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Female Reproductive System and Immunology

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Book cover Avian Reproduction

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1001))

Abstract

Health of the reproductive organs is essential for formation and production of high quality and hygienic eggs. It is of importance to review the structures and functions of female reproductive system for better understanding of the mechanism by which the eggs are formed. The unique functions of ovarian cells for follicular growth and differentiation as well as steroidogenesis and oocyte maturation are regulated by gonadotropins and gonadal steroids. The oviduct is responsible for egg formation, while the unique function to store sperms for a prolonged period takes place in the specific tissue of this organ. The unique innate and adaptive immuno-defense systems that play essential role to prevent infection are developed in the ovary and oviduct. Toll-like receptors (TLRs) that recognize the molecular pattern of microbes and initiate the immunoresponse are expressed in those organs. Avian β-defensins (AvBDs), a member of antimicrobial peptides, are synthesized by the ovarian and oviductal cells. Challenge of those cells by TLR ligands upregulates the expression of proinflammatory cytokines, which in turn stimulate the expression of AvBDs. The adaptive immune system in the ovary and oviduct is also unique, since the migration of lymphocytes is enhanced by estrogens. In contrast to the development of immuno-defense system, spontaneous ovarian cancer and uterine fibroids appear more frequently in chickens than in mammals, and thus chickens could be used as a model for studying these diseases. Thus the avian reproductive organs have unique functions not only for egg formation but also for the immuno-defense system, which is essential for prevention of infection and production of hygienic eggs.

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References

  • Abdel-Mageed AM, Isobe N, Yoshimura Y. Effects of different TLR ligands on the expression of proinflammatory cytokines and avian beta-defensins in the uterine and vaginal tissues of laying hens. Vet Immunol Immunopathol. 2014;162:132–41.

    Article  CAS  PubMed  Google Scholar 

  • Abdel-Mageed AM, Isobe N, Yoshimura Y. Effects of viral-associated molecular patterns on the expression of cathelicidins in the hen vagina. J Poult Sci. 2016;53:240–47.

    Google Scholar 

  • Abdelsalam M, Isobe N, Yoshimura Y. Changes in the localization of immunoreactive avian beta-defensin-8,-10 and-12 in hen ovarian follicles during follicular growth. J Poul Sci. 2010;47:77–84.

    Article  CAS  Google Scholar 

  • Abdelsalam M, Isobe N, Yoshimura Y. Effects of lipopolysaccharide on the expression of proinflammatory cytokines and chemokines and influx of leukocytes in the hen ovary. Poult Sci. 2011;90:2054–62.

    Article  CAS  PubMed  Google Scholar 

  • Abdelsalam M, Isobe N, Yoshimura Y. Effects of lipopolysaccharide and interleukins on the expression of avian beta-defensins in hen ovarian follicular tissue. Poult Sci. 2012;91:2877–84.

    Article  CAS  PubMed  Google Scholar 

  • Ahlborn GJ, Clare DA, Sheldon BW, Kelly RW. Identification of eggshell membrane proteins and purification of ovotransferrin and beta-NAGase from hen egg white. Protein J. 2006;25:71–81.

    Article  CAS  PubMed  Google Scholar 

  • Alexopoulou L, Holt AC, Medzhitov R, Flavell RA. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature. 2001;413:732–8.

    Article  CAS  PubMed  Google Scholar 

  • Ariyadi B, Isobe N, Yoshimura Y. Differences in the mucosal surface barrier formed by mucin in the lower oviductal segments between laying and molting hens. Poult Sci. 2012;91:1173–8.

    Article  CAS  PubMed  Google Scholar 

  • Ariyadi B, Isobe N, Yoshimura Y. Induction of mucin expression by estrogen and lipopolysaccharide in the lower oviductal segments in hens. Poult Sci. 2013a;92:3205–13.

    Article  CAS  PubMed  Google Scholar 

  • Ariyadi B, Isobe N, Yoshimura Y. Expression of tight junction molecule “claudins” in the lower oviductal segments and their changes with egg-laying phase and gonadal steroid stimulation in hens. Theriogenology. 2013b;79:211–8.

    Article  CAS  PubMed  Google Scholar 

  • Ariyadi B, Isobe N, Yoshimura Y. Toll-like receptor signaling for the induction of mucin expression by lipopolysaccharide in the hen vagina. Poult Sci. 2014;93:673–9.

    Article  CAS  PubMed  Google Scholar 

  • Bae HD, Kobayashi M, Horio F, Murai A. Identification of the amino acid residues involved in human IgG transport into egg yolks of Japanese quail (Coturnix japonica). Mol Immunol. 2010;47:1404–10.

    Article  CAS  PubMed  Google Scholar 

  • Bahr JM, Wang SC, Huang MY, Calvo FO. Steroid concentrations in isolated theca and granulosa layers of preovulatory follicles during the ovulatory cycle of the domestic hen. Biol Reprod. 1983;29:326–34.

