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Molecular and biochemical events in sperm storage tubules of oviduct in birds

Published online by Cambridge University Press:  07 December 2017

G.S. KHILLARE ,
K.V.H. SASTRY ,
R. AGRAWAL ,
A. PRAKASH ,
J. MOHAN  and
R.P. SINGH
G.S. KHILLARE*
Affiliation:
Division of Avian Physiology and Reproduction, Central Avian Research Institute, Izatnagar, Bareilly-243122, India
K.V.H. SASTRY
Affiliation:
Regional Station, Central Avian Research Institute, Bhubaneswar, Odisha, India
R. AGRAWAL
Affiliation:
Division of Avian Physiology and Reproduction, Central Avian Research Institute, Izatnagar, Bareilly-243122, India
A. PRAKASH
Affiliation:
Division of Avian Physiology and Reproduction, Central Avian Research Institute, Izatnagar, Bareilly-243122, India
J. MOHAN
Affiliation:
Division of Avian Physiology and Reproduction, Central Avian Research Institute, Izatnagar, Bareilly-243122, India
R.P. SINGH
Affiliation:
Division of Avian Physiology and Genetics, Salim Ali Centre for Ornithology and Natural History, Anaikkatty- 641 108, Coimbatore, India
*
Corresponding author: khillaregautam@gmail.com
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Abstract

In birds, after natural mating or artificial insemination (AI), sperms are transported through cloaca or vagina at the utero-vaginal junction (UVJ) of oviduct. Only 1% of the deposited sperm passes through the selection process in the vagina to reach the UVJ. In the UVJ, sperm enter the tubular invagination of the surface epithelium of the mucosa collectively called ‘sperm storage tubules’ (SSTs) where they are stored for longer duration retaining their fertilising capacity. The storage capacity and duration varies from species to species. This enables the birds to produce fertile eggs continuously. Shortly before and during egg production, sperm residing in the SST upon release will ascend the oviduct to the site of fertilisation in the infundibulum. Within the SSTs, sperm motility is suppressed and is initiated at some stage before fertilisation. Restoration of sperm motility is necessary for the release of spermatozoa from the SSTs. The exact mechanism by which sperm are stored in these tubules and released has not been established and hence, this is the focus of this review.

Keywords

sperm storage tubulesutero-vaginal junctionsperm storagebirds
Type
Reviews
Information
World's Poultry Science Journal , Volume 74 , Issue 1 , March 2018 , pp. 35 - 44
Copyright
Copyright © World's Poultry Science Association 2018 

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References

AIRE, T.A. and STEINBACH, J. (1976) Histochemical studies of the development of alkaline phosphatase activities in the ovary and oviduct of the fowl (Gallus domesticus). Acta Anatomica (Basel) 95: 207-217.CrossRefGoogle ScholarPubMed
ALLEN, T.E. and GRIGG, G.W. (1957) Sperm transport in the fowl. Australian Journal of Agricultural Research 81: 788-799.CrossRefGoogle Scholar
ASHIZAWA, K. and NISHIYAMA, H. (1983) Prolonged survival of fowl spermatozoa in the oviductal tissues in organ culture . British Poultry Science 24: 27-32.CrossRefGoogle ScholarPubMed
ASHIZAWA, K., HASHIGUCHI, A. and TSUZUKI, Y. (1994) Intercellular free ca+ concentration in fowl spermatozoa and its relationship to motility and respiration in spermatozoa. Journal of Reproduction and Fertility 96: 395-398.CrossRefGoogle Scholar
BAKST, M.R. and AKUFFO, V. (2007) Alkaline phosphatase reactivity in the vagina And utero-vaginal junction sperm storage tubules of turkeys in egg production: implications for sperm storage. British Poultry Science 48: 515-518.CrossRefGoogle Scholar
