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Leo E. Otterbein, PH.D.

TitleAssociate Professor of Surgery
InstitutionBeth Israel Deaconess Medical Center
DepartmentSurgery
AddressCenter for Life Science
Surgery - EC/CLS 603
3 Blackfan Circle
Boston MA 02115
Phone617/735-2851
Fax617/735-2844

 Mentoring 
 current student opportunities
Available: 09/01/13, Expires: 08/31/14

To investigate the ability of carbon monoxide to regulate the innate immune response against a pathogen. The prospective student will assess the role of the mitochondria as the cellular target for CO that regulates sensing, phagocytosis and clearance of the bacteria by macrophages and neutrophils. The student will learn both cell culture and small animal modeling techniques, with an independent project.

Available: 09/01/13, Expires: 08/31/14

Therapeutic Gases: We are investigating the biology of gas molecules focused on carbon monoxide (CO) and nitric oxide and the enzyme systems that regulate them during pathological conditions particularly sepsis, organ transplant and cancer. Our approach is cell/molecular through to preclinical relevant animal models. CO and NO are both in clinical trials and thus any discoveries may be immediately translated to the clinic. Our studies have revealed that CO and HO-1 are necessary for innate immunity during sepsis to induce homeostatic responses. Recently, we have applied live bacteria models and showed that CO/HO-1 potentiates macrophage-mediated phagocytosis and killing of bacteria (including gram pos and neg, and tuberculosis). At present our work focuses on the role of CO on innate immunity where CO is applied post-infection to mimic clinical settings. We are now exploring the effects on viral infections as well. Additional studies ongoing in the laboratory include the effects of gases on tumor growth and vascular injury particularly how the gas molecules regulate the DNA damage and signaling and the role of stem/progenitor cells. We found that CO can inhibit tumorigenesis and sensitize tumors to chemotherapy while protecting normal cells. CO also recruits bone marrow progenitors to the site of injury. In our approaches, we use biochemical, molecular biology and cell culture techniques. We use the transgenic and knockout models for our in vivo testing including large animal models. Currently, we are generating HO-1-loxp mice. We have all the methodology for studying the gas biology. The environment in our laboratory is very interactive and allows frequent discussions and work on independent projects.


 Bibliographic 
 selected publications
Publications listed below are automatically derived from MEDLINE/PubMed and other sources, which might result in incorrect or missing publications. Faculty can login to make corrections and additions.
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  1. Jangi S, Otterbein L, Robson S. The molecular basis for the immunomodulatory activities of unconjugated bilirubin. Int J Biochem Cell Biol. 2013 Dec; 45(12):2843-51.
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  2. Wegiel B, Gallo D, Csizmadia E, Harris C, Belcher J, Vercellotti GM, Penacho N, Seth P, Sukhatme V, Ahmed A, Pandolfi PP, Helczynski L, Bjartell A, Persson JL, Otterbein LE. Carbon monoxide expedites metabolic exhaustion to inhibit tumor growth. Cancer Res. 2013 Dec 1; 73(23):7009-21.
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  3. Andria B, Bracco A, Attanasio C, Castaldo S, Cerrito MG, Cozzolino S, Di Napoli D, Giovannoni R, Mancini A, Musumeci A, Mezza E, Nasti M, Scuderi V, Staibano S, Lavitrano M, Otterbein LE, Calise F. Biliverdin Protects against Liver Ischemia Reperfusion Injury in Swine. PLoS One. 2013; 8(7):e69972.
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  4. Xue J, Kass DJ, Bon J, Vuga L, Tan J, Csizmadia E, Otterbein L, Soejima M, Levesque MC, Gibson KF, Kaminski N, Pilewski JM, Donahoe M, Sciurba FC, Duncan SR. Plasma B lymphocyte stimulator and B cell differentiation in idiopathic pulmonary fibrosis patients. J Immunol. 2013 Sep 1; 191(5):2089-95.
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  5. Kuramitsu K, Sverdlov DY, Liu SB, Csizmadia E, Burkly L, Schuppan D, Hanto DW, Otterbein LE, Popov Y. Failure of fibrotic liver regeneration in mice is linked to a severe fibrogenic response driven by hepatic progenitor cell activation. Am J Pathol. 2013 Jul; 183(1):182-94.
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  6. Nowak-Machen M, Schmelzle M, Hanidziar D, Junger W, Exley M, Otterbein L, Wu Y, Csizmadia E, Doherty G, Sitkovsky M, Robson SC. Pulmonary natural killer T cells play an essential role in mediating hyperoxic acute lung injury. Am J Respir Cell Mol Biol. 2013 May; 48(5):601-9.
