Distinct roles for secreted semaphorin signaling in spinal motor axon guidance

Neuron

Volumn 48, Issue 6, 2005, Pages 949-964

  Huber, Andrea B ^a,d   Kania, Artur ^b,c   Tran, Tracy S ^a   Gu, Chenghua ^a   De Marco Garcia, Natalia ^c   Lieberam, Ivo ^c   Johnson, Dontais ^a   Jessell, Thomas M ^c   Ginty, David D ^a   Kolodkin, Alex L ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^c Och Spine at New York Presbyterian Hospitals   (United States)

^d INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROPILIN 1; SEMAPHORIN; SEMAPHORIN 3A;

ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL GROWTH; CELL POPULATION; CONTROLLED STUDY; EMBRYO; FASCICULATION; MOUSE; NERVE FIBER; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; SIGNAL TRANSDUCTION; SPINAL CORD NERVE CELL;

ANIMALS; BODY PATTERNING; BRACHIAL PLEXUS; CELL DIFFERENTIATION; CHICK EMBRYO; FORELIMB; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GROWTH CONES; HINDLIMB; LIMB BUD; LUMBOSACRAL PLEXUS; MEMBRANE PROTEINS; MICE; MOTOR NEURONS; MUSCLE, SKELETAL; NERVE TISSUE PROTEINS; NEUROPILIN-1; NEUROPILIN-2; NEUROPILINS; SEMAPHORIN-3A; SEMAPHORINS; SIGNAL TRANSDUCTION; SPINAL CORD;

EID: 29144461035     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2005.12.003     Document Type: Article

References (71)

