Paternal under-nutrition programs metabolic syndrome in offspring which can be reversed by antioxidant/vitamin food fortification in fathers

Scientific Reports

Volumn 6, Issue , 2016, Pages

  McPherson, Nicole O ^a   Fullston, Tod ^a   Kang, Wan Xian ^a   Sandeman, Lauren Y ^a   Corbett, Mark A ^a   Owens, Julie A ^a   Lane, Michelle ^a,b  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b MONASH IVF   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; INSULIN; LEPTIN; LIPID; REACTIVE OXYGEN METABOLITE;

ANIMAL; BLOOD; BODY COMPOSITION; C57BL MOUSE; COMPLICATION; EMBRYO DEVELOPMENT; FEMALE; FORTIFIED FOOD; FOUNDER EFFECT; GENETICS; MALE; MALE INFERTILITY; MALNUTRITION; METABOLIC SYNDROME X; METABOLISM; OBESITY; PATERNAL INHERITANCE; SPERMATOZOON COUNT; SPERMATOZOON MOTILITY;

ADIPOSITY; ANIMALS; ANTIOXIDANTS; BODY COMPOSITION; EMBRYONIC DEVELOPMENT; FEMALE; FOOD, FORTIFIED; FOUNDER EFFECT; INFERTILITY, MALE; INSULIN; LEPTIN; LIPIDS; MALE; MALNUTRITION; METABOLIC SYNDROME; MICE, INBRED C57BL; PATERNAL INHERITANCE; REACTIVE OXYGEN SPECIES; SPERM COUNT; SPERM MOTILITY;

EID: 84973343759     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep27010     Document Type: Article

References (59)

