Home LiteratureArticle Details
PMID: 7612831 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

Phospholipase A2 as a mechanosensor.

Biophysical journal ·Vol. 68 ·No. 5 ·1995-05-00 ·Pages 1888-94

Lehtonen JY, Kinnunen PK

Abstract

Osmotic swelling of large unilamellar vesicles (LUVs) causes membrane stretching and thus reduces the lateral packing of lipids. This is demonstrated to modulate strongly the catalytic activity of phospholipase A2 (PLA2) toward a fluorescent phospholipid, 1-palmitoyl-2-[(6-pyren-1-yl)]decanoyl-sn-glycero-3-phosphocholine (PPDPC) residing in LUVs composed of different unsaturated and saturated phosphatidylcholines. The magnitude of the osmotic pressure gradient delta omega required for maximal PLA2 activity as well as the extent of activation depend on the degree of saturation of the membrane phospholipid acyl chains. More specifically, delta omega needed for maximal hydrolytic activity increases in the sequence DOPC < SOPC < DMPC in accordance with the increment in the intensity of chain-chain van der Waals interactions. Previous studies on the hydrolysis of substrate monolayers by C. adamanteus and N. naja PLA2 revealed maximal hydrolytic rates for these two enzymes to be achieved at lipid packing densities corresponding to surface pressures of 12 and 18 mN m-1, respectively. In keeping with the above the magnitudes of delta omega producing maximal activity of Crotalus adamanteus and Naja naja toward PPDPC/DMPC LUVs were 40 and 20 mOsm/kg, respectively. Our findings suggest a novel possibility of regulating the activity of PLA2 and perhaps also other lipid packing density-dependent enzymes in vivo by osmotic forces applied on cellular membranes. Importantly, our results reveal serendipitously that the responsiveness of membranes to osmotic stress is modulated by the acyl chain composition of the lipids.

MeSH Terms
Animals Crotalus Elapidae Fluorescent Dyes Kinetics Liposomes Osmolar Concentration Phosphatidylcholines Phospholipases A/metabolism Phospholipases A2
Chemicals
Fluorescent Dyes Liposomes Phosphatidylcholines 1-palmitoyl-2-pyrenedecanoylphosphatidylcholine Phospholipases A Phospholipases A2
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Lehtonen J Y
Department of Medical Chemistry, FIN-00014 University of Helsinki, Finland.
Kinnunen P K
References (74)
74 references, click to expand
  1. Mechanotransduction across the cell surface and through the cytoskeleton.
    Science. 1993 May 21;260(5111):1124-7 PMID: 7684161
  2. Effects of sphingosine on peripheral membrane interactions: comparison of adriamycin, cytochrome c, and phospholipase A2.
    Biochemistry. 1993 May 25;32(20):5373-80 PMID: 8388718
  3. Mechanosensitive channels transduce osmosensitivity in supraoptic neurons.
    Nature. 1993 Jul 22;364(6435):341-3 PMID: 7687327
  4. Rate-limiting step in electron transport. Osmotically sensitive diffusion of quinones through voids in the bilayer.
    J Biol Chem. 1993 Jul 25;268(21):15442-54 PMID: 8340373
  5. Phase separated anionic domains in ternary mixed lipid monolayers at the air-water interface.
    Chem Phys Lipids. 1993 Apr;65(1):31-42 PMID: 8348675
  6. Sensitivity of phospholipase C (Bacillus cereus) activity to lipid packing in sonicated lipid mixtures.
    Biochemistry. 1993 Aug 24;32(33):8547-52 PMID: 7689334
  7. Protein tyrosine phosphorylation is involved in osmoregulation of ionic conductances.
    J Biol Chem. 1993 Sep 25;268(27):19919-22 PMID: 7690749
  8. Influence of plasma on the osmotic sensitivity of large unilamellar vesicles prepared by extrusion.
    J Biol Chem. 1994 Mar 11;269(10):7364-70 PMID: 8125954
  9. Osmotic regulation of gene action.
    Proc Natl Acad Sci U S A. 1994 Mar 1;91(5):1657-61 PMID: 8127862
  10. Effect of monolayer surface pressure on the activities of phosphoinositide-specific phospholipase C-beta 1, -gamma 1, and -delta 1.
