An autocrine Wnt5a-Ror signaling loop mediates sympathetic target innervation

Developmental Biology

Volumn 377, Issue 1, 2013, Pages 79-89

  Ryu, Yun Kyoung ^a   Collins, Sarah Ellen ^a   Ho, Hsin Yi Henry ^b   Zhao, Haiqing ^a   Kuruvilla, Rejji ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Autocrine Wnt signaling; Axon branching; Conditional mouse mutants; Sympathetic neural development

Indexed keywords

PROTEIN KINASE ROR; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG; WNT5A PROTEIN;

ANIMAL CELL; ARTICLE; AUTOCRINE EFFECT; CELL COMPARTMENTALIZATION; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; GENE DELETION; IN VIVO STUDY; MALE; MOUSE; NERVE CELL CULTURE; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SYMPATHETIC INNERVATION; SYMPATHETIC NERVE;

MUS;

EID: 84876317436     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2013.02.013     Document Type: Article

References (37)

1. Altar C.A., DiStefano P.S. Neurotrophin trafficking by anterograde transport. Trends Neurosci. 1998, 21(10):433-437.
2. Angers S., Moon R.T. Proximal events in Wnt signal transduction. Nat. Rev. Mol. Cell Biol. 2009, 10(7):468-477.
3. 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(3):e18373.
4. Bodmer D., Levine-Wilkinson S., Richmond A., Hirsh S., Kuruvilla R. Wnt5a mediates nerve growth factor-dependent axonal branching and growth in developing sympathetic neurons. J. Neurosci. 2009, 29(23):7569-7581.
5. Budnik V., Salinas P.C. Wnt signaling during synaptic development and plasticity. Curr. Opin. Neurobiol. 2011, 21(1):151-159.
6. Cervantes S., Yamaguchi T.P., Hebrok M. Wnt5a is essential for intestinal elongation in mice. Dev. Biol. 2009, 326(2):285-294.
7. Danielian P.S., Muccino D., Rowitch D.H., Michael S.K., McMahon A.P. Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase. Curr. Biol. 1998, 8(24):1323-1326.
8. Davis E.K., Zou Y., Ghosh A. Wnts acting through canonical and noncanonical signaling pathways exert opposite effects on hippocampal synapse formation. Neural Dev. 2008, 3:32.
9. Esler M. The 2009 Carl Ludwig Lecture: pathophysiology of the human sympathetic nervous system in cardiovascular diseases: the transition from mechanisms to medical management. J. Appl. Physiol. 2010, 108(2):227-237.
10. Gibson D.A., Ma L. Developmental regulation of axon branching in the vertebrate nervous system. Development 2011, 138(2):183-195.
11. Glebova N.O., Ginty D.D. Heterogeneous requirement of NGF for sympathetic target innervation in vivo. J. Neurosci. 2004, 24(3):743-751.
12. Glebova N.O., Ginty D.D. Growth and survival signals controlling sympathetic nervous system development. Annu. Rev. Neurosci. 2005, 28:191-222.
13. Goldstein D.S., Robertson D., Esler M., Straus S.E., Eisenhofer G. Dysautonomias: clinical disorders of the autonomic nervous system. Ann. Intern. Med. 2002, 137(9):753-763.
14. Gong S., Doughty M., Harbaugh C.R., Cummins A., Hatten M.E., Heintz N., Gerfen C.R. Targeting Cre recombinase to specific neuron populations with bacterial artificial chromosome constructs. J. Neurosci. 2007, 27(37):9817-9823.
15. Hall A.C., Lucas F.R., Salinas P.C. Axonal remodeling and synaptic differentiation in the cerebellum is regulated by WNT-7a signaling. Cell 2000, 100(5):525-535.
16. Hall A.K., Landis S.C. Early commitment of precursor cells from the rat superior cervical ganglion to neuronal or nonneuronal fates. Neuron 1991, 6(5):741-752.
17. He F., Xiong W., Yu X., Espinoza-Lewis R., Liu C., Gu S., Nishita M., Suzuki K., Yamada G., Minami Y., et al. Wnt5a regulates directional cell migration and cell proliferation via Ror2-mediated noncanonical pathway in mammalian palate development. Development 2008, 135(23):3871-3879.
18. Ho H.Y., Susman M.W., Bikoff J.B., Ryu Y.K., Jonas A.M., Hu L., Kuruvilla R., Greenberg M.E. Wnt5a-Ror-Dishevelled signaling constitutes a core developmental pathway that controls tissue morphogenesis. Proc. Natl. Acad. Sci. USA 2012, 109(11):4044-4051.
19. 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(21):5840-5848.
20. Kennedy T.E., Tessier-Lavigne M. Guidance and induction of branch formation in developing axons by target-derived diffusible factors. Curr. Opin. Neurobiol. 1995, 5(1):83-90.
21. Krylova O., Herreros J., Cleverley K.E., Ehler E., Henriquez J.P., Hughes S.M., Salinas P.C. WNT-3, expressed by motoneurons, regulates terminal arborization of neurotrophin-3-responsive spinal sensory neurons. Neuron 2002, 35(6):1043-1056.
22. 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(18):5873-5883.
23. Lindeberg J., Usoskin D., Bengtsson H., Gustafsson A., Kylberg A., Soderstrom S., Ebendal T. Transgenic expression of Cre recombinase from the tyrosine hydroxylase locus. Genesis 2004, 40(2):67-73.
24. Liu Y., Shi J., Lu C.C., Wang Z.B., Lyuksyutova A.I., Song X.J., Zou Y. Ryk-mediated Wnt repulsion regulates posterior-directed growth of corticospinal tract. Nat. Neurosci. 2005, 8(9):1151-1159.
25. Low P.A. Autonomic neuropathies. Curr. Opin. Neurol. 2002, 15(5):605-609.
26. Montcouquiol M., Crenshaw E.B., Kelley M.W. Noncanonical Wnt signaling and neural polarity. Annu. Rev. Neurosci. 2006, 29:363-386.
27. Nishita M., Enomoto M., Yamagata K., Minami Y. Cell/tissue-tropic functions of Wnt5a signaling in normal and cancer cells. Trends Cell Biol. 2010, 20(6):346-354.
28. Packard M., Koo E.S., Gorczyca M., Sharpe J., Cumberledge S., Budnik V. The Drosophila Wnt, wingless, provides an essential signal for pre- and post-synaptic differentiation. Cell 2002, 111(3):319-330.
29. Pattyn A., Morin X., Cremer H., Goridis C., Brunet J.F. The homeobox gene Phox2b is essential for the development of autonomic neural crest derivatives. Nature 1999, 399(6734):366-370.
30. Port F., Basler K. Wnt trafficking: new insights into Wnt maturation, secretion and spreading. Traffic 2010, 11(10):1265-1271.
31. Salinas P.C., Zou Y. Wnt signaling in neural circuit assembly. Annu. Rev. Neurosci. 2008, 31:339-358.
32. 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(2):177-191.
33. Varela-Nallar L., Alfaro I.E., Serrano F.G., Parodi J., Inestrosa N.C. Wingless-type family member 5A (Wnt-5a) stimulates synaptic differentiation and function of glutamatergic synapses. Proc. Natl. Acad. Sci. USA 2010, 107(49):21164-21169.
34. Veeman M.T., Axelrod J.D., Moon R.T. A second canon. Functions and mechanisms of beta-catenin-independent Wnt signaling. Dev. Cell 2003, 5(3):367-377.
35. Yamaguchi T.P., Bradley A., McMahon A.P., Jones S. A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development 1999, 126(6):1211-1223.
36. Yoshikawa S., McKinnon R.D., Kokel M., Thomas J.B. Wnt-mediated axon guidance via the Drosophila Derailed receptor. Nature 2003, 422(6932):583-588.
37. Zou Y., Lyuksyutova A.I. Morphogens as conserved axon guidance cues. Curr. Opin. Neurobiol. 2007, 17(1):22-28.