Spermatogenesis recovery in protein-restricted rats subjected to a normal protein diet after weaning
Michelle C. Melo A , Fernanda R. C. L. Almeida A , André L. Caldeira-Brant A , Gleydes G. Parreira A and Hélio Chiarini-Garcia A B
+ Author Affiliations
- Author Affiliations
A Laboratory of Structural Biology and Reproduction, Federal University of Minas Gerais, Belo Horizonte, MG 31270-901, Brazil.
B Corresponding author. Email: chiarini@icb.ufmg.br
Reproduction, Fertility and Development 26(6) 787-796 https://doi.org/10.1071/RD13032
Submitted: 2 February 2013 Accepted: 13 May 2013 Published: 7 June 2013
Abstract
This study investigated the pre- and postnatal effects of protein restriction (8% vs 20% crude protein) on different parameters of spermatogenesis in adult rat offspring. Body and testis weights as well as the seminiferous tubular diameter were reduced in those animals that received the protein-restricted diet after weaning, although these parameters recovered when a 20% protein diet was offered subsequently. The numbers of spermatogonia, spermatocytes, spermatids and Leydig cells were reduced in undernourished animals, whilst the Sertoli cell number did not change. Prenatal programming effect was observed only in the spermatogonial or proliferative phase of spermatogenesis. However, the intake of the normal protein diet after weaning brought many of the testicular parameters evaluated back to normal in 70-day-old rats. A significant reduction of the meiotic index, Sertoli cell supporting capacity and spermatogenic efficiency was observed in animals subjected to protein undernutrition throughout their lives. The data presented show that protein restriction impairs the normal development of the testis in different ways, depending on the period during which the restriction was imposed, and the negative effects on spermatogenesis are more severe when undernutrition occurs from conception to adulthood; however, the return to a normal protein diet after weaning recovers the spermatogenic process.
Additional keywords: prenatal programming, protein malnutrition, spermatogonia, testis.
References
Abercrombie, M. (1946). Estimation of nuclear populations from microtome sections. Anat. Rec. 94, 230–247.| Estimation of nuclear populations from microtome sections.Crossref | GoogleScholarGoogle Scholar |
Amann, R. P., and Alquimist, J. O. (1962). Reproductive capacity of dairy bulls. VIII. Direct and indirect measurement of testicular sperm production. J. Dairy Sci. 45, 774–781.
| Reproductive capacity of dairy bulls. VIII. Direct and indirect measurement of testicular sperm production.Crossref | GoogleScholarGoogle Scholar |
Caron, E., Ciofi, P., Prevot, V., and Bouret, S. G. (2012). Alteration in neonatal nutrition causes perturbations in hypothalamic neural circuits controlling reproductive function. J. Neurosci. 32, 11 486–11 494.
| Alteration in neonatal nutrition causes perturbations in hypothalamic neural circuits controlling reproductive function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1Ors7rP&md5=c4eb945040c6e69eb7b08af9458c2355CAS |
Chiarini-Garcia, H., and Meistrich, M. L. (2008). High-resolution light microscopic characterization of spermatogonia. Methods Mol. Biol. 450, 95–107.
| High-resolution light microscopic characterization of spermatogonia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXkslOht7s%3D&md5=b6cd0272dc075c750dd16f998ecd8f7dCAS | 18370053PubMed |
Chiarini-Garcia, H., Parreira, G. G., and Almeida, F. R. C. L. (2011). Glycol methacrylate embedding for improved morphological, morphometrical and immunohistochemical investigation under light microscopy: testes as a model. Methods Mol. Biol. 689, 3–18.
| Glycol methacrylate embedding for improved morphological, morphometrical and immunohistochemical investigation under light microscopy: testes as a model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhslOlsro%3D&md5=c1f7ea7091df39e1f9c229acd3792a1eCAS | 21153783PubMed |
de Rooij, D. G., and Russell, L. D. (2000). All you wanted to know about spermatogonia but were afraid to ask. J. Androl. 21, 776–798.
| 1:STN:280:DC%2BD3MzgtlyrtA%3D%3D&md5=45d205b5480aac7d6fd0a6d91aa67565CAS | 11105904PubMed |
Desai, M., Crowther, N. J., Lucas, A., and Hales, C. N. (1996). Organ-selective growth in the offspring of protein-restricted mothers. Br. J. Nutr. 76, 591–603.
| Organ-selective growth in the offspring of protein-restricted mothers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xnt1Kiur0%3D&md5=1bf09a9c86620b3aa54845e85d49632aCAS | 8942365PubMed |
Drumond, A. L., Meistrich, M. L., and Chiarini-Garcia, H. (2011). Spermatogonial morphology and kinetics during testis development in mice: a high-resolution light microscopy approach. Reproduction 142, 145–155.
| Spermatogonial morphology and kinetics during testis development in mice: a high-resolution light microscopy approach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFSqu7zL&md5=eee01a35d086699f10ebaa2797f1f0c1CAS | 21521798PubMed |
França, L. R., and Russell, L. D. (1998). The testis of domestic mammals. In ‘Male Reproduction: a Multidisciplinary Overview’. (Eds F. Martinez-Garcia and J. Regadera.) pp. 198–219. (Churchill Communications: Madrid.)
