Vascular endothelial growth factor promotes anatomical and functional recovery of injured peripheral nerves in the avascular cornea

FASEB Journal

Volumn 27, Issue 7, 2013, Pages 2756-2767

  Pan, Zan ^a   Fukuoka, Shima ^a   Karagianni, Natalia ^a   Guaiquil, Victor H ^a   Rosenblatt, Mark I ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Eye; Nerve regeneration; Neurofluorescent thy1 YFP mice; Neurotrophic; Receptor; Wound healing

Indexed keywords

MESSENGER RNA; NEUROPILIN RECEPTOR 1; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2;

ARTICLE; CONTROLLED STUDY; CONVALESCENCE; CORNEA; CORNEA EPITHELIUM; CORNEA STROMA; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; NERVE GROWTH; NERVE INJURY; NERVE REGENERATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; WESTERN BLOTTING; WOUND HEALING;

EYE; NERVE REGENERATION; NEUROFLUORESCENT THY1-YFP MICE; NEUROTROPHIC; RECEPTOR; WOUND HEALING;

ANIMALS; ANTIBODIES, NEUTRALIZING; CELLS, CULTURED; CINNAMATES; CORNEA; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE REGENERATION; NEURITES; PERIPHERAL NERVE INJURIES; PHENYLUREA COMPOUNDS; QUINOLINES; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; RECOVERY OF FUNCTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRIGEMINAL GANGLION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

MUS;

EID: 84879672460     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-225185     Document Type: Article

References (37)

1. Callaghan, B. C., Cheng, H. T., Stables, C. L., Smith, A. L., and Feldman, E. L. (2012) Diabetic neuropathy: clinical manifestations and current treatments. Lancet Neurol. 11, 521-534
2. Zochodne, D. W. (2012) The challenges and beauty of peripheral nerve regrowth. J. Peripher. Nerv. Syst. 17, 1-18
3. Jin, K., Mao, X. O., and Greenberg, D. A. (2006) Vascular endothelial growth factor stimulates dendrite outgrowth from cerebral cortical neurons via Rho kinase signaling. J. Neurobiol. 66, 236-242 (Pubitemid 43202761)
4. Margaritescu, O., Pirici, D., and Margaritescu, C. (2011) VEGF expression in human brain tissue after acute ischemic stroke. Rom. J. Morphol. Embryol. 52, 1283-1292
5. Jin, K. L., Mao, X. O., and Greenberg, D. A. (2000) Vascular endothelial growth factor: direct neuroprotective effect in in vitro ischemia. Proc. Natl. Acad. Sci. U. S. A. 97, 10242-10247
6. Khaibullina, A. A., Rosenstein, J. M., and Krum, J. M. (2004) Vascular endothelial growth factor promotes dendrite maturation in primary CNS neuronal cultures. Brain Res. Dev. Brain Res. 148, 59-68 (Pubitemid 38147805)
7. Yu, C. Q., Zhang, M., Matis, K. I., Kim, C., and Rosenblatt, M. I. (2008) Vascular endothelial growth factor mediates corneal nerve repair. Invest. Ophthalmol. Vis. Sci. 49, 3870-3878
8. Sondell, M., Sundler, F., and Kanje, M. (2000) Vascular endothelial growth factor is a neurotrophic factor which stimulates axonal outgrowth through the flk-1 receptor. Eur. J. Neurosci. 12, 4243-4254 (Pubitemid 32037835)
9. Jin, K., Zhu, Y., Sun, Y., Mao, X. O., Xie, L., and Greenberg, D. A. (2002) Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc. Natl. Acad. Sci. U. S. A. 99, 11946-11950 (Pubitemid 34994504)
10. Lunn, J. S., Sakowski, S. A., Kim, B., Rosenberg, A. A., and Feldman, E. L. (2009) Vascular endothelial growth factor prevents G93A-SOD1-induced motor neuron degeneration. Dev. Neurobiol. 69, 871-884
11. Sathasivam, S. (2008) VEGF and ALS. Neurosci. Res. 62, 71-77
12. Neufeld, G., Cohen, T., Gengrinovitch, S., and Poltorak, Z. (1999) Vascular endothelial growth factor (VEGF) and its receptors. FASEB J. 13, 9-22 (Pubitemid 29038270)
13. Widenfalk, J., Lipson, A., Jubran, M., Hofstetter, C., Ebendal, T., Cao, Y., and Olson, L. (2003) Vascular endothelial growth factor improves functional outcome and decreases secondary degeneration in experimental spinal cord contusion injury. Neuroscience 120, 951-960 (Pubitemid 36966647)
14. Schratzberger, P., Walter, D. H., Rittig, K., Bahlmann, F. H., Pola, R., Curry, C., Silver, M., Krainin, J. G., Weinberg, D. H., Ropper, A. H., and Isner, J. M. (2001) Reversal of experimental diabetic neuropathy by VEGF gene transfer. J. Clin. Invest. 107, 1083-1092 (Pubitemid 32422905)
15. Lok, J., Gupta, P., Guo, S., Kim, W. J., Whalen, M. J., van Leyen, K., and Lo, E. H. (2007) Cell-cell signaling in the neurovascular unit. Neurochem. Res. 32, 2032-2045 (Pubitemid 350059847)
16. Marfurt, C. F., Cox, J., Deek, S., and Dvorscak, L. (2010) Anatomy of the human corneal innervation. Exp. Eye Res. 90, 478-492
17. Yu, C. Q., and Rosenblatt, M. I. (2007) Transgenic corneal neurofluorescence in mice: a new model for in vivo investigation of nerve structure and regeneration. Invest. Ophthalmol. Vis. Sci. 48, 1535-1542 (Pubitemid 351261336)
18. Malin, S. A., Davis, B. M., and Molliver, D. C. (2007) Production of dissociated sensory neuron cultures and considerations for their use in studying neuronal function and plasticity. Nat. Protoc. 2, 152-160 (Pubitemid 47040078)
19. Rogers, M. S., Birsner, A. E., and D'Amato, R. J. (2007) The mouse cornea micropocket angiogenesis assay. Nat. Protoc. 2, 2545-2550
20. Bates, B. D., Mitchell, K., Keller, J. M., Chan, C. C., Swaim, W. D., Yaskovich, R., Mannes, A. J., and Iadarola, M. J. (2010) Prolonged analgesic response of cornea to topical resiniferatoxin, a potent TRPV1 agonist. Pain 149, 522-528
21. de Castro, F., Silos-Santiago, I., Lopez de Armentia, M., Barbacid, M., and Belmonte, C. (1998) Corneal innervation and sensitivity to noxious stimuli in trkA knockout mice. Eur. J. Neurosci. 10, 146-152
22. Kappas, N. C., Zeng, G., Chappell, J. C., Kearney, J. B., Hazarika, S., Kallianos, K. G., Patterson, C., Annex, B. H., and Bautch, V. L. (2008) The VEGF receptor Flt-1 spatially modulates Flk-1 signaling and blood vessel branching. J. Cell Biol. 181, 847-858 (Pubitemid 351786988)
23. Kendall, R. L., Wang, G., and Thomas, K. A. (1996) Identification of a natural soluble form of the vascular endothelial growth factor receptor, FLT-1, and its heterodimerization with KDR. Biochem. Biophys. Res. Commun. 226, 324-328 (Pubitemid 26331903)
24. Zhu, Y., Jin, K., Mao, X. O., and Greenberg, D. A. (2003) Vascular endothelial growth factor promotes proliferation of cortical neuron precursors by regulating E2F expression. FASEB J. 17, 186-193 (Pubitemid 36164388)
25. Grunewald, M., Avraham, I., Dor, Y., Bachar-Lustig, E., Itin, A., Jung, S., Chimenti, S., Landsman, L., Abramovitch, R., and Keshet, E. (2006) VEGF-induced adult neovascularization: recruitment, retention, and role of accessory cells. Cell 124, 175-189 (Pubitemid 43069318)
26. Senger, D. R., Claffey, K. P., Benes, J. E., Perruzzi, C. A., Sergiou, A. P., and Detmar, M. (1997) Angiogenesis promoted by vascular endothelial growth factor: regulation through α1β1 and α2β1 integrins. Proc. Natl. Acad. Sci. U. S. A. 94, 13612-13617
27. Sitohy, B., Nagy, J. A., and Dvorak, H. F. (2012) Anti-VEGF/VEGFR therapy for cancer: reassessing the target. Cancer Res. 72, 1909-1914
28. Kirchmair, R., Tietz, A. B., Panagiotou, E., Walter, D. H., Silver, M., Yoon, Y. S., Schratzberger, P., Weber, A., Kusano, K., Weinberg, D. H., Ropper, A. H., Isner, J. M., and Losordo, D. W. (2007) Therapeutic angiogenesis inhibits or rescues chemother-apy-induced peripheral neuropathy: taxol- and thalidomide-induced injury of vasa nervorum is ameliorated by VEGF. Mol. Ther. 15, 69-75 (Pubitemid 46043651)
29. Baker, K. S., Anderson, S. C., Romanowski, E. G., Thoft, R. A., and SundarRaj, N. (1993) Trigeminal ganglion neurons affect corneal epithelial phenotype. Influence on type VII collagen expression in vitro. Invest. Ophthalmol. Vis. Sci. 34, 137-144 (Pubitemid 23045111)
30. Garcia-Hirschfeld, J., Lopez-Briones, L. G., and Belmonte, C. (1994) Neurotrophic influences on corneal epithelial cells. Exp. Eye Res. 59, 597-605
31. Rosenberg, M. E., Tervo, T. M., Muller, L. J., Moilanen, J. A., and Vesaluoma, M. H. (2002) In vivo confocal microscopy after herpes keratitis. Cornea 21, 265-269 (Pubitemid 34250603)
32. Nishida, T., and Yanai, R. (2009) Advances in treatment for neurotrophic keratopathy. Curr. Opin. Ophthalmol. 20, 276-281
33. Ueno, H., Ferrari, G., Hattori, T., Saban, D. R., Katikireddy, K. R., Chauhan, S. K., and Dana, R. (2012) Dependence of corneal stem/progenitor cells on ocular surface innervation. Invest. Ophthalmol. Vis. Sci. 53, 867-872
34. Li, Z., Burns, A. R., Han, L., Rumbaut, R. E., and Smith, C. W. (2011) IL-17 and VEGF are necessary for efficient corneal nerve regeneration. Am. J. Pathol. 178, 1106-1116
35. Forbes, D. J., Pozos, R. S., and Nelson, J. D. (1987) Co-culture of rat trigeminal ganglion neurons and corneal epithelium. Curr. Eye Res. 6, 507-514 (Pubitemid 17039762)
36. Ebihara, N., Matsuda, A., Nakamura, S., Matsuda, H., and Murakami, A. (2011) Role of the IL-6 classic- and trans-signaling pathways in corneal sterile inflammation and wound healing. Invest. Ophthalmol. Vis. Sci. 52, 8549-8557
37. Li, Z. R., Li, Y. P., Lin, M. L., Su, W. R., Zhang, W. X., Zhang, Y., Yao, L., and Liang, D. (2012) Activated macrophages induce neovascularization through upregulation of MMP-9 and VEGF in rat corneas. Cornea 31, 1028-1035