Morphological and Structural Investigations of Egyptian Water Buffalo (Bubalus Bubalis) Sertoli Cells

Amira Derbalah; Karam Roshdy; Samir A.A. El-Gendy; Catrin Sian Rutland

doi:10.6000/1927-520X.2017.06.01.1

Authors

Amira Derbalah Department of Histology, Faculty of Veterinary Medicine, Alexandria University, Egypt
Karam Roshdy Department of Histology, Faculty of Veterinary Medicine, Alexandria University, Egypt
Samir A.A. El-Gendy Department of Anatomy and Embryology, Faculty of Veterinary Medicine, Alexandria University, Egypt
Catrin Sian Rutland School of Veterinary Medicine and Science, Faculty of Medicine, University of Nottingham, UK

DOI:

https://doi.org/10.6000/1927-520X.2017.06.01.1

Keywords:

Egypt, Testis, Buffalo, Bubalus Bubalis, morphology, Sertoli Cells.

Abstract

Buffaloes are essential part of the economy in many countries and provide sustainable food in addition to being working animals. Inefficiency in reproduction has become problematic in recent years due to a number of factors and although much research concentrates on the female, very little is known about the male buffalo reproductive system. To address this deficiency in the literature, testes were obtained from 20 clinically healthy water buffalo (Bubalus Bubalis) bulls aged 3 years old. Scanning electron microscopy showed that the Sertoli cells were columnar to triangle shaped with many processes. In the middle portion of the seminiferous tubules, the Sertoli cell had two types of processes with sheet like and slender cord like appearances. The sheet like processes had simple smooth margins originating from Sertoli cells, surrounding the surfaces of spermatogonia and spermatocytes. The slender cord like processes formed networks around other spermatogenic cells. Transmission electron microscopy showed that the Sertoli cells contained a large irregular shaped nucleus with deep nuclear membrane indentations, few mitochondria, aggregates of ribosomes and few rough endoplasmic reticulum which were observed within the indentations. Each nucleus contained a multivesicular nuclear body, containing vesicles, tubules and ribosome like dense structures. The work herein describes the structure and location of key reproductive cells within the water buffalo. Understanding the features of the male reproductive system is essential in order to advance studies into the reproductive decline of this species and the Bovidae family.

References

Warriach HM, McGill DM, Bush RD, Wynn PC, Chohan KR. A review of recent developments in buffalo reproduction - a review. Asian-Australasian Journal of Animal Sciences 2015; 28(3): 451-5. https://doi.org/10.5713/ajas.14.0259 DOI: https://doi.org/10.5713/ajas.14.0259

Bongso TA, Hilmi M, Basrur PK. Testicular cells in hybrid water buffaloes (Bubalus bubalis). Research in Veterinary Science 1983; 35(3): 253-8. DOI: https://doi.org/10.1016/S0034-5288(18)32016-2

Kumar S, Nagarajan M, Sandhu JS, Kumar N, Behl V. Phylogeography and domestication of Indian river buffalo. BMC Evolutionary Biology 2007; 7: 186. https://doi.org/10.1186/1471-2148-7-186 DOI: https://doi.org/10.1186/1471-2148-7-186

Luktuke SN, Ahuja LD. Studies on Ovulation in Buffaloes. J Reprod Fertil 1961; 2(2): 200-201.

Nam NH. Characteristics of reproduction of the water buffalo and techniques used to improve their reproductive performance. J Sci Dev 2010; 8(1): 100-10.

Gordon I. Controlled reproduction in cattle and buffaloes. UK: CABI 1996.

Qureshi MS, Khan S, Ahmad N. Pregnancy depresses milk yield in Dairy Buffaloes. Ital J Anim Sci 2007; 6: 1290-3. https://doi.org/10.4081/ijas.2007.s2.1290 DOI: https://doi.org/10.4081/ijas.2007.s2.1290

Usmani RH, Dailey RA, Inskeep EK. Effects of limited suckling and varying prepartum nutrition on postpartum reproductive traits of milked buffaloes. Journal of Dairy Science 1990; 73(6): 1564-70. https://doi.org/10.3168/jds.S0022-0302(90)78826-1 DOI: https://doi.org/10.3168/jds.S0022-0302(90)78826-1

Azmi TI, Bongso TA, Harisah M, Basrur PK. The Sertoli cell of the water buffalo--an electron microscopic study. Canadian Journal of Veterinary Research = Revue Canadienne de Recherche Veterinaire 1990; 54(1): 93-8.

