Carboxyl ester lipase hybrid 1 (CEL-HYB1) haplotypes confer varying risk for chronic pancreatitis

Abstract The CEL-HYB1 hybrid allele of the carboxyl ester lipase (CEL) gene and its pseudogene (CELP) has been associated with chronic pancreatitis (CP). Recent work indicated that amino acid positions 488 and 548 in CEL-HYB1 determined pathogenicity. Haplotype Thr488-Ile548 was associated with CP w...

Full description

Saved in:
Bibliographic Details
Main Authors: Gergő Berke, Máté Sándor, Xunjun K. Xiao, Mark E. Lowe, Maren Ewers, Bálint Erőss, Emmanuelle Masson, Balázs Csaba Németh, Áron Vincze, László Czakó, Agnieszka Magdalena Rygiel, Jonas Rosendahl, Jian-Min Chen, Heiko Witt, Péter Hegyi, Miklós Sahin-Tóth, Eszter Hegyi
Format: Article
Language:English
Published: Nature Portfolio 2024-12-01
Series:Scientific Reports
Subjects:
Online Access:https://doi.org/10.1038/s41598-024-82077-4
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1846101259946295296
author Gergő Berke
Máté Sándor
Xunjun K. Xiao
Mark E. Lowe
Maren Ewers
Bálint Erőss
Emmanuelle Masson
Balázs Csaba Németh
Áron Vincze
László Czakó
Agnieszka Magdalena Rygiel
Jonas Rosendahl
Jian-Min Chen
Heiko Witt
Péter Hegyi
Miklós Sahin-Tóth
Eszter Hegyi
author_facet Gergő Berke
Máté Sándor
Xunjun K. Xiao
Mark E. Lowe
Maren Ewers
Bálint Erőss
Emmanuelle Masson
Balázs Csaba Németh
Áron Vincze
László Czakó
Agnieszka Magdalena Rygiel
Jonas Rosendahl
Jian-Min Chen
Heiko Witt
Péter Hegyi
Miklós Sahin-Tóth
Eszter Hegyi
author_sort Gergő Berke
collection DOAJ
description Abstract The CEL-HYB1 hybrid allele of the carboxyl ester lipase (CEL) gene and its pseudogene (CELP) has been associated with chronic pancreatitis (CP). Recent work indicated that amino acid positions 488 and 548 in CEL-HYB1 determined pathogenicity. Haplotype Thr488-Ile548 was associated with CP while haplotypes Thr488-Thr548 and Ile488-Thr548 were benign. However, functional analysis revealed that Thr488 is the primary determinant of CEL-HYB1 misfolding and associated endoplasmic reticulum (ER) stress. To address this contradiction, we analyzed a cohort from Hungary and found significantly increased CEL-HYB1 carrier frequency in CP cases (9/319, 2.8%) versus controls (5/618, 0.8%), yielding an odds ratio of 3.6 (95% confidence interval 1.2–10.7, P = 0.024). All CEL-HYB1 positive carriers from Hungary had the Thr488-Thr548 haplotype. We analyzed the haplotype distribution of reported CEL-HYB1 carriers from three European cohorts and found that 14/29 CP cases from Germany and 2/6 CP cases from Poland carried the Thr488-Ile548 haplotype, which was absent in CEL-HYB1 positive controls from Germany (n = 13) and Poland (n = 8). All patients (n = 17) and controls (n = 9) from France carrying CEL-HYB1 contained the Thr488-Thr548 haplotype. Functional studies using transfected cells indicated that both CEL-HYB1 haplotypes induced significant ER stress and the Thr488-Ile548 haplotype had a stronger effect. We conclude that the Thr488-Thr548 haplotype of CEL-HYB1 is widespread in Europe and increases CP risk by almost fourfold. In contrast, the Thr488-Ile548 haplotype is regionally restricted, but confers markedly stronger CP risk.
