Sustained diacylglycerol accumulation resulting from prolonged G protein-coupled receptor agonist-induced phosphoinositide breakdown in hepatocytes

Journal of Cellular Biochemistry

Volumn 94, Issue 2, 2005, Pages 389-402

  Nilssen, Laila Sortvik ^a,b   Dajani, Olav ^a   Christoffersen, Thoralf ^a   Sandnes, Dagny ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

Author keywords

Diacylglycerol; G protein coupled receptors; Hepatocytes; Phospholipase C; Phospholipase D

Indexed keywords

ANGIOTENSIN; BUTANOL; DIACYLGLYCEROL; G PROTEIN COUPLED RECEPTOR; INOSITOL 1,4,5 TRISPHOSPHATE; NORADRENALIN; PHOSPHATIDIC ACID; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLINOSITIDE; PHOSPHATIDYLINOSITOL 4 PHOSPHATE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PHOSPHOLIPASE C; PHOSPHOLIPASE D; PROSTAGLANDIN F2 ALPHA; VASOPRESSIN; WORTMANNIN; 1,2-DIACYLGLYCEROL; ANDROSTANE DERIVATIVE; ANGIOTENSIN II; OXYTOCIC AGENT; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLINOSITOL 4-PHOSPHATE; POLYPHOSPHOINOSITIDE; PROTEIN KINASE INHIBITOR; VASOCONSTRICTOR AGENT; VASOPRESSIN DERIVATIVE;

ANIMAL CELL; ARTICLE; CATALYSIS; CONTROLLED STUDY; DESENSITIZATION; ENZYME ACTIVITY; HALF LIFE TIME; HYDROLYSIS; LIVER CELL; MALE; NONHUMAN; PHOSPHOINOSITIDE METABOLISM; PRIORITY JOURNAL; RAT; RECEPTOR UPREGULATION; ANIMAL; CELL CULTURE; CYTOLOGY; DRUG EFFECT; DRUG POTENTIATION; ENZYME ACTIVATION; METABOLISM; WISTAR RAT;

1-BUTANOL; ANDROSTADIENES; ANGIOTENSIN II; ANIMALS; CELLS, CULTURED; DIGLYCERIDES; DINOPROST; ENZYME ACTIVATION; HEPATOCYTES; MALE; NOREPINEPHRINE; OXYTOCICS; PHOSPHATIDIC ACIDS; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PHOSPHATIDYLINOSITOL PHOSPHATES; PHOSPHATIDYLINOSITOLS; PHOSPHOLIPASE C; PHOSPHOLIPASE D; PROTEIN KINASE INHIBITORS; RATS; RATS, WISTAR; RECEPTORS, G-PROTEIN-COUPLED; VASOCONSTRICTOR AGENTS; VASOPRESSINS;

EID: 18444375296     PISSN: 07302312     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcb.20260     Document Type: Article

References (79)

