Ultra-differentiation of Sperm Head in Lesser Egyptian Jerboa, Jaculus jaculus (Family: Dipodidae)
Keywords:Ultra-structure, Sperm head, Lesser Egyptian Jerboa, Jaculus jaculus, Rodents
In the present study, events of sperm head differentiation in Lesser Egyptian Jerboa, Jaculus jaculus were studied for the first time. Adult males of J. jaculus were collected during their period of sexual activity from sandy regions of Marsa-Matrouh at northwest of Egypt. Tissues of their testes were prepared for ultrathin sections, which examined under a Joel "JEM-1200EXII" operating at 60-70kv. Early and late spermatids were photographed to describe the successive stages of sperm head differentiation.
Early spermatids have rounded or oval nuclei with fine chromatin granules and their cytoplasm showed numerous mitochondria, one or more chromatoid bodies and segments of rough endoplasmic reticulum. The first stage of spermatid development usually starts when the Golgi body produces secretory vesicles. These vesicles usually differentiate into an oval dense acrosomal granule, the rest forming a thin layer of acrosomal cap which extends to cover the anterior half of the nucleus and stop on at the nuclear shelf in the equatorial nuclear region. This cap is separated from the nuclear envelope by a narrowed subacrosomal space. Novel and complex structures are observed in the developing acrosome, which is, the crown, anterior, and posterior acrosomal segments, anterior and posterior acrosomal caps, as well as a long dorsal and a short ventral acrosomal caps; posterior subacrosomal spaces and subacrosomal cone at the tip of the elongated nucleus.
Cytoskeletal elements are responsible for re-shaping of the nucleus. A light comprehensive strength of cytoskeletal elements usually induces nuclear prolongation and formation of implantation fossa that appears in the ventrodorsal region at the posterior side of the nucleus. Manchette microtubules, solitary microtubules, and microfilaments may generate gentle compressive strength to accelerate nuclear prolongation.
Manchette microtubules, which disposed of parallel to one another and to the long axis of the nucleus, could exert the force, required to produce the spermatid nucleus elongation forward and perhaps backward and to protect DNA during nuclear condensation. A translucent space appears to surround the posterior half of the nucleus in order to mitigate the pressure on the nucleus and regulate the elongation with the protection of genetic material during nuclear condensation. Worth mentioning, that the translucent perinuclear space is a unique structure was not described or discussed before.
. Jeong, S.J., Yoo, J. and Jeong, M.J. (2004). Ultrastructure of the abnormal head of the epididymal spermatozoa in the big white-toothed shrew, Crocidura lasiura. Korean J. Electron Microscopy, 34(3): 179-184.
. Tang, X.M., Lalli, M.F. and Clermont, Y. (1982). A cytochemical study of the Golgi apparatus of the spermatid during spermiogenesis in the rat. Am. J. Anat., 163: 283-294.
. Burgos, M.H. and Gutierrez, L.S. (1986). The Golgi complex of the early spermatid in guinea pig. Anat. Rec., 216: 139-145.
. Ho, H.C., Tang, C.Y. and Suarez, S.S. (1999). Three-dimensional structure of the Golgi apparatus in mouse spermatids: a scanning electron microscopic study. Anat. Rec., 256: 189-194.
. Moreno, R.D., Ramalho-Santos, J., Chan, E.K., Wessel, G.M. and Schatten, G. (2000a). The Golgi apparatus segregates from the lysosomal/acrosomal vesicle during rhesus spermiogenesis: structural alterations. Dev. Biol., 219: 334- 349.
. Moreno, R.D., Ramalho-Santos, J., Sutovsky, P., Chan, E.K.L. and Schatten, G. (2000b). Vesicular traffic and Golgi apparatus dynamics during mammalian spermatogenesis: Implications for acrosome architecture. Biol. Reprod., 63: 89-98.
. Rattner, J.B. and Brinkley, B.R. (1972). Ultrastructure of mammalian spermiogenesis. 3. The organization and morphogenesis of the manchette during rodent spermiogenesis. J. Ultrastruct. Res., 41(3): 209-18.
. Meistrich, M.L., Trostle-Weige, P.K., Russell, L.D. (1990). Abnormal manchette development in spermatids of azh/azh mutant mice. Am. J. Anat., 188(1): 74-86.
