Neutrophil migration in inflammation: Nitric oxide inhibits rolling, adhesion and induces apoptosis

Nitric Oxide - Biology and Chemistry

Volumn 9, Issue 3, 2003, Pages 153-164

  Secco, Daniela Dal ^a   Paron, Juliane Alves ^a   De Oliveira, Sandra H P ^a   Ferreira, Sérgio Henrique ^a   Silva, João Santana ^a   Cunha, Fernando De Queiroz ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Adhesion; Apoptosis; Inflammation; Neutrophil migration; Nitric oxide; Nitric oxide synthase

Indexed keywords

AMINOGUANIDINE; BACTERIUM LIPOPOLYSACCHARIDE; CARRAGEENAN; ESCHERICHIA COLI ENDOTOXIN; FORMYLMETHIONYLLEUCYLPHENYLALANINE; N(G) NITROARGININE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL PROTECTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM INJURY; ENZYME MECHANISM; INFLAMMATION; LEUKOCYTE ACTIVATION; LEUKOCYTE ADHERENCE; LEUKOCYTE ROLLING; MALE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RAT; SPECIES COMPARISON; WILD TYPE;

ESCHERICHIA COLI;

EID: 0347757088     PISSN: 10898603     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.niox.2003.11.001     Document Type: Article

References (75)

