Effect of intracortical vascular endothelial growth factor infusion and blockade during the critical period in the rat visual cortex

Brain Research

Volumn 1473, Issue , 2012, Pages 141-154

  Argandoña, Enrike G ^a   Bengoetxea, Harkaitz ^b   Bulnes, Susana ^b   Rico Barrio, Irantzu ^b   Ortuzar, Naiara ^b   Lafuente, Jose V ^b  

^a UNIVERSITY OF FRIBOURG   (Switzerland)

^b UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

Author keywords

Diaschisis; Neuroprotection; Neurorestoration; Neurovascular unit; VEGF

Indexed keywords

ANTIGEN; CHOLINESTERASE; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; BLOOD VESSEL PERMEABILITY; BRAIN INJURY; CELL DEATH; CELL DENSITY; CONTROLLED STUDY; ENDOTHELIAL BARRIER ANTIGEN; HISTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IMMUNOPATHOLOGY; MACROGLIA; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; RAT; VASCULARIZATION; VISUAL CORTEX; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CRITICAL PERIOD (PSYCHOLOGY); IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; INJECTIONS, INTRAVENTRICULAR; MICROSCOPY, CONFOCAL; NEOVASCULARIZATION, PHYSIOLOGIC; RATS; RATS, LONG-EVANS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VISUAL CORTEX;

ANIMALIA; RATTUS;

EID: 84865502441     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2012.07.008     Document Type: Article

References (93)

1. P.D. Adelson, L.W. Jenkins, R.L. Hamilton, P. Robichaud, M.P. Tran, and P.M. Kochanek Histopathologic response of the immature rat to diffuse traumatic brain injury J. Neurotrauma 18 2001 967 976
2. S. Albayrak, Q. Zhao, B.K. Siesj, and M.L. Smith Effect of transient focal ischemia on bloodbrain barrier permeability in the rat: correlation to cell injury Acta Neuropathol. 94 1997 158 163
3. V. Anderson, M. Spencer-Smith, and A. Wood Do children really recover better? Neurobehavioural plasticity after early brain insult Brain 134 2011 2197 2221
4. R.J. Andrews Transhemispheric diaschisis. A review and comment Stroke 22 1997 943 949
5. E.G. Argandoa, H. Bengoetxea, and J.V. Lafuente Lack of experience-mediated differences in the immunohistochemical expression of bloodbrain barrier markers (EBA and GluT-1) during the postnatal development of the rat visual cortex Dev. Brain Res. 156 2005 158 166
6. E.G. Argandoa, H. Bengoetxea, and J.V. Lafuente Physical exercise is required for environmental enrichment to offset the quantitative effects of dark-rearing on the S-100beta astrocytic density in the rat visual cortex J. Anat. 215 2009 132 140
7. E.G. Argandoa, and J.V. Lafuente Effects of dark-rearing on the vascularization of the developmental rat visual cortex Brain Res. 732 1996 43 51
8. E.G. Argandoa, H. Bengoetxea, and J.V. Lafuente Effects of intracortical administration and neutralisation of vascular endothelial growth factor in the developing rat brain Int. J. Neuroprot. Neuroregen. 3 2006 45 52
9. E.G. Argandoa, and J.V. Lafuente Influence of visual experience deprivation on the postnatal development of the microvascular bed in layer IV of the rat visual cortex Brain Res. 855 2000 137 142
10. E.G. Argandoa, and J.V. Lafuente The effect of experience on postnatal development of the vascularization of the visual cortex Rev. Neurol. 340 2002 983 988
11. E.G. Argandoa, H. Bengoetxea, N. Ortuzar, S. Bulnes, I. Rico-Barrio, and J.V. Lafuente Vascular endothelial growth factor: adaptive changes in the neuroglialvascular unit Curr. Neurovasc. Res. 9 2012 72 81
12. M. Bastide, T. Ouk, F. Plaisier, O. Ptrault, S. Stolc, and R. Bordet Neurogliovascular unit after cerebral ischemia: is the vascular wall a pharmacological target Psychoneuroendocrinology 32 Suppl. 1 2007 S36 S39
13. H. Bengoetxea, E.G. Argandoa, and J.V. Lafuente Effects of visual experience on vascular endothelial growth factor expression during the postnatal development of the rat visual cortex Cereb. Cortex 18 2008 1630 1639
14. N. Berardi, T. Pizzorusso, and L. Maffei Critical periods during sensory development Curr. Opin. Neurobiol. 10 2000 138 145
15. J.E. Black, K.R. Isaacs, B.J. Anderson, A.A. Alcantara, and W.T. Greenough Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats PNAS 87 1990 5568 5572
16. T. Chu, Y. Liu, Z. Wang, P. Zhu, W. Jiao, J. Wen, and S. Gong Sustained vascular endothelial growth factor blockade by antivascular endothelial growth factor antibodies results in nonunion in the process of fracture healing in rabbits J. Trauma 66 2009 1180 1183
17. S.D. Croll, R.M. Ransohoff, N. Cai, Q. Zhang, F.J. Martin, T. Wei, L.J. Kasselman, J. Kintner, A.J. Murphy, G.D. Yancopoulos, and S.J. Wiegand VEGF-mediated inflammation precedes angiogenesis in adult brain Exp. Neurol. 187 2004 388 402
18. A.S. Cunningham, R. Salvador, J.P. Coles, D.A. Chatfield, P.G. Bradley, A.J. Johnston, L.A. Steiner, T.D. Fryer, F.I. Aigbirhio, P. Smielewski, G.B. Williams, T.A. Carpenter, J.H. Gillard, J.D. Pickard, and D.K. Menon Physiological thresholds for irreversible tissue damage in contusional regions following traumatic brain injury Brain 128 2005 1931 1942
19. G.J. del Zoppo The neurovascular unit, matrix proteases, and innate inflammation Ann. N.Y. Acad. Sci. 1207 2010 46 49
20. D.H. Dobrogowska, A.S. Lossinsky, M. Tarnawski, and A.W. Vorbrodt Increased bloodbrain barrier permeability and endothelial abnormalities induced by vascular endothelial growth factor J. Neurocytol. 27 1998 163 173
21. L.W. Duchen General pathology of neurons and neuroglia J.H. Adams, L.W. Duchen, Greenfield's Neuropathology 1992 Oxford University Press New York 1 68
22. H.F. Dvorak VPF/VEGF and the angiogenic response Semin. Perinatol. 24 2000 75 78
23. M. Fagiolini, T. Pizzorusso, N. Berardi, L. Domenici, and L. Maffei Functional postnatal development of the rat primary visual cortex and the role of visual experience: dark rearing and monocular deprivation Vision Res. 34 1994 709 720
24. N. Ferrara, and S. Bunting Vascular endothelial growth factor, a specific regulator of angiogenesis Curr. Opin. Nephrol. Hypertens. 5 1996 35 44
25. N. Ferrara, and T. Davis-Smyth The biology of vascular endothelial growth factor Endocr. Rev. 18 1997 4 25
26. N. Ferrara, and H.P. Gerber The role of vascular endothelial growth factor in angiogenesis Acta Haematol. 106 2001 148 156
27. N. Ferrara, H.P. Gerber, and J. LeCouter The biology of VEGF and its receptors Nat. Med. 9 2003 669 676
28. I. Fineman, C.C. Giza, B.V. Nahed, S.M. Lee, and D.A. Hovda Inhibition of neocortical plasticity during development by a moderate concussive brain injury J. Neurotrauma 17 2000 739 749
29. S. Fischer, M. Clauss, M. Wiesnet, D. Renz, W. Schaper, and G.F. Karliczek Hypoxia induces permeability in brain microvessel endothelial cells via VEGF and NO Am. J. Physiol. 276 1999 812 820
30. S. Fischer, M. Wobben, H.H. Marti, D. Renz, and W. Schaper Hypoxia-induced hyperpermeability in brain microvessel endothelial cells involves VEGF-mediated changes in the expression of zonula occludens-1 Microvasc. Res. 63 2002 70 80
31. E. Geretti, A. Shimizu, and M. Klagsbrun Neuropilin structure governs VEGF and semaphorin binding and regulates angiogenesis Angiogenesis 11 2008 31 39
32. M.N. Ghabriel, C. Zhu, G. Hermanis, and G. Allt Immunological targeting of the endothelial barrier antigen (EBA) in vivo leads to opening of the bloodbrain barrier Brain Res. 878 2000 127 135
33. M.N. Ghabriel, C. Zhu, and C. Leigh Electron microscope study of bloodbrain barrier opening induced by immunological targeting of the endothelial barrier antigen Brain Res. 934 2002 140 151
34. C.D. Gilbert Adult cortical dynamics Physiol. Rev. 78 1998 467 485
35. C.C. Giza, G.S. Griesbach, and D.A. Hovda Experience-dependent behavioral plasticity is disturbed following traumatic injury to the immature brain Behav. Brain Res. 157 2005 11 22
36. D.A. Greenberg, and K. Jin From angiogenesis to neuropathology Nature 438 2005 954 959
37. F. Greifzu, S. Schmidt, K.F. Schmidt, K. Kreikemeier, O.W. Witte, and S. Lwel Global impairment and therapeutic restoration of visual plasticity mechanisms after a localized cortical stroke PNAS 108 2011 15450 15455
38. G.G. Gurkoff, C.C. Giza, and D.A. Hovda Lateral fluid percussion injury in the developing rat causes an acute, mild behavioral dysfunction in the absence of significant cell death Brain Res. 1077 2006 24 36
39. R.V. Harrison, N. Harel, J. Panesar, and R.J. Mount Blood capillary distribution correlates with hemodynamic-based functional imaging in cerebral cortex Cereb. Cortex 12 2002 225 233
40. B.T. Hawkins, and T.P. Davis The bloodbrain barrier/neurovascular unit in health and disease Pharmacol. Rev. 57 2005 173 185
41. T.K. Hensch Critical period mechanisms in developing visual cortex Curr. Top. Dev. Biol. 69 2005 215 237
42. D.M. Hermann, and A. Zechariah Implications of vascular endothelial growth factor for postischemic neurovascular remodeling J. Cereb. Blood Flow Metab. 29 2009 1620 1643
43. J. Herz, R. Reitmeir, S.I. Hagen, B.S. Reinboth, Z. Guo, A. Zechariah, A. ElAli, T.R. Doeppner, M. Bacigaluppi, S. Pluchino, U. Kilic, E. Kilic, and D.M. Hermann Intracerebroventricularly delivered VEGF promotes contralesional corticorubral plasticity after focal cerebral ischemia via mechanisms involving anti-inflammatory actions Neurobiol. Dis. 45 2012 1077 1085
44. H.W. Hoffmeyer, P. Enager, K.J. Thomsen, and M.J. Lauritzen Nonlinear neurovascular coupling in rat sensory cortex by activation of transcallosal fibers J. Cereb. Blood Flow Metab. 27 2007 575 587
45. T.T. Hu, G. Van den Bergh, L. Thorrez, K. Heylen, U.T. Eysel, and L. Arckens Recovery from retinal lesions: molecular plasticity mechanisms in visual cortex far beyond the deprived zone Cereb. Cortex 21 2011 2883 2892
46. K. Jin, X.O. Mao, S.P. Batteur, E. McEachron, A. Leahy, and D.A. Greenberg Caspase3 and the regulation of hypoxic neuronal death by vascular endothelial growth factor Neuroscience 108 2001 351 358
47. K.L. Jin, X.O. Mao, and D.A. Greenberg Vascular endothelial growth factor: direct neuroprotective effect in in vitro ischemia PNAS 97 2000 10242 10247
48. D. Kaya, Y. Gursoy-Ozdemir, M. Yemisci, N. Tuncer, S. Aktan, and T. Dalkara VEGF protects brain against focal ischemia without increasing bloodbrain permeability when administered intracerebroventricularly J. Cereb. Blood Flow Metab. 25 2005 1111 1118
