Probing the diabetes and colorectal cancer relationship using gene - environment interaction analyses

Niki Dimou¹, Andre E Kim², Orlagh Flanagan³, Neil Murphy³, Virginia Diez-Obrero^{4

5

6

7}, Anna Shcherbina^{8

9}, Elom K Aglago¹⁰, Emmanouil Bouras¹¹, Peter T Campbell¹², Graham Casey¹³, Steven Gallinger¹⁴, Stephen B Gruber¹⁵, Mark A Jenkins¹⁶, Yi Lin¹⁷, Victor Moreno^{7

18

19

20}, Edward Ruiz-Narvaez²¹, Mariana C Stern²², Yu Tian^{23

24}, Kostas K Tsilidis^{10

11}, Volker Arndt²⁵, Elizabeth L Barry²⁶, James W Baurley^{27

28}, Sonja I Berndt²⁹, Stéphane Bézieau³⁰, Stephanie A Bien¹⁷, D Timothy Bishop³¹, Hermann Brenner^{25

32

33}, Arif Budiarto^{27

34}, Robert Carreras-Torres³⁵, Tjeng Wawan Cenggoro²⁷, Andrew T Chan^{36

37

38

39

40

41}, Jenny Chang-Claude^{23

42}, Stephen J Chanock²⁹, Xuechen Chen^{25

43}, David V Conti², Christopher H Dampier^{13

44}, Matthew Devall⁴⁵, David A Drew⁴⁶, Jane C Figueiredo⁴⁷, Graham G Giles^{16

48

49}, Andrea Gsur⁵⁰, Tabitha A Harrison¹⁷, Akihisa Hidaka¹⁷, Michael Hoffmeister²⁵, Jeroen R Huyghe¹⁷, Kristina Jordahl¹⁷, Eric Kawaguchi², Temitope O Keku⁵¹, Susanna C Larsson⁵², Loic Le Marchand⁵³, Juan Pablo Lewinger², Li Li⁴⁵, Bharuno Mahesworo²⁷, John Morrison², Polly A Newcomb^{17

54}, Christina C Newton⁵⁵, Mireia Obon-Santacana⁵⁶, Jennifer Ose^{57

58}, Rish K Pai⁵⁹, Julie R Palmer⁶⁰, Nikos Papadimitriou³, Bens Pardamean²⁷, Anita R Peoples^{57

58}, Paul D P Pharoah⁶¹, Elizabeth A Platz⁶², John D Potter^{17

63

64}, Gad Rennert^{65

66

67}, Peter C Scacheri⁶⁸, Robert E Schoen⁶⁹, Yu-Ru Su⁷⁰, Catherine M Tangen⁷¹, Stephen N Thibodeau⁷², Duncan C Thomas²², Cornelia M Ulrich^{57

58}, Caroline Y Um⁵⁵, Franzel J B van Duijnhoven⁷³, Kala Visvanathan⁶³, Pavel Vodicka^{74

