Association of serum VEGF levels with prefrontal cortex volume in schizophrenia

Molecular Psychiatry

Volumn 21, Issue 5, 2016, Pages 686-692

  Pillai, A ^a   Howell, K R ^a,h   Ahmed, A O ^b   Weinberg, D ^c   Allen, K M ^c,d,e   Bruggemann, J ^c,d,e   Lenroot, R ^c,d,e   Liu, D ^f,g   Galletly, C ^f,g   Weickert, C S ^c,d,e   Weickert, T W ^c,d,e  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c NEUROSCIENCE RESEARCH AUSTRALIA   (Australia)

^d UNIVERSITY OF NEW SOUTH WALES   (Australia)

^e SCHIZOPHRENIA RESEARCH INSTITUTE   (Australia)

^f UNIVERSITY OF ADELAIDE   (Australia)

^g Central Adelaide Local Health Network   (Australia)

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

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 6; MESSENGER RNA; VASCULOTROPIN; BIOLOGICAL MARKER; IL6 PROTEIN, HUMAN; VASCULOTROPIN A; VEGFA PROTEIN, HUMAN;

ADULT; ARTICLE; BLOOD SAMPLING; BRAIN SIZE; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FRONTAL CORTEX; HUMAN; INFLAMMATION; MAJOR CLINICAL STUDY; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; POLYMERASE CHAIN REACTION; PREFRONTAL CORTEX; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SCHIZOAFFECTIVE PSYCHOSIS; SCHIZOPHRENIA; BLOOD; DIAGNOSTIC IMAGING; IMAGE PROCESSING; ORGAN SIZE; PATHOLOGY; PSYCHOLOGICAL RATING SCALE; PSYCHOSIS;

ADULT; BIOMARKERS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; INTERLEUKIN-6; MAGNETIC RESONANCE IMAGING; MALE; ORGAN SIZE; PREFRONTAL CORTEX; PSYCHIATRIC STATUS RATING SCALES; PSYCHOTIC DISORDERS; RNA, MESSENGER; SCHIZOPHRENIA; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84942673336     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/mp.2015.96     Document Type: Article

References (78)

1. Wheeler AL, Voineskos AN. A review of structural neuroimaging in schizophrenia: from connectivity to connectomics. Front Hum Neurosci 2014; 8: 653
2. Honea R, Crow TJ, Passingham D, Mackay CE. Regional deficits in brain volume in schizophrenia: a meta-Analysis of voxel-based morphometry studies. Am J Psychiatry 2005; 162: 2233-2245
3. Shenton ME, Dickey CC, Frumin M, McCarley RW. A review of MRI findings in schizophrenia. Schizophr Res 2001; 49: 1-52
4. Ho BC, Andreasen NC, Ziebell S, Pierson R, Magnotta V. Long-Term antipsychotic treatment and brain volumes: a longitudinal study of first-episode schizophrenia. Arch Gen Psychiatry 2011; 68: 128-137
5. Miller D, Andreasen N, O'Leary D, Watkins G, Boles Ponto L, Hichwa R. Comparison of the effects of risperidone and haloperidol on regional cerebral blood flow in schizophrenia. Biol Psychiatry 2001; 49: 704-715
6. Bartlett EJ, Brodie JD, Simkowitz P, Schlösser R, Dewey SL, Lindenmayer JP et al. Effect of a haloperidol challenge on regional brain metabolism in neurolepticresponsive and nonresponsive schizophrenic patients. Am J Psychiatry 1998; 155: 337-343
7. Andreasen N, O'Leary D, Flaum M, Nopoulos P, Watkins G, Ponto L et al. Hypofrontality in schizophrenia: distributed dysfunctional circuits in neuroleptic-naive patients. Lancet 1997; 349: 1730-1734
8. Wiser AK, Andreasen NC, O'Leary DS, Watkins GL, Boles Ponto LL, Hichwa RD. Dysfunctional cortico-cerebellar circuits cause cognitive dysmetriain schizophrenia. Neuroreport 1998; 9: 1895-1899
9. Dirnberger G, Fuller R, Frith C, Jahanshahi M. Neural correlates of executive dysfunction in schizophrenia: failure to modulate brain activity with task demands. Neuroreport 2014; 25: 1308-1315
10. Hoeben A, Landuyt B, Highley MS, Wildiers H, Van Oosterom AT, De Bruijn EA. Vascular endothelial growth factor and angiogenesis. Pharmacol Rev 2004; 56: 549-580
11. Lacoste B, Comin CH, Ben-Zvi A, Kaeser PS, Xu X, Costa Lda F et al. Sensory-related neural activity regulates the structure of vascular networks in the cerebral cortex. Neuron 2014; 83: 1117-1130
12. Harder D, Zhang C, Gebremedhin D. Astrocytes function in matching blood flow to metabolic activity. News Physiol Sci 2002; 17: 27-31
13. Williamson P. Hypofrontality in schizophrenia: a review of the evidence. Can J Psychiatry 1987; 32: 399-404
14. Marti HM, Risau W. Systemic hypoxia changes the organ-specific distribution of vascular endothelial growth factor and its receptors. Proc Natl Acad Sci USA 1998; 95: 15809-15814
15. Ruiz de Almodovar C, Lambrechts D, Mazzone M, Carmeliet P. Role and therapeutic potential of VEGF in the nervous system. Physiol Rev 2009; 89: 607-648
16. Bengoetxea H, Argandoña EG, Lafuente JV. Effects of visual experience on vascular endothelial growth factor expression during the postnatal development of the rat visual cortex. Cereb Cortex 2008; 18: 1630-1639
17. Pillai A, Mahadik SP. Differential effects of haloperidol and olanzapine on levels of vascular endothelial growth factor and angiogenesis in rat hippocampus. Schizophr Res 2006; 87: 48-59
18. Olsson AK, Dimberg A, Kreuger J, Claesson-Welsh L. VEGF receptor signalling - in control of vascular function. Nat Rev Mol Cell Biol 2006; 7: 359-371
19. Shalaby F, Rossant J, Yamaguchi TP, Gertsenstein M, Wu XF, Breitman ML et al. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 1995; 376: 62-66
20. Storkebaum E, Carmeliet P. VEGF: a critical player in neurodegeneration. J Clin Invest 2004; 113: 14-18
21. Jin K, Zhu Y, Sun Y, Mao XO, Xie L, Greenberg DA. Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc Natl Acad Sci USA 2002; 99: 11946-11950
22. Khaibullina AA, Rosenstein JM, Krum JM. Vascular endothelial growth factor promotes neurite maturation in primary CNS neuronal cultures. Brain Res 2004; 148: 59-68
23. Rosenstein JM, Mani N, Khaibullina A, Krum JM. Neurotrophic effects of vascular endothelial growth factor on organotypic cortical explants and primary cortical neurons. J Neurosci 2003; 23: 11036-11044
24. Fulzele S, Pillai A. Decreased VEGF mRNA expression in the dorsolateral prefrontal cortex of schizophrenia subjects. Schizophr Res 2009; 115: 372-373
25. Blumberg HP, Wang F, Chepenik LG, Kalmar JH, Edmiston E, Duman RS et al. Influence of vascular endothelial growth factor variation on human hippocampus morphology. Biol Psychiatry 2008; 64: 901-903
26. Flynn SW, Lang DJ, Mackay AL, Goghari V, Vavasour IM, Whittall KP et al. Abnormalities of myelination in schizophrenia detected in vivo with MRI, and post-mortem with analysis of oligodendrocyte proteins. Mol Psychiatry 2003; 8: 811-820
27. Asami T, Bouix S, Whitford TJ, Shenton ME, Salisbury DF, McCarley RW. Longitudinal loss of gray matter volume in patients with first-episode schizophrenia: DARTEL automated analysis and ROI validation. Neuroimage 2012; 59: 986-996
