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Mechanisms of hypothalamic-pituitary and immune system regulation: The role of gonadotropin-releasing hormone and immune mediators

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Abstract

Different aspects of the reciprocal regulatory influence of systems producing the immune and gonadotropin-releasing hormone (GnRH) in pre- and postnatal ontogeny are discussed in this review. GnRH is a neurohormone synthesized by a small population of neurons located in the anterior hypothalamus, which regulates the secretion of gonadotropines in the anterior lobe of the pituitary gland and they finally regulate the synthesis of sex steroids. Particular attention is given to analysis of the data involving the role of thymic peptides and cytokines in GnRH-system regulation in the normal condition and in the case of inflammation development caused by endotoxines in adult animals. The main prospects of the studies involving the influence of proinflammatory cytokines on GnRH-neuron migration and differentiation in prenatal ontogenesis are also discussed.

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References

  • Ashdown, H., Dumont, Y., Ng, M., et al., The Role of Cytokines in Mediating Effects of Prenatal Infection on the Fetus: Implications for Schizophrenia, Mol. Psychiatry, 2006, vol. 11, pp. 47–55.

    Article  PubMed  CAS  Google Scholar 

  • Bennett, I.L.. and Beeson, P.B., The Properties and Biologic Effects of Bacterial Pyrogens, Medicine, 1950, vol. 29, pp. 365–400.

    Article  PubMed  CAS  Google Scholar 

  • Bless, E.P., Westaway, W.A., Schwarting, G.A., et al., Effects of gamma-Aminobutyric Acid (A) Receptor Manipulation on Migrating Gonadotropin-Releasing Hormone Neurons Through the Entire Migratory Route in Vivo and in Vitro, Endocrinology, 2000, vol. 141, pp. 1254–1262.

    Article  PubMed  CAS  Google Scholar 

  • Bruijn de, M.F., Ma, X., Robin, C., et al., Hematopoietic Stem Cells Localize to the Endothelial Cell Layer in the Midgestation Mouse Aorta, Immunity, 2002, vol. 16, pp. 673–683.

    Article  PubMed  Google Scholar 

  • Bruneau, G., Izvol’skaya, M., Batailler, M., et al., Prolonged Neurogenesis during Early Development of Gonadotropin Releasing Hormone Neurones in Sheep (Ovis aries): In vivo and in vitro Studies, Neuroendocrinology, 2003, vol. 77, pp. 177–186.

    Article  PubMed  CAS  Google Scholar 

  • Buznikov, G.A., Shmukler, Y.B., and Lauder, J.M., From Oocyte to Neuron: Do Neurotransmitters Function in the Same Way through Development?, Cell Mol. Neurobiol., 1996, vol. 16, pp. 529–569.

    Article  Google Scholar 

  • Cai, Z., Pan, Z.L., Pang, Y., et al., Cytokine Induction in Fetal Rat Brains and Brain Injury in Neonatal Rats after Maternal Lipopolysaccharide Administration, Pediatr. Res., 2000, vol. 47, pp. 64–72.

    Article  PubMed  CAS  Google Scholar 

  • Chung, W.C., Moyle, S.S., and Tsai, P.S., Fibroblast Growth Factor 8 Signaling Through Fibroblast Growth Factor Receptor 1 Is Required for the Emergence of Gonadotropin-Releasing Hormone Neurons, Endocrinology, 2008, vol. 149, pp. 4997–5003.

    Article  PubMed  CAS  Google Scholar 

  • Ciechanowska, M., Lapot, M., Malewski, T., et al., Effect of Stress on the Expression of GnRH and GnRH Receptor (GnRH-R) Genes in the Preoptic Area-Hypothalamus and GnRH-R Gene in the Stalk/Median Eminence and Anterior Pituitary Gland in Ewes during Follicular Phase of the Estrous Cycle, Acta Neurobiol. Exp. (Wars.), 2007, vol. 67, pp. 1–12.

