{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,23]],"date-time":"2026-03-23T19:52:20Z","timestamp":1774295540272,"version":"3.50.1"},"reference-count":50,"publisher":"American Association for Cancer Research (AACR)","issue":"23","content-domain":{"domain":["aacrjournals.org"],"crossmark-restriction":true},"short-container-title":[],"published-print":{"date-parts":[[2013,12,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>One classical feature of cancer cells is their metabolic acquisition of a highly glycolytic phenotype. Carbon monoxide (CO), one of the products of the cytoprotective molecule heme oxygenase-1 (HO-1) in cancer cells, has been implicated in carcinogenesis and therapeutic resistance. However, the functional contributions of CO and HO-1 to these processes are poorly defined. In human prostate cancers, we found that HO-1 was nuclear localized in malignant cells, with low enzymatic activity in moderately differentiated tumors correlating with relatively worse clinical outcomes. Exposure to CO sensitized prostate cancer cells but not normal cells to chemotherapy, with growth arrest and apoptosis induced in vivo in part through mitotic catastrophe. CO targeted mitochondria activity in cancer cells as evidenced by higher oxygen consumption, free radical generation, and mitochondrial collapse. Collectively, our findings indicated that CO transiently induces an anti-Warburg effect by rapidly fueling cancer cell bioenergetics, ultimately resulting in metabolic exhaustion. Cancer Res; 73(23); 7009\u201321. \u00a92013 AACR.<\/jats:p>","DOI":"10.1158\/0008-5472.can-13-1075","type":"journal-article","created":{"date-parts":[[2013,10,12]],"date-time":"2013-10-12T00:07:14Z","timestamp":1381536434000},"page":"7009-7021","update-policy":"https:\/\/doi.org\/10.1158\/crossmark_policy","source":"Crossref","is-referenced-by-count":357,"title":["Carbon Monoxide Expedites Metabolic Exhaustion to Inhibit Tumor Growth"],"prefix":"10.1158","volume":"73","author":[{"given":"Barbara","family":"Wegiel","sequence":"first","affiliation":[{"name":"Authors' Affiliations:\u20081Department of Surgery, Transplant Institute, 2Department of Medicine, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts; 3Department of Clinical Sciences, Section of Urological Cancers, 4School of Life and Health Sciences, Aston University, Aston Triangle, Birmingham, United Kingdom; 5Department of Laboratory Medicine, University Hospital Malm\u00f6, Lund University, Malm\u00f6, Sweden; and 6Department of Medicine and Vascular Biology Center, University of Minnesota, Minneapolis, Alfama Inc., Oeiras, Portugal"}]},{"given":"David","family":"Gallo","sequence":"additional","affiliation":[{"name":"Authors' Affiliations:\u20081Department of Surgery, Transplant Institute, 2Department of Medicine, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts; 3Department of Clinical Sciences, Section of Urological Cancers, 4School of Life and Health Sciences, Aston University, Aston Triangle, Birmingham, United Kingdom; 5Department of Laboratory Medicine, University Hospital Malm\u00f6, Lund University, Malm\u00f6, Sweden; and 6Department of Medicine and Vascular Biology Center, University of Minnesota, Minneapolis, Alfama Inc., Oeiras, Portugal"}]},{"given":"Eva","family":"Csizmadia","sequence":"additional","affiliation":[{"name":"Authors' Affiliations:\u20081Department of Surgery, Transplant Institute, 2Department of Medicine, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts; 3Department of Clinical Sciences, Section of Urological Cancers, 4School of Life and Health Sciences, Aston University, Aston Triangle, Birmingham, United Kingdom; 5Department of Laboratory Medicine, University Hospital Malm\u00f6, Lund University, Malm\u00f6, Sweden; and 6Department of Medicine and Vascular Biology Center, University of Minnesota, Minneapolis, Alfama Inc., Oeiras, Portugal"}]},{"given":"Clair","family":"Harris","sequence":"additional","affiliation":[{"name":"Authors' Affiliations:\u20081Department of Surgery, Transplant Institute, 2Department of Medicine, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts; 3Department of Clinical Sciences, Section of Urological Cancers, 4School of Life and Health Sciences, Aston University, Aston Triangle, Birmingham, United Kingdom; 5Department of Laboratory Medicine, University Hospital Malm\u00f6, Lund University, Malm\u00f6, Sweden; and 6Department of Medicine and Vascular Biology Center, University of Minnesota, Minneapolis, Alfama Inc., Oeiras, Portugal"}]},{"given":"John","family":"Belcher","sequence":"additional","affiliation":[{"name":"Authors' Affiliations:\u20081Department of Surgery, Transplant Institute, 