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Protein gene product (PGP) 9.5 immunoreactivity in nerve fibres and pinealocytes of guinea-pig pineal gland: interrelationship with tyrosine-hydroxylase- and neuropeptide-Y-immunoreactive nerve fibres

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Abstract

This light-microscopic (LM) immunohistochemical study has evaluated the presence and distribution of the pan-neural and neuroendocrine marker protein gene product (PGP) 9.5 in pinealocytes and nerve fibres of guinea-pig pineal gland. The pattern of PGP 9.5-immunoreactive (ir) nerve fibres has been compared with that of fibres staining for tyrosine hydroxylase (TH) or neuropeptide Y (NPY). The vast majority of pinealocytes stained for PGP 9.5, although with variable intensity. PGP 9.5 immunoreactivity was localized in pinealocytic cell bodies and processes. Double-immunofluorescence revealed that PGP 9.5 immunoreactivity was absent from glial cells identified with a monoclonal antibody against glial fibrillary acidic protein (GFAP), PGP 9.5 immunoreactivity was also present in a large number of nerve fibres and varicosities distributed throughout the pineal gland. The number of TH-ir and NPY-ir nerve fibres was lower compared with those containing PGP 9.5 immunoreactivity. All fibres staining for NPY also stained for TH. NPY-ir nerve fibres were found to be much more numerous than previously reported for this species. The double-immunofluorescence analysis indicated that almost all TH-ir nerve fibres of the pineal gland contained PGP 9.5 immunoreactivity. However, few PGP 9.5-ir nerve fibres, located in the periphery and the central part of the gland, were TH-negative. A large number of PGP 9.5-ir fibres was concentrated in the pineal stalk. In contrast, TH-ir and NPY-ir nerve fibres were rare in this part of the pineal gland. Our data provide evidence that immunohistochemistry for PGP 9.5 may be a useful tool further to differentiate central and peripheral origins of pineal innervation. Furthermore, the staining of pinealocytes for PGP 9.5 may be exploited to study the three-dimensional morphology and the architecture of pinealocytes and their processes under various experimental conditions.

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References

  • Ariano MA, Kenny SL (1985) Peptide coincidence in rat superior cervical ganglion. Brain Res 340:181–185

    Article  PubMed  CAS  Google Scholar 

  • Buijs RM, Pévet P (1980) Vasopressin and oxytocin-containing fibers in the pineal gland and subcommissural organ of the rat. Cell Tissue Res 205:11–17

    Article  PubMed  CAS  Google Scholar 

  • Cajal SR (1904) Textural del sistema nervioso del hombre y de los vertebrados, vol 2, part 2. Moya, Madrid

    Google Scholar 

  • Chronwald EM, DiMaggio DA, Massari VJ, Pickel VM, Ruggiero DA, O'Donohue TL (1985) The anatomy of neuropeptide-Y-containing neurons in rat brain. Neuroscience 15:1159–1181

    Article  Google Scholar 

  • Dalsgaard JC, Rydh M, Haegerstrand A (1989) Cutaneous innervation in man visualized with protein gene product 9.5 (PGP 9.5) antibodies. Histochemistry 92:385–389

    Article  PubMed  CAS  Google Scholar 

  • Eurich A (1991) Versilberungsstudien an der Zirbeldrüse von Meerschweinchen. Inaugural-Dissertation, Fachberich Human-medizin, Mainz

    Google Scholar 

  • Favaro G (1904) Le fibre nervose prepineali e pineali nell'encefalo dei mammiferi. Arch Ital Anat 3:750–789

    Google Scholar 

  • Gulbenkian S, Wharton J, Polak JM (1987) The visualization of cardiovascular innervation in the guinea pig using an antiserum to protein gene product 9.5 (PGP 9.5). J Auton Nerv Syst 18:235–247

    Article  PubMed  CAS  Google Scholar 

  • Huang S-K, Klein DC, Korf H-W (1992) Immunocytochemical demonstration of rod-opsin, S-antigen, and neuron-specific proteins in the human pineal gland. Cell Tissue Res 267:493–498

    Article  PubMed  CAS  Google Scholar 

  • Jackson P, Thomson RJ (1981) The demonstration of new human brain-specific proteins by high-resolution two-dimensional polyacrylamide electrophoresis. J Neurol Sci 49:429–438

    Article  PubMed  CAS  Google Scholar 

  • Kappers Ja (1960) The development, topographical relations and innervation of the epiphysis cerebri in the albino rat. Z Zell-forsch Mikrosk Anat 52:163–215

