{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,18]],"date-time":"2026-01-18T07:41:23Z","timestamp":1768722083257,"version":"3.49.0"},"reference-count":53,"publisher":"Ovid Technologies (Wolters Kluwer Health)","issue":"4","content-domain":{"domain":["ahajournals.org"],"crossmark-restriction":true},"short-container-title":["Circ Cardiovasc Genet"],"published-print":{"date-parts":[[2014,8]]},"abstract":"\n Background\u2014<\/jats:title>\n \n Low levels of high-density lipoprotein (HDL) cholesterol constitutes a major risk factor for atherosclerosis. Recent studies from our group reported a genetic association between the WW domain-containing oxidoreductase (\n WWOX<\/jats:italic>\n ) gene and HDL cholesterol levels. Here, through next-generation resequencing, in vivo functional studies and gene microarray analyses, we investigated the role of\n WWOX<\/jats:italic>\n in HDL and lipid metabolism.\n <\/jats:p>\n <\/jats:sec>\n \n Methods and Results\u2014<\/jats:title>\n \n Using next-generation resequencing of the\n WWOX<\/jats:italic>\n region, we first identified 8 variants significantly associated and perfectly segregating with the low-HDL trait in 2 multigenerational French Canadian dyslipidemic families. To understand in vivo functions of WWOX, we used liver-specific\n Wwox<\/jats:italic>\n \n hep\u2212\/\u2212<\/jats:italic>\n <\/jats:sup>\n and total\n Wwox<\/jats:italic>\n \u2212\/\u2212<\/jats:sup>\n mice models, where we found decreased ApoA-I and Abca1 levels in hepatic tissues. Analyses of lipoprotein profiles in\n Wwox<\/jats:italic>\n \u2212\/\u2212<\/jats:sup>\n , but not\n Wwox<\/jats:italic>\n \n hep\u2212\/\u2212<\/jats:italic>\n <\/jats:sup>\n littermates, also showed marked reductions in serum HDL cholesterol concentrations, concordant with the low-HDL findings observed in families. We next obtained evidence of a sex-specific effect in female\n Wwox<\/jats:italic>\n \n hep\u2212\/\u2212<\/jats:italic>\n <\/jats:sup>\n mice, where microarray analyses revealed an increase in plasma triglycerides and altered lipid metabolic pathways. We further identified a significant reduction in\n ApoA-I<\/jats:italic>\n and Lpl and an upregulation in\n Fas<\/jats:italic>\n ,\n Angptl4<\/jats:italic>\n , and\n Lipg<\/jats:italic>\n , suggesting that the effects of Wwox involve multiple pathways, including cholesterol homeostasis, ApoA-I\/ABCA1 pathway, and fatty acid biosynthesis\/triglyceride metabolism.\n <\/jats:p>\n <\/jats:sec>\n \n Conclusions\u2014<\/jats:title>\n \n Our data indicate that\n WWOX<\/jats:italic>\n disruption alters HDL and lipoprotein metabolism through several mechanisms and may account for the low-HDL phenotype observed in families expressing the\n WWOX<\/jats:italic>\n variants. These findings thus describe a novel gene involved in cellular lipid homeostasis, which effects may impact atherosclerotic disease development.\n <\/jats:p>\n <\/jats:sec>","DOI":"10.1161\/circgenetics.113.000248","type":"journal-article","created":{"date-parts":[[2014,5,29]],"date-time":"2014-05-29T05:42:36Z","timestamp":1401342156000},"page":"491-504","update-policy":"https:\/\/doi.org\/10.1161\/crossmarkpolicy","source":"Crossref","is-referenced-by-count":42,"title":["The\n WWOX<\/i>\n Gene Modulates High-Density Lipoprotein and Lipid Metabolism"],"prefix":"10.1161","volume":"7","author":[{"given":"Iulia","family":"Iatan","sequence":"first","affiliation":[{"name":"From the Cardiovascular Research Laboratories, Department of Biochemistry, Faculty of Medicine, Division of Cardiology, McGill University, Royal Victoria Hospital, Montreal, Quebec, Canada (I.I., H.Y.C., I.R., Z.A., J.G.); Department of Human Genetics (M.V.P.L.R., D.W.-V., E.N., P.P.) and Department of Medicine (M.V.P.L.R., D.W.-V., E.N., P.P.), David Geffen School of Medicine at University of California at Los Angeles; Department of Molecular Carcinogenesis, University of Texas MD Anderson Cancer..."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hong Y.","family":"Choi","sequence":"additional","affiliation":[{"name":"From the Cardiovascular Research Laboratories, Department of Biochemistry, Faculty of Medicine, Division of Cardiology, McGill University, Royal Victoria Hospital, Montreal, Quebec, Canada (I.I., H.Y.C., I.R., Z.A., J.G.); Department of Human Genetics (M.V.P.L.R., D.W.