1. Ackermann KE, Gish BG, Honchar MP, Sherman WR. 1987. Evidence that inositol 1-phosphate in brain of lithium-treated rats results mainly from phosphatidylinositol metabolism. Biochem J 242:517-524.
2. Allan CJ, Exton JH. 1993. Quantification of inositol phospholipid breakdown in isolated rat hepatocytes. Biochem J 290:865-872.
3. Augert G, Blackmore P, Exton J. 1989a. Changes in the concentration and fatty acid composition of phosphoinositides induced by hormones in hepatocytes. J Biol Chem 264:2574-2580.
4. Augert G, Bocckino SB, Blackmore PF, Exton JH. 1989b. Hormonal stimulation of diacylglycerol formation in hepatocytes. Evidence for phosphatidylcholine breakdown. J Biol Chem 264:21689-21698.
5. Bae YS, Cantley LG, Chen CS, Kim SR, Kwon KS, Rhee SG. 1998. Activation of phospholipase C-γ by phosphatidylinositol 3,4,5-trisphosphate. J Biol Chem 273: 4465-4469.
6. Balla T, Downing GJ, Jaffe H, Kim S, Zolyomi A, Catt KJ. 1997. Isolation and molecular cloning of wortmannin-sensitive bovine type III phosphatidylinositol 4-kinases. J Biol Chem 272:18358-18366.
7. Berridge MJ. 1993. Inositol trisphosphate and calcium signalling. Nature 361:315-325.
8. Berry MN, Friend DS. 1969. High-yield preparation of isolated rat liver parenchymal cells: A biochemical and fine structural study. J Cell Biol 43:506-520.
9. Biden TJ, Prague ML, Davison AG. 1992. Evidence for phosphatidylinositol hydrolysis in pancreatic islets stimulated with carbamoylcholine. Kinetic analysis of inositol polyphosphate metabolism. Biochem J 285(Pt 2): 541-549.
10. Biden TJ, Davison AG, Prugue ML. 1993. Regulation by membrane potential of phosphatidylinositol hydrolysis in pancreatic islets. J Biol Chem 268:11065-11072.
11. Bocckino SB, Blackmore PF, Wilson PB, Exton JH. 1987. Phosphatidate accumulation in hormone-treated hepatocytes via a phospholipase D mechanism. J Biol Chem 262: 15309-15315.
12. Button D, Rothman A, Bongiorno C, Kupperman E, Wolner B, Taylor P. 1994. Agonist-selective regulation of polyphosphoinositide metabolism in pulmonary artery smooth muscle cells. J Biol Chem 269:6390-6398.
13. Cheng J, Weber JD, Baldassare JJ, Raben DM. 1997. Ablation of Go alpha-subunit results in a transformed phenotype and constitutively active phosphatidylcholine-specific phospholipase C. J Biol Chem 272:17312-17319.
14. Chilvers ER, Batty IH, Challiss RA, Barnes PJ, Nahorski SR. 1991. Determination of mass changes in phosphatidylinositol 4,5-bisphosphate and evidence for agonist-stimulated metabolism of inositol 1,4,5-trisphosphate in airway smooth muscle. Biochem J 275(Pt 2):373-379.
15. Christoffersen T, Refsnes M, Bronstad GO, Istby E, Huse J, Haffner F, Sand TE, Hunt NH, Sonne O. 1984. Changes in hormone responsiveness and cyclic AMP metabolism in rat hepatocytes during primary culture and effects of supplementing the medium with insulin and dexamethasone. Eur J Biochem 138:217-226.
16. Clarke NG, Dawson RM. 1981. Alkaline O N-transacylation. A new method for the quantitative deacylation of phospholipids. Biochem J 195:301-306.
17. Cockcroft S. 1998. Phosphatidylinositol transfer proteins: A requirement in signal transduction and vesicle traffic. Bioessays 20:423-432.
18. Cook SJ, Wakelam MJ. 1989. Analysis of the water-soluble products of phosphatidylcholine breakdown by ion-exchange chromatography. Bombesin and TPA (12-O-tetradecanoylphorbol 13-acetate) stimulate choline generation in Swiss 3T3 cells by a common mechanism. Biochem J 263:581-587.
19. Cook SJ, Wakelam MJ. 1992. Epidermal growth factor increases sn-1,2-diacylglycerol levels and activates phospholipase D-catalysed phosphatidylcholine breakdown in Swiss 3T3 cells in the absence of inositol-lipid hydrolysis. Biochem J 285(Pt 1):247-253.
