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Reproductive success of males of the ICR outbred line during propagation against the background of antigenic stimulation

  • Developmental Physiology
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Abstract

Diversity of viruses, bacteria, microscopic fungi, and endo- and ectoparasites is an inevitable environmental factor that influences the host reproduction and that is determined not only by negative effects of infectious diseases but also by activation of protective mechanisms, which provide a confrontation to the pressure of parasites. In the present work, hemocyanin was injected into males of the ICR outbred line in order to study reproductive consequences of antigenic stimulation of males. Intact females were added to control and antigen-stimulated males at the initial stage of antibody formation. During 6 days of combined keeping, a significantly greater amount of ovulated egg cells and living embryos were registered in the females added to males that were injected with hemocyanin compared with that theoretically expected for equal reproductive yield. Females covered by antigen-stimulated males bred larger embryos compared with those in the control. Indices of female fertility depended on prevalence of cellular (Th1) or humoral (Th2) immune responses in antigen-stimulated males. Shift of Th1/Th2 balance resulted in higher preimplantation embryonic losses in females covered by males with a prevalence of cellular immune response; however, they bred larger embryos. Thus, it was established that activation of the immune system in males does not influence their reproductive abilities. This allows us, on the one hand, to explain the contribution of protective reactions of the organism in the increase in fertility of the mammals that inhabit territories with high specific abundance of parasites; on the other hand, it demonstrates new ways of the management of the reproduction of animals bred under human control.

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References

  • Arakawa, H., Arakawa, K., and Deak, T., Acute Illness Induces the Release of Aversive Odor Cues from Adult, but not Prepubertal, Male Rats and Suppresses Social Investigation by Conspecifics, Behav. Neurosci., 2009, vol. 123, no. 5, pp. 964–78.

    Article  PubMed  CAS  Google Scholar 

  • Arakawa, H., Arakawa, K., and Deak, T., Sickness-Related Odor Communication Signals as Determinants of Social Behavior in Rat: A Role for Inflammatory Processes, Horm. Behav., 2010, vol. 57, no. 3, pp. 330–341.

    Article  PubMed  CAS  Google Scholar 

  • Arteaga-Silva, M., Vargas-Villavicencio, J.A., Vigueras-Villaseñor, R.M., et al., Taenia crassiceps Infection Disrupts Estrous Cycle and Reproductive Behavior in BALB/C Female Mice, Acta Trop., 2009, vol. 109, no. 2, pp. 141–145.

    Article  PubMed  Google Scholar 

  • Benfield, D.A., Nelson, E., Collins, J.E., et al., Characterization of Swine Infertility and Respiratory Syndrome (SIRS) Virus (Isolate ATCC VR-2332), J. Vet Diagn. Invest., 1992, vol. 4, no. 2, pp. 127–133.

    Article  PubMed  CAS  Google Scholar 

  • Billington, W.D., Influence of Immunological Dissimilarity of Mother and Foetus on Size of Placenta in Mice, Nature, 1964, vol. 202, pp. 317–318.

    Article  PubMed  CAS  Google Scholar 

  • Clarke, A.G., The Effects of Maternal Pre-Immunization on Pregnancy in the Mouse, J. Reprod. Fertil., 1971, vol. 24, no. 3, pp. 369–375.

    Article  PubMed  CAS  Google Scholar 

  • Cunningham, A.F. and Toellner, K.M., Rapid Development of Th2 Activity during T Cell Priming, Clin. Dev. Immunol., 2003, vol. 10, no. 1, pp. 1–6.

    Article  PubMed  CAS  Google Scholar 

  • Deter, J., Chaval, Y., Galan, M., Berthier, K., Salvador, A.R., Casanova, Garcia, J.C., Morand, S., Cosson, J.F., and Charbonnel, N., Linking Demography and Host Dispersal to Trichuris arvicolae Distribution in a Cyclic Vole Species, Int. J. Parasitol., 2007, vol. 37, no. 7, pp. 813–824.

    Article  PubMed  Google Scholar 

  • Faivre, B., Gregoire, A., Preault, M., et al., Immune Activation Rapidly Mirrored in a Secondary Sexual Trait, Science, 2003, vol. 300, p. 103.

    Article  PubMed  CAS  Google Scholar 

  • Feore, S.M., Bennett, M., Chantrey, J., et al., The Effect of Cowpox Virus Infection on Fecundity in Bank Voles and Wood Mice, Proc. Biol. Sci., 1997, vol. 22, no. 264, pp. 1457–1461.

