Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-18T07:25:58.830Z Has data issue: false hasContentIssue false
  • English
  • Français

Duration of spermatogenesis and daily sperm production in the rodent Proechimys guyannensis

Published online by Cambridge University Press:  16 June 2016

Nathália L.M. Lara ,
Ivan C. Santos ,
Guilherme M.J. Costa ,
Dirceu A. Cordeiro-Junior ,
Antônio C. G. Almeida ,
Ana P. Madureira ,
Marcos S. Zanini  and
Luiz R. França
Nathália L.M. Lara
Affiliation:
Laboratory of Cellular Biology, Department of Morphology, Federal University of Minas Gerais, Belo Horizonte, Minas Gerais 31270–901, Brazil.
Ivan C. Santos
Affiliation:
Department of Biosystems Engineering, Federal University of São João Del-Rei, São João Del-Rei, Minas Gerais 36307–352, Brazil.
Guilherme M.J. Costa
Affiliation:
Laboratory of Cellular Biology, Department of Morphology, Federal University of Minas Gerais, Belo Horizonte, Minas Gerais 31270–901, Brazil.
Dirceu A. Cordeiro-Junior
Affiliation:
Laboratory of Cellular Biology, Department of Morphology, Federal University of Minas Gerais, Belo Horizonte, Minas Gerais 31270–901, Brazil.
Antônio C. G. Almeida
Affiliation:
Department of Biosystems Engineering, Federal University of São João Del-Rei, São João Del-Rei, Minas Gerais 36307–352, Brazil.
Ana P. Madureira
Affiliation:
Department of Biosystems Engineering, Federal University of São João Del-Rei, São João Del-Rei, Minas Gerais 36307–352, Brazil.
Marcos S. Zanini
Affiliation:
Department of Veterinary Medicine, Federal University of Espirito Santo, Vitoria, Espirito Santo 29075–910, Brazil.
Luiz R. França*
Affiliation:
Laboratory of Cellular Biology, Department of Morphology, Federal University of Minas Gerais, Belo Horizonte, Minas Gerais 31270–901, Brazil.
*
All correspondence to: Luiz Renato de França. Laboratory of Cellular Biology, Department of Morphology, INPA/Manaus, Brazil; and Federal University of Minas Gerais, Belo Horizonte, Minas Gerais 31270–901, Brazil. Tel: +55 31 3409 2816 or +55 31 99618 1992. Fax: +55 31 3409 2780. E-mail: lrfranca@icb.ufmg.br or lrfranca@inpa.gov.br
Get access Rights & Permissions [Opens in a new window]

Summary

The spiny rat (Proechimys guyannensis) is a neotropical rodent that is used in biomedical research, particularly research related to chronic resistance to epilepsy and infectious diseases. To our knowledge, there are few reports concerning the reproductive biology of this species. Therefore, besides providing basic biometric and morphometric data, in the present study we investigated testis function and spermatogenesis in adult spiny rats. The mean testis weight and gonadosomatic index obtained were 1.63 ± 0.2 g and 1.15 ± 0.1% respectively. Based on the development of the acrosomic system, 12 stages of the seminiferous epithelium cycle were characterized. Stages VI and VII presented the highest frequencies (~17–19%), whilst stages II to V showed the lowest frequencies (~2–4%). The most advanced germ cell types labelled at 1 h or 20 days after BrdU injections were respectively preleptotene/leptotene spermatocytes at stage VII and elongated spermatids at stage III. The mean duration of one cycle was 7.5 ± 0.01 days and the entire spermatogenic process lasted 33.7 ± 0.06 days (~4.5 cycles). The seminiferous tubules (ST) occupied ~96 ± 1% of the testis parenchyma, whereas Leydig cells comprised only 1.5 ± 0.4%. The number of Sertoli cells (SC) per testis gram and the SC efficiency (spermatids/SC) were respectively 78 × 106 ± 11 × 106 and 7.9 ± 1. The daily sperm production per testis gram (spermatogenic efficiency; daily sperm production (DSP)/g/testis) was 78 × 106 ± 8 × 106. To our knowledge, this spermatogenic efficiency is among the highest found for mammals investigated to date and is probably related to the very short duration of spermatogenesis and the very high ST percentage and SC number obtained for this species.

Keywords

P. guyannensisSertoli cell efficiencySperm productionSpermatogenesisSpiny ratTestis
Type
Research Article
Information
Zygote , Volume 24 , Issue 5 , October 2016 , pp. 783 - 793
Copyright
Copyright © Cambridge University Press 2016 

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

Abercrombie, M. (1946). Estimation of nuclear populations from microtome sections. Anat. Rec. 94, 238–48.CrossRefGoogle ScholarPubMed
Almeida, F.F., Leal, M.C. & França, L.R. (2006). Testis morphometry, duration of spermatogenesis, and spermatogenic efficiency in the wild boar (Sus scrofa scrofa). Biol. Reprod. 75, 792–9.CrossRefGoogle ScholarPubMed
Amann, R.P. & Almquist, J.O. (1962). Reproductive capacity of dairy bulls. VI. Effect of unilateral vasectomy and ejaculation frequency on sperm reserves; aspects of epididymal physiology. J. Reprod. Fertil. 3, 260–8.Google Scholar
Amann, R.P. & Schanbacher, B.D. (1983). Physiology of male reproduction. J. Anim. Sci. 57, 380–403.Google Scholar
Arida, R.M., Scorza, F.A., Carvalho, R.A. & Cavalheiro, E.A. (2005). Proechimys guyannensis: an animal model of resistance to epilepsy. Epilepsia 46, 189–97.Google Scholar
Auharek, A.S., Avelar, G.F., Lara, N.L.M., Sharpe, R.M. & França, L.R. (2011). Sertoli cell numbers and spermatogenic efficiency are increased in inducible nitric oxide synthase mutant mice. Int. J. Androl. 34, 621–9.Google Scholar
Avelar, G.F., Leal, M.C. & França, L.R. (2004). Sertoli and Leydig cells number per testis and daily sperm production in different mice strains. Miniposter presented at the 13th European Workshop on Molecular & Cellular Endocrinology of the Testis (eds Levy, F.O., Taskén, K. & Hansson, V.) Edinburgh, United Kingdom.Google Scholar
Catzeflis, F. & Patton, J. (2008). Proechimys guyannensis. IUCN 2012. IUCN Red List of Threatened Species. Version 2012.2. www.iucnredlist.org.Google Scholar
Cavalheiro, E.A. (1995). The pilocarpine model of epilepsy. Ital. J. Neurol. Sci. 16, 33–7.CrossRefGoogle ScholarPubMed
Clermont, Y. (1972). Kinetics of spermatogenesis in mammals: seminiferous epithelium cycle and spermatogonial renewal. Physiol. Rev. 52, 198–236.Google Scholar
Clermont, Y. & Harvey, S.C. (1965). Duration of the cycle of the seminiferous epithelium of normal, hypophysectomized and hypophysectomized-hormone treated albino rats. Endocrinology 76, 80–9.Google Scholar
Clermont, Y. & Trott, M. (1969). Duration of the cycle of the seminiferous epithelium in the mouse and hamster determined by means of 3H-thymidine and radioautography. Fertil. Steril. 20, 805–17.Google Scholar
Comizzoli, P., Mermillod, P. & Mauget, R. (2000). Reproductive biotechnologies for endangered mammalian species. Reprod. Nutr. Dev. 40, 493–504.Google Scholar
Cordeiro-Junior, D.A., Costa, G.M.J., Talamoni, A.S. & França, L.R. (2010). Spermatogenic efficiency in the spiny rat, Trinomys moojeni (Rodentia: Echimyidae). Anim. Reprod. Sci. 119, 97–105.Google Scholar
Costa, G.M., Chiarini-Garcia, H., Morato, R.G., Alvarenga, R.L.L.S. & França, L.R. (2008). Duration of spermatogenesis and daily sperm production in the jaguar (Panthera onca). Theriogenology 70, 113646.CrossRefGoogle ScholarPubMed
Costa, G.M., Leal, M.C., Silva, J.V., Cássia, A., Ferreira, S., Guimarães, D.A. & França, L.R. (2010). Spermatogenic cycle length and sperm production in a feral pig species (collared peccary, Tayassu tajacu). J. Androl. 31, 221–30.Google Scholar
