Neonatal Exposure to Fenoterol and Betamethasone: Effects on the Behavioral Development in the Rat

REFERENCES

• Akirav I., Kozenicky M., Tal D., Sandi C., Venero C., Richter-Levin G. A facilitative role for corticosterone in the acquisition of a spatial task under moderate stress. Learning & Memory 2004; 11: 188–195
   PubMed Web of Science ®Google Scholar
• Anotayanonth S., Subhedar N. V., Garner P., Neilson J. P., Harigopal S. Betamimetics for inhibiting preterm labor. Cochrane Database of Systematic Reviews 2004; 1
   Google Scholar
• Avishai-Eliner S., Brunson K., Sandman C., Baram T. Stressed-out, or in (utero)?. Trends in Neuroscience 2002; 25: 518–524
   PubMed Web of Science ®Google Scholar
• Ballard P. L., Granberg P., Ballard R. A. Glucocorticoid levels in maternal and cord serum after prenatal betamethasone therapy to prevent respiratory distress syndrome. Journal of Clinical Investigation 1975; 56: 1548–1554
   PubMed Web of Science ®Google Scholar
• Benesova O., Pavlik A. Perinatal treatment with glucocorticoids and the risk of maldevelopment of the brain. Neuropharmacology 1988; 28: 89–97
   Google Scholar
• Boehringer Ingelheim KG. Partusisten® Fachinfo, , et al. Bundesverband der Pharmazeutischen Industrie e.V, AulendorfGermany 1996
   Google Scholar
• Brabham T., Phelka A., Zimmer C., Nash A., Lopez J. F., Vasquez D. M. Effects of prenatal dexamethasone on spatial learning and response to stress is influenced by maternal factors. American Journal of Physiology—Regulatory Integrative and Comparative Physiology 2000; 279: R1899–R1909
   PubMed Web of Science ®Google Scholar
• Bremner J. D., Vermetten E. Stress and development: Behavioral and biological consequences. Development and Psychopathology 2001; 13: 473–489
   PubMed Web of Science ®Google Scholar
• Brunello N., den Boer J. A., Judd L. L., Kasper S., Kelsey J. E., Lader M., et al. Social phobia: Diagnosis and epidemiology, neurobiology and pharmacology, comorbidity and treatment. Journal of Affective Disorders 2000; 60: 61–74
   PubMed Web of Science ®Google Scholar
• Buitelaar J. K., Huizink A. C., Mulder E. J., de Medina P. G., Visser G. H. Prenatal stress and cognitive development and temperament in infants. Neurobiology of Aging 2003; 24(Suppl 1)S53–S60
   Google Scholar
• Catalani A., Marinelli M., Scaccianoce S., Nicolai R., Muscolo L. A., Porcu A., et al. Progeny of mothers drinking corticosterone during lactation has lower stress-induced corticosterone secretion and better cognitive performance. Brain Research 1993; 624: 209–215
   PubMed Web of Science ®Google Scholar
• Claes S. J. Corticotropin-releasing hormone (CRH) in psychiatry: from stress to psychopathology. Annals of Medicine 2004; 36: 50–61
   PubMed Web of Science ®Google Scholar
• Coe C. L., Kramer M., Czeh B., Gould E., Reeves A. J., Kirschbaum C., et al. Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile rhesus monkeys. Biological Psychiatry 2003; 54: 1025–1034
   PubMed Web of Science ®Google Scholar
• Connors S. L., Crowell D. E., Eberhart C. G., Copeland J., Newschaffer C. J., Spence S. J., et al. Beta2-adrenergic receptor activation and genetic polymorphisms in autism: Data from dizygotic twins. Journal of Child Neurology 2005; 20: 876–884
   PubMed Web of Science ®Google Scholar
• Cratty M. S., Ward H. E., Johnson E. A., Azzaro A. J., Birkle D. L. Prenatal stress increases corticotrophin-releasing factor (CRF) content and release in rat amygdala. Brain Research 1995; 675: 297–302
   PubMed Web of Science ®Google Scholar