BAKST, M.R., DONOGHUE, A.M., YOHO, D.E., MOYLE, J.R., WHIPPLE, S.M., CAMP, M.J., LIN, G.Q. and BRAMWELL, R.K. (2010) Comparisons of sperm storage tubule distribution and number in 4 strains of mature broiler breeders and in turkey hens before and after the onset of photostimulation. Poultry Science 89: 986-992.CrossRefGoogle ScholarPubMed
BAKST, M.R., WISHART, G. and BRILLARD, J.P. (1994) Oviductal sperm selection, transport and storage in poultry. Poultry Science Review 5: 117-143.Google Scholar
BARNA, J., BOLDIZSAR, H. and ZSOLNAI-HARCZI, I. (1996) Amino acid secretion of the hen's oviduct during the egg formation cycle. Acta Veterinaria Hungarica 44: 233-241.Google ScholarPubMed
BIRKHEAD, T.R. and BRILLARD, J.P. (2007) Reproductive isolation in birds: postcopulatory prezygotic barriers. Trends in Ecology & Evolution 22: 266-272.CrossRefGoogle ScholarPubMed
BIRKHEAD, T.R. and FLETCHER, F. (1994) Numbers of Spermatozoa Attached to and Penetrating Perivitelline Layers of Japanese quail Eggs. The Auk 111: 997-1000.CrossRefGoogle Scholar
BIRKHEAD, T.R. and MOLLER, A.P. (1992) Numbers and size of sperm storage tubules and the duration of sperm storage in birds: a comparative study. Biological Journal of the Linnean Society 45: 363-372.CrossRefGoogle Scholar
BIRKHEAD, T.R., CUNNINGHAM, E.J.A. and CHENG, K.M. (1996) The insemination window provides a distorted view of sperm competition in birds. Proceedings of Royal Society Biological Sciences 263: 1187-1192.Google Scholar
BOBR, L.W. (1962) Oviducal distribution of spermatozoa and ferti1ity of the domestic fow1. Ph.D. Thesis, University California (Davis).Google Scholar
BOBR, L.W., LORENZ, F.W. and OQASAWARA, F.X. (1964) Distribution-of spermatozoa in the oviduct and fertility in domestic birds. Residence sites of spermatozoa, in fowl oviducts. Journal of Reproduction and Fertility 8: 39-47.CrossRefGoogle ScholarPubMed
BRÉQUE, C., SURAI, P. and BRILLARD, J.P. (2003) Roles of antioxidants on prolonged storage of avian spermatozoa in vivo and in vitro. Molecular Reproduction and Development 66: 314-323.CrossRefGoogle ScholarPubMed
BRÉQUE, C., SURAI, P. and BRILLARD, J.P. (2006) Antioxidant status of the lower oviduct in the chicken varies with age and dietary vitamin E supplementation. Molecular Reproduction and Development 73: 1045-1051.CrossRefGoogle ScholarPubMed
BRILLARD, J.P. (1993) Sperm storage and transport following natural mating and artificial insemination. Poultry Science 72: 923-928.CrossRefGoogle ScholarPubMed
BRILLARD, J.P. and BAKST, M.R. (1990) Quantification of spermatozoa in the sperm storage tubules of turkey hens and its relation to sperm numbers in the perivitelline layer of eggs. Biology of Reproduction 43: 271-275.CrossRefGoogle ScholarPubMed
BRISKIE, J.V. and MONTGOMERIE, R. (1993) Pattern of sperm storage in relation to sperm competition in passerine birds. The Condor 95: 442-454.CrossRefGoogle Scholar
BURKE, W.H. and OGASAWARA, F.X. (1969) Presence of spermatozoa in uterovaginal fluids of the hen at various stages of the ovulatory cycle. Poultry Science 48: 408-413.CrossRefGoogle ScholarPubMed
BURKE, W.B., OQASAWARA, F.X. and FUQUA, C.L. (1972) A study of the ultra structure of the uterovaginal sperm storage glands of the hen, Gallus domesticus, in relation to a mechanism for the release of spermatozoa. Journal of Reproduction and Fertility 29: 29-36.CrossRefGoogle Scholar
CONNEELY, O.M., DOBSON, A.D., TSAI, M.J., BEATTIE, W.G., TOFY, D.O., HUCKABY, C.S., ZARUCKIA, T., SCHRADER, W.T. and O'MALLEY, B.W. (1987) Sequence and expression of a functional chicken progesterone receptor. Molecular Endocrinology1: 517-525.CrossRefGoogle ScholarPubMed
CRICHTON, E.G., KRUTZSCH, P.H. and CHVAPIL, M. (1982) Studies on prolonged spermatozoa survival in chiroptera II. The role of zinc in the spermatozoa storage phenomenon. Comparative Biochemistry and Physiology 71: 71-73.CrossRefGoogle Scholar
DAS, S.C., ISOBE, N. and YOSHIMURA, Y. (2007) Changes in the mRNA expressions of sperm transforming growth factor β-isoforms and their receptors with reference to fertility during in vitro storage of fowl semen. Journal of Poultry Science 44: 189-197.CrossRefGoogle Scholar
DAS, S.C., ISOBE, N., NISHIBORI, M. and YOSHIMURA, Y. (2006) Expression of transforming growth factor-b isoforms and their receptors in uterovaginal junction of hen oviduct in presence or absence of resident sperm with reference to sperm storage. Reproduction 132: 781-790.CrossRefGoogle ScholarPubMed
DAS, S.C., NAGASAKA, N. and YOSHIMURA, Y. (2005a) Effects of repeated artificial insemination on the structure and function of oviductal sperm storage tubules in hens. Journal Poultry Science 42: 39-47.CrossRefGoogle Scholar
DAS, S.C., NAGASAKA, N. and YOSHIMURA, Y. (2005b) Changes in the expression of estrogen receptor mRNA in the utero-vaginal junction containing sperm storage tubules in laying hens after repeated artificial insemination. Theriogenology 65: 893-790.CrossRefGoogle ScholarPubMed
DAS, S.C., ISOBE, N. and YOSHIMURA, Y. (2008) Mechanism of prolonged sperm storage and sperm survivability in hen oviduct: a review American Journal of Reproductive Immunology 60: 477-481.CrossRefGoogle ScholarPubMed
DEGEN, A.A. and HAWES, R.O. (1972) Fertility in the domestic hen following the surgical removal of the uterovaginal junction. Poultry Science 51: 464-470.CrossRefGoogle Scholar
FRIEB, A.E., SINOWATZ, F., WROBEL, R. and SCKLEK-WINNISCH, R. (1978) The Uterovaginal Sperm Host Glands of the Quail (Coturnix coturnix japonica) An Ultrastructural and Ultracytochemical Study. Cell and Tissue Research 191: 101-114.Google Scholar
FROMAN, D. (2003) Deduction of a model for sperm storage in the oviduct of the domestic fowl (Gallus domesticus) . Biology of Reproduction 69: 248-253.CrossRefGoogle Scholar
FROMAN, D.P., FELTMANN, A.J., PENDARVIS, K., COOKSEY, S.M., BURGESS, S.C. and RHOADS, D.D. (2011) physiology and endocrinology symposium: A proteome-based model for sperm mobility phenotype. Journal of Animal Science 89: 1330-1337.CrossRefGoogle ScholarPubMed
FUJII, S. (1963) Histological and histochemical studies on the oviduct of the domestic fowl with special reference to the region of utero-vaginal junction. Archives of Histology and Cytology 23: 447-449.Google Scholar
FUJII, S. and TAMURA, T. (1963) Location of sperm in the oviduct of the domestic fowl with special reference to storage of sperm in the vaginal gland. Journal Faculty of Fisheries and Animal Husbandry Hiroshima University 5: 145-163.Google Scholar
GILBERT, A.B., REYNOLDS, M.B. and LORENZ, F.W. (1968) Distribution of spermatozoa in the oviduct and fertility, in domestic bird. V. Biotochemistry of the uterovaginal sperm host gland in the domestic hen. Journal of Reproduction and Fertility 16: 1433.CrossRefGoogle Scholar
HATCH, S.A. (1983) Mechanisms and ecological significance of sperm storage in the Northern Fulmar with reference to its occurrence in other birds. Auk 100: 593-600.CrossRefGoogle Scholar
HIGAKI, K., YOSHIMURA, Y., TAMURA, T. and OKAMOTO, T. (1995) Localisation of spermatozoa and leukocytes in vagina and utero-vaginal junction after copulation in Japanese quail (Coturnix coturnix japonica). Japanese Poultry Science 32: 387-393.CrossRefGoogle Scholar
HIYAMA, G., MATSUZAKI, M., MIZUSHIMA, S., DOHRA, H., IKEGAMI, K., YOSHIMURA, T., SHIBA, K., INABA, K. and SASANAMI, T. (2014) Sperm activation by heat shock protein 70 supports the migration of sperm released from sperm storage tubules in Japanese quail (Coturnix japonica). Reproduction 147: 167-178.CrossRefGoogle ScholarPubMed
HODGES, R.D. (1974) The reproductive system, in: The Histology of the Fowl, pp. 300-417 (London: Academic Press).Google Scholar
