Semaphorin 5A is a bifunctional axon guidance cue for axial motoneurons in vivo

Developmental Biology

Volumn 326, Issue 1, 2009, Pages 190-200

  Hilario, Jona D ^a   Rodino Klapac, Louise R ^a   Wang, Chunping ^a   Beattie, Christine E ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

Morpholinos; Motor axon guidance; Thrombospondin repeat domain; Zebrafish

Indexed keywords

PLEXIN; PLEXIN A3; RNA; SEMAPHORIN; SEMAPHORIN 5A; THROMBOSPONDIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; IN VIVO STUDY; MOTONEURON; MYOTOME; NERVE FIBER; NERVE GROWTH; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; ZEBRA FISH;

DANIO RERIO; MAMMALIA; RATTUS; VERTEBRATA;

EID: 58549112561     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2008.11.007     Document Type: Article

References (66)

1. Adams J.C., and Tucker R.P. The thrombospondin type 1 repeat (TSR) superfamily: diverse proteins with related roles in neuronal development. Dev. Dyn. 218 (2000) 280-299
2. Adams R.H., Betz H., and Puschel A.W. A novel class of murine semaphorins with homology to thrombospondin is differentially expressed during early embryogenesis. Mech. Dev. 57 (1996) 33-45
3. Artigiani S., Conrotto P., Fazzari P., Gilestro G.F., Barberis D., Giordano S., Comoglio P.M., and Tamagnone L. Plexin-B3 is a functional receptor for semaphorin 5A. EMBO Rep. 5 (2004) 710-714
4. Avnur Z., and Geiger B. Immunocytochemical localization of native chondroitin-sulfate in tissues and cultured cells using specific monoclonal antibody. Cell 38 (1984) 811-822
5. Beattie C.E. Control of motor axon guidance in the zebrafish embryo. Brain Res. Bull. 53 (2000) 489-500
6. Beattie C.E., and Eisen J.S. Notochord alters the permissiveness of myotome for pathfinding by an identified motoneuron in embryonic zebrafish. Development 124 (1997) 713-720
7. Beattie C.E., Melancon E., and Eisen J.S. Mutations in the stumpy gene reveal intermediate targets for zebrafish motor axons. Development 127 (2000) 2653-2662
8. Beattie C.E., Granato M., and Kuwada J.Y. Cellular, genetic and molecular mechanisms of axonal guidance in the zebrafish. Results Probl. Cell Differ. 40 (2002) 252-269
9. Birely J., Schneider V.A., Santana E., Dosch R., Wagner D.S., Mullins M.C., and Granato M. Genetic screens for genes controlling motor nerve-muscle development and interactions. Dev. Biol. 280 (2005) 162-176
10. Bink R.J., Habuchi H., Lele Z., Dolk E., Joore J., Rauch G.J., Geisler R., Wilson S.W., den Hertog J., Kimata K., and Zivkovic D. Heparan sulfate 6-O-sulfotransferase is essential for muscle development in zebrafish. J. Biol. Chem. 278 (2003) 31118-31127
11. Burstyn-Cohen T., Tzarfaty V., Frumkin A., Feinstein Y., Stoeckli E., and Klar A. F-Spondin is required for accurate pathfinding of commissural axons at the floor plate. Neuron 23 (1999) 233-246
12. Chen E., Stringer S.E., Rusch M.A., Selleck S.B., and Ekker S.C. A unique role for 6-O sulfation modification in zebrafish vascular development. Dev. Biol. 284 (2005) 364-376
13. Colamarino S.A., and Tessier-Lavigne M. The axonal chemoattractant Netrin-1 is also a chemorepellent for trochlear motor axons. Cell 81 (1995) 621-629
