Epigenome-wide and transcriptome-wide analyses reveal gestational diabetes is associated with alterations in the human leukocyte antigen complex

Clinical Epigenetics

Volumn 7, Issue 1, 2015, Pages

  Binder, Alexandra M ^a   LaRocca, Jessica ^b,c   Lesseur, Corina ^d   Marsit, Carmen J ^d   Michels, Karin B ^a,b,c  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b HARVARD UNIVERSITY   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

Gestational diabetes; Human leukocyte antigen; Methylome; Transcriptome

Indexed keywords

HLA A ANTIGEN; HLA B ANTIGEN; HLA C ANTIGEN; LEUKOCYTE ANTIGEN;

ANTIGEN ANTIBODY COMPLEX; ARTICLE; BODY MASS; CAPN1 GENE; CLINICAL ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; EPIGENETICS; ETHNICITY; FEMALE; FETAL REPROGRAMMING; FETUS DEVELOPMENT; GENE; GENE EXPRESSION; GENE FUNCTION; GENE LOCATION; GENE LOCUS; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOME ANALYSIS; HIGH RISK PREGNANCY; HLA A GENE; HLA B GENE; HLA C GENE; HLA DOA GENE; HUMAN; HUMAN TISSUE; IMMUNE RESPONSE; INTRON; MAJOR HISTOCOMPATIBILITY COMPLEX; MATERNAL AGE; MATERNAL SMOKING; PREGNANCY DIABETES MELLITUS; PREGNANCY OUTCOME; PRIORITY JOURNAL; PROMOTER REGION; RISK ASSESSMENT; SNRPN GENE; SNURF GENE; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS;

EID: 84938493701     PISSN: 18687075     EISSN: 18687083     Source Type: Journal    
DOI: 10.1186/s13148-015-0116-y     Document Type: Article

References (66)