1. Malech H.L., Gallin J.I. Neutrophils in human diseases. N. Engl. J. Med. 317:1987;687-694.
2. Holdsworth S.R., Bellomo R. Differential effects of steroids on leukocyte-mediated glomerulonephritis in the rabbit. Kidney Int. 26:1984;162-169.
3. Weissmann G., Korchak H. Rheumatoid arthritis: the role of neutrophil activation. Inflammation. 8:1984;S3-S14.
4. Wandall J.H. Function of exudative neutrophilic granulocytes in patients with Crohn's disease or ulcerative colitis. Scand. J. Gastroenterol. 20:1985;1151-1156.
5. Sundy J.S., Haynes B.F. Vasculits: phatogenic mechanisms of vessel damage. Gallin J.I., Goldstein I.M., Snyderman R. In Inflammation: Clinical Correlates. 1999;995-1016 Lippincott Williams & Wilkins, Philadelphia.
6. Burke-Gaffney A., Hellewell P.G. Tumor necrosis factor-alpha-induced ICAM-1 expression in human vascular endothelial and lung epithelial cells: modulation by tyrosine kinase inhibitors. Br. J. Pharmacol. 119:1996;1149-1158.
7. Zhang X.W., Liu Q., Wang Y., Thorlacius H. CXC chemokines, MIP-2 and KC, induce P-selectin-dependent neutrophil rolling and extravascular migration in vivo. Br. J. Pharmacol. 133:2001;413-421.
8. Munder K., Colditz I.G. Migratory responses of ovine neutrophils to inflammatory mediators in vitro and in vivo. J. Leukoc. Biol. 53:1993;273-278.
9. Binder R., Kress A., Kirschfink M. Modulation of C5a-mediated effector functions of human polymorphonuclear leukocytes by tumor necrosis factor alpha and granulocyte macrophage colony-stimulating factor. Exp. Clin. Immunogenet. 16:1999;212-225.
10. Drost E.M., MacNee W. Potential role of IL-8, platelet-activating factor and TNF-α in the sequestration of neutrophils in the lung: effects on neutrophil deformability, adhesion receptor expression, and chemotaxis. Eur. J. Immunol. 32:2002;393-403.
11. Szekanecz Z., Kim J., Koch A.E. Chemokines and chemokine receptors in rheumatoid arthritis. Semin. Immunol. 15:2003;15-21.
12. Papayianni A., Serhan C.N., Brady H.R. Lipoxin A4 and B4 inhibit leukotriene-stimulated interactions of human neutrophils and endothelial cells. J. Immunol. 156:1996;2264-2272.
13. Pouliot M., Serhan C.N. Lipoxin A4 and aspirin-triggered 15-epi-LXA4 inhibit tumor necrosis factor-alpha-initiated neutrophil responses and trafficking: novel regulators of a cytokine-chemokine axis relevant to periodontal diseases. Periodontal Res. 34:1999;370-373.
14. Lee S.W., Hong Y.S., Chun C.M., Moon J.D., Kim S.J., Jung I.C., Yoon Y.H., Lee B.A., Moon S.W., Choi S.H., Moon C.K. Anti-inflammatory effects of IL-4 and IL-10 on human polymorphonuclear leukocytes. J. Korean Med. Sci. 17:2002;7-14.
15. Moilanen E., Whittle B., Moncada S. Nitric oxide as a factor in inflammation. Gallin J.I., Snyderman R. In Inflammation: Basic Principles and Clinical Correlates. 1999;787-800 Lippincott Williams & Wilkins, Philadelphia.
16. Grisham M.B., Jourd'Heuil D., Wink D.A. Nitric oxide. I. Physiological chemistry of nitric oxide and its metabolites: implications in inflammation. Am. J. Physiol. 276:1999;G315-G321.
17. Ialenti A., Ianaro A., Maffia P., Sautebin L., Di Rosa M. Nitric oxide inhibits leukocyte migration in carrageenan-induced rat pleurisy. Inflamm. Res. 49:2000;411-417.
18. Paul-Clark M.J., Gilroy D.W., Willis D., Willoughby D.A., Tomlinson A. Nitric oxide synthase inhibitors have opposite effects on acute inflammation depending on their route of administration. J. Immunol. 2:2001;1169-1177.
19. McCartney-Francis N.L., Song X.-Y., Mizel D.E., Wahl S.M. Selective inhibition of inducible nitric oxide synthase exacerbates erosive joint disease. J. Immunol. 166:2001;2734-2740.
20. Moncada S., Palmer R.M.J., Higgs E.A. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol. Rev. 43:1991;109-142.
21. Knowles R.G., Moncada S. Nitric oxide synthases in mammals. Biochem. J. 298:1994;249-258.
22. Alderton W.K., Cooper C.E., Knowles R.G. Nitric oxide synthases: structure, function and inhibition. Biochem. J. 357:2001;593-615.
23. Kubes P., Suzuki M., Granger D.N. Nitric oxide: an endogenous modulator of leukocyte adhesion. Proc. Natl. Acad. Sci. USA. 88:1991;4651-4655.
24. Sundqvist T., Forslund T., Bengtsson T., Axelsson K.L. S-Nitroso-N-acetylpenicillamine reduces leukocyte adhesion to type I collagen. Inflammation. 18:1994;625-631.
25. Lopez-Neblina F., Toledo-Pereyra L.H., Mirmiran R., Paez-Rollys A.J. Time dependence of Na-nitroprusside administration in the prevention of neutrophil infiltration in the rat ischemic kidney. Transplantation. 61:1996;179-183.
26. Guidot D.M., Hybertson B.M., Kitlowski R.P., Repine J.E. Inhaled NO prevents IL-1-induced neutrophil accumulation and associated acute edema in isolated rat lungs. Am. J. Physiol. 271:1996;L225-L229.
