Summary
The pineal complex of the river lamprey, Lampetra japonica, was examined by means of immunocytochemistry with antisera against serotonin, the precursor of melatonin, and two photoreceptor proteins, rod-opsin (the apoprotein of the photopigment rhodopsin) and S-antigen. Serotonin-immunoreactive cells were observed in both the pineal and the parapineal organ. The proximal portion of the pineal organ (atrium) comprised numerous serotonin-immunoreactive cells displaying spherical somata. In the distal end-vesicle of the pineal organ, the serotonin-immunoreactive elements resembled photoreceptors in their size and shape. These cells projecting into the pineal lumen and toward the basal lamina were especially conspicuous in the ventral portion of the end-vesicle. In addition, single serotonin-immunoreactive nerve cells were found in this location. Retinal photoreceptors were never seen to contain immunoreactive serotonin; amacrine cells were the only retinal elements exhibiting serotonin immunoreaction. Strong S-antigen immunoreactivity was found in numerous photoreceptors located in the pineal end-vesicle. In contrast, the S-antigen immunoreactivity was weak in the spherical cells of the atrium. Thus, the pattern of S-antigen immunoreactivity was roughly opposite to that of serotonin. Similar findings were obtained in the parapineal organ. The rod-opsin immunoreaction was restricted to the outer segments of photoreceptors in the pineal end-vesicle and parapineal organ. No rodopsin immunoreactive outer segments occurred in the proximal portion of the atrium. Double immunostaining was employed to investigate whether immunoreactive opsin and serotonin are colocalized in one and the same cell. This approach revealed that (i) most of the rodopsin-immunoreactive outer segments in the end-vesicle belonged to serotonin-immunonegative photoreceptors; (ii) nearly all serotonin-immunoreactive cells in the end-vesicle bore short rod-opsin-immunoreactive outer segments protruding into the pineal lumen; and (iii) the spherical serotonin-immunoreactive cells in the pineal stalk lacked rod-opsin immunoreaction and an outer segment. These results support the concept that multiple cell lines of the photoreceptor type exist in the pineal complex at an early evolutionary stage.
Similar content being viewed by others
References
Brecha N (1983) A review of retinal neurotransmitters: Histochemical and biochemical studies. In: Emson PC (ed) Neurochemical anatomy. Raven Press, New York, pp 85–129
Cole WC, Youson JH (1982) Morphology of the pineal complex of the anadromous sea lamprey, Petromyzon marinus. Am J Anat 165:131–163
Collin J-P (1969) Contribution à l'étude de l'organe pinéal. De l'épiphyse sensorielle à la glande pinéale: Modalités de transformation et implication fonctionnelles. Ann Stat Biol Besse-en-Chandesse (Suppl) 1:1–359
Collin J-P (1971) Differentiation and regression of the cells of the sensory line in the epiphysis cerebri. In: Wolstenholme GEW, Knight J (eds) The pineal gland. Churchill-Livingstone, Edinburgh, London, pp 79–125
Collin J-P, Oksche A (1981) Structural and functional relationships in the nonmammalian pineal gland, Vol. 1: Anatomy and biochemistry. CRC Press, Boca Raton, pp 27–67
Deguchi T (1979) Circadian rhythm of serotonin N-acetyltransferase activity in organ culture of chicken pineal gland. Science 203:1245–1247
Deguchi T (1981) Rhodopsin-like photosensitivity of the isolated chicken pineal gland. Nature 290:706
Ekström P (1987) Photoreceptors and CSF-contacting neurons in the pineal organ of a teleost fish have direct axonal connections with the brain: An HRP-electron microscope study. J Neurosci 7:987–995
Ekström P, Korf HW (1985) Pineal neurons projecting to the brain of the rainbow trout, Salmo gairdneri Richardson (Teleostei). In vitro retrograde filling with horseradish peroxidase. Cell Tissue Res 240:693–700
Ekström P, Korf HW (1986a) Substance P-like immunoreactive neurons in the photosensory pineal organ of the rainbow trout, Salmo gairdneri Richardson (Teleostei). Cell Tissue Res 246:359–364
Ekström P, Korf HW (1986b) Putative cholinergic elements in the photosensory pineal organ and retina of a teleost, Phoxinus phoxinus L. (Cyprinidae). Cell Tissue Res 246:321–329
Ekström P, Meissl H (1990) Electron microscopic analysis of S-antigen and serotonin-immunoreactive neural and sensory elements in the photosensory pineal organ of the salmon. J Comp Neurol 292:73–82
