Combined parental obesity negatively impacts preimplantation mouse embryo development, kinetics, morphology and metabolism

Human Reproduction

Volumn 30, Issue 9, 2015, Pages 2084-2096

  Finger, Bethany J ^a   Harvey, Alexandra J ^a   Green, Mark P ^a   Gardner, David K ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

high fat diet; obesity; time lapse; zona pellucida

Indexed keywords

GLUCOSE; GLUCOSE TRANSPORTER 1; LACTIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLASTOCYST; CELL COUNT; CELL LINEAGE; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; FLUORESCENCE ANALYSIS; GENE EXPRESSION; GLUCOSE INTAKE; MALE; MATERNAL OBESITY; MOUSE; NONHUMAN; OBESITY; PATERNAL OBESITY; PREIMPLANTATION EMBRYO; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; ZONA PELLUCIDA; ANIMAL; C57BL MOUSE; COMPLICATION; DISEASE MODEL; EMBRYO CULTURE; METABOLISM; PHYSIOLOGY; PREGNANCY;

ANIMALS; BLASTOCYST; DISEASE MODELS, ANIMAL; EMBRYO CULTURE TECHNIQUES; EMBRYONIC DEVELOPMENT; FEMALE; MALE; MICE; MICE, INBRED C57BL; OBESITY; PREGNANCY; ZONA PELLUCIDA;

EID: 84940756164     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/dev142     Document Type: Article

References (88)

