Paternal diet-induced obesity impairs embryo development and implantation in the mouse

Fertility and Sterility

Volumn 95, Issue 4, 2011, Pages 1349-1353

  Mitchell, Megan ^a   Bakos, Hassan W ^a,b   Lane, Michelle ^a,b  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b Repromed   (Australia)

Author keywords

blastocyst; fetal growth; obesity; Paternal; pregnancy

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOPSY; BLASTOCYST; CELL COUNT; CELL DIVISION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; FETUS GROWTH; FETUS WEIGHT; LIPID DIET; MALE; MATING; MOUSE; NIDATION; NONHUMAN; OBESITY; PLACENTA DEVELOPMENT; PLACENTA WEIGHT; PREGNANCY; PRIORITY JOURNAL; ZYGOTE;

ANIMALS; DIETARY FATS; EMBRYO IMPLANTATION; EMBRYO IMPLANTATION, DELAYED; EMBRYONIC DEVELOPMENT; FATHERS; FEMALE; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED CBA; OBESITY; PATERNAL BEHAVIOR; PREGNANCY;

EID: 79952440453     PISSN: 00150282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.fertnstert.2010.09.038     Document Type: Article

References (60)

1. Australian Bureau of Statistics. 4364.0 - National Health Survey 2007-2008: summary of results. Available at: http://www.abs.gov.au/ausstats/ abs@nsf/mf/4364.0/. Accessed July 9, 2010.
2. National Center for Health Statistics, US Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Health Statistics. Health, United States, 2008, with special feature on the health of young adults. Available at: www.cdc.gov/nchs/data/hus/hus08.pdf. Accessed July 9, 2010.
3. Economic and Social Data Service, National Centre for Social Research, University College London, Department of Epidemiology and Public Health. Health survey for England SN 6112. Available at: www.dh.gov.uk/en/ Publicationsandstatistics/PublishedSurvey/HealthSurveyForEngland/index.htm. Accessed July 9, 2010.
4. M.A. Hassan, and S.R. Killick Is previous aberrant reproductive outcome predictive of subsequently reduced fecundity? Hum Reprod 20 2005 657 664 (Pubitemid 40425491)
5. J.W. van der Steeg, P. Steures, M.J. Eijkemans, J.D. Habbema, P.G. Hompes, and J.M. Burggraaff Obesity affects spontaneous pregnancy chances in subfertile, ovulatory women Hum Reprod 23 2008 324 328 (Pubitemid 351651248)
6. H. Lashen, K. Fear, and D.W. Sturdee Obesity is associated with increased risk of first trimester and recurrent miscarriage: matched case-control study Hum Reprod 19 2004 1644 1646 (Pubitemid 38997196)
7. S.Y. Ku, S.D. Kim, B.C. Jee, C.S. Suh, Y.M. Choi, and J.G. Kim Clinical efficacy of body mass index as predictor of in vitro fertilization and embryo transfer outcomes J Korean Med Sci 21 2006 300 303
8. C. Lenoble, J. Guibert, G. Lefebvre, and M. Dommergues [Effect of women's weight on the success rate of in vitro fertilization] Gynecol Obstet Fertil 36 2008 940 944
9. J.B. Loveland, H.D. McClamrock, A.M. Malinow, and F.I. Sharara Increased body mass index has a deleterious effect on in vitro fertilization outcome J Assist Reprod Genet 18 2001 382 386 (Pubitemid 32726994)
10. R.H. Nguyen, A.J. Wilcox, R. Skjaerven, and D.D. Baird Men's body mass index and infertility Hum Reprod 22 2007 2488 2493 (Pubitemid 47289065)
11. C.H. Ramlau-Hansen, A.M. Thulstrup, E.A. Nohr, J.P. Bonde, T.I. Sorensen, and J. Olsen Subfecundity in overweight and obese couples Hum Reprod 22 2007 1634 1637 (Pubitemid 47055153)
