PlexinA2 limits recovery from corticospinal axotomy by mediating oligodendrocyte-derived Sema6A growth inhibition

Molecular and Cellular Neuroscience

Volumn 50, Issue 2, 2012, Pages 193-200

  Shim, Sang Ohk ^a   Cafferty, William B J ^a   Schmidt, Eric C ^a,d   Kim, Byung G ^a,b   Fujisawa, Hajime ^c   Strittmatter, Stephen M ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Ajou University School of Medicine   (South Korea)

^c NAGOYA UNIVERSITY   (Japan)

^d ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Axonal regeneration; Corticospinal; Myelin inhibition; Plexin; Recovery; Semaphorin; Spinal cord injury; Trauma

Indexed keywords

NGR1 PROTEIN; PLEXIN; PLEXIN A2; PROTEIN; SEMA6A PROTEIN; SYNAPTOPHYSIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CERVICAL SPINAL CORD; CONTROLLED STUDY; FEMALE; GRAY MATTER; GROWTH INHIBITION; IN VITRO STUDY; MALE; MEDULLARY PYRAMID; MOUSE; NERVE CELL INHIBITION; NERVE FIBER GROWTH; NERVE FIBER TRANSECTION; NERVE SPROUTING; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PYRAMIDAL TRACT; PYRAMIDOTOMY; SENSORY NERVE CELL; WILD TYPE;

ANIMALS; AXOTOMY; MICE; MICE, KNOCKOUT; NERVE REGENERATION; NERVE TISSUE PROTEINS; NEUROPSYCHOLOGICAL TESTS; OLIGODENDROGLIA; PYRAMIDAL TRACTS; RECEPTORS, CELL SURFACE; SEMAPHORINS;

MAMMALIA; MUS;

EID: 84861684557     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2012.04.007     Document Type: Article

References (38)