75

76}, Ludmila Vodickova^{74

75

76}, Emily White^{17

63}, Alicja Wolk⁵², Michael O Woods⁷⁷, Conghui Qu¹⁷, Anshul Kundaje^#^{8

9}, Li Hsu^#^{17

78}, W James Gauderman^#², Marc J Gunter^#^{3

10}, Ulrike Peters^#^{17

63}

Affiliations

¹ Nutrition and Metabolism Branch, International Agency for Research on Cancer, Lyon, France. DimouN@iarc.who.int.
² Division of Biostatistics, Department of Population and Public Health Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
³ Nutrition and Metabolism Branch, International Agency for Research on Cancer, Lyon, France.
⁴ Unit of Biomarkers and Susceptibility, Oncology Data Analytics Program, Catalan Institute of Oncology, Barcelona, 08908, Spain.
⁵ Colorectal Cancer Group, ONCOBELL Program, Bellvitge Biomedical Research Institute, Barcelona, 08908, Spain.
⁶ Consortium for Biomedical Research in Epidemiology and Public Health, Barcelona, 08908, Spain.
⁷ Department of Clinical Sciences, Faculty of Medicine, University of Barcelona, Barcelona, 08908, Spain.
⁸ Department of Genetics, Stanford University, Stanford, CA, USA.
⁹ Department of Computer Science, Stanford University, Stanford, CA, USA.
¹⁰ School of Public Health, Imperial College London, London, United Kingdom.
¹¹ Department of Hygiene and Epidemiology, University of Ioannina School of Medicine, Ioannina, Greece.
¹² Department of Epidemiology and Population Health, Albert Einstein College of Medicine, Bronx, NY, USA.
¹³ Department of Public Health Sciences, Center for Public Health Genomics, Charlottesville, VA, USA.
¹⁴ Lunenfeld Tanenbaum Research Institute, Mount Sinai Hospital, University of Toronto, Toronto, ON, Canada.
¹⁵ Center for Precision Medicine, Department of Medical Oncology and Therapeutics Research, City of Hope National Medical Center, Duarte, CA, USA.
¹⁶ Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne, Melbourne, Victoria, Australia.
¹⁷ Public Health Sciences Division, Fred Hutchinson Cancer Center, Seattle, WA, USA.
¹⁸ Oncology Data Analytics Program, Catalan Institute of Oncology-IDIBELL, L'Hospitalet de Llobregat, Barcelona, Spain.
¹⁹ CIBER Epidemiología y Salud Pública (CIBERESP), Madrid, Spain.
²⁰ ONCOBEL Program, Bellvitge Biomedical Research Institute (IDIBELL), L'Hospitalet de Llobregat, Barcelona, Spain.
²¹ Department of Nutritional Sciences, University of Michigan School of Public Health, Ann Arbor, MI, USA.
²² Department of Population and Public Health Sciences & USC Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
²³ Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany.
²⁴ School of Public Health, Capital Medical University, Beijing, China.
²⁵ Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ), Heidelberg, Germany.
²⁶ Department of Epidemiology, Geisel School of Medicine at Dartmouth, Hanover, NH, USA.
²⁷ Bioinformatics and Data Science Research Center, Bina Nusantara University, Jakarta, Indonesia.
²⁸ BioRealm LLC, Walnut, CA, USA.
²⁹ Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.
³⁰ Nantes Université, CHU Nantes, Service de Génétique médicale, F-44000, Nantes, France.
³¹ Leeds Institute of Cancer and Pathology, University of Leeds, Leeds, UK.
³² Division of Preventive Oncology, German Cancer Research Center (DKFZ) and National Center for Tumor Diseases (NCT), Heidelberg, Germany.
³³ German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany.
³⁴ Computer Science Department, School of Computer Science, Bina Nusantara University, Jakarta, Indonesia.
³⁵ Colorectal Cancer Group, ONCOBELL Program, Bellvitge Biomedical Research Institute (IDIBELL), L'Hospitalet de Llobregat, 8908, Barcelona, Spain.
³⁶ Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA.
³⁷ Channing Division of Network Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA, USA.
³⁸ Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA.
³⁹ Broad Institute of Harvard and MIT, Cambridge, MA, USA.
⁴⁰ Department of Epidemiology, Harvard T.H. Chan School of Public Health, Harvard University, Boston, MA, USA.
⁴¹ Department of Immunology and Infectious Diseases, Harvard T.H. Chan School of Public Health, Harvard University, Boston, MA, USA.
⁴² University Medical Centre Hamburg-Eppendorf, University Cancer Centre Hamburg (UCCH), Hamburg, Germany.
⁴³ Medical Faculty Heidelberg, Heidelberg University, Heidelberg, Germany.
⁴⁴ Department of General Surgery, University of Virginia School of Medicine, Charlottesville, VA, USA.
⁴⁵ Department of Family Medicine, University of Virginia, Charlottesville, VA, USA.
⁴⁶ Clinical & Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA.
⁴⁷ Department of Medicine, Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, CA, USA.
⁴⁸ Cancer Epidemiology Division, Cancer Council Victoria, Melbourne, VIC, Australia.
⁴⁹ Precision Medicine, School of Clinical Sciences at Monash Health, Monash University, Clayton, VIC, Australia.
⁵⁰ Center for Cancer Research, Medical University of Vienna, Vienna, Austria.
⁵¹ Center for Gastrointestinal Biology and Disease, University of North Carolina, Chapel Hill, NC, USA.
⁵² Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden.
⁵³ University of Hawaii Cancer Center, Honolulu, HI, USA.
⁵⁴ School of Public Health, University of Washington, Seattle, WA, USA.
⁵⁵ Department of Population Science, American Cancer Society, Atlanta, GA, USA.
⁵⁶ Unit of Nutrition, Environment and Cancer, Cancer Epidemiology Research Program, Catalan Institute of Oncology (ICO-IDIBELL), Avda Gran Via Barcelona 199-203, 08908L'Hospitalet de Llobregat, Barcelona, Spain.
⁵⁷ Huntsman Cancer Institute, University of Utah, Salt Lake City, UT, USA.
⁵⁸ Department of Population Health Sciences, University of Utah, Salt Lake City, UH, USA.
⁵⁹ Department of Laboratory Medicine and Pathology, Mayo Clinic Arizona, Scottsdale, AZ, USA.
⁶⁰ Slone Epidemiology Center at Boston University, Boston, MA, USA.
⁶¹ Department of Public Health and Primary Care, University of Cambridge, Cambridge, UK.
⁶² Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA.
⁶³ Department of Epidemiology, School of Public Health, University of Washington, Seattle, WA, USA.
⁶⁴ Research Centre for Hauora and Health, Massey University, Wellington, New Zealand.
⁶⁵ Department of Community Medicine and Epidemiology, Lady Davis Carmel Medical Center, Haifa, Israel.
⁶⁶ Ruth and Bruce Rappaport Faculty of Medicine, Technion-Israel Institute of Technology, Haifa, Israel.
⁶⁷ Clalit National Cancer Control Center, Haifa, Israel.
⁶⁸ Department of Genetics and Genome Sciences, Case Western Reserve University, Cleveland, OH, USA.
⁶⁹ Department of Medicine and Epidemiology, University of Pittsburgh Medical Center, Pittsburgh, PA, USA.
⁷⁰ Biostatistics Division, Kaiser Permanente Washington Health Research Institute, Seattle, WA, USA.
⁷¹ SWOG Statistical Center, Fred Hutchinson Cancer Center, Seattle, WA, USA.
⁷² Division of Laboratory Genetics, Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, MN, USA.
⁷³ Division of Human Nutrition and Health, Wageningen University & Research, Wageningen, The Netherlands.
⁷⁴ Department of Molecular Biology of Cancer, Institute of Experimental Medicine of the Czech Academy of Sciences, Prague, Czech Republic.
⁷⁵ Institute of Biology and Medical Genetics, First Faculty of Medicine, Charles University, Prague, Czech Republic.
⁷⁶ Faculty of Medicine and Biomedical Center in Pilsen, Charles University, Pilsen, Czech Republic.
⁷⁷ Memorial University of Newfoundland, Discipline of Genetics, St. John's, NL, Canada.
⁷⁸ Department of Biostatistics, University of Washington, Seattle, WA, USA.

