Sexually dimorphic effect of In Vitro Fertilization (IVF) on adult mouse fat and liver metabolomes

Endocrinology (United States)

Volumn 155, Issue 11, 2014, Pages 4554-4567

  Feuer, Sky K ^a   Donjacour, Annemarie ^a   Simbulan, Rhodel K ^a   Lin, Wingka ^a   Liu, Xiaowei ^a   Maltepe, Emin ^a   Rinaudo, Paolo F ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CORTICOSTERONE; GLUCOSE; GLUTATHIONE; GLUTATHIONE DISULFIDE; GLYCEROPHOSPHOETHANOLAMINE; URATE;

ADIPOSE TISSUE; ADULT; AMINO ACID METABOLISM; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; DUAL ENERGY X RAY ABSORPTIOMETRY; EMBRYO; EMBRYO CULTURE; EMBRYO TRANSFER; FEMALE; FERTILIZATION IN VITRO; GLUCOSE BLOOD LEVEL; GLYCOGENOLYSIS; IN VIVO STUDY; LIPID METABOLISM; LIVER METABOLISM; MALE; MASS SPECTROMETRY; METABOLOME; METABOLOMICS; MOUSE; NONHUMAN; NUCLEOTIDE METABOLISM; OBESITY; ORGAN SIZE; OXIDATIVE STRESS; PENTOSE PHOSPHATE CYCLE; PROTEIN SYNTHESIS; PYRIMIDINE METABOLISM; SEX DIFFERENCE; SPHINGOLIPID METABOLISM; TIME OF DEATH; UREA CYCLE; ANIMAL; BLASTOCYST; C57BL MOUSE; CELL CULTURE; LIVER; METABOLISM; PREGNANCY; SEXUAL DEVELOPMENT;

ADIPOSE TISSUE; ANIMALS; BLASTOCYST; CELLS, CULTURED; FEMALE; FERTILIZATION IN VITRO; LIVER; MALE; METABOLOME; METABOLOMICS; MICE; MICE, INBRED C57BL; PREGNANCY; SEX CHARACTERISTICS;

EID: 84908030003     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2014-1465     Document Type: Article

References (48)