1. Acton BM, Jurisicova A, Jurisica I, Casper RF. Alterations in mitochondrial membrane potential during preimplantation stages of mouse and human embryo development. Mol Hum Reprod 2004; 10: 23-32
2. Andersen CL, Jensen JL, Orntoft TF. Normalization of real-Time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 2004; 64: 5245-5250
3. Bakos HW, Henshaw RC, Mitchell M, Lane M. Paternal body mass index is associated with decreased blastocyst development and reduced live birth rates following assisted reproductive technology. Fertil Steril 2011; 95: 1700-1704
4. Bakos HW, Mitchell M, Setchell BP, Lane M. The effect of paternal diet-induced obesity on sperm function and fertilization in a mouse model. Int J Androl 2011; 34: 402-410
5. Bellver J, Mifsud A, Grau N, Privitera L, Meseguer M. Similar morphokinetic patterns in embryos derived from obese and normoweight infertile women: a time-lapse study. Hum Reprod 2013; 28: 794-800
6. Bermejo-Alvarez P, Rosenfeld CS, Roberts RM. Effect of maternal obesity on estrous cyclicity, embryo development and blastocyst gene expression in a mouse model. Hum Reprod 2012; 27: 3513-3522
7. Binder NK, Hannan NJ, Gardner DK. Paternal diet-induced obesity retards early mouse embryo development, mitochondrial activity and pregnancy health. PLoS One 2012; 7: e52304
8. Binder NK, Mitchell M, Gardner DK. Parental diet-induced obesity leads to retarded early mouse embryo development and altered carbohydrate utilisation by the blastocyst. Reprod Fertil Dev 2012; 24: 804-812
9. Binder NK, Hannan NJ, Sheedy JR, Gardner DK. Male obesity is associated with changed spermatozoa Cox4i1 mRNA level and altered seminal vesicle fluid composition in a mouse model. Mol Hum Reprod 2015; 21: 424-434
10. Boden G. Obesity and Free Fatty Acids (FFA). Endocrinol Metab Clin North Am 2008; 37: 635
11. Bromfield JJ, Schjenken JE, Chin PY, Care AS, Jasper MJ, Robertson SA. Maternal tract factors contribute to paternal seminal fluid impact on metabolic phenotype in offspring. Proc Natl Acad Sci USA 2014; 111: 2200-2205
12. Cagnone GL, Dufort I, Vigneault C, Sirard MA. Differential gene expression profile in bovine blastocysts resulting from hyperglycemia exposure during early cleavage stages. Biol Reprod 2012; 86: 2, 1-12
13. Chavatte-Palmer P, Tarrade A, Levy R. Developmental origins of health and disease in adults: role of maternal environment. Gynecol Obstet Fertil 2012; 40: 517-519
14. Cross JC, Werb Z, Fisher SJ. Implantation and the placenta: key pieces of the development puzzle. Science 1994; 266: 1508-1518
15. De Celis R, Feria-Velasco A, González-Unzaga M, Torres-Calleja J, Pedrón-Nuevo N. Semen quality of workers occupationally exposed to hydrocarbons. Fertil Steril 2000; 73: 221-228
16. Dupont C, Harvey AJ, Armant DR, Zelinski MB, Brenner CA. Expression profiles of cohesins, shugoshins and spindle assembly checkpoint genes in rhesus macaque oocytes predict their susceptibility for aneuploidy during embryonic development. Cell Cycle 2012; 11: 740-748
17. Dupont C, Faure C, Sermondade N, Boubaya M, Eustache F, Clement P, Briot P, Berthaut I, Levy V, Cedrin-Durnerin I et al. Obesity leads to higher risk of sperm DNA damage in infertile patients. Asian J Androl 2013; 15: 622-625
18. Ferraretti AP, Goossens V, Kupka M, Bhattacharya S, de Mouzon J, Castilla JA, Erb K, Korsak V, Nyboe Andersen A. Assisted reproductive technology in Europe, 2009: results generated from European registers by ESHRE. Hum Reprod 2013; 28: 2318-2331
19. Feuer SK, Camarano L, Rinaudo PF. ART and health: clinical outcomes and insights on molecular mechanisms from rodent studies. Mol Human Reprod 2013; 19: 189-204
20. Fullston T, Palmer NO, Owens JA, Mitchell M, Bakos HW, Lane M. Diet-induced paternal obesity in the absence of diabetes diminishes the reproductive health of two subsequent generations of mice. Hum Reprod 2012; 27: 1391-1400
