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Impact of maternal hyperlipidic hypercholesterolaemic diet on male reproductive organs and testosterone concentration in rabbits

Published online by Cambridge University Press:  03 March 2014

C. Dupont ,
D. Ralliard-Rousseau ,
A. Tarrade ,
C. Faure ,
M. Dahirel ,
B. Sion ,
F. Brugnon ,
R. Levy  and
P. Chavatte-Palmer Open the ORCID record for P. Chavatte-Palmer [Opens in a new window]
C. Dupont
Affiliation:
INRA, UMR1198 Biologie du Développement et Reproduction, Jouy-en-Josas, France ENVA, Maisons Alfort, France APHP, Hosp Jean-Verdier, Bondy, France Université Paris 13, Sorbonne Paris Cité, Unité de Recherche en Epidémiologie Nutritionnelle (UREN), Bobigny, France
D. Ralliard-Rousseau
Affiliation:
INRA, UMR1198 Biologie du Développement et Reproduction, Jouy-en-Josas, France ENVA, Maisons Alfort, France
A. Tarrade
Affiliation:
INRA, UMR1198 Biologie du Développement et Reproduction, Jouy-en-Josas, France ENVA, Maisons Alfort, France PremUp, 4 av. de l’Observatoire, Paris, France
C. Faure
Affiliation:
APHP, Hosp Jean-Verdier, Bondy, France Université Paris 13, Sorbonne Paris Cité, Unité de Recherche en Epidémiologie Nutritionnelle (UREN), Bobigny, France
M. Dahirel
Affiliation:
INRA, UMR1198 Biologie du Développement et Reproduction, Jouy-en-Josas, France ENVA, Maisons Alfort, France PremUp, 4 av. de l’Observatoire, Paris, France
B. Sion
Affiliation:
Clermont Université, Université d’Auvergne, Pharmacologie Fondamentale et Clinique de la Douleur, Clermont-Ferrand, France INSERM, NEURO-DOL, Clermont-Ferrand, France
F. Brugnon
Affiliation:
CHU Clermont Ferrand, CHU Estaing, Assistance Médicale à la Procréation, CECOS, Place Aubrac, Clermont Ferrand, France Université d’Auvergne, Génétique Reproduction et Développement, Place Henri Dunant, Clermont FerrandFrance
R. Levy
Affiliation:
APHP, Hosp Jean-Verdier, Bondy, France Université Paris 13, Sorbonne Paris Cité, Unité de Recherche en Epidémiologie Nutritionnelle (UREN), Bobigny, France
P. Chavatte-Palmer*
Affiliation:
INRA, UMR1198 Biologie du Développement et Reproduction, Jouy-en-Josas, France ENVA, Maisons Alfort, France PremUp, 4 av. de l’Observatoire, Paris, France
*
*Address for correspondence: P. Chavatte-Palmer, UMR1198 Biologie du Développement et Reproduction, F-78350 Jouy-en Josas, France. (Email [email protected])
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Abstract

The concept of Developmental Origins of Health and Disease initially stemmed from the developmental programming of metabolic diseases. Reproductive functions and fertility in adulthood may also be programmed during foetal development. We studied the impact of dietary-induced maternal hyperlipidaemia and hypercholesterolaemia (HH), administered at 10 weeks of age and throughout the gestation and lactation, on male reproductive functions of rabbit offspring. Male rabbits born to HH dams and fed a control diet had significantly lighter testes and epididymes compared with rabbits born to control dams at adulthood. No significant changes in sperm concentration, sperm DNA integrity and sperm membrane composition were observed, but serum-free testosterone concentrations were decreased in HH males. This study confirms the importance of maternal metabolic status for the development of male reproductive organs.

Keywords

DOHADfoetal programmingmale reproductive functionmaternal dietmaternal hyperlipidaemia and hypercholesterolaemiarabbit
Type
Brief Report
Information
Journal of Developmental Origins of Health and Disease , Volume 5 , Issue 3 , June 2014 , pp. 183 - 188
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2014 

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References

1. Hanson, MA, Gluckman, PD. Developmental origins of health and disease: new insights. Basic Clin Pharmacol Toxicol. 2008; 102, 90–93.CrossRefGoogle ScholarPubMed
2. Dupont, C, Cordier, AG, Junien, C, et al. Maternal environment and the reproductive function of the offspring. Theriogenology. 2012; 78, 1405–1414.Google Scholar
3. Gluckman, PD, Hanson, MA. Living with the past: evolution, development, and patterns of disease. Science. 2004; 305, 1733–1736.Google Scholar
4. Francois, I, de Zegher, F, Spiessens, C, D’Hooghe, T, Vanderschueren, D. Low birth weight and subsequent male subfertility. Pediatr Res. 1997; 42, 899–901.Google Scholar
5. Vanbillemont, G, Lapauw, B, Bogaert, V, et al. Birth weight in relation to sex steroid status and body composition in young healthy male siblings. J Clin Endocrinol Metab. 2010; 95, 1587–1594.Google Scholar
6. Alejandro, B, Perez, R, Pedrana, G, et al. Low maternal nutrition during pregnancy reduces the number of sertoli cells in the newborn lamb. Reprod Fertil Dev. 2002; 14, 333–337.Google Scholar
7. Kotsampasi, B, Balaskas, C, Papadomichelakis, G, Chadio, SE. Reduced sertoli cell number and altered pituitary responsiveness in male lambs undernourished in utero. Anim Reprod Sci. 2009; 114, 135–147.Google Scholar
8. Rae, MT, Kyle, CE, Miller, DW, et al. The effects of undernutrition, in utero, on reproductive function in adult male and female sheep. Anim Reprod Sci. 2002; 72, 63–71.Google Scholar
9. Da Silva, P, Aitken, RP, Rhind, SM, Racey, PA, Wallace, JM. Influence of placentally mediated fetal growth restriction on the onset of puberty in male and female lambs. Reproduction. 2001; 122, 375–383.Google Scholar
10. Christante, CM, Taboga, SR, Pinto-Fochi, ME, Goes, RM. Maternal obesity disturbs the postnatal development of gonocytes in the rat without impairment of testis structure at prepubertal age. Reproduction. 2013; 146, 549–558.Google Scholar
11. Fischer, B, Chavatte-Palmer, P, Viebahn, C, Navarrete Santos, A, Duranthon, V. Rabbit as a reproductive model for human health. Reproduction. 2012; 144, 1–10.Google Scholar
12. Cordier, AG, Leveille, P, Dupont, C, et al. Dietary lipid and cholesterol induce ovarian dysfunction and abnormal LH response to stimulation in rabbits. PLoS One. 2013; 8, e63101.CrossRefGoogle ScholarPubMed
13. Picone, O, Laigre, P, Fortun-Lamothe, L, et al. Hyperlipidic hypercholesterolemic diet in prepubertal rabbits affects gene expression in the embryo, restricts fetal growth and increases offspring susceptibility to obesity. Theriogenology. 2011; 75, 287–299.Google Scholar
14. Montoudis, A, Simoneau, L, Lafond, J. Influence of a maternal cholesterol-enriched diet on [1-14C]-linoleic acid and L-[4, 5-3H]-leucine entry in plasma of rabbit offspring. Life Sci. 2004; 74, 1751–1762.Google Scholar
15. Palinski, W, D’Armiento, FP, Witztum, JL, et al. Maternal hypercholesterolemia and treatment during pregnancy influence the long-term progression of atherosclerosis in offspring of rabbits. Circ Res. 2001; 89, 991–996.CrossRefGoogle ScholarPubMed
16. Marseille-Tremblay, C, Gravel, A, Lafond, J, Mounier, C. Effect of an enriched cholesterol diet during gestation on fatty acid synthase, HMG-CoA reductase and SREBP-1/2 expressions in rabbits. Life Sci. 2007; 81, 772–778.CrossRefGoogle ScholarPubMed
17. Gondos, B, Conner, LA. Ultrastructure of developing germ cells in the fetal rabbit testis. Am J Anat. 1973; 136, 23–42.Google Scholar
18. Jost, A, Perlman, S, Magre, S. The initial stages of testicular differentiation in the rabbit fetus. Arch Anat Microsc Morphol Exp. 1985; 74, 69–75.Google Scholar
19. Fortun-Lamothe, L, Lamboley-Gaüzère, B, Bannelier, C. Prediction of body composition in rabbit females using total body electrical conductivity (TOBEC). Livest Prod Sci. 2002; 78, 133–142.CrossRefGoogle Scholar
20. Kumar, N, Sood, S, Arora, B, Singh, M, Beena, . Effect of duration of fluoride exposure on the reproductive system in male rabbits. J Hum Reprod Sci. 2010; 3, 148–152.Google Scholar
21. Grizard, G, Sion, B, Bauchart, D, Boucher, D. Separation and quantification of cholesterol and major phospholipid classes in human semen by high-performance liquid chromatography and light-scattering detection. J Chromatogr B Biomed Sci Appl. 2000; 740, 101–107.Google Scholar
22. Dupont, C, Faure, C, Sermondade, N, et al. Obesity leads to higher risk of sperm DNA damage in infertile patients. Asian J Androl. 2013; 15, 622–625.Google Scholar
23. Hue-Beauvais, C, Chavatte-Palmer, P, Aujean, E, et al. An obesogenic diet started before puberty leads to abnormal mammary gland development during pregnancy in the rabbit. Dev Dyn. 2011; 240, 347–356.Google Scholar
24. Sun, B, Purcell, RH, Terrillion, CE, et al. Maternal high-fat diet during gestation or suckling differentially affects offspring leptin sensitivity and obesity. Diabetes. 2012; 61, 2833–2841.Google Scholar
25. Sharpe, RM, McKinnell, C, Kivlin, C, Fisher, JS. Proliferation and functional maturation of sertoli cells, and their relevance to disorders of testis function in adulthood. Reproduction. 2003; 125, 769–784.Google Scholar
26. Chavarro, JE, Toth, TL, Wright, DL, Meeker, JD, Hauser, R. Body mass index in relation to semen quality, sperm DNA integrity, and serum reproductive hormone levels among men attending an infertility clinic. Fertil Steril. 2010; 93, 2222–2231.Google Scholar
27. Furukawa, S, Fujita, T, Shimabukuro, M, et al. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest. 2004; 114, 1752–1761.Google Scholar
28. 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.Google Scholar
29. Sakkas, D, Alvarez, JG. Sperm DNA fragmentation: mechanisms of origin, impact on reproductive outcome, and analysis. Fertil Steril. 2010; 93, 1027–1036.Google Scholar
30. Fullston, T, Ohlsson Teague, EM, Palmer, NO, et al. 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; 10, 4226–4243.Google Scholar
31. Jenkins, TG, Carrell, DT. The paternal epigenome and embryogenesis: poising mechanisms for development. Asian J Androl. 2011; 13, 76–80.Google Scholar