Skip to main content
PMC home page
Biochemical Journal logoLink to Biochemical Journal
. 1994 May 15;300(Pt 1):51–56. doi: 10.1042/bj3000051

Membrane-associated diacylglycerol kinase activity is increased by noradrenaline, but not by angiotensin II, in arterial smooth muscle.

J Ohanian 1, A M Heagerty 1
PMCID: PMC1138121  PMID: 8198550

Abstract

In rat small arteries, noradrenaline stimulates the sustained production of arachidonoyl-phosphatidic acid, whereas there is only a slight and transient increase with angiotensin II [Ohanian, Ollerenshaw, Collins and Heagerty (1990) J. Biol. Chem. 265, 8921-8928]. Diacylglycerol kinase (DGK) is the enzyme responsible for generating phosphatidic acid from 1,2-diacylglycerol (DAG). To investigate whether agonists influence DGK activity, we have studied this enzyme in both particulate and soluble fractions prepared from rat small arteries. Soluble DGK activity was inhibited by octyl glucoside. Therefore a deoxycholate assay was used for this fraction, whereas an octyl glucoside mixed-micelle assay was used to examine particulate fractions. Particulate DGK selectively phosphorylated long-chain DAG at a rate 2.5-3-fold higher than that for the synthetic substrate dioctanoylglycerol. In contrast, the substrate preference of the soluble isoenzyme(s) was: dioctanoylglycerol > arachidonoyl-DAG= dioleoylglycerol. Stimulation of intact arteries with noradrenaline (15 microM) increased membrane-associated DGK activity 3-fold, transiently. Angiotensin II (100 nM) stimulation did not alter the DGK activity of this fraction. The activity of the soluble DGK was increased by both agonists, but only transiently. These results demonstrate that rat small arteries contain a membrane-associated DGK which metabolizes arachidonoyl-containing substrate. Also, the activity of this enzyme is regulated differentially by vasoconstrictor hormones. It is concluded that modulation of DGK activity may represent one point at which agonists using the same signal-transduction pathway may tailor the cellular response.