Eisenberg, J.F. & Redford, K.H. (1999). Mammals of the Neotropics . The Central Neotropics: Ecuador, Peru, Bolivia, Brazil. Chicago: The University of Chicago Press.Google Scholar
Eler, E.S, da Silva, M.N.F., Silva, C.E.F. & Feldberg, E. (2012). Comparative cytogenetics of spiny rats of the genus Proechimys (Rodentia, Echimyidae) from the Amazon region. Genet. Mol. Res 11, 830–46.Google Scholar
Everard, C.O.R. & Tikasingh, E.S. (1973). Ecology of the rodents, Proechimys guyannensis trinitatis and Oryzomys capito velutinus on Trinidad. J. Mammal. 54, 875–86.CrossRefGoogle Scholar
Fabene, P.F., Bertini, G., Correia, L., Cavalheiro, E.A. & Bentivoglio, M. (2001). The thalamus of the Amazon spiny rat Proechimys guyannensis, an animal model of resistance to epilepsy, and pilocarpine-induced long-term changes of protein expression. Thalamus Related Syst. 1, 117–33.Google Scholar
França, L.R. (2007). Espermatogénesis (Espermatogénesis, producción y tránsito del esperma a través del epidídimo). [Spermatogenesis (Spermatogenesis, sperm production and transit through the epididymis).] Separata 15, 16–27.Google Scholar
França, L.R., Avelar, G.F. & Almeida, F.F. (2005). Spermatogenesis and sperm transit through the epididymis in mammals with emphasis on pigs. Theriogenology 63, 300–318.Google Scholar
França, L.R. & Godinho, C.L. (2003). Testis morphometry, seminiferous epithelium cycle length, and daily sperm production in domestic cats (Felis catus). Biol. Reprod. 68, 1554–61.CrossRefGoogle ScholarPubMed
França, L.R. & Hess, R.A. (2005). Structure of the Sertoli cell. In Sertoli Cell Biology (eds Skinner, M.K. & Griswold, M.D.), pp. 19–40. San Diego, CA, USA: Elsevier Academic Press.Google Scholar
França, L.R., Ogawa, T., Avarbock, M.R., Brinster, R.L. & Russell, L.D. (1998). Germ cell genotype control cells cycle during spermatogenesis in the rat. Biol. Reprod. 59, 1371–7.Google Scholar
França, L.R. & Russell, L.D. (1998). The testis of domestic mammals. In Male Reproduction: A Multidisciplinary Overview (eds Regadera, J. & Martinez-Garcia, F.), pp. 198–219. Madrid: Churchill Livingstone.Google Scholar
Geoffroy Saint-Hilaire, E. (1803). Catalogue des mammifères du Muséum National d'Histoire Naturelle. [Mammals Catalogue from the National Museum of Natural History.] Paris: Muséum National d'Histoire Naturelle.Google Scholar
Hawking, F., Walker, P.J., Worms, M.J. (1964), New small animals for laboratory experiment, viz: Herpestes sanguineus (African black tailed mongoose), host of filarial worm, Monnigofilaria setariosa. Orizomys goeldi, Proechimys guyanensis, from Brazil. Thamnomys surdaster, Congo tree rat, host of Plasmodium berghei; colonized in laboratory. Trop Med Hyg 58, 292.Google Scholar
Hess, R.A. & França, L.R. (2007). Spermatogenesis and the cycle of the seminiferous epithelium. In Molecular Mechanisms in Spermatogenesis (ed. Cheng, C.Y.), pp. 1–15. Austin: Landes Bioscience. Google Scholar
Hochereau-de Reviers, M.T. & Lincoln, G.A. (1978). Seasonal variation in the histology of the testis of the red deer, Cervus elaphus. J. Reprod. Fertil. 54, 209–13.Google Scholar
Holsberger, D.R. & Cooke, P.S. (2005). Understanding the role of thyroid hormone in Sertoli cell development: a mechanistic hypothesis. Cell Tissue Res. 322, 133–40.Google Scholar
Johnson, L. & Neaves, W.B. (1981). Age related changes in Leydig cell population, seminiferous tubules and sperm production in stallions. Biol. Reprod. 24, 703–12.Google Scholar