HOLM, L., EKWALL, H., WISHART, G.J. and RIDDERSTRALE, Y. (2000) Localisation of calcium and zinc in the sperm storage tubule of chicken, quail and turkey using X-ray microanalysis. Journal of Reproduction and Fertility 118: 331-336.CrossRefGoogle ScholarPubMed
HOWARTH, B. (Jr) (1974) Sperm storage as a function of the female reproductive tract, in: JOHNSON, A.D. & FOLEY, C.W. (Eds) The oviduct and its functions, pp. 237-270 (New York, Academic Press).Google Scholar
HUANG, A., ISOBE, N., OBITSU, T. and YOSHIMURA, Y. (2016) Expression of lipases and lipid receptors in sperm storage tubules and possible role of fatty acids in sperm survival in the hen oviduct. Theriogenology 85: 1334-1342.CrossRefGoogle ScholarPubMed
ITO, T., YOSHIZAKI, N., TOKUMOTO, T., ONO, H., YOSHIMURA, T., TSUKADA, A., KANSAKU, N. and SASANAMI, T. (2011) Progesterone is a sperm-releasing factor from the sperm-storage tubules in birds. Endocrinology 152: 3952-3962.CrossRefGoogle ScholarPubMed
LAKE, P.E. (1975) Gamate production and fertile period with particular reference to domesticated birds. Symposia of the Zoological Society of London 35: 225-328.Google Scholar
LONG, E.L., SONSTEGARD, T.S., LONG, J.A., VAN TASSELL, C.P. and ZUELKE, K.A. (2003) Serial analysis of gene expression in turkey sperm storage tubules in the presence and absence of resident sperm. Biology of Reproduction 69: 469-474.CrossRefGoogle ScholarPubMed
LORENZ, F.W. (1966) Behaviour of spermatozoa in the oviduct in relation to mating Japanese quail. Poultry Science 75: 135-139.Google Scholar
LORENZ, F.W. (1950) Onset and duration of fertility in turkeys. Poultry Science 29: 20-26.CrossRefGoogle Scholar
MERO, K.N. and OGASAWARA, F.X. (1970) Dimensions of the uterovaginal sperm storage tubules of the chicken and their possible significance in sperm release. Poultry Science 49: 1304-1308.CrossRefGoogle ScholarPubMed
NARISAWA, S., HUANG, L., IWASAKI, A., HASEGAWA, H. and ALPERS, D.H. (2003) Accelerated fat absorption in intestinal alkaline phosphatase knockout mice. Molecular and Cellular Biology 2003: 7525-7530.CrossRefGoogle Scholar
OKA, T. and SCHIMKE, R.T. (1969a) Interaction of estrogen and progesterone in chick oviduct development. I. Antagonistic effect of progesterone on estrogen-induced proliferation and differentiation of tubular gland cells. Journal of Cell Biology 41: 816-831.CrossRefGoogle ScholarPubMed
OKA, T. and SCHIMKE, R.T. (1969b) Interaction of estrogens and progesterone in chick oviduct development II. Effects of estrogen and progesterone on tubular gland cell function. The Journal of Cell Biology 43: 123-137.CrossRefGoogle ScholarPubMed
PALMITER, R.D. and WRENN, J.T. (1971) Interaction of estrogen and progesterone in chick oviduct development. Tubular gland cell cytodifferentiation. Journal of Cell Biology 50: 598-615.CrossRefGoogle ScholarPubMed
PESCATORE, A.J. and MARQUEZ, B.J. (1977) Sperm storage tubule development in immature turkeys injected with female sex steroids. Poultry Science 56: 1746-1747.Google Scholar
PETERSON, A.J. and WEBSTER, M. (1974) Oestrogen concentration in the peripheral plasma of maturing pullets. British Poultry Science 15: 569-572.CrossRefGoogle ScholarPubMed
REDDISH, J.M., KIRBY, J.D. and ANTHONY, N.B. (1996) Analysis of poultry fertility data and analysis of the duration of fertility in naturally mating Japanese quail. Poultry Science 75: 135-139.CrossRefGoogle ScholarPubMed
SASANAMI, T., IZUMI, S., SAKURAI, N., HIRATA, T., MIZUSHIMA, S., MATSUZAKI, M., HIYAMA, G., YORINAGA, E., YOSHIMURA, T., UKENA, K. and TSUTSUI, K. (2015) A unique mechanism of successful fertilisation in a domestic bird. Scientific Reports 5: 7700, DOI:10.1038/srep07700.CrossRefGoogle Scholar
SENIOR, B.E. (1974) Oestradiol concentration in the peripheral plasma of the domestic hen from 7 weeks of age until the time of sexual maturity. Journal of Reproduction and Fertility 41: 107-112.CrossRefGoogle ScholarPubMed