20. Cook SJ, Palmer S, Plevin R, Wakelam MJ. 1990. Mass measurement of inositol 1,4,5-trisphosphate and sn-1,2-diacylglycerol in bombesin-stimulated Swiss 3T3 mouse fibroblasts. Biochem J 265:617-620.
21. Cook SJ, Briscoe CP, Wakelam MJ. 1991. The regulation of phospholipase D activity and its role in sn-1,2-diradylglycerol formation in bombesin- and phorbol 12-myristate 13-acetate-stimulated Swiss 3T3 cells. Biochem J 280(Pt 2):431-438.
22. 2+-mobilizing hormones. Biochem J 212:733-747.
23. Cunningham E, Thomas GM, Ball A, Hues I, Cockcroft S. 1995. Phosphatidylinositol transfer protein dictates the rate of inositol trisphosphate production by promoting the synthesis of PIP2. Curr Biol 5:775-783.
24. Dajani OF, Sandnes D, Melien O, Rezvani F, Nilssen LS, Thoresen GH, Christoffersen T. 1999. Role of diacylglycerol (DAG) in hormonal induction of S phase in hepatocytes: The DAG-dependent protein kinase C pathway is not activated by epidermal growth factor (EGF), but is involved in mediating the enhancement of responsiveness to EGF by vasopressin, angiotensin II, and norepinephrine. J Cell Physiol 180:203-214.
25. Downes CP, Hawkins PT, Stephens L. 1989. Identification of the stimulated reaction in intact cells, its substrate supply, and the metabolism of inositol phosphates. In: Michell RH, Drummond AH, Downes CP, editors. Inositol lipids in cell signalling. London: Academic Press, pp 3-38.
26. Exton JH. 1990. Signaling through phosphatidylcholine breakdown. J Biol Chem 265:1-4.
27. Exton JH. 1997. Phospholipase D: Enzymology, mechanisms of regulation, and function. Physiol Rev 77:303-320.
28. Exton JH. 2002. Phospholipase D-structure, regulation, and function. Rev Physiol Biochem Pharmacol 144:1-94.
29. Falasca M, Logan SK, Lehto VP, Baccante G, Lemmon MA, Schlessinger J. 1998. Activation of phospholipase C γ by PI 3-kinase-induced PH domain-mediated membrane targeting. Embo J 17:414-422.
30. Fisher SK. 1995. Homologous and heterologous regulation of receptor-stimulated phosphoinositide hydrolysis. Eur J Pharmacol 288:231-250.
31. Fisher SK, Heacock AM, Seguin EB, Agranoff BW. 1990. Polyphosphoinositides are the major source of inositol phosphates in carbamoylcholine-stimulated SK-N-SH neuroblastoma cells. Mol Pharmacol 38:54-63.
32. Fonseca MI, Button DC, Brown RD. 1995. Agonist regulation of α-adrenergic receptor subcellular distribution and function. J Biol Chem 270:8902-8909.
33. Hammond SM, Altshuller YM, Sung TC, Rudge SA, Rose K, Engebrecht J, Morris AJ, Frohman MA. 1995. Human ADP-ribosylation factor-activated phosphatidylcholine-specific phospholipase D defines a new and highly conserved gene family. J Biol Chem 270:29640-29643.
34. + currents in NG108-15 cells treated with U73122, a phospholipase C inhibitor, or neomycin. Br J Pharmacol 120:841-850.
35. Honda A, Nogami M, Yokozeki T, Yamazaki M, Nakamura H, Watanabe H, Kawamoto K, Nakayama K, Morris AJ, Frohman MA, Kanaho Y. 1999. Phosphatidylinositol 4-phosphate 5-kinase alpha is a downstream effector of the small G protein ARF6 in membrane ruffle formation. Cell 99:521-532.
36. Huang C, Handlogten ME, Miller RT. 2002. Parallel activation of phosphatidylinositol 4-kinase and phospholipase C by the extracellular calcium-sensing receptor. J Biol Chem 277:20293-20300.
37. 3H-labeled inositol bis- and monophosphates in agonist-activated rat parotid acinar cells. J Biol Chem 264:9400-9407.
38. Imai A, Gershengorn MC. 1986. Phosphatidylinositol 4,5-bisphosphate turnover is transient while phosphatidylinositol turnover is persistent in thyrotropin-releasing hormone-stimulated rat pituitary cells. Proc Natl Acad Sci USA 83:8540-8544.
