Regulatory variants at KLF14 influence type 2 diabetes risk via a female-specific effect on adipocyte size and body composition
Open accessAbstract
Individual risk of type 2 diabetes (T2D) is modified by perturbations to the mass, distribution and function of adipose tissue. To investigate the mechanisms underlying these associations, we explored the molecular, cellular and whole-body effects of T2D-associated alleles near KLF14. We show that KLF14 diabetes-risk alleles act in adipose tissue to reduce KLF14 expression and modulate, in trans, the expression of 385 genes. We demonstrate, in human cellular studies, that reduced KLF14 expression increases pre-adipocyte proliferation but disrupts lipogenesis, and in mice, that adipose tissue-specific deletion of Klf14 partially recapitulates the human phenotype of insulin resistance, dyslipidemia and T2D. We show that carriers of the KLF14 T2D risk allele shift body fat from gynoid stores to abdominal stores and display a marked increase in adipocyte cell size, and that these effects on fat distribution, and the T2D association, are female specific. The metabolic risk associated with variation at this imprinted locus depends on the sex both of the subject and of the parent from whom the risk allele derives.
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Similar functional descriptions have been reported for individual loci implicated in schizophrenia, cardiovascular disease, type 2 diabetes and Alzheimer's disease.
“Similar functional descriptions have been reported for individual loci implicated in schizo phrenia64, cardiovascular disease104, type 2 diabetes105 and Alzheimer’s disease106, among others.”
From A brief history of human disease genetics (2020) · cites this paper as [105]
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Self-citation
- Authors
- Small, K. S., Todorčević, M., Civelek, M., El-Sayed Moustafa, J. S., Wang, X., Simon, M. M., Fernandez-Tajes, J., Mahajan, A., Horikoshi, M., Hugill, A., Glastonbury, C. A., Quaye, L., Neville, M. J., Sethi, S., Yon, M., Pan, C., Che, N., Viñuela, A., Tsai, P.-C., Nag, A., Buil, A., Thorleifsson, G., Raghavan, A., Ding, Q., Morris, A. P., Bell, J. T., Thorsteinsdottir, U., Stefansson, K., Laakso, M., Dahlman, I., Arner, P., Gloyn, A. L., Musunuru, K., Lusis, A. J., Cox, R. D., Karpe, F., & McCarthy, M. I.
- Affiliations
- King's College London (GB)
- Churchill Hospital (GB)
- University of California, Los Angeles (US)
- University of Pennsylvania (US)
- Mary Lyon Centre at MRC Harwell (GB)
- Centre for Human Genetics (GB)
- University of Geneva (CH)
- Harvard University (US)
- Chinese Academy of Sciences (CN)
- University of Eastern Finland (FI)
- Karolinska Institutet (SE)
- Corresponding author
- Small, Kerrin S.
- McCarthy, Mark I.
- ORCID
- Small, Kerrin S.
- Todorčević, Marijana
- Civelek, Mete
- Wang, Xiao
- Simon, Michelle M.
- Fernandez-Tajes, Juan
- Mahajan, Anubha
- Horikoshi, Momoko
- Glastonbury, Craig A.
- Neville, Matt J.
- Sethi, Siddharth
- Yon, Marianne
- Pan, Calvin
- Viñuela, Ana
- Tsai, Pei-Chien
- Nag, Abhishek
- Buil, Alfonso
- Raghavan, Avanthi
- Ding, Qiurong
- Morris, Andrew P.
- Bell, Jordana T.
- Laakso, Markku
- Dahlman, Ingrid
- Arner, Peter
- Gloyn, Anna L.
- Lusis, Aldons J.
- Cox, Roger D.
- Karpe, Fredrik
- McCarthy, Mark I.
- Venue
- Nature Genetics
- Published
- 2018-04
- Volume
- 50
- Issue
- 4
- Pages
- 572-580
- ISSN
- 1061-4036 (ISSN-L)
- 1546-1718
- PMC
- PMC5935235
- OpenAlex
- W2796811655
- Cited by
- 168
- References
- 71
- Citations by year
- 2026: 3 · 2025: 11 · 2024: 29 · 2023: 22 · 2022: 24 · 2021: 25 · 2020: 22 · 2019: 19 · 2018: 13
- FWCI
- 15.41
- Type
- journal article
- Language
- en
- Update notices
- correction (2018-08-07)
- Open access
- Licence
- Locations
- Nature Genetics (publishedVersion)
- PubMed (publishedVersion)
- Research Explorer (The University of Manchester) (acceptedVersion, other-oa)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Discovery Research Portal (University of Dundee) (submittedVersion, other-oa)
- Research Portal (King's College London) (submittedVersion, other-oa)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- Wayne and Gladys Valley Foundation
- Kaiser Permanente
- Wellcome Trust (106130/Z/14/Z, 200837/Z/16/Z)
- National Institute for Health and Care Research (FP7/2007–2013, NF-SI-0611-10099)
- British Heart Foundation (RG17/1/32663)
- King's College London
- European Commission (201681, 259749, 2007–2013, FP7 2007-2013, 095101, FP7/2007, 203141, 098381, 200837)
- Tekes (1510/31/06)
- Novo Nordisk Fonden (NNF17OC0026888, NNF18OC0033896)
- National Institutes of Health (FP7/2007-2013, 095101)
- University of California, San Francisco
- Medical Research Council (FP7/20072013, /L020149/1, MR/L020149/1, L020149, J010642/1, MR/J010642/1, J010642, MR/L01999X/1, MC U142661184)
- NIHR Oxford Biomedical Research Centre
- National Institute on Aging (R01AG033067)
- National Heart, Lung, and Blood Institute (R00HL121172, P01HL028481)
- National Institute of Diabetes and Digestive and Kidney Diseases (106130, 090532, U01DK105535, R01DK099571, 098381, 203141)
- Topics
- Health Sciences › Medicine › Epidemiology › Adipokines, Inflammation, and Metabolic Diseases
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
- Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
- Keywords
- KLF14, type 2 diabetes, adipose tissue, adipocyte size, body fat distribution, sex differences, insulin resistance, dyslipidemia, genomic imprinting, lipogenesis, gene expression regulation
- MeSH terms
- Alleles, Animals, Body Composition, Diabetes Mellitus, Type 2, Enhancer Elements, Genetic, Female, Humans, Male, Mice, Inbred C57BL, Phenotype, Risk Factors, Sex Characteristics, Gene Expression, Adipocytes, Mice, Knockout, Genomic Imprinting, Cell Size, Lipogenesis, Body Fat Distribution, Mice, Sp Transcription Factors, Kruppel-Like Transcription Factors, Genome-Wide Association Study
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
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