Effects of maternal immune activation on adult neurogenesis in the subventricular zone-olfactory bulb pathway and olfactory discrimination

Schizophrenia Research

Volumn 151, Issue 1-3, 2013, Pages 1-11

  Liu, Yuan Hsuan ^a   Lai, Wen Sung ^b   Tsay, Huey Jen ^a   Wang, Tsu Wei ^a,c   Yu, Jenn Yah ^a  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^c NATIONAL TAIWAN NORMAL UNIVERSITY   (Taiwan)

Author keywords

Adult neurogenesis; Olfaction; Olfactory bulb; Prenatal immune activation; Schizophrenia; Subventricular zone

Indexed keywords

INTERLEUKIN 6;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL LINEAGE; CELL PROLIFERATION; CELL TYPE; CONTROLLED STUDY; FEMALE; IMMUNOMODULATION; MALE; MATERNAL IMMUNE ACTIVATION; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROBLAST; NONHUMAN; OLFACTORY BULB; OLFACTORY DISCRIMINATION; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; SUBVENTRICULAR ZONE; TASK PERFORMANCE;

ADULT NEUROGENESIS; OLFACTION; OLFACTORY BULB; PRENATAL IMMUNE ACTIVATION; SCHIZOPHRENIA; SUBVENTRICULAR ZONE;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL PROLIFERATION; CEREBRAL VENTRICLES; DISCRIMINATION (PSYCHOLOGY); DISEASE MODELS, ANIMAL; FEMALE; GLIAL FIBRILLARY ACIDIC PROTEIN; HIPPOCAMPUS; MICE; MICROTUBULE-ASSOCIATED PROTEINS; NEUROGENESIS; NEUROPEPTIDES; OLFACTORY BULB; OLFACTORY PATHWAYS; POLY I-C; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; SMELL; SOXB1 TRANSCRIPTION FACTORS;

EID: 84889097849     PISSN: 09209964     EISSN: 15732509     Source Type: Journal    
DOI: 10.1016/j.schres.2013.09.007     Document Type: Article

References (70)

