Microvessels promote motor nerve survival and regeneration through local VEGF release following ectopic reattachment

Microcirculation

Volumn 11, Issue 8, 2004, Pages 633-644

  Bearden, Shawn E ^a,b   Segal, Steven S ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Nucl Eng Idaho State University   (United States)

Author keywords

Angiogenesis; Denervation; Microcirculation; Neurotization; Regeneration

Indexed keywords

VASCULOTROPIN; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; BLOOD VESSEL INNERVATION; BLOOD VESSEL SHUNT; BRAIN BLOOD VESSEL; BRAIN MICROCIRCULATION; CELL SURVIVAL; CHEEK POUCH; CONCENTRATION RESPONSE; CONTROLLED STUDY; HAMSTER; IMMUNOLOCALIZATION; MALE; MICROVASCULATURE; MOTOR NERVE; MUSCLE INNERVATION; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NERVE FIBER TRANSECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION;

ANIMALS; AXONS; AXOTOMY; BLOOD VESSELS; CHORISTOMA; CRICETINAE; MICROCIRCULATION; MOTOR NEURONS; MUSCLE CONTRACTION; MUSCLE, SKELETAL; NEOVASCULARIZATION, PHYSIOLOGIC; NERVE REGENERATION; NERVE TRANSFER; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

CRICETINAE;

EID: 10944254866     PISSN: 10739688     EISSN: None     Source Type: Journal    
DOI: 10.1080/10739680490517659     Document Type: Article

References (52)