    Article  CAS  PubMed  Google Scholar 

  • Bakst M, Wishart G, Brillard J. Oviductal sperm selection, transport, and storage in poultry. Poul Sci Rev. 1994;5:117–43.

    Google Scholar 

  • Bar A, Vax E, Hunziker W, Halevy O, Striem S. The role of gonadal hormones in gene expression of calbindin (Mr 28,000) in the laying hen. Gen Comp Endocrinol. 1996;103:115–22.

    Article  CAS  PubMed  Google Scholar 

  • Barnes DM. Bird chimeras may be models for certain neurological diseases. Science. 1986;232:930–2.

    Article  CAS  PubMed  Google Scholar 

  • Barua A, Edassery SL, McNeal S, Bahr JM, Bitterman P, Basu S, Sharma S, Abramowicz JS. Enhancement of ovarian tumor detection by DR6-targeted ultrasound imaging agents in laying hen model of spontaneous ovarian cancer. International Journal of Gynecological Cancer. 2016;26(8):1375–85.

    Google Scholar 

  • Barua A, Yoshimura Y. Effects of aging and sex steroids on the localization of T cell subsets in the ovary of chicken, Gallus domesticus. Gen Comp Endocrinol. 1999a;114:28–35.

    Article  CAS  PubMed  Google Scholar 

  • Barua A, Yoshimura Y. Immunolocalization of MHC-II+ cells in the ovary of immature, young laying and old laying hens Gallus domesticus. J Reprod Fertil. 1999b;116:385–9.

    Article  CAS  PubMed  Google Scholar 

  • Barua A, Yoshimura Y. Ovarian cell-mediated immune response to Salmonella enteritidis infection in laying hens (Gallus domesticus). Poult Sci. 2004;83:997–1002.

    Article  CAS  PubMed  Google Scholar 

  • Barua A, Yoshimura Y, Tamura T. The effects of age and sex steroids on the macrophage population in the ovary of the chicken, Gallus domesticus. J Reprod Fertil. 1998a;114:253–8.

    Article  CAS  PubMed  Google Scholar 

  • Barua A, Yoshimura Y, Tamura T. Effects of ageing and oestrogen on the localization of immunoglobulin-containing cells in the chicken ovary. J Reprod Fertil. 1998b;114:11–6.

    Article  CAS  PubMed  Google Scholar 

  • Barua A, Yoshimura Y, Tamura T. Localization of macrophages in the ovarian follicles during the follicular growth and postovulatory regression in chicken, Gallus domesticus. Poult Sci. 1998c;77:1417–21.

    Article  CAS  PubMed  Google Scholar 

  • Barua A, Michiue H, Yoshimura Y. Changes in the localization of MHC class II positive cells in hen ovarian follicles during the processes of follicular growth, postovulatory regression and atresia. Reproduction. 2001;121:953–7.

    Article  CAS  PubMed  Google Scholar 

  • Barua A, Abramowicz JS, Bahr JM, Bitterman P, Dirks A, Holub KA, Sheiner E, Bradaric MJ, Edassery SL, Luborsky JL. Detection of ovarian tumors in chicken by sonography: a step toward early diagnosis in humans? J Ultrasound Med. 2007a;26:909–19.

    Article  PubMed  Google Scholar 

  • Barua A, Bradaric MJ, Kebede T, Espionosa S, Edassery SL, Bitterman P, Rotmensch J, Luborsky JL. Anti-tumor and anti-ovarian autoantibodies in women with ovarian cancer. Am J Reprod Immunol. 2007b;57:243–9.

    Article  CAS  PubMed  Google Scholar 

  • Barua A, Bitterman P, Abramowicz JS, Dirks AL, Bahr JM, Hales DB, Bradaric MJ, Edassery SL, Rotmensch J, Luborsky JL. Histopathology of ovarian tumors in laying hens: a preclinical model of human ovarian cancer. Int J Gynecol Cancer. 2009a;19:531–9.

    Article  PubMed  PubMed Central  Google Scholar 

  • Barua A, Edassery SL, Bitterman P, Abramowicz JS, Dirks AL, Bahr JM, Hales DB, Bradaric MJ, Luborsky JL. Prevalence of antitumor antibodies in laying hen model of human ovarian cancer. Int J Gynecol Cancer. 2009b;19:500–7.

    Article  PubMed  PubMed Central  Google Scholar 

  • Barua A, Bradaric MJ, Bitterman P, Abramowicz JS, Sharma S, Basu S, Lopez H, Bahr JM. Dietary supplementation of Ashwagandha (Withania somnifera, Dunal) enhances NK cell function in ovarian tumors in the laying hen model of spontaneous ovarian cancer. Am J Reprod Immunol. 2013;70:538–50.

    Article  CAS  PubMed  Google Scholar 

  • Barua A, Yellapa A, Bahr JM, Machado SA, Bitterman P, Basu S, Sharma S, Abramowicz JS. Enhancement of ovarian tumor detection with αvβ3 integrin-targeted ultrasound molecular imaging agent in laying hens: a preclinical model of spontaneous ovarian cancer. Int J Gynecol Cancer. 2014;24:19–28.