^# Contributed equally.

PMID: 37365285
PMCID: PMC10403521
DOI: 10.1038/s41416-023-02312-z

Probing the diabetes and colorectal cancer relationship using gene - environment interaction analyses

Niki Dimou et al. Br J Cancer. 2023 Aug.

. 2023 Aug;129(3):511-520.

doi: 10.1038/s41416-023-02312-z. Epub 2023 Jun 26.

Authors

Affiliations

¹ Nutrition and Metabolism Branch, International Agency for Research on Cancer, Lyon, France. DimouN@iarc.who.int.
² Division of Biostatistics, Department of Population and Public Health Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
³ Nutrition and Metabolism Branch, International Agency for Research on Cancer, Lyon, France.
⁴ Unit of Biomarkers and Susceptibility, Oncology Data Analytics Program, Catalan Institute of Oncology, Barcelona, 08908, Spain.
⁵ Colorectal Cancer Group, ONCOBELL Program, Bellvitge Biomedical Research Institute, Barcelona, 08908, Spain.
⁶ Consortium for Biomedical Research in Epidemiology and Public Health, Barcelona, 08908, Spain.
⁷ Department of Clinical Sciences, Faculty of Medicine, University of Barcelona, Barcelona, 08908, Spain.
⁸ Department of Genetics, Stanford University, Stanford, CA, USA.
⁹ Department of Computer Science, Stanford University, Stanford, CA, USA.
¹⁰ School of Public Health, Imperial College London, London, United Kingdom.
¹¹ Department of Hygiene and Epidemiology, University of Ioannina School of Medicine, Ioannina, Greece.
¹² Department of Epidemiology and Population Health, Albert Einstein College of Medicine, Bronx, NY, USA.
¹³ Department of Public Health Sciences, Center for Public Health Genomics, Charlottesville, VA, USA.
¹⁴ Lunenfeld Tanenbaum Research Institute, Mount Sinai Hospital, University of Toronto, Toronto, ON, Canada.
¹⁵ Center for Precision Medicine, Department of Medical Oncology and Therapeutics Research, City of Hope National Medical Center, Duarte, CA, USA.
¹⁶ Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne, Melbourne, Victoria, Australia.
¹⁷ Public Health Sciences Division, Fred Hutchinson Cancer Center, Seattle, WA, USA.
¹⁸ Oncology Data Analytics Program, Catalan Institute of Oncology-IDIBELL, L'Hospitalet de Llobregat, Barcelona, Spain.
¹⁹ CIBER Epidemiología y Salud Pública (CIBERESP), Madrid, Spain.
²⁰ ONCOBEL Program, Bellvitge Biomedical Research Institute (IDIBELL), L'Hospitalet de Llobregat, Barcelona, Spain.
²¹ Department of Nutritional Sciences, University of Michigan School of Public Health, Ann Arbor, MI, USA.
²² Department of Population and Public Health Sciences & USC Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
²³ Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany.
²⁴ School of Public Health, Capital Medical University, Beijing, China.
²⁵ Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ), Heidelberg, Germany.
²⁶ Department of Epidemiology, Geisel School of Medicine at Dartmouth, Hanover, NH, USA.
²⁷ Bioinformatics and Data Science Research Center, Bina Nusantara University, Jakarta, Indonesia.
²⁸ BioRealm LLC, Walnut, CA, USA.
²⁹ Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.
³⁰ Nantes Université, CHU Nantes, Service de Génétique médicale, F-44000, Nantes, France.
³¹ Leeds Institute of Cancer and Pathology, University of Leeds, Leeds, UK.
³² Division of Preventive Oncology, German Cancer Research Center (DKFZ) and National Center for Tumor Diseases (NCT), Heidelberg, Germany.
³³ German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany.
³⁴ Computer Science Department, School of Computer Science, Bina Nusantara University, Jakarta, Indonesia.
³⁵ Colorectal Cancer Group, ONCOBELL Program, Bellvitge Biomedical Research Institute (IDIBELL), L'Hospitalet de Llobregat, 8908, Barcelona, Spain.
³⁶ Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA.
³⁷ Channing Division of Network Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA, USA.
