Frontiers in Genetics (Aug 2021)
Association of Genetic Variants Affecting microRNAs and Pancreatic Cancer Risk
- Ye Lu,
- Ye Lu,
- Chiara Corradi,
- Manuel Gentiluomo,
- Evangelina López de Maturana,
- George E. Theodoropoulos,
- Susanne Roth,
- Evaristo Maiello,
- Luca Morelli,
- Livia Archibugi,
- Livia Archibugi,
- Livia Archibugi,
- Jakob R. Izbicki,
- Patricia Sarlós,
- Vytautas Kiudelis,
- Martin Oliverius,
- Mateus Nóbrega Aoki,
- Yogesh Vashist,
- Casper H. J. van Eijck,
- Maria Gazouli,
- Renata Talar-Wojnarowska,
- Andrea Mambrini,
- Raffaele Pezzilli,
- Bas Bueno-de-Mesquita,
- Péter Hegyi,
- Péter Hegyi,
- Pavel Souček,
- John P. Neoptolemos,
- Gregorio Di Franco,
- Cosimo Sperti,
- Emanuele F. Kauffmann,
- Viktor Hlaváč,
- Faik G. Uzunoğlu,
- Stefano Ermini,
- Ewa Małecka-Panas,
- Maurizio Lucchesi,
- Giuseppe Vanella,
- Giuseppe Vanella,
- Giuseppe Vanella,
- Frederike Dijk,
- Beatrice Mohelníková-Duchoňová,
- Franco Bambi,
- Maria Chiara Petrone,
- Krzysztof Jamroziak,
- Feng Guo,
- Feng Guo,
- Katerina Kolarova,
- Giovanni Capretti,
- Giovanni Capretti,
- Anna Caterina Milanetto,
- Laura Ginocchi,
- Martin Loveček,
- Marta Puzzono,
- Hanneke W. M. van Laarhoven,
- Silvia Carrara,
- Audrius Ivanauskas,
- Konstantinos Papiris,
- Daniela Basso,
- Paolo G. Arcidiacono,
- Ferenc Izbéki,
- Roger Chammas,
- Roger Chammas,
- Pavel Vodicka,
- Pavel Vodicka,
- Pavel Vodicka,
- Thilo Hackert,
- Claudio Pasquali,
- Maria L. Piredda,
- Eithne Costello-Goldring,
- Giulia Martina Cavestro,
- Andrea Szentesi,
- Andrea Szentesi,
- Francesca Tavano,
- Barbara Włodarczyk,
- Hermann Brenner,
- Hermann Brenner,
- Hermann Brenner,
- Edita Kreivenaite,
- Xin Gao,
- Xin Gao,
- Stefania Bunduc,
- Stefania Bunduc,
- Roel C. H. Vermeulen,
- Martin A. Schneider,
- Anna Latiano,
- Domenica Gioffreda,
- Sabrina G. G. Testoni,
- Juozas Kupcinskas,
- Rita T. Lawlor,
- Gabriele Capurso,
- Gabriele Capurso,
- Gabriele Capurso,
- Núria Malats,
- Daniele Campa,
- Federico Canzian
Affiliations
- Ye Lu
- Genomic Epidemiology Group, German Cancer Research Center (DKFZ), Heidelberg, Germany
- Ye Lu
- Medical Faculty Heidelberg, University of Heidelberg, Heidelberg, Germany
- Chiara Corradi
- Department of Biology, University of Pisa, Pisa, Italy
- Manuel Gentiluomo
- Department of Biology, University of Pisa, Pisa, Italy
- Evangelina López de Maturana
- Genetic and Molecular Epidemiology Group, Spanish National Cancer Research Centre (CNIO), Madrid, Spain
- George E. Theodoropoulos
- First Propaedeutic University Surgery Clinic, Hippocratio General Hospital, Medical School, National and Kapodistrian University of Athens, Athens, Greece
- Susanne Roth
- Department of General Surgery, University of Heidelberg, Heidelberg, Germany
- Evaristo Maiello
- Department of Oncology, Fondazione IRCCS “Casa Sollievo della Sofferenza” Hospital, San Giovanni Rotondo, Italy
- Luca Morelli
- General Surgery, Department of Translational Research and New Technologies in Medicine and Surgery, University of Pisa, Pisa, Italy
- Livia Archibugi
- Digestive and Liver Disease Unit, Sant’Andrea Hospital, Rome, Italy
- Livia Archibugi
- 0Faculty of Medicine and Psychology, Sapienza University of Rome, Rome, Italy
- Livia Archibugi
- 1Pancreato-Biliary Endoscopy and Endosonography Division, Pancreas Translational and Clinical Research Center, IRSSC San Raffaele Scientific Institute, Milan, Italy
- Jakob R. Izbicki
- 2Department of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
- Patricia Sarlós
- 3First Department of Medicine, Medical School, University of Pécs, Pécs, Hungary
- Vytautas Kiudelis
- 4Department of Gastroenterology, Institute for Digestive Research, Medical Academy, Lithuanian University of Health Sciences, Kaunas, Lithuania
- Martin Oliverius
- 5Department of Surgery, Faculty Hospital Kralovske Vinohrady and Third Faculty of Medicine, Charles University, Prague, Czechia