2Department of Medicine, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts; 3Department of Clinical Sciences, Section of Urological Cancers, 4School of Life and Health Sciences, Aston University, Aston Triangle, Birmingham, United Kingdom; 5Department of Laboratory Medicine, University Hospital Malm\u00f6, Lund University, Malm\u00f6, Sweden; and 6Department of Medicine and Vascular Biology Center, University of Minnesota, Minneapolis, Alfama Inc., Oeiras, Portugal"}]},{"given":"Gregory M.","family":"Vercellotti","sequence":"additional","affiliation":[{"name":"Authors' Affiliations:\u20081Department of Surgery, Transplant Institute, 2Department of Medicine, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts; 3Department of Clinical Sciences, Section of Urological Cancers, 4School of Life and Health Sciences, Aston University, Aston Triangle, Birmingham, United Kingdom; 5Department of Laboratory Medicine, University Hospital Malm\u00f6, Lund University, Malm\u00f6, Sweden; and 6Department of Medicine and Vascular Biology Center, University of Minnesota, Minneapolis, Alfama Inc., Oeiras, Portugal"}]},{"given":"Nuno","family":"Penacho","sequence":"additional","affiliation":[{"name":"Authors' Affiliations:\u20081Department of Surgery, Transplant Institute, 2Department of Medicine, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts; 3Department of Clinical Sciences, Section of Urological Cancers, 4School of Life and Health Sciences, Aston University, Aston Triangle, Birmingham, United Kingdom; 5Department of Laboratory Medicine, University Hospital Malm\u00f6, Lund University, Malm\u00f6, Sweden; and 6Department of Medicine and Vascular Biology Center, University of Minnesota, Minneapolis, Alfama Inc., Oeiras, Portugal"}]},{"given":"Pankaj","family":"Seth","sequence":"additional","affiliation":[{"name":"Authors' Affiliations:\u20081Department of Surgery, Transplant Institute, 2Department of Medicine, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts; 3Department of Clinical Sciences, Section of Urological Cancers, 4School of Life and Health Sciences, Aston University, Aston Triangle, Birmingham, United Kingdom; 5Department of Laboratory Medicine, University Hospital Malm\u00f6, Lund University, Malm\u00f6, Sweden; and 6Department of Medicine and Vascular Biology Center, University of Minnesota, Minneapolis, Alfama Inc., Oeiras, Portugal"}]},{"given":"Vikas","family":"Sukhatme","sequence":"additional","affiliation":[{"name":"Authors' Affiliations:\u20081Department of Surgery, Transplant Institute, 2Department of Medicine, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts; 3Department of Clinical Sciences, Section of Urological Cancers, 4School of Life and Health Sciences, Aston University, Aston Triangle, Birmingham, United Kingdom; 5Department of Laboratory Medicine, University Hospital Malm\u00f6, Lund University, Malm\u00f6, Sweden; and 6Department of Medicine and Vascular Biology Center, University of Minnesota, Minneapolis, Alfama Inc., Oeiras, Portugal"}]},{"given":"Asif","family":"Ahmed","sequence":"additional","affiliation":[{"name":"Authors' Affiliations:\u20081Department of Surgery, Transplant Institute, 2Department of Medicine, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts; 3Department of Clinical Sciences, Section of Urological Cancers, 4School of Life and Health Sciences, Aston University, Aston Triangle, Birmingham, United Kingdom; 5Department of Laboratory Medicine, University Hospital Malm\u00f6, Lund University, Malm\u00f6, Sweden; and 6Department of Medicine and Vascular Biology Center, University of Minnesota, Minneapolis, Alfama Inc., Oeiras, Portugal"}]},{"given":"Pier Paolo","family":"Pandolfi","sequence":"additional","affiliation":[{"name":"Authors' Affiliations:\u20081Department of Surgery, Transplant Institute, 2Department of Medicine, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts; 3Department of Clinical Sciences, Section of Urological Cancers, 4School of Life and Health Sciences, Aston University, Aston Triangle, Birmingham, United Kingdom; 5Department of Laboratory Medicine, University Hospital Malm\u00f6, Lund University, Malm\u00f6, Sweden; and 6Department of Medicine and Vascular Biology Center, University of Minnesota, Minneapolis, Alfama Inc., Oeiras, Portugal"}]},{"given":"Leszek","family":"Helczynski","sequence":"additional","affiliation":[{"name":"Authors' Affiliations:\u20081Department of Surgery, Transplant Institute, 2Department of Medicine, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts; 3Department of Clinical Sciences, Section of Urological Cancers, 4School of Life and Health Sciences, Aston University, Aston Triangle, Birmingham, United