14. Eisen J.S., Myers P.Z., and Westerfield M. pathway selection by growth cones of identified motoneurones in live zebra fish embryos. Nature 320 (1986) 269-271
15. Eisen J.S., Pike S.H., and Debu B. The growth cones of identified motoneurons in embryonic zebrafish select appropriate pathways in the absence of specific cellular interactions. Neuron 2 (1989) 1097-1104
16. Falk J., Bechara A., Fiore R., Nawabi H., Zhou H., Hoyo-Becerra C., Bozon M., Rougon G., Grumet M., Puschel A.W., Sanes J.R., and Castellani V. Dual functional activity of semaphorin 3B is required for positioning the anterior commissure. Neuron 48 (2005) 63-75
17. Feldner J., Becker T., Goishi K., Schweitzer J., Lee P., Schachner M., Klagsbrun M., and Becker C.G. Neuropilin-1a is involved in trunk motor axon outgrowth in embryonic zebrafish. Dev. Dyn. 234 (2005) 535-549
18. Feldner J., Reimer M.M., Schweitzer J., Wendik B., Meyer D., Becker T., and Becker C.G. PlexinA3 restricts spinal exit points and branching of trunk motor nerves in embryonic zebrafish. J. Neurosci. 27 (2007) 4978-4983
19. Fiore R., Rahim B., Christoffels V.M., Moorman A.F., and Puschel A.W. Inactivation of the sema5a gene results in embryonic lethality and defective remodeling of the cranial vascular system. Mol. Cell. Biol. 25 (2005) 2310-2319
20. Flanagan-Steet H., Fox M.A., Meyer D., and Sanes J.R. Neuromuscular synapses can form in vivo by incorporation of initially aneural postsynaptic specializations. Development 132 (2005) 4471-4481
21. Fox M.A., and Sanes J.R. Synaptotagmin I and II are present in distinct subsets of central synapses. J. Comp. Neurol. 503 (2007) 280-296
22. Funato H., Saito-Nakazato Y., and Takahashi H. Axonal growth from the habenular nucleus along the neuromere boundary region of the diencephalon is regulated by semaphorin 3F and Netrin-1. Mol. Cell. Neurosci. 16 (2000) 206-220
23. He Z., Wang K.C., Koprivica V., Ming G., and Song H.J. Knowing how to navigate: mechanisms of semaphorin signaling in the nervous system. Sci. STKE 2002 (2002) RE1
24. Hutson L.D., and Chien C.B. Wiring the zebrafish: axon guidance and synaptogenesis. Curr. Opin. Neurobiol. 12 (2002) 87-92
25. Ito Y., Oinuma I., Katoh H., Kaibuchi K., and Negishi M. Sema4D/plexin-B1 activates GSK-3beta through R-Ras GAP activity, inducing growth cone collapse. EMBO Rep. 7 (2006) 704-709
26. Jin Z., Chau M.D., and Bao Z.Z. Sema3D, Sema3F, and Sema5A are expressed in overlapping and distinct patterns in chick embryonic heart. Dev. Dyn. 235 (2006) 163-169
27. Kantor D.B., Chivatakarn O., Peer K.L., Oster S.F., Inatani M., Hansen M.J., Flanagan J.G., Yamaguchi Y., Sretavan D.W., Giger R.J., and Kolodkin A.L. Semaphorin 5A is a bifunctional axon guidance cue regulated by heparan and chondroitin sulfate proteoglycans. Neuron 44 (2004) 961-975
28. Kim M.J., Liu I.H., Song Y., Lee J.A., Halfter W., Balice-Gordon R.J., Linney E., and Cole G.J. Agrin is required for posterior development and motor axon outgrowth and branching in embryonic zebrafish. Glycobiology 17 (2007) 231-247
29. Kimmel C.B., Ballard W.W., Kimmel S.R., Ullmann B., and Schilling T.F. Stages of embryonic development of the zebrafish. Dev. Dyn. 203 (1995) 253-310
30. Klostermann A., Lohrum M., Adams R.H., and Puschel A.W. The chemorepulsive activity of the axonal guidance signal semaphorin d requires dimerization. J. Biol. Chem. 273 (1998) 7326-7331