    Article  PubMed  Google Scholar 

  • Barua A, Yellapa A, Bahr JM, Machado SA, Bitterman P, Basu S, Sharma S, Abramowicz JS. VEGFR2-targeted ultrasound imaging agent enhances the detection of ovarian tumors at early stage in laying hens, a preclinical model of spontaneous ovarian cancer. Ultrason Imaging. 2015;37:224–37.

    Article  PubMed  Google Scholar 

  • Beyer C, Schett G, Distler O, Distler JH. Animal models of systemic sclerosis: prospects and limitations. Arthritis Rheum. 2010;62:2831–44.

    Article  CAS  PubMed  Google Scholar 

  • Bradaric MJ, Penumatsa K, Barua A, Edassery SL, Yu Y, Abramowicz JS, Bahr JM, Luborsky JL. Immune cells in the normal ovary and spontaneous ovarian tumors in the laying hen (Gallus domesticus) model of human ovarian cancer. PLoS One. 2013;8(9):e74147.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brionne A, Nys Y, Hennequet-Antier C, Gautron J. Hen uterine gene expression profiling during eggshell formation reveals putative proteins involved in the supply of minerals or in the shell mineralization process. BMC Genomics. 2014;15:220. doi:10.1186/1471-2164-15-220.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Brownlie R, Allan B. Avian toll-like receptors. Cell Tissue Res. 2011;343:121–30.

    Article  CAS  PubMed  Google Scholar 

  • Bulet P, Stöcklin R, Menin L. Anti-microbial peptides: from invertebrates to vertebrates. Immunol Rev. 2004;198:169–84.

    Article  CAS  PubMed  Google Scholar 

  • Calvo FO, Bahr JM. Adenylyl cyclase system of the small preovulatory follicles of the domestic hen: responsiveness to follicle-stimulating hormone and luteinizing hormone. Biol Reprod. 1983;29:542–7.

    Article  CAS  PubMed  Google Scholar 

  • Chousalkar KK, Roberts JR. Ultrastructural study of infectious bronchitis virus infection in infundibulum and magnum of commercial laying hens. Vet Microbiol. 2007;122:223–36.

    Article  CAS  PubMed  Google Scholar 

  • Corradino RA. Calbindin D28K regulation in precociously matured chick egg shell gland in vitro. Gen Comp Endocrinol. 1993;91:158–66.

    Article  CAS  PubMed  Google Scholar 

  • Craig-Schmidt MC, Faircloth SA, Teer PA, Weete JD, Wu CY. The essential fatty acid deficient chicken as a model for cystic fibrosis. Am J Clin Nutr. 1986;44:816–24.

    CAS  PubMed  Google Scholar 

  • Cuperus T, Coorens M, Van Dijk A, Haagsman HP. Avian host defense peptides. Dev Comp Immunol. 2013;41:352–69.

    Article  CAS  PubMed  Google Scholar 

  • Davison TF. The immunologists' debt to the chicken. Br Poult Sci. 2003;44:6–21.

    Article  CAS  PubMed  Google Scholar 

  • De Buck J, Van Immerseel F, Haesebrouck F, Ducatelle R. Colonization of the chicken reproductive tract and egg contamination by Salmonella. J Appl Microbiol. 2004;97:233–45.

    Article  CAS  PubMed  Google Scholar 

  • De Zoete MR, Bouwman LI, Keestra AM, Van Putten JPM. Cleavage and activation of a Toll-like receptor by microbial proteases. Proc Natl Acad Sci U S A. 2011;108:4968–73.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du JW, Hincke MT, Rose-Martel M, Hennequet-Antier C, Brionne A, Cogburn LA, Nys Y, Gautron J. Identifying specific proteins involved in eggshell membrane formation using gene expression analysis and bioinformatics. BMC Genomics. 2015;16:792.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Elis S, Batellier F, Couty I, Balzergue S, Martin-Magniette ML, Monget P, Blesbois E, Govoroun MS. Search for the genes involved in oocyte maturation and early embryo development in the hen. BMC Genomics. 2008;9:110.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Forster C. Tight junctions and the modulation of barrier function in disease. Histochem Cell Biol. 2008;130:55–70.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fredrickson TN. Ovarian tumors of the hen. Environ Health Perspect. 1987;73:35–51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujii S, Tamura T. Location of sperms in the oviduct of the domestic fowl with special reference to storage of sperms in the vaginal gland. J Fac Fish Anim Husb, Hiroshima Univ. 1963;5:145–63.

    Google Scholar 

  • Gautron J, Murayama E, Vignal A, Morisson M, Mckee MD, Rehault S, Labas V, Belghazi M, Vidal ML, Nys Y, Hincke MT. Cloning of ovocalyxin-36, a novel chicken eggshell protein related to lipopolysaccharide-binding proteins, bactericidal permeability-increasing proteins, and plunc family proteins. J Biol Chem. 2007;282:5273–86.

