VEGF-A and Semaphorin3A: Modulators of vascular sympathetic innervation

Developmental Biology

Volumn 334, Issue 1, 2009, Pages 119-132

  Long, Jennifer B ^a   Jay, Steven M ^a   Segal, Steven S ^b   Madri, Joseph A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

Author keywords

Carotid artery; Femoral artery; Neuropilin 1; Semaphorin3A; Superior cervical ganglion; Sympathetic innervation; Vascular endothelial growth factor A

Indexed keywords

EID: 69949131673     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2009.07.023     Document Type: Article

References (64)

1. Adams R.H., Wilkinson G.A., Weiss C., Diella F., Gale N.W., Deutsch U., Risau W., and Klein R. Roles of ephrinB ligands and EphB receptors in cardiovascular development: demarcation of arterial/venous domains, vascular morphogenesis, and sprouting angiogenesis. Genes Dev. 13 (1999) 295-306
2. Appleton B.A., Wu P., Maloney J., Yin J., Liang W.C., Stawicki S., Mortara K., Bowman K.K., Elliott J.M., Desmarais W., Bazan J.F., Bagri A., Tessier-Lavigne M., Koch A.W., Wu Y., Watts R.J., and Wiesmann C. Structural studies of neuropilin/antibody complexes provide insights into semaphorin and VEGF binding. EMBO J. 26 (2007) 4902-4912
3. Bagnard D., Vaillant C., Khuth S.T., Dufay N., Lohrum M., Puschel A.W., Belin M.F., Bolz J., and Thomasset N. Semaphorin 3A-vascular endothelial growth factor-165 balance mediates migration and apoptosis of neural progenitor cells by the recruitment of shared receptor. J. Neurosci. 21 (2001) 3332-3341
4. Belliveau D.J., Krivko I., Kohn J., Lachance C., Pozniak C., Rusakov D., Kaplan D., and Miller F.D. NGF and neurotrophin-3 both activate TrkA on sympathetic neurons but differentially regulate survival and neuritogenesis. J. Cell Biol. 136 (1997) 375-388
5. Birch D.J., Turmaine M., Boulos P.B., and Burnstock G. Sympathetic innervation of human mesenteric artery and vein. J. Vasc. Res. 45 (2008) 323-332
6. Carmeliet P. Blood vessels and nerves: common signals, pathways and diseases. Nat. Rev. Genet. 4 (2003) 710-720
7. Chen H., He Z., Bagri A., and Tessier-Lavigne M. Semaphorin-neuropilin interactions underlying sympathetic axon responses to class III semaphorins. Neuron 6 (1998) 1283-1290
8. Cheng L., Jia H., Lohr M., Bagherzadeh A., Holmes D.I., Selwood D., and Zachary I. Anti-chemorepulsive effects of vascular endothelial growth factor and placental growth factor-2 in dorsal root ganglion neurons are mediated via neuropilin-1 and cyclooxygenase-derived prostanoid production. J. Biol. Chem. 279 (2004) 30654-30661
9. Damon D.H. Vascular endothelial-derived semaphorin 3 inhibits sympathetic axon growth. Am. J. Physiol. Heart Circ. Physiol. 290 (2006) H1220-H1225
10. Damon D.H., Teriele J.A., and Marko S.B. Vascular-derived artemin: a determinant of vascular sympathetic innervation?. Am. J. Physiol. Heart Circ. Physiol. 293 (2007) H266-H273
11. Enciso J.M., Gratzinger D., Camenisch T.D., Canosa S., Pinter E., and Madri J.A. Elevated glucose inhibits VEGF-A-mediated endocardial cushion formation: modulation by PECAM-1 and MMP-2. J. Cell Biol. 160 (2003) 605-615
12. Enomoto H., Crawford P.A., Gorodinsky A., Heuckeroth R.O., Johnson Jr. E.M., and Milbrandt J. RET signaling is essential for migration, axonal growth and axon guidance of developing sympathetic neurons. Development 128 (2001) 3963-3974