- Mateus Nóbrega Aoki
- 6Laboratory for Applied Science and Technology in Health, Carlos Chagas Institute, Curitiba, Brazil
- Yogesh Vashist
- 2Department of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
- Casper H. J. van Eijck
- 7Department of Surgery, Erasmus Medical Center, Erasmus University, Rotterdam, Netherlands
- Maria Gazouli
- 8Laboratory of Biology, Medical School, National and Kapodistrian University of Athens, Athens, Greece
- Renata Talar-Wojnarowska
- 9Department of Digestive Tract Diseases, Medical University of Lodz, Lodz, Poland
- Andrea Mambrini
- 0Oncological Department, Azienda USL Toscana Nord Ovest, Oncological Unit of Massa Carrara, Carrara, Italy
- Raffaele Pezzilli
- 1Department of Gastroenterology, San Carlo Hospital, Potenza, Italy
- Bas Bueno-de-Mesquita
- 2Department for Determinants of Chronic Diseases (DCD), National Institute for Public Health and the Environment (RIVM), Bilthoven, Netherlands
- Péter Hegyi
- 3Institute for Translational Medicine, Medical School, University of Pécs, Pécs, Hungary
- Péter Hegyi
- 4Department of Medicine, Centre for Translational Medicine, University of Szeged, Szeged, Hungary
- Pavel Souček
- 5Biomedical Center, Faculty of Medicine in Pilsen, Charles University, Pilsen, Czechia
- John P. Neoptolemos
- Department of General Surgery, University of Heidelberg, Heidelberg, Germany
- Gregorio Di Franco
- General Surgery, Department of Translational Research and New Technologies in Medicine and Surgery, University of Pisa, Pisa, Italy
- Cosimo Sperti
- 6Department of Surgery-DiSCOG, Padua University Hospital, Padua, Italy
- Emanuele F. Kauffmann
- 7Division of General and Transplant Surgery, University of Pisa, Pisa, Italy
- Viktor Hlaváč
- 5Biomedical Center, Faculty of Medicine in Pilsen, Charles University, Pilsen, Czechia
- Faik G. Uzunoğlu
- 2Department of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
- Stefano Ermini
- 8Blood Transfusion Service, Azienda Ospedaliero-Universitaria Meyer, Children's Hospital, Florence, Italy
- Ewa Małecka-Panas
- 9Department of Digestive Tract Diseases, Medical University of Lodz, Lodz, Poland
- Maurizio Lucchesi
- 0Oncological Department, Azienda USL Toscana Nord Ovest, Oncological Unit of Massa Carrara, Carrara, Italy
- Giuseppe Vanella
- Digestive and Liver Disease Unit, Sant’Andrea Hospital, Rome, Italy
- Giuseppe Vanella
- 0Faculty of Medicine and Psychology, Sapienza University of Rome, Rome, Italy
- Giuseppe Vanella
- 1Pancreato-Biliary Endoscopy and Endosonography Division, Pancreas Translational and Clinical Research Center, IRSSC San Raffaele Scientific Institute, Milan, Italy
- Frederike Dijk
- 9Deparment of Pathology, Cancer Center Amsterdam, Amsterdam University Medical Centers, University of Amsterdam, Amsterdam, Netherlands
- Beatrice Mohelníková-Duchoňová
- 0Department of Oncology, Faculty of Medicine and Dentistry, Palacky University Olomouc and University Hospital Olomouc, Olomouc, Czechia
- Franco Bambi
- 8Blood Transfusion Service, Azienda Ospedaliero-Universitaria Meyer, Children's Hospital, Florence, Italy
- Maria Chiara Petrone
- 1Pancreato-Biliary Endoscopy and Endosonography Division, Pancreas Translational and Clinical Research Center, IRSSC San Raffaele Scientific Institute, Milan, Italy
- Krzysztof Jamroziak
- 1Department of Hematology, Institute of Hematology and Transfusion Medicine, Warsaw, Poland
- Feng Guo
- Medical Faculty Heidelberg, University of Heidelberg, Heidelberg, Germany
- Feng Guo
- 2Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ), Heidelberg, Germany
- Katerina Kolarova
- 0Department of Oncology, Faculty of Medicine and Dentistry, Palacky University Olomouc and University Hospital Olomouc, Olomouc, Czechia
- Giovanni Capretti
- 3Department of Biomedical Sciences, Humanitas University, Milan, Italy
