Tracing the trajectory of behavioral impairments and oxidative stress in an animal model of neonatal inflammation

Neuroscience

Volumn 298, Issue , 2015, Pages 455-466

  MacRae, M ^a   Macrina, T ^a   Khoury, A ^a   Migliore, M M ^a   Kentner, A C ^a  

^a MASSACHUSETTS COLLEGE OF PHARMACY AND HEALTH SCIENCES   (United States)

Author keywords

Corticosterone; Development; Enrichment; Inflammation; Maternal care; Oxidative stress

Indexed keywords

CORTICOSTERONE; GLUTATHIONE; LIPOPOLYSACCHARIDE;

ADOLESCENT; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; COGNITIVE DEFECT; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; EMOTIONAL DISORDER; ENVIRONMENTAL ENRICHMENT; FEMALE; INFLAMMATION; JUVENILE ANIMAL; MALE; MATERNAL BEHAVIOR; NEWBORN; NONHUMAN; OXIDATIVE STRESS; PREFRONTAL CORTEX; PRIORITY JOURNAL; PUBERTY; RAT; SOCIAL BEHAVIOR; SPATIAL MEMORY; AGE; ANIMAL; BLOOD; CHEMICALLY INDUCED; COMPLICATION; DEVELOPMENTAL DISABILITIES; DISEASE COURSE; DRUG EFFECTS; MENTAL DISORDERS; METABOLISM; NONPARAMETRIC TEST; PATHOLOGY; PHYSIOLOGY; SEX DIFFERENCE; SPRAGUE DAWLEY RAT; TIME;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; CORTICOSTERONE; DEVELOPMENTAL DISABILITIES; DISEASE PROGRESSION; FEMALE; GLUTATHIONE; INFLAMMATION; LIPOPOLYSACCHARIDES; MALE; MATERNAL BEHAVIOR; MENTAL DISORDERS; OXIDATIVE STRESS; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; SEX FACTORS; SOCIAL BEHAVIOR; STATISTICS, NONPARAMETRIC; TIME FACTORS;

EID: 84928894739     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2015.04.048     Document Type: Article

References (68)