13. Fan J., and Raper J.A. Localized collapsing cues can steer growth cones without inducing their full collapse. Neuron 14 (1995) 263-274
14. Fleming B.P., Gibbins I.L., Morris J.L., and Gannon B.J. Noradrenergic and peptidergic innervation of the extrinsic vessels and microcirculation of the rat cremaster muscle. Microvasc. Res. 38 (1989) 255-268
15. Fuh G., Garcia C.K., and de Vos A.M. The interaction of neuropilin-1 with vascular endothelial growth factor and its receptor flt-1. J. Biol. Chem. 275 (2000) 26690-26695
16. Geretti E., Shimizu A., and Klagsbrun M. Neuropilin structure governs VEGF and semaphorin binding and regulates angiogenesis. Angiogenesis 11 (2008) 31-39
17. Glebova N.O., and Ginty D.D. Heterogeneous requirement of NGF for sympathetic target innervation in vivo. J. Neurosci. 24 (2004) 743-751
18. Glebova N.O., and Ginty D.D. Growth and survival signals controlling sympathetic nervous system development. Annu. Rev. Neurosci. 28 (2005) 191-222
19. Grasby D.J., Morris J.L., and Segal S.S. Heterogeneity of vascular innervation in hamster cheek pouch and retractor muscle. J. Vasc. Res. 36 (1999) 465-476
20. Griffith S.G., Crowe R., Lincoln J., Haven A.J., and Burnstock G. Regional differences in the density of perivascular nerves and varicosities, noradrenaline content and responses to nerve stimulation in the rabbit ear artery. Blood Vessels 19 (1982) 41-52
21. Hallaq H., Pinter E., Enciso J., McGrath J., Zeiss C., Brueckner M., Madri J., Jacobs H.C., Wilson C.M., Vasavada H., Jiang X., and Bogue C.W. A null mutation of Hhex results in abnormal cardiac development, defective vasculogenesis and elevated Vegfa levels. Development 131 (2004) 5197-5209
22. He Z., and Tessier-Lavigne M. Neuropilin is a receptor for the axonal chemorepellent semaphorin III. Cell 90 (1997) 739-751
23. Herzog Y., Kalcheim C., Kahane N., Reshef R., and Neufeld G. Differential expression of neuropilin-1 and neuropilin-2 in arteries and veins. Mech. Dev. 109 (2001) 115-119
24. Honma Y., Araki T., Gianino S., Bruce A., Heuckeroth R., Johnson E., and Milbrandt J. Artemin is a vascular-derived neurotropic factor for developing sympathetic neurons. Neuron 35 (2002) 267-282
25. Jay S.M., Shepherd B.R., Bertram J.P., Pober J.S., and Saltzman W.M. Engineering of multifunctional gels integrating highly efficient growth factor delivery with endothelial cell transplantation. Faseb J. 22 (2008) 2949-2956
26. Kawasaki T., Bekku Y., Suto F., Kitsukawa T., Taniguchi M., Nagatsu I., Nagatsu T., Itoh K., Yagi T., and Fujisawa H. Requirement of neuropilin 1-mediated Sema3A signals in patterning of the sympathetic nervous system. Development 3 (2002) 671-680
27. Kitsukawa T., Shimizu M., Sanbo M., Hirata T., Taniguchi M., Bekku Y., Yagi T., and Fujisawa H. Neuropilin-semaphorin III/D-mediated chemorepulsive signals play a crucial role in peripheral nerve projection in mice. Neuron 19 (1997) 995-1005
28. Kolodkin A.L. Growth cones and the cues that repel them. Trends Neurosci. 19 (1996) 507-513
29. Kolodkin A.L., Levengood D.V., Rowe E.G., Tai Y.T., Giger R.J., and Ginty D.D. Neuropilin is a semaphorin III receptor. Cell 90 (1997) 753-762
30. Kuruvilla R., Zweifel L.S., Glebova N.O., Lonze B.E., Valdez G., Ye H., and Ginty D.D. A neurotrophin signaling cascade coordinates sympathetic neuron development through differential control of TrkA trafficking and retrograde signaling. Cell 118 (2004) 243-255
