forces between neutral phospholipid bilayers: evidence for hydration attraction.
    Biochemistry. 1988 Oct 4;27(20):7711-22 PMID: 3207702
  9. Evidence for a regulatory role of cholesterol superlattices in the hydrolytic activity of secretory phospholipase A2 in lipid membranes.
    Biochemistry. 1999 Mar 30;38(13):3867-73 PMID: 10194297
  10. Impairment of the ryanodine-sensitive calcium release channels in the cardiac sarcoplasmic reticulum and its underlying mechanism during the hypodynamic phase of sepsis.
    Shock. 2001 Jul;16(1):33-9 PMID: 11442313
  11. Phase transitions and heterogeneity in lipid bilayers.
    Science. 1973 Aug 10;181(4099):557-9 PMID: 4721050
  12. Role of phosphatidylethanolamine lipids in the stabilization of protein-lipid contacts.
    Biophys Chem. 1997 Sep 1;67(1-3):269-79 PMID: 9397529
  13. Studies on membrane fusion. III. The role of calcium-induced phase changes.
    Biochim Biophys Acta. 1977 Mar 17;465(3):579-98 PMID: 13835
  14. Fluorescence resonance energy transfer study of the associative state of membrane-bound complexes of complement proteins C5b-8.
    J Immunol. 1985 Jul;135(1):459-64 PMID: 3923109
  15. Deformation free energy of bilayer membrane and its effect on gramicidin channel lifetime.
    Biophys J. 1986 Dec;50(6):1061-70 PMID: 2432948
  16. Detection of phase separation in fluid phosphatidylserine/phosphatidylcholine mixtures.
    Biophys J. 1994 Nov;67(5):1906-11 PMID: 7858127
  17. Visualization of domain formation in the inner and outer leaflets of a phospholipid bilayer.
    J Cell Biol. 1988 Jun;106(6):1885-92 PMID: 3384848
  18. Action of phospholipases A2 on phosphatidylcholine bilayers. Effects of the phase transition, bilayer curvature and structural defects.
    Biochim Biophys Acta. 1978 Apr 4;508(2):185-96 PMID: 565217
  19. The modulation of protein kinase C activity by membrane lipid bilayer structure.
    J Biol Chem. 1994 Feb 18;269(7):4866-71 PMID: 7508929
  20. Phospholipid composition of the mammalian red cell membrane can be rationalized by a superlattice model.
    Proc Natl Acad Sci U S A. 1998 Apr 28;95(9):4964-9 PMID: 9560211
  21. Free Brownian motion of individual lipid molecules in biomembranes.
    Biophys J. 1999 Nov;77(5):2638-42 PMID: 10545363
  22. Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum.
    Am J Physiol. 1983 Jul;245(1):C1-14 PMID: 6346892
  23. Correlation between protein kinase C alpha activity and membrane phase behavior.
    Biophys J. 1999 Feb;76(2):916-27 PMID: 9929493
  24. Shape, size, and distribution of Ca(2+) release units and couplons in skeletal and cardiac muscles.
    Biophys J. 1999 Sep;77(3):1528-39 PMID: 10465763
  25. Hydration at the membrane protein-lipid interface.
    Biophys J. 1992 Oct;63(4):897-902 PMID: 1384744
  26. Action of phospholipase A2 on unmodified phosphatidylcholine bilayers: organizational defects are preferred sites of action.
    J Membr Biol. 1980 Jul 15;55(2):113-21 PMID: 7411590
  27. Hydrolysis of dipalmitoylphosphatidylcholine small unilamellar vesicles by porcine pancreatic phospholipase A2.
    J Biol Chem. 1986 Apr 25;261(12):5328-33 PMID: 3754257
  28. Lipid polymorphism and the roles of lipids in membranes.
    Chem Phys Lipids. 1986 Jun-Jul;40(2-4):127-44 PMID: 3742670
  29. Changes in vesicle morphology induced by lateral phase separation modulate phospholipase A2 activity.
    Biochemistry. 1997 Aug 26;36(34):10551-7 PMID: 9265636
  30. Quantitation of protein.
    Methods Enzymol. 1990;182:50-68 PMID: 2314256
  31. Depletion potential in hard-sphere mixtures: theory and applications
    Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics. 2000 Oct;62(4 Pt B):5360-77 PMID: 11089098
