Home | Help | Feedback | Subscriptions | Archive | Search | Table of Contents

This Article Full Text Full Text (PDF, 452K) PPT slides of all figures Alert me when this article is cited Citation Map Services Email this article Similar articles in this journal Similar articles in PubMed Alert me to new content in the JEM Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via CrossRef Citing Articles via Google Scholar Google Scholar Articles by Brouard, S. Articles by Soares, M. P. Search for Related Content PubMed PubMed Citation Articles by Brouard, S. Articles by Soares, M. P. Social Bookmarking                            What's this?

Original Article

^a Immunobiology Research Center, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts 02215
^b Department of Internal Medicine, Pulmonary and Critical Care Section, Yale University, School of Medicine, New Haven, Connecticut 06520
^c Department of Neurobiology, Weill Medical College of Cornell University, New York, New York 10021
Immunobiology Research Center, Beth Israel Deaconess Medical Center, Harvard Medical School, 99 Brookline Ave., Boston, MA 02215.617-632-0880617-632-0885

Heme oxygenase 1 (HO-1) inhibits apoptosis by regulating cellular prooxidant iron. We now show that there is an additional mechanism by which HO-1 inhibits apoptosis, namely by generating the gaseous molecule carbon monoxide (CO). Overexpression of HO-1, or induction of HO-1 expression by heme, protects endothelial cells (ECs) from apoptosis. When HO-1 enzymatic activity is blocked by tin protoporphyrin (SnPPIX) or the action of CO is inhibited by hemoglobin (Hb), HO-1 no longer prevents EC apoptosis while these reagents do not affect the antiapoptotic action of bcl-2. Exposure of ECs to exogenous CO, under inhibition of HO-1 activity by SnPPIX, substitutes HO-1 in preventing EC apoptosis. The mechanism of action of HO-1/CO is dependent on the activation of the p38 mitogen-activated protein kinase (MAPK) signaling transduction pathway. Expression of HO-1 or exposure of ECs to exogenous CO enhanced p38 MAPK activation by TNF-. Specific inhibition of p38 MAPK activation by the pyridinyl imidazol SB203580 or through overexpression of a p38 MAPK dominant negative mutant abrogated the antiapoptotic effect of HO-1. Taken together, these data demonstrate that the antiapoptotic effect of HO-1 in ECs is mediated by CO and more specifically via the activation of p38 MAPK by CO.

Key Words: apoptosis • endothelial cells • heme oxygenase 1 • carbon monoxide • p38 mitogen-activated protein kinase

Abbreviations used in this paper: Act.D, actinomycin D; BAEC, bovine aortic endothelial cell; CoPPIX, cobalt protoporphyrin; DFO, deferoxamine mesylate; EC, endothelial cell; ERK, extracellular signal–regulated kinase; FePP, iron protoporphyrin; GFP, green fluorescent protein; Hb, hemoglobin; HO-1, heme oxygenase 1; JNK, c-Jun NH₂-terminal kinase; MAPK, mitogen-activated protein kinase; M, monocyte/macrophage(s); ppm, parts per million; SnPPIX, tin protoporphyrin; VASP, vasodilatator-stimulated phosphoprotein.

© 2000 The Rockefeller University Press

CiteULike    Complore    Connotea    Del.icio.us    Digg    Facebook    Reddit    Technorati    Twitter    What's this?