1. Reece EA, Leguizamón G, Wiznitzer A. Gestational diabetes: the need for a common ground. Lancet. 2009;373:1789–97.
2. Ferrara A. Increasing prevalence of gestational diabetes mellitus: a public health perspective. Diabetes Care. 2007;30 Suppl 2:S141–146.
3. Catalano PM, Tyzbir ED, Wolfe RR, Roman NM, Amini SB, Sims EA. Longitudinal changes in basal hepatic glucose production and suppression during insulin infusion in normal pregnant women. Am J Obstet Gynecol. 1992;167(4 Pt 1):913–9.
4. Friedman JE, Ishizuka T, Shao J, Huston L, Highman T, Catalano P. Impaired glucose transport and insulin receptor tyrosine phosphorylation in skeletal muscle from obese women with gestational diabetes. Diabetes. 1999;48:1807–14.
5. O’Sullivan JB. Body weight and subsequent diabetes mellitus. JAMA. 1982;248:949–52.
6. Moore TR. Fetal exposure to gestational diabetes contributes to subsequent adult metabolic syndrome. Am J Obstet Gynecol. 2010;202:643–9.
7. Taricco E, Radaelli T, Nobile de Santis MS, Cetin I. Foetal and placental weights in relation to maternal characteristics in gestational diabetes. Placenta. 2003;24:343–7.
8. Gauster M, Desoye G, Tötsch M, Hiden U. The placenta and gestational diabetes mellitus. Curr Diab Rep. 2012;12:16–23.
9. Lappas M, Hiden U, Desoye G, Froehlich J, Hauguel-de Mouzon S, Jawerbaum A. The role of oxidative stress in the pathophysiology of gestational diabetes mellitus. Antioxid Redox Signal. 2011;15:3061–100.
10. Colomiere M, Permezel M, Riley C, Desoye G, Lappas M. Defective insulin signaling in placenta from pregnancies complicated by gestational diabetes mellitus. Eur J Endocrinol Eur Fed Endocr Soc. 2009;160:567–78.
11. Gaither K, Quraishi AN, Illsley NP. Diabetes alters the expression and activity of the human placental GLUT1 glucose transporter. J Clin Endocrinol Metab. 1999;84:695–701.
12. Desoye G, Gauster M, Wadsack C. Placental transport in pregnancy pathologies. Am J Clin Nutr. 2011;94(6 Suppl):1896S–902S.
13. Day PE, Cleal JK, Lofthouse EM, Hanson MA, Lewis RM. What factors determine placental glucose transfer kinetics? Placenta. 2013;34:953–8.
14. Weintrob N, Karp M, Hod M. Short- and long-range complications in offspring of diabetic mothers. J Diabetes Complications. 1996;10:294–301.
15. Catalano PM, Thomas A, Huston-Presley L, Amini SB. Increased fetal adiposity: a very sensitive marker of abnormal in utero development. Am J Obstet Gynecol. 2003;189:1698–704.
16. Cetin I, de Santis MSN, Taricco E, Radaelli T, Teng C, Ronzoni S, et al. Maternal and fetal amino acid concentrations in normal pregnancies and in pregnancies with gestational diabetes mellitus. Am J Obstet Gynecol. 2005;192:610–7.
17. Sánchez-Vera I, Bonet B, Viana M, Quintanar A, Martín MD, Blanco P, et al. Changes in plasma lipids and increased low-density lipoprotein susceptibility to oxidation in pregnancies complicated by gestational diabetes: consequences of obesity. Metabolism. 2007;56:1527–33.
18. Barker DJ. In utero programming of chronic disease. Clin Sci Lond Engl 1979. 1998;95:115–28.
19. Gluckman PD, Hanson MA, Cooper C, Thornburg KL. Effect of in utero and early-life conditions on adult health and disease. N Engl J Med. 2008;359:61–73.
20. Hochberg Z, Feil R, Constancia M, Fraga M, Junien C, Carel J-C, et al. Child health, developmental plasticity, and epigenetic programming. Endocr Rev. 2011;32:159–224.
21. Enquobahrie DA, Williams MA, Qiu C, Meller M, Sorensen TK. Global placental gene expression in gestational diabetes mellitus. Am J Obstet Gynecol. 2009;200:206. e1–13.
22. Radaelli T, Lepercq J, Varastehpour A, Basu S, Catalano PM, Hauguel-De Mouzon S. Differential regulation of genes for fetoplacental lipid pathways in pregnancy with gestational and type 1 diabetes mellitus. Am J Obstet Gynecol. 2009;201:209. e1–209.e10.
23. Radaelli T, Varastehpour A, Catalano P, Mouzon SH. Gestational diabetes induces placental genes for chronic stress and inflammatory pathways. Diabetes. 2003;52:2951–8.
24. Zhao Y-H, Wang D-P, Zhang L-L, Zhang F, Wang D-M, Zhang W-Y. Genomic expression profiles of blood and placenta reveal significant immune-related pathways and categories in Chinese women with gestational diabetes mellitus. Diabet Med. 2011;28:237–46.
