Impaired migration signaling in the hippocampus following prenatal hypoxia

Neuropharmacology

Volumn 57, Issue 5-6, 2009, Pages 511-522

  Golan, M Hava ^a   Mane, Revital ^a   Molczadzki, Gabriela ^a   Zuckerman, Michal ^a   Kaplan Louson, Vered ^a   Huleihel, Mahmoud ^a   Perez Polo, J Regino ^b  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b University of Texas Medical Branch School of Medicine   (United States)

Author keywords

14 3 3 ; APP; Dab1; Magnesium sulfate; Reelin

Indexed keywords

AMYLOID PRECURSOR PROTEIN; BRAIN DERIVED NEUROTROPHIC FACTOR; MAGNESIUM SULFATE; NEUROGENIC DIFFERENTIATION FACTOR; REELIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; BRAIN NERVE CELL; CELL MIGRATION; COGNITIVE DEFECT; FETUS HYPOXIA; GENE EXPRESSION; GESTATIONAL AGE; HIPPOCAMPUS; INFLAMMATION; ISCHEMIA; MOTOR DYSFUNCTION; MOUSE; NERVE CELL NECROSIS; NERVOUS SYSTEM DEVELOPMENT; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; ANIMALS, NEWBORN; CELL ADHESION MOLECULES, NEURONAL; CELL DEATH; CELL MOVEMENT; CENTRAL NERVOUS SYSTEM AGENTS; DENTATE GYRUS; DISEASE MODELS, ANIMAL; ENCEPHALITIS; EXTRACELLULAR MATRIX PROTEINS; FETAL HYPOXIA; HIPPOCAMPUS; HYPOXIA, BRAIN; MAGNESIUM SULFATE; MICE; MICE, INBRED C57BL; NERVE TISSUE PROTEINS; NEUROGENESIS; NEURONS; RANDOM ALLOCATION; SERINE ENDOPEPTIDASES; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 69649089751     PISSN: 00283908     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2009.07.028     Document Type: Article

References (59)

