Intracerebroventricularly delivered VEGF promotes contralesional corticorubral plasticity after focal cerebral ischemia via mechanisms involving anti-inflammatory actions

Neurobiology of Disease

Volumn 45, Issue 3, 2012, Pages 1077-1085

  Herz, Josephine ^a   Reitmeir, Raluca ^a   Hagen, Sabine I ^a   Reinboth, Barbara S ^a   Guo, Zeyun ^a   Zechariah, Anil ^a   ElAli, Ayman ^a   Doeppner, Thorsten R ^a   Bacigaluppi, Marco ^b   Pluchino, Stefano ^b   Kilic, Ülkan ^c   Kilic, Ertugrul ^d   Hermann, Dirk M ^a  

^a UNIVERSITY HOSPITAL ESSEN   (Germany)

^b SAN RAFFAELE HOSPITAL   (Italy)

^c BEZMIALEM VAKIF UNIVERSITY   (Turkey)

^d YEDITEPE UNIVERSITY   (Turkey)

Author keywords

Axonal sprouting; Brain plasticity; Ischemic stroke; Neuroinflammation; Neuroprotection

Indexed keywords

CD45 ANTIGEN; INTERLEUKIN 1BETA; INTERLEUKIN 6; VASCULOTROPIN 165;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BRAIN ISCHEMIA; CONTROLLED STUDY; CORTICORUBRAL TRACT; CYTOKINE RELEASE; DOWN REGULATION; DRUG ADMINISTRATION ROUTE; DRUG RESPONSE; FEMALE; GRIP STRENGTH; HEMISPHERE; IMMUNOHISTOCHEMISTRY; IMMUNOSUPPRESSIVE TREATMENT; INFLAMMATORY INFILTRATE; INNERVATION; LEUKOCYTE MIGRATION; MALE; MICROGLIA; MIDDLE CEREBRAL ARTERY OCCLUSION; MOTOR COORDINATION; MOTOR PERFORMANCE; MOUSE; NERVE CELL PLASTICITY; NERVE FIBER; NERVE STIMULATION; NEUROANATOMICAL TRACT TRACING; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL TRACT; RED NUCLEUS; STROKE; SYNAPTIC TRANSMISSION;

ANIMALS; ANTI-INFLAMMATORY AGENTS; BIOTIN; BRAIN EDEMA; CEREBRAL CORTEX; CEREBRAL INFARCTION; CYTOKINES; DEXTRANS; DISEASE MODELS, ANIMAL; FUNCTIONAL LATERALITY; GENE EXPRESSION REGULATION; HAND STRENGTH; INFARCTION, MIDDLE CEREBRAL ARTERY; INJECTIONS, INTRAVENTRICULAR; MALE; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; NERVE DEGENERATION; NEURAL PATHWAYS; NEURONAL PLASTICITY; ORGANOMETALLIC COMPOUNDS; ORGANOPHOSPHORUS COMPOUNDS; RED NUCLEUS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84856588450     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2011.12.026     Document Type: Article

References (44)