21. Fullston T, Ohlsson Teague EMC, Palmer NO, DeBlasio MJ, Mitchell M, Corbett M, Print CG, Owens JA, Lane M. Paternal obesity initiates metabolic disturbances in two generations of mice with incomplete penetrance to the F2 generation and alters the transcriptional profile of testis and sperm microRNA content. FASEB J 2013; 27: 4226-4243
22. Gardner DK, Leese HJ. Concentrations of nutrients in mouse oviduct fluid and their effects on embryo development and metabolism in vitro. Reproduction 1990; 88: 361-368
23. Gardner DK, Wale PL. Analysis of metabolism to select viable human embryos for transfer. Fertil Steril 2013; 99: 1062-1072
24. Gardner DK, Lane M. Mammalian preimplantation embryo culture. Methods Mol Biol 2014; 1092: 167-182
25. Gardner DK, Harvey AJ. Blastocyst metabolism. Reprod Fert Dev 2015; 27: 638-654
26. Gardner DK, Lane M, Watson AJ A Laboratory Guide to the Mammalian Embryo. Oxford University Press, New York, USA, 2004
27. Gardner DS, Pearce S, Dandrea J, Walker R, Ramsay M, Stephenson T, Symonds ME. Peri-implantation undernutrition programs blunted angiotensin II evoked baroreflex responses in young adult sheep. Hypertension 2004; 43: 1290-1296
28. Ge Z-J, Liang Q-X, Hou Y, Han Z-M, Schatten H, Sun Q-Y, Zhang C-L. Maternal obesity and diabetes may cause DNA methylation alteration in the spermatozoa of offspring in mice. Reprod Biol Endocrinol 2014; 12: 29-29
29. Guh DP, Zhang W, Bansback N, Amarsi Z, Birmingham CL, Anis AH. The incidence of co-morbidities related to obesity and overweight: a systematic review and meta-Analysis. BMC Public Health 2009; 9: 88
30. Gulaya NM, Margitich VM, Govseeva NM, Klimashevsky VM, Gorpynchenko II, Boyko MI. Phospholipid composition of human sperm and seminal plasma in relation to sperm fertility. Arch Androl 2001; 46: 169-175
31. Gupta V, Bamezai RN. Human pyruvate kinase M2: a multifunctional protein. Protein Sci 2010; 19: 2031-2044
32. Groover AL, Ryals JM, Guilford BL, Wilson NM, Christianson JA, Wright DE. Exercise-mediated improvements in painful neuropathy associated with prediabetes in mice. Pain 2013; 154: 2658-2667
33. Hardy K, Handyside AH, Winston RM. The human blastocyst: cell number, death and allocation during late preimplantation development in vitro. Development 1989; 107: 597-604
34. Hardy K, Spanos S, Becker D, Iannelli P, Winston RML, Stark J. From cell death to embryo arrest: Mathematical models of human preimplantation embryo development. Proc Natl Acad Sci USA 2001; 98: 1655-1660
35. Harvey AJ, Kind KL, Pantaleon M, Armstrong DT, Thompson JG. Oxygen-regulated gene expression in bovine blastocysts. Biol Reprod 2004; 71: 1108-1119
36. Hillian AD, McMullen MR, Sebastian BM, Rowchowdhury S, Kashyap SR, Schauer PR, Kirwan JP, Feldstein AE, Nagy LE. Mice lacking C1q are protected from high fat diet-induced hepatic insulin resistance and impaired glucose homeostasis. J Biol Chem 2013; 288: 22565-22575
37. Igosheva N, Abramov AY, Poston L, Eckert JJ, Fleming TP, Duchen MR, McConnell J. Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes. PLoS One 2010; 5: 0010074
38. Jensen TK, Andersson A-M, Jorgensen N, Andersen A-G, Carlsen E, Petersen JH, Skakkebak NE. Body mass index in relation to semen quality and reproductive hormonesamong 1, 558 Danish men. Fertil Steril 2004; 82: 863-870
39. Kaser DJ, Racowsky C. Clinical outcomes following selection of human preimplantation embryos with time-lapse monitoring: a systematic review. Hum Reprod Update 2014; 20: 617-631
40. Kind KL, Collett RA, Harvey AJ, Thompson JG. Oxygen-regulated expression of GLUT-1, GLUT-3, and VEGF in the mouse blastocyst. Mol Reprod Dev 2005; 70: 37-44
41. Kirkegaard K, Ahlström A, Ingerslev HJ, Hardarson T. Choosingthebestembryo by time lapse versus standard morphology. Fertil Steril 2015; 103: 323-332
42. Kort HI, Massey JB, Elsner CW, Mitchell-Leef D, Shapiro DB, Witt MA, Roudebush WE. Impact of body mass index values on sperm quantity and quality. J Androl 2006; 27: 450-452
43. Krisher RL, Prather RS A role for the Warburg effect in preimplantation embryo development: metabolic modification to support rapid cell proliferation. Mol Reprod Dev 2012; 79: 311-320
