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First published online October 19, 2007
Journal of Experimental Biology 210, 3821-3829 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.007161

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Immunohistochemical characterization of a parapinopsin-containing photoreceptor cell involved in the ultraviolet/green discrimination in the pineal organ of the river lamprey Lethenteron japonicum

Emi Kawano-Yamashita^1,2, Akihisa Terakita^2,3,*, Mitsumasa Koyanagi², Yoshinori Shichida^3,4, Tadashi Oishi⁵ and Satoshi Tamotsu^1,*

¹ Graduate School of Humanities and Sciences, Nara Women's University, Nara 630-8506, Japan
² Department of Biology and Geosciences, Graduate School of Science, Osaka City University, Osaka 558-8585, Japan
³ Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Corporation, Kyoto 606-8502, Japan
⁴ Department of Biophysics, Graduate School of Science, Kyoto University, Kyoto 606-8502, Japan
⁵ Nara Saho College, Nara 630-8566, Japan

View larger version (13K): [in this window] [in a new window]   Fig. 1. RT-PCR analysis of lamprey parapinopsin and lamprey rhodopsin gene expression in the pineal organ (p), retina (r) and brain (b) of the lamprey. The lamprey parapinopsin gene is expressed only in the pineal organ, whereas the lamprey rhodopsin gene is expressed in both the pineal organ and the retina. GAPDH serves as an internal standard.

View larger version (92K): [in this window] [in a new window]   Fig. 2. Immunohistochemical localization of lamprey parapinopsin in the pineal organ. (A) Lamprey parapinopsin immunoreactivity is localized in the outer segment of the dorsal and peripheral photoreceptor cells of the pineal organ. A weak immunoreaction is observed in the cell bodies and the basal processes. (B) The lamprey parapinopsin immunoreactivity is localized in the pineal stalk. (C) In the parapineal organ, lamprey parapinopsin immunoreactivity is mainly localized in the dorsal region. (D) In control staining for lamprey parapinosin, no immunoreactivity was observed. l, lumen. Scale bars, 100 µm.

View larger version (97K): [in this window] [in a new window]   Fig. 3. Immunohistochemical localization of lamprey parapinopsin and lamprey rhodopsin in the pineal organ by confocal imaging. (A) Lamprey parapinopsin immunoreactivity (green) is localized in the dorsal and peripheral regions. (B) Lamprey rhodopsin immunoreactivity (magenta) is localized in the ventral and peripheral regions. (C) In the peripheral region, the photoreceptor cells contain either lamprey parapinopsin or lamprey rhodopsin (arrowheads). (D) Panel C at higher magnification. l, lumen; p, pineal organ; pp, parapineal organ. Scale bars, 100 µm.

View larger version (31K): [in this window] [in a new window]   Fig. 4. Comparison of the localization of lamprey parapinopsin-containing cells with that of lamprey rhodopsin-containing cells in the pineal organ. (A) Schematic drawing of the top view of the pineal organ. The horizontal lines show the position of the sections of B and C. (B) In the cross-section around the peripheral portion (about 200 µm rostrally from the centre), there are more lamprey parapinopsin-containing cells (green) than lamprey rhodopsin-containing cells (red). (C) In the cross-section around the central portion, there are fewer lamprey parapinopsin-containing cells (green) than lamprey rhodopsin-containing cells (red). There are more lamprey parapinopsin-containing cells in the peripheral portion than in the central portion. l, lumen; p, pineal organ; ps, pineal stalk. Scale bars, 100 µm.

View larger version (86K): [in this window] [in a new window]   Fig. 5. The basal processes of lamprey parapinopsin-containing cells. Lamprey parapinopsin-containing cells are connected with each other via the basal processes and form a neuropile over a wide area in the whole-mount specimen of the dorsal portion (arrowheads in B). Inset in A shows dye coupling found in the UV-photoreceptor cells. B is a high magnification of the boxed region in A. Scale bars, 50 µm.

View larger version (124K): [in this window] [in a new window]   Fig. 6. Light micrograph (A) and electron micrographs (B–E) of pineal photoreceptor cells. (A) Pineal photoreceptor cells exist in the dorsal (arrowheads) and ventral region (arrows). (B) The outer segment of lamprey parapinopsin-containing cells (electron dense) is in the dorsal region. It is similar in shape to that of cone-type photoreceptor cells. (C) The outer segment of pineal photoreceptor cells, which is lamprey parapinopsin immunonegative (electron lucent), is in the ventral region. (D,E) Synaptic ribbons in the basal processes of dorsal (D, arrowheads) and ventral (E, arrowheads) photoreceptor cells. l, lumen. Scale bars, 10 µm in (A), 1 µm in (B,C) and 0.5 µm in (D,E).

View larger version (124K): [in this window] [in a new window]   Fig. 7. Ganglion cells in the pineal organ. Most of the ganglion cells are localized in the basal layer of the ventral and peripheral region. A few ganglion cells are localized in the dorsal region. l, lumen. Scale bar, 100 µm.

View larger version (114K): [in this window] [in a new window]   Fig. 8. Neural connection between lamprey parapinopsin-containing cells and ganglion cells by confocal imaging. The basal processes of lamprey parapinopsin-containing cells (green) are extended to and directly connect with ganglion cells (magenta) in the peripheral (A,B) and dorsal (C,D) regions. The single optical section (inset in A), which was taken by confocal laser-scanning microscopy, reveals that the varicosity-like structure and spherules of the lamprey parapinopsin immunoreactive process contact the ganglion cells. The arrows and arrowheads show the contact points. l, lumen. Scale bars, 30 µm.