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  7. Schallner N, Romão CC, Biermann J, Lagrèze WA, Otterbein LE, Buerkle H, Loop T, Goebel U. Carbon Monoxide Abrogates Ischemic Insult to Neuronal Cells via the Soluble Guanylate Cyclase-cGMP Pathway. PLoS One. 2013; 8(4):e60672.
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  8. Seixas JD, Mukhopadhyay A, Santos-Silva T, Otterbein LE, Gallo DJ, Rodrigues SS, Guerreiro BH, Gonçalves AM, Penacho N, Marques AR, Coelho AC, Reis PM, Romão MJ, Romão CC. Characterization of a versatile organometallic pro-drug (CORM) for experimental CO based therapeutics. Dalton Trans. 2013 Apr 2; 42(17):5985-98.
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  9. Kahloon RA, Xue J, Bhargava A, Csizmadia E, Otterbein L, Kass DJ, Bon J, Soejima M, Levesque MC, Lindell KO, Gibson KF, Kaminski N, Banga G, Oddis CV, Pilewski JM, Sciurba FC, Donahoe M, Zhang Y, Duncan SR. Patients with idiopathic pulmonary fibrosis with antibodies to heat shock protein 70 have poor prognoses. Am J Respir Crit Care Med. 2013 Apr; 187(7):768-75.
    View in: PubMed
  10. Sun S, Sursal T, Adibnia Y, Zhao C, Zheng Y, Li H, Otterbein LE, Hauser CJ, Itagaki K. Mitochondrial DAMPs Increase Endothelial Permeability through Neutrophil Dependent and Independent Pathways. PLoS One. 2013; 8(3):e59989.
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  11. Otterbein LE. Quoth the Raven: carbon monoxide and nothing more. Med Gas Res. 2013; 3(1):7.
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  12. Hanafy KA, Oh J, Otterbein LE. Carbon monoxide and the brain: time to rethink the dogma. Curr Pharm Des. 2013; 19(15):2771-5.
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  13. Onyiah JC, Sheikh SZ, Maharshak N, Steinbach EC, Russo SM, Kobayashi T, Mackey LC, Hansen JJ, Moeser AJ, Rawls JF, Borst LB, Otterbein LE, Plevy SE. Carbon monoxide and heme oxygenase-1 prevent intestinal inflammation in mice by promoting bacterial clearance. Gastroenterology. 2013 Apr; 144(4):789-98.
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  14. Wegiel B, Hanto DW, Otterbein LE. The social network of carbon monoxide in medicine. Trends Mol Med. 2013 Jan; 19(1):3-11.
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  15. Mahan VL, Zurakowski D, Otterbein LE, Pigula FA. Inhaled carbon monoxide provides cerebral cytoprotection in pigs. PLoS One. 2012; 7(8):e41982.
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  16. Banerjee P, Basu A, Wegiel B, Otterbein LE, Mizumura K, Gasser M, Waaga-Gasser AM, Choi AM, Pal S. Heme oxygenase-1 promotes survival of renal cancer cells through modulation of apoptosis- and autophagy-regulating molecules. J Biol Chem. 2012 Sep 14; 287(38):32113-23.
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  17. Haschemi A, Kosma P, Gille L, Evans CR, Burant CF, Starkl P, Knapp B, Haas R, Schmid JA, Jandl C, Amir S, Lubec G, Park J, Esterbauer H, Bilban M, Brizuela L, Pospisilik JA, Otterbein LE, Wagner O. The sedoheptulose kinase CARKL directs macrophage polarization through control of glucose metabolism. Cell Metab. 2012 Jun 6; 15(6):813-26.
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  18. Wang H, Wu H, Rocuts F, Gu Z, Bach FH, Otterbein LE. Activation of Peroxisome Proliferator-Activated Receptor ? Prolongs Islet Allograft Survival. Cell Transplant. 2012; 21(10):2111-8.
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  19. Wegiel B, Otterbein LE. Go green: the anti-inflammatory effects of biliverdin reductase. Front Pharmacol. 2012; 3:47.
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  20. Stoeckius M, Erat A, Fujikawa T, Hiromura M, Koulova A, Otterbein L, Bianchi C, Tobiasch E, Dagon Y, Sellke FW, Usheva A. Essential roles of Raf/extracellular signal-regulated kinase/mitogen-activated protein kinase pathway, YY1, and Ca2+ influx in growth arrest of human vascular smooth muscle cells by bilirubin. J Biol Chem. 2012 May 4; 287(19):15418-26.
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  21. Wang H, Ferran C, Attanasio C, Calise F, Otterbein LE. Induction of protective genes leads to islet survival and function. J Transplant. 2011; 2011:141898.
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  22. Wegiel B, Gallo D, Csizmadia E, Roger T, Kaczmarek E, Harris C, Zuckerbraun BS, Otterbein LE. Biliverdin inhibits Toll-like receptor-4 (TLR4) expression through nitric oxide-dependent nuclear translocation of biliverdin reductase. Proc Natl Acad Sci U S A. 2011 Nov 15; 108(46):18849-54.
