Cardioprotective and Antiapoptotic Effects of Heme Oxygenase-1 in the Failing Heart
Open accessAbstract
Background— Heme oxygenase-1 (HO-1) is an inducible stress-response protein that imparts antioxidant and antiapoptotic effects. However, its pathophysiological role in cardiac remodeling and chronic heart failure (HF) is unknown. We hypothesized that induction of HO-1 in HF alleviates pathological remodeling. Methods and Results— Adult male nontransgenic and myocyte-restricted HO-1 transgenic mice underwent either sham operation or coronary ligation to induce HF. Four weeks after ligation, nontransgenic HF mice exhibited postinfarction left ventricular (LV) remodeling and dysfunction, hypertrophy, fibrosis, oxidative stress, apoptosis, and reduced capillary density, associated with a 2-fold increase in HO-1 expression in noninfarcted myocardium. Compared with nontransgenic mice, HO-1 transgenic HF mice exhibited significantly ( P <0.05) improved postinfarction survival (94% versus 57%) and less LV dilatation (end-diastolic volume, 46±8 versus 85±32 μL), mechanical dysfunction (ejection fraction, 65±9% versus 49±16%), hypertrophy (LV/tibia length 4.4±0.4 versus 5.2±0.6 mg/mm), interstitial fibrosis (11.2±3.1% versus 18.5±3.5%), and oxidative stress (3-fold reduction in tissue malondialdehyde). Moreover, myocyte-specific HO-1 overexpression in HF promoted tissue neovascularization and ameliorated myocardial p53 expression (2-fold reduction) and apoptosis. In isolated mitochondria, mitochondrial permeability transition was inhibited by HO-1 in a carbon monoxide (CO)–dependent manner and was recapitulated by the CO donor tricarbonylchloro(glycinato)ruthenium(II) (CORM-3). HO-1–derived CO also prevented H 2 O 2 -induced cardiomyocyte apoptosis and cell death. Finally, in vivo treatment with CORM-3 alleviated postinfarction LV remodeling, p53 expression, and apoptosis. Conclusions— HO-1 induction in the failing heart is an important cardioprotective adaptation that opposes pathological LV remodeling, and this effect is mediated, at least in part, by CO-dependent inhibition of mitochondrial permeability transition and apoptosis. Augmentation of HO-1 or its product, CO, may represent a novel therapeutic strategy for ameliorating HF.
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Overexpression of cardiomyocyte-targeted HO-1 improves survival after myocardial infarction by reducing myocyte-specific apoptosis and postinfarction left ventricular remodeling, in part, by preserving mitochondrial function.
“In vivo, overexpression of cardiomyocyte-targeted HO-1 improved survival after myocardial infarction by reducing myocyte-specific apoptosis and postinfarction left ventricular remodeling, in part, by preserving mitochondrial function (440).”
From Redox regulation of mitochondrial function (2012) · cites this paper as [440]
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Cites
Tumor suppressor p53 is a regulator of bcl-2 and bax gene expression in vitro and in vivo.
Miyashita, T., Krajewski, S., Krajewska, M., Wang, H., Lin, H., Liebermann, D. A., Hoffman‐Liebermann, B., & Reed, J. C. (1994) · PubMed · Cited by 2,143 · see citing works
Reduced stress defense in heme oxygenase 1-deficient cells
Poss, K. D., & Tonegawa, S. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.20.10925 · Cited by 1,293 · see citing works
Measurement of Mitochondrial Membrane Potential Using Fluorescent Rhodamine Derivatives
Scaduto, R. C., & Grotyohann, L. W. (1999) · Biophysical Journal · doi:10.1016/s0006-3495(99)77214-0 · Cited by 1,232 · see citing works
Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice
Lee, T.-S., & Chau, L.-Y. (2002) · Nature Medicine · doi:10.1038/nm0302-240 · Cited by 1,019 · see citing works
Heme oxygenase 1 is required for mammalian iron reutilization
Poss, K. D., & Tonegawa, S. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.20.10919 · Cited by 1,016 · see citing works
Carbon Monoxide Generated by Heme Oxygenase 1 Suppresses Endothelial Cell Apoptosis
Brouard, S., Otterbein, L. E., Anrather, J., Tobiasch, E., Bach, F. H., Choi, A. M. K., & Soares, M. P. (2000) · The Journal of Experimental Medicine · doi:10.1084/jem.192.7.1015 · Cited by 984 · see citing works
Heme oxygenase: colors of defense against cellular stress
