Growth differentiation factor 15 (GDF-15) is a potential biomarker of both diabetic kidney disease and future cardiovascular events in cohorts of individuals with type 2 diabetes: a proteomics approach

References

• Tuttle KR, Bakris GL, Bilous RW, Chiang JL, de Boer IH, Goldstein-Fuchs J, et al. Diabetic kidney disease: a report from an ADA Consensus Conference. Am J Kidney Dis. 2014;64:510–33.
   PubMed Web of Science ®Google Scholar
• Carlsson AC, Ingelsson E, Sundstrom J, Carrero JJ, Gustafsson S, Feldreich T, et al. Use of proteomics to investigate kidney function decline over 5 years. Clin J Am Soc Nephrol. 2017;12:1226–35.
   PubMed Web of Science ®Google Scholar
• Carlsson AC, Sundstrom J, Carrero JJ, Gustafsson S, Stenemo M, Larsson A, et al. Use of a proximity extension assay proteomics chip to discover new biomarkers associated with albuminuria. Eur J Prev Cardiolog. 2017;24:340–8.
   PubMed Web of Science ®Google Scholar
• Colhoun HM, Marcovecchio ML. Biomarkers of diabetic kidney disease. Diabetologia. 2018;61:996–1011.
   PubMed Web of Science ®Google Scholar
• Pena MJ, Mischak H, Heerspink HJ. Proteomics for prediction of disease progression and response to therapy in diabetic kidney disease. Diabetologia. 2016;59:1819–31.
   PubMed Web of Science ®Google Scholar
• Lind L, Fors N, Hall J, Marttala K, Stenborg A. A comparison of three different methods to evaluate endothelium-dependent vasodilation in the elderly: the Prospective Investigation of the Vasculature in Uppsala Seniors (PIVUS) study. Arterioscler Thromb Vasc Biol. 2005;25:2368–75.
   PubMed Web of Science ®Google Scholar
• Hedstrand H. A study of middle-aged men with particular reference to risk factors for cardiovascular disease. Ups J Med Sci Suppl. 1975;19:1–61.
   PubMedGoogle Scholar
• Carlsson AC, Arnlov J, Sundstrom J, Michaelsson K, Byberg L, Lind L. Physical activity, obesity and risk of cardiovascular disease in middle-aged men during a median of 30 years of follow-up. Eur J Prev Cardiolog. 2016;23:359–65.
   PubMed Web of Science ®Google Scholar
• Carlsson AC, Ostgren CJ, Nystrom FH, Lanne T, Jennersjo P, Larsson A, et al. Association of soluble tumor necrosis factor receptors 1 and 2 with nephropathy, cardiovascular events, and total mortality in type 2 diabetes. Cardiovasc Diabetol. 2016;15:40.
   PubMed Web of Science ®Google Scholar
• Assarsson E, Lundberg M, Holmquist G, Bjorkesten J, Thorsen SB, Ekman D, et al. Homogenous 96-plex PEA immunoassay exhibiting high sensitivity, specificity, and excellent scalability. PLoS One. 2014;9:e95192.
   PubMed Web of Science ®Google Scholar
• Ganna A, Salihovic S, Sundstrom J, Broeckling CD, Hedman AK, Magnusson PK, et al. Large-scale metabolomic profiling identifies novel biomarkers for incident coronary heart disease. PLoS Genet. 2014;10:e1004801.
   PubMed Web of Science ®Google Scholar
• Azur MJ, Stuart EA, Frangakis C, Leaf PJ. Multiple imputation by chained equations: what is it and how does it work?. Int J Methods Psychiatr Res. 2011;20:40–9.
   PubMed Web of Science ®Google Scholar
• Hougaard P. Frailty models for survival data. Lifetime Data Anal. 1995;1:255–73.
   PubMedGoogle Scholar
• R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, 2019. R Core Team [Internet]. Available from: https://www.R-project.org/.
   Google Scholar
• de Boer IH, Rue TC, Hall YN, Heagerty PJ, Weiss NS, Himmelfarb J. Temporal trends in the prevalence of diabetic kidney disease in the United States. JAMA 2011;305:2532–9.
   PubMed Web of Science ®Google Scholar
• Macisaac RJ, Ekinci EI, Jerums G. Markers of and risk factors for the development and progression of diabetic kidney disease. Am J Kidney Dis. 2014;63:S39–S62.
   PubMed Web of Science ®Google Scholar
• Moresco RN, De Carvalho J. Applying proteomics to diagnosis of diabetic kidney disease. Expert Rev Proteomics. 2017;14:841–3.
