Plexin-A4 mediates axon-repulsive activities of both secreted and transmembrane semaphorins and plays roles in nerve fiber guidance

Journal of Neuroscience

Volumn 25, Issue 14, 2005, Pages 3628-3637

  Suto, Fumikazu ^a   Ito, Keisuke ^a   Uemura, Masato ^b   Shimizu, Masayuki ^c   Shinkawa, Yutaka ^d   Sanbo, Makoto ^e   Shinoda, Tomoyasu ^d   Tsuboi, Miu ^d   Takashima, Seiji ^f   Yagi, Takeshi ^g   Fujisawa, Hajime ^d  

^a NATIONAL INSTITUTE OF GENETICS   (Japan)

^b RIKEN   (Japan)

^c KUMAMOTO UNIVERSITY   (Japan)

^d NAGOYA UNIVERSITY   (Japan)

^e NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

^f OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^g OSAKA UNIVERSITY   (Japan)

Author keywords

Anterior commissure; Axon repulsion; Barrel formation; DRG axon; Neuropilin; Plexin; Semaphorin; Sympathetic axon

Indexed keywords

CHEMOREPELLENT; MEMBRANE PROTEIN; NEUROPILIN; NEUROPILIN 1; NEUROPILIN 2; PLEXIN; PLEXIN A1; PLEXIN A2; PLEXIN A3; PLEXIN A4; SEMAPHORIN; SEMAPHORIN 3A; SEMAPHORIN 3F; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; GENE DISRUPTION; GENE TARGETING; GROWTH CONE; HUMAN; HUMAN CELL; IN VIVO STUDY; MOUSE; MUTANT; NERVE FIBER; NERVE PROJECTION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; REGULATORY MECHANISM; SENSORY NERVE; SIGNAL TRANSDUCTION; SPINAL GANGLION;

ANIMALS; ANIMALS, NEWBORN; AXONS; CELL ADHESION MOLECULES, NEURONAL; CELLS, CULTURED; CLONING, MOLECULAR; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTRON TRANSPORT COMPLEX IV; EMBRYO; GANGLIA, SPINAL; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MICE; MICE, KNOCKOUT; NERVE FIBERS; NERVE TISSUE PROTEINS; NEURITES; NEURONS; NEUROPILIN-1; PROSENCEPHALON; RECEPTORS, CELL SURFACE; RECOMBINANT PROTEINS; SEMAPHORINS; SYMPATHETIC NERVOUS SYSTEM; TUBULIN; TYROSINE 3-MONOOXYGENASE;

EID: 20144389584     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4480-04.2005     Document Type: Article

References (44)

