Brisk production of nitric oxide and associated formation of S-nitrosothiols in early hemorrhage

Journal of Applied Physiology

Volumn 100, Issue 4, 2006, Pages 1267-1277

  Atkins, James L ^a   Day, Billy W ^b   Handrigan, Michael T ^a   Zhang, Zhe ^b   Pamnani, Motilal B ^c   Gorbunov, Nikolai V ^a  

^a WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

Author keywords

Blood cells; Physiology; Shock

Indexed keywords

BIOTIN; N [3 (AMINOMETHYL)BENZYL]ACETAMIDINE; N(G) NITRO DEXTRO ARGININE METHYL ESTER; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PLASMA PROTEIN; S NITROSOTHIOL; VASOCONSTRICTOR AGENT;

ANIMAL EXPERIMENT; ARTERIAL BLOOD; ARTICLE; BLEEDING; CHEMOLUMINESCENCE; CONTROLLED STUDY; ELECTRON SPIN RESONANCE; ERYTHROCYTE; FLUORESCENCE; HEMOGLOBIN DETERMINATION; HEMORRHAGIC HYPOTENSION; MALE; MASS SPECTROMETRY; MEAN ARTERIAL PRESSURE; NITROSYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RAT; SPIN TRAPPING;

ANIMALS; BLOOD PRESSURE; CERULOPLASMIN; ENZYME INHIBITORS; ERYTHROCYTES; HEMOGLOBIN A, GLYCOSYLATED; HEMORRHAGE; MALE; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; RATS; RATS, SPRAGUE-DAWLEY; REGIONAL BLOOD FLOW; S-NITROSOTHIOLS; TIME FACTORS;

EID: 33646341501     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.01059.2005     Document Type: Article

References (70)

