Genetic Variation in HSD17B13 Reduces the Risk of Developing Cirrhosis and Hepatocellular Carcinoma in Alcohol Misusers.


Journal

Hepatology (Baltimore, Md.)
ISSN: 1527-3350
Titre abrégé: Hepatology
Pays: United States
ID NLM: 8302946

Informations de publication

Date de publication:
07 2020
Historique:
received: 19 08 2019
accepted: 18 09 2019
pubmed: 21 10 2019
medline: 7 5 2021
entrez: 21 10 2019
Statut: ppublish

Résumé

Carriage of rs738409:G in patatin-like phospholipase domain containing 3 (PNPLA3) is associated with an increased risk for developing alcohol-related cirrhosis and hepatocellular carcinoma (HCC). Recently, rs72613567:TA in hydroxysteroid 17-beta dehydrogenase 13 (HSD17B13) was shown to be associated with a reduced risk for developing alcohol-related liver disease and to attenuate the risk associated with carriage of PNPLA3 rs738409:G. This study explores the risk associations between these two genetic variants and the development of alcohol-related cirrhosis and HCC. Variants in HSD17B13 and PNPLA3 were genotyped in 6,171 participants, including 1,031 with alcohol-related cirrhosis and HCC, 1,653 with alcohol-related cirrhosis without HCC, 2,588 alcohol misusers with no liver disease, and 899 healthy controls. Genetic associations with the risks for developing alcohol-related cirrhosis and HCC were determined using logistic regression analysis. Carriage of HSD17B13 rs72613567:TA was associated with a lower risk for developing both cirrhosis (odds ratio [OR], 0.79; 95% confidence interval [CI], 0.72-0.88; P = 8.13 × 10 Carriage of variants in PNPLA3 and HSD17B13 differentially affect the risk for developing advanced alcohol-related liver disease. A genotypic/phenotypic risk score might facilitate earlier diagnosis of HCC in this population.

Sections du résumé

BACKGROUND AND AIMS
Carriage of rs738409:G in patatin-like phospholipase domain containing 3 (PNPLA3) is associated with an increased risk for developing alcohol-related cirrhosis and hepatocellular carcinoma (HCC). Recently, rs72613567:TA in hydroxysteroid 17-beta dehydrogenase 13 (HSD17B13) was shown to be associated with a reduced risk for developing alcohol-related liver disease and to attenuate the risk associated with carriage of PNPLA3 rs738409:G. This study explores the risk associations between these two genetic variants and the development of alcohol-related cirrhosis and HCC.
APPROACH AND RESULTS
Variants in HSD17B13 and PNPLA3 were genotyped in 6,171 participants, including 1,031 with alcohol-related cirrhosis and HCC, 1,653 with alcohol-related cirrhosis without HCC, 2,588 alcohol misusers with no liver disease, and 899 healthy controls. Genetic associations with the risks for developing alcohol-related cirrhosis and HCC were determined using logistic regression analysis. Carriage of HSD17B13 rs72613567:TA was associated with a lower risk for developing both cirrhosis (odds ratio [OR], 0.79; 95% confidence interval [CI], 0.72-0.88; P = 8.13 × 10
CONCLUSIONS
Carriage of variants in PNPLA3 and HSD17B13 differentially affect the risk for developing advanced alcohol-related liver disease. A genotypic/phenotypic risk score might facilitate earlier diagnosis of HCC in this population.

Identifiants

pubmed: 31630428
doi: 10.1002/hep.30996
doi:

Substances chimiques

17-Hydroxysteroid Dehydrogenases EC 1.1.-
HSD17B13 protein, human EC 1.1.-.-

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

88-102

Informations de copyright

© 2019 by the American Association for the Study of Liver Diseases.

