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Targeted proteomics identifies potential biomarkers of dysglycaemia, beta cell function and insulin sensitivity in Black African men and women

Abstract

Aims/hypothesis

Using a targeted proteomics approach, we aimed to identify and validate circulating proteins associated with impaired glucose metabolism (IGM) and type 2 diabetes in a Black South African cohort. In addition, we assessed sex-specific associations between the validated proteins and pathophysiological pathways of type 2 diabetes.

Methods

This cross-sectional study included Black South African men (n=380) and women (n=375) who were part of the Middle-Aged Soweto Cohort (MASC). Dual-energy x-ray absorptiometry was used to determine fat mass and visceral adipose tissue, and fasting venous blood samples were collected for analysis of glucose, insulin and C-peptide and for targeted proteomics, measuring a total of 184 pre-selected protein biomarkers. An OGTT was performed on participants without diabetes, and peripheral insulin sensitivity (Matsuda index), HOMA-IR, basal insulin clearance, insulin secretion (C-peptide index) and beta cell function (disposition index) were estimated. Participants were classified as having normal glucose tolerance (NGT; n=546), IGM (n=116) or type 2 diabetes (n=93). Proteins associated with dysglycaemia (IGM or type 2 diabetes) in the MASC were validated in the Swedish EpiHealth cohort (NGT, n=1706; impaired fasting glucose, n=550; type 2 diabetes, n=210).

Results

We identified 73 proteins associated with dysglycaemia in the MASC, of which 34 were validated in the EpiHealth cohort. Among these validated proteins, 11 were associated with various measures of insulin dynamics, with the largest number of proteins being associated with HOMA-IR. In sex-specific analyses, IGF-binding protein 2 (IGFBP2) was associated with lower HOMA-IR in women (coefficient –0.35; 95% CI –0.44, –0.25) and men (coefficient –0.09; 95% CI –0.15, –0.03). Metalloproteinase inhibitor 4 (TIMP4) was associated with higher insulin secretion (coefficient 0.05; 95% CI 0.001, 0.11; p for interaction=0.025) and beta cell function (coefficient 0.06; 95% CI 0.02, 0.09; p for interaction=0.013) in women only. In contrast, a stronger positive association between IGFBP2 and insulin sensitivity determined using an OGTT (coefficient 0.38; 95% CI 0.27, 0.49) was observed in men (p for interaction=0.004). A posteriori analysis showed that the associations between TIMP4 and insulin dynamics were not mediated by adiposity. In contrast, most of the associations between IGFBP2 and insulin dynamics, except for insulin secretion, were mediated by either fat mass index or visceral adipose tissue in men and women. Fat mass index was the strongest mediator between IGFBP2 and insulin sensitivity (total effect mediated 40.7%; 95% CI 37.0, 43.6) and IGFBP2 and HOMA-IR (total effect mediated 39.1%; 95% CI 31.1, 43.5) in men.

Conclusions/interpretation

We validated 34 proteins that were associated with type 2 diabetes, of which 11 were associated with measures of type 2 diabetes pathophysiology such as peripheral insulin sensitivity and beta cell function. This study highlights biomarkers that are similar between cohorts of different ancestry, with different lifestyles and sociodemographic profiles. The African-specific biomarkers identified require validation in African cohorts to identify risk markers and increase our understanding of the pathophysiology of type 2 diabetes in African populations.

Graphical abstract

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Data availability

The datasets generated and/or analysed during the current study are available from the corresponding author on reasonable request.

Abbreviations

DI:

Disposition index

DXA:

Dual-energy x-ray absorptiometry

FDR:

False discovery rate

FMI:

Fat mass index

IFG:

Impaired fasting glucose

IGFBP2:

IGF-binding protein 2

IGM:

Impaired glucose metabolism

IGT:

Impaired glucose tolerance

KIM1:

Kidney injury molecule

MASC:

Middle-Aged Soweto Cohort

NGT:

Normal glucose tolerance

SAT:

Subcutaneous adipose tissue

SCF:

Stem cell factor

TIMP4:

Metalloproteinase inhibitor 4

TNFRSF11A:

TNF receptor superfamily member 11A

tPA:

Tissue-type plasminogen activator

VAT:

Visceral adipose tissue

VSIG2:

V-set and immunoglobulin domain-containing protein 2

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Acknowledgements

We are grateful to the participants in these cohorts, as well as the field staff of the Developmental Pathways for Health Research Unit. The graphical abstract was created with BioRender.com.

Authors’ relationships and activities

TO and TF are members of the Editorial Board of Diabetologia. The authors declare that there are no other relationships that might bias, or be perceived to bias, their work.

Contribution statement

All authors have participated sufficiently in the work represented by the article and take public responsibility for the content. Participation included (i) conception or design of the work presented by the article, (ii) drafting the article or revising it for critically important content, and (iii) final approval of the version to be published. AEM is responsible for the integrity of the work as a whole.

Funding

The study was jointly funded by the South African Medical Research Council via the South African National Department of Health, the UK Medical Research Council (via the Newton Fund) and the GSK Africa Non-Communicable Disease Open Lab (via supporting grant project number ES/N013891/1) and the South African National Research Foundation (grant number UID:99108) and Västerbotten County Council, Sweden. TC is an International Training Fellow supported by Wellcome Trust grant number 214205/Z/18/Z. The study sponsors/funders were not involved in the design of the study, the collection, analysis and interpretation of data or writing the report, and did not impose any restrictions regarding publication of the report.

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Mendham, A.E., Micklesfield, L.K., Karpe, F. et al. Targeted proteomics identifies potential biomarkers of dysglycaemia, beta cell function and insulin sensitivity in Black African men and women. Diabetologia (2022). https://doi.org/10.1007/s00125-022-05788-1

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Keywords

  • Adiposity
  • Beta cell function
  • Ethnicity
  • IGFBP2
  • Impaired glucose metabolism
  • Insulin clearance
  • Insulin secretion
  • Insulin sensitivity
  • Obesity
  • TIMP4
  • Type 2 diabetes