    Google Scholar 

  • Cronin, A.S., Horan, T.L., Spergel, D.J., et al., Neurotrophic Effects of BDNF on Embryonic Gonadotropin-Releasing Hormone (GnRH) Neurons, Eur. J. Neurosci., 2004, vol. 20, pp. 338–344.

    Article  PubMed  Google Scholar 

  • Dubois, E.A., Zandbergen, M.A., Peut, J., et al., Evolutionary Development of Three Gonadotropin-Releasing Hormone (GnRH) Systems in Vertebrates, Brain Res. Bull., 2002, vol. 57, pp. 413–418.

    Article  PubMed  CAS  Google Scholar 

  • Farookhi, R., Wesolowski, E., Trasler, J.M., and Robaire, B., Modulation by Neonatal Thymectomy of the Reproductive Axis in Male and Female Rats during Development, Biol. Reprod., 1988, vol. 38, pp. 91–99.

    Article  PubMed  CAS  Google Scholar 

  • Feleder, C., Arias, P., Refojo, D., et al., Interleukin-1 Inhibits NMDA-Stimulated GnRH Secretion: Associated Effects on the Release of Hypothalamic Inhibitory Amino Acid Neurotransmitters, Neuroimmunomodulation, 2000, vol. 7, pp. 46–50.

    Article  PubMed  CAS  Google Scholar 

  • Feleder, C., Wuttke, W., and Moguilevsky, J.A., Hypothalamic Relationships between Interleukin-6 and LHRH Release Affected by Bacterial Endotoxin in Adult Male Rats. Involvement of the Inhibitory Amino Acid System, Biol. Signals Recept., 1998, vol. 7, pp. 7–14.

    Article  PubMed  CAS  Google Scholar 

  • Fenton, M.J. and Golenbock, D.T., LPS-Binding Proteins and Receptors, J. Leukocyte Biol., 1998, vol. 64, pp. 25–32.

    PubMed  CAS  Google Scholar 

  • Gamble, J.A., Karunadasa, D.K., Pape, J.R., et al., Disruption of Ephrin Signaling Associates with Disordered Axophilic Migration of the Gonadotropin-Releasing Hormone Neurons, J. Neurosci., 2005, vol. 25, pp. 3142–3150.

    Article  PubMed  CAS  Google Scholar 

  • Giacobini, P., Messina, A., Morello, F., et al., Semaphorin 4D Regulates Gonadotropin Hormone-Releasing Hormone-1 Neuronal Migration through PlexinB1-Met Complex, J. Cell Biol., 2008, vol. 183, pp. 555–566.

    Article  PubMed  CAS  Google Scholar 

  • Gilmore, J.H., Jarskog, L.F., and Vadlamudi, S., Maternal Infection Regulates BDNF and NGF Expression in Fetal and Neonatal Brain and Maternal-Fetal Unit of the Rat, J. Neuroimmunol., 2003, vol. 138, pp. 49–55.

    Article  PubMed  CAS  Google Scholar 

  • Goya, R.G., Reggiani, P.C., Vesenbeckh, S.M., et al., Thymulin Gene Therapy Prevents the Reduction in Circulating Gonadotropins Induced by Thymulin Deficiency in Mice, Am. J. Physiol. Endocrinol. Metab., 2007, vol. 293, pp. 182–187.

    Article  CAS  Google Scholar 

  • Gutierrez, H., Dolcet, X., Tolcos, M., et al., HGF Regulates the Development of Cortical Pyramidal Dendrites, Development, 2004, vol. 131, pp. 3717–3726.

    Article  PubMed  CAS  Google Scholar 

  • Hadden, J.W., Thymic Endocrinology, Ann. N. Y. Acad. Sci., 1998, vol. 840, pp. 352–358.