Références

Singal AK, Bataller R, Ahn J, Ahn J, Kamath PS, Shah VH. ACG clinical guideline: alcoholic liver disease. Am J Gastroenterology 2018;113:175-194.
Asrani SK, Devarbhavi H, Eaton J, Kamath PS. Burden of liver diseases in the world. J Hepatol 2019;70:151-171.
Rehm J, Samokhvalov AV, Shield KD. Global burden of alcoholic liver diseases. J Hepatol 2013;59:160-168.
Burra P, Senzolo M, Adam R, Delvart V, Karam V, Germani G. et al.; for ELITA and on behalf of ELTR Liver Transplant Centers. Liver transplantation for alcoholic liver disease in Europe: a study from the ELTR (European Liver Transplant Registry). Am J Transplant 2010;10:138-148.
Parker R, Aithal GP, Becker U, Gleeson D, Masson S, Wyatt JI, Rowe IA; WALDO study group. Natural history of histologically proven alcohol-related liver disease: a systematic review. J Hepatol 2019;71:586-593.
Leevy CM. Cirrhosis in alcoholics. Med Clin North Am 1968;52:1445-1455.
Teli MR, Day CP, Burt AD, Bennett MK, James OF. Determinants of progression to cirrhosis or fibrosis in pure alcoholic fatty liver. Lancet 1995;346:987-990.
Kodama K, Tokushige K, Hashimoto E, Taniai M, Shiratori K. Hepatic and extrahepatic malignancies in cirrhosis caused by nonalcoholic steatohepatitis and alcoholic liver disease. Alcohol Clin Exp Res 2013;37:E247-E252.
Mancebo A, González-Diéguez ML, Cadahía V, Varela M, Pérez R, Navascués CA, et al. Annual incidence of hepatocellular carcinoma among patients with alcoholic cirrhosis and identification of risk groups. Clin Gastroenterol Hepatol 2013;11:95-101.
Ganne-Carrié N, Chaffaut C, Bourcier V, Archambeaud I, Perarnau JM, Oberti F, et al. Estimate of hepatocellular carcinoma incidence in patients with alcoholic cirrhosis. J Hepatol 2018;69:1274-1283.
Ganne-Carrié N, Nahon P. Hepatocellular carcinoma in the setting of alcohol-related liver disease. J Hepatol 2019;70:284-293.
Kim D, Li AA, Perumpail BJ, Gadiparthi C, Kim W, Cholankeril G, et al. Changing trends in etiology- and ethnicity-based annual mortality rates of cirrhosis and hepatocellular carcinoma in the United States. Hepatology 2019;69:1064-1074.
Stickel F, Moreno C, Hampe J, Morgan MY. Genetics of alcohol dependence and alcohol-related liver disease. J Hepatol 2017;66:195-211.
Stickel F, Buch S, Lau K,Meyer zu Schwabedissen H, Berg T, Ridinger M, et al. Genetic variation in the PNPLA3 gene is associated with alcoholic liver injury in Caucasians. Hepatology 2011;53:86-95.
Chamorro AJ, Torres JL, Mirón-Canelo JA, González-Sarmiento R, Laso FJ, Marcos M. Systematic review with meta-analysis: the I148M variant of patatin-like phospholipase domain-containing 3 gene (PNPLA3) is significantly associated with alcoholic liver cirrhosis. Aliment Pharmacol Ther 2014;40:571-581.
Singal AG, Manjunath H, Yopp AC, Beg MS, Marrero JA, Gopal P, et al. The effect of PNPLA3 on fibrosis progression and development of hepatocellular carcinoma: a meta-analysis. Am J Gastroenterol 2014;109:325-334.
Trépo E, Nahon P, Bontempi G, Valenti L, Falleti E, Nischalke HD, et al. Association between the PNPLA3 (rs738409 C>G) variant and hepatocellular carcinoma: evidence from a meta-analysis of individual participant data. Hepatology 2014;59:2170-2177.
Stickel F, Buch S, Nischalke HD, Weiss KH, Gotthardt D, Fischer J, et al. Genetic variants in PNPLA3 and TM6SF2 predispose to the development of hepatocellular carcinoma in individuals with alcohol-related cirrhosis. Am J Gastroenterol 2018;113:1475-1483.
Buch S, Stickel F, Trépo E, Way M, Herrmann A, Nischalke HD, et al. A two-stage genome-wide association study confirms PNPLA3 and identifies TM6SF2 and MBOAT7 as novel risk loci for alcohol-related cirrhosis. Nat Genet 2015;47:1443-1448.
Abul-Husn NS, Cheng X, Li AH, Xin Y, Schurmann C, Stevis P, et al. A protein-truncating HSD17B13 variant and protection from chronic liver disease. N Engl J Med 2018;378:1096-1106.
Yang J, Trépo E, Nahon P, Cao Q, Moreno C, Letouzé E, et al. A 17-beta-hydroxysteroid dehydrogenase 13 variant protects from hepatocellular carcinoma development in alcoholic liver disease. Hepatology 2019;70:231-240.
European Association for the Study of the Liver. EASL Clinical Practice Guidelines: management of hepatocellular carcinoma. J Hepatol 2018;69:182-236.
Pugh RN, Murray-Lyon IM, Dawson JL, Pietroni MC, Williams R. Transection of the oesophagus for bleeding oesophageal varices. Br J Surg 1973;60:646-649.
American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. 4th ed. Washington, DC: American Psychiatric Press; 1994.
Witte JS, Visscher PM, Wray NR. The contribution of genetic variants to disease depends on the ruler. Nat Rev Genet 2014;15:765-776.
Anderson CA, Pettersson FH, Clarke GM, Cardon LR, Morris AP, Zondervan KT. Data quality control in genetic case-control association studies. Nat Protoc 2010;5:1564-1573.