1. Alvarez-Buylla A., Garcia-Verdugo J.M. Neurogenesis in adult subventricular zone. J. Neurosci. 2002, 22(3):629-634.
2. Arndt T.L., Stodgell C.J., Rodier P.M. The teratology of autism. Int. J. Dev. Neurosci. 2005, 23(2-3):189-199.
3. Atanasova B., Graux J., El Hage W., Hommet C., Camus V., Belzung C. Olfaction: a potential cognitive marker of psychiatric disorders. Neurosci. Biobehav. Rev. 2008, 32(7):1315-1325.
4. Baharnoori M., Bhardwaj S.K., Srivastava L.K. Neonatal behavioral changes in rats with gestational exposure to lipopolysaccharide: a prenatal infection model for developmental neuropsychiatric disorders. Schizophr. Bull. 2012, 38(3):444-456.
5. Balu D.T., Lucki I. Adult hippocampal neurogenesis: regulation, functional implications, and contribution to disease pathology. Neurosci. Biobehav. Rev. 2009, 33(3):232-252.
6. Bath K.G., Mandairon N., Jing D., Rajagopal R., Kapoor R., Chen Z.Y., Khan T., Proenca C.C., Kraemer R., Cleland T.A., Hempstead B.L., Chao M.V., Lee F.S. Variant brain-derived neurotrophic factor (Val66Met) alters adult olfactory bulb neurogenesis and spontaneous olfactory discrimination. J. Neurosci. 2008, 28(10):2383-2393.
7. Bielsky I.F., Hu S.B., Szegda K.L., Westphal H., Young L.J. Profound impairment in social recognition and reduction in anxiety-like behavior in vasopressin V1a receptor knockout mice. Neuropsychopharmacology 2004, 29(3):483-493.
8. Boksa P. Effects of prenatal infection on brain development and behavior: a review of findings from animal models. Brain Behav. Immun. 2010, 24(6):881-897.
9. Bolteus A.J., Bordey A. GABA release and uptake regulate neuronal precursor migration in the postnatal subventricular zone. J. Neurosci. 2004, 24(35):7623-7631.
10. Borrell J., Vela J.M., Arevalo-Martin A., Molina-Holgado E., Guaza C. Prenatal immune challenge disrupts sensorimotor gating in adult rats. Implications for the etiopathogenesis of schizophrenia. Neuropsychopharmacology 2002, 26(2):204-215.
11. Bovetti S., Gribaudo S., Puche A.C., De Marchis S., Fasolo A. From progenitors to integrated neurons: role of neurotransmitters in adult olfactory neurogenesis. J. Chem. Neuroanat. 2011, 42(4):304-316.
12. Brennand K.J., Simone A., Jou J., Gelboin-Burkhart C., Tran N., Sangar S., Li Y., Mu Y., Chen G., Yu D., McCarthy S., Sebat J., Gage F.H. Modelling schizophrenia using human induced pluripotent stem cells. Nature 2011, 473(7346):221-225.
13. Breton-Provencher V., Saghatelyan A. Newborn neurons in the adult olfactory bulb: unique properties for specific odor behavior. Behav. Brain Res. 2012, 227(2):480-489.
14. Brown A.S., Begg M.D., Gravenstein S., Schaefer C.A., Wyatt R.J., Bresnahan M., Babulas V.P., Susser E.S. Serologic evidence of prenatal influenza in the etiology of schizophrenia. Arch. Gen. Psychiatry 2004, 61(8):774-780.
15. Cui K., Ashdown H., Luheshi G.N., Boksa P. Effects of prenatal immune activation on hippocampal neurogenesis in the rat. Schizophr. Res. 2009, 113(2-3):288-297.
16. Dammann O., Leviton A. Does prepregnancy bacterial vaginosis increase a mother's risk of having a preterm infant with cerebral palsy?. Dev. Med. Child Neurol. 1997, 39(12):836-840.
17. Doetsch F., Caille I., Lim D.A., Garcia-Verdugo J.M., Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 1999, 97(6):703-716.
18. Dong H.-W., Allen Institute for Brain Science Allen reference atlas: a digital color brain atlas of the C57Black//6J male mouse 2008, Wiley, Hoboken, NJ.
19. Fan Y., Abrahamsen G., McGrath J.J., Mackay-Sim A. Altered cell cycle dynamics in schizophrenia. Biol. Psychiatry 2012, 71(2):129-135.
20. Fatemi S.H., Reutiman T.J., Folsom T.D., Huang H., Oishi K., Mori S., Smee D.F., Pearce D.A., Winter C., Sohr R., Juckel G. Maternal infection leads to abnormal gene regulation and brain atrophy in mouse offspring: implications for genesis of neurodevelopmental disorders. Schizophr. Res. 2008, 99(1-3):56-70.
21. Ferguson J.N., Young L.J., Hearn E.F., Matzuk M.M., Insel T.R., Winslow J.T. Social amnesia in mice lacking the oxytocin gene. Nat. Genet. 2000, 25(3):284-288.
22. Feron F., Perry C., Hirning M.H., McGrath J., Mackay-Sim A. Altered adhesion, proliferation and death in neural cultures from adults with schizophrenia. Schizophr. Res. 1999, 40(3):211-218.
23. 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.
24. Gheusi G., Cremer H., McLean H., Chazal G., Vincent J.D., Lledo P.M. Importance of newly generated neurons in the adult olfactory bulb for odor discrimination. Proc. Natl. Acad. Sci. U. S. A. 2000, 97(4):1823-1828.
