Beta-Adrenergic Receptor Agonists Increase Phospholipid Methylation, Membrane Fluidity, and Beta-adrenergic Receptor-adenylate Cyclase Coupling

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1979 Jan 1

PMID 34151

Citations 65

Authors

F Hirata

W J Strittmatter

J Axelrod

Affiliations

Soon will be listed here.

Abstract

The beta-adrenergic agonist L-isoproterenol stimulated the enzymic synthesis of phosphatidyl-N-monomethylethanolamine and phosphatidylcholine in rat reticulocyte ghosts containing the methyl donor S-adenosyl-L-methionine. The stimulation was stereospecific, dose-dependent, and inhibited by the beta-adrenergic agonist propranolol. The addition of GTP inside the resealed ghosts shifted the dose-response of phospholipid methylation by L-isoproterenol to the left by 2 orders of magnitude. Direct stimulation of adenylate cyclase [ATP pyrophosphate-lyase (cyclizing), EC 4.6.1.1] with sodium fluoride or cholera toxin did not increase the methylation of phospholipids. At a concentration of S-adenosyl-L-methionine that stimulates synthesis of phosphatidyl-N-monomethylethanolamine, the activity of isoproterenol-sensitive adenylate cyclase was increased 2-fold without changes in the basal activity of adenylate cyclase and the number of beta-adrenergic receptors. The increase of phospholipid methylation by L-isoproterenol decreased membrane viscosity and increased translocation of methylated lipids. These findings indicate that enhancement of phospholipid methylation by L-isoproterenol decreases membrane microviscosity and thus increases lateral movement of the beta-adrenergic receptors and coupling with adenylate cyclase.

Citing Articles

Erythrocytes membrane fluidity changes induced by adenylyl cyclase cascade activation: study using fluorescence recovery after photobleaching.

Semenov A, Lugovtsov A, Rodionov S, Maksimov E, Priezzhev A, Shirshin E Eur Biophys J. 2024; 53(4):239-247.

PMID: 38625405 PMC: 11098875. DOI: 10.1007/s00249-024-01707-x.

Protein kinase A activity and NO are involved in the regulation of crucian carp (Carassius carassius) red blood cell osmotic fragility.

Andreyeva A, Kladchenko E, Sudnitsyna J, Krivchenko A, Mindukshev I, Gambaryan S Fish Physiol Biochem. 2021; 47(4):1105-1117.

PMID: 34052972 DOI: 10.1007/s10695-021-00971-4.

Synthesis of phosphatidylcholine through phosphatidylethanolamine N-methylation in tissues of the mussel Mytilus galloprovincialis.

Athamena A, Trajkovic-Bodennec S, Brichon G, Zwingelstein G, Bodennec J Lipids. 2011; 46(12):1141-54.

PMID: 21769692 DOI: 10.1007/s11745-011-3590-9.

Cognitive impairment in folate-deficient rats corresponds to depleted brain phosphatidylcholine and is prevented by dietary methionine without lowering plasma homocysteine.

Troen A, Chao W, Crivello N, DAnci K, Shukitt-Hale B, Smith D J Nutr. 2008; 138(12):2502-9.

PMID: 19022979 PMC: 2755637. DOI: 10.3945/jn.108.093641.

A model for modulation of neuronal synchronization by D4 dopamine receptor-mediated phospholipid methylation.

Kuznetsova A, Deth R J Comput Neurosci. 2007; 24(3):314-29.

PMID: 17929154 DOI: 10.1007/s10827-007-0057-3.

References

Blostein R, Chu L . Sidedness of (sodium, potassium)-adenosine triphosphate of inside-out red cell membrane vesicles. Interactions with potassium. J Biol Chem. 1977; 252(9):3035-43. View

Klein I, Moore L, Pastan I . Effect of liposomes containing cholesterol on adenylate cyclase activity of cultured mammalian fibroblasts. Biochim Biophys Acta. 1978; 506(1):42-53. DOI: 10.1016/0005-2736(78)90433-9. View

Lyles D, Landsberger F . Sendai virus-induced hemolysis: reduction in heterogeneity of erythrocyte lipid bilayer fluidity. Proc Natl Acad Sci U S A. 1977; 74(5):1918-22. PMC: 431043. DOI: 10.1073/pnas.74.5.1918. View

Bilezikian J, Spiegel A, Brown E, Aurbach G . Identification and persistence of beta adrenergic receptors during maturation of the rat reticulocyte. Mol Pharmacol. 1977; 13(5):775-85. View

Bilezikian J, Spiegel A, Gammon D, Aurbach G . The role of guanyl nucleotides in the expression on of catecholamine-responsive adenylate cyclase during maturation of the rat reticulocyte. Mol Pharmacol. 1977; 13(5):786-95. View

Hirata F, Viveros O, Diliberto Jr E, Axelrod J . Identification and properties of two methyltransferases in conversion of phosphatidylethanolamine to phosphatidylcholine. Proc Natl Acad Sci U S A. 1978; 75(4):1718-21. PMC: 392410. DOI: 10.1073/pnas.75.4.1718. View

Hirata F, Axelrod J . Enzymatic synthesis and rapid translocation of phosphatidylcholine by two methyltransferases in erythrocyte membranes. Proc Natl Acad Sci U S A. 1978; 75(5):2348-52. PMC: 392550. DOI: 10.1073/pnas.75.5.2348. View

Steiner A, KIPNIS D, UTIGER R, Parker C . Radioimmunoassay for the measurement of adenosine 3',5'-cyclic phosphate. Proc Natl Acad Sci U S A. 1969; 64(1):367-73. PMC: 286171. DOI: 10.1073/pnas.64.1.367. View

Cuatrecasas P . Membrane receptors. Annu Rev Biochem. 1974; 43(0):169-214. DOI: 10.1146/annurev.bi.43.070174.001125. View

10.

Steck T, Kant J . Preparation of impermeable ghosts and inside-out vesicles from human erythrocyte membranes. Methods Enzymol. 1974; 31:172-80. DOI: 10.1016/0076-6879(74)31019-1. View

11.

Shinitzky M, Barenholz Y . Dynamics of the hydrocarbon layer in liposomes of lecithin and sphingomyelin containing dicetylphosphate. J Biol Chem. 1974; 249(8):2652-7. View

12.

Puchwein G, Pfeuffer T, Helmreich E . Uncoupling of catecholamine activation of pigeon erythrocyte membrane adenylate cyclase by filipin. J Biol Chem. 1974; 249(10):3232-40. View

13.

Hirata F, Axelrod J . Enzymatic methylation of phosphatidylethanolamine increases erythrocyte membrane fluidity. Nature. 1978; 275(5677):219-20. DOI: 10.1038/275219a0. View

14.

Williams L, JARETT L, Lefkowitz R . Adipocyte beta-adrenergic receptors. Identification and subcellular localization by (-)-[3H]dihydroalprenolol binding. J Biol Chem. 1976; 251(10):3096-104. View