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Morphofunctional evaluation of the testis, duration of spermatogenesis and spermatogenic efficiency in the Japanese fancy mouse (Mus musculus molossinus)

Published online by Cambridge University Press:  11 July 2017

Guilherme M.J. Costa ,
Marcelo C. Leal  and
Luiz R. França
Guilherme M.J. Costa
Affiliation:
Laboratory of Cellular Biology, Department of Morphology, Institute of Biological Sciences, Federal University of Minas Gerais, Belo Horizonte, MG, Brazil.
Marcelo C. Leal
Affiliation:
Federal University of Lavras (UFLA), Animal Science, Lavras, MG, Brazil.
Luiz R. França*
Affiliation:
Laboratory of Cellular Biology, Department of Morphology, Institute of Biological Sciences, Federal University of Minas Gerais, Belo Horizonte, MG, Brazil. National Institute of Amazonian Research (INPA), Manaus, AM, Brazil.
*
All correspondence to: Luiz Renato de França. Laboratory of Cellular Biology, Department of Morphology, Institute of Biological Sciences, Federal University of Minas Gerais, Belo Horizonte, MG, Brazil. Tel: +55 31 96181992 or +55 92 996055655. E-mail: [email protected] or [email protected]
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Summary

Japanese fancy mouse, mini mouse or pet mouse are common names used to refer to strains of mice that present with different colour varieties and coat types. Although many genetic studies that involve spotting phenotype based on the coat have been performed in these mice, there are no reports of quantitative data in the literature regarding testis structure and spermatogenic efficiency. Hence, in this study we researched testis function and spermatogenesis in the adult Japanese fancy mouse. The following values of 68 ± 6 mg and 0.94 ± 0.1% were obtained as mean testis weight and gonadosomatic index, respectively. In comparison with other investigated mice strains, the fancy mouse Leydig cell individual size was much smaller, resulting in higher numbers of these cells per gram of testis. As found for laboratory mice strains, as a result of the development of the acrosomic system, 12 stages of the seminiferous epithelium cycle have been described in this study. The combined frequencies of pre-meiotic and post-meiotic stages were respectively 24% and 64% and very similar to the laboratory mice. The more differentiated germ cell types marked at 1 h or 9 days after tritiated thymidine administration were preleptotene/leptotene and pachytene spermatocytes at the same stage (VIII). The mean duration of one spermatogenic cycle was 8.8 ± 0.01 days and the total length of spermatogenesis lasted 37.8 ± 0.01 days (4.5 cycles). A high number of germ cell apoptosis was evident during meiosis, resulting in lower Sertoli cell and spermatogenic efficiencies, when compared with laboratory mice strains.

Keywords

Germ cell apoptosisLeydig cellSertoli cellSperm productionSpermatogenesis
Type
Research Article
Information
Zygote , Volume 25 , Issue 4 , August 2017 , pp. 498 - 506
Copyright
Copyright © Cambridge University Press 2017 

