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PMID: 9153277 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Vitamin C blocks inflammatory platelet-activating factor mimetics created by cigarette smoking.

The Journal of clinical investigation ·Vol. 99 ·No. 10 ·1997-05-15 ·Pages 2358-64

Lehr HA, Weyrich AS, Saetzler RK, Jurek A, Arfors KE, Zimmerman GA, Prescott SM, McIntyre TM

Abstract

Cigarette smoking within minutes induces leukocyte adhesion to the vascular wall and formation of intravascular leukocyte-platelet aggregates. We find this is inhibited by platelet-activating factor (PAF) receptor antagonists, and correlates with the accumulation of PAF-like mediators in the blood of cigarette smoke-exposed hamsters. These mediators were PAF-like lipids, formed by nonenzymatic oxidative modification of existing phospholipids, that were distinct from biosynthetic PAF. These PAF-like lipids induced isolated human monocytes and platelets to aggregate, which greatly increased their secretion of IL-8 and macrophage inflammatory protein-1alpha. Both events were blocked by a PAF receptor antagonist. Similarly, blocking the PAF receptor in vivo blocked smoke-induced leukocyte aggregation and pavementing along the vascular wall. Dietary supplementation with the antioxidant vitamin C prevented the accumulation of PAF-like lipids, and it prevented cigarette smoke-induced leukocyte adhesion to the vascular wall and formation of leukocyte-platelet aggregates. This is the first in vivo demonstration of inflammatory phospholipid oxidation products and it suggests a molecular mechanism coupling cigarette smoke with rapid inflammatory changes. Inhibition of PAF-like lipid formation and their intravascular sequela by vitamin C suggests a simple dietary means to reduce smoking-related cardiovascular disease.

