Carbon monoxide protects against hemorrhagic shock and resuscitation-induced microcirculatory injury and tissue injury

Shock

Volumn 43, Issue 2, 2015, Pages 166-171

  Nassour, Ibrahim ^a   Kautza, Benjamin ^a   Rubin, Mark ^a   Escobar, Daniel ^a   Luciano, Jason ^a   Loughran, Patricia ^a   Gomez, Hernando ^a   Scott, Jeffrey ^b   Gallo, David ^b   Brumfield, John ^a,c   Otterbein, Leo E ^b   Zuckerbraun, Brian S ^a,c  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

adhesion molecule; carbon monoxideYreleasing molecule; Endothelium; sinusoid

Indexed keywords

CARBON MONOXIDE; PROTOPORPHYRIN TIN; RINGER LACTATE SOLUTION; CELL ADHESION MOLECULE; CYTOKINE; INTERCELLULAR ADHESION MOLECULE 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL INJURY; C57BL 6 MOUSE; CELL ACTIVATION; CELL CULTURE; COHORT ANALYSIS; CONTROLLED STUDY; DISEASE EXACERBATION; ENDOTHELIUM CELL; ENDOTHELIUM INJURY; HEMORRHAGIC SHOCK; IN VITRO STUDY; IN VIVO STUDY; LEUKOCYTE ADHERENCE; MEAN ARTERIAL PRESSURE; MOUSE; NONHUMAN; ORGAN INJURY; RESUSCITATION; SHAM PROCEDURE; TISSUE INJURY; ADVERSE EFFECTS; ANIMAL; BLOOD; C57BL MOUSE; CELL ADHESION; DRUG EFFECTS; INJURIES; LEUKOCYTE; LIVER; METABOLISM; MICROCIRCULATION; MICROVASCULATURE; PATHOLOGY; PHYSIOLOGY; PRECLINICAL STUDY; PROCEDURES; SCANNING ELECTRON MICROSCOPY; SHOCK, HEMORRHAGIC; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME; ULTRASTRUCTURE; VASCULAR ENDOTHELIUM; VASCULARIZATION;

ANIMALS; CARBON MONOXIDE; CELL ADHESION; CELL ADHESION MOLECULES; CELLS, CULTURED; CYTOKINES; DRUG EVALUATION, PRECLINICAL; ENDOTHELIUM, VASCULAR; INTERCELLULAR ADHESION MOLECULE-1; LEUKOCYTES; LIVER; MICE, INBRED C57BL; MICROCIRCULATION; MICROSCOPY, ELECTRON, SCANNING; MICROVESSELS; RESUSCITATION; SHOCK, HEMORRHAGIC; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME;

EID: 84921964513     PISSN: 10732322     EISSN: 15400514     Source Type: Journal    
DOI: 10.1097/SHK.0000000000000264     Document Type: Article

References (34)