12. A.S. Aggerholm, A.M. Thulstrup, G. Toft, C.H. Ramlau-Hansen, and J.P. Bonde Is overweight a risk factor for reduced semen quality and altered serum sex hormone profile? Fertil Steril 90 2008 619 626
13. S.J. Winters, C. Wang, E. Abdelrahaman, V. Hadeed, M.A. Dyky, and A. Brufsky Inhibin-B levels in healthy young adult men and prepubertal boys: is obesity the cause for the contemporary decline in sperm count because of fewer Sertoli cells? J Androl 27 2006 560 564 (Pubitemid 44126269)
14. E.M. Pauli, R.S. Legro, L.M. Demers, A.R. Kunselman, W.C. Dodson, and P.A. Lee Diminished paternity and gonadal function with increasing obesity in men Fertil Steril 90 2008 346 351
15. J.E. Chavarro, T.L. Toth, D.L. Wright, J.D. Meeker, and R. Hauser Body mass index in relation to semen quality, sperm DNA integrity, and serum reproductive hormone levels among men attending an infertility clinic Fertil Steril 93 2010 2222 2231
16. S. Koloszar, I. Fejes, Z. Zavaczki, J. Daru, J. Szollosi, and A. Pal Effect of body weight on sperm concentration in normozoospermic males Arch Androl 51 2005 299 304 (Pubitemid 40992439)
17. T.M. Stewart, D.Y. Liu, C. Garrett, N. Jorgensen, E.H. Brown, and H.W. Baker Associations between andrological measures, hormones and semen quality in fertile Australian men: inverse relationship between obesity and sperm output Hum Reprod 24 2009 1561 1568
18. A.O. Hammoud, N. Wilde, M. Gibson, A. Parks, D.T. Carrell, and A.W. Meikle Male obesity and alteration in sperm parameters Fertil Steril 90 2008 2222 2225
19. H.I. Kort, J.B. Massey, C.W. Elsner, D. Mitchell-Leef, D.B. Shapiro, and M.A. Witt Impact of body mass index values on sperm quantity and quality J Androl 27 2006 450 452 (Pubitemid 43667994)
20. M. Sallmen, D.P. Sandler, J.A. Hoppin, A. Blair, and D.D. Baird Reduced fertility among overweight and obese men Epidemiology 17 2006 520 523 (Pubitemid 44223059)
21. A.M. Ingalls, M.M. Dickie, and G.D. Snell Obese, a new mutation in the house mouse J Hered 41 1950 317 318
22. H.W. Bakos, M. Mitchell, B.P. Setchell, and M. Lane The effect of paternal diet-induced obesity on sperm function and fertilization in a mouse model Int J Androl 2010 10.1111/j.1365-2605.2010.01092.x
23. B.I. Ghanayem, R. Bai, G.E. Kissling, G. Travlos, and U. Hoffler Diet-Induced obesity in male mice is associated with reduced fertility and potentiation of acrylamide-induced reproductive toxicity Biol Reprod 82 2009 96 104
24. D.V. Tortoriello, J. McMinn, and S.C. Chua Dietary-induced obesity and hypothalamic infertility in female DBA/2J mice Endocrinology 145 2004 1238 1247 (Pubitemid 38281005)
25. M.J. De Blasio, M. Dodic, A.J. Jefferies, K.M. Moritz, E.M. Wintour, and J.A. Owens Maternal exposure to dexamethasone or cortisol in early pregnancy differentially alters insulin secretion and glucose homeostasis in adult male sheep offspring Am J Physiol 293 2007 E75 E82
26. M. Mitchell, K.S. Cashman, D.K. Gardner, J.G. Thompson, and M. Lane Disruption of mitochondrial malate-aspartate shuttle activity in mouse blastocysts impairs viability and fetal growth Biol Reprod 80 2009 295 301
27. D.K. Gardner, M.W. Lane, and M. Lane EDTA stimulates cleavage stage bovine embryo development in culture but inhibits blastocyst development and differentiation Mol Reprod Dev 57 2000 256 261