1. S. Arber, B. Han, M. Mendelsohn, M. Smith, T.M. Jessell, and S. Sockanathan Requirement for the Homeobox gene Hb9 in the consolidation of motor neuron identity Neuron 23 1999 659 674
2. O. Behar, J.A. Golden, H. Mashimo, F.J. Schoen, and M.C. Fishman Semaphorin III is needed for normal patterning and growth of nerves, bones, and heart Nature 383 1996 525 528
3. H. Chen, A. Chedotal, Z. He, C.S. Goodman, and M. Tessier-Lavigne Neuropilin-2, a novel member of the neuropilin family, is a high affinity receptor for the semaphorins Sema I and Sema IV but not Sema III Neuron 19 1997 547 559
4. H. Chen, A. Bagri, J.A. Zupicich, Y. Zou, E. Stoeckli, S.J. Pleasure, D.H. Lowenstein, W.C. Skarnes, A. Chedotal, and M. Tessier-Lavigne Neuropilin-2 regulates the development of selective cranial and sensory nerves and hippocampal mossy fiber projections Neuron 25 2000 43 56
5. H.J. Cheng, A. Bagri, A. Yaron, E. Stein, S.J. Pleasure, and M. Tessier-Lavigne Plexin-A3 mediates semaphorin signaling and regulates the development of hippocampal axonal projections Neuron 32 2001 249 263
6. S. Cohen, L. Funkelstein, J. Livet, G. Rougon, C.E. Henderson, V. Castellani, and F. Mann A semaphorin code defines subpopulations of spinal motor neurons during mouse development Eur. J. Neurosci. 21 2005 1767 1776
7. B.M. Davis, E. Frank, F.A. Johnson, and S.A. Scott Development of central projections of lumbosacral sensory neurons in the chick J. Comp. Neurol. 279 1989 556 566
8. B.J. Dickson Molecular Mechanisms of Axon Guidance Science 298 2002 1959 1963
9. J. Eberhart, M.E. Swartz, S.A. Koblar, E.B. Pasquale, and C.E. Krull EphA4 constitutes a population-specific guidance cue for motor neurons Dev. Biol. 247 2002 89 101
10. J. Eberhart, J. Barr, S. O'Connell, A. Flagg, M.E. Swartz, K.S. Cramer, K.W. Tosney, E.B. Pasquale, and C.E. Krull Ephrin-A5 exerts positive or inhibitory effects on distinct subsets of EphA4-positive motor neurons J. Neurosci. 24 2004 1070 1078
11. L. Feiner, A.M. Koppel, H. Kobayashi, and J.A. Raper Secreted chick semaphorins bind recombinant neuropilin with similar affinities but bind different subsets of neurons in situ Neuron 19 1997 539 545
12. G. Feng, M.B. Laskowski, D.A. Feldheim, H. Wang, R. Lewis, J. Frisen, J.G. Flanagan, and J.R. Sanes Roles for ephrins in positionally selective synaptogenesis between motor neurons and muscle fibers Neuron 25 2000 295 306
13. B.A. Ferguson Development of motor innervation of the chick following dorsal-ventral limb bud rotations J. Neurosci. 3 1983 1760 1762
14. A. Ghosh, and C.J. Shatz A role for subplate neurons in the patterning of connections from thalamus to neocortex Development 117 1993 1031 1047
15. R.J. Giger, J.F. Cloutier, A. Sahay, R.K. Prinjha, D.V. Levengood, S.E. Moore, S. Pickering, D. Simmons, S. Rastan, and F.S. Walsh Neuropilin-2 is required in vivo for selective axon guidance responses to secreted semaphorins Neuron 25 2000 29 41
16. Q. Gong, and M.T. Shipley Evidence that pioneer olfactory axons regulate telencephalon cell cycle kinetics to induce the formation of the olfactory bulb Neuron 14 1995 91 101
17. E.C. Greene The Anatomy of the Rat, Volume XXVII 1935 Hafner Press New York
18. C. Gu, E.R. Rodriguez, D.V. Reimert, T. Shu, B. Fritzsch, L.J. Richards, A.L. Kolodkin, and D.D. Ginty Neuropilin-1 conveys semaphorin and VEGF signaling during neural and cardiovascular development Dev. Cell 5 2003 45 57
19. G. Haase, E. Dessaud, A. Garces, B. de Bovis, M. Birling, P. Filippi, H. Schmalbruch, S. Arber, and O. deLapeyriere GDNF acts through PEA3 to regulate cell body positioning and muscle innervation of specific motor neuron pools Neuron 35 2002 893 905
20. V. Hamburger, and H.L. Hamilton A series of normal stages in the development of the chick embryo J. Morphol. 88 1951 49 92
21. M.G. Hanson, and L.T. Landmesser Normal patterns of spontaneous activity are required for correct motor axon guidance and the expression of specific guidance molecules Neuron 43 2004 687 701
22. S. He, and M. Tessier-Lavigne Molecular basis of axonal chemorepulsion: Neuropilin is a semaphorin/collapsin receptor Cell 90 1997 739 751