Johnson, L., Varner, D.D., Roberts, M.E., Smith, T.L., Keillor, G.E. & Scrutchfield, W.L. (2000). Efficiency of spermatogenesis: a comparative approach. Anim. Reprod. Sci. 60–61, 471–80.Google Scholar
Kenagy, G.J. & Trombulak, S.C. (1986). Size and function of mammalian testes in relation to body size. J. Mammal. 67, 1–22.CrossRefGoogle Scholar
Kerr, J.B., Loveland, K.L., O'Bryan, M.K. & de Kretser, D.M. (2006). Cytology of the testis and intrinsic control mechanisms. In Physiology of Reproduction (ed. Neill, J.D.), pp. 827–947. Birmingham: Elsevier.Google Scholar
Lange, R.R. & Schmidt, E.M.S. (2007). Rodentia: Roedores Silvestres (Capivara, Cutia, Paca, Ouriço). [Rodentia: Wild rodents (Capybara, agouti, paca, porcupine).] In Tratado de Animais Selvagens: Medicina Veterinária (eds Cubas, Z.S., Silva, J.C.R. & Catão-Dias, J.L.), pp. 475–491. São Paulo: Roca. Google Scholar
Leal, M.C. & França, L.R. (2006). The seminiferous epithelium cycle length in the black tufted-ear marmoset (Callithrix penicillata) is similar to humans. Biol. Reprod. 74, 616–24.Google Scholar
Leal, M.C. & França, L.R. (2008). Postnatal Sertoli and Leydig cell proliferation and the establishment of puberty and sexual maturity in Chinchilla lanigera (Rodentia, Chinchillidae). Reprod. Fertil. Dev. 20, 665–73.CrossRefGoogle ScholarPubMed
Leal, M.C. & França, L.R. (2009). Slow increase of Sertoli cell efficiency and daily sperm production causes delayed establishment of full sexual maturity in the rodent Chinchilla lanigera . Theriogenology 71, 509–18.Google Scholar
Leblond, C.P. & Clermont, Y. (1952). Definition of the stages of the cycle of the seminiferous epithelium in the rat. Ann. N. Y. Acad. Sci. 55, 548–84.Google Scholar
Madureira, A.P., Passos, S.R., Resende, D.R., Souza, N.F., Almeida, A.C.G. & Zanini, M.S. (2014). Zoological techniques parameters of Proechimys guyannensis (Rodentia, Echimydae) bred in captivity. Rev Inst. Adolfo Lutz 73, 124–9.Google Scholar
Neves, E.S., Chiarini-Garcia, H. & França, L.R. (2002). Comparative testis morphometry and seminiferous epithelium cycle length in donkeys and mules. Biol. Reprod. 67, 247–55.Google Scholar
Nowak, R.M. (1999). Walker's Mammals of the World. Baltimore: Johns Hopkins University Press.Google Scholar
Orth, J.M., Gunsalus, G.L. & Lamperti, A.A. (1988). Evidence from Sertoli cell depleted rats indicates that spermatid number in adults depends on numbers of Sertoli cells produced during perinatal development. Endocrinology 122, 787–94.Google Scholar
Patton, J.L., Da Silva, M.N.F. & Malcolm, J.R. (2000). Mammals of the Rio Juruá and the evolutionary and ecological diversification of Amazonia. B. . Am. Mus. Nat. Hist. 244, 1–306.Google Scholar
Paula, T.A.R., Chiarini-Garcia, H. & França, L.R. (1999). Seminiferous epithelium cycle and its duration in capybaras (Hydrochoerus hydrochaeris). Tissue Cell 31, 327–34.Google Scholar
Rocha, D.C., Debeljuk, L. & França, L.R. (1999). Exposure to constant light during testis development increases daily sperm production in adult Wistar rats. Tissue Cell 31, 372–9.Google Scholar
Rocha, L., Arida, R.M., Carvalho, R.A., Scorza, F.A., Neri-Bazan, L. & Cavalheiro, E.A. (2006). GABA and opioid binding distribution in the brain of the seizure-resistant Proechimys guyannensis: an autoradiography study. Synapse 60, 392–8.Google Scholar