1. Bilbo S.D., Newsum N.J., Sprunger D.B., Watkins L.R., Rudy J.W., Maier S.F. Differential effects of neonatal handling on early life infection-induced alterations in cognition in adulthood. Brain Behav Immun 2007, 21:332-342.
2. Bitanihirewe B.K.Y., Peleg-Raibstein D., Mouttet F., Feldon J., Meyer U. Late prenatal immune activation in mice leads to behavioral and neurochemical abnormalities relevant to the negative symptoms of schizophrenia. Neuropsychopharmacology 2010, 35:2462-2478.
3. Browne R.W., Bloom M.S., Schisterman E.F., Hovey K., Trevisan M., Wu C., Liu A., Wactawskiwende J. Analytical and biological variation of biomarkers of oxidative stress during the menstrual cycle. Biomarkers 2008, 13:160-183.
4. Boksa P. Effects of prenatal infection on brain development and behavior: a review of findings from animal models. Brain Behav Immun 2010, 24:881-897.
5. Caldji C., Tannenbaum B., Sharma S., Francis D., Plotsky P.M., Meaney M.J. Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc Nat Acad Sci U S A 1998, 95:5335-5340.
6. Cechetti F., Worm P.V., Lovatel G., Moysés F., Siqueira I.R., Netto C.A. Environmental enrichment prevents behavioral deficits and oxidative stress caused by chronic cerebral hypoperfusion in the rat. Life Sci 2012, 91:29-36.
7. Prevalence of autism spectrum disorder-autism and developmental disability monitoring network, 11 sites, United States, 2010. Surveill Summ Mortal Wkly Rep 2014, 63:1-21. Centers for Disease Control and Prevention.
8. Connors E.J., Shaik A.N., Migliore M.M., Kentner A.C. Environmental enrichment mitigates the sex-specific effects of gestational inflammation on social engagement and the hypothalamic pituitary adrenal axis-feedback system. Brain Behav Immun 2014, 42:178-190.
9. Connors E.J., Migliore M.M., Shaik A.N., Kentner A.C. Environmental enrichment models a naturalistic form of maternal separation and shapes the anxiety response patterns of offspring. Psychoneuroendocrinology 2015, 52:153-167.
10. Coyle J.T., Tsai G., Goff D. Converging evidence of NMDA receptor hypofunction in the pathophysiology of schizophrenia. Ann N Y Acad Sci 2003, 1003:318-327.
11. Dahlqvist P., Rönnbäck A., Bergström S.A., Söderström I., Olsson T. Environmental enrichment reverses learning impairment in the Morris water maze after focal cerebral ischemia in rats. Eur J Neurosci 2004, 19:2288-2298.
12. Dean M., Kasari C., Shih W., Frankel F., Whitney R., Landa R., et al. The peer relationships of girls with ASD at school: comparison to boys and girls with and without ASD. J Child Psychol Psychiatry 2014, 55:1218-1225.
13. Dinel A.-L., Joffre C., Trifilieff P., Aubert A., Foury A., Le Ruyet P., Layé S. Inflammation early in life is a vulnerable factor for emotional behavior at adolescence and for lipopolysaccharide-induced spatial memory and neurogenesis alterations at adulthood. J Neuroinflammation 2014, 11:155.
14. Do K.Q., Trabesinger A.H., Kirsten-Krüger M., Lauer C.J., Dydak U., Hell D., Holsboer F., Boesiger P., Cuénod M. Schizophrenia: glutathione deficit in cerebrospinal fluid and prefrontal cortex in vivo. Eur J Neurosci 2000, 12:3721-3728.
15. Fan L.-W., Tien L.-T., Zheng B., Pang Y., Lin R.C.S., Simpson K.L., Ma T., Rhodes P.G., Cai Z. Dopaminergic neuronal injury in the adult rat brain following neonatal exposure to lipopolysaccharide and the silent neurotoxicity. Brain Behav Immun 2011, 25:286-297.
16. Forrest C.M., Khalil O.S., Pisa M., Smith R.A., Darlington L.G., Stone T.W. Prenatal activation of toll-like receptors-3 by administration of the viral mimetic poly(I:C) changes synaptic proteins, N-methyl-d-aspartate receptors and neurogenesis markers in offspring. Mol Brain 2012, 5:22.
