Journal of Endocrinology and Reproduction

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Epididymis of the Lizard Eutropis carinata: A Light Microscopic and Ultrastructural Seasonal Study


Affiliations
1 Department of Zoology, Ahmednagar College, Ahmednagar - 414001, Maharashtra, India
2 Department of Studies in Zoology, Manasagangotri, University of Mysore, Mysuru - 570005, Karnataka, India
3 Department of Neuropathology, Electron Microscopy Laboratory, National Institute of Mental Health and Neurosciences (NIMHANS), Bengaluru - 560030, Karnataka, India
     

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The epididymis of the lizard Eutropis carinata can be divided into four regions viz., an initial segment (extra testicular) Efferent ductules (Eds) and three regions, the anterior region, a broad middle, and a narrow posterior, comparable to the caput, corpus, and cauda epididymidis of mammals. The anterior region of the epididymis is closely associated with a whitish initial segment (extra testicular), the Efferent ductules (Eds). The epididymal wall consists of an epithelial layer lining the lumen resting on a basement membrane surrounded by four to five layers of smooth circular muscles, a layer of connective tissue, and a layer of serosa. The ultrastructure study of the initial segment of epididymis the Eds during breeding season discloses four cell types in its epithelium viz., ciliated, non-ciliated, Apical-Mitochondria Rich Cells (AMRC), and basal cells. The anterior, middle, and posterior regions of the epididymis show five different cell types namely principal, basal, AMRC, narrow, and clear cells. Ciliated and non-ciliated cells are limited to the initial segment of the epididymis while, principal, narrow, and clear cells are found in the rest of the three regions of the epididymis. Basal and AMRC are found in all four regions. AMRCs are the most abundant cell type in the initial segment while principal cells are the major components of the epithelial lining of the remaining regions of the epididymis. During the non-breeding season, all the cell types are present but with regression and altered cytology of the cells without any sign of cellular activity in the different regions of the epididymis. During the breeding season, even the circulating testosterone levels are significantly higher compared to the non-breeding season. This is the first report describing different cell types in the initial segment and three different regions of the epididymis with ultrastructural seasonal variations in the Keeled Indian Mabuya, Eutropis carinata (Scincidae)

Keywords

Electron Microscopy, Epididymis, Epithelial Cells, Light Microscopy, Lizard, Seasonal Study, Ultrastructure.
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  • Toshimori K. Biology of spermatozoa maturation: An overview with an introduction to this issue. Microscopy Research and Technique. 2003; 61(1):1-6. https://doi. org/10.1002/jemt.10311

  • Robaire B, Hinton BT, Orgebin-Crist MC. The epididymis. In Neill K Ed: Knobil and Neill’s Physiology of Reproduction. 2006: pp. 1071-1148. Academic Press. https://doi.org/10.1016/B978-012515400-0/50027-0

  • Fox H. The urogenital system of reptiles. Biology of the Reptilia. 1977; 6(505):1-57.

  • Shanbhag BA. Reproductive biology of Indian reptiles. Proceedings of Indian National Science Academy. 2002; 68(6):497-528.

  • Crews D. Temperature-dependent sex determination: the interplay of steroid hormones and temperature. Zoological Science. 1996; 13(1):1-3. https://doi.org/10.2108/zsj.13.1

  • Pieau C, Dorizzi M, Richard-Mercier N. Temperaturedependent sex determination and gonadal differentiation in reptiles. Genes and Mechanisms in Vertebrate Sex Determination. 2001; p. 117-41. https:// doi.org/10.1007/978-3-0348-7781-7_7

  • McDiarmid RW, Foster MS, Guyer C, Chernoff N, Gibbons JW editors. Reptile Biodiversity: Standard Methods for Inventory and Monitoring. Univ of California Press. 2012 Jan 10. https://doi.org/10.1525/9780520952072

