Paternal obesity induces metabolic and sperm disturbances in male offspring that are exacerbated by their exposure to an “obesogenic” diet

Physiological Reports

Volumn 3, Issue 3, 2015, Pages

  Fullston, Tod ^a   McPherson, Nicole O ^a,b   Owens, Julie A ^a   Kang, Wan Xian ^a   Sandeman, Lauren Y ^a   Lane, Michlle ^a,c  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c MONASH IVF   (Australia)

Author keywords

Metabolic syndrome; Obesogenic environment; Paternal obesity; Paternal programming; Second hit; Subfertility

Indexed keywords

FATTY ACID; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; INSULIN; LEPTIN; REACTIVE OXYGEN METABOLITE; TESTOSTERONE; TRIACYLGLYCEROL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; GLUCOSE TOLERANCE TEST; INSULIN BLOOD LEVEL; INSULIN TOLERANCE TEST; LIPID DIET; MALE; MOUSE; NONHUMAN; OBESITY; SEMEN ABNORMALITY; SPERM QUALITY; SPERMATOZOON COUNT; SPERMATOZOON MOTILITY; TRIACYLGLYCEROL BLOOD LEVEL; WEIGHT GAIN;

EID: 84943650348     PISSN: None     EISSN: 2051817X     Source Type: Journal    
DOI: 10.14814/phy2.12336     Document Type: Article

References (57)

