Axon guidance and injury-lessons from Wnts and Wnt signaling

Current Opinion in Neurobiology

Volumn 27, Issue , 2014, Pages 232-240

  Onishi, Keisuke ^a   Hollis, Edmund ^a   Zou, Yimin ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FRIZZLED PROTEIN; PROTEIN TYROSINE KINASE; RECEPTOR TYROSINE KINASE RELATED TYROSINE KINASE; REGULATOR PROTEIN; UNCLASSIFIED DRUG; WNT PROTEIN; WNT5A PROTEIN; WNTS PROTEIN;

CELL POLARITY; GROWTH CONE; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NERVE GROWTH; NERVE PROJECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; SPINAL CORD INJURY; WNT SIGNALING PATHWAY; ANIMAL; METABOLISM; NERVE FIBER; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; AXONS; CELL POLARITY; SIGNAL TRANSDUCTION; SPINAL CORD INJURIES; WNT PROTEINS;

EID: 84902207778     PISSN: 09594388     EISSN: 18736882     Source Type: Journal    
DOI: 10.1016/j.conb.2014.05.005     Document Type: Review

References (54)

1. Lyuksyutova A.I., Lu C.C., Milanesio N., King L.A., Guo N., Wang Y., Nathans J., Tessier-Lavigne M., Zou Y. Anterior-posterior guidance of commissural axons by Wnt-frizzled signaling. Science 2003, 302:1984-1988.
2. Yoshikawa S., McKinnon R.D., Kokel M., Thomas J.B. Wnt-mediated axon guidance via the Drosophila Derailed receptor. Nature 2003, 422:583-588.
3. Zou Y. Wnt signaling in axon guidance. Trends Neurosci 2004, 27:528-532.
4. Liu Y., Shi J., Lu C.C., Wang Z.B., Lyuksyutova A.I., Song X., Zou Y. Ryk-mediated Wnt repulsion regulates posterior-directed growth of corticospinal tract. Nat Neurosci 2005, 8:1151-1159.
5. Dickson B.J. Wnts send axons up and down the spinal cord. Nat Neurosci 2005, 8:1130-1132.
6. Keeble T.R., Halford M.M., Seaman C., Kee N., Macheda M., Anderson R.B., Stacker S.A., Cooper H.M. The Wnt receptor Ryk is required for Wnt5a-mediated axon guidance on the contralateral side of the corpus callosum. J Neurosci 2006, 26:5840-5848.
7. Li L., Hutchins B.I., Kalil K. Wnt5a induces simultaneous cortical axon outgrowth and repulsive axon guidance through distinct signaling mechanisms. J Neurosci 2009, 29:5873-5883.
8. Li L., Hutchins B.I., Kalil K. Wnt5a induces simultaneous cortical axon outgrowth and repulsive turning through distinct signaling mechanisms. Sci Signal 2010, 3(pt2).
9. Fenstermaker A.G., Prasad A.A., Bechara A., Adolfs Y., Tissir F., Goffinet A., Zou Y., Pasterkamp R.J. Wnt/planar cell polarity signaling controls the anterior-posterior organization of monoaminergic axons in the brainstem. J Neurosci 2010, 30:16053-16064.
10. Blakely B.D., Bye C.R., Fernando C.V., Horne M.K., Macheda M.L., Stacker S.A., Arenas E., Parish C.L. Wnt5a regulates midbrain dopaminergic axon growth and guidance. PLoS ONE 2011, 6:e18373.
11. Pan C.L., Howell J.E., Clark S.G., Hilliard M., Cordes S., Bargmann C.I., Garriga G. Multiple Wnts and frizzled receptors regulate anteriorly directed cell and growth cone migrations in Caenorhabditis elegans. Dev Cell 2006, 10:367-377.
12. Hilliard M.A., Bargmann C.I. Wnt signals and frizzled activity orient anterior-posterior axon outgrowth in C. elegans. Dev Cell 2006, 10:379-390.
13. Prasad B.C., Clark S.G. Wnt signaling establishes anteroposterior neuronal polarity and requires retromer in C. elegans. Development 2006, 133:1757-1766.
14. Zou Y. Navigating the anterior-posterior axis with wnts. Neuron 2006, 49:787-789.
15. Schmitt A.M., Shi J., Wolf A.M., Lu C.C., King L.A., Zou Y. Wnt-Ryk signalling mediates medial-lateral retinotectal topographic mapping. Nature 2006, 439:31-37.
