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Stress
The International Journal on the Biology of Stress
Volume 19, 2016 - Issue 2
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Original Research Report

Disruptions in the hypothalamic–pituitary–gonadal axis in rat offspring following prenatal maternal exposure to lipopolysaccharide

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Pages 198-205 | Received 01 Aug 2015, Accepted 30 Jan 2016, Published online: 03 Mar 2016

References

  • Alarid ET, Windle JJ, Whyte DB, Mellon PL. (1996). Immortalization of pituitary cells at discrete stages of development by directed oncogenesis in transgenic mice. Development 122(10):3319–29
  • Altman J, Bayer SA. (1987). Atlas of prenatal rat brain development. Boca Raton, FL: CRC Press
  • Amath A, Foster JA, Sidor MM. (2012). Developmental alterations in CNS stress-related gene expression following postnatal immune activation. Neuroscience 220:90–9
  • Ashdown H, Dumont Y, Ng M, Poole S, Boksa P, Luheshi GN. (2006). The role of cytokines in mediating effects of prenatal infection on the fetus: implications for schizophrenia. Mol Psychiatry 11:47–55
  • Basta-Kaim A, Fijał K, Ślusarczyk J, Trojan E, Głombik K, Budziszewska B, Leśkiewicz M, et al (2015). Prenatal administration of lipopolysaccharide induces sex-dependent changes in glutamic acid decarboxylase and parvalbumin in the adult rat brain. Neuroscience 287:78–92
  • Ben-Ari Y, Khazipov R, Leinekugel X, Caillard O, Gaiarsa JL. (1997). GABAA, NMDA and AMPA receptors: a developmentally regulated ‘ménage à trois’. Trends Neurosci 20:523–9
  • Ben-Ari Y. (2001). Developing networks play a similar melody. Trends Neurosci 24:353–60
  • Breen K, Brown A, Burd I, Chai J, Friedman A, Elovitz MA. (2012). TLR-4-dependent and -independent mechanisms of fetal brain injury in the setting of preterm birth. Reprod Sci 19:839–50
  • Cai Z, Pan ZL, Pang Y, Evans OB, Rhodes PG. (2000). Cytokine induction in fetal rat brains and brain injury in neonatal rats after maternal lipopolysaccharide administration. Pediatr Res 47:64–72
  • Caraty A, Locatelli A, Moenter SM, Karsch FJ. (1994). Sampling of hypophyseal portal blood of conscious sheep for direct monitoring of hypothalamic neurosecretory substances. In: Levine JE, editor. Methods in neuroscience. San Diego, CA: Academic Press. p. 163al–bl
  • Carreau S, Bouraima-Lelong H, Delalande C. (2012). Estrogen, a female hormone involved in spermatogenesis. Adv Med Sci 57(1):31–6
  • Chattopadhyay N, Jeong KH, Yano S, Huang S, Pang JL, Ren X, Terwilliger E, et al (2007). Calcium receptor stimulates chemotaxis and secretion of MCP-1 in GnRH neurons in vitro: potential impact on reduced GnRH neuron population in CaR-null mice. Am J Physiol Endocrinol Metab 292(2):E523–32
  • Check JN. (1995). Falsely elevated steroidal assay levels repeated to heterophile antibodies against various animal species. Gynecol Obstet Invest 40:139–40
  • Dozio E, Ruscica M, Galliera E, Corsi MM, Magni P. (2009). Leptin, ciliary neurotrophic factor, leukemia inhibitory factor and interleukin-6: class-I cytokines involved in the neuroendocrine regulation of the reproductive function. Curr Protein Pept Sci 10:577–84
  • Dygalo NN, Shemenkova TV2, Kalinina TS, Shishkina GT. (2014). A critical point of male gonad development: neuroendocrine correlates of accelerated testicular growth in rats during early life. PLoS One 9(4):e93007
  • Gonzales RJ, Ansar S, Duckles SP, Krause DN. (2007). Androgenic/estrogenic balance in the male rat cerebral circulation: metabolic enzymes and sex steroid receptors. J Cereb Blood Flow Metab Off J Int Soc 27:1841–52
  • Herde MK, Iremonger KJ, Constantin S, Herbison AE. (2013). GnRH neurons elaborate a long-range projection with shared axonal and dendritic functions. J Neurosci 33(31):12689–97
  • Herman AP, Tomaszewska-Zaremba D. (2010). Effect of endotoxin on the expression of GnRH and GnRHR genes in the hypothalamus and anterior pituitary gland of anestrous ewes. Anim Reprod Sci 120:105–11