This article has been cited by other articles:

• Silva, G., Jeney, V., Chora, A., Larsen, R., Balla, J., Soares, M. P. (2009). Oxidized Hemoglobin Is an Endogenous Proinflammatory Agonist That Targets Vascular Endothelial Cells. J. Biol. Chem. 284: 29582-29595 [Abstract] [Full Text]  
• Clapp, C., Thebault, S., Jeziorski, M. C., Martinez De La Escalera, G. (2009). Peptide Hormone Regulation of Angiogenesis. Physiol. Rev. 89: 1177-1215 [Abstract] [Full Text]  
• Wei, Y., Liu, X.-m., Peyton, K. J., Wang, H., Johnson, F. K., Johnson, R. A., Durante, W. (2009). Hypochlorous acid-induced heme oxygenase-1 gene expression promotes human endothelial cell survival. Am. J. Physiol. Cell Physiol. 297: C907-C915 [Abstract] [Full Text]  
• Ryter, S. W., Choi, A. M. K. (2009). Heme Oxygenase-1/Carbon Monoxide: From Metabolism to Molecular Therapy. Am. J. Respir. Cell Mol. Bio. 41: 251-260 [Abstract] [Full Text]  
• Zheng, L., Zhou, Z., Lin, L., Alber, S., Watkins, S., Kaminski, N., Choi, A. M. K., Morse, D. (2009). Carbon Monoxide Modulates {alpha}-Smooth Muscle Actin and Small Proline Rich-1a Expression in Fibrosis. Am. J. Respir. Cell Mol. Bio. 41: 85-92 [Abstract] [Full Text]  
• Morales, A. A., Gutman, D., Cejas, P. J., Lee, K. P., Boise, L. H. (2009). Reactive Oxygen Species Are Not Required for an Arsenic Trioxide-induced Antioxidant Response or Apoptosis. J. Biol. Chem. 284: 12886-12895 [Abstract] [Full Text]  
• Zaki, M. H., Fujii, S., Okamoto, T., Islam, S., Khan, S., Ahmed, K. A., Sawa, T., Akaike, T. (2009). Cytoprotective Function of Heme Oxygenase 1 Induced by a Nitrated Cyclic Nucleotide Formed during Murine Salmonellosis. J. Immunol. 182: 3746-3756 [Abstract] [Full Text]  
• Kinderlerer, A. R., Pombo Gregoire, I., Hamdulay, S. S., Ali, F., Steinberg, R., Silva, G., Ali, N., Wang, B., Haskard, D. O., Soares, M. P., Mason, J. C. (2009). Heme oxygenase-1 expression enhances vascular endothelial resistance to complement-mediated injury through induction of decay-accelerating factor: a role for increased bilirubin and ferritin. Blood 113: 1598-1607 [Abstract] [Full Text]  
• Engel, S. M., Janevic, T. M., Stein, C. R., Savitz, D. A. (2009). Maternal Smoking, Preeclampsia, and Infant Health Outcomes in New York City, 1995-2003. Am J Epidemiol 169: 33-40 [Abstract] [Full Text]  
• Burger, D., Xiang, F., Hammoud, L., Lu, X., Feng, Q. (2009). Role of heme oxygenase-1 in the cardioprotective effects of erythropoietin during myocardial ischemia and reperfusion. Am. J. Physiol. Heart Circ. Physiol. 296: H84-H93 [Abstract] [Full Text]  
• Cao, Y.-A., Wagers, A. J., Karsunky, H., Zhao, H., Reeves, R., Wong, R. J., Stevenson, D. K., Weissman, I. L., Contag, C. H. (2008). Heme oxygenase-1 deficiency leads to disrupted response to acute stress in stem cells and progenitors. Blood 112: 4494-4502 [Abstract] [Full Text]  
• Idriss, N. K., Blann, A. D., Lip, G. Y.H. (2008). Hemoxygenase-1 in Cardiovascular Disease. J Am Coll Cardiol 52: 971-978 [Abstract] [Full Text]  
• Patil, K., Bellner, L., Cullaro, G., Gotlinger, K. H., Dunn, M. W., Schwartzman, M. L. (2008). Heme Oxygenase-1 Induction Attenuates Corneal Inflammation and Accelerates Wound Healing after Epithelial Injury. IOVS 49: 3379-3386 [Abstract] [Full Text]  
• Kim, H. S., Loughran, P. A., Rao, J., Billiar, T. R., Zuckerbraun, B. S. (2008). Carbon monoxide activates NF-{kappa}B via ROS generation and Akt pathways to protect against cell death of hepatocytes. Am. J. Physiol. Gastrointest. Liver Physiol. 295: G146-G152 [Abstract] [Full Text]  
