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Mitochondrial Respiratory Chain and NAD(P)H Oxidase Are Targets for theAntiproliferative Effect of Carbon Monoxide in Human Airway SmoothMuscle
Open accessAbstract
Carbon monoxide (CO), one of the end products of heme oxygenase activity, inhibits smooth muscle proliferation by decreasing ERK1/2 phosphorylation and cyclin D1 expression, a signaling pathway that is known to be modulated by reactive oxygen species (ROS) in airway smooth muscle cells (ASMCs). Two important sources of ROS involved in cell signaling are the membrane NAD(P)H oxidase and the mitochondrial respiratory chain. Thus, that CO could modulate redox signaling in ASMCs by interacting with the heme moiety of NAD(P)H oxidase and/or the respiratory chain is a plausible hypothesis. Here we show that a recently identified carbon monoxide-releasing molecule, [Ru(CO)3Cl2]2 (or CORM-2) 1) inhibits NAD(P)H oxidase cytochrome b558 activity, 2) increases oxidant production by the mitochondria, and 3) inhibits ASMC proliferation and phosphorylation of the ERK1/2 mitogen-activated protein kinase and expression of cyclin D1, two critical pathways involved in muscle proliferation. No such effects were observed with the negative control (Ru(Me2SO)4Cl2), which does not contain CO groups. Because both diphenylene iodinium or apocynin (inhibitors of NAD(P)H oxidase) and rotenone (a molecule that increases mitochondrial ROS production by blocking the respiratory chain) mimicked the effect of CORM-2 on cyclin D1 expression and ASMC proliferation, the antiproliferative effect of CORM-2 is probably related to inhibition of cytochromes on both NAD(P)H oxidase and the respiratory chain. The involvement of increased mitochondria-derived oxidants is substantiated by the findings showing that the antioxidant N-acetylcysteine partially inhibited the effects of CORM-2. This study provides a new mechanism to explain redox signaling by CO.
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“These peptides have been shown to mediate protection in animal models of ischemia/reperfusion (922) and insulin resistance (27).”
From Sources of Vascular Nitric Oxide and Reactive Oxygen Species and Their Regulation (2019) · cites this paper as [922]
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“Furthermore, heme oxygenase-1 (HO-1), an antioxidant enzyme upregulated by Nrf2, inhibited NOX2 activation in smooth muscle cells and LPS-stimulated macrophages [171,172].”
From ROS Generation in Microglia: Understanding Oxidative Stress and Inflammation in Neurodegenerative Disease (2020) · cites this paper as [171]
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1 retracted
Song, R., Mahidhara, R. S., Liu, F., Ning, W., Otterbein, L. E., & Choi, A. M. K. (2002) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.4851 · Cited by 127
RetractedBoveris, A., & Chance, B. (1973) · Biochemical Journal · doi:10.1042/bj1340707 · Cited by 2,626
THE HEME OXYGENASE SYSTEM:A Regulator of Second Messenger Gases
Maines, M. D. (1997) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.37.1.517 · Cited by 2,489
Li, N., Ragheb, K., Lawler, G., Sturgis, J., Rajwa, B. P., Melendez, J. A., & Robinson, J. P. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m210432200 · Cited by 1,465
Heme oxygenase-1: unleashing the protective properties of heme
Otterbein, L. E., Soares, M. P., Yamashita, K., & Bach, F. H. (2003) · Trends in Immunology · doi:10.1016/s1471-4906(03)00181-9 · Cited by 1,166
Carbon Monoxide-Releasing Molecules
Motterlini, R., Clark, J., Foresti, R., Sarathchandra, P., Mann, B. E., & Green, C. J. (2002) · Circulation Research · doi:10.1161/hh0202.104530 · Cited by 999