1. Artigiani S, Conrotto P, Fazzari P, Gilestro GF, Barberis D, Giordano S, Comoglio PM, Tamagnone L (2004) Plexin-B3 is a functional receptor for semaphorin 5A. EMBO Rep 5:710-714.
2. Bagri A, Cheng HJ, Yaron A, Pleasure SJ, Tessier-Lavigne M (2003) Stereotyped pruning of long hippocampal axon branches triggered by retraction inducers of the semaphorin family. Cell 113:285-299.
3. Chédotal A, Del Rio JA, Ruiz M, He Z, Borrell V, de Castro F, Ezan F, Goodman CS, Tessier-Lavigne M, Sotelo C, Soriano E (1998) Semaphorins III and IV repel hippocampal axons via two distinct receptors. Development 125:4313-4323.
4. Chen H, Chédotal A, He Z, Goodman CS, Tessier-Lavigne M (1997) Neuropilin-2, a novel member of the neuropilin family, is a high affinity receptor for the semaphorins Sema E and Sema IV but not Sema III. Neuron 19:547-559.
5. Chen H, He Z, Bagri A, Tessier-Lavigne M (1998) Semaphorin-neuropilin interactions underlying sympathetic axon responses to class III semaphorins. Neuron 21:1283-1290.
6. Chen H, Bagri A, Zupicich JA, Zou Y, Stoeckli E, Pleasure SJ, Lowenstein DH, Skarnes WC, Chédotal A, Tessier-Lavigne M (2000) Neuropilin-2 regulates the development of selective cranial and sensory nerves and hippocampal mossy fiber projections. Neuron 25:43-56.
7. Cheng HJ, Bagri A, Yaron A, Stein E, Pleasure SJ, Tessier-Lavigne M (2001) Plexin-A3 mediates semaphorin signaling and regulates the development of hippocampal axonal projections. Neuron 32:249-263.
8. Cowan CA, Yokoyama N, Saxena A, Chumley MJ, Silvany RE, Baker LA, Srivastava D, Henkemeyer M (2004) Ephrin-B2 reverse signaling is required for axon pathfinding and cardiac valve formation but not early vascular development. Dev Biol 271:263-271.
9. Dodd J, Morton SB, Karagogeos D, Yamamoto M, Jessell TM (1988) Spatial regulation of axonal glycoprotein expression on subsets of embryonic spinal neurons. Neuron 1:105-116.
10. Evan GI, Lewis GK, Ramsay G, Bishop JM (1985) Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol Cell Biol 5:3610-3616.
11. Fan J, Raper JA (1995) Localized collapsing cues can steer growth cones without inducing their full collapse. Neuron 14:263-274.
12. Flanagan JG, Leder P(1990) The kit ligand: a cell surface molecule altered in steel. Cell 63:185-194.
13. Flanagan JG, Cheng HJ, Feldheim DA, Lu Q, Hattori M, Vanderhaeghen P (2000) Alkaline phosphatase fusions of ligands or receptors as in situ probes for staining of cells, tissues and embryos. Methods Enzymol 327:17-35.
14. Fujii T, Nakao F, Shibata Y, Shioi G, Kodama E, Fujisawa H, Takagi S (2002) Caenorhabditis elegans PlexinA, PLX-1, interacts with transmembrane semaphorins and regulates epidermal morphogenesis. Development 129:2053-2063.
15. Giger RJ, Cloutier JF, Sahay A, Prinjha RK, Levengood DV, Moore SE, Pickering S, Simmons D, Rastan S, Walsh FS, Kolodkin AL, Ginty DD, Geppert M (2000) Neuropilin-2 is required in vivo for selective axon guidance responses to secreted semaphorins. Neuron 25:29-41.
16. Gu C, Yoshida Y, Livet J, Reimert DV, Mann F, Merte J, Henderson CE, Jessell TM, Kolodkin AL, Ginty DD (2005) Semaphorins 3E and plexin-D1 control vascular pattern independently of neuropilins. Science 307:265-268.
17. He Z, Tessier-Lavigne M (1997) Neuropilin is a receptor for the axonal chemorepellent semaphorin III. Cell 90:739-751.
18. Kameyama T, Murakami Y, Suto F, Kawakami A, Takagi S, Hirata T, Fujisawa H (1996a) Identification of plexin family molecules in mice. Biochem Biophys Res Commun 226:396-402.
19. Kameyama T, Murakami Y, Suto F, Kawakami A, Takagi S, Hirata T, Fujisawa H (1996b) Identification of a neuronal cell surface molecule, plexin, in mice. Biochem Biophys Res Commun 226:524-529.
20. Katoh K, Takahashi Y, Hayashi S, Kondoh H (1987) Improved mammalian vectors for high expression of G418 resistance. Cell Struct Funct 12:575-580.
21. Kawakami A, Kitsukawa T, Takagi S, Fujisawa H (1996) Developmentally regulated expression of a cell surface protein, neuropilin, in the mouse nervous system. J Neurobiol 29:1-17.
22. Kawasaki T, Bekku Y, Suto F, Kitsukawa T, Taniguchi M, Nagatsu I, Nagatsu T, Itoh K, Yagi T, Fujisawa H (2002) Requirement of neuropilin-1-mediated Sema3A signals in patterning of the sympathetic nervous system. Development 129:671-680.
