Skip to main content
British Journal of Pharmacology logoLink to British Journal of Pharmacology
. 1995 May;115(2):255–260. doi: 10.1111/j.1476-5381.1995.tb15871.x

Potentiation of the hyporeactivity induced by in vivo endothelial injury in the rat carotid artery by chronic treatment with fish oil.

G A Joly 1, V B Schini 1, H Hughes 1, P M Vanhoutte 1
PMCID: PMC1908320  PMID: 7670727

Abstract

1. The present study investigates whether or not chronic feeding of rats with a diet enriched in fish oil affects the reactivity of balloon-injured carotid arteries. The left carotid arteries were injured in vivo by the repeated passage of a balloon catheter. Both the right (control artery) and the left carotid arteries were excised 24 h after the injury, and suspended in organ chambers for the measurement of changes in isometric tension in the presence of indomethacin. 2. Phenylephrine evoked similar concentration-contraction curves in the right (control) carotid arteries without endothelium from control and fish oil-fed rats. Balloon injury decreased the contractility of carotid arteries to phenylephrine in both types of rats and the pEC50 for phenylephrine was significantly decreased in balloon-injured arteries from control rats compared to those obtained in arteries from fish oil-fed rats (pEC50 7.59 +/- 0.1 and 7.28 +/- 0.06, respectively) while maximal contractions were similar (1.93 +/- 0.15 g and 1.79 +/- 0.12 g, respectively). 3. The treatment of control right carotid arteries without endothelium with either NG-nitro-L-arginine (an inhibitor of nitric oxide synthase) or superoxide dismutase (which protects nitric oxide from degradation) did not affect significantly the contractions to phenylephrine in either group. In these preparations, methylene blue (an inhibitor of soluble guanylate cyclase) decreased slightly but significantly maximal contractions to phenylephrine in both groups. The treatment of balloon-injured carotid arteries with NG-nitro-L-arginine or methylene blue partly restored contractions to phenylephrine in arteries from both types of rat.(ABSTRACT TRUNCATED AT 250 WORDS)