Full text

PDF
51

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Allan C. J., Exton J. H. Quantification of inositol phospholipid breakdown in isolated rat hepatocytes. Biochem J. 1993 Mar 15;290(Pt 3):865–872. doi: 10.1042/bj2900865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Besterman J. M., Pollenz R. S., Booker E. L., Jr, Cuatrecasas P. Diacylglycerol-induced translocation of diacylglycerol kinase: use of affinity-purified enzyme in a reconstitution system. Proc Natl Acad Sci U S A. 1986 Dec;83(24):9378–9382. doi: 10.1073/pnas.83.24.9378. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bocckino S. B., Wilson P. B., Exton J. H. Phosphatidate-dependent protein phosphorylation. Proc Natl Acad Sci U S A. 1991 Jul 15;88(14):6210–6213. doi: 10.1073/pnas.88.14.6210. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Capponi A. M., Lew P. D., Vallotton M. B. Cytosolic free calcium levels in monolayers of cultured rat aortic smooth muscle cells. Effects of angiotensin II and vasopressin. J Biol Chem. 1985 Jul 5;260(13):7836–7842. [PubMed] [Google Scholar]
  5. Chuang M., Lee M. W., Zhao D., Severson D. L. Metabolism of a long-chain diacylglycerol by permeabilized A10 smooth muscle cells. Am J Physiol. 1993 Oct;265(4 Pt 1):C927–C933. doi: 10.1152/ajpcell.1993.265.4.C927. [DOI] [PubMed] [Google Scholar]
  6. Danthuluri N. R., Deth R. C. Acute desensitization to angiotensin II: evidence for a requirement of agonist-induced diacylglycerol production during tonic contraction of rat aorta. Eur J Pharmacol. 1986 Jul 15;126(1-2):135–139. doi: 10.1016/0014-2999(86)90749-1. [DOI] [PubMed] [Google Scholar]
  7. Florin-Christensen J., Florin-Christensen M., Delfino J. M., Stegmann T., Rasmussen H. Metabolic fate of plasma membrane diacylglycerols in NIH 3T3 fibroblasts. J Biol Chem. 1992 Jul 25;267(21):14783–14789. [PubMed] [Google Scholar]
  8. Goto K., Kondo H. Molecular cloning and expression of a 90-kDa diacylglycerol kinase that predominantly localizes in neurons. Proc Natl Acad Sci U S A. 1993 Aug 15;90(16):7598–7602. doi: 10.1073/pnas.90.16.7598. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Griendling K. K., Rittenhouse S. E., Brock T. A., Ekstein L. S., Gimbrone M. A., Jr, Alexander R. W. Sustained diacylglycerol formation from inositol phospholipids in angiotensin II-stimulated vascular smooth muscle cells. J Biol Chem. 1986 May 5;261(13):5901–5906. [PubMed] [Google Scholar]
  10. Heagerty A. M., Ollerenshaw J. D. The phosphoinositide signalling system and hypertension. J Hypertens. 1987 Oct;5(5):515–524. doi: 10.1097/00004872-198710000-00002. [DOI] [PubMed] [Google Scholar]
  11. Jackowski S., Rock C. O. Stimulation of phosphatidylinositol 4,5-bisphosphate phospholipase C activity by phosphatidic acid. Arch Biochem Biophys. 1989 Feb 1;268(2):516–524. doi: 10.1016/0003-9861(89)90318-4. [DOI] [PubMed] [Google Scholar]
  12. Jensen P. E., Mulvany M. J., Aalkjaer C. Endogenous and exogenous agonist-induced changes in the coupling between [Ca2+]i and force in rat resistance arteries. Pflugers Arch. 1992 Apr;420(5-6):536–543. doi: 10.1007/BF00374630. [DOI] [PubMed] [Google Scholar]
  13. Kanoh H., Kondoh H., Ono T. Diacylglycerol kinase from pig brain. Purification and phospholipid dependencies. J Biol Chem. 1983 Feb 10;258(3):1767–1774. [PubMed] [Google Scholar]
  14. Kanoh H., Sakane F., Yamada K. Diacylglycerol kinase isozymes from brain and lymphoid tissues. Methods Enzymol. 1992;209:162–172. doi: 10.1016/0076-6879(92)09020-4. [DOI] [PubMed] [Google Scholar]
  15. Kanoh H., Yamada K., Sakane F., Imaizumi T. Phosphorylation of diacylglycerol kinase in vitro by protein kinase C. Biochem J. 1989 Mar 1;258(2):455–462. doi: 10.1042/bj2580455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kato M., Takenawa T. Purification and characterization of membrane-bound and cytosolic forms of diacylglycerol kinase from rat brain. J Biol Chem. 1990 Jan 15;265(2):794–800. [PubMed] [Google Scholar]
  17. Knauss T. C., Jaffer F. E., Abboud H. E. Phosphatidic acid modulates DNA synthesis, phospholipase C, and platelet-derived growth factor mRNAs in cultured mesangial cells. Role of protein kinase C. J Biol Chem. 1990 Aug 25;265(24):14457–14463. [PubMed] [Google Scholar]
  18. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  19. Lemaitre R. N., Glomset J. A. Arachidonoyl-specific diacylglycerol kinase. Methods Enzymol. 1992;209:173–182. doi: 10.1016/0076-6879(92)09021-t. [DOI] [PubMed] [Google Scholar]
  20. Lemaitre R. N., King W. C., MacDonald M. L., Glomset J. A. Distribution of distinct arachidonoyl-specific and non-specific isoenzymes of diacylglycerol kinase in baboon (Papio cynocephalus) tissues. Biochem J. 1990 Feb 15;266(1):291–299. doi: 10.1042/bj2660291. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. MacDonald M. L., Mack K. F., Williams B. W., King W. C., Glomset J. A. A membrane-bound diacylglycerol kinase that selectively phosphorylates arachidonoyl-diacylglycerol. Distinction from cytosolic diacylglycerol kinase and comparison with the membrane-bound enzyme from Escherichia coli. J Biol Chem. 1988 Jan 25;263(3):1584–1592. [PubMed] [Google Scholar]
