Neuronal Nogo-A regulates neurite fasciculation, branching and extension in the developing nervous system

Development

Volumn 137, Issue 15, 2010, Pages 2539-2550

  Petrinovic, Marija M ^a,b   Duncan, Carri S ^a,b   Bourikas, Dimitris ^a   Weinman, Oliver ^a,b   Montani, Laura ^a,b   Schroeter, Aileen ^a,b   Maerki, David ^a   Sommer, Lukas ^a   Stoeckli, Esther T ^a   Schwab, Martin E ^a,b  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b ETH ZURICH   (Switzerland)

Author keywords

Branching; Chick; Fasciculation; Mouse; Neurite outgrowth; Nogo A; Repulsion

Indexed keywords

NOGO A ANTIBODY; PROTEIN LINGO1; PROTEIN NGR; PROTEIN NOGO A; RECEPTOR; RHO KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRANCHING MORPHOGENESIS; CELL ADHESION; CELL ELONGATION; CHICK EMBRYO; DORSAL ROOT; EMBRYO; FORELIMB; HINDLIMB; INNERVATION; MOUSE; NERVE CELL; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; PERIPHERAL NERVOUS SYSTEM FUNCTION; PRIORITY JOURNAL; RAT; SPINAL GANGLION;

ANIMALS; AXONS; CHICK EMBRYO; GANGLIA, SPINAL; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MODELS, BIOLOGICAL; MYELIN PROTEINS; NERVOUS SYSTEM; NEURONS; RATS; RATS, WISTAR; RECOMBINATION, GENETIC; RHO-ASSOCIATED KINASES;

SPONDIAS PURPUREA;

EID: 77955753417     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.048371     Document Type: Article

References (49)