• Kivela, A. M., Kansanen, E., Jyrkkanen, H.-K., Nurmi, T., Yla-Herttuala, S., Levonen, A.-L. (2008). Enterolactone Induces Heme Oxygenase-1 Expression through Nuclear Factor-E2-Related Factor 2 Activation in Endothelial Cells. J. Nutr. 138: 1263-1268 [Abstract] [Full Text]  
• Rushworth, S. A., MacEwan, D. J. (2008). HO-1 underlies resistance of AML cells to TNF-induced apoptosis. Blood 111: 3793-3801 [Abstract] [Full Text]  
• Brennan, A. J, Sharp, J. A, Khalil, E., Digby, M. R, Mailer, S. L, Lefevre, C. M, Nicholas, K. R (2008). A population of mammary epithelial cells do not require hormones or growth factors to survive. J Endocrinol 196: 483-496 [Abstract] [Full Text]  
• Wang, L., Lee, J.-Y. S., Kwak, J. H., He, Y., Kim, S. I., Choi, M. E. (2008). Protective effects of low-dose carbon monoxide against renal fibrosis induced by unilateral ureteral obstruction. Am. J. Physiol. Renal Physiol. 294: F508-F517 [Abstract] [Full Text]  
• Angeloni, C., Leoncini, E., Malaguti, M., Angelini, S., Hrelia, P., Hrelia, S. (2008). Role of quercetin in modulating rat cardiomyocyte gene expression profile. Am. J. Physiol. Heart Circ. Physiol. 294: H1233-H1243 [Abstract] [Full Text]  
• Courtney, A. E., McNamee, P. T., Heggarty, S., Middleton, D., Maxwell, A. P. (2008). Association of functional haem oxygenase-1 gene promoter polymorphism with polycystic kidney disease and IgA nephropathy. Nephrol Dial Transplant 23: 608-611 [Abstract] [Full Text]  
• Dulak, J., Deshane, J., Jozkowicz, A., Agarwal, A. (2008). Heme Oxygenase-1 and Carbon Monoxide in Vascular Pathobiology: Focus on Angiogenesis. Circulation 117: 231-241 [Abstract] [Full Text]  
• Anderson, G. P. (2007). The COPD CO-factor. Eur Respir J 30: 1032-1034 [Full Text]  
• Sun, M.-H., Pang, J.-H. S., Chen, S.-L., Kuo, P.-C., Chen, K.-J., Kao, L.-Y., Wu, J.-Y., Lin, K.-K., Tsao, Y.-P. (2007). Photoreceptor Protection against Light Damage by AAV-Mediated Overexpression of Heme Oxygenase-1. IOVS 48: 5699-5707 [Abstract] [Full Text]  
• Kinobe, R. T., Ji, Y., Vlahakis, J. Z., Motterlini, R., Brien, J. F., Szarek, W. A., Nakatsu, K. (2007). Effectiveness of Novel Imidazole-Dioxolane Heme Oxygenase Inhibitors in Renal Proximal Tubule Epithelial Cells. J. Pharmacol. Exp. Ther. 323: 763-770 [Abstract] [Full Text]  
• Seldon, M. P., Silva, G., Pejanovic, N., Larsen, R., Gregoire, I. P., Filipe, J., Anrather, J., Soares, M. P. (2007). Heme Oxygenase-1 Inhibits the Expression of Adhesion Molecules Associated with Endothelial Cell Activation via Inhibition of NF-{kappa}B RelA Phosphorylation at Serine 276. J. Immunol. 179: 7840-7851 [Abstract] [Full Text]  
• Kobayashi, A., Ishikawa, K., Matsumoto, H., Kimura, S., Kamiyama, Y., Maruyama, Y. (2007). Synergetic Antioxidant and Vasodilatory Action of Carbon Monoxide in Angiotensin II Induced Cardiac Hypertrophy. Hypertension 50: 1040-1048 [Abstract] [Full Text]  
• Martin, M. J., Tanos, T., Garcia, A. B., Martin, D., Gutkind, J. S., Coso, O. A., Marinissen, M. J. (2007). The G{alpha}12/13 Family of Heterotrimeric G Proteins and the Small GTPase RhoA Link the Kaposi Sarcoma-associated Herpes Virus G Protein-coupled Receptor to Heme Oxygenase-1 Expression and Tumorigenesis. J. Biol. Chem. 282: 34510-34524 [Abstract] [Full Text]  
• Yang, X., Lee, P. J., Long, L., Trembath, R. C., Morrell, N. W. (2007). BMP4 Induces HO-1 via a Smad-Independent, p38MAPK-Dependent Pathway in Pulmonary Artery Myocytes. Am. J. Respir. Cell Mol. Bio. 37: 598-605 [Abstract] [Full Text]  
• Kim, K. M., Pae, H.-O., Zheng, M., Park, R., Kim, Y.-M., Chung, H.-T. (2007). Carbon Monoxide Induces Heme Oxygenase-1 via Activation of Protein Kinase R Like Endoplasmic Reticulum Kinase and Inhibits Endothelial Cell Apoptosis Triggered by Endoplasmic Reticulum Stress. Circ. Res. 101: 919-927 [Abstract] [Full Text]  