1. Alcantara S., Ruiz M., D'Arcangelo G., Ezan F., de Lecea L., Curran T., Sotelo C., and Soriano E. Regional and cellular patterns of reelin mRNA expression in the forebrain of the developing and adult mouse. Journal of Neuroscience 18 (1998) 7779-7799
2. Altman J., and Bayer S.A. Mosaic organization of the hippocampal neuroepithelium and the multiple germinal sources of dentate granule cells. Journal of Comparative Neurology 301 3 (1990) 325-342
3. Altman J., and Bayer S.A. Prolonged sojourn of developing pyramidal cells in the intermediate zone of the hippocampus and their settling in the stratum pyramidale. Journal of Comparative Neurology 301 3 (1990) 343-364
4. Andrade N., Komnenovic V., Blake S.M., Jossin Y., Howell B., Goffinet A., Schneider W.J., and Nimpf J. ApoER2/VLDL receptor and Dab1 in the rostral migratory stream function in postnatal neuronal migration independently of reelin. Proceedings of the National Academy of Sciences of the United States of America 104 (2007) 8508-8513
5. Boksa P. Animal models of obstetric complications in relation to schizophrenia. Brain Research. Brain Research Reviews 45 (2004) 1-17
6. Cai Z., and Rhodes P.G. Intrauterine hypoxia-ischemia alters expression of the NMDA receptor in the young rat brain. Neurochemical Research 26 5 (2001) 487-495
7. Chun J.J., and Shatz C.J. A fibronectin-like molecule is present in the developing cat cerebral cortex and is correlated with subplate neurons. Journal of Cell Biology 106 3 (1988) 857-872
8. Crowther C.A., Hiller J.E., Doyle L.W., Haslam R.R., and Australasian Collaborative Trial of Magnesium Sulphate (ACTOMg SO4) Collaborative Group. Effect of magnesium sulfate given for neuroprotection before preterm birth: a randomized controlled trial. JAMA: The Journal of the American Medical Association 290 (2003) 2669-2676
9. D'Arcangelo G. Reelin mouse mutants as models of cortical development disorders. Epilepsy & Behavior: E&B 8 (2006) 81-90
10. D'Arcangelo G., Homayouni R., Keshvara L., Rice D.S., Sheldon M., and Curran T. Reelin is a ligand for lipoprotein receptors. Neuron 24 (1999) 471-479
11. Duley L. Evidence and practice: the magnesium sulphate story. Best Practice & Research. Clinical Obstetrics & Gynaecology 19 (2005) 57-74
12. Fatemi S.H. Reelin mutations in mouse and man: from reeler mouse to schizophrenia, mood disorders, autism and lissencephaly. Molecular Psychiatry 6 (2001) 129-133
13. Gill M.B., and Perez-Polo J.R. Hypoxia ischemia-mediated cell death in neonatal rat brain. Neurochemical Research (2008)
14. Golan H., Kashtutsky I., Hallak M., Sorokin Y., and Huleihel M. Maternal hypoxia during pregnancy delays the development of motor reflexes in newborn mice. Developmental Neuroscience 26 (2004) 24-29
15. Golan H., Kashtuzki I., Hallak M., Sorokin Y., and Huleihel M. Maternal hypoxia during pregnancy induces fetal neurodevelopmental brain damage: partial protection by magnesium sulfate. Journal of Neuroscience Research 78 (2004) 430-441
16. Graham E.M., Sheldon R.A., Flock D.L., Ferriero D.M., Martin L.J., O'Riordan D.P., and Northington F.J. Neonatal mice lacking functional fas death receptors are resistant to hypoxic-ischemic brain injury. Neurobiology of Disease 17 (2004) 89-98
17. Gressens P. Pathogenesis of migration disorders. Current Opinion in Neurology 19 (2006) 135-140
18. Grojean S., Pourie G., Vert P., and Daval J.L. Differential neuronal fates in the CA1 hippocampus after hypoxia in newborn and 7-day-old rats: effects of pre-treatment with MK-801. Hippocampus 13 (2003) 970-977
19. Hallak M., Hotra J.W., and Kupsky W.J. Magnesium sulfate protection of fetal rat brain from severe maternal hypoxia. Obstetrics and Gynecology 96 (2000) 124-128
20. Herz J., and Chen Y. Reelin, lipoprotein receptors and synaptic plasticity. Nature Reviews. Neuroscience 7 (2006) 850-859
21. Hoareau C., Borrell V., Soriano E., Krebs M.O., Prochiantz A., and Allinquant B. Amyloid precursor protein cytoplasmic domain antagonizes reelin neurite outgrowth inhibition of hippocampal neurons. Neurobiology of Aging 29 (2008) 542-553
22. Hoe H.S., Tran T.S., Matsuoka Y., Howell B.W., and Rebeck G.W. DAB1 and reelin effects on amyloid precursor protein and ApoE receptor 2 trafficking and processing. The Journal of Biological Chemistry 281 (2006) 35176-35185