Neglia G, Gasparrini B, Di Palo R, De Rosa C, Zicarelli L, Campanile G. Comparison of pregnancy rates with two estrus synchronization protocols in Italian Mediterranean Buffalo cows. Theriogenology 2003; 60(1): 125-33. https://doi.org/10.1016/S0093-691X(02)01328-6 DOI: https://doi.org/10.1016/S0093-691X(02)01328-6

Rossi P, Vecchio D, Neglia G, Di Palo R, Gasparrini B, D'Occhio MJ, et al. Seasonal fluctuations in the response of Italian Mediterranean buffaloes to synchronization of ovulation and timed artificial insemination. Theriogenology 2014; 82(1): 132-7. https://doi.org/10.1016/j.theriogenology.2014.03.005 DOI: https://doi.org/10.1016/j.theriogenology.2014.03.005

Kumaresan A, Ansari MR, Garg A. Modulation of post-thaw sperm functions with oviductal proteins in buffaloes. Anim Reprod Sci 2005; 90(1-2): 73-84. https://doi.org/10.1016/j.anireprosci.2005.01.009 DOI: https://doi.org/10.1016/j.anireprosci.2005.01.009

Bardin CW, Cheng CY, Musto NA, Gunsalus GL. The Sertoli cell. In: Knobil E, Neill JD, Ewing LL, Greenwald GS, Markert CL, Pfaff DW, editors. The Physiology of Reproduction. New York, NY, USA. Raven Press 1988; pp. 933-74.

Griswold MD, McLean JD. The Sertoli cell. In: Neill JD, Editors. Physiology of Reproduction. New York, NY, USA. Elsevier 2006; pp. 949-75. https://doi.org/10.1016/b978-012515400-0/50024-5 DOI: https://doi.org/10.1016/B978-012515400-0/50024-5

Dym M, Fawcett DW. The blood-testis barrier in the rat and the physiological compartmentation of the seminiferous epithelium. Biology of Reproduction 1970; 3(3): 308-26. DOI: https://doi.org/10.1093/biolreprod/3.3.308

Mruk DD, Cheng CY. Sertoli-Sertoli and Sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis. Endocrine Reviews 2004; 25(5): 747-806. https://doi.org/10.1210/er.2003-0022 DOI: https://doi.org/10.1210/er.2003-0022

Hedger MP, Hales DB. Immunophysiology of the male reproductive tract. In: Neill JD, Editor. Physiologyof Reproduction. New York, NY, USA. Elsevier 2006; pp. 1195-286. https://doi.org/10.1016/b978-012515400-0/50030-0 DOI: https://doi.org/10.1016/B978-012515400-0/50030-0

Russell L. Observations on Rat Sertoli Ectoplasmic (Junctional) Specializations in Their Association with Germ-Cells of Rat Testis. Tissue Cell 1977; 9(3): 475-98. https://doi.org/10.1016/0040-8166(77)90007-6 DOI: https://doi.org/10.1016/0040-8166(77)90007-6

Weber JE, Russell LD, Wong V, Peterson RN. 3-Dimensional Reconstruction of a Rat Stage V Sertoli-Cell .2. Morphometry of Sertoli Sertoli and Sertoli Germ-Cell Relationships. Am J Anat 1983; 167(2): 163-79. https://doi.org/10.1002/aja.1001670203 DOI: https://doi.org/10.1002/aja.1001670203

Russell LD, Tallondoran M, Weber JE, Wong V, Peterson RN. 3-Dimensional Reconstruction of a Rat Stage-V Sertoli-Cell .3. A Study of Specific Cellular Relationships. Am J Anat 1983; 167(2): 181-92. https://doi.org/10.1002/aja.1001670204 DOI: https://doi.org/10.1002/aja.1001670204

Vogl AW, Soucy LJ, Foo V. Ultrastructure of Sertoli-Cell Penetrating Processes Found in Germ-Cells of the Golden-Mantled Ground-Squirrel (Spermophilus-Lateralis). Am J Anat 1985; 172(1): 75-86. https://doi.org/10.1002/aja.1001720106 DOI: https://doi.org/10.1002/aja.1001720106

Fawcett D. Ultrastructure and function of the Sertoli cell. Male reproductive system. In: Hamilton DW, Greepa RO, Editors. Handbook of Physiology. Washington, DC, USA. American Physiology Society 1975; pp. 21-55.

Johnson L. Spermatogenesis. In: Cupps PT, Editor. Reproduction in Domestic Animals. 4th ed. San Diego, CA, USA. AcademicPress Inc. 1991; pp. 173-219. https://doi.org/10.1016/b978-0-08-057109-6.50010-0 DOI: https://doi.org/10.1016/B978-0-08-057109-6.50010-0

Russell LD. Form, dimensions, and cytology of mammalian Sertoli cells. In: Russell LD, Griswold MD, Editors. The Sertoli Cell. 1st ed. Clearwater, FL, USA. Cache River Press 1993.

