Satoda M et al. (1995), Differential expression of two cell surface pro...

XB-ART-20313

J Neurosci 1995 Jan 01;151 Pt 2:942-55.

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Differential expression of two cell surface proteins, neuropilin and plexin, in Xenopus olfactory axon subclasses.

Satoda M , Takagi S , Ohta K , Hirata T , Fujisawa H .

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Immunohistochemistry by using monoclonal antibodies named A5 and B2, which specifically recognize cell surface proteins the neuropilin and the plexin, respectively, revealed that olfactory axons in Xenopus tadpoles were classified into several subgroups by virtue of the expression levels of these two cell surface molecules. The vomeronasal axons expressed the plexin but not the neuropilin. The plexin-positive and neuropilin-negative vomeronasal axons form a discrete fiber bundle, even after they joined with the principal olfactory axons. However, the principal olfactory axons were divided into at least two subclasses; the neuropilin-predominant axons which expressed high levels of the neuropilin and low levels of the plexin, and the plexin-predominant axons which expressed high levels of the plexin and low levels of the neuropilin. Within the olfactory nerve the pathways for these two principal olfactory axon subclasses were initially intermingled with each other, but were gradually segregated throughout their courses from the nose to the cerebrum. Eventually, the neuropilin-predominant and the plexin-predominant principal olfactory axon subclasses projected to specified glomeruli in topographically related regions within the main olfactory bulb. Neuroanatomical tracings of the olfactory projection also confirmed the gradual segregation of the pathways for the principal olfactory axons. These results allow us to speculate that both the neuropilin and the plexin are involved in axon interactions, and play roles in the organization of the precise patterns of the olfactory pathway and projection.

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Species referenced: Xenopus laevis
Genes referenced: nrp1 plxna1
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	Figure 1. A schematic representation of the fasciculation patterns of olfactory axons in Xenopus tadpoles at stage 55 (a ventral view of the left nasal chamber). The principal olfactory axons derived from different parts within the principal nasal chamber (PNC) are fasciculated into six major olfactory fiber bundles (OF& l-6): The axons derived from the rostrolateral, rostrocentral, and rostromedial parts of the chamber form the OFBl, OFB2, and OFB3, respectively. The axons from the caudolateral, caudocentral, and caudomedial parts of the chamber are fasciculated into the OFB6,OFB5, and OFB41 respectively. The OFBS is located dorsally to the other OFBs, and not visible by the ventral view. All OFBs are joined into the olfactory nerve (ON). The axons form the vomeronasal organ (IWO) are fasciculated into the vomeronasal nerve (VW) which runs along the ventral aspect of the olfactory nerve. CH, the choana; R, rostral; C, caudal; M, medial; L, lateral.

	Figure 3. Topographies of the olfactory projection in Xenopus tadpoles at stage 55 detected by selective labeling of the OFBs (see Fig. 1) with the lipophilic dye Dil. A, A dorsocaudal view of the left nasal chamber (outlined by dotted lines) after the retrograde labeling of the OFB4 with the dye. A caudomedial part of the principal nasal chamber becomes dye positive, indicating the origin for the OFB4 within the principal nasal epithelium. EN, the external naris. B, A schematic representation of the origins for each OFB within the principal nasal epithelium detected by the retrograde labeling of the OFBs with the dye (a dorsal view of the left nasal chamber). The numbers I-6 indicate the dye-positive areas after labeling the OFBs 1 to 6, respectively. VNO, the vomeronasal organ; EN, the external naris; ON, the olfactory nerve. R, rostral; C, caudal; M, medial; L, lateral. The axes in B also apply to A. C-H, Projections of the OFB 1 (C), OFE32 (D), OFB3 (E), OPB6 (F), OTB5 (G), and OPB4 (H) within the main olfactory bulb (ventral views of the left cerebrums). When the OPB2 was labeled with the dye, the vomeronasal nerve projected to the accessory olfactory bulb (an arrowhead) becomes dye positive (0). The top and the bottom of each figure are the rostra1 and the caudal, respectively. The left and right sides of each figure are the medial and the lateral, respectively. Scale bars: A, 500 pm; C, 500 pm for C-H.
	Figure 4. Immunofluorescent staining of the olfactory receptors and axons in a Xenopus tadpole at stage 55 with MAbB2 (A-D) and MAbAS (E). A, Almost all cells in the vomeronasal epithelium and fine fascicles of vomeronasal axons (small arrows) beneath the epithelium are positively stained with MAbB2. B, Bundles of the vomeronasal axons (large arrows) among the Bowman’s glands (asterisks) are positively stained with MAbB2. C, The vomeronasal nerve (a large arrow) is stained with MAbB2. Bundles of the principal olfactory axons (smd arrows) are also stained by MAbB2 in different degrees. Asterisks, the Bowman’s glands. D, Most cells in the principal olfactory epithelium and fine fascicles of principal olfactory axons (small arrows) beneath the epithelium are stained with MAbB2. E, An adjacent section to the one in C was stained with MAbAS. The vomeronasal nerve (a large arrow) is negative for MAbAS-immunostaining. Bundles of the principal olfactory axons (small arrows) are stained with MAbA5 in different degrees. Asterisk, the Bowman’s gland. Scale bars: A and D, 50 hrn; B, 200 pm for B, C, and E.

	Figure 6. Immunofluorescent staining of the main olfactory bulb and the accessory olfactory bulb with MAbAS in a Xenopus tadpole at stage 55. Adjacent two sections made at the levels of the main olfactory bulb (A,C) and the accessory olfactory bulb (BJ) were stained with MAbAS (A,@ and MAbB2 (CD). Rit4, ZM, and CL indicate the rostromedial, intermediate, and caudolateral glomerular groups, respectively (see Fig. 2 and the text). Dotted lines in A and C outline the IM glomerular groups. The IM glomerular group is strongly stained with both MAbAS and MAbB2 (A,C). Arrows in A and C indicate the vomeronasal nerve. Arrows in B and D indicate the accessory olfactory bulb. The top and the bottom of each figure are the dorsal and the ventral, respectively. The left and right sides of each figure are the medial and the lateral, respectively. Vertical lines in A and C indicate the middle of the cerebrum. Scale bar (in A), 50 pm for A-D.

	Figure 8. Identification of antigens for MAbAS and MAbB2 in the olfactory system of Xenopus tadpoles at stage 55 by immunoblot. The antiaens for MAbAS and MAbB2 were affinitv nurified from the olfactory- tissues, separated by SDS-PAGE (5% acrylamide gel), then transferred to nitrocellulose filters. The antigen for MAbA5 was detected by using a monoclonal antibody lG7 which is specific for the neuropilin (lane 2). The antigen for MAbB2 was detected by using a guinea pig anti-plexin antiserum (lane 3). Upper and Iower arrows indicate the positions for the plexin and the neuropilin, respectively. Lane I, molecular weight markers at 205 kDa and 116 kDa.
	Figure 9. A schematic representation ofthe model for the organization of the olfactory projection. NPI and PL indicate neuropilin-predominant and plexin-predominant principal olfactory receptors (PL) differentiated within the principal olfactory epithelium (POE), at early stages of development, respectively. Their axons arrive at appropriate positions within the main olfactory bulb (MOB). NP2, NP3 and PL2, PL3 indicate neuropilin-predominant and plexin-predominant receptors which differentiate at later stageso f development,a t random positions within the principal olfactory epithelium, respectively. Axons of these lately formed receptors choice appropriate preformed axons or axon bundles by virtue oftheir cell surface labels with the neuropilin or plexin, and then arrive at their correct termination sites within the main olfactory bulb. M, medial; L, lateral.