format Article
id doaj-art-4939d8c0c883479b9a2572b713b88d7c
institution Kabale University
issn 2045-2322
language English
publishDate 2024-12-01
publisher Nature Portfolio
record_format Article
series Scientific Reports
spelling doaj-art-4939d8c0c883479b9a2572b713b88d7c2024-12-29T12:19:02ZengNature PortfolioScientific Reports2045-23222024-12-011411710.1038/s41598-024-82077-4Carboxyl ester lipase hybrid 1 (CEL-HYB1) haplotypes confer varying risk for chronic pancreatitisGergő Berke0Máté Sándor1Xunjun K. Xiao2Mark E. Lowe3Maren Ewers4Bálint Erőss5Emmanuelle Masson6Balázs Csaba Németh7Áron Vincze8László Czakó9Agnieszka Magdalena Rygiel10Jonas Rosendahl11Jian-Min Chen12Heiko Witt13Péter Hegyi14Miklós Sahin-Tóth15Eszter Hegyi16Institute for Translational Medicine, Medical School, University of PécsDepartment of Surgery, University of California Los AngelesDepartment of Pediatrics, Washington University School of MedicineDepartment of Pediatrics, Washington University School of MedicinePediatric Nutritional Medicine & Else Kröner-Fresenius-Centre (EKFZ) for Nutritional Medicine, Technical University Munich (TUM)Institute for Translational Medicine, Medical School, University of PécsUMR 1078, Univ Brest, GGBHungarian Centre of Excellence for Molecular Medicine, Translational Pancreatology Research Group, University of SzegedDivision of Gastroenterology, First Department of Medicine, Medical School, University of PécsDepartment of Medicine, Albert Szent-Györgyi Medical School, University of SzegedDepartment of Medical Genetics, Institute of Mother and ChildDepartment of Internal Medicine I, Martin-Luther-University Halle-WittenbergUMR 1078, Univ Brest, GGBPediatric Nutritional Medicine & Else Kröner-Fresenius-Centre (EKFZ) for Nutritional Medicine, Technical University Munich (TUM)Institute for Translational Medicine, Medical School, University of PécsDepartment of Surgery, University of California Los AngelesInstitute for Translational Medicine, Medical School, University of PécsAbstract The CEL-HYB1 hybrid allele of the carboxyl ester lipase (CEL) gene and its pseudogene (CELP) has been associated with chronic pancreatitis (CP). Recent work indicated that amino acid positions 488 and 548 in CEL-HYB1 determined pathogenicity. Haplotype Thr488-Ile548 was associated with CP while haplotypes Thr488-Thr548 and Ile488-Thr548 were benign. However, functional analysis revealed that Thr488 is the primary determinant of CEL-HYB1 misfolding and associated endoplasmic reticulum (ER) stress. To address this contradiction, we analyzed a cohort from Hungary and found significantly increased CEL-HYB1 carrier frequency in CP cases (9/319, 2.8%) versus controls (5/618, 0.8%), yielding an odds ratio of 3.6 (95% confidence interval 1.2–10.7, P = 0.024). All CEL-HYB1 positive carriers from Hungary had the Thr488-Thr548 haplotype. We analyzed the haplotype distribution of reported CEL-HYB1 carriers from three European cohorts and found that 14/29 CP cases from Germany and 2/6 CP cases from Poland carried the Thr488-Ile548 haplotype, which was absent in CEL-HYB1 positive controls from Germany (n = 13) and Poland (n = 8). All patients (n = 17) and controls (n = 9) from France carrying CEL-HYB1 contained the Thr488-Thr548 haplotype. Functional studies using transfected cells indicated that both CEL-HYB1 haplotypes induced significant ER stress and the Thr488-Ile548 haplotype had a stronger effect. We conclude that the Thr488-Thr548 haplotype of CEL-HYB1 is widespread in Europe and increases CP risk by almost fourfold. In contrast, the Thr488-Ile548 haplotype is regionally restricted, but confers markedly stronger CP risk.https://doi.org/10.1038/s41598-024-82077-4PancreatitisGenetic association studyLipaseMisfoldingEndoplasmic reticulum stress