Kingdom; 5Department of Laboratory Medicine, University Hospital Malm\u00f6, Lund University, Malm\u00f6, Sweden; and 6Department of Medicine and Vascular Biology Center, University of Minnesota, Minneapolis, Alfama Inc., Oeiras, Portugal"}]},{"given":"Anders","family":"Bjartell","sequence":"additional","affiliation":[{"name":"Authors' Affiliations:\u20081Department of Surgery, Transplant Institute, 2Department of Medicine, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts; 3Department of Clinical Sciences, Section of Urological Cancers, 4School of Life and Health Sciences, Aston University, Aston Triangle, Birmingham, United Kingdom; 5Department of Laboratory Medicine, University Hospital Malm\u00f6, Lund University, Malm\u00f6, Sweden; and 6Department of Medicine and Vascular Biology Center, University of Minnesota, Minneapolis, Alfama Inc., Oeiras, Portugal"}]},{"given":"Jenny Liao","family":"Persson","sequence":"additional","affiliation":[{"name":"Authors' Affiliations:\u20081Department of Surgery, Transplant Institute, 2Department of Medicine, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts; 3Department of Clinical Sciences, Section of Urological Cancers, 4School of Life and Health Sciences, Aston University, Aston Triangle, Birmingham, United Kingdom; 5Department of Laboratory Medicine, University Hospital Malm\u00f6, Lund University, Malm\u00f6, Sweden; and 6Department of Medicine and Vascular Biology Center, University of Minnesota, Minneapolis, Alfama Inc., Oeiras, Portugal"}]},{"given":"Leo E.","family":"Otterbein","sequence":"additional","affiliation":[{"name":"Authors' Affiliations:\u20081Department of Surgery, Transplant Institute, 2Department of Medicine, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts; 3Department of Clinical Sciences, Section of Urological Cancers, 4School of Life and Health Sciences, Aston University, Aston Triangle, Birmingham, United Kingdom; 5Department of Laboratory Medicine, University Hospital Malm\u00f6, Lund University, Malm\u00f6, Sweden; and 6Department of Medicine and Vascular Biology Center, University of Minnesota, Minneapolis, Alfama Inc., Oeiras, Portugal"}]}],"member":"1086","published-online":{"date-parts":[[2013,12,1]]},"reference":[{"key":"2022061703524793400_bib1","doi-asserted-by":"crossref","first-page":"225","DOI":"10.3322\/caac.20006","article-title":"Cancer statistics, 2009","volume":"59","author":"Jemal","year":"2009","journal-title":"CA Cancer J Clin"},{"key":"2022061703524793400_bib2","doi-asserted-by":"crossref","first-page":"112","DOI":"10.1186\/1471-2407-6-112","article-title":"Non-hormonal systemic therapy in men with hormone-refractory prostate cancer and metastases: a systematic review from the Cancer Care Ontario Program in Evidence-based Care's Genitourinary Cancer Disease Site Group","volume":"6","author":"Winquist","year":"2006","journal-title":"BMC Cancer"},{"key":"2022061703524793400_bib3","doi-asserted-by":"crossref","first-page":"1340","DOI":"10.1126\/science.1193494","article-title":"The control of the metabolic switch in cancers by oncogenes and tumor suppressor genes","volume":"330","author":"Levine","year":"2010","journal-title":"Science"},{"key":"2022061703524793400_bib4","doi-asserted-by":"crossref","first-page":"575","DOI":"10.1126\/science.61.1588.575","article-title":"Iron, the oxygen-carrier of respiration-ferment","volume":"61","author":"Warburg","year":"1925","journal-title":"Science"},{"key":"2022061703524793400_bib5","doi-asserted-by":"crossref","first-page":"610","DOI":"10.1038\/nature08802","article-title":"Heteroplasmic mitochondrial DNA mutations in normal and tumour cells","volume":"464","author":"He","year":"2010","journal-title":"Nature"},{"key":"2022061703524793400_bib6","doi-asserted-by":"crossref","first-page":"567","DOI":"10.1093\/carcin\/bgq012","article-title":"Selection of cancer cells with repressed mitochondria triggers colon cancer progression","volume":"31","author":"Sanchez-Arago","year":"2010","journal-title":"Carcinogenesis"},{"key":"2022061703524793400_bib7","first-page":"1141","article-title":"Role of superoxide dismutase in cancer: a review","volume":"39","author":"Oberley","year":"1979","journal-title":"Cancer Res"},{"key":"2022061703524793400_bib8","first-page":"3686","article-title":"Superoxide dismutase and superoxide radical in Morris hepatomas","volume":"40","author":"Bize","year":"1980","journal-title":"Cancer Res"},{"key":"2022061703524793400_bib9","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1111\/j.1749-6632.2000.tb06199.x","article-title":"Glucose deprivation-induced oxidative stress in human tumor cells. 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