28. Yang Y, Fung SJ, Rothwell A, Tianmei S, Weickert CS. Increased interstitial white matter neuron density in the dorsolateral prefrontal cortex of people with schizophrenia. Biol Psychiatry 2011; 69: 63-70
29. Joshi D, Fung SJ, Rothwell A, Weickert CS. Higher gamma-Aminobutyric acid neuron density in the white matter of orbital frontal cortex in schizophrenia. Biol Psychiatry 2012; 72: 725-733
30. Volk DW, Lewis DA. Early developmental disturbances of cortical inhibitory neurons: contribution to cognitive deficits in schizophrenia. Schizophr Bull 2014; 40: 952-957
31. Fillman SG, Cloonan N, Catts VS, Miller LC, Wong J, McCrossin T et al. Increased inflammatory markers identified in the dorsolateral prefrontal cortex of individuals with schizophrenia. Mol Psychiatry 2013; 18: 206-214
32. Catts VS, Wong J, Fillman SG, Fung SJ, Weickert CS. Increased expression of astrocyte markers in schizophrenia: association with neuroinflammation. Aust N Z J Psychiatry 2014; 48: 722-734
33. Bellon A, Krebs MO, Jay TM. Factoring neurotrophins into a neurite-based pathophysiological model of Schizophrenia. Prog Neurobiol 2011; 94: 77-90
34. Argaw AT, Zhang Y, Snyder BJ, Zhao ML, Kopp N, Lee SC et al. IL-1beta regulates blood-brain barrier permeability via reactivation of the hypoxia-Angiogenesis program. J Immunol 2006; 177: 5574-5584
35. Miller BJ, Buckley P, Seabolt W, Mellor A, Kirkpatrick B. Meta-Analysis of cytokine alterations in schizophrenia: clinical status and antipsychotic effects. Biol Psychiatry 2011; 70: 663-671
36. First MB, Williams JBW, Spitzer RL, Gibbon M. Structured Clinical Interview for DSMIV-TR Axis I Disorders, Clinical Trials Version (SCID-CT). Biometrics Research, New York State Psychiatric Institute: New York, 2007
37. Kay SR, Fiszbein A, Opler LA. The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr Bull 1987; 13: 261-276
38. Wechsler D. Wechsler Adult Intelligence Scale-Third Edition. Psychological Corporation: San Antonio, 1997
39. Wechsler D. Wechsler Test of Adult Reading. The Psychological Corporation: San Antonio, 2001
40. Wechsler D. Wechsler Memory Scale-Revised. The Psychological Corporation: San Antonio, 1987
41. Lezak M. Neuropsychological Assessment 4th (ed). Oxford University Press: New York, 2004
42. Moore L, Kyaw M, Vercammen A, Lenroot R, Kulkarni J, Curtis J et al. Serum testosterone levels are related to cognitive function in men with schizophrenia. Psychoneuroendocrinology 2013; 38: 1717-1728
43. Weickert CS, Sheedy D, Rothmond DA, Dedova I, Fung S, Garrick T et al. Selection of reference gene expression in a schizophrenia brain cohort. Aust N Z J Psychiatry 2010; 44: 59-70
44. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-Time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25: 402-408
45. Leucht S, Wahlbeck K, Hamann J, Kissling W. New generation antipsychotics versus low-potency conventional antipsychotics: a systematic review and meta-Analysis. Lancet 2003; 361: 1581-1589
46. Woods SW. Chlorpromazine equivalent doses for the newer atypical antipsychotics. J Clin Psychiatry 2003; 64: 663-667
47. Goldstein JM, Goodman JM, Seidman LJ, Kennedy DN, Makris N, Lee H et al. Cortical abnormalities in schizophrenia identified by structural magnetic resonance imaging. Arch Gen Psychiatry 1999; 56: 537-547
48. Buchanan RW, Vladar K, Barta PE, Pearlson GD. Structural evaluation of the prefrontal cortex in schizophrenia. Am J Psychiatry 1998; 155: 1049-1055
49. Vita A, De Peri L, Deste G, Sacchetti E. Progressive loss of cortical gray matter in schizophrenia: a meta-Analysis and meta-regression of longitudinal MRI studies. Transl Psychiatry 2012; 2: e190
50. Squarcina L, Perlini C, Peruzzo D, Castellani U, Marinelli V, Bellani M et al. The use of dynamic susceptibility contrast (DSC) MRI to automatically classify patients with first episode psychosis. Schizophr Res 2015; 165: 38-44
51. Shifren JL, Doldi N, Ferrara N, Mesiano S, Jaffe RB. In the human fetus, vascular endothelial growth factor is expressed in epithelial cells and myocytes, but not vascular endothelium: implications for mode of action. J Clin Endocrinol Metab 1994; 79: 316-322
52. Peters KG, De Vries C, Williams LT. Vascular endothelial growth factor receptor expression during embryogenesis and tissue repair suggests a role in endothelial differentiation and blood vessel growth. Proc Natl Acad Sci USA 1993; 90: 8915-8919
53. He H, Venema VJ, Gu X, Venema RC, Marrero MB, Caldwell RB. Vascular endothelial growth factor signals endothelial cell production of nitric oxide and prostacyclin through flk-1/KDR activation of c-Src. J Biol Chem 1999; 274: 25130-25135