• Daniels W. M., Pietersen C. Y., Carstens M. E., Stein D. J. Maternal separation in rats leads to anxiety-like behavior and a blunted ACTH response and altered neurotransmitter levels in response to a subsequent stressor. Metabolic Brain Disease 2004; 19: 3–14
   PubMed Web of Science ®Google Scholar
• Davies M. F., Tsui J. Y., Flannery J. A., Li X., DeLorey T. M., Hoffman B. B. Augmentation of the noradrenergic system in alpha-2 adrenergic receptor deficient mice: Anatomical changes associated with enhanced fear memory. Brain Research 2003; 986: 157–165
   PubMedGoogle Scholar
• DeKosky S. T., Nonneman A. J., Scheff S. W. Morphologic and behavioral effects of perinatal glucocorticoid administration. Physiology & Behavior 1982; 29: 895–900
   PubMedGoogle Scholar
• de Weerth C., van Hees Y., Buitelaar J. K. Prenatal maternal cortisol levels and infant behavior during the first 5 months. Early Human Development 2003; 74: 139–151
   PubMed Web of Science ®Google Scholar
• Dobbing J., Sands J. Comparative aspects of the brain growth spurt. Early Human Development 1979; 3: 79–83
   PubMed Web of Science ®Google Scholar
• Drago F., Di Leo F., Giardina L. Prenatal stress induces body weight deficit and behavioral alterations in rats: The effect of diazepam. European Neuropsychopharmacology 1999; 9: 239–45
   PubMed Web of Science ®Google Scholar
• Dygalo N. N., Bannova A. V., Kalinina T. S., Shishkina G. T. Clonidine increases caspase-3 mRNA level and DNA fragmentation in the developing rat brainstem. Developmental Brain Research 2004; 152: 225–231
   PubMedGoogle Scholar
• Erdtsieck-Ernste E. B. H. W., Feenstra M. G. P., Botterblom M., Boer G. J. Postnatal exposure to the β-adrenoceptor agonist clenbuterol has regionally selective direct and long-term effects on rat brain β-adrenoceptors and monoamine metabolism. Developmental Brain Research 1993; 71: 27–35
   PubMedGoogle Scholar
• Escorihuela R. M., Fernandez-Teruel M., Tobena A., Vivas N. M., Marmol F., Badia A., et al. Early environmental stimulation produces long-lasting changes on β-adrenoceptor transduction system. Neurobiology of Learning and Memory 1995; 64: 49–57
   PubMedGoogle Scholar
• Ferguson S. A., Paule M. G., Holson R. R. Neonatal dexamethasone on day 7 in rats causes behavioral alterations reflective of hippocampal, but not cerebellar, deficits. Neurotoxicology and Teratology 2001; 23: 57–69
   PubMedGoogle Scholar
• Flagel S. B., Vasquez D. M., Watson S. J., Neal C. R. Effects of tapering neonatal dexamethasone on rat growth neurodevelopment and stress response. American Journal of Physiology—Regulatory Integrative and Comparative Physiology 2002; 282: R55–R63
   PubMed Web of Science ®Google Scholar
• Fujioka T., Fujioka A., Tan N., Chowdhury G. M., Mouri H., Sakata Y., et al. Mild prenatal stress enhances learning performance in the non-adopted rat offspring. Neuroscience 2001; 103: 301–307
   PubMed Web of Science ®Google Scholar
• Gerhard I., Henninger T., von Holst B., Kubli F. Wehenhemmung mit Fenoterol. I. Prospektive Untersuchung zum Einfluß der Tokolyse auf den Zustand des Neugeborenen und die frühkindliche Entwicklung bis zu vier Jahren. Zeitschrift für Geburtshilfe und Perinatologie 1989; 193: 29–41
   PubMedGoogle Scholar
• Gleiter C. H., Deckert J. Adverse CNS-effects of beta-adrenoceptor blockers. Pharmacopsychiatry 1996; 29: 201–211
   PubMedGoogle Scholar
• Gordon J. A., Hen R. The serotonergic system and anxiety. Neuromolecular Medicine 2004; 5: 27–40
   PubMed Web of Science ®Google Scholar
• Griffin W. C., Skinner H. D., Salm A. K., Birkle D. L. Mild prenatal stress in rats is associated with enhanced conditioned fear. Physiology & Behavior 2003; 79: 209–215
   PubMed Web of Science ®Google Scholar