1. Atwal J.K., Pinkston-Gosse J., Syken J., Stawicki S., Wu Y., Shatz C., Tessier-Lavigne M. PirB is a functional receptor for myelin inhibitors of axonal regeneration. Science 2008, 322:967-970.
2. Cafferty W.B., Strittmatter S.M. The Nogo-Nogo receptor pathway limits a spectrum of adult CNS axonal growth. J. Neurosci. 2006, 26:12242-12250.
3. Cafferty W.B., Yang S.H., Duffy P.J., Li S., Strittmatter S.M. Functional axonal regeneration through astrocytic scar genetically modified to digest chondroitin sulfate proteoglycans. J. Neurosci. 2007, 27:2176-2185.
4. Cafferty W.B., Duffy P., Huebner E., Strittmatter S.M. MAG and OMgp synergize with Nogo-A to restrict axonal growth and neurological recovery after spinal cord trauma. J. Neurosci. 2010, 30:6825-6837.
5. Cohen R.I., Rottkamp D.M., Maric D., Barker J.L., Hudson L.D. A role for semaphorins and neuropilins in oligodendrocyte guidance. J. Neurochem. 2003, 85:1262-1278.
6. Coles C.H., Shen Y., Tenney A.P., Siebold C., Sutton G.C., Lu W., Gallagher J.T., Jones E.Y., Flanagan J.G., Aricescu A.R. Proteoglycan-specific molecular switch for RPTP{sigma} clustering and neuronal extension. Science 2011, 33:484-488.
7. De Winter F., Oudega M., Lankhorst A.J., Hamers F.P., Blits B., Ruitenberg M.J., Pasterkamp R.J., Gispen W.H., Verhaagen J. Injury-induced class 3 semaphorin expression in the rat spinal cord. Exp. Neurol. 2002, 175:61-75.
8. Fournier A.E., GrandPre T., Strittmatter S.M. Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. Nature 2001, 409:341-346.
9. Goldberg J.L., Vargas M.E., Wang J.T., Mandemakers W., Oster S.F., Sretavan D.W., Barres B.A. An oligodendrocyte lineage-specific semaphorin, Sema5A, inhibits axon growth by retinal ganglion cells. J. Neurosci. 2004, 24:4989-4999.
10. Haklai-Topper L., Mlechkovich G., Savariego D., Gokhman I., Yaron A. Cis interaction between Semaphorin6A and Plexin-A4 modulates the repulsive response to Sema6A. EMBO J. 2010, 29:2635-2645.
11. Harel N.Y., Strittmatter S.M. Can regenerating axons recapitulate developmental guidance during recovery from spinal cord injury?. Nat. Rev. Neurosci. 2006, 7:603-616.
12. Huebner E.A., Kim B.G., Duffy P.J., Brown R.H., Strittmatter S.M. A multi-domain fragment of nogo-a is a potent inhibitor of cortical axon regeneration via nogo receptor 1. J. Biol. Chem. 2011, 20:18026-18036.
13. Janssen B.J., Robinson R.A., Perez-Branguli F., Bell C.H., Mitchell K.J., Siebold C., Jones E.Y. Structural basis of semaphorin-plexin signalling. Nature 2010, 467:1118-1122.
14. Kaneko S., Iwanami A., Nakamura M., Kishino A., Kikuchi K., Shibata S., Okano H.J., Ikegami T., Moriya A., Konishi O., Nakayama C., Kumagai K., Kimura T., Sato Y., Goshima Y., Taniguchi M., Ito M., He Z., Toyama Y., Okano H. A selective Sema3A inhibitor enhances regenerative responses and functional recovery of the injured spinal cord. Nat. Med. 2006, 12:1380-1389.
15. Kerjan G., Dolan J., Haumaitre C., Schneider-Maunoury S., Fujisawa H., Mitchell K.J., Chedotal A. The transmembrane semaphorin Sema6A controls cerebellar granule cell migration. Nat. Neurosci. 2005, 8:1516-1524.
16. Kim J.E., Liu B.P., Park J.H., Strittmatter S.M. Nogo-66 receptor prevents raphespinal and rubrospinal axon regeneration and limits functional recovery from spinal cord injury. Neuron 2004, 44:439-451.
17. Leighton P.A., Mitchell K.J., Goodrich L.V., Lu X., Pinson K., Scherz P., Skarnes W.C., Tessier-Lavigne M. Defining brain wiring patterns and mechanisms through gene trapping in mice. Nature 2001, 410:174-179.
18. Lindholm T., Skold M.K., Suneson A., Carlstedt T., Cullheim S., Risling M. Semaphorin and neuropilin expression in motoneurons after intraspinal motoneuron axotomy. Neuroreport 2004, 15:649-654.
19. Liu B.P., Cafferty W.B., Budel S.O., Strittmatter S.M. Extracellular regulators of axonal growth in the adult central nervous system. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2006, 361:1593-1610.