54. Howell KR, Kutiyanawalla A, Pillai A. Long-Term continuous corticosterone treatment decreases VEGF receptor-2 expression in frontal cortex. PLoS One 2011; 6: e20198
55. Pasternak O, Westin CF, Bouix S, Seidman LJ, Goldstein JM, Woo TU et al. Excessive extracellular volume reveals a neurodegenerative pattern in schizophrenia onset. J Neurosci 2012; 32: 17365-17372
56. Pasternak O, Westin CF, Dahlben B, Bouix S, Kubicki M. The extent of diffusion MRI markers of neuroinflammation and white matter deterioration in chronic schizophrenia. Schizophr Res 2015; 161: 113-118
57. Xiu MH, Yang GG, Tan YL, Chen da C, Tan SP, Wang ZR et al. Decreased interleukin-10 serum levels in first-episode drug-naïve schizophrenia: Relationship to psychopathology. Schizophr Res 2014; 156: 9-14
58. Cohen T, Nahari D, Cerem LW, Neufeld G, Levi BZ. Interleukin 6 induces the expression of vascular endothelial growth factor. J Biol Chem 1996; 271: 736-741
59. Meyer U. Prenatal poly(i: C) exposure and other developmental immune activation models in rodent systems. Biol Psychiatry 2014; 75: 307-315
60. Horváth S, Mirnics K. Immune system disturbances in schizophrenia. Biol Psychiatry 2014; 75: 316-323
61. Arrode-Brusés G, Brusés JL. Maternal immune activation by poly I: C induces expression of cytokines IL-1β and IL-13, chemokine MCP-1 and colony stimulating factor VEGF in fetal mouse brain. J Neuroinflammation 2012; 9: 83
62. Khan D, Fernando P, Cicvaric A, Berger A, Pollak A, Monje FJ et al. Long-Term effects of maternal immune activation on depression-like behavior in the mouse. Transl Psychiatry 2014; 4: e363
63. van Haren NE, Hulshoff Pol HE, Schnack HG, Cahn W, Mandl RC, Collins DL et al. Focal gray matter changes in schizophrenia across the course of the illness: a 5-year follow-up study. Neuropsychopharmacology 2007; 32: 2057-2066
64. Keilhoff G, Grecksch G, Bernstein HG, Roskoden T, Becker A. Risperidone and haloperidol promote survival of stem cells in the rat hippocampus. Eur Arch Psychiatry Clin Neurosci 2010; 260: 151-162
65. Misztal-Dethloff B, Stepien H, Komorowski J. Effect of diazepam and chlorpromazine on proliferative activity and vascular endothelial growth factor (VEGF) secretion from cultured endothelial HECa10 cells in vitro. Pharmacol Rep 2005; 57: 670-674
66. Di Nicola M, Cattaneo A, Hepgul N, Di Forti M, Aitchison KJ, Janiri L et al. Serum and gene expression profile of cytokines in first-episode psychosis. Brain Behav Immun 2013; 31: 90-95
67. Murphy BP, Pang TY, Hannan AJ, Proffitt TM, McConchie M, Kerr M et al. Vascular endothelial growth factor and brain-derived neurotrophic factor in quetiapine treated first-episode psychosis. Schizophr Res Treatment 2014; 2014: 719395
68. Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med 2003; 9: 669-676
69. Morita S, Ukai S, Miyata S. VEGF-dependent continuous angiogenesis in the median eminence of adult mice. Eur J Neurosci 2013; 37: 508-518
70. Ozawa K, Kondo T, Hori O, Kitao Y, Stern DM, Eisenmenger W et al. Expression of the oxygen-regulated protein ORP150 accelerates wound healing by modulating intracellular VEGF transport. J Clin Invest 2001; 108: 41-50
71. Kerr BA, Byzova TV. alphaB-crystallin: a novel VEGF chaperone. Blood 2010; 115: 3181-3183
72. Yeo TK, Senger DR, Dvorak HF, Freter L, Yeo KT. Glycosylation is essential for efficient secretion but not for permeability-enhancing activity of vascularpermeability factor (vascular endothelial growth-factor). Biochem Biophys Res Commun 1991; 179: 1568-1575
73. Perlstein WM, Carter CS, Noll DC, Cohen JD. Relation of prefrontal cortex dysfunction to working memory and symptoms in schizophrenia. Am J Psychiatry 2001; 158: 1105-1113
74. Kikinis Z, Fallon JH, Niznikiewicz M, Nestor P, Davidson C, Bobrow L et al. Gray matter volume reduction in rostral middle frontal gyrus in patients with chronic schizophrenia. Schizophr Res 2010; 123: 153-159
75. Weickert TW, Goldberg TE, Gold JM, Bigelow LB, Egan MF, Weinberger DR. Cognitive impairments in patients with schizophrenia displaying preserved and compromised intellect. Arch Gen Psychiatry 2000; 57: 907-913
76. Wongupparaj P, Kumari V, Morris RG. Executive function processes mediate the impact of working memory impairment on intelligence in schizophrenia. Eur Psychiatry 2015; 30: 1-7
77. Halmai Z, Dome P, Dobos J, Gonda X, Szekely A, Sasvari-Szekely M et al. Peripheral vascular endothelial growth factor level is associated with antidepressant treatment response: results of a preliminary study. J Affect Disord 2013; 144: 269-273
78. Ahmed AO, Bhat IA. Psychopharmacological treatment of neurocognitive deficits in people with schizophrenia: a review of old and new targets. CNS Drugs 2014; 28: 301-318