• True, A. L., Olive, M., Boehm, M., San, H., Westrick, R. J., Raghavachari, N., Xu, X., Lynn, E. G., Sack, M. N., Munson, P. J., Gladwin, M. T., Nabel, E. G. (2007). Heme Oxygenase-1 Deficiency Accelerates Formation of Arterial Thrombosis Through Oxidative Damage to the Endothelium, Which Is Rescued by Inhaled Carbon Monoxide. Circ. Res. 101: 893-901 [Abstract] [Full Text]  
• Datta, D., Dormond, O., Basu, A., Briscoe, D. M., Pal, S. (2007). Heme oxygenase-1 modulates the expression of the anti-angiogenic chemokine CXCL-10 in renal tubular epithelial cells. Am. J. Physiol. Renal Physiol. 293: F1222-F1230 [Abstract] [Full Text]  
• Li, M.-H., Jang, J.-H., Na, H.-K., Cha, Y.-N., Surh, Y.-J. (2007). Carbon Monoxide Produced by Heme Oxygenase-1 in Response to Nitrosative Stress Induces Expression of Glutamate-Cysteine Ligase in PC12 Cells via Activation of Phosphatidylinositol 3-Kinase and Nrf2 Signaling. J. Biol. Chem. 282: 28577-28586 [Abstract] [Full Text]  
• Haschemi, A., Wagner, O., Marculescu, R., Wegiel, B., Robson, S. C., Gagliani, N., Gallo, D., Chen, J.-F., Bach, F. H., Otterbein, L. E. (2007). Cross-Regulation of Carbon Monoxide and the Adenosine A2a Receptor in Macrophages. J. Immunol. 178: 5921-5929 [Abstract] [Full Text]  
• Sheftel, A. D., Kim, S. F., Ponka, P. (2007). Non-heme Induction of Heme Oxygenase-1 Does Not Alter Cellular Iron Metabolism. J. Biol. Chem. 282: 10480-10486 [Abstract] [Full Text]  
• Slebos, D.-J., Ryter, S. W., van der Toorn, M., Liu, F., Guo, F., Baty, C. J., Karlsson, J. M., Watkins, S. C., Kim, H. P., Wang, X., Lee, J. S., Postma, D. S., Kauffman, H. F., Choi, A. M. K. (2007). Mitochondrial Localization and Function of Heme Oxygenase-1 in Cigarette Smoke-Induced Cell Death. Am. J. Respir. Cell Mol. Bio. 36: 409-417 [Abstract] [Full Text]  
• Zuckerbraun, B. S., Chin, B. Y., Bilban, M., de Costa d'Avila, J., Rao, J., Billiar, T. R., Otterbein, L. E. (2007). Carbon monoxide signals via inhibition of cytochrome c oxidase and generation of mitochondrial reactive oxygen species. FASEB J. 21: 1099-1106 [Abstract] [Full Text]  
• Ryter, S. W., Morse, D., Choi, A. M. K. (2007). Carbon Monoxide and Bilirubin: Potential Therapies for Pulmonary/Vascular Injury and Disease. Am. J. Respir. Cell Mol. Bio. 36: 175-182 [Abstract] [Full Text]  
• Wang, X., Wang, Y., Kim, H. P., Nakahira, K., Ryter, S. W., Choi, A. M. K. (2007). Carbon Monoxide Protects against Hyperoxia-induced Endothelial Cell Apoptosis by Inhibiting Reactive Oxygen Species Formation. J. Biol. Chem. 282: 1718-1726 [Abstract] [Full Text]  
• Olszanecki, R., Rezzani, R., Omura, S., Stec, D. E., Rodella, L., Botros, F. T., Goodman, A. I., Drummond, G., Abraham, N. G. (2007). Genetic suppression of HO-1 exacerbates renal damage: reversed by an increase in the antiapoptotic signaling pathway. Am. J. Physiol. Renal Physiol. 292: F148-F157 [Abstract] [Full Text]  
• Was, H., Cichon, T., Smolarczyk, R., Rudnicka, D., Stopa, M., Chevalier, C., Leger, J. J., Lackowska, B., Grochot, A., Bojkowska, K., Ratajska, A., Kieda, C., Szala, S., Dulak, J., Jozkowicz, A. (2006). Overexpression of Heme Oxygenase-1 in Murine Melanoma: Increased Proliferation and Viability of Tumor Cells, Decreased Survival of Mice. Am. J. Pathol. 169: 2181-2198 [Abstract] [Full Text]  
• Stocker, R., Perrella, M. A. (2006). Heme Oxygenase-1: A Novel Drug Target for Atherosclerotic Diseases?. Circulation 114: 2178-2189 [Full Text]  
• Aburaya, M., Tanaka, K.-I., Hoshino, T., Tsutsumi, S., Suzuki, K., Makise, M., Akagi, R., Mizushima, T. (2006). Heme Oxygenase-1 Protects Gastric Mucosal Cells against Non-steroidal Anti-inflammatory Drugs. J. Biol. Chem. 281: 33422-33432 [Abstract] [Full Text]  
