Npn-1 contributes to axon-axon interactions that differentially control sensory and motor innervation of the limb

PLoS Biology

Volumn 9, Issue 2, 2011, Pages

  Huettl, Rosa Eva ^a   Soellner, Heidi ^a   Bianchi, Elisa ^a   Novitch, Bennett G ^b   Huber, Andrea B ^a  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRE RECOMBINASE; NEUROPILIN 1; NEUROTROPHIN 3 RECEPTOR; PROTEIN TYROSINE KINASE A; SEMAPHORIN 3A; INTEGRASE;

ANIMAL EXPERIMENT; ARTICLE; CELL INTERACTION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; FASCICULATION; LIMB MOVEMENT; LOCOMOTION; MOTONEURON; MOUSE; NERVE FIBER; NERVE PLEXUS; NERVE PROJECTION; NONHUMAN; PERIKARYON; PROTEIN FUNCTION; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; SOMATOSENSORY CORTEX; ANIMAL; GENE DELETION; INNERVATION; LIMB; METABOLISM; PATHOLOGY; SENSORY RECEPTOR; TIME;

ANIMALS; AXONS; EXTREMITIES; FASCICULATION; GENE DELETION; INTEGRASES; MICE; MOTOR NEURONS; NEUROPILIN-1; SENSORY RECEPTOR CELLS; TIME FACTORS;

EID: 79952259443     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001020     Document Type: Article

References (39)