25. Ruchat S-M, Houde A-A, Voisin G, St-Pierre J, Perron P, Baillargeon J-P, et al. Gestational diabetes mellitus epigenetically affects genes predominantly involved in metabolic diseases. Epigenetics. 2013;8:935–43.
26. Finer S, Mathews C, Lowe R, Smart M, Hillman S, Foo L, et al. Maternal gestational diabetes is associated with genome-wide DNA methylation variation in placenta and cord blood of exposed offspring. Hum Mol Genet. 2015;24:3021–9.
27. Cho YM, Kim TH, Lim S, Choi SH, Shin HD, Lee HK, et al. Type 2 diabetes-associated genetic variants discovered in the recent genome-wide association studies are related to gestational diabetes mellitus in the Korean population. Diabetologia. 2009;52:253–61.
28. Lauenborg J, Grarup N, Damm P, Borch-Johnsen K, Jørgensen T, Pedersen O, et al. Common type 2 diabetes risk gene variants associate with gestational diabetes. J Clin Endocrinol Metab. 2009;94:145–50.
29. Thorand B, Löwel H, Schneider A, Kolb H, Meisinger C, Fröhlich M, et al. C-reactive protein as a predictor for incident diabetes mellitus among middle-aged men: results from the MONICA Augsburg cohort study, 1984–1998. Arch Intern Med. 2003;163:93–9.
30. Taniguchi A, Nagasaka S, Fukushima M, Sakai M, Okumura T, Yoshii S, et al. C-reactive protein and insulin resistance in non-obese Japanese type 2 diabetic patients. Metabolism. 2002;51:1578–81.
31. Pradhan AD, Manson JE, Rifai N, Buring JE, Ridker PM. C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. JAMA. 2001;286:327–34.
32. Freeman DJ, Norrie J, Caslake MJ, Gaw A, Ford I, Lowe GDO, et al. C-reactive protein is an independent predictor of risk for the development of diabetes in the West of Scotland Coronary Prevention Study. Diabetes. 2002;51:1596–600.
33. Qiu C, Sorensen TK, Luthy DA, Williams MA. A prospective study of maternal serum C-reactive protein (CRP) concentrations and risk of gestational diabetes mellitus. Paediatr Perinat Epidemiol. 2004;18:377–84.
34. Lain KY, Catalano PM. Metabolic changes in pregnancy. Clin Obstet Gynecol. 2007;50:938–48.
35. Colomiere M, Permezel M, Lappas M. Diabetes and obesity during pregnancy alter insulin signalling and glucose transporter expression in maternal skeletal muscle and subcutaneous adipose tissue. J Mol Endocrinol. 2010;44:213–23.
36. Desoye G, Hauguel-de Mouzon S. The human placenta in gestational diabetes mellitus. The insulin and cytokine network. Diabetes Care. 2007;30 Suppl 2:S120–126.
37. Lappas M, Mitton A, Mittion A, Permezel M. In response to oxidative stress, the expression of inflammatory cytokines and antioxidant enzymes are impaired in placenta, but not adipose tissue, of women with gestational diabetes. J Endocrinol. 2010;204:75–84.
38. Hivert M-F, Sullivan LM, Fox CS, Nathan DM, D’Agostino Sr RB, Wilson PWF, et al. Associations of adiponectin, resistin, and tumor necrosis factor-alpha with insulin resistance. J Clin Endocrinol Metab. 2008;93:3165–72.
39. Ouchi N, Parker JL, Lugus JJ, Walsh K. Adipokines in inflammation and metabolic disease. Nat Rev Immunol. 2011;11:85–97.
40. Stankov K, Benc D, Draskovic D. Genetic and epigenetic factors in etiology of diabetes mellitus type 1. Pediatrics. 2013;132:1112–22.
41. Nejentsev S, Howson JMM, Walker NM, Szeszko J, Field SF, Stevens HE, et al. Localization of type 1 diabetes susceptibility to the MHC class I genes HLA-B and HLA-A. Nature. 2007;450:887–92.
42. Erlich H, Valdes AM, Noble J, Carlson JA, Varney M, Concannon P, et al. HLA DR-DQ haplotypes and genotypes and type 1 diabetes risk: analysis of the type 1 diabetes genetics consortium families. Diabetes. 2008;57:1084–92.
43. Mauricio D, de Leiva A. Autoimmune gestational diabetes mellitus: a distinct clinical entity? Diabetes Metab Res Rev. 2001;17:422–8.
44. Törn C, Gupta M, Sanjeevi CB, Aberg A, Frid A, Landin-Olsson M. Different HLA-DR-DQ and MHC class I chain-related gene A (MICA) genotypes in autoimmune and nonautoimmune gestational diabetes in a Swedish population. Hum Immunol. 2004;65:1443–50.
