1,988
Views
0
CrossRef citations to date
0
Altmetric
Research Article

Altered PTPRD DNA Methylation Associates with Restricted Adipogenesis in Healthy First-Degree Relatives of Type 2 Diabetes Subjects

, , , , , , , , , , , , , & show all
Pages 873-888 | Received 12 Sep 2019, Accepted 17 Mar 2020, Published online: 02 Jun 2020

References

  • Lönn M , MehligK , BengtssonC , LissnerL. Adipocyte size predicts incidence of Type 2 diabetes in women. FASEB J.24, 326“331 (2010).
  • Longo M , RacitiGA , ZatteraleFet al. Epigenetic modifications of the Zfp/ZNF423 gene control murine adipogenic commitment and are dysregulated in human hypertrophic obesity. Diabetologia61, 369“380 (2018).
  • Longo M , ZatteraleF , NaderiJet al. Adipose tissue dysfunction as determinant of obesity-associated metabolic complications. Int. J. Mol. Sci.20(9), 2358 (2019).
  • Arner P , ArnerE , HammarstedtA , SmithU. Genetic predisposition for Type 2 diabetes, but not for overweight/obesity, is associated with a restricted adipogenesis. PLoS ONE6, e18284 (2011).
  • InterAct Consortium , ScottRA , LangenbergCet al. The link between family history and risk of Type 2 diabetes is not explained by anthropometric, lifestyle or genetic risk factors: the EPIC-InterAct study. Diabetologia56, 60“69 (2013).
  • Henninger AM , EliassonB , JenndahlLE , HammarstedtA. Adipocyte hypertrophy, inflammation and fibrosis characterize subcutaneous adipose tissue of healthy, non-obese subjects predisposed to Type 2 diabetes. PLoS ONE9, e105262 (2014).
  • Lotta LA , GulatiP , DayFRet al. Integrative genomic analysis implicates limited peripheral adipose storage capacity in the pathogenesis of human insulin resistance. Nat. Genet.49, 17“26 (2014).
  • Cederberg H , Stancˇakov ´A , KuusistoJ , LaaksoM , SmithU. Family history of Type 2 diabetes increases the risk of both obesity and its complications: is Type 2 diabetes a disease of inappropriate lipid storage?J. Intern. Med.277, 540“551 (2015).
  • Smith U , KahnBB. Adipose tissue regulates insulin sensitivity: role of adipogenesis, de novo lipogenesis and novel lipids. J. Intern. Med.280, 465“475 (2016).
  • Acosta JR , DouagiI , AnderssonDPet al. Increased fat cell size: a major phenotype of subcutaneous white adipose tissue in non-obese individuals with Type 2 diabetes. Diabetologia59, 560“570 (2016).
  • Multhaup ML , SeldinMM , JaffeAEet al. Mouse-human experimental epigenetic analysis unmasks dietary targets and genetic liability for diabetic phenotypes. Cell Metab.21, 138“149 (2015).
  • Keller M , HoppL , LiuXet al. Genome-wide DNA promoter methylation and transcriptome analysis in human adipose tissue unravels novel candidate genes for obesity. Mol. Metab.6, 86“100 (2016).
  • Rönn T , VolkovP , DavegÃ¥rdhCet al. A six months exercise intervention influences the genome-wide DNA methylation pattern in human adipose tissue. PLoS Genet.9, e1003572 (2013).
  • Vazquez G , DuvalS , JacobsDRJr , SilventoinenK. Comparison of body mass index, waist circumference, and waist/hip ratio in predicting incident diabetes: a meta-analysis. Epidemiol. Rev.29, 115“128 (2007).
  • Broholm C , OlssonAH , PerfilyevAet al. Human adipogenesis is associated with genome-wide DNA methylation and gene-expression changes. Epigenomics8, 1601“1617 (2016).
  • Parrillo L , SpinelliR , NicolòAet al. Nutritional factors, DNA methylation, and risk of Type 2 diabetes and obesity: perspectives and challenges. Int. J. Mol. Sci.20(12), 2983 (2019).
