Contribution of capsaicin-sensitive sensory neurons to antithrombin-induced reduction of ischemia/reperfusion-induced liver injury in rats

Naoaki Harada; Kenji Okajima; Mehtap Yuksel; Hirotaka Isobe

doi:10.1160/TH04-02-0106

Thrombosis and Haemostasis, Table of Contents

Thromb Haemost 2005; 93(01): 48-56
DOI: 10.1160/TH04-02-0106

Blood Coagulation, Fibrinolysis and Cellular Haemostasis

Schattauer GmbH

Contribution of capsaicin-sensitive sensory neurons to antithrombin-induced reduction of ischemia/reperfusion-induced liver injury in rats

Naoaki Harada

¹Department of Diagnostic Medicine, Graduate School of Medical Sciences, Kumamoto University, Kumamoto, Japan

,

Kenji Okajima

¹Department of Diagnostic Medicine, Graduate School of Medical Sciences, Kumamoto University, Kumamoto, Japan

,

Mehtap Yuksel

¹Department of Diagnostic Medicine, Graduate School of Medical Sciences, Kumamoto University, Kumamoto, Japan

,

Hirotaka Isobe

¹Department of Diagnostic Medicine, Graduate School of Medical Sciences, Kumamoto University, Kumamoto, Japan

› Author Affiliations

Abstract

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Keywords

Antithrombin - ischemia/reperfusion - capsaicin-sensitive sensory neurons - calcitonin gene-related peptide - prostacyclin

