Adipose tissue transcriptomics and epigenomics in low birthweight men and controls: role of high-fat overfeeding

Diabetologia

Volumn 59, Issue 4, 2016, Pages 799-812

  Gillberg, Linn ^a,b   Perfilyev, Alexander ^c   Brøns, Charlotte ^a   Thomasen, Martin ^a   Grunnet, Louise G ^a   Volkov, Petr ^c   Rosqvist, Fredrik ^d   Iggman, David ^d,e   Dahlman, Ingrid ^f   Risérus, Ulf ^d   Rönn, Tina ^c   Nilsson, Emma ^a,c   Vaag, Allan ^a,b   Ling, Charlotte ^c  

^a Rigshospitalet   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c LUND UNIVERSITY   (Sweden)

^d UPPSALA UNIVERSITY   (Sweden)

^e Center for Clinical Research Dalarna   (Sweden)

^f KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Diet; Epigenetics; Gene expression; High fat overfeeding; Low birthweight; Metabolism; Obesity; Type 2 diabetes

Indexed keywords

FATTY ACID TRANSPORTER; MESSENGER RNA; ACYL COENZYME A DESATURASE; COMPLEXIN I; FADS2 PROTEIN, HUMAN; NERVE PROTEIN; TRANSCRIPTOME; VESICULAR TRANSPORT ADAPTOR PROTEIN;

1 ACYLGLYCEROL 3 PHOSPHATE O ACYLTRANSFERASE 9 GENE; ADIPOSE TISSUE; ARTICLE; ATP CITRATE LYASE GENE; BIRTH WEIGHT; CDK5 GENE; CELL COMPOSITION; CELL DEATH INDUCING DFFA LIKE EFFECTOR A GENE; CLINICAL ARTICLE; CONTROLLED STUDY; CPG ISLAND; CPLX1 GENE; CREATINE KINASE MITOCHONDRIAL 2 GENE; DIACYLGLYCEROL O ACYLTRANSFERASE 2 GENE; DNA METHYLATION; ELOVL FATTY ACID ELONGASE 6 GENE; EPIGENETICS; FATTY ACID DESATURASE 2 GENE; GASDERMIN B GENE; GENE; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; IGFBP5 GENE; INSULIN RESISTANCE; LEUCINE RICH REPEAT NEURONAL 3 GENE; LIPID DIET; LOW BIRTH WEIGHT; MALE; MICROARRAY ANALYSIS; NEURONATIN GENE; NON INSULIN DEPENDENT DIABETES MELLITUS; OBESITY; OVERNUTRITION; PATCHED DOMAIN CONTAINING 3 GENE; PHOSPHOLIPASE A2 GROUP IIA; PRIORITY JOURNAL; SOLUTE CARRIER FAMILY 2 MEMBER 5 GENE; SOLUTE CARRIER FAMILY 27 MEMBER 2 GENE; STEAROYL COA DESATURASE GENE; SUBCUTANEOUS FAT; TESTIS SPECIFIC TRANSCRIPT Y LINKED 9A; THROMBOSPONDIN 1 GENE; TRANSCRIPTOMICS; UPREGULATION; UROTENSIN 2 DOMAIN GENE; ADULT; ADVERSE EFFECTS; GENETICS; METABOLISM; PHYSIOLOGY; YOUNG ADULT;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ADIPOSE TISSUE; ADULT; DIABETES MELLITUS, TYPE 2; DIET, HIGH-FAT; DNA METHYLATION; EPIGENOMICS; FATTY ACID DESATURASES; HUMANS; INFANT, LOW BIRTH WEIGHT; MALE; NERVE TISSUE PROTEINS; TRANSCRIPTOME; YOUNG ADULT;

EID: 84959547501     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-015-3852-9     Document Type: Article

References (44)