1000 Genomes Project Consortium, Auton A, Brooks LD, Durbin RM, Garrison EP, Kang HM, Korbel JO, et al. A global reference for human genetic variation. Nature 2015;526:68-74.
Li D, Zhao H, Gelernter J. Strong association of the alcohol dehydrogenase 1B gene (ADH1B) with alcohol dependence and alcohol-induced medical diseases. Biol Psychiatry 2011;70:504-512.
Li D, Zhao H, Gelernter J. Strong protective effect of the aldehyde dehydrogenase gene (ALDH2) 504lys (*2) allele against alcoholism and alcohol-induced medical diseases in Asians. Hum Genet 2012;131:725-737.
Lee FI. Cirrhosis and hepatoma in alcoholics. Gut 1966;7:77-85.
Schlichting P, Christensen E, Andersen PK, Fauerholdt L, Juhl E, Poulsen H, et al. Prognostic factors in cirrhosis identified by Cox’s regression model. Hepatology 1983;3:889-995.
D’Amico G, Morabito A, Pagliaro L, Marubini E. Survival and prognostic indicators in compensated and decompensated cirrhosis. Dig Dis Sci 1986;31:468-475.
Ginés P, Quintero E, Arroyo V, Terés J, Bruguera M, Rimola A, et al. Compensated cirrhosis: natural history and prognostic factors. Hepatology 1987;7:122-128.
Meffert PJ, Repp KD, Völzke H, Weiss FU, Homuth G, Kühn JP, et al. The PNPLA3 SNP rs738409: G allele is associated with increased liver disease-associated mortality but reduced overall mortality in a population-based cohort. J Hepatol 2018;68:858-860.
Atkinson SR, Way MJ, McQuillin A, Morgan MY, Thursz MR. Reply to: “The PNPLA3 SNP rs738409: G allele is associated with increased liver disease-associated mortality but reduced overall mortality in a population-based cohort”. J Hepatol 2018;68:860-862.
Ferenci P, Pfeiffenberger J, Stättermayer AF, Stauber RE, Willheim C, Weiss KH, et al. HSD17B13 truncated variant is associated with a mild hepatic phenotype in Wilson’s Disease. JHEP Rep 2019;1:2-8.
Saloniemi T, Jokela H, Strauss L, Pakarinen P, Poutanen M. The diversity of sex steroid action: novel functions of hydroxysteroid (17β) dehydrogenases as revealed by genetically modified mouse models. J Endocrinol 2012;212:27-40.
Su W, Peng J, Li S, Dai YB, Wang CJ, Xu H, et al. Liver X receptor α induces 17β-hydroxysteroid dehydrogenase-13 expression through SREBP-1c. Am J Physiol Endocrinol Metab 2017;312:E357-E367.
Su W, Wang Y, Jia X, Wu W, Li L, Tian X, et al. Comparative proteomic study reveals 17β-HSD13 as a pathogenic protein in nonalcoholic fatty liver disease. Proc Natl Acad Sci USA 2014;111:11437-11442.
Kampf C, Mardinoglu A, Fagerberg L, Hallström BM, Edlund K, Lundberg E, et al. The human liver-specific proteome defined by transcriptomics and antibody-based profiling. FASEB J 2014;28:2901-2914.
Adam M, Heikelä H, Sobolewski C, Portius D, Mäki-Jouppila J, Mehmood A, et al. Hydroxysteroid (17β) dehydrogenase 13 deficiency triggers hepatic steatosis and inflammation in mice. FASEB J 2018;32:3434-3447.
Horiguchi Y, Araki M, Motojima K. 17beta-Hydroxysteroid dehydrogenase type 13 is a liver-specific lipid droplet-associated protein. Biochem Biophys Res Commun 2008;370:235-238.
Ma Y, Belyaeva OV, Brown PM, Fujita K, Valles K, Karki S, et al. 17-beta hydroxysteroid dehydrogenase 13 is a hepatic retinol dehydrogenase associated with histological features of nonalcoholic fatty liver disease. Hepatology 2019;69:1504-1519.
Saeed A, Dullaart RPF, Schreuder TCMA, Blokzijl H, Faber KN. Disturbed vitamin A metabolism in non-alcoholic fatty liver disease (NAFLD). Nutrients 2017;10:29.
Kim SC, Kim CK, Axe D, Cook A, Lee M, Li T, et al. All-trans-retinoic acid ameliorates hepatic steatosis in mice by a novel transcriptional cascade. Hepatology 2014;59:1750-1760.
Wang XD, Liu C, Chung J, Stickel F, Seitz HK, Russell RM. Chronic alcohol intake reduces retinoic acid concentration and enhances AP-1 (c-Jun and c-Fos) expression in rat liver. Hepatology 1998;28:744-750.
Cortes E, Lachowski D, Rice A, Chronopoulos A, Robinson B, Thorpe S, et al. Retinoic acid receptor-β is downregulated in hepatocellular carcinoma and cirrhosis and its expression inhibits myosin-driven activation and durotaxis in hepatic stellate cells. Hepatology 2019;69:785-802.
Muto Y, Moriwaki H, Saito A. Prevention of second primary tumors by an acyclic retinoid in patients with hepatocellular carcinoma. N Engl J Med 1999;340:1046-1047.
Chen J, Zhuo JY, Yang F, Liu ZK, Zhou L, Xie HY, et al. 17-beta-hydroxysteroid dehydrogenase 13 inhibits the progression and recurrence of hepatocellular carcinoma. Hepatobiliary Pancreat Dis Int 2018;17:220-226.
Rotroff DM, Pijut SS, Marvel SW, Jack JR, Havener TM, Pujol A, et al. ACCORD/ACCORDion Investigators. Genetic variants in HSD17B3, SMAD3, and IPO11 impact circulating lipids in response to fenofibrate in individuals with type 2 diabetes. Clin Pharmacol Ther 2018;103:712-721.

