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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)

Part of: Micrographia Collection

Published online by Cambridge University Press:  14 April 2020

Imran Tarique ,
Mansoor Tariq ,
Xuebing Bai ,
Qu Wenjia ,
Ping Yang ,
Yufei Huang ,
Yang Sheng ,
Waseem Ali Vistro  and
Quisheng Chen Open the ORCID record for Quisheng Chen [Opens in a new window]
Imran Tarique
Affiliation:
MOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu Province210095, China
Mansoor Tariq
Affiliation:
Department of Veterinary Pathology, Sindh Agriculture University, Tandojam, Pakistan
Xuebing Bai
Affiliation:
MOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu Province210095, China
Qu Wenjia
Affiliation:
MOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu Province210095, China
Ping Yang
Affiliation:
MOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu Province210095, China
Yufei Huang
Affiliation:
MOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu Province210095, China
Yang Sheng
Affiliation:
MOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu Province210095, China
Waseem Ali Vistro
Affiliation:
MOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu Province210095, China
Quisheng Chen*
Affiliation:
MOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu Province210095, China
*
*Author for correspondence: Quisheng Chen, E-mail: [email protected]
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Abstract

Post-testicular maturation of spermatozoa is crucial for attaining the morphological and functional capabilities needed for successful fertilization. Epididymal epithelia offer a favorable environment for spermatozoa that are stored long term in the turtle epididymis; however, sperm–epithelial interactions during storage, which are enormously important for sperm functional and morphological maturation, are still largely unknown in turtles. The present study examined the epididymis during the sperm-storage period (November–April) in the Chinese soft-shelled turtle (Pelodiscus sinensis). Light and transmission electron microscopy were used to determine the cellular features of each epididymal segment (caput, corpus, and cauda) and their epithelial interactions with the spermatozoa. Spermatozoa were mainly located in the lumena of caput, corpus, and cauda epididymides. Numerous spermatozoa were bound to apical surfaces of the epithelia, and several were even embedded in the epithelial cytoplasm of the caput and corpus epididymides. No embedded spermatozoa were found in the cauda epididymis. In all epididymal segments, principal and clear cells showed the synthetic activity, evidenced by a well-developed endoplasmic reticulum network and high and low electron-dense secretory materials, respectively. Principal and clear cells in the caput and corpus segments showed embedded spermatozoa in electron-dense secretions and in the lipid droplets within the cytoplasm. No lysosomes were observed around the embedded spermatozoa. The lumena of the caput and corpus segments showed few apocrine and low electron density secretions. In the lumen of the cauda epididymidis, different secretions, such as holocrine with low and high electron density and their fragmentation, apocrine, and dictyosome, were found and are summarized. Altogether, sperm physical interactions with secretions either in the cytoplasm of epithelium or in the lumen may support the viability, morphological maintenance, and transfer of various proteins involved in long-term sperm storage in the turtle. This interaction could help us to understand the mechanisms of long-term sperm storage and provide more insights into the reproductive strategies of turtle sperm preservation.

Keywords

dictyosomeepididymisholocrinesperm storageturtle
Type
Micrographia
Information
Microscopy and Microanalysis , Volume 26 , Issue 3 , June 2020 , pp. 542 - 550
Copyright
Copyright © Microscopy Society of America 2020