. Russell, L.D., Russell, J.A., MacGregor, G.R., Meistrich, M.L. (1991). Linkage of manchette microtubules to the nuclear envelope and observations of the role of the manchette in nuclear shaping during spermiogenesis in rodents. Am. J. Anat., 192: 97-120.
. Fouquet, J., Kann, M., Soues, S. and Melki, R. (2000). ARP1 in Golgi organisation and attachment of manchette microtubules to the nucleus during mammalian spermatogenesis. J. Cell Sci., 113: 877-886.
. Kierszenbaum, A.L. (2002). Intramanchette transport (IMT): Managing the making of the spermatid head, centrosome, and tail. Mol. Reprod. Dev., 63(1): 1-4.
. Yokota, S. (2008). Historical survey on chromatoid body research. Acta Histochem. Cytochem., 41(4): 65-82.
. Jin, Q.S., Kamata, M., Garcia del Saz, E. and Seguchi, H. (1995). Ultracytochemical study of trimetaphosphatase activity during acrosomal formation in the mouse testis. Histol. Histopathol., 10: 681-689.
. Sapsford, C.S., Rae, C.A. and Cleland, K.W. (1970). Ultrastructural studies on the development and form of the principal piece sheath of the bandicoot spermatozoon. Aust. J. Zool., 18: 21-48.
. Oko, R. and Clermont, Y. (1989). Light microscopic immunocytochemical study of fibrous sheath and outer dense fiber formation in the rat spermatid. Anat. Rec., 225: 46-55.
. Kim, Y.H., de Kretser, D.M., Temple-Smith, P.D., Hearn, M.T., McFarlane, J.R. (1997). Isolation and characterization of human and rabbit sperm tail fibrous sheath. Mol. Hum. Reprod., 3(4): 307-313.
. Rawe, V.Y., Galaverna, G.D., Acosta, A.A., Olmedo, S.B., Chemes, H.E. (2001). Incidence of tail structure distortions associated with dysplasia of the fibrous sheath in human spermatozoa. Hum. Reprod., 16(5):879-86.
. Eddy, E.M., Toshimori, K. and O'Brien, D.A. (2003). Fibrous sheath of mammalian spermatozoa. Microsc. Res. Tech., 61: 103-115.
. Ricci, M. and Breed, W.G. (2005). Morphogenesis of the fibrous sheath in the marsupial spermatozoon. J. Anat., 207(2): 155-164.
. Guan, J., Kinoshita, M. and Yuan, L. (2009). Spatiotemporal Association of DNAJB13 with the annulus during mouse sperm flagellum development. BMC Dev. Biol., 9: 23. doi: 10.1186/1471-213X-9-23.
. Dadoune, J.P. and Alfonsi, M.F. (1986). Ultrastructural and cytochemical changes of the head components of human spermatids and spermatozoa. Gamete Res., 14: 33-46.
. Toyama, Y., Iwamoto, T., Yajima, M., Baba, K. and Yuasa, S. (2000). Decapitated and decaudated spermatozoa in man, and pathogenesis based on the ultrastructure. Int. J. Androl., 23(2): 109-115.
. Burgos, M.H. and Fawcett, D.W. (1955). Studies on the fine structure of the mammalian testis. I. Differentiation of the spermatid in the cat (Felis domestica). J. Biophys. Biochem. Cytol., 25;1(4):287-300.
. Sapsford, C.S., Rae, C.A., Cleland, K.W. (1969). Ultrastructual studies on maturing spermatids and on sertoli cells in the bandicoot Perameles nasuts Geoffroy (Marsupialia). Australian Journal of Zoology, 17: 195-292.
. Fawcett, D.W., Anderson, W.A. and Phillips, D.M. (1971). Morphogenetic factors influencing the shape of the sperm head. Developmental Biology, 26(2): 220-251.
. Singwi, M.S. and Lall, S.B. (1983). Spermatogenesis in the non-scrotal bat-Rhinopoma kinneari Wroughton (Microchiroptera: Mammalia). Acta Anat. (Basel), 116(2): 136-145.
. Holt, W.V. and Moore, H.D. (1984). Ultrastructural aspects of spermatogenesis in the common marmoset (Callithrix jacchus). J. Anat., 138: 175-188.