Auteurs

Felix Stickel (F)

Department of Gastroenterology and Hepatology, University Hospital of Zürich, Switzerland.

Philipp Lutz (P)

Department of Internal Medicine I, University of Bonn, Bonn, Germany.

Stephan Buch (S)

Medical Department 1, University Hospital Dresden, TU Dresden, Germany.

Hans Dieter Nischalke (HD)

Department of Internal Medicine I, University of Bonn, Bonn, Germany.

Ines Silva (I)

Department of Internal Medicine and Center for Alcohol Research, Salem Medical Center University Hospital Heidelberg, Heidelberg, Germany.

Vanessa Rausch (V)

Department of Internal Medicine and Center for Alcohol Research, Salem Medical Center University Hospital Heidelberg, Heidelberg, Germany.

Janett Fischer (J)

Division of Hepatology, Clinic and Polyclinic for Gastroenterology, Hepatology, Infectiology and Pneumology, University Clinic Leipzig, Leipzig, Germany.

Karl Heinz Weiss (KH)

Department of Internal Medicine IV, Medical University of Heidelberg, Germany.

Daniel Gotthardt (D)

Department of Internal Medicine IV, Medical University of Heidelberg, Germany.

Jonas Rosendahl (J)

Department of Gastroenterology, University Hospital Halle/Saale, Germany.

Astrid Marot (A)

Division of Gastroenterology and Hepatology, Centre Hospitalier Universitaire Vaudois, University of Lausanne, Switzerland.

Mona Elamly (M)

Division of Gastroenterology and Hepatology, Centre Hospitalier Universitaire Vaudois, University of Lausanne, Switzerland.

Marcin Krawczyk (M)

Department of Medicine II, Saarland University Medical Center, Homburg, Germany.
Laboratory of Metabolic Liver Diseases, Department of General, Transplant and Liver Surgery, Centre for Preclinical Research, Medical University of Warsaw, Warsaw, Poland.

Markus Casper (M)

Department of Medicine II, Saarland University Medical Center, Homburg, Germany.

Frank Lammert (F)

Department of Medicine II, Saarland University Medical Center, Homburg, Germany.

Thomas W M Buckley (TWM)

Molecular Psychiatry Laboratory, Division of Psychiatry, University College London, UK.

Andrew McQuillin (A)

Molecular Psychiatry Laboratory, Division of Psychiatry, University College London, UK.

Ulrich Spengler (U)

Department of Internal Medicine I, University of Bonn, Bonn, Germany.

