Russian Journal of Developmental Biology

, Volume 43, Issue 5, pp 292–300 | Cite as

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

  • L. A. Gerlinskaya
  • S. O. Maslennikova
  • E. L. Zav’yalov
  • G. V. Kontsevaya
  • M. P. Moshkin
Developmental Physiology


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.


hemocyanin male antigenic stimulation pregnancy embryonic losses weight of embryos immune response Th1 Th2 IgG1 IgG2a 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 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.PubMedCrossRefGoogle Scholar
  2. 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.PubMedCrossRefGoogle Scholar
  3. 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.PubMedCrossRefGoogle Scholar
  4. 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.PubMedCrossRefGoogle Scholar
  5. Billington, W.D., Influence of Immunological Dissimilarity of Mother and Foetus on Size of Placenta in Mice, Nature, 1964, vol. 202, pp. 317–318.PubMedCrossRefGoogle Scholar
  6. 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.PubMedCrossRefGoogle Scholar
  7. 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.PubMedCrossRefGoogle Scholar
  8. 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.PubMedCrossRefGoogle Scholar
  9. Faivre, B., Gregoire, A., Preault, M., et al., Immune Activation Rapidly Mirrored in a Secondary Sexual Trait, Science, 2003, vol. 300, p. 103.PubMedCrossRefGoogle Scholar
  10. 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.CrossRefGoogle Scholar
  11. 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.PubMedCrossRefGoogle Scholar
  12. Fietta, P. and Delsante, G., Focus on Human Natural Killer Cells, Riv. Biol., 2009, vol. 102, no. 2, pp. 219–235.PubMedGoogle Scholar
  13. 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.PubMedCrossRefGoogle Scholar
  14. 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.PubMedCrossRefGoogle Scholar
  15. 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.PubMedCrossRefGoogle Scholar
  16. 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.CrossRefGoogle Scholar
  17. 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.PubMedCrossRefGoogle Scholar
  18. Guégan, J.F., Thomas, F., Hochberg, M.E., et al., Disease Diversity and Human Fertility, Evolution, 2001, vol. 55, no. 7, pp. 1308–1314.PubMedGoogle Scholar
  19. 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.PubMedCrossRefGoogle Scholar
  20. 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.PubMedCrossRefGoogle Scholar
  21. 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.PubMedGoogle Scholar
  22. James, D.A., Effects of Antigenic Dissimilarity between Mother and Foetus on Placental Size in Mice, Nature, 1965, vol. 202, pp. 613–614.CrossRefGoogle Scholar
  23. 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.PubMedCrossRefGoogle Scholar
  24. 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.CrossRefGoogle Scholar
  25. Larson, S.J. and Dunn, A.J., Behavioral Effects of Cytokines, Brain. Behav. Immun., 2001, vol. 15, no. 4, pp. 371–387.PubMedCrossRefGoogle Scholar
  26. 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.CrossRefGoogle Scholar
  27. 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.Google Scholar
  28. 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.CrossRefGoogle Scholar
  29. 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.PubMedCrossRefGoogle Scholar
  30. 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.Google Scholar
  31. Nour, N.M., Schistosomiasis: Health Effects on Women, Rev. Obstet. Gynecol., 2010, vol. 3, no. 1, pp. 28–32.PubMedGoogle Scholar
  32. 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.PubMedCrossRefGoogle Scholar
  33. 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
  34. 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.PubMedCrossRefGoogle Scholar
  35. 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.PubMedCrossRefGoogle Scholar
  36. 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.PubMedCrossRefGoogle Scholar
  37. 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.PubMedCrossRefGoogle Scholar
  38. Weiss, G., Goldsmith, L.T., Taylor, R.N., et al., Inflammation in Reproductive Disorders, Reprod. Sci., 2009, vol. 16, no. 2, pp. 216–229.PubMedCrossRefGoogle Scholar
  39. 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.Google Scholar
  40. 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.CrossRefGoogle Scholar
  41. 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.PubMedGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2012

Authors and Affiliations

  • L. A. Gerlinskaya
    • 1
  • S. O. Maslennikova
    • 2
    • 3
  • E. L. Zav’yalov
    • 2
    • 3
  • G. V. Kontsevaya
    • 2
    • 3
  • M. P. Moshkin
    • 2
    • 3
  1. 1.Institute of Cytology and Genetics, Siberian BranchRussian Academy of SciencesNovosibirskRussia
  2. 2.Tomsk State UniversityTomskRussia
  3. 3.Institute of Systematics and Ecology of Animals, Siberian BranchRussian Academy of SciencesNovosibirskRussia

Personalised recommendations