Ekström P, Foster RG, Korf HW, Schalken JJ (1987) Antibodies against retinal photoreceptor-specific proteins reveal axonal projections from the photosensory pineal organ in teleosts. J Comp Neurol 265:25–33
Eldred WD, Nolte J (1981) Multiple classes of photoreceptors and neurons in the frontal organ of Rana pipiens. J Comp Neurol 203:269–295
Falcon J (1984) Identification et propriétes des cellules photoneuroendocrines de l'organe pinéal. Thesis, University of Poitiers
Guerlotte J, Falcon J, Voisin P, Collin J-P (1986) Indoles in the photoreceptor cells of the lamprey pineal complex. Ann d'Endocrinol 47:62–64
Hamm HE, Takahashi JS, Menaker M (1983) Light-induced decrease of serotonin N-acetlytransferase activity and melatonin in the chicken pineal gland and retina. Brain Res 266:287–293
Hartwig HG, Oksche A (1981) Photoneuroendocrine cells and systems: A concept revisited. In: Oksche A, Pévet P (eds) The pineal organ: photobiology-biochronometry-endocrinology. Elsevier, Amsterdam, pp 49–59
Joss JMP (1973) The pineal complex, melatonin, and color change in the lamprey Lampetra. Gen Comp Endocrinol 21:188–195
Joss JMP (1977) Hydroxyindole-O-methyltransferase (HIOMT) activity and the uptake of 3H-melatonin in the lamprey, Geotria australis Gray. Gen Comp Endocrinol 31:270–275
Korf HW (1974) Acetylcholinesterase-positive neurons in the pineal and parapineal organs of the rainbow trout, Salmo gairdneri (with special reference to the pineal tract). Cell Tissue Res 155:475–489
Korf HW (1976) Histological, histochemical and electron microscopical studies on the nervous appratus of the pineal organ in the tiger salamander, Ambystoma tigrinum. Cell Tissue Res 174:475–497
Korf HW (1986) Zur Frage photoneuroendokriner Zellen und Systeme: Vergleichende Untersuchungen am Pinealkomplex. Habilitationsschrift, Fachbereich Humanmedizin, Giessen
Korf HW, Ekström P (1987) Photoreceptor differentiation and neuronal organization of the pineal organ. In: Trentini GP, Gaetani C de, Pévet P (eds) Fundamentals and clinics in pineal research. Raven Press, New York, pp 35–47
Korf HW, Oksche A (1986a) Photoneuroendocrine aspects of the pineal gland: phylogeny and ontogeny. In: Gupta D, Reiter RJ (eds) The pineal gland during development: From fetus to adult. Croom Helm, London, pp 1–13
Korf HW, Oksche A (1986b) The pineal organ. In: Pang PKT, Schreibman MP (eds) Vertebrate endocrinology. Fundamentals and biomedical implications. Vol. 1. Morphological considerations. Academic Press, Orlando, pp 105–145
Korf HW, Liesner R, Meissl H, Kirk A (1981) Pineal complex of the clawed toad, Xenopus laevis Daud.: Structure and function. Cell Tissue Res 216:113–130
Korf HW, Foster RG, Ekström P, Schalken JJ (1985a) Opsin-like immunoreaction in the retinae and pineal organs of four mammalian species. Cell Tissue Res 242:645–648
Korf HW, Møller M, Gery I, Zigler JS, Klein DC (1985b) Immunocytochemical demonstration of retinal-S-antigen in the pineal organ of four mammalian species. Cell Tissue Res 239:81–85
Kuo C-H, Tamotsu S, Morita Y, Shinozawa T, Akiyama M, Miki N (1988) Presence of retina-specific proteins in the lamprey pineal complex. Brain Res 442:147–151
Meiniel A (1973) L'épiphyse et l'oeil pariétal de l'embryon de Lacerta vivipara. J. Recherche qualitative des monoamines en fluorescence ultraviolette et incorporation de 5-hydroxytryptophane-3 (= 5 HTP-3) au niveau des photorecepteurs rudimentaires sécrétoires. Arch Anat Histol Embryol Norm Exp 56:111–130
Meiniel A (1976) Contribution à l'étude du complexe pariétal embryonnaire des lacertiliens. Différenciation cellulaire de l'épiphyse de Lacerta vivipara (Jacquin) en rapport avec les activités sensorielle, sécrétoire et neurohumorale (biosynthèses indoliques). Thesis University Clermont Fr
Meiniel A (1979) Detection and localization of biogenic amines in the pineal complex of Lampetra planeri (Petromyzontidae). Prog Brain Res 52:303–307
Meiniel A (1980) Ultrastructure of serotonin-containing cells in the pineal organ of Lampetra planeri (Petromyzontidae). Cell Tissue Res 207:407–427
Meiniel A (1981) New aspects of the phylogenetic evolution of sensory cell lines in the vertebrate pineal complex. In: Oksche A, Pévet P (eds) The pineal organ: photobiology-biochronometry-endocrinology. Elsevier, Amsterdam, pp 27–48
Meiniel A, Hartwig HG (1980) Indoleamines in the pineal complex of Lampetra planeri (Petromyzontidae). A fluorescence microscopic and microspectrofluorimetric study. J Neural Transm 48:65–83