    Article  Google Scholar 

  • Fichorova, R.N., Impact of T. vaginalis Infection on Innate Immune Responses and Reproductive Outcome, J. Reprod. Immunol., 2009, vol. 83, nos. 1–2, pp. 185–189.

    Article  PubMed  CAS  Google Scholar 

  • Fietta, P. and Delsante, G., Focus on Human Natural Killer Cells, Riv. Biol., 2009, vol. 102, no. 2, pp. 219–235.

    PubMed  Google Scholar 

  • Fitzgerald, N.A. and Shellam, G.R., Host Genetic Influences on Fetal Susceptibility to Murine Cytomegalovirus after Maternal or Fetal Infection, J. Infect. Dis., 1991, vol. 163, no. 2, pp. 276–281.

    Article  PubMed  CAS  Google Scholar 

  • Garamszegi, L.Z., Török, J., Michl, G., et al., Female Survival, Lifetime Reproductive Success and Mating Status in a Passerine Bird, Oecologia, 2004, vol. 138, no. 1, pp. 48–56.

    Article  PubMed  Google Scholar 

  • Garraud, O., Perraut, R., Riveau, G., and Nutman, T.B., Class and Subclass Selection in Parasite-Specific Antibody Responses, Trends. Parasitol., 2003, vol. 19, no. 7, pp. 300–304.

    Article  PubMed  CAS  Google Scholar 

  • Gerlinskaya, L.A., Moshkin, M.P., and Evsikov, V.I., Allogenic Stimulation in Early Pregnancy Improves Pre- and Postnatal Ontogenesis in BALB.cLac Mice, J. Reprod. Develop., 2000, vol. 46, no. 6, pp. 387–396.

    Article  CAS  Google Scholar 

  • Goldbard, S.B., Verbanac, K.M., and Warner, C.M., Role of the H-2 Complex in Preimplantation Mouse Embryo Development, Biol. Reprod., 1982, vol. 26, no. 4, pp. 591–596.

    Article  PubMed  CAS  Google Scholar 

  • Guégan, J.F., Thomas, F., Hochberg, M.E., et al., Disease Diversity and Human Fertility, Evolution, 2001, vol. 55, no. 7, pp. 1308–1314.

    PubMed  Google Scholar 

  • Hetherington, C.M. and Humber, D.P., The Effects of Active Immunization of the Decidual Cell Reaction and Ectopic Blastocyst Development in Mice, J. Reprod. Fertil., 1975, vol. 43, no. 2, pp. 333–336.

    Article  PubMed  CAS  Google Scholar 

  • Hetherington, C.M., Absence of Effect of Maternal Immunization to Paternal Antigens on Placental Weight, Fetal Weight and Litter Size in the Mouse, J. Reprod. Fertil., 1978, vol. 53, no. 1, pp. 81–84.

    Article  PubMed  CAS  Google Scholar 

  • Ho, H.N., Yang, Y.S., Hsieh, R.P., Lin, H.R., Chen, S.U., Chen, H.F., Huang, S.C., Lee, T.Y., and Gill, T.J., Sharing of Human Leukocyte Antigens in Couples with Unexplained Infertility Affects the Success of in vitro Fertilization and Tubal Embryo Transfer, Am. J. Obstet. Gynecol., 1994, vol. 170, pp. 63–71.

    PubMed  CAS  Google Scholar 

  • James, D.A., Effects of Antigenic Dissimilarity between Mother and Foetus on Placental Size in Mice, Nature, 1965, vol. 202, pp. 613–614.

    Article  Google Scholar 

  • Johansson, M., Bromfield, J.J., Jasper, M.J., and Robertson, S.A., Semen Activates the Female Immune Response during Early Pregnancy in Mice, Immunology, 2004, vol. 112, no. 2, pp. 290–300.

    Article  PubMed  CAS  Google Scholar 

  • Kavaliers, M. and Colwell, D.D., Discrimination by Female Mice between the Odours of Parasitized and Non-Parasitized Males, Proc. Biol. Sci., 1995, vol. 22, no. 261, pp. 31–35.

    Article  Google Scholar 

  • Larson, S.J. and Dunn, A.J., Behavioral Effects of Cytokines, Brain. Behav. Immun., 2001, vol. 15, no. 4, pp. 371–387.

    Article  PubMed  CAS  Google Scholar 

  • Litvinova, E.A., Kudaeva, O.T., Mershieva, L.V., et al., High Level of Circulating Testosterone Abolishes Decline of Scent Attractiveness in Antigen-Treated Male Mice, Anim. Behav., 2005, vol. 69, no. 3, pp. 511–517.