  • Haider S, Rai U. Epididymis of the Indian wall lizard (Hemidactylus flaviviridis) during the sexual cycle and in response to mammalian pituitary gonadotropins and testosterone. Journal of Morphology. 1987; 191(2):151- 60. https://doi.org/10.1002/jmor.1051910206

  • Shivanandappa T, Sarkar HBD. Androgenic regulation of epididymal function in the skink, Mabuya carinata (Schn.). Journal of Experimental Zoology. 1987; 241(3):369-76. https://doi.org/10.1002/jez.1402410312

  • Averal HI, Manimekalai M, Akbarsha MA. Differentiation along the ductus epididymis of the Indian garden lizard Calotes versicolor (Daudin). Biological Structures and Morphogenesis. 1992; 4(2):53-7.

  • Manimekalai M, Akbarsha MA. Secretion of glycoprotein granules in the epididymis of the agamid lizard Calotes versicolor (Daudin) is region-specific. Biological Structures and Morphogenesis. 1992; 4(3):96-101.

  • Akbarsha MA, Meeran MM. Occurrence of ampulla in the ductus deferens of the Indian garden lizard Calotes versicolor Daudin. Journal of Morphology. 1995; 225(3):261-8. https://doi.org/10.1002/jmor.1052250303

  • Meeran MM, Daisy P, Akbarsha MA. Histological differentiation along the ductus epididymis of the lizard Calotes versicolor Daudin. Journal of Animal Morphology and Physiology. 2001; 48:85-96.

  • Depeiges A, Dacheux JL. Acquisition of sperm motility and its maintenance during storage in the lizard, Lacerta vivipara. Reproduction. 1985; 74(1):23-7. https://doi. org/10.1530/jrf.0.0740023

  • Shivakumar GR, Sarkar HBD, Sekharappa BM. Histochemical profile of testis and epididymis in the lizard Psammophilus dorsalis (GRAY). Indian Journal of Experimental Biology. 1979; 17(8):826-30.

  • Guerrero SM, Calderón ML, de Pérez GR, Pinilla MP. Morphology of the male reproductive duct system of Caiman crocodilus (Crocodylia, Alligatoridae). Annals of Anatomy-Anatomischer Anzeiger. 2004; 186(3):235- 45. https://doi.org/10.1016/S0940-9602(04)80009-8

  • Holmes HJ, Gist DH. Excurrent duct system of the male turtle Chrysemys picta. Journal of Morphology. 2004; 261(3):312-22. https://doi.org/10.1002/jmor.10251

  • Olukole SG, Oyeyemi MO, Oke BO. Biometrical and histometrical observations on the testis and epididymis of the African sideneck turtle (Pelusios castaneus). European Journal of Anatomy. 2014; 18(2):102-8.

  • Mesure M, Chevalier M, Depeiges A, et al. Structure and ultrastructure of the epididymis of the viviparous lizard during the annual hormonal cycle: Changes of the epithelium related to secretory activity. Journal of Morphology. 1991; 210(2):133-45. https://doi. org/10.1002/jmor.1052100204

  • Pagliarini Cabral SR, Zieri R, Franco‐Belussi L, e al. Morphological changes of the epididymis and description of the excurrent ducts of Phrynops geoffroanus (Testudines: Chelidae) during the reproductive cycle. The Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology. 2011; 294(1):145- 55. https://doi.org/10.1002/ar.21302

  • Akbarsha MA, Kadalmani B, Tamilarasan V. Histological variation along and ultrastructural organization of the epithelium of the ductus epididymidis of the fan‐throated lizard Sitana ponticeriana Cuvier. Acta Zoologica. 2006; 87(3):181-96. https://doi.org/10.1111/ j.1463-6395.2006.00231.x

  • Akbarsha MA, Kadalmani B, Tamilarasan V. Efferent ductules of the fan-throated lizard Sitana ponticeriana Cuvier: light and transmission electron microscopy study. Acta Zoologica. 2007; 88(3):265-74. https://doi. org/10.1111/j.1463-6395.2007.00278.x

  • Sarkar HBD, Shivanandappa T. Reproductive cycles of reptiles. In: Reproductive Cycles of Indian Vertebrates. Bombay: Allied Publishers. 1989; p. 225-72.