1. Adams WE. (1942). The blood supply of nerves, I: historical review. J Anat 76:323-341.
2. Aitken JR. (1950). Growth of nerve implants in voluntary muscle. J Anat 84:38-49.
3. Al-Majed AA, Neumann GM, Brushart TM, Gordon T. (2000). Brief electrical stimulation promotes the speed and accuracy of motor axonal regeneration. J Neurosci 20:2602-2608.
4. Annex BH, Torgan GE, Lin P, Taylor DA, Thompson MA, Peters KG, Kraus WE. (1998). Induction and maintenance of increased VEGF protein by chronic motor nerve stimulation in skeletal muscle. Am J Physiol 274:H860-H867.
5. Au E, Roskams AJ. (2003). Olfactory ensheathing cells of the lamina propria in vivo and in vitro. Glia 41:224-236.
6. Bates D, Taylor GI, Minichiello J, Farlie P, Cichowitz A, Watson N, Klagsbrun M, Mamluk R, Newgreen DF. (2003). Neurovascular congruence results from a shared patterning mechanism that utilizes Semaphorin3A and Neuropilin-1. Dev Biol 255:77-98.
7. Bearden SE, Segal SS. (2004). Neurovascular interactions in adult mouse skeletal muscles. Microcirculation, in Press.
8. Bocker-Meffert S, Rosenstiel P, Rohl C, Warneke N, Held-Feindt J, Sievers J, Lucius R. (2002). Erythropoietin and VEGF promote neural outgrowth from retinal explants in postnatal rats. Invest Ophthalmol Vis Sci 43:2021-2026.
9. Breier G, Albrecht U, Sterrer S, Risau W. (1992). Expression of vascular endothelial growth factor during embryonic angiogenesis and endothelial cell differentiation. Development 114:521-532.
10. Brogi E, Wu T, Namiki A, Isner JM. (1994). Indirect angiogenic cytokines upregulate VEGF and bFGF gene expression in vascular smooth muscle cells, whereas hypoxia upregulates VEGF expression only. Circulation 90:649-652.
11. Emanueli C, Salis MB, Pinna A, Graiani G, Manni L, Madeddu P. (2002). Nerve growth factor promotes angiogenesis and arteriogenesis in ischemic hindlimbs. Circulation 106:2257-2262.
12. Ferrara N. (2002). Role of vascular endothelial growth factor in physiologic and pathologic angiogenesis: therapeutic implications. Semin Oncol 29:10-14.
13. Gale NW, Baluk P, Pan L, Kwan M, Holash J, DeChiara TM, McDonald DM, Yancopoulos GD. (2001). Ephrin-B2 selectively marks arterial vessels and neovascularization sites in the adult, with expression in both endothelial and smooth-muscle cells. Dev Biol 230:151-160.
14. Gerber HP, McMurtrey A, Kowalski J, Yan M, Keyt BA, Dixit V, Ferrara N. (1998). Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway: requirement for Flk-1 /KDR activation. J Biol Chem 273:30336-30343.
15. Gingras M, Bergeron J, Dery J, Durham HD, Berthod F. (2003). In vitro development of a tissue-engineered model of peripheral nerve regeneration to study neurite growth. FASEB J 17:2124-2126.
16. Gratton JP, Morales-Ruiz M, Kureishi Y, Fulton D, Walsh K, Sessa WC. (2001). Akt down-regulation of p38 signaling provides a novel mechanism of vascular endothelial growth factor-mediated cytoprotection in endothelial cells. J Biol Chem 276:30359-30365.
17. Gu XH, Terenghi G, Kangesu T, Navsaria HA, Springall DR, Leigh IM, Green GJ, Polak JM. (1995). Regeneration pattern of blood vessels and nerves in cultured keratinocyte grafts assessed by confocal. laser scanning microscopy. Br J Dermatol 132:376-383.
18. Gutmann E, Gutmann L, Medawar PB, Young JZ. (1942). The rate of nerve regeneration. J Exp Biol 19:14-44.
19. Hobson MI, Brown R, Green CJ, Terenghi G. (1997). Inter-relationships between angiogenesis and nerve regeneration: a histochemical study. Br J Plast Surg 50:125-131.
20. Hobson MI, Green CJ, Terenghi G. (2000). VEGF enhances intraneural angiogenesis and improves nerve regeneration after axotomy. J Anat 197:591-605.
21. Houck KA, Leung DW, Rowland AM, Winer J, Ferrara N. (1992). Dual regulation of vascular endothelial growth factor bioavailability by genetic and proteolytic mechanisms. J Biol Chem 267:26031-26037.
22. Keynes RJ, Hopkins WG, Huang LH. (1984). Regeneration of mouse peripheral nerves in degenerating skeletal muscle: guidance by residual muscle fibre basement membrane. Brain Res 295:275-281.
23. Ladoux A, Frelin C. (1993). Expression of vascular endothelial growth factor by cultured endothelial cells from brain microvessels. Biochem Biophys Res Commun 194:799-803.
24. Lambrechts D, Storkebaum E, Morimoto M, Del-Favero J, Desmet F, Marklund SL, Wyns S, Thijs V, Andersson J, Van Marion I, Al-Chalabi A, Bornes S, Musson R, Hansen V, Beckman L, Adolfsson R, Pall HS, Prats H, Vermeire S, Rutgeerts P, Katayama S, Awata T, Leigh N, Lang-Lazdunski L, Dewerchin M, Shaw C, Moons L, Vlietinck R, Morrison KE, Robberecht W, Van Broeckhoven C, Collen D, Andersen PM, Carmeliet P. (2003). VEGF is a modifier of amyotrophic lateral sclerosis in mice and humans and protects motoneurons against ischemic death. Nat Genet 34:383-394.
25. Leventhal C, Rafii S, Rafii D, Shahar A, Goldman SA. (1999). Endothelial trophic support of neuronal production and recruitment from the adult mammalian subependyma. Mol Cell Neurosci 13:450-464.
26. Louissaint A Jr, Rao S, Leventhal C, Goldman SA. (2002). Coordinated interaction of neurogenesis and angiogenesis in the adult songbird brain. Neuron 34:945-960.
