Frontiers in Oncology (Dec 2021)
Identification of Recessively Inherited Genetic Variants Potentially Linked to Pancreatic Cancer Risk
- Ye Lu,
- Ye Lu,
- Manuel Gentiluomo,
- Angelica Macauda,
- Domenica Gioffreda,
- Maria Gazouli,
- Maria C. Petrone,
- Dezső Kelemen,
- Laura Ginocchi,
- Luca Morelli,
- Konstantinos Papiris,
- William Greenhalf,
- Jakob R. Izbicki,
- Vytautas Kiudelis,
- Beatrice Mohelníková-Duchoňová,
- Bas Bueno-de-Mesquita,
- Pavel Vodicka,
- Pavel Vodicka,
- Pavel Vodicka,
- Hermann Brenner,
- Hermann Brenner,
- Hermann Brenner,
- Markus K. Diener,
- Raffaele Pezzilli,
- Audrius Ivanauskas,
- Roberto Salvia,
- Andrea Szentesi,
- Andrea Szentesi,
- Mateus Nóbrega Aoki,
- Balázs C. Németh,
- Cosimo Sperti,
- Krzysztof Jamroziak,
- Roger Chammas,
- Roger Chammas,
- Martin Oliverius,
- Livia Archibugi,
- Livia Archibugi,
- Livia Archibugi,
- Stefano Ermini,
- János Novák,
- Juozas Kupcinskas,
- Ondřej Strouhal,
- Ondřej Strouhal,
- Pavel Souček,
- Giulia M. Cavestro,
- Anna C. Milanetto,
- Giuseppe Vanella,
- Giuseppe Vanella,
- Giuseppe Vanella,
- John P. Neoptolemos,
- George E. Theodoropoulos,
- Hanneke W. M. van Laarhoven,
- Andrea Mambrini,
- Stefania Moz,
- Zdenek Kala,
- Martin Loveček,
- Daniela Basso,
- Faik G. Uzunoglu,
- Thilo Hackert,
- Sabrina G. G. Testoni,
- Viktor Hlaváč,
- Angelo Andriulli,
- Maurizio Lucchesi,
- Francesca Tavano,
- Silvia Carrara,
- Péter Hegyi,
- Péter Hegyi,
- Paolo G. Arcidiacono,
- Olivier R. Busch,
- Rita T. Lawlor,
- Marta Puzzono,
- Ugo Boggi,
- Feng Guo,
- Ewa Małecka-Panas,
- Gabriele Capurso,
- Gabriele Capurso,
- Gabriele Capurso,
- Stefano Landi,
- Renata Talar-Wojnarowska,
- Oliver Strobel,
- Xin Gao,
- Yogesh Vashist,
- 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
- Manuel Gentiluomo
- Department of Biology, University of Pisa, Pisa, Italy
- Angelica Macauda
- Genomic Epidemiology Group, German Cancer Research Center (DKFZ), Heidelberg, Germany
- Domenica Gioffreda
- Division of Gastroenterology and Research Laboratory, Fondazione Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) Casa Sollievo della Sofferenza, San Giovanni Rotondo, Italy
- Maria Gazouli
- Department of Basic Medical Sciences, Laboratory of Biology, Medical School, National and Kapodistrian University of Athens, Athens, Greece
- Maria C. Petrone
- Pancreato-Biliary Endoscopy and Endosonography Division, Pancreas Translational and Clinical Research Center, San Raffaele Scientific Institute Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS), Milan, Italy
- Dezső Kelemen
- Department of Surgery, Medical School, University of Pécs, Pécs, Hungary
- Laura Ginocchi
- Oncological Department, Oncological Unit of Massa Carrara, Azienda Unità Sanitaria Locale (USL) Toscana Nord Ovest, Carrara, Italy
- Luca Morelli
- General Surgery, Department of Translational Research and New Technologies in Medicine and Surgery, University of Pisa, Pisa, Italy
- Konstantinos Papiris
- 0Endoscopic Surgery Department, Hippocratio General Hospital of Athens, Athens, Greece
- William Greenhalf
- 1Department of Molecular and Clinical Cancer Medicine, University of Liverpool, Liverpool, United Kingdom
- Jakob R. Izbicki
- 2Department of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
- Vytautas Kiudelis
- 3Department of Gastroenterology, Institute for Digestive Research, Medical Academy, Lithuanian University of Health Sciences, Kaunas, Lithuania
- Beatrice Mohelníková-Duchoňová
- 4Department of Oncology, Faculty of Medicine and Dentistry, Palacky University Olomouc and University Hospital Olomouc, Olomouc, Czechia