17. Garay P.A., Hsiao E.Y., Patterson P.H., McAllister A.K. Maternal immune activation causes age- and region-specific changes in brain cytokines in offspring throughout development. Brain Behav Immun 2013, 31:54-68.
18. Gu F., Chauhan V., Chauhan A. Glutathione redox imbalance in brain disorders. Curr Opin Clin Nutr Metab Care 2015, 18:89-95.
19. Harré E.-M., Galic M.A., Mouihate A., Noorbakhsh F., Pittman Q.J. Neonatal inflammation produces selective behavioural deficits and alters N-methyl-d-aspartate receptor subunit mRNA in the adult rat brain. Eur J Neurosci 2008, 27:644-653.
20. Herring A., Lewejohann L., Panzer A.-L., Donath A., Kröll O., Sachser N., Paulus W., Keyvani K. Preventative and therapeutic types of environmental enrichment counteract beta amyloid pathology by different molecular mechanisms. Neurobiol Dis 2011, 42:530-538.
21. Holland F.H., Ganguly P., Potter D.N., Chartoff E.H., Brenhouse H.C. Early life stress disrupts social behavior and prefrontal cortex parvalbumin interneurons at an earlier time-point in females than males. Neurosci Lett 2014, 566:131-136.
22. Ibi D., Nagai T., Kitahara Y., Mizoguchi H., Koike H., Shiraki A., Takuma K., Kamei H., Noda Y., Nitta A., Nabeshima T., Yoneda Y., Yamada K. Neonatal polyI:C treatment in mice results in schizophrenia-like behavioral and neurochemical abnormalities in adulthood. Neurosci Res 2009, 64:297-305.
23. Johnson E.M., Traver K.L., Hoffman S.W., Harrison C.R., Herman J.P. Environmental enrichment protects against functional deficits caused by traumatic brain injury. Front Behav Neurosci 2013, 7:44.
24. Kaffman A., Meaney M.J. Neurodevelopmental sequelae of postnatal maternal care in rodents: clinical and research implications of molecular insights. J Child Psychol Psychiatry 2007, 48:224-244.
25. Kempermann G., Gast D., Gage F.H. Neuroplasticity in old age: sustained fivefold induction of hippocampal neurogenesis by long-term environmental enrichment. Ann Neurol 2002, 52:135-143.
26. Khalil O.S., Forrest C.M., Pisar M., Smith R.A., Darlington L.G., Stone T.W. Prenatal activation of maternal TLR3 receptors by viral-mimetic poly(I:C) modifies GLUN2B expression in embryos and sonic hedgehog in offspring in the absence of kynurenine pathway activation. Immunopharmacol Immunotoxicol 2013, 35:581-593.
27. Konkle A.T.M., Kentner A.C., Baker S.L., Stewart A., Bielajew C. Environmental enrichment-related variations in behavioral, biochemical, and physiologic responses of Sprague-Dawley and Long Evans rats. J Am Assoc Lab Anim Sci 2010, 49:427-436.
28. Kumar B., Kuhad A., Chopra K. Neuropsychopharmacological effect of sesamol in unpredictable chronic mild stress model of depression: behavioral and biochemical evidences. Psychopharmacology 2011, 214:819-828.
29. Lai M., Lombardo M.V., Auyeung B., Chakrabart B., Baron-Cohen S. Sex/gender differences in autism: setting the scene for future research. J Am Acad Child Adolesc Psychiatry 2015, 54:11-24.
30. Lanté F., Meunier J., Guiramand J., Maurice T., Cavalier M., de Jesus Ferreira M.-C., Aimar R., Cohen-Solal C., Vignes M., Barbanel G. Neurodevelopmental damage after prenatal infection: role of oxidative stress in the fetal brain. Free Radical Biol Med 2007, 42:1231-1245.
31. Lapin I.P. Only controls: effects of handling, sham injection, and intraperitoneal injection of saline on behavior of mice in an elevated plus-maze. J Pharmacol Toxicol Methods 1995, 34:73-77.
32. Lee S.Y., Lee J.-Y., Oh S.J., Kim H.C., Kim S.K. Expression of hepatic and ovarian antioxidant enzymes during estrous cycle in rats. Toxicol Lett 2012, 3:329-336.
33. Liu Y.-H., Lai W.-S., Tsay H.-J., Wang T.-W., Yu J.-Y. Effects of maternal immune activation on adult neurogenesis in the subventricular zone-olfactory bulb pathway and olfactory discrimination. Schizophr Res 2013, 151:1-11.
