Paternal obesity, interventions, and mechanistic pathways to impaired health in offspring

Annals of Nutrition and Metabolism

Volumn 64, Issue 3-4, 2014, Pages 231-238

  McPherson, Nicole O ^a   Fullston, Tod ^a   Aitken, R John ^b   Lane, Michelle ^a,c  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b UNIVERSITY OF NEWCASTLE   (Australia)

^c Repromed   (Australia)

Author keywords

DNA damage; Embryos; Epigenetics; Fertility; Infertility; Male obesity; Mutation; Sperm

Indexed keywords

ESTROGEN; FOLLITROPIN; GLUCOSE; INHIBIN B; INSULIN; LUTEINIZING HORMONE; MICRORNA; REACTIVE OXYGEN METABOLITE; SEX HORMONE; SEX HORMONE BINDING GLOBULIN; TESTOSTERONE; UNTRANSLATED RNA;

ACETYLATION; ARTICLE; CELL FUNCTION; DNA DAMAGE; DNA METHYLATION; DNA REPAIR; DNA REPLICATION; DNA STRAND BREAKAGE; EMBRYO DEVELOPMENT; EMBRYO TRANSFER; ENVIRONMENTAL FACTOR; EPIGENETICS; FERTILIZATION IN VITRO; GLUCOSE HOMEOSTASIS; GLUCOSE TOLERANCE; HOX GENE; HUMAN; INHERITANCE; INSULIN SENSITIVITY; MALE; MALE FERTILITY; META ANALYSIS (TOPIC); METHYLATION; OBESITY; OXIDATIVE STRESS; PANCREAS ISLET CELL; PATERNAL OBESITY; PHENOTYPE; PRIORITY JOURNAL; PROGENY; PROMOTER REGION; REPRODUCTIVE HEALTH; RODENT MODEL; SPERM QUALITY; SPERMATOGENESIS; SPERMATOZOON; SPERMATOZOON COUNT; SPERMATOZOON MOTILITY; ADVERSE EFFECTS; ANIMAL; CHILD; CHILD NUTRITION; DIET; FAMILY HEALTH; FATHER; FEMALE; FETUS DEVELOPMENT; GENETIC EPIGENESIS; HEALTH CARE POLICY; HEALTH PROMOTION; LIFESTYLE; MOTOR ACTIVITY; PATERNAL BEHAVIOR; PATHOLOGY; PATIENT COMPLIANCE; PREGNANCY;

ANIMALIA; RODENTIA;

ANIMALS; CHILD; CHILD NUTRITIONAL PHYSIOLOGICAL PHENOMENA; DIET; DNA DAMAGE; EPIGENESIS, GENETIC; FAMILY HEALTH; FATHERS; FEMALE; FETAL DEVELOPMENT; HEALTH PROMOTION; HUMANS; LIFE STYLE; MALE; MOTOR ACTIVITY; NUTRITION POLICY; OBESITY; PATERNAL BEHAVIOR; PATIENT COMPLIANCE; PREGNANCY; SPERMATOZOA;

EID: 84908594457     PISSN: 02506807     EISSN: 14219697     Source Type: Journal    
DOI: 10.1159/000365026     Document Type: Article

References (30)

1. Sermondade N, Faure C, Fezeu L, Shayeb AG, Bonde JP, Jensen TK, Van Wely M, Cao J, Martini AC, Eskandar M, Chavarro JE, Koloszar S, Tw igt JM, Ramlau-Hansen CH, Borges E Jr, Lotti F, Steegers-Theunissen RP, Zorn B, Polotsky AJ, La Vignera S, Eskenazi B, Tremellen K, Magnusdottir EV, Fejes I, Hercberg S, Levy R, Czernichow S: BM I in relation to sperm count: an updated systematic review and collaborative meta-analysis. Hum Reprod Update 2013; 19: 221-231.
2. Fariello RM, Pariz JR, Spaine DM, Cedenho AP, Bertolla RP, Fr aietta R: Association between obesity and alteration of sperm DNA integrity and mitochondrial activity. BJU Int 2012; 110: 863-867.
3. Ribas-Maynou J, Garcia-Peiro A, Fernandez-Encinas A, Amengua l MJ, Prada E, Cortes P, Navarro J, Benet J: Double stranded sperm DNA breaks, measured by comet assay, are associated with unexplained recurrent miscarriage in couples without a female factor. PLoS One 2012; 7:e 44679.
4. Palmer NO, Bakos HW, Fullston T, Lane M: Impact of obesity on male fertility, sperm function and molecular composition. Spermatogenesis 2012; 2: 253-263.
5. Danielz ik S, Langnase K, Mast M, Spethmann C, Muller MJ: Impact of parental BMI on the manifestation of overweight 5-7 year old children. Eur J Nutr 2002; 41: 132-138.
6. Ng SF, Lin RC, Laybutt DR, Barres R, Owens JA, Morris MJ: Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring. Nature 2010; 467: 963-966.
7. Watkins AJ, Sinclair KD: Paternal low protein diet affects adult offspring cardiovascular and metabolic function in mice. Am J Physiol Heart Circ Physiol 2014; 306:H1444-H1452.
8. Binder NK, Hannan NJ, Gardn er DK: Paternal diet-induced obesity retards early mouse embryo development, mitochondrial activity and pregnancy health. PLoS One 2012; 7:e52304.
9. McPherson NOB, H. W., Setchell BP, Owens JA, Lane M: Improving metabolic health in obese male mice via diet and exercise restores embryo development and fetal growth. PLoS One 2013; 8:e71459.
10. Fullston T, Teague EM, Palmer NO, de Blasio MJ, Mitchell M, Print CG, Owens JA, Lane M: Paternal obesity initiates metabolic disturbances in two generations of mice and alters the transcription profile of tesis and sperm microRNA content. FASEB J 2013; 27: 4226-4243.
11. Ng SF,Lin RC,Maloney C.A.,Youngson NA,Owens JA,Morris MJ, Paternal high-fat diet consumption induces common changes in the transcriptomes of retroperitoneal adipose and pancreatic islet tissu es in female rat offspring. FASEB J, 2014, 28, 1830-1841.
12. Fullston T, Palmer NO, Owens JA, Mitchell M, Bakos HW, Lane M: Diet-induced paternal obesity in the absence of diabetes di minishes the reproductive health of two subsequent generations of mice. Hum Reprod 2012; 27: 1391-1400.
13. Reis LO, Zani EL, Saad RD, Chaim EA, de Oliveira LC, Fregonesi A: Bariatric sur gery does not interfere with sperm quality-A preliminary long-term study. Reprod Sci 2012; 19: 1057-1062.
14. Stephens SM, Polotsky AJ: Big enough for an aromatase inhibitor? How adiposity affects male fertility. Semin Reprod Med 2013; 31: 251-257.
15. Ibrahim HA, Zhu Y, Wu C, Lu C, Ezekwe MO, Liao SF, Haung K: Selenium-enriched probiotics improves murine male fertility compromised b y high fat diet. Biol Trace Elem Res 2012; 147: 251-260.
16. Chen XL, Gong LZ, Xu JX: Antioxidative activity and protective effect of probiotics against high-fat diet-induced sperm damage in rats. Animal 2013; 7: 287-292.
17. Saez Lancellotti TE, Boarelli PV, Romero AA, Funes AK, Cid-Barria M, Cabrillana ME, Monclus MA, Simon L, Vicenti AE, Fornes MW: Semen quality and sperm function loss by hypercholesterolemic diet was recovered by addition of olive oil to diet in rabbit. PLoS One 2013; 8:e52386.
18. Hakonsen LB, Thulstrup AM, Aggerholm AS, Olsen J, Bonde JP, Andersen CY, Bungum M, Ernst EH, Hansen ML, Ramlau-Hansen CH: Does weight loss improve semen quality and reproductive hormones? Results from a cohort of severely obese men. Reprod Health 2011; 8: 24.
19. 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.
20. 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 .
21. Hammoud SS, Nix DA, Hammoud AO, Gibson M, Cairns BR, Carrell DT: Genome-wide analysis identifies changes in histone retention and epigenetic modifications at developmental and imprinted gene loci in the sperm of infertile men. Hum Reprod 2011; 26: 2558-2569.
22. Noblanc A, Damon-Soubeyrand C, Karrich B, Henry-Berger J, Cadet R, Saez F, Guiton R, Janny L, Pons-Rejraji H, Alvare z JG, Drevet JR, Kocer A: DNA oxidative damage in mammalian spermatozoa: where and why is the male nucleus affected? Free Radic Biol Med 2013; 65: 719-723.
23. Aitken RJ, Koopman P, Lewis SE: Seeds of concern. Nature 2004; 432: 48-52.
24. Palmer NO, Fullston T, Mitchell M, Setchell BP, Lane M: SIRT6 in mouse spermatogenesis is modulated by diet-induced obesity. Reprod Fertil Dev 2011; 23: 929-939.
25. Doyle K, Fitzpatrick FA: Redox signaling, alkylation (carbonylation) of conserved cysteines inactivates class I histone deacetylases 1, 2, and 3 and antagonizes their transcriptiona l repressor function. J Biol Chem 2010; 285: 17417-17424.
26. Gannon JR, Emery BR, Jenkins TG, Carrell DT: The sperm epigenome: implications for the embryo. Adv Exp Med Biol 2014; 791: 53-66.
27. Pathak S, Kedia-Mokashi N, Saxena M, D'Souza R, Maitra A, Parte P, Gill-Sharma M, Balasinor N: 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 2009; 91: 2253-2263.
28. Tunc O, Tremellen K: Oxidative DNA damage impairs global sperm DNA methylation in infertile men. J Assist Reprod Genet 2009; 26: 537-544.
29. Ostermeier GC, Miller D, Huntriss JD, Diamond MP, Krawetz SA: Reproductive biology: delivering spermatozoan RNA to the oocyte. Nature 2004; 429: 154.
30. Gapp K, Jawaid A, Sarkies P, Bohacek J, Pelczar P, Prados J, Farinelli L, Miska E, Mansuy IM: Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice. Nat Neurosci 2014; 17: 667-669.