31. Li Q., Michaud M., Stewart W., Schwartz M., and Madri J.A. Modeling the neurovascular niche: murine strain differences mimic the range of responses to chronic hypoxia in the premature newborn. J. Neurosci. Res. 86 (2007) 1227-1242
32. Lin G., Chen K.C., Hsieh P.S., Yeh C.H., Lue T.F., and Lin C.S. Neurotrophic effects of vascular endothelial growth factor and neurotrophins on cultured major pelvic ganglia. B.J.U. Int. 92 (2003) 631-635
33. Livak K.J., and Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25 (2001) 402-408
34. Looft-Wilson R.C., Haug S.J., Neufer P.D., and Segal S.S. Independence of connexin expression and vasomotor conduction from sympathetic innervation in hamster feed arteries. Microcirculation 11 (2004) 397-408
35. Madri J.A., Pratt B.M., and Tucker A.M. Phenotypic modulation of endothelial cells by transforming growth factor-beta depends upon the composition and organization of the extracellular matrix. J. Cell Biol. 106 (1988) 1375-1384
36. Marko S.B., and Damon D.H. VEGF promotes vascular sympathetic innervation. Am. J. Physiol. Heart Circ. Physiol. 294 (2008) H2646-H2652
37. Miao H.Q., Soker S., Feiner L., Alonso J.L., Raper J.A., and 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. 146 (1999) 233-242
38. Miquerol L., Gertsenstein M., Harpal K., Rossant J., and Nagy A. Multiple developmental roles of VEGF suggested by a LacZ-tagged allele. Dev. Biol. 212 (1999) 307-322
39. Miquerol L., Langille B.L., and Nagy A. Embryonic development is disrupted by modest increases in vascular endothelial growth factor gene expression. Development 18 (2000) 3941-3946
40. Nordal R.A., Nagy A., Pintilie M., and Wong C.S. Hypoxia and hypoxia-inducible factor-1 target genes in central nervous system radiation injury: a role for vascular endothelial growth factor. Clin. Cancer Res. 10 (2004) 3342-3353
41. Ogunshola O.O., Antic A., Donoghue M.J., Fan S.Y., Kim H., Stewart W.B., Madri J.A., and Ment L.R. Paracrine and autocrine functions of neuronal vascular endothelial growth factor (VEGF) in the central nervous system. J. Biol. Chem. 277 (2002) 11410-11415
42. Pinter E., Haigh J., Nagy A., and Madri J.A. Hyperglycemia-induced vasculopathy in the murine conceptus is mediated via reductions of VEGF-A expression and VEGF receptor activation. Am. J. Pathol. 158 (2001) 1199-1206
43. Rosenstein J.M., and Krum J.M. New roles for VEGF in nervous tissue-beyond blood vessels. Exp. Neurol. 187 (2004) 246-253
44. Rosoff W.J., Urbach J.S., Esrick M.A., McAllister R.G., Richards L.J., and Goodhill G.J. A new chemotaxis assay shows the extreme sensitivity of axons to molecular gradients. Nat. Neurosci. 7 (2004) 678-682
45. Ruffolo Jr. R.R., Nichols A.J., Stadel J.M., and Hieble J.P. Structure and function of alpha-adrenoceptors. Pharmacol. Rev. 43 (1991) 475-505
46. Schwamborn J.C., Fiore R., Bagnard D., Kappler J., Kaltschmidt C., and Puschel A.W. Semaphorin 3A stimulates neurite extension and regulates gene expression in PC12 cells. J. Biol. Chem. 279 (2004) 30923-30926
47. Schwarz Q., Gu C., Fujisawa H., Sabelko K., Gertsenstein M., Nagy A., Taniguchi M., Kolodkin A.L., Ginty D.D., Shima D.T., and Ruhrberg C. Vascular endothelial growth factor controls neuronal migration and cooperates with Sema3A to pattern distinct compartments of the facial nerve. Genes Dev. 18 (2004) 2822-2834
