Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-26T05:28:11.990Z Has data issue: false hasContentIssue false

Regulation of egg formation in the oviduct of laying hen

Published online by Cambridge University Press:  11 July 2018

N. SAH
Affiliation:
Department of Human Nutrition, Food and Animal Sciences, University of Hawaii at Manoa, Honolulu, HI 96822, USA
B. MISHRA*
Affiliation:
Department of Human Nutrition, Food and Animal Sciences, University of Hawaii at Manoa, Honolulu, HI 96822, USA
*
Corresponding author: bmishra@hawaii.edu
Get access

Abstract

In the adult hen, the oviduct receives the ovum from the ovary and provides the biological environment for the formation and potential fertilisation of the egg. During egg formation, albumin, from the magnum is deposited around the yolk, followed by the eggshell membranes from the isthmus, which subsequently surround the egg. As the yolk traverses through the oviduct, calcium is deposited on to it, from the uterus, forming a hardened eggshell. Ovalbumin, avidin and ovomucin secreted from magnum provides content and antimicrobial activity in the egg-white. Collagen X and fibrilin 1 from the isthmus make up the fibrous eggshell membranes. Calbindin 1, ovocleidin-116 and secreted phosphoprotein 1 secreted from the shell gland contribute in calcium ion remodelling for eggshell mineralisation. This review summarises the expression pattern and functional role of genes having a leading role in the egg formation.

Type
Review
Copyright
Copyright © World's Poultry Science Association 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

ANASTASI, A., BROWN, M.A., KEMBHAVI, A.A., NICKLIN, M.J., SAYERS, C.A., SUNTER, D.C. and BARRETT, A.J. (1983) Cystatin, a protein inhibitor of cysteine proteinases. Improved purification from egg white, characterisation, and detection in chicken serum. The Biochemical Journal 211: 129-138.Google Scholar
ARAZI, H., YOSELEWITZ, I., MALKA, Y., KELNER, Y., GENIN, O. and PINES, M. (2009) Osteopontin and calbindin gene expression in the eggshell gland as related to eggshell abnormalities. Poultry Science 88: 647-653.Google Scholar
ATIKUZZAMAN, M., ALVAREZ-RODRIGUEZ, M., VICENTE-CARRILLO, A., JOHNSSON, M., WRIGHT, D. and RODRIGUEZ-MARTINEZ, H. (2017) Conserved gene expression in sperm reservoirs between birds and mammals in response to mating. BMC Genomics 18: 98.Google Scholar
ATIKUZZAMAN, M., MEHTA BHAI, R., FOGELHOLM, J., WRIGHT, D. and RODRIGUEZ-MARTINEZ, H. (2015) Mating induces the expression of immune- and pH-regulatory genes in the utero-vaginal junction containing mucosal sperm-storage tubuli of hens. Reproduction 150: 473-483.Google Scholar
BARON, F., JAN, S., GONNET, F., PASCO, M., JARDIN, J., GIUDICI, B., GAUTIER, M., GUÉRIN-DUBIARD, C. and NAU, F. (2014) Ovotransferrin plays a major role in the strong bactericidal effect of egg white against the bacillus cereus group. Journal of Food Protection 77: 955-962.Google Scholar
BOURIN, M., GAUTRON, J., BERGES, M., ATTUCCI, S., LE BLAY, G., LABAS, V., NYS, Y. and REHAULT-GODBERT, S. (2011) Antimicrobial potential of egg yolk ovoinhibitor, a multidomain kazal-like inhibitor of chicken egg. Journal of Agricultural and Food Chemistry 59: 12368-12374.Google Scholar
BRIONNE, A., NYS, Y., HENNEQUET-ANTIER, C. and GAUTRON, J. (2014) Hen uterine gene expression profiling during eggshell formation reveals putative proteins involved in the supply of minerals or in the shell mineralisation process. BMC Genomics 15: 220.Google Scholar
CHIEN, Y.C., HINCKE, M.T. and MCKEE, M.D. (2008) Avian eggshell structure and osteopontin. In: Cells Tissues Organs, pp. 38-43.Google Scholar