-V., E.N., P.P.) and Department of Medicine (M.V.P.L.R., D.W.-V., E.N., P.P.), David Geffen School of Medicine at University of California at Los Angeles; Department of Molecular Carcinogenesis, University of Texas MD Anderson Cancer..."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Isabelle","family":"Ruel","sequence":"additional","affiliation":[{"name":"From the Cardiovascular Research Laboratories, Department of Biochemistry, Faculty of Medicine, Division of Cardiology, McGill University, Royal Victoria Hospital, Montreal, Quebec, Canada (I.I., H.Y.C., I.R., Z.A., J.G.); Department of Human Genetics (M.V.P.L.R., D.W.-V., E.N., P.P.) and Department of Medicine (M.V.P.L.R., D.W.-V., E.N., P.P.), David Geffen School of Medicine at University of California at Los Angeles; Department of Molecular Carcinogenesis, University of Texas MD Anderson Cancer..."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"M.V. Prasad Linga","family":"Reddy","sequence":"additional","affiliation":[{"name":"From the Cardiovascular Research Laboratories, Department of Biochemistry, Faculty of Medicine, Division of Cardiology, McGill University, Royal Victoria Hospital, Montreal, Quebec, Canada (I.I., H.Y.C., I.R., Z.A., J.G.); Department of Human Genetics (M.V.P.L.R., D.W.-V., E.N., P.P.) and Department of Medicine (M.V.P.L.R., D.W.-V., E.N., P.P.), David Geffen School of Medicine at University of California at Los Angeles; Department of Molecular Carcinogenesis, University of Texas MD Anderson Cancer..."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hyunsuk","family":"Kil","sequence":"additional","affiliation":[{"name":"From the Cardiovascular Research Laboratories, Department of Biochemistry, Faculty of Medicine, Division of Cardiology, McGill University, Royal Victoria Hospital, Montreal, Quebec, Canada (I.I., H.Y.C., I.R., Z.A., J.G.); Department of Human Genetics (M.V.P.L.R., D.W.-V., E.N., P.P.) and Department of Medicine (M.V.P.L.R., D.W.-V., E.N., P.P.), David Geffen School of Medicine at University of California at Los Angeles; Department of Molecular Carcinogenesis, University of Texas MD Anderson Cancer..."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jaeho","family":"Lee","sequence":"additional","affiliation":[{"name":"From the Cardiovascular Research Laboratories, Department of Biochemistry, Faculty of Medicine, Division of Cardiology, McGill University, Royal Victoria Hospital, Montreal, Quebec, Canada (I.I., H.Y.C., I.R., Z.A., J.G.); Department of Human Genetics (M.V.P.L.R., D.W.-V., E.N., P.P.) and Department of Medicine (M.V.P.L.R., D.W.-V., E.N., P.P.), David Geffen School of Medicine at University of California at Los Angeles; Department of Molecular Carcinogenesis, University of Texas MD Anderson Cancer..."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mohammad Abu","family":"Odeh","sequence":"additional","affiliation":[{"name":"From the Cardiovascular Research Laboratories, Department of Biochemistry, Faculty of Medicine, Division of Cardiology, McGill University, Royal Victoria Hospital, Montreal, Quebec, Canada (I.I., H.Y.C., I.R., Z.A., J.G.); Department of Human Genetics (M.V.P.L.R., D.W.-V., E.N., P.P.) and Department of Medicine (M.V.P.L.R., D.W.-V., E.N., P.P.), David Geffen School of Medicine at University of California at Los Angeles; Department of Molecular Carcinogenesis, University of Texas MD Anderson Cancer..."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Zaidoun","family":"Salah","sequence":"additional","affiliation":[{"name":"From the Cardiovascular Research Laboratories, Department of Biochemistry, Faculty of Medicine, Division of Cardiology, McGill University, Royal Victoria Hospital, Montreal, Quebec, Canada (I.I., H.Y.C., I.R., Z.A., J.G.); Department of Human Genetics (M.V.P.L.R., D.W.-V., E.N., P.P.) and Department of Medicine (M.V.P.L.R., D.W.-V., E.N., P.P.), David Geffen School of Medicine at University of California at Los Angeles; Department of Molecular Carcinogenesis, University of Texas MD Anderson Cancer..."