34. MacRae M., Kenkel W.M., Kentner A.C. Social rejection following neonatal inflammation is mediated by olfactory scent cues. Brain Behav Immun 2015, in press. 10.1016/j.bbi.2015.02.026.
35. McGovern C.W., Sigman M. Continuity and change from early childhood to adolescence in autism. J Child Psychol Psychiatry 2005, 46:401-408.
36. Meyer U., Nyffeler M., Engler A., Urwyler A., Schedlowski M., Knuesel I., Yee B.K., Feldon J. The time of prenatal immune challenge determines the specificity of inflammation-mediated brain and behavioral pathology. J Neurosci 2006, 26:4752-4762.
37. Meyer U., Schwendener S., Feldon J., Yee B.K. Prenatal and postnatal maternal contributions in the infection model of schizophrenia. Exp Brain Res 2006, 173:243-257.
38. Meyer U., Engler A., Weber L., Schedlowski M., Feldon J. Preliminary evidence for a modulation of fetal dopaminergic development by maternal immune activation during pregnancy. Neuroscience 2008, 154:701-709.
39. Meyer U., Nyffeler M., Yee B.K., Knuesel I., Feldon J. Adult brain and behavioral pathological markers of prenatal immune challenge during early/middle and later fetal development in mice. Brain Behav Immun 2008, 22:469-486.
40. Mitra R., Sapolsky R.M. Short-term enrichment makes male rats more attractive, more defensive and alters hypothalamic neurons. PLoS One 2012, 7:e36092.
41. Mitra S., Chakrabarti N., Dutta S.S., Ray S., Bhattacharya P., Sinha P., Bhattacharyya A. Gender-specific brain regional variation of neurons, endogenous estrogen, neuroinflammation and glial cells during rotenone-induced mouse model of Parkinson's disease. Neuroscience 2015, 292:46-70.
42. Moore C.L. Sex differences in urinary odors produced by young laboratory rats (Rattus norvegicus). J Comp Psychol 1985, 99:336-341.
43. Morgan C., Novak I., Dale R.C., Guzzetta A., Badawi N. GAME (Goals -Activity - Motor Enrichment): protocol of a single blind randomized controlled trial of motor training, parent education and environmental enrichment for infants at high risk of cerebral palsy. BMC Neurol 2014, 14:203.
44. Morley-Fletcher S., Rea M., Maccari S., Laviola G. Environmental enrichment during adolescence reverses the effects of prenatal stress on play behaviour and HPA axis reactivity in rats. Eur J Neurosci 2003, 18:3367-3374.
45. O'Callaghan M.J., Croft A.P., Little H.J. Effects of intraperitoneal injections of saline on the alcohol and sucrose consumption of C57/BL10 mice. Psychopharmacology 2002, 160:206-212.
46. Ozacmak V.H., Sayan H. The effects of 17β estradiol and progesterone on oxidative stress biomarkers in ovariectomized female rat brain subjected to global cerebral ischemia. Physiol Res 2009, 58:909-912.
47. Paintlia M.K., Paintlia A.S., Contreras M., Singh I., Singh A. Lipopolysaccharide-induced peroxisomal dysfunction exacerbates cerebral white matter injury: attenuation by N-acetylcystein. Exp Neurol 2008, 210:560-576.
48. Paris J.J., Brunton P.J., Russell J.A., Frye C.A. Immune stress in late pregnant rats decreases length of gestation and fecundity, and alters later cognitive and affective behaviour of surviving pre-adolescent offspring. Stress 2011, 14:652-664.
49. Patterson P.H. Immune involvement in schizophrenia and autism: etiology, pathology, and animal models. Behav Brain Res 2009, 204:313-321.
50. Peña Y., Prunell M., Rotllant D., Armario A., Escorihuela R.M. Enduring effects of environmental enrichment from weaning to adulthood on pituitary-adrenal function, pre-pulse inhibition and learning in male and female rats. Psychoneuroendocrinology 2009, 34:1390-1404.
51. Penteado S.H., Teodorov E., Kirsten T.B., Eluf B.P., Reis-Silva T.M., Acenjo M.K., de Melo R.C., Suffredini I.B., Bernardi M.M. Prenatal lipopolysaccharide disrupts maternal behavior, reduces nest odor preference in pups, and induces anxiety: studies of F1 and F2 generations. Eur J Pharmacol 2014, 738:342-351.