• Grillon C., Cordova J., Morgan C. A., Charney D. S., Davis M. Effects of the beta-blocker propranolol on cued and contextual fear conditioning in humans. Psychopharmacology 2004; 175: 342–352
   PubMedGoogle Scholar
• Gurguis G. N., Blakeley J. E., Antai-Otong D., Vo S. P., Orsulak P. J., Petty F., et al. Adrenergic receptor function in panic disorder. II. Neutrophil beta 2 receptors: Gs protein coupling effects of imipramine treatment and relationship to treatment outcome. Journal of Psychiatric Research 1999; 33: 309–322
   PubMed Web of Science ®Google Scholar
• Gutteling B. M., de Weerth C., Willemsen-Swinkels S. H., Huizink A. C., Mulder E. J., Visser G. H., et al. The effect of prenatal stress on temperament and problem behavior of 27-months-old toddlers. European Child & Adolescent Psychiatry 2005; 14: 41–51
   PubMed Web of Science ®Google Scholar
• Hadders-Algra M., Touwen B. C. L., Huisjes H. J. Long-term follow-up of children prenatally exposed to ritodrine. British Journal of Obstetrics and Gynaecology 1986; 93: 156–161
   PubMedGoogle Scholar
• Harwood P. D. Therapeutic dosage in small and large mammals. Science 1963; 139: 684–685
   PubMed Web of Science ®Google Scholar
• Haussmann M., Carroll J., Weesner G., Daniels M., Matteri R., Lay D., Jr. Administration of ACTH to restrained pregnant sows alters their pigs’ hypothalamic-pituitary-adrenal (HPA) axis. Journal of Animal Science 2000; 78: 2399–2411
   PubMed Web of Science ®Google Scholar
• Joels M., van Riel E. Mineralocorticoid and glucocorticoid receptor-mediated effects on serotonergic transmission in health and disease. Annals of the New York Academy of Sciences 2004; 1032: 301–303
   PubMedGoogle Scholar
• Kalin N. H., Shelton S. E., Davidson R. J. The role of the central nucleus of the amygdala in mediating fear and anxiety in the primate. Journal of Neuroscience 2004; 24: 5506–5515
   PubMed Web of Science ®Google Scholar
• Kalinichev M., Easterling K. W., Plotsky P. M., Holtzman S. G. Long-lasting changes in stress-induced corticosterone response and anxiety-like behaviors as a consequence of neonatal maternal separation in Long-Evans rats. Pharmacology Biochemistry and Behavior 2002; 73: 131–140
   PubMed Web of Science ®Google Scholar
• Kamphuis P. J. G. H., Croiset G., Bakker J. M., van Bel F., van Ree J. M., Wiegant V. M. Neonatal dexamethasone treatment affects social behavior of rats in later life. Neuropharmacology 2004; 47: 461–474
   PubMedGoogle Scholar
• Kanitz E., Tuchscherer M., Puppe B., Tuchscherer A., Stabenow B. Consequences of repeated early isolation in domestic piglets (Sus scrofa) on their behavioral neuroendocrine and immunological responses. Brain Behavior and Immunity 2004; 18: 35–45
   PubMed Web of Science ®Google Scholar
• Kofman O. The role of prenatal stress in the etiology of developmental behavioral disorders. Neuroscience and Biobehavioral Reviews 2002; 26: 457–470
   PubMed Web of Science ®Google Scholar
• Kosten T. A., Zhang X. Y., Kehoe P. Infant rats with chronic neonatal isolation experience show decreased extracellular serotonin levels in ventral striatum at baseline and in response to cocaine. Developmental Brain Research 2004; 152: 19–24
   PubMedGoogle Scholar
• Kreider M. L., Seidler F. J., Slotkin T. A. Beta-adrenoceptor modulation of transiently overexpressed alpha 2-adrenoceptors in brain and peripheral tissues: Cellular mechanisms underlying the developmental toxicity of terbutaline. Brain Research Bulletin 2004; 62: 305–314
   PubMed Web of Science ®Google Scholar