44. Kupka MS, Gnoth C, Buehler K, Dahncke W, Kruessel J-S. Impact of female and male obesity on IVF/ICSI: results of 700, 000 ART-cycles in Germany. Gynecol Endocrinol 2011; 27: 144-149
45. Lane M, Gardner DK. Amino acids and vitamins prevent culture-induced metabolic perturbations and associated loss of viability of mouse blastocysts. Hum Reprod 1998; 13: 991-997
46. Lane M, Robker RL, Robertson SA. Parenting from before conception. Science 2014; 345: 756-760
47. Leary C, Leese HJ, Sturmey RG. Humanembryos from overweight and obese women display phenotypic and metabolic abnormalities. Hum Reprod 2015; 30: 122-132
48. Leese HJ, Barton AM. Pyruvate and glucose uptake by mouse ova and preimplantation embryos. Reproduction 1984; 72: 9-13
49. Luzzo KM, Wang Q, Purcell SH, Chi M, Jimenez PT, Grindler N, Schedl T, Moley KH. High fat diet induced developmental defects in the mouse: oocyte meiotic aneuploidy and fetal growth retardation/brain defects. PLoS One 2012; 7: 12
50. Maheshwari A, Stofberg L, Bhattacharya S. Effect of overweight and obesity on assisted reproductive technology: a systematic review. Hum Reprod Update 2007; 13: 433-444
51. Maloney C, Hay S, Young L, Sinclair K, Reese W. Amethyl-deficient diet fed to rat dams during the peri-conception period programs glucose homeostasis in adult male but not female offspring. J Nutr 2011; 14: 95-100
52. Martini AC, Tissera A, Estofán D, Molina RI, Mangeaud A, de Cuneo MF, Ruiz RD. Overweight and seminal quality: a study of 794 patients. Fertil Steril 2010; 94: 1739-1743
53. Martyn JA, Kaneki M, Yasuhara S. Obesity-induced insulin resistance and hyperglycemia: etiologic factors and molecular mechanisms. Anesthesiology 2008; 109: 137-148
54. McCord JM. The evolution of free radicals and oxidative stress. Am J Med 2000; 108: 652-659
55. McPherson NO, Fullston T, Bakos HW, Setchell BP, Lane M. Obese father's metabolic state, adiposity, and reproductive capacity indicate son's reproductive health. Fertil Steril 2014; 101: 865-873 e861
56. Meseguer M, Herrero J, Tejera A, Hilligsoe KM, Ramsing NB, Remohí J. The use of morphokinetics as a predictor of embryo implantation. Hum Reprod 2011; 26: 2658-2671
57. Meseguer M, Rubio I, Cruz M, Basile N, Marcos J, Requena A. Embryo incubation and selection in a time-lapse monitoring system improves pregnancy outcome compared with a standard incubator: a retrospective cohort study. Fertil Steril 2012; 98: 1481-1489 e1410
58. Minge C, Robker R, Norman R. PPAR Gamma: Coordinating metabolic and immune contributions to female fertility. PPAR Res 2008; 2008: 243791, doi: 10.1155/2008/243791
59. Mitchell M, Bakos HW, Lane M. Paternal diet-induced obesity impairs embryo development and implantation in the mouse. Fertil Steril 2011; 95: 1349-1353
60. Mokdad AH, Ford ES, Bowman BA, Dietz WH, Vinicor F, Bales VS, Marks JS. Prevalence of obesity, diabetes, and obesity-related health risk factors. JAMA 2003; 289: 76-79
61. Montag M, Schimming T, Köster M, Zhou C, Dorn C, Rösing B, van der Ven H, van der Ven K. Oocyte zona birefringence intensity is associated with embryonic implantation potential in ICSI cycles. Reprod Biomed Online 2008; 16: 239-244
62. Muller PY, Janovjak H, Miserez AR, Dobbie Z. Processing of gene expression data generated by quantitative real-Time RT-PCR. Biotechniques 2002; 32: 1372-1380
63. Ng M, Fleming T, Robinson M, Thomson B, Graetz N, Margono C, Mullany EC, Biryukov S, Abbafati C, Abera SF et al. Global, regional, and national prevalence of overweight and obesity in children and adults during 1980?: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 2014; 384: 766-781
64. Norman RJ, Clark AM. Obesity and reproductive disorders: a review. Reprod Fertility Dev 1997; 10: 55-63
65. Palmer NO, Bakos HW, Owens JA, Setchell BP, Lane M. Diet and exercise in an obese mouse fed a high-fat diet improve metabolic health and reverse perturbed sperm function. Am J Physiol Endocrinol Metab 2012; 302: e768-e780
66. Pantaleon M, Kaye PL. Glucose transporters in preimplantation development. Reproduction 1998; 3: 77-81