Otterbein, L. E., & Choi, A. M. K. (2000) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.2000.279.6.l1029 · Cited by 870 · see citing works
A mechanistic role for cardiac myocyte apoptosis in heart failure
Wencker, D., Chandra, M., Nguyen, K., Miao, W., Garantziotis, S., Factor, S. M., Shirani, J., Armstrong, R. C., & Kitsis, R. N. (2003) · Journal of Clinical Investigation · doi:10.1172/jci17664 · Cited by 765 · see citing works
Cardioprotective Actions by a Water-Soluble Carbon Monoxide–Releasing Molecule
Clark, J., NAUGHTON, P. J., Shurey, S., Green, C. J., Johnson, T. R., Mann, B. E., Foresti, R., & Motterlini, R. (2003) · Circulation Research · doi:10.1161/01.res.0000084381.86567.08 · Cited by 676 · see citing works
Heme oxygenase-1 protects against vascular constriction and proliferation
Duckers, H. J., Boehm, M., True, A. L., Yet, S., San, H., Park, J. L., Webb, R. C., Lee, M.-E., Nabel, G. J., & Nabel, E. G. (2001) · Nature Medicine · doi:10.1038/89068 · Cited by 524 · see citing works
Sato, K., Balla, J., Otterbein, L. E., Smith, R. N., Brouard, S., Lin, Y., Csizmadia, E., Sévigny, J., Robson, S. C., Vercellotti, G. M., et al. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.6.4185 · Cited by 462 · see citing works
Yet, S., Tian, R., Layne, M. D., Wang, Z. Y., Maemura, K., Solovyeva, M., Ith, B., Melo, L. G., Zhang, L., Ingwall, J. S., et al. (2001) · Circulation Research · doi:10.1161/hh1401.093314 · Cited by 420 · see citing works
Myocyte apoptosis in heart failure
VANEMPEL, V., Bertrand, A., Hofstra, L., Crijns, H. J. G. M., Doevendans, P. A., & Windt, L. J. D. (2005) · Cardiovascular Research · doi:10.1016/j.cardiores.2005.04.012 · Cited by 374 · see citing works
Heme oxygenase and the cardiovascular–renal system
Abraham, N. G., & Kappas, A. (2005) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2005.03.010 · Cited by 356 · see citing works
Morita, T., & Kourembanas, S. (1995) · Journal of Clinical Investigation · doi:10.1172/jci118334 · Cited by 354 · see citing works
Death begets failure in the heart
Foo, R., Mani, K. M., & Kitsis, R. N. (2005) · Journal of Clinical Investigation · doi:10.1172/jci24569 · Cited by 307 · see citing works
Melo, L. G., Agrawal, R. S., Zhang, L., Rezvani, M., Mangi, A. A., Ehsan, A., Griese, D. P., Dell’Acqua, G., Mann, M. J., Oyama, J., et al. (2002) · Circulation · doi:10.1161/hc0502.103363 · Cited by 303 · see citing works
The mitochondrial permeability transition pore and ischemia-reperfusion injury
Baines, C. P. (2009) · Basic Research in Cardiology · doi:10.1007/s00395-009-0004-8 · Cited by 280 · see citing works
Divergent Tumor Necrosis Factor Receptor–Related Remodeling Responses in Heart Failure
Hamid, T., Gu, Y., Ortines, R. V., Bhattacharya, C., Wang, G., Xuan, Y., & Prabhu, S. D. (2009) · Circulation · doi:10.1161/circulationaha.108.802918 · Cited by 276 · see citing works
Self-citationInhibition of tumor angiogenesis by p53: a new role for the guardian of the genome
Teodoro, J. G., Evans, S. K., & Green, M. R. (2007) · Journal of Molecular Medicine · doi:10.1007/s00109-007-0221-2 · Cited by 262 · see citing works
Cell death during ischemia: relationship to mitochondrial depolarization and ROS generation
Levraut, J., Iwase, H., Shao, Z. H., Hoek, T. L. V., & Schumacker, P. T. (2003) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00708.2002 · Cited by 226 · see citing works
Christou, H. A., Morita, T., Hsieh, C.-M., Koike, H., Arkonac, B. M., Perrella, M. A., & Kourembanas, S. (2000) · Circulation Research · doi:10.1161/01.res.86.12.1224 · Cited by 204 · see citing works
Carbon monoxide inhibits apoptosis in vascular smooth muscle cells
Liu, X. (2002) · Cardiovascular Research · doi:10.1016/s0008-6363(02)00410-8 · Cited by 182 · see citing works
H mox-1 Constitutes an Adaptive Response to Effect Antioxidant Cardioprotection
Yoshida, T., Maulik, N., Ho, Y., Alam, J., & Das, D. K. (2001) · Circulation · doi:10.1161/01.cir.103.12.1695 · Cited by 144 · see citing works
Srisook, K., Han, S.-S., Choi, H.-S., Li, M., UEDA, H. M. D., Kim, C., & Cha, Y. (2005) · Biochemical Pharmacology · doi:10.1016/j.bcp.2005.10.042 · Cited by 134 · see citing works
Wang, G., Liem, D. A., Vondriska, T. M., Honda, H. M., Kôrge, P., Pantaleon, D. M., Qiao, X., Wang, Y., Weiss, J. N., & Ping, P. (2004) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00796.2004 · Cited by 130 · see citing works