23. F. Helmbacher, S. Schneider-Maunoury, P. Topilko, L. Tiret, and P. Charnay Targeting of the EphA4 tyrosine kinase receptor affects dorsal/ventral pathfinding of limb motor axons Development 127 2000 3313 3324
24. F. Helmbacher, E. Dessaud, S. Arber, O. deLapeyriere, C.E. Henderson, R. Klein, and F. Maina Met signaling is required for recruitment of motor neurons to PEA3-positive motor pools Neuron 39 2003 767 777
25. M. Hollyday Motoneuron histogenesis and the development of limb innervation Curr. Top. Dev. Biol. 15 1980 181 215
26. M.G. Honig, C. Lance-Jones, and L. Landmesser The development of sensory projection patterns in embryonic chick hindlimb under experimental conditions Dev. Biol. 118 1986 532 548
27. A.B. Huber, A.L. Kolodkin, D.D. Ginty, and J.F. Cloutier Signaling at the growth cone: Ligand-receptor complexes and the control of axon growth and guidance Annu. Rev. Neurosci. 26 2003 509 563
28. T.M. Jessell Neuronal specification in the spinal cord: inductive signals and transcriptional codes Nat. Rev. Genet. 1 2000 20 29
29. A. Kania, and T.M. Jessell Topographic motor projections in the limb imposed by LIM homeodomain protein regulation of ephrin-A:EphA interactions Neuron 38 2003 581 596
30. A. Kania, R.L. Johnson, and T.M. Jessell Coordinate roles for LIM homeobox genes in directing the dorsoventral trajectory of motor axons in the vertebrate limb Cell 102 2000 161 173
31. T. Kitsukawa, M. Shimizu, M. Sanbo, T. Hirata, M. Taniguchi, Y. Bekku, T. Yagi, and H. Fujisawa Neuropilin-semaphorin III/D-mediated chemorepulsive signals play a crucial role in peripheral nerve projection in mice Neuron 19 1997 995 1005
32. A.L. Kolodkin, D.V. Levengood, E.G. Rowe, Y.T. Tai, R.J. Giger, and D.D. Ginty Neuropilin is a semaphorin III receptor Cell 90 1997 753 762
33. T.B. Kuhn, M.D. Brown, and J.R. Bamburg Rac1-dependent actin filament organization in growth cones is necessary for beta1-integrin-mediated advance but not for growth on poly-D-lysine J. Neurobiol. 37 1999 524 540
34. C. Lance-Jones, and L. Landmesser Motoneuron projection patterns in the chick hindlimb following early partial reversals of the spinal cord J. Physiol. 302 1980 581 602
35. C. Lance-Jones, and L. Landmesser Pathway selection by chick lumbosacral motoneurons during normal development Proc. R Soc. Lond. B Biol. Sci. 214 1981 1 18
36. L. Landmesser The development of motor projection patterns in the chick hind limb J. Physiol. 284 1978 391 414
37. L. Landmesser The distribution of motoneurons supplying chick hind limb muscles J. Physiol. 284 1978 371 414
38. L. Landmesser The acquisition of motoneuron subtype identity and motor circuit formation Int. J. Dev. Neurosci. 19 2001 175 182
39. L. Landmesser, and M.G. Honig Altered sensory projections in the chick hindlimb following the early removal of motoneurons Dev. Biol. 118 1986 511 531
40. L. Landmesser, L. Dahm, K. Schultz, and U. Rutishauser Distinct roles for adhesion molecules during innervation of embryonic chick muscle Dev. Biol. 119 1988 645 670
41. L. Landmesser, L. Dahm, J. Tang, and U. Rutishauser Polysialic acid as a regulator of intramuscular nerve branching during embryonic development Neuron 4 1990 655 667
42. I. Lieberam, D. Agalliu, T. Nagasawa, J. Ericson, and T.M. Jessell A Cxcl12-CXCR4 chemokine signaling pathway defines the initial trajectory of Mammalian motor axons Neuron 47 2005 667 679
43. J. Livet, M. Sigrist, S. Stroebel, V. De Paola, S.R. Price, C.E. Henderson, T.M. Jessell, and S. Arber ETS gene Pea3 controls the central position and terminal arborization of specific motor neuron pools Neuron 35 2002 877 892
44. Y. Murakami, F. Suto, M. Shimizu, T. Shinoda, T. Kameyama, and H. Fujisawa Differential expression of plexin-A subfamily members in the mouse nervous system Dev. Dyn. 220 2001 246 258
45. F. Nakamura, R.G. Kalb, and S.M. Strittmatter Molecular basis of semaphorin-mediated axon guidance J. Neurobiol. 44 2000 219 229
46. S.R. Price, N.V. De Marco Garcia, B. Ranscht, and T.M. Jessell Regulation of motor neuron pool sorting by differential expression of type II cadherins Cell 109 2002 205 216
47. P. Rakic Prenatal development of the visual system in Rhesus monkey Proc. R. Soc. Lond. B. Biol. Sci. 278 1977 245 260
48. M.J. Renzi, T.L. Wexler, and J.A. Raper Olfactory sensory axons expressing a dominant-negative semaphorin receptor enter the CNS early and overshoot their target Neuron 28 2000 437 447