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  23. Haschemi A, Chin BY, Jeitler M, Esterbauer H, Wagner O, Bilban M, Otterbein LE. Carbon monoxide induced PPAR? SUMOylation and UCP2 block inflammatory gene expression in macrophages. PLoS One. 2011; 6(10):e26376.
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  24. Otterbein LE, Hedblom A, Harris C, Csizmadia E, Gallo D, Wegiel B. Heme oxygenase-1 and carbon monoxide modulate DNA repair through ataxia-telangiectasia mutated (ATM) protein. Proc Natl Acad Sci U S A. 2011 Aug 30; 108(35):14491-6.
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  25. Kuramitsu K, Gallo D, Yoon M, Chin BY, Csizmadia E, Hanto DW, Otterbein LE. Carbon monoxide enhances early liver regeneration in mice after hepatectomy. Hepatology. 2011 Jun; 53(6):2016-26.
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  26. Sheikh SZ, Hegazi RA, Kobayashi T, Onyiah JC, Russo SM, Matsuoka K, Sepulveda AR, Li F, Otterbein LE, Plevy SE. An anti-inflammatory role for carbon monoxide and heme oxygenase-1 in chronic Th2-mediated murine colitis. J Immunol. 2011 May 1; 186(9):5506-13.
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  27. Cerrito MG, Scagliarini A, Froio A, Liloia A, Busnelli M, Giovannoni R, Otterbein LE, Mainetti L, Villa M, Bach FH, Leone BE, Biasi GM, Lavitrano M. Heme oxygenase-1 inhibition prevents intimal hyperplasia enhancing nitric oxide-dependent apoptosis of vascular smooth muscle cells. Biol Pharm Bull. 2011; 34(8):1204-14.
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  28. Hanto DW, Maki T, Yoon MH, Csizmadia E, Chin BY, Gallo D, Konduru B, Kuramitsu K, Smith NR, Berssenbrugge A, Attanasio C, Thomas M, Wegiel B, Otterbein LE. Intraoperative administration of inhaled carbon monoxide reduces delayed graft function in kidney allografts in Swine. Am J Transplant. 2010 Nov; 10(11):2421-30.
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  29. Motterlini R, Otterbein LE. The therapeutic potential of carbon monoxide. Nat Rev Drug Discov. 2010 Sep; 9(9):728-43.
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  30. Wegiel B, Evans S, Hellsten R, Otterbein LE, Bjartell A, Persson JL. Molecular pathways in the progression of hormone-independent and metastatic prostate cancer. Curr Cancer Drug Targets. 2010 Jun; 10(4):392-401.
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  31. Wegiel B, Gallo DJ, Raman KG, Karlsson JM, Ozanich B, Chin BY, Tzeng E, Ahmad S, Ahmed A, Baty CJ, Otterbein LE. Nitric oxide-dependent bone marrow progenitor mobilization by carbon monoxide enhances endothelial repair after vascular injury. Circulation. 2010 Feb 2; 121(4):537-48.
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  32. Vandorpe DH, Xu C, Shmukler BE, Otterbein LE, Trudel M, Sachs F, Gottlieb PA, Brugnara C, Alper SL. Hypoxia activates a Ca2+-permeable cation conductance sensitive to carbon monoxide and to GsMTx-4 in human and mouse sickle erythrocytes. PLoS One. 2010; 5(1):e8732.
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  33. Wegiel B, Jiborn T, Abrahamson M, Helczynski L, Otterbein L, Persson JL, Bjartell A. Cystatin C is downregulated in prostate cancer and modulates invasion of prostate cancer cells via MAPK/Erk and androgen receptor pathways. PLoS One. 2009; 4(11):e7953.
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  34. Chin BY, Otterbein LE. Carbon monoxide is a poison... to microbes! CO as a bactericidal molecule. Curr Opin Pharmacol. 2009 Aug; 9(4):490-500.
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  35. Otterbein LE. The evolution of carbon monoxide into medicine. Respir Care. 2009 Jul; 54(7):925-32.
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  36. Wegiel B, Baty CJ, Gallo D, Csizmadia E, Scott JR, Akhavan A, Chin BY, Kaczmarek E, Alam J, Bach FH, Zuckerbraun BS, Otterbein LE. Cell surface biliverdin reductase mediates biliverdin-induced anti-inflammatory effects via phosphatidylinositol 3-kinase and Akt. J Biol Chem. 2009 Aug 7; 284(32):21369-78.
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  37. Bilban M, Haslinger P, Prast J, Klinglmüller F, Woelfel T, Haider S, Sachs A, Otterbein LE, Desoye G, Hiden U, Wagner O, Knöfler M. Identification of novel trophoblast invasion-related genes: heme oxygenase-1 controls motility via peroxisome proliferator-activated receptor gamma. Endocrinology. 2009 Feb; 150(2):1000-13.