- Giovanni Capretti
- 4Pancreatic Surgery Unit, Humanitas Clinical and Research Center IRCCS, Milan, Italy
- Anna Caterina Milanetto
- 6Department of Surgery-DiSCOG, Padua University Hospital, Padua, Italy
- Laura Ginocchi
- 0Oncological Department, Azienda USL Toscana Nord Ovest, Oncological Unit of Massa Carrara, Carrara, Italy
- Martin Loveček
- 5Department of Surgery I, Faculty of Medicine and Dentistry, Palacky University Olomouc and University Hospital Olomouc, Olomouc, Czechia
- Marta Puzzono
- 6Division of Experimental Oncology, Gastroenterology and Gastrointestinal Endoscopy Unit, Vita-Salute San Raffaele University, IRCCS San Raffaele Scientific Institute, Milan, Italy
- Hanneke W. M. van Laarhoven
- 7Department of Medical Oncology, Cancer Center Amsterdam, Amsterdam University Medical Center, University of Amsterdam, Amsterdam, Netherlands
- Silvia Carrara
- 8Division of Gastroenterology and Digestive Endoscopy, Department of Gastroenterology, Humanitas Clinical and Research Center IRCCS, Milan, Italy
- Audrius Ivanauskas
- 4Department of Gastroenterology, Institute for Digestive Research, Medical Academy, Lithuanian University of Health Sciences, Kaunas, Lithuania
- Konstantinos Papiris
- 9Endoscopic Surgery Department, Hippocratio General Hospital of Athens, Athens, Greece
- Daniela Basso
- 0Department of Medicine-DIMED, Padua University Hospital, Padua, Italy
- Paolo G. Arcidiacono
- 1Pancreato-Biliary Endoscopy and Endosonography Division, Pancreas Translational and Clinical Research Center, IRSSC San Raffaele Scientific Institute, Milan, Italy
- Ferenc Izbéki
- 1Szent György University Teaching Hospital of County Fejér, Székesfehérvár, Hungary
- Roger Chammas
- 2Department of Radiology and Oncology, Institute of Cancer of São Paulo (ICESP), São Paulo, Brazil
- Roger Chammas
- 3Faculty of Medicine, University of São Paulo, São Paulo, Brazil
- Pavel Vodicka
- 4Department of Molecular Biology of Cancer, Institute of Experimental Medicine of the Czech Academy of Sciences, Prague, Czechia
- Pavel Vodicka
- 5Biomedical Centre and Department of Surgery, Faculty of Medicine in Pilsen, Charles University, Pilsen, Czechia
- Pavel Vodicka
- 6First Faculty of Medicine, Institute of Biology and Medical Genetics, Charles University, Prague, Czechia
- Thilo Hackert
- Department of General Surgery, University of Heidelberg, Heidelberg, Germany
- Claudio Pasquali
- 6Department of Surgery-DiSCOG, Padua University Hospital, Padua, Italy
- Maria L. Piredda
- 7ARC-NET, Centre for Applied Research on Cancer, University and Hospital Trust of Verona, Verona, Italy
- Eithne Costello-Goldring
- 8Department of Molecular and Clinical Cancer Medicine, University of Liverpool, Liverpool, United Kingdom
- Giulia Martina Cavestro
- 6Division of Experimental Oncology, Gastroenterology and Gastrointestinal Endoscopy Unit, Vita-Salute San Raffaele University, IRCCS San Raffaele Scientific Institute, Milan, Italy
- Andrea Szentesi
- 3Institute for Translational Medicine, Medical School, University of Pécs, Pécs, Hungary
- Andrea Szentesi
- 4Department of Medicine, Centre for Translational Medicine, University of Szeged, Szeged, Hungary
- Francesca Tavano
- 9Division of Gastroenterology and Research Laboratory, Fondazione IRCCS “Casa Sollievo della Sofferenza” Hospital, San Giovanni Rotondo, Italy
- Barbara Włodarczyk
- 9Department of Digestive Tract Diseases, Medical University of Lodz, Lodz, Poland
- Hermann Brenner
- 2Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ), Heidelberg, Germany
- Hermann Brenner
- 0Division of Preventive Oncology, German Cancer Research Center (DKFZ) and National Center for Tumor Diseases (NCT), Heidelberg, Germany
- Hermann Brenner
- 1German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany
- Edita Kreivenaite
