Skip to main content

Arachidonic Acid Metabolites on Renin and Vascular Smooth Muscle Cell Growth

  • Chapter
Endocrinology of the Vasculature

Part of the book series: Contemporary Endocrinology ((COE,volume 1))

Abstract

The interaction of hormones, growth factors, or cytokines to their specific cell surface receptors can lead to the stimulation of a cascade of biochemical events including the activation of several phospholipases which in turn can result in the release of several lipid second messengers (1) as outlined. Thus, the action of angiotensin II (AII) or other vascular smooth muscle cell (VSMC) growth factors can activate one or more phospholipases, phosphoinositide phospholipase C (PI-PLC), phosphatidylcholine-specific PLC (PC-PLC), or phospholipase D (PLD). This process results in the formation of the second messengers inositol trisphosphate (IP3), which leads to calcium (Ca2+) mobilization from intracellular stores, as well as diacylglycerol (DAG) which in turn can activate the Ca2+- and phospholipid-sensitive protein kinase C (PKC) (2-5). It has been suggested that the cellular response to AII is obtained by the temporal integration of the IP3/Ca2+-calmodulin branch responsible for the initial transient response and the DAG/PKC branch responsible for the sustained phase of All action (6). DAG is also a rich source of AA that can be released by the action of the enzyme DAG lipase (7) whereas the enzyme DAG-kinase can convert DAG to phosphatidic acid.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 89.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 119.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Liscovitch M. Crosstalk among multiple signal-activated phospholipases. Trends Biochem Sci 1992;17:393–399.

    Article  PubMed  CAS  Google Scholar 

  2. Berridge MJ. Inositol trisphosphate and diacylglycerol as second messengers. Biochem J 1984;220: 345–360.

    PubMed  CAS  Google Scholar 

  3. Nishizuka Y. Role of protein kinase C in cell surface signal transduction and tumor promotion. Nature 1984;308:693–698.

    Article  PubMed  CAS  Google Scholar 

  4. Alexander RW, Brock T, Gimbrone MA, Rittenhouse SE. All increases inositol trisphosphate and Ca2+ in vascular smooth muscle. Hypertension 1985;7:447–451.

    Google Scholar 

  5. Griendling KK, Rittenhouse SE, Brock TA, Ekstein LS, Gimbrone MA Jr. Sustained diacylglycerol formation from inositol phospholipids in AII-stimulated VSMC. J Biol Chem 1986;261:5901–5906.

    PubMed  CAS  Google Scholar 

  6. Kojima, I, Kojima K, Kreutter D, Rasmussen H. The temporal integration of the aldosterone secretory response to AII occurs via two intracellular pathways. J Biol Chem 1984;259:14448–14457.

    PubMed  CAS  Google Scholar 

  7. Bell RL, Kennerly DA, Stanford N, Majerus PW. Diglyceride lipase: a pathway for arachidonate release from human platelets. Proc Natl Acad Sci USA 1979;76:3238–3241.

    Article  PubMed  CAS  Google Scholar 

  8. Berridge MJ, Irvine RF. Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature 1984;312:315–321.

    Article  PubMed  CAS  Google Scholar 

  9. Millar JBA, Rozengurt E. A. A release by bombesin. A novel postreceptor target for heterologous mito-genic desensitization. J Biol Chem 1990;265:19973–19979.

    PubMed  CAS  Google Scholar 

  10. Rao GN, Lasseue B, Alexander RW, Griendling KK. AII stimulatesphosphorylation ofhigh-molecularmass phospholipase A2 in VSMC. Biochem J 1994;299:197–201.

    PubMed  CAS  Google Scholar 

  11. Smith WL. The eicosanoids and their biochemical mechanisms of action. BiochemJ 1989;259:315–324.

    CAS  Google Scholar 

  12. Fitzpatrick FA, Murphy RC. Cytochrome P-450 metabolism of AA: formation and biological actions of “epoxygenase”-derived eicosanoids. Pharmacol Rev 1989;40:229–241.