Gardner, D. S., Lea, R. G., and Sinclair, K. D. (2008). Developmental programming of reproduction and fertility: what is the evidence? Animal 2, 1128–1134.
| Developmental programming of reproduction and fertility: what is the evidence?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38vptFSisQ%3D%3D&md5=d35f15b8eb98d0c10353af615d21e004CAS | 22443724PubMed |
Genovese, P., Núñez, M. E., Pombo, C., and Bielli, A. (2010). Undernutrition during foetal and post-natal life affects testicular structure and reduces the number of Sertoli cells in the adult rat. Reprod. Domest. Anim. 45, 233–236.
| Undernutrition during foetal and post-natal life affects testicular structure and reduces the number of Sertoli cells in the adult rat.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cjgs1OktQ%3D%3D&md5=8cff053ce9f0e9c7ba662bbd523c7f59CAS | 19281598PubMed |
Griswold, M. D. (1995). Interactions between germ cells and Sertoli cells in the testis. Biol. Reprod. 52, 211–216.
| Interactions between germ cells and Sertoli cells in the testis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjt12lur0%3D&md5=bee3ec57def9519a70900844025733fbCAS | 7711190PubMed |
Gunn, R. G., Sim, D. A., and Hunter, E. A. (1995). Effects of nutrition in utero and in early life on the subsequent lifetime reproductive performance of Scottish Blackface ewes in two management systems. Anim. Sci. 60, 223–230.
| Effects of nutrition in utero and in early life on the subsequent lifetime reproductive performance of Scottish Blackface ewes in two management systems.Crossref | GoogleScholarGoogle Scholar |
Herbert, D. C. (1980). Growth patterns and hormonal profile of male rats with protein–calorie malnutrition. Anat. Rec. 197, 339–354.
| Growth patterns and hormonal profile of male rats with protein–calorie malnutrition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXltlWis7o%3D&md5=66fd97f258732595840a24c19ddb80acCAS | 6776847PubMed |
Hess, R. A., Cooke, P. S., Bunick, D., and Kirby, J. D. (1993). Adult testicular enlargement induced by neonatal hypothyroidism is accompanied by increased Sertoli and germ cell numbers. Endocrinology 132, 2607–2613.
| Adult testicular enlargement induced by neonatal hypothyroidism is accompanied by increased Sertoli and germ cell numbers.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3s3nvFanuw%3D%3D&md5=dcced8d761d44e7633a89a369283f53dCAS | 8504761PubMed |
Huckins, C. (1978). The morphology and kinetics of spermatogonial degeneration in normal adult rats: an analysis using a simplified classification of the germinal epithelium. Anat. Rec. 190, 905–926.
| The morphology and kinetics of spermatogonial degeneration in normal adult rats: an analysis using a simplified classification of the germinal epithelium.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE1c7kt1Ogtw%3D%3D&md5=b16a947ae56a2d49b9bd52a4674057b7CAS | 637327PubMed |
I’Anson, H., Foster, D. L., Foxcroft, G. R., and Booth, P. J. (1991). Nutrition and reproduction. Oxf. Rev. Reprod. Biol. 13, 239–311.
| 1:STN:280:DyaK3szgvFyqsw%3D%3D&md5=6759615d9b55eb6550b05e33f33d80e5CAS | 1845336PubMed |
Ibáñez, L., Potau, N., Ferrer, A., Rodriguez-Hierro, F., Marcos, M. V., and de Zegher, F. (2002). Reduced ovulation rate in adolescent girls born small for gestational age. J. Clin. Endocrinol. Metab. 87, 3391–3393.
| Reduced ovulation rate in adolescent girls born small for gestational age.Crossref | GoogleScholarGoogle Scholar | 12107255PubMed |
Jean-Faucher, C., Berger, M., Turckheim, M., Veyssiere, G., and Jean, C. (1982). Effect of pre-weaning undernutrition on testicular development in male mice. Int. J. Androl. 5, 627–635.
| Effect of pre-weaning undernutrition on testicular development in male mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXlt1Cgsw%3D%3D&md5=2d080f8f7c8b9be4e19d0f0e987e3700CAS | 6819237PubMed |
Olar, T. T., Amann, R. P., and Pickett, B. W. (1983). Relationships among testicular size, daily production and output of spermatozoa and extragonadal spermatozoal reserves of the dog. Biol. Reprod. 29, 1114–1120.
| Relationships among testicular size, daily production and output of spermatozoa and extragonadal spermatozoal reserves of the dog.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2c%2FotVKmug%3D%3D&md5=f406adcdf4468a1ddab890885eb70d69CAS | 6652178PubMed |
Rae, M. T., Kyle, C. E., Millar, D. W., Hammond, A. J., Brooks, A. N., and Rhind, S. M. (2002). The effects of undernutrition, in utero, on reproductive function in adult male and female sheep. Anim. Reprod. Sci. 72, 63–71.