1. Tessier-Lavigne M, Goodman C. S, (1996) The molecular biology of axon guidance. Science 274: 1123-1133.
2. Dickson B. J, (2002) Molecular mechanisms of axon guidance. Science 298: 1959-1964.
3. Tran T. S, Kolodkin A. L, Bharadwaj R, (2007) Semaphorin regulation of cellular morphology. Annu Rev Cell Dev Biol 23: 263-292.
4. Sweeney L. B, Couto A, Chou Y. H, Berdnik D, Dickson B. J, et al. (2007) Temporal target restriction of olfactory receptor neurons by Semaphorin-1a/PlexinA-mediated axon-axon interactions. Neuron 53: 185-200.
5. Imai T, Yamazaki T, Kobayakawa R, Kobayakawa K, Abe T, et al. (2009) Pre-target axon sorting establishes the neural map topography. Science 325: 585-590.
6. Helmbacher F, Schneider-Maunoury S, Topilko P, Tiret L, Charnay P, (2000) Targeting of the EphA4 tyrosine kinase receptor affects dorsal/ventral pathfinding of limb motor axons. Development 127: 3313-3324.
7. Eberhart J, Swartz M. E, Koblar S. A, Pasquale E. B, Krull C. E, (2002) EphA4 constitutes a population-specific guidance cue for motor neurons. Dev Biol 247: 89-101.
8. Kania A, Jessell T. M, (2003) Topographic motor projections in the limb imposed by LIM homeodomain protein regulation of ephrin-A:EphA interactions. Neuron 38: 581-596.
9. Kramer E. R, Knott L, Su F, Dessaud E, Krull C. E, et al. (2006) Cooperation between GDNF/Ret and ephrinA/EphA4 signals for motor-axon pathway selection in the limb. Neuron 50: 35-47.
10. Huber A. B, Kania A, Tran T. S, Gu C, De Marco Garcia N, et al. (2005) Distinct roles for secreted semaphorin signaling in spinal motor axon guidance. Neuron 48: 949-964.
11. Luria V, Krawchuk D, Jessell T. M, Laufer E, Kania A, (2008) Specification of motor axon trajectory by ephrin-B:EphB signaling: symmetrical control of axonal patterning in the developing limb. Neuron 60: 1039-1053.
12. Tang J, Landmesser L, Rutishauser U, (1992) Polysialic acid influences specific pathfinding by avian motoneurons. Neuron 8: 1031-1044.
13. Tang J, Rutishauser U, Landmesser L, (1994) Polysialic acid regulates growth cone behavior during sorting of motor axons in the plexus region. Neuron 13: 405-414.
14. Gallarda B. W, Bonanomi D, Muller D, Brown A, Alaynick W. A, et al. (2008) Segregation of axial motor and sensory pathways via heterotypic trans-axonal signaling. Science 320: 233-236.
15. Landmesser L, Honig M. G, (1986) Altered sensory projections in the chick hindlimb following the early removal of motoneurons. Dev Biol 118: 511-531.
16. Wang G, Scott S. A, (1999) Independent development of sensory and motor innervation patterns in embryonic chich hindlimbs. Dev Biol 208: 324-336.
17. Gu C, Rodriguez E. R, Reimert D. V, Shu T, Fritzsch B, et al. (2003) Neuropilin-1 conveys semaphorin and VEGF signaling during neural and cardiovascular development. Dev Cell 5: 45-57.
18. Dessaud E, Yang L. L, Hill K, Cox B, Ulloa F, et al. (2007) Interpretation of the sonic hedgehog morphogen gradient by a temporal adaptation mechanism. Nature 450: 717-720.
19. Wichterle H, Lieberam I, Porter J. A, Jessell T. M, (2002) Directed differentiation of embryonic stem cells into motor neurons. Cell 1100: 385-397.
20. Arber S, Han B, Mendelsohn M, Smith M, Jessell T. M, et al. (1999) Requirement for the Homeobox gene Hb9 in the consolidation of motor neuron identity. Neuron 23: 659-674.
21. Pietri T, Eder O, Blanche M, Thiery J. P, Dufour S, (2003) The human tissue plasminogen activator-Cre mouse: a new tool for targeting specifically neural crest cells and their derivatives in vivo. Dev Biol 259: 176-187.
22. Srinivas S, Watanabe T, Lin C. S, William C. M, Tanabe Y, et al. (2001) Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol 1: 4.
23. Brockschnieder D, Pechmann Y, Sonnenberg-Riethmacher E, Riethmacher D, (2006) An improved mouse line for Cre-induced cell ablation due to diphtheria toxin A, expressed from the Rosa26 locus. Genesis 44: 322-327.
24. O'Donnell M, Chance R. K, Bashaw G. J, (2009) Axon growth and guidance: receptor regulation and signal transduction. Annu Rev Neurosci 32: 383-412.
25. Fekete D. M, Campero A. M, (2007) Axon guidance in the inner ear. Int J Dev Biol 51: 549-556.
26. Hjorth J, Key B, (2002) Development of axon pathways in the zebrafish central nervous system. Int J Dev Biol 46: 609-619.
27. Niquille M, Garel S, Mann F, Hornung J. P, Otsmane B, et al. (2009) Transient neuronal populations are required to guide callosal axons: a role for semaphorin 3C. PLoS Biol 7: e1000230 doi:10.1371/journal.pbio.1000230.
28. Pittman A. J, Law M. Y, Chien C. B, (2008) Pathfinding in a large vertebrate axon tract: isotypic interactions guide retinotectal axons at multiple choice points. Development 135: 2865-2871.
29. Wright D. E, White F. A, Gerfen R. W, Silos-Santiago I, Snider W. D, (1995) The guidance molecule semaphorin III is expressed in regions of spinal cord and periphery avoided by growing sensory axons. J Comp Neurol 361: 321-333.
30. Katsuki T, Ailani D, Hiramoto M, Hiromi Y, (2009) Intra-axonal patterning: intrinsic compartmentalization of the axonal membrane in Drosophila neurons. Neuron 64: 188-199.
31. Winckler B, Forscher P, Mellman I, (1999) A diffusion barrier maintains distribution of membrane proteins in polarized neurons. Nature 397: 698-701.
32. White F. A, Behar O, (2000) The development and subsequent elimination of aberrant peripheral axon projections in Semaphorin3A null mutant mice. Dev Biol 225: 79-86.
33. Haupt C, Kloos K, Faus-Kessler T, Huber A. B, (2010) Semaphorin 3A-Neuropilin-1 signaling regulates peripheral axon fasciculation and pathfinding but not developmental cell death patterns. Eur J Neurosci 31: 1164-1172.
34. Lin W, Sanchez H. B, Deerinck T, Morris J. K, Ellisman M, et al. (2000) Aberrant development of motor axons and neuromuscular synapses in erbB2-deficient mice. Proc Natl Acad Sci U S A 97: 1299-1304.
35. Moret F, Renaudot C, Bozon M, Castellani V, (2007) Semaphorin and neuropilin co-expression in motoneurons sets axon sensitivity to environmental semaphorin sources during motor axon pathfinding. Development 134: 4491-4501.
36. Geretti E, Shimizu A, Klagsbrun M, (2008) Neuropilin structure governs VEGF and semaphorin binding and regulates angiogenesis. Angiogenesis 11: 31-39.
37. Castellani V, (2002) The function of neuropilin/L1 complex. Adv Exp Med Biol 515: 91-102.
38. Honig M. G, Camilli S. J, Xue Q. S, (2002) Effects of L1 blockade on sensory axon outgrowth and pathfinding in the chick hindlimb. Dev Biol 243: 137-154.
39. Honig M. G, Rutishauser U. S, (1996) Changes in the segmental pattern of sensory neuron projections in the chick hindlimb under conditions of altered cell adhesion molecule function. Dev Biol 175: 325-337.