31. Kruger R.P., Lee J., Li W., and Guan K.L. Mapping netrin receptor binding reveals domains of Unc5 regulating its tyrosine phosphorylation. J. Neurosci. 24 (2004) 10826-10834
32. Livesey F.J. Netrins and netrin receptors. Cell Mol. Life Sci. 56 (1999) 62-68
33. Manitt C., and Kennedy T.E. Where the rubber meets the road: netrin expression and function in developing and adult nervous systems. Prog. Brain Res. 137 (2002) 425-442
34. Melancon E., Liu D.W., Westerfield M., and Eisen J.S. Pathfinding by identified zebrafish motoneurons in the absence of muscle pioneers. J. Neurosci. 17 (1997) 7796-7804
35. Nakamura F., Kalb R.G., and Strittmatter S.M. Molecular basis of semaphorin-mediated axon guidance. J. Neurobiol. 44 (2000) 219-229
36. Negishi M., Oinuma I., and Katoh H. Plexins: axon guidance and signal transduction. Cell. Mol. Life Sci. 62 (2005) 1363-1371
37. Neugebauer K.M., Emmett C.J., Venstrom K.A., and Reichardt L.F. Vitronectin and thrombospondin promote retinal neurite outgrowth: developmental regulation and role of integrins. Neuron 6 (1991) 345-358
38. Oinuma I., Ishikawa Y., Katoh H., and Negishi M. The semaphorin 4D receptor plexin-B1 is a GTPase activating protein for R-Ras. Science 305 (2004) 862-865
39. O'Shea K.S., Liu L.H., and Dixit V.M. Thrombospondin and a 140 kd fragment promote adhesion and neurite outgrowth from embryonic central and peripheral neurons and from PC12 Cells. Neuron 7 (1991) 231-237
40. Osterhout D.J., Frazier W.A., and Higgins D. Thrombospondin promotes process outgrowth in neurons from the peripheral and central nervous systems. Dev. Biol. 150 (1992) 256-265
41. Palaisa K.A., and Granato M. Analysis of zebrafish sidetracked mutants reveals a novel role for plexin a3 in intraspinal motor axon guidance. Development 134 (2007) 3251-3257
42. Pasterkamp R.J., and Kolodkin A.L. Semaphorin junction: making tracks toward neural connectivity. Curr. Opin. Neurobiol. 13 (2003) 79-89
43. Pineda D., Garcia B., Olmos J.L., Davila J.C., Real M.A., and Guirado S. Semaphorin5A expression in the developing chick telencephalon. Brain Res. Bull. 66 (2005) 436-440
44. Rauvala H., Huttunen H.J., Fages C., Kaksonen M., Kinnunen T., Imai S., Raulo E., and Kilpeläinen I. Heparin-binding proteins HB-GAM (Pleiotrophin) and amphoterin in the regulation of cell motility. Matrix Biol. 19 (2000) 377-387
45. Robu M.E., Larson J.D., Nasevicius A., Beiraghi S., Brenner C., Farber S.A., and Ekker S.C. P53 activation by knockdown technologies. PLoS Genet. 3 (2007) e78
46. Rodino-Klapac L.R., and Beattie C.E. Zebrafish topped is required for ventral motor axon guidance. Dev. Biol. 273 (2004) 308-320
47. Sahay A., Molliver M.E., Ginty D.D., and Kolodkin A.L. Semaphorin 3f is critical for development of limbic system circuitry and is required in neurons for selective CNS axon guidance events. J. Neurosci. 23 (2003) 6671-6680
48. Sato-Maeda M., Tawarayama H., Obinata M., Kuwada J.Y., and Shoji W. Sema3a1 guides spinal motor axons in a cell- and stage-specific manner in zebrafish. Development 133 (2006) 937-947
