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The Journal of Neuroscience, February 16, 2005, 25(7):1711-1717; doi:10.1523/JNEUROSCI.4393-04.2005

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Development/Plasticity/Repair
Chemokine Signaling Guides Axons within the Retina in Zebrafish

Qin Li,¹ Komei Shirabe,^1,2 Christine Thisse,³ Bernard Thisse,³ Hitoshi Okamoto,⁴ Ichiro Masai,⁵ and John Y. Kuwada¹

¹Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, Michigan 48109-1048, ²Department of Anatomy, Biology, and Medicine, Oita Medical University, Hasama-machi, Oita 879-5593, Japan, ³Institut de Genetique et de Biologie Moleculaire et Cellulaire, 67404 Illkirch, France, and ⁴Laboratory for Developmental Gene Regulation and ⁵Masai Initiative Research Unit, The Institute of Physical and Chemical Research (RIKEN), Wako-shi, Saitama 351-0198, Japan

Chemokines are a large family of secreted proteins that play an important role in the migration of leukocytes during hematopoiesis and inflammation. Chemokines and their receptors are also widely distributed in the CNS. Although recent investigations are beginning to elucidate chemokine function within the CNS, relatively little is known about the CNS function of this important class of molecules. To better appreciate the CNS function of chemokines, the role of signaling by stromal cell-derived factor-1 (SDF-1) through its receptor, chemokine (CXC motif) receptor 4 (CXCR4), was analyzed in zebrafish embryos. The SDF-1/CXCR4 expression pattern suggested that SDF-1/CXCR4 signaling was important for guiding retinal ganglion cell axons within the retina to the optic stalk to exit the retina. Antisense knockdown of the ligand and/or receptor and a genetic CXCR4 mutation both induced retinal axons to follow aberrant pathways within the retina. Furthermore, retinal axons deviated from their normal pathway and extended to cells ectopically expressing SDF-1 within the retina. These data suggest that chemokine signaling is both necessary and sufficient for directing retinal growth cones within the retina.

Key words: zebrafish; retinal ganglion cell; SDF-1; CXCR4; axonogenesis; axon

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Received Oct 21, 2004; revised December 29, 2004; accepted December 30, 2004.

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