Self-citationBABIOR, B. M., Lambeth, J. D., & Nauseef, W. M. (2002) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.2001.2642 · Cited by 911
Poderoso, J. J., Carreras, M. C., Lisdero, C., Riobó, N., Schöpfer, F., & Boveris, A. (1996) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1996.0146 · Cited by 726
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
Self-citationIntracellular hydrogen peroxide and superoxide anion detection in endothelial cells
Carter, W. O., Narayanan, P. K., & Robinson, J. P. (1994) · Journal of Leukocyte Biology · doi:10.1002/jlb.55.2.253 · Cited by 640
Otterbein, L. E., Zuckerbraun, B. S., Haga, M., Liu, F., Song, R., Usheva, A., Stachulak, C., Bodyak, N. D., Smith, R. N., Csizmadia, E., et al. (2003) · Nature Medicine · doi:10.1038/nm817 · Cited by 527
Carbon Monoxide Controls the Proliferation of Hypoxic Vascular Smooth Muscle Cells
Morita, T., Mitsialis, S. A., Koike, H., Liu, Y., & Kourembanas, S. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.52.32804 · Cited by 332
Vasoactive properties of CORM‐3, a novel water‐soluble carbon monoxide‐releasing molecule
Foresti, R., Hammad, J., Clark, J., Johnson, T. R., Mann, B. E., Friebe, A., Green, C. J., & Motterlini, R. (2004) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0705825 · Cited by 304
Self-citationCarbon Monoxide Specifically Inhibits Cytochrome C Oxidase of Human Mitochondrial Respiratory Chain
Alonso, J., Cardellach, F., López, S., Casademont, J., & Miró, Ò. (2003) · Pharmacology & Toxicology · doi:10.1034/j.1600-0773.2003.930306.x · Cited by 270
Bioactivity and Pharmacological Actions of Carbon Monoxide-Releasing Molecules
Motterlini, R., Mann, B. E., Johnson, T. R., Clark, J., Foresti, R., & Green, C. J. (2003) · Current Pharmaceutical Design · doi:10.2174/1381612033453785 · Cited by 256
Self-citationRac1 inhibits TNF‐α‐induced endothelial cell apoptosis: dual regulation by reactive oxygen species
Deshpande, S. S., Angkeow, P., Huang, J., Ozaki, M., & Irani, K. (2000) · The FASEB Journal · doi:10.1096/fj.99-0910com · Cited by 235
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
Diphenyleneiodonium Inhibits the Cell Redox Metabolism and Induces Oxidative Stress
Riganti, C., Gazzano, E., Polimeni, M., Costamagna, C., Bosìa, A., & Ghigo, D. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m406314200 · Cited by 198
NADPH oxidase activity is required for endothelial cell proliferation and migration
Abid, M. R., Kachra, Z., Spokes, K., & Aird, W. C. (2000) · FEBS Letters · doi:10.1016/s0014-5793(00)02305-x · Cited by 191
An NAD(P)H oxidase regulates growth and transcription in melanoma cells
Brar, S. S., Kennedy, T. P., Sturrock, A., Huecksteadt, T. P., Quinn, M. T., Whorton, A. R., & Hoidal, J. R. (2002) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00496.2001 · Cited by 183
Tryptase and agonists of PAR-2 induce the proliferation of human airway smooth muscle cells
Berger, P., Perng, D., Thabrew, H., Compton, S. J., Cairns, J. A., McEuen, A. R., Marthan, R., de Lara, J.-M. T., & Walls, A. F. (2001) · Journal of Applied Physiology · doi:10.1152/jappl.2001.91.3.1372 · Cited by 176
Peyton, K. J., Reyna, S. V., Chapman, G. B., Ensenat, D., Liu, X., Wang, H., Schafer, A. I., & Durante, W. (2002) · Blood · doi:10.1182/blood.v99.12.4443 · Cited by 156
Heme oxygenase‐1 in growth control and its clinical application to vascular disease
Durante, W. (2003) · Journal of Cellular Physiology · doi:10.1002/jcp.10274 · Cited by 154
Characterization of a Rac1 Signaling Pathway to Cyclin D1 Expression in Airway Smooth Muscle Cells
