Assessing the fetal effects of maternal obesity via transcriptomic analysis of cord blood: A prospective case-control study

BJOG: An International Journal of Obstetrics and Gynaecology

Volumn 123, Issue 2, 2016, Pages 180-189

  Edlow, A G ^a,d   Hui, L ^a,b   Wick, H C ^c   Fried, I ^c   Bianchi, D W ^a  

^a TUFTS MEDICAL CENTER   (United States)

^b MERCY HOSPITAL FOR WOMEN   (Australia)

^c Tufts University   (United States)

^d Mother Infant Research Institute   (United States)

Author keywords

Brain; cord blood; fetal; fetal programming; maternal obesity; metabolic; transcriptome

Indexed keywords

INSULIN RECEPTOR; LIPID; RNA;

ADULT; ARTICLE; BODY MASS; CASE CONTROL STUDY; CELL SURVIVAL; CESAREAN SECTION; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; FETAL BRAIN; FETUS; FETUS DEVELOPMENT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE MAPPING; GENETIC ANALYSIS; GESTATIONAL AGE; HUMAN; HUMAN CELL; HUMAN TISSUE; LEAN BODY WEIGHT; LIPID HOMEOSTASIS; MALE; MATERNAL OBESITY; NERVE DEGENERATION; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; OXIDATIVE STRESS; PREGNANT WOMAN; PRIORITY JOURNAL; PROSPECTIVE STUDY; RNA EXTRACTION; RNA HYBRIDIZATION; SCORING SYSTEM; SENSORY NERVE CELL; SEX DIFFERENCE; SIGNAL TRANSDUCTION; TERTIARY CARE CENTER; TISSUE SPECIFICITY; TRANSCRIPTOMICS; UMBILICAL CORD BLOOD; BLOOD; DNA MICROARRAY; EPIDEMIOLOGY; FETUS BLOOD; GENETICS; INSULIN RESISTANCE; OBESITY; PREGNANCY; PREGNANCY COMPLICATION; PRENATAL EXPOSURE; UNITED STATES;

ADULT; BODY MASS INDEX; CASE-CONTROL STUDIES; FEMALE; FETAL BLOOD; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; INFANT, NEWBORN; INSULIN RESISTANCE; MALE; OBESITY; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PREGNANCY; PREGNANCY COMPLICATIONS; PRENATAL EXPOSURE DELAYED EFFECTS; PROSPECTIVE STUDIES; UNITED STATES;

EID: 84952837338     PISSN: 14700328     EISSN: 14710528     Source Type: Journal    
DOI: 10.1111/1471-0528.13795     Document Type: Article

References (61)