1. Akaike T, Noguchi Y, Ijiri S, Setoguchi K, Suga M, Zheng YM, Dietzschold B, and Maeda H. Pathogenesis of influenza virus-induced pneumonia: involvement of both nitric oxide and oxygen radicals. Proc Natl Acad Sci USA 93: 2448-2453, 1996.
2. Al-Sa'doni HH, Megson IL, Bisland S, Butler AR, and Flitney FW. Neocuproine, a selective Cu(I) chelator, and the relaxation of rat vascular smooth muscle by S-nitrosothiols. Br J Pharmacol 121: 1047-1050, 1997.
3. Antonini E, Brunori M, Wyman J, and Noble RW. Preparation and kinetic properties of intermediates in the reaction of hemoglobin with ligands. J Biol Chem 241: 3236-3238, 1966.
4. Beckner ME, Chen X, An J, Day BW, and Pollack IF. Proteomic characterization of harvested pseudopodia with differential gel electrophoresis and specific antibodies. Lab Invest 85: 316-327, 2005.
5. Bitterman H, Brod V, Weisz G, Kushnir D, and Bitterman N. Effects of oxygen on regional hemodynamics in hemorrhagic shock. Am J Physiol Heart Circ Physiol 271: H203-H211, 1996.
6. + channels. Microcirculation 11: 279-293, 2004.
7. Chen RM, Chen TL, Lin YL, Chen TG, and Tai YT. Ketamine reduces nitric oxide biosynthesis in human umbilical vein endothelial cells by down-regulating endothelial nitric oxide synthase expression and intracellular calcium levels. Crit Care Med 33: 1044-1049, 2005.
8. Cosby K, Partovi KS, Crawford JH, Patel RP, Reiter CD, Martyr S, Yang BK, Waclawiw MA, Zalos G, Xu X, Huang KT, Shields H, Kim-Shapiro DB, Schechter AN, Cannon RO III, and Gladwin MT. Nitrite reduction to nitric oxide by deoxyhemoglobin vasodilates the human circulation. Nat Med 9: 1498-1505, 2003.
9. Crane MS, Ollosson R, Moore KP, Rossi AG, and Megson IL. Novel role for low molecular weight plasma thiols in nitric oxide-mediated control of platelet function. J Biol Chem 277: 46858-46863, 2002.
10. Davies NA, Brealey DA, Stidwill R, Singer M, Svistunenko DA, and Cooper CE. Nitrosyl heme production compared in endotoxemic and hemorrhagic shock. Free Radic Biol Med 38: 41-49, 2005.
11. Day B and Friedman SM. Intracellular sodium and potassium changes in vascular smooth muslce during hemorrhagic shock. Surg Gynecol Obstet 147: 25-26, 1978.
12. Eduardo SS and Assreuy J. Long-lasting changes of rat blood pressure to vasoconstrictors and vasodilators induced by nitric oxide donor infusion: involvement of potassium channels. J Pharmacol Exp Ther 290: 380-387, 1999.
13. Fukuto JM, Dutton AS, and Houk KN. The chemistry and biology of nitroxyl (HNO): a chemically unique species with novel and important biological activity. Chembiochem 6: 612-619, 2005.
14. Garvey EP, Oplinger JA, Furfine ES, Kiff RJ, Laszlo F, Whittle BJ, and Knowles RG. 1400W is a slow, tight binding, and highly selective inhibitor of inducible nitric-oxide synthase in vitro and in vivo. J Biol Chem 272: 4959-4963, 1997.
15. Gorbunov NV, Asher LV, Ayyagari V, and Atkins JL. Inflammatory leukocytes and iron turnover in experimental hemorrhagic lung trauma. Exp Mol Pathol 2005.
16. Gorbunov NV, McFaul SJ, Van AS, Morrissette C, Zaucha GM, and Nath J. Assessment of inflammatory response and sequestration of blood iron transferrin complexes in a rat model of lung injury resulting from exposure to low-frequency shock waves. Crit Care Med 32: 1028-1034, 2004.
17. Gorbunov NV, Yalowich JC, Gaddam A, Thampatty P, Ritov VB, Kisin ER, Elsayed NM, and Kagan VE. Nitric oxide prevents oxidative damage produced by tert-butyl hydroperoxide in erythroleukemia cells via nitrosylation of heme and non-heme iron. Electron paramagnetic resonance evidence. J Biol Chem 272: 12328-12341, 1997.
18. Gorren AC, de Boer E, and Wever R. The reaction of nitric oxide with copper proteins and the photodissociation of copper-NO complexes. Biochim Biophys Acta 916: 38-47, 1987.
19. Handrigan MT, Bentley TB, Oliver JD, Tabaku LS, Burge JR, and Atkins JL. Choice of fluid influences outcome in prolonged hypotensive resuscitation after hemorrhage in awake rats. Shock 23: 337-343, 2005.
20. Harbrecht BG, Wu B, Watkins SC, Marshall HPJ, Peitzman AB, and Billiar TR. Inhibition of nitric oxide synthase during hemorrhagic shock increases hepatic injury. Shock 4: 332-337, 1995.
21. Hierholzer C, Harbrecht B, Menezes JM, Kane J, MacMicking J, Nathan CF, Peitzman AB, Billiar TR, and Tweardy DJ. Essential role of induced nitric oxide in the initiation of the inflammatory response after hemorrhagic shock. J Exp Med 187: 917-928, 1998.
22. Hille R, Olson JS, and Palmer G. Spectral transitions of nitrosyl hemes during ligand binding to hemoglobin. J Biol Chem 254: 12110-12120, 1979.