45. Papadopoulou A, Lynch KF, Shaat N, Nilsson A, Lernmark B, Berntorp K, et al. The type 1 diabetes protective HLA DQB1*0602 allele is less frequent in gestational diabetes mellitus. Diabetologia. 2009;52:1339–42.
46. Damm P, Kühl C, Buschard K, Jakobsen BK, Svejgaard A, Sodoyez-Goffaux F, et al. Prevalence and predictive value of islet cell antibodies and insulin autoantibodies in women with gestational diabetes. Diabet Med J Br Diabet Assoc. 1994;11:558–63.
47. Füchtenbusch M, Ferber K, Standl E, Ziegler AG. Prediction of type 1 diabetes postpartum in patients with gestational diabetes mellitus by combined islet cell autoantibody screening: a prospective multicenter study. Diabetes. 1997;46:1459–67.
48. Nilsson C, Ursing D, Törn C, Aberg A, Landin-Olsson M. Presence of GAD antibodies during gestational diabetes mellitus predicts type 1 diabetes. Diabetes Care. 2007;30:1968–71.
49. Steinborn A, Saran G, Schneider A, Fersis N, Sohn C, Schmitt E. The presence of gestational diabetes is associated with increased detection of anti-HLA-class II antibodies in the maternal circulation. Am J Reprod Immunol N Y N 1989. 2006;56:124–34.
50. Houseman EA, Accomando WP, Koestler DC, Christensen BC, Marsit CJ, Nelson HH, et al. DNA methylation arrays as surrogate measures of cell mixture distribution. BMC Bioinformatics. 2012;13:86.
51. Michels KB, Harris HR, Barault L. Birthweight, maternal weight trajectories and global DNA methylation of LINE-1 repetitive elements. PLoS One. 2011;6, e25254.
52. Bibikova M, Barnes B, Tsan C, Ho V, Klotzle B, Le JM, et al. High density DNA methylation array with single CpG site resolution. Genomics. 2011;98:288–95.
53. Marsit CJ, Lambertini L, Maccani MA, Koestler DC, Houseman EA, Padbury JF, et al. Placenta-imprinted gene expression association of infant neurobehavior. J Pediatr. 2012;160:854–60. e2.
54. Marsit CJ, Maccani MA, Padbury JF, Lester BM. Placental 11-beta hydroxysteroid dehydrogenase methylation is associated with newborn growth and a measure of neurobehavioral outcome. PLoS One. 2012;7, e33794.
55. Marabita F, Almgren M, Lindholm ME, Ruhrmann S, Fagerström-Billai F, Jagodic M, et al. An evaluation of analysis pipelines for DNA methylation profiling using the Illumina HumanMethylation450 BeadChip platform. Epigenetics. 2013;8:333–46.
56. Du P, Kibbe WA, Lin SM. lumi: a pipeline for processing Illumina microarray. Bioinforma Oxf Engl. 2008;24:1547–8.
57. Pidsley R, Y Wong CC, Volta M, Lunnon K, Mill J, Schalkwyk LC. A data-driven approach to preprocessing Illumina 450K methylation array data. BMC Genomics. 2013;14:293.
58. Teschendorff AE, Marabita F, Lechner M, Bartlett T, Tegner J, Gomez-Cabrero D, et al. A beta-mixture quantile normalization method for correcting probe design bias in Illumina Infinium 450 k DNA methylation data. Bioinforma Oxf Engl. 2013;29:189–96.
59. Price ME, Cotton AM, Lam LL, Farré P, Emberly E, Brown CJ, et al. Additional annotation enhances potential for biologically-relevant analysis of the Illumina Infinium HumanMethylation450 BeadChip array. Epigenetics Chromatin. 2013;6:4.
60. Leek JT, Scharpf RB, Bravo HC, Simcha D, Langmead B, Johnson WE, et al. Tackling the widespread and critical impact of batch effects in high-throughput data. Nat Rev Genet. 2010;11:733–9.
61. Teschendorff AE, Zhuang J, Widschwendter M. Independent surrogate variable analysis to deconvolve confounding factors in large-scale microarray profiling studies. Bioinforma Oxf Engl. 2011;27:1496–505.
62. Jaffe AE, Murakami P, Lee H, Leek JT, Fallin MD, Feinberg AP, et al. Bump hunting to identify differentially methylated regions in epigenetic epidemiology studies. Int J Epidemiol. 2012;41:200–9.
63. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostat Oxf Engl. 2003;4:249–64.
64. Bolstad BM, Irizarry RA, Astrand M, Speed TP. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinforma Oxf Engl. 2003;19:185–93.
65. Jiang J, Conrath D: Semantic Similarity Based on Corpus Statistics and Lexical Taxonomy. In International Conference Research on Computational Linguistics. Taiwan; 1997.
66. Storey JD, Tibshirani R. Statistical significance for genomewide studies. Proc Natl Acad Sci. 2003;100:9440–5.