39. Irvine RF, Anggard EE, Letcher AJ, Downes CP. 1985. Metabolism of inositol 1,4,5-trisphosphate and inositol 1,3,4-trisphosphate in rat parotid glands. Biochem J 229: 505-511.
40. Irving HR, Exton JH. 1987. Phosphatidylcholine breakdown in rat liver plasma membranes. Roles of guanine nucleotides and P2-purinergic agonists. J Biol Chem 262: 3440-3443.
41. Jenkins G, Fisette P, Anderson R. 1994. Type I phosphatidylinositol 4-phosphate 5-kinase isoforms are specifically stimulated by phosphatidic acid. J Biol Chem 269: 11547-11554.
42. Luberto C, Hannun YA. 1998. Sphingomyelin synthase, a potential regulator of intracellular levels of ceramide and diacylglycerol during SV40 transformation. Does sphingomyelin synthase account for the putative phosphatidylcholine-specific phospholipase C? J Biol Chem 273: 14550-14559.
43. McKenzie F, Seuwen K, Pouyssegur J. 1992. Stimulation of phosphatidylcholine breakdown by thrombin and carbachol but not by tyrosine kinase receptor ligands in cells transfected with Ml muscarinic receptors. Rapid desensitization of phosphocholine-specific (PC) phospholipase D but sustained activity of PC-phospholipase C. J Biol Chem 267:22759-22769.
44. Meyers R, Cantley LC. 1997. Cloning and characterization of a wortmannin-sensitive human phosphatidylinositol 4-kinase. J Biol Chem 272:4384-4390.
45. Mitchell CJ, Kelly MM, Blewitt M, Wilson JR, Biden TJ. 2001. Phospholipase C-γ mediates the hydrolysis of phosphatidylinositol, but not of phosphatidylinositol 4,5-bisphoshate, in carbamylcholine-stimulated islets of Langerhans. J Biol Chem 276:19072-19077.
46. Moehren G, Gustavsson L, Hoek JB. 1994. Activation and desensitization of phospholipase D in intact rat hepatocytes. J Biol Chem 269:838-848.
47. 3 in circular muscle cells. Am J Physiol 261:G945-G951.
48. Nakanishi S, Catt K, Balla T. 1995. A wortmannin-sensitive phosphatidylinositol 4-kinase that regulates hormone-sensitive pools of inositolphospholipids. PNAS 92:5317-5321.
49. Nieto M, Kennedy E, Goldstein D, Brown JH. 1994. Rapid heterologous desensitization of muscarinic and thrombin receptor-mediated phospholipase D activation. Mol Pharmacol 46:406-413.
50. Nishizuka Y. 1995. Protein kinase C and lipid signaling for sustained cellular responses. Faseb J 9:484-496.
51. Oakley RH, Laporte SA, Holt JA, Barak LS, Caron MG. 2001. Molecular determinants underlying the formation of stable intracellular G protein-coupled receptor-beta -arrestin complexes after receptor endocytosis. J Biol Chem 276:19452-19460.
52. 32P]Pi and the accumulation of inositol phosphates in vasopressin-stimulated hepatocytes. Biochem J 238:491-499.
53. 3 in unstimulated and vasopressin-stimulated rat hepatocytes. Cell Signal 1:147-156.
54. Pettitt TR, Martin A, Horton T, Liossis C, Lord JM, Wakelam MJ. 1997. Diacylglycerol and phosphatidate generated by phospholipases C and D, respectively, have distinct fatty acid compositions and functions. Phospholipase D-derived diacylglycerol does not activate protein kinase C in porcine aortic endothelial cells. J Biol Chem 272:17354-17359.
55. Plevin R, Wakelam MJ. 1992. Rapid desensitization of vasopressin- stimulated phosphatidylinositol 4,5-bisphosphate and phosphatidylcholine hydrolysis questions the role of these pathways in sustained diacylglycerol formation in A10 vascular-smooth-muscle cells. Biochem J 285:759-766.
56. Plevin R, Cook SJ, Palmer S, Wakelam MJ. 1991. Multiple sources of sn-1,2-diacylglycerol in platelet-derived-growth-factor-stimulated Swiss 3T3 fibroblasts. Evidence for activation of phosphoinositidase C and phosphatidylcholine-specific phospholipase D. Biochem J 279(Pt 2):559-565.
57. Preiss JE, Loomis CR, Bell RM, Niedel JE. 1987. Quantitative measurement of sn-1,2-diacylglycerols. Methods Enzymol 141:294-300.