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Muhannad","family":"Abu-Remaileh","sequence":"additional","affiliation":[{"name":"From the Cardiovascular Research Laboratories, Department of Biochemistry, Faculty of Medicine, Division of Cardiology, McGill University, Royal Victoria Hospital, Montreal, Quebec, Canada (I.I., H.Y.C., I.R., Z.A., J.G.); Department of Human Genetics (M.V.P.L.R., D.W.-V., E.N., P.P.) and Department of Medicine (M.V.P.L.R., D.W.-V., E.N., P.P.), David Geffen School of Medicine at University of California at Los Angeles; Department of Molecular Carcinogenesis, University of Texas MD Anderson Cancer..."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Daphna","family":"Weissglas-Volkov","sequence":"additional","affiliation":[{"name":"From the Cardiovascular Research Laboratories, Department of Biochemistry, Faculty of Medicine, Division of Cardiology, McGill University, Royal Victoria Hospital, Montreal, Quebec, Canada (I.I., H.Y.C., I.R., Z.A., J.G.); Department of Human Genetics (M.V.P.L.R., D.W.-V., E.N., P.P.) and Department of Medicine (M.V.P.L.R., D.W.-V., E.N., P.P.), David Geffen School of Medicine at University of California at Los Angeles; Department of Molecular Carcinogenesis, University of Texas MD Anderson Cancer..."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Elina","family":"Nikkola","sequence":"additional","affiliation":[{"name":"From the Cardiovascular Research Laboratories, Department of Biochemistry, Faculty of Medicine, Division of Cardiology, McGill University, Royal Victoria Hospital, Montreal, Quebec, Canada (I.I., H.Y.C., I.R., Z.A., J.G.); Department of Human Genetics (M.V.P.L.R., D.W.-V., E.N., P.P.) and Department of Medicine (M.V.P.L.R., D.W.-V., E.N., P.P.), David Geffen School of Medicine at University of California at Los Angeles; Department of Molecular Carcinogenesis, University of Texas MD Anderson Cancer..."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mete","family":"Civelek","sequence":"additional","affiliation":[{"name":"From the Cardiovascular Research Laboratories, Department of Biochemistry, Faculty of Medicine, Division of Cardiology, McGill University, Royal Victoria Hospital, Montreal, Quebec, Canada (I.I., H.Y.C., I.R., Z.A., J.G.); Department of Human Genetics (M.V.P.L.R., D.W.-V., E.N., P.P.) and Department of Medicine (M.V.P.L.R., D.W.-V., E.N., P.P.), David Geffen School of Medicine at University of California at Los Angeles; Department of Molecular Carcinogenesis, University of Texas MD Anderson Cancer..."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Zuhier","family":"Awan","sequence":"additional","affiliation":[{"name":"From the Cardiovascular Research Laboratories, Department of Biochemistry, Faculty of Medicine, Division of Cardiology, McGill University, Royal Victoria Hospital, Montreal, Quebec, Canada (I.I., H.Y.C., I.R., Z.A., J.G.); Department of Human Genetics (M.V.P.L.R., D.W.-V., E.N., P.P.) and Department of Medicine (M.V.P.L.R., D.W.-V., E.N., P.P.), David Geffen School of Medicine at University of California at Los Angeles; Department of Molecular Carcinogenesis, University of Texas MD Anderson Cancer..."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Carlo M.","family":"Croce","sequence":"additional","affiliation":[{"name":"From the Cardiovascular Research Laboratories, Department of Biochemistry, Faculty of Medicine, Division of Cardiology, McGill University, Royal Victoria Hospital, Montreal, Quebec, Canada (I.I., H.Y.C., I.R., Z.A., J.G.); Department of Human Genetics (M.V.P.L.R., D.W.-V., E.N., P.P.) and Department of Medicine (M.V.P.L.R., D.W.-V., E.N., P.P.), David Geffen School of Medicine at University of California at Los Angeles; Department of Molecular Carcinogenesis, University of Texas MD Anderson Cancer..."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Rami I.","family":"Aqeilan","sequence":"additional","affiliation":[{"name":"From the Cardiovascular Research Laboratories, Department of Biochemistry, Faculty of Medicine, Division of Cardiology, McGill University, Royal Victoria Hospital, Montreal, Quebec, Canada (I.I., H.Y.C., I.R., Z.A., J.G.); Department of Human Genetics (M.V.P.L.R., D.W.