Skip to main content
SpringerLink
Log in

Insulin stimulates turnover of phosphatidylcholine in rat adipocytes

  • Published:
Molecular and Cellular Biochemistry Aims and scope Submit manuscript

Abstract

The present study investigated the effect of insulin on phosphatidylcholine turnover in rat adipocytes labelled to equilibrium with [14C]-choline. Insulin induced a rapid turnover of this major phospholipid that was maximal by 1 min and transient in nature. Following a 1 min stimulation of the cells with insulin at a maximally effective concentration (7 nM), a 4–6% decrease in the percentage of total cellular choline associated with this phospholipid was observed. This reflected a significant transient increase in the percentage of total cellular choline associated with phosphorylcholine, which together with diacylglycerol are the phospholipase C cleavage products of phosphatidylcholine. These effects were observed over a physiological range of insulin concentrations. No effect of insulin on any other choline phospholipid or metabolite (sphingomyelin, lysophophatidylcholine, glycerophosphocholine or choline) was seen. These results suggest that insulin stimulates a phospholipase C-mediated turnover of phosphatidylcholine in rat adipocytes. The rapid nature of this turnover suggests a potential role in signal transduction.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Abdel-Latif AA: Calcium mobilizing receptors polyphosphoinosides and the generation of second messengers. Pharmacol Rev 38:227–272, 1986

    Google Scholar 

  2. Berridge MJ: Inositol trisphosphate and calcium signalling. Nature 361:315–325, 1993

    Google Scholar 

  3. Downes CP: Cellular functions of myoinositol. Biochem soc Trans 17:259–268, 1989

    Google Scholar 

  4. Farese RV, Kuo JY, Babischkin JS, Davis JS: Insulin provokes a transient activation of phospholipase C in the rat epididymal fat pad. J Biol Chem 261:8589–8592, 1986

    Google Scholar 

  5. Farese RV, Standaert ML, Barnes DE, Davis JS, Pollet RJ: Phorbol ester provokes insulin-like effects on glucose transport, amino acid uptake and pyruvate dehydrogenase activity in BC3H-1 myocytes. Endocrinology 116:2650–2655, 1985

    Google Scholar 

  6. Farese RV, Cooper DR, Konda TS, Nair G, Standaert ML, Pollet RJ: Mechanisms whereby insulin increases diacylglycerol in BC3H-1 myocytes. Biochem J 256, 185–188, 1988

    Google Scholar 

  7. Cheriqui G, Caron M, Wicek D, Lascols O, Capeau J, Picard J: Decreased insulin responsiveness in fat cells rendered protein kinase C deficient by treatment with a phorbol ester. Endocrinology 118: 1759–1769, 1986

    Google Scholar 

  8. Koepfer-Hobelsberger B, Wieland OJ: Insulin activates phospholipase C in fat cells: Similarity with the activation of pyruvate dehydrogenase. Mol Cell Endocrinol 36:123–129, 1984

    Google Scholar 

  9. Saltiel AR, Sherline P, Fox JA: Insulin-stimulated diacylglycerol production results from hydrolysis of a novel phosphatidylinositol glycan. J Biol Chem 262:1116–1121, 1987

    Google Scholar 

  10. Augert G, Exton JH: Insulin and oxytocin effects on phosphoinositide metabolism in adipocytes. J Biol Chem 263:3600–3609, 1988

    Google Scholar 

  11. Etindi R, Fain JN: Insulin does not activate a phosphoinositide-specific phospholipase C in adipocytes. Mol Cell Endocrinol, 67:149–153, 1989

    Google Scholar 

  12. Sakai M, Wells WW: Action of insulin on the subcellular metabolism of polyphosphoinositides in rat hepatocytes. J Biol Chem 261: 10058–10062, 1986

    Google Scholar 

  13. Kelly KL, Mato JM, Merida I, Jarett L: Glucose transport and antilipolysis are differentially regulated by the polar head group of an insulin-sensitive glycophospholipid. Proc Natl Acad Sci USA 84: 6404–6407, 1987

    Google Scholar 

  14. Mato JM, Kelly KL, Abler A, Jarett L: Identification of a novel insulin sensitive glycophospholipid from H35 hepatoma cells. J Biol Chem 262:2131–2137, 1987

    Google Scholar 

  15. Macaulay SL, Larkins RG: Phospholipase C mimics insulin action on pyruvate dehydrogenase and insulin mediator generation but not glucose transport or utilization. Cell Sig 2:9–19, 1990

    Google Scholar 

  16. Macaulay SL, Larkins RG: Isolation of an insulin sensitive phosphatidylinositol-glycan from rat adipocytes. Biochem J 271:427–435, 1990

    Google Scholar 

  17. Romero G, Luttrell L, Rogol A, Zeller K, Hewlett E, Larner J: Phosphatidylinositol-glycan anchors of membrane proteins: Potential precursors of insulin mediators. Science 240:509–511, 1988