    Google Scholar 

  13. Yamamoto S. “Enzymatic” lipid peroxidation: reactions of mammalian LOs. Free Radical Biol Med 1991;10:149–159.

    Article  CAS  Google Scholar 

  14. Nadler J, Natarajan R, Stern N. Specific action of the LO pathway in mediating AII-induced aldosterone synthesis in isolated adrenal glomerulosa cells. J Clin Invest 1987;80:1763–1769.

    Article  PubMed  CAS  Google Scholar 

  15. Natarajan R, Stern N, Hseuh W, Do Y, Nadler J. Role of the LO pathway in mediating AII-induced aldosterone biosynthesis in human adrenal glomerulosa cells. J Clin Endocrinol Metab 1988;67:584–591.

    Article  PubMed  CAS  Google Scholar 

  16. Antonipillai I, Nadler J, Robin EC, Horton R. The inhibitory role of 12- and 15-LO products on renin release. Hypertension 1987;10:61–66.

    Article  PubMed  CAS  Google Scholar 

  17. Antonipillai I, Horton R, Natarajan R, Nadler J. A 12-LO product of arachidonate metabolism is involved in angiotensin action on renin release. Endocrinology 1989;125:2028–2034.

    Article  PubMed  CAS  Google Scholar 

  18. Natarajan R, Gonzales N, Hornsby PJ, Nadler J. Mechanism of AII-induced proliferation in bovine adrenal cortical cells. Endocrinology 1992;131:1174–1180.

    Article  PubMed  CAS  Google Scholar 

  19. Yamamoto S. Mammalian LOs: molecular structures and functions. Biochem Biophys Acta 1992;1128:117–131.

    Article  PubMed  CAS  Google Scholar 

  20. Funk CD. Molecular biology in the eicosanoid field. In: Cohn WE, Moldave K, eds. Progress in Nucleic acid Research and Molecular Biology. Academic, New York, 1993;45:67–98.

    Google Scholar 

  21. Sigal E. The molecular biology of mammalian AA metabolism. Am J Physiol(Lung Cell Mol Physiol) 1991;260:L13–L28.

    CAS  Google Scholar 

  22. Funk CD, Furci L, FitzGerald GA. Molecular cloning, primary structure and expression of the human platelet/erythroleukemia cell 12-LO. Proc Natl Acad Sci USA 1990;87:5638–5642.

    Article  PubMed  CAS  Google Scholar 

  23. Izumi T, Hoshiko S, Radmark O, Samuelsson S. Cloning of the cDNA for human 12-LO. Proc Natl Acad Sci USA 1990;87:7477–7481.

    Article  PubMed  CAS  Google Scholar 

  24. Yoshimoto T, Suzuki H, Yamamoto S, Takai T, Yokoyama C, Tanabe T. Cloning and sequence analysis of the cDNA for arachidonate 12-LO ofporcine leukocytes. Proc Natl Acad Sci USA 1990;87:2142–2146.

    Article  PubMed  CAS  Google Scholar 

  25. Ueda N, Hiroshima A, Natsui K, Shinjo F, Yoshimoto T, Yamamoto S, Ii K, Gerozissis K, Dray F. Localization of arachidonate 12-LO in parenchymal cells of porcine anterior pituitary. J Biol Chem 1990;265:2311–2316.

    PubMed  CAS  Google Scholar 

  26. Natarajan R, Gu JL, Rossi J, Gonzales N, Lanting L, Xu L, Nadler J. Elevated glucose and All increase 12-LO activity and expression in porcine aortic smooth muscle cells Proc Natl Acad Sci USA 1993;90:4947–4951.

    Article  PubMed  CAS  Google Scholar 

  27. Gu JL, Natarajan R, Ben-Ezra J, Valente G, Scott S, Yoshimoto T, Yamamoto S, Rossi JJ, Nadler J. Evidence that a leukocyte-type of 12-LO is expressed and regulated by All in human adrenal glomerulosa cells. Endocrinology 1994;134:70–77.