    Biochemistry. 1994 Mar 15;33(10):3032-7 PMID: 8130216
  11. Lateral tensions and pressures in membranes and lipid monolayers.
    Biochim Biophys Acta. 1982 Jun 14;688(2):572-80 PMID: 7104340
  12. The interaction of phospholipid membranes with poly(ethylene glycol). Vesicle aggregation and lipid exchange.
    Biochim Biophys Acta. 1982 Jun 14;688(2):645-52 PMID: 6896656
  13. Action of lipoprotein lipase on mixed triacylglycerol/phosphatidylcholine monolayers. Activation by apolipoprotein C-II.
    J Biol Chem. 1983 May 10;258(9):5477-82 PMID: 6853529
  14. Mechanism of poly(ethylene glycol) interaction with proteins.
    Biochemistry. 1985 Nov 19;24(24):6756-62 PMID: 4074726
  15. Hydrolysis of dipalmitoylphosphatidylcholine large unilamellar vesicles by porcine pancreatic phospholipase A2.
    J Biol Chem. 1986 Apr 25;261(12):5334-40 PMID: 3754258
  16. The osmotic response of large unilamellar vesicles studied by quasielastic light scattering.
    Biochim Biophys Acta. 1986 Nov 17;862(2):379-86 PMID: 3778898
  17. Hydrolysis of 1-palmitoyl-2-[6-(pyren-1-yl)]hexanoyl-sn-glycero- 3-phospholipids by phospholipase A2: effect of the polar head-group.
    Biochim Biophys Acta. 1987 Feb 23;917(3):411-7 PMID: 3801511
  18. Pressure-sensitive ion channel in Escherichia coli.
    Proc Natl Acad Sci U S A. 1987 Apr;84(8):2297-301 PMID: 2436228
  19. Triggering of the activity of phospholipase A2 by an electric field.
    Biochemistry. 1987 Aug 11;26(16):4907-10 PMID: 3663632
  20. The elasticity of uniform, unilamellar vesicles of acidic phospholipids during osmotic swelling is dominated by the ionic strength of the media.
    Biochemistry. 1987 Aug 25;26(17):5439-47 PMID: 3676261
  21. Control of the action of phospholipases A by "vertical compression" of the substrate monolayer.
    Biochemistry. 1987 Sep 8;26(18):5816-9 PMID: 3676292
  22. Function follows form: generation of intracellular signals by cell deformation.
    FASEB J. 1991 Apr;5(7):2013-9 PMID: 1707019
  23. Role of phospholipase in generating lipid second messengers in signal transduction.
    FASEB J. 1991 Apr;5(7):2068-77 PMID: 1901288
  24. Poly(ethylene glycol)-induced lipid mixing but not fusion between synthetic phosphatidylcholine large unilamellar vesicles.
    Biochemistry. 1991 Apr 30;30(17):4193-200 PMID: 2021611
  25. Bilayer packing stress and defects in mixed dilinoleoylphosphatidylethanolamine and palmitoyloleoylphosphatidylcholine and their susceptibility to phospholipase A2.
    Biochemistry. 1991 May 7;30(18):4516-21 PMID: 2021642
  26. The elasticity of synthetic phospholipid vesicles obtained by photon correlation spectroscopy.
    Biochemistry. 1991 Jun 11;30(23):5688-96 PMID: 2043611
  27. Synergistic action of diacylglycerol and unsaturated fatty acid for protein kinase C activation: its possible implications.
    Proc Natl Acad Sci U S A. 1991 Jun 15;88(12):5149-53 PMID: 1905018
  28. Changes in the lipid dynamics of liposomal membranes induced by poly(ethylene glycol): free volume alterations revealed by inter- and intramolecular excimer-forming phospholipid analogs.
    Biophys J. 1994 Jun;66(6):1981-90 PMID: 8075332
  29. Identification of a defect in the phospholipase D/diacylglycerol pathway in cellular senescence.
    J Biol Chem. 1994 Oct 21;269(42):26040-4 PMID: 7929315
  30. Lipid bilayer heterogeneities and modulation of phospholipase A2 activity.
    Chem Phys Lipids. 1994 Sep 6;73(1-2):209-22 PMID: 8001182
  31. Poly(ethylene glycol)-induced and temperature-dependent phase separation in fluid binary phospholipid membranes.
    Biophys J. 1995 Feb;68(2):525-35 PMID: 7696506
  32. Action of phospholipase A at interfaces.
    J Biol Chem. 1973 Jun 10;248(11):4023-34 PMID: 4736081
  33. Action of pancreatic phospholipase A2 on phosphatidylcholine bilayers in different physical states.
    Biochim Biophys Acta. 1975 Oct 6;406(2):169-77 PMID: 1191645
  34. Characterization and physical properties of the major form of phospholipase A2 from cobra venom (Naja naja naja) that has a molecular weight of 11,000.
