Testosterone enhancement during pregnancy influences social coping and gene expression of oxytocin and vasopressin in the brain of adult rats

• Autorzy: Dzirbikova Z. , Talarovicova A. , Stefanik P. , Olexova L. , Krskova L.
• Języki publikacji: EN

Abstrakty

EN

Steroid hormones are important mediators of prenatal maternal effects and play an important role in fetal programming. The aim of our study was to investigate how testosterone enhancement during pregnancy influences neurobehavioral aspects of social coping of rat offspring in adulthood. Pregnant rat dams were exposed to depot form of testosterone during the last third of pregnancy (i.e., beginning on the 14th day of pregnancy). Their adult offspring were later tested in a social interaction test and expression of oxytocin and arginine-vasopressin mRNA in the hypothalamic nuclei was evaluated. Our research showed that prenatal exposure to higher levels of testosterone activated socio‑cohesive and socio‑aversive interactions, but only in males. The testosterone‑exposed group also showed decreased oxytocin mRNA expression in the supraoptic and paraventricular nuclei of the hypothalamus, and increased arginine-vasopressin mRNA expression in the supraoptic and suprachiasmatic nuclei as compared to controls. However, we did not observe any sex differences in the expression of oxytocin and arginine‑vasopressin mRNA in these regions. Our findings show that testosterone enhancement in pregnancy could have long‑lasting effects on oxytocin and arginine-vasopressin levels in the brain of adult animals, but lead to changes in behavioral aspects of coping strategies only in males.

• Wydawca: -
• Czasopismo: Acta Neurobiologiae Experimentalis
• Rocznik: 2018
• Tom: 78
• Numer: 3
• Opis fizyczny: p.264-270,fig.,ref.

Twórcy

autor

Dzirbikova Z.

• Department of Animal Physiology and Ethology, Faculty of Natural Sciences, Comenius University in Bratislava, Bratislava, Slovakia

autor

Talarovicova A.

• Department of Biological Sciences, North Carolina State University, Raleigh, North Carolina, USA

autor

Stefanik P.

• Department of Animal Physiology and Ethology, Faculty of Natural Sciences, Comenius University in Bratislava, Bratislava, Slovakia

autor

Olexova L.

• Department of Animal Physiology and Ethology, Faculty of Natural Sciences, Comenius University in Bratislava, Bratislava, Slovakia

autor

Krskova L.

• Department of Animal Physiology and Ethology, Faculty of Natural Sciences, Comenius University in Bratislava, Bratislava, Slovakia