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  38. Wegiel B, Bjartell A, Tuomela J, Dizeyi N, Tinzl M, Helczynski L, Nilsson E, Otterbein LE, Härkönen P, Persson JL. Multiple cellular mechanisms related to cyclin A1 in prostate cancer invasion and metastasis. J Natl Cancer Inst. 2008 Jul 16; 100(14):1022-36.
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  39. Wegiel B, Chin BY, Otterbein LE. Inhale to survive, cycle or die? Carbon monoxide and cellular proliferation. Cell Cycle. 2008 May 15; 7(10):1379-84.
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  40. Bilban M, Haschemi A, Wegiel B, Chin BY, Wagner O, Otterbein LE. Heme oxygenase and carbon monoxide initiate homeostatic signaling. J Mol Med (Berl). 2008 Mar; 86(3):267-79.
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  41. Feghali-Bostwick CA, Gadgil AS, Otterbein LE, Pilewski JM, Stoner MW, Csizmadia E, Zhang Y, Sciurba FC, Duncan SR. Autoantibodies in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2008 Jan 15; 177(2):156-63.
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  42. Lee SS, Gao W, Mazzola S, Thomas MN, Csizmadia E, Otterbein LE, Bach FH, Wang H. Heme oxygenase-1, carbon monoxide, and bilirubin induce tolerance in recipients toward islet allografts by modulating T regulatory cells. FASEB J. 2007 Nov; 21(13):3450-7.
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  43. Goldberg A, Parolini M, Chin BY, Czismadia E, Otterbein LE, Bach FH, Wang H. Toll-like receptor 4 suppression leads to islet allograft survival. FASEB J. 2007 Sep; 21(11):2840-8.
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  44. Haschemi A, Wagner O, Marculescu R, Wegiel B, Robson SC, Gagliani N, Gallo D, Chen JF, Bach FH, Otterbein LE. Cross-regulation of carbon monoxide and the adenosine A2a receptor in macrophages. J Immunol. 2007 May 1; 178(9):5921-9.
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  45. Scott JR, Chin BY, Bilban MH, Otterbein LE. Restoring HOmeostasis: is heme oxygenase-1 ready for the clinic? Trends Pharmacol Sci. 2007 May; 28(5):200-5.
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  46. Chin BY, Jiang G, Wegiel B, Wang HJ, Macdonald T, Zhang XC, Gallo D, Cszimadia E, Bach FH, Lee PJ, Otterbein LE. Hypoxia-inducible factor 1alpha stabilization by carbon monoxide results in cytoprotective preconditioning. Proc Natl Acad Sci U S A. 2007 Mar 20; 104(12):5109-14.
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  47. Zuckerbraun BS, Chin BY, Bilban M, 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. 2007 Apr; 21(4):1099-106.
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  48. Ramlawi B, Scott JR, Feng J, Mieno S, Raman KG, Gallo D, Csizmadia E, Yoke Chin B, Bach FH, Otterbein LE, Sellke FW. Inhaled carbon monoxide prevents graft-induced intimal hyperplasia in swine. J Surg Res. 2007 Mar; 138(1):121-7.
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  49. Zhang X, Shan P, Jiang G, Zhang SS, Otterbein LE, Fu XY, Lee PJ. Endothelial STAT3 is essential for the protective effects of HO-1 in oxidant-induced lung injury. FASEB J. 2006 Oct; 20(12):2156-8.
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  50. Zuckerbraun BS, Chin BY, Wegiel B, Billiar TR, Czsimadia E, Rao J, Shimoda L, Ifedigbo E, Kanno S, Otterbein LE. Carbon monoxide reverses established pulmonary hypertension. J Exp Med. 2006 Sep 4; 203(9):2109-19.
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  51. Raman KG, Barbato JE, Ifedigbo E, Ozanich BA, Zenati MS, Otterbein LE, Tzeng E. Inhaled carbon monoxide inhibits intimal hyperplasia and provides added benefit with nitric oxide. J Vasc Surg. 2006 Jul; 44(1):151-8.
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  52. Bilban M, Bach FH, Otterbein SL, Ifedigbo E, d'Avila JC, Esterbauer H, Chin BY, Usheva A, Robson SC, Wagner O, Otterbein LE. Carbon monoxide orchestrates a protective response through PPARgamma. Immunity. 2006 May; 24(5):601-10.
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  53. Belcher JD, Mahaseth H, Welch TE, Otterbein LE, Hebbel RP, Vercellotti GM. Heme oxygenase-1 is a modulator of inflammation and vaso-occlusion in transgenic sickle mice. J Clin Invest. 2006 Mar; 116(3):808-16.