Self-citationSRIVASTAVA, S., CHANDRASEKAR, B., GU, Y., LUO, J., Hamid, T., Hill, B. G., & Prabhu, S. D. (2007) · Cardiovascular Research · doi:10.1016/j.cardiores.2007.02.016 · Cited by 118 · see citing works
Self-citationSharov, V. G., Todor, A. V., Khanal, S., Imai, M., & Sabbah, H. N. (2006) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2006.09.013 · Cited by 112 · see citing works
Luo, J., Hill, B. G., Gu, Y., Cai, J., Srivastava, S., Bhatnagar, A., & Prabhu, S. D. (2007) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00284.2007 · Cited by 104 · see citing works
Self-citationJavadov, S. A., Huang, C., Kirshenbaum, L. A., & Karmazyn, M. (2004) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2004.10.007 · Cited by 80 · see citing works
Expression of Heme Oxygenase-1 in Response to Myocardial Infarction in Rats
Lakkisto, P., Palojoki, E., Bäcklund, T., Saraste, A., Tikkanen, I. T., Voipio‐Pulkki, L., & Pulkki, K. J. (2002) · Journal of Molecular and Cellular Cardiology · doi:10.1006/jmcc.2002.2094 · Cited by 75 · see citing works
Srivastava, S., Vladykovskaya, E. N., Barski, O. A., Spite, M. R., Kaiserová, K., Petrash, J. M., Chung, S. S. M., Hunt, G., Dawn, B., & Bhatnagar, A. (2009) · Circulation Research · doi:10.1161/circresaha.109.200568 · Cited by 71 · see citing works
Self-citationLiu, X., Simpson, J. A., Brunt, K. R., Ward, C. A., Hall, S. R. R., Kinobe, R. T., Barrette, V. F., Tse, M. Y., Pang, S. C.-N., Pachori, A. S., et al. (2007) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00741.2006 · Cited by 70 · see citing works
Li, Q., Guo, Y., Tan, W. H., Ou, Q., Wu, W., Sturza, D., Dawn, B., Hunt, G., Cui, C.-J., & Bolli, R. (2007) · Circulation · doi:10.1161/circulationaha.107.689810 · Cited by 57 · see citing works
Self-citationLi, M., Cha, Y., & Surh, Y. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.02.046 · Cited by 51 · see citing works
Raju, V. S., Imai, N., & Liang, C. (1999) · Journal of Molecular and Cellular Cardiology · doi:10.1006/jmcc.1999.0995 · Cited by 45 · see citing works
Grabellus, F., Schmid, Ç., Levkau, B., Breukelmann, D., Halloran, P. F., August, C., Takeda, N., Takeda, A., Wilhelm, M. J., Deng, M. C.-H. K., et al. (2002) · The Journal of Pathology · doi:10.1002/path.1106 · Cited by 35 · see citing works
A SAGE-based comparison between glomerular and aortic endothelial cells
Sengoelge, G., Luo, W., Fine, D. M., Perschl, A. M., Fierlbeck, W., Haririan, A., Sörensson, J., Rehman, T.-U., Hauser, P., Trevick, J. S., et al. (2005) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00076.2004 · Cited by 29 · see citing works
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Fang, X., Wang, H., Han, D., Xie, E., Yang, X., Wei, J., Gu, S., Gao, F., Zhu, N., Yin, X., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1821022116 · Cited by 2,142 · see citing works
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Sugamura, K., & Keaney (2011) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2011.05.004 · Cited by 769 · see citing works
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Handy, D. E., & Loscalzo, J. (2012) · Antioxidants & Redox Signaling · doi:10.1089/ars.2011.4123 · Cited by 588 · see citing works
Animal Models of Heart Failure: A Scientific Statement From the American Heart Association
Houser, S. R., Margulies, K. B., Murphy, A. M., Spinale, F. G., Francis, G. S., Prabhu, S. D., Rockman, H. A., Kass, D. A., Molkentin, J. D., Sussman, M. A., et al. (2012) · Circulation Research · doi:10.1161/res.0b013e3182582523 · Cited by 435 · see citing works
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Wang, H., Wang, B., Normoyle, K. P., Jackson, K., Spitler, K., Sharrock, M. F., Miller, C. M., Best, C., Llano, D., & Du, R. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00307 · Cited by 356 · see citing works
Ismahil, M. A., Hamid, T., Bansal, S. S., Patel, B., Kingery, J. R., & Prabhu, S. D. (2013) · Circulation Research · doi:10.1161/circresaha.113.301720 · Cited by 340 · see citing works
Self-citationActivated T Lymphocytes are Essential Drivers of Pathological Remodeling in Ischemic Heart Failure
Bansal, S. S., Ismahil, M. A., Goel, M., Patel, B., Hamid, T., Rokosh, G. D., & Prabhu, S. D. (2017) · Circulation Heart Failure · doi:10.1161/circheartfailure.116.003688 · Cited by 323 · see citing works