References

References
1 Rosenberg RD. Biochemistry of heparin antithrombin interactions, and the physiological role of this natural anticoagulant mechanism. Am J Med 1989; 87 suppl 3B 2S-9S.
2 Okajima K, Ueyama H, Hashimoto Y. et al Homozygous variant of antithrombin III that lacks affinity for heparin: AT III Kumamoto. Thromb Haemost 1989; 61: 20-24.
3 Okajima K, Abe H, Maeda S. et al Antithrombin III Nagasaki (Ser116-Pro): a heterozygous variant with defective heparin binding associated with thrombosis. Blood 1993; 81: 1300-5.
4 Jaeschke H. Molecular mechanisms of hepatic ischemia-reperfusion injury and preconditioning. Am J Physiol Gastointest Liver Physiol 2003; 284: G15-G26.
5 Harada N, Okajima K, Kushimoto S. et al Antithrombin reduces ischemia/reperfusion injury of rat liver by increasing the hepatic level of prostacyclin. Blood 1999; 93: 157-64.
6 Kainoh M, Imai R, Umetsu T. et al Prostacyclin and beraprost sodium as suppressors of activated rat polymorphonuclear leukocytes. Biochem Pharmacol 1990; 39: 477-84.
7 Eisenhut T, Sinha B, Grottrup-Wolfers E. et al Prostacyclin analogs suppress the synthesis of tumor necrosis factor- α in LPS-stimulated human peripheral blood mononuclear cells. Immunopharmacology 1993; 26: 259-64.
8 Uchiba M, Okajima K. Antithrombin does not directly promote the endothelial production of prostacyclin in cultured endothelial cells. Thromb Haemost 2001; 86: 722-3.
9 Dray A. Inflammatory mediators of pain. Br J Anaesth 1995; 75: 125-31.
10 Szallasi A, Blumberg PM. Vanilloid receptors: new insights enhance potential as a therapeutic target. Pain 1996; 68: 195-208.
11 Crossman D, McEwan J, MacDermot J. et al Human calcitonin gene-related peptide activates adenylate cyclase and releases prostacyclin from human umbilical vein endothelial cells. Br J Pharmacol 1987; 92: 695-701.
12 Fields HL. Pain. New York: McGraw-Hill; 1987
13 Harada N, Okajima K, Uchiba M. et al Ischemia/ reperfusion-induced increase in the hepatic level of prostacyclin is mainly mediated by activation of capsaicin- sensitive sensory neurons in rats. J Lab Clin Med 2002; 139: 218-26.
14 Borov Borovikova LV, Ivanova S, Zhang M. et al Vagus nerve stimulation attenuates the systemic in flammatory response to endotoxin. Nature 2000; 405: 458-62.
15 Uchiba M, Okajima K, Murakami K. et al Effect of antithrombin III (AT III) and Trp49-modified AT III on plasma level of 6-keto-PGF1 α in rats. Thromb Res 1995; 80: 201-8.
16 Perkins MN, Campbell EA. Capsazepine reversal of the antinociceptive action of capsaicin in vivo. Br J Pharmacol 1992; 107: 329-33.
17 Laszlo F, Whittle JR B, Moncada S. Time-dependent enhancement or inhibition of endotoxin-induced vascular injury in rat intestine by nitric oxide synthase inhibitors. Br J Pharmacol 1994; 111: 1309-15.
18 Uno K, Iuchi Y, Fujii J. et al In vivo study on cross talk between inducible nitric-oxide synthase and cyclooxygenase in rat gastric mucosa: effect of cyclooxygenase activity on nitric oxide production. J Pharmacol Exp Ther 2004; 309: 995-1002.
19 Kaneko H, Kaunitz J, Taché Y. Vagal mechanisms underlying gastric protection induced by chemical activation of raphe pallidus in rats. Am J Physiol 1998; 275: G1056-1062.
20 Arai I, Hamasaki Y, Futaki N. et al Effect of NS-398, a new nonsteroidal anti-inflammatory agent, on gastric ulceration and acid secretion in rats. Res Commun Chem Pathol Pharmacol 1993; 81: 259-70.
21 Hayashi H, Chaudry IH, Clemens MG. et al Hepatic ischemia models for determining the effects of ATP-MgCl2 treatment. J Surg Res 1986; 40: 167-75.
22 Lee SM, Clemens MG. Effect of α -tocopherol on hepatic mixed function oxidases in hepatic ischemia/ reperfusion. Hepatology 1992; 15: 176-81.
23 Harada N, Okajima K, Uchiba M. et al Contribution of capsaicin-sensitive sensory neurons to stress-induced increases in gastric tissue levels of prostaglandins in rats. Am J Physiol Gastrointest Liver Physiol 2003; 285: G1214-G1224.
24 Liu L, Simon SA. Capsazepine, a vanilloid receptor antagonist, inhibits nicotinic acetylcholine receptors in rat trigeminal ganglia. Neurosci Lett 1997; 228: 29-32.
25 Akiyoshi H, Gonda T, Terada T. A comparative histochemical and immunohistochemical study of aminergic, cholinergic and peptidergic innervation in rat, hamster, guinea pig, dog and human livers. Liver 1998; 18: 352-9.
26 Torry RJ, Labarrere CA, Nelson D. et al Localization and characterization of antithrombin in human kidney. J Histchem Cytochem 1999; 47: 313-21.
27 Ito Y, Abril ER, Bethea NW. et al Role of nitric oxide in hepatic microvascular injury elicited by acetaminophen in mice. Am J Physiol Gastrointest Liver Physiol 2004; 286: G60-67.
28 Shito M, Wakabayashi G, Ueda M. et al Interleukin 1 receptor blockade reduces tumor necrosis factor production, tissue injury, and mortality after hepatic ischemia- reperfusion in the rat. Transplantation 1997; 63: 143-8.
29 Warren JS, Yabroff KR, Remick DG. et al Tumor necrosis factor participates in the pathogenesis of acute immune complex alveolitis in the rat. J Clin Invest 1989; 84: 1873-82.
30 Kushimoto S, Okajima K, Uchiba M. et al Role of granulocyte elastase in ischemia/reperfusion injury of rat liver. Crit Care Med 1996; 24: 1908-12.
31 Tognetto M, Amadesi S, Harrison S. et al Anandamide excites central terminals of dorsal root ganglion neurons via vanilloid receptor-1 activation. J Neurosci 2001; 21: 1104-9.
32 Holzer P. Neural emergency system in the stomach. Gastroenterology 1998; 114: 823-39.
33 Harada N, Okajima K, Kushimoto S. Gabexate mesilate, a synthetic protease inhibitor, reduces ischemia/ reperfusion injury of rat liver by inhibiting leukocyte activation. Crit Care Med 1999; 27: 1958-64.
34 van Nieuw Amerongen GP, van Hinsbergh VW. Targets for pharmacological intervention of endothelial hyperpermeability and barrier function. Vascular Phamacol 2003; 39: 257-72.
35 Koj A, Regoeczi E. Effect of experimental inflammation on the synthesis and distribution of antithrombin III and alpha-1-antitrypsin in rabbits. Br J Exp Pathol 1978; 59: 473-81.
36 Bull HA, Hothersall J, Chowdhury N. et al Neuropeptides induce release of nitric oxide from human dermal microvascular endothelial cells. J Invest Dermatol 1996; 106: 655-60.
37 Armstrong JM, Chapple D, Dusting GJ. et al Cardiovascular actions of prostacyclin (PGI 2 ) in chloralose anesthetized dogs. Br J Pharmacol 1977; 61: 136-41.
38 Gibbs LS, Lai L, Malik AB. Tumor necrosis factor enhances the neutrophil-dependent increase in endothelial permeability. J Cell Physiol 1990; 145: 496-500.
39 Granger DN, Kubes P. The microcirculation and inflammation: modulation of leukocyte-endothelial cell adhesion. J Leukoc Biol 1994; 55: 662-75.
40 Opree A, Kress M. Involvement of the proinflammatory cytokines tumor necrosis factor-alpha, IL-1β , and IL-6 but not IL-8 in the development of heat hyper- algesia: Effects on heat-evoked calcitonin gene-related peptide release from rat skin. J Neurosci 2000; 20: 6289-93.
41 Tominaga M, Caterina MJ, Malmberg AB. et al The cloned capsaicin receptor integrates multiple painproducing stimuli. Neuron 1998; 21: 531-43.
42 Oelschlager C, Romisch J, Staubitz A. et al Antithrombin III inhibits nuclear factor kappaB activation in human monocytes and vascular endothelial cells. Blood 2002; 99: 4015-20.
43 Uchiba M, Okajima K, Murakami K. et al Attenuation of endotoxin-induced pulmonary vascular injury by antithrombin III. Am J Physiol 1996; 270: L921-L930.
44 Isobe H, Okajima K, Uchiba M. et al Antithrombin prevents endotoxin-induced hypotension by inhibiting the induction of nitric oxide synthase in rats. Blood 2002; 99: 1638-45.
45 Mizutani A, Okajima K, Uchiba M. et al Antithrombin reduces ischemia/reperfusion-induced renal injury in rats by inhibiting leukocyte activation through promotion of prostacyclin production. Blood 2003; 101: 3029-36.