1. Sauaia A, Moore FA, Moore EE, Moser KS, Brennan R, Read RA, Pons PT: Epidemiology of trauma deaths: a reassessment. J Trauma 38:185-193, 1995.
2. Mollen KP, Levy RM, Prince JM, Hoffman RA, Scott MJ, Kaczorowski DJ, Vallabhaneni R, Vodovotz Y, Billiar TR: Systemic inflammation and end organ damage following trauma involves functional TLR4 signaling in both bone marrow-derived cells and parenchymal cells. J Leukoc Biol 83:80-88, 2008.
3. Scalia R, Armstead VE, Minchenko AG, Lefer AM: Essential role of P-selectin in the initiation of the inflammatory response induced by hemorrhage and reinfusion. J Exp Med 189:931-938, 1999.
4. Schumacher J, Binkowski K, Dendorfer A, Klotz KF: Organ-specific extravasation of albumin-bound Evans blue during nonresuscitated hemorrhagic shock in rats. Shock 20:565-568, 2003.
5. van Meurs M, Wulfert FM, Knol AJ, De Haes A, Houwertjes M, Aarts LP, Molema G: Early organ-specific endothelial activation during hemorrhagic shock and resuscitation. Shock 29:291-299, 2008.
6. Akgur FM, Zibari GB, McDonald JC, Granger DN, Brown MF: Kinetics of Pselectin expression in regional vascular beds after resuscitation of hemorrhagic shock: a clue to the mechanism of multiple system organ failure. Shock 13: 140-144, 2000.
7. Vallabhaneni R, Kaczorowski DJ, Yaakovian MD, Rao J, Zuckerbraun BS: Heme oxygenase 1 protects against hepatic hypoxia and injury from hemorrhage via regulation of cellular respiration. Shock 33:274-281, 2010.
8. Pannen BH, Kohler N, Hole B, Bauer M, Clemens MG, Geiger KK: Protective role of endogenous carbon monoxide in hepatic microcirculatory dysfunction after hemorrhagic shock in rats. J Clin Invest 102:1220-1228, 1998.
9. Rensing H, Bauer I, Peters I, Wein T, Silomon M, Jaeschke H, Bauer M: Role of reactive oxygen species for hepatocellular injury and heme oxygenase-1 gene expression after hemorrhage and resuscitation. Shock 12:300-308, 1999.
10. Rensing H, Jaeschke H, Bauer I, Patau C, Datene V, Pannen BH, Bauer M: Differential activation pattern of redox-sensitive transcription factors and stressinducible dilator systems heme oxygenase-1 and inducible nitric oxide synthase in hemorrhagic and endotoxic shock. Crit Care Med 29:1962-1971, 2001.
11. Kubulus D, Rensing H, Paxian M, Thierbach JT, Meisel T, Redl H, Bauer M, Bauer I: Influence of heme-based solutions on stress protein expression and organ failure after hemorrhagic shock. Crit Care Med 33:629-637, 2005.
12. Zuckerbraun BS, McCloskey CA, Gallo D, Liu F, Ifedigbo E, Otterbein LE, Billiar TR: Carbon monoxide prevents multiple organ injury in a model of hemorrhagic shock and resuscitation. Shock 23:527-532, 2005.
13. Leffler CW, Parfenova H, Jaggar JH: Carbon monoxide as an endogenous vascular modulator. Am J Physiol Heart Circ Physiol 301:H1YH11, 2011.
14. Brouard S, Berberat PO, Tobiasch E, Seldon MP, Bach FH, Soares MP: Heme oxygenase-1Yderived carbon monoxide requires the activation of transcription factor NF-kappa B to protect endothelial cells from tumor necrosis factoralpha-mediated apoptosis. J Biol Chem 277:17950-17961, 2002.
15. SoaresMP, Seldon MP, Gregoire IP, Vassilevskaia T, Berberat PO, Yu J, Tsui TY, Bach FH: Heme oxygenase-1 modulates the expression of adhesion molecules associated with endothelial cell activation. J Immunol 172:3553-3563, 2004.
16. Soares MP, Usheva A, Brouard S, Berberat PO, Gunther L, Tobiasch E, Bach FH: Modulation of endothelial cell apoptosis by heme oxygenase-1Yderived carbon monoxide. Antioxid Redox Signal 4:321-329, 2002.