23. Hughes MN. Relationships between nitric oxide, nitroxyl ion, nitrosonium cation and peroxynitrite. Biochim Biophys Acta 1411: 263-272, 1999.
24. Illner H and Shires GT. The effect of hemorrhagic shock on potassium transport in skeletal muscle. Surg Gynecol Obstet 150: 17-25, 1980.
25. Inoue K, Akaike T, Miyamoto Y, Okamoto T, Sawa T, Otagiri M, Suzuki S, Yoshimura T, and Maeda H. Nitrosothiol formation catalyzed by ceruloplasmin. Implication for cytoprotective mechanism in vivo. J Biol Chem 274: 27069-27075, 1999.
26. Jaffrey SR and Snyder SH. The biotin switch method for the detection of S-nitrosylated proteins. Sci STKE 86: L1, 2001.
27. Jaszewski AR, Fann YC, Chen YR, Sato K, Corbett J, and Mason RP. EPR spectroscopy studies on the structural transition of nitrosyl hemoglobin in the arterial-venous cycle of DEANO-treated rats as it relates to the proposed nitrosyl hemoglobin/nitrosothiol hemoglobin exchange. Free Radic Biol Med 35: 444-451, 2003.
28. Kelly E, Shah NS, Morgan NN, Watkins SC, Peitzman AB, and Billiar TR. Physiologic and molecular characterization of the role of nitric oxide in hemorrhagic shock: evidence that type II nitric oxide synthase does not regulate vascular decompensation. Shock 7: 157-163, 1997.
29. Kiang JG, Lu X, Tabaku LS, Bentley TB, Atkins JL, and Tsokos GC. Resuscitation with lactated Ringer solution limits the expression of molecular events associated with lung injury after hemorrhage. J Appl Physiol 98: 550-556, 2005.
30. Koch MA, Hasser EM, and Schadt JC. Influence of nitric oxide on the hemodynamic response to hemorrhage in conscious rabbits. Am J Physiol Regul Integr Comp Physiol 268: R171-R182, 1995.
31. Komarov AM, Kramer JH, Mak IT, and Weglicki WB. EPR detection of endogenous nitric oxide in postischemic heart using lipid and aqueous-soluble dithiocarbamate-iron complexes. Mol Cell Biochem 175: 91-97, 1997.
32. Kubulus D, Rensing H, Paxian M, Thierbach JT, Meisel T, Redl H, Bauer M, and Bauer I. Influence of heme-based solutions on stress protein expression and organ failure after hemorrhagic shock. Crit Care Med 33: 629-637, 2005.
33. Landry DW and Oliver JA. The pathogenesis of vasodilatory shock. N Engl J Med 345: 588-595, 2001.
34. Lin YF, Raab-Graham K, Jan YN, and Jan LY. NO stimulation of ATP-sensitive potassium channels: involvement of Ras/mitogen-activated protein kinase pathway and contribution to neuroprotection. Proc Natl Acad Sci USA 101: 7799-7804, 2004.
35. Liu LM, Ward JA, and Dubick MA. Hemorrhage-induced vascular hyporeactivity to norepinephrine in select vasculatures of rats and the roles of nitric oxide and endothelin. Shock 19: 208-214, 2003.
36. McKinley BA, Houtchens BA, and Janata J. Continuous monitoring of interstitial fluid potassium during hemorrhagic shock in dogs. Crit Care Med 9: 845-851, 1981.
37. Miranda KM, Paolocci N, Katori T, Thomas DD, Ford E, Bartberger MD, Espey MG, Kass DA, Feelisch M, Fukuto JM, and Wink DA. A biochemical rationale for the discrete behavior of nitroxyl and nitric oxide in the cardiovascular system. Proc Natl Acad Sci USA 100: 9196-9201, 2003.
38. Molina PE. Neurobiology of the stress response: contribution of the sympathetic nervous system to the neuroimmune axis in traumatic injury. Shock 24: 3-10, 2005.
39. Molina PE, Zambell KL, Zhang P, Vande SC, and Carnal J. Hemodynamic and immune consequences of opiate analgesia after trauma/hemorrhage. Shock 21: 526-534, 2004.
40. Morales D, Madigan J, Cullinane S, Chen J, Heath M, Oz M, Oliver JA, and Landry DW. Reversal by vasopressin of intractable hypotension in the late phase of hemorrhagic shock. Circulation 100: 226-229, 1999.
41. Musser JB, Bentley TB, Griffith S, Sharma P, Karaian JE, and Mongan PD. Hemorrhagic shock in swine: nitric oxide and potassium sensitive adenosine triphosphate channel activation. Anesthesiology 101: 399-408, 2004.
42. Nelli S, Hillen M, Buyukafsar K, and Martin W. Oxidation of nitroxyl anion to nitric oxide by copper ions. Br J Pharmacol 131: 356-362, 2000.
43. Oliver JD, Atkins JL, Bentley TB, and Pamnani M. Microdialysis measurement of interstitial potassium concentrations during hemorrhagic shock (Abstract). FASEB J 16: A54. 2002.
44. Pajk W, Schwarz B, Knotzer H, Friesenecker B, Mayr A, Dunser M, and Hasibeder W. Jejunal tissue oxygenation and microvascular flow motion during hemorrhage and resuscitation. Am J Physiol Heart Circ Physiol 283: H2511-H2517, 2002.
45. Peitzman AB, Billiar TR, Harbrecht BG, Kelly E, Udekwu AO, and Simmons RL. Hemorrhagic shock. Curr Probl Surg 32: 925-1002, 1995.
46. Pieber D, Horina G, Sandner-Kiesling A, Pieber TR, and Heinemann A. Pressor and mesenteric arterial hyporesponsiveness to angiotensin II is an early event in haemorrhagic hypotension in anaesthetised rats. Cardiovasc Res 44: 166-175, 1999.