    Article  Google Scholar 

  • Litvinova, E.A., Garms, A.I., Zaidman, A.M., et al., Redistribution of Immune Defense in Male Mice with Female Odor Exposure, Zh. Obshch. Biol., 2009, no. 1, pp. 46–55.

  • Moshkin, M.P., Gerlinskaya, L.A., and Evsikov, V.I., The Role of the Immune System in Behavioral Strategies of Reproduction, J. Reprod. Develop., 2000, vol. 46, no. 6, pp. 341–365.

    Article  CAS  Google Scholar 

  • Moshkin, M., Gerlinskaya, L., Morozova, O., et al., Behavior, Chemosignals and Endocrine Functions in Male Mice Infected with Tick-Borne Encephalitis Virus, Psychoneuroendocrinology, 2002, vol. 27, pp. 603–608.

    Article  PubMed  CAS  Google Scholar 

  • Moshkin, M.P., Kondratyuk, E.Yu., Litvinova, E.A., et al., Activation of Specific Immunity as a Stimulant for the Male Fertility of Females. “The Phenomenon of the Daughters of Lot”, Zh. Obshch. Biol., 2010, no. 5, pp. 425–435.

  • Nour, N.M., Schistosomiasis: Health Effects on Women, Rev. Obstet. Gynecol., 2010, vol. 3, no. 1, pp. 28–32.

    PubMed  Google Scholar 

  • Roberts, A.I., Devadas, S., Zhang, X., et al., The Role of Activation-Induced Cell Death in the Differentiation of T-Helper-Cell Subsets, Immunol. Res., 2003, vol. 28, no. 3, pp. 285–293.

    Article  PubMed  Google Scholar 

  • Rudnev, S.G. and Romanyukha, A.A., Principles of Immune System Adaptation, Usp. Sovrem. Biol., 2008, vol. 128, no. 3, pp. 260–270.

    Google Scholar 

  • Sarkar, C., Basu, B., Chakroborty, D., Dasgupta, P.S., and Basu, S., The Immunoregulatory Role of Dopamine: An Update, Brain. Behav. Immun., 2010, vol. 24, no. 4, pp. 525–528.

    Article  PubMed  CAS  Google Scholar 

  • Thomas, F., Teriokhin, A.T., Budilova, E.V., et al., Human Birth Weight Evolution across Contrasting Environments, J. Evol. Biol., 2004, vol. 17, no. 3, pp. 542–53.

    Article  PubMed  CAS  Google Scholar 

  • Velando, A., Drummond, H., and Torres, R., Senescent Birds Redouble Reproductive Effort When Ill: Confirmation of the Terminal Investment Hypothesis, Proc. Biol. Sci., 2006, vol. 273, pp. 1443–1448.

    Article  PubMed  Google Scholar 

  • Warner, C.M. and Gollnick, S.O., Expression of H-2K Major Histocompatibility Antigens on Preimplantation Mouse Embryos, Biol. Reprod., 1993, vol. 48, no. 5, pp. 1082–1087.

    Article  PubMed  CAS  Google Scholar 

  • Weiss, G., Goldsmith, L.T., Taylor, R.N., et al., Inflammation in Reproductive Disorders, Reprod. Sci., 2009, vol. 16, no. 2, pp. 216–229.

    Article  PubMed  CAS  Google Scholar 

  • Willis, C. and Poulin, R., Preference of Female Rats for the Odours of Non-Parasitised Males: The Smell of Good Genes, Folia Parasitologia, 2000, vol. 47, pp. 6–10.

    CAS  Google Scholar 

  • Zala, S.M., Potts, W.K., and Penn, D.J., Scent-Marking Displays Provide Honest Signals of Health and Infection, Behav. Ecol., 2004, vol. 15, no. 2, pp. 338–344.

    Article  Google Scholar 

  • Zuk, M. and McKean, K.A., Sex Differences in Parasite Infections: Patterns and Processes, Int. J. Parasitol., 1996, vol. 26, no. 10, pp. 1009–1023.

    PubMed  CAS  Google Scholar 

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Correspondence to L. A. Gerlinskaya.

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Original Russian Text © L.A. Gerlinskaya, S.O. Maslennikova, E.L. Zav’yalov, G.V. Kontsevaya, M.P. Moshkin, 2012, published in Ontogenez, 2012, Vol. 43, No. 5, pp. 357–365.

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Gerlinskaya, L.A., Maslennikova, S.O., Zav’yalov, E.L. et al. Reproductive success of males of the ICR outbred line during propagation against the background of antigenic stimulation. Russ J Dev Biol 43, 292–300 (2012). https://doi.org/10.1134/S1062360412050037

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  • DOI: https://doi.org/10.1134/S1062360412050037

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