1. Aitken, R. J., T. B. Smith, M. S. Jobling, M. A. Baker, and G. N. De Iuliis. 2014. Oxidative stress and male reproductive health. Asian J. Androl. 16:31-38
2. Asrih, M., and F. R. Jornayvaz. 2014. Diets and nonalcoholic fatty liver disease: the good and the bad. Clin. Nutr. 33:186-190
3. Bakos, H. W., J. G. Thompson, D. Feil, and M. Lane. 2008. Sperm DNA damage is associated with assisted reproductive technology pregnancy. Int. J. Androl. 31:518-526
4. Bakos, H. W., R. C. Henshaw, M. Mitchell, and M. Lane. 2011a. Paternal body mass index is associated with decreased blastocyst development and reduced live birth rates following assisted reproductive technology. Fertil. Steril. 95:1700-1704
5. Bakos, H. W., M. Mitchell, B. P. Setchell, and M. Lane. 2011b. The effect of paternal diet-induced obesity on sperm function and fertilization in a mouse model. Int. J. Androl. 34:402-410
6. Bygren, L. O., G. Kaati, and S. Edvinsson. 2001. Longevity determined by paternal ancestors’ nutrition during their slow growth period. Acta. Biotheor. 49:53-59
7. Cervantes-Rodriguez, M., M. Martinez-Gomez, E. Cuevas, L. Nicolas, F. Castelan, P. W. Nathanielsz, et al. 2014. Sugared water consumption by adult offspring of mothers fed a protein-restricted diet during pregnancy results in increased offspring adiposity: the second hit effect. Br. J. Nutr. 111:616-624
8. Dacheux, J. L., and F. Dacheux. 2014. New insights into epididymal function in relation to sperm maturation. Reproduction 147:R27-R42
9. Danielzik, S., K. Langnase, M. Mast, C. Spethmann, and M. J. Muller. 2002. Impact of parental BMI on the manifestation of overweight 5-7 year old children. Eur. J. Nutr. 41:132-138
10. De Blasio, M. J., M. Dodic, A. J. Jefferies, K. M. Moritz, E. M. Wintour, and J. A. Owens. 2007. Maternal exposure to dexamethasone or cortisol in early pregnancy differentially alters insulin secretion and glucose homeostasis in adult male sheep offspring. Am. J. Physiol. Endocrinol. Metab. 293:E75-E82
11. Dunn, G. A., and T. L. Bale. 2009. Maternal high-fat diet promotes body length increases and insulin insensitivity in second-generation mice. Endocrinology 150:4999-5009
12. Dunn, G. A., and T. L. Bale. 2011. Maternal high-fat diet effects on third-generation female body size via the paternal lineage. Endocrinology 152:2228-2236
13. Fall, C. H. 2011. Evidence for the intra-uterine programming of adiposity in later life. Ann. Hum. Biol. 38:410-428
14. Fatemi, N., M. H. Sanati, M. Jamali Zavarehei, H. Ayat, V. Esmaeili, A. Golkar-Narenji, et al. 2013. Effect of tertiarybutyl hydroperoxide (TBHP)-induced oxidative stress on mice sperm quality and testis histopathology. Andrologia 45:232-239
15. Freeman, E., R. Fletcher, C. E. Collins, P. J. Morgan, T. Burrows, and R. Callister. 2012. Preventing and treating childhood obesity: time to target fathers. Int. J. Obes. (Lond) 36:12-15
16. Frenette, G., C. Lessard, and R. Sullivan. 2002. Selected proteins of “prostasome-like particles” from epididymal cauda fluid are transferred to epididymal caput spermatozoa in bull. Biol. Reprod. 67:308-313
17. Fullston, T., N. O. Palmer, J. A. Owens, M. Mitchell, H. W. Bakos, and M. Lane. 2012. Diet-induced paternal obesity in the absence of diabetes diminishes the reproductive health of two subsequent generations of mice. Hum. Reprod. 27:1391-1400
18. Fullston, T., E. M. Ohlsson Teague, N. O. Palmer, M. J. DeBlasio, M. Mitchell, M. Corbett, et al. 2013. 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. 27:4226-4243
19. Gallo, L. A., M. Tran, J. S. Master, K. M. Moritz, and M. E. Wlodek. 2012a. Maternal adaptations and inheritance in the transgenerational programming of adult disease. Cell Tissue Res. 349:863-880
20. Gallo, L. A., M. Tran, K. M. Moritz, A. J. Jefferies, and M. E. Wlodek. 2012b. Pregnancy in aged rats that were born small: cardiorenal and metabolic adaptations and secondgeneration fetal growth. FASEB J. 26:4337-4347
21. Gardner, D. K., M. Lane, and A. J. Watson. 2004. A laboratory guide to the mammalian embryo. Oxford University Press, New York.
22. Gluckman, P. D., M. A. Hanson, and H. G. Spencer. 2005. Predictive adaptive responses and human evolution. Trends Ecol. Evol. 20:527-533
23. Hales, C. N., and D. J. Barker. 1992. Type 2 (non-insulindependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 35:595-601
24. Kaati, G., L. O. Bygren, and S. Edvinsson. 2002. Cardiovascular and diabetes mortality determined by nutrition during parents’ and grandparents’ slow growth period. Eur. J. Hum. Genet. 10:682-688
25. Kazama, M., and A. Hino. 2012. Sea urchin spermatozoa generate at least two reactive oxygen species; the type of reactive oxygen species changes under different conditions. Mol. Reprod. Dev. 79:283-295
26. Kong, A., M. L. Frigge, G. Masson, S. Besenbacher, P. Sulem, G. Magnusson, et al. 2012. Rate of de novo mutations and the importance of father’s age to disease risk. Nature 488:471-475
27. Lane, M., N. O. McPherson, T. Fullston, M. Spillane, L. Sandeman, W. X. Kang, et al. 2014a. Oxidative stress in mouse sperm impairs embryo development, fetal growth and alters adiposity and glucose regulation in female offspring. PLoS ONE 9:e100832.
28. Lane, M., R. L. Robker, and S. A. Robertson. 2014b. Parenting from before conception. Science 345:756-760