1. Aloy, E. M., Weinmann, O., Pot, C., Kasper, H., Dodd, D. A., Rulicke, T., Rossi, F. and Schwab, M. E. (2006). Synaptic destabilization by neuronal Nogo-A. Brain Cell Biol. 35, 137-156.
2. Bandtlow, C. and Dechant, G. (2004). From cell death to neuronal regeneration, effects of the p75 neurotrophin receptor depend on interactions with partner subunits. Sci. STKE 2004, pe24.
3. Bouquet, C., Soares, S., von Boxberg, Y., Ravaille-Veron, M., Propst, F. and Nothias, F. (2004). Microtubule-associated protein 1B controls directionality of growth cone migration and axonal branching in regeneration of adult dorsal root ganglia neurons. J. Neurosci. 24, 7204-7213.
4. Caroni, P. and Schwab, M. E. (1988). Antibody against myelin-associated inhibitor of neurite growth neutralizes nonpermissive substrate properties of CNS white matter. Neuron 1, 85-96.
5. Chen, M. S., Huber, A. B., van der Haar, M. E., Frank, M., Schnell, L., Spillmann, A. A., Christ, F. and Schwab, M. E. (2000). Nogo-A is a myelin-associated neurite outgrowth inhibitor and an antigen for monoclonal antibody IN-1. Nature 403, 434-439.
6. Chilton, J. K. (2006). Molecular mechanisms of axon guidance. Dev. Biol. 292, 13-24.
7. Dickson, B. J. (2002). Molecular mechanisms of axon guidance. Science 298, 1959-1964.
8. Dimou, L., Schnell, L., Montani, L., Duncan, C., Simonen, M., Schneider, R., Liebscher, T., Gullo, M. and Schwab, M. E. (2006). Nogo-A-deficient mice reveal strain-dependent differences in axonal regeneration. J. Neurosci. 26, 5591-5603.
9. Dodd, D. A., Niederoest, B., Bloechlinger, S., Dupuis, L., Loeffler, J. P. and Schwab, M. E. (2005). Nogo-A, -B, and -C are found on the cell surface and interact together in many different cell types. J. Biol. Chem. 280, 12494-12502.
10. Eberhart, J., Swartz, M., Koblar, S. A., Pasquale, E. B., Tanaka, H. and Krull, C. E. (2000). Expression of EphA4, ephrin-A2 and ephrin-A5 during axon outgrowth to the hindlimb indicates potential roles in pathfinding. Dev. Neurosci. 22, 237-250.
11. Fournier, A. E., Kalb, R. G. and Strittmatter, S. M. (2000). Rho GTPases and axonal growth cone collapse. Methods Enzymol. 325, 473-482.
12. Fournier, A. E., GrandPre, T. and Strittmatter, S. M. (2001). Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. Nature 409, 341-346.
13. Fournier, A. E., Takizawa, B. T. and Strittmatter, S. M. (2003). Rho kinase inhibition enhances axonal regeneration in the injured CNS. J. Neurosci. 23, 1416-1423.
14. Gonzenbach, R. R. and Schwab, M. E. (2008). Disinhibition of neurite growth to repair the injured adult CNS: focusing on Nogo. Cell. Mol. Life Sci. 65, 161-176.
15. Hamburger, V. and Hamilton, H. L. (1951). A series of normal stages in the development of the chick embryo. J. Morphol. 88, 49-92.
16. Huber, A. B., Weinmann, O., Brosamle, C., Oertle, T. and Schwab, M. E. (2002). Patterns of Nogo mRNA and protein expression in the developing and adult rat and after CNS lesions. J. Neurosci. 22, 3553-3567.
17. Huber, A. B., Kania, A., Tran, T. S., Gu, C., De Marco Garcia, N., Lieberam, I., Johnson, D., Jessell, T. M., Ginty, D. D. and Kolodkin, A. L. (2005). Distinct roles for secreted semaphorin signaling in spinal motor axon guidance. Neuron 48, 949-964.
18. Hunt, D., Coffin, R. S., Prinjha, R. K., Campbell, G. and Anderson, P. N. (2003). Nogo-A expression in the intact and injured nervous system. Mol. Cell. Neurosci. 24, 1083-1102.
19. Josephson, A., Widenfalk, J., Widmer, H. W., Olson, L. and Spenger, C. (2001). NOGO mRNA expression in adult and fetal human and rat nervous tissue and in weight drop injury. Exp. Neurol. 169, 319-328. (Pubitemid 32524426)
20. Kalil, K., Szebenyi, G. and Dent, E. W. (2000). Common mechanisms underlying growth cone guidance and axon branching. J. Neurobiol. 44, 145-158.
21. Kapfhammer, J. P. and Schwab, M. E. (1994). Inverse patterns of myelination and GAP-43 expression in the adult CNS: neurite growth inhibitors as regulators of neuronal plasticity? J. Comp. Neurol. 340, 194-206.
22. Landmesser, L., Dahm, L., Schultz, K. and Rutishauser, U. (1988). Distinct roles for adhesion molecules during innervation of embryonic chick muscle. Dev. Biol. 130, 645-670.
23. Landmesser, L., Dahm, L., Tang, J. C. and Rutishauser, U. (1990). Polysialic acid as a regulator of intramuscular nerve branching during embryonic development. Neuron 4, 655-667. (Pubitemid 20185082)
24. Liebscher, T., Schnell, L., Schnell, D., Scholl, J., Schneider, R., Gullo, M., Fouad, K., Mir, A., Rausch, M., Kindler, D. et al. (2005). Nogo-A antibody improves regeneration and locomotion of spinal cord-injured rats. Ann. Neurol. 58, 706-719.
25. Luo, Y., Raible, D. and Raper, J. A. (1993). Collapsin: a protein in brain that induces the collapse and paralysis of neuronal growth cones. Cell 75, 217-227.
26. Maina, F., Hilton, M. C., Ponzetto, C., Davies, A. M. and Klein, R. (1997). Met receptor signaling is required for sensory nerve development and HGF promotes axonal growth and survival of sensory neurons. Genes Dev. 11, 3341-3350.
27. McGee, A. W., Yang, Y., Fischer, Q. S., Daw, N. W. and Strittmatter, S. M. (2005). Experience-driven plasticity of visual cortex limited by myelin and Nogo receptor. Science 309, 2222-2226.
28. McLaughlin, T., Hindges, R., Yates, P. A. and O'Leary, D. D. (2003). Bifunctional action of ephrin-B1 as a repellent and attractant to control bidirectional branch extension in dorsal-ventral retinotopic mapping. Development 130, 2407-2418.
29. Mi, S., Lee, X., Shao, Z., Thill, G., Ji, B., Relton, J., Levesque, M., Allaire, N., Perrin, S., Sands, B. et al. (2004). LINGO-1 is a component of the Nogo-66 receptor/p75 signaling complex. Nat. Neurosci. 7, 221-228.
30. Milner, L. D., Rafuse, V. F. and Landmesser, L. T. (1998). Selective fasciculation and divergent pathfinding decisions of embryonic chick motor axons projecting to fast and slow muscle regions. J. Neurosci. 18, 3297-3313.
31. Mingorance-Le Meur, A., Zheng, B., Soriano, E. and del Rio, J. A. (2007). Involvement of the myelin-associated inhibitor Nogo-A in early cortical development and neuronal maturation. Cereb. Cortex 17, 2375-2386.
32. Montani, L., Gerrits, B., Gehrig, P., Kempf, A., Dimou, L., Wollscheid, B. and Schwab, M. E. (2009). Neuronal Nogo-A modulates growth cone motility via Rho-GTP/LIMK1/cofilin in the unlesioned adult nervous system. J. Biol. Chem. 284, 10793-10807.
33. Oertle, T., van der Haar, M. E., Bandtlow, C. E., Robeva, A., Burfeind, P., Buss, A., Huber, A. B., Simonen, M., Schnell, L., Brosamle, C. et al. (2003). Nogo-A inhibits neurite outgrowth and cell spreading with three discrete regions. J. Neurosci. 23, 5393-5406.
34. Perrin, F. E. and Stoeckli, E. T. (2000). Use of lipophilic dyes in studies of axonal pathfinding in vivo. Microsc. Res. Tech. 48, 25-31.
35. Pourquie, O., Coltey, M., Thomas, J. L. and Le Douarin, N. M. (1990). A widely distributed antigen developmentally regulated in the nervous system. Development 109, 743-752.
36. Rafuse, V. F. and Landmesser, L. T. (2000). The pattern of avian intramuscular nerve branching is determined by the innervating motoneuron and its level of polysialic acid. J. Neurosci. 20, 1056-1065.
37. Rutishauser, U. (2008). Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Nat. Rev. Neurosci. 9, 26-35.
38. Rutishauser, U., Gall, W. E. and Edelman, G. M. (1978). Adhesion among neural cells of the chick embryo. IV. Role of the cell surface molecule CAM in the formation of neurite bundles in cultures of spinal ganglia. J. Cell Biol. 79, 382-393.
39. Schaeren-Wiemers, N. and Gerfin-Moser, A. (1993). A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridization using digoxigenin-labelled cRNA probes. Histochemistry 100, 431-440. (Pubitemid 24049312)
40. Schwab, M. E. (2004). Nogo and axon regeneration. Curr. Opin. Neurobiol. 14, 118-124.
41. Simonen, M., Pedersen, V., Weinmann, O., Schnell, L., Buss, A., Ledermann, B., Christ, F., Sansig, G., van der Putten, H. and Schwab, M. E. (2003). Systemic deletion of the myelin-associated outgrowth inhibitor Nogo-A improves regenerative and plastic responses after spinal cord injury. Neuron 38, 201-211.
42. Tang, J., Landmesser, L. and Rutishauser, U. (1992). Polysialic acid influences specific pathfinding by avian motoneurons. Neuron 8, 1031-1044.
43. Tang, J., Rutishauser, U. and Landmesser, L. (1994). Polysialic acid regulates growth cone behavior during sorting of motor axons in the plexus region. Neuron 13, 405-414.
44. Tosney, K. W. and Landmesser, L. T. (1985). Development of the major pathways for neurite outgrowth in the chick hindlimb. Dev. Biol. 109, 193-214.
45. Van Vactor, D. (1998). Adhesion and signaling in axonal fasciculation. Curr. Opin. Neurobiol. 8, 80-86.
46. Wang, G. and Scott, S. A. (2000). The "waiting period" of sensory and motor axons in early chick hindlimb: its role in axon pathfinding and neuronal maturation. J. Neurosci. 20, 5358-5366.
47. Wang, K. H., Brose, K., Arnott, D., Kidd, T., Goodman, C. S., Henzel, W. and Tessier-Lavigne, M. (1999). Biochemical purification of a mammalian slit protein as a positive regulator of sensory axon elongation and branching. Cell 96, 771-784.
48. Wang, X., Chun, S. J., Treloar, H., Vartanian, T., Greer, C. A. and Strittmatter, S. M. (2002). Localization of Nogo-A and Nogo-66 receptor proteins at sites of axon-myelin and synaptic contact. J. Neurosci. 22, 5505-5515.
49. Yiu, G. and He, Z. (2006). Glial inhibition of CNS axon regeneration. Nat. Rev. Neurosci. 7, 617-627. (Pubitemid 44106744)