   PubMed Web of Science ®Google Scholar
• Schutte E, Gansevoort RT, Benner J, Lutgers HL, Lambers Heerspink HJ. Lambers Heerspink HJ. Will the future lie in multitude? A critical appraisal of biomarker panel studies on prediction of diabetic kidney disease progression. Nephrol Dial Transplant. 2015;30:iv96–104.
   PubMed Web of Science ®Google Scholar
• Looker HC, Colombo M, Hess S, Brosnan MJ, Farran B, Dalton RN, et al. Biomarkers of rapid chronic kidney disease progression in type 2 diabetes. Kidney Int. 2015;88:888–96.
   PubMed Web of Science ®Google Scholar
• Pena MJ, Heinzel A, Heinze G, Alkhalaf A, Bakker SJ, Nguyen TQ, et al. A panel of novel biomarkers representing different disease pathways improves prediction of renal function decline in type 2 diabetes. PLoS One. 2015;10:e0120995.
   PubMed Web of Science ®Google Scholar
• Adela R, Banerjee SK. GDF-15 as a Target and biomarker for diabetes and cardiovascular diseases: a translational prospective. J Diabetes Res. 2015;2015:490842.
   PubMed Web of Science ®Google Scholar
• Doerstling S, Hedberg P, Ohrvik J, Leppert J, Henriksen E. Growth differentiation factor 15 in a community-based sample: age-dependent reference limits and prognostic impact. Ups J Med Sci. 2018;123:86–93.
   PubMed Web of Science ®Google Scholar
• Gerstein HC, Pare G, Hess S, Ford RJ, Sjaarda J, Raman K, et al. Growth differentiation factor 15 as a novel biomarker for metformin. Diabetes Care. 2017;40:280–3.
   PubMed Web of Science ®Google Scholar
• Hong JH, Chung HK, Park HY, Joung KH, Lee JH, Jung JG, et al. GDF15 is a novel biomarker for impaired fasting glucose. Diabetes Metab J. 2014;38:472–9.
   PubMedGoogle Scholar
• Schernthaner-Reiter MH, Kasses D, Tugendsam C, Riedl M, Peric S, Prager G, et al. Growth differentiation factor 15 increases following oral glucose ingestion: effect of meal composition and obesity. Eur J Endocrinol. 2016;175:623–31.
   PubMed Web of Science ®Google Scholar
• Hamon SM, Griffin TP, Islam MN, Wall D, Griffin MD, O’Shea PM. Defining reference intervals for a serum growth differentiation factor-15 (GDF-15) assay in a Caucasian population and its potential utility in diabetic kidney disease (DKD). Clin Chem Lab Med. 2019;57:510–20.
   PubMed Web of Science ®Google Scholar
• Bao X, Borné Y, Muhammad IF, Nilsson J, Lind L, Melander O, et al. Growth differentiation factor 15 is positively associated with incidence of diabetes mellitus: the Malmo Diet and Cancer-Cardiovascular Cohort. Diabetologia 2019;62:78–86.
   PubMed Web of Science ®Google Scholar
• Hellemons ME, Mazagova M, Gansevoort RT, Henning RH, de Zeeuw D, Bakker SJ, et al. Growth-differentiation factor 15 predicts worsening of albuminuria in patients with type 2 diabetes. Diabetes Care. 2012;35:2340–6.
   PubMed Web of Science ®Google Scholar
• Lajer M, Jorsal A, Tarnow L, Parving HH, Rossing P. Plasma growth differentiation factor-15 independently predicts all-cause and cardiovascular mortality as well as deterioration of kidney function in type 1 diabetic patients with nephropathy. Diabetes Care. 2010;33:1567–72.
   PubMed Web of Science ®Google Scholar
• Yilmaz H, Celik HT, Gurel OM, Bilgic MA, Namuslu M, Bozkurt H, et al. Increased serum levels of GDF-15 associated with mortality and subclinical atherosclerosis in patients on maintenance hemodialysis. Herz 2015;40:305–12.
   PubMed Web of Science ®Google Scholar
• Wang TJ, Wollert KC, Larson MG, Coglianese E, McCabe EL, Cheng S, et al. Prognostic utility of novel biomarkers of cardiovascular stress: the Framingham Heart Study. Circulation. 2012;126:1596–604.