Self-citationBansal, S. S., Ismahil, M. A., Goel, M., Zhou, G., Rokosh, G. D., Hamid, T., & Prabhu, S. D. (2019) · Circulation · doi:10.1161/circulationaha.118.036065 · Cited by 302 · see citing works
Self-citationHamid, T., Guo, S. Z., Kingery, J. R., Xiang, X., Dawn, B., & Prabhu, S. D. (2010) · Cardiovascular Research · doi:10.1093/cvr/cvq274 · Cited by 253 · see citing works
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Ayer, A., Zarjou, A., Agarwal, A., & Stocker, R. (2016) · Physiological Reviews · doi:10.1152/physrev.00003.2016 · Cited by 243 · see citing works
A review on heme oxygenase-1 induction: is it a necessary evil
Waza, A. A., Hamid, Z., Ali, S., Bhat, S. A., & Bhat, M. A. (2018) · Inflammation Research · doi:10.1007/s00011-018-1151-x · Cited by 243 · see citing works
Redox signaling in cardiovascular health and disease
Madamanchi, N. R., & Runge, M. S. (2013) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2013.04.001 · Cited by 223 · see citing works
CORM-3 Reactivity toward Proteins: The Crystal Structure of a Ru(II) Dicarbonyl−Lysozyme Complex
Santos‐Silva, T., Mukhopadhyay, A., Seixas, J. D., Bernardes, G. J. L., Romão, C. C., & Romão, M. J. (2011) · Journal of the American Chemical Society · doi:10.1021/ja108820s · Cited by 216 · see citing works
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Otterbein, L. E., Foresti, R., & Motterlini, R. (2016) · Circulation Research · doi:10.1161/circresaha.116.306588 · Cited by 215 · see citing works
The Role of Nrf2-Mediated Pathway in Cardiac Remodeling and Heart Failure
Zhou, S., Sun, W., Zhang, Z., & Zheng, Y. (2014) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2014/260429 · Cited by 203 · see citing works
Oxidative stress induces mitochondrial iron overload and ferroptotic cell death
Chen, Y., Guo, X., Zeng, Y., Mo, X., Hong, S., He, H., Li, J., Fatima, S., & Liu, Q. (2023) · Scientific Reports · doi:10.1038/s41598-023-42760-4 · Cited by 202 · see citing works
Heme Oxygenase-1 As a Target for Drug Discovery
Motterlini, R., & Foresti, R. (2013) · Antioxidants and Redox Signaling · doi:10.1089/ars.2013.5658 · Cited by 178 · see citing works
Hydrogen Sulfide Attenuates Cardiac Dysfunction After Heart Failure Via Induction of Angiogenesis
Polhemus, D. J., Kondo, K., Bhushan, S., Bir, S. C., Kevil, C. G., Murohara, T., Lefer, D. J., & Calvert, J. W. (2013) · Circulation Heart Failure · doi:10.1161/circheartfailure.113.000299 · Cited by 171 · see citing works
Heme oxygenase-1 regulates mitochondrial quality control in the heart
Hull, T. D., Boddu, R., Guo, L., Tisher, C. C., Traylor, A., Patel, B., Joseph, R., Prabhu, S. D., Suliman, H. B., Piantadosi, C. A., et al. (2016) · JCI Insight · doi:10.1172/jci.insight.85817 · Cited by 171 · see citing works
Self-citationMetabolic Control by Heat Stress Determining Cell Fate to Ferroptosis for Effective Cancer Therapy
Xie, S., Sun, W., Zhang, C., Dong, B., Yang, J., Hou, M., Xiong, L., Cai, B., Liu, X., & Xue, W. (2021) · ACS Nano · doi:10.1021/acsnano.1c00380 · Cited by 162 · see citing works
Targeting Ferroptosis against Ischemia/Reperfusion Cardiac Injury
Lillo‐Moya, J., Rojas-Solé, C., Muñoz-Salamanca, D., Panieri, E., Saso, L., & Rodrigo, R. (2021) · Antioxidants · doi:10.3390/antiox10050667 · Cited by 161 · see citing works
Iacono, L. L., Boczkowski, J., Zini, R., Salouage, I., Berdeaux, A., Motterlini, R., & Morin, D. (2011) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2011.02.033 · Cited by 160 · see citing works
Carbon monoxide: Mechanisms of action and potential clinical implications
Rochette, L., Cottin, Y., Zeller, M., & Vergely, C. (2012) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2012.09.007 · Cited by 145 · see citing works
Cardioprotective Effect of Beta-3 Adrenergic Receptor Agonism
Niu, X., Watts, V. L., Cingolani, O. H., Sivakumaran, V., Leyton-Mange, J. S., Ellis, C. L., Miller, K. L., Vandegaer, K., Bedja, D., Gabrielson, K. L., et al. (2012) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2011.12.046 · Cited by 141 · see citing works
Maamoun, H., Tarek, B., Pintus, G., Munusamy, S., & Agouni, A. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00070 · Cited by 141 · see citing works
