Maternal sleep deprivation inhibits hippocampal neurogenesis associated with inflammatory response in young offspring rats

Neurobiology of Disease

Volumn 68, Issue , 2014, Pages 57-65

  Zhao, Qiuying ^a   Peng, Cheng ^b   Wu, Xiaohui ^a   Chen, Yubo ^a   Wang, Cheng ^a   You, Zili ^a  

^a UNIVERSITY OF ELECTRONIC SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b CHENGDU UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

Author keywords

Inflammatory response; Microglial activation; Neurogenesis; Offspring; Pregnancy; Sleep deprivation

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA; DOUBLECORTIN PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; NEUROPEPTIDE; SUCROSE;

ANHEDONIA; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COGNITION; CONTROLLED STUDY; FEMALE; GESTATIONAL AGE; HIPPOCAMPUS; INFLAMMATION; MALE; MATERNAL SLEEP DEPRIVATION; MEMORY; MICROGLIA; MORRIS WATER MAZE TEST; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PREPUBERTY; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SLEEP DEPRIVATION; SPATIAL LEARNING; SUCROSE PREFERENCE TEST; AGE; ANIMAL; BODY WEIGHT; COGNITION DISORDERS; COMPLICATION; FOOD PREFERENCE; MAZE TEST; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PREGNANCY; PRENATAL EXPOSURE; SEX RATIO; WISTAR RAT;

AGE FACTORS; ANIMALS; BODY WEIGHT; COGNITION DISORDERS; FEMALE; FOOD PREFERENCES; GESTATIONAL AGE; HIPPOCAMPUS; INTERLEUKIN-10; MALE; MAZE LEARNING; MICROTUBULE-ASSOCIATED PROTEINS; NEUROGENESIS; NEUROPEPTIDES; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, WISTAR; SEX RATIO; SLEEP DEPRIVATION; SUCROSE;

EID: 84899900749     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2014.04.008     Document Type: Article

References (73)