  • Parrillo L , CostaV , RacitiGAet al. Hoxa5 undergoes dynamic DNA methylation and transcriptional repression in the adipose tissue of mice exposed to high-fat diet. Int. J. Obes.40, 929“937 (2016).
  • Laakso M , ZilinskaiteJ , HansenTet al. Insulin sensitivity, insulin release and glucagon-like peptide-1 levels in persons with impaired fasting glucose and/or impaired glucose tolerance in the EUGENE2 study. Diabetologia51, 502“511 (2008).
  • Isakson P , HammarstedtA , GustafsonB , SmithU. Impaired preadipocyte differentiation in human abdominal obesity: role of Wnt, tumor necrosis factor-alpha, and inflammation. Diabetes58, 1550“1557 (2009).
  • Desiderio A , LongoM , ParrilloLet al. Epigenetic silencing of the ANKRD26 gene correlates to the pro-inflammatory profile and increased cardio-metabolic risk factors in human obesity. Clin. Epigenetics11, 181 (2019).
  • Li H , HandsakerB , WysokerAet al. The Sequence Alignment/Map format and SAMtools. Bioinformatics25, 2078“2079 (2009).
  • Zhang Y , LiuT , MeyerCAet al. Model-based analysis of ChIP-Seq (MACS). Genome Biol.9, R137 (2008).
  • Robinson MD , McCarthyDJ , SmythGK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics26, 139“140 (2010).
  • Benjamini Y , HochbergY. Controlling the false discovery rate “ a practical and powerful approach to multiple testing. J. Royal Statist. Soc., Series B.57, 289“300 (1995).
  • Li B , DeweyCN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics12, 323 (2011).
  • de Cristofaro T , DiPalma T , FicheraIet al. An essential role for Pax8 in the transcriptional regulation of cadherin-16 in thyroid cells. Mol. Endocrinol.26, 67“78 (2012).
  • Raciti GA , SpinelliR , DesiderioAet al. Specific CpG hyper-methylation leads to Ankrd26 gene down-regulation in white adipose tissue of a mouse model of diet-induced obesity. Sci. Rep.7, 43526 (2017).
  • Liotti A , CabaroS , CimminoIet al. Prep1 deficiency improves metabolic response in white adipose tissue. Biochim. Biophys. Acta1863(5), 515“525 (2018).
  • Longo M , SpinelliR , D’EspositoVet al. Pathologic endoplasmic reticulum stress induced by glucotoxic insults inhibits adipocyte differentiation and induces an inflammatory phenotype. Biochim. Biophys. Acta1863, 1146“1156 (2016).
  • Lyko F . The DNA methyltransferase family: a versatile toolkit for epigenetic regulation. Nat. Rev. Genet.19, 81“92 (2018).
  • Tsai FJ , YangCF , ChenCCet al. A genome-wide association study identifies susceptibility variants for Type 2 diabetes in Han Chinese. PLoS Genet.6, e1000847 (2010).
  • Barciszewska AM , NowakS , NaskrÄ™t-BarciszewskaMZ. The degree of global DNA hypomethylation in peripheral blood correlates with that in matched tumor tissues in several neoplasia. PLoS ONE9, e92599 (2014).
  • Laakso M . Biomarkers for Type 2 diabetes. Mol. Metab.27S, S139“S146 (2019).
  • Nilsson E , MatteA , PerfilyevAet al. Epigenetic alterations in human liver from subjects with Type 2 diabetes in parallel with reduced folate levels. J. Clin. Endocrinol. Metab.100, e1491“e1501 (2015).
  • Dayeh T , VolkovP , SalöSet al. Genome-wide DNA methylation analysis of human pancreatic islets from type 2 diabetic and nondiabetic donors identifies candidate genes that influence insulin secretion. PLoS Genet.10(3), e1004160 (2014).