Meissl H, George SR (1985) Effect of GABA and its antagonists, bicuculline and picrotoxin, on nerve cell discharges of the photosensory pineal organ of the frog, Rana esculenta. Brain Res 332:39–46
Møller M, Glistrup OV, Olsen W (1983) Contrast enhancement of the brownish horseradish peroxidase-activated 3,3-diaminobenzidine tetrahydrochloride reaction product in black and white photomicrography by use of interference filters. J Histochem Cytochem 32:37–42
Morita Y, Dodt E (1971) Photosensory responses from the pineal eye of the lamprey (Petromyzon fluviatilis). Proc Int Un Physiol Sci 9:405
Morita Y, Dodt E (1973) Slow photic responses of the isolated pineal organ of lamprey. Nova Acta Leopoldina 38:331–339
Morita Y, Tabata M, Tamotsu S (1985) Intracellular response and input resistance change of pineal photoreceptors and ganglion cells. Neurosci Res 2 (Suppl):S79-S88
Morita Y, Samejima M, Uchida K (1987) The role of direct photosensory pineal organ in the LD and circadian rhythm. In: Hiroshige T, Honma K (eds) Comparative aspects of circadian clocks. Hokkaido University Press, Sapporo, pp 73–81
Morita Y, Tamotsu S, Uchida K (1989) Multiplicity of electrophysiological and immunocytochemical properties in the pineal photosensory system. In: Reiter RJ, Pang SF (eds) Adv Pineal Res, Vol 3. Libbey, London, pp 43–48
Oksche A (1970) Zur Differenzierung sensorischer und sekretorischer Strukturelemente im Zentralnervensystem. Verh Dt Zool Ges 64:72–79
Oksche A (1971) Sensory and glandular elements of the pineal organ. In: Wolstenholme GEW, Knight J (eds) The pineal gland. Churchill Livingstone, Edinburgh, London, pp 127–146
Oksche A (1986) Historical perspectives of photoneuroendocrine systems. In: O'Brien P, Klein DC (eds) Pineal and retinal relationships. Academic Press, Orlando, pp 1–13
Oksche A, Hartwig HG (1979) Pineal sense organs—components of photoneuroendocrine systems. Prog Brain Res 52:113–130
Paul E, Hartwig HG, Oksche A (1971) Neurone und zentralnervöse Verbindungen des Pinealorgans der Anuren. Z Zellforsch 112:466–493
Pu GA, Dowling JE (1981) Anatomical and physiological characteristics of pineal photoreceptor cells in the larval lamprey, Petromyzon marinus. J Neurophysiol 46:1018–1038
Robertson LM, Takahashi JS (1988) Circadian clock in cell culture: I. Oscillation of melatonin release from dissociated chick pineal cells in flow-through microcarrier culture. J Neurosci 8:12–21
Rodríguez EM, Korf HW, Oksche A, Yulis CR, Hein S (1988) Pinealocytes immunoreactive with antisera against secretory glycoproteins of the subcommissural organ: A comparative study. Cell Tissue Res 254:469–480
Sternberger LA, Hardy PH, Cuculis JJ, Meyer HG (1970) The unlabeled antibody enzyme method of immunohistochemistry. Preparation and properties of soluble antigen-antibody complex (horseradish peroxidase-anti horseradish peroxidase) and its use in identification of spirochetes. J Histochem Cytochem 18:315–333
Tamotsu S, Morita Y (1986) Photoreception in pineal organs of larval and adult lampreys, Lampetra japonica. J Comp Physiol A159:1–5
Tamotsu S, Morita Y (1990) Blue sensitive visual pigment and photoregeneration in pineal photoreceptors measured by high performance liquid chromatography. Comp Biochem Physiol 96B:487–490
Tretjakoff D (1915) Die Parietalorgane von Petromyzon fluviatilis. Z Wiss Zool 113:1–112
Vigh-Teichmann I, Korf HW, Nürnberger F, Oksche A, Vigh B, Olsson R (1983) Opsin-immunoreactive outer segments in the pineal and parapineal organs of the lamprey (Lampetra fluviatilis), the eel (Anguilla anguilla) and the rainbow trout (Salmo gairdneri). Cell Tissue Res 230:289–307
Wainwright SD, Wainwright LK (1980) Regulation of the cycle in chick pineal serotonin N-acetyltransferase activity in vitro by light. J Neurochem 35:451–457
Wake K (1973) Acetylcholinesterase-containing nerve cells and their distribution in the pineal organ of the goldfish Carassius auratus. Z Zellforsch 145:287–298
Wake K, Ueck M, Oksche A (1974) Acetylcholinesterase-containing nerve cells in the pineal complex and subcommissural area of the frogs, Rana ridibunda and Rana esculenta. Cell Tissue Res 154:423–442
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Tamotsu, S., Korf, H.W., Morita, Y. et al. Immunocytochemical localization of serotonin and photoreceptor-specific proteins (rod-opsin, S-antigen) in the pineal complex of the river lamprey, Lampetra japonica, with special reference to photoneuroendocrine cells. Cell Tissue Res 262, 205–216 (1990). https://doi.org/10.1007/BF00309875
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00309875