    Article  PubMed  CAS  Google Scholar 

  28. Kim JA, Gu JL, Natarajan R, Esteban J, Berliner JA, Nadler J. A leukocyte-type of 12-LO is expressed in human vascular and mononuclear cells: evidence for upregulation by AII. Arteriosclerosis Throm Vasc Biol 1995;15:942–948.

    Article  CAS  Google Scholar 

  29. Chen X, Kurre U, Jenkins NA, Copeland NG, Funk CD. cDNA cloning, expression, mutagenesis c-terminal iso-leucine, genomic structure, and chromosomal localizations of murine 12-LOs. J Biol Chem 1994;269:13979–13987.

    PubMed  CAS  Google Scholar 

  30. Sigal E, Craik CS, Highland E, Grunberger D, Costelo LL, Dixon RAF, Nadel JA. Molecular cloning and primary structure of human 15-LO. Biochem Biophys Res Commun 1988;157:457–464.

    Article  PubMed  CAS  Google Scholar 

  31. DeMarzo, N, Sloane DL, Dicharry L, Highland E, Sigal E. Molecular cloning and expression of an airway 12-LO. Am J Physiol 1992;262:L198–L207.

    CAS  Google Scholar 

  32. Steinberg D, Parthasarathy S, Carew TE, Khoo JC, Witztum JL. Beyond cholesterol. Modifications of low density lipoprotein that increase its atherogenecity. New Engl J Med 1989;320:915–924.

    Article  PubMed  CAS  Google Scholar 

  33. Parthasarathy S, Steinberg D, Witztum JL. The role of oxidized low density lipoproteins in the pathogenesis of atherosclerosis. Annu Rev Med 1992;43:219–225.

    Article  PubMed  CAS  Google Scholar 

  34. Parthasarathy S, Wieland E, Steinberg D. A role for endothelial cell LO in the oxidative modification of low density lipoprotein. Proc Natl Acad Sci USA 1989;86:1046–1050.

    Article  PubMed  CAS  Google Scholar 

  35. Sparrow CP, Parthasarathy S, Steinberg D. Enzymatic modification of low density lipoprotein by purified LO plus phospholipase A2 mimics cell-mediated oxidative modification. J Lipid Res 1988;29:745–753.

    PubMed  CAS  Google Scholar 

  36. Yla-Hertualla, S, Rosenfeld ME, Parthasarathy S, Glass CK, Sigal E, Witztum JL, Steinberg D. Colocalization of 15-LO mRNA and protein with epitopes of oxidized low density lipoprotein in macrophage-rich areas of atherosclerotic lesions. Proc Natl Acad Sci USA 1990;87:6959–6963.

    Article  Google Scholar 

  37. Yla-Herttuala S, Rosenfeld M, Parthasarathy S, Sigal E, Sarkioja T, Witztum JL, Steinberg D. Gene expression in macrophage-rich human atherosclerotic lesions. LO and acetyl low density lipoprotein receptor messenger RNA colocalize with oxidation-specific lipid-protein adducts. J Clin Invest 1991;87:1146–1152.

    Article  PubMed  CAS  Google Scholar 

  38. Henricksson P, Hamberg M, Diczfalusy U. Formation of 15-HETE as a major hydroxyeicosatetraenoic acid in the atherosclerotic vessel wall. Biochem Biophys Acta 1985;834:272–274.

    Article  Google Scholar 

  39. Simon TC, Makheja AN, Bailey JM. Formation of 15-hydroxyeicosa-tetraenoic acid (15-HETE) as the predominant eicosanoid from Watanabe heritable hyperlipidemic and cholesterol-fed rabbits. Atherosclerosis 1989;75:31–38.

    Article  PubMed  CAS  Google Scholar 

  40. Wang T, Powell W. Increased levels of monohydroxy metabolites of arachidonic and linoleic acids in LDL and aorta from atherosclerotic rabbits. Biochem Biophys Acta 1991;1084:129–138.

