The persistent effects of maternal infection on the offspring's cognitive performance and rates of hippocampal neurogenesis

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 44, Issue , 2013, Pages 279-289

  Jiang, Peifang ^a   Zhu, Tao ^b   Zhao, Wenting ^a   Shen, Jue ^a   Yu, Yonglin ^a   Xu, Jialu ^a   Chen, Xi ^a   Yu, Huimin ^a  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b ZHEJIANG UNIVERSITY   (China)

Author keywords

Cognitive performance; Intrauterine infection; Neurogenesis; PI3K Akt signaling pathway

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; PROTEIN KINASE B;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; COGNITION; CONTROLLED STUDY; ENZYME ACTIVITY; ESCHERICHIA COLI; FEMALE; GLIA CELL; HIPPOCAMPUS; INTRAUTERINE INFECTION; LEARNING DISORDER; MALE; MEMORY DISORDER; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; PERINATAL PERIOD; PROGENY; PROTEIN EXPRESSION; RAT; SPATIAL LEARNING; SPATIAL MEMORY;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BACTERIAL INFECTIONS; BROMODEOXYURIDINE; CELL COUNT; COGNITION DISORDERS; EXPLORATORY BEHAVIOR; FEMALE; GLIAL FIBRILLARY ACIDIC PROTEIN; HIPPOCAMPUS; MALE; MAZE LEARNING; NEUROGENESIS; ORIENTATION; PHOSPHOPYRUVATE HYDRATASE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS;

EID: 84877081498     PISSN: 02785846     EISSN: 18784216     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2013.03.007     Document Type: Article

References (42)