Florian Eyer (F)

Department of Clinical Toxicology, Klinikum Rechts der Isar, Technical University of Munich, Germany.

Arndt Vogel (A)

Department of Gastroenterology, Hepatology and Endocrinology, Hannover Medical School, Germany.

Silke Marhenke (S)

Department of Gastroenterology, Hepatology and Endocrinology, Hannover Medical School, Germany.

Johann von Felden (J)

First Department of Medicine, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Henning Wege (H)

First Department of Medicine, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Rohini Sharma (R)

Department of Metabolism, Digestion & Reproduction, Division of Surgery and Cancer, Imperial College London, London, UK.

Stephen Atkinson (S)

Department of Metabolism, Digestion & Reproduction, Division of Surgery and Cancer, Imperial College London, London, UK.

Andre Franke (A)

Institute of Clinical Molecular Biology, Kiel University, Kiel, Germany.

Sophie Nehring (S)

Medical Department 1, University Hospital Dresden, TU Dresden, Germany.

Vincent Moser (V)

Medical Department 1, University Hospital Dresden, TU Dresden, Germany.

Clemens Schafmayer (C)

Department of Visceral and Thoracic Surgery, Kiel University, Kiel, Germany.

Laurent Spahr (L)

Departments of Gastroenterology and Hepatology, University Hospitals of Geneva and Faculty of Medicine, Geneva, Switzerland.

Carolin Lackner (C)

Institute of Pathology, Medical University of Graz, Austria.

Rudolf E Stauber (RE)

Division of Gastroenterology and Hepatology, Department of Internal Medicine, Medical University of Graz, Austria.

Ali Canbay (A)

Ruhr-Universität Bochum, Universitätsklinikum Knappschaftskrankenhaus Bochum GmbH, Bochum, Germany.

Alexander Link (A)

Ruhr-Universität Bochum, Universitätsklinikum Knappschaftskrankenhaus Bochum GmbH, Bochum, Germany.

Luca Valenti (L)

Department of Pathophysiology and Transplantation, Università degli Studi di Milano, Milan, Italy.
Translational Medicine - Department of Transfusion Medicine and Hematology, Fondazione IRCCS Ca'Granda Ospedale Maggiore Policlinico, Milan, Italy.

Jane I Grove (JI)

NIHR Nottingham Biomedical Research Centre, Nottingham University Hospitals NHS Trust and the University of Nottingham, Nottingham, UK.
Nottingham Digestive Diseases Centre, University of Nottingham, Nottingham, UK.

Guruprasad P Aithal (GP)

NIHR Nottingham Biomedical Research Centre, Nottingham University Hospitals NHS Trust and the University of Nottingham, Nottingham, UK.
Nottingham Digestive Diseases Centre, University of Nottingham, Nottingham, UK.

Jens U Marquardt (JU)

Department of Medicine I, Johannes Gutenberg-Universität Mainz, Mainz, Germany.

Waleed Fateen (W)

NIHR Nottingham Biomedical Research Centre, Nottingham University Hospitals NHS Trust and the University of Nottingham, Nottingham, UK.
Nottingham Digestive Diseases Centre, University of Nottingham, Nottingham, UK.

Steffen Zopf (S)

Medical Department 1, University of Erlangen-Nuremberg, Germany.

Jean-Francois Dufour (JF)

University Clinic for Visceral Surgery and Medicine, Inselspital, University of Berne, Berne, Switzerland.

Jonel Trebicka (J)

Department of Internal Medicine I, Goethe University Frankfurt, Frankfurt, Germany.

Christian Datz (C)

Department of Internal Medicine, Hospital Oberndorf, Teaching Hospital of the Paracelsus Private Medical University of Salzburg, Oberndorf, Austria.

Pierre Deltenre (P)

Division of Gastroenterology and Hepatology, Centre Hospitalier Universitaire Vaudois, University of Lausanne, Switzerland.

Sebastian Mueller (S)

Department of Internal Medicine and Center for Alcohol Research, Salem Medical Center University Hospital Heidelberg, Heidelberg, Germany.

Thomas Berg (T)

Division of Hepatology, Clinic and Polyclinic for Gastroenterology, Hepatology, Infectiology and Pneumology, University Clinic Leipzig, Leipzig, Germany.

Jochen Hampe (J)

Medical Department 1, University Hospital Dresden, TU Dresden, Germany.

Marsha Y Morgan (MY)

UCL Institute for Liver & Digestive Health, Division of Medicine, Royal Free Campus, University College London, UK.

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