- Bas Bueno-de-Mesquita
- 5Department for Determinants of Chronic Diseases (DCD), National Institute for Public Health and the Environment (RIVM), Bilthoven, Netherlands
- Pavel Vodicka
- 6Department of Molecular Biology of Cancer, Institute of Experimental Medicine of the Czech Academy of Sciences, Prague, Czechia
- Pavel Vodicka
- 7Faculty of Medicine and Biomedical Center in Pilsen, Charles University, Pilsen, Czechia
- Pavel Vodicka
- 8First Faculty of Medicine, Institute of Biology and Medical Genetics, Prague, Czechia
- Hermann Brenner
- 9Division 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
- Markus K. Diener
- 2Department of General Surgery, University of Heidelberg, Heidelberg, Germany
- Raffaele Pezzilli
- 3Department of Internal Medicine, San Carlo Hospital, Potenza, Italy
- Audrius Ivanauskas
- 3Department of Gastroenterology, Institute for Digestive Research, Medical Academy, Lithuanian University of Health Sciences, Kaunas, Lithuania
- Roberto Salvia
- 4Department of General and Pancreatic Surgery, The Pancreas Institute, University and Hospital Trust of Verona, Verona, Italy
- Andrea Szentesi
- 5Institute for Translational Medicine, Medical School, University of Pécs, Pécs, Hungary
- Andrea Szentesi
- 6Centre for Translational Medicine, Department of Medicine, University of Szeged, Szeged, Hungary
- Mateus Nóbrega Aoki
- 7Laboratory for Applied Science and Technology in Health, Carlos Chagas Institute, Curitiba, Brazil
- Balázs C. Németh
- 8First Department of Medicine, University of Szeged, Szeged, Hungary
- Cosimo Sperti
- 9Department of Surgery-Dipartimento di Scienze Chirurgiche Oncologiche e Gastroenterologiche (DiSCOG), Padua University Hospital, Padua, Italy
- Krzysztof Jamroziak
- 0Department of Hematology, Transplantation and Internal Medicine, Medical University of Warsaw, Warsaw, Poland
- Roger Chammas
- 1Department of Radiology and Oncology, Institute of Cancer of São Paulo (ICESP), São Paulo, Brazil
- Roger Chammas
- 2Faculty of Medicine, University of São Paulo, São Paulo, Brazil
- Martin Oliverius
- 3Department of Surgery, Faculty Hospital Kralovske Vinohrady and Third Faculty of Medicine, Charles University, Prague, Czechia
- Livia Archibugi
- Pancreato-Biliary Endoscopy and Endosonography Division, Pancreas Translational and Clinical Research Center, San Raffaele Scientific Institute Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS), Milan, Italy
- Livia Archibugi
- 4Digestive and Liver Disease Unit, Sant’ Andrea Hospital, Rome, Italy
- Livia Archibugi
- 5Faculty of Medicine and Psychology, Sapienza University of Rome, Rome, Italy
- Stefano Ermini
- 6Blood Transfusion Service, Children’s Hospital, Azienda Ospedaliero-Universitaria Meyer, Florence, Italy
- János Novák
- 7Pándy Kálmán Hospital of Békés County, Gyula, Hungary
- Juozas Kupcinskas
- 3Department of Gastroenterology, Institute for Digestive Research, Medical Academy, Lithuanian University of Health Sciences, Kaunas, Lithuania
- Ondřej Strouhal
- 4Department of Oncology, Faculty of Medicine and Dentistry, Palacky University Olomouc and University Hospital Olomouc, Olomouc, Czechia
- Ondřej Strouhal
- 8Institute of Molecular and Translational Medicine, Faculty of Medicine and Dentistry, Palacky University Olomouc, Olomouc, Czechia
- Pavel Souček
- 9Biomedical Center, Faculty of Medicine in Pilsen, Charles University, Pilsen, Czechia
- Giulia M. Cavestro
- 0Division of Experimental Oncology, Gastroenterology and Gastrointestinal Endoscopy Unit, Vita-Salute San Raffaele University, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Anna C. Milanetto
- 9Department of Surgery-Dipartimento di Scienze Chirurgiche Oncologiche e Gastroenterologiche (DiSCOG), Padua University Hospital, Padua, Italy
- Giuseppe Vanella
- Pancreato-Biliary Endoscopy and Endosonography Division, Pancreas Translational and Clinical Research Center, San Raffaele Scientific Institute Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS), Milan, Italy
- Giuseppe Vanella
- 4Digestive and Liver Disease Unit, Sant’ Andrea Hospital, Rome, Italy
- Giuseppe Vanella
- 5Faculty of Medicine and Psychology, Sapienza University of Rome, Rome, Italy
- John P. Neoptolemos
- 2Department of General Surgery, University of Heidelberg, Heidelberg, Germany
- George E. Theodoropoulos
- 1First Propaedeutic University Surgery Clinic, Hippocratio General Hospital, Medical School, National and Kapodistrian University of Athens, Athens, Greece
- Hanneke W. M. van Laarhoven
- 2Department of Medical Oncology, Cancer Center Amsterdam, Amsterdam University Medical Centers, University of Amsterdam, Amsterdam, Netherlands
- Andrea Mambrini
- Oncological Department, Oncological Unit of Massa Carrara, Azienda Unità Sanitaria Locale (USL) Toscana Nord Ovest, Carrara, Italy
- Stefania Moz
- 3Department of Medicine (DIMED), Padua University Hospital, Padua, Italy
- Zdenek Kala
- 4Department of Surgery, University Hospital Brno Bohunice, Faculty of Medicine, Masaryk University, Brno, Czechia
- Martin Loveček
- 5Department of Surgery I, Faculty of Medicine and Dentistry, Palacky University Olomouc and University Hospital Olomouc, Olomouc, Czechia
- Daniela Basso
- 3Department of Medicine (DIMED), Padua University Hospital, Padua, Italy
- Faik G. Uzunoglu
- 2Department of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
- Thilo Hackert
- 2Department of General Surgery, University of Heidelberg, Heidelberg, Germany
- Sabrina G. G. Testoni
- Pancreato-Biliary Endoscopy and Endosonography Division, Pancreas Translational and Clinical Research Center, San Raffaele Scientific Institute Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS), Milan, Italy
- Viktor Hlaváč
- 9Biomedical Center, Faculty of Medicine in Pilsen, Charles University, Pilsen, Czechia
- Angelo Andriulli
- Division of Gastroenterology and Research Laboratory, Fondazione Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) Casa Sollievo della Sofferenza, San Giovanni Rotondo, Italy
- Maurizio Lucchesi
- Oncological Department, Oncological Unit of Massa Carrara, Azienda Unità Sanitaria Locale (USL) Toscana Nord Ovest, Carrara, Italy
- Francesca Tavano
- Division of Gastroenterology and Research Laboratory, Fondazione Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) Casa Sollievo della Sofferenza, San Giovanni Rotondo, Italy
- Silvia Carrara
- 6Division of Gastroenterology and Digestive Endoscopy, Department of Gastroenterology, Humanitas Clinical and Research Center Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS), Milan, Italy
- Péter Hegyi
- 5Institute for Translational Medicine, Medical School, University of Pécs, Pécs, Hungary
- Péter Hegyi
- 6Centre for Translational Medicine, Department of Medicine, University of Szeged, Szeged, Hungary
- Paolo G. Arcidiacono
- Pancreato-Biliary Endoscopy and Endosonography Division, Pancreas Translational and Clinical Research Center, San Raffaele Scientific Institute Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS), Milan, Italy
- Olivier R. Busch
- 7Department of Surgery, Cancer Center Amsterdam, Amsterdam University Medical Centers, University of Amsterdam, Amsterdam, Netherlands