1. Abumiya T., Yokota C., Kuge Y., Minematsu K. Aggravation of hemorrhagic transformation by early intraarterial infusion of low-dose vascular endothelial growth factor after transient focal cerebral ischemia in rats. Brain Res. 2005, 1049:95-103.
2. Andres R.H., Horie N., Slikker W., Keren-Gill H., Zhan K., Sun G., Manley N.C., Pereira M.P., Sheikh L.S., McMIllan E.L., Schaar B.T., Svendsen C.N., Bliss T.M., Steinberg G.K. Human neural stem cells enhance structural plasticity and axonal transport in the ischaemic brain. Brain 2011, 134:1777-1789.
3. Bacigaluppi M., Pluchino S., Peruzzotti-Jametti L., Kilic E., Kilic U., Salani G., Brambilla E., West M.J., Comi G., Martino G., Hermann D.M. Delayed post-ischaemic neuroprotection following systemic neural stem cell transplantation involves multiple mechanisms. Brain 2009, 132:2239-2251.
4. Biber K., Vinet J., Boddeke H.W. Neuron-microglia signaling: chemokines as versatile messengers. J. Neuroimmunol. 2008, 198:69-74.
5. Boulanger L.M. Immune proteins in brain development and synaptic plasticity. Neuron 2009, 64:93-109.
6. Buchli A.D., Schwab M.E. Inhibition of Nogo: a key strategy to increase regeneration, plasticity and functional recovery of the lesioned central nervous system. Ann. Med. 2005, 37:556-567.
7. Ceulemans A.G., Zgavc T., Kooijman R., Hachimi-Idrissi S., Sarre S., Michotte Y. The dual role of the neuroinflammatory response after ischemic stroke: modulatory effects of hypothermia. J. Neuroinflammation 2010, 7:74.
8. Chopp M., Li Y., Zhang J. Plasticity and remodeling of brain. J. Neurol. Sci. 2008, 265:97-101.
9. Dimitrijevic O.B., Stamatovic S.M., Keep R.F., Andjelkovic A.V. Absence of the chemokine receptor CCR2 protects against cerebral ischemia/reperfusion injury in mice. Stroke 2007, 38:1345-1353.
10. Dirnagl U., Iadecola C., Moskowitz M.A. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci. 1999, 22:391-397.
11. ElAli A., Hermann D.M. Apolipoprotein E controls ATP-binding cassette transporters in the ischemic brain. Sci. Signal. 2010, 3:ra72.
12. Engelhardt B., Ransohoff R.M. The ins and outs of T-lymphocyte trafficking to the CNS: anatomical sites and molecular mechanisms. Trends Immunol. 2005, 26:485-495.
13. Golz G., Uhlmann L., Ludecke D., Markgraf N., Nitsch R., Hendrix S. The cytokine/neurotrophin axis in peripheral axon outgrowth. Eur. J. Neurosci. 2006, 24:2721-2730.
14. Hayashi M., Luo Y., Laning J., Strieter R.M., Dorf M.E. Production and function of monocyte chemoattractant protein-1 and other beta-chemokines in murine glial cells. J. Neuroimmunol. 1995, 60:143-150.
15. Hermann D.M., Zechariah A. Implications of vascular endothelial growth factor for postischemic neurovascular remodeling. J. Cereb. Blood Flow Metab. 2009, 29:1620-1643.
16. Hermann D.M., Kilic E., Hata R., Hossmann K.A., Mies G. Relationship between metabolic dysfunctions, gene responses and delayed cell death after mild focal cerebral ischemia in mice. Neuroscience 2001, 104:947-955.
17. Jordan J., Segura T., Brea D., Galindo M.F., Castillo J. Inflammation as therapeutic objective in stroke. Curr. Pharm. Des. 2008, 14:3549-3564.
18. Kilic E., Spudich A., Kilic U., Rentsch K.M., Vig R., Matter C.M., Wunderli-Allenspach H., Fritschy J.M., Bassetti C., Hermann D.M. ABCC1: a gateway for pharmacological compounds to the ischaemic brain. Brain 2008, 131:2679-2689.
19. Kilic E., ElAli A., Kilic U., Guo Z., Ugur M., Uslu U., Bassetti C.L., Schwab M.E., Hermann D.M. Role of Nogo-A in neuronal survival in the reperfused ischemic brain. J. Cereb. Blood Flow Metab. 2010, 30:969-984.
20. Kriz J., Lalancette-Hebert M. Inflammation, plasticity and real-time imaging after cerebral ischemia. Acta Neuropathol. 2009, 117:497-509.
21. Lakhan S.E., Kirchgessner A., Hofer M. Inflammatory mechanisms in ischemic stroke: therapeutic approaches. J. Transl. Med. 2009, 7:97.
22. Lalancette-Hebert M., Gowing G., Simard A., Weng Y.C., Kriz J. Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J. Neurosci. 2007, 27:2596-2605.
23. Lee S.C., Liu W., Brosnan C.F., Dickson D.W. GM-CSF promotes proliferation of human fetal and adult microglia in primary cultures. Glia 1994, 12:309-318.
24. Liu Z., Li Y., Zhang R.L., Cui Y., Chopp M. Bone marrow stromal cells promote skilled motor recovery and enhance contralesional axonal connections after ischemic stroke in adult mice. Stroke 2011, 42:740-744.