Bibliografia

• Auyeung B, Lombardo MV, Baron‑Cohen S (2013) Prenatal and postnatal hormone effects on the human brain and cognition. Pflugers Arch 465: 557–571.
• Bao AM, Swaab DF (2010) Sex differences in the brain, behavior, and neuropsychiatric disorders. Neuroscientist 16: 550–565.
• Baron‑Cohen S, Auyeung B, Nørgaard‑Pedersen B, Hougaard DM, Abdallah MW, Melgaard  L, Cohen AS, Chakrabarti B, Ruta  L, Lombardo MV (2015) Elevated fetal steroidogenic activity in autism. Mol Psychiatry 20: 369–376.
• Baron‑Cohen S, Knickmeyer RC, Belmonte MK (2005) Sex differences in the brain: implications for explaining autism. Science 310: 819–823.
• Baum MJ, Woutersen PJ, Slob AK (1991) Sex difference in whole‑body androgen content in rats on fetal days 18 and 19 without evidence that androgen passes from males to females. Biol Reprod 44: 747–751.
• Bayer SA, Altman J (2004) Development of the telencephalon: neural stem cells, neurogenesis, and neuronal migration. In: The rat nervous system (Paxinos G, Ed.). Academic Press, New York, p. 27–73.
• Celec P, Ostatnikova D, Hodosy J (2015) On the effects of testosterone on brain behavioral functions. Front Neurosci 9: 12.
• Coppens CM, De Boer SF, Koolhaas JM (2010) Coping styles and behavioral flexibility: towards underlying mechanisms. Philos Trans R Soc Lond B Biol Sci 365: 4021–4028.
• Dela Cruz C, Pereira OC (2012) Prenatal testosterone supplementation alters puberty onset, aggressive behavior, and partner preference in adult male rats. J Physiol Sci 62: 123–131.
• Dhakar MB, Stevenson EL, Caldwell HK (2013) Oxytocin, vasopressin and their interplay with gonadal steroids. Oxytocin, Vasopressin, and Related Peptides in the Regulation of Behavior (Choleris E., Pfaff DW, Kavaliers M, Eds.). Cambridge University Press, New York, p. 20–56.
• Dloniak SM, French JA, Holekamp KE (2006) Rank‑related maternal effects of androgens on behavior in wild spotted hyaenas. Nature 440: 1190–1193.
• Dumais KM, Bredewold R, Mayer TE, Veenema AH (2013) Sex differences in oxytocin receptor binding in forebrain regions: Correlations with social interest in brain region‑ and sex‑ specific ways. Horm Behav 64: 693–701.
• Dumais KM, Veenema AH (2016) Vasopressin and oxytocin receptor systems in the brain: Sex differences and sex‑specific regulation of social behavior. Front Neuroendocrinol 40: 1–23.
• Dzirbikova Z, Kiss A, Okuliarova M, Kopkan L, Cervenka L (2011) Expressions of per1 clock gene and genes of signaling peptides vasopressin, vasoactive intestinal peptide, and oxytocin in the suprachiasmatic and paraventricular nuclei of hypertensive TGR[mREN2]27 rats. Cell Mol Neurobiol 31: 225–232.
• File SE (1980) The use of social interaction as a method for detecting anxiolytic activity of chlordiazepoxide‑like drugs. J  Neurosci Methods 2: 219–238.
• Filova B, Ostatnikova D, Celec P, Hodosy J (2013) The effect of testosterone on the formation of brain structures. Cells Tissues Organs 197: 169–177.
• Geschwind N, Galaburda AM (1985) Cerebral lateralisation: Biological mechanisms, associations and pathology: III. A hypothesis and a program for research. Arch Neurol 42: 634–654.
• Groothuis TG, Müller W, von Engelhardt N, Carere C, Eising C (2005) Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci Biobehav Rev 29: 329–352.
• Heinrichs M, von Dawans B, Domes G (2009) Oxytocin, vasopressin, and human social behavior. Front Neuroendocrinol 30: 548–557.
• Insel TR, Winslow JT, Wang Z, Young LJ (1998) Oxytocin, vasopressin, and the neuroendocrine basis of pair bond formation. Adv Exp Med Biol 449: 215–224.
• Jac M, Kiss A, Sumova A, Illnerova H, Jezova D (2000) Daily profiles of arginine vasopressin mRNA in the suprachiasmatic, supraoptic and paraventricular nuclei of the rat hypothalamus under various photoperiods. Brain Res 887: 472–476.
• Kaiser S, Sachser N (2009) Effects of prenatal social stress on offspring development: pathology or adaptation? Curr Dir Psychol Sci 18: 118–121.
• Kapoor A, Matthews SG (2011) Testosterone is involved in mediating the effects of prenatal stress in male guinea pig offspring. J  Physiol 589: 755–766.
• Kemme K, Kaiser S, Sachser N (2007) Prenatal maternal programming determines testosterone response during social challenge. Horm Behav 51: 387–394.