• Basuroy, S., Bhattacharya, S., Tcheranova, D., Qu, Y., Regan, R. F., Leffler, C. W., Parfenova, H. (2006). HO-2 provides endogenous protection against oxidative stress and apoptosis caused by TNF-{alpha} in cerebral vascular endothelial cells. Am. J. Physiol. Cell Physiol. 291: C897-C908 [Abstract] [Full Text]  
• Bainbridge, S. A., Belkacemi, L., Dickinson, M., Graham, C. H., Smith, G. N. (2006). Carbon Monoxide Inhibits Hypoxia/Reoxygenation-Induced Apoptosis and Secondary Necrosis in Syncytiotrophoblast. Am. J. Pathol. 169: 774-783 [Abstract] [Full Text]  
• Pryor, W. A., Houk, K. N., Foote, C. S., Fukuto, J. M., Ignarro, L. J., Squadrito, G. L., Davies, K. J. A. (2006). Free radical biology and medicine: it's a gas, man!. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291: R491-R511 [Abstract] [Full Text]  
• Silva, G., Cunha, A., Gregoire, I. P., Seldon, M. P., Soares, M. P. (2006). The Antiapoptotic Effect of Heme Oxygenase-1 in Endothelial Cells Involves the Degradation of p38{alpha} MAPK Isoform. J. Immunol. 177: 1894-1903 [Abstract] [Full Text]  
• D'Amico, G., Lam, F., Hagen, T., Moncada, S. (2006). Inhibition of cellular respiration by endogenously produced carbon monoxide. J. Cell Sci. 119: 2291-2298 [Abstract] [Full Text]  
• Settivari, R. S., Bhusari, S., Evans, T., Eichen, P. A., Hearne, L. B., Antoniou, E., Spiers, D. E. (2006). Genomic analysis of the impact of fescue toxicosis on hepatic function. J ANIM SCI 84: 1279-1294 [Abstract] [Full Text]  
• Kim, H. J., Tsoy, I., Park, M. K., Lee, Y. S., Lee, J. H., Seo, H. G., Chang, K. C. (2006). Iron Released by Sodium Nitroprusside Contributes to Heme Oxygenase-1 Induction via the cAMP-Protein Kinase A-Mitogen-Activated Protein Kinase Pathway in RAW 264.7 Cells. Mol. Pharmacol. 69: 1633-1640 [Abstract] [Full Text]  
• Kim, J. H., Yang, J. I., Jung, M. H., Hwa, J. S., Kang, K.-R., Park, D. J., Roh, G. S., Cho, G. J., Choi, W. S., Chang, S.-H. (2006). Heme Oxygenase-1 Protects Rat Kidney from Ureteral Obstruction via an Antiapoptotic Pathway. J. Am. Soc. Nephrol. 17: 1373-1381 [Abstract] [Full Text]  
• Parfenova, H., Basuroy, S., Bhattacharya, S., Tcheranova, D., Qu, Y., Regan, R. F., Leffler, C. W. (2006). Glutamate induces oxidative stress and apoptosis in cerebral vascular endothelial cells: contributions of HO-1 and HO-2 to cytoprotection. Am. J. Physiol. Cell Physiol. 290: C1399-C1410 [Abstract] [Full Text]  
• Marinissen, M. J., Tanos, T., Bolos, M., de Sagarra, M. R., Coso, O. A., Cuadrado, A. (2006). Inhibition of Heme Oxygenase-1 Interferes with the Transforming Activity of the Kaposi Sarcoma Herpesvirusencoded G Protein-coupled Receptor. J. Biol. Chem. 281: 11332-11346 [Abstract] [Full Text]  
• Ryter, S. W., Alam, J., Choi, A. M. K. (2006). Heme Oxygenase-1/Carbon Monoxide: From Basic Science to Therapeutic Applications. Physiol. Rev. 86: 583-650 [Abstract] [Full Text]  
• Leffler, C. W., Parfenova, H., Jaggar, J. H., Wang, R. (2006). Carbon monoxide and hydrogen sulfide: gaseous messengers in cerebrovascular circulation. J. Appl. Physiol. 100: 1065-1076 [Abstract] [Full Text]  
• Andreadi, C. K., Howells, L. M., Atherfold, P. A., Manson, M. M. (2006). Involvement of Nrf2, p38, B-Raf, and Nuclear Factor-{kappa}B, but Not Phosphatidylinositol 3-Kinase, in Induction of Hemeoxygenase-1 by Dietary Polyphenols. Mol. Pharmacol. 69: 1033-1040 [Abstract] [Full Text]  