52. Priyanka H.P., Sharma U., Gopinath S., Sharma V., Hima L., ThyagaRajan S. Menstrual cycle and reproductive aging alters immune reactivity, NGF expression, antioxidant enzyme activities, and intracellular signaling pathways in the peripheral blood mononuclear cells of healthy women. Brain Behav Immun 2013, 32:131-143.
53. Raine A., Mellingen K., Liu J., Venables P., Mednick A.A. Effects of environmental enrichment at ages 3-5years on schizotypical personality and antisocial behavior at ages 17 and 23years. Am J Psychiatry 2003, 160:1627-1635.
54. Ravenelle R., Byrnes E.M., Byrnes J.J., McInnis C., Park J.H., Donaldson S.T. Environmental enrichment effects on the neurobehavioral profile of selective outbred trait anxiety rats. Behav Brain Res 2013, 252:49-57.
55. Richter S.H., Garner J.P., Würbel H. Environmental standardization: cure or cause of poor reproducibility in animal experiments?. Nat Methods 2009, 6:257-261.
56. Schneider T., Turczak J., Przewłocki R. Environmental enrichment reverses behavioral alterations in rats prenatally exposed to valproic acid: issues for a therapeutic approach in autism. Neuropsychopharmacology 2006, 31(1):36-46.
57. Shattuck P.T., Seltzer M.M., Greenberg J.S., Orsmond G.I., Bolt D., Kring S., Lounds J., Lord C. Change in autism symptoms and maladaptive behaviors in adolescence and adults with autism spectrum disorder. J Autism Dev Disord 2007, 37:1735-1747.
58. Shi L., Fatemi S.H., Sidwell R.W., Patterson P.H. Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring. J Neurosci 2003, 23:297-302.
59. Spencer S.J., Martin S., Mouihate A., Pittman Q.J. Early-life immune challenge: defining a critical window for effects on adult responses to immune challenge. Neuropsychopharmacology 2006, 31:1910-1918.
60. Spires T.L., Grote H.E., Varshney N.K., Cordery P.M., van Dellen A., Blakemore C., Hannan A.J. Environmental enrichment rescues protein deficits in a mouse model of Huntington's disease, indicating a possible disease mechanism. J Neurosci 2004, 24:2270-2276.
61. Stolp H.B., Johansson P.A., Habgood M.D., Dziegielewska K.M., Saunders N.R., Ek C.J. Effects of neonatal systemic inflammation on blood-brain barrier permeability and behaviour in juvenile and adult rats. Cardiovasc Psychiatry Neurol 2011, 469046:1-10.
62. Taylor P.V., Veenema A.H., Paul M.J., Bredewold R., Isaacs S., de Vries G.J. Sexually dimorphic effects of a prenatal immune challenge on social play and vasopressin expression in juvenile rats. Biol Sex Differ 2012, 3:15.
63. Van Praag H., Kempermann G., Gage F.H. Running wheel increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 1999, 2:266-270.
64. Van Praag H., Kempermann G., Gage F.H. Neural consequences of environmental enrichment. Nat Rev Neurosci 2000, 1:191-198.
65. Vorhees C.V., Graham D.L., Braun A.A., Schaefer T.L., Skelton M.R., Richtand N.M., Williams M.T. Prenatal immune challenge in rats: effects of polyinosinic-polycytidylic acid on spatial learning, prepulse inhibition, conditioned fear, and responses to MK-801 and amphetamine. Neurotoxicol Teratol 2015, 47:54-65.
66. Woo C.C., Leon M. Environmental enrichment as an effective treatment for autism: a randomized controlled trial. Behav Neurosci 2013, 127:487-497.
67. Zhang Z., van Praag H. Maternal immune activation differentially impacts mature and adult-born hippocampal neurons in male mice. Brain Behav Immun 2015, 45:60-70.
68. Zuckerman L., Rehavi M., Nachman R., Weiner I. Immune activation during pregnancy in rats leads to a postpubertal emergence of disrupted latent inhibition, dopaminergic hyperfunction, and altered limbic morphology in the offspring: a novel neurodevelopmental model of schizophrenia. Neuropsychopharmacology 2003, 28:1778-1789.