    CAS  Google Scholar 

  • He, D., Sato, I., Kimura, F., et al., Lipopolysaccharide Inhibits Luteinizing Hormone Release through Interaction with Opioid and Excitatory Amino Acid Inputs to Gonadotropin-Releasing Hormone Neurones in Female Rats: Possible Evidence for a Common Mechanism Involved in Infection and Immobilization Stress, Neuroendocrinology, 2003, vol. 15, pp. 559–563.

    CAS  Google Scholar 

  • Healy, D.L., Bacher, J., and Hodgen, G.D., Thymic Regulation of Primate Fetal Ovarian-Adrenal Differentiation, Biol. Reprod., 1985, vol. 32, pp. 1127–1133.

    Article  PubMed  CAS  Google Scholar 

  • Igaz, P., Salvi, R., Rey, J.P., et al., Effects of Cytokines on Gonadotropin-Releasing Hormone (GnRH) Gene Expression in Primary Hypothalamic Neurons and in GnRH Neurons Immortalized Conditionally, Endocrinology, 2006, vol. 147, pp. 1037–1043.

    Article  PubMed  CAS  Google Scholar 

  • Ivey, N.S., Martin, E.N.., Scheld, W.M., et al., A New Method for Measuring Blood-Brain Barrier Permeability Demonstrated with Europium-Bound Albumin during Experimental Lipopolysaccharide (LPS) Induced Meningitis in the Rat, J. Neurosci. Methods, 2005, vol. 142, pp. 91–95.

    Article  PubMed  CAS  Google Scholar 

  • Izvol’skaya, M., Duittoz, A.H., Tillet, Y., et al., The Influence of Catecholamine on the Migration of Gonadotropin-Releasing Hormone-Producing Neurons in the Rat Foetuses, Brain. Struct. Funct., 2009, vol. 213, pp. 289–300.

    Article  CAS  Google Scholar 

  • Jacobson, J.D., Crofford, L.J., Sun, L., et al., Cyclical Expression of GnRH and GnRH Receptor mRNA in Lymphoid Organs, Neuroendocrinology, 1998, vol. 67, pp. 117–125.

    Article  PubMed  CAS  Google Scholar 

  • Kalra, P.S., Edwards, T.G., Xu, B., et al., The Anti-Gonadotropic Effects of Cytokines: the Role of Neuropeptides, Domest. Anim. Endocrinol., 1998, vol. 15, pp. 321–332.

    Article  PubMed  CAS  Google Scholar 

  • Kang, S.S., Kim, S.R., Leonhardt, S., et al., Effect of Interleukin-1β on Gonadotropin-Releasing Hormone (GnRH) and GnRH Receptor Gene Expression in Castrated Male Rats, J. Neuroendocrinol., 2000, vol. 12, pp. 421–429.

    Article  PubMed  CAS  Google Scholar 

  • Karsch, F.J., Battaglia, D.F., Breen, K.M., et al., Mechanisms for Ovarian Cycle Disruption by Immune/Inflammatory Stress, Stress, 2002, vol. 5, pp. 101–112.

    Article  PubMed  CAS  Google Scholar 

  • Kimura, M., Yu, W.H., Rettori, V., et al., Granulocyte-Macrophage Colony Stimulating Factor Suppresses LHRH Release by Inhibition of Nitric Oxide Synthase and Stimulation of Gamma-Aminobutyric Acid Release, Neuroimmunomodulation, 1997, vol. 4, pp. 237–243.

    PubMed  CAS  Google Scholar 

  • Li, X.F., Kinsey-Jones, J.S., Knox, A.M., et al., Neonatal Lipopolysaccharide Exposure Exacerbates Stress-Induced Suppression of Luteinizing Hormone Pulse Frequency in Adulthood, Endocrinology, 2007, vol. 148, pp. 5984–5990.

    Article  PubMed  CAS  Google Scholar 

  • Liverman, C.S., Kaftan, H.A., Cui, L., et al., Altered Expression of Pro-Inflammatory and Developmental Genes in the Fetal Brain in a Mouse Model of Maternal Infection, Neurosci. Let., 2006, vol. 399, pp. 220–225.