23. Holcberg G., Amash A., Sapir O., Hallak M., Sheiner E., Ducler D., Katz M., and Huleihel M. Different effects of magnesium sulfate and angiotensin II on the capacity of the fetal and maternal compartments of normal human placenta to secrete TNF-alpha and IL-6. Journal of Reproductive Immunology 69 (2006) 115-125
24. Homayouni R., Rice D.S., Sheldon M., and Curran T. Disabled-1 binds to the cytoplasmic domain of amyloid precursor-like protein 1. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 19 (1999) 7507-7515
25. Hu X., Nesic-Taylor O., Qiu J., Rea H.C., Fabian R., Rassin D.K., and Perez-Polo J.R. Activation of nuclear factor-kappaB signaling pathway by interleukin-1 after hypoxia/ischemia in neonatal rat hippocampus and cortex. Journal of Neurochemistry 93 (2005) 26-37
26. Hu X., Qiu J., Grafe M.R., Rea H.C., Rassin D.K., and Perez-Polo J.R. Bcl-2 family members make different contributions to cell death in hypoxia and/or hyperoxia in rat cerebral cortex. International Journal of Developmental Neuroscience: The Official Journal of the International Society for Developmental Neuroscience 21 (2003) 371-377
27. Impagnatiello F., Guidotti A.R., Pesold C., Dwivedi Y., Caruncho H., Pisu M.G., Uzunov D.P., Smalheiser N.R., Davis J.M., Pandey G.N., Pappas G.D., Tueting P., Sharma R.P., and Costa E. A decrease of reelin expression as a putative vulnerability factor in schizophrenia. Proc Natl Acad Sci. 95 26 (1998) 15718-15723
28. Johnston M.V. Neurotransmitters and vulnerability of the developing brain. Brain and Development 17 5 (1996) 301-306
29. Jossin Y., Bar I., Ignatova N., Tissir F., De Rouvroit C.L., and Goffinet A.M. The reelin signaling pathway: some recent developments. Cerebral Cortex (New York, N.Y.: 1991) 13 (2003) 627-633
30. Jossin Y., Gui L., and Goffinet A.M. Processing of reelin by embryonic neurons is important for function in tissue but not in dissociated cultured neurons. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 27 (2007) 4243-4252
31. Kato M., and Dobyns W.B. Lissencephaly and the molecular basis of neuronal migration. Human Molecular Genetics 12 Spec No 1 (2003) R89-R96
32. Liu C.L., Siesjo B.K., and Hu B.R. Pathogenesis of hippocampal neuronal death after hypoxia-ischemia changes during brain development. Neuroscience 127 (2004) 113-123
33. Lorenzo A., Yuan M., Zhang Z., Paganetti P.A., Sturchler-Pierrat C., Staufenbiel M., Mautino J., Vigo F.S., Sommer B., and Yankner B.A. Amyloid beta interacts with the amyloid precursor protein: a potential toxic mechanism in alzheimer's disease. Nature Neuroscience 3 (2000) 460-464
34. Louzoun-Kaplan V., Zuckerman M., Perez-Polo J.R., and Golan H.M. Prenatal hypoxia down regulates the GABA pathway in newborn mice cerebral cortex; partial protection by MgSO4. International Journal of Developmental Neuroscience: The Official Journal of the International Society for Developmental Neuroscience 26 (2008) 77-85
35. Marmarou C.R., Walker S.A., Davis C.L., and Povlishock J.T. Quantitative analysis of the relationship between intra- axonal neurofilament compaction and impaired axonal transport following diffuse traumatic brain injury. Journal of Neurotrauma 22 (2005) 1066-1080
36. Martinez A., Alcantara S., Borrell V., et al. TrkB and TrkC signaling are required for maturation and synaptogenesis of hippocampal connections. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 18 (1998) 7336-7350
37. McAllister A.K., Katz L.C., and Lo D.C. Opposing roles for endogenous BDNF and NT-3 in regulating cortical dendritic growth. Neuron 18 (1997) 767-778
38. McAllister A.K., Lo D.C., and Katz L.C. Neurotrophins regulate dendritic growth in developing visual cortex. Neuron 15 (1995) 791-803
39. Nakajima W., Ishida A., Lange M.S., Gabrielson K.L., Wilson M.A., Martin L.J., Blue M.E., and Johnston M.V. Apoptosis has a prolonged role in the neurodegeneration after hypoxic ischemia in the newborn rat. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 20 (2000) 7994-8004
40. Nelson K.B., and Grether J.K. Can magnesium sulfate reduce the risk of cerebral palsy in very low birthweight infants?. Pediatrics 95 (1995) 263-269