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  54. Hegazi RA, Rao KN, Mayle A, Sepulveda AR, Otterbein LE, Plevy SE. Carbon monoxide ameliorates chronic murine colitis through a heme oxygenase 1-dependent pathway. J Exp Med. 2005 Dec 19; 202(12):1703-13.
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  55. Mazzola S, Forni M, Albertini M, Bacci ML, Zannoni A, Gentilini F, Lavitrano M, Bach FH, Otterbein LE, Clement MG. Carbon monoxide pretreatment prevents respiratory derangement and ameliorates hyperacute endotoxic shock in pigs. FASEB J. 2005 Dec; 19(14):2045-7.
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  56. Otterbein LE, May A, Chin BY. Carbon monoxide increases macrophage bacterial clearance through Toll-like receptor (TLR)4 expression. Cell Mol Biol (Noisy-le-grand). 2005 Oct 3; 51(5):433-40.
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  57. Sarady-Andrews JK, Liu F, Gallo D, Nakao A, Overhaus M, Ollinger R, Choi AM, Otterbein LE. Biliverdin administration protects against endotoxin-induced acute lung injury in rats. Am J Physiol Lung Cell Mol Physiol. 2005 Dec; 289(6):L1131-7.
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  58. Ollinger R, Bilban M, Erat A, Froio A, McDaid J, Tyagi S, Csizmadia E, Graça-Souza AV, Liloia A, Soares MP, Otterbein LE, Usheva A, Yamashita K, Bach FH. Bilirubin: a natural inhibitor of vascular smooth muscle cell proliferation. Circulation. 2005 Aug 16; 112(7):1030-9.
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  59. Moore BA, Overhaus M, Whitcomb J, Ifedigbo E, Choi AM, Otterbein LE, Bauer AJ. Brief inhalation of low-dose carbon monoxide protects rodents and swine from postoperative ileus. Crit Care Med. 2005 Jun; 33(6):1317-26.
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  60. 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. 2005 Jun; 23(6):527-32.
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  61. Zuckerbraun BS, Otterbein LE, Boyle P, Jaffe R, Upperman J, Zamora R, Ford HR. Carbon monoxide protects against the development of experimental necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol. 2005 Sep; 289(3):G607-13.
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  62. Nakao A, Neto JS, Kanno S, Stolz DB, Kimizuka K, Liu F, Bach FH, Billiar TR, Choi AM, Otterbein LE, Murase N. Protection against ischemia/reperfusion injury in cardiac and renal transplantation with carbon monoxide, biliverdin and both. Am J Transplant. 2005 Feb; 5(2):282-91.
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  63. Ott MC, Scott JR, Bihari A, Badhwar A, Otterbein LE, Gray DK, Harris KA, Potter RF. Inhalation of carbon monoxide prevents liver injury and inflammation following hind limb ischemia/reperfusion. FASEB J. 2005 Jan; 19(1):106-8.
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  64. Neto JS, Nakao A, Kimizuka K, Romanosky AJ, Stolz DB, Uchiyama T, Nalesnik MA, Otterbein LE, Murase N. Protection of transplant-induced renal ischemia-reperfusion injury with carbon monoxide. Am J Physiol Renal Physiol. 2004 Nov; 287(5):F979-89.
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  65. Nakao A, Otterbein LE, Overhaus M, Sarady JK, Tsung A, Kimizuka K, Nalesnik MA, Kaizu T, Uchiyama T, Liu F, Murase N, Bauer AJ, Bach FH. Biliverdin protects the functional integrity of a transplanted syngeneic small bowel. Gastroenterology. 2004 Aug; 127(2):595-606.
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  66. Song R, Zhou Z, Kim PK, Shapiro RA, Liu F, Ferran C, Choi AM, Otterbein LE. Carbon monoxide promotes Fas/CD95-induced apoptosis in Jurkat cells. J Biol Chem. 2004 Oct 22; 279(43):44327-34.
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  67. Lavitrano M, Smolenski RT, Musumeci A, Maccherini M, Slominska E, Di Florio E, Bracco A, Mancini A, Stassi G, Patti M, Giovannoni R, Froio A, Simeone F, Forni M, Bacci ML, D'Alise G, Cozzi E, Otterbein LE, Yacoub MH, Bach FH, Calise F. Carbon monoxide improves cardiac energetics and safeguards the heart during reperfusion after cardiopulmonary bypass in pigs. FASEB J. 2004 Jul; 18(10):1093-5.
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  68. Sarady JK, Zuckerbraun BS, Bilban M, Wagner O, Usheva A, Liu F, Ifedigbo E, Zamora R, Choi AM, Otterbein LE. Carbon monoxide protection against endotoxic shock involves reciprocal effects on iNOS in the lung and liver. FASEB J. 2004 May; 18(7):854-6.