Full text

PDF
255

Selected References

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

  1. BLIGH E. G., DYER W. J. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959 Aug;37(8):911–917. doi: 10.1139/o59-099. [DOI] [PubMed] [Google Scholar]
  2. Beasley D., Schwartz J. H., Brenner B. M. Interleukin 1 induces prolonged L-arginine-dependent cyclic guanosine monophosphate and nitrite production in rat vascular smooth muscle cells. J Clin Invest. 1991 Feb;87(2):602–608. doi: 10.1172/JCI115036. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bullock G. R., Taylor S. G., Weston A. H. Influence of the vascular endothelium on agonist-induced contractions and relaxations in rat aorta. Br J Pharmacol. 1986 Dec;89(4):819–830. doi: 10.1111/j.1476-5381.1986.tb11187.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Busse R., Lückhoff A., Bassenge E. Endothelium-derived relaxant factor inhibits platelet activation. Naunyn Schmiedebergs Arch Pharmacol. 1987 Nov;336(5):566–571. doi: 10.1007/BF00169315. [DOI] [PubMed] [Google Scholar]
  5. Cahill P. D., Sarris G. E., Cooper A. D., Wood P. D., Kosek J. C., Mitchell R. S., Miller D. C. Inhibition of vein graft intimal thickening by eicosapentanoic acid: reduced thromboxane production without change in lipoprotein levels or low-density lipoprotein receptor density. J Vasc Surg. 1988 Jan;7(1):108–118. [PubMed] [Google Scholar]
  6. Codde J. P., Beilin L. J., Croft K. D., Vandongen R. The effect of dietary fish oil and salt on blood pressure and eicosanoid metabolism of spontaneously hypertensive rats. J Hypertens. 1987 Apr;5(2):137–142. doi: 10.1097/00004872-198704000-00002. [DOI] [PubMed] [Google Scholar]
  7. Fingerle J., Johnson R., Clowes A. W., Majesky M. W., Reidy M. A. Role of platelets in smooth muscle cell proliferation and migration after vascular injury in rat carotid artery. Proc Natl Acad Sci U S A. 1989 Nov;86(21):8412–8416. doi: 10.1073/pnas.86.21.8412. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fleming I., Gray G. A., Julou-Schaeffer G., Parratt J. R., Stoclet J. C. Incubation with endotoxin activates the L-arginine pathway in vascular tissue. Biochem Biophys Res Commun. 1990 Sep 14;171(2):562–568. doi: 10.1016/0006-291x(90)91183-s. [DOI] [PubMed] [Google Scholar]
  9. Furchgott R. F., Vanhoutte P. M. Endothelium-derived relaxing and contracting factors. FASEB J. 1989 Jul;3(9):2007–2018. [PubMed] [Google Scholar]
  10. Gerzer R., Karrenbrock B., Siess W., Heim J. M. Direct comparison of the effects of nitroprusside, SIN 1, and various nitrates on platelet aggregation and soluble guanylate cyclase activity. Thromb Res. 1988 Oct 1;52(1):11–21. doi: 10.1016/0049-3848(88)90036-9. [DOI] [PubMed] [Google Scholar]
  11. Gupta S., McArthur C., Grady C., Ruderman N. B. Stimulation of vascular Na(+)-K(+)-ATPase activity by nitric oxide: a cGMP-independent effect. Am J Physiol. 1994 May;266(5 Pt 2):H2146–H2151. doi: 10.1152/ajpheart.1994.266.5.H2146. [DOI] [PubMed] [Google Scholar]
  12. Harker L. A., Kelly A. B., Hanson S. R., Krupski W., Bass A., Osterud B., FitzGerald G. A., Goodnight S. H., Connor W. E. Interruption of vascular thrombus formation and vascular lesion formation by dietary n-3 fatty acids in fish oil in nonhuman primates. Circulation. 1993 Mar;87(3):1017–1029. doi: 10.1161/01.cir.87.3.1017. [DOI] [PubMed] [Google Scholar]
  13. Ignarro L. J. Biological actions and properties of endothelium-derived nitric oxide formed and released from artery and vein. Circ Res. 1989 Jul;65(1):1–21. doi: 10.1161/01.res.65.1.1. [DOI] [PubMed] [Google Scholar]
  14. Joly G. A., Schini V. B., Vanhoutte P. M. Balloon injury and interleukin-1 beta induce nitric oxide synthase activity in rat carotid arteries. Circ Res. 1992 Aug;71(2):331–338. doi: 10.1161/01.res.71.2.331. [DOI] [PubMed] [Google Scholar]
  15. Kilbourn R. G., Belloni P. Endothelial cell production of nitrogen oxides in response to interferon gamma in combination with tumor necrosis factor, interleukin-1, or endotoxin. J Natl Cancer Inst. 1990 May 2;82(9):772–776. doi: 10.1093/jnci/82.9.772. [DOI] [PubMed] [Google Scholar]
  16. Knowles R. G., Salter M., Brooks S. L., Moncada S. Anti-inflammatory glucocorticoids inhibit the induction by endotoxin of nitric oxide synthase in the lung, liver and aorta of the rat. Biochem Biophys Res Commun. 1990 Nov 15;172(3):1042–1048. doi: 10.1016/0006-291x(90)91551-3. [DOI] [PubMed] [Google Scholar]
  17. Lam J. Y., Badimon J. J., Ellefson R. D., Fuster V., Chesebro J. H. Cod liver oil alters platelet-arterial wall response to injury in pigs. Circ Res. 1992 Oct;71(4):769–775. doi: 10.1161/01.res.71.4.769. [DOI] [PubMed] [Google Scholar]
  18. Landymore R. W., Kinley C. E., Cooper J. H., MacAulay M., Sheridan B., Cameron C. Cod-liver oil in the prevention of intimal hyperplasia in autogenous vein grafts used for arterial bypass. J Thorac Cardiovasc Surg. 1985 Mar;89(3):351–357. [PubMed] [Google Scholar]
  19. Locher R., Vogt E., Steiner A., Vetter W. The phosphoinositide turnover of vascular smooth muscle cells is influenced by fish oil. J Hypertens Suppl. 1988 Dec;6(4):S222–S224. doi: 10.1097/00004872-198812040-00066. [DOI] [PubMed] [Google Scholar]
