In vivo visualization of nitric oxide and interactions among platelets, leukocytes, and endothelium following hemorrhagic shock and reperfusion
Rent the article at a discountRent now
* Final gross prices may vary according to local VAT.Get Access
We examined changes in nitric oxide (NO) distribution in the mesenteric microcirculation after hemorrhagic shock and reperfusion (H/R), and correlated NO production to leukocyte and platelet behavior.
Materials and methods
The behavior of leukocytes and platelets in mesenteric venules was observed by intravital microscopy at 0.5 and 24 h after H/R in male Wistar rats. Transvascular leakage of fluorescein isothiocyanate-labeled albumin was assessed by epi-illumination. The NO-sensitive dye, 4,5-diaminofluorescein diacetate, was used for imaging NO release.
H/R significantly increased vascular albumin leakage and adhesion of leukocytes and platelets (P < 0.05). In H/R 0.5 h rats, NO production in the venular endothelium declined. However, NO production was elevated in H/R 24 h rats in mast cells (P < 0.05). Leukocyte adherence, platelet adherence, and venular permeability were attenuated by iNOS inhibition.
Mesenteric endothelial cell dysfunction after H/R 0.5 h is associated with reduced NO, whereas after H/R 24 h is related to increase NO in mast cells.
- Koike K, Moore EE, Moore FA, Kim FJ, Carl VS, Banerjee A. Gut phospholipase A2 mediates neutrophil priming and lung injury after mesenteric ischemia-reperfusion. Am J Physiol. 1995;268:G397–403.
- Childs EW, Udobi KF, Hunter FA, Dhevan V. Evidence of transcellular albumin transport after hemorrhagic shock. Shock. 2005;23:565–70.
- Childs EW, Udobi KF, Wood JG, Hunter FA, Smalley DM, Cheung LY. In vivo visualization of reactive oxidants and leukocyte-endothelial adherence following hemorrhagic shock. Shock. 2002;18:423–7. CrossRef
- Suematsu M, Tamatani T, Delano FA, Miyasaka M, Forrest M, Suzuki H, et al. Microvascular oxidative stress preceding leukocyte activation elicited by in vivo nitric oxide suppression. Am J Physiol. 1994;266:H2410–5.
- Kurose I, Wolf R, Grisham MB, Granger DN. Modulation of ischemia/reperfusion-induced microvascular dysfunction by nitric oxide. Circ Res. 1994;74:376–82.
- Barocelli E, Ballabeni V, Ghizzardi P, Cattaruzza F, Bertoni S, Lagrasta CA, et al. The selective inhibition of inducible nitric oxide synthase prevents intestinal ischemia-reperfusion injury in mice. Nitric Oxide. 2006;14:212–8. CrossRef
- Hierholzer C, Kalff JC, Billiar TR, Bauer AJ, Tweardy DJ, Harbrecht BG. Induced nitric oxide promotes intestinal inflammation following hemorrhagic shock. Am J Physiol Gastrointest Liver Physiol. 2004;286:G225–33. CrossRef
- Moncada S, Palmer RM, Higgs EA. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev. 1991;43:109–42.
- Kubes P, Kanwar S, Niu XF, Gaboury JP. Nitric oxide synthesis inhibition induces leukocyte adhesion via superoxide and mast cells. FASEB J. 1993;7:1293–9.
- Kajimura M, Michel CC. Flow modulates the transport of K+ through the walls of single perfused mesenteric venules in anaesthetised rats. J Physiol. 1999;521 Pt 3:665–77. CrossRef
- Nakaki T, Kato R. Nitric oxide in vascular remodeling. Jpn Heart J. 1996;37:431–45.
- Kojima H, Nakatsubo N, Kikuchi K, Kawahara S, Kirino Y, Nagoshi H, et al. Detection and imaging of nitric oxide with novel fluorescent indicators: diaminofluoresceins. Anal Chem. 1998;70:2446–53. CrossRef
- Kashiwagi S, Kajimura M, Yoshimura Y, Suematsu M. Nonendothelial source of nitric oxide in arterioles but not in venules: alternative source revealed in vivo by diaminofluorescein microfluorography. Circ Res. 2002;91:e55–64. CrossRef
- Suematsu M, Okitsu T, Suzuki H, Schmid-Shonbein GW, Ishimura Y. Intravital observation of platelet–endothelial cell interaction during nitric oxide suppression. In: Tsuchiya M, Katori M, Suematsu M, Zweifach BW, editors. Endothelial cell function in blood flow. Amsterdam: Excerpta Medica; 1994. p. 26–33.
- Suematsu M, DeLano FA, Poole D, Engler RL, Miyasaka M, Zweifach BW, et al. Spatial and temporal correlation between leukocyte behavior and cell injury in postischemic rat skeletal muscle microcirculation. Lab Invest. 1994;70:684–95.
- Suematsu M, Suzuki H, Tamatani T, Iigou Y, DeLano FA, Miyasaka M, et al. Impairment of selectin-mediated leukocyte adhesion to venular endothelium in spontaneously hypertensive rats. J Clin Invest. 1995;96:2009–16. CrossRef
- Katayama T, Ikeda Y, Handa M, Tamatani T, Sakamoto S, Ito M, et al. Immunoneutralization of glycoprotein Ibalpha attenuates endotoxin-induced interactions of platelets and leukocytes with rat venular endothelium in vivo. Circ Res. 2000;86:1031–7.