³⁸ Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA.
³⁹ Broad Institute of Harvard and MIT, Cambridge, MA, USA.
⁴⁰ Department of Epidemiology, Harvard T.H. Chan School of Public Health, Harvard University, Boston, MA, USA.
⁴¹ Department of Immunology and Infectious Diseases, Harvard T.H. Chan School of Public Health, Harvard University, Boston, MA, USA.
⁴² University Medical Centre Hamburg-Eppendorf, University Cancer Centre Hamburg (UCCH), Hamburg, Germany.
⁴³ Medical Faculty Heidelberg, Heidelberg University, Heidelberg, Germany.
⁴⁴ Department of General Surgery, University of Virginia School of Medicine, Charlottesville, VA, USA.
⁴⁵ Department of Family Medicine, University of Virginia, Charlottesville, VA, USA.
⁴⁶ Clinical & Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA.
⁴⁷ Department of Medicine, Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, CA, USA.
⁴⁸ Cancer Epidemiology Division, Cancer Council Victoria, Melbourne, VIC, Australia.
⁴⁹ Precision Medicine, School of Clinical Sciences at Monash Health, Monash University, Clayton, VIC, Australia.
⁵⁰ Center for Cancer Research, Medical University of Vienna, Vienna, Austria.
⁵¹ Center for Gastrointestinal Biology and Disease, University of North Carolina, Chapel Hill, NC, USA.
⁵² Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden.
⁵³ University of Hawaii Cancer Center, Honolulu, HI, USA.
⁵⁴ School of Public Health, University of Washington, Seattle, WA, USA.
⁵⁵ Department of Population Science, American Cancer Society, Atlanta, GA, USA.
⁵⁶ Unit of Nutrition, Environment and Cancer, Cancer Epidemiology Research Program, Catalan Institute of Oncology (ICO-IDIBELL), Avda Gran Via Barcelona 199-203, 08908L'Hospitalet de Llobregat, Barcelona, Spain.
⁵⁷ Huntsman Cancer Institute, University of Utah, Salt Lake City, UT, USA.
⁵⁸ Department of Population Health Sciences, University of Utah, Salt Lake City, UH, USA.
⁵⁹ Department of Laboratory Medicine and Pathology, Mayo Clinic Arizona, Scottsdale, AZ, USA.
⁶⁰ Slone Epidemiology Center at Boston University, Boston, MA, USA.
⁶¹ Department of Public Health and Primary Care, University of Cambridge, Cambridge, UK.
⁶² Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA.
⁶³ Department of Epidemiology, School of Public Health, University of Washington, Seattle, WA, USA.
⁶⁴ Research Centre for Hauora and Health, Massey University, Wellington, New Zealand.
⁶⁵ Department of Community Medicine and Epidemiology, Lady Davis Carmel Medical Center, Haifa, Israel.
⁶⁶ Ruth and Bruce Rappaport Faculty of Medicine, Technion-Israel Institute of Technology, Haifa, Israel.
⁶⁷ Clalit National Cancer Control Center, Haifa, Israel.
⁶⁸ Department of Genetics and Genome Sciences, Case Western Reserve University, Cleveland, OH, USA.
⁶⁹ Department of Medicine and Epidemiology, University of Pittsburgh Medical Center, Pittsburgh, PA, USA.
⁷⁰ Biostatistics Division, Kaiser Permanente Washington Health Research Institute, Seattle, WA, USA.
⁷¹ SWOG Statistical Center, Fred Hutchinson Cancer Center, Seattle, WA, USA.
⁷² Division of Laboratory Genetics, Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, MN, USA.
⁷³ Division of Human Nutrition and Health, Wageningen University & Research, Wageningen, The Netherlands.
⁷⁴ Department of Molecular Biology of Cancer, Institute of Experimental Medicine of the Czech Academy of Sciences, Prague, Czech Republic.
⁷⁵ Institute of Biology and Medical Genetics, First Faculty of Medicine, Charles University, Prague, Czech Republic.
⁷⁶ Faculty of Medicine and Biomedical Center in Pilsen, Charles University, Pilsen, Czech Republic.
⁷⁷ Memorial University of Newfoundland, Discipline of Genetics, St. John's, NL, Canada.
⁷⁸ Department of Biostatistics, University of Washington, Seattle, WA, USA.