16. Sato M., Umetsu D., Murakami S., Yasugi T., Tabata T. DWnt4 regulates the dorsoventral specificity of retinal projections in the Drosophila melanogaster visual system. Nat Neurosci 2006, 9:67-75.
17. Hua Z.L., Smallwood P.M., Nathans J. Frizzled3 controls axonal development in distinct populations of cranial and spinal motor neurons. Elife 2013, 2:e01482.
18. Fantetti K.N., Zou Y., Fekete D.M. Wnts and Wnt inhibitors do not influence axon outgrowth from chicken statoacoustic ganglion neurons. Hear Res 2011, 278:86-95.
19. Zou Y., Lyuksyutova A.I. Morphogens as conserved axon guidance cues. Curr Opin Neurobiol 2007, 17:22-28.
20. Zallen J.A. Planar polarity and tissue morphogenesis. Cell 2007, 129:1051-1063.
21. Goodrich L.V., Strutt D. Principles of planar polarity in animal development. Development 2011, 138:1877-1892.
22. Shafer B., Onishi K., Lo C., Colakoglu G., Zou Y. Vangl2 promotes Wnt/planar cell polarity-like signaling by antagonizing Dvl1-mediated feedback inhibition in growth cone guidance. Dev Cell 2011, 20:177-191.
23. Onishi K., Shafer B., Lo C., Tissir F., Goffinet A.M., Zou Y. Antagonistic functions of Dishevelleds regulate Frizzled3 endocytosis via filopodia tips in Wnt-mediated growth cone guidance. J Neurosci 2013, 33:19071-19085.
24. Wolf A.M., Lyuksyutova A.I., Fenstermaker A.G., Shafer B., Lo C.G., Zou Y. Phosphatidylinositol-3-kinase-atypical protein kinase C signaling is required for Wnt attraction and anterior-posterior axon guidance. J Neurosci 2008, 28:3456-3467.
25. Goodrich L.V. The plane facts of PCP in the CNS. Neuron 2008, 60:9-16.
26. Shimizu K., Sato M., Tabata T. The Wnt5/planar cell polarity pathway regulates axonal development of the Drosophila mushroom body neuron. J Neurosci 2011, 31:4944-4954.
27. Mrkusich E.M., Flanagan D.J., Whitington P.M. The core planar cell polarity gene prickle interacts with flamingo to promote sensory axon advance in the Drosophila embryo. Dev Biol 2011, 358:224-230.
28. Zou Y. Does planar cell polarity signaling steer growth cones?. Curr Top Dev Biol 2012, 101:141-160.
29. Buck K.B., Zheng J.Q. Growth cone turning induced by direct local modification of microtubule dynamics. J Neurosci 2002, 22:9358-9367.
30. Wen Z., Han L., Bamburg J.R., Shim S., Ming G.L., Zheng J.Q. BMP gradients steer nerve growth cones by a balancing act of LIM kinase and Slingshot phosphatase on ADF/cofilin. J Cell Biol 2007, 178:107-119.
31. Witte H., Bradke F. The role of the cytoskeleton during neuronal polarization. Curr Opin Neurobiol 2008, 18:479-487.
32. Flynn K.C., Hellal F., Neukirchen D., Jacob S., Tahirovic S., Dupraz S., Stern S., Garvalov B.K., Gurniak C., Shaw A.E., et al. ADF/cofilin-mediated actin retrograde flow directs neurite formation in the developing brain. Neuron 2012, 76:1091-1107.
33. Hutchins B.I., Li L., Kalil K. Wnt/calcium signaling mediates axon growth and guidance in the developing corpus callosum. Dev Neurobiol 2010, 71:269-283.
34. Li L, Fothergill T., Hutchins B.I., Dent E.W., Kalil K. Wnt5a evokes cortical axon outgrowth and repulsive guidance by tau mediated reorganization of dynamic microtubules. Dev Neurobiol. 2013 Jul 2, [Epub ahead of print]. 10.1002/dneu.22102.
35. Macheda M.L., Sun W.W., Kugathasan K., Hogan B.M., Bower N.I., Halford M.M., Zhang Y.F., Jacques B.E., Lieschke G.J., Dabdoub A., Stacker S.A. The Wnt receptor Ryk plays a role in mammalian planar cell polarity signaling. J Biol Chem. 2012 Aug 24, 287(35):29312-29323. Epub 2012 Jul 6. 10.1074/jbc.M112.362681.