29. Lewis, S. E., and R. J. Aitken. 2005. DNA damage to spermatozoa has impacts on fertilization and pregnancy. Cell Tissue Res. 322:33-41
30. Li, L., C. Law, R. Lo Conte, and C. Power. 2009. Intergenerational influences on childhood body mass index: the effect of parental body mass index trajectories. Am. J. Clin. Nutr. 89:551-557
31. Li, C. C., P. E. Young, C. A. Maloney, S. A. Eaton, M. J. Cowley, M. E. Buckland, et al. 2013. Maternal obesity and diabetes induces latent metabolic defects and widespread epigenetic changes in isogenic mice. Epigenetics 8:602-611
32. McPherson, N. O., T. Fullston, H. W. Bakos, B. P. Setchell, and M. Lane. 2014. Obese father’s metabolic state, adiposity, and reproductive capacity indicate son’s reproductive health. Fertil. Steril. 101:865-873 e861.
33. Mitchell, M., H. W. Bakos, and M. Lane. 2011. Paternal dietinduced obesity impairs embryo development and implantation in the mouse. Fertil. Steril. 95:1349-1353
34. Nasr-Esfahani, M. H., J. R. Aitken, and M. H. Johnson. 1990. Hydrogen peroxide levels in mouse oocytes and early cleavage stage embryos developed in vitro or in vivo. Development 109:501-507
35. Ng, S. F., R. C. Lin, D. R. Laybutt, R. Barres, J. A. Owens, and M. J. Morris. 2010. Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring. Nature 467:963-966
36. Ng, M., T. Fleming, M. Robinson, B. Thomson, N. Graetz, C. Margono, et al. 2014. Global, regional, and national prevalence of overweight and obesity in children and adults during 1980-2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 384:766-781
37. Nguyen, D. M., and H. B. El-Serag. 2010. The epidemiology of obesity. Gastroenterol. Clin. North Am. 39:1-7
38. Noblanc, A., C. Damon-Soubeyrand, B. Karrich, J. Henry-Berger, R. Cadet, F. Saez, et al. 2013. DNA oxidative damage in mammalian spermatozoa: where and why is the male nucleus affected? Free Radic. Biol. Med. 65:719-723
39. Ogus, S., Y. Ke, J. Qiu, B. Wang, and F. F. Chehab. 2003. Hyperleptinemia precipitates diet-induced obesity in transgenic mice overexpressing leptin. Endocrinology 144:2865-2869
40. Ost, A., A. Lempradl, E. Casas, M. Weigert, T. Tiko, M. Deniz, et al. 2014. Paternal diet defines offspring chromatin state and intergenerational obesity. Cell 159:1352-1364
41. Palacios, N., X. Gao, M. L. McCullough, E. J. Jacobs, A. V. Patel, T. Mayo, et al. 2011. Obesity, diabetes, and risk of Parkinson’s disease. Mov. Disord. 26:2253-2259
42. Palmer, N. O., T. Fullston, M. Mitchell, B. P. Setchell, and M. Lane. 2011. SIRT6 in mouse spermatogenesis is modulated by diet-induced obesity. Reprod. Fertil. Dev. 23:929-939
43. Pembrey, M. E., L. O. Bygren, G. Kaati, S. Edvinsson, K. Northstone, M. Sjostrom, et al. 2006. Sex-specific, male-line transgenerational responses in humans. Eur. J. Hum. Genet. 14:159-166
44. Romano, T., J. D. Wark, and M. E. Wlodek. 2014. Physiological skeletal gains and losses in rat mothers during pregnancy and lactation are not observed following uteroplacental insufficiency. Reprod. Fertil. Dev. 26:385-394
45. Sermondade, N., C. Faure, L. Fezeu, R. Levy, S. Czernichow, and Obesity-Fertility Collaborative Group. 2012. Obesity and increased risk for oligozoospermia and azoospermia. Arch. Intern. Med. 172:440-442
46. Setchell, B. P. 1998. The parkes lecture. Heat and the testis. J. Reprod. Fertil. 114:179-194
47. Shafik, A., and S. Olfat. 1981. Lipectomy in the treatment of scrotal lipomatosis. Br. J. Urol. 53:55-61
48. Simeoni, U., I. Ligi, C. Buffat, and F. Boubred. 2011. Adverse consequences of accelerated neonatal growth: cardiovascular and renal issues. Pediatr. Nephrol. 26:493-508
49. Suh, M., K. J. Merrells, A. Dick, and C. G. Taylor. 2011. Testes of obese rats are highly responsive to n-3 long-chain fatty acids. Br. J. Nutr. 106:1005-1012
50. Tunc, O., H. W. Bakos, and K. Tremellen. 2011. Impact of body mass index on seminal oxidative stress. Andrologia 43:121-128
51. Veenendaal, M. V., R. C. Painter, S. R. de Rooij, P. M. Bossuyt, J. A. van der Post, P. D. Gluckman, et al. 2013. Transgenerational effects of prenatal exposure to the 1944-45 Dutch famine. BJOG 120:548-553
52. Wahlqvist, M. L., L. Y. Huang, M. S. Lee, P. H. Chiang, Y. H. Chang, and A. P. Tsao. 2014. Dietary quality of elders and children is interdependent in Taiwanese communities: a NAHSIT mapping study. Ecol. Food Nutr. 53:81-97
53. Watkins, A. J., and K. D. Sinclair. 2014. Paternal low protein diet affects adult offspring cardiovascular and metabolic function in mice. Am. J. Physiol. Heart Circ. Physiol. 306: H1444-H1452
54. Weitzman, S. A., P. W. Turk, D. H. Milkowski, and K. Kozlowski. 1994. Free radical adducts induce alterations in DNA cytosine methylation. Proc. Natl. Acad. Sci. USA 91:1261-1264
55. Whitaker, K. L., M. J. Jarvis, R. J. Beeken, D. Boniface, and J. Wardle. 2010. Comparing maternal and paternal intergenerational transmission of obesity risk in a large population-based sample. Am. J. Clin. Nutr. 91:1560-1567
56. WHO and World Health Organisation. 2010. WHO laboratory manual for the examination and processing of human semen. Cambridge University Press, Cambridge.
57. Youngson, N. A., and E. Whitelaw. 2011. The effects of acquired paternal obesity on the next generation. Asian J. Androl. 13:195-196