  • Jones RC, Stone GM, Zupp J. Reproduction in the male echidna. In: Augee ML (Ed.): Platypus and Echidnas. Royal Society of New South Wales, Sydney, Australia. 1992. pp.:115–26.

  • Depeiges A, Dufaure JP. Binding to spermatozoa of a major soluble protein secreted by the epididymis of the lizard Lacerta vivipara. Gamete Research. 1983; 7(4):401-6. https://doi.org/10.1002/mrd.1120070411

  • Nirmal BK, Rai U. Epididymal protein secretion and its androgenic control in wall lizards Hemidactylus flaviviridis (Ruppell). Indian Journal of Experimental Biology. 2000; 38:720-6.

  • Aranha I, Bhagya M, Yajurvedi HN. Ultrastructural study of the epididymis and the vas deferens and electrophoretic profile of their luminal fluid proteins in the lizard Mabuya carinata. Journal of Submicroscopic Cytology and Pathology. 2006; 38(1):37-43.

  • Cardone A, Comitato R, Angelini F. Spermatogenesis, epididymis morphology and plasma sex steroid secretion in the male lizard Podarcis sicula exposed to diuron. Environmental Research. 2008; 108(2):214-23. https:// doi.org/10.1016/j.envres.2008.07.011

  • Dosemane D, Bhagya M. In vitro study of the spermatozoa motility in the lizard Eutropis carinata. International Journal of Zoological Research. 2015; 11(3):89. https:// doi.org/10.3923/ijzr.2015.89.95

  • Medini R, Bhagya M, Samson S. Identification and characterisation of the epididymal proteins in the lizard, Eutropis carinata (Reptilia, Squamata) (Schneider, 1801). General and Comparative Endocrinology. 2018; 259:76-84. https://doi.org/10.1016/j.ygcen.2017.11.005

  • Dacheux JL, Gatti JL, Dacheux F. Contribution of epididymal secretory proteins for spermatozoa maturation. Microscopy Research and Technique. 2003; 61(1):7-17. https://doi.org/10.1002/jemt.10312

  • Zhang L, Yang P, Bian X, et al. Modification of sperm morphology during long-term sperm storage in the reproductive tract of the Chinese soft-shelled turtle, Pelodiscus sinensis. Scientific Reports. 2015; 5(1):1-0. https://doi.org/10.1038/srep16096

  • Tarique I, Tariq M, Bai X, et al. Interaction of Epididymal Epithelia and their Secretions with Spermatozoa Supports Functional and Morphological Changes During Long-Term Storage in the Chinese Soft-Shelled Turtle (Pelodiscus sinensis). Microscopy and Microanalysis. 2020; 26(3):542-50. https://doi. org/10.1017/S1431927620001373

  • Shivanandappa T, Sarkar HBD. Histochemical localization of steroidogenic enzymes in the reptilian epididymis. Current Science. 1986; 20:175-8.

  • Stefanini MA, Miglino MA, LJ AD, Orsi AM. Morphological study of the vas deferens of the pigeon (Columba livia). Italian Journal of Anatomy and Embryology Archivio Italiano di Anatomia ed Embriologia. 1999; 104(3):133-9. https://doi. org/10.1002/(SICI)1097-4687(199912)242:3<247::AIDJMOR4> 3.0.CO;2-G

  • Aire TA. Aspects of the functional morphology of the ductus epididymidis in domestic anseriform and galliform birds. Anatomia, Histologia, Embryologia. 2000; 29(3):179-91. https://doi.org/10.1046/j.1439- 0264.2000.00259.x

  • Yeung CH, Cooper TG, Bergmann M, Schulze H. Organization of tubules in the human caput epididymidis and the ultrastructure of their epithelia. American Journal of Anatomy. 1991; 191(3):261-79. https://doi. org/10.1002/aja.1001910306