. Mori, T., Arai, S., Shiraishi, S. and Uchida, T.A. (1991). Ultrastructural Observations on Spermatozoa of the Soricidae, with Special Attention to a Subfamily Revision of the Japanese Water Shrew Chimarrogale himalayica. J. Mamm. Soc. Japan, 16: 1-12.
. Lin, M. and Jones, R.C. (2000). Spermiogenesis and spermiation in a monotreme mammal, the platypus, Ornithorhynchus anatinus. Journal of Anatomy, 196(2): 217-232.?
. Jeong, S.J., Park, J.C., Kim, H.J., Bae, C.S., Yoon, M.H., Lim, D.S., Jeong, M.J. (2006). Comparative fine structure of the epididymal spermatozoa from three Korean shrews with considerations on their phylogenetic relationships. Biocell, 30(2): 279-286.
. Challice, C.E. (1953). Electron microscope studies of spermiogenesis in some rodents. J. R. Microsc. Soc., 73(3): 115-27.
. Minamino, T. (1955). Spermiogenesis in the albino rat as revealed by electron microscopy. Electron Microsc., 4: 249-253.
. Pelletier, R.M. and Friend, D.S. (1983). Development of membrane differentiations in the guinea pig spermatid during spermiogenesis. Am. J. Anat., 167: 119-141.
. Lim, S.L., Qu, Z.P., Kortschak, R.D., Lawrence, D.M., Geoghegan, J., Hempfling, A.L., Bergmann, M., Goodnow, C.C., Ormandy, C.J., Wong, L., Mann, J., Scott, H.S., Jamsai, D., Adelson, D.L., O'Bryan, M.K. (2015). HENMT1 and piRNA Stability Are Required for Adult Male Germ Cell Transposon Repression and to Define the Spermatogenic Program in the Mouse. PLoS Genet., 11(10): e1005620. doi: 10.1371/journal.pgen.1005620.
. Shahin, A.A.B. and Ibraheem, M.H. (1998). Sperm morphology of the dipodid rodents (Jerboas) common in Egypt. Belgian Journal of Zoology,? 128(2): 189-200.
. Sarhan, O.M.M. (2009). Spermiogenesis of Egyptian mammals: 1-Sperm head and tail differentiation of fat-tailed gerbil Pachyuromys duprasi. Egypt. J. Zool., 53: 283-309.
. Sarhan, O.M. and Hefny, H.A. (2016). Ultra-differentiation of sperm tail of Lesser Egyptian Jerboa, Jaculus jaculus (Family: Dipodidae). J. Adv. Lab. Res. Biol., 7(1), 27-35.
. IUCN (International Union for Conservation of Nature, 2015). Jaculus jaculus. In: IUCN 2015. The IUCN Red List of Threatened Species. Version 2015.2. http://www.iucnredlist.org. Downloaded on 14 July 2015.
. Jung-Hun, L. ( 2003). Cell Differentiation and Ultrastructure of the Seminiferous Epithelium in Myotis macrodactylus. Korean Journal of Electron Microscopy, 33(1): 25-39.
. Lin, M., Harman, A. and Rodger, J.C. (1997). Spermiogenesis and spermiation in a marsupial, the tammar wallaby (Macropus eugenii). J. Anat., 190: 377-395.
. Tovich, P.R., Sutovsky, P. and Oko, R.J. (2004). Novel aspect of perinuclear theca assembly revealed by immunolocalization of non-nuclear somatic histones during bovine spermiogenesis. Biol. Reprod., 71(4):1182-94.
. Bedford, J.M. and Nicander, L. (1971). Ultrastructural changes in the acrosome and sperm membranes during maturation of spermatozoa in the testis and epididymis of the rabbit and monkey. J. Anat., 108: 527-543.
. Kurohmaru, M., Kobayashi, H., Hattori, S., Nishida, T. and Hayashi, Y. (1994). Spermatogenesis and ultrastructure of a peculiar acrosomal formation in the musk shrew, Suncus murinus. J. Anat., 185(3): 503-509.
. Kurohmaru, M., Maeda, S., Suda, A., Hondo, E., Ogawa, K., Endo, H., Kimura, J., Yamada, J., Rerkamnuaychoke, W., Chungsamarnyart, N., Hayashi, Y., Nishida, T. (1996). An ultrastructural and lectin-histochemical study on the seminiferous epithelium of the common tree shrew (Tupaia glis). J. Anat., 189(1): 87-95.