49. Sato-Maeda M., Obinata M., and Shoji W. Position fine-tuning of caudal primary motoneurons in the zebrafish spinal cord. Development 135 (2008) 323-332
50. Schneider V.A., and Granato M. Motor axon migration: a long way to go. Dev. Biol. 263 (2003) 1-11
51. Schneider V.A., and Granato M. The myotomal diwanka (lh3) glycosyltransferase and type XVIII collagen are critical for motor growth cone migration. Neuron 50 (2006) 683-695
52. Schweitzer J., Becker T., Lefebvre J., Granato M., Schachner M., and Becker C.G. Tenascin-C is involved in motor axon outgrowth in the trunk of developing zebrafish. Dev. Dyn. 234 (2005) 550-566
53. Semaphorin Nomenclature Committee. Unified nomenclature for the semaphorins/collapsins. Cell 97 (1999) 551-552
54. Serafini T., Colamarino S.A., Leonardo E.D., Wang H., Beddington R., Skarnes W.C., and Tessier-Lavigne M. Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system. Cell 87 (1996) 1001-1014
55. Shoji W., Isogai S., Sato-Maeda M., Obinata M., and Kuwada J. Semaphorin3a1 regulates angioblast migration and vascular development in zebrafish embryos. Development 130 (2003) 3227-3236
56. Tamagnone L., Artigiani S., Chen H., He Z., Ming G.I., Song H., Chedotal A., Winberg M.L., Goodman C.S., Poo M., Tessier-Lavigne M., and Comoglio P.M. Plexins are a large family of receptors for transmembrane, secreted, and gpi-anchored semaphorins in vertebrates. Cell 99 (1999) 71-80
57. Tanaka H., Maeda R., Shoji W., Wada H., Masai I., Shiraki T., Kobayashi M., Nakayama R., and Okamoto H. Novel mutations affecting axon guidance in zebrafish and a role for plexin signalling in the guidance of trigeminal and facial nerve axons. Development 134 (2007) 3259-3269
58. Thisse C., Thisse B., Schilling T.F., and Postlethwait J.H. Structure of the zebrafish snail1 gene and its expression in wild-type, spadetail and no tail mutant embryos. Development 119 (1993) 1203-1215
59. Toyofuku T., Zhang H., Kumanogoh A., Takegahara N., Suto F., Kamei J., Aoki K., Yabuki M., Hori M., Fujisawa H., and Kikutani H. 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 (2004) 435-447
60. Toyofuku T., Zhang H., Kumanogoh A., Takegahara N., Yabuki M., Harada K., Hori M., and Kikutani H. Guidance of myocardial patterning in cardiac development by Sema6D reverse signalling. Nat. Cell Biol. 6 (2004) 1204-1211
61. Trevarrow B., Marks D.L., and Kimmel C.B. Organization of hindbrain segments in the zebrafish embryo. Neuron 4 (1990) 669-679
62. Winberg M.L., Noordermeer J.N., Tamagnone L., Comoglio P.M., Spriggs M.K., Tessier-Lavigne M., and Goodman C.S. Plexin A is a neuronal semaphorin receptor that controls axon guidance. Cell 95 (1998) 903-916
63. Wong J.T., Wong S.T., and O'Connor T.P. Ectopic semaphorin-1a functions as an attractive guidance cue for developing peripheral neurons. Nat. Neurosci. 2 (1999) 798-803
64. Zeller J., and Granato M. The zebrafish diwanka gene controls an early step of motor growth cone migration. Development 126 (1999) 3461-3472
65. Zhang J., and Granato M. The zebrafish unplugged gene controls motor axon pathway selection. Development 127 (2000) 2099-2111
66. Zhang J., Lefebvre J.L., Zhao S., and Granato M. Zebrafish unplugged reveals a role for muscle-specific kinase homologs in axonal pathway choice. Nat. Neurosci. 7 (2004) 1303-1309