58. Quest AFG, Raben DM, Bell RM. 1996. Diacylglycerols biosynthetic intermediates and lipid second messengers. In: Bell RM, et al., editor. Handbook of Lipid Research. New York: Plenum Press, pp 1-58.
59. 2+-mobilizing hormones in hepatocytes. Pharmacol Toxicol 84:234-240.
60. Schacht J. 1976. Inhibition by neomycin of polyphosphoinositide turnover in subcellular fractions of guinea-pig cerebral cortex in vitro. J Neurochem 27:1119-1124.
61. Schacht J. 1981. Extraction and purification of polyphosphoinositides. Methods Enzymol 72:626-631.
62. Schmidt M, Fasselt B, Rümenapp U, Bienek C, Wieland T, van Koppen CJ, Jakobs KH. 1995. Rapid and persistent desensitization of m3 muscarinic acetylcholine receptor-stimulated phospholipase D. J Biol Chem 270:19949-19956.
63. Seglen PO. 1976. Preparation of isolated rat liver cells. Methods Cell Biol 13:29-83.
64. Slivka S, Meier K, Insel P. 1988. Alpha 1-adrenergic receptors promote phosphatidylcholine hydrolysis in MDCK-D1 cells. A mechanism for rapid activation of protein kinase C. J Biol Chem 263:12242-12246.
65. Stephens L, Jackson TR, Hawkins PT. 1993. Activation of phosphatidylinositol 4,5-bisphosphate supply by agonists and non-hydrolysable GTP analogues. Biochem J 296(Pt 2):481-488.
66. 2+ induced by vasopressin in isolated hepatocytes. J Biol Chem 259:5574-5584.
67. Tilly BC, van Paridon PA, Verlaan I, de Laat SW, Moolenaar WH. 1988. Epidermal-growth-factor-induced formation of inositol phosphates in human A431 cells. Differences from the effect of bradykinin. Biochem J 252:857-863.
68. Tobin AB, Lambert DG, Nahorski SR. 1992. Rapid desensitization of muscarinic m3 receptor-stimulated polyphosphoinositide responses. Mol Pharmacol 42:1042-1048.
69. Tolias KF, Cantley LC, Carpenter CL. 1995. Rho family GTPases bind to phosphoinositide kinases. J Biol Chem 270:17656-17659.
70. van Dijk MC, Muriana FJ, de Widt J, Hilkmann H, van Blitterswijk WJ. 1997. Involvement of phosphatidylcholine-specific phospholipase C in platelet-derived growth factor-induced activation of the mitogen-activated protein kinase pathway in Rat-1 fibroblasts. J Biol Chem 272:11011-11016.
71. Wakelam MJ. 1998. Diacylglycerol-when is it an intracellular messenger?. Biochim Biophys Acta 1436:117-126.
72. Weernink PAO, Schulte P, Guo Y, Wetzel J, Amano M, Kaibuchi K, Haverland S, Voss M, Schmidt M, Mayr GW, Jakobs KH. 2000. Stimulation of phosphatidylinositol-4-phosphate 5-kinase by Rho-kinase. J Biol Chem 275: 10168-10174.
73. Willars GB, McArdle CA, Nahorski SR. 1998a. Acute desensitization of phospholipase C-coupled muscarinic M3 receptors but not gonadotropin-releasing hormone receptors co-expressed in alphaT3-1 cells: Implications for mechanisms of rapid desensitization. Biochem J 333(Pt 2):301-308.
74. Willars GB, Nahorski SR, Challiss RA. 1998b. Differential regulation of muscarinic acetylcholine receptor-sensitive polyphosphoinositide pools and consequences for signaling in human neuroblastoma cells. J Biol Chem 273: 5037-5046.
75. Wilson D, Neufeld E, Majerus P. 1985. Phosphoinositide interconversion in thrombin-stimulated human platelets. J Biol Chem 260:1046-1051.
76. 2+ mobilization and inositol 1,4,5-trisphosphate binding. J Biol Chem 266:22234-22241.
77. Wojcikiewicz RJ, Tobin AB, Nahorski SR. 1993. Desensitization of cell signalling mediated by phosphoinositidase C. Trends Pharmacol Sci 14:279-285.
78. Woodcock EA. 1995. Inositol phosphates in the heart: Controversy and consensus. J Mol Med 73:313-323.
79. Wright T, Rangan L, Shin H, Raben D. 1988. Kinetic analysis of 1,2-diacylglycerol mass levels in cultured fibroblasts. Comparison of stimulation by alpha-thrombin and epidermal growth factor. J Biol Chem 263:9374-9380.