Skip to main content

Regulation of egg formation in the oviduct of laying hen

  • N. SAH (a1) and B. MISHRA (a1)

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.

Corresponding author
Corresponding author:
Hide All
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.
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.
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.
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.
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.
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.
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.
CHIEN, Y.C., HINCKE, M.T. and MCKEE, M.D. (2008) Avian eggshell structure and osteopontin. In: Cells Tissues Organs, pp. 38-43.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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).
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
KITAMOTO, T., NAKASHIMA, M. and IKAI, A. (1982) Hen egg white ovomacroglobulin has a protease inhibitory activity. Journal of Biochemistry 92: 1679-1682.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
MANN, K. (2008) Proteomic analysis of the chicken egg vitelline membrane. Proteomics 8: 2322-2332.
MATSUSHIMA, I. (1958) An undescribed trypsin inhibitor in egg white. Science 127: 1178-1179.
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.
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.
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.
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.
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.
PINES, M., KNOPOV, V. and BAR, A. (1995) Involvement of osteopontin in eggshell formation in the laying chicken. Matrix Biology 14: 765-771.
RATH, N. C., LIYANAGE, R., MAKKAR, S.K. and LAY, J.O. (2017) Protein profiles of hatchery eggshell membrane. Proteome Science 15: 9.
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.
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.
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.
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.
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.
VU, T.H. and WERB, Z. (2000) Matrix metalloproteinases: effectors of development and normal physiology. Genes & Development 14: 2123-2133.
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.
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.
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.
WOOD-GUSH, D.G.M. and GILBERT, A.B. (1970) The rate of egg loss through internal laying. British Poultry Science 11: 161-163.
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.
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.
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.
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.
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.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

World's Poultry Science Journal
  • ISSN: 0043-9339
  • EISSN: 1743-4777
  • URL: /core/journals/world-s-poultry-science-journal
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed