Long-Term Effects of Prenatal Hypoxia on Schizophrenia-Like Phenotype in Heterozygous Reeler Mice

Molecular Neurobiology

Volumn 53, Issue 5, 2016, Pages 3267-3276

  Howell, Kristy R ^a,b   Pillai, Anilkumar ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

Behavior; Blood flow; Mice; Prenatal hypoxia; Reelin; Schizophrenia; Stress; VEGF

Indexed keywords

CORTICOSTERONE; GLUCOCORTICOID RECEPTOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; REELIN; VASCULOTROPIN; VASCULOTROPIN A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; BLOOD FLOW; BRAIN LEVEL; BRAIN SIZE; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; FEMALE; FRONTAL CORTEX; HIPPOCAMPUS; HYPOXIA; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRENATAL HYPOXIA; PRENATAL PERIOD; PREPULSE INHIBITION; SCHIZOPHRENIA; SPATIAL MEMORY; ANIMAL; ANIMAL BEHAVIOR; BLOOD; COMPLICATION; HETEROZYGOTE; MAZE TEST; METABOLISM; MOUSE MUTANT; PATHOLOGY; PATHOPHYSIOLOGY; PHENOTYPE; PHYSIOLOGY; STARTLE REFLEX; TASK PERFORMANCE; TIME FACTOR;

ANIMALS; BEHAVIOR, ANIMAL; CORTICOSTERONE; HETEROZYGOTE; HIPPOCAMPUS; HYPOXIA; MAZE LEARNING; MICE, NEUROLOGIC MUTANTS; PHENOTYPE; PREPULSE INHIBITION; RECEPTORS, GLUCOCORTICOID; REFLEX, STARTLE; SCHIZOPHRENIA; TASK PERFORMANCE AND ANALYSIS; TIME FACTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84930800610     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-015-9265-4     Document Type: Article

References (46)

1. Lillrank SM, Lipska BK, Weinberger DR (1995) Neurodevelopmental animal models of schizophrenia. Clin Neurosci 3(2):98–104
2. Bayer TA, Falkai P, Maier W (1999) Genetic and non-genetic vulnerability factors in schizophrenia: the basis of the “two hit hypothesis”. J Psychiatr Res 33(6):543–548
3. Marenco S, Weinberger DR (2000) The neurodevelopmental hypothesis of schizophrenia: following a trail of evidence from cradle to grave. Dev Psychopathol 12:501–527
4. Fatemi SH, Folsom TD (2009) The neurodevelopmental hypothesis of schizophrenia, revisited. Schizophr Bull 35(3):528–548
5. Rapoport JL, Addington AM, Frangou S, Psych MR (2005) The neurodevelopmental model of schizophrenia: update 2005. Mol Psychiatry 10(5):434–449
6. Harrison PJ, Weinberger DR (2005) Schizophrenia genes, gene expression, and neuropathology: on the matter of their convergence. Mol Psychiatry 10(1):40–68
7. Demjaha A, MacCabe JH, Murray RM (2011) How genes and environmental factors determine the different neurodevelopmental trajectories of schizophrenia and bipolar disorder. Schizophr Bull
8. Clarke MK, Harley M, Cannon M (2006) The role of obstetric events in schizophrenia. Schizophr Bull 32(1):3–8
9. Nicodemus KK, Marenco S, Batten AJ, Vakkalanka R, Egan MF, Straub RE, Weinberger DR (2008) Serious obstetric complications interact with hypoxia-regulated/vascular-expression genes to influence schizophrenia risk. Mol Psychiatry 13(9):873–877
10. Boksa P (2004) Animal models of obstetric complications in relation to schizophrenia. Brain Res Rev 45:1–17
11. Van Erp TG, Saleh PA, Rosso IM, Huttunen M, Lönnqvist J, Pirkola T, Salonen O, Valanne L et al (2002) Contributions of genetic risk and fetal hypoxia to hippocampal volume in patients with schizophrenia or schizoaffective disorder, their unaffected siblings, and healthy unrelated volunteers. Am J Psychiatry 159:1514–1520
12. Schmidt-Kastner R, van Os J, Steinbusch HWM, Schmitz C (2006) Gene regulation by hypoxia and the neurodevelopmental origin of schizophrenia. Schizophr Res 84(2–3):253–271
13. Hoeben A, Landuyt B, Highley MS, Wildiers H, Van Oosterom AT, De Bruijn EA (2004) Vascular endothelial growth factor and angiogenesis. Pharmacol Rev 56(4):549–580
14. Storkebaum E, Carmeliet P (2004) VEGF: a critical player in neurodegeneration. J Clin Invest 113(1):14–18
15. Forsythe JA, Jiang BH, Iyer NV, Agani F, Leung SW, Koos RD, Semenza GL (1996) Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 16(9):4604–4613
16. Hanson DR, Gottesman II (2005) Theories of schizophrenia: a genetic-inflammatory-vascular synthesis. BMC Med Genet 6:7
17. Fulzele S, Pillai A (2009) Decreased VEGF mRNA expression in the dorsolateral prefrontal cortex of schizophrenia subjects. Schizophr Res 115(2–3):372–373
18. Mayoral SR, Omar G, Penn AA (2009) Sex differences in a hypoxia model of preterm brain damage. Pediatr Res 66(3):248–253
19. Asami T, Bouix S, Whitford TJ, Shenton ME, Salisbury DF, McCarley RW (2012) Longitudinal loss of gray matter volume in patients with first-episode schizophrenia: DARTEL automated analysis and ROI validation. Neuroimage 59(2):986–996
20. Parlapani E, Schmitt A, Erdmann A, Bernstein HG, Breunig B, Gruber O, Petroianu G, von Wilmsdorff M et al (2009) Association between myelin basic protein expression and left entorhinal cortex pre-alpha cell layer disorganization in schizophrenia. Brain Res 1301:126–134
21. Flynn SW, Lang DJ, Mackay AL, Goghari V, Vavasour IM, Whittall KP, Smith GN, Arango V et al (2003) Abnormalities of myelination in schizophrenia detected in vivo with MRI, and post-mortem with analysis of oligodendrocyte proteins. Mol Psychiatry 8(9):811–820
22. Impagnatiello F, Guidotti AR, Pesold C, Dwivedi Y, Caruncho H, Pisu MG, Uzunov DP, Smalheiser NR et al (1998) A decrease of reelin expression as a putative vulnerability factor in schizophrenia. Proc Natl Acad Sci U S A 95(26):15718–15723
23. Fatemi SH, Earle JA, McMenomy T (2000) Reduction in Reelin immunoreactivity in hippocampus of subjects with schizophrenia, bipolar disorder and major depression. Mol Psychiatry 5(6):654–663, 571
24. Jossin Y (2004) Neuronal migration and the role of reelin during early development of the cerebral cortex. Mol Neurobiol 30(3):225–251
25. Laviola G, Ognibene E, Romano E, Adriani W, Keller F (2009) Gene-environment interaction during early development in the heterozygous reeler mouse: clues for modelling of major neurobehavioral syndromes. Neurosci Biobehav Rev 33(4):560–572
26. Nullmeier S, Panther P, Dobrowolny H, Frotscher M, Zhao S, Schwegler H, Wolf R (2011) Region-specific alteration of GABAergic markers in the brain of heterozygous reeler mice. Eur J Neurosci 33(4):689–698
27. Golan MH, Mane R, Molczadzki G, Zuckerman M, Kaplan-Louson V, Huleihel M, Perez-Polo JR (2009) Impaired migration signaling in the hippocampus following prenatal hypoxia. Neuropharmacology 57(5–6):511–522
28. Costa E, Davis J, Pesold C, Tueting P, Guidotti A (2002) The heterozygote reeler mouse as a model for the development of a new generation of antipsychotics. Curr Opin Pharmacol 2(1):56–62
29. Pillai A, Mahadik SP (2008) Increased truncated TrkB receptor expression and decreased BDNF/TrkB signaling in the frontal cortex of reeler mouse model of schizophrenia. Schizophr Res 100(1–3):325–333
30. Howell KR, Pillai A (2014) Effects of prenatal hypoxia on schizophrenia-related phenotypes in heterozygous reeler mice: a gene × environment interaction study. Eur Neuropsychopharmacol 24(8):1324–1336
31. Terry AV Jr, Parikh V, Gearhart DA, Pillai A, Hohnadel E, Warner S, Nasrallah HA, Mahadik SP (2006) Time-dependent effects of haloperidol and ziprasidone on nerve growth factor, cholinergic neurons, and spatial learning in rats. J Pharmacol Exp Ther 318:709–724
32. Callahan PM, Terry AV Jr, Tehim A (2014) Effects of the nicotinic α7 receptor partial agonist GTS-21 on NMDA-glutamatergic receptor related deficits in sensorimotor gating and recognition memory in rats. Psychopharmacology (Berlin) 231(18):3695–3706
33. Schulz KM, Pearson JN, Neeley EW, Berger R, Leonard S, Adams CE, Stevens KE (2011) Maternal stress during pregnancy causes sex-specific alterations in offspring memory performance, social interactions, indices of anxiety, and body mass. Physiol Behav 104(2):340–347
34. Chung S, Son GH, Park SH, Park E, Lee KH, Geum D, Kim K (2005) Differential adaptive responses to chronic stress of maternally stressed male mice offspring. Endocrinology 146(7):3202–3210
35. Tazumi T, Hori E, Uwano T, Umeno K, Tanebe K, Tabuchi E, Ono T, Nishijo H (2005) Effects of prenatal maternal stress by repeated cold environment on behavioral and emotional development in the rat offspring. Behav Brain Res 162(1):153–160
36. Liddle PF, Friston KJ, Frith CD, Hirsch SR, Jones T, Frackowiak RS (1992) Patterns of cerebral blood flow in schizophrenia. Br J Psychiatry 160:179–186
37. Sahin S, Yüksel C, Güler J, Karadayı G, Akturan E, Göde E, Ozhan AA, Uçok A (2013) The history of childhood trauma among individuals with ultra high risk for psychosis is as common as among patients with first-episode schizophrenia. Early Interv Psychiatry 7:414–420
38. Larsson S, Andreassen OA, Aas M, Røssberg JI, Mork E, Steen NE, Barrett EA, Lagerberg TV et al (2013) High prevalence of childhood trauma in patients with schizophrenia spectrum and affective disorder. Compr Psychiatry 54(2):123–127
39. Lysaker PH, Meyer PS, Evans JD, Clements CA, Marks KA (2001) Childhood sexual trauma and psychosocial functioning in adults with schizophrenia. Psychiatr Serv 52(11):1485–1488
40. Lima-Ojeda JM, Vogt MA, Richter SH, Dormann C, Schneider M, Gass P, Inta D (2014) Lack of protracted behavioral abnormalities following intermittent or continuous chronic mild hypoxia in perinatal C57BL/6 mice. Neurosci Lett 577:77–82
41. Levy AP, Levy NS, Wegner S, Goldberg MA (1995) Transcriptional regulation of the rat vascular endothelial growth factor gene by hypoxia. J Biol Chem 270(22):13333–13340
42. Arany Z, Foo SY, Ma Y, Ruas JL, Bommi-Reddy A, Girnun G, Cooper M, Laznik D et al (2008) HIF-independent regulation of VEGF and angiogenesis by the transcriptional coactivator PGC-1alpha. Nature 451(7181):1008–1012
43. Howell KR, Hoda MN, Pillai A (2013) VEGF activates NR2B phosphorylation through Dab1 pathway. Neurosci Lett 552:30–34
44. Pruessner M, Béchard-Evans L, Boekestyn L, Iyer SN, Pruessner JC, Malla AK (2013) Attenuated cortisol response to acute psychosocial stress in individuals at ultra-high risk for psychosis. Schizophr Res 146(1–3):79–86
45. David DJ, Samuels BA, Rainer Q, Wang JW, Marsteller D et al (2009) Neurogenesis-dependent and -independent effects of fluoxetine in an animal model of anxiety/depression. Neuron 62:479–493
46. Kutiyanawalla A, Promsote W, Terry A, Pillai A (2012) Cysteamine treatment ameliorates alterations in GAD67 expression and spatial memory in heterozygous reeler mice. Int J Neuropsychopharmacol 15(8):1073–1086