• Kreider M. L., Tate C. A., Cousins M. M., Oliver C. A., Seidler F. J., Slotkin T. A. Lasting effects of developmental dexamethasone treatment on neural cell number and size synaptic activity and cell signalling: Critical periods of vulnerability dose-effect relationships regional targets and sex selectivity. Neuropsychopharmacology 2006; 31: 12–35
   PubMedGoogle Scholar
• Liu D., Caldji C., Sharma S., Plotsky P. M., Meaney M. J. Influence of neonatal rearing conditions on stress-induced adrenocorticotropin responses and norepinephrine release in the hypothalamic paraventricular nucleus. Journal of Neuroendocrinology 2000; 12: 5–12
   PubMed Web of Science ®Google Scholar
• Lupien S. J., McEwen B. S. The acute effects of corticosteroids on cognition: Integration of animal and human model studies. Brain Research Reviews 1997; 24: 1–27
   PubMed Web of Science ®Google Scholar
• MacArthur B. A., Howie N., Dezoete J. A., Elkins J. School progress and cognitive development of 6-year-old children whose mothers were treated antenatally with betamethasone. Pediatrics 1982; 70: 99–105
   PubMed Web of Science ®Google Scholar
• Maccari S., Darnaudery M., Morley-Fletcher S., Zuena A., Cinque C., Van Reeth O. Prenatal stress and long-term consequences: Implications of glucocorticoid hormones. Neuroscience and Biobehavioral Reviews 2003; 27: 119–127
   PubMed Web of Science ®Google Scholar
• Macri S., Mason G. J., Würbel H. Dissociation in the effects of neonatal maternal separations on maternal care and the offspring's HPA and fear responses in rats. European Journal of Neuroscience 2004; 20: 1017–1024
   PubMedGoogle Scholar
• Maheu F. S., Joober R., Beaulieu S., Lupien S. J. Differential effects of adrenergic and corticosteroid hormonal systems on human short- and long-term declarative memory for emotionally arousing material. Behavioral Neuroscience 2004; 118: 420–428
   PubMed Web of Science ®Google Scholar
• McGaugh J. L. The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annual Review of Neuroscience 2004; 27: 1–28
   PubMed Web of Science ®Google Scholar
• Meyer A., Seidler F. J., Aldridge J. E., Slotkin T. A. Developmental exposure to terbutaline alters cell signaling in mature rat brain regions and augments the effects of subsequent neonatal exposure to the organophosphorus insecticide chlorpyrifos. Toxicology and Applied Pharmacology 2005; 198: 154–166
   Google Scholar
• Moya F. R., Sanchez I., Baudy D. B. Effects of betamethasone and thyroid hormone on fetal rat lung maturation in vivo. Developmental Pharmacology and Therapeutics 1992; 18: 14–19
   PubMedGoogle Scholar
• Neal C. R., Weidemann G., Kabbaj G. M., Vasquez D. M. Effect of neonatal dexamethasone exposure on growth and neurological development in the adult rat. American Journal of Physiology—Regulatory Integrative and Comparative Physiology 2004; 287: 375–385
   Google Scholar
• NIH. Effect of corticosteroids for fetal maturation on perinatal outcomes. NIH Consensus Development Panel on the Effect of Corticosteroids for Fetal Maturation on Perinatal Outcomes. Journal of the American Medical Association 1995; 273: 413–418
   Web of Science ®Google Scholar
• Oitzl M., Reichardt M., Joels M., de Kloet E. R. Point mutation in the mouse glucocorticoid receptor preventing DNA binding impairs spatial memory. Proceedings of the National Academy of Sciences 2001; 98: 12790–12795
   PubMed Web of Science ®Google Scholar
• Okuda S., Roozendaal B., McGaugh J. L. Glucocorticoid effects on object recognition memory require training-associated emotional arousal. Proceedings of the National Academy of Sciences 2004; 101: 853–858
   PubMed Web of Science ®Google Scholar