    Google Scholar 

  18. Saltiel AR, Fox JA, Sherline P, Cauatecasas P: Insulin stimulated hydrolysis of a novel glycolipid generates modulators of cAMP phosphodiesterase. Science 233:967–972, 1986

    Google Scholar 

  19. Jarett L, Wong EHA, Macaulay SL, Smith JA: Insulin mediators from rat skeletal muscle have differential effects on insulin-sensitive pathways of intact adipocytes. Science 227:533–535, 1985

    Google Scholar 

  20. Stralfors P: Insulin stimulation of glucose uptake can be mediated by diacylglycerol in adipocytes. Nature 335:554–556, 1988

    Google Scholar 

  21. Besterman JM, Duronio V, Cuatrecasas P: Rapid formation of diacylglycerol from phosphatidylcholine: A pathway for generation of a second messenger. Proc Natl Acad Sci 83:6785–6789, 1986

    Google Scholar 

  22. Irving HR, Exton JH: Phospharidylcholine breakdown in rat liver plasma membranes. J Biol Chem 262:11764–11770, 1987

    Google Scholar 

  23. Martin TW, Michaelis K: P2-purinergic agonists stimulate phosphodiesteratic cleavage of phosphatidylcholine in endothelial cells. J Biol Chem 264:8847–8856, 1989

    Google Scholar 

  24. Nair GP, Standaert ML, Pollet RJ, Cooper DR: Effects of insulin and phorbol esters on diacylglycerol generation and synthesis and hydrolysis of phosphatidylcholine in BC3H1 myocytes. Biochem Biophys Res Commun 154:1345–1349, 1988

    Google Scholar 

  25. Kelly KL, Gutierrez G, Martin A: Hormonal regulation of phosphatidylcholine synthesis by reversible modulation of cytidylyl transferase. Biochem J 255:693–698, 1988

    Google Scholar 

  26. Rodbell M: Metabolism of isolated fat cells: II The similar effects of phospholipase C and of insulin on glucose and amino acid metabolism. J Biol Chem 239:375–380, 1964

    Google Scholar 

  27. Alvarez JF, Varela L, Ruiz-Albus JM, Mato JM: Localization of the insulin sensitive phosphatidylinositol glycan at the outer surface of the cell membrane. Biochem Biophys Res Commun 152:1455–1462, 1988

    Google Scholar 

  28. Dunlop ME, Metz SA: A phospholipase D-like mechanism in pancreatic islet cells. Biochem Biophys Res Commun 163:922–928, 1989

    Google Scholar 

  29. Standaert ML, Farese RV, Cooper DR, Pollet RJ: Insulin induced glycerolipid mediators and the stimulation of glucose transport in BC3H-1 myocytes. J Biol Chem 263:8696–8705, 1988

    Google Scholar 

  30. Nishizuka Y: Turnover of inositol phospholipids and signal transduction. Science 225:1365–1370, 1984

    Google Scholar 

  31. Spach DH, Nemenhoff RA, Blackshear PJ: Protein phosphorylation and protein kinase activities in BC3H-1 myocytes. J Biol Chem 261: 1116–1121, 1986

    Google Scholar 

  32. Cooper DR, Konda TS, Standaert ML, Davis JS, Pollet RJ, Farese RV: Insulin increases membrane and cytosolic protein kinase C activity in BC3H-1 myocytes. J Biol Chem 262:3633–3639, 1987

    Google Scholar 

  33. Draznin B, Leitner JW, Sussman KE, Sherman NA: Insulin and glucose modulate protein kinase C activity in rat adipocytes. Biochem Biophys Res Commun 156:570–575, 1988

    Google Scholar 

  34. Egan JJ, Saltis J, Wek SA, Simpson IA, Londos C: Insulin, oxytocin and vasopressin stimulate protein kinase C activity in adipocyte plasma membranes. Proc Natl Acad Sci USA 87:1052–1056, 1990

    Google Scholar 

  35. Blackshear PJ, McNeill Haupt D, Stumpo DJ: Insulin activation of protein kinase C: A reassessment. J Biol Chem 266:10946–10952, 1991

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. CSIRO Division of Biomolecular Engineering, 343 Royal Pde., 3052, Parkville, Victoria, Australia

    S. Lance Macaulay

  2. Department of Medicine, Royal Melbourne Hospital, University of Melbourne, Grattan Street 343 Royal Pde., 3050, Parkville, Australia

    S. Lance Macaulay & Richard G. Larkins

Authors
  1. S. Lance Macaulay
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Richard G. Larkins
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Macaulay, S.L., Larkins, R.G. Insulin stimulates turnover of phosphatidylcholine in rat adipocytes. Mol Cell Biochem 136, 23–28 (1994). https://doi.org/10.1007/BF00931600

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00931600

Key words

Search

Navigation