    Article  CAS  Google Scholar 

  • Magni, P., Dozio, E., Ruscica, M., et al., Leukemia Inhibitory Factor Induces the Chemomigration of Immortalized Gonadotropin-Releasing Hormone Neurons through the Independent Activation of the Janus Kinase/Signal Transducer and Activator of Transcription 3, Mitogen-Activated Protein Kinase/Extracellularly Regulated Kinase 1/2, and Phosphatidylinositol 3-Kinase/Akt Signaling Pathways, Mol. Endocrinol., 2007, vol. 21, pp. 1163–1174.

    Article  PubMed  CAS  Google Scholar 

  • Marchetti, B., Gallo, F., and Farinella, Z., Luteinizing Hormone-Releasing Hormone Is a Primary Signaling Molecule in the Neuroimmune Network, Ann. N. Y. Acad. Sci., 1998, vol. 840, pp. 205–248.

    Article  PubMed  CAS  Google Scholar 

  • Marchetti, B., Guarcello, V., Morale, M.C., et al., Luteinizing Hormone-Releasing Hormone (LHRH) Agonist Restoration of Age-Associated Decline of Thymus Weight, Thymic LHRH Receptors, and Thymocyte Proliferative Capacity, Endocrinology, 1989, vol. 125, pp. 1037–1045.

    Article  PubMed  CAS  Google Scholar 

  • Markakis, E.A. and Swanson, L.W., Spatiotemporal Patterns of Secretomotor Neuron Generation in the Parvicellular Neuroendocrine System, Brain. Res. Rev., 1997, vol. 24, pp. 255–291.

    Article  PubMed  CAS  Google Scholar 

  • Maroder, M., Bellavia, D., Vacca, A., et al., The Thymus at the Crossroad of Neuroimmune Interactions, Ann. N. Y. Acad. Sci., 2000, vol. 917, pp. 741–747.

    PubMed  CAS  Google Scholar 

  • McCann, S.M., Kimura, M., Karanth, S., et al., The Mechanism of Action of Cytokines to Control the Release of Hypothalamic and Pituitary Hormones in Infection, Ann. N. Y. Acad. Sci., 2000, vol. 917, pp. 4–18.

    PubMed  CAS  Google Scholar 

  • Metcalf, D., The Unsolved Enigmas of Leukemia Inhibitory Factor, Stem Cells, 2003, vol. 21, pp. 5–14.

    Article  PubMed  CAS  Google Scholar 

  • Millar, R.P., Lu, Z.L., Pawson, A.J., et al., Gonadotropin-Releasing Hormone Receptors, Endocrinol. Rev., 2004, vol. 25, pp. 235–275.

    Article  CAS  Google Scholar 

  • Montgomery, R.A. and Dallman, M.J., Analysis of Cytokine Gene Expression during Fetal Thymic Ontogeny using the Polymerase Chain Reaction, J. Immunol., 1991, vol. 147, pp. 554–560.

    PubMed  CAS  Google Scholar 

  • Morale, M.C., Batticane, N., and Bartoloni, G., Blocade of Central and Peripheral Luteinizing Hormone-Releasing Hormone (LHRH) Receptors in Neonatal Rats with a Potent LHRH-Antagonist Inhibits the Morphofunctional Development of the Thymus and Maturation of the Cell-Mediated and Humoral Immune Responses, Endocrinology, 1991, vol. 128, pp. 1073–1085.

    Article  PubMed  CAS  Google Scholar 

  • Nagai, Y., Akashi, S., Nagafuku, M., et al., Essential Role of MD2 in LPS Responsiveness and TLR4 Distribution, Nat. Immunol., 2002, vol. 3, pp. 667–672.