Page, K., Li, J., Hodge, J. A., Liu, P. T., Hoek, T. L. V., Becker, L. B., Pestell, R. G., Rosner, M. R., & Hershenson, M. B. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.31.22065 · Cited by 137
Young, T. A., Cunningham, C. C., & Bailey, S. M. (2002) · Archives of Biochemistry and Biophysics · doi:10.1016/s0003-9861(02)00338-7 · Cited by 128
Uncoupling protein-2 deficiency promotes oxidant stress and delays liver regeneration in mice
Horimoto, M., Fülöp, P., Derdák, Z., Wands, J. R., & Baffy, G. (2004) · Hepatology · doi:10.1002/hep.20047 · Cited by 120
Dang, P. M., Dewas, C., Gaudry, M., Fay, M., Pédruzzi, E., Gougerot‐Pocidalo, M., & Benna, J. E. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.29.20704 · Cited by 118
Inhibition of preadipocyte proliferation by mitochondrial reactive oxygen species
Carrière, A., Fernandez, Y., Rigoulet, M., Pénicaud, L., & Casteilla, L. (2003) · FEBS Letters · doi:10.1016/s0014-5793(03)00862-7 · Cited by 114
Invited Review: The circle of life: cell cycle regulation in airway smooth muscle
Ammit, A. J., & Panettieri, R. A. (2001) · Journal of Applied Physiology · doi:10.1152/jappl.2001.91.3.1431 · Cited by 103
Lee, T., & Chau, L. (2001) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.2001.280.3.c709 · Cited by 96
Alonso, M., Melani, M., Converso, D. P., Jaitovich, A., Paz, C., Carreras, M. C., Medina, J. H., & Poderoso, J. J. (2004) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2004.02323.x · Cited by 95
Choi, B.-M., Pae, H., Kim, Y., & Chung, H. (2003) · Hepatology · doi:10.1053/jhep.2003.50114 · Cited by 93
Brar, S. S., Kennedy, T. P., Whorton, A. R., Murphy, T. M., Chitano, P., & Hoidal, J. R. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.28.20017 · Cited by 90
Taillé, C., Almolki, A., Benhamed, M., Zedda, C., Megret, J., Berger, P., Lesèche, G., Fadel, É., Yamaguchi, T., Marthan, R., et al. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m300364200 · Cited by 82
Self-citationOldenburg, O. (2003) · Journal of Molecular and Cellular Cardiology · doi:10.1016/s0022-2828(03)00083-x · Cited by 73
Rotenone Induces Apoptosis via Activation of Bad in Human Dopaminergic SH-SY5Y Cells
Watabe, M., & Nakaki, T. (2004) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.104.071381 · Cited by 73
Patel, H. J., Belvisi, M. G., Donnelly, L., Yacoub, M. H., Chung, K. F., & Mitchell, J. A. (1999) · The FASEB Journal · doi:10.1096/fasebj.13.13.1810 · Cited by 71
Protective Role of Heme Oxygenases against Endotoxin-induced Diaphragmatic Dysfunction in Rats
Taillé, C., Foresti, R., Lanone, S., Zedda, C., Green, C. J., Aubier, M., Motterlini, R., & Boczkowski, J. (2001) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/ajrccm.163.3.2004202 · Cited by 71
Self-citationBogoyevitch, M. A., Ng, D. C. H., Court, N. W., Draper, K. A., Dhillon, A. S., & Abas, L. (2000) · Journal of Molecular and Cellular Cardiology · doi:10.1006/jmcc.2000.1187 · Cited by 62
Thabut, G., Benna, J. E., Samb, A., Corda, S., Megret, J., Lesèche, G., Vicaut, É., Aubier, M., & Boczkowski, J. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m200315200 · Cited by 43
Self-citationStanford, S. J., Walters, M. J., Hislop, A. A., Haworth, S. G., Evans, T. W., Mann, B. E., Motterlini, R., & Mitchell, J. A. (2003) · European Journal of Pharmacology · doi:10.1016/s0014-2999(03)02001-6 · Cited by 42
Self-citationRegulation of Airway Smooth Muscle Cyclin D1 Transcription by Protein Kinase C-δ
Page, K., Li, J., Corbit, K. C., Rumilla, K. M., Soh, J., Weinstein, I. B., Albanese, C., Pestell, R. G., Rosner, M. R., & Hershenson, M. B. (2002) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/ajrcmb.27.2.20010016oc · Cited by 39