• Kimura T, Makino Y, Saji F, Takemura  M, Inoue T, Kikuchi T, Kubota Y, Azuma C, Nobunaga T, Tokugawa Y, Tanizawa O (1994) Molecular characterization of a cloned human receptor. Eur J Endocrinol 131: 385–390.
• Knickmeyer RC, Baron‑Cohen S (2006) Fetal testosterone and sex differences in typical social development and in autism. J Child Neurol 21: 825–845.
• Koehbach J, Stockner T, Bergmayr C, Muttenthaler M, Gruber CW (2013) Insights into the molecular evolution of oxytocin receptor ligand binding. Biochem Soc Trans 41: 197–204.
• Koolhaas JM, de Boer SF, Coppens CM, Buwalda B (2010) Neuroendocrinology of coping styles: towards understanding the biology of individual variation. Front Neuroendocrinol 31: 307–321.
• Koolhaas JM, Korte SM, de Boer SF, van der Vegt BJ, van Reenen CG, Hopster H, De Jong IC, Ruis MA, Blokhuis HJ (1999) Coping styles in animals: current status in behavior and stress‑physiology. Neurosci Biobehav Rev 23: 925–935.
• Lombardo MV, Ashwin E, Auyeung B, Chakrabarti B, Lai MC, Taylor K, Hackett G, Bullmore ET, Baron‑Cohen S (2012) Fetal programming effects of testosterone on the reward system and behavioral approach tendencies in humans. Biol Psychiatry 72: 839–847.
• Martel MM (2013) Sexual selection and sex differences in the prevalence of childhood externalizing and adolescent internalizing disorders. Psychol Bull 139: 1221–1259.
• Martel MM, Roberts BA (2014) Prenatal testosterone increases sensitivity to prenatal stressors in males with disruptive behavior disorders. Neurotoxicol Teratol 44: 11–17.
• Meyer‑Lindenberg A, Domes G, Kirsch P, Heinrichs M (2011) Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine. Nat Rev Neurosci 12: 524–538.
• Mousseau TA, Fox CW (1998) The adaptive significance of maternal effects. Trends Ecol Evol 13: 403–407.
• Neumann ID, Slattery DA (2016) Oxytocin in general anxiety and social fear: a translational approach. Biol Psychiatry 79: 213–221.
• O’Connor TG, Barrett ES (2014) Mechanisms of prenatal programing: identifying and distinguishing the impact of steroid hormones. Front Endocrinol 5: 52.
• Patisaul HB, Scordalakes EM, Young LJ, Rissman EF (2003) Oxytocin, but not oxytocin receptor, is regulated by oestrogen receptor ß in the female mouse hypothalamus. J Neuroendocrinol 15: 787–793.
• Paul MJ, Terranova JI, Probst CK, Murray EK, Ismail NI, de Vries GJ (2014) Sexually dimorphic role for vasopressin in the development of social play. Front Behav Neurosci 8: 58.
• Pivina SG, Akulova VK, Ordyan NE (2007) Characteristics of behavior and stress reactivity of the hypophyseal‑adrenocortical system in rats with prenatal inhibition of testosterone metabolism. Neurosci Behav Physiol 37: 53–58.
• Song Z, McCann KE, McNeill JK IV, Larkin TE II, Huhman KL, Albers HE (2014) Oxytocin induces social communication by activating arginine‑vasopressin V1a receptors and not oxytocin receptors. Psychoneuroendocrinology 50: 14–19.
• Steinman MQ, Trainor BC (2017) Sex differences in the effects of social defeat on brain and behavior in the California mouse: Insights from a monogamous rodent. Semin Cells Dev Biol 61: 92–98.
• Talarovičová A, Kršková L, Blažeková J (2009) Testosterone enhancement during pregnancy influences the 2D:4D ratio and open field motor activity of rat siblings in adulthood. Horm Behav 55: 235–239.
• Taylor PV, Veenema AH, Paul MJ, Bredewold R, Isaacs S, de Vries GJ (2012) Sexually dimorphic effects of a prenatal immune challenge on social play and vasopressin expression in juvenile rats. Biol Sex Differ 3: 15. Weinberg J, Sliwowska JH, Lan N, Hellemans KGC (2008) Prenatal alcohol exposure: foetal programming, the hypothalamic‑pituitary‑adrenal axis and sex differences in outcome. J Neuroendocrinol 20: 470–488.
• Weisz J, Ward IL (1980) Plasma testosterone and progesterone titers of pregnant rats, their male and female fetuses, and neonatal offspring. Endocrinology 106: 306–316.
• Wolf CJ, Hotchkiss A, Ostby JS, LeBlanc GA, Gray LE Jr (2002) Effects of prenatal testosterone propionate on the sexual development of male and female rats: a dose‑response study. Toxicol Sci 65: 71–86.
• Xu XJ, Zhang HF, Shou XJ, Li J, Jing WL, Zhou Y, Qian Y, Han SP, Zhang R, Han  JS (2015) Prenatal hyperandrogenic environment induced autistic‑like behavior in rat offspring. Physiol Behav 13: 13–20.

Identyfikatory

DOI

10.21307/ane‑2018‑024