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References

Abercrombie, M. (1946). Estimation of nuclear populations from microtome sections. Anat. Record. 94, 238–48.Google Scholar
Amann, R.P. (1962). Reproductive capacity of dairy bulls. IV. Spermatogenesis and testicular germ cell degeneration. Am. J. Anat. 110, 69–78.Google Scholar
Amann, R.P. & Schanbacher, B.D. (1983). Physiology of male reproduction. J. Anim. Sci. 2, 380–403.Google Scholar
Amann, R.P., 1983. Endocrine changes associated with onset of spermatogenesis in Holstein bulls. J. Dairy Sci. 66, 2606–22.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. In 13th European Workshop on Molecular & Cellular Endocrinology of Testis (eds Levy, F.O., Taskén, K. & Hansson, V.), p. H1. Dunblane, Scotland.Google Scholar
Bhattacharyya, T., Gregorova, S., Mihola, O., Anger, M., Sebestova, J., Denny, P., Simecek, P. & Forejt, J. (2013). Mechanistic basis of infertility of mouse intersubspecific hybrids. Proc. Natl. Acad. Sci. USA 110, E468–77.CrossRefGoogle ScholarPubMed
Bundy, D.C. (1995). Photographic emulsions and processing. In Autoradiography and Correlative Imaging (eds Stumpf, W.E. & Solomon, H.F.), pp: 49–57. San Diego: Academic Press.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.CrossRefGoogle ScholarPubMed
Clermont, Y. (1972). Kinetics of spermatogenesis in mammals seminiferous epithelium cycle and spermatogonial renewal. Physiol. Rev. 52, 198–236.CrossRefGoogle ScholarPubMed
Comizzoli, P., Mermillod, P. & Mauget, R. (2000). Reproductive biotechnologies for endangered mammalian species. Reprod. Nutr. Dev. 40, 493–504.CrossRefGoogle ScholarPubMed
Cordeiro-Júnior, D.A., Costa, G.M., Talamoni, S.A. & França, L.R. (2010) Spermatogenic efficiency in the spiny rat, Trinomys moojeni (Rodentia: Echimyidae). Anim. Reprod. Sci. 119, 97–105.Google Scholar
Costa, G., Leal, M., Silva, J., Ferreira, A.C., Guimarães, D.A. & França, L.R. (2010a). Spermatogenic cycle length and sperm production in a feral pig species (collared peccary, Tayassu tajacu). J. Androl. 31, 221–30.CrossRefGoogle Scholar
Costa, G., Leal, M., Ferreira, A.C., Guimarães, D.A. & França, L.R. (2010b). Duration of spermatogenesis and spermatogenic efficiency in two large neotropical rodent species: the agouti (Dasyprocta leporina) and paca (Agouti paca). J. Androl. 31, 489–99.CrossRefGoogle Scholar
Davies, C.J. (1912). Fancy Mice, Their Varieties and Management as Pets or for Show. London: Cornell University Library.Google Scholar
França, L.R. & Hess, R.A. (2005). Structure of the Sertoli cell. In Sertoli Cell Biology (eds Skinner, M. & Griswold, M.), pp: 19–40. San Diego: Elsevier Academic Press.Google Scholar
França, L.R. & Russell, L.D. (1998). The testis of domestic animals, In Male Reproduction: A Multidisciplinary Overview (eds Martýnez, F. & Regadera, J.), pp. 197–219. Madrid: Churchill Livingston.Google Scholar
França, L.R., Ogawa, T., Avarbock, M.R., Brinster, R.L. & Russell, L.D. (1998). Germ cell genotype controls cell cycle during spermatogenesis in the rat. Biol. Reprod. 59, 1371–7.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, 300–18.Google Scholar
França, L.R. (1992). Daily sperm production in Piau boars estimated from Sertoli cell population and Sertoli cell index, In Proceedings of the 12th International Congress on Animal Reproduction and Artificial Insemination (ed. Dieleman, S. J.), pp. 1716–8. The Netherlands: Elsevier Science.Google Scholar
Gerber, J., Heinrich, J. & Brehm, R. (2016). Blood–testis barrier and Sertoli cell function: lessons from SCC×43KO mice. Reproduction 151, R15–27.Google Scholar
Gioiosa, L., Palanza, P., Parmigiani, S. & vom Saal, F.S. (2015). Effects of developmental exposure to low doses of bisphenol A on behavior and physiology in mice (Mus musculus). Dose Response 13, 1–8.Google Scholar