- 4Department of Gastroenterology, Institute for Digestive Research, Medical Academy, Lithuanian University of Health Sciences, Kaunas, Lithuania
- Xin Gao
- 2Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ), Heidelberg, Germany
- Xin Gao
- 1German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany
- Stefania Bunduc
- 3Institute for Translational Medicine, Medical School, University of Pécs, Pécs, Hungary
- Stefania Bunduc
- 2Fundeni Clinical Institute, Bucharest, Romania
- Roel C. H. Vermeulen
- 3Institute for Risk Assessment Sciences (IRAS), Utrecht University, Utrecht, Netherlands
- Martin A. Schneider
- Department of General Surgery, University of Heidelberg, Heidelberg, Germany
- Anna Latiano
- 9Division of Gastroenterology and Research Laboratory, Fondazione IRCCS “Casa Sollievo della Sofferenza” Hospital, San Giovanni Rotondo, Italy
- Domenica Gioffreda
- 9Division of Gastroenterology and Research Laboratory, Fondazione IRCCS “Casa Sollievo della Sofferenza” Hospital, San Giovanni Rotondo, Italy
- Sabrina G. G. Testoni
- 1Pancreato-Biliary Endoscopy and Endosonography Division, Pancreas Translational and Clinical Research Center, IRSSC San Raffaele Scientific Institute, Milan, Italy
- Juozas Kupcinskas
- 4Department of Gastroenterology, Institute for Digestive Research, Medical Academy, Lithuanian University of Health Sciences, Kaunas, Lithuania
- Rita T. Lawlor
- 7ARC-NET, Centre for Applied Research on Cancer, University and Hospital Trust of Verona, Verona, Italy
- Gabriele Capurso
- Digestive and Liver Disease Unit, Sant’Andrea Hospital, Rome, Italy
- Gabriele Capurso
- 0Faculty of Medicine and Psychology, Sapienza University of Rome, Rome, Italy
- Gabriele Capurso
- 1Pancreato-Biliary Endoscopy and Endosonography Division, Pancreas Translational and Clinical Research Center, IRSSC San Raffaele Scientific Institute, Milan, Italy
- Núria Malats
- Genetic and Molecular Epidemiology Group, Spanish National Cancer Research Centre (CNIO), Madrid, Spain
- Daniele Campa
- Department of Biology, University of Pisa, Pisa, Italy
- Federico Canzian
- Genomic Epidemiology Group, German Cancer Research Center (DKFZ), Heidelberg, Germany
- DOI
- https://doi.org/10.3389/fgene.2021.693933
- Journal volume & issue
-
Vol. 12
Abstract
Genetic factors play an important role in the susceptibility to pancreatic cancer (PC). However, established loci explain a small proportion of genetic heritability for PC; therefore, more progress is needed to find the missing ones. We aimed at identifying single nucleotide polymorphisms (SNPs) affecting PC risk through effects on micro-RNA (miRNA) function. We searched in silico the genome for SNPs in miRNA seed sequences or 3 prime untranslated regions (3'UTRs) of miRNA target genes. Genome-wide association data of PC cases and controls from the Pancreatic Cancer Cohort (PanScan) Consortium and the Pancreatic Cancer Case–Control (PanC4) Consortium were re-analyzed for discovery, and genotyping data from two additional consortia (PanGenEU and PANDoRA) were used for replication, for a total of 14,062 cases and 11,261 controls. None of the SNPs reached genome-wide significance in the meta-analysis, but for three of them the associations were in the same direction in all the study populations and showed lower value of p in the meta-analyses than in the discovery phase. Specifically, rs7985480 was consistently associated with PC risk (OR = 1.12, 95% CI 1.07–1.17, p = 3.03 × 10−6 in the meta-analysis). This SNP is in linkage disequilibrium (LD) with rs2274048, which modulates binding of various miRNAs to the 3'UTR of UCHL3, a gene involved in PC progression. In conclusion, our results expand the knowledge of the genetic PC risk through miRNA-related SNPs and show the usefulness of functional prioritization to identify genetic polymorphisms associated with PC risk.
Keywords