    Article  PubMed  CAS  Google Scholar 

  41. Kuhn H, Belkner J, Zaiss S, Fahrenklemper T, Wohlfeil S. Involvement of 15-LO in early stages of atherogenesis. J Exp Med 1994;179:1903–1911.

    Article  PubMed  CAS  Google Scholar 

  42. Folcik VA, Nivar-Aristy RA, Krajewski LP, Cathcart MA. LO contributes to the oxidation of lipids in human atherosclerotic plaques. J Clin Invest 1995;96:504–510.

    Article  PubMed  CAS  Google Scholar 

  43. Benz DJ, Mol M, Ezaki M, Mori-Ito N, Zelan I, Miyanohara A, Friedmann T, Parthasarathy S, Steinberg D, Witztum JL. Enhanced levels of lipoperoxides in low density lipoprotein incubated with murine fibroblasts expressing high levels of human 15-LO. J Biol Chem 1995;270:5191–5197.

    Article  PubMed  CAS  Google Scholar 

  44. Ruderman NB, Williamson JR, Brownlee M. Glucose and diabetic vascular disease. FASEB J 1992;6:2905–2914.

    PubMed  CAS  Google Scholar 

  45. Natarajan R, Gonzales N, Xu L, Nadler J. VSMC exhibit increased growth in response to elevated glucose. Biochem Biophys Res Commun 1992;187:552–560.

    Article  PubMed  CAS  Google Scholar 

  46. Setty BNY, Stuart MJ.15-Hydroxy-5,8,11,13,-eicosatetraenoic acid inhibits human vascular CO. J Clin Invest 1986;77:202–211.

    Article  PubMed  CAS  Google Scholar 

  47. Brown ML, Jakubowski JA, Leventis LL, Deykin D. Elevated glucose alters eicosanoid release from porcine aortic endothelial cells. J Clin Invest 1988;82:2136–2141.

    Article  PubMed  CAS  Google Scholar 

  48. Setty BNY, Graeber JE, Stuart MJ. The mitogenic effects of 15- and 12-hydroxyeicosatetraenoic acids on endothelial cells may be mediated via diacylglycerol kinase inhibition. J Biol Chem 1987;262: 17613–17622.

    PubMed  CAS  Google Scholar 

  49. Nakao J, Ooyama T, Ito H, Chang WC, Murota S. Comparative effects of LO products of AA on rat aortic smooth muscle cell migration. Atherosclerosis 1982;44:339–342.

    Article  PubMed  CAS  Google Scholar 

  50. Antonipillai I, Nadler J, Jost-Vu E, Bughi S, Natarajan R, Horton R. Progressive changes in eicosanoids occur in diabetic renal vascular disease. J Invest Med 1995;43:229A.

    Google Scholar 

  51. Conrad DJ, Kuhn H, Mulkins M, Highland E, Sigal E. Specific inflammatory cytokines regulate the expression of human monocyte 15-LO. Proc Natl Acad Sci USA 1992;89:217–222.

    Article  PubMed  CAS  Google Scholar 

  52. Nasser GM, Morrow JD, Robert Lill, Lakkis FJ, Badr KF. Induction of 15-LO by IL-13 in human blood monocytes. J Biol Chem 1994;269:27631–27634.

    Google Scholar 

  53. Natarajan R, Bai W, Gu JL, Rangarajan V, Nadler J. Regulation of 12-LO by platelet-derived growth factor in VSMC. In: Samuelsson B, Paoletti R, Ramwell PW, eds. Advances in Prostaglandin, Thromboxane and Leukotriene Research. Raven, New York, 1995, pp. 435–437.

    Google Scholar 

  54. Dethlefsen SM, Sheprod D, D’Amore PA. AA metabolites in bFGF-, PDGF- and serum-stimulated vascular cell growth. Exp Cell Res 1994;212:262–273.