25. Gilmore J.H., Jarskog L.F., Vadlamudi S. Maternal poly I:C exposure during pregnancy regulates TNF alpha, BDNF, and NGF expression in neonatal brain and the maternal-fetal unit of the rat. J. Neuroimmunol. 2005, 159(1-2):106-112.
26. Girard S., Tremblay L., Lepage M., Sebire G. IL-1 receptor antagonist protects against placental and neurodevelopmental defects induced by maternal inflammation. J. Immunol. 2010, 184(7):3997-4005.
27. Golan H.M., Lev V., Hallak M., Sorokin Y., Huleihel M. Specific neurodevelopmental damage in mice offspring following maternal inflammation during pregnancy. Neuropharmacology 2005, 48(6):903-917.
28. Gonzalez-Perez O., Gutierrez-Fernandez F., Lopez-Virgen V., Collas-Aguilar J., Quinones-Hinojosa A., Garcia-Verdugo J.M. Immunological regulation of neurogenic niches in the adult brain. Neuroscience 2012, 226:270-281.
29. Graciarena M., Depino A.M., Pitossi F.J. Prenatal inflammation impairs adult neurogenesis and memory related behavior through persistent hippocampal TGFbeta1 downregulation. Brain Behav. Immun. 2010, 24(8):1301-1309.
30. Kageyama R., Imayoshi I., Sakamoto M. The role of neurogenesis in olfaction-dependent behaviors. Behav. Brain Res. 2012, 227(2):459-463.
31. Kempermann G., Gage F.H. Genetic influence on phenotypic differentiation in adult hippocampal neurogenesis. Brain Res. Dev. Brain Res. 2002, 134(1-2):1-12.
32. Keohane A., Ryan S., Maloney E., Sullivan A.M., Nolan Y.M. Tumour necrosis factor-alpha impairs neuronal differentiation but not proliferation of hippocampal neural precursor cells: Role of Hes1. Mol. Cell. Neurosci. 2010, 43(1):127-135.
33. Koo J.W., Duman R.S. IL-1beta is an essential mediator of the antineurogenic and anhedonic effects of stress. Proc. Natl. Acad. Sci. U. S. A. 2008, 105(2):751-756.
34. Lante 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 Radic. Biol. Med. 2007, 42(8):1231-1245.
35. Larouche A., Roy M., Kadhim H., Tsanaclis A.M., Fortin D., Sebire G. Neuronal injuries induced by perinatal hypoxic-ischemic insults are potentiated by prenatal exposure to lipopolysaccharide: animal model for perinatally acquired encephalopathy. Dev. Neurosci. 2005, 27(2-4):134-142.
36. Lledo P.M., Saghatelyan A. Integrating new neurons into the adult olfactory bulb: joining the network, life-death decisions, and the effects of sensory experience. Trends Neurosci. 2005, 28(5):248-254.
37. Lois C., Alvarez-Buylla A. Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc. Natl. Acad. Sci. U. S. A. 1993, 90(5):2074-2077.
38. Makinodan M., Tatsumi K., Manabe T., Yamauchi T., Makinodan E., Matsuyoshi H., Shimoda S., Noriyama Y., Kishimoto T., Wanaka A. Maternal immune activation in mice delays myelination and axonal development in the hippocampus of the offspring. J. Neurosci. Res. 2008, 86(10):2190-2200.
39. Malaspina D., Perera G.M., Lignelli A., Marshall R.S., Esser P.D., Storer S., Furman V., Wray A.D., Coleman E., Gorman J.M., Van Heertum R.L. SPECT imaging of odor identification in schizophrenia. Psychiatry Res. 1998, 82(1):53-61.
40. McCurdy R.D., Feron F., Perry C., Chant D.C., McLean D., Matigian N., Hayward N.K., McGrath J.J., Mackay-Sim A. Cell cycle alterations in biopsied olfactory neuroepithelium in schizophrenia and bipolar I disorder using cell culture and gene expression analyses. Schizophr. Res. 2006, 82(2-3):163-173.
41. Mednick S.A., Machon R.A., Huttunen M.O., Bonett D. Adult schizophrenia following prenatal exposure to an influenza epidemic. Arch. Gen. Psychiatry 1988, 45(2):189-192.
42. 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(18):4752-4762.
43. Meyer U., Nyffeler M., Schwendener S., Knuesel I., Yee B.K., Feldon J. Relative prenatal and postnatal maternal contributions to schizophrenia-related neurochemical dysfunction after in utero immune challenge. Neuropsychopharmacology 2008, 33(2):441-456.
44. 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 late fetal development in mice. Brain Behav. Immun. 2008, 22(4):469-486.
45. Miller M.T., Stromland K., Ventura L., Johansson M., Bandim J.M., Gillberg C. Autism associated with conditions characterized by developmental errors in early embryogenesis: a mini review. Int. J. Dev. Neurosci. 2005, 23(2-3):201-219.
46. Nguyen A.D., Shenton M.E., Levitt J.J. Olfactory dysfunction in schizophrenia: a review of neuroanatomy and psychophysiological measurements. Harv. Rev. Psychiatry 2010, 18(5):279-292.
47. Nguyen A.D., Pelavin P.E., Shenton M.E., Chilakamarri P., McCarley R.W., Nestor P.G., Levitt J.J. Olfactory sulcal depth and olfactory bulb volume in patients with schizophrenia: an MRI study. Brain Imaging Behav. 2011, 5(4):252-261.