Zhao, Y., Zhang, L., Qiao, Y., Zhou, X., Wu, G., Wang, L., Peng, Y., Dong, X., Huang, H., Si, L., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0075927 · Cited by 138 · see citing works
Protein S-glutathiolation: Redox-sensitive regulation of protein function
Hill, B., & Bhatnagar, A. (2011) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2011.07.009 · Cited by 122 · see citing works
Self-citationLee, S. E., Jeong, S. I., Yang, H., Park, C., Jin, Y., & Park, Y. S. (2011) · Journal of Cellular Biochemistry · doi:10.1002/jcb.23158 · Cited by 115 · see citing works
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Pulliam, D. A., Deepa, S. S., Liu, Y., Hill, S., Lin, A., Bhattacharya, A., Shi, Y., Sloane, L. B., Viscomi, C. F., Zeviani, M., et al. (2014) · Biochemical Journal · doi:10.1042/bj20140291 · Cited by 108 · see citing works
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Li, H., Yao, W., Irwin, M. G., Wang, T., Wang, S., Zhang, L., & Xia, Z. (2015) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2015.03.007 · Cited by 106 · see citing works
Dunn, L., Kong, S. M. Y., Tumanov, S., Chen, W., Cantley, J., Ayer, A., Maghzal, G. J., Midwinter, R. G., Chan, K. H., Ng, M., et al. (2020) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.120.315393 · Cited by 99 · see citing works
Chronic oral exposure to the aldehyde pollutant acrolein induces dilated cardiomyopathy
Ismahil, M. A., Hamid, T., Haberzettl, P., Gu, Y., Chandrasekar, B., Srivastava, S., Bhatnagar, A., & Prabhu, S. D. (2011) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00120.2011 · Cited by 99 · see citing works
Self-citationPotential Therapeutic Effects of Natural Heme Oxygenase-1 Inducers in Cardiovascular Diseases
Barbagallo, I. A., Galvano, F., Frigiola, A., Cappello, F., Riccioni, G., Murabito, P., D’Orazio, N., Torella, M., Gazzolo, D., & Volti, G. L. (2012) · Antioxidants and Redox Signaling · doi:10.1089/ars.2011.4360 · Cited by 94 · see citing works
Han, D. H., Wang, Y., Chen, J., Zhang, J., Yu, P., Zhang, R., Li, S., Bo, T., Wang, Y., Qiu, Y. F., et al. (2019) · Journal of Pineal Research · doi:10.1111/jpi.12571 · Cited by 93 · see citing works
Myocardial ischemic reperfusion induces de novo Nrf2 protein translation
Xu, B., Zhang, J. Y., Strom, J. G., Lee, S., & Chen, Q. M. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2014.06.002 · Cited by 89 · see citing works
Belcher, J. D., Young, M. A., Chen, C., Nguyen, J., Burhop, K. E., Tran, P. D., & Vercellotti, G. M. (2013) · Blood · doi:10.1182/blood-2013-02-486282 · Cited by 88 · see citing works
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Yang, G., Wang, Z.-J., Bai, F., Qin, X., Cao, J., Lv, J., & Zhang, M. (2015) · Molecules · doi:10.3390/molecules20046626 · Cited by 79 · see citing works
A novel Danshensu derivative confers cardioprotection via PI3K/Akt and Nrf2 pathways
Cui, G., Shan, L., Hung, M.-W., Lei, S., Choi, I., Zhang, Z., Yu, P., Hoi, M. P. M., Wang, Y., & Lee, S. M. (2013) · International Journal of Cardiology · doi:10.1016/j.ijcard.2012.12.012 · Cited by 78 · see citing works
Mitochondrial quality-control dysregulation in conditional HO-1–/– mice
Suliman, H. B., Keenan, J. E., & Piantadosi, C. A. (2017) · JCI Insight · doi:10.1172/jci.insight.89676 · Cited by 78 · see citing works
Pleural Mesothelial Cell Differentiation and Invasion in Fibrogenic Lung Injury
Zolak, J. S., JAGIRDAR, R. M., Surolia, R., Karki, S., Oliva, O. M., Hock, T., Guroji, P., Ding, Q., Liu, R.-M., Bolisetty, S., et al. (2013) · American Journal Of Pathology · doi:10.1016/j.ajpath.2012.12.030 · Cited by 77 · see citing works
Chen, S., Jiang, H., Cao, Y. W., Wang, Y., Hu, Z., Zhu, Z., & Chai, Y. (2016) · Scientific Reports · doi:10.1038/srep24245 · Cited by 77 · see citing works
Seixas, J. D., Mukhopadhyay, A., Santos‐Silva, T., Otterbein, L. E., Gallo, D. J., Rodrigues, S. S., Guerreiro, B. H., Gonçalves, A. M., Penacho, N., Marques, A. R., et al. (2012) · Dalton Transactions · doi:10.1039/c2dt32174b · Cited by 76 · see citing works
Ayyappan, P., Vineetha, V. P., & Raghu, K. G. (2014) · PLoS ONE · doi:10.1371/journal.pone.0096220 · Cited by 75 · see citing works
Zheng, G., Zhan, Y., Wang, H., Luo, Z., Zheng, F., Zhou, Y., Wu, Y., Wang, S., Wu, Y., Xiang, G., et al. (2019) · EBioMedicine · doi:10.1016/j.ebiom.2018.12.059 · Cited by 76 · see citing works