• Neto, J. S., Nakao, A., Toyokawa, H., Nalesnik, M. A., Romanosky, A. J., Kimizuka, K., Kaizu, T., Hashimoto, N., Azhipa, O., Stolz, D. B., Choi, A. M. K., Murase, N. (2006). Low-dose carbon monoxide inhalation prevents development of chronic allograft nephropathy. Am. J. Physiol. Renal Physiol. 290: F324-F334 [Abstract] [Full Text]  
• Hill, M., Pereira, V., Chauveau, C., Zagani, R., Remy, S., Tesson, L., Mazal, D., Ubillos, L., Brion, R., Ashgar, K., Mashreghi, M. F., Kotsch, K., Moffett, J., Doebis, C., Seifert, M., Boczkowski, J., Osinaga, E., Anegon, I. (2005). Heme oxygenase-1 inhibits rat and human breast cancer cell proliferation: mutual cross inhibition with indoleamine 2,3-dioxygenase. FASEB J. 19: 1957-1968 [Abstract] [Full Text]  
• Wu, L., Wang, R. (2005). Carbon Monoxide: Endogenous Production, Physiological Functions, and Pharmacological Applications. Pharmacol. Rev. 57: 585-630 [Abstract] [Full Text]  
• Sarady-Andrews, J. K., Liu, F., Gallo, D., Nakao, A., Overhaus, M., Ollinger, R., Choi, A. M., Otterbein, L. E. (2005). Biliverdin administration protects against endotoxin-induced acute lung injury in rats. Am. J. Physiol. Lung Cell. Mol. Physiol. 289: L1131-L1137 [Abstract] [Full Text]  
• Sollwedel, A., Bertoja, A. Z., Zenclussen, M. L., Gerlof, K., Lisewski, U., Wafula, P., Sawitzki, B., Woiciechowsky, C., Volk, H.-D., Zenclussen, A. C. (2005). Protection from Abortion by Heme Oxygenase-1 Up-Regulation Is Associated with Increased Levels of Bag-1 and Neuropilin-1 at the Fetal-Maternal Interface. J. Immunol. 175: 4875-4885 [Abstract] [Full Text]  
• Jin, Y., Choi, A. M. K. (2005). Cytoprotection of Heme Oxygenase-1/Carbon Monoxide in Lung Injury. Proc Am Thorac Soc 2: 232-235 [Abstract] [Full Text]  
• Morse, D., Choi, A. M. K. (2005). Heme Oxygenase-1: From Bench to Bedside. Am. J. Respir. Crit. Care Med. 172: 660-670 [Abstract] [Full Text]  
• Zuckerbraun, B. S., Otterbein, L. E., Boyle, P., Jaffe, R., Upperman, J., Zamora, R., Ford, H. R. (2005). Carbon monoxide protects against the development of experimental necrotizing enterocolitis. Am. J. Physiol. Gastrointest. Liver Physiol. 289: G607-G613 [Abstract] [Full Text]  
• Laxmanan, S., Datta, D., Geehan, C., Briscoe, D. M., Pal, S. (2005). CD40: A Mediator of Pro- and Anti-Inflammatory Signals in Renal Tubular Epithelial Cells. J. Am. Soc. Nephrol. 16: 2714-2723 [Abstract] [Full Text]  
• Kim, H. P., Wang, X., Zhang, J., Suh, G. Y., Benjamin, I. J., Ryter, S. W., Choi, A. M. K. (2005). Heat Shock Protein-70 Mediates the Cytoprotective Effect of Carbon Monoxide: Involvement of p38{beta} MAPK and Heat Shock Factor-1. J. Immunol. 175: 2622-2629 [Abstract] [Full Text]  
• Kim, H. P., Wang, X., Nakao, A., Kim, S. I., Murase, N., Choi, M. E., Ryter, S. W., Choi, A. M. K. (2005). Caveolin-1 expression by means of p38{beta} mitogen-activated protein kinase mediates the antiproliferative effect of carbon monoxide. Proc. Natl. Acad. Sci. USA 102: 11319-11324 [Abstract] [Full Text]  
• Minamoto, K., Harada, H., Lama, V. N., Fedarau, M. A., Pinsky, D. J. (2005). Reciprocal regulation of airway rejection by the inducible gas-forming enzymes heme oxygenase and nitric oxide synthase. JEM 202: 283-294 [Abstract] [Full Text]  
• Li, W., Tanaka, K., Morioka, K., Uesaka, T., Yamada, N., Takamori, A., Handa, M., Tanabe, S., Ihaya, A. (2005). Thymidine Phosphorylase Gene Transfer Inhibits Vascular Smooth Muscle Cell Proliferation by Upregulating Heme Oxygenase-1 and p27KIP1. Arterioscler. Thromb. Vasc. Bio. 25: 1370-1375 [Abstract] [Full Text]  
• Choi, A. M.K., Dolinay, T. (2005). . Am. J. Respir. Crit. Care Med. 171: 1318-1319 [Full Text]  
• Parfenova, H., Carratu, P., Tcheranova, D., Fedinec, A., Pourcyrous, M., Leffler, C. W. (2005). Epileptic seizures cause extended postictal cerebral vascular dysfunction that is prevented by HO-1 overexpression. Am. J. Physiol. Heart Circ. Physiol. 288: H2843-H2850 [Abstract] [Full Text]  