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  69. Ryter SW, Otterbein LE. Carbon monoxide in biology and medicine. Bioessays. 2004 Mar; 26(3):270-80.
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  70. Akamatsu Y, Haga M, Tyagi S, Yamashita K, Graça-Souza AV, Ollinger R, Czismadia E, May GA, Ifedigbo E, Otterbein LE, Bach FH, Soares MP. Heme oxygenase-1-derived carbon monoxide protects hearts from transplant associated ischemia reperfusion injury. FASEB J. 2004 Apr; 18(6):771-2.
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  71. Song R, Mahidhara RS, Zhou Z, Hoffman RA, Seol DW, Flavell RA, Billiar TR, Otterbein LE, Choi AM. Carbon monoxide inhibits T lymphocyte proliferation via caspase-dependent pathway. J Immunol. 2004 Jan 15; 172(2):1220-6.
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  72. Kim PK, Zuckerbraun BS, Otterbein LE, Vodovotz Y, Billiar TR. 'Til cell death do us part: nitric oxide and mechanisms of hepatotoxicity. Biol Chem. 2004 Jan; 385(1):11-5.
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  73. Otterbein LE, Otterbein SL, Ifedigbo E, Liu F, Morse DE, Fearns C, Ulevitch RJ, Knickelbein R, Flavell RA, Choi AM. MKK3 mitogen-activated protein kinase pathway mediates carbon monoxide-induced protection against oxidant-induced lung injury. Am J Pathol. 2003 Dec; 163(6):2555-63.
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  74. Zuckerbraun BS, Billiar TR, Otterbein SL, Kim PK, Liu F, Choi AM, Bach FH, Otterbein LE. Carbon monoxide protects against liver failure through nitric oxide-induced heme oxygenase 1. J Exp Med. 2003 Dec 1; 198(11):1707-16.
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  75. Nakao A, Kimizuka K, Stolz DB, Neto JS, Kaizu T, Choi AM, Uchiyama T, Zuckerbraun BS, Nalesnik MA, Otterbein LE, Murase N. Carbon monoxide inhalation protects rat intestinal grafts from ischemia/reperfusion injury. Am J Pathol. 2003 Oct; 163(4):1587-98.
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  76. Nakao A, Moore BA, Murase N, Liu F, Zuckerbraun BS, Bach FH, Choi AM, Nalesnik MA, Otterbein LE, Bauer AJ. Immunomodulatory effects of inhaled carbon monoxide on rat syngeneic small bowel graft motility. Gut. 2003 Sep; 52(9):1278-85.
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  77. Ameredes BT, Otterbein LE, Kohut LK, Gligonic AL, Calhoun WJ, Choi AM. Low-dose carbon monoxide reduces airway hyperresponsiveness in mice. Am J Physiol Lung Cell Mol Physiol. 2003 Dec; 285(6):L1270-6.
    View in: PubMed
  78. Otterbein LE, Soares MP, Yamashita K, Bach FH. Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol. 2003 Aug; 24(8):449-55.
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  79. Nakao A, Kimizuka K, Stolz DB, Seda Neto J, Kaizu T, Choi AM, Uchiyama T, Zuckerbraun BS, Bauer AJ, Nalesnik MA, Otterbein LE, Geller DA, Murase N. Protective effect of carbon monoxide inhalation for cold-preserved small intestinal grafts. Surgery. 2003 Aug; 134(2):285-92.
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  80. Berberat PO, Katori M, Kaczmarek E, Anselmo D, Lassman C, Ke B, Shen X, Busuttil RW, Yamashita K, Csizmadia E, Tyagi S, Otterbein LE, Brouard S, Tobiasch E, Bach FH, Kupiec-Weglinski JW, Soares MP. Heavy chain ferritin acts as an antiapoptotic gene that protects livers from ischemia reperfusion injury. FASEB J. 2003 Sep; 17(12):1724-6.
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  81. Morse D, Pischke SE, Zhou Z, Davis RJ, Flavell RA, Loop T, Otterbein SL, Otterbein LE, Choi AM. Suppression of inflammatory cytokine production by carbon monoxide involves the JNK pathway and AP-1. J Biol Chem. 2003 Sep 26; 278(39):36993-8.
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  82. Song R, Kubo M, Morse D, Zhou Z, Zhang X, Dauber JH, Fabisiak J, Alber SM, Watkins SC, Zuckerbraun BS, Otterbein LE, Ning W, Oury TD, Lee PJ, McCurry KR, Choi AM. Carbon monoxide induces cytoprotection in rat orthotopic lung transplantation via anti-inflammatory and anti-apoptotic effects. Am J Pathol. 2003 Jul; 163(1):231-42.