27. Manek S, Terenghi G, Shurey C, Nishikawa H, Green CJ, Polak JM. (1993). Neovascularisation precedes neural changes in the rat groin skin flap following denervation: an immunohistochemical study. Br J Plast Surg 46:48-55.
28. Mukouyama YS, Shin D, Britsch S, Taniguchi M, Anderson DJ. (2002). Sensory nerves determine the pattern of arterial differentiation and blood vessel branching in the skin. Cell 109:693-705.
29. Nguyen QT, Sanes JR, Lichtman JW. (2002). Pre-existing pathways promote precise projection patterns. Nat Neurosci 5:861-867.
30. Nomura M, Yamagishi S, Harada S, Hayashi Y, Yamashima T, Yamashita J, Yamamoto H. (1995). Possible participation of autocrine and paracrine vascular endothelial growth factors in hypoxia-induced proliferation of endothelial cells and pericytes. J Biol Chem 270:28316-28324.
31. Ogunshola OO, Antic A, Donoghue MJ, Fan SY, Kim H, Stewart WB, Madri JA, Ment LR. (2002). Paracrine and autocrine functions of neuronal vascular endothelial growth factor (VEGF) in the central nervous system. J Biol Chem 277:11410-11415.
32. Ogunshola OO, Stewart WB, Mihalcik V, Solli T, Madri JA, Ment LR. (2000). Neuronal VEGF expression correlates with angiogenesis in postnatal developing rat brain. Brain Res Dev Brain Res 119:139-153.
33. Oosthuyse B, Moons L, Storkebaum E, Beck H, Nuyens D, Brusselmans K, Van Dorpe J, Hellings P, Gorselink M, Heymans S, Theilmeier G, Dewerchin M, Laudenbach V, Vermylen P, Raat H, Acker T, Vleminckx V, Van Den Bosch L, Cashman N, Fujisawa H, Drost MR, Sciot R, Bruyninckx F, Hicklin DJ, Ince C, Gressens P, Lupu F, Plate KH, Robberecht W, Herbert JM, Collen D, Carmeliet P. (2001). Deletion of the hypoxia-response element in the vascular endothelial growth factor promoter causes motor neuron degeneration. Nat Genet 28:131-138.
34. Park JE, Keller GA, Ferrara N. (1993). The vascular endothelial growth factor (VEGF) isoforms: differential deposition into the subepithelial extracellular matrix and bioactivity of extracellular matrix-bound VEGF. Mol Biol Cell 4:1317-1326.
35. Payne SH Jr, Brushart TM. (1997). Neurotization of the rat soleus muscle: a quantitative analysis of reinnervation. J Hand Surg [Am] 22:640-643.
36. Pierzga JM, Segal SS. (1994). Spatial relationships between neuromuscular junctions and microvessels in hamster cremaster muscle. Microvasc Res 48:50-67.
37. Pleasure D, Bannerman P, Ara J, Scarlato M, Itoh T. (2002). Prospects for vascular endothelial growth factor neurotherapeutics. Arch Neurol 59:692-694.
38. Ramón y Cajal S, DeFelipe J, Jones EG. History of Neuroscience, 5: Cajal's Degeneration and Regeneration of the Nervous System. New York: Oxford University Press, 1991.
39. Samii A, Unger J, Lange W. (1999). Vascular endothelial growth factor expression in peripheral nerves and dorsal root ganglia in diabetic neuropathy in rats. Neurosci Lett 262:159-162.
40. Schratzberger P, Schratzberger G, Silver M, Curry C, Kearney M, Magner M, Alroy J, Adelman LS, Weinberg DH, Ropper AH, Isner JM. (2000). Favorable effect of VEGF gene transfer on ischemic peripheral neuropathy. Nat Med 6:405-413.
41. Segal SS, Cunningham SA, Jacobs TL. (2000). Motor nerve topology reflects myocyte morphology in hamster retractor and epitrochlearis muscles. J Morphol 246:103-117.
42. Shen Q, Goderie SK, Jin L, Karanth N, Sun Y, Abramova N, Vincent P, Pumiglia K, Temple S. (2004). Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 304:1338-1340.
43. Shin D, Garcia-Cardena G, Hayashi S, Gerety S, Asahara T, Stavrakis G, Isner J, Folkman J, Gimbrone MA Jr, Anderson DJ. (2001). Expression of ephrinB2 identifies a stable genetic difference between arterial and venous vascular smooth muscle as well as endothelial cells, and marks subsets of microvessels at sites of adult neovascularization. Dev Biol 230:139-150.
44. Simovic D, Isner JM, Ropper AH, Pieczek A, Weinberg DH. (2001). Improvement in chronic ischemic neuropathy after intramuscular phVEGF165 gene transfer in patients with critical limb ischemia. Arch Neurol 58:761-768.
45. Sondell M, Lundborg G, Kanje M. (1999). Vascular endothelial growth factor has neurotrophic activity and stimulates axonal outgrowth, enhancing cell survival and Schwann cell proliferation in the peripheral nervous system. J Neurosci 19:5731-5740.
46. Sondell M, Sandler F, 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.
47. Taylor GI. (1999). Free vascularized nerve transfer in the upper extremity. Hand Clin 15:673-695, ix-x.
48. Tischer E, Mitchell R, Hartman T, Silva M, Gospodarowicz D, Fiddes JC, Abraham JA. (1991). The human gene for vascular endothelial growth factor: multiple protein forms are encoded through alternative exon splicing. J Biol Chem 266:11947-11954.
49. Waller A. (1850). Experiments on the section of the glossopharyngeal and hypoglossal nerves of the frog, and observations of the alterations produced thereby in the structure of their primitive fibres. Philos Trans R Soc Lond 140:423-429.
50. Waris T. (1978). Innervation of scar tissue in the skin of the rat. Scand J Plast Reconstr Surg 12:173-180.
51. Waris T. (1978). Reinnervation of free skin autografts in the rat. Scand J Plast Reconstr Surg 12:85-93.
52. Weibel ER. (1979). Stereological Methods. London: Academic Press.