- Kubes P, Gaboury JP. Rapid mast cell activation causes leukocyte-dependent and -independent permeability alterations. Am J Physiol. 1996;271:H2438–46.
- Garvey EP, Oplinger JA, Furfine ES, Kiff RJ, Laszlo F, Whittle BJ, et al. 1400 W is a slow, tight binding, and highly selective inhibitor of inducible nitric-oxide synthase in vitro and in vivo. J Biol Chem. 1997;272:4959–63. CrossRef
- Zhao X, Chen YR, He G, Zhang A, Druhan LJ, Strauch AR, et al. Endothelial nitric oxide synthase (NOS3) knockout decreases NOS2 induction, limiting hyperoxygenation and conferring protection in the postischemic heart. Am J Physiol Heart Circ Physiol. 2007;292:H1541–50. CrossRef
- Granger DN, Kvietys PR, Perry MA. Leukocyte–endothelial cell adhesion induced by ischemia and reperfusion. Can J Physiol Pharmacol. 1993;71:67–75.
- Deitch EA, Xu D, Franko L, Ayala A, Chaudry IH. Evidence favoring the role of the gut as a cytokine-generating organ in rats subjected to hemorrhagic shock. Shock. 1994;1:141–5. CrossRef
- Cooper D, Chitman KD, Williams MC, Granger DN. Time-dependent platelet-vessel wall interactions induced by intestinal ischemia-reperfusion. Am J Physiol Gastrointest Liver Physiol. 2003;284:G1027–33.
- Nishijima K, Kiryu J, Tsujikawa A, Honjo M, Nonaka A, Yamashiro K, et al. In vivo evaluation of platelet–endothelial interactions after transient retinal ischemia. Invest Ophthalmol Vis Sci. 2001;42:2102–9.
- Khandoga A, Biberthaler P, Enders G, Axmann S, Hutter J, Messmer K, et al. Platelet adhesion mediated by fibrinogen-intercellular adhesion molecule-1 binding induces tissue injury in the postischemic liver in vivo. Transplantation. 2002;74:681–8. CrossRef
- Cooper D, Russell J, Chitman KD, Williams MC, Wolf RE, Granger DN. Leukocyte dependence of platelet adhesion in postcapillary venules. Am J Physiol Heart Circ Physiol. 2004;286:H1895–900. CrossRef
- Kim MH, Harris NR. Leukocyte adherence inhibits adenosine-dependent venular control of arteriolar diameter and nitric oxide. Am J Physiol Heart Circ Physiol. 2006;291:H724–31. CrossRef
- Harris NR, Whatley JR, Carter PR, Specian RD. Venular constriction of submucosal arterioles induced by dextran sodium sulfate. Inflamm Bowel Dis. 2005;11:806–13. CrossRef
- Chen KH, Reece LM, Leary JF. Mitochondrial glutathione modulates TNF-alpha-induced endothelial cell dysfunction. Free Radic Biol Med. 1999;27:100–9. CrossRef
- Eppihimer MJ, Russell J, Anderson DC, Epstein CJ, Laroux S, Granger DN. Modulation of P-selectin expression in the postischemic intestinal microvasculature. Am J Physiol. 1997;273:G1326–32.
- Parmentier S, Bohme GA, Lerouet D, Damour D, Stutzmann JM, Margaill I, et al. Selective inhibition of inducible nitric oxide synthase prevents ischaemic brain injury. Br J Pharmacol. 1999;127:546–52. CrossRef
- Lin HI, Chou SJ, Wang D, Feng NH, Feng E, Chen CF. Reperfusion liver injury induces down-regulation of eNOS and up-regulation of iNOS in lung tissues. Transplant Proc. 2006;38:2203–6. CrossRef
- Kubes P, Ibbotson G, Russell J, Wallace JL, Granger DN. Role of platelet-activating factor in ischemia/reperfusion-induced leukocyte adherence. Am J Physiol. 1990;259:G300–5.
- Boros M, Kaszaki J, Nagy S. Histamine release during intestinal ischemia-reperfusion: role of iron ions and hydrogen peroxide. Circ Shock. 1991;35:174–80.
- Messina A, Knight KR, Dowsing BJ, Zhang B, Phan LH, Hurley JV, et al. Localization of inducible nitric oxide synthase to mast cells during ischemia/reperfusion injury of skeletal muscle. Lab Invest. 2000;80:423–31.
- Gilchrist M, Savoie M, Nohara O, Wills FL, Wallace JL, Befus AD. Nitric oxide synthase and nitric oxide production in in vivo-derived mast cells. J Leukoc Biol. 2002;71:618–24.
- Hierholzer C, Billiar TR. Molecular mechanisms in the early phase of hemorrhagic shock. Langenbecks Arch Surg. 2001;386:302–8. CrossRef
- In vivo visualization of nitric oxide and interactions among platelets, leukocytes, and endothelium following hemorrhagic shock and reperfusion
Volume 58, Issue 8 , pp 463-471
- Cover Date
- Print ISSN
- Online ISSN
- SP Birkhäuser Verlag Basel
- Additional Links
- Intravital microscopy
- Ischemia reperfusion
- Nitric oxide (NO)
- Industry Sectors
- Author Affiliations
- 1. Department of Obstetrics and Gynecology, Ehime University School of Medicine, Shitsukawa, Toon, Ehime, 791-0295, Japan
- 2. Department of Obstetrics and Gynecology, Uwajima City Hospital, Uwajima, Ehime, 798-8510, Japan