    J Biol Chem. 1975 Dec 10;250(23):9008-12 PMID: 1194273
  35. Kinetic analysis of phospholipase A2 activity toward mixed micelles and its implications for the study of lipolytic enzymes.
    J Biol Chem. 1975 Dec 10;250(23):9013-20 PMID: 1194274
  36. Effects of colipase and taurodeoxycholate on the catalytic and physical properties of pancreatic lipase B at an oil water interface.
    J Biol Chem. 1976 Jan 25;251(2):378-83 PMID: 1388
  37. Effects of local anaesthetics on phospholipases.
    Biochim Biophys Acta. 1976 Jul 20;441(1):93-102 PMID: 952985
  38. Increase in membrane fluidity in liposomes and plant protoplasts upon osmotic swelling.
    Biochim Biophys Acta. 1979 Feb 2;550(3):546-9 PMID: 420831
  39. Regulation of phospholipase A2 activity by the lipid-water interface: a monolayer approach.
    Biochemistry. 1979 Jun 26;18(13):2691-7 PMID: 573135
  40. Hydrolysis of mixed monomolecular films of triglyceride/lecithin by pancreatic lipase.
    J Biol Chem. 1979 Oct 25;254(20):10090-4 PMID: 489586
  41. Correlation of enzymatic activity and anticoagulant properties of phospholipase A2.
    Eur J Biochem. 1980 Nov;112(1):25-32 PMID: 7449762
  42. Protooncogene induction and reprogramming of cardiac gene expression produced by pressure overload.
    Proc Natl Acad Sci U S A. 1988 Jan;85(2):339-43 PMID: 2963328
  43. Stretch-inactivated ion channels coexist with stretch-activated ion channels.
    Science. 1989 Feb 10;243(4892):807-9 PMID: 2536958
  44. Enzymatic and physical characterization of diacylglycerol-phosphatidylcholine interactions in bilayers and monolayers.
    Biochemistry. 1989 Jan 10;28(1):32-40 PMID: 2706255
  45. Lipid-lipid interactions as regulators of carboxylester lipase activity.
    J Biol Chem. 1989 May 25;264(15):8612-8 PMID: 2722791
  46. A sensitive and continuous fluorometric assay for phospholipase A2 using pyrene-labeled phospholipids in the presence of serum albumin.
    Anal Biochem. 1989 Feb 15;177(1):103-9 PMID: 2742139
  47. Conformations and orientations of a signal peptide interacting with phospholipid monolayers.
    Biochemistry. 1989 Apr 4;28(7):2789-97 PMID: 2525918
  48. Osmoelastic coupling in biological structures: decrease in membrane fluidity and osmophobic association of phospholipid vesicles in response to osmotic stress.
    Biochemistry. 1989 May 2;28(9):3710-5 PMID: 2546579
  49. Signaling through phosphatidylcholine breakdown.
    J Biol Chem. 1990 Jan 5;265(1):1-4 PMID: 2104616
  50. Regulation of ornithine decarboxylase expression by anisosmotic shock in alpha-difluoromethylornithine-resistant L1210 cells.
    J Biol Chem. 1990 Mar 5;265(7):4025-32 PMID: 2105957
  51. Exclusion of poly(ethylene glycol) from liposome surfaces.
    Biochim Biophys Acta. 1990 Mar;1022(3):303-10 PMID: 2156556
  52. Mechanosensitive ion channels.
    J Membr Biol. 1990 Feb;113(2):93-107 PMID: 1690807
  53. Hydrolytic action of phospholipase A2 in monolayers in the phase transition region: direct observation of enzyme domain formation using fluorescence microscopy.
    Biochim Biophys Acta. 1990 Apr 30;1023(3):365-79 PMID: 2334729
  54. A novel transglutaminase-mediated post-translational modification of phospholipase A2 dramatically increases its catalytic activity.