  22. Maroney A. C., Macara I. G. Phorbol ester-induced translocation of diacylglycerol kinase from the cytosol to the membrane in Swiss 3T3 fibroblasts. J Biol Chem. 1989 Feb 15;264(5):2537–2544. [PubMed] [Google Scholar]
  23. Moritz A., De Graan P. N., Gispen W. H., Wirtz K. W. Phosphatidic acid is a specific activator of phosphatidylinositol-4-phosphate kinase. J Biol Chem. 1992 Apr 15;267(11):7207–7210. [PubMed] [Google Scholar]
  24. Nishizuka Y. Studies and perspectives of protein kinase C. Science. 1986 Jul 18;233(4761):305–312. doi: 10.1126/science.3014651. [DOI] [PubMed] [Google Scholar]
  25. Ohanian J., Izzard A., Littlewood M., Heagerty A. Regulation of diacylglycerol metabolism by vasoconstrictor hormones in intact small arteries. Circ Res. 1993 Jun;72(6):1163–1171. doi: 10.1161/01.res.72.6.1163. [DOI] [PubMed] [Google Scholar]
  26. Ohanian J., Ollerenshaw J., Collins P., Heagerty A. Agonist-induced production of 1,2-diacylglycerol and phosphatidic acid in intact resistance arteries. Evidence that accumulation of diacylglycerol is not a prerequisite for contraction. J Biol Chem. 1990 May 25;265(15):8921–8928. [PubMed] [Google Scholar]
  27. Ollerenshaw J. D., Heagerty A. M., Swales J. D. Noradrenaline stimulation of the phosphoinositide system: evidence for a novel hydrophobic inositol-containing compound in resistance arterioles. Br J Pharmacol. 1988 Jun;94(2):363–370. doi: 10.1111/j.1476-5381.1988.tb11538.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Pacini L., Limatola C., Frati L., Luly P., Spinedi A. Muscarinic stimulation of SK-N-BE(2) human neuroblastoma cells elicits phosphoinositide and phosphatidylcholine hydrolysis: relationship to diacylglycerol and phosphatidic acid accumulation. Biochem J. 1993 Jan 1;289(Pt 1):269–275. doi: 10.1042/bj2890269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Qian Z., Drewes L. R. Cross-talk between receptor-regulated phospholipase D and phospholipase C in brain. FASEB J. 1991 Mar 1;5(3):315–319. doi: 10.1096/fasebj.5.3.2001791. [DOI] [PubMed] [Google Scholar]
  30. Rider M. H., Baquet A. Activation of rat liver plasma-membrane diacylglycerol kinase by vasopressin and phenylephrine. Biochem J. 1988 Nov 1;255(3):923–928. doi: 10.1042/bj2550923. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sakane F., Yamada K., Kanoh H. Different effects of sphingosine, R59022 and anionic amphiphiles on two diacylglycerol kinase isozymes purified from porcine thymus cytosol. FEBS Lett. 1989 Sep 25;255(2):409–413. doi: 10.1016/0014-5793(89)81134-2. [DOI] [PubMed] [Google Scholar]
  32. Sakane F., Yamada K., Kanoh H., Yokoyama C., Tanabe T. Porcine diacylglycerol kinase sequence has zinc finger and E-F hand motifs. Nature. 1990 Mar 22;344(6264):345–348. doi: 10.1038/344345a0. [DOI] [PubMed] [Google Scholar]
  33. Schaap D., de Widt J., van der Wal J., Vandekerckhove J., van Damme J., Gussow D., Ploegh H. L., van Blitterswijk W. J., van der Bend R. L. Purification, cDNA-cloning and expression of human diacylglycerol kinase. FEBS Lett. 1990 Nov 26;275(1-2):151–158. doi: 10.1016/0014-5793(90)81461-v. [DOI] [PubMed] [Google Scholar]
  34. Schaap D., van der Wal J., van Blitterswijk W. J., van der Bend R. L., Ploegh H. L. Diacylglycerol kinase is phosphorylated in vivo upon stimulation of the epidermal growth factor receptor and serine/threonine kinases, including protein kinase C-epsilon. Biochem J. 1993 Feb 1;289(Pt 3):875–881. doi: 10.1042/bj2890875. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Somlyo A. P., Walker J. W., Goldman Y. E., Trentham D. R., Kobayashi S., Kitazawa T., Somlyo A. V. Inositol trisphosphate, calcium and muscle contraction. Philos Trans R Soc Lond B Biol Sci. 1988 Jul 26;320(1199):399–414. doi: 10.1098/rstb.1988.0084. [DOI] [PubMed] [Google Scholar]
  36. Stathopoulos V. M., Coco-Maroney A., Wei C. W., Goth M., Zaricznyj C., Macara I. G. Identification of two cytosolic diacylglycerol kinase isoforms in rat brain, and in NIH-3T3 and ras-transformed fibroblasts. Biochem J. 1990 Dec 15;272(3):569–575. doi: 10.1042/bj2720569. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. van Blitterswijk W. J., Hilkmann H., de Widt J., van der Bend R. L. Phospholipid metabolism in bradykinin-stimulated human fibroblasts. I. Biphasic formation of diacylglycerol from phosphatidylinositol and phosphatidylcholine, controlled by protein kinase C. J Biol Chem. 1991 Jun 5;266(16):10337–10343. [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES