Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-20T17:32:12.937Z Has data issue: false hasContentIssue false
  • English
  • Français

Maternal protein restriction in pregnancy and/or lactation affects seminiferous tubule organization in male rat offspring

Published online by Cambridge University Press:  08 June 2012

G. L. Rodríguez-González ,
R. M. Vigueras-Villaseñor ,
S. Millán ,
N. Moran ,
R. Trejo ,
P. W. Nathanielsz ,
F. Larrea  and
E. Zambrano
G. L. Rodríguez-González
Affiliation:
Department of Reproductive Biology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico
R. M. Vigueras-Villaseñor
Affiliation:
Department of Experimental Medicine, Instituto Nacional de Pediatría, Mexico City, Mexico
S. Millán
Affiliation:
Department of Reproductive Biology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico
N. Moran
Affiliation:
Department of Reproductive Biology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico
R. Trejo
Affiliation:
Research Coordination, Instituto Mexicano del Seguro Social, Mexico City, Mexico
P. W. Nathanielsz
Affiliation:
Department of Obstetrics, Center for Pregnancy and Newborn Research, University of Texas Health Science Center, San Antonio, TX, USA
F. Larrea
Affiliation:
Department of Reproductive Biology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico
E. Zambrano*
Affiliation:
Department of Reproductive Biology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico
*
*Address for correspondence: E. Zambrano, Department of Reproductive Biology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Vasco de Quiroga 15, Sección XVI, Tlalpan 14000, México, DF México. (Email [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Maternal protein restriction (MPR) during pregnancy impaired the reproduction of male offspring. We investigated, during the first wave of spermatogenesis, whether MPR exerts deleterious effects on germ cell proliferation and differentiation, as well as androgen receptor (AR) protein expression, which was used as a marker for Sertoli cell (SC) maturation. At the beginning of pregnancy (day 0), dams were fed a control diet (C: 20% casein) or a restricted isocaloric diet (R: 10% casein). After birth, four groups were established: CC, RR, CR and RC (first letter diet during pregnancy and second during lactation). Male offspring were studied at postnatal days 14, 21 and 36. At birth, pup body weight was unchanged. Body weight and testis weight were reduced in RR and CR groups at all ages evaluated. MPR delayed the germinal epithelium development at all ages evaluated. On performing Western blot and immunohistochemistry, AR expression was found to be lower in the three restricted groups. The results suggest that MPR during pregnancy and/or lactation delays SC maturation and germ cell differentiation, and affects intratubular organization. These changes might be responsible for the lower fertility rate at older ages.