    Article  PubMed  CAS  Google Scholar 

  55. Nakao J, Ito H, Chang WC, Koshihara Y, Murota S. Aortic smooth muscle cell migration caused by PDGF is mediated by LO products of AA. Biochem Biophys Res Commun 1983;112:866–871.

    Article  PubMed  CAS  Google Scholar 

  56. Natarajan R, Rosdahl J, Gonzales N, Bai W. The regulation of vascular smooth muscle cell 12-LO by inflammatory cytokines. J Invest Med 1995;43:309A.

    Google Scholar 

  57. Kim JA, Gu JL, Berliner JA, Natarajan R, Nadler J. Inflammatory cytokines regulate 12-LO expression in human vascular smooth muscle and endothelial cells. Circulation 1995;92(Suppl. 1):I160.

    Article  Google Scholar 

  58. Natarajan R, Gonzales N, Lanting L, Nadler J. Role of the LO pathway in AII-induced vascular smooth muscle cell hypertrophy. Hypertension 1994;23(Suppl. 1):I142–I147.

    Article  PubMed  CAS  Google Scholar 

  59. Haliday E, Ramesha C, Ringold G. TNF induces c-fos via a novel pathway requiring the conversion of AA to a LO metabolite. EMBO J 1991;10:109–115.

    PubMed  CAS  Google Scholar 

  60. Yu CL, Tsai M, Stacey DW. Serum stimulation of NIH 3T3 cells induces the production of lipids able to inhibit GTPase-activating protein activity. Mol Cell Biol 1990;10:6683–6689.

    PubMed  CAS  Google Scholar 

  61. Shearman MS, Naor Z, Segikuchi K, Kishimoto A, Nishizuka Y. Selective activation of the y-subspecies of protein kinase C from bovine cerebellum by AA and its LO metabolites. FEBS Lett 1989;243:177–182.

    Article  PubMed  CAS  Google Scholar 

  62. Natarajan R, Lanting L, Xu L, Nadler JL. Role of specific isoforms of protein kinase C in AII and LO action in rat adrenal glomerulosa cells. Mol Cell Endocrinol 1994;101:59–66.

    Article  PubMed  CAS  Google Scholar 

  63. Legrand AB, Lawson JA, Meyrick BO, Blair IA, Oates JA. Substitution of 15-hydroxyeicosatetraenoic acid in the phosphoinositide signaling pathway. J Biol Chem 1991;266:7570–7577.

    PubMed  CAS  Google Scholar 

  64. Takahashi Y, Glasgow WC, Suzuki H, Taketani Y, Yamamoto S, Anton M, Kuhn H, Brash A. Investigation of the oxygenation of phospholipids by the porcine leukocyte and human platelet arachidonate 12-LOs. Eur J Biochem 1993;218:165–171.

    Article  PubMed  CAS  Google Scholar 

  65. Saito F, Hori MT, Ideguchi Y, Berger M, Golub M, Stern N, Tuck ML. 12-LO products modulate Ca2+ signals in VSMC. Hypertension 1992;20:138–143.

    Article  PubMed  CAS  Google Scholar 

  66. Liu B, Khan WA, Hannun YA, Timar J, Taylor JD, Lundy S, Butovich, I, Honn, KV. 12(S)Hydroxyeicosatetraenoic acid and 13(S)-hydroxyoctadecadienoic acid regulation of protein kinase C-a in melanoma cells: role of receptor-mediated hydrolysis of inositol phospholipids. Proc Natl Acad Sci USA 1995;92:9323–9327.

    Article  PubMed  CAS  Google Scholar 

  67. Rao G, Baas AS, Glasgow WC, Eling TE, Runge MS, Alexander RW. Activation of MAP kinases by AA and its metabolites in VSMC. J Biol Chem 1994;269:32586–32591.