    Article  CAS  PubMed  Google Scholar 

  • Gong DQ, Wilson PW, Bain MM, Mcdade K, Kalina J, Herve-Grepinet V, Nys Y, Dunn IC. Gallin; an antimicrobial peptide member of a new avian defensin family, the ovodefensins, has been subject to recent gene duplication. BMC Immunol. 2010;11:12.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hakim AA, Barry CP, Barnes HJ, Anderson KE, Petitte J, Whitaker R, Lancaster JM, Wenham RM, Carver DK, Turbov J, Berchuck A, Kopelovich L, Rodriguez GC. Ovarian adenocarcinomas in the laying hen and women share similar alterations in p53, ras, and HER-2/neu. Cancer Prevention Research. 2009;2(2):114–21.

    Google Scholar 

  • Hincke MT, Gautron J, Panheleux M, Garcia-Ruiz J, Mckee MD, Nys Y. Identification and localization of lysozyme as a component of eggshell membranes and eggshell matrix. Matrix Biol. 2000;19:443–53.

    Article  CAS  PubMed  Google Scholar 

  • Jackson JA, Friberg AC, Bahr JM. Preovulatory changes in glycosaminoglycans and collagen content in the stigma region of the follicle of the domestic hen. Biol Reprod. 1991;45:301–7.

    Article  CAS  PubMed  Google Scholar 

  • Jackson E, Anderson K, Ashwell C, Petitte J, Mozdziak PE. CA125 expression in spontaneous ovarian adenocarcinomas from laying hens. Gynecol Oncol. 2007;104:192–8.

    Article  CAS  PubMed  Google Scholar 

  • Johnson AL. Reproduction in the female. In: Whittow GG, editor. Sturkie’s avian physiology. 5th ed. San Diego: Academic Press; 2000. p. 569–96.

    Chapter  Google Scholar 

  • Johnson AL. Ovarian follicle selection and granulosa cell differentiation. Poult Sci. 2015;94:781–5.

    Article  CAS  PubMed  Google Scholar 

  • Jonchère V, Brionne A, Gautron J, Nys Y. Identification of uterine ion transporters for mineralisation precursors of the avian eggshell. BMC Physiol. 2012;12:10.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jung JG, Park TS, Kim JN, Han BK, Lee SD, Song G, Han JY. Characterization and application of oviductal epithelial cells in vitro in Gallus domesticus. Biol Reprod. 2011;85:798–807.

    Article  CAS  PubMed  Google Scholar 

  • Kadono H, Yamade T. Changes of body temperature related to oviposition and ovulation induced by LH in the domestic hen. Nihon Juigaku Zasshi. 1985;47:55–61.

    Article  CAS  PubMed  Google Scholar 

  • Keestra AM, De Zoete MR, Van Aubel RA, Van Putten JP. The central leucine-rich repeat region of chicken TLR16 dictates unique ligand specificity and species-specific interaction with TLR2. J Immunol. 2007;178:7110–9.

    Article  CAS  PubMed  Google Scholar 

  • Khan MF, Bahr JM, Yellapa A, Bitterman P, Abramowicz JS, Edassery SL, Basu S, Rotmensch J, Barua A. Expression of leukocyte inhibitory immunoglobulin-like transcript 3 receptors by ovarian tumors in laying hen model of spontaneous ovarian cancer. Transl Oncol. 2012;5:85–91.

    Article  PubMed  PubMed Central  Google Scholar 

  • Koike TI, Shimada K, Cornett LE. Plasma levels of immunoreactive mesotocin and vasotocin during oviposition in chickens: relationship to oxytocic action of the peptides in vitro and peptide interaction with myometrial membrane binding sites. Gen Comp Endocrinol. 1988;70:119–26.

    Article  CAS  PubMed  Google Scholar 

  • Kunnas TA, Joensuu TK, Viitala KK, Sopanen P, Tuohimaa P, Kulomaa MS. Induction of avidin messenger-ribonucleic-acid in the chick oviduct by progesterone and other steroids. Endocrinology. 1992;130:3421–6.

    Article  CAS  PubMed  Google Scholar 

  • Lee SI, Ji MR, Jang YJ, Jeon MH, Kim JS, Park JK, Jeon IS, Byun SJ. Characterization and miRNA-mediated posttranscriptional regulation of vitelline membrane outer layer protein I in the adult chicken oviduct. In Vitro Cell Dev Biol Anim. 2015;51:222–9.

    Article  CAS  Google Scholar 

  • Lillpers K, Wilhelmson M. Age-dependent changes in oviposition pattern and egg production traits in the domestic hen. Poult Sci. 1993;72:2005–11.

    Article  CAS  PubMed  Google Scholar 

  • Lim W, Jeong W, Kim J, Yoshimura Y, Bazer FW, Han JY, Song G. Expression and regulation of β-defensin 11 in the oviduct in response to estrogen and in ovarian tumors of chickens. Mol Cell Endocrinol. 2013;366:1–8.