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References

Ahammad, MU, Nishino, C, Tatemoto, H, Okura, N, Kawamoto, Y, Okamoto, S & Nakada, T (2011). Maturational changes in motility, acrosomal proteolytic activity, and penetrability of the inner perivitelline layer of fowl sperm, during their passage through the male genital tract. Theriogenology 76(6), 1100–1109.CrossRefGoogle ScholarPubMed
Akbarsha, MA, Faisal, K & Radha, A (2015). The epididymis: Structure and function. In Mammalian Endocrinology and Male Reproductive Biology, 1st ed., pp. 119–120. Boca Raton:CRC/Taylor & Francis.Google Scholar
Almeida-Santos, SM, Laporta-Ferreira, IL, Antoniazzi, MM & Jared, C (2004). Sperm storage in males of the snake Crotalus durissus terrificus (Crotalinae: Viperidae) in southeastern Brazil. Comp Biochem Physiol A Mol Integr Physiol 139(2), 169–174.CrossRefGoogle Scholar
Bian, X, Gandahi, JA, Liu, Y, Yang, P, Liu, Y, Zhang, L, Zhang, Q & Chen, Q (2013 a). The ultrastructural characteristics of the spermatozoa stored in the cauda epididymidis in Chinese soft-shelled turtle Pelodiscus sinensis during the breeding season. Micron 44, 202–209.CrossRefGoogle ScholarPubMed
Bian, X, Zhang, L, Yang, L, Yang, P, Ullah, S, Zhang, Q & Chen, Q (2013 b). Ultrastructure of epididymal epithelium and its interaction with the sperm in the soft-shelled turtle Pelodiscus sinensis. Micron 54–55, 65–74.CrossRefGoogle ScholarPubMed
Caballero, J, Frenette, G & Sullivan, R (2010). Post testicular sperm maturational changes in the bull: Important role of the epididymosomes and prostasomes. Vet Med Int 2011, 757194.Google ScholarPubMed
Chen, H, Huang, Y, Yang, P, Liu, T, Ahmed, N, Wang, L, Wang, T, Bai, X, Haseeb, A & Chen, Q (2019). Lipophagy contributes to long-term storage of spermatozoa in the epididymis of the Chinese soft-shelled turtle (Pelodiscus sinensis). Reprod Fertil Develop 31(4), 774–786.CrossRefGoogle Scholar
Chen, H, Yang, P, Chu, X, Huang, Y, Liu, T, Zhang, Q, Li, Q, Hu, L, Waqas, Y, Ahmed, N & Chen, Q (2016). Cellular evidence for nano-scale exosome secretion and interactions with spermatozoa in the epididymis of the Chinese soft-shelled turtle, Pelodiscus sinensis. Oncotarget 7(15), 19242–19250.CrossRefGoogle ScholarPubMed
Cornwall, GA (2009). New insights into epididymal biology and function. Hum Reprod Update 15(2), 213–227.CrossRefGoogle ScholarPubMed
Dacheux, J-L & Dacheux, F (2014). New insights into epididymal function in relation to sperm maturation. Reproduction 147(2), R27.CrossRefGoogle ScholarPubMed
Depeiges, A & Dacheux, JL (1984). Sperm motility in a non-mammalian vertebrate: The lizard lacerta vivipara acquisition of sperm motility and its maintenance during storage. Ann NY Acad Sci 438(1), 537–539.CrossRefGoogle Scholar
Esponda, P & Bedford, JM (1987). Post-testicular change in the reptile sperm surface with particular reference to the snake, Natrix fasciata. J Exp Zool 241(1), 123–132.CrossRefGoogle ScholarPubMed
Fornes, MW & de Rosas, JC (1989). Changes in the rat sperm head during epididymal transit. Gamete Res 24(4), 453–459.CrossRefGoogle ScholarPubMed
Fornés, MW & De Rosas, JC (1991). Interactions between rat epididymal epithelium and spermatozoa. Anat Rec 231(2), 193–200.CrossRefGoogle ScholarPubMed
Gist, DH, Dawes, SM, Turner, TW, Sheldon, S & Congdon, JD (2002). Sperm storage in turtles: A male perspective. J Exp Zool 292(2), 180–186.CrossRefGoogle ScholarPubMed
Gupta, G (2017). Sperm maturation in epididymis. In Male Infertility: Understanding, Causes and Treatment, Singh, R & Singh, K (Eds.), pp. 37–45. Singapore: Springer.CrossRefGoogle Scholar
Hashemi, HF & Goodman, JM (2015). The life cycle of lipid droplets. Curr Opin Cell Biol 33, 119–124.CrossRefGoogle ScholarPubMed
Helfenstein, F, Podevin, M & Richner, H (2010). Sperm morphology, swimming velocity, and longevity in the house sparrow Passer domesticus. Behav Ecol Sociobiol 64(4), 557–565.CrossRefGoogle Scholar
Hermo, L, Dworkin, J & Oko, R (1988). Role of epithelial clear cells of the rat epididymis in the disposal of the contents of cytoplasmic droplets detached from spermatozoa. Am J Anat 183(2), 107–124.CrossRefGoogle ScholarPubMed
Holt, WV (1982). Functional development of the mammalian sperm plasma membrane. In Oxford Reviews of Reproductive Biology, vol. 4, Finn, CA (Ed.), pp. 195–240. Oxford: Clarendon Press.Google Scholar