  32. The organization of n-alkanes in lipid bilayers.
    Biochim Biophys Acta. 1980 Apr 24;597(3):445-63 PMID: 6892885
  33. The molecular architecture of calcium microdomains in rat cardiomyocytes.
    Ann N Y Acad Sci. 2002 Nov;976:488-99 PMID: 12502603
  34. The ATPase and ATP-binding functions of P-glycoprotein--modulation by interaction with defined phospholipids.
    Eur J Biochem. 1998 Aug 15;256(1):170-8 PMID: 9746361
  35. Lipid-dependent activation of protein kinase C-alpha by normal alcohols.
    J Biol Chem. 1999 Nov 26;274(48):34036-44 PMID: 10567370
  36. Nucleotide specificity of cardiac sarcoplasmic reticulum. GTP-induced calcium accumulation and GTPase activity.
    J Biol Chem. 1985 Aug 15;260(17):9618-23 PMID: 2991255
  37. The effects of bilayer thickness and tension on gramicidin single-channel lifetime.
    Biochim Biophys Acta. 1983 Oct 26;735(1):95-103 PMID: 6194820
  38. Experimental evidence for hydrophobic matching and membrane-mediated interactions in lipid bilayers containing gramicidin.
    Biophys J. 1999 Feb;76(2):937-45 PMID: 9929495
  39. Molecular basis of mechanotransduction in living cells.
    Physiol Rev. 2001 Apr;81(2):685-740 PMID: 11274342
  40. Entropically driven ordering in a binary colloidal suspension near a planar wall.
    Phys Rev E Stat Nonlin Soft Matter Phys. 2001 Jul;64(1 Pt 1):012401 PMID: 11461307
  41. Effect of the lipid phase transition on the lactose permease from Escherichia coli.
    Biochemistry. 2000 Nov 28;39(47):14538-42 PMID: 11087408
  42. Correlation between bilayer destabilization and activity enhancement by diacylglycerols in reconstituted Ca-ATPase vesicles.
    Arch Biochem Biophys. 1986 Jan;244(1):382-6 PMID: 2936304
  43. Action of pancreatic phospholipase A2 on phosphatidylcholine bilayers in different physical states.
    Biochim Biophys Acta. 1975 Oct 6;406(2):169-77 PMID: 1191645
  44. Gel to liquid-crystalline transition temperatures of water dispersions of two pairs of positional isomers of unsaturated mixed-acid phosphatidylcholines.
    Biochemistry. 1981 Jun 9;20(12):3633-6 PMID: 7260060
  45. Intrinsic curvature hypothesis for biomembrane lipid composition: a role for nonbilayer lipids.
    Proc Natl Acad Sci U S A. 1985 Jun;82(11):3665-9 PMID: 3858841
  46. Lipid model membranes. Characterization of mixed phospholipid vesicles.
    Biochemistry. 1973 Jun 19;12(13):2545-54 PMID: 4350955
  47. Junctophilins: a novel family of junctional membrane complex proteins.
    Mol Cell. 2000 Jul;6(1):11-22 PMID: 10949023
  48. Probability of alamethicin conductance states varies with nonlamellar tendency of bilayer phospholipids.
    Biophys J. 1993 Jul;65(1):23-7 PMID: 8369434
  49. Protein-mediated lipid transfer. The effects of lipid-phase transition and of charged lipids.
    Biochem J. 1983 Jul 1;213(1):21-4 PMID: 6615421
  50. Bilayer reconstitution of voltage-dependent ion channels using a microfabricated silicon chip.
    Biophys J. 2001 Oct;81(4):2389-94 PMID: 11566808
  51. Effect of changing the size of lipid headgroup on peptide insertion into membranes.
    Biophys J. 1997 Jul;73(1):239-44 PMID: 9199788
  52. Ryanodine receptors, FKBP12, and heart failure.
    Front Biosci. 2002 Apr 1;7:d970-7 PMID: 11897558
  53. Attenuation of channel kinetics and conductance by cholesterol: an interpretation using structural stress as a unifying concept.
    J Membr Biol. 1995 Jan;143(1):51-63 PMID: 7714888
  54. The role of cholesterol in the activity of reconstituted Ca-ATPase vesicles containing unsaturated phosphatidylethanolamine.
    J Biol Chem. 1986 Apr 15;261(11):5081-7 PMID: 3007490
  55. Fourier-transform infrared studies of CaATPase partitioning in phospholipid mixtures of 1,2-dipalmitoylphosphatidylcholine-d62 with 1-palmitoyl-2-oleoylphosphatidylethanolamine and 1-stearoyl-2-oleoylphosphatidylcholine.
    Biochemistry. 1985 Jul 2;24(14):3422-8 PMID: 2931112
  56. Ca2+-induced phase separation in phosphatidylserine, phosphatidylethanolamine and phosphatidylcholine mixed membranes.
    Biochim Biophys Acta. 1981 May 6;643(2):276-82 PMID: 6261813
Article Info
Journal
Biophysical journal
Abbr.
Biophys J
ISSN
0006-3495
Published
2003-08-00
Pages
933-42
Language
English
Region
United States
NLM ID
0370626
PMCID
PMC1303214
Subset
IM
Grants
NHLBI NIH HHS · HL-52620 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]