COLBERT, D.A., KNOLL, B.J., WOO, S.L., MACE, M.L., TSAI, M.J. and O'MALLEY, B.W. (1980) Differential hormonal responsiveness of the ovalbumin gene and its pseudogenes in the chick oviduct. Biochemistry 19: 5586-5592.Google Scholar
COLELLA, R., JOHNSON, A. and BIRD, J.W. (1991) Steady-state cystatin mRNA levels in chicken tissues in response to estrogen. Biomedica Biochimica Acta 50: 607-611.Google Scholar
CORDEIRO, C.M.M., ESMAILI, H., ANSAH, G. and HINCKE, M.T. (2013) Ovocalyxin-36 is a pattern recognition protein in phicken eggshell membranes. PLoS ONE 8: e84112.Google Scholar
CORSON, G.M., CHALBERG, S.C., DIETZ, H.C., CHARBONNEAU, N.L. and SAKAI, L.Y. (1993) Fibrillin binds calcium and is coded by cdnas that reveal a multidomain structure and alternatively spliced exons at the 5′ end. Genomics 17: 476-484.Google Scholar
DU, J., HINCKE, M.T., ROSE-MARTEL, M., HENNEQUET-ANTIER, C., BRIONNE, A., COGBURN, L.A., NYS, Y. and GAUTRON, J. (2015) Identifying specific proteins involved in eggshell membrane formation using gene expression analysis and bioinformatics. BMC Genomics 16: 1-13.Google Scholar
EBERS, K.L., ZHANG, C.Y., ZHANG, M.Z., BAILEY, R.H. and ZHANG, S. (2009) Transcriptional profiling avian beta-defensins in chicken oviduct epithelial cells before and after infection with Salmonella enterica serovar Enteritidis. BMC Microbiology 9: 153.Google Scholar
EK-RYLANDER, B., FLORES, M., WENDEL, M., HEINEGARD, D. and ANDERSSON, G. (1994) Dephosphorylation of osteopontin and bone sialoprotein by osteoclastic tartrate-resistant acid phosphatase. Modulation of osteoclast adhesion in vitro. Journal of Biological Chemistry 269: 14853-14856.Google Scholar
FEENEY, R.E., STEVENS, F.C. and OSUGA, D.T. (1963) The specificities of chicken ovomucoid and ovoinhibitor. The Journal of Biological Chemistry 238: 1415-1418.Google Scholar
FREEMAN, C.L., HARDING, J.H., QUIGLEY, D. and RODGER, P.M. (2010) Structural control of crystal nuclei by an eggshell protein. Angewandte Chemie International Edition 49: 5135-5137.Google Scholar
GAUTRON, J., HINCKE, M.T., PANHELEUX, M., GARCIA-RUIZ, J.M., BOLDICKE, T. and NYS, Y. (2001) Ovotransferrin is a matrix protein of the hen eggshell membranes and basal calcified layer. Connective Tissue Research 42: 255-267.Google Scholar
GIANSANTI, F., LEBOFFE, L. and ANTONINI, G. (2012) Antiviral Activity of Lactoferrin and Ovotransferrin Derived Peptides Towards Herpesviridae. Herpesviridae - A Look Into This Unique Family of Viruses, pp. 295-320 (InTech).Google Scholar
GONG, D., WILSON, P.W., BAIN, M.M., MCDADE, K., KALINA, J., HERVÉ-GRÉPINET, V., NYS, Y. and DUNN, I.C. (2010) Gallin; an antimicrobial peptide member of a new avian defensin family, the ovodefensins, has been subject to recent gene duplication. BMC Immunology 11: 12.Google Scholar
HARRIS, E.D., BLOUNT, J.E. and LEACH, R.M. (1980) Localisation of lysyl oxidase in hen oviduct: implications in eggshell membrane formation and composition. Science 208: 55-56.Google Scholar
HERNÁNDEZ-HERNÁNDEZ, A., GÓMEZ-MORALES, J., RODRÍGUEZ-NAVARRO, A.B., GAUTRON, J., NYS, Y. and GARCÍA-RUIZ, J.M. (2008) Identification of some active proteins in the process of hen eggshell formation. In: Crystal Growth and Design. 2008, pp. 4330-4339.Google Scholar
HINCKE, M.T., GAUTRON, J., TSANG, C.P., MCKEE, M.D. and NYS, Y. (1999) Molecular cloning and ultrastructural localisation of the core protein of an eggshell matrix proteoglycan, ovocleidin-116. The Journal of Biological Chemistry 274: 32915-32923.Google Scholar