MeSH Terms
Animals Antioxidants/pharmacology Ascorbic Acid/pharmacology Azepines/pharmacology Blood Platelets/drug effects,physiology Cell Adhesion Cell Aggregation Chemokine CCL4 Cricetinae Humans Interleukin-8/blood Macrophage Inflammatory Proteins/blood Monocytes/drug effects,physiology Neutrophils/drug effects,physiology Platelet Activating Factor/analogs & derivatives,antagonists & inhibitors,pharmacology,physiology Platelet Aggregation/drug effects Platelet Aggregation Inhibitors/pharmacology Platelet Membrane Glycoproteins/antagonists & inhibitors,physiology Receptors, Cell Surface Receptors, G-Protein-Coupled Reference Values Smoking/blood Time Factors Triazoles/pharmacology
Chemicals
Antioxidants Azepines Chemokine CCL4 Interleukin-8 Macrophage Inflammatory Proteins Platelet Activating Factor Platelet Aggregation Inhibitors Platelet Membrane Glycoproteins Receptors, Cell Surface Receptors, G-Protein-Coupled Triazoles platelet activating factor receptor WEB 2086 Ascorbic Acid
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Lehr H A
Institute for Pathology, Johannes Gutenberg University, Mainz, Germany.
Weyrich A S
Saetzler R K
Jurek A
Arfors K E
Zimmerman G A
Prescott S M
McIntyre T M
References (41)
41 references, click to expand
  1. Cigarette smoke stimulates release of neutrophil chemotactic activity from cultured bovine bronchial epithelial cells.
    Clin Sci (Lond). 1995 Mar;88(3):337-44 PMID: 7736704
  2. Oxidatively fragmented phosphatidylcholines activate human neutrophils through the receptor for platelet-activating factor.
    J Biol Chem. 1991 Jun 15;266(17):11104-10 PMID: 1645725
  3. Oxidatively modified LDL contains phospholipids with platelet-activating factor-like activity and stimulates the growth of smooth muscle cells.
    J Clin Invest. 1995 Nov;96(5):2322-30 PMID: 7593619
  4. Gene-targeted mice in leukocyte adhesion research.
    Microcirculation. 1995 Aug;2(2):141-50 PMID: 7497166
  5. Increased adhesiveness of isolated monocytes to endothelium is prevented by vitamin C intake in smokers.
    Circulation. 1996 Apr 15;93(8):1488-92 PMID: 8608614
  6. Activated platelets signal chemokine synthesis by human monocytes.
    J Clin Invest. 1996 Mar 15;97(6):1525-34 PMID: 8617886
  7. Cigarette smoke condensate-induced adhesion molecule expression and transendothelial migration of monocytes.
    Am J Physiol. 1996 May;270(5 Pt 2):H1624-33 PMID: 8928867
  8. Modulation of oxidant stress in vivo in chronic cigarette smokers.
    Circulation. 1996 Jul 1;94(1):19-25 PMID: 8964113
  9. The role of oxidized lipoproteins in atherogenesis.
    Free Radic Biol Med. 1996;20(5):707-27 PMID: 8721615
  10. A rapid method of total lipid extraction and purification.
    Can J Biochem Physiol. 1959 Aug;37(8):911-7 PMID: 13671378
  11. Monocyte tethering by P-selectin regulates monocyte chemotactic protein-1 and tumor necrosis factor-alpha secretion. Signal integration and NF-kappa B translocation.
    J Clin Invest. 1995 May;95(5):2297-303 PMID: 7537762
  12. Leukotrienes as mediators in ischemia-reperfusion injury in a microcirculation model in the hamster.
    J Clin Invest. 1991 Jun;87(6):2036-41 PMID: 1645749
  13. Role of leukotrienes in leukocyte adhesion following systemic administration of oxidatively modified human low density lipoprotein in hamsters.
    J Clin Invest. 1991 Jul;88(1):9-14 PMID: 2056134
  14. Effect of cigarette smoking on the levels of platelet-activating factor-like lipid(s) in plasma lipoproteins.
    Atherosclerosis. 1991 Mar;87(1):47-55 PMID: 1872924
  15. Neutrophil kinetics during active cigarette smoking in rabbits.
    J Appl Physiol (1985). 1991 Aug;71(2):630-7 PMID: 1657860
  16. Effect of a cigarette smoke extract on the metabolism of the proinflammatory autacoid, platelet-activating factor.
    Circ Res. 1992 Feb;70(2):341-7 PMID: 1735133
  17. Vitamin C intake and mortality among a sample of the United States population.
    Epidemiology. 1992 May;3(3):194-202 PMID: 1591317
  18. Novel leukocyte agonists are released by endothelial cells exposed to peroxide.
    J Biol Chem. 1992 Jul 25;267(21):15168-75 PMID: 1321830
  19. Hetrazepine PAF antagonists.
    J Lipid Mediat. 1992 Jun-Jul;5(2):177-82 PMID: 1326346
  20. Formation of platelet-activating factor-like phospholipids by Fe2+/ascorbate/EDTA-induced lipid peroxidation.
    Biochim Biophys Acta. 1993 Feb 24;1166(2-3):264-74 PMID: 8443246
  21. Oxidants in cigarette smoke. Radicals, hydrogen peroxide, peroxynitrate, and peroxynitrite.
    Ann N Y Acad Sci. 1993 May 28;686:12-27; discussion 27-8 PMID: 8512242
  22. Oxidized LDL-induced leukocyte/endothelium interaction in vivo involves the receptor for platelet-activating factor.
    Arterioscler Thromb. 1993 Jul;13(7):1013-8 PMID: 8391309
  23. Cigarette smoke elicits leukocyte adhesion to endothelium in hamsters: inhibition by CuZn-SOD.
    Free Radic Biol Med. 1993 Jun;14(6):573-81 PMID: 8325532
  24. Activation of neutrophils within pulmonary microvessels of rabbits exposed to cigarette smoke.
    Am J Respir Cell Mol Biol. 1993 Jul;9(1):82-9 PMID: 7687850
  25. Inflammatory roles of P-selectin.
    J Clin Invest. 1993 Aug;92(2):559-70 PMID: 7688760
  26. Mechanism of cigarette smoke condensate induced adhesion of human monocytes to cultured endothelial cells.
    J Cell Physiol. 1994 Jul;160(1):154-62 PMID: 7517402
  27. Vitamin C prevents cigarette smoke-induced leukocyte aggregation and adhesion to endothelium in vivo.
    Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7688-92 PMID: 7519784
  28. Protection from oxidized LDL-induced leukocyte adhesion to microvascular and macrovascular endothelium in vivo by vitamin C but not by vitamin E.
    Circulation. 1995 Mar 1;91(5):1525-32 PMID: 7867194
  29. Increase in circulating products of lipid peroxidation (F2-isoprostanes) in smokers. Smoking as a cause of oxidative damage.
    N Engl J Med. 1995 May 4;332(18):1198-203 PMID: 7700313
  30. Leukocyte recruitment to airways by cigarette smoke and particle phase in contrast to cytotoxicity of vapor.
    Science. 1975 Aug 22;189(4203):634-7 PMID: 1162344
  31. Activated polymorphonuclear leucocytes consume vitamin C.
    FEBS Lett. 1984 Dec 3;178(1):25-30 PMID: 6094256
  32. Free-radical chemistry of cigarette smoke and its toxicological implications.
    Environ Health Perspect. 1985 Dec;64:111-26 PMID: 3007083
  33. Solid-phase extraction and reversed-phase high-performance liquid chromatographic technique for isolation and estimation of platelet activating factor in plasma.
    J Chromatogr. 1986 Oct 31;382:89-98 PMID: 3782417
  34. Biologically significant scavenging of the myeloperoxidase-derived oxidant hypochlorous acid by ascorbic acid. Implications for antioxidant protection in the inflamed rheumatoid joint.
    FEBS Lett. 1987 Mar 9;213(1):15-7 PMID: 3030805
  35. Evidence for existence of various homologues and analogues of platelet activating factor in a lipid extract of bovine brain.
    Biochem Biophys Res Commun. 1987 May 29;145(1):415-25 PMID: 3593346
  36. An oxidized derivative of phosphatidylcholine is a substrate for the platelet-activating factor acetylhydrolase from human plasma.
    J Biol Chem. 1989 Apr 5;264(10):5331-4 PMID: 2494162
  37. Ascorbate is an outstanding antioxidant in human blood plasma.
    Proc Natl Acad Sci U S A. 1989 Aug;86(16):6377-81 PMID: 2762330
  38. The effect of cigarette smoking on neutrophil kinetics in human lungs.
    N Engl J Med. 1989 Oct 5;321(14):924-8 PMID: 2779614
  39. Risk of angina pectoris and plasma concentrations of vitamins A, C, and E and carotene.
    Lancet. 1991 Jan 5;337(8732):1-5 PMID: 1670647
  40. Effect of vitamin C and E supplementation on susceptibility of plasma lipoproteins to peroxidation induced by acute smoking.
    Atherosclerosis. 1990 Nov;85(1):47-54 PMID: 2282108
  41. Human plasma platelet-activating factor acetylhydrolase. Oxidatively fragmented phospholipids as substrates.
    J Biol Chem. 1991 Jun 15;266(17):11095-103 PMID: 2040620
Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
0021-9738
Published
1997-05-15
Pages
2358-64
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC508074
Subset
IM
Grants
NHLBI NIH HHS · HL-44513 · United States
NHLBI NIH HHS · HL-46022 · United States
NHLBI NIH HHS · HL-50153 · United States
Corrections
CommentIn
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