1. Brons C, Jacobsen S, Hiscock N et al (2012) Effects of high-fat overfeeding on mitochondrial function, glucose and fat metabolism, and adipokine levels in low-birth-weight subjects. Am J Physiol Endocrinol Metab 302:E43–E51
2. Cornier MA, Bergman BC, Bessesen DH (2006) The effects of short-term overfeeding on insulin action in lean and reduced-obese individuals. Metabolism 55:1207–1214
3. Li Y, Ley SH, Tobias DK et al (2015) Birth weight and later life adherence to unhealthy lifestyles in predicting type 2 diabetes: prospective cohort study. BMJ 351:h3672
4. Whincup PH, Kaye SJ, Owen CG et al (2008) Birth weight and risk of type 2 diabetes: a systematic review. JAMA 300:2886–2897
5. Brons C, Jacobsen S, Nilsson E et al (2010) Deoxyribonucleic acid methylation and gene expression of PPARGC1A in human muscle is influenced by high-fat overfeeding in a birth-weight-dependent manner. J Clin Endocrinol Metab 95:3048–3056
6. Gillberg L, Jacobsen SC, Ronn T, Brons C, Vaag A (2014) PPARGC1A DNA methylation in subcutaneous adipose tissue in low birth weight subjects—impact of 5 days of high-fat overfeeding. Metabolism 63:263–271
7. Jacobsen SC, Brons C, Bork-Jensen J et al (2012) Effects of short-term high-fat overfeeding on genome-wide DNA methylation in the skeletal muscle of healthy young men. Diabetologia 55:3341–3349
8. Kirchner H, Osler ME, Krook A, Zierath JR (2013) Epigenetic flexibility in metabolic regulation: disease cause and prevention? Trends Cell Biol 23:203–209
9. Nilsson E, Jansson PA, Perfilyev A et al (2014) Altered DNA methylation and differential expression of genes influencing metabolism and inflammation in adipose tissue from subjects with type 2 diabetes. Diabetes 63:2962–2976
10. Nitert MD, Dayeh T, Volkov P et al (2012) Impact of an exercise intervention on DNA methylation in skeletal muscle from first-degree relatives of patients with type 2 diabetes. Diabetes 61:3322–3332
11. Ronn T, Volkov P, Davegardh C et al (2013) A six months exercise intervention influences the genome-wide DNA methylation pattern in human adipose tissue. PLoS Genet 9:e1003572
12. Ronn T, Volkov P, Gillberg L et al (2015) Impact of age, BMI and HbA1c levels on the genome-wide DNA methylation and mRNA expression patterns in human adipose tissue and identification of epigenetic biomarkers in blood. Hum Mol Genet 24:3792–3813
13. Jacobsen SC, Gillberg L, Bork-Jensen J et al (2014) Young men with low birthweight exhibit decreased plasticity of genome-wide muscle DNA methylation by high-fat overfeeding. Diabetologia 57:1154–1158
14. Ouchi N, Parker JL, Lugus JJ, Walsh K (2011) Adipokines in inflammation and metabolic disease. Nat Rev Immunol 11:85–97
15. Smith U (2002) Impaired (‘diabetic’) insulin signaling and action occur in fat cells long before glucose intolerance—is insulin resistance initiated in the adipose tissue? Int J Obes Relat Metab Disord 26:897–904
16. Brons C, Jensen CB, Storgaard H et al (2009) Impact of short-term high-fat feeding on glucose and insulin metabolism in young healthy men. J Physiol 587:2387–2397
17. Kelley DE, Wing R, Buonocore C, Sturis J, Polonsky K, Fitzsimmons M (1993) Relative effects of calorie restriction and weight loss in noninsulin-dependent diabetes mellitus. J Clin Endocrinol Metab 77:1287–1293
18. Alligier M, Meugnier E, Debard C et al (2012) Subcutaneous adipose tissue remodeling during the initial phase of weight gain induced by overfeeding in humans. J Clin Endocrinol Metab 97:E183–E192
19. Shea J, French CR, Bishop J et al (2009) Changes in the transcriptome of abdominal subcutaneous adipose tissue in response to short-term overfeeding in lean and obese men. Am J Clin Nutr 89:407–415
20. Rosqvist F, Iggman D, Kullberg J et al (2014) Overfeeding polyunsaturated and saturated fat causes distinct effects on liver and visceral fat accumulation in humans. Diabetes 63:2356–2368
21. Franck N, Gummesson A, Jernas M et al (2011) Identification of adipocyte genes regulated by caloric intake. J Clin Endocrinol Metab 96:E413–E418