Hasegawa, A., Mochida, K., Matoba, S., Yonezawa, K., Ohta, A., Watanabe, G., Taya, K. & Ogura, A. (2012). Efficient production of offspring from Japanese wild-derived strains of mice (Mus musculus molossinus) by improved assisted reproductive technologies. Biol. Reprod. 86, 1–7.Google Scholar
Hess, R.A. & França, L.R. (2007). Spermatogenesis. Cycle of the seminiferous epithelium, In Molecular Mechanisms in Spermatogenesis (ed. Cheng, C.Y.), pp. 1–15. Austin, USA: 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.CrossRefGoogle ScholarPubMed
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 the Leydig cell population, seminiferous tubules and sperm production in stallions. Biol. Reprod. 24, 703–12.Google Scholar
Johnson, L., Varner, D.D., Robert, M.E., Smith, T.L., Keillor, G.E. & Scrutchfield, W.L. (2000). Efficiency of spermatogenesis: a comparative approach. Anim. Reprod. Sci. 61, 471–80.Google Scholar
Kerr, J.B., Loveland, K.L., O'Bryan, M.K. & Kretser, D.M. (2006). Cytology of the testis and intrinsic control mechanisms, In: Physiology of Reproduction (ed. Neill, J.D.), pp. 827–947. Birmingham, UK: Elsevier, Birmingham.Google Scholar
Koide, T., Moriwaki, K., Uchida, K., Mita, A., Sagai, T., Yonekawa, H., Katoh, H., Miyashita, N., Tsuchiya, K., Nielsen, T.J. & Shiroishi, T. (1998). A new inbred strain JF1 established from Japanese fancy mouse carrying the classic piebald allele. Mamm. Genome 9, 15–9.Google Scholar
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
Minezawa, M., Moriwaki, K. & Kondo, K. (1979). Geographical distribution of HbbP alleles in the Japanese wild mouse, Mus musculus molossinus. Jpn. J. Genet. 54, 165–73.Google Scholar
Moriwaki, K., Miyashita, N., Mita, A., Gotoh, H., Tsuchiya, K., Kato, H., Mekada, K., Noro, C., Oota, S., Yoshiki, A., Obata, Y., Yonekawa, H. & Shiroishi, Y. (2009). Unique inbred strain MSM/Ms established from the Japanese wild mouse. Exp. Anim. 58, 123–34.CrossRefGoogle ScholarPubMed
Pukazhenthi, B., Comizzoli, P., Travis, A.J. & Wildt, D.E. (2006). Applications of emerging technologies to the study and conservation of threatened and endangered species. Reprod. Fertil. Dev. 18, 77–90.CrossRefGoogle Scholar
Reissmann, M. & Ludwig, A. (2013). Pleiotropic effects of coat colour-associated mutations in humans, mice and other mammals. Semin. Cell Dev. Biol. 24, 576–86.Google Scholar
Rochester, J.R. (2013). Bisphenol A and human health: a review of the literature. Reprod. Toxicol. 42, 132–55.Google Scholar
Russell, L.D. & Clermont, Y. (1977). Degeneration of germ cells in normal, hypophysectomized and hormone treated hypophysectomized rats. Anat. Rec. 187, 347–66.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, UK: Elsevier.Google Scholar
Sharpe, R.M., Fraser, H.M., Brougham, M.F., McKinnell, C., Morris, K.D., Kelnar, C.J., Wallace, W.H. & 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
Sprando, R.L. (1990). Perfusion of the rat testis through the heart using heparin. In Histological and Histopathological Evaluation of the Testis (eds Russell, L.D., Ettlin, R.A., Sinha-Hikim, A.P.. & Clegg, E.D.), pp. 277–80. Clearwater: Cache River Press.Google Scholar
Steingrímsson, E., Copeland, N.G. & Jenkins, N.A. (2006). Mouse coat colour mutations: from fancy mice to functional genomics. Dev. Dyn. 235, 2401–2411.CrossRefGoogle ScholarPubMed
Subramanian, V.V. & Hochwagen, A. (2014). The meiotic checkpoint network: step-by-step through meiotic prophase. Cold Spring Harb. Perspect. Biol. 6, a016675.Google Scholar
Yonekawa, H., Moriwaki, K., Gotoh, O., Watanabe, J., Hayashi, J.I., Miyashita, N., Petras, M.L. & Tagashira, Y. (1988). Hybrid origin of Japanese mice Mus musculus molossinus: evidence from restriction analysis of mitochondrial DNA. Mol. Biol. Evol. 5, 63–78.Google Scholar
Yoshiki, A. & Moriwaki, K. (2006). Mouse phenome research: implications of genetic background. ILAR J. 47, 94–102.Google Scholar