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The Journal of Neuroscience, April 6, 2005, 25(14):3628-3637; doi:10.1523/JNEUROSCI.4480-04.2005

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Development/Plasticity/Repair
Plexin-A4 Mediates Axon-Repulsive Activities of Both Secreted and Transmembrane Semaphorins and Plays Roles in Nerve Fiber Guidance

Fumikazu Suto,^1 * Keisuke Ito,^2 * Masato Uemura,³ Masayuki Shimizu,⁴ Yutaka Shinkawa,⁵ Makoto Sanbo,⁷ Tomoyasu Shinoda,⁵ Miu Tsuboi,⁵ Seiji Takashima,⁸ Takeshi Yagi,⁹ and Hajime Fujisawa⁶

Divisions of ¹Developmental Genetics and ²Brain Function, National Institute of Genetics, Mishima 411-8540, Japan, ³Laboratory for Cell Adhesion and Tissue Patterning, Center for Developmental Biology, The Institute of Physical and Chemical Research (RIKEN), Kobe 650-0047, Japan, ⁴Division of Cellular Interactions, Institute of Molecular Embryology and Genetics, Kumamoto University, Kumamoto 860-0811, Japan, ⁵Group of Developmental Neurobiology and ⁶The 21st Century COE Program, Division of Biological Science, Nagoya University Graduate School of Science, Chikusa-ku, Nagoya 464-8602, Japan, ⁷Laboratory of Neurobiology and Behavioral Genetics, National Institute for Physiological Science, Myodaiji, Okazaki 444-8585, Japan, ⁸Division of Cardiology, Department of Internal Medicine and Therapeutics, Osaka University Graduate School of Medicine, Suita 565-0871, Japan, and ⁹KOKORO Biology Group, Laboratories for Integrated Biology, Graduate School of Frontier Biosciences, Osaka University, Suita 565-0871, Japan

It has been proposed that four members of the plexin A subfamily (plexin-As; plexin-A1, -A2, -A3, and -A4) and two neuropilins (neuropilin-1 and neuropilin-2) form complexes and serve as receptors for class 3 secreted semaphorins (Semas), potent neural chemorepellents. The roles of given plexin-As in semaphorin signaling and axon guidance, however, are mostly unknown. Here, to elucidate functions of plexin-A4 in semaphorin signaling and axon guidance events in vivo, we generated plexin-A4 null mutant mice by targeted disruption of the plexin-A4 gene. Plexin-A4 mutant mice were defective in the trajectory and projection of peripheral sensory axons and sympathetic ganglion (SG) axons and the formation of the anterior commissure and the barrels. The defects in peripheral sensory and SG axons were fundamentally related to those of neuropilin-1 or Sema3A mutant embryos reported but were more moderate than the phenotype in these mutants. The growth cone collapse assay showed that dorsal root ganglion axons and SG axons of plexin-A4 mutant embryos partially lost their responsiveness to Sema3A. These results suggest that plexin-A4 plays roles in the propagation of Sema3A activities and regulation of axon guidance and that other members of the plexin-A subfamily are also involved in the propagation of Sema3A activities. Plexin-A4-deficient SG axons did not lose their responsiveness to Sema3F, suggesting that plexin-A4 serves as a Sema3A-specific receptor, at least in SG axons. In addition, the present study showed that plexin-A4 bound class 6 transmembrane semaphorins, Sema6A and Sema6B, and mediated their axon-repulsive activities, independently of neuropilin-1. Our results imply that plexin-A4 mediates multiple semaphorin signals and regulates axon guidance in vivo.

Key words: axon repulsion; semaphorin; plexin; neuropilin; DRG axon; sympathetic axon; anterior commissure; barrel formation

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Received Nov 1, 2004; revised February 21, 2005; accepted February 24, 2005.

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