-V., E.N., P.P.) and Department of Medicine (M.V.P.L.R., D.W.-V., E.N., P.P.), David Geffen School of Medicine at University of California at Los Angeles; Department of Molecular Carcinogenesis, University of Texas MD Anderson Cancer..."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"P\u00e4ivi","family":"Pajukanta","sequence":"additional","affiliation":[{"name":"From the Cardiovascular Research Laboratories, Department of Biochemistry, Faculty of Medicine, Division of Cardiology, McGill University, Royal Victoria Hospital, Montreal, Quebec, Canada (I.I., H.Y.C., I.R., Z.A., J.G.); Department of Human Genetics (M.V.P.L.R., D.W.-V., E.N., P.P.) and Department of Medicine (M.V.P.L.R., D.W.-V., E.N., P.P.), David Geffen School of Medicine at University of California at Los Angeles; Department of Molecular Carcinogenesis, University of Texas MD Anderson Cancer..."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"C. Marcelo","family":"Aldaz","sequence":"additional","affiliation":[{"name":"From the Cardiovascular Research Laboratories, Department of Biochemistry, Faculty of Medicine, Division of Cardiology, McGill University, Royal Victoria Hospital, Montreal, Quebec, Canada (I.I., H.Y.C., I.R., Z.A., J.G.); Department of Human Genetics (M.V.P.L.R., D.W.-V., E.N., P.P.) and Department of Medicine (M.V.P.L.R., D.W.-V., E.N., P.P.), David Geffen School of Medicine at University of California at Los Angeles; Department of Molecular Carcinogenesis, University of Texas MD Anderson Cancer..."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jacques","family":"Genest","sequence":"additional","affiliation":[{"name":"From the Cardiovascular Research Laboratories, Department of Biochemistry, Faculty of Medicine, Division of Cardiology, McGill University, Royal Victoria Hospital, Montreal, Quebec, Canada (I.I., H.Y.C., I.R., Z.A., J.G.); Department of Human Genetics (M.V.P.L.R., D.W.-V., E.N., P.P.) and Department of Medicine (M.V.P.L.R., D.W.-V., E.N., P.P.), David Geffen School of Medicine at University of California at Los Angeles; Department of Molecular Carcinogenesis, University of Texas MD Anderson Cancer..."}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"276","reference":[{"key":"e_1_3_4_2_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0140-6736(04)17018-9"},{"key":"e_1_3_4_3_2","doi-asserted-by":"publisher","DOI":"10.1056\/NEJM199304223281603"},{"key":"e_1_3_4_4_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.ajhg.2008.07.002"},{"key":"e_1_3_4_5_2","doi-asserted-by":"publisher","DOI":"10.1194\/jlr.M009175"},{"key":"e_1_3_4_6_2","doi-asserted-by":"publisher","DOI":"10.1038\/ng.76"},{"key":"e_1_3_4_7_2","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2350-11-148"},{"key":"e_1_3_4_8_2","doi-asserted-by":"publisher","DOI":"10.1001\/jama.2009.978-a"},{"key":"e_1_3_4_9_2","first-page":"2140","article-title":"WWOX, a novel WW domain-containing protein mapping to human chromosome 16q23.3-24.1, a region frequently affected in breast cancer.","volume":"60","author":"Bednarek AK","year":"2000","unstructured":"Bednarek AK, Laflin KJ, Daniel RL, Liao Q, Hawkins KA, Aldaz CM. WWOX, a novel WW domain-containing protein mapping to human chromosome 16q23.3-24.1, a region frequently affected in breast cancer. Cancer Res. 2000;60:2140\u20132145.","journal-title":"Cancer Res"},{"key":"e_1_3_4_10_2","doi-asserted-by":"publisher","DOI":"10.1093\/hmg\/9.11.1651"},{"key":"e_1_3_4_11_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0609783104"},{"key":"e_1_3_4_12_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0007775"},{"key":"e_1_3_4_13_2","first-page":"585","article-title":"Role of the WWOX tumor suppressor gene in bone homeostasis and the pathogenesis of osteosarcoma.","volume":"1","author":"Del Mare S","year":"2011","unstructured":"Del Mare S, Kurek KC, Stein GS, Lian JB, Aqeilan RI. Role of the WWOX tumor suppressor gene in bone homeostasis and the pathogenesis of osteosarcoma. 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