Sonic hedgehog is indirectly required for intraretinal axon pathfinding by regulating chemokine expression in the optic stalk

Development (Cambridge)

Volumn 139, Issue 14, 2012, Pages 2604-2613

  Hörndli, Cornelia Stacher ^a,b   Chien, Chi Bin ^a,b,c  

^a Department of Neurobiology and Anatomy ^*  (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF UTAH HEALTH SCIENCES CENTER   (United States)

Author keywords

Axon guidance; Cxcl12; Hh signaling; Shh; Tissue patterning; Zebrafish

Indexed keywords

CHEMOKINE; CXCL12A; PROTEIN PATCHED; PROTEIN PATCHED 2; SMOOTHENED PROTEIN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI1; TRANSCRIPTION FACTOR PAX2; UNCLASSIFIED DRUG;

ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EMBRYO PATTERN FORMATION; NERVE FIBER; NERVE FIBER GROWTH; NONHUMAN; OPTIC CHIASM; OPTIC DISK; OPTIC NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RETINA GANGLION CELL; SIGNAL TRANSDUCTION; ZEBRA FISH;

DANIO RERIO; ERINACEIDAE;

EID: 84863098669     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.077594     Document Type: Article

References (51)

1. Arthur, A., Shi, S., Zannettino, A. C. W., Fujii, N., Gronthos, S. and Koblar, S. A. (2009). Implanted adult human dental pulp stem cells induce endogenous axon guidance. Stem Cells 27, 2229-2237.
2. Barresi, M. J. F., Hutson, L. D., Chien, C.-B. and Karlstrom, R. O. (2005). Hedgehog regulated Slit expression determines commissure and glial cell position in the zebrafish forebrain. Development 132, 3643-3656.
3. Bourikas, D., Pekarik, V., Baeriswyl, T., Grunditz, A., Sadhu, R., Nardó, M. and Stoeckli, E. T. (2005). Sonic hedgehog guides commissural axons along the longitudinal axis of the spinal cord. Nat. Neurosci. 8, 297-304.
4. Briscoe, J. and Ericson, J. (1999). The specification of neuronal identity by graded Sonic Hedgehog signalling. Semin. Cell Dev. Biol. 10, 353-362.
5. Chalasani, S. H., Sabelko, K. A., Sunshine, M. J., Littman, D. R. and Raper, J. A. (2003). A chemokine, SDF-1, reduces the effectiveness of multiple axonal repellents and is required for normal axon pathfinding. J. Neurosci. 23, 1360-1371.
6. Chalasani, S. H., Sabol, A., Xu, H., Gyda, M. A., Rasband, K., Granato, M., Chien, C.-B. and Raper, J. A. (2007). Stromal cell-derived factor-1 antagonizes slit/robo signaling in vivo. J. Neurosci. 27, 973-980.
7. Charron, F., Stein, E., Jeong, J., McMahon, A. P. and Tessier-Lavigne, M. (2003). The morphogen sonic hedgehog is an axonal chemoattractant that collaborates with netrin-1 in midline axon guidance. Cell 113, 11-23.
8. Chen, W., Burgess, S. and Hopkins, N. (2001). Analysis of the zebrafish smoothened mutant reveals conserved and divergent functions of hedgehog activity. Development 128, 2385-2396.
9. Dakubo, G. D., Wang, Y. P., Mazerolle, C., Campsall, K., McMahon, A. P. and Wallace, V. A. (2003). Retinal ganglion cell-derived sonic hedgehog signaling is required for optic disc and stalk neuroepithelial cell development. Development 130, 2967-2980.
10. Dakubo, G. D., Beug, S. T., Mazerolle, C. J., Thurig, S., Wang, Y. and Wallace, V. A. (2008). Control of glial precursor cell development in the mouse optic nerve by sonic hedgehog from retinal ganglion cells. Brain Res. 1228, 27-42.
11. Deiner, M. S., Kennedy, T. E., Fazeli, A., Serafini, T., Tessier-Lavigne, M. and Sretavan, D. W. (1997). Netrin-1 and DCC mediate axon guidance locally at the optic disc: loss of function leads to optic nerve hypoplasia. Neuron 19, 575-589.
12. Domanitskaya, E., Wacker, A., Mauti, O., Baeriswyl, T., Esteve, P., Bovolenta, P. and Stoeckli, E. T. (2010). Sonic hedgehog guides post-crossing commissural axons both directly and indirectly by regulating Wnt activity. J. Neurosci. 30, 11167-11176.
13. Ekker, S. C., Ungar, A. R., Greenstein, P., von Kessler, D. P., Porter, J. A., Moon, R. T. and Beachy, P. A. (1995). Patterning activities of vertebrate hedgehog proteins in the developing eye and brain. Curr. Biol. 5, 944-955.