1. Black, R. E. et al. Maternal and child undernutrition and overweight in low-income and middle-income countries. Lancet 382, 427-451 (2013).
2. Black, R. E. et al. Maternal and child undernutrition: global and regional exposures and health consequences. Lancet 371, 243-260 (2008).
3. de Rooij, S. R. et al. Glucose tolerance at age 58 and the decline of glucose tolerance in comparison with age 50 in people prenatally exposed to the Dutch famine. Diabetologia 49, 637-643 (2006).
4. Kaati, G., Bygren, L. O. & Edvinsson, S. Cardiovascular and diabetes mortality determined by nutrition during parents' and grandparents' slow growth period. Eur J Hum Genet 10, 682-688 (2002).
5. Fullston, T. et al. Diet-induced paternal obesity in the absence of diabetes diminishes the reproductive health of two subsequent generations of mice. Hum Reprod 27, 1391-1400 (2012).
6. Fullston, T. et al. Paternal obesity initiates metabolic disturbances in two generations of mice and alters the transcription profile of tesis and sperm microRNA content. FASEB J 27, 4226-4243 (2013).
7. Ng, S. F. et al. Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring. Nature 467, 963-966 (2010).
8. Tunc, O., Bakos, H. W. & Tremellen, K. Impact of body mass index on seminal oxidative stress. Andrologia 43, 121-128 (2011).
9. Palmer, N. O., Bakos, H. W., Owens, J. A., Setchell, B. P. & 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 302, E768-780 (2012).
10. Zhao, J., Zhai, L., Liu, Z., Wu, S. & Xu, L. Leptin level and oxidative stress contribute to obesity-induced low testosterone in murine testicular tissue. Oxidative medicine and cellular longevity 2014, 190945 (2014).
11. Bakos, H. W., Henshaw, R. C., 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 95, 1700-1704 (2011).
12. Binder, N. K., Hannan, N. J. & Gardner, D. K. Paternal diet-induced obesity retards early mouse embryo development, mitochondrial activity and pregnancy health. PLoS One 7, e52304 (2012).
13. McPherson, N. O., Fullston, T., Owens J. A. & Lane, M. Paternal lifestyle interventions in obese males restores early embryo development and fetal weights, improving the metabolic health and adiposity status in subsequent female offspring. J Dev Orig Health Dis 2, S10-S10 (2013).
14. Das, J. K., Salam, R. A., Kumar, R. & Bhutta, Z. A. Micronutrient fortification of food and its impact on woman and child health: a systematic review. Systematic reviews 2, 67 (2013).
15. Tunc, O., Thompson, J. & Tremellen, K. Improvement in sperm DNA quality using an oral antioxidant therapy. Reprod Biomed Online 18, 761-768 (2009).
16. Lambrot, R. et al. Low paternal dietary folate alters the mouse sperm epigenome and is associated with negative pregnancy outcomes. Nature communications 4, 2889 (2013).
17. Dulloo, A. G., Jacquet, J., Seydoux, J. & Montani, J. P. The thrifty 'catch-up fat' phenotype: its impact on insulin sensitivity during growth trajectories to obesity and metabolic syndrome. Int J Obes (Lond) 30 Suppl 4, S23-35 (2006).
18. Lane, M. et al. Oxidative stress in mouse sperm impairs embryo development, fetal growth and alters adiposity and glucose regulation in female offspring PLOS One 9(7), e100832 (2014).
19. Ahsan, U. et al. Role of selenium in male reproduction-A review. Anim Reprod Sci 146, 55-62 (2014).
20. Tremellen, K., Miari, G., Froiland, D. & Thompson, J. A randomised control trial examining the effect of an antioxidant (Menevit) on pregnancy outcome during IVF-ICSI treatment. Aust N Z J Obstet Gynaecol 47, 216-221 (2007).
21. Buhling, K. J. & Laakmann, E. The effect of micronutrient supplements on male fertility. Current opinion in obstetrics & gynecology 26, 199-209 (2014).
22. Ng, S. F. et al. Paternal high-fat diet consumption induces common changes in the transcriptomes of retroperitoneal adipose and pancreatic islet tissues in female rat offspring. FASEB journal: official publication of the Federation of American Societies for Experimental Biology. 28, 1830-41 (2014).
23. Young, M. D., Wakefield, M. J., Smyth, G. K. & Oshlack, A. Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11, R14 (2010).
24. Watkins, A. J. & Sinclair, K. D. Paternal low protein diet affects adult offspring cardiovascular and metabolic function in mice. American journal of physiology. Heart and circulatory physiology. 306, H1444-52 (2014).
25. Radford, E. J. et al. In utero effects. In utero undernourishment perturbs the adult sperm methylome and intergenerational metabolism. Science 345, 1255903 (2014).
26. Jove, M. et al. Caloric restriction reveals a metabolomic and lipidomic signature in liver of male mice. Aging Cell 13, 828-837 (2014).
27. Gomez, J. et al. Effect of 8.5% and 25% caloric restriction on mitochondrial free radical production and oxidative stress in rat liver. Biogerontology 8, 555-566 (2007).
28. WHO & World Health Organisation. WHO laboratory manual for the examination and processing of human semen. 5th edition edn, Ch. 2, 21-58 (Cambridge University Press, 2010).