20. Matsuoka R.L., Nguyen-Ba-Charvet K.T., Parray A., Badea T.C., Chedotal A., Kolodkin A.L. Transmembrane semaphorin signalling controls laminar stratification in the mammalian retina. Nature 2011, 470:259-263.
21. Mire E., Thomasset N., Jakeman L.B., Rougon G. Modulating Sema3A signal with a L1 mimetic peptide is not sufficient to promote motor recovery and axon regeneration after spinal cord injury. Mol. Cell. Neurosci. 2008, 37:222-235.
22. Nogi T., Yasui N., Mihara E., Matsunaga Y., Noda M., Yamashita N., Toyofuku T., Uchiyama S., Goshima Y., Kumanogoh A., Takagi J. Structural basis for semaphorin signalling through the plexin receptor. Nature 2010, 467:1123-1127.
23. Pasterkamp R.J., Giger R.J., Ruitenberg M.J., Holtmaat A.J., De Wit J., De Winter F., Verhaagen J. Expression of the gene encoding the chemorepellent semaphorin III is induced in the fibroblast component of neural scar tissue formed following injuries of adult but not neonatal CNS. Mol. Cell. Neurosci. 1999, 13:143-166.
24. Rohm B., Ottemeyer A., Lohrum M., Puschel A.W. Plexin/neuropilin complexes mediate repulsion by the axonal guidance signal semaphorin 3A. Mech. Dev. 2000, 93:95-104.
25. Runker A.E., Little G.E., Suto F., Fujisawa H., Mitchell K.J. Semaphorin-6A controls guidance of corticospinal tract axons at multiple choice points. Neural Dev. 2008, 3:34.
26. Shen Y., Tenney A.P., Busch S.A., Horn K.P., Cuascut F.X., Liu K., He Z., Silver J., Flanagan J.G. PTPsigma is a receptor for chondroitin sulfate proteoglycan, an inhibitor of neural regeneration. Science 2009, 326:592-596.
27. Suto F., Ito K., Uemura M., Shimizu M., Shinkawa Y., Sanbo M., Shinoda T., Tsuboi M., Takashima S., Yagi T., Fujisawa H. Plexin-a4 mediates axon-repulsive activities of both secreted and transmembrane semaphorins and plays roles in nerve fiber guidance. J. Neurosci. 2005, 25:3628-3637.
28. Suto F., Tsuboi M., Kamiya H., Mizuno H., Kiyama Y., Komai S., Shimizu M., Sanbo M., Yagi T., Hiromi Y., Chedotal A., Mitchell K.J., Manabe T., Fujisawa H. Interactions between plexin-A2, plexin-A4, and semaphorin 6A control lamina-restricted projection of hippocampal mossy fibers. Neuron 2007, 53:535-547.
29. Takahashi T., Strittmatter S.M. Plexina1 autoinhibition by the plexin sema domain. Neuron 2001, 29:429-439.
30. Takahashi T., Fournier A., Nakamura F., Wang L.H., Murakami Y., Kalb R.G., Fujisawa H., Strittmatter S.M. Plexin-neuropilin-1 complexes form functional semaphorin-3A receptors. Cell 1999, 99:59-69.
31. Tamagnone L., Artigiani S., Chen H., He Z., Ming G.-l., Song H.-j., Chedotal A., Winberg M.L., Goodman C.S., Poo M.-m. Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates. Cell 1999, 99:71-80.
32. Tessier-Lavigne M., Goodman C.S. The molecular biology of axon guidance. Science 1996, 274:1123-1133.
33. Thallmair M., Metz G.A., Z'Graggen W.J., Raineteau O., Kartje G.L., Schwab M.E. Neurite growth inhibitors restrict plasticity and functional recovery following corticospinal tract lesions. Nat. Neurosci. 1998, 1:124-131.
34. Tran T.S., Kolodkin A.L., Bharadwaj R. Semaphorin regulation of cellular morphology. Annu. Rev. Cell Dev. Biol. 2007, 23:263-292.
35. Venkatesh K., Chivatakarn O., Lee H., Joshi P.S., Kantor D.B., Newman B.A., Mage R., Rader C., Giger R.J. The Nogo-66 receptor homolog NgR2 is a sialic acid-dependent receptor selective for myelin-associated glycoprotein. J. Neurosci. 2005, 25:808-822.
36. Winberg M.L., Noordermeer J.N., Tamagnone L., Comoglio P.M., Spriggs M.K., Tessier-Lavigne M., Goodman C.S. Plexin A is a neuronal semaphorin receptor that controls axon guidance. Cell 1998, 95:903-916.
37. Xu X.M., Fisher D.A., Zhou L., White F.A., Ng S., Snider W.D., Luo Y. The transmembrane protein semaphorin 6A repels embryonic sympathetic axons. J. Neurosci. 2000, 20:2638-2648.
38. Zheng B., Atwal J., Ho C., Case L., He X.L., Garcia K.C., Steward O., Tessier-Lavigne M. Genetic deletion of the Nogo receptor does not reduce neurite inhibition in vitro or promote corticospinal tract regeneration in vivo. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:1205-1210.