Real-Time Measurement of Intracellular Reactive Oxygen Species Using Mito Tracker Orange (CMH2TMRos)
Kweon, S.-M., Kim, H., Lee, Z., Kim, S., Kim, S.-I., Paik, S., & Ha, K. (2001) · Bioscience Reports · doi:10.1023/a:1013290316939 · Cited by 36
Hancock, J. T., White, J. I., Jones, O. T. G., & Silver, I. A. (1991) · Free Radical Biology and Medicine · doi:10.1016/0891-5849(91)90184-5 · Cited by 24
Research works printed but not linked: 4
- Piantadosi, 2002, Antioxid. RedoxSignal., 4, 259
- Thorup, 1999, Am. J. Physiol., 277, F882
- Johnson, 2003, Am. J. Physiol., 285, R536
- Otterbein, 2002, Antioxid. RedoxSignal., 4, 309
Cited by
Sorted by citations
Heme Oxygenase-1/Carbon Monoxide: From Basic Science to Therapeutic Applications
Ryter, S. W., Alam, J., & Choi, A. M. K. (2006) · Physiological Reviews · doi:10.1152/physrev.00011.2005 · Cited by 2,342
The therapeutic potential of carbon monoxide
Motterlini, R., & Otterbein, L. E. (2010) · Nature Reviews Drug Discovery · doi:10.1038/nrd3228 · Cited by 1,643
Self-citationSimpson, D. S. A., & Oliver, P. L. (2020) · Antioxidants · doi:10.3390/antiox9080743 · Cited by 1,044
“Furthermore, heme oxygenase-1 (HO-1), an antioxidant enzyme upregulated by Nrf2, inhibited NOX2 activation in smooth muscle cells and LPS-stimulated macrophages [171,172].”
BackgroundPharmacological and Clinical Aspects of Heme Oxygenase
Abraham, N. G., & Kappas, A. (2008) · Pharmacological Reviews · doi:10.1124/pr.107.07104 · Cited by 1,115
“In particular, CO suppresses the expression of the cdk2 activators, cyclin A and D1, while stimulating the expression of the cdk2 inhibitor, p21 (Taillé et al., 2005; Tulis et al., 2005).”
Sautin, Y. Y., Nakagawa, T., Zharikov, S. I., & Johnson, R. J. (2007) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00600.2006 · Cited by 799
“NADPH oxidase activity was measured using the lucigenin-enhanced chemiluminescence method in crude cell homogenates and microsomal membrane fractions by following previously described procedures with minor modifications (15, 54).”
Method
Metadata
- Authors
- Taillé, C., El-Benna, J., Lanone, S., Boczkowski, J., & Motterlini, R.
- Affiliations
- Inserm (FR)
- Northwick Park Institute for Medical Research (GB)
- Corresponding author
- Boczkowski, Jorge
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2005-07
- Volume
- 280
- Issue
- 27
- Pages
- 25350-25360
- ISSN
- 0021-9258 (ISSN-L)
- OpenAlex
- W2148052253
- Cited by
- 246
- References
- 44
- Citations by year
- 2026: 2 · 2025: 6 · 2024: 7 · 2023: 4 · 2022: 14 · 2021: 7 · 2020: 7 · 2019: 8 · 2018: 8 · 2017: 11 · 2016: 7 · 2015: 11 · 2014: 6 · 2013: 12 · 2012: 13
- FWCI
- 7.65
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heme Oxygenase-1 and Carbon Monoxide
- Health Sciences › Medicine › Physiology (medical) › Nitric Oxide and Endothelin Effects
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
- Keywords
- carbon monoxide, airway smooth muscle, smooth muscle cell proliferation, NADPH oxidase, cytochrome b558, mitochondrial respiratory chain, reactive oxygen species, redox signaling, ERK1/2 phosphorylation, cyclin D1, heme oxygenase, rotenone, apocynin, N-acetylcysteine
- MeSH terms
- Bronchi, Carbon Monoxide, Cell Division, Cells, Cultured, Electron Transport, Humans, Mitochondria, NADH, NADPH Oxidoreductases, Organometallic Compounds, Phosphorylation, Platelet-Derived Growth Factor, NADPH Oxidases, Cyclin D1, Mitogen-Activated Protein Kinase 1, Myocytes, Smooth Muscle, Mitogen-Activated Protein Kinase 3
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