• Wang, H., Lee, S. S., Gao, W., Czismadia, E., McDaid, J., Ollinger, R., Soares, M. P., Yamashita, K., Bach, F. H. (2005). Donor Treatment With Carbon Monoxide Can Yield Islet Allograft Survival and Tolerance. Diabetes 54: 1400-1406 [Abstract] [Full Text]  
• Liu, X.-m., Peyton, K. J., Ensenat, D., Wang, H., Schafer, A. I., Alam, J., Durante, W. (2005). Endoplasmic Reticulum Stress Stimulates Heme Oxygenase-1 Gene Expression in Vascular Smooth Muscle: ROLE IN CELL SURVIVAL. J. Biol. Chem. 280: 872-877 [Abstract] [Full Text]  
• Lam, C. F., Croatt, A. J., Richardson, D. M., Nath, K. A., Katusic, Z. S. (2005). Heart failure increases protein expression and enzymatic activity of heme oxygenase-1 in the lung. Cardiovasc Res 65: 203-210 [Abstract] [Full Text]  
• Arai-Gaun, S., Katai, N., Kikuchi, T., Kurokawa, T., Ohta, K., Yoshimura, N. (2004). Heme Oxygenase-1 Induced in Muller Cells Plays a Protective Role in Retinal Ischemia-Reperfusion Injury in Rats. IOVS 45: 4226-4232 [Abstract] [Full Text]  
• Neto, J. S., Nakao, A., Kimizuka, K., Romanosky, A. J., Stolz, D. B., Uchiyama, T., Nalesnik, M. A., Otterbein, L. E., Murase, N. (2004). Protection of transplant-induced renal ischemia-reperfusion injury with carbon monoxide. Am. J. Physiol. Renal Physiol. 287: F979-F989 [Abstract] [Full Text]  
• Song, R., Zhou, Z., Kim, P. K. M., Shapiro, R. A., Liu, F., Ferran, C., Choi, A. M. K., Otterbein, L. E. (2004). Carbon Monoxide Promotes Fas/CD95-induced Apoptosis in Jurkat Cells. J. Biol. Chem. 279: 44327-44334 [Abstract] [Full Text]  
• Stocker, R., Keaney, J. F. Jr. (2004). Role of Oxidative Modifications in Atherosclerosis. Physiol. Rev. 84: 1381-1478 [Abstract] [Full Text]  
• Fujimoto, H., Ohno, M., Ayabe, S., Kobayashi, H., Ishizaka, N., Kimura, H., Yoshida, K.-i., Nagai, R. (2004). Carbon Monoxide Protects Against Cardiac Ischemia--Reperfusion Injury In Vivo via MAPK and Akt--eNOS Pathways. Arterioscler. Thromb. Vasc. Bio. 24: 1848-1853 [Abstract] [Full Text]  
• Deng, Y.-M., Wu, B. J., Witting, P. K., Stocker, R. (2004). Probucol Protects Against Smooth Muscle Cell Proliferation by Upregulating Heme Oxygenase-1. Circulation 110: 1855-1860 [Abstract] [Full Text]  
• Zhou, H., Lu, F., Latham, C., Zander, D. S., Visner, G. A. (2004). Heme Oxygenase-1 Expression in Human Lungs with Cystic Fibrosis and Cytoprotective Effects against Pseudomonas Aeruginosa In Vitro. Am. J. Respir. Crit. Care Med. 170: 633-640 [Abstract] [Full Text]  
• Roberts, G. P., Youn, H., Kerby, R. L. (2004). CO-Sensing Mechanisms. Microbiol. Mol. Biol. Rev. 68: 453-473 [Abstract] [Full Text]  
• Tongers, J., Fiedler, B., Konig, D., Kempf, T., Klein, G., Heineke, J., Kraft, T., Gambaryan, S., Lohmann, S. M, Drexler, H., Wollert, K. C (2004). Heme oxygenase-1 inhibition of MAP kinases, calcineurin/NFAT signaling, and hypertrophy in cardiac myocytes. Cardiovasc Res 63: 545-552 [Abstract] [Full Text]  
• Salahudeen, A. K. (2004). Cold ischemic injury of transplanted kidneys: new insights from experimental studies. Am. J. Physiol. Renal Physiol. 287: F181-F187 [Abstract] [Full Text]  
• KIM, H. P., WANG, X., GALBIATI, F., RYTER, S. W., CHOI, A. M. K. (2004). Caveolae compartmentalization of heme oxygenase-1 in endothelial cells. FASEB J. 18: 1080-1089 [Abstract] [Full Text]  
• Nystul, T. G., Roth, M. B. (2004). Carbon monoxide-induced suspended animation protects against hypoxic damage in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 101: 9133-9136 [Abstract] [Full Text]  