    J Biol Chem. 1990 Oct 5;265(28):17180-8 PMID: 1976627
  55. Mechanosensitive ion channels of E. coli activated by amphipaths.
    Nature. 1990 Nov 15;348(6298):261-3 PMID: 1700306
  56. Activation of protein kinase C in lipid monolayers.
    J Biol Chem. 1991 Jan 5;266(1):40-4 PMID: 1985909
  57. Mechanical loading stimulates cell hypertrophy and specific gene expression in cultured rat cardiac myocytes. Possible role of protein kinase C activation.
    J Biol Chem. 1991 Jan 15;266(2):1265-8 PMID: 1702436
  58. Small-volume extrusion apparatus for preparation of large, unilamellar vesicles.
    Biochim Biophys Acta. 1991 Jan 30;1061(2):297-303 PMID: 1998698
  59. Activation of phospholipase A2 by adriamycin in vitro. Role of drug-lipid interactions.
    J Biol Chem. 1991 Apr 5;266(10):6302-7 PMID: 2007582
  60. Structure of recombinant human rheumatoid arthritic synovial fluid phospholipase A2 at 2.2 A resolution.
    Nature. 1991 Jul 4;352(6330):79-82 PMID: 2062381
  61. The role of phospholipases and phospholipid-derived signals in cell activation.
    Curr Opin Cell Biol. 1991 Apr;3(2):206-12 PMID: 1652988
  62. Cell volume in the regulation of hepatic function: a mechanism for metabolic control.
    Biochim Biophys Acta. 1991 Dec 12;1071(4):331-50 PMID: 1661157
  63. Molecular motions and dynamics of a diunsaturated acyl chain in a lipid bilayer: implications for the role of polyunsaturation in biological membranes.
    Biochemistry. 1992 Apr 7;31(13):3377-85 PMID: 1554719
  64. Conformation of phosphatidylcholine in neat and cholesterol-containing liquid-crystalline bilayers. Application of a novel method.
    Biochemistry. 1992 Sep 15;31(36):8560-5 PMID: 1390642
  65. Intracellular signaling by hydrolysis of phospholipids and activation of protein kinase C.
    Science. 1992 Oct 23;258(5082):607-14 PMID: 1411571
  66. E/M dips. Evidence for lipids regularly distributed into hexagonal super-lattices in pyrene-PC/DMPC binary mixtures at specific concentrations.
    Biophys J. 1992 Oct;63(4):903-10 PMID: 1420934
  67. Controlling lipase stereoselectivity via the surface pressure.
    J Biol Chem. 1993 Jan 15;268(2):792-4 PMID: 8419355
  68. Role of lateral phase separation in the modulation of phospholipase A2 activity.
    Biochemistry. 1993 Jan 19;32(2):583-9 PMID: 8422369
  69. Phospholipase C: a putative mechanotransducer for endothelial cell response to acute hemodynamic changes.
    Biochem Biophys Res Commun. 1993 Jan 29;190(2):576-81 PMID: 8427600
  70. New insights on mammalian phospholipase A2(s); comparison of arachidonoyl-selective and -nonselective enzymes.
    FASEB J. 1993 Feb 1;7(2):339-48 PMID: 8440410
  71. An osmosensing signal transduction pathway in yeast.
    Science. 1993 Mar 19;259(5102):1760-3 PMID: 7681220
  72. Osmotic properties of large unilamellar vesicles prepared by extrusion.
    Biophys J. 1993 Feb;64(2):443-53 PMID: 8457670
  73. Mechanical stretch rapidly activates multiple signal transduction pathways in cardiac myocytes: potential involvement of an autocrine/paracrine mechanism.
    EMBO J. 1993 Apr;12(4):1681-92 PMID: 8385610
  74. Conformational changes in oxidized phospholipids and their preferential hydrolysis by phospholipase A2: a monolayer study.
    Biochemistry. 1993 May 11;32(18):4962-7 PMID: 8490032
Article Info
Journal
Biophysical journal
Abbr.
Biophys J
ISSN
0006-3495
Published
1995-05-00
Pages
1888-94
Language
English
Region
United States
NLM ID
0370626
PMCID
PMC1282092
Subset
IM
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]