Guidance from Above: Common Cues Direct Distinct Signaling Outcomes in Vascular and Neural Patterning

Overview

Journal Trends Cell Biol

Specialty Cell Biology

Date 2009 Feb 10

PMID 19200729

Citations 37

Authors

Maria V Gelfand

Shangyu Hong

Chenghua Gu

Affiliations

Soon will be listed here.

Abstract

The nervous and vascular systems are both exquisitely branched and complicated systems and their proper development requires careful guidance of nerves and vessels. The recent realization that common ligand-receptor pairs are used in guiding the patterning of both systems has prompted the question of whether similar signaling pathways are used in both systems. This review highlights recent progress in our understanding of the similarities and differences in the intracellular signaling mechanisms downstream of semaphorins, ephrins and vascular endothelial growth factor in neurons and endothelial cells during neural and vascular development. We present evidence that similar intracellular signaling principles underlying cytoskeletal regulation are used to control neural and vascular guidance, although the specific molecules used in neurons and endothelial cells are often different.

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References

Vikis H, Li W, He Z, Guan K . The semaphorin receptor plexin-B1 specifically interacts with active Rac in a ligand-dependent manner. Proc Natl Acad Sci U S A. 2000; 97(23):12457-62. PMC: 18785. DOI: 10.1073/pnas.220421797. View

Himanen J, Saha N, Nikolov D . Cell-cell signaling via Eph receptors and ephrins. Curr Opin Cell Biol. 2007; 19(5):534-42. PMC: 3327877. DOI: 10.1016/j.ceb.2007.08.004. View

Schubert V, Dotti C . Transmitting on actin: synaptic control of dendritic architecture. J Cell Sci. 2007; 120(Pt 2):205-12. DOI: 10.1242/jcs.03337. View

Lee S, Chen T, Barber C, Jordan M, Murdock J, Desai S . Autocrine VEGF signaling is required for vascular homeostasis. Cell. 2007; 130(4):691-703. PMC: 3010851. DOI: 10.1016/j.cell.2007.06.054. View

Iwasato T, Katoh H, Nishimaru H, Ishikawa Y, Inoue H, Saito Y . Rac-GAP alpha-chimerin regulates motor-circuit formation as a key mediator of EphrinB3/EphA4 forward signaling. Cell. 2007; 130(4):742-53. DOI: 10.1016/j.cell.2007.07.022. View

Salikhova A, Wang L, Lanahan A, Liu M, Simons M, Leenders W . Vascular endothelial growth factor and semaphorin induce neuropilin-1 endocytosis via separate pathways. Circ Res. 2008; 103(6):e71-9. PMC: 2674948. DOI: 10.1161/CIRCRESAHA.108.183327. View

Jones C, Li D . Common cues regulate neural and vascular patterning. Curr Opin Genet Dev. 2007; 17(4):332-6. PMC: 2279096. DOI: 10.1016/j.gde.2007.07.004. View

Serini G, Valdembri D, Zanivan S, Morterra G, Burkhardt C, Caccavari F . Class 3 semaphorins control vascular morphogenesis by inhibiting integrin function. Nature. 2003; 424(6947):391-7. DOI: 10.1038/nature01784. View

Georgakopoulos A, Litterst C, Ghersi E, Baki L, Xu C, Serban G . Metalloproteinase/Presenilin1 processing of ephrinB regulates EphB-induced Src phosphorylation and signaling. EMBO J. 2006; 25(6):1242-52. PMC: 1422162. DOI: 10.1038/sj.emboj.7601031. View

10.

Cowan C, Henkemeyer M . The SH2/SH3 adaptor Grb4 transduces B-ephrin reverse signals. Nature. 2001; 413(6852):174-9. DOI: 10.1038/35093123. View

11.

Sakurai Y, Ohgimoto K, Kataoka Y, Yoshida N, Shibuya M . Essential role of Flk-1 (VEGF receptor 2) tyrosine residue 1173 in vasculogenesis in mice. Proc Natl Acad Sci U S A. 2005; 102(4):1076-81. PMC: 545830. DOI: 10.1073/pnas.0404984102. View

12.

Oinuma I, Katoh H, Negishi M . Molecular dissection of the semaphorin 4D receptor plexin-B1-stimulated R-Ras GTPase-activating protein activity and neurite remodeling in hippocampal neurons. J Neurosci. 2004; 24(50):11473-80. PMC: 6730355. DOI: 10.1523/JNEUROSCI.3257-04.2004. View

13.

Gerhardt H, Golding M, Fruttiger M, Ruhrberg C, Lundkvist A, Abramsson A . VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol. 2003; 161(6):1163-77. PMC: 2172999. DOI: 10.1083/jcb.200302047. View

14.

Tolias K, Bikoff J, Kane C, Tolias C, Hu L, Greenberg M . The Rac1 guanine nucleotide exchange factor Tiam1 mediates EphB receptor-dependent dendritic spine development. Proc Natl Acad Sci U S A. 2007; 104(17):7265-70. PMC: 1855368. DOI: 10.1073/pnas.0702044104. View

15.

Cowan C, Henkemeyer M . Ephrins in reverse, park and drive. Trends Cell Biol. 2002; 12(7):339-46. DOI: 10.1016/s0962-8924(02)02317-6. View

16.

Eickholt B, Walsh F, Doherty P . An inactive pool of GSK-3 at the leading edge of growth cones is implicated in Semaphorin 3A signaling. J Cell Biol. 2002; 157(2):211-7. PMC: 2199247. DOI: 10.1083/jcb.200201098. View

17.

Segura I, Essmann C, Weinges S, Acker-Palmer A . Grb4 and GIT1 transduce ephrinB reverse signals modulating spine morphogenesis and synapse formation. Nat Neurosci. 2007; 10(3):301-10. DOI: 10.1038/nn1858. View

18.

Aoto J, Ting P, Maghsoodi B, Xu N, Henkemeyer M, Chen L . Postsynaptic ephrinB3 promotes shaft glutamatergic synapse formation. J Neurosci. 2007; 27(28):7508-19. PMC: 6672605. DOI: 10.1523/JNEUROSCI.0705-07.2007. View

19.

Tolosa L, Mir M, Asensio V, Olmos G, Llado J . Vascular endothelial growth factor protects spinal cord motoneurons against glutamate-induced excitotoxicity via phosphatidylinositol 3-kinase. J Neurochem. 2008; 105(4):1080-90. DOI: 10.1111/j.1471-4159.2007.05206.x. View

20.

Tran T, Kolodkin A, Bharadwaj R . Semaphorin regulation of cellular morphology. Annu Rev Cell Dev Biol. 2007; 23:263-92. DOI: 10.1146/annurev.cellbio.22.010605.093554. View