McDowell AM, Trump F. Histologic fixatives suitable for diagnostic light and electron microscopy. Archives of Pathology and Laboratory Medicine 1976; 100: 405-515.

Hayat M. Basic Techniques for Transmission Electron Microscope. 2nd ed. Baltimore, USA. Academic Press 1986.

Evan AP, Dail WG, Dammrose D, Palmer C. Scanning electron microscopy of cell surfaces following removal of extracellular material. The Anatomical Record 1976; 185(4): 433-45. https://doi.org/10.1002/ar.1091850405 DOI: https://doi.org/10.1002/ar.1091850405

Kwon GO, Park YS, Lee SH, Yamamoto E, Hosaka Y, Ueda H, et al. Ultrastructure and function of Sertoli cell processes

in the Korean native goat. Okajimas Folia Anatomica JAPONICA 2002; 79(4): 121-7. https://doi.org/10.2535/ofaj.79.121 DOI: https://doi.org/10.2535/ofaj.79.121

Hamasaki M, Murakami M. Three-dimensional profiles of Sertoli cell processes and associated appendices as viewed by SEM. Journal of Electron Microscopy 1986; 35(2): 132-43.

Park YS, Abe M, Takehana K, Iwasa K. Three-dimensional structure of dog Sertoli cells: a computer-aided reconstruction from serial semi-thin sections. Archives of Histology and Cytology 1993; 56(1): 65-73. https://doi.org/10.1679/aohc.56.65 DOI: https://doi.org/10.1679/aohc.56.65

Terzakis JA. The nucleolar channel system of human endometrium. The Journal of Cell Biology 1965; 27(2): 293-304. https://doi.org/10.1083/jcb.27.2.293 DOI: https://doi.org/10.1083/jcb.27.2.293

Zibrin M. Multivesicular Nuclear Body with Nucleolar Activity in Sertoli Cells of Bulls - Ultrastructural Study. Z Zellforsch Mik Ana 1972; 135(2): 155-64. https://doi.org/10.1007/BF00315123 DOI: https://doi.org/10.1007/BF00315123

Osman DI, Ploen L. Fine-Structure of Sertoli Cells in the Camel (Camelus-Dromedarius). Anim Reprod Sci 1986; 10(1): 37-46. https://doi.org/10.1016/0378-4320(86)90138-7 DOI: https://doi.org/10.1016/0378-4320(86)90138-7

Curtis SK, Amann RP. Testicular development and establishment of spermatogenesis in Holstein bulls. Journal of Animal Science 1981; 53(6): 1645-57. https://doi.org/10.2527/jas1982.5361645x DOI: https://doi.org/10.2527/jas1982.5361645x

Kurohmaru M, Yamashiro S, Azmi TI, Basrur PK. An ultrastructural study of the Sertoli cell in the water buffalo (Bubalus bubalis). Anatomia, Histologia, Embryologia 1992; 21(1): 82-90. https://doi.org/10.1111/j.1439-0264.1992.tb00323.x DOI: https://doi.org/10.1111/j.1439-0264.1992.tb00323.x

Jurado SB, Kurohmaru M, Hayashi Y. An Ultrastructural-Study of the Sertoli-Cell in the Shiba Goat. J Vet Med Sci 1994; 56(1): 33-8. https://doi.org/10.1292/jvms.56.33 DOI: https://doi.org/10.1292/jvms.56.33

Andriana BB, Ishii M, Kanai Y, Kimura J, Fukuta K, Kurohmaru M, et al. Multivesicular nuclear body in sertoli cells of the lesser mouse deer, Tragulus javanicus. Okajimas Folia Anatomica Japonica 2003; 80(2-3): 35-9. https://doi.org/10.2535/ofaj.80.35 DOI: https://doi.org/10.2535/ofaj.80.35

More IAR, Armstrong EM, Mcseveney D, Chatfield WR. Morphogenesis and Fate of Nucleolar Channel System in Human Endometrial Glandular Cell. J Ultra Mol Struct R 1974; 47(1): 74-85. https://doi.org/10.1016/S0022-5320(74)90027-6 DOI: https://doi.org/10.1016/S0022-5320(74)90027-6

More IA, McSeveney D. The three dimensional structure of the nucleolar channel system in the endometrial glandular cell: serial sectioning and high voltage electron microscopic studies. Journal of Anatomy 1980; 130(Pt 4): 673-82.

Osman DI, Ploen L. Fine-Structure of the Modified Sertoli Cells in the Terminal Segment of the Seminiferous Tubules of the Bull, Ram and Goat. Anim Reprod Sci 1979; 2(4): 343-51. https://doi.org/10.1016/0378-4320(79)90021-6 DOI: https://doi.org/10.1016/0378-4320(79)90021-6