^# Contributed equally.

PMID: 37365285
PMCID: PMC10403521
DOI: 10.1038/s41416-023-02312-z

Abstract

Background: Diabetes is an established risk factor for colorectal cancer. However, the mechanisms underlying this relationship still require investigation and it is not known if the association is modified by genetic variants. To address these questions, we undertook a genome-wide gene-environment interaction analysis.

Methods: We used data from 3 genetic consortia (CCFR, CORECT, GECCO; 31,318 colorectal cancer cases/41,499 controls) and undertook genome-wide gene-environment interaction analyses with colorectal cancer risk, including interaction tests of genetics(G)xdiabetes (1-degree of freedom; d.f.) and joint testing of Gxdiabetes, G-colorectal cancer association (2-d.f. joint test) and G-diabetes correlation (3-d.f. joint test).

Results: Based on the joint tests, we found that the association of diabetes with colorectal cancer risk is modified by loci on chromosomes 8q24.11 (rs3802177, SLC30A8 - OR_AA: 1.62, 95% CI: 1.34-1.96; OR_AG: 1.41, 95% CI: 1.30-1.54; OR_GG: 1.22, 95% CI: 1.13-1.31; p-value_3-d.f.: 5.46 × 10^-11) and 13q14.13 (rs9526201, LRCH1 - OR_GG: 2.11, 95% CI: 1.56-2.83; OR_GA: 1.52, 95% CI: 1.38-1.68; OR_AA: 1.13, 95% CI: 1.06-1.21; p-value_2-d.f.: 7.84 × 10^-09).

Discussion: These results suggest that variation in genes related to insulin signaling (SLC30A8) and immune function (LRCH1) may modify the association of diabetes with colorectal cancer risk and provide novel insights into the biology underlying the diabetes and colorectal cancer relationship.

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Conflict of interest statement

The authors declare no competing interests.

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Probing the diabetes and colorectal cancer relationship using gene - environment interaction analyses

Affiliations

Probing the diabetes and colorectal cancer relationship using gene - environment interaction analyses

Authors

Affiliations

Abstract

Conflict of interest statement

References

Publication types

MeSH terms

Substances

Grants and funding

LinkOut - more resources

Full Text Sources

Medical

Molecular Biology Databases