SINGH, R.P., SASTRY, K.V.H., PANDEY, N.K., SHIT, N., AGRAWAL, R., SINGH, K.B., MOHAN, J., SAXENA, V.K. and MOUDGAL, R.P. (2011a) Characterisation of lactate dehydrogenase enzyme in seminal plasma of Japanese quail (Coturnix coturnix japonica). Theriogenology 75: 555-562.Google ScholarPubMed
SINGH, R.P., SASTRY, K.V.H., PANDEY, N.K., SHIT, N., AGRAWAL, R., SINGH, K.B., MOHAN, J., SAXENA, V.K. and MOUDGAL, R.P. (2011b) Cloacal gland foam enhances motility and disaggregation of spermatozoa in Japanese quail (Coturnix japonica). Theriogenology 75: 563-539.CrossRefGoogle ScholarPubMed
SINOWATZ, F., WROBEL, K. and FRIES, A. (1976) On the histotopochemistry of the uterovaginal region in the quail (Coturnix coturnix japonica). Acta Histochemica 15: 1011-1014.Google Scholar
SITTMANN, K. and and ABPLANALP, H. (1965) Duration and recovery of fertility in Japanese quail (Coturnix coturnix japonica). British Poultry Science 6: 245-250.CrossRefGoogle ScholarPubMed
TILLY, J.L., KOWALSKI, K.I. and JOHNSON, A.L. (1991) Stage of ovarian follicular development associated with the initiation of steroidogenic competence in avian granulosa cells. Biology of Reproduction 44: 305-314.CrossRefGoogle ScholarPubMed
TINGARI, M.D. and LAKE, P.E. (1973) Ultrastructural studies on the utero-vaginal sperm-host glands of the domestic hens, Gallus domesticus . Journal of Reproduction and Fertility 34: 423-431.CrossRefGoogle Scholar
VAN KREY, H.P., SCHUPPIN, G.T., DENBOW, D.M. and HULET, R.M. (1987) Turkey breeder hen Infertility associated with plasma cells in the uterovaginal sperm storage glands. Theriogenology 27: 913-921.CrossRefGoogle Scholar
VAN DRIMMELEN, G.C. (1946) ‘Spermnests’ in the oviduct of the domestic hen. Journal of the South African Veterinary Medical Association 17: 42-45.Google Scholar
VAN KREY, H.P., BALANDER, R.J. and COMPTON, M.M. (1981) Storage and evacuation of spermatozoa from uterovaginal sperm host gland in domestic fowl. Poultry Science 60: 871-873.CrossRefGoogle ScholarPubMed
VAN KREY, H.P., OGASAWARA, F.X. and PANGBORN, J. (1967) Light and electron microscope studies of possible sperm gland emptying mechanisms. Poultry Science 46: 69-78.CrossRefGoogle ScholarPubMed
WANG, Z., ZHANG, S.Y., LI, F.X., MA, J., LIANG, B. and WANG, Y.L. (2005) Sperm storage in the Rickett's big-footed bat during hibernation. Progress in Natural Science 15: 1011-1014.Google Scholar
WISHART, G.J. and STEELE, M.G. (1990) The influence of sperm surface characteristics on sperm function in the female reproductive tract, in: Control of Fertility in Domestic Birds, pp. 101-112 (Les Colloques de 1'INRA).Google Scholar
WISHART, G.J. and HORROCKS, A.J. (2000) Fertilisation in birds and Fertilisation in Protozoa and Metazoan Animals, in: TARIN, J.J. & CARO, A. (Eds), pp. 193-222 (Springer, New York, NY).CrossRefGoogle Scholar
YOSHIMURA, Y., KOIKE, K. and OKAMOTO, T. (2000) Immunolocalisation of progesterone and estrogen receptors in the sperm storage tubules of laying and diethylstilbestrol-injected immature hens. Poultry Science 79: 94-98.CrossRefGoogle Scholar
ZANIBONI, L. and BAKST, M.R. (2004) Localisation of aquaporins in the sperm storage tubules in the turkey oviduct. Poultry Science 83: 1209-1212.CrossRefGoogle ScholarPubMed
ZAVALETA, D. and OGASAWARA, F.X. (1987) A review of the mechanism of the release of spermatozoa from storage tubules in the fowl and turkey oviduct. World's Poultry Science Journal 43: 132-139.CrossRefGoogle Scholar
ZHENG, W.M., NISHIBORI, M., ISOBE, N. and YOSHIMURA, Y. (2001) An in situ hybridisation study of the effect of artificial insemination on the localisation of cells expressing MHC class II mRNA in the chicken oviduct. Reproduction 122: 581-586.CrossRefGoogle Scholar