spellingShingle Gergő Berke
Máté Sándor
Xunjun K. Xiao
Mark E. Lowe
Maren Ewers
Bálint Erőss
Emmanuelle Masson
Balázs Csaba Németh
Áron Vincze
László Czakó
Agnieszka Magdalena Rygiel
Jonas Rosendahl
Jian-Min Chen
Heiko Witt
Péter Hegyi
Miklós Sahin-Tóth
Eszter Hegyi
Carboxyl ester lipase hybrid 1 (CEL-HYB1) haplotypes confer varying risk for chronic pancreatitis
Scientific Reports
Pancreatitis
Genetic association study
Lipase
Misfolding
Endoplasmic reticulum stress
title Carboxyl ester lipase hybrid 1 (CEL-HYB1) haplotypes confer varying risk for chronic pancreatitis
title_full Carboxyl ester lipase hybrid 1 (CEL-HYB1) haplotypes confer varying risk for chronic pancreatitis
title_fullStr Carboxyl ester lipase hybrid 1 (CEL-HYB1) haplotypes confer varying risk for chronic pancreatitis
title_full_unstemmed Carboxyl ester lipase hybrid 1 (CEL-HYB1) haplotypes confer varying risk for chronic pancreatitis
title_short Carboxyl ester lipase hybrid 1 (CEL-HYB1) haplotypes confer varying risk for chronic pancreatitis
title_sort carboxyl ester lipase hybrid 1 cel hyb1 haplotypes confer varying risk for chronic pancreatitis
topic Pancreatitis
Genetic association study
Lipase
Misfolding
Endoplasmic reticulum stress
url https://doi.org/10.1038/s41598-024-82077-4
work_keys_str_mv AT gergoberke carboxylesterlipasehybrid1celhyb1haplotypesconfervaryingriskforchronicpancreatitis
AT matesandor carboxylesterlipasehybrid1celhyb1haplotypesconfervaryingriskforchronicpancreatitis
AT xunjunkxiao carboxylesterlipasehybrid1celhyb1haplotypesconfervaryingriskforchronicpancreatitis
AT markelowe carboxylesterlipasehybrid1celhyb1haplotypesconfervaryingriskforchronicpancreatitis
AT marenewers carboxylesterlipasehybrid1celhyb1haplotypesconfervaryingriskforchronicpancreatitis
AT balinteross carboxylesterlipasehybrid1celhyb1haplotypesconfervaryingriskforchronicpancreatitis
AT emmanuellemasson carboxylesterlipasehybrid1celhyb1haplotypesconfervaryingriskforchronicpancreatitis
AT balazscsabanemeth carboxylesterlipasehybrid1celhyb1haplotypesconfervaryingriskforchronicpancreatitis
AT aronvincze carboxylesterlipasehybrid1celhyb1haplotypesconfervaryingriskforchronicpancreatitis
AT laszloczako carboxylesterlipasehybrid1celhyb1haplotypesconfervaryingriskforchronicpancreatitis
AT agnieszkamagdalenarygiel carboxylesterlipasehybrid1celhyb1haplotypesconfervaryingriskforchronicpancreatitis
AT jonasrosendahl carboxylesterlipasehybrid1celhyb1haplotypesconfervaryingriskforchronicpancreatitis
AT jianminchen carboxylesterlipasehybrid1celhyb1haplotypesconfervaryingriskforchronicpancreatitis
AT heikowitt carboxylesterlipasehybrid1celhyb1haplotypesconfervaryingriskforchronicpancreatitis
AT peterhegyi carboxylesterlipasehybrid1celhyb1haplotypesconfervaryingriskforchronicpancreatitis
AT miklossahintoth carboxylesterlipasehybrid1celhyb1haplotypesconfervaryingriskforchronicpancreatitis
AT eszterhegyi carboxylesterlipasehybrid1celhyb1haplotypesconfervaryingriskforchronicpancreatitis