48. Smith M.K., Peters M.C., Richardson T.P., Garbern J.C., and Mooney D.J. Locally enhanced angiogenesis promotes transplanted cell survival. Tissue Eng. 10 (2004) 63-71
49. Soker S., Takashima S., Miao H.Q., Neufeld G., and Klagsbrun M. Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 92 (1998) 735-745
50. Sondell M., and Kanje M. Postnatal expression of VEGF and its receptor flk-1 in peripheral ganglia. Neuroreport 12 (2001) 105-108
51. Sondell M., Lundborg G., and Kanje M. 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 (1999) 5731-5740
52. Sondell M., Sundler F., and Kanje M. Vascular endothelial growth factor is a neurotrophic factor which stimulates axonal outgrowth through the flk-1 receptor. Eur. J. Neurosci. 12 (2000) 4243-4254
53. Spandidos A., Wang X., Wang H., Dragnev S., Thurber T., and Seed B. A comprehensive collection of experimentally validated primers for Polymerase Chain Reaction quantitation of murine transcript abundance. BMC Genomics 9 (2008) 633
54. Srinivas S., Watanabe T., Lin C.S., William C.M., Tanabe Y., Jessell T.M., and Costantini F. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 1 4 (2001)
55. Storkebaum E., Lambrechts D., Dewerchin M., Moreno-Murciano M.P., Appelmans S., Oh H., Van Damme P., Rutten B., Man W.Y., De Mol M., Wyns S., Manka D., Vermeulen K., Van Den Bosch L., Mertens N., Schmitz C., Robberecht W., Conway E.M., Collen D., Moons L., and Carmeliet P. Treatment of motor neuron degeneration by intracerebroventricular delivery of VEGF in a rat model of ALS. Nat. Neurosci. 8 (2005) 85-92
56. Sun L., Tran N., Tang F., App H., Hirth P., McMahon G., and Tang C. Synthesis and biological evaluations of 3-substituted indolin-2-ones: a novel class of tyrosine kinase inhibitors that exhibit selectivity toward particular receptor tyrosine kinases. J. Med. Chem. 41 (1988) 2588-2603
57. Suto F., Ito K., Uemura M., Shimizu M., Shinkawa Y., Sanbo M., Shinoda T., Tsuboi M., Takashima S., Yagi T., and Fujisawa H. Plexin-a4 mediates axon-repulsive activities of both secreted and transmembrane semaphorins and plays roles in nerve fiber guidance. J. Neurosci. 14 (2005) 3628-3637
58. Tan A.Y., Chen P.S., Chen L.S., and Fishbein M.C. Autonomic nerves in pulmonary veins. Heart Rhythm 3 Suppl (2007) S57-S60
59. Tessier-Lavigne M., and Goodman C.S. The molecular biology of axon guidance. Science 274 (1996) 1123-1133
60. Vieira J.M., Schwarz Q., and Ruhrberg C. Selective requirements for NRP1 ligands during neurovascular patterning. Development 134 (2007) 1833-1843
61. Wang X., and Seed B. A PCR primer bank for quantitative gene expression analysis. Nucleic Acids Res. 31 (2003) e154
62. Wingerd K.L., Goodman N.L., Tresser J.W., Smail M.M., Leu S.T., Rohan S.J., Pring J.L., Jackson D.Y., and Clegg D.O. Alpha 4 integrins and vascular cell adhesion molecule-1 play a role in sympathetic innervation of the heart. J. Neurosci. 22 (2002) 10772-10780
63. Xu X., Francis R., Wei C.J., Linask K.L., and Lo C.W. Connexin 43-mediated modulation of polarized cell movement and the directional migration of cardiac neural crest cells. Development 133 (2006) 3629-3639
64. Young H.M., Anderson R.B., and Anderson C.R. Guidance cues involved in the development of the peripheral autonomic nervous system. Auton. Neurosci. 112 (2004) 1-14