Keywords

androgen receptorfertilityprotein restrictionSertoli cellspermatogenesis
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 3 , Issue 5 , October 2012 , pp. 321 - 326
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1. Ashton, N. Perinatal development and adult blood pressure. Braz J Med Biol Res. 2000; 33, 731–740.CrossRefGoogle ScholarPubMed
2. Edwards, LJ, Coulter, CL, Symonds, ME, McMillen, IC. Prenatal undernutrition, glucocorticoids and the programming of adult hypertension. Clin Exp Pharmacol Physiol. 2001; 28, 938–941.CrossRefGoogle ScholarPubMed
3. Langley-Evans, SC, Gardner, DS, Welham, SJ. Intrauterine programming of cardiovascular disease by maternal nutritional status. Nutrition. 1998; 14, 39–47.CrossRefGoogle ScholarPubMed
4. 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.CrossRefGoogle ScholarPubMed
5. Rhind, SM, Rae, MT, Brooks, AN. Effects of nutrition and environmental factors on the fetal programming of the reproductive axis. Reproduction. 2001; 122, 205–214.CrossRefGoogle ScholarPubMed
6. Zambrano, E, Rodriguez-Gonzalez, GL, Guzman, C, et al. . A maternal low protein diet during pregnancy and lactation in the rat impairs male reproductive development. J Physiol. 2005; 563, 275–284.CrossRefGoogle ScholarPubMed
7. Rae, MT, Palassio, S, Kyle, CE, et al. . Effect of maternal undernutrition during pregnancy on early ovarian development and subsequent follicular development in sheep fetuses. Reproduction. 2001; 122, 915–922.CrossRefGoogle ScholarPubMed
8. Guzman, C, Cabrera, R, Cardenas, M, et al. . Protein restriction during fetal and neonatal development in the rat alters reproductive function and accelerates reproductive ageing in female progeny. J Physiol. 2006; 572, 97–108.CrossRefGoogle ScholarPubMed
9. 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.CrossRefGoogle ScholarPubMed
10. Genovese P, Nunez ME, Pombo C, Bielli A. Undernutrition during foetal and post-natal life affects testicular structure and reduces the number of Sertoli cells in the adult rat. Reprod Domest Anim 2010; 45, 233–236.CrossRefGoogle Scholar
11. Olaso, R, Habert, R. Genetic and cellular analysis of male germ cell development. J Androl. 2000; 21, 497–511.CrossRefGoogle ScholarPubMed
12. Toledo FC, Perobelli JE, Pedrosa FP, Anselmo-Franci JA, Kempinas WD. In utero protein restriction causes growth delay and alters sperm parameters in adult male rats. Reprod Biol Endocrinol. 2011; 9, 94.Google Scholar
13. Zambrano, E, Bautista, CJ, Deas, M, et al. . A low maternal protein diet during pregnancy and lactation has sex- and window of exposure-specific effects on offspring growth and food intake, glucose metabolism and serum leptin in the rat. J Physiol. 2006; 571, 221–230.CrossRefGoogle ScholarPubMed
14. Vigueras-Villasenor, RM, Moreno-Mendoza, NA, Reyes-Torres, G, et al. . The effect of estrogen on testicular gonocyte maturation. Reprod Toxicol. 2006; 22, 513–520.CrossRefGoogle ScholarPubMed
15. Yang, ZW, Wreford, NG, de Kretser, DM. A quantitative study of spermatogenesis in the developing rat testis. Biol Reprod. 1990; 43, 629–635.Google ScholarPubMed
16. Zambrano, E, Martinez-Samayoa, PM, Bautista, CJ, et al. . Sex differences in transgenerational alterations of growth and metabolism in progeny (F2) of female offspring (F1) of rats fed a low protein diet during pregnancy and lactation. J Physiol. 2005; 566, 225–236.CrossRefGoogle ScholarPubMed
17. Teixeira, CV, Silandre, D, de Souza Santos, AM, et al. . Effects of maternal undernutrition during lactation on aromatase, estrogen, and androgen receptors expression in rat testis at weaning. J Endocrinol. 2007; 192, 301–311.CrossRefGoogle ScholarPubMed
18. 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 ScholarPubMed
19. Clermont, Y, Perey, B. Quantitative study of the cell population of the seminiferous tubules in immature rats. Am J Anat. 1957; 100, 241–267.CrossRefGoogle ScholarPubMed
20. Lau, C, Rogers, JM. Embryonic and fetal programming of physiological disorders in adulthood. Birth Defects Res C Embryo Today. 2004; 72, 300–312.CrossRefGoogle ScholarPubMed
21. 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.CrossRefGoogle ScholarPubMed
22. Griswold, MD. The central role of Sertoli cells in spermatogenesis. Semin Cell Dev Biol. 1998; 9, 411–416.CrossRefGoogle ScholarPubMed
23. Bensoussan, K, Morales, CR, Hermo, L. Vitamin E deficiency causes incomplete spermatogenesis and affects the structural differentiation of epithelial cells of the epididymis in the rat. J Androl. 1998; 19, 266–288.CrossRefGoogle ScholarPubMed
24. Watanabe, T, Ebara, S, Kimura, S, et al. . Maternal vitamin B12 deficiency affects spermatogenesis at the embryonic and immature stages in rats. Congenit Anom (Kyoto). 2007; 47, 9–15.CrossRefGoogle ScholarPubMed
25. Aitken, RJ, De Iuliis, GN, Finnie, JM, Hedges, A, McLachlan, RI. Analysis of the relationships between oxidative stress, DNA damage and sperm vitality in a patient population: development of diagnostic criteria. Hum Reprod. 2010; 25, 2415–2426.CrossRefGoogle Scholar