1. Abdul Aziz N.H., et al. Prenatal exposure to chronic mild stress increases corticosterone levels in the amniotic fluid and induces cognitive deficits in female offspring, improved by treatment with the antidepressant drug amitriptyline. Behav. Brain Res. 2012, 231:29-39.
2. Abel K.M., et al. Birth weight, schizophrenia, and adult mental disorder: is risk confined to the smallest babies?. Arch. Gen. Psychiatry 2010, 67:923-930.
3. Alvarenga T.A., et al. Effects of sleep deprivation during pregnancy on the reproductive capability of the offspring. Fertil. Steril. 2013, 100:1752-1757.
4. Andersen S.L., Teicher M.H. Desperately driven and no brakes: developmental stress exposure and subsequent risk for substance abuse. Neurosci. Biobehav. Rev. 2009, 33:516-524.
5. Ashdown H., et al. The role of cytokines in mediating effects of prenatal infection on the fetus: implications for schizophrenia. Mol. Psychiatry 2006, 11:47-55.
6. Baker S., et al. Effects of gestational stress: 1. Evaluation of maternal and juvenile offspring behavior. Brain Res. 2008, 5:98-110.
7. Bale T.L. Neuroendocrine and immune influences on the CNS: it's a matter of sex. Neuron 2009, 64:13-16.
8. Block M.L., et al. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat. Rev. Neurosci. 2007, 8:57-69.
9. Calegare B.F., et al. Biochemical, biometrical and behavioral changes in male offspring of sleep-deprived mice. Psychoneuroendocrinology 2010, 35:775-784.
10. Carvey P.M., et al. Prenatal exposure to the bacteriotoxin lipopolysaccharide leads to long-term losses of dopamine neurons in offspring: a potential, new model of Parkinson's disease. Front. Biosci. 2003, 1:s826-s837.
11. Cerciat M., et al. Selective estrogen receptor modulators decrease the production of interleukin-6 and interferon-gamma-inducible protein-10 by astrocytes exposed to inflammatory challenge in vitro. Glia 2010, 58:93-102.
12. Chang J.J., et al. Sleep deprivation during pregnancy and maternal and fetal outcomes: is there a relationship?. Sleep Med. Rev. 2010, 14:107-114.
13. Colton C.A. Heterogeneity of microglial activation in the innate immune response in the brain. J. Neuroimmune Pharmacol. 2009, 4:399-418.
14. Czeh B., et al. Quantitative changes in hippocampal microvasculature of chronically stressed rats: no effect of fluoxetine treatment. Hippocampus 2010, 20:174-185.
15. Derecki N.C., et al. Regulation of learning and memory by meningeal immunity: a key role for IL-4. J. Exp. Med. 2010, 207:1067-1080.
16. Deverman B.E., Patterson P.H. Cytokines and CNS development. Neuron 2009, 64:61-78.
17. Diz-Chaves Y., et al. Prenatal stress increases the expression of proinflammatory cytokines and exacerbates the inflammatory response to LPS in the hippocampal formation of adult male mice. Brain Behav. Immun. 2013, 28:196-206.
18. Fisher H.L., et al. The varying impact of type, timing and frequency of exposure to childhood adversity on its association with adult psychotic disorder. Psychol. Med. 2010, 40:1967-1978.
19. Frodl T., O'keane V. How does the brain deal with cumulative stress? A review with focus on developmental stress, HPA axis function and hippocampal structure in humans. Neurobiol. Dis. 2013, 52:24-37.
20. Gage F.H. Neurogenesis in the adult brain. J. Neurosci. 2002, 22:612-613.
21. Gil-Mohapel J., et al. Hippocampal cell loss and neurogenesis after fetal alcohol exposure: insights from different rodent models. Brain Res. Rev. 2010, 64:283-303.
22. Giovanoli S., et al. Stress in puberty unmasks latent neuropathological consequences of prenatal immune activation in mice. Science 2013, 339:1095-1099.
23. Gould E. How widespread is adult neurogenesis in mammals?. Nat. Rev. Neurosci. 2007, 8:481-488.
24. Griffin W.S. Inflammation and neurodegenerative diseases. Am. J. Clin. Nutr. 2006, 83:470S-474S.
25. Grigoryan G., Segal M. Prenatal stress affects network properties of rat hippocampal neurons. Biol. Psychiatry 2013, 73:1095-1102.
26. Harry G.J., Kraft A.D. Microglia in the developing brain: a potential target with lifetime effects. Neurotoxicology 2012, 33:191-206.
27. Hollenbach D., et al. Non-pharmacological interventions for sleep quality and insomnia during pregnancy: A systematic review. J. Can. Chiropr. Assoc. 2013, 57:260-270.
28. Holloway T., et al. Prenatal stress induces schizophrenia-like alterations of serotonin 2A and metabotropic glutamate 2 receptors in the adult offspring: role of maternal immune system. J. Neurosci. 2013, 33:1088-1098.
29. Howerton C.L., Bale T.L. Prenatal programing: at the intersection of maternal stress and immune activation. Horm. Behav. 2012, 62:237-242.
30. Kettenmann H., et al. Physiology of microglia. Physiol. Rev. 2011, 91:461-553.
31. Kizilirmak A., et al. Insomnia in pregnancy and factors related to insomnia. ScientificWorldJournal 2012, 197093:24.
32. Kohman R.A., Rhodes J.S. Neurogenesis, inflammation and behavior. Brain Behav. Immun. 2013, 27:22-32.
33. Kreutzberg G.W. Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 1996, 19:312-318.
34. Lemaire V., et al. Postnatal stimulation of the pups counteracts prenatal stress-induced deficits in hippocampal neurogenesis. Biol. Psychiatry 2006, 59:786-792.
35. Lu Z., et al. Phagocytic activity of neuronal progenitors regulates adult neurogenesis. Nat. Cell Biol. 2011, 13:1076-1083.
36. Lucassen P.J., et al. Prenatal stress reduces postnatal neurogenesis in rats selectively bred for high, but not low, anxiety: possible key role of placental 11beta-hydroxysteroid dehydrogenase type 2. Eur. J. Neurosci. 2009, 29:97-103.
37. Lucassen P.J., et al. Regulation of adult neurogenesis by stress, sleep disruption, exercise and inflammation: Implications for depression and antidepressant action. Eur. Neuropsychopharmacol. 2010, 20:1-17.
38. Luo X.G., Chen S.D. The changing phenotype of microglia from homeostasis to disease. Trans. Neurodegener. 2012, 1:2047-9158.