  20. Lockette W. E., Webb R. C., Culp B. R., Pitt B. Vascular reactivity and high dietary eicosapentaenoic acid. Prostaglandins. 1982 Nov;24(5):631–639. doi: 10.1016/0090-6980(82)90033-8. [DOI] [PubMed] [Google Scholar]
  21. Martin W., Villani G. M., Jothianandan D., Furchgott R. F. Selective blockade of endothelium-dependent and glyceryl trinitrate-induced relaxation by hemoglobin and by methylene blue in the rabbit aorta. J Pharmacol Exp Ther. 1985 Mar;232(3):708–716. [PubMed] [Google Scholar]
  22. McCall T. B., Boughton-Smith N. K., Palmer R. M., Whittle B. J., Moncada S. Synthesis of nitric oxide from L-arginine by neutrophils. Release and interaction with superoxide anion. Biochem J. 1989 Jul 1;261(1):293–296. doi: 10.1042/bj2610293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. McCord J. M., Fridovich I. The utility of superoxide dismutase in studying free radical reactions. II. The mechanism of the mediation of cytochrome c reduction by a variety of electron carriers. J Biol Chem. 1970 Mar 25;245(6):1374–1377. [PubMed] [Google Scholar]
  24. Mülsch A., Busse R. NG-nitro-L-arginine (N5-[imino(nitroamino)methyl]-L-ornithine) impairs endothelium-dependent dilations by inhibiting cytosolic nitric oxide synthesis from L-arginine. Naunyn Schmiedebergs Arch Pharmacol. 1990 Jan-Feb;341(1-2):143–147. doi: 10.1007/BF00195071. [DOI] [PubMed] [Google Scholar]
  25. Radomski M. W., Palmer R. M., Moncada S. Glucocorticoids inhibit the expression of an inducible, but not the constitutive, nitric oxide synthase in vascular endothelial cells. Proc Natl Acad Sci U S A. 1990 Dec;87(24):10043–10047. doi: 10.1073/pnas.87.24.10043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Radomski M. W., Palmer R. M., Moncada S. Modulation of platelet aggregation by an L-arginine-nitric oxide pathway. Trends Pharmacol Sci. 1991 Mar;12(3):87–88. doi: 10.1016/0165-6147(91)90510-y. [DOI] [PubMed] [Google Scholar]
  27. Schini V. B., Durante W., Catovsky S., Vanhoutte P. M. Eicosapentaenoic acid potentiates the production of nitric oxide evoked by interleukin-1 beta in cultured vascular smooth muscle cells. J Vasc Res. 1993 Jul-Aug;30(4):209–217. doi: 10.1159/000158996. [DOI] [PubMed] [Google Scholar]
  28. Schini V. B., Junquero D. C., Scott-Burden T., Vanhoutte P. M. Interleukin-1 beta induces the production of an L-arginine-derived relaxing factor from cultured smooth muscle cells from rat aorta. Biochem Biophys Res Commun. 1991 Apr 15;176(1):114–121. doi: 10.1016/0006-291x(91)90897-g. [DOI] [PubMed] [Google Scholar]
  29. Scott-Burden T., Schini V. B., Elizondo E., Junquero D. C., Vanhoutte P. M. Platelet-derived growth factor suppresses and fibroblast growth factor enhances cytokine-induced production of nitric oxide by cultured smooth muscle cells. Effects on cell proliferation. Circ Res. 1992 Nov;71(5):1088–1100. doi: 10.1161/01.res.71.5.1088. [DOI] [PubMed] [Google Scholar]
  30. Shimokawa H., Lam J. Y., Chesebro J. H., Bowie E. J., Vanhoutte P. M. Effects of dietary supplementation with cod-liver oil on endothelium-dependent responses in porcine coronary arteries. Circulation. 1987 Oct;76(4):898–905. doi: 10.1161/01.cir.76.4.898. [DOI] [PubMed] [Google Scholar]
  31. Smith D. L., Willis A. L., Nguyen N., Conner D., Zahedi S., Fulks J. Eskimo plasma constituents, dihomo-gamma-linolenic acid, eicosapentaenoic acid and docosahexaenoic acid inhibit the release of atherogenic mitogens. Lipids. 1989 Jan;24(1):70–75. doi: 10.1007/BF02535267. [DOI] [PubMed] [Google Scholar]
  32. Sperling R. I., Benincaso A. I., Knoell C. T., Larkin J. K., Austen K. F., Robinson D. R. Dietary omega-3 polyunsaturated fatty acids inhibit phosphoinositide formation and chemotaxis in neutrophils. J Clin Invest. 1993 Feb;91(2):651–660. doi: 10.1172/JCI116245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Weiner B. H., Ockene I. S., Levine P. H., Cuénoud H. F., Fisher M., Johnson B. F., Daoud A. S., Jarmolych J., Hosmer D., Johnson M. H. Inhibition of atherosclerosis by cod-liver oil in a hyperlipidemic swine model. N Engl J Med. 1986 Oct 2;315(14):841–846. doi: 10.1056/NEJM198610023151401. [DOI] [PubMed] [Google Scholar]
  34. Wood K. S., Buga G. M., Byrns R. E., Ignarro L. J. Vascular smooth muscle-derived relaxing factor (MDRF) and its close similarity to nitric oxide. Biochem Biophys Res Commun. 1990 Jul 16;170(1):80–88. doi: 10.1016/0006-291x(90)91243-l. [DOI] [PubMed] [Google Scholar]
  35. Yin K., Chu Z. M., Beilin L. J. Blood pressure and vascular reactivity changes in spontaneously hypertensive rats fed fish oil. Br J Pharmacol. 1991 Apr;102(4):991–997. doi: 10.1111/j.1476-5381.1991.tb12289.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Yin K., Chu Z. M., Beilin L. J. Study of mechanisms of glucocorticoid hypertension in rats: endothelial related changes and their amelioration by dietary fish oils. Br J Pharmacol. 1992 Jun;106(2):435–442. doi: 10.1111/j.1476-5381.1992.tb14352.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from British Journal of Pharmacology are provided here courtesy of The British Pharmacological Society

RESOURCES