1. Barker DJ. The origins of the developmental origins theory. J Intern Med. 2007;261:412-417.
2. Kwong WY, Wild AE, Roberts P, Willis AC, Fleming TP. Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension. Development. 2000;127:4195-4202.
3. Fernández-Gonzalez R, Moreira P, Bilbao A, et al. Long-term effect of in vitro culture of mouse embryos with serum on mRNA expression of imprinting genes, development, and behavior. Proc Natl Acad Sci USA. 2004;101:5880-5885.
4. Fernández-Gonzalez R, Moreira PN, Pérez-Crespo M, et al. Longterm effects of mouse intracytoplasmic sperm injection with DNA-fragmented sperm on health and behavior of adult offspring. Biol Reprod. 2008;78:761-772.
5. Ceelen M, van Weissenbruch MM, Vermeiden JP, van Leeuwen FE, Delemarre-van de Waal HA. Cardiometabolic differences in children born after in vitro fertilization: follow-up study. J Clin Endocrinol Metab. 2008;93:1682-1688.
6. Ceelen M, van Weissenbruch MM, Roos JC, Vermeiden JP, van Leeuwen FE, Delemarre-van de Waal HA. Body composition in children and adolescents born after in vitro fertilization or spontaneous conception. J Clin Endocrinol Metab. 2007;92:3417-3423.
7. Ceelen M, van Weissenbruch MM, Prein J, et al. Growth during infancy and early childhood in relation to blood pressure and body fat measures at age 8-18 years of IVF children and spontaneously conceived controls born to subfertile parents. Hum Reprod. 2009;24:2788-2795.
8. Scherrer U, Rimoldi SF, Rexhaj E, et al. Systemic and pulmonary vascular dysfunction in children conceived by assisted reproductive technologies. Circulation. 2012;125:1890-1896.
9. Feuer SK, Liu X, Donjacour A, et al. Use of a mouse in vitro fertilization model to understand the developmental origins of health and disease hypothesis. Endocrinology. 2014;155:1956-1969.
10. Donjacour A, Liu X, Lin W, Simbulan R, Rinaudo PF. In vitro fertilization affects growth and glucose metabolism in a sex-specific manner in an outbred mouse model. Biol Reprod. 2014;90:80.
11. Rexhaj E, Paoloni-Giacobino A, Rimoldi SF, et al. Mice generated by in vitro fertilization exhibit vascular dysfunction and shortened life span. J Clin Invest. 2013;123:5052-5060.
12. Gabory A, Attig L, Junien C. Sexual dimorphism in environmental epigenetic programming. Mol Cell Endocrinol. 2009;304:8-18.
13. Geer EB, Shen W. Gender differences in insulin resistance, body composition, and energy balance. Gend Med. 2009;6(suppl 1):60-75.
14. Bermejo-Alvarez P, Rizos D, Rath D, Lonergan P, Gutierrez-Adan A. Sex determines the expression level of one third of the actively expressed genes in bovine blastocysts. Proc Natl Acad Sci USA. 2010;107:3394-3399.
15. Gilbert JS, Banek CT. Sex differences in the developmental programming of adult disease. INTECH Open Access Publisher; 2012.
16. Kaddurah-Daouk R, Kristal BS, Weinshilboum RM. Metabolomics: a global biochemical approach to drug response and disease. Annu Rev Pharmacol Toxicol. 2008;48:653-683.
17. Weisberg SP, Hunter D, Huber R, et al. CCR2 modulates inflammatory and metabolic effects of high-fat feeding. J Clin Invest. 2006;116:115-124.
18. Lawitts JA, Biggers JD. Culture of preimplantation embryos. Methods Enzymol. 1993;225:153-164.
19. Evans AM, DeHaven CD, Barrett T, Mitchell M, Milgram E. Integrated, nontargeted ultrahigh performance liquid chromatography/electrospray ionization tandem mass spectrometry platform for the identification and relative quantification of the small-molecule complement of biological systems. Anal Chem. 2009;81:6656-6667.
20. Lawton KA, Berger A, Mitchell M, et al. Analysis of the adult human plasma metabolome. Pharmacogenomics. 2008;9:383-397.
21. Dehaven CD, Evans AM, Dai H, Lawton KA. Organization of GC/MS and LC/MS metabolomics data into chemical libraries. J Cheminform. 2010;2:9.
22. Xia J, Psychogios N, Young N, Wishart DS. MetaboAnalyst: a web server for metabolomic data analysis and interpretation. Nucleic Acids Res. 2009;37:W652-W660.
23. Xia J, Mandal R, Sinelnikov IV, Broadhurst D, Wishart DS. MetaboAnalyst 2.0-a comprehensive server for metabolomic data analysis. Nucleic Acids Res. 2012;40:W127-W133.
24. Schwarzer C, Esteves TC, Araúzo-Bravo MJ, et al. ART culture conditions change the probability of mouse embryo gestation through defined cellular and molecular responses. Hum Reprod. 2012;27:2627-2640.