27. Lefer A.M., Lefer D.J. The role of nitric oxide and cell adhesion molecules on the microcirculation in ischaemia-reperfusion. Cardiovasc. Res. 32:1996;743-751.
28. Hickey M.J., Kubes P. Role of nitric oxide in regulation of leukocyte-endothelial cell interactions. Exp. Physiol. 82:1997;339-348.
29. Hickey M.J., Sharkey K.A., Sihota E.G., Reinhardt P.H., Macmicking J.D., Nathan C., Kubes P. Inducible nitric oxide synthase-deficient mice have enhanced leukocyte-endothelium interactions in endotoxemia. FASEB J. 11:1997;955-964.
30. Spiecker M., Darius H., Kaboth K., Hubner F., Liao J.K. Differential regulation of endothelial cell adhesion molecule expression by nitric oxide donors and antioxidants. J. Leukoc. Biol. 63:1998;732-739.
31. Kosonen O., Kankaanranta H., Malo-Ranta U., Moilanen E. Nitric oxide-releasing compounds inhibit neutrophil adhesion to endothelial cells. Eur. J. Pharmacol. 382:1999;111-117.
32. Hickey M.J. Role of inducible nitric oxide synthase in the regulation of leukocyte recruitment. Clin. Sci. 100:2001;1-12.
33. Lelamali K., Wand W., Gengaro P., Edelstein C., Schrier R.W. Effects of nitric oxide and peroxynitrite on endotoxin-induced leukocyte adhesion to endothelium. J. Cell. Physiol. 188:2001;337-342.
34. Gauthier T.W., Davenpeck K.L., Lefer A.M. Nitric oxide attenuates leukocyte-endothelial interaction via P-selectin in splanchnic ischemia-reperfusion. Am. J. Physiol. 267:1994;G562-G568.
35. Armstead V.E., Minchenco A.G., Schuhl R.A., Hayward R., Nossuli T.O., Lefer A.M. Regulation of P-selectin expression in human endothelial cells by nitric oxide. Am. J. Physiol. 273:1997;H740-H746.
36. Sato Y., Walley K.R., Klut M.E., English D., D'Yachkova Y., Hogg J.C., van Eeden S.F. Nitric oxide reduces the sequestration of polymorphonuclear leukocytes in lung by changing deformability and CD18 expression. Am. J. Respir. Crit. Care Med. 159:1999;1469-1476.
37. Pruefer D., Scalia R., Lefer A.M. Homocysteine provokes leukocyte-endothelium interaction by downregulation of nitric oxide. General Pharmacol. 33:1999;487-498.
38. Ajuebor M.N., Virág L., Flower R.J., Perretti M., Szabó C. Role of inducible nitric oxide synthase in the regulation of neutrophil migration in zymosan-induced inflammation. Immunology. 95:1998;625-630.
39. Cuzzocrea S., Mazzon E., Calabro G., Dugo L., De Sarro A., Van de Loo F.A.J., Caputi A.P. Inducible nitric oxide synthase-knockout mice exhibit resistance to pleurisy and lung injury caused by carrageenan. Am. J. Respir. Crit. Care Med. 162:2000;1859-1866.
40. Franco-Penteado C.F., DeSouza I., Teixeira S.A., Ribeiro-DaSilva G., De Nucci G., Antunes E. Involvement of nitric oxide on the peritoneal neutrophil influx induced by staphylococcal enterotoxin B in mouse. Toxicon. 39:2001;1383-1386.
41. Savill J.S., Wyllie A.H., Henson J.E., Walport M.J., Henson P.M., Haslett C. Macrophage phagocytosis of aging neutrophils in inflammation. Programmed cell death in the neutrophil leads to its recognition by macrophages. J. Clin. Invest. 83:1989;865-875.
42. Savill J.S., Dransfield I., Hogg N., Haslett C. Vitronectin receptor-mediated phagocytosis of cells undergoing apoptosis. Nature. 343:1990;170-173.
43. Haslett C., Savill J.S., Whyte M.K., Stern M., Dransfield I., Meagher L.C. Granulocyte apoptosis and the control of inflammation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 345:1994;327-333.
44. Savill J. Apoptosis in resolution of inflammation. J. Leukoc. Biol. 61:1997;375-380.
45. Albina J.E., Cui S., Mateo R.B., Reichner J.S. Nitric oxide-mediated apoptosis in murine peritoneal macrophages. J. Immunol. 150:1993;5080-5085.
46. Ankarcrona M., Dypbukt J.M., Brüne B., Nicotera P. Interleukin-1β-induced nitric oxide production activates apoptosis in pancreatic RINm5F cells. Exp. Cell Res. 213:1994;172-177.
47. Fehsel K., Kröcke K.-D., Meyer K.L., Huber H., Wahn V., Kolb-Bachofen V. Nitric oxide induces apoptosis in mouse thymocytes. J. Immunol. 155:1995;2858-2865.
48. Blaylock M.G., Cuthbertson B.H., Galley H.F., Ferguson N.R., Webster N.R. The effect of nitric oxide and peroxynitrite on apoptosis in human polymorphonuclear leukocytes. Free Radic. Biol. Med. 25:1998;748-752.
49. Fortenberry J.D., Owens M.L., Brown M.R., Atkinson D., Brown L.A.S. Exogenous nitric oxide enhances neutrophil cell death and DNA fragmentation. Am. Respir. Cell Mol. Biol. 18:1998;421-428.
50. Rodriguez-López A.M., Martínez-Salgado C., Eleno N., Arévalo M., López-Novoa J.M. Nitric oxide is involved in apoptosis induced by thapsigargin in rat mesangial cells. Cell Physiol. Biochem. 9:1999;285-296.
51. Singhal P.C., Patel P., Nahar N., Franki N., Kapasi A., Reddy K., Shah N., Nwakoby I.E., Mehrotra B. Ethanol-induced neutrophil apoptosis is mediated through nitric oxide. J. Leukoc. Biol. 66:1999;930-936.