Carbon monoxide: A vital signalling molecule and potent toxin in the myocardium
Peers, C., & Steele, D. S. (2011) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2011.05.013 · Cited by 74 · see citing works
Pan, L., Liu, X., Shen, Y., Wang, N.-Z., Xu, J., Wu, D., Xiong, Q., Deng, H., Huang, G.-Y., & Zhu, Y. Z. (2013) · International Journal of Cardiology · doi:10.1016/j.ijcard.2013.06.007 · Cited by 74 · see citing works
Towards Improved Therapeutic CORMs: Understanding the Reactivity of CORM-3 with Proteins
Santos‐Silva, T., Mukhopadhyay, A., Seixas, J. D., Bernardes, G. J. L., Romão, C. C., & Romão, M. J. (2011) · Current Medicinal Chemistry · doi:10.2174/092986711796504583 · Cited by 73 · see citing works
Shan, H., Li, T., Zhang, L., Yang, R., Li, Y., Zhang, M., Dong, Y., Zhou, Y., Xu, C., Yang, B., et al. (2018) · EBioMedicine · doi:10.1016/j.ebiom.2018.11.056 · Cited by 72 · see citing works
Leukocyte iNOS is required for inflammation and pathological remodeling in ischemic heart failure
Kingery, J. R., Hamid, T., Lewis, R. K., Ismahil, M. A., Bansal, S. S., Rokosh, G. D., Townes, T. M., Ildstad, S. T., Jones, S. P., & Prabhu, S. D. (2017) · Basic Research in Cardiology · doi:10.1007/s00395-017-0609-2 · Cited by 69 · see citing works
Self-citationHsp60 and heme oxygenase-1 (Hsp32) in acute myocardial infarction
Novo, G., Cappello, F., Rizzo, M., Fazio, G., Zambuto, S., Tortorici, E., Gammazza, A. M., Corrao, S., Zummo, G., de Macario, E. C., et al. (2011) · Translational research · doi:10.1016/j.trsl.2011.01.003 · Cited by 69 · see citing works
Cardioprotection of Tetrahedral DNA Nanostructures in Myocardial Ischemia-Reperfusion Injury
Zhang, M., Zhu, J., Qin, X., Zhou, M., Zhang, X., Gao, Y., Zhang, T., Xiao, D., Cui, W., & Cai, X. (2019) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.9b10645 · Cited by 69 · see citing works
The impact of age-related dysregulation of the angiotensin system on mitochondrial redox balance
Vajapey, R. S., Rini, D. A., Walston, J. D., & Abadir, P. M. (2014) · Frontiers in Physiology · doi:10.3389/fphys.2014.00439 · Cited by 69 · see citing works
Carbon monoxide – beyond toxicity?
Stucki, D., & Stahl, W. (2020) · Toxicology Letters · doi:10.1016/j.toxlet.2020.08.010 · Cited by 66 · see citing works
Patel, B., Ismahil, M. A., Hamid, T., Bansal, S. S., & Prabhu, S. D. (2017) · PLoS ONE · doi:10.1371/journal.pone.0170781 · Cited by 64 · see citing works
Self-citationZhang, T., & Xiang, L. (2019) · Cellular & Molecular Biology Letters · doi:10.1186/s11658-019-0142-4 · Cited by 64 · see citing works
Santos, M. F. A., Seixas, J. D., Coelho, A. C., Mukhopadhyay, A., Reis, P. M., Romão, M. J., Romão, C. C., & Santos‐Silva, T. (2012) · Journal of Inorganic Biochemistry · doi:10.1016/j.jinorgbio.2012.06.018 · Cited by 63 · see citing works
Bajić, Z., Šobot, T., Škrbić, R., Stojiljković, M. P., Ponorac, N., Matavulj, A., & Djuric, D. M. (2022) · Biomolecules · doi:10.3390/biom12040536 · Cited by 65 · see citing works
Issan, Y., Kornowski, R., Aravot, D., Shainberg, A., Laniado-Schwartzman, M., Sodhi, K., Abraham, N. G., & Hochhauser, E. (2014) · PLoS ONE · doi:10.1371/journal.pone.0092246 · Cited by 68 · see citing works
Kain, V., Ingle, K. A., Kabarowski, J. H. S., Barnes, S., Limdi, N. A., Prabhu, S. D., & Halade, G. V. (2018) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2018.03.004 · Cited by 62 · see citing works
Self-citationCui, G., Luk, S. C. W., Li, R. A., Chan, K. K., Lei, S. W., Wang, L., Shen, H., Leung, G., & Lee, S. M. (2014) · Journal of Cardiovascular Pharmacology · doi:10.1097/fjc.0000000000000161 · Cited by 61 · see citing works
Meeran, M. F. N., Jagadeesh, G. S., & Selvaraj, P. (2015) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2015.12.006 · Cited by 61 · see citing works
Increased Heme Levels in the Heart Lead to Exacerbated Ischemic Injury
Sawicki, K. T., Shang, M., Wu, R., Chang, H., Khechaduri, A., Sato, T., Kamide, C., Liu, T., Prasad, S. V. N., & Ardehali, H. (2015) · Journal of the American Heart Association · doi:10.1161/jaha.115.002272 · Cited by 58 · see citing works
Pinocembrin ameliorates post-infarct heart failure through activation of Nrf2/HO-1 signaling pathway
Chen, X., Wan, W., Guo, Y., Ye, T., Fo, Y., Sun, Y., Qu, C., Yang, B., & Zhang, C. (2021) · Molecular Medicine · doi:10.1186/s10020-021-00363-7 · Cited by 57 · see citing works