48. Nyffeler M., Meyer U., Yee B.K., Feldon J., Knuesel I. Maternal immune activation during pregnancy increases limbic GABAA receptor immunoreactivity in the adult offspring: implications for schizophrenia. Neuroscience 2006, 143(1):51-62.
49. Petreanu L., Alvarez-Buylla A. Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J. Neurosci. 2002, 22(14):6106-6113.
50. Piontkewitz Y., Bernstein H.G., Dobrowolny H., Bogerts B., Weiner I., Keilhoff G. Effects of risperidone treatment in adolescence on hippocampal neurogenesis, parvalbumin expression, and vascularization following prenatal immune activation in rats. Brain Behav. Immun. 2012, 26(2):353-363.
51. Rampon C., Tang Y.P., Goodhouse J., Shimizu E., Kyin M., Tsien J.Z. Enrichment induces structural changes and recovery from nonspatial memory deficits in CA1 NMDAR1-knockout mice. Nat. Neurosci. 2000, 3(3):238-244.
52. Reif A., Fritzen S., Finger M., Strobel A., Lauer M., Schmitt A., Lesch K.P. Neural stem cell proliferation is decreased in schizophrenia, but not in depression. Mol. Psychiatry 2006, 11(5):514-522.
53. Rupp C.I., Fleischhacker W.W., Kemmler G., Kremser C., Bilder R.M., Mechtcheriakov S., Szeszko P.R., Walch T., Scholtz A.W., Klimbacher M., Maier C., Albrecht G., Lechner-Schoner T., Felber S., Hinterhuber H. Olfactory functions and volumetric measures of orbitofrontal and limbic regions in schizophrenia. Schizophr. Res. 2005, 74(2-3):149-161.
54. Rupp C.I., Fleischhacker W.W., Kemmler G., Oberbauer H., Scholtz A.W., Wanko C., Hinterhuber H. Various bilateral olfactory deficits in male patients with schizophrenia. Schizophr. Bull. 2005, 31(1):155-165.
55. Samuelsson A.M., Jennische E., Hansson H.A., Holmang A. Prenatal exposure to interleukin-6 results in inflammatory neurodegeneration in hippocampus with NMDA/GABA(A) dysregulation and impaired spatial learning. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2006, 290(5):R1345-R1356.
56. 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(1):297-302.
57. Shi L., Smith S.E., Malkova N., Tse D., Su Y., Patterson P.H. Activation of the maternal immune system alters cerebellar development in the offspring. Brain Behav. Immun. 2009, 23(1):116-123.
58. Smith S.E., Li J., Garbett K., Mirnics K., Patterson P.H. Maternal immune activation alters fetal brain development through interleukin-6. J. Neurosci. 2007, 27(40):10695-10702.
59. Spooren A., Kolmus K., Laureys G., Clinckers R., De Keyser J., Haegeman G., Gerlo S. Interleukin-6, a mental cytokine. Brain Res. Rev. 2011, 67(1-2):157-183.
60. Suh H., Deng W., Gage F.H. Signaling in adult neurogenesis. Annu. Rev. Cell Dev. Biol. 2009, 25:253-275.
61. Takamura A., Okamoto Y., Kawarabayashi T., Yokoseki T., Shibata M., Mouri A., Nabeshima T., Sun H., Abe K., Urisu T., Yamamoto N., Shoji M., Yanagisawa K., Michikawa M., Matsubara E. Extracellular and intraneuronal HMW-AbetaOs represent a molecular basis of memory loss in Alzheimer's disease model mouse. Mol. Neurodegener. 2011, 6(1):20.
62. Turetsky B.I., Moberg P.J., Yousem D.M., Doty R.L., Arnold S.E., Gur R.E. Reduced olfactory bulb volume in patients with schizophrenia. Am. J. Psychiatry 2000, 157(5):828-830.
63. Urakubo A., Jarskog L.F., Lieberman J.A., Gilmore J.H. Prenatal exposure to maternal infection alters cytokine expression in the placenta, amniotic fluid, and fetal brain. Schizophr. Res. 2001, 47(1):27-36.
64. Wang H., Shimizu E., Tang Y.P., Cho M., Kyin M., Zuo W., Robinson D.A., Alaimo P.J., Zhang C., Morimoto H., Zhuo M., Feng R., Shokat K.M., Tsien J.Z. Inducible protein knockout reveals temporal requirement of CaMKII reactivation for memory consolidation in the brain. Proc. Natl. Acad. Sci. U. S. A. 2003, 100(7):4287-4292.
65. Wang T.W., Zhang H., Gyetko M.R., Parent J.M. Hepatocyte growth factor acts as a mitogen and chemoattractant for postnatal subventricular zone-olfactory bulb neurogenesis. Mol. Cell. Neurosci. 2011, 48(1):38-50.
66. Wolf S.A., Melnik A., Kempermann G. Physical exercise increases adult neurogenesis and telomerase activity, and improves behavioral deficits in a mouse model of schizophrenia. Brain Behav. Immun. 2011, 25(5):971-980.
67. Wu Y.W., Colford J.M. Chorioamnionitis as a risk factor for cerebral palsy: a meta-analysis. JAMA 2000, 284(11):1417-1424.
68. Wu J.H., Han Y.T., Yu J.Y., Wang T.W. Pheromones from males of different familiarity exert divergent effects on adult neurogenesis in the female Accessory Olfactory Bulb. Dev. Neurobiol. 2013, 73(8):632-645.
69. Zhao C., Deng W., Gage F.H. Mechanisms and functional implications of adult neurogenesis. Cell 2008, 132(4):645-660.
70. 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(10):1778-1789.