17. Choi YK, Por ED, Kwon YG, Kim YM: Regulation of ROS production and vascular function by carbon monoxide. Oxid Med Cell Longev 9:794-237, 2012.
18. ZuckerbraunBS, Chin BY, BilbanM, d'Avila JC, Rao J, Billiar TR, Otterbein LE: Carbon monoxide signals via inhibition of cytochrome c oxidase and generation of mitochondrial reactive oxygen species. FASEB J 21:1099-1106, 2007.
19. Lagoa CE, Vodovotz Y, Stolz DB, Lhuillier F, McCloskey C, Gallo D, Yang R, Ustinova E, Fink MP, Billiar TR, et al.: The role of hepatic type 1 plasminogen activator inhibitor (PAI-1) during murine hemorrhagic shock. Hepatology 42: 390-399, 2005.
20. Lowell CA, Fumagalli L, Berton G: Deficiency of Src family kinases p59/61hck and p58c-fgr results in defective adhesion-dependent neutrophil functions. J Cell Biol 133:895-910, 1996.
21. Hierholzer C, Billiar TR: Molecular mechanisms in the early phase of hemorrhagic shock. Langenbecks Arch Surg 386:302-308, 2001.
22. Kowalewska PM, Burrows LL, Fox-Robichaud AE: Intravital microscopy of the murine urinary bladder microcirculation. Microcirculation 18:613-622, 2011.
23. Lee WY, Kubes P: Leukocyte adhesion in the liver: distinct adhesion paradigm from other organs. J Hepatol 48:504-512, 2008.
24. Fiore E, Fusco C, Romero P, Stamenkovic I: Matrix metalloproteinase 9 (MMP-9/gelatinase B) proteolytically cleaves ICAM-1 and participates in tumor cell resistance to natural killer cellYmediated cytotoxicity. Oncogene 21: 5213-5223, 2002.
25. Katz DL, Evans MA, ChanW, Nawaz H, Comerford BP, Hoxley ML, Njike VY, Sarrel PM: Oats, antioxidants and endothelial function in overweight, dyslipidemic adults. J Am Coll Nutr 23:397-403, 2004.
26. Pober JS, Min W, Bradley JR: Mechanisms of endothelial dysfunction, injury, and death. Annu Rev Pathol 4:71-95, 2009.
27. DiStasi MR, Ley K: Opening the flood-gates: how neutrophil-endothelial interactions regulate permeability. Trends Immunol 30:547-556, 2009.
28. Sarady JK, Otterbein SL, Liu F, Otterbein LE, Choi AM: Carbon monoxide modulates endotoxin-induced production of granulocyte macrophage colonystimulating factor in macrophages. Am J Respir Cell Mol Biol 27:739-745, 2002.
29. Urquhart P, Rosignoli G, Cooper D, Motterlini R, Perretti M: Carbon monoxide-releasing molecules modulate leukocyte-endothelial interactions under flow. J Pharmacol Exp Ther 321:656-662, 2007.
30. Nakahira K, Kim HP, Geng XH, Nakao A, Wang X, Murase N, Drain PF, Wang X, Sasidhar M, Nabel EG, et al.: Carbon monoxide differentially inhibits TLR signaling pathways by regulating ROS-induced trafficking of TLRs to lipid rafts. J Exp Med 203:2377-2389, 2006.
31. Bauer I, Bauer M, Pannen BH, Leinwand MJ, Zhang JX, Clemens MG: Chronic ethanol consumption exacerbates liver injury following hemorrhagic shock: role of sinusoidal perfusion failure. Shock 4:324-331, 1995.
32. BauerM, Pannen BH, Bauer I, Herzog C,Wanner GA, Hanselmann R, Zhang JX, Clemens MG, Larsen R: Evidence for a functional link between stress response and vascular control in hepatic portal circulation. Am J Physiol 271:G929YG935, 1996.
33. Kubulus D, Mathes A, Pradarutti S, Raddatz A, Heiser J, Pavlidis D, Wolf B, Bauer I, Rensing H: Hemin arginate-induced heme oxygenase 1 expression improves liver microcirculation and mediates an anti-inflammatory cytokine response after hemorrhagic shock. Shock 29:583-590, 2008.
34. Suematsu M, Suzuki H, Delano FA, Schmid-Schonbein GW: The inflammatory aspect of the microcirculation in hypertension: oxidative stress, leukocytes/endothelial interaction, apoptosis. Microcirculation 9:259-276, 2002.