1. World Health Organization. New data highlight increases in hypertension, diabetes incidence. 2012; [www.who.int/mediacentre/news/releases/2012/world-health-statistics-20120516/en/]. Accessed 7 March 2015.
2. Flegal KM, Carroll MD, Kit BK, Ogden CL. Prevalence of obesity and trends in the distribution of body mass index among US adults, 1999-2010. JAMA 2012; 307: 491-7.
3. Flegal KM, Carroll MD, Ogden CL, Curtin LR. Prevalence and trends in obesity among US adults, 1999-2008. JAMA 2010; 303: 235-41.
4. Kim SY, Dietz PM, England L, Morrow B, Callaghan WM. Trends in pre-pregnancy obesity in nine states, 1993-2003. Obesity (Silver Spring) 2007; 15: 986-93.
5. Catalano PM, Ehrenberg HM. The short- and long-term implications of maternal obesity on the mother and her offspring. BJOG 2006; 113: 1126-33.
6. 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.
7. Boney CM, Verma A, Tucker R, Vohr BR. Metabolic syndrome in childhood: association with birth weight, maternal obesity, and gestational diabetes mellitus. Pediatrics 2005; 115: e290-6.
8. Crespo PS, Prieto Perera JA, Lodeiro FA, Azuara LA. Metabolic syndrome in childhood. Public Health Nutr 2007; 10: 1121-5.
9. Lawlor DA, Smith GD, O'Callaghan M, Alati R, Mamun AA, Williams GM, et al., Epidemiologic evidence for the fetal overnutrition hypothesis: findings from the mater-university study of pregnancy and its outcomes. Am J Epidemiol 2007; 165: 418-24.
10. Franco JG, Fernandes TP, Rocha CP, Calviño C, Pazos-Moura CC, Lisboa PC, et al., Maternal high-fat diet induces obesity and adrenal and thyroid dysfunction in male rat offspring at weaning. J Physiol 2012; 590: 5503-18.
11. Elahi MM, Cagampang FR, Mukhtar D, Anthony FW, Ohri SK, Hanson MA. Long-term maternal high-fat feeding from weaning through pregnancy and lactation predisposes offspring to hypertension, raised plasma lipids and fatty liver in mice. Br J Nutr 2009; 102: 514-9.
12. Gniuli D, Calcagno A, Caristo ME, Mancuso A, Macchi V, Mingrone G, et al., Effects of high-fat diet exposure during fetal life on type 2 diabetes development in the progeny. J Lipid Res 2008; 49: 1936-45.
13. McCurdy CE, Bishop JM, Williams SM, Grayson BE, Smith MS, Friedman JE, et al., Maternal high-fat diet triggers lipotoxicity in the fetal livers of nonhuman primates. J Clin Invest 2009; 119: 323-35.
14. Hinkle SN, Schieve LA, Stein AD, Swan DW, Ramakrishnan U, Sharma AJ. Associations between maternal prepregnancy body mass index and child neurodevelopment at 2 years of age. Int J Obes (Lond) 2012; 36: 1312-9.
15. Van Lieshout RJ, Taylor VH, Boyle MH. Pre-pregnancy and pregnancy obesity and neurodevelopmental outcomes in offspring: a systematic review. Obes Rev 2011; 12: e548-59.
16. Neggers YH, Goldenberg RL, Ramey SL, Cliver SP. Maternal prepregnancy body mass index and psychomotor development in children. Acta Obstet Gynecol Scand 2003; 82: 235-40.
17. Heikura U, Taanila A, Hartikainen AL, Olsen P, Linna SL, von Wendt L, et al., Variations in prenatal sociodemographic factors associated with intellectual disability: a study of the 20-year interval between two birth cohorts in northern Finland. Am J Epidemiol 2008; 167: 169-77.
18. Tanda R, Salsberry PJ, Reagan PB, Fang MZ. The impact of prepregnancy obesity on children's cognitive test scores. Matern Child Health J 2013; 17: 222-9.
19. Krakowiak P, Walker CK, Bremer AA, Baker AS, Ozonoff S, Hansen RL, et al., Maternal metabolic conditions and risk for autism and other neurodevelopmental disorders. Pediatrics 2012; 129: e1121-8.
20. Rodriguez A, Miettunen J, Henriksen TB, Olsen J, Obel C, Taanila A, et al., Maternal adiposity prior to pregnancy is associated with ADHD symptoms in offspring: evidence from three prospective pregnancy cohorts. Int J Obes (Lond) 2008; 32: 550-7.