  • Iwasa T, Matsuzaki T, Kinouchi R, Fujisawa S, Murakami M, Kiyokawa M. (2009). Neonatal LPS injection alters the body weight regulation systems of rats under non-stress and immune stress conditions. Int J Dev Neurosci 28:119–24
  • Jasoni CL, Porteous RW, Herbison AE. (2009). Anatomical location of mature GnRH neurons corresponds with their birthday in the developing mouse. Dev Dyn 238:524
  • Kalra PS, Edwards TG, Xu B, Jain M, Kalra SP. (1998). The anti-gonadotropic effects of cytokines: the role of neuropeptides. Domest Anim Endocrinol 15:321–32
  • Kimura M, Yu WH, Rettori V, McCann SM. (1997). Granulocyte-macrophage colony stimulating factor suppresses LHRH release by inhibition of nitric oxide synthase and stimulation of gamma-aminobutyric acid release. Neuroimmunomodulation 4:237–43
  • Kirsten TB, Lippi LL, Bevilacqua E, Bernardi MM. (2013). LPS exposure increases maternal corticosterone levels, causes placental injury and increases IL-1Β levels in adult rat offspring: relevance to autism. PLoS One 8(12):e82244
  • Knox AM, Li XF, Kinsey-Jones JS, Wilkinson ES, Wu XQ, Cheng YS, Milligan SR, et al (2009). Neonatal lipopolysaccharide exposure delays puberty and alters hypothalamic Kiss1 and Kiss1r mRNA expression in the female rat. J Neuroendocrinol 21:683–9
  • Li X, Shao B, Lin C, O’Byrne KT, Lin Y. (2015). Stress-induced inhibition of LH pulses in female rats: role of GABA in arcuate nucleus. J Mol Endocrinol 55(1):9–19
  • Lindzey J, Wetsel WC, Couse JF, Stoker T, Cooper R, Korach KS. (1998). Effects of castration and chronic steroid treatments on hypothalamic gonadotropin-releasing hormone content and pituitary gonadotropins in male wild-type and estrogen receptor-alpha knockout mice. Endocrinology 139(10):4092–101
  • Low VF, Fiorini Z, Fisher L, Jasoni CL. (2012). Netrin-1 stimulates developing GnRH neurons to extend neurites to the median eminence in a calcium-dependent manner. PLoS One 7(10):e46999
  • Luu-The V, Labrie F. (2010). The intracrine sex steroid biosynthesis pathways. Prog Brain Res 181:177–92
  • Magni P, Dozio E, Ruscica M, Watanobe H, Cariboni A, Zaninetti R, Motta M, Maggi R. (2007). 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 21(5):1163–74
  • McCann SM, Kimura M, Karanth S, Yu WH, Mastronardi CA. (2000). The mechanism of action of cytokines to control the release of hypothalamic and pituitary hormones in infection. Ann N Y Acad Sci 917:4–18
  • Melnikova VI, Sharova NP, Maslova EV, Voronova SN, Zakharova LA. (2010). Ontogenesis of rat immune system: proteasome expression in different cell populations of the developing thymus. Cell Immunol 266:83–9
  • Mouihate A, Mehdawi H. (2015). Toll-like receptor 4-mediated immune stress in pregnant rats activates STAT3 in the fetal brain: role of interleukin-6. Pediatr Res. [Epub ahead of print]. doi:10.1038/pr.2015.86
  • Munkhzaya M, Matsuzaki T, Iwasa T, Tungalagsuvd A, Kawami T, Kato T, Kuwahara A, Irahara M. (2015). The suppressive effect of immune stress on LH secretion is absent in the early neonatal period in rats. Int J Dev Neurosci 46:38–43
  • Nagai Y, Akashi S, Nagafuku M, Ogata M, Iwakura Y, Akira S, Kitamura T, et al (2002). Essential role of MD2 in LPS responsiveness and TLR4 distribution. Nat Immunol 3:667–72
  • Nemeskeri A, Kurcz M, Halasz B. (1984). Changes in hypophyseal luteinizing hormone (LH) content during fetal and early postnatal life, and capacity of fetal and early postnatal pituitaries to synthesize and release LH in vitro. Neuroendocrinology 38(5):393–6
  • Pallarés ME, Adrover E, Baier CJ, Bourguignon NS, Monteleone MC, Brocco MA, González-Calvar SI, Antonelli MC. (2013). Prenatal maternal restraint stress exposure alters the reproductive hormone profile and testis development of the rat male offspring. Stress 16(4):429–40