| The effects of undernutrition, in utero, on reproductive function in adult male and female sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XltFahsLw%3D&md5=50fee9a577d3a8ad8cd4294ffbc9b427CAS | 12106966PubMed |
Reeves, P. G., Nielsen, F. H., and Fahey, G. C. (1993). AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J. Nutr. 123, 1939–1951.
| 1:CAS:528:DyaK2cXltlegsw%3D%3D&md5=c16e1f984b11a244e77c7ded678489fbCAS | 8229312PubMed |
Roosen-Runge, E. C. (1973). Germinal-cell loss is normal metazoan spermatogenesis. J. Reprod. Fertil. 35, 339–348.
| Germinal-cell loss is normal metazoan spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2c%2FivFShtw%3D%3D&md5=598c18220a11b7e61eca4f4293ab9441CAS | 4584655PubMed |
Russell, L. D., Ettlin, R. A., Sinha Hikim, A. P., and Clegg, E. D. (1990). `Histological and Histopathological Evaluation of the Testis. (Cache River Press: Vienna)
Russell, L. D., Chiarini-Garcia, H., Korsmeyer, S. J., and Knudson, C. M. (2002). Bax-dependent spermatogonia apoptosis is required for testicular development and spermatogenesis. Biol. Reprod. 66, 950–958.
| Bax-dependent spermatogonia apoptosis is required for testicular development and spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitlCltb8%3D&md5=8ec158f95223f6d85051cd9f12a73681CAS | 11906913PubMed |
Sharpe, R. M. (1994). Regulation of spermatogenesis. In ‘The Physiology of Reproduction’. (Eds E. Knobil and J. D. Neil.) pp. 1363–1434. (Raven Press: New York.)
Silva, J. E., and Rabelo, R. (1997). Regulation of the uncoupling protein gene expression. Eur. J. Endocrinol. 136, 251–264.
| Regulation of the uncoupling protein gene expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXitlyrsb8%3D&md5=43ed9c32e8335ed125318c525cc45152CAS | 9100546PubMed |
Sinha Hikim, A. P., Bartke, A., and Russell, L. D. (1988). Morphometric studies on hamster testes in gonadally active and inactive states: light microscope findings. Biol. Reprod. 39, 1225–1237.
| Morphometric studies on hamster testes in gonadally active and inactive states: light microscope findings.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1M7hvVCjtw%3D%3D&md5=48b6b6b103e4be5c49441ab830aaba9eCAS | 3219392PubMed |
Steinberger, A., and Steinberger, E. (1971). Replication pattern of Sertoli cells in maturing rat testis in vivo and in organ culture. Biol. Reprod. 4, 84–87.
| 1:STN:280:DyaE38%2FitVWksg%3D%3D&md5=84b5f8f9fbf5155bd2b194ab05300f09CAS | 5110903PubMed |
Toledo, F. C., Perobelli, J. E., Pedrosa, F. P. C., Anselmo-Franci, J. A., and Kempinas, W. D. G. (2011). In utero protein restriction causes growth delay and alters sperm parameters in adult male rats. Reprod. Biol. Endocrinol. 9, 94.
| In utero protein restriction causes growth delay and alters sperm parameters in adult male rats.Crossref | GoogleScholarGoogle Scholar | 21702915PubMed |
Wang, Z. X., Wreford, N. G., and de Kretser, D. M. (1989). Determination of Sertoli cell numbers in the developing rat testis by stereological methods. Int. J. Androl. 12, 58–64.
| Determination of Sertoli cell numbers in the developing rat testis by stereological methods.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1M3jtlCmsQ%3D%3D&md5=03643b9a909a1e9f45113067717a9df3CAS | 2714873PubMed |
Young, K. A., Zirkin, B. R., and Nelson, R. J. (2000). Testicular regression in response to food restriction and short photoperiod in white-footed mice (Peromyscus leucopus) is mediated by apoptosis. Biol. Reprod. 62, 347–354.
| Testicular regression in response to food restriction and short photoperiod in white-footed mice (Peromyscus leucopus) is mediated by apoptosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXotVOruw%3D%3D&md5=a712733956bf40d78790ab5bdeefff98CAS | 10642572PubMed |
Zambrano, E., Gonzáles-Rodrigues, G. L., Guzmán, C., García-Becerra, R., Boeck, L., Díaz, L., Menjivar, M., Larrea, F., and Nathanielsz, P. W. (2005). A maternal low-protein diet during pregnancy and lactation in rats impairs male reproductive development. J. Physiol. 563, 275–284.
| A maternal low-protein diet during pregnancy and lactation in rats impairs male reproductive development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXitVSnuro%3D&md5=49bf3b6c639552aa63a7a030624b6b4fCAS | 15611025PubMed |