Gu, J. F., Song, Z.-P., Dong-mei, G., Hu, W. G., Chen, Y.-G., & Zhang, D. (2012) · Cardiovascular Toxicology · doi:10.1007/s12012-012-9178-7 · Cited by 57 · see citing works
Lee, S. E., Yang, H., Jeong, S. I., Jin, Y.-H., Park, C.-S., & Park, Y. S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0041676 · Cited by 57 · see citing works
Conditioning the whole heart—not just the cardiomyocyte
Bell, R. M., & Yellon, D. M. (2012) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2012.04.001 · Cited by 55 · see citing works
Chen, X., Wei, S.-Y., Li, J.-S., Zhang, Q., Wang, Y., Zhao, S.-L., Yu, J. Q., Wang, C., Qin, Y., Wei, Q., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0147084 · Cited by 54 · see citing works
Zeng, J., Zhao, J., Dong, B., Cai, X., Jiang, J., Xue, R., Yao, F., Dong, Y., & Liu, C. (2019) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2019.01.002 · Cited by 53 · see citing works
Danshen injection prevents heart failure by attenuating post-infarct remodeling
Wang, L., Yu, J., Asare, P. F., Xing, X., Gao, H., Li, Y., Li, L., Zhu, Y., Gao, X., & Fan, G. (2017) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2017.04.027 · Cited by 52 · see citing works
An Overview of the Potential Therapeutic Applications of CO-Releasing Molecules
Ismailova, A., Kuter, D., Bohle, D. S., & Butler, I. S. (2018) · Bioinorganic Chemistry and Applications · doi:10.1155/2018/8547364 · Cited by 52 · see citing works
Sahu, B. D., Putcha, U. K., Kuncha, M., Rachamalla, S. S., & Sistla, R. (2014) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-014-2092-5 · Cited by 50 · see citing works
Wang, B., Yang, Q., Bai, W., Xing, Y., Lu, X., Sun, Y., & Zhao, Y. (2014) · PLoS ONE · doi:10.1371/journal.pone.0098047 · Cited by 50 · see citing works
Jaźwa, A., Stępniewski, J., Zamykal, M., Jagodzinska, J., Meloni, M., Emanueli, C., Józkowicz, A., & Dulak, J. (2012) · Cardiovascular Research · doi:10.1093/cvr/cvs284 · Cited by 49 · see citing works
Cao, J. J., Tsenovoy, P. L., Thompson, E. A., Falck, J. R., Touchon, R. C., Sodhi, K., Rezzani, R., Shapiro, J. I., & Abraham, N. G. (2015) · Prostaglandins & Other Lipid Mediators · doi:10.1016/j.prostaglandins.2015.01.002 · Cited by 49 · see citing works
Neutrophils are indispensable for adverse cardiac remodeling in heart failure
Antipenko, S. V., Mayfield, N., Jinno, M., Gunzer, M., Ismahil, M. A., Hamid, T., Prabhu, S. D., & Rokosh, G. D. (2024) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2024.02.005 · Cited by 49 · see citing works
Self-citationBeneficial effect of prolonged heme oxygenase 1 activation in a rat model of chronic heart failure
Collino, M., Pini, A., Mugelli, N., Mastroianni, R., Bani, D., Fantozzi, R., Papucci, L., Fazi, M., & Masini, E. (2013) · Disease Models & Mechanisms · doi:10.1242/dmm.011528 · Cited by 48 · see citing works
Worou, M. E., Belmokhtar, K., Bonnet, P., Vourc’h, P., Machet, M. C., Khamis, G., & Eder, V. (2011) · Cardiovascular Research · doi:10.1093/cvr/cvr072 · Cited by 47 · see citing works
Allwood, M. A., Kinobe, R. T., Ballantyne, L. L., Romanova, N. A., Melo, L. G., Ward, C. A., Brunt, K. R., & Simpson, J. A. (2014) · Cardiovascular Pathology · doi:10.1016/j.carpath.2014.03.007 · Cited by 46 · see citing works
Ma, D., Fang, Q., Wang, P., Gao, R., Wu, W., Lu, T., Cao, L., Hu, X., & Wang, J. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.626960 · Cited by 43 · see citing works
Issan, Y., Hochhauser, E., Kornowski, R., Leshem‐Lev, D., Lev, E. I., Sharoni, R., Vanella, L., Puri, N., Schwartzman, M. L., Abraham, N. G., et al. (2012) · Canadian Journal of Cardiology · doi:10.1016/j.cjca.2012.01.013 · Cited by 44 · see citing works
Borgdorff, M. A. J., Koop, A. M. C., Bloks, V. W., Dickinson, M. G., Paul Steendijk, A., Silljé, H. H. W., van Wiechen, M. P. H., Berger, R. M. F., & Bartelds, B. (2014) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2014.11.024 · Cited by 43 · see citing works
Yang, X., Jiang, H., & Shi, Y. (2017) · Cell & Bioscience · doi:10.1186/s13578-017-0146-6 · Cited by 43 · see citing works
Wang, H., Chen, Q., Gong, F., Xie, C., Zhou, S., & Gao, L. (2013) · Life Sciences · doi:10.1016/j.lfs.2013.10.007 · Cited by 43 · see citing works
Garlie, J. B., Hamid, T., Gu, Y., Ismahil, M. A., Chandrasekar, B., & Prabhu, S. D. (2011) · Basic Research in Cardiology · doi:10.1007/s00395-011-0196-6 · Cited by 43 · see citing works