    PubMed  CAS  Google Scholar 

  68. Rao GN, Alexander RW, Runge MS. Linoleic acid and its metabolites, hydroperoxyocatadecadienoic acids, stimulate c-fos, c-jun, and c-myc mRNA expression, mitogen-activated protein kinase activation, and growth in rat aortic smooth muscle cells. J Clin Invest 1995;96:842–847.

    Article  PubMed  CAS  Google Scholar 

  69. Davis RJ. The mitogen-activated protein kinase signal transduction pathway. J Biol Chem 1993; 268:14553–14556.

    PubMed  CAS  Google Scholar 

  70. Sedor JR, Davidson EW, Dunn MJ. Effects of nonsteroidal anti-inflammatory drugs in healthy subjects. Am J Med 1986;81(Suppl. 28):S8–S70.

    Google Scholar 

  71. Churchill PC. Second messengers in renin release. Am J Physiol 1985;249:F175–F183.

    PubMed  CAS  Google Scholar 

  72. Lee FO, Nadler JL, Hsueh WA. Effect of a synthetic prostacyclin analogue on renin release in man. J Hypertens 1986;4(Supp1.):S10–S13.

    CAS  Google Scholar 

  73. Mcgiff JC, Quilley CP, Carrol A. The contribution of cytochrome P450 dependent arachidonic metabolites to integrated renal function. Steroids 1993;58:573–579.

    Article  PubMed  CAS  Google Scholar 

  74. Keeton TK., Campbell WB. The pharmacologic alteration of renin release. Pharmacol Rev 1980;32:81–227.

    PubMed  CAS  Google Scholar 

  75. Ito S, Carretero OA, Abe K, Beierwalters WH, Yoshinaga K Effect ofprostanoids on renin release from rabbit afferent arterioles with and without macula densa. Kidney Int 1989;35:1138–1144.

    Article  PubMed  CAS  Google Scholar 

  76. Schricker K, Hamann M, Kaissling B, Kurtz A. Renal autacoids are involved in the stimulation of renin gene expression by low perfusion pressure. Kidney Int 1994;46:1330–1336.

    Article  PubMed  CAS  Google Scholar 

  77. Antonopillai I, Nadler J, Horton R. Angiotensin feedback inhibition on renin is expressed via the lipoxygenase pathway. Endocrine 1988;122:1277–1281.

    Article  Google Scholar 

  78. Antonopillai I. 12 lipoxygenase products are potent inhibitors ofprostacyclin induced renin release. Proc Soc Exp Biol Med 1990;194:224–230.

    Google Scholar 

  79. Henrich WL, Falck JR, Campbell WB. Inhibition of renin secretion from rat renal cortical slices by (R)12-HETE. Am J Physiol 1992;263:F665–F670.

    PubMed  CAS  Google Scholar 

  80. Stern N, Knoll E, Gilad S, Kisch E. Specific role of lipoxygenase products in renin suppression during high salt intake. 21st International Aldosterone Conference, p. 11, 1995 (abstract).

    Google Scholar 

  81. Gu JL, Veerapanane D, Rossi J, Natarajan R, Thomas L, Nadler J. Ribozyme-mediated inhibition of expression of leukocyte-type 12-LO in porcine aortic VSMC. Circ Res 1995;77:14–20.

    Article  PubMed  CAS  Google Scholar 

Download references

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1996 Springer Science+Business Media New York

About this chapter

Cite this chapter

Natarajan, R., Stern, N., Nadler, J. (1996). Arachidonic Acid Metabolites on Renin and Vascular Smooth Muscle Cell Growth. In: Sowers, J.R. (eds) Endocrinology of the Vasculature. Contemporary Endocrinology, vol 1. Humana Press, Totowa, NJ. https://doi.org/10.1007/978-1-4612-0231-8_26

Download citation

  • DOI: https://doi.org/10.1007/978-1-4612-0231-8_26

  • Publisher Name: Humana Press, Totowa, NJ

  • Print ISBN: 978-1-4612-6672-3

  • Online ISBN: 978-1-4612-0231-8

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics