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Perinatal Inflammation Reprograms Neuroendocrine, Immune, and Reproductive Functions: Profile of Cytokine Biomarkers

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Abstract

Viral and bacterial infections causing systemic inflammation are significant risk factors for developing body. Inflammatory processes can alter physiological levels of regulatory factors and interfere with developmental mechanisms. The brain is the main target for the negative impact of inflammatory products during critical ontogenetic periods. Subsequently, the risks of various neuropsychiatric diseases such as Alzheimer’s and Parkinson’s diseases, schizophrenia, and depression are increased in the offspring. Inflammation-induced physiological disturbances can cause immune and behavioral disorders, reproductive deficiencies, and infertility. The influence of maternal immune stress is mediated by the regulation of pro-inflammatory cytokines such as interleukin (IL)-1β, IL-6, monocyte chemotactic protein 1, leukemia-inhibiting factor, and tumor necrosis factor-alpha secretion in the maternal-fetal system. The increasing number of patients with neuronal and reproductive disorders substantiates the identification of biomarkers for these disorders targeted at their therapy.

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References

  1. Zakharova, L.A. 2009. 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 & Immune Drug Discovery 3: 11–27.

    Article  CAS  Google Scholar 

  2. Zakharova, L.A., Izvolskaia, M.S. 2012. Interactions between the reproductive and immune systems during ontogenesis: The role of GnRH, sex steroids and immunomediators. In Sex steroids Kahn SM editor Zagreb InTech 341–370.

  3. Zakharova, L. 2015. Perinatal stress in brain programming and pathogenesis of psychoneurological disorders. The Biological Bulletin 42: 12–20. https://doi.org/10.1134/S1062359015010124.

    Article  CAS  Google Scholar 

  4. Izvolskaia, M., V. Sharova, and L. Zakharova. 2018. Prenatal programming of neuroendocrine system development by lipopolysaccharide: Long-term effects. International Journal of Molecular Sciences 19: E 3695. https://doi.org/10.3390/ijms19113695.

    Article  CAS  Google Scholar 

  5. Ardalan, M., T. Chumak, Z. Vexler, and C. Mallard. 2019. Sex-dependent effects of perinatal inflammation on the brain: Implication for neuro-psychiatric disorders. International Journal of Molecular Sciences 20 (9): E2270. https://doi.org/10.3390/ijms20092270.

    Article  CAS  PubMed  Google Scholar 

  6. Saghazadeh, A., B. Ataeinia, K. Keynejad, A. Abdolalizadeh, A. Hirbod-Mobarakeh, and N.A. Rezaei. 2019. Meta-analysis of pro-inflammatory cytokines in autism spectrum disorders: Effects of age, gender, and latitude. Journal of Psychiatric Research 115: 90–102. https://doi.org/10.1016/j.jpsychires.2019.05.019.

    Article  PubMed  Google Scholar 

  7. Hagberg, H., P. Gressens, and C. Mallard. 2012. Inflammation during fetal and neonatal life: Implications for neurologic and neuropsychiatric disease in children and adults. Annals of Neurology 71: 444–457. https://doi.org/10.1038/nrneurol.2015.13.

    Article  CAS  PubMed  Google Scholar 

  8. Lucchina, L., and A.M. Depino. 2014. Altered peripheral and central inflammatory responses in a mouse model of autism. Autism Research 7: 273–289. https://doi.org/10.1002/aur.1338.

    Article  PubMed  Google Scholar 

  9. Gilstrap, L.C., 3rd, and S.M. Ramin. 2001. Urinary tract infections during pregnancy. Obstetrics and Gynecology Clinics of North America 28: 581–591. https://doi.org/10.1016/s0889-8545(05)70219-9.

    Article  PubMed  Google Scholar 

  10. Cui, K., H. Ashdown, G.N. Luheshi, and P. Boksa. 2009. Effects of prenatal immune activation on hippocampal neurogenesis in the rat. Schizophrenia Research 113: 288–297. https://doi.org/10.1016/j.schres.2009.05.003.

    Article  PubMed  Google Scholar 

  11. Wang, S., J.Y. Yan, Y.K. Lo, P.M. Carvey, and Z. Ling. 2009. Dopaminergic and serotoninergic deficiencies in young adult rats prenatally exposed to the bacterial lipopolysaccaharide. Brain Research 1265: 196–204. https://doi.org/10.1016/j.brainres.2009.02.022.

    Article  CAS  PubMed  Google Scholar 

  12. Vivekanantham, S., S. Shah, R. Dewji, A. Dewji, C. Khatri, and R. Ologunde. 2015. Neuroinflammation in Parkinson’s disease: Role in neurodegeneration and tissue repair. The International Journal of Neuroscience 125: 717–725. https://doi.org/10.3109/00207454.2014.982795.

    Article  CAS  PubMed  Google Scholar 

  13. Clark, L.F., and T. Kodadek. 2016. The immune system and neuroinflammation as potential sources of blood-based biomarkers for Alzheimer’s disease, Parkinson’s disease, and Huntington’s disease. ACS Chemical Neuroscience 7: 520–527. https://doi.org/10.1021/acschemneuro.6b00042.

    Article  CAS  PubMed  Google Scholar 

  14. Sharova, V.S., M.S. Izvolskaia, and L.A. Zakharova. 2015. Lipopolysaccharide-induced maternal inflammation affects the gonadotropin-releasing hormone neuron development in fetal mice. Neuroimmunomodulation 22 (4): 222–232. https://doi.org/10.1159/000365482.

    Article  CAS  PubMed  Google Scholar 

  15. Ignatiuk, V.M., M.S. Izvolskaya, V.S. Sharova, S.N. Voronova, and L.A. Zakharova. 2019. Disruptions in the reproductive system of female rats after prenatal lipopolysaccharide-induced immunological stress: Role of sex steroids. Stress 21 (5): 1–9. https://doi.org/10.1080/10253890.2018.1508440.

    Article  CAS  Google Scholar 

  16. Lei, L., S. Jin, K.E. Mayo, and T.K. Woodruff. 2010. The interactions between the stimulatory effect of follicle-stimulating hormone and the inhibitory effect of estrogen on mouse primordial folliculogenesis. Biology of Reproduction 82 (1): 13–22. https://doi.org/10.1095/biolreprod.109.077404.

    Article  CAS  PubMed  Google Scholar 

  17. Carvey, P.M., Q. Chang, J.W. Lipton, and Z. Ling. 2003. Prenatal exposure to the bacteriotoxin lipopolysaccharide leads to long-term losses of dopamine neurons in offspring: A potential, new model of Parkinson’s disease. Frontiers in Bioscience 8: s826–s837. https://doi.org/10.2741/1158.

    Article  CAS  PubMed  Google Scholar 

  18. American Psychiatric Association, ed. 2013. Diagnostic and statistical manual of mental disorders, fifth edition (DSM-5). 5th ed. Arlington: American Psychiatric Association.

    Google Scholar 

  19. Hazlett, H.C., M. Poe, G. Gerig, М. Styner, С. Chappell, R.G. Smith, C. Vachet, and J. Piven. 2011. Early brain overgrowth in autism associated with an increase in cortical surface area before age 2 years. Archives of General Psychiatry 68: 467–476. https://doi.org/10.1001/archgenpsychiatry.2011.39.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Mannion, A., G. Leader, and O. Healy. 2013. An investigation of comorbid psychological disorders, sleep problems, gastrointestinal symptoms and epilepsy in children and adolescents with autism spectrum disorder. Research in Autism Spectrum Disorder 7: 35–42.

    Article  Google Scholar 

  21. Beard, C.M., L.A. Panser, and S.K. Katusic. 2011. Is excess folic acid supplementation a risk factor for autism? Medical Hypotheses 77: 15–17. https://doi.org/10.1016/j.mehy.2011.03.013.

    Article  CAS  PubMed  Google Scholar 

  22. Zhou, S.S., Y.M. Zhou, D. Li, and Q. Ma. 2013. Early infant exposure to excess multivitamin: A risk factor for autism? Autism Research and Treatment 963697. https://doi.org/10.1155/2013/963697.

  23. Nicolson, G.L., R. Gan, N.L. Nicolson, and J. Haier. 2007. Evidence for Mycoplasma ssp., Chlamydia pneunomiae, and human herpesvirus-6 coinfections in the blood of patients with autistic spectrum disorders. Journal of Neuroscience Research 85: 1143–1148. https://doi.org/10.1002/jnr.21203.

    Article  CAS  PubMed  Google Scholar 

  24. Patterson, P.H. 2011. Maternal infection and immune involvement in autism. Trends in Molecular Medicine 17: 389–394. https://doi.org/10.1016/j.molmed.2011.03.001.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Atladóttir, H.Ó., T.B. Henriksen, D.E. Schendel, and E.T. Parner. 2012. Autism after infection, febrile episodes, and antibiotic use during pregnancy: An exploratory study. Pediatrics 130: e1447–e1454. https://doi.org/10.1542/peds.2012-1107.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Melnikova, V.I., M.A. Afanasyeva, S.N. Voronova, and L.A. Zakharova. 2012. The effect of catecholamine deficit on the development of the immune system in rats. Doklady Biological Sciences 443: 68–70. https://doi.org/10.1134/S001249661202007X.

    Article  CAS  PubMed  Google Scholar 

  27. Lifantseva, N.V., T.O. Koneeva, S.N. Voronova, L.A. Zakharova, and V.I. Melnikova. 2016. The inhibition of dopamine synthesis in fetuses changes the pattern of T-lymphocyte maturation in the thymus of adult rats. Doklady. Biochemistry and Biophysics 470 (1): 342–344. https://doi.org/10.1134/S1607672916050082.

    Article  CAS  PubMed  Google Scholar 

  28. Chaste, P., and M. Leboyer. 2012. Autism risk factors: Genes, environment, and gene-environment interactions. Dialogues in Clinical Neuroscience 14: 281–292.

    PubMed  PubMed Central  Google Scholar 

  29. Onore, C., M. Careaga, and P. Ashwood. 2012. The role of immune dysfunction in the pathophysiology of autism. Brain, Behavior, and Immunity 26 (3): 383–392. https://doi.org/10.1016/j.bbi.2011.08.007.

    Article  CAS  PubMed  Google Scholar 

  30. Rose, D., and P. Ashwood. 2014. Potential cytokine biomarkers in autism spectrum disorders. Biomarkers in Medicine 8 (9): 1171–1181. https://doi.org/10.2217/bmm.14.39.

    Article  CAS  PubMed  Google Scholar 

  31. Mead, J., and P. Ashwood. 2015. Evidence supporting an altered immune response in ASD. Immunology Letters 163: 49–55. https://doi.org/10.1016/j.imlet.2014.11.006.

    Article  CAS  PubMed  Google Scholar 

  32. Krakowiak, P., P.E. Goines, D.J. Tancredid, P. Ashwoodc, R.L. Hansenc, I. Hertz-Picciottoa, and J. Van de Waterb. 2017. Neonatal cytokine profiles associated with autism spectrum disorder. Biological Psychiatry 81: 442–451. https://doi.org/10.1016/j.biopsych.2015.08.007.

    Article  CAS  PubMed  Google Scholar 

  33. Atladóttir, H.Ó., P. Thorsen, D.E. Schendel, L. Østergaard, S. Lemcke, and E.T. Parner. 2010. Association of hospitalization for infection in childhood with diagnosis of autism spectrum disorders. Archives of Pediatrics & Adolescent Medicine 164: 470–477. https://doi.org/10.1001/archpediatrics.2010.9.

    Article  Google Scholar 

  34. Gottfried, C., V. Bambini-Junior, F. Francis, R. Riesgo, and W. Savino. 2015. The impact of neuroimmune alterations in autism spectrum disorder. Frontiers in Psychiatry 6: 121. https://doi.org/10.3389/fpsyt.2015.00121.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Vargas, D.L., C. Nascimbene, C. Krishnan, A.W. Zimmerman, and C.A. Pardo. 2005. Neuroglial activation and neuroinflammation in the brain of patients with autism. Annals of Neurology 57: 67–81. https://doi.org/10.1002/ana.20315.

    Article  CAS  PubMed  Google Scholar 

  36. Masi, A., E.J. Breen, G.A. Alvares, N. Glozier, I.B. Hickie, A. Hunt, J. Hui, J. Beilby, D. Ravine, J. Wray, A.J.O. Whitehouse, and J. Adam. 2017. Guastella cytokine levels and associations with symptom severity in male and female children with autism spectrum disorder. Molecular Autism 8: 63. https://doi.org/10.1186/s13229-017-0176-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Autism and Developmental Disabilities Monitoring Network Surveillance Year. 2008. Principal investigators, prevalence of autism spectrum disorders–Autism and developmental disabilities monitoring network, 14 sites, United States. MMWR Surveillance Summaries 61 (3): 1–19 https://www.cdc.gov/MMWR/PREVIEW/MMWRHTML/SS6103A1.HTM. Accessed 30 March 2012.

    Google Scholar 

  38. Werling, D.M., N.N. Parikshak, and D.H. Geschwind. 2016. Gene expression in human brain implicates sexually dimorphic pathways in autism spectrum disorders. Nature Communications 7: 0717. https://doi.org/10.1038/ncomms10717.

    Article  CAS  Google Scholar 

  39. Harro, M., D. Eensoo, and E. Kiiveetal. 2001. Platelet monoamineoxidase in healthy 9-and 15-years old children: The effect of gender, smoking and puberty. Progress in Neuro-Psychopharmacology and Biological Psychiatry 25: 1497–1511. https://doi.org/10.1016/s0278-5846(01)00212-3.

    Article  CAS  PubMed  Google Scholar 

  40. Ahmad, S.F., A. Nadeem, M.A. Ansari, S.A. Bakheet, L.Y. Al-Ayadhi, and S.M. Attia. 2017. Upregulation of IL-9 and JAK-STAT signaling pathway in children with autism. Progress in Neuro-Psychopharmacology & Biological Psychiatry 79 (Pt B): 472–480. https://doi.org/10.1016/j.pnpbp.2017.08.002.

    Article  CAS  Google Scholar 

  41. Bransfield, R.C., J.S. Wulfman, W.T. Harvey, and A.I. Usman. 2008. The association between tick-borne infections, Lyme borreliosis and autism spectrum disorders. Medical Hypotheses 70: 967–974. https://doi.org/10.1016/j.mehy.2007.09.006.

    Article  PubMed  Google Scholar 

  42. Abib, R.T., A. Gaman, A.A. Dargél, R. Tamouza, F. Kapczinski, C. Gottfried, and M. Leboyer. 2018. Intracellular pathogen infections and immune response in autism. Neuroimmunomodulation 25 (5–6): 271–279. https://doi.org/10.1159/000491821.

    Article  CAS  PubMed  Google Scholar 

  43. Jyonouchi, H., L. Geng, and A.L. Davidow. 2014. Cytokine profiles by peripheral blood monocytes are associated with changes in behavioral symptoms following immune insults in a subset of ASD subjects: An inflammatory subtype? Journal of Neuroinflammation 11: 187. https://doi.org/10.1186/s12974-014-0187-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Beurel, E., and R.S. Jope. 2009. Lipopolysaccharide-induced interleukin-6 production is controlled by glycogen synthase kinase-3 and STAT3 in the brain. Journal of Neuroinflammation 6: 9. https://doi.org/10.1186/1742-2094-6-9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Martin, M., K. Rehani, R.S. Jope, and S.M. Michalek. 2005. Toll-like receptor-mediated cytokine production is differentially regulated by glycogen synthase kinase 3. Nature Immunology 6: 777–784. https://doi.org/10.1038/ni1221.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Liu, J.T., B.Y. Chen, J.Q. Zhang, F. Kuang, and L.W. Chen. 2015. Lead exposure induced microgliosis and astrogliosis in hippocampus of young mice potentially by triggering TLR4-MyD88-NFκB signaling cascades. Toxicology Letters 239 (2): 97–107. https://doi.org/10.1016/j.toxlet.2015.09.015.

    Article  CAS  PubMed  Google Scholar 

  47. Holmlund, U., G. Cebers, and A.R. Dahlfors. 2002. Expression and regulation of the pattern recognition receptors toll-like receptor-2 and toll-like receptor-4 in the human placenta. Immunology 107 (1): 145–151. https://doi.org/10.1046/j.1365-2567.2002.01491.x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Beijar, E.C., C. Mallard, and T.L. Powell. 2006. Expression and subcellular localization of TLR-4 in term and first trimester human placenta. Placenta 27 (2–3): 322–326. https://doi.org/10.1016/j.placenta.2004.12.012.

    Article  CAS  PubMed  Google Scholar 

  49. Lye, P., E. Bloise, M. Javam, W. Gibb, S.J. Lye, and S.G. Matthews. 2015. Impact of bacterial and viral challenge on multidrug resistance in first- and third-trimester human placenta. The American Journal of Pathology 185 (6): 1666–1675. https://doi.org/10.1016/j.ajpath.2015.02.013.

    Article  CAS  PubMed  Google Scholar 

  50. Kirsten, T.B., and M.M. Bernardi. 2017. Prenatal lipopolysaccharide induces hypothalamic dopaminergic hypoactivity and autistic-like behaviors: Repetitive self-grooming and stereotypies. Behavioural Brain Research 331: 25–29. https://doi.org/10.1016/j.bbr.2017.05.013.

    Article  CAS  PubMed  Google Scholar 

  51. Custódio, C.S., B.S.F. Mello, A.J.M.C. Filho, C.N. de Carvalho Lima, R.C. Cordeiro, and F. Miyajima. 2018. Neonatal immune challenge with lipopolysaccharide triggers long-lasting sex- and age-related behavioral and immune/Neurotrophic alterations in mice: Relevance to autism Spectrum disorders. Molecular Neurobiology 55 (5): 3775–3788. https://doi.org/10.1007/s12035-017-0616-1.

    Article  CAS  PubMed  Google Scholar 

  52. Foley, K.A., D.F. MacFabe, M. Kavaliers, and K.P. Ossenkopp. 2015. Sexually dimorphic effects of prenatal exposure to lipopolysaccharide, and prenatal and postnatal exposure to propionic acid, on acoustic startle response and prepulse inhibition in adolescent rats: Relevance to autism spectrum disorders. Behavioural Brain Research 278: 244–225. https://doi.org/10.1007/s12035-017-0616-1.

    Article  CAS  PubMed  Google Scholar 

  53. Pradhan, S., and K. Andreasson. 2013. Commentary: Progressive inflammation as a contributing factor to early development of Parkinson’s disease. Experimental Neurology 241: 148–155. https://doi.org/10.1016/j.expneurol.2012.12.008.

    Article  PubMed  Google Scholar 

  54. Choi, I., D.J. Choi, H. Yang, J.H. Woo, M.Y. Chang, J.Y. Kim, W. Sun, S.M. Park, I. Jou, S.H. Lee, and E.H. Joe. 2016. PINK1 expression increases during brain development and stem cell differentiation, and affects the development of GFAP-positive astrocytes. Molecular Brain 9: 5. https://doi.org/10.1186/s13041-016-0186-6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Alexander, G.E. 2004. Biology of Parkinson’s disease: Pathogenesis and pathophysiology of a multisystem neurodegenerative disorder. Dialogues in Clinical Neuroscience 6: 259–280.

    PubMed  PubMed Central  Google Scholar 

  56. Lotankar, S., K.S. Prabhavalkar, and L.K. Bhatt. 2017. Biomarkers for Parkinson’s disease: Recent advancement. Neuroscience Bulletin 33 (5): 585–597. https://doi.org/10.1007/s12264-017-0183-5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. De Virgilio, A., A. Greco, G. Fabbrini, M. Inghilleri, M.I. Rizzom, A. Gallo, M. Conte, C. Rosato, M. Ciniglio Appiani, and M. de Vincentiis. 2016. Parkinson’s disease: Autoimmunity and neuroinflammation. Autoimmunity Reviews 15 (10): 1005–1011. https://doi.org/10.1016/j.autrev.2016.07.022.

    Article  CAS  PubMed  Google Scholar 

  58. Konno, T., J. Siuda, and Z.K. Wszolek. 2016. Genetics of Parkinson’s disease: A review of SNCA and LRRK2. Wiadomości Lekarskie 69: 328–332.

    PubMed  Google Scholar 

  59. Calne, D.B., and J.W. Langston. 1983. Aetiology of Parkinson’s disease. Lancet 2 (8365–8366): 1457–1459.

    Article  CAS  Google Scholar 

  60. Ling, Z.D., Q. Chang, J.W. Lipton, C.W. Tong, T.M. Landers, and P.M. Carvey. 2004. Combined toxicity of prenatal bacterial endotoxin exposure and postnatal 6-hydroxydopamine in the adult rat midbrain. Neuroscience 124: 619–628. https://doi.org/10.1016/j.neuroscience.2003.12.017.

    Article  CAS  PubMed  Google Scholar 

  61. Ling, Z., Q.A. Chang, C.W. Tong, S.E. Leurgans, J.W. Lipton, and P.M. Carvey. 2004. Rotenone potentiates dopamine neuron loss in animals exposed to lipopolysaccharide prenatally. Experimental Neurology 190: 373–383. https://doi.org/10.1016/j.expneurol.2004.08.006.

    Article  CAS  PubMed  Google Scholar 

  62. Richardson, J.R., W.M. Caudle, M. Wang, E.D. Dean, K.D. Pennell, and G.W. Miller. 2006. Developmental exposure to the pesticide dieldrin alters the dopamine system and increases neurotoxicity in an animal model of Parkinson’s disease. The FASEB Journal 20: 1695–1697. https://doi.org/10.1096/fj.06-5864fje.

    Article  CAS  PubMed  Google Scholar 

  63. Lloyd, S.A., C.J. Faherty, and R.J. Smeyne. 2006. Adult and in utero exposure to cocaine alters sensitivity to the Parkinsonian toxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Neuroscience 137: 905–913. https://doi.org/10.1016/j.neuroscience.2005.09.035.

    Article  CAS  PubMed  Google Scholar 

  64. Machado, V., S.J. Haas, O. von Bohlen Und Halbach, A. Wree, K. Krieglstein, K. Unsicker, and B. Spittau. 2016. Growth/differentiation factor-15 deficiency compromises dopaminergic neuron survival and microglial response in the 6-hydroxydopamine mouse model of Parkinson’s disease. Neurobiology of Disease 88: 1–15. https://doi.org/10.1016/j.nbd.2015.12.016.

    Article  CAS  PubMed  Google Scholar 

  65. Chen, S., Y. Liu, Y. Niu, Y. Xu, Q. Zhou, X. Xu, J. Wang, and M. Yu. 2017. Increased abundance of myeloid-derived suppressor cells and Th17 cells in peripheral blood of newly-diagnosed Parkinson’s disease patients. Neuroscience Letters 648: 21–25. https://doi.org/10.1016/j.neulet.2017.03.045.

    Article  CAS  PubMed  Google Scholar 

  66. Sommer, A., B. Winner, and I. Prots. 2017. The Trojan horse-neuroinflammatory impact of T cells in neurodegenerative diseases. Molecular Neurodegeneration 12 (1): 78. https://doi.org/10.1186/s13024-017-0222-8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Rathnayake, D., T. Chang, and P. Udagama. 2019. Selected serum cytokines and nitric oxide as potential multi-marker biosignature panels for Parkinson disease of varying durations: A case-control study. BMC Neurology 19: 56. https://doi.org/10.1186/s12883-019-1286-6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Kim, R., H.J. Kim, A. Kim, M. Jang, A. Kim, Y. Kim, D. Yoo, J.H. Im, J.H. Choi, and B. Jeon. 2018. Peripheral blood inflammatory markers in early Parkinson’s disease. Journal of Clinical Neuroscience 58: 30–33. https://doi.org/10.1016/j.jocn.2018.10.079.

    Article  PubMed  Google Scholar 

  69. Ling, Z., D.A. Gayle, S.Y. Ma, J.W. Lipton, C.W. Tong, J.S. Hong, and P.M. Carvey. 2002. In utero bacterial endotoxin exposure causes loss of tyrosine hydroxylase neurons in the postnatal rat midbrain. Movement Disorders 17 (1): 116–124. https://doi.org/10.1002/mds.10078.

    Article  PubMed  Google Scholar 

  70. Ling, Z., Y. Zhu, C.W. Tong, J.A. Snyder, J.W. Lipton, and P.M. Carvey. 2009. Prenatal lipopolysaccharide does not accelerate progressive dopamine neuron loss in the rat as a result of normal aging. Experimental Neurology 216: 312–320. https://doi.org/10.1016/j.expneurol.2008.12.004.

    Article  CAS  PubMed  Google Scholar 

  71. Bernardi, M.M., T.B. Kirsten, S.M. Matsuoka, E. Teodorov, S.F. Habr, S.H. Penteado, and J. Palermo-Neto. 2010. Prenatal lipopolysaccharide exposure affects maternal behavior and male offspring sexual behavior in adulthood. Neuroimmunomodulation 17: 47–55. https://doi.org/10.1159/000243085.

    Article  CAS  PubMed  Google Scholar 

  72. Solati, J., R. Hajikhani, B. Rashidieh, and M.F. Jalilian. 2012. Effects of prenatal lipopolysaccharide exposure on reproductive activities and serum concentrations of pituitary-gonadal hormones in mice offspring. International Journal of Fertility and Sterility 6: 51–58.

    PubMed  Google Scholar 

  73. Wang, H., L.L. Yang, Y.F. Hu, B.W. Wang, Y.Y. Huang, C. Zhang, Y.H. Chen, and D.X. Xu. 2014. Maternal LPS exposure during pregnancy impairs testicular development, steroidogenesis and spermatogenesis in male offspring. PLoS One 9 (9). https://doi.org/10.1371/journal.pone.0106786.

  74. Ashdown, H., Y. Dumont, M. Ng, S. Poole, P. Boksa, and G.N. Luheshi. 2006. The role of cytokines in mediating effects of prenatal infection on the fetus: Implications for schizophrenia. Molecular Psychiatry 11: 47–55. https://doi.org/10.1038/sj.mp.4001748.

    Article  CAS  PubMed  Google Scholar 

  75. Liverman, C.S., H.A. Kaftan, L. Cui, S.G. Hersperger, E. Taboada, R.M. Klein, and N.E. Berman. 2006. Altered expression of pro-inflammatory and developmental genes in the fetal brain in a mouse model of maternal infection. Neuroscience Letters 399 (3): 220–225. https://doi.org/10.1016/j.neulet.2006.01.064.

    Article  CAS  PubMed  Google Scholar 

  76. Bornstein, S.R., H. Rutkowski, and I. Vrezas. 2004. Cytokines and steroidogenesis. Molecular and Cellular Endocrinology 215 (1–2): 135–141. https://doi.org/10.1016/j.mce.2003.11.022.

    Article  CAS  PubMed  Google Scholar 

  77. Skinner, M.K. 2005. Regulation of primordial follicle assembly and development. Human Reproduction Update 11 (5): 461–471. https://doi.org/10.1093/humupd/dmi020.

    Article  PubMed  Google Scholar 

  78. Cheng, L., D.P. Gearing, L.S. White, D.L. Compton, K. Schooley, and P.J. Donovan. 1994. Role of leukemia inhibitory factor and its receptor in mouse primordial germ cell growth. Development 120 (11): 3145–3153.

    CAS  PubMed  Google Scholar 

  79. Eddie, S.L., A.J. Childs, H.N. Jabbour, and R.A. Anderson. 2012. Developmentally regulated IL6-type cytokines signal to germ cells in the human fetal ovary. Molecular Human Reproduction 18: 88–95. https://doi.org/10.1093/molehr/gar061.

    Article  CAS  PubMed  Google Scholar 

  80. Izvolskaia, M.S., V.S. Sharova, V.M. Ignatiuk, S.N. Voronova, and L.A. Zakharova. 2019. Abolition of prenatal lipopolysaccharide-induced reproductive disorders in rat male offspring by fulvestrant. Andrologia 51: e13204. https://doi.org/10.1111/and.13204.

    Article  CAS  PubMed  Google Scholar 

  81. Williams, K., C. McKinnell, P.T. Saunders, M. Walker, J.S. Fisher, K.J. Turner, N. Atanassova, and M. Sharpe. 2001. Neonatal exposure to potent and environmental oestrogens and abnormalities of the male reproductive system in the rat: Evidence for importance of the androgen-oestrogen balance and assessment of the relevance to man. Human Reproduction Update 7: 236–247. https://doi.org/10.1677/JOE-09-0109.

    Article  CAS  PubMed  Google Scholar 

  82. Chen, Y., K. Breen, and M.E. Pepling. 2009. Estrogen can signal through multiple pathways to regulate oocyte cyst breakdown and primordial follicle assembly in the neonatal mouse ovary. The Journal of Endocrinology 202 (3): 407–417. https://doi.org/10.1677/JOE-09-0109.

    Article  CAS  PubMed  Google Scholar 

  83. Talmor, A., and B. Dunphy. 2015. Female obesity and infertility. Best Practice & Research. Clinical Obstetrics & Gynaecology 29 (4): 498–506. https://doi.org/10.1016/j.bpobgyn.2014.10.014.

    Article  Google Scholar 

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Funding

This work was conducted under the Institute of Developmental Biology Russian Academy of Sciences Government basic research program, No. 0108–2019-0002.

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Authors and Affiliations

  1. Koltzov Institute of Developmental Biology, Russian Academy of Sciences, 26 Vavilov Street, Moscow, 119334, Russia

    Marina Izvolskaia, Viktoriya Sharova & Liudmila Zakharova

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  1. Marina Izvolskaia
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  2. Viktoriya Sharova
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  3. Liudmila Zakharova
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Correspondence to Viktoriya Sharova.

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All experimental procedures described in this study have been approved by the Animal Ethics Committee of Koltzov Institute of Developmental Biology Russian Academy of Sciences.

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Izvolskaia, M., Sharova, V. & Zakharova, L. Perinatal Inflammation Reprograms Neuroendocrine, Immune, and Reproductive Functions: Profile of Cytokine Biomarkers. Inflammation 43, 1175–1183 (2020). https://doi.org/10.1007/s10753-020-01220-1

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