49. M. Khan, Y.B. Im, A. Shunmugavel, A.G. Gilg, R.K. Dhindsa, A.K. Singh, and I. Singh Administration of S-nitrosoglutathione after traumatic brain injury protects the neurovascular unit and reduces secondary injury in a rat model of controlled cortical impact J. Neuroinflammation 6 2009 32
50. B. Kolb, and J. Cioe Recovery from early cortical damage in rats. IX. Differential behavioral and anatomical effects of temporal cortex lesions at different ages of neural maturation Behav. Brain Res. 144 2003 67 76
51. J.M. Krum, and A. Khaibullina Inhibition of endogenous VEGF impedes revascularization and astroglial proliferation: roles for VEGF in brain repair Exp. Neurol. 181 2003 241 257
52. J.M. Krum, N. Mani, and J.M. Rosenstein Angiogenic and astroglial responses to vascular endothelial growth factor administration in adult rat brain Neuroscience 110 2002 589 604
53. J.V. Lafuente, E.G. Argandoa, and B. Mitre VEGFR-2 expression in brain injury: its distribution related to brainblood barrier markers J. Neural Transm. 113 2006 487 496
54. J.V. Lafuente, N. Ortuzar, H. Bengoetxea, S. Bulnes, and E.G. Argandoa Vascular endothelial growth factor and other angioglioneurins: key molecules in brain development and restoration Int. Rev. Neurobiol. 102 2012 317 346
55. C. Lecrux, and E. Hamel The neurovascular unit in brain function and disease Acta Physiol. 203 2011 47 59 (Oxf)
56. B. Lin, M.D. Ginsberg, W. Zhao, O.F. Alonso, L. Belayev, and R. Busto Quantitative analysis of microvascular alterations in traumatic brain injury by endothelial barrier antigen immunohistochemistry J. Neurotrauma 18 2001 389 397
57. C. Lodovichi, N. Berardi, T. Pizzorusso, and L. Maffei Effects of neurotrophins on cortical plasticity: same or different? J. Neurosci. 20 2000 2155 2165
58. J. Lok, P. Gupta, S. Guo, W.J. Kim, M.J. Whalen, K. van Leyen, and E.H. Lo Cellcell signaling in the neurovascular unit Neurochem. Res. 32 2007 2032 2045
59. A. Louissaint, S. Rao, C. Leventhal, and S.A. Goldman Coordinated interaction of neurogenesis and angiogenesis in the adult songbird brain Neuron 34 2002 945 960
60. N. Mani, A. Khaibullina, J.M. Krum, and J.M. Rosenstein Astrocyte growth effects of vascular endothelial growth factor (VEGF) application to perinatal neocortical explants: receptor mediation and signal transduction pathways Exp. Neurol. 192 2005 394 406
61. H.J. Marti, M. Bernaudin, A. Bellail, H. Schoch, M. Euler, E. Petit, and W. Risau Hypoxia-induced vascular endothelial growth factor expression precedes neovascularization after cerebral ischemia Am. J. Pathol. 156 2000 965 976
62. M.H. Maurer, W.K. Tripps, R.E. Feldmann, and W. Kuschinsky Expression of vascular endothelial growth factor and its receptors in rat neural stem cells Neurosci. Lett. 344 2003 165 168
63. K.V. Moser, and C. Humpel Vascular endothelial growth factor counteracts NMDAinduced cell death of adult cholinergic neurons in rat basal nucleus of Meynert Brain Res. Bull. 65 2005 125 131
64. N. Murase, J. Duque, R. Mazzocchio, and L.G. Cohen Influence of interhemispheric interactions on motor function in chronic stroke Ann. Neurol. 55 2004 400 409
65. R.A. Nordal, and C.S. Wong Molecular targets in radiation-induced bloodbrain barrier disruption Int. J. Radiat. Oncol. Biol. Phys. 62 2005 279 287
66. E. Norsted, B. Gomuc, and B. Meister Protein components of the bloodbrain barrier (BBB) in the mediobasal hypothalamus J. Chem. Neuroanat. 36 2008 107 121
67. B. Oosthuyse, L. Moons, E. Storkebaum, H. Beck, D. Nuyens, K. Brusselmans, J. Van Dorpe, P. Hellings, M. Gorselink, S. Heymans, G. Theilmeier, M. Dewerchin, V. Laudenbach, P. Vermylen, H. Raat, T. Acker, V. Vleminckx, L. Van Den Bosch, N. Cashman, H. Fujisawa, M.R. Drost, R. Sciot, F. Bruyninckx, D.J. Hicklin, C. Ince, P. Gressens, F. Lupu, K.H. Plate, W. Robberecht, J.M. Herbert, D. Collen, and P. Carmeliet Deletion of the hypoxia-response element in the vascular endothelial growth factor promoter causes motor neuron degeneration Nat. Genet. 28 2001 131 138
68. N. Ortuzar, E.G. Argandoa, H. Bengoetxea, and J.V. Lafuente Combination of intracortically administered VEGF and environmental enrichment enhances brain protection in developing rats J. Neural Transm. 118 2011 135 144
69. N. Ortuzar, E.G. Argandoa, H. Bengoetxea, O. Leis, S. Bulnes, and J.V. Lafuente Effects of VEGF administration or neutralization on the BBB of developing rat brain Acta Neurochir. Suppl. 106 2010 55 59
70. T.D. Palmer, A.R. Willhoite, and F.H. Gage Vascular niche for adult hippocampal neurogenesis J. Comp. Neurol. 425 2000 479 494
71. B.R. Payne, and S.G. Lomber Plasticity of the visual cortex after injury: what's different about the young brain? Neuroscientist 8 2002 174 185
72. M. Pekny, and M. Nilsson Astrocyte activation and reactive gliosis Glia 50 2005 427 434
73. K.H. Plate, G. Breier, H.A. Weich, and W. Risau Vascular endothelial growth factor is a potential tumour angiogenesis factor in human gliomas in vivo Nature 359 1992 845 848
74. M.L. Prins, S.M. Lee, C.L. Cheng, D.P. Becker, and D.A. Hovda Fluid percussion brain injury in the developing and adult rat: a comparative study of mortality, morphology, intracranial pressure and mean arterial blood pressure Dev. Brain Res. 95 1996 272 282
75. R. Reitmeir, E. Kilic, B.S. Reinboth, Z. Guo, A. ElAli, A. Zechariah, U. Kilic, and D.M. Hermann Vascular endothelial growth factor induces contralesional corticobulbar plasticity and functional neurological recovery in the ischemic brain Acta Neuropathol. 123 2012 273 284
76. J.M. Rosenstein, N. Mani, A. Khaibullina, and J.M. Krum Neurotrophic effects of vascular endothelial growth factor on organotypic cortical explants and primary cortical neurons J. Neurosci. 23 2003 11036 11044
77. C. Ruiz de Almodovar, D. Lambrechts, M. Mazzone, and P. Carmeliet Role and therapeutic potential of VEGF in the nervous system Physiol. Rev. 89 2009 607 648
78. H.J. Schoch, S. Fischer, and H.H. Marti Hypoxia-induced vascular endothelial growth factor expression causes vascular leakage in the brain Brain 125 2002 2549 2557
79. A.M. Sirevaag, J.E. Black, D. Shafron, and W.T. Greenough Direct evidence that complex experience increases capillary branching and surface area in visual cortex of young rats Brain Res. 471 1988 299 304
80. M.K. Skold, M. Risling, and S. Holmin Inhibition of vascular endothelial growth factor receptor 2 activity in experimental brain contusions aggravates injury outcome and leads to early increased neuronal and glial degeneration Eur. J. Neurosci. 23 2006 21 34
81. M.V. Sofroniew Molecular dissection of reactive astrogliosis and glial scar formation Trends Neurosci. 32 2009 638 647
82. E. Storkebaum, D. Lambrechts, and P. Carmeliet VEGF: once regarded as a specific angiogenic factor, now implicated in neuroprotection Bioessays 26 2004 943 954
83. Y. Sun, K. Jin, L. Xie, J. Childs, X.O. Mao, A. Logvinova, and D.A. Greenberg VEGF-induced neuroprotection, neurogenesis, and angiogenesis after focal cerebral ischemia J. Clin. Invest. 111 2003 1843 1851
84. S.B. Tieman, S. Mollers, D.G. Tieman, and J. White The blood supply of the cat's visual cortex and its postnatal development Brain Res. 998 2004 100 112
85. W. Tong, T. Igarashi, D.M. Ferriero, and L.J. Noble Traumatic brain injury in the immature mouse brain: characterization of regional vulnerability Exp. Neurol. 176 2002 105 116
86. I. Unal-Cevik, M. Kilinc, Y. Gursoy-Ozdemir, G. Gurer, and T. Dalkara Loss of NeuN immunoreactivity after cerebral ischemia does not indicate neuronal cell loss: a cautionary note Brain Res. 1015 2004 169 174
87. N. van Bruggen, H. Thibodeaux, J.T. Palmer, W.P. Lee, L. Fu, B. Cairns, D. Tumas, R. Gerlai, S.P. Williams, M. van Lookeren Campagne, and N. Ferrara VEGF antagonism reduces edema formation and tissue damage after ischemia/reperfusion injury in the mouse brain J. Clin. Invest. 104 1999 1613 1620
88. R.L. Vangilder, C.L. Rosen, T.L. Barr, and J.D. Huber Targeting the neurovascular unit for treatment of neurological disorders Pharmacol. Ther. 130 2011 239 247
89. C. Von Monakow Die Lokalisation im Großhirn und der Abbau der Funktion durch Kortikale Herde 1914 J.F. Bergmann Wiesbaden, Germany pp 2634
90. A. Wick, W. Wick, J. Waltenberger, M. Weller, J. Dichgans, and J.B. Schulz Neuroprotection by hypoxic preconditioning requires sequential activation of vascular endothelial growth factor receptor and Akt J. Neurosci. 22 2002 6401 6407
91. J. Widenfalk, A. Lipson, M. Jubran, C. Hofstetter, T. Ebendal, Y. Cao, and L. Olson Vascular endothelial growth factor improves functional outcome and decreases secondary degeneration in experimental spinal cord contusion injury Neuroscience 120 2003 951 960
92. J. Yang, L. Guo, R. Liu, and H. Liu Neuroprotective effects of VEGF administration after focal cerebral ischemia/reperfusion: dose response and time window Neurochem. Int. 60 2012 592 596
93. S. Zacchigna, D. Lambrechts, and P. Carmeliet Neurovascular signalling defects in neurodegeneration Nat. Rev. Neurosci. 9 2008 169 181