• Peters D. A. V. Prenatal stress: Effect on development of rat brain adrenergic receptors. Pharmacology Biochemistry and Behavior 1984; 21: 417–422
   PubMed Web of Science ®Google Scholar
• Pfannschmidt N., Schmiegelow P., Lindner J. Zur Glukokortikoid-bedingten Reifungsbeschleunigung speziell der Lunge bei drohendem Atemnot-Syndrom Frühgeborener. Medizinische Welt 1983; 34: 1432–1436
   PubMedGoogle Scholar
• Pitzer M., Schmidt M. H., Esser G., Laucht M. Child development after maternal tocolysis with beta-sympathomimetic drugs. Child Psychiatry & Human Development 2001; 31: 165–182
   PubMedGoogle Scholar
• Polowczyk D., Tejani N., Lauersen N., Siddio F. Evaluation of seven- to nine-year-old children exposed to ritodrine in utero. Obstetrics and Gynecology 1984; 64: 485–488
   PubMedGoogle Scholar
• Re G., Badino P., Novelli A., Girardi G. Effects of clenbuterol as a repartitioning agent on beta-adrenoceptor concentrations in heart bronchi and brain of veal calves. Veterinary Journal 1997; 153: 63–70
   PubMedGoogle Scholar
• Resnik R. Issues in the management of preterm labor. Journal of Obstetrics and Gynaecology Research 2005; 31: 354–358
   PubMedGoogle Scholar
• Rhodes M. C., Seidler F. J., Abdel-Rahman A., Tate C. A., Nyska A., Rincavage H. L., et al. Terbutaline is a developmental neurotoxicant: Effects on neuroproteins and morphology in cerebellum, hippocampus, and somatosensory cortex. Journal of Pharmacology and Experimental Therapeutics 2004; 308: 529–537
   PubMedGoogle Scholar
• Rieger M., Pirke K.-M., Buske-Kirschbaum A., Wurmser H., Papousek M., Hellhammer D. H. Influence of stress during pregnancy on HPA activity and neonatal behavior. Annals of the New York Academy of Sciences 2004; 1032: 228–230
   PubMedGoogle Scholar
• Rominger K. L., Pollmann W. Vergleichende Pharmakokinetik von Fenoterol-Hydrobromid bei Ratte, Hund und Mensch. Arzneimittelforschung 1972; 22: 1190–1196
   PubMedGoogle Scholar
• Schneider M. L., Clarke A. S., Kraemer G. W., Roughton E. C., Lubach G. R., Rimm-Kaufman S., et al. Prenatal stress alters brain biogenic amine levels in primates. Development and Psychopathology 1998; 10: 427–440
   PubMed Web of Science ®Google Scholar
• Schramm N. L., McDonald M. P., Limbird L. E. The a2-adrenergic receptor plays a protective role in mouse behavioral models of depression and anxiety. Journal of Neuroscience 2001; 21: 45875–45882
   Google Scholar
• Seckl J. Prenatal glucocorticoids and long-term programming. European Journal of Endocrinology 2004; 151: U49–U62
   PubMed Web of Science ®Google Scholar
• Shiota K., Kayamura T. Effects of prenatal heat stress on postnatal growth behavior and learning capacity in mice. Biology of the Neonate 1989; 56: 6–14
   PubMedGoogle Scholar
• Shishkina G. T., Kalinina T. S., Dygalo N. N. Attenuation of a2A-adrenergic receptor expression in neonatal rat brain by RNA interference or antisense oligonucleotide reduced anxiety in adulthood. Neuroscience 2004; 129: 521–528
   PubMed Web of Science ®Google Scholar
• Slattery M., Morrison J. Preterm delivery. Lancet 2002; 360: 1489–1497
   PubMed Web of Science ®Google Scholar
• Slotkin T. A., Barnes G. A., McCook E. C., Seidler F. J. Programming of brainstem serotonin transporter development by prenatal glucocorticoids. Developmental Brain Research 1996; 93: 155–161
   PubMedGoogle Scholar
• Slotkin T. A., Kreider M. L., Tate C. A., Seidler F. J. Critical prenatal and postnatal periods for persistent effects of dexamethasone on serotonergic and dopaminergic systems. Neuropsychopharmacology 2006; 31: 904–911
   PubMed Web of Science ®Google Scholar