21. Ahlin K, Himmelmann K, Hagberg G, Kacerovsky M, Cobo T, Wennerholm UB, et al., Non-infectious risk factors for different types of cerebral palsy in term-born babies: a population-based, case-control study. BJOG 2013; 120: 724-31.
22. Edlow AG, Vora NL, Hui L, Wick HC, Cowan JM, Bianchi DW. Maternal obesity affects fetal neurodevelopmental and metabolic gene expression: a pilot study. PLoS One 2014; 9: e88661.
23. Basu S, Leahy P, Challier JC, Minium J, Catalano P. Hauguel-de Mouzon S. Molecular phenotype of monocytes at the maternal-fetal interface. Am J Obstet Gynecol 2011; 205: 265.e261-8.
24. Thakali KM, Saben J, Faske JB, Lindsey F, Gomez-Acevedo H, Lowery CL Jr, et al., Maternal pregravid obesity changes gene expression profiles toward greater inflammation and reduced insulin sensitivity in umbilical cord. Pediatr Res 2014; 76: 202-10.
25. Lassance L, Haghiac M, Leahy P, Basu S, Minium J, Zhou J, et al., Identification of early transcriptome signatures in placenta exposed to insulin and obesity. Am J Obstet Gynecol 2015; 212: 647.e1-11.
26. Pavlidis P, Li Q, Noble WS. The effect of replication on gene expression microarray experiments. Bioinformatics 2003; 19: 1620-7.
27. Larrabee PB, Johnson KL, Lai C, Ordovas J, Cowan JM, Tantravahi U, et al., Global gene expression analysis of the living human fetus using cell-free messenger RNA in amniotic fluid. JAMA 2005; 293: 836-42.
28. Massingham LJ, Johnson KL, Bianchi DW, Pei S, Peter I, Cowan JM, et al., Proof of concept study to assess fetal gene expression in amniotic fluid by nanoarray PCR. J Mol Diagn 2011; 13: 565-70.
29. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, et al., Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004; 5: R80.
30. Gentleman R. Reproducible research: a bioinformatics case study. Stat Appl Genet Mol Biol 2005; 4:Article2.
31. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 1995; 57: 289-300.
32. Ingenuity Systems. Calculating and interpreting the p-values for functions, pathways, and lists in IPA. 2013. [www.ingenuity.com/wp-content/themes/ingenuity-qiagen/pdf/ipa/functions-pathways-pval-whitepaper.pdf]. Accessed 14 March 2013.
33. Ingenuity Systems. Ingenuity upstream regulator analysis whitepaper. 2014. http://pages.ingenuity.com/IngenuityUpstreamRegulatorAnalysisWhitepaper.html. Accessed October 27, 2014.
34. Hui L, Wick HC, Moise KJ Jr, Johnson A, Luks F, Haeri S, et al., Global gene expression analysis of amniotic fluid cell-free RNA from recipient twins with twin-twin transfusion syndrome. Prenat Diagn 2013; 33: 873-83.
35. Edlow AG, Slonim DK, Wick HC, Hui L, Bianchi DW. The pathway not taken: understanding 'omics data in the perinatal context. Am J Obstet Gynecol 2015; 213: 59.e1-172.
36. Wick HC, Drabkin H, Ngu H, Sackman M, Fournier C, Haggett J, et al., DFLAT: functional annotation for human development. BMC Bioinformatics 2014; 15: 45.
37. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, et al., Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 2005; 102: 15545-50.
38. Wu C, Orozco C, Boyer J, Leglise M, Goodale J, Batalov S, et al., BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol 2009; 10: R130.
39. Pennings JL, Kuc S, Rodenburg W, Koster MP, Schielen PC, de Vries A. Integrative data mining to identify novel candidate serum biomarkers for pre-eclampsia screening. Prenat Diagn 2011; 31: 1153-9.
40. Borengasser SJ, Zhong Y, Kang P, Lindsey F, Ronis MJ, Badger TM, et al., Maternal obesity enhances white adipose tissue differentiation and alters genome-scale DNA methylation in male rat offspring. Endocrinology 2013; 154: 4113-25.