  • Crujeiras AB , Diaz-LagaresA , SandovalJet al. DNA methylation map in circulating leukocytes mirrors subcutaneous adipose tissue methylation pattern: a genome-wide analysis from non-obese and obese patients. Sci. Rep.7, 41903 (2017).
  • Nitert MD , DayehT , VolkovPet al. Impact of an exercise intervention on DNA methylation in skeletal muscle from first-degree relatives of patients with Type 2 diabetes. Diabetes61, 3322“3332 (2012).
  • Chen T , UedaY , DodgeJE , WangZ , LiE. Establishment and maintenance of genomic methylation patterns in mouse embryonic stem cells by Dnmt3a and Dnmt3b. Mol. Cell. Biol.23, 5594“5605 (2003).
  • Liao J , KarnikR , GuHet al. Targeted disruption of DNMT1, DNMT3A and DNMT3B in human embryonic stem cells. Nat. Genet.47, 469“478 (2015).
  • Yang X , WuR , ShanW , YuL , XueB , ShiH. DNA methylation biphasically regulates 3T3-L1 preadipocyte differentiation. Mol. Endocrinol.30, 677“687 (2016).
  • Guo W , ChenJ , YangY , ZhuJ , WuJ. Epigenetic programming of Dnmt3a mediated by AP2α is required for granting preadipocyte the ability to differentiate. Cell Death Dis.7, e2496 (2016).
  • Zhang P , ZhaoM , LiangGet al. Whole-genome DNA methylation in skin lesions from patients with psoriasis vulgaris. J. Autoimmun.41, 17“24 (2013).
  • Maunakea AK , NagarajanRP , BilenkyMet al. Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature466, 253“257 (2010).
  • Jones PA . Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat. Rev. Genet.13, 484“492 (2012).
  • Blattler A , YaoL , WittHet al. Global loss of DNA methylation uncovers intronic enhancers in genes showing expression changes. Genome Biol.15, 469 (2014).
  • Bakshi A , BretzCL , CainTL , KimJ. Intergenic and intronic DNA hypomethylated regions as putative regulators of imprinted domains. Epigenomics10, 445“461 (2018).
  • Toker AW . Protein tyrosine phosphatases and signalling. J. Endocrinol.185, 19“33 (2005).
  • Ren JM , LiPM , ZhangWRet al. Transgenic mice deficient in the LAR protein-tyrosine phosphatase exhibit profound defects in glucose homeostasis. Diabetes47, 493“497 (1998).
  • Chagnon MJ , ElcheblyM , UetaniNet al. Altered glucose homeostasis in mice lacking the receptor protein tyrosine phosphatase sigma. Can. J. Physiol. Pharmacol.84, 755“763 (2006).
  • Batt J , AsaS , FladdC , RotinD. Pituitary, pancreatic and gut neuroendocrine defects in protein tyrosine phosphatase-sigma-deficient mice. Mol. Endocrinol.16, 155“169 (2002).
  • Kim WK , JungH , KimDHet al. Regulation of adipogenic differentiation by LAR tyrosine phosphatase in human mesenchymal stem cells and 3T3-L1 preadipocytes. J. Cell Sci.122, 4160“4167 (2009).
  • Corbin LJ , RichmondRC , WadeKHet al. BMI as a modifiable risk factor for Type 2 diabetes: refining and understanding causal estimates using mendelian randomization. Diabetes65, 3002“3007 (2016).
  • Kivimäki M , KuosmaE , FerrieJEet al. Overweight, obesity, and risk of cardiometabolic multimorbidity: pooled analysis of individual-level data for 120 813 adults from 16 cohort studies from the USA and Europe. Lancet Public Health2, e277“e285 (2016).
  • Chen YT , LinWD , LiaoWL , LinYJ , ChangJG , TsaiFJ. PTPRD silencing by DNA hypermethylation decreases insulin receptor signaling and leads to Type 2 diabetes. Oncotarget6, 12997“13005 (2015).