14. Ericson, J, Briscoe, J., Rashbass, P., van Heyningen, V. and Jessell, T. M. (1997). Graded sonic hedgehog signaling and the specification of cell fate in the ventral neural tube. Cold Spring Harb. Symp. Quant. Biol. 62, 451-466.
15. Fabre, P. J., Shimogori, T. and Charron, F. (2010). Segregation of ipsilateral retinal ganglion cell axons at the optic chiasm requires the Shh receptor Boc. J. Neurosci. 30, 266-275.
16. Gordon, L., Mansh, M., Kinsman, H. and Morris, A. R. (2010). Xenopus sonic hedgehog guides retinal axons along the optic tract. Dev. Dyn. 239, 2921-2932.
17. Hammond, K. L., Loynes, H. E., Folarin, A. A., Smith, J. and Whitfield, T. T. (2003). Hedgehog signalling is required for correct anteroposterior patterning of the zebrafish otic vesicle. Development 130, 1403-1417.
18. Ingham, P. W. and McMahon, A. P. (2001). Hedgehog signaling in animal development: paradigms and principles. Genes Dev. 15, 3059-3087.
19. Kay, J. N., Link, B. A. and Baier, H. (2005). Staggered cell-intrinsic timing of ath5 expression underlies the wave of ganglion cell neurogenesis in the zebrafish retina. Development 132, 2573-2585.
20. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B. and Schilling, T. F. (1995). Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253-310.
21. Knaut, H., Werz, C., Geisler, R., The Tübingen 2000 Screen Consortium and Nüsslein-Volhard, C. (2003). A zebrafish homologue of the chemokine receptor Cxcr4 is a germ-cell guidance receptor. Nature 421, 279-282.
22. Kolpak, A., Zhang, J. and Bao, Z.-Z. (2005). Sonic hedgehog has a dual effect on the growth of retinal ganglion axons depending on its concentration. J. Neurosci. 25, 3432-3441.
23. Kolpak, A. L., Jiang, J., Guo, D., Standley, C., Bellve, K., Fogarty, K. and Bao, Z.-Z. (2009). Negative guidance factor-induced macropinocytosis in the growth cone plays a critical role in repulsive axon turning. J. Neurosci. 29, 10488-10498.
24. Kwan, K. M., Fujimoto, E., Grabher, C., Mangum, B. D., Hardy, M. E., Campbell, D. S., Parant, J. M., Yost, H. J., Kanki, J. P. and Chien, C.-B. (2007). The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev. Dyn. 236, 3088-3099.
25. Laessing, U. and Stuermer, C. A. (1996). Spatiotemporal pattern of retinal ganglion cell differentiation revealed by the expression of neurolin in embryonic zebrafish. J. Neurobiol. 29, 65-74.
26. Langheinrich, U., Hennen, E., Stott, G. and Vacun, G. (2002). Zebrafish as a model organism for the identification and characterization of drugs and genes affecting p53 signaling. Curr. Biol. 12, 2023-2028.
27. Li, Q., Shirabe, K., Thisse, C., Thisse, B., Okamoto, H., Masai, I. and Kuwada, J. Y. (2005). Chemokine signaling guides axons within the retina in zebrafish. J. Neurosci. 25, 1711-1717.
28. Li, Z., Joseph, N. M. and Easter, S. S., Jr (2000). The morphogenesis of the zebrafish eye, including a fate map of the optic vesicle. Dev. Dyn. 218, 175-188.
29. Lieberam, I., Agalliu, D., Nagasawa, T., Ericson, J. and Jessell, T. M. (2005). A Cxcl12-CXCR4 chemokine signaling pathway defines the initial trajectory of mammalian motor axons. Neuron 47, 667-679.
30. Macdonald, R., Barth, K. A., Xu, Q., Holder, N., Mikkola, I. and Wilson, S. W. (1995). Midline signalling is required for Pax gene regulation and patterning of the eyes. Development 121, 3267-3278.
31. Macdonald, R., Scholes, J., Strähle, U., Brennan, C., Holder, N., Brand, M. and Wilson, S. W. (1997). The Pax protein Noi is required for commissural axon pathway formation in the rostral forebrain. Development 124, 2397-2408.
32. Neumann, C. J. and Nuesslein-Volhard, C. (2000). Patterning of the zebrafish retina by a wave of sonic hedgehog activity. Science 289, 2137-2139.
33. Okada, A., Charron, F., Morin, S., Shin, D. S., Wong, K., Fabre, P. J., Tessier-Lavigne, M. and McConnell, S. K. (2006). Boc is a receptor for sonic hedgehog in the guidance of commissural axons. Nature 444, 369-373.