28. M. Kamjoo, D.R. Brison, and S.J. Kimber Apoptosis in the preimplantation mouse embryo: effect of strain difference and in vitro culture Mol Reprod Dev 61 2002 67 77 (Pubitemid 135715267)
29. M. Lane, and D.K. Gardner Differential regulation of mouse embryo development and viability by amino acids J Reprod Fertil 109 1997 153 164
30. S.T. Kim, and K.H. Moley Paternal effect on embryo quality in diabetic mice is related to poor sperm quality and associated with decreased glucose transporter expression Reproduction 136 2008 313 322
31. C. Paul, A.A. Murray, N. Spears, and P.T. Saunders A single, mild, transient scrotal heat stress causes DNA damage, subfertility and impairs formation of blastocysts in mice Reproduction 136 2008 73 84 (Pubitemid 351984721)
32. B. Zhu, S.K. Walker, H. Oakey, B.P. Setchell, and S. Maddocks Effect of paternal heat stress on the development in vitro of preimplantation embryos in the mouse Andrologia 36 2004 384 394 (Pubitemid 39540777)
33. M. Luna, E. Finkler, J. Barritt, N. Bar-Chama, B. Sandler, and A.B. Copperman Paternal age and assisted reproductive technology outcome in ovum recipients Fertil Steril 92 2009 1772 1775
34. W.Y. Kwong, A.E. Wild, P. Roberts, A.C. Willis, and T.P. Fleming Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension Development 127 2000 4195 4202
35. T.J. Cicero, L.A. Davis, M.C. LaRegina, E.R. Meyer, and M.S. Schlegel Chronic opiate exposure in the male rat adversely affects fertility Pharmacol Biochem Behav 72 2002 157 163 (Pubitemid 34251322)
36. S.A. Venners, X. Wang, C. Chen, L. Wang, D. Chen, and W. Guang Paternal smoking and pregnancy loss: a prospective study using a biomarker of pregnancy Am J Epidemiol 159 2004 993 1001 (Pubitemid 38608277)
37. N. Balasinor, M.K. Gill-Sharma, P. Parte, S. D'Souza, N. Kedia, and H.S. Juneja Effect of paternal administration of an antiestrogen, tamoxifen on embryo development in rats Mol Cell Endocrinol 190 2002 159 166 (Pubitemid 34462060)
38. M. Mitchell, S.J. Schulz, D.T. Armstrong, and M. Lane Metabolic and mitochondrial dysfunction in early mouse embryos following maternal dietary protein intervention Biol Reprod 80 2009 622 630
39. A.J. Watkins, A. Wilkins, C. Cunningham, V.H. Perry, M.J. Seet, and C. Osmond Low protein diet fed exclusively during mouse oocyte maturation leads to behavioural and cardiovascular abnormalities in offspring J Physiol 586 2008 2231 2244 (Pubitemid 351524574)
40. J.M. Friedman Genetic disease in the offspring of older fathers Obstet Gynecol 57 1981 745 749 (Pubitemid 11126059)
41. S. Garcia-Palomares, S. Navarro, J.F. Pertusa, C. Hermenegildo, M.A. Garcia-Perez, and F. Rausell Delayed fatherhood in mice decreases reproductive fitness and longevity of offspring Biol Reprod 80 2009 343 349
42. S. Garcia-Palomares, J.F. Pertusa, J. Minarro, M.A. Garcia-Perez, C. Hermenegildo, and F. Rausell Long-term effects of delayed fatherhood in mice on postnatal development and behavioral traits of offspring Biol Reprod 80 2009 337 342
43. S. Saha, A.G. Barnett, C. Foldi, T.H. Burne, D.W. Eyles, and S.L. Buka Advanced paternal age is associated with impaired neurocognitive outcomes during infancy and childhood PLoS Med 6 2009 e40
44. J.S. Chang, S. Selvin, C. Metayer, V. Crouse, A. Golembesky, and P.A. Buffler Parental smoking and the risk of childhood leukemia Am J Epidemiol 163 2006 1091 1100 (Pubitemid 43987573)