Self-citationTomczyk, M., Kraszewska, I., Szade, K., Bukowska-Straková, K., Meloni, M., Józkowicz, A., Dulak, J., & Jaźwa, A. (2017) · Basic Research in Cardiology · doi:10.1007/s00395-017-0629-y · Cited by 41 · see citing works
Metal-based carbon monoxide releasing molecules with promising cytotoxic properties
Mansour, A. M., Khaled, R. M., Ferraro, G., Shehab, O. R., & Merlino, A. (2024) · Dalton Transactions · doi:10.1039/d4dt00087k · Cited by 41 · see citing works
Distefano, G., & Sciacca, P. (2012) · The Italian Journal of Pediatrics/Italian journal of pediatrics · doi:10.1186/1824-7288-38-41 · Cited by 40 · see citing works
Lin, H., Li, Y., Zhu, H., Wang, Q., Chen, Z., Chen, L., Zhu, Y., Zheng, C., Wang, Y., Liao, W., et al. (2019) · Cardiovascular Research · doi:10.1093/cvr/cvz016 · Cited by 41 · see citing works
Ferroptosis contributes to catecholamine-induced cardiotoxicity and pathological remodeling
Chen, Y., Guo, X., Zeng, Y., Mo, X., Hong, S., He, H., Li, J., Steinmetz, R. N., & Liu, Q. (2023) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2023.07.025 · Cited by 42 · see citing works
Pleiotropic antioxidant potential of rosuvastatin in preventing cardiovascular disorders
Mahalwar, R., & Khanna, D. (2013) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2013.04.025 · Cited by 40 · see citing works
Chen, T.-M., Li, J., Liu, L., Li, F., Li, X.-Y., Wang, Y., Abraham, N. G., & Cao, J. J. (2013) · International Journal of Molecular Sciences · doi:10.3390/ijms14022684 · Cited by 40 · see citing works
Heme oxygenase-1: an emerging therapeutic target to curb cardiac pathology
Czibik, G., Dérumeaux, G., Sawaki, D., Valen, G., & Motterlini, R. (2014) · Basic Research in Cardiology · doi:10.1007/s00395-014-0450-9 · Cited by 39 · see citing works
- Authors
- Wang, G., Hamid, T., Keith, R. J., Zhou, G., Partridge, C. R., Xiang, X., Kingery, J. R., Lewis, R. K., Li, Q., Rokosh, D. G., Ford, R., Spinale, F. G., Riggs, D. W., Srivastava, S., Bhatnagar, A., Bolli, R., & Prabhu, S. D.
- Affiliations
- University of Louisville (US)
- From the Institute of Molecular Cardiology, Department of Medicine, University of Louisville (G.W., T.H., R.J.K., G.Z., C.R.P., X.X., J.R.K., R.K.L., Q.L., D.G.R., D.W.R., S.S., A.B., R.B., S.D.P.) and Louisville Veterans Affairs Medical Center, Louisville, Ky (S.D.P.); and Department of Surgery, Medical University of South Carolina, Charleston (R.F., F.G.S.).
- ORCID
- Venue
- Circulation
- Published
- 2010-05-04
- Volume
- 121
- Issue
- 17
- Pages
- 1912-1925
- ISSN
- 0009-7322 (ISSN-L)
- 1524-4539
- PMC
- PMC2917269
- OpenAlex
- W2052867135
- Cited by
- 249
- References
- 38
- Citations by year
- 2026: 4 · 2025: 9 · 2024: 10 · 2023: 9 · 2022: 14 · 2021: 16 · 2020: 12 · 2019: 18 · 2018: 13 · 2017: 17 · 2016: 12 · 2015: 16 · 2014: 23 · 2013: 26 · 2012: 21
- FWCI
- 9.90
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Circulation (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Heart, Lung, and Blood Institute (P01HL078825, R01HL070897, R01HL059378, R37HL055757, HL 78825, HL 55757, HL-76794, R01HL099014, R01HL055757, R01HL055477, HL70897, HL55477, R01HL076794)
- National Institute of Environmental Health Sciences ((ES11860, P01ES011860)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heme Oxygenase-1 and Carbon Monoxide
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac Fibrosis and Remodeling
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heat shock proteins research
- Keywords
- heme oxygenase-1, chronic heart failure, cardiac remodeling, cardiomyocyte apoptosis, carbon monoxide, mitochondrial permeability transition, p53, oxidative stress, myocardial fibrosis, cardiomyocyte hypertrophy, CORM-3, myocardial neovascularization, myocardial infarction, cardioprotection, malondialdehyde
- MeSH terms
- Animals, Carbon Monoxide, Cardiotonic Agents, Chronic Disease, Fibrosis, Heart Failure, Humans, Male, Mice, Inbred C57BL, Mice, Transgenic, Mitochondria, Myocardial Infarction, Myocardium, Organometallic Compounds, Stroke Volume, Up-Regulation, Gene Expression, Apoptosis, Oxidative Stress, Ventricular Dysfunction, Left, Neovascularization, Physiologic, Ventricular Remodeling, Mice, Heme Oxygenase-1
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