HINCKE, M.T., TSANG, C.P., COURTNEY, M., HILL, V. and NARBAITZ, R. (1995) Purification and immunochemistry of a soluble matrix protein of the chicken eggshell (ovocleidin 17). Calcified Tissue International 56: 578-583.Google Scholar
HOUSLEY, P.R., GRIPPO, J.F., DAHMER, M.K. and PRATT, W.B. (1984) Chapter 12 - Inactivation, Activation, and Stabilisation of Glucocorticoid Receptors. Biochemical Actions of Hormones. pp. 347-376.Google Scholar
HRABIA, A., LEŚNIAK-WALENTYN, A., SECHMAN, A. and GERTLER, A. (2014) Chicken oviduct - The target tissue for growth hormone action: Effect on cell proliferation and apoptosis and on the gene expression of some oviduct-specific proteins. Cell and Tissue Research 357: 363-372.Google Scholar
JEONG, W., LIM, W., KIM, J., AHN, S.E., LEE, H.C., JEONG, J.-W., HAN, J.Y., SONG, G. and BAZER, F.W. (2012) Cell-specific and temporal aspects of gene expression in the chicken oviduct at different stages of the laying cycle. Biology of Reproduction 86: 172.Google Scholar
JOENSUU, T., TUOHIMAA, P. and VILJA, P. (1991) Avidin and ovalbumin induction by progesterone in chicken oviduct detected by sensitive immunoenzymometric assays. The Journal of Endocrinology 130: 191-197.Google Scholar
JOHNSON, A.L. and BRIDGHAM, J.T. (2001) Regulation of steroidogenic acute regulatory protein and luteinizing hormone receptor messenger ribonucleic acid in hen granulosa cells. Endocrinology 142: 3116-3124.Google Scholar
JONCHERE, V., REHAULT-GODBERT, S., HENNEQUET-ANTIER, C., CABAU, C., SIBUT, V., COGBURN, L.A., NYS, Y. and GAUTRON, J. (2010) Gene expression profiling to identify eggshell proteins involved in physical defense of the chicken egg. BMC Genomics 11: 57.Google Scholar
JUNG, J.G., LIM, W., PARK, T.S., KIM, J.N., HAN, B.K., SONG, G. and HAN, J.Y. (2011) Structural and histological characterisation of oviduct magnum and lectin-binding patterns in Gallus domesticus. Reproductive Biology and Endocrinology 9: 62.Google Scholar
KAWASHIMA, M., TAKAHASHI, T., KAMIYOSHI, M. and TANAKA, K. (1996) Effects of progesterone, estrogen, and androgen on progesterone receptor binding in hen oviduct uterus (shell gland). Poultry Science 75: 257-260.Google Scholar
KIM, J. and CHOI, Y.H. (2014) Differential abundance of egg white proteins in laying hens treated with corticosterone. Journal of Agricultural and Food Chemistry 62: 12346-12359.Google Scholar
KITAMOTO, T., NAKASHIMA, M. and IKAI, A. (1982) Hen egg white ovomacroglobulin has a protease inhibitory activity. Journal of Biochemistry 92: 1679-1682.Google Scholar
KOBAYASHI, K., HATTORI, M., HARA-KUDO, Y., OKUBO, T., YAMAMOTO, S., TAKITA, T. and SUGITA-KONISHI, Y. (2004) Glycopeptide derived from hen egg ovomucin has the ability to bind enterohemorrhagic Escherichia coli O157:H7. Journal of Agricultural and Food Chemistry 52: 5740-5746.Google Scholar
KODALI, V.K., GANNON, S.A., PARAMASIVAM, S., RAJE, S., POLENOVA, T. and THORPE, C. (2011) A novel disulfide-rich protein motif from avian eggshell membranes. PLoS ONE 6: e18187.Google Scholar
KOLACZKOWSKA, A., KOLACZKOWSKI, M., SOKOLOWSKA, A., MIECZNIKOWSKA, H., KUBIAK, A., ROLKA, K. and POLANOWSKI, A. (2010) The antifungal properties of chicken egg cystatin against candida yeast isolates showing different levels of azole resistance. Mycoses 53: 314-320.Google Scholar
LAVELIN, I., YARDEN, N., BEN-BASSAT, S., BAR, A. and PINES, M. (1998) Regulation of osteopontin gene expression during eggshell formation in the laying hen by mechanical strain. Matrix Biology 17: 615-623.Google Scholar
LEE, J.-Y., JEONG, W., LIM, W., KIM, J., BAZER, F.W., HAN, J.Y. and SONG, G. (2012) Chicken pleiotrophin: regulation of tissue specific expression by estrogen in the oviduct and distinct expression pattern in the ovarian carcinomas. PloS one 7: e34215.Google Scholar
LEŚNIAK-WALENTYN, A. and HRABIA, A. (2016a) Expression and localisation of matrix metalloproteinases (MMP-2, -7, -9) and their tissue inhibitors (TIMP-2, -3) in the chicken oviduct during maturation. Cell and Tissue Research 364: 185-197.Google Scholar
LEŚNIAK-WALENTYN, A. and HRABIA, A. (2016b) Involvement of matrix metalloproteinases (MMP-2, -7, -9) and their tissue inhibitors (TIMP-2, -3) in the chicken oviduct regression and recrudescence. Cell and Tissue Research 366: 443-454.Google Scholar
LIM, C.H., JEONG, W., LIM, W., KIM, J., SONG, G. and BAZER, F.W. (2012a) Differential expression of select members of the SLC family of genes and regulation of expression by microRNAs in the chicken oviduct. Biology of Reproduction 87: 145.Google Scholar
LIM, W., JEONG, W., KIM, J., KA, H., BAZER, F.W., HAN, J.Y. and SONG, G. (2012b) Differential expression of secreted phosphoprotein 1 in response to estradiol-17beta and in ovarian tumors in chickens. Biochemical and Biophysical Research Communications 422: 494-500.Google Scholar
LIM, W., JEONG, W., KIM, J.-H., LEE, J.-Y., KIM, J., BAZER, F.W., HAN, J.Y. and SONG, G. (2011) Differential expression of alpha 2 macroglobulin in response to dietylstilbestrol and in ovarian carcinomas in chickens. Reproductive Biology and Endocrinology 9: 137.Google Scholar
MAGEED, A.M.A., ISOBE, N. and YOSHIMURA, Y. (2008) Expression of avian beta-defensins in the oviduct and effects of lipopolysaccharide on their expression in the vagina of hens. Poultry Science 87: 979-984.Google Scholar
MAGEED, A.M., ISOBE, N. and YOSHIMURA, Y. (2009) Immunolocalisation of avian beta-defensins in the hen oviduct and their changes in the uterus during eggshell formation. Reproduction 138: 971-978.Google Scholar
MANN, K. (2008) Proteomic analysis of the chicken egg vitelline membrane. Proteomics 8: 2322-2332.Google Scholar
MATSUSHIMA, I. (1958) An undescribed trypsin inhibitor in egg white. Science 127: 1178-1179.Google Scholar
MIKŠÍK, I., SEDLÁKOVÁ, P., LACINOVÁ, K., PATARIDIS, S. and ECKHARDT, A. (2010) Determination of insoluble avian eggshell matrix proteins, in: Analytical and Bioanalytical Chemistry, pp. 205-214.Google Scholar
MINAMI, T., HORIUCHI, K., MIURA, M., ABID, M.R., TAKABE, W., NOGUCHI, N., KOHRO, T., GE, X., ABURATANI, H., HAMAKUBO, T., KODAMA, T. and AIRD, W.C. (2004) Vascular endothelial growth factor- and thrombin-induced termination factor, down syndrome critical region-1, attenuates endothelial cell proliferation and angiogenesis. Journal of Biological Chemistry 279: 50537-50554.Google Scholar
MISHRA, B., KIZAKI, K., SATO, T., ITO, A. and HASHIZUME, K. (2012) The role of extracellular matrix metalloproteinase inducer (EMMPRIN) in the regulation of bovine endometrial cell functions. Biology of Reproduction 87: 149.Google Scholar
MURAMATSU, T., HIRAMOTO, K. and OKUMURA, J-I. (1991) Changes in ovalbumin and protein synthesis in vivo in the magnum of laying hens during the egg formation cycle. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry 99: 141-146.Google Scholar
NYS, Y., BAKER, K. and LAWSON, D.E.M. (1992) Estrogen and a calcium flux dependent factor modulate the calbindin gene expression in the uterus of laying hens. General and Comparative Endocrinology 87: 87-94.Google Scholar
PINES, M., KNOPOV, V. and BAR, A. (1995) Involvement of osteopontin in eggshell formation in the laying chicken. Matrix Biology 14: 765-771.Google Scholar
RATH, N. C., LIYANAGE, R., MAKKAR, S.K. and LAY, J.O. (2017) Protein profiles of hatchery eggshell membrane. Proteome Science 15: 9.Google Scholar
RÉHAULT-GODBERT, S., LABAS, V., HELLOIN, E., HERVÉ-GRÉPINET, V., SLUGOCKI, C., BERGES, M., BOURIN, M.C., BRIONNE, A., POIRIER, J.C., GAUTRON, J., COSTE, F. and NYS, Y. (2013) Ovalbumin-related protein X is a heparin-binding ov-serpin exhibiting antimicrobial activities. Journal of Biological Chemistry 288: 17285-17295.Google Scholar
REYES-GRAJEDA, J.P., MORENO, A. and ROMERO, A. (2004) Crystal structure of ovocleidin-17, a major protein of the calcified Gallus gallus eggshell: implications in the calcite mineral growth pattern. The Journal of Biological Chemistry 279: 40876-40881.Google Scholar
SOCHA, J.K., SECHMAN, A., MIKA, M. and HRABIA, A. (2017) Effect of growth hormone on steroid concentrations and mRNA expression of their receptor, and selected egg-specific protein genes in the chicken oviduct during pause in laying induced by fasting. Domestic Animal Endocrinology 61: 1-10.Google Scholar
SUN, C., XU, G. and YANG, N. (2013) Differential label-free quantitative proteomic analysis of avian eggshell matrix and uterine fluid proteins associated with eggshell mechanical property. Proteomics 13: 3523-3536.Google Scholar
TSUGE, Y., SHIMOYAMADA, M. and WATANABE, K. (1997) Structural features of newcastle disease virus- and anti-ovomucin antibody-binding glycopeptides from pronase-treated ovomucin. Journal of Agricultural and Food Chemistry 45: 2393-2398.Google Scholar
VU, T.H. and WERB, Z. (2000) Matrix metalloproteinases: effectors of development and normal physiology. Genes & Development 14: 2123-2133.Google Scholar
WANG, X., FORD, B.C., PRAUL, C.A. and LEACH, R.M. (2002) Collagen X expression in oviduct tissue during the different stages of the egg laying cycle. Poultry Science 81: 805-808.Google Scholar
WHITE, H.B. and WHITEHEAD, C.C. (1987) Role of avidin and other biotin-binding proteins in the deposition and distribution of biotin in chicken eggs. Discovery of a new biotin-binding protein. The Biochemical Journal 241: 677-684.Google Scholar
WILLEMS, E., DECUYPERE, E., BUYSE, J. and EVERAERT, N. (2014) Importance of albumen during embryonic development in avian species, with emphasis on domestic chicken. World's Poultry Science Journal 70: 503-518.Google Scholar
WOOD-GUSH, D.G.M. and GILBERT, A.B. (1970) The rate of egg loss through internal laying. British Poultry Science 11: 161-163.Google Scholar
YACOUB, H.A., ELAZZAZY, A.M., ABUZINADAH, O.A.H., AL-HEJIN, A.M., MAHMOUD, M.M. and HARAKEH, S.M. (2015) Antimicrobial activities of chicken β-defensin (4 and 10) peptides against pathogenic bacteria and fungi. Frontiers in Cellular and Infection Microbiology 5: 36.Google Scholar
YOSEFI, S., BRAW-TAL, R. and BAR, A. (2003) Intestinal and eggshell calbindin, and bone ash of laying hens as influenced by age and molting. Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology 136: 673-682.Google Scholar
YOSHIMURA, Y., OHASHI, H., SUBEDI, K., NISHIBORI, M. and ISOBE, N. (2006) Effects of age, egg-laying activity, and salmonella-inoculation on the expression of gallinacin mRNA in the vagina of the hen oviduct. Journal of Reproduction and Development 52: 211-218.Google Scholar
ZHAO, J.P., ZHANG, Q., JIAO, H.C., WANG, X.J., JIANG, M.J., LUO, H. and LIN, H. (2016) Ovalbumin expression in the oviduct magnum of hens is related to the rate of egg laying and shows distinct stress-type-specific responses. Journal of Animal Physiology and Animal Nutrition 100: 876-883.Google Scholar
ZHAO, R., XU, G.Y., LIU, Z.Z., LI, J.Y. and YANG, N. (2006) A study on eggshell pigmentation: biliverdin in blue-shelled chickens. Poultry Science 85: 546-549.Google Scholar