45. T. Sorahan, P. Prior, R.J. Lancashire, S.P. Faux, M.A. Hulten, and I.M. Peck Childhood cancer and parental use of tobacco: deaths from 1971 to 1976 Br J Cancer 76 1997 1525 1531 (Pubitemid 27501139)
46. E.L. Abel, M.W. Church, and B.A. Dintcheff Prenatal alcohol exposure shortens life span in rats Teratology 36 1987 217 220 (Pubitemid 17161545)
47. E.L. Abel, and C. Moore Effects of paternal alcohol consumption in mice Alcohol Clin Exp Res 11 1987 533 535 (Pubitemid 18022807)
48. S. Danielzik, K. Langnase, M. Mast, C. Spethmann, and M.J. Muller Impact of parental BMI on the manifestation of overweight 5-7 year old children Eur J Nutr 41 2002 132 138 (Pubitemid 36056334)
49. L. Li, C. Law, R. Lo Conte, and C. Power Intergenerational influences on childhood body mass index: the effect of parental body mass index trajectories Am J Clin Nutr 89 2009 551 557
50. A.N. Fatehi, M.M. Bevers, E. Schoevers, B.A. Roelen, B. Colenbrander, and B.M. Gadella DNA damage in bovine sperm does not block fertilization and early embryonic development but induces apoptosis after the first cleavages J Androl 27 2006 176 188
51. M. Perez-Crespo, P. Moreira, B. Pintado, and A. Gutierrez-Adan Factors from damaged sperm affects its integrity and its ability to promote embryo implantation in mice J Androl 29 2008 47 54
52. H.W. Bakos, J.G. Thompson, D. Feil, and M. Lane Sperm DNA damage is associated with assisted reproductive technology pregnancy Int J Androl 31 2008 518 526
53. A. Borini, N. Tarozzi, D. Bizzaro, M.A. Bonu, L. Fava, and C. Flamigni Sperm DNA fragmentation: paternal effect on early post-implantation embryo development in ART Hum Reprod 21 2006 2876 2881 (Pubitemid 44567001)
54. E. Seli, D.K. Gardner, W.B. Schoolcraft, O. Moffatt, and D. Sakkas Extent of nuclear DNA damage in ejaculated spermatozoa impacts on blastocyst development after in vitro fertilization Fertil Steril 82 2004 378 383 (Pubitemid 39092038)
55. A. Iyer, D.P. Fairlie, J.B. Prins, B.D. Hammock, and L. Brown Inflammatory lipid mediators in adipocyte function and obesity Nat Rev Endocrinol 6 2010 71 82
56. K.P. Karalis, P. Giannogonas, E. Kodela, Y. Koutmani, M. Zoumakis, and T. Teli Mechanisms of obesity and related pathology: linking immune responses to metabolic stress FEBS J 276 2009 5747 5754
57. A.C. Martini, A. Tissera, D. Estofan, R.I. Molina, A. Mangeaud, and M. Fiol de Cuneo Overweight and seminal quality: a study of 794 patients Fertil Steril 94 2010 1739 1743
58. H.K. Poon, K.H. Lee, C.L. Wong, W.S. O, and P.H. Chow A lack of contact of sperm with accessory sex gland secretions deregulates DNA methylation and imprinted gene expression in rodent embryos Syst Biol Reprod Med 55 2009 200 213
59. T. Kriegel, F. Heidenreich, K. Kettner, T. Pursche, B. Hoflack, and S. Grunewald Identification of diabetes- and obesity-associated proteomic changes in human spermatozoa by difference gel electrophoresis Reprod Biomed Online 19 2009 660 670
60. C. Yauk, A. Polyzos, A. Rowan-Carroll, C.M. Somers, R.W. Godschalk, and F.J. Van Schooten Germ-line mutations, DNA damage, and global hypermethylation in mice exposed to particulate air pollution in an urban/industrial location Proc Natl Acad Sci U S A 105 2008 605 610 (Pubitemid 351171755)