    PubMed  CAS  Google Scholar 

  • Nowotny, A., Molecular Aspects of Endotoxic Reactions, Bacteriol. Rev., 1969, vol. 33, no. 1, pp. 72–98.

    PubMed  CAS  Google Scholar 

  • Pan, W., Yu, C., Hsuchou, H., et al., Neuroinflammation Facilitates LIF Entry Into Brain: Role of TNF, Am. J. Physiol. Cell Physiol., 2008, vol. 294, pp. 436–442.

    Google Scholar 

  • Petrie, H.T., Cell Migration and the Control of Postnatal T-Cell Lymphopoiesis in the Thymus, Nat. Rev. Immunol, 2003, vol. 3, pp. 859–866.

    Article  PubMed  CAS  Google Scholar 

  • Porter, P.J. and Kass, E.H., Role of the Posterior Hypothalamus in Mediating the Lethal Action of Bacterial Endotoxin in the Rat, J. Immunol., 1965, vol. 94, pp. 641–648.

    PubMed  CAS  Google Scholar 

  • Pronina, T., Ugrumov, M., Adamskaya, E., et al., Influence of Serotonin on the Development and Migration of Gonadotropin-Releasing Hormone Neurones in Rat Fetuses, J. Neuroendocrinol., 2003, vol. 15, pp. 549–558.

    Article  PubMed  CAS  Google Scholar 

  • Przekop, F. and Tomaszewska, D., Responses in the Hypothalamic Monoaminergic System Activity in Ewes to Beta-Endorphin, CRF and Their Antagonists, Acta Neurobiol. Exp. (Wars.), 1996, vol. 56, pp. 807–817.

    CAS  Google Scholar 

  • Ramakrishnappa, N., Rajamahendran, R., Lin, Y.M., and Leung, P.C., GnRH in Non-Hypothalamic Reproductive Tissues, Anim. Reprod. Sci., 2005, vol. 88, pp. 95–113.

    Article  PubMed  CAS  Google Scholar 

  • Rao, L.V., Cleveland, R.P., Kimmel, R.J., and Ataya, K.M., Hematopoietic Stem Cell Antigen-1 (Sca-1) Expression in Different Lymphoid Tissues of Female Mice Treated with GnRH Agonist, Am. J. Reprod. Immunol., 1995, vol. 34, pp. 257–266.

    PubMed  CAS  Google Scholar 

  • Rebar, R.W., Miyake, A., Low, T.L., et al., Thymosin Stimulates Secretion of Luteinizing Hormone-Releasing Factor, Science, 1981, vol. 214, pp. 669–671.

    Article  PubMed  CAS  Google Scholar 

  • Rettori, V., Belova, N., Kamat, A., et al., Blockade by Interleukin-1-Alpha of Nitricoxidergic Control of Luteinizing Hormone-Releasing Hormone Release in Vivo and in Vitro, Neuroimmunomodulation, 1994, vol. 1, pp. 86–91.

    Article  PubMed  CAS  Google Scholar 

  • Rettori, V., Gimeno, M.F., Karara, A., et al., Interleukin 1 Alpha Inhibits Prostaglandin E2 Release to Suppress Pulsatile Release of Luteinizing Hormone but Not Follicle-Stimulating Hormone, Proc. Natl. Acad. Sci. USA, 1991, vol. 88, pp. 2763–2767.

    Article  PubMed  CAS  Google Scholar 

  • Rivest, S. and Rivier, C., Interleukin-1 Inhibits the Endogenous Expression of the Early Gene C-Fos Located within the Nucleus of LH-RH Neurons and Interferes with Hypothalamic LH-RH Release during Proestrus in the Rat, Brain Res., 1993, vol. 613, pp. 132–142.

    Article  PubMed  CAS  Google Scholar 

  • Rousset, C.I., Chalon, S., Cantagrel, S., et al., Maternal Exposure to LPS Induces Hypomyelination in the Internal Capsule and Programmed Cell Death in the Deep Gray Matter in Newborn Rats, Pediatr. Res., 2006, vol. 59, pp. 428–433.

    Article  PubMed  CAS  Google Scholar 

  • Schwanzel-Fukuda, M. and Pfaff, D.W., Origin of Luteinizing Hormone-Releasing Hormone Neurons, Nature, 1989, vol. 338, pp. 161–164.

    Article  PubMed  CAS  Google Scholar 

  • Schwarting, G.A., Wierman, M.E., and Tobet, S.A., Gonadotropin-Releasing Hormone Neuronal Migration, Semin. Reprod. Med., 2007, vol. 25, pp. 305–312.

    Article  PubMed  CAS  Google Scholar 

  • Siler-Khodr, T.M. and Khodr, G.S., Luteinizing Hormone Releasing Factor Content of the Human Placenta, Am. J. Obstet. Gynecol., 1978, vol. 130, pp. 216–219.

    PubMed  CAS  Google Scholar 

  • Simonian, S.X. and Herbison, A.E., Differing, Spatially Restricted Roles of Ionotropic Glutamate Receptors in Regulating the Migration of GnRH Neurons during Embryogenesis, J. Neurosci., 2001, vol. 21, pp. 934–943.

    PubMed  CAS  Google Scholar 

  • Singh, A.K. and Jiang, Y., How Does Peripheral Lipopolysaccharide Induce Gene Expression in the Brain of Rats?, Toxicology, 2004, vol. 201, pp. 197–207.

    Article  PubMed  CAS  Google Scholar 

  • Son, B.R., Marquez-Curtis, L.A., Kucia, M., et al., Migration of Bone Marrow and Cord Blood Mesenchymal Stem Cells in vitro Is Regulated by Stromal-Derived Factor-1-CXCR4 and Hepatocyte Growth Factor-C-Met Axes and Involves Matrix Metalloproteinases, Stem Cells, 2006, vol. 24, pp. 1254–1264.

    Article  PubMed  CAS  Google Scholar 

  • Sternberg, E.M., Neural-Immune Interactions in Health and Disease, J. Clin. Invest., 1997, vol. 100, pp. 2641–2647.

    Article  PubMed  CAS  Google Scholar 

  • Tilders, F.J., De Rijk, R.H., Van Dam, A.M., et al., Activation of the Hypothalamus-Pituitary-Adrenal Axis by Bacterial Endotoxins: Routes and Intermediate Signals, Psychoneuroendocrinology, 1994, vol. 19, pp. 209–232.

    Article  PubMed  CAS  Google Scholar 

  • Turnbull, A.V. and Rivier, C.L., Regulation of the Hypothalamic-Pituitary-Adrenal Axis by Cytokines: Actions and Mechanisms of Action, Physiol. Rev., 1999, vol. 79, pp. 1–71.

    PubMed  CAS  Google Scholar 

  • Urakubo, A., Jarskog, L.F., Lieberman, J.A., et al., Prenatal Exposure to Maternal Infection Alters Cytokine Expression in the Placenta, Amniotic Fluid, and Fetal Brain, Schizophr. Res., 2001, vol. 47, pp. 27–36.

    Article  PubMed  CAS  Google Scholar 

  • Verma, S., Nakaoke, R., Dohgu, S., et al., Release of Cytokines by Brain Endothelial Cells: A Polarized Response to Lipopolysaccharide, Brain. Behav. Immun., 2006, vol. 20, pp. 449–455.

    Article  PubMed  CAS  Google Scholar 

  • Wang, S., Yan, J.Y., Lo, Y.K., et al., Dopaminergic and Serotoninergic Deficiencies in Young Adult Rats Prenatally Exposed to the Bacterial Lipopolysaccharide, Brain Res., 2009, vol. 1265, pp. 196–204.