• Mayerhofer, M., Florian, S., Krauth, M.-T., Aichberger, K. J., Bilban, M., Marculescu, R., Printz, D., Fritsch, G., Wagner, O., Selzer, E., Sperr, W. R., Valent, P., Sillaber, C. (2004). Identification of Heme Oxygenase-1 As a Novel BCR/ABL-Dependent Survival Factor in Chronic Myeloid Leukemia. Cancer Res. 64: 3148-3154 [Abstract] [Full Text]  
• Guo, Y., Stein, A. B., Wu, W.-J., Tan, W., Zhu, X., Li, Q.-H., Dawn, B., Motterlini, R., Bolli, R. (2004). Administration of a CO-releasing molecule at the time of reperfusion reduces infarct size in vivo. Am. J. Physiol. Heart Circ. Physiol. 286: H1649-H1653 [Abstract] [Full Text]  
• Ryter, S. W., Morse, D., Choi, A. M. K. (2004). Carbon Monoxide: To Boldly Go Where NO Has Gone Before. Sci Signal 2004: re6-re6 [Abstract] [Full Text]  
• Soares, M. P., Seldon, M. P., Gregoire, I. P., Vassilevskaia, T., Berberat, P. O., Yu, J., Tsui, T.-Y., Bach, F. H. (2004). Heme Oxygenase-1 Modulates the Expression of Adhesion Molecules Associated with Endothelial Cell Activation. J. Immunol. 172: 3553-3563 [Abstract] [Full Text]  
• Sikorski, E. M., Hock, T., Hill-Kapturczak, N., Agarwal, A. (2004). The story so far: molecular regulation of the heme oxygenase-1 gene in renal injury. Am. J. Physiol. Renal Physiol. 286: F425-F441 [Abstract] [Full Text]  
• Wasserman, S. M, Topper, J. N (2004). Adaptation of the endothelium to fluid flow: in vitro analyses of gene expression and in vivo implications. Vasc Med 9: 35-45 [Abstract]  
• Song, R., Mahidhara, R. S., Zhou, Z., Hoffman, R. A., Seol, D.-W., Flavell, R. A., Billiar, T. R., Otterbein, L. E., Choi, A. M. K. (2004). Carbon Monoxide Inhibits T Lymphocyte Proliferation via Caspase-Dependent Pathway. J. Immunol. 172: 1220-1226 [Abstract] [Full Text]  
• Zuckerbraun, B. S., Billiar, T. R., Otterbein, S. L., Kim, P. K.M., Liu, F., Choi, A. M.K., Bach, F. H., Otterbein, L. E. (2003). Carbon Monoxide Protects against Liver Failure through Nitric Oxide-induced Heme Oxygenase 1. JEM 198: 1707-1716 [Abstract] [Full Text]  
• Lemos, F. B.C., Ijzermans, J. N.M., Zondervan, P. E., Peeters, A. M.A., van den Engel, S., Mol, W. M., Weimar, W., Baan, C. C. (2003). Differential Expression of Heme Oxygenase-1 and Vascular Endothelial Growth Factor in Cadaveric and Living Donor Kidneys after Ischemia-Reperfusion. J. Am. Soc. Nephrol. 14: 3278-3287 [Abstract] [Full Text]  
• Otterbein, L. E., Otterbein, S. L., Ifedigbo, E., Liu, F., Morse, D. E., Fearns, C., Ulevitch, R. J., Knickelbein, R., Flavell, R. A., Choi, A. M. (2003). MKK3 Mitogen-Activated Protein Kinase Pathway Mediates Carbon Monoxide-Induced Protection Against Oxidant-Induced Lung Injury. Am. J. Pathol. 163: 2555-2563 [Abstract] [Full Text]  
• Toth, B., Yokoyama, Y., Kuebler, J. F., Schwacha, M. G., Rue, L. W. III, Bland, K. I., Chaudry, I. H. (2003). Sex Differences in Hepatic Heme Oxygenase Expression and Activity Following Trauma and Hemorrhagic Shock. Arch Surg 138: 1375-1382 [Abstract] [Full Text]  
• Nakao, A., Kimizuka, K., Stolz, D. B., Neto, J. S., Kaizu, T., Choi, A. M. K., Uchiyama, T., Zuckerbraun, B. S., Nalesnik, M. A., Otterbein, L. E., Murase, N. (2003). Carbon Monoxide Inhalation Protects Rat Intestinal Grafts from Ischemia/Reperfusion Injury. Am. J. Pathol. 163: 1587-1598 [Abstract] [Full Text]  
• Morse, D., Pischke, S. E., Zhou, Z., Davis, R. J., Flavell, R. A., Loop, T., Otterbein, S. L., Otterbein, L. E., Choi, A. M. K. (2003). Suppression of Inflammatory Cytokine Production by Carbon Monoxide Involves the JNK Pathway and AP-1. J. Biol. Chem. 278: 36993-36998 [Abstract] [Full Text]  

Home | Help | Feedback | Subscriptions | Archive | Search

TABLE OF CONTENTS