52. Baez S. Simultaneous measurements of radii and wall thickness of microvessels in the anesthetized rat. Circ. Res. 25:1969;315-329.
53. Fortes Z.B., Farsky S.P., Oliveira M.A., Garcia-Leme J. Direct vital microscopic study of defective leukocyte-endothelial interactions in diabetes mellitus. Diabetes. 40:1991;1267-1273.
54. J.A.G. Rhodin, Architecture of the vessel wall, in: D.F. Bohr, A.P. Somlyo, H.V. Sparks (Eds.), Handbook of Physiology, vol. II: The Cardiovascular System, Bethesda, 1986, Md 1-31.
55. Granger D.N., Benoit J.N., Suzuki M., Grisham M.B. Leukocyte adherence to venular endothelium during ischemia-reperfusion. Am. J. Physiol. 257:1989;G683-G688.
56. G -methylarginine Biochem. Biophys. Res. Commun. 170:1990;96-103.
57. G -nitro-L-arginine, and aminoguanidine on constitutive and inducible nitric oxide synthase in rat aorta Biochem. Biophys. Res. Commun. 199:1994;147-154.
58. Palmer R.M.J., Ashton D.S., Moncada S. Vascular endothelial cells synthesize nitric oxide from L-arginine. Nature. 333:1988;664-666.
59. Guoyao W.U., Morris S.M. Jr. Arginine metabolism: nitric oxide and beyond. Biochem. J. 336:1998;1-17.
60. Cirino G., Fiorucci S., Sessa W.C. Endothelial nitric oxide synthase: the Cinderela of inflammation? Trends Pharmacol. Sci. 24:2003;91-95.
61. MacNaul K.L., Hutchinson N.I. Differential expression of iNOS and cNOS mRNA in human vascular smooth muscle cells and endothelial cells under normal and inflammatory conditions. Biochem. Biophys. Res. Commun. 196:1993;1330-1334.
62. Binion D.G., Fu S., Ramanujam K.S., Chai Y.C., Dweik R.A., Drazba J.A., Wade J.G., Ziats N.P., Erzurum S.C., Wilson K.T. iNOS expression in human intestinal microvascular endothelial cells inhibits leukocyte adhesion. Am. J. Physiol. 275, Gastrointest. Liver Physiol. 38:1998;G592-G603.
63. Tavares-Murta B.M., Machado J.S., Ferreira S.H., Cunha F.Q. Nitric oxide mediates the inhibition of neutrophil migration induced by systemic administration of LPS. Inflammation. 25:2001;247-253.
64. Kubes P., Kurose I., Granger D.N. NO donors prevent integrin-induced leukocyte adhesion but not P-selectin-dependent rolling in postischemic venules. Am. J. Physiol. 267:1994;H931-H937.
65. Kubes P., Sihota E., Hickey M.J. Endogenous but not exogenous nitric oxide decrease TNF-α-induced leukocyte rolling. Am. J. Physiol. 273, Gastrointest. Liver Physiol. 36:1997;G628-G635.
66. Tsukada K., Omert L.A., Menezes J., Harbrecht B.G., Miyagishima M., Hierholzer C., Billiar T.R. Neutrophil accumulation and damage to the gastric mucosa in resuscitated hemorrhagic shock is independent of inducible nitric oxide synthase. Shock. 11:1999;319-324.
67. Cockrell A., Laroux S., Jourd'heuil D., Kawachi S., Gray L., Van der Heyde H., Grisham M.B. Role of inducible nitric oxide synthase in leukocyte extravasation in vivo. Biochem. Biophys. Res. Commun. 257:1999;684-686.
68. Fox-Robichaud A., Payne D., Kubes P. Inhaled NO reaches distal vasculatures to inhibit endothelium - but not leukocyte-dependent cell adhesion. Am. J. Phisiol. 277, Lung Cell. Mol. Physiol. 21:1999;L1224-L1231.
69. Ward C., Wong T.H., Murray J., Rahman I., Haslett C., Chilvers E.R., Rossi A.G. Induction of human neutrophil apoptosis by nitric oxide donors: evidence for a caspase-dependent, cyclic-GMP-independent, mechanism. Biochem. Pharmacol. 59:2000;305-314.
70. Taylor E.L., Megson I.L., Haslett C., Rossi A.G. Dissociation of DNA fragmentation from other hallmarks of apoptosis in nitric oxide-treated neutrophils: differences between individual nitric oxide donor drugs. Biochem. Biophys. Res. Commun. 289:2001;1229-1236.
71. Arndt H., Russell J.B., Kurose I., Kubes P., Granger D.N. Mediators of leukocyte adhesion in rat mesenteric venules elicited by inhibition of nitric oxide synthesis. Gastroenterology. 105:1993;675-680.
72. Kurose I., Kubes P., Wolf R., Anderson D.C., Paulson J., Miyasaka M., Granger D.N. Inhibition of nitric oxide production. Mechanisms of vascular albumin leakage. Circ. Res. 73:1993;164-171.
73. Niu X.-f., Smith C.W., Kubes P. Intracellular oxidative stress induced by nitric oxide synthesis inhibition increases endothelial cell adhesion to neutrophils. Circ. Res. 74:1994;1133-1140.
74. Ou J., Carlos T.M., Watkins S.C., Saavedra J.E., Keefer L.K., Kim Y.-M., Harbrecht B.G., Billiar T.R. Differential effects of nonselective nitric oxide synthase (NOS) and selective inducible NOS inhibition on hepatic necrosis, apoptosis, ICAM-1 expression, and neutrophil accumulation during endotoxemia. Nitric Oxide: Biol. Chem. 1:1997;404-416.
75. Alam M.S., Akaike T., Okamoto S., Kubota T., Yoshitake J., Sawa T., Miyamoto Y., Tamura F., Maeda H. Role of nitric oxide in host defense in murine salmonellosis as a function of its antibacterial and antiapoptotic activities. Infect. Immun. 70:2002;3130-3142.