- Rita T. Lawlor
- 8Applied Research on Cancer (ARC)-Net Research Center, University and Hospital Trust of Verona, Verona, Italy
- Marta Puzzono
- 0Division of Experimental Oncology, Gastroenterology and Gastrointestinal Endoscopy Unit, Vita-Salute San Raffaele University, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Ugo Boggi
- 9Division of General and Transplant Surgery, Pisa University Hospital, Pisa, Italy
- Feng Guo
- 9Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ), Heidelberg, Germany
- Ewa Małecka-Panas
- 0Department of Digestive Tract Diseases, Medical University of Lodz, Lodz, Poland
- Gabriele Capurso
- Pancreato-Biliary Endoscopy and Endosonography Division, Pancreas Translational and Clinical Research Center, San Raffaele Scientific Institute Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS), Milan, Italy
- Gabriele Capurso
- 4Digestive and Liver Disease Unit, Sant’ Andrea Hospital, Rome, Italy
- Gabriele Capurso
- 5Faculty of Medicine and Psychology, Sapienza University of Rome, Rome, Italy
- Stefano Landi
- Department of Biology, University of Pisa, Pisa, Italy
- Renata Talar-Wojnarowska
- 0Department of Digestive Tract Diseases, Medical University of Lodz, Lodz, Poland
- Oliver Strobel
- 2Department of General Surgery, University of Heidelberg, Heidelberg, Germany
- Xin Gao
- 9Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ), Heidelberg, Germany
- Yogesh Vashist
- 1Centre for Surgical Oncology, Medias Klinikum Burghausen, Burghausen, Germany
- 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/fonc.2021.771312
- Journal volume & issue
-
Vol. 11
Abstract
Although 21 pancreatic cancer susceptibility loci have been identified in individuals of European ancestry through genome-wide association studies (GWASs), much of the heritability of pancreatic cancer risk remains unidentified. A recessive genetic model could be a powerful tool for identifying additional risk variants. To discover recessively inherited pancreatic cancer risk loci, we performed a re-analysis of the largest pancreatic cancer GWAS, the Pancreatic Cancer Cohort Consortium (PanScan) and the Pancreatic Cancer Case-Control Consortium (PanC4), including 8,769 cases and 7,055 controls of European ancestry. Six single nucleotide polymorphisms (SNPs) showed associations with pancreatic cancer risk according to a recessive model of inheritance. We replicated these variants in 3,212 cases and 3,470 controls collected from the PANcreatic Disease ReseArch (PANDoRA) consortium. The results of the meta-analyses confirmed that rs4626538 (7q32.2), rs7008921 (8p23.2) and rs147904962 (17q21.31) showed specific recessive effects (p<10−5) compared with the additive effects (p>10−3), although none of the six SNPs reached the conventional threshold for genome-wide significance (p < 5×10−8). Additional bioinformatic analysis explored the functional annotations of the SNPs and indicated a possible relationship between rs36018702 and expression of the BCL2L11 and BUB1 genes, which are known to be involved in pancreatic biology. Our findings, while not conclusive, indicate the importance of considering non-additive genetic models when performing GWAS analysis. The SNPs associated with pancreatic cancer in this study could be used for further meta-analysis for recessive association of SNPs and pancreatic cancer risk and might be a useful addiction to improve the performance of polygenic risk scores.
Keywords
- pancreatic cancer
- susceptibility
- genome-wide association study
- recessive model
- genetic polymorphisms