25. Xia J, Wishart DS. MSEA: a web-based tool to identify biologically meaningful patterns in quantitative metabolomic data. Nucleic Acids Res. 2010;38:W71-W77.
26. Banrezes B, Sainte-Beuve T, Canon E, Schultz RM, Cancela J, Ozil JP. Adult body weight is programmed by a redox-regulated and energy-dependent process during the pronuclear stage in mouse. PLoS One. 2011;6:e29388.
27. Yang X, Schadt EE, Wang S, et al. Tissue-specific expression and regulation of sexually dimorphic genes in mice. Genome Res. 2006;16:995-1004.
28. Wells JC. Sexual dimorphism of body composition. Best Pract Res Clin Endocrinol Metab. 2007;21:415-430.
29. Guo C, Li C, Myatt L, Nathanielsz PW, Sun K. Sexually dimorphic effects of maternal nutrient reduction on expression of genes regulating cortisol metabolism in fetal baboon adipose and liver tissues. Diabetes. 2013;62:1175-1185.
30. Mittelstrass K, Ried JS, Yu Z, et al. Discovery of sexual dimorphisms in metabolic and genetic biomarkers. PLoS Genet. 2011;7:e1002215.
31. Wrenzycki C, Lucas-Hahn A, Herrmann D, Lemme E, Korsawe K, Niemann H. In vitro production and nuclear transfer affect dosage compensation of the X-linked gene transcripts G6PD, PGK, and Xist in preimplantation bovine embryos. Biol Reprod. 2002;66:127-134.
32. Bermejo-Alvarez P, Rizos D, Lonergan P, Gutierrez-Adan A. Transcriptional sexual dimorphism during preimplantation embryo development and its consequences for developmental competence and adult health and disease. Reproduction. 2011;141:563-570.
33. Xu F, Tavintharan S, Sum CF, Woon K, Lim SC, Ong CN. Metabolic signature shift in type 2 diabetes mellitus revealed by mass spec-trometry-based metabolomics. J Clin Endocrinol Metab. 2013;98:E1060-E1065.
34. Kim HJ, Kim JH, Noh S, Hur HJ, et al. Metabolomic analysis of livers and serum from high-fat diet induced obese mice. J Proteome Res. 2011;10:722-731.
35. Viollet B, Guigas B, Leclerc J, et al. AMP-activated protein kinase in the regulation of hepatic energy metabolism: from physiology to therapeutic perspectives. Acta Physiol (Oxf). 2009;196:81-98.
36. Li T, Francl JM, Boehme S, et al. Glucose and insulin induction of bile acid synthesis: mechanisms and implication in diabetes and obesity. J Biol Chem. 2012;287:1861-1873.
37. Watanabe M, Horai Y, Houten SM, et al. Lowering bile acid pool size with a synthetic farnesoid X receptor (FXR) agonist induces obesity and diabetes through reduced energy expenditure. J Biol Chem. 2011;286:26913-26920.
38. Du F, Navarro-Garcia F, Xia Z, Tasaki T, Varshavsky A. Pairs of dipeptides synergistically activate the binding of substrate by ubiquitin ligase through dissociation of its autoinhibitory domain. Proc Natl Acad Sci USA. 2002;99:14110-14115.
39. Wing SS. The UPS in diabetes and obesity. BMC Biochem. 2008;9(suppl 1):S6.
40. Muoio DM, Newgard CB. Obesity-related derangements in metabolic regulation. Annu Rev Biochem. 2006;75:367-401.
41. Baldwin W, McRae S, Marek G, et al. Hyperuricemia as a mediator of the proinflammatory endocrine imbalance in the adipose tissue in a murine model of the metabolic syndrome. Diabetes. 2011;60:1258-1269.
42. Sautin YY, Nakagawa T, Zharikov S, Johnson RJ. Adverse effects of the classic antioxidant uric acid in adipocytes: NADPH oxidase-mediated oxidative/nitrosative stress. Am J Physiol Cell Physiol. 2007;293:C584-C596.
43. Zafir A, Banu N. Modulation of in vivo oxidative status by exogenous corticosterone and restraint stress in rats. Stress. 2009;12:167-177.
44. Calzadilla P, Sapochnik D, Cosentino S, et al. N-acetylcysteine reduces markers of differentiation in 3T3-L1 adipocytes. Int J Mol Sci. 2011;12:6936-6951.
45. Vigilanza P, Aquilano K, Baldelli S, Rotilio G, Ciriolo MR. Modulation of intracellular glutathione affects adipogenesis in 3T3-L1 cells. J Cell Physiol. 2011;226:2016-2024.
46. Imhoff BR, Hansen JM. Differential redox potential profiles during adipogenesis and osteogenesis. Cell Mol Biol Lett. 2011;16:149-161.
47. Sackmann-Sala L, Berryman DE, Munn RD, Lubbers ER, Kopchick JJ. Heterogeneity among white adipose tissue depots in male C57BL/6J mice. Obesity. 2012;20:101-111.
48. Fuente-Martín E, Argente-Arizón P, Ros P, Argente J, Chowen JA. Sex differences in adipose tissue: it is not only a question of quantity and distribution. Adipocyte. 2013;2:128-134.