22. Brons C, Jensen CB, Storgaard H et al (2008) Mitochondrial function in skeletal muscle is normal and unrelated to insulin action in young men born with low birth weight. J Clin Endocrinol Metab 93:3885–3892
23. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC (1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28:412–419
24. Poulsen P, Grunnet LG, Pilgaard K et al (2009) Increased risk of type 2 diabetes in elderly twins. Diabetes 58:1350–1355
25. Irizarry RA, Hobbs B, Collin F et al (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4:249–264
26. Bibikova M, Barnes B, Tsan C et al (2011) High density DNA methylation array with single CpG site resolution. Genomics 98:288–295
27. Houseman EA, Molitor J, Marsit CJ (2014) Reference-free cell mixture adjustments in analysis of DNA methylation data. Bioinformatics 30:1431–1439
28. Leff T, Granneman JH (2010) Adipose tissue in health and disease. Wiley-VCH Verlag, Weinheim
29. Jespersen NZ, Larsen TJ, Peijs L et al (2013) A classical brown adipose tissue mRNA signature partly overlaps with brite in the supraclavicular region of adult humans. Cell Metab 17:798–805
30. Melton EM, Cerny RL, Watkins PA, DiRusso CC, Black PN (2011) Human fatty acid transport protein 2a/very long chain acyl-CoA synthetase 1 (FATP2a/Acsvl1) has a preference in mediating the channeling of exogenous n-3 fatty acids into phosphatidylinositol. J Biol Chem 286:30670–30679
31. Jones PA (2012) Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 13:484–492
32. Pilgaard K, Faerch K, Carstensen B et al (2010) Low birthweight and premature birth are both associated with type 2 diabetes in a random sample of middle-aged Danes. Diabetologia 53:2526–2530
33. Yao M, Li J, Xie T et al (2015) Polymorphisms of rs174616 in the FADS1-FADS2 gene cluster is associated with a reduced risk of type 2 diabetes mellitus in northern Han Chinese people. Diabetes Res Clin Pract 109:206–212
34. Abderrahmani A, Niederhauser G, Plaisance V et al (2004) Complexin I regulates glucose-induced secretion in pancreatic beta-cells. J Cell Sci 117:2239–2247
35. Markan KR, Jurczak MJ, Allison MB et al (2010) Enhanced glycogen metabolism in adipose tissue decreases triglycerideride mobilization. Am J Physiol Endocrinol Metab 299:E117–E125
36. Virtue S, Vidal-Puig A (2010) Adipose tissue expandability, lipotoxicity and the metabolic syndrome—an allostatic perspective. Biochim Biophys Acta 1801:338–349
37. Melton EM, Cerny RL, DiRusso CC, Black PN (2013) Overexpression of human fatty acid transport protein 2/very long chain acyl-CoA synthetase 1 (FATP2/Acsvl1) reveals distinct patterns of trafficking of exogenous fatty acids. Biochem Biophys Res Commun 440:743–748
38. Lappas M (2014) Effect of pre-existing maternal obesity, gestational diabetes and adipokines on the expression of genes involved in lipid metabolism in adipose tissue. Metabolism 63:250–262
39. Soronen J, Laurila PP, Naukkarinen J et al (2012) Adipose tissue gene expression analysis reveals changes in inflammatory, mitochondrial respiratory and lipid metabolic pathways in obese insulin-resistant subjects. BMC Med Genomics 5:9
40. Taniguchi CM, Emanuelli B, Kahn CR (2006) Critical nodes in signalling pathways: insights into insulin action. Nat Rev Mol Cell Biol 7:85–96
41. Mootha VK, Lindgren CM, Eriksson KF et al (2003) PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34:267–273
42. Olsson AH, Yang BT, Hall E et al (2011) Decreased expression of genes involved in oxidative phosphorylation in human pancreatic islets from patients with type 2 diabetes. Eur J Endocrinol 165:589–595
43. Choi JH, Banks AS, Estall JL et al (2010) Anti-diabetic drugs inhibit obesity-linked phosphorylation of PPARgamma by Cdk5. Nature 466:451–456
44. Kouidhi S, Berrhouma R, Rouissi K et al (2013) Human subcutaneous adipose tissue Glut 4 mRNA expression in obesity and type 2 diabetes. Acta Diabetol 50:227–232