    Article  CAS  PubMed  Google Scholar 

  • Linden SK, Sutton P, Karlsson NG, Korolik V, McGuckin MA. Mucin in the mucosal barrier to infection. Mucosal Immunol. 2008;1:183–97.

    Article  CAS  PubMed  Google Scholar 

  • Machado SA, Bahr JM, Hales DB, Braundmeier AG, Quade BJ, Nowak RA. Validation of the aging hen (Gallus gallus domesticus) as an animal model for uterine leiomyomas. Biol Reprod. 2012;87:86.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mageed AMA, Isobe N, Yoshimura Y. Expression of avian beta-defensins in the oviduct and effects of lipopolysaccharide on their expression in the vagina of hens. Poult Sci. 2008;87:979–84.

    Article  PubMed  CAS  Google Scholar 

  • Mageed AMA, Isobe N, Yoshimura Y. Immunolocalization of avian beta-defensins in the hen oviduct and their changes in the uterus during eggshell formation. Reproduction. 2009;138:971–8.

    Article  PubMed  CAS  Google Scholar 

  • Mageed AMA, Isobe N, Yoshimura Y. Changes in the density of immunoreactive avian β-Defensin-3 and-11 in the hen uterus in response to lipopolysaccharide inoculation. Poult Sci. 2011;48:73–7.

    Article  CAS  Google Scholar 

  • Marie P, Labas V, Brionne A, Harichaux G, Hennequet-Antier C, Nys Y, Gautron J. Data set for the proteomic inventory and quantitative analysis of chicken uterine fluid during eggshell biomineralization. Data Brief. 2014;1:65–9.

    Article  PubMed  PubMed Central  Google Scholar 

  • Michailidis G, Theodoridis A, Avdi M. Transcriptional profiling of Toll-like receptors in chicken embryos and in the ovary during sexual maturation and in response to Salmonella enteritidis infection. Anim Reprod Sci. 2010;122:294–302.

    Article  CAS  PubMed  Google Scholar 

  • Michailidis G, Theodoridis A, Avdi M. Effects of sexual maturation and Salmonella infection on the expression of Toll-like receptors in the chicken vagina. Anim Reprod Sci. 2011;123:234–41.

    Article  CAS  PubMed  Google Scholar 

  • Michailidis G, Avdi M, Argiriou A. Transcriptional profiling of antimicrobial peptides avian beta-defensins in the chicken ovary during sexual maturation and in response to Salmonella enteritidis infection. Res Vet Sci. 2012;92:60–5.

    Article  CAS  PubMed  Google Scholar 

  • Mine Y, Oberle C, Kassify Z. Eggshell matrix proteins as defense mechanism of avian eggs. J Agric Food Chem. 2003;51:249–53.

    Article  CAS  PubMed  Google Scholar 

  • Mori M, Yamashita M, Yoshikuni M, Fukada S, Nagahama Y. Maturation-promoting factor and P34cdc2 kinase during oocyte maturation of the Japanese quail. Dev Biol. 1991;146:246–9.

    Article  CAS  PubMed  Google Scholar 

  • Murai A, Murota R, Doi K, Yoshida T, Aoyama H, Kobayashi M, Horio F. Avian IgY is selectively incorporated into the egg yolks of oocytes by discriminating Fc amino acid residues located on the C upsilon 3/C upsilon 4 interface. Dev Comp Immunol. 2013;39:378–87.

    Article  CAS  PubMed  Google Scholar 

  • Murdoch WJ. Ovulatory factor in ovarian carcinogenesis. Adv Exp Med Biol. 2008;622:119–28.

    Article  CAS  PubMed  Google Scholar 

  • Nap AW, Dunselman GA, de Goeij AF, Evers JL, Groothuis PG. Inhibiting MMP activity prevents the development of endometriosis in the chicken chorioallantoic membrane model. Hum Reprod. 2004;19:2180–7.

    Article  CAS  PubMed  Google Scholar 

  • Nerren JR, He HQ, Genovese K, Kogut MH. Expression of the avian-specific toll-like receptor 15 in chicken heterophils is mediated by Gram-negative and Gram-positive bacteria, but not TLR agonists. Vet Immunol Immunopathol. 2010;136:151–6.

    Article  CAS  PubMed  Google Scholar 

  • Netea MG, Joosten LA, Latz E, Mills KH, Natoli G, Stunnenberg HG, O'Neill LA, Xavier RJ. Trained immunity: a program of innate immune memory in health and disease. Science. 2016;352:aaf1098.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nii T, Sonoda Y, Isobe N, Yoshimura Y. Effects of lipopolysaccharide on the expression of proinflammatory cytokines and chemokines and the subsequent recruitment of immunocompetent cells in the oviduct of laying and molting hens. Poult Sci. 2011;90:2332–41.

    Article  CAS  PubMed  Google Scholar 

  • Nii T, Isobe N, Yoshimura Y. Effects of repeated lipopolysaccharide stimulation on the development of antigen-presenting cells and T cells pool in hen vagina. Poult Sci. 2013;50:83–9.

    Article  CAS  Google Scholar 

  • Nii T, Isobe N, Yoshimura Y. Effects of avian infectious bronchitis virus antigen on eggshell formation and immunoreaction in hen oviduct. Theriogenology. 2014;81:1129–38.

    Article  CAS  PubMed  Google Scholar 

  • Nii T, Isobe N, Yoshimura Y. The effect of estrogen on the early cytotoxic response to IB virus infection in hen oviduct. Vet Immunol Immunopathol. 2015;164:56–66.

    Article  CAS  PubMed  Google Scholar 

  • Nishio S, Kohno Y, Iwata Y, Arai M, Okumura H, Oshima K, Nadano D, Matsuda T. Glycosylated chicken ZP2 accumulates in the egg coat of immature oocytes and remains localized to the germinal disc region of mature eggs. Biol Reprod. 2014;91:107.

    Article  PubMed  CAS  Google Scholar 

  • Nitta H, Osawa Y, Bahr JM. Multiple steroidogenic cell populations in the thecal layer of preovulatory follicles of the chicken ovary. Endocrinology. 1991;129:2033–340.

    Article  CAS  PubMed  Google Scholar 

  • Ohashi H, Subedi K, Nishibori M, Isobe N, Yoshimura Y. Expressions of antimicrobial peptide gallinacin-1,-2 and −3 mRNAs in the oviduct of laying hens. Poult Sci. 2005;42:337–45.

    Article  CAS  Google Scholar 

  • Ozoe A, Isobe N, Yoshimura Y. Expression of Toll-like receptors (TLRs) and TLR4 response to lipopolysaccharide in hen oviduct. Vet Immunol Immunopathol. 2009;127:259–68.

    Article  CAS  PubMed  Google Scholar 

  • Poland AL, Sheldon BW. Altering the thermal resistance of foodborne bacterial pathogens with an eggshell membrane waste by-product. J Food Prot. 2001;64:486–92.

    Article  CAS  PubMed  Google Scholar 

  • Promkuntod N, Antarasena C, Prommuang P, Prommuang P. Isolation of avian influenza virus A subtype H5N1 from internal contents (albumen and allantoic fluid) of Japanese quail (Coturnix Coturnix japonica) eggs and oviduct during a natural outbreak. Ann N Y Acad Sci. 2006;1081:171–3.

    Article  PubMed  Google Scholar 

  • Qin N, Fan XC, Zhang YY, Xu XX, Tyasi TL, Jing Y, Mu F, Wei ML, Xu RF. New insights into implication of the SLIT/ROBO pathway in the prehierarchical follicle development of hen ovary. Poult Sci. 2015;94:2235–346.

    Article  CAS  PubMed  Google Scholar 

  • Rangel PL, Gutierrez CG. Reproduction in hens: is testosterone necessary for the ovulatory process? Gen Comp Endocrinol. 2014;203:250–61.

    Article  CAS  PubMed  Google Scholar 

  • Roach JC, Glusman G, Rowen L, Kaur A, Purcell MK, Smith KD, Hood LE, Aderem A. The evolution of vertebrate Toll-like receptors. Proc Natl Acad Sci U S A. 2005;102:9577–82.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rzasa J. The effect of arginine vasotocin on prostaglandin production of the hen uterus. Gen Comp Endocrinol. 1984;53:260–3.

    Article  CAS  PubMed  Google Scholar 

  • Saito N, Sato K, Shimada K. Prostaglandin levels in peripheral and follicular plasma, the isolated theca and granulosa layers of pre- and postovulatory follicles, and the myometrium and mucosa of the shell gland (uterus) during a midsequence-oviposition of the hen (Gallus domesticus). Biol Reprod. 1987;36:89–96.

    Article  CAS  PubMed  Google Scholar 

  • Schneider WJ. Vitellogenin receptors: oocyte-specific members of the low-density lipoprotein receptor supergene family. Int Rev Cytol. 1996;166:103–37.

    Article  CAS  PubMed  Google Scholar 

  • Shimada K, Saito N, Itogawa K, Koike TI. Changes in plasma concentrations of arginine vasotocin after intrauterine injections of prostaglandin F-2 alpha and acetylcholine at various times during the oviposition cycle of the domestic hen (Gallus domesticus). J Reprod Fertil. 1987;80:143–50.

    Article  CAS  PubMed  Google Scholar 

  • Shin K, Yamauchi K, Teraguchi S, Hayasawa H, Imoto I. Susceptibility of Helicobacter pylori and its urease activity to the peroxidase–hydrogen peroxide–thiocyanate antimicrobial system. J Med Microbiol. 2002;51:231–7.

    Article  CAS  PubMed  Google Scholar 

  • Short ML, Nickel J, Schmitz A, Renkawitz R. Lysozyme gene expression and regulation. Experientia. 1996;75:243–57.

    CAS  Google Scholar 

  • Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA Cancer J Clin. 2014;64:9–29.

    Article  PubMed  Google Scholar 

  • Sonoda Y, Mageed AMA, Isobe N, Yoshimura Y. Induction of avian beta-defensins by CpG oligodeoxynucleotides and proinflammatory cytokines in hen vaginal cells in vitro. Reproduction. 2013;145:621–31.

    Article  CAS  PubMed  Google Scholar 

  • St Paul M, Brisbin JT, Abdul-Careem MF, Sharif S. Immunostimulatory properties of Toll-like receptor ligands in chickens. Vet Immunol Immunopathol. 2013;152:191–9.

    Article  CAS  PubMed  Google Scholar 

  • Stammer K, Edassery SL, Barua A, Bitterman P, Bahr JM, Hales DB, Luborsky JL. Selenium-binding protein 1 expression in ovaries and ovarian tumors in the laying hen, a spontaneous model of human ovarian cancer. Gynecol Oncol. 2008;109:115–21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Subedi K, Isobe N, Nishibori M, Yoshimura Y. Changes in the expression of toll-like receptor mRNAs during follicular growth and in response to lipopolysaccharide in the ovarian follicles of laying hens. J Reprod Dev. 2007;53:1227–35.

    Article  CAS  PubMed  Google Scholar 

  • Subedi K, Isobe N, Yoshimura Y. Changes in the localization of immunoreactive avian beta-defensin-12 in ovarian follicles during follicular growth and in response to lipopolysaccharide. Poult Sci. 2008;45:210–4.

    Article  CAS  Google Scholar 

  • Sundaresan NR, Saxena VK, Sastry KV, Nagarajan K, Jain P, Singh R, Anish D, Ravindra PV, Saxena M, Ahmed KA. Cytokines and chemokines in postovulatory follicle regression of domestic chicken (Gallus gallus domesticus). Dev Comp Immunol. 2008;32:253–64.

    Article  CAS  PubMed  Google Scholar 

  • Taizi M, Deutsch VR, Leitner A, Ohana A, Goldstein RS. A novel and rapid in vivo system for testing therapeutics on human leukemias. Exp Hematol. 2006;34:1698–708.

    Article  CAS  PubMed  Google Scholar 

  • Takahashi T, Kawashima M, Kamiyoshi M, Tanaka K. Arginine vasotocin receptor-binding in the hen uterus (shell gland) before and after oviposition. Eur J Endocrinol. 1994;130:366–72.

    Article  CAS  PubMed  Google Scholar 

  • Takahashi T, Tajima H, Nakagawa-Mizuyachi K, Nakayama H, Kawashima M. Changes in prostaglandin F2alpha receptor bindings in the hen oviduct uterus before and after oviposition. Poult Sci. 2011;90:1767–73.

    Article  CAS  PubMed  Google Scholar 

  • Takata T, Liang J, Nakano H, Yoshimura Y. Invasion of Salmonella enteritidis in the tissues of reproductive organs in laying Japanese quail: an immunocytochemical study. Poult Sci. 2003;82:1170–3.

    Article  CAS  PubMed  Google Scholar 

  • Temperley ND, Berlin S, Paton IR, Griffin DK, Burt DW. Evolution of the chicken Toll-like receptor gene family: a story of gene gain and gene loss. BMC Genomics. 2008;9:62.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tojo H, Fujii M, Ogawa K. Proteolytic-enzymes and gonadal-hormones of the ovarian follicle wall during ovulation in the domestic-fowl (Gallus-Domesticus). J Reprod Fertil. 1982;64:73–7.

    Article  CAS  PubMed  Google Scholar 

  • Van Dijk A, Veldhuizen EJ, Haagsman HP. Avian defensins. Vet Immunol Immunopathol. 2008;124:1–18.

    Article  CAS  PubMed  Google Scholar 

  • Wales AD, Davies RH. A critical review of Salmonella Typhimurium infection in laying hens. Avian Pathol. 2011;40:429–36.

    Article  CAS  PubMed  Google Scholar 

  • Wellman-Labadie O, Picman J, Hincke MT. Antimicrobial activity of cuticle and outer eggshell protein extracts from three species of domestic birds. Br Poult Sci. 2008;49:133–43.

    Article  CAS  PubMed  Google Scholar 

  • Withanage GS, Sasai K, Fukata T, Miyamoto T, Lillehoj HS, BABA E. Increased lymphocyte subpopulations and macrophages in the ovaries and oviducts of laying hens infected with Salmonella enterica serovar Enteritidis. Avian Pathol. 2003;32:583–90.

    Article  CAS  PubMed  Google Scholar 

  • Woods DC, Schorey JS, Johnson AL. Toll-like receptor signaling in hen ovarian granulosa cells is dependent on stage of follicle maturation. Reproduction. 2009;137:987–96.

    Article  CAS  PubMed  Google Scholar 

  • Xiao YJ, Hughes AL, Ando J, Matsuda Y, Cheng JF, Skinner-Noble D, Zhang GL. A genome-wide screen identifies a single beta-defensin gene cluster in the chicken: implications for the origin and evolution of mammalian defensins. BMC Genomics. 2004;5(1):56.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yoshimura Y. Avian β-defensins expression for the innate immune system in hen reproductive organs. Poult Sci. 2015;94:804–9.

    Article  CAS  PubMed  Google Scholar 

  • Yoshimura Y, Bahr JM. Localization of progesterone receptors in pre- and postovulatory follicles of the domestic hen. Endocrinology. 1991;128:323–30.

    Article  CAS  PubMed  Google Scholar 

  • Yoshimura Y, Koga O. Ultrastructural changes of the stigma of the follicle during the process of ovulation in the hen. Cell Tissue Res. 1982;224:349–59.

    Article  CAS  PubMed  Google Scholar 

  • Yoshimura Y, Okamoto T. Phagocytosis of carbon particles by theca interna fibroblasts in hen ovary. Japanese Poult Sci. 1998;35:314–8.

    Article  CAS  Google Scholar 

  • Yoshimura Y, Tanaka K, Koga O. Studies on the contractility of follicular wall with special reference to the mechanism of ovulation in hens. Br Poult Sci. 1983;24:213–8.

    Article  CAS  PubMed  Google Scholar 

  • Yoshimura Y, Chang C, Okamoto T, Tamura T. Immunolocalization of androgen receptor in the small, preovulatory, and postovulatory follicles of laying hens. Gen Comp Endocrinol. 1993a;91:81–9.

    Article  CAS  PubMed  Google Scholar 

  • Yoshimura Y, Okamoto T, Tamura T. Ultrastructural changes of oocyte and follicular wall during oocyte maturation in the Japanese quail (Coturnix Coturnix japonica). J Reprod Fertil. 1993b;97:189–96.

    Article  CAS  PubMed  Google Scholar 

  • Yoshimura Y, Okamoto T, Tamura T. Electron microscope observations on LH-induced oocyte maturation in Japanese quail (Coturnix Coturnix japonica). J Reprod Fertil. 1993c;98:401–7.

    Google Scholar 

  • Yoshimura Y, Okamoto T, Tamura T. Changes in localization of ovarian immunoreactive estrogen receptor during follicular development in hens. Gen Comp Endocrinol. 1995;100:368–74.

    Article  CAS  PubMed  Google Scholar 

  • Yoshimura Y, Okamoto T, Tamura T. Localisation of MHC class II, lymphocytes and immunoglobulins in the oviduct of laying and moulting hens. Br Poult Sci. 1997;38:590–6.

    Article  CAS  PubMed  Google Scholar 

  • Yoshimura Y, Mizuguchi M, Fujii M, Isobe N. Enzyme histochemical localization of peroxidase activity in the oviduct of immature laying and non-laying hens. Poult Sci. 2006a;43:401–7.

    Article  CAS  Google Scholar 

  • Yoshimura Y, Ohashi H, Subedi K, Nishibori M, Isobe N. Effects of age, egg-laying activity, and Salmonella inoculation on the expressions of gallinacin mRNA in the vagina of the hen oviduct. J Reprod Dev. 2006b;52:211–8.

    Article  CAS  PubMed  Google Scholar 

  • Yu Y, Edassery SL, Barua A, Abramowicz JS, Bahr JM, Hellstrom I, Luborsky JL. The hen model of human ovarian cancer develops anti-mesothelin autoantibodies in response to mesothelin-expressing tumors. J Ovarian Res. 2011;4:12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng WM, Yoshimura Y. Localization of macrophages in the chicken oviduct: effects of age and gonadal steroids. Poult Sci. 1999;78:1014–8.

    Article  CAS  PubMed  Google Scholar 

  • Zheng WM, Yoshimura Y, Tamura T. Effects of age and gonadal steroids on the localization of antigen-presenting cells, and T and B cells in the chicken oviduct. J Reprod Fertil. 1998;114:45–54.

    Article  CAS  PubMed  Google Scholar 

  • Zheng WM, Izaki J, Furusawa S, Yoshimura Y. Localization of immunoglobulin G gamma-chain mRNA-expressing cells in the oviduct of laying and diethylstilbestrol-treated immature hens. Gen Comp Endocrinol. 2000;120:345–52.

    Article  CAS  PubMed  Google Scholar 

  • Zhu GY, Kang L, Wei QQ, Cui XX, Wang SZ, Chen YX, Jiang YL. Expression and regulation of MMP1, MMP3, and MMP9 in the chicken ovary in response to gonadotropins, sex hormones, and TGFB1. Biol Reprod. 2014;90(3):57.

    Article  PubMed  CAS  Google Scholar 

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Yoshimura, Y., Barua, A. (2017). Female Reproductive System and Immunology. In: Sasanami, T. (eds) Avian Reproduction. Advances in Experimental Medicine and Biology, vol 1001. Springer, Singapore. https://doi.org/10.1007/978-981-10-3975-1_3

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