    Article  PubMed  CAS  Google Scholar 

  • Watanobe, H. and Hayakawa, Y., Hypothalamic Interleukin-1 and Tumor Necrosis Factor, but Not Interleukin-6, Mediate the Endotoxin-Induced Suppression of the Reproductive Axis in Rats, Endocrinology, 2003, vol. 144, pp. 4868–4875.

    Article  PubMed  CAS  Google Scholar 

  • Yamazaki, H., Sakata, E., Yamane, T., et al., Presence and Distribution of Neural Crest-Derived Cells in the Murine Developing Thymus and Their Potential for Differentiation, Int. Immunol., 2005, vol. 17, pp. 549–558.

    Article  PubMed  CAS  Google Scholar 

  • Yarilin, A.A. and Belyakov, I.M., Cytokines in the Thymus: Production and Biological Effects, Curr. Med. Chem., 2004, vol. 11, pp. 447–464.

    Article  PubMed  CAS  Google Scholar 

  • Yoshida, K., Rutishauser, U., Crandall, J.E., et al., Polysialic Acid Facilitates Migration of Luteinizing Hormone-Releasing Hormone Neurons on Vomeronasal Axons, J. Neurosci., 1999, vol. 19, pp. 794–801.

    PubMed  CAS  Google Scholar 

  • Yu, H.M., Yuan, T.M., Gu, W.Z., et al., Expression of Glial Fibrillary Acidic Protein in Developing Rat Brain After Intrauterine Infection, Neuropathology, 2004, vol. 24, pp. 136–143.

    Article  PubMed  Google Scholar 

  • Zakharova, L., Ermilova, I.Y., Melnikova, V., et al., Hypothalamic Control of the Cell-Mediated Immunity and of the Luteinizing Hormone-Releasing Hormone Level in Thymus and Peripheral Blood of Rat Fetuses, Neuroimmunomodulation, 2005, vol. 12, pp. 85–91.

    Article  PubMed  CAS  Google Scholar 

  • Zakharova, L.A., Malyukova, I.V., and Proshlyakova, E.V., Hypothalamo-Pituitary Control of the Cell-Mediated Immunity in Rat Embryos: Role of LHRH in Regulation of Lymphocyte Proliferation, J. Reprod. Immunol., 2000, vol. 47, pp. 17–32.

    Article  PubMed  CAS  Google Scholar 

  • Zakharova, L.A., Plasticity of Neuroendocrine-Immune Interactions during Ontogeny: Role of Perinatal Programming in Pathogenesis of Inflammation and Stress-Related Diseases in Adults, Recent Patents on Endocrine, Metabolic and Immune Drug Discovery, 2009, vol. 3, pp. 11–27.

    Article  CAS  Google Scholar 

  • Zakharova, L.A., Potapova, I.V., Malyukova, E.V., et al., Effect of Hypothalamus-Pituitary Component of the Neuroendocrine System on the Development of Con A-Induced Proliferative Response of Rat Fetal Thymocytes, Dokl. Akad. Nauk, 1997, vol. 357, no. 2, pp. 269–271.

    PubMed  CAS  Google Scholar 

  • Zhu, Y., Carvey, P.M., and Ling, Z., Altered Glutathione Homeostasis in Animals Prenatally Exposed to Lipopolysaccharide, Neurochem. Int., 2007, vol. 50, pp. 671–680.

    Article  PubMed  CAS  Google Scholar 

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Original Russian Text © M.S. Izvol’skaya, V.S. Sharova, L.A. Zakharova, 2010, published in Izvestiya Akademii Nauk, Seriya Biologicheskaya, 2010, No. 4, pp. 451–461.

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Izvol’skaya, M.S., Sharova, V.S. & Zakharova, L.A. Mechanisms of hypothalamic-pituitary and immune system regulation: The role of gonadotropin-releasing hormone and immune mediators. Biol Bull Russ Acad Sci 37, 382–391 (2010). https://doi.org/10.1134/S1062359010040084

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