29. Suarez, S. S. Control of hyperactivation in sperm. Hum Reprod Update 14, 647-657 (2008).
30. Sakkas, D., Urner, F., Menezo, Y. & Leppens, G. Effects of glucose and fructose on fertilization, cleavage, and viability of mouse embryos in vitro. Biol Reprod 49, 1288-1292 (1993).
31. Dal Canto, M. et al. Cleavage kinetics analysis of human embryos predicts development to blastocyst and implantation. Reprod Biomed Online 25, 474-480 (2012).
32. Liang, F. et al. Paternal ethanol exposure and behavioral abnormities in offspring: Associated alterations in imprinted gene methylation. Neuropharmacology 81C, 126-133 (2014).
33. Edwards, A. M. & Cameron, E. Z. Forgotten fathers: paternal influences on mammalian sex allocation. Trends in ecology & evolution 29, 158-164 (2014).
34. Symonds, M. E., Pope, M., Sharkey, D. & Budge, H. Adipose tissue and fetal programming. Diabetologia 55, 1597-1606 (2012).
35. Fullston, T. et al. Paternal obesity induces metabolic and sperm disturbances in male offspring that are exacerbated by their exposure to an "obesogenic" diet. Physiological reports 3, doi: 10.14814/phy2.12336 (2015).
36. Prentice, A. M. The emerging epidemic of obesity in developing countries. Int J Epidemiol 35, 93-99 (2006).
37. Carone, B. R. et al. Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 143, 1084-1096 (2010).
38. Benefice, E., Garnier, D., Simondon, K. B. & Malina, R. M. Relationship between stunting in infancy and growth and fat distribution during adolescence in Senegalese girls. Eur J Clin Nutr 55, 50-58 (2001).
39. Anderson, L. M. et al. Preconceptional fasting of fathers alters serum glucose in offspring of mice. Nutrition 22, 327-331 (2006).
40. Aitken, R. J., Koopman, P. & Lewis, S. E. Seeds of concern. Nature 432, 48-52 (2004).
41. de Lamirande, E. & Gagnon, C. Impact of reactive oxygen species on spermatozoa: a balancing act between beneficial and detrimental effects. Hum Reprod 10 Suppl 1, 15-21 (1995).
42. Aitken, J. & Fisher, H. Reactive oxygen species generation and human spermatozoa: the balance of benefit and risk. BioEssays : news and reviews in molecular, cellular and developmental biology 16, 259-267 (1994).
43. Alvarez, J. G. & Storey, B. T. Differential incorporation of fatty acids into and peroxidative loss of fatty acids from phospholipids of human spermatozoa. Mol Reprod Dev 42, 334-346 (1995).
44. Koppers, A. J., Garg, M. L. & Aitken, R. J. Stimulation of mitochondrial reactive oxygen species production by unesterified, unsaturated fatty acids in defective human spermatozoa. Free radical biology & medicine 48, 112-119 (2010).
45. Saez, F., Ouvrier, A. & Drevet, J. R. Epididymis cholesterol homeostasis and sperm fertilizing ability. Asian J Androl 13, 11-17 (2011).
46. Pathak, S. et al. Effect of tamoxifen treatment on global and insulin-like growth factor 2-H19 locus-specific DNA methylation in rat spermatozoa and its association with embryo loss. Fertil Steril 91, 2253-2263 (2009).
47. Ostermeier, G. C., Goodrich, R. J., Diamond, M. P., Dix, D. J. & Krawetz, S. A. Toward using stable spermatozoal RNAs for prognostic assessment of male factor fertility. Fertil Steril 83, 1687-1694 (2005).
48. Bromfield, J. J. et al. Maternal tract factors contribute to paternal seminal fluid impact on metabolic phenotype in offspring. Proc Natl Acad Sci USA 111, 2200-2205 (2014).
49. Jiang, L. et al. Sperm, but not oocyte, DNA methylome is inherited by zebrafish early embryos. Cell 153, 773-784 (2013).
50. Bakos, H. W., Mitchell, M., Setchell, B. P. & Lane, M. The effect of paternal diet-induced obesity on sperm function and fertilization in a mouse model. Int J Androl 5, 402-10 (2010).
51. Bakos, H. W., Mitchell, M., Setchell, B. P. & Lane, M. The effect of paternal diet-induced obesity on sperm function and fertilization in a mouse model. Int J Androl 34, 402-410 (2011).
52. Noblanc, A. et al. DNA oxidative damage in mammalian spermatozoa: where and why is the male nucleus affected? Free radical biology & medicine 65, 719-723 (2013).
53. Nagy, A., Gertsenstein, M., Vintersten, K. & Behringer, R. Manipulating the Mouse Embryo. A Laboratory Manual. Third Edition, Section C, 92-95 (Cold Spring Harbour Laboratory Press, 2003).
54. Gardner, D. K., Lane, M. & Watson, A. J. A Laboratory Guide to the Mammalian Embryo, Ch. 2, 26-27 (Oxford University Press, 2004).
55. Zander, D. L., Thompson, J. G. & Lane, M. Perturbations in mouse embryo development and viability caused by ammonium are more severe after exposure at the cleavage stages. Biol Reprod 74, 288-294 (2006).
56. Nagy, T. R. & Clair, A. L. Precision and accuracy of dual-energy X-ray absorptiometry for determining in vivo body composition of mice. Obes Res 8, 392-398 (2000).
57. Kim, D. et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14, R36 (2013).
58. Anders, S., Pyl, P. T. & Huber, W. HTSeq-a Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166-169 (2015).
59. Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139-140 (2010).