  • Sprando RL, Collins TF, Black TN, et al. Light microscopic observations on the reproductive tract of the male sand rat, Psammomys obesus. Tissue and Cell. 1999; 31(1):99-115. https://doi.org/10.1054/tice.1999.0003

  • Clulow J, Jones RC, Hansen LA. Micropuncture and cannulation studies of fluid composition and transport in the ductuli efferentes testis of the rat: comparisons with the homologous metanephric proximal tubule. Experimental Physiology: Translation and Integration. 1994; 79(6):915-28. https://doi.org/10.1113/expphysiol.1994. sp003817

  • Hoffer AP, Greenberg J. The structure of the epididymis, efferent ductules and ductus deferens of the guinea pig: A light microscope study. The Anatomical Record. 1978; 190(3):659-77. https://doi.org/10.1002/ar.1091900304

  • Greenberg J, Forssmann WG. Studies of the guinea pig epididymis. Anatomy and Embryology. 1983; 168(2):173-94. https://doi.org/10.1007/BF00315815

  • Jones R, Hamilton DW, Fawcett DW. Morphology of the epithelium of the extratesticular rete testis, ductuli efferentes and ductus epididymidis of the adult male rabbit. American Journal of Anatomy. 1979; 156(3):373-400. https://doi.org/10.1002/aja.1001560307

  • Piomboni P. Microanatomy of the epididymis and vas deferens. Journal of Submicroscopic Cytology and Pathology. 1997; 29(4):583-93.

  • Goyal HO. Morphology of the bovine epididymis. American Journal of Anatomy. 1985; 172(2):155-72. https://doi.org/10.1002/aja.1001720205

  • Robaire B, Hermo L. Efferent ducts, epididymis, and vas deferens: structure, functions, and their regulation. In: The Physiology of Reproduction. 1988; 1:999-1080.

  • Goyal HO, Williams CS. Regional differences in the morphology of the goat epididymis: a light microscopic and ultrastructural study. American Journal of Anatomy. 1991; 190(4):349-69. https://doi.org/10.1002/ aja.1001900404

  • Veri JP, Hermq L, Robaire B. Immunocytochemical localization of the Yf subunit of glutathione S‐transferase P shows regional variation in the staining of epithelial cells of the testis, efferent ducts, and epididymis of the male rat. Journal of Andrology. 1993; 14(1):23-44.

  • Yeung CH, Nashan D, Sorg C, et al. Basal cells of the human epididymis—antigenic and ultrastructural similarities to tissue-fixed macrophages. Biology of Reproduction. 1994; 50(4):917-26. https://doi. org/10.1095/biolreprod50.4.917

  • Holschbach C, Cooper TG. A possible extratubular origin of epididymal basal cells in mice. Reproduction. 2002; 123(4):517-25. https://doi.org/10.1530/rep.0.1230517

  • Akbarsha MA, Tamilarasan V, Kadalmani B, Daisy P. Ultrastructural evidence for secretion from the epithelium of ampulla ductus deferentis of the fan‐throated lizard Sitana ponticeriana Cuvier. Journal of Morphology. 2005; 266(1):94-111. https://doi.org/10.1002/jmor.10369

  • Desantis S, Labate M, Maria Labate G, Cirillo F. Evidence of regional differences in the lectin histochemistry along the ductus epididymis of the lizard, Podarcis sicula Raf. The Histochemical Journal. 2002; 34:123-30. https://doi. org/10.1023/A:1020986313281

  • Seiler P, Wenzel I, Wagenfeld A, et al. The appearance of basal cells in the developing murine epididymis and their temporal expression of macrophage antigens. International Journal of Andrology. 1998; 21(4):217-26. https://doi.org/10.1046/j.1365-2605.1998.00116.x

  • Palacios J, Regadera J, Nistal M, Paniagua R. Apical mitochondria‐rich cells in the human epididymis: An ultrastructural, enzymohistochemical, and immunohistochemical study. The Anatomical Record. 1991; 231(1):82-8. https://doi.org/10.1002/ar.1092310109

  • Martínez-García F, Regadera J, Cobo P, et al. The apical mitochondria‐rich cells of the mammalian epididymis. Andrologia. 1995; 27(4):195-206. https://doi.org/10.1111/j.1439-0272.1995.tb01093.x

  • Adamali HI, Hermo L. Apical and narrow cells are distinct cell types differing in their structure, distribution, and functions in the adult rat epididymis. Journal of Andrology. 1996; 17(3):208-22.

  • Medini R, Bhagya M, Samson S. Identification and characterisation of the epididymal proteins in the lizard, Eutropis carinata (Reptilia, Squamata) (Schneider, 1801). General and Comparative Endocrinology. 2018; 259:76-84. https://doi.org/10.1016/j.ygcen.2017.11.005

  • Medini R, Bhagya M, Samson S. Seasonal changes in the protein profile and enzyme activity of the epididymal luminal fluid in the lizard, Eutropis carinata (Schneider, 1801). Animal Biology. 2018; 68(4):387-404. https://doi.org/10.1163/15707563-17000124

  • Medini R, Bhagya M, Ravindra PV. Expression of β-hexosaminidase in the male reproductive system of the lizard, Eutropis carinata (Reptilia, Squamata) (Schneider, 1801). Cell and Tissue Research. 2018; 374:413-21. https://doi.org/10.1007/s00441-018-2874-2


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  • Epididymis of the Lizard Eutropis carinata: A Light Microscopic and Ultrastructural Seasonal Study

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Authors

Ivan Aranha
Department of Zoology, Ahmednagar College, Ahmednagar - 414001, Maharashtra, India
M. Bhagya
Department of Studies in Zoology, Manasagangotri, University of Mysore, Mysuru - 570005, Karnataka, India
B. K. Chandrashekar Sagar
Department of Neuropathology, Electron Microscopy Laboratory, National Institute of Mental Health and Neurosciences (NIMHANS), Bengaluru - 560030, Karnataka, India

Abstract


The epididymis of the lizard Eutropis carinata can be divided into four regions viz., an initial segment (extra testicular) Efferent ductules (Eds) and three regions, the anterior region, a broad middle, and a narrow posterior, comparable to the caput, corpus, and cauda epididymidis of mammals. The anterior region of the epididymis is closely associated with a whitish initial segment (extra testicular), the Efferent ductules (Eds). The epididymal wall consists of an epithelial layer lining the lumen resting on a basement membrane surrounded by four to five layers of smooth circular muscles, a layer of connective tissue, and a layer of serosa. The ultrastructure study of the initial segment of epididymis the Eds during breeding season discloses four cell types in its epithelium viz., ciliated, non-ciliated, Apical-Mitochondria Rich Cells (AMRC), and basal cells. The anterior, middle, and posterior regions of the epididymis show five different cell types namely principal, basal, AMRC, narrow, and clear cells. Ciliated and non-ciliated cells are limited to the initial segment of the epididymis while, principal, narrow, and clear cells are found in the rest of the three regions of the epididymis. Basal and AMRC are found in all four regions. AMRCs are the most abundant cell type in the initial segment while principal cells are the major components of the epithelial lining of the remaining regions of the epididymis. During the non-breeding season, all the cell types are present but with regression and altered cytology of the cells without any sign of cellular activity in the different regions of the epididymis. During the breeding season, even the circulating testosterone levels are significantly higher compared to the non-breeding season. This is the first report describing different cell types in the initial segment and three different regions of the epididymis with ultrastructural seasonal variations in the Keeled Indian Mabuya, Eutropis carinata (Scincidae)

Keywords


Electron Microscopy, Epididymis, Epithelial Cells, Light Microscopy, Lizard, Seasonal Study, Ultrastructure.

References





DOI: https://doi.org/10.18519/jer%2F2023%2Fv27%2F222227