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  83. Morse D, Otterbein LE, Watkins S, Alber S, Zhou Z, Flavell RA, Davis RJ, Choi AM. Deficiency in the c-Jun NH2-terminal kinase signaling pathway confers susceptibility to hyperoxic lung injury in mice. Am J Physiol Lung Cell Mol Physiol. 2003 Jul; 285(1):L250-7.
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  84. Moore BA, Otterbein LE, Türler A, Choi AM, Bauer AJ. Inhaled carbon monoxide suppresses the development of postoperative ileus in the murine small intestine. Gastroenterology. 2003 Feb; 124(2):377-91.
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  85. Otterbein LE, Zuckerbraun BS, Haga M, Liu F, Song R, Usheva A, Stachulak C, Bodyak N, Smith RN, Csizmadia E, Tyagi S, Akamatsu Y, Flavell RJ, Billiar TR, Tzeng E, Bach FH, Choi AM, Soares MP. Carbon monoxide suppresses arteriosclerotic lesions associated with chronic graft rejection and with balloon injury. Nat Med. 2003 Feb; 9(2):183-90.
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  86. Sarady JK, Otterbein SL, Liu F, Otterbein LE, Choi AM. Carbon monoxide modulates endotoxin-induced production of granulocyte macrophage colony-stimulating factor in macrophages. Am J Respir Cell Mol Biol. 2002 Dec; 27(6):739-45.
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  87. Song R, Mahidhara RS, Liu F, Ning W, Otterbein LE, Choi AM. Carbon monoxide inhibits human airway smooth muscle cell proliferation via mitogen-activated protein kinase pathway. Am J Respir Cell Mol Biol. 2002 Nov; 27(5):603-10.
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  88. Zhang X, Shan P, Otterbein LE, Alam J, Flavell RA, Davis RJ, Choi AM, Lee PJ. Carbon monoxide inhibition of apoptosis during ischemia-reperfusion lung injury is dependent on the p38 mitogen-activated protein kinase pathway and involves caspase 3. J Biol Chem. 2003 Jan 10; 278(2):1248-58.
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  89. Song R, Ning W, Liu F, Ameredes BT, Calhoun WJ, Otterbein LE, Choi AM. Regulation of IL-1beta -induced GM-CSF production in human airway smooth muscle cells by carbon monoxide. Am J Physiol Lung Cell Mol Physiol. 2003 Jan; 284(1):L50-6.
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  90. Ryter SW, Otterbein LE, Morse D, Choi AM. Heme oxygenase/carbon monoxide signaling pathways: regulation and functional significance. Mol Cell Biochem. 2002 May-Jun; 234-235(1-2):249-63.
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  91. Choi AM, Otterbein LE. Emerging role of carbon monoxide in physiologic and pathophysiologic states. Antioxid Redox Signal. 2002 Apr; 4(2):227-8.
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  92. Sethi JM, Otterbein LE, Choi AM. Differential modulation by exogenous carbon monoxide of TNF-alpha stimulated mitogen-activated protein kinases in rat pulmonary artery endothelial cells. Antioxid Redox Signal. 2002 Apr; 4(2):241-8.
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  93. Otterbein LE. Carbon monoxide: innovative anti-inflammatory properties of an age-old gas molecule. Antioxid Redox Signal. 2002 Apr; 4(2):309-19.
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  94. Otterbein LE, Choi AM. The saga of leucine zippers continues: in response to oxidative stress. Am J Respir Cell Mol Biol. 2002 Feb; 26(2):161-3.
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  95. Chapman JT, Otterbein LE, Elias JA, Choi AM. Carbon monoxide attenuates aeroallergen-induced inflammation in mice. Am J Physiol Lung Cell Mol Physiol. 2001 Jul; 281(1):L209-16.
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  96. Sato K, Balla J, Otterbein L, Smith RN, Brouard S, Lin Y, Csizmadia E, Sevigny J, Robson SC, Vercellotti G, Choi AM, Bach FH, Soares MP. Carbon monoxide generated by heme oxygenase-1 suppresses the rejection of mouse-to-rat cardiac transplants. J Immunol. 2001 Mar 15; 166(6):4185-94.
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  97. Lu Y, Parkyn L, Otterbein LE, Kureishi Y, Walsh K, Ray A, Ray P. Activated Akt protects the lung from oxidant-induced injury and delays death of mice. J Exp Med. 2001 Feb 19; 193(4):545-49.
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  98. Otterbein LE, Choi AM. Heme oxygenase: colors of defense against cellular stress. Am J Physiol Lung Cell Mol Physiol. 2000 Dec; 279(6):L1029-37.
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  99. Brouard S, Otterbein LE, Anrather J, Tobiasch E, Bach FH, Choi AM, Soares MP. Carbon monoxide generated by heme oxygenase 1 suppresses endothelial cell apoptosis. J Exp Med. 2000 Oct 2; 192(7):1015-26.