41. Niu S., Renfro A., Quattrocchi C.C., Sheldon M., and D'Arcangelo G. Reelin promotes hippocampal dendrite development through the VLDLR/ApoER2-Dab1 pathway. Neuron 41 (2004) 71-84
42. Northington F.J., Ferriero D.M., Flock D.L., and Martin L.J. Delayed neurodegeneration in neonatal rat thalamus after hypoxia-ischemia is apoptosis. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 21 (2001) 1931-1938
43. Northington F.J., Ferriero D.M., and Martin L.J. Neurodegeneration in the thalamus following neonatal hypoxia-ischemia is programmed cell death. Developmental Neuroscience 23 (2001) 186-191
44. Olsson A., Csajbok L., Ost M., Hoglund K., Nylen K., Rosengren L., Nellgard B., and Blennow K. Marked increase of beta-amyloid(1-42) and amyloid precursor protein in ventricular cerebrospinal fluid after severe traumatic brain injury. Journal of Neurology 251 (2004) 870-876
45. Pocock R., and Hobert O. Oxygen levels affect axon guidance and neuronal migration in caenorhabditis elegans. Nat Neurosci 11 8 (2008) 894-900
46. Qiu J., Hu X., Nesic O., Grafe M.R., Rassin D.K., Wood T.G., and Perez-Polo J.R. Effects of NF-kappaB oligonucleotide "decoys" on gene expression in P7 rat hippocampus after hypoxia/ischemia. Journal of Neuroscience Research 77 (2004) 108-118
47. Sheldon R.A., Hall J.J., Noble L.J., and Ferriero D.M. Delayed cell death in neonatal mouse hippocampus from hypoxia-ischemia is neither apoptotic nor necrotic. Neuroscience Letters 304 (2001) 165-168
48. Sibai B.M. Magnesium sulfate prophylaxis in preeclampsia: lessons learned from recent trials. American Journal of Obstetrics and Gynecology 190 (2004) 1520-1526
49. Smith K.E., Keeney S., Zhang L., Perez-Polo J.R., and Rassin D.K. The association of early blood oxygenation with child development in preterm infants with acute respiratory disorders. International Journal of Developmental Neuroscience: The Official Journal of the International Society for Developmental Neuroscience 26 (2008) 125-131
50. Solecki D.J., Govek E.E., and Hatten M.E. mPar6 alpha controls neuronal migration. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 26 (2006) 10624-10625
51. Tissir F., and Goffinet A.M. Reelin and brain development. Nature Reviews. Neuroscience 4 (2003) 496-505
52. Toyo-oka K., Shionoya A., Gambello M.J., et al. 14-3-3epsilon is important for neuronal migration by binding to NUDEL: a molecular explanation for miller-dieker syndrome. Nature Genetics 34 (2003) 274-285
53. Trommsdorff M., Gotthardt M., Hiesberger T., Shelton J., Stockinger W., Nimpf J., Hammer R.E., Richardson J.A., and Herz J. Reeler/Disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell 97 (1999) 689-701
54. Wei X., Zhao L., Ma Z., Holtzman D.M., Yan C., Dodel R.C., Hampel H., Oertel W., Farlow M.R., and Du Y. Caffeic acid phenethyl ester prevents neonatal hypoxic-ischaemic brain injury. Brain: A Journal of Neurology 127 (2004) 2629-2635
55. Weiss K.H., Johanssen C., Tielsch A., Herz J., Deller T., Frotscher M., and Forster E. Malformation of the radial glial scaffold in the dentate gyrus of reeler mice, scrambler mice, and ApoER2/VLDLR-deficient mice. The Journal of Comparative Neurology 460 (2003) 56-65
56. Yasuoka K., Hirata K., Kuraoka A., He J.W., and Kawabuchi M. Expression of amyloid precursor protein-like molecule in astroglial cells of the subventricular zone and rostral migratory stream of the adult rat forebrain. Journal of Anatomy 205 (2004) 135-146
57. Young-Pearse T.L., Bai J., Chang R., Zheng J.B., LoTurco J.J., and Selkoe D.J. A critical function for beta-amyloid precursor protein in neuronal migration revealed by in utero RNA interference. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 27 (2007) 14459-14469
58. Zhang X., Zhou K., Wang R., Cui J., Lipton S.A., Liao F.F., Xu H., and Zhang Y.W. Hypoxia-inducible factor 1alpha (HIF-1alpha)-mediated hypoxia increases BACE1 expression and beta-amyloid generation. The Journal of Biological Chemistry 282 (2007) 10873-10880
59. Zhao S., Chai X., Bock H.H., Brunne B., Forster E., and Frotscher M. Rescue of the reeler phenotype in the dentate gyrus by wild-type coculture is mediated by lipoprotein receptors for reelin and disabled 1. The Journal of Comparative Neurology 495 (2006) 1-9