47. Piepot HA, Groeneveld AB, van Lambalgen AA, and Sipkema P. The role of inducible nitric oxide synthase in lipopolysaccharide-mediated hyporeactivity to vasoconstrictors differs among isolated rat arteries. Clin Sci (Lond) 102: 297-305, 2002.
48. Rana MW, Singh G, Wang P, Ayala A, Zhou M, and Chaudry IH. Protective effects of preheparinization on the microvasculature during and after hemorrhagic shock. J Trauma 32: 420-426, 1992.
49. Rassaf T, Bryan NS, Maloney RE, Specian V, Kelm M, Kalyanaraman B, Rodriguez J, and Feelisch M. NO adducts in mammalian red blood cells: too much or too little? Nat Med 9: 481-482, 2003.
50. Rensing H, Bauer I, Datene V, Patau C, Pannen BH, and Bauer M. Differential expression pattern of heme oxygenase-1/heat shock protein 32 and nitric oxide synthase-II and their impact on liver injury in a rat model of hemorrhage and resuscitation. Crit Care Med 27: 2766-2775, 1999.
51. Savoye G, Tamion F, Richard V, Varin R, and Thuillez C. Hemorrhagic shock resuscitation affects early and selective mesenteric artery endothelial function through a free radical-dependent mechanism. Shock 23: 411-416, 2005.
52. Sayeed MM, Adler RJ, Chaudry IH, and Baue AE. Effect of hemorrhagic shock on hepatic transmembrane potentials and intracellular electrolytes in vivo. Am J Physiol Regul Integr Comp Physiol 240: R211-R219, 1981.
53. Schmidt HH, Hofmann H, Schindler U, Shutenko ZS, Cunningham DD, and Feelisch No M. NO from NO synthase. Proc Natl Acad Sci USA 93: 14492-14497, 1996.
54. Sharma AC, Singh G, and Gulati A. Decompensation characterized by decreased perfusion of the heart and brain during hemorrhagic shock: role of endothelin-1. J Trauma 53: 531-536, 2002.
55. Singel DJ and Stamler JS. Chemical physiology of blood flow regulation by red blood cells: role of nitric oxide and S-nitrosohemoglobin. Annu Rev Physiol 67: 99-145, 2005.
56. Stamler JS. Hemoglobin and nitric oxide. N Engl J Med 349: 402-405, 2003.
57. Stamler JS, Singel DJ, and Loscalzo J. Biochemistry of nitric oxide and its redox-activated forms. Science 258: 1898-1902, 1992.
58. Szabo C and Thiemermann C. Invited opinion: role of nitric oxide in hemorrhagic, traumatic, and anaphylactic shock and thermal injury. Shock 2: 145-155, 1994.
59. Thiemermann C, Szabo C, Mitchell JA, and Vane JR. Vascular hyporeactivity to vasoconstrictor agents and hemodynamic decompensation in hemorrhagic shock is mediated by nitric oxide. Proc Natl Acad Sci USA 90: 267-271, 1993.
60. Torres J and Wilson MT. The reactions of copper proteins with nitric oxide. Biochim Biophys Acta 1411: 310-322, 1999.
61. Torres LN, Torres F, I, Barbee RW, Tiba MH, Ward KR, and Pittman RN. Continuous peripheral resistance measurement during hemorrhagic hypotension. Am J Physiol Heart Circ Physiol 287: H2341-H2345, 2004.
62. Trump BF, Berezesky IK, Chang SH, Pendergrass RE, and Mergner WJ. The role of ion shifts in cell injury. Scan Electron Microsc 3: 1-13, 1979.
63. Tsuchiya K, Kirima K, Yoshizumi M, Houchi H, Tamaki T, and Mason RP. The role of thiol and nitrosothiol compounds in the nitric oxide-forming reactions of the iron-N-methyl-D-glucamine dithiocarbamate complex. Biochem J 367: 771-779, 2002.
64. Visser CC, Voorwinden LH, Harders LR, Eloualid M, van BL, Crommelin DJ, Danhof M, and de Boer AG. Coupling of metal containing homing devices to liposomes via a maleimide linker: use of TCEP to stabilize thiol-groups without scavenging metals. J Drug Target 12: 569-573, 2004.
65. Wang P, Ba ZF, and Chaudry IH. Endothelial cell dysfunction occurs after hemorrhage in nonheparinized but not in preheparinized models. J Surg Res 54: 499-506, 1993.
66. Wang P, Ba ZF, Reich SS, Zhou M, Holme KR, and Chaudry IH. Effects of nonanticoagulant heparin on cardiovascular and hepatocellular function after hemorrhagic shock. Am J Physiol Heart Circ Physiol 270: H1294-H1302, 1996.
67. Westphal M and Traber DL. Ketamine in critical illness: another no-NO agent? Crit Care Med 33: 1162-1163, 2005.
68. Zhao KS, Huang X, Liu J, Huang Q, Jin C, Jiang Y, Jin J, and Zhao G. New approach to treatment of shock - restitution of vasoreactivity. Shock 18: 189-192, 2002.
69. Zuckerbraun BS, McCloskey CA, Gallo D, Liu F, Ifedigbo E, Otterbein LE, and Billiar TR. Carbon monoxide prevents multiple organ injury in a model of hemorrhagic shock and resuscitation. Shock 23: 527-532, 2005.
70. Zweier JL, Wang P, Samouilov A, and Kuppusamy P. Enzymeindependent formation of nitric oxide in biological tissues. Nat Med 1: 804-809, 1995.