• Slotkin T. A., Seidler F. J. Developmental exposure to terbutaline and chlorpyrifos, separately or sequentially, elicits presynaptic serotonergic hyperactivity in juvenile and adolescent rats. Brain Research Bulletin 2007; 73: 4–6
   Google Scholar
• Slotkin T. A., Tate C. A., Cousins M. M., Seidler F. J. β-Adrenoceptor signaling in the developing brain: Sensitization or desensitization in response to terbutaline. Developmental Brain Research 2001; 131: 113–125
   PubMedGoogle Scholar
• Strange B. A., Dolan R. J. β-Adrenergic modulation of emotional memory-evoked human amygdala and hippocampal responses. Proceedings of the National Academy of Sciences 2004; 101: 11454–11458
   PubMed Web of Science ®Google Scholar
• Szuran T. F., Pliska V., Pokorny J., Welzl H. Prenatal stress in rats: Effects on plasma corticosterone hippocampal glucocorticoid receptors and maze performance. Physiology & Behavior 2000; 71: 353–362
   PubMed Web of Science ®Google Scholar
• Tanaka M., Yoshida M., Emoto H., Ishii H. Noradrenaline systems in the hypothalamus amygdala and locus coeruleus are involved in the provocation of anxiety: basic studies. European Journal of Pharmacology 2000; 405: 397–406
   PubMed Web of Science ®Google Scholar
• Tejkalova H., Benesova O., Kristofikova Z., Binkova B., Dlohozkova N., Buresova M. The assessment of the behavioral teratogenic risk of the tocolytic drug phenoterol. Homeostasis in Health and Disease 1991; 33: 89–93
   PubMedGoogle Scholar
• Tsigos C., Chrousos G. P. Hypothalamic-pituitary-adrenal axis neuroendocrine factors and stress. Journal of Psychosomatic Research 2002; 53: 865–871
   PubMed Web of Science ®Google Scholar
• Uno H., Eisele S., Sakai A., Shelton S., Baker E., DeJesus O., et al. Neurotoxicity of glucocorticoids in the primate brain. Hormones and Behavior 1994; 28: 336–348
   PubMed Web of Science ®Google Scholar
• Vallee M., Mayo W., Dellu F., Le Moal M., Simon H., Maccari S. Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: Correlation with stress-induced corticosterone secretion. Journal of Neuroscience 1997; 17: 2626–2636
   PubMed Web of Science ®Google Scholar
• Wagner J. P., Seidler F. J., Schachat F. H., Slotkin T. A. Beta adrenergic control of c-fos protooncogene expression in developing rat brain regions. The Journal of Pharmacology and Experimental Therapeutics 1994; 269: 1292–1299
   PubMedGoogle Scholar
• Wang R.-X., Limbird L. E. Distribution of mRNA encoding three a2-adrenergic receptor subtypes in the developing mouse embryo suggests a role for the a2A subtype in apoptosis. Molecular Pharmacology 1997; 52: 1071–1080
   PubMedGoogle Scholar
• Ward H. E., Johnson E. A., Salm A. K., Birkle D. L. Effects of prenatal stress on defensive withdrawal behavior and corticotrophin releasing factor systems in rat brain. Physiology & Behavior 2000; 70: 359–366
   PubMed Web of Science ®Google Scholar
• Welberg L., Seckl J., Holmes M. Prenatal glucocorticoid programming of brain corticosteroid receptors and corticotropin-reeasing hormone: Possible implications for behavior. Neuroscience 2001; 104: 71–79
   PubMed Web of Science ®Google Scholar
• Zerrate M. C., Pletnikov M., Connors S. L., Vargas D. L., Seidler F. J., Zimmerman A. W., et al. Neuroinflammation and behavioral abnormalities after neonatal terbutaline treatment in rats: implications for autism. The Journal of Pharmacology and Experimental Therapeutics 2007; 322: 16–22
   PubMed Web of Science ®Google Scholar
• Zimmerberg B., Brown R. C. Prenatal experience and postnatal stress modulate the adult neurosteroid and catecholaminergic stress response. International Journal of Developmental Neuroscience 1998; 16: 217–228
   PubMedGoogle Scholar