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  100. Otterbein LE, Bach FH, Alam J, Soares M, Tao Lu H, Wysk M, Davis RJ, Flavell RA, Choi AM. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med. 2000 Apr; 6(4):422-8.
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  101. Petrache I, Otterbein LE, Alam J, Wiegand GW, Choi AM. Heme oxygenase-1 inhibits TNF-alpha-induced apoptosis in cultured fibroblasts. Am J Physiol Lung Cell Mol Physiol. 2000 Feb; 278(2):L312-9.
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  102. Petrache I, Choi ME, Otterbein LE, Chin BY, Mantell LL, Horowitz S, Choi AM. Mitogen-activated protein kinase pathway mediates hyperoxia-induced apoptosis in cultured macrophage cells. Am J Physiol. 1999 Sep; 277(3 Pt 1):L589-95.
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  103. Otterbein LE, Lee PJ, Chin BY, Petrache I, Camhi SL, Alam J, Choi AM. Protective effects of heme oxygenase-1 in acute lung injury. Chest. 1999 Jul; 116(1 Suppl):61S-63S.
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  104. Otterbein LE, Kolls JK, Mantell LL, Cook JL, Alam J, Choi AM. Exogenous administration of heme oxygenase-1 by gene transfer provides protection against hyperoxia-induced lung injury. J Clin Invest. 1999 Apr; 103(7):1047-54.
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  105. Otterbein LE, Mantell LL, Choi AM. Carbon monoxide provides protection against hyperoxic lung injury. Am J Physiol. 1999 Apr; 276(4 Pt 1):L688-94.
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  106. Gaine SP, Booth G, Otterbein L, Flavahan NA, Choi AM, Wiener CM. Induction of heme oxygenase-1 with hemoglobin depresses vasoreactivity in rat aorta. J Vasc Res. 1999 Mar-Apr; 36(2):114-9.
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  107. Otterbein LE, Chin BY, Mantell LL, Stansberry L, Horowitz S, Choi AM. Pulmonary apoptosis in aged and oxygen-tolerant rats exposed to hyperoxia. Am J Physiol. 1998 Jul; 275(1 Pt 1):L14-20.
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  108. Otterbein L, Chin BY, Otterbein SL, Lowe VC, Fessler HE, Choi AM. Mechanism of hemoglobin-induced protection against endotoxemia in rats: a ferritin-independent pathway. Am J Physiol. 1997 Feb; 272(2 Pt 1):L268-75.
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  109. Fessler HE, Otterbein L, Chung HS, Choi AM. Alpha-2 adrenoceptor blockade protects rats against lipopolysaccharide. Am J Respir Crit Care Med. 1996 Dec; 154(6 Pt 1):1689-93.
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  110. Kotanidou A, Choi AM, Winchurch RA, Otterbein L, Fessler HE. Urethan anesthesia protects rats against lethal endotoxemia and reduces TNF-alpha release. J Appl Physiol. 1996 Nov; 81(5):2305-11.
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  111. Lee PJ, Alam J, Sylvester SL, Inamdar N, Otterbein L, Choi AM. Regulation of heme oxygenase-1 expression in vivo and in vitro in hyperoxic lung injury. Am J Respir Cell Mol Biol. 1996 Jun; 14(6):556-68.
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  112. Otterbein L, Sylvester SL, Choi AM. Hemoglobin provides protection against lethal endotoxemia in rats: the role of heme oxygenase-1. Am J Respir Cell Mol Biol. 1995 Nov; 13(5):595-601.
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  113. Camhi SL, Alam J, Otterbein L, Sylvester SL, Choi AM. Induction of heme oxygenase-1 gene expression by lipopolysaccharide is mediated by AP-1 activation. Am J Respir Cell Mol Biol. 1995 Oct; 13(4):387-98.
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  114. Choi AM, Sylvester S, Otterbein L, Holbrook NJ. Molecular responses to hyperoxia in vivo: relationship to increased tolerance in aged rats. Am J Respir Cell Mol Biol. 1995 Jul; 13(1):74-82.
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  115. Bassett DJ, Elbon CL, Ishii Y, Yang H, Otterbein L, Boswell GA, Kerr JS. EDU pretreatment decreases polymorphonuclear leukocyte migration into rat lung airways. Toxicol Appl Pharmacol. 1994 Jul; 127(1):76-82.
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  116. Noronha-Blob L, Lowe VC, Otterbein L, Steranka L, Burch RM. NPC 15669 reduces mortality associated with sepsis in rats. J Pharmacol Exp Ther. 1993 Nov; 267(2):664-9.
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  117. Otterbein L, Lowe VC, Kyle DJ, Noronha-Blob L. Additive effects of a bradykinin antagonist, NPC 17761, and a leumedin, NPC 15669, on survival in animal models of sepsis. Agents Actions. 1993; 39 Spec No:C125-7.
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