34. Omenetti, A., Syn, W.-K., Jung, Y., Francis, H., Porrello, A., Witek, R. P., Choi, S. S., Yang, L., Mayo, M. J., Gershwin, M. E. et al. (2009). Repair-related activation of hedgehog signaling promotes cholangiocyte chemokine production. Hepatology 50, 518-527.
35. Park, K. W., Urness, L. D., Senchuk, M. M., Colvin, C. J., Wythe, J. D., Chien, C.-B. and Li, D. Y. (2005). Identification of new netrin family members in zebrafish: developmental expression of netrin 2 and netrin 4. Dev. Dyn. 234, 726-731.
36. Perron, M., Boy, S., Amato, M. A., Viczian, A., Koebernick, K., Pieler, T. and Harris, W. A. (2003). A novel function for Hedgehog signalling in retinal pigment epithelium differentiation. Development 130, 1565-1577.
37. Pittman, A. J., Law, M.-Y. and Chien, C.-B. (2008). Pathfinding in a large vertebrate axon tract: isotypic interactions guide retinotectal axons at multiple choice points. Development 135, 2865-2871.
38. Poulain, F. E., Gaynes, J. A., Stacher Hörndli, C., Law, M.-Y. and Chien, C.-B. (2010). Analyzing retinal axon guidance in zebrafish. Methods Cell Biol. 100, 3-26.
39. Sánchez-Camacho, C. and Bovolenta, P. (2008). Autonomous and non-autonomous Shh signalling mediate the in vivo growth and guidance of mouse retinal ganglion cell axons. Development 135, 3531-3541.
40. Schauerte, H. E., van Eeden, F. J., Fricke, C., Odenthal, J., Strähle, U. and Haffter, P. (1998). Sonic hedgehog is not required for the induction of medial floor plate cells in the zebrafish. Development 125, 2983-2993.
41. Thisse, C. and Thisse, B. (2008). High-resolution in situ hybridization to whole-mount zebrafish embryos. Nat. Protoc. 3, 59-69.
42. Trousse, F., Martí, E., Gruss, P., Torres, M. and Bovolenta, P. (2001). Control of retinal ganglion cell axon growth: a new role for Sonic hedgehog. Development 128, 3927-3936.
43. Valentin, G., Haas, P. and Gilmour, D. (2007). The chemokine SDF1a coordinates tissue migration through the spatially restricted activation of Cxcr7 and Cxcr4b. Curr. Biol. 17, 1026-1031.
44. Varga, Z. M., Amores, A., Lewis, K. E., Yan, Y. L., Postlethwait, J. H., Eisen, J. S. and Westerfield, M. (2001). Zebrafish smoothened functions in ventral neural tube specification and axon tract formation. Development 128, 3497-3509.
45. Wallace, V. A. and Raff, M. C. (1999). A role for Sonic hedgehog in axon-to-astrocyte signalling in the rodent optic nerve. Development 126, 2901-2909.
46. Wilson, B. D., Ii, M., Park, K. W., Suli, A., Sorensen, L. K., Larrieu-Lahargue, F., Urness, L. D., Suh, W., Asai, J., Kock, G. A. H. et al. (2006). Netrins promote developmental and therapeutic angiogenesis. Science 313, 640-644.
47. Xiang, Y., Li, Y., Zhang, Z., Cui, K., Wang, S., Yuan, X.-b., Wu, C.-P., Poo, M.-M. and Duan, S. (2002). Nerve growth cone guidance mediated by G protein-coupled receptors. Nat. Neurosci. 5, 843-848.
48. Yam, P. T., Langlois, S. D., Morin, S. and Charron, F. (2009). Sonic hedgehog guides axons through a noncanonical, Src-family-kinase-dependent signaling pathway. Neuron 62, 349-362.
49. Yamazaki, M., Nakamura, K., Mizukami, Y., Ii, M., Sasajima, J., Sugiyama, Y., Nishikawa, T., Nakano, Y., Yanagawa, N., Sato, K. et al. (2008). Sonic hedgehog derived from human pancreatic cancer cells augments angiogenic function of endothelial progenitor cells. Cancer Sci. 99, 1131-1138.
50. Yang, H., Xiang, J., Wang, N., Zhao, Y., Hyman, J., Li, S., Jiang Jin, Chen, J. K., Yang, Z. and Lin, S. (2009). Converse conformational control of smoothened activity by structurally related small molecules. J. Biol. Chem. 284, 20876-20884.
51. Yoon, J. W., Gilbertson, R., Iannaccone, S., Iannaccone, P. and Walterhouse, D. (2009). Defining a role for Sonic hedgehog pathway activation in desmoplastic medulloblastoma by identifying GLI1 target genes. Int. J. Cancer 124, 109-119.