36. Andre P., Wang Q., Wang N., Gao B., Schilit A., Halford M.M., Stacker S.A., Zhang X., Yang Y. The Wnt coreceptor Ryk regulates Wnt/planar cell polarity by modulating the degradation of the core planar cell polarity component Vangl2. J Biol Chem 2012, 287:44518-44525.
37. Hollis E.R., Zou Y. Expression of the Wnt signaling system in central nervous system axon guidance and regeneration. Front Mol Neurosci 2012, 5:5.
38. Liu Y., Wang X., Lu C.C., Kerman R., Steward O., Xu X.M., Zou Y. Repulsive Wnt signaling inhibits axon regeneration after CNS injury. J Neurosci 2008, 28:8376-8382.
39. Fabes J., Anderson P., Brennan C., Bolsover S. Regeneration-enhancing effects of EphA4 blocking peptide following corticospinal tract injury in adult rat spinal cord. Eur J Neurosci 2007, 26:2496-2505.
40. Goldshmit Y., Galea M.P., Wise G., Bartlett P.F., Turnley A.M. Axonal regeneration and lack of astrocytic gliosis in EphA4-deficient mice. J Neurosci 2004, 24:10064-10073.
41. Löw K., Culbertson M., Bradke F., Tessier-Lavigne M., Tuszynski M.H. Netrin-1 is a novel myelin-associated inhibitor to axon growth. J Neurosci 2008, 28:1099-1108.
42. Pasterkamp R.J., Giger R.J., Ruitenberg M.J., Holtmaat A.J.G.D., 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.
43. Pasterkamp R.J., Verhaagen J. Semaphorins in axon regeneration: developmental guidance molecules gone wrong?. Philos Trans R Soc B: Biol Sci 2006, 361:1499-1511.
44. Fernandez-Martos C.M., Gonzalez-Fernandez C., Gonzalez P., Maqueda A., Arenas E., Rodriguez F.J. Differential expression of Wnts after spinal cord contusion injury in adult rats. PLoS One 2011, 6:e27000.
45. Gonzalez-Fernandez C., Fernandez-Martos C.M., Shields S., Arenas E., Rodriguez F.J. Wnts are expressed in the spinal cord of adult mice and are differentially induced after injury. J Neurotrauma 2013.
46. Miyashita T., Koda M., Kitajo K., Yamazaki M., Takahashi K., Kikuchi A., Yamashita T. Wnt-Ryk signaling mediates axon growth inhibition and limits functional recovery after spinal cord injury. J Neurotrauma 2009, 26:955-964.
47. Hollis E.R.2nd, Zou Y. Reinduced Wnt signaling limits regenerative potential of sensory axons in the spinal cord following conditioning lesion. Proc Natl Acad Sci USA 2012 Sep 4, 109(36):14663-14668. Epub 2012 Aug 17. 10.1073/pnas.1206218109.
48. McQuarrie I.G., Grafstein B. Axon outgrowth enhanced by a previous nerve injury. Arch Neurol 1973, 29:53-55.
49. Richardson P.M., Issa V.M. Peripheral injury enhances central regeneration of primary sensory neurones. Nature 1984, 309:791-793.
50. Li X., Li Y-h, Yu S., Liu Y. Upregulation of Ryk expression in rat dorsal root ganglia after peripheral nerve injury. Brain Res Bull 2008, 77:178-184.
51. Stam F.J., MacGillavry H.D., Armstrong N.J., de Gunst M.C., Zhang Y., van Kesteren R.E., Smit A.B., Verhaagen J. Identification of candidate transcriptional modulators involved in successful regeneration after nerve injury. Eur J Neurosci 2007, 25:3629-3637.
52. White B.D., Nathe R.J., Maris D.O., Nguyen N.K., Goodson J.M., Moon R.T., Horner P.J. Beta-catenin signaling increases in proliferating NG2+ progenitors and astrocytes during post-traumatic gliogenesis in the adult brain. Stem Cells 2010, 28:297-307.
53. Fancy S.P.J., Baranzini S.E., Zhao C., Yuk D.-I., Irvine K.-A., Kaing S., Sanai N., Franklin R.J.M., Rowitch D.H. Dysregulation of the Wnt pathway inhibits timely myelination and remyelination in the mammalian CNS. Genes Dev 2009, 23:1571-1585.
54. Tury A., Tolentino K., Zou Y. Altered expression of atypical PKC and Ryk in the spinal cord of a mouse model of amyotrophic lateral sclerosis. Dev Neurobiol. 2013 Oct 7, [Epub ahead of print]. 10.1002/dneu.22137.