41. Shankar K, Zhong Y, Kang P, Lau F, Blackburn ML, Chen JR, et al., Maternal obesity promotes a proinflammatory signature in rat uterus and blastocyst. Endocrinology 2011; 152: 4158-70.
42. Stachowiak EK, Oommen S, Vasu VT, Srinivasan M, Stachowiak M, Gohil K, et al., Maternal obesity affects gene expression and cellular development in fetal brains. Nutr Neurosci 2013; 16: 96-103.
43. Stachowiak EK, Srinivasan M, Stachowiak MK, Patel MS. Maternal obesity induced by a high fat diet causes altered cellular development in fetal brains suggestive of a predisposition of offspring to neurological disorders in later life. Metab Brain Dis 2013; 28: 721-5.
44. Romero R, Tromp G. High-dimensional biology in obstetrics and gynecology: functional genomics in microarray studies. Am J Obstet Gynecol 2006; 195: 360-3.
45. Maron JL, Johnson KL, Slonim D, Lai CQ, Ramoni M, Alterovitz G, et al., Gene expression analysis in pregnant women and their infants identifies unique fetal biomarkers that circulate in maternal blood. J Clin Invest 2007; 117: 3007-19.
46. Sullivan PF, Fan C, Perou CM. Evaluating the comparability of gene expression in blood and brain. Am J Med Genet B Neuropsychiatr Genet 2006; 141B: 261-8.
47. Tylee DS, Kawaguchi DM, Glatt SJ. On the outside, looking in: a review and evaluation of the comparability of blood and brain "-omes". Am J Med Genet B Neuropsychiatr Genet 2013; 162B: 595-603.
48. Peterson LJ, Flood PM. Oxidative stress and microglial cells in Parkinson's disease. Mediators Inflamm 2012; 2012: 401264.
49. Pasinetti GM, Eberstein JA. Metabolic syndrome and the role of dietary lifestyles in Alzheimer's disease. J Neurochem 2008; 106: 1503-14.
50. Grant WB, Campbell A, Itzhaki RF, Savory J. The significance of environmental factors in the etiology of Alzheimer's disease. J Alzheimers Dis 2002; 4: 179-89.
51. Cai D. Neuroinflammation and neurodegeneration in overnutrition-induced diseases. Trends Endocrinol Metab 2013; 24: 40-7.
52. Mehta SH, Kerver JM, Sokol RJ, Keating DP, Paneth N. The association between maternal obesity and neurodevelopmental outcomes of offspring. J Pediatr 2014; 165: 891-6.
53. Buckley AJ, Keseru B, Briody J, Thompson M, Ozanne SE, Thompson CH. Altered body composition and metabolism in the male offspring of high fat-fed rats. Metabolism 2005; 54: 500-7.
54. Catalano PM, Presley L, Minium J, Hauguel-de Mouzon S. Fetuses of obese mothers develop insulin resistance in utero. Diabetes Care 2009; 32: 1076-80.
55. Challier JC, Basu S, Bintein T, Minium J, Hotmire K, Catalano PM, et al., Obesity in pregnancy stimulates macrophage accumulation and inflammation in the placenta. Placenta 2008; 29: 274-81.
56. Elovitz MA, Mrinalini C, Sammel MD. Elucidating the early signal transduction pathways leading to fetal brain injury in preterm birth. Pediatr Res 2006; 59: 50-5.
57. Garay PA, Hsiao EY, Patterson PH, McAllister AK. Maternal immune activation causes age- and region-specific changes in brain cytokines in offspring throughout development. Brain Behav Immun 2013; 31: 54-68.
58. Saben J, Lindsey F, Zhong Y, Thakali K, Badger TM, Andres A, et al., Maternal obesity is associated with a lipotoxic placental environment. Placenta 2014; 35: 171-7.
59. Sun B, Purcell RH, Terrillion CE, Yan J, Moran TH, Tamashiro KL. Maternal high-fat diet during gestation or suckling differentially affects offspring leptin sensitivity and obesity. Diabetes 2012; 61: 2833-41.
60. Cerf ME, Williams K, Nkomo XI, Muller CJ, Du Toit DF, Louw J, et al., Islet cell response in the neonatal rat after exposure to a high-fat diet during pregnancy. Am J Physiol Regul Integr Comp Physiol 2005; 288: R1122-8.
61. Maron JL, Johnson KL, Parkin C, Iyer L, Davis JM, Bianchi DW. Cord blood genomic analysis highlights the role of redox balance. Free Radic Biol Med 2010; 49: 992-6.