   PubMed Web of Science ®Google Scholar
• Bidadkosh A, Lambooy SPH, Heerspink HJ, Pena MJ, Henning RH, Buikema H, et al. Predictive properties of biomarkers GDF-15, NTproBNP, and hs-TnT for morbidity and mortality in patients with type 2 diabetes with nephropathy. Diabetes Care. 2017;40:784–92.
   PubMed Web of Science ®Google Scholar
• Frimodt-Moller M, von Scholten BJ, Reinhard H, Jacobsen PK, Hansen TW, Persson FI, et al. Growth differentiation factor-15 and fibroblast growth factor-23 are associated with mortality in type 2 diabetes - an observational follow-up study. PLoS One. 2018;13:e0196634.
   PubMed Web of Science ®Google Scholar
• Resl M, Clodi M, Vila G, Luger A, Neuhold S, Wurm R, et al. Targeted multiple biomarker approach in predicting cardiovascular events in patients with diabetes. Heart. 2016;102:1963–8.
   PubMed Web of Science ®Google Scholar
• Shin MY, Kim JM, Kang YE, Kim MK, Joung KH, Lee JH, et al. Association between growth differentiation factor 15 (GDF15) and cardiovascular risk in patients with newly diagnosed type 2 diabetes mellitus. J Korean Med Sci. 2016;31:1413–8.
   PubMed Web of Science ®Google Scholar
• Carlsson AC, Larsson A, Helmersson-Karlqvist J, Lind L, Ingelsson E, Larsson TE, et al. Urinary kidney injury molecule-1 and the risk of cardiovascular mortality in elderly men. Clin J Am Soc Nephrol. 2014;9:1393–401.
   PubMed Web of Science ®Google Scholar
• Carlsson AC, Larsson A, Helmersson-Karlqvist J, Lind L, Ingelsson E, Larsson TE, et al. Urinary kidney injury molecule 1 and incidence of heart failure in elderly men. Eur J Heart Fail. 2013;15:441–6.
   PubMed Web of Science ®Google Scholar
• Damman K, Masson S, Hillege HL, Maggioni AP, Voors AA, Opasich C, et al. Clinical outcome of renal tubular damage in chronic heart failure. Eur Heart J. 2011;32:2705–12.
   PubMed Web of Science ®Google Scholar
• Xu JR, Yang Y, Liu XM, Sun JY, Wang YJ. Polymorphisms of the TIM-1 gene are associated with rheumatoid arthritis in the Chinese Hui minority ethnic population. Genet Mol Res. 2012;11:61–9.
   PubMed Web of Science ®Google Scholar
• Lind L, Arnlov J, Lindahl B, Siegbahn A, Sundstrom J, Ingelsson E. Use of a proximity extension assay proteomics chip to discover new biomarkers for human atherosclerosis. Atherosclerosis. 2015;242:205–10.
   PubMed Web of Science ®Google Scholar
• Feldreich T, Nowak C, Fall T, Carlsson AC, Carrero JJ, Ripsweden J, et al. Circulating proteins as predictors of cardiovascular mortality in end-stage renal disease. J Nephrol. 2019;32:111–9.
   PubMed Web of Science ®Google Scholar
• David WS. Myoglobinuria. Neurol Clin. 2000;18:215–43.
   PubMed Web of Science ®Google Scholar
• Lenglet A, Liabeuf S, Desjardins L, Neirynck N, Glorieux G, Lemke HD, et al. Prognostic implications of plasma myoglobin levels in patients with chronic kidney disease. Int J Artif Organs. 2012;35:959–68.
   PubMed Web of Science ®Google Scholar
• Kousios A, Kouis P, Panayiotou AG. Matrix metalloproteinases and subclinical atherosclerosis in chronic kidney disease: a systematic review. Int J Nephrol. 2016;2016:1.
   Google Scholar
• Coll B, Rodriguez JA, Craver L, Orbe J, Martinez-Alonso M, Ortiz A, et al. Serum levels of matrix metalloproteinase-10 are associated with the severity of atherosclerosis in patients with chronic kidney disease. Kidney Int. 2010;78:1275–80.
   PubMed Web of Science ®Google Scholar
• Toni M, Hermida J, Goni MJ, Fernandez P, Parks WC, Toledo E, et al. Matrix metalloproteinase-10 plays an active role in microvascular complications in type 1 diabetic patients. Diabetologia. 2013;56:2743–52.
   PubMed Web of Science ®Google Scholar
• Vestra Saller DM, Mauer A, Fioretto M. P. Role of mesangial expansion in the pathogenesis of diabetic nephropathy. J Nephrol. 2001;14:S51–S7.
   PubMed Web of Science ®Google Scholar