Holt, WV, Elliott, RM, Fazeli, A, Sostaric, E, Georgiou, AS, Satake, N, Prathalingam, N & Watson, PF (2006). Harnessing the biology of the oviduct for the benefit of artificial insemination. Soc Reprod Fertil Suppl 62, 247–259.Google ScholarPubMed
Holt, WV & Fazeli, A (2010). The oviduct as a complex mediator of mammalian sperm function and selection. Mol Reprod Develop 77(11), 934–943.CrossRefGoogle Scholar
Holt, WV & Fazeli, A (2016). Sperm storage in the female reproductive tract. Annu Rev Anim Biosci 4(1), 291–310.CrossRefGoogle ScholarPubMed
Horst, GVD, Seier, JV, Spinks, AC & Hendricks, S (1999). The maturation of sperm motility in the epididymis and vas deferens of the vervet monkey, Cercopithecus aethiops. Int J Androl 22(3), 197–207.CrossRefGoogle Scholar
Jean-Louis, D & Françoise, D (2014). New insights into epididymal function in relation to sperm maturation. Reproduction 147(2), R27–R42.Google Scholar
Jones, R (1998). Plasma membrane structure and remodelling during sperm maturation in the epididymis. J Reprod Fertil 53, 73–84.Google ScholarPubMed
Jones, R (2002). Plasma membrane composition and organisation during maturation of spermatozoa in the epididymis. In The Epididymis: From Molecules to Clinical Practice: A Comprehensive Survey of the Efferent Ducts, the Epididymis and the Vas Deferens, Robaire, B & Hinton, BT (Eds.), pp. 405–416. Boston, MA, USA: Springer.Google Scholar
Jones, RC (1999). To store or mature spermatozoa? The primary role of the epididymis. Int J Androl 22(2), 57–67.CrossRefGoogle ScholarPubMed
Jones, RC, Dacheux, J-L, Nixon, B & Ecroyd, HW (2007). Role of the epididymis in sperm competition. Asian J Androl 9(4), 493–499.CrossRefGoogle ScholarPubMed
Kaplan, M, Russell, LD, Peterson, RN & Martan, J (1984). Boar sperm cytoplasmic droplets: Their ultrastructure, their numbers in the epididymis and at ejaculation and their removal during isolation of sperm plasma membranes. Tissue Cell 16(3), 455–468.CrossRefGoogle ScholarPubMed
Kirchhoff, C (1999). Gene expression in the epididymis. Int Rev Cytol 188, 133–202.CrossRefGoogle ScholarPubMed
Liu, H-W, Shang, S-T, Chao, C-F & Muller, C (1991). The secretion of two sperm maturation-related glycoproteins in BALB/c mouse epididymis. Cell Tissue Res 265(3), 409–414.CrossRefGoogle ScholarPubMed
Miller, D (2010). Physiology and Endocrinology Symposium: Sperm–oviduct interactions in livestock and poultry. J Anim Sci 89, 1312–1314.CrossRefGoogle ScholarPubMed
Novo, M, Riesgo, A, Roldán, C, Giribet, G & Díaz Cosín, DJ (2012). A place for nourishment or a slaughterhouse? Elucidating the role of spermathecae in the terrestrial annelid Hormogaster elisae (Clitellata: Opisthopora: Hormogastridae). Zoomorphology 131(2), 171–184.CrossRefGoogle Scholar
Olson, GE, NagDas, SK & Winfrey, VP (2002). Structural differentiation of spermatozoa during post-testicular maturation. In The Epididymis: From Molecules to Clinical Practice: A Comprehensive Survey of the Efferent Ducts, the Epididymis and the Vas Deferens, Robaire, B & Hinton, BT (Eds.), pp. 371–387. Boston, MA, USA: Springer.Google Scholar
Păunescu, TG, Shum, WWC, Huynh, C, Lechner, L, Goetze, B, Brown, D & Breton, S (2014). High-resolution helium ion microscopy of epididymal epithelial cells and their interaction with spermatozoa. Mol Hum Reprod 20(10), 929–937.CrossRefGoogle ScholarPubMed
Phelps, BM, Primakoff, P, Koppel, DE, Low, MG & Myles, DG (1988). Restricted lateral diffusion of PH-20, a PI-anchored sperm membrane protein. Science 240(4860), 1780–1782.CrossRefGoogle ScholarPubMed
Waits, L, Dunkle, S, Wilkinson, FE, Moreau, P, Safranski, K, Reust, T, Morré, DM & Morré, DJ (1990). Cell-free transfer of sterols from dictyosome-like structures to plasma membrane vesicles of guinea pig testes. Protoplasma 154(1), 8–15.CrossRefGoogle Scholar
Yuan, S, Zheng, H, Zheng, Z & Yan, W (2013). Proteomic analyses reveal a role of cytoplasmic droplets as an energy source during epididymal sperm maturation. PLoS One 8, e77466.CrossRefGoogle ScholarPubMed
Zhang, L, Han, XK, Qi, YY, Liu, Y & Chen, QS (2008). Seasonal effects on apoptosis and proliferation of germ cells in the testes of the Chinese soft-shelled turtle, Pelodiscus sinensis. Theriogenology 69(9), 1148–1158.CrossRefGoogle ScholarPubMed