23. Kikuchi K, Ishida H, Kimura T (1997) Molecular cloning of a novel member of semaphorin family genes, semaphorin Z. Mol Brain Res 51:229-237.
24. Kitsukawa T, Shimizu M, Sanbo M, Hirata T, Taniguchi M, Bekku Y, Yagi T, Fujisawa H (1997) Neuropilin-semaphorin III/D-mediated chemorepulsive signals play a crucial role in peripheral nerve projection in mice. Neuron 19:995-1005.
25. Kolodkin AL, Levengood DV, Rowe EG, Tai Y-T, Giger RJ, Ginty DD (1997) Neuropilin is a semaphorin III receptor. Cell 90:753-762.
26. Leighton PA, Mitchell KJ, Goodrich LV, Lu X, Pinson K, Scherz P, Skarnes WC, Tessier-Lavigne M (2001) Defining brain wiring patterns and mechanisms through gene trapping in mice. Nature 410:174-179.
27. Luo Y, Raible D, Raper JA (1993) Collapsin: a protein in brain that induces the collapse and paralysis of neuronal growth cones. Cell 75:217-227.
28. Maestrini E, Tamagnone L, Longati P, Cremona O, Gulisano M, Bione S, Tamanini F, Neel BG, Toniole D, Comoglio PM (1996) A family of transmembrane proteins with homology to the MET-hepatocyte growth factor receptor. Proc Natl Acad Sci USA 93:674-678.
29. Miyashita T, Yeo SY, Hirate Y, Segawa H, Wada H, Little MH, Yamada T, Takahashi N, Okamoto H (2004) PlexinA4 is necessary as a downstream target of Islet2 to mediate Slit signaling for promotion of sensory axon branching. Development 131:3705-3715.
30. Murakami Y, Suto F, Shimizu M, Shinoda T, Kameyama T, Fujisawa H (2001) Differential expression of plexin-A subfamily members in the mouse nervous system. Dev Dyn 220:246-258.
31. Nakamura F, Tanaka M, Takahashi T, Kalb RG, Strittmatter SM (1998) Neuropilin-1 extracellular domains mediate semaphorin D/III-induced growth cone collapse. Neuron 21:1093-1100.
32. Püschel AW, Adams RH, Betz H (1995) Murine semaphorin D/collapsing is a member of a diverse gene family and creates domains inhibitory for axonal extension. Neuron 14:941-948.
33. Sahay A, Molliver ME, Ginty DD, Kolodkin AL (2003) Semaphorin 3F is critical for development of limbic system circuitry and is required in neurons for selective CNS axon guidance events. J Neurosci 23:6671-6680.
34. Semaphorin Nomenclature Committee (1999) Unified nomenclature for the semaphorins/collapsins. Cell 97:551-552.
35. Suto F, Murakami Y, Nakamura F, Goshima Y, Fujisawa H (2003) Identification and characterization of a novel mouse plexin, plexin-A4. Mech Dev 120:385-396.
36. Takahashi T, Fournier A, Nakamura F, Wang LH, Murakami Y, Kalb RG, Fujisawa H, Strittmatter SM (1999) Plexin-Neuropilin-1 complexes form functional semaphorin-3A receptors. Cell 99:59-69.
37. Takashima S, Kitakaze M, Asakura M, Asanuma H, Sanada S, Tashiro F, Niwa H, Miyazaki J, Hirota S, Kitamura Y, Kitsukawa T, Fujisawa H, Klagsbrun M, Hori M (2002) Targeting of both mouse neuropilin-1 and neuropilin-2 genes severely impairs developmental yolk sac and embryonic angiogenesis. Proc Natl Acad Sci USA 99:3657-3662.
38. Tamagnone L, Artigiani S, Chen H, He Z, Ming G-L, Song H-J, Chédotal A, Winberg ML, Goodman CS, Poo M-M, Tessier-Lavigne M, Comoglio PM (1999) Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates. Cell 99:71-80.
39. Taniguchi M, Yuasa S, Fujisawa H, Naruse I, Saga S, Mishina M, Yagi T (1997) Disruption of semaphorin III/D gene causes severe abnormality in peripheral nerve projection. Neuron 19:519-530.
40. Toyofuku T, Zhang H, Kumanogoh A, Takegahara N, Suto F, Kamei J, Aoki K, Yabuki M, Hori M, Fujisawa H, Kikutani H (2004) Dual roles of Sema6D in cardiac morphogenesis through region-specific association of its receptor, Plexin-A1, with off-track and vascular endothelial growth factor receptor type 2. Genes Dev 18:435-447.
41. Ulupinar E, Datwani A, Behar O, Fujisawa H, Erzurumlu R (1999) Role of semaphorin III in the developing rodent trigeminal system. Mol Cell Neurosci 13:281-292.
42. Winberg ML, Noordermeer JN, Tamagnone L, Comoglio PM, Spriggs MK, Tessier-Lavigne M, Goodman CS (1998) Plexin A is a neuronal semaphorin receptor that controls axon guidance. Cell 95:903-916.
43. Woolsey TA, Van der Loos H (1970) The structural organization of layer IV in the somatosensory region (S1) of mouse cerebral cortex. Brain Res 17:205-242.
44. Xu X-M, Fisher DA, Zhou L, White FA, Ng S, Snider WD, Luo Y (2000) The transmembrane protein semaphorin 6A repels embryonic sympathetic axons. J Neurosci 20:2638-2648.