39. Mccormick C.M., et al. Social instability stress in adolescent male rats alters hippocampal neurogenesis and produces deficits in spatial location memory in adulthood. Hippocampus 2012, 22:1300-1312.
40. Meerlo P., et al. New neurons in the adult brain: the role of sleep and consequences of sleep loss. Sleep Med. Rev. 2009, 13:187-194.
41. Meyer U., et al. Towards an immuno-precipitated neurodevelopmental animal model of schizophrenia. Neurosci. Biobehav. Rev. 2005, 29:913-947.
42. Meyer U., et al. Adult behavioral and pharmacological dysfunctions following disruption of the fetal brain balance between pro-inflammatory and IL-10-mediated anti-inflammatory signaling. Mol. Psychiatry 2008, 13:208-221.
43. Michelucci A., et al. Characterization of the microglial phenotype under specific pro-inflammatory and anti-inflammatory conditions: Effects of oligomeric and fibrillar amyloid-beta. J. Neuroimmunol. 2009, 210:3-12.
44. Mirescu C., et al. Sleep deprivation inhibits adult neurogenesis in the hippocampus by elevating glucocorticoids. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:19170-19175.
45. Monje M.L., et al. Inflammatory blockade restores adult hippocampal neurogenesis. Science 2003, 302:1760-1765.
46. Mueller B.R., Bale T.L. Early prenatal stress impact on coping strategies and learning performance is sex dependent. Physiol. Behav. 2007, 91:55-65.
47. Novati A., et al. Chronic sleep restriction causes a decrease in hippocampal volume in adolescent rats, which is not explained by changes in glucocorticoid levels or neurogenesis. Neuroscience 2011, 190:145-155.
48. O'keane V., et al. A review of Atypical depression in relation to the course of depression and changes in HPA axis organization. Psychoneuroendocrinology 2012, 37:1589-1599.
49. Oomen C.A., et al. Severe early life stress hampers spatial learning and neurogenesis, but improves hippocampal synaptic plasticity and emotional learning under high-stress conditions in adulthood. J. Neurosci. 2010, 30:6635-6645.
50. Oomen C.A., et al. Early maternal deprivation affects dentate gyrus structure and emotional learning in adult female rats. Psychopharmacology (Berlin) 2011, 214:249-260.
51. Pan Y., et al. The effects of central pro-and anti-inflammatory immune challenges on depressive-like behavior induced by chronic forced swim stress in rats. Behav. Brain Res. 2013, 247:232-240.
52. Perlman W.R., et al. Age-related differences in glucocorticoid receptor mRNA levels in the human brain. Neurobiol. Aging 2007, 28:447-458.
53. Perry V.H., et al. Systemic infections and inflammation affect chronic neurodegeneration. Nat. Rev. Immunol. 2007, 7:161-167.
54. Pien G.W., Schwab R.J. Sleep disorders during pregnancy. Sleep 2004, 27:1405-1417.
55. Pires G.N., et al. Sleep impairment during pregnancy: possible implications on mother-infant relationship. Med. Hypotheses 2010, 75:578-582.
56. Rayen I., et al. Fluoxetine during development reverses the effects of prenatal stress on depressive-like behavior and hippocampal neurogenesis in adolescence. PLoS One 2011, 6:e24003.
57. Sahay A., et al. Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 2011, 472:466-470.
58. Sierra A., et al. Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell 2010, 7:483-495.
59. Sompol P., et al. N-acetylserotonin promotes hippocampal neuroprogenitor cell proliferation in sleep-deprived mice. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:8844-8849.
60. Strauss G.P. The emotion paradox of anhedonia in schizophrenia: or is it?. Schizophr. Bull. 2013, 39:247-250.
61. Suchecki D., Palermo Neto J. Prenatal stress and emotional response of adult offspring. Physiol. Behav. 1991, 49:423-426.
62. Suter M., et al. Maternal tobacco use modestly alters correlated epigenome-wide placental DNA methylation and gene expression. Epigenetics 2011, 6:1284-1294.
63. Thomal J.T., et al. Sleep restriction during pregnancy: hypertension and renal abnormalities in young offspring rats. Sleep 2010, 33:1357-1362.
64. Van Waes V., et al. Ethanol attenuates spatial memory deficits and increases mGlu1a receptor expression in the hippocampus of rats exposed to prenatal stress. Alcohol. Clin. Exp. Res. 2009, 33:1346-1354.
65. Velazquez-Moctezuma J., et al. The effect of prenatal stress on adult sexual behavior in rats depends on the nature of the stressor. Physiol. Behav. 1993, 53:443-448.
66. Wake H., et al. Microglia: actively surveying and shaping neuronal circuit structure and function. Trends Neurosci. 2013, 36:209-217.
67. Walhovd K.B., et al. Long-term influence of normal variation in neonatal characteristics on human brain development. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:20089-20094.
68. Walker F.R., et al. Dynamic structural remodelling of microglia in health and disease: A review of the models, the signals and the mechanisms. Brain Behav. Immun. 2014, 37C:1-14.
69. Wilcoxon J.S., et al. Behavioral deficits associated with fetal alcohol exposure are reversed by prenatal thyroid hormone treatment: a role for maternal thyroid hormone deficiency in FAE. Mol. Psychiatry 2005, 10:961-971.
70. You Z., et al. Pro- and anti-inflammatory cytokines expression in rat's brain and spleen exposed to chronic mild stress: involvement in depression. Behav. Brain Res. 2011, 225:135-141.
71. Zhang Q., et al. The effects of CACNA1C gene polymorphism on spatial working memory in both healthy controls and patients with schizophrenia or bipolar disorder. Neuropsychopharmacology 2012, 37:677-684.
72. Zhang K., et al. Interleukin-1beta inhibits the differentiation of hippocampal neural precursor cells into serotonergic neurons. Brain Res. 2013, 15:193-201.
73. Zucchi F.C., et al. Maternal stress induces epigenetic signatures of psychiatric and neurological diseases in the offspring. PLoS One 2013, 8:22.