1. Arvidsson A., Collin T., Kirik D., Kokaia Z., Lindvall O. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 2002, 8:963-970.
2. Back S.A., Riddle A., McClure M.M. Maturation-dependent vulnerability of perinatal white matter in premature birth. Stroke 2007, 38:724-730.
3. Brazil D.P., Park J., Hemmings B.A. PKB binding proteins. Getting in on the Akt. Cell 2002, 111:293-303.
4. Bruel-Jungerman E., Laroche S., Rampon C. New neurons in the dentate gyrus are involved in the expression of enhanced long-term memory following environmental enrichment. Eur J Neurosci 2005, 21:513-521.
5. Brunet A., Datta S.R., Greenberg M.E. Transcription-dependent and -independent control of neuronal survival by the PI3K-Akt signaling pathway. Curr Opin Neurobiol 2001, 11:297-305.
6. Buser J.R., Maire J., Riddle A., Gong X., Nguyen T., Nelson K., et al. Arrested preoligodendrocyte maturation contributes to myelination failure in premature infants. Ann Neurol 2012, 71:93-109.
7. Cameron H.A., Woolley C.S., McEwen B.S., Gould E. Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 1993, 56:337-344.
8. Chan C.B., Liu X., Pradoldej S., Hao C., An J., Yepes M., et al. Phosphoinositide 3-kinase enhancer regulates neuronal dendritogenesis and survival in neocortex. J Neurosci 2011, 31:8083-8092.
9. Chavali P.L., Saini R.K., Matsumoto Y., Agren H., Funa K. Nuclear orphan receptor TLX induces Oct-3/4 for the survival and maintenance of adult hippocampal progenitors upon hypoxia. J Biol Chem 2011, 286:9393-9404.
10. Fagel D.M., Ganat Y., Silbereis J., Ebbitt T., Stewart W., Zhang H., et al. Cortical neurogenesis enhanced by chronic perinatal hypoxia. Exp Neurol 2006, 199:77-91.
11. Fatemi S.H., Emamian E.S., Sidwell R.W., Kist D.A., Stary J.M., Earle J.A., et al. Human influenza viral infection in utero alters glial fibrillary acidic protein immunoreactivity in the developing brains of neonatal mice. Mol Psychiatry 2002, 7:633-640.
12. Felling R.J., Snyder M.J., Romanko M.J., Rothstein R.P., Ziegler A.N., Yang Z., et al. Neural stem/progenitor cells participate in the regenerative response to perinatal hypoxia/ischemia. J Neurosci 2006, 26:4359-4369.
13. Goldman S.A., Luskin M.B. Strategies utilized by migrating neurons of the postnatal vertebrate forebrain. Trends Neurosci 1998, 21:107-114.
14. Gould E. How widespread is adult neurogenesis in mammals?. Nat Rev Neurosci 2007, 8:481-488.
15. Gould E., Beylin A., Tanapat P., Reeves A., Shors T.J. Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 1999, 2:260-265.
16. Gould E., Reeves A.J., Graziano M.S., Gross C.G. Neurogenesis in the neocortex of adult primates. Science 1999, 286:548-552.
17. Guo Y.J., Zhang Z.J., Wang S.H., Sui Y.X., Sun Y. Notch1 signaling, hippocampal neurogenesis and behavioral responses to chronic unpredicted mild stress in adult ischemic rats. Prog Neuropsychopharmacol Biol Psychiatry 2009, 33:688-694.
18. Ihara M., Tomimoto H. Lessons from a mouse model characterizing features of vascular cognitive impairment with white matter changes. J Aging Res 2011, 2011:978761.
19. Jiang P., Sun Y., Zhu T., Zhan C., Gu W., Yuan T., et al. Endogenous neurogenesis in the hippocampus of developing rat after intrauterine infection. Brain Res 2012, 1459:1-14.
20. Kafa I.M., Uysal M., Bakirci S., Ayberk Kurt M. Sepsis induces apoptotic cell death in different regions of the brain in a rat model of sepsis. Acta Neurobiol Exp (Wars) 2010, 70:246-260.
21. Kempermann G., Kuhn H.G., Gage F.H. More hippocampal neurons in adult mice living in an enriched environment. Nature 1997, 386:493-495.
22. Kuhn H.G., Dickinson-Anson H., Gage F.H. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 1996, 16:2027-2033.
23. Kuzumaki N., Ikegami D., Tamura R., Hareyama N., Imai S., Narita M., et al. Hippocampal epigenetic modification at the brain-derived neurotrophic factor gene induced by an enriched environment. Hippocampus 2011, 21:127-132.
24. Le Belle J.E., Orozco N.M., Paucar A.A., Saxe J.P., Mottahedeh J., Pyle A.D., et al. Proliferative neural stem cells have high endogenous ROS levels that regulate self-renewal and neurogenesis in a PI3K/Akt-dependant manner. Cell Stem Cell 2011, 8:59-71.
25. Li Y., Luikart B.W., Birnbaum S., Chen J., Kwon C.H., Kernie S.G., et al. TrkB regulates hippocampal neurogenesis and governs sensitivity to antidepressive treatment. Neuron 2008, 59:399-412.
26. Luikart B.W., Zhang W., Wayman G.A., Kwon C.H., Westbrook G.L., Parada L.F. Neurotrophin-dependent dendritic filopodial motility: a convergence on PI3K signaling. J Neurosci 2008, 28:7006-7012.
27. Magavi S.S., Leavitt B.R., Macklis J.D. Induction of neurogenesis in the neocortex of adult mice. Nature 2000, 405:951-955.
28. Messaris E., Betrosian A.P., Memos N., Chatzigianni E., Boutsikou M., Economou V., et al. Administration of human protein C improves survival in an experimental model of sepsis. Crit Care Med 2010, 38:209-216.
29. Parcellier A., Tintignac L.A., Zhuravleva E., Hemmings B.A. PKB and the mitochondria: AKTing on apoptosis. Cell Signal 2008, 20:21-30.
30. Parent J.M., Silverstein F.S. Replacing neocortical neurons after stroke. Ann Neurol 2007, 61:185-186.
31. Paterniti I., Esposito E., Mazzon E., Bramanti P., Cuzzocrea S. Evidence for the role of PI(3)-kinase-AKT-eNOS signalling pathway in secondary inflammatory process after spinal cord compression injury in mice. Eur J Neurosci 2011, 33:1411-1420.
32. Romero R., Chaiworapongsa T., Espinoza J. Micronutrients and intrauterine infection, preterm birth and the fetal inflammatory response syndrome. J Nutr 2003, 133:1668S-1673S.
33. Segovia G., Yague A.G., Garcia-Verdugo J.M., Mora F. Environmental enrichment promotes neurogenesis and changes the extracellular concentrations of glutamate and GABA in the hippocampus of aged rats. Brain Res Bull 2006, 70:8-14.
34. Semmler A., Okulla T., Sastre M., Dumitrescu-Ozimek L., Heneka M.T. Systemic inflammation induces apoptosis with variable vulnerability of different brain regions. J Chem Neuroanat 2005, 30:144-157.
35. Shen Y., Yu H.M., Yuan T.M., Gu W.Z., Wu Y.D. Intrauterine infection induced oligodendrocyte injury and inducible nitric oxide synthase expression in the developing rat brain. J Perinat Med 2007, 35:203-209.
36. Song W., Volosin M., Cragnolini A.B., Hempstead B.L., Friedman W.J. ProNGF induces PTEN via p75NTR to suppress Trk-mediated survival signaling in brain neurons. J Neurosci 2010, 30:15608-15615.
37. Temple S., Alvarez-Buylla A. Stem cells in the adult mammalian central nervous system. Curr Opin Neurobiol 1999, 9:135-141.
38. van Praag H., Kempermann G., Gage F.H. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 1999, 2:266-270.
39. Yang Z., Levison S.W. Hypoxia/ischemia expands the regenerative capacity of progenitors in the perinatal subventricular zone. Neuroscience 2006, 139:555-564.
40. Yu H.M., Yuan T.M., Gu W.Z., Li J.P. Expression of glial fibrillary acidic protein in developing rat brain after intrauterine infection. Neuropathology 2004, 24:136-143.
41. Yuan T.M., Yu H.M., Gu W.Z., Li J.P. White matter damage and chemokine induction in developing rat brain after intrauterine infection. J Perinat Med 2005, 33:415-422.
42. Zhang Y., Park T.S., Gidday J.M. Hypoxic preconditioning protects human brain endothelium from ischemic apoptosis by Akt-dependent survivin activation. Am J Physiol Heart Circ Physiol 2007, 292:H2573-H2581.