67. Paria BC, Huet-Hudson YM, Dey SK. Blastocyst's state of activity determines the 'window' of implantation in the receptive mouse uterus. Proc Natl Acad Sci USA 1993; 90: 10159-10162
68. Robker RL, Akison LK, Bennett BD, Thrupp PN, Chura LR, Russell DL, Lane M, Norman RJ. Obese women exhibit differences in ovarian metabolites, hormones, and gene expression compared with moderate-weight women. J Clin Endocrinol Metab 2009; 94: 1533-1540
69. Rubio I, Galan A, Larreategui Z, Ayerdi F, Bellver J, Herrero J, Meseguer M. Clinical validation of embryo culture and selection by morphokinetic analysis: a randomized, controlled trial of the EmbryoScope. Fertil Steril 2014; 102: 1287-1294 e1285
70. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Meth 2012; 9: 671-675
71. Silveira PP, Portella AK, Goldani MZ, Barbieri MA. Developmental origins of health and disease (DOHaD). J Pediatr 2007; 83: 494-504
72. Simon P. Q-Gene: processing quantitative real-Time RT-PCR data. Bioinformatics 2003; 19: 1439-1440
73. Sinclair KD, Singh R. Modelling the developmental origins of health and disease in the early embryo. Theriogenology 2007; 67: 43-53
74. Skinner MK. Role of epigenetics in developmental biology and transgenerational inheritance. Birth Defects Res C 2011; 93: 51-55
75. Styne-Gross A, Elkind-Hirsch K, Scott Jr. RT. Obesity does not impact implantation rates or pregnancy outcome in women attempting conception through oocyte donation. Fertil Steril 2005; 83: 1629-1634
76. Sun Q, Yue P, Deiuliis JA, Lumeng CN, Kampfrath T, Mikolaj MB, Cai Y, Ostrowski MC, Lu B, Parthasarathy S et al. Ambient air pollution exaggerates adipose inflammation and insulin resistance in a mouse model of diet-induced obesity. Circulation 2009; 119: 538-546
77. Sutton-McDowall ML, Gilchrist RB, Thompson JG. The pivotal role of glucose metabolism in determining oocyte developmental competence. Reproduction 2010; 139: 685-695
78. van der Steeg JW, Steures P, Eijkemans MJ, Habbema JD, Hompes PG, Burggraaff JM, Oosterhuis GJ, Bossuyt PM, van der Veen F, Mol BW. Obesity affects spontaneous pregnancy chances in subfertile, ovulatory women. Hum Reprod 2008; 23: 324-328
79. Van Hoeck V, Sturmey RG, Bermejo-Alvarez P, Rizos D, Gutierrez-Adan A, Leese HJ, Bols PEJ, Leroy JLMR. Elevated non-esterified fatty acid concentrations during bovine oocyte maturation compromise early embryo physiology. PLoS One 2011; 6: e23183
80. Wadhwa PD, Buss C, Entringer S, Swanson JM. Developmental origins of health and disease: brief history of the approach and current focus on epigenetic mechanisms. Semin Reprod Med 2009; 27: 358-368
81. Wale PL, Gardner DK. Time-lapse analysis of mouse embryo development in oxygen gradients. Reprod Biomed Online 2010; 21: 402-410
82. Wang H, Dey SK. Roadmap to embryo implantation: clues from mouse models. Nat Rev Genet 2006; 7: 185-199
83. Watkins A, Lucas E, Fleming T. Impact of the periconceptional environment on the programming of adult disease. J DOHaD 2010; 1: 97-95
84. Winzell MS, Ahrén B. The high-fat diet-fed mouse: a model for studying mechanisms and treatment of impaired glucose tolerance and type 2 diabetes. Diabetes 2004; 53: S215-S219
85. Wong CC, Loewke KE, Bossert NL, Behr B, DeJonge CJ, Baer TM, Pera RAR. Non-invasive imaging of human embryos before embryonic genome activation predicts development to the blastocyst stage. Nat Biotech 2010; 28: 1115-1121
86. Wong C, Chen AA, Behr B, Shen S. Time-lapse microscopy and image analysis in basic and clinical embryo development research. Reprod Biomed Online 2013; 26: 120-129
87. World Health Organisation. Obesity and Overweight. [Fact Sheet]. 2015. Retrieved 20/01/2015 from http://www.who.int/mediacentre/factsheets/fs311/en (10 June 2015, date last accessed
88. Wu LL, Russell DL, Wong SL, Chen M, Tsai T-S, St John JC, Norman RJ, Febbraio MA, Carroll J, Robker RL. Mitochondrial dysfunction in oocytes of obese mothers: transmission to offspring and reversal by pharmacological endoplasmic reticulum stress inhibitors. Development 2015; 142: 681-691