25. Lok J., Gupta P., Guo S., Kim W.J., Whalen M.J., van Leyen K., Lo E.H. Cell-cell signaling in the neurovascular unit. Neurochem. Res. 2007, 32:2032-2045.
26. Madinier A., Bertrand N., Mossiat C., Prigent-Tessier A., Beley A., Marie C., Garnier P. Microglial involvement in neuroplastic changes following focal brain ischemia in rats. PLoS One 2009, 4:e8101.
27. Markus T.M., Tsai S.Y., Bollnow M.R., Farrer R.G., O'Brien T.E., Kindler-Baumann D.R., Rausch M., Rudin M., Wiessner C., Mir A.K., Schwab M.E., Kartie G.L. Recovery and brain reorganization after stroke in adult and aged rats. Ann. Neurol. 2005, 58:950-953.
28. Miao H.Q., Soker S., Feiner L., Alonso J.L., Raper J.A., Klagsbrun M. Neuropilin-1 mediates collapsin-1/semaphorin III inhibition of endothelial cell motility: functional competition of collapsin-1 and vascular endothelial growth factor-165. J. Cell Biol. 1999, 146:233-242.
29. Muessel M.J., Klein R.M., Wilson A.M., Berman N.E. Ablation of the chemokine monocyte chemoattractant protein-1 delays retrograde neuronal degeneration, attenuates microglial activation, and alters expression of cell death molecules. Brain Res. Mol. Brain Res. 2002, 103:12-27.
30. Opatz J., Kury P., Schiwy N., Järve A., Estrada V., Brazda N., Bosse F., Müller H.W. SDF-1 stimulates neurite growth on inhibitory CNS myelin. Mol. Cell. Neurosci. 2009, 40:293-300.
31. Papadopoulos C.M., Tsai S.Y., Alsbiei T., O'Brien T.E., Schwab M.E., Kartje G.L. Functional recovery and neuroanatomical plasticity following middle cerebral artery occlusion and IN-1 antibody treatment in the adult rat. Ann. Neurol. 2002, 51:433-441.
32. Reitmeir R., Kilic E., Kilic U., Bacigaluppi M., ElAli A., Salani G., Pluchino S., Gassmann M., Hermann D.M. Post-acute delivery of erythropoietin induces stroke recovery by promoting perilesional tissue remodelling and contralesional pyramidal tract plasticity. Brain 2011, 134:84-99.
33. Reitmeir R., Kilic E., Reinboth B.S., Guo Z., ElAli A., Zechariah A., Kilic U., Hermann D.M. Vascular endothelial growth factor induces contralesional corticobulbar plasticity and functional neurological recovery in the ischemic brain. Acta Neuropathol 2011, 10.1007/s00401-011-0914-z.
34. Seymour A.B., Andrews E.M., Tsai S.Y., Markus T.M., Bollnow M.R., Brennemann M.R., O'Brien T.E., Castro A.J., Schwab M.E., Kartie G.L. Delayed treatment with monoclonal antibody IN-1 1week after stroke results in recovery of function and corticorubral plasticity in adult rats. J. Cereb. Blood Flow Metab. 2005, 25:1366-1375.
35. Soker S., Takashima S., Miao H.Q., Neufeld G., Klagsbrun M. Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 1998, 92:735-745.
36. Sun Y., Jin K., Xie L., Childs J., Mao X.O., Logvinova A., Greenberg D.A. VEGF-induced neuroprotection, neurogenesis, and angiogenesis after focal cerebral ischemia. J. Clin. Invest. 2003, 111:1843-1851.
37. Suzuki S., Tanaka K., Suzuki N. Ambivalent aspects of interleukin-6 in cerebral ischemia: inflammatory versus neurotrophic aspects. J. Cereb. Blood Flow Metab. 2009, 29:464-479.
38. Wang Y., Kilic E., Kilic U., Weber B., Bassetti C.L., Marti H.H., Hermann D.M. VEGF overexpression induces post-ischaemic neuroprotection, but facilitates haemodynamic steal phenomena. Brain 2005, 128:52-63.
39. Wang Q., Tang X.N., Yenari M.A. The inflammatory response in stroke. J. Neuroimmunol. 2007, 184:53-68.
40. Wang Y., Jin K., Mao X.O., Xie L., Banwait S., Marti H.H., Greenberg D.A. VEGF-overexpressing transgenic mice show enhanced post-ischemic neurogenesis and neuromigration. J. Neurosci. Res. 2007, 85:740-747.
41. Wiessner C., Bareyre F.M., Allegrini P.R., Mir A.K., Frentzel S., Zurini M., Schnell L., Oertle T., Schwab M.E. Anti-Nogo-A antibody infusion 24hours after experimental stroke improved behavioral outcome and corticospinal plasticity in normotensive and spontaneously hypertensive rats. J. Cereb. Blood Flow Metab. 2003, 23:154-165.
42. Zhang Z.G., Chopp M. Neurorestorative therapies for stroke: underlying mechanisms and translation to the clinic. Lancet Neurol. 2009, 8:491-500.
43. Zhang Z.G., Zhang L., Jiang Q., Zhang R., Davies K., Powers C., Bruggen N., Chopp M. VEGF enhances angiogenesis and promotes blood-brain barrier leakage in the ischemic brain. J. Clin. Invest. 2000, 106:829-838.
44. Zörner B., Schwab M.E. Anti-Nogo on the go: from animal models to a clinical trial. Ann. N. Y. Acad. Sci. 2010, 1198:E22-E34.