49. A. Sahay, M.E. Molliver, D.D. Ginty, and A.L. Kolodkin 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
50. M. Sahin, P.L. Greer, M.Z. Lion, H. Poucher, J. Eberhart, S. Schmidt, T.M. Wright, S.M. Shamah, S. O'Connell, and C.W. Cowan Eph-dependent tyrosine phosphorylation of ephexin1 modulates growth cone collapse Neuron 46 2005 191 204
51. S. Sockanathan, and T.M. Jessell Motor neuron-derived retinoid signaling specifies the subtype identity of spinal motor neurons Cell 94 1998 503 514
52. S. Srinivas, T. Watanabe, C.S. Lin, C.M. William, Y. Tanabe, T.M. Jessell, and F. Costantini Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus BMC Dev. Biol. 1 2001 4
53. F. Suto, K. Ito, M. Uemura, M. Shimizu, Y. Shinkawa, M. Sanbo, T. Shinoda, M. Tsuboi, S. Takashima, T. Yagi, and H. Fujisawa Plexin-a4 mediates axon-repulsive activities of both secreted and transmembrane semaphorins and plays roles in nerve fiber guidance J. Neurosci. 25 2005 3628 3637
54. T. Takahashi, A. Fournier, F. Nakamura, L.H. Wang, Y. Murakami, R.G. Kalb, H. Fujisawa, and S.M. Strittmatter Plexin-neuropilin-1 complexes form functional semaphorin-3A receptors Cell 99 1999 59 69
55. J. Tang, L. Landmesser, and U. Rutishauser Polysialic acid influences specific pathfinding by avian motoneurons Neuron 8 1992 1031 1044
56. J. Tang, U. Rutishauser, and L. Landmesser Polysialic acid regulates growth cone behavior during sorting of motor axons in the plexus region Neuron 13 1994 405 414
57. M. Taniguchi, S. Yuasa, H. Fujisawa, I. Naruse, S. Saga, M. Mishina, and T. Yagi Disruption of semaphorin III/D gene causes severe abnormality in peripheral nerve projection Neuron 19 1997 519 530
58. M. Tessier-Lavigne, and C.S. Goodman The molecular biology of axon guidance Science 274 1996 1123 1133
59. K.W. Tosney, and L. Landmesser Development of the major pathways for neurite outgrowth in the chick hindlimb Dev. Biol. 109 1985 193 214
60. K.W. Tosney, and L. Landmesser Growth cone morphology and trajectory in the lumbosacral region of the chick embryo J. Neurosci. 5 1985 2345 2358
61. K.W. Tosney, and M.S. Hageman Different subsets of axonal guidance cues are essential for sensory neurite outgrowth to cutaneous and muscle targets in the dorsal ramus of the embryonic chick J. Exp. Zool. 251 1989 232 244
62. T. Tsuchida, M. Ensini, S.B. Morton, M. Baldassare, T. Edlund, T.M. Jessell, and S.L. Pfaff Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes Cell 79 1994 957 970
63. A. Varela-Echavarria, A. Tucker, A.W. Puschel, and S. Guthrie Motor axon subpopulations respond differentially to the chemorepellents netrin-1 and semaphorin D Neuron 18 1997 193 207
64. G. Wang, and S.A. Scott Independent development of sensory and motor innervation patterns in embryonic chick hindlimb Dev. Biol. 208 1999 324 336
65. G. Wang, and S.A. Scott The "waiting period" of sensory and motor axons in early chick hindlimb: its role in axon pathfinding and neuronal maturation J. Neurosci. 20 2000 5358 5366
66. Y. Watanabe, R. Toyoda, and H. Nakamura Navigation of trochlear motor axons along the midbrain-hindbrain boundary by neuropilin 2 Development 131 2004 681 692
67. V. Whitelaw, and M. Hollyday Neuroal pathway constraints in the motor innervation of the chick hindlimb following dorsoventral rotations of distal limb segments J. Neurosci. 3 1983 1226 1233
68. H. Wichterle, I. Lieberam, J.A. Porter, and T.M. Jessell Directed differentiation of embryonic stem cells into motor neurons Cell 1100 2002 385 397
69. D.E. Wright, F.A. White, R.W. Gerfen, I. Silos-Santiago, and W.D. Snider The guidance molecule semaphorin III is expressed in regions of spinal cord and periphery avoided by growing sensory axons J. Comp. Neurol. 361 1995 321 333
70. A. Yaron, P.H. Huang, H.J. Cheng, and M. Tessier-Lavigne Differential requirement for Plexin-A3 and -A4 in mediating responses of sensory and sympathetic neurons to distinct class 3 Semaphorins Neuron 45 2005 513 523
71. Y. Zou, E. Stoeckli, H. Chen, and M. Tessier-Lavigne Squeezing axons out of the gray matter: a role for slit and semaphorin proteins from midline and ventral spinal cord Cell 102 2000 363 375