  • Pinilla L, Trimiño E, Garnelo P, Bellido C, Aguilar R, Gaytán F, Aguilar E. (1993). Changes in pituitary secretion during the early postnatal period and anovulatory syndrome induced by neonatal oestrogen or androgen in rats. J Reprod Fertil 97:13–20
  • Sharova VS, Izvolskaia MS, Voronova SN, Zakharova LA. (2011). Effect of bacterial endotoxin on migration of gonadotropin-releasing hormone producing neurons in rat embryogenesis. J Dev Biol 42:439–46
  • Sharova VS, Izvolskaya MS, Zakharova LA. (2013). Effect of prenatal infection of mice with bacterial endotoxin on the migration of neurons producing gonadotropin-releasing hormone. Dokl Biol Sci 452:273–6
  • Sharova VS, Izvolskaia MS, Zakharova LA. (2015). Lipopolysaccharide-induced maternal inflammation affects the gonadotropin-releasing hormone neuron development in fetal mice. Neuroimmunomodulation 22(4):222–32
  • Simpson ER, Michael MD, Agarwal VR, Hinshelwood MM, Bulun SE, Zhao Y. (1997). Cytochromes P450 11: expression of the CYP19 (aromatase) gene: an unusual case of alternative promoter usage. FASEB J 11(1):29–36
  • Sominsky L, Meehan CL, Walker AK, Bobrovskaya L, McLaughlin EA, Hodgson DM. (2012). Immune regulation of ovarian development:programming by neonatal immune challenge. Horm Behav Behav 62:345–55
  • Spencer SJ, Boisse L, Mouihate A, Pittman QJ. (2006). Long term alterations in neuroimmune responses of female rats after neonatal exposure to lipopolysaccharide. Brain Behav Immun 20:325–30
  • Straley ME, Togher KL, Nolan AM, Kenny LC, O’Keeffe GW. (2014). LPS alters placental inflammatory and endocrine mediators and inhibits fetal neurite growth in affected offspring during late gestation. Placenta 35:533–8
  • Teixeira CV, Silandre D, de Souza Santos AM, Delalande C, Sampaio FJ, Carreau S, da Fonte Ramos C. (2007). Effects of maternal undernutrition during lactation on aromatase, estrogen, and androgen receptors expression in rat testis at weaning. J Endocrinol 192(2):301–11
  • Walker FR, Hodyl NA, Hodgson DM. (2009). Neonatal bacterial endotoxin challenge interacts with stress in the adult male rat to modify KLH specific antibody production but not KLH stimulated ex vivo cytokine release. J. Neuroimmunol. 207:57–65
  • Wang S, Yan JY, Lo YK, Carvey PM, Ling Z. (2009). Dopaminergic and serotoninergic deficiencies in young adult rats prenatally exposed to the bacterial lipopolysaccharide. Brain Res 1265(10):196–204
  • Wang H, Yang LL, Hu YF, Wang BW, Huang YY, Zhang C, Chen YH, Xu DX. (2014). Maternal LPS exposure during pregnancy impairs testicular development, steroidogenesis and spermatogenesis in male offspring. PLoS One 9(9):e106786
  • Weisz J, Gunsalus P. (1973). Estrogen levels in immature female rats: true or spurious – ovarian or adrenal? Endocrinology 93:1057–65
  • Wu XQ, Li XF, Ye B, Popat N, Milligan SR, Lightman SL, O’Byrne KT. (2011). Neonatal programming by immunological challenge: effects on ovarian function in the adult rat. Reproduction 141(2):241–8
  • Yamanaka C, Lebrethon MC, Vandersmissen E, Gerard A, Purnelle G, Lemaitre M, Wilk S, Bourguignon JP. (1999). Early prepubertal ontogeny of pulsatile gonadotropin-releasing hormone (GnRH) secretion: I. Inhibitory autofeedback control through prolyl endopeptidase degradation of GnRH. Endocrinology 140(10):4609–15
  • Yano H, Readhead C, Nakashima M, Ren SG, Melmed S. (1998). Pituitary-directed leukemia inhibitory factor transgene causes Cushing’s syndrome: neuro-immune-endocrine modulation of pituitary development. Mol Endocrinol 12(11):1708–20
  • Yao L, Kan EM, Lu J, Hao A, Dheen ST, Kaur C, Ling EA. (2013). Toll-like receptor 4 mediates microglial activation and production of inflammatory mediators in neonatal rat brain following hypoxia: role of TLR4 in hypoxic microglia. J Neuroinflammation 10:23
  • Zakharova LA, Izvolskaia MS. (2012). Interactions between the reproductive and immune systems during ontogenesis: the role of GnRH, sex steroids and immunomediators. In: Kahn SM, editor. “Sex steroids”. Zagreb: InTech. p. 341–70

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