Russell, L.D., Ettlin, R.A., Sinha-Hikim, A.P. & Clegg, E.D. (1990). Histological and histopathological evaluation of the testis. Florida: Cache River Press.Google Scholar
Scorza, C.A., Araujo, B.H., Leite, L.A., Torres, L.B., Otalora, L.F.P., Oliveira, M.S., Garrido-Sanabria, E.R. & Cavalheiro, E.A. (2011). Morphological and electrophysiological properties of pyramidal-like neurons in the stratum oriens of cornu ammonis 1 and cornu ammonis 2 area of Proechimys. Neuroscience 177, 252–68.Google Scholar
Setchell, B.P. & Breed, W.G. (2006). Anatomy, vasculature and innervation of the male reproductive tract. In Physiology of Reproduction (ed. Neill, J.D.), pp. 771–825. Birmingham: Elsevier.Google Scholar
Sharpe, R.M. (1994). Regulation of spermatogenesis. In The Physiology of Reproduction (eds Knobil, E. & Neill, J.D.), pp. 1363–1434. New York: Raven Press.Google Scholar
Sharpe, R.M., Fraser, H.M., Brougham, M.F., McKinnell, C., Morris, K.D., Kelnar, C.J.H., Wallace, W.H.B. & Walker, M. (2003). Role of the neonatal period of pituitary-testicular activity in germ cell proliferation and differentiation in the primate testis. Hum. Reprod. 18, 2110–7.Google Scholar
Short, R.V. (1997). The testis: the witness of the mating system, the site of mutation and the engine of desire. Acta Paediatr. Suppl. 422, 3–7 Google Scholar
Silva, C.E., Eler, E.S., da Silva, M.N. & Feldberg, E. (2012). Karyological analysis of Proechimys cuvieri and Proechimys guyannensis (Rodentia, Echimyidae) from central Amazon. Genet. Mol. Biol. 35, 88–94.Google Scholar
Silva, J.C., Pimenta, G.M.B., Andersen, M.L., Schoorlemmer, G.H.M., Tufik, S. & Cavalheiro, E.A. (2014). Characterization of the sleep–wake cycle of the neotropical rodent Proechimys guyannensis . SAGE Open Med. 2, 1–6.CrossRefGoogle ScholarPubMed
Silva, R.C., Costa, G.M., Andrade, L.M. & França, L.R. (2010). Testis stereology, seminiferous epithelium cycle length, and daily sperm production in the ocelot (Leopardus pardalis). Theriogenology 73, 157–67.Google Scholar
Sinha-Hikim, A.P., Bartke, A. & Russell, L.D. (1988). Morphometric studies on hamster testis in gonadally active and inactive states: light microscope findings. Biol. Reprod. 39, 1225–37.Google Scholar
Sousa, A.L., Campos-Junior, P.H.A., Costa, G.M.J. & França, L.R. (2014). Spermatogenic cycle length and sperm production in the freshwater turtle Kinosternon scorpioides . Biol. Reprod. 90, 1–10.CrossRefGoogle ScholarPubMed
Steiner, C., Sourrouille, P. & Catzeflis, F. (2000). Molecular characterization and mitochondrial sequence variation in two sympatric species of Proechimys (Rodentia: Echimyidae) in French Guiana. Biochem. Syst. Ecol. 28, 963–73.Google Scholar
Tesh, R.B. (1970). Notes on the reproduction, growth, and development of echimyid rodents in Panama. J. Mammal. 51, 199–202.Google Scholar
Van Haaster, L.H. & De Rooij, D.G. (1993). Spermatogenesis is accelerated in the immature Djungarian and Chinese hamster and rat. Biol. Reprod. 49, 1229–35.Google Scholar
Weir, B.J. (1973). Another hystricomorph rodent: keeping casiragua (Proechimys guairae) in captivity. Lab. Anim. 7, 125–34.Google Scholar
Wildt, D.E. (2005). Lions, tigers, and pandas, oh my. J. Androl. 26, 452–4.Google Scholar
Wilson, D.E & Reeder, D.M. (2005). Mammal Species of the World, A Taxonomic and Geographic Reference. Baltimore: Johns Hopkins University Press.Google Scholar