    Article  CAS  Google Scholar 

  • Korf H-W, Moller M (1984) The innervation of the mammalian pineal gland with special reference to central pinealopetal projections. In: Reiter RJ (ed) Pineal research reviews, vol 2. Liss, New York, pp 41–86

    Google Scholar 

  • Korf H-W, Moller M, Gery I, Zigler JS, Klein DC (1985) Immuno-cytochemical demonstration of retinal S-antigen in the pineal gland of four mammalian species. Cell Tissue Res 239:81–85

    Article  PubMed  CAS  Google Scholar 

  • Korf H-W, Oksche A, Ekström P, Gery I, Ziegler Jr JS, Klein DC (1986) Pinealocyte projections into the mammalian brain revealed with S-antigen antiserum. Science 231:735–737

    Article  PubMed  CAS  Google Scholar 

  • Korf H-W, Sato T, Oksche A (1990) Complex relationships between the pineal organ and the medial habenular nucleus-pretectal region of the mouse as revealed by S-antigen immunocytochemistry. Cell Tissue Res 261:493–500

    Article  PubMed  CAS  Google Scholar 

  • Larsen PJ, Moller M, Mikkelsen JD (1991) The intracerebral course of paraventricular efferents involved in the regulation of pineal gland activity. In: Arendt J, Pévet P (eds) Advances in pineal research, vol 5. Libbey, London, pp 25–30

    Google Scholar 

  • Lingappa JR, Zigmond RE (1987) A histochemical study of the adrenergic innervation of the rat pineal gland: evidence for overlap of the innervation from the two superior cervical ganglia and for sprouting following unilateral denervation. Neuroscience 21:893–902

    Article  PubMed  CAS  Google Scholar 

  • Lowe J, McDermott H, Landon M, Mayer JR, Wilkinson KD (1990) Ubiquitin carboxyl-terminal hydrolase (PGP 9.5) is selectively present in ubiquitinated inclusion bodies characteristic of human neurodengenerative diseases. J Pathol 161:153–160

    Article  PubMed  CAS  Google Scholar 

  • Lundberg L-M, Alm P, Wharton J, Polak JM (1988) Protein gene product 9.5 (PGP 9.5). A new neuronal marker visualizing the whole uterine innervation and pregnancy-induced and developmental changes in the guinea pig. Histochemistry 90:9–17

    Article  PubMed  CAS  Google Scholar 

  • McClure C, McMillan PJ, Alfonso Miranda C (1986) Demonstration of differential immunohistochemical localization of the neurone-specific enolase antigen in rat pinealocytes. Am J Anat 176:461–467

    Article  PubMed  CAS  Google Scholar 

  • Moller M, Ingild A, Bock E (1978) Immunohistochemical demonstration of S-100 protein and GFA protein in interstitial cells of rat pineal gland. Brain Res 140:1–13

    Article  PubMed  CAS  Google Scholar 

  • Moller M, Mikkelsen JD, Fahrenkrug J, Korf H-W (1985) The presence of vasoactive intestinal polypeptide (VIP)-like immunoreactive nerve fibers and VIP-receptors in the pineal gland of the mongolian gerbil (Meriones unguiculatus). An immunohistochemical and receptor autoradiographic study. Cell Tissue Res 241:333–340

    Article  PubMed  CAS  Google Scholar 

  • Müller MJ (1990) Licht- und elektronenmikroskopische Untersuchungen zur Morphologie und Zytoarchitektonik der Zirbeldrüse des Meerschweinchens. Inaugural-Dissertation, Fachbereich Humanmedizin, Mainz

    Google Scholar 

  • Müller S, Weihe E (1991) Interrelation of peptidergic innervation with mast cells and ED1-positive cells in rat thymus. Brain Behav Immun 5:55–72

    Article  PubMed  Google Scholar 

  • Nohr D, Weihe E (1991) The neuroimmune link in the bronchus-associated lymphoid tissue (BALT) of cat and rat: peptides and neural markers. Brain Behav Immun 5:84–101

    Article  PubMed  CAS  Google Scholar 

  • Pévet P (1977) On the present of different populations of pinealocytes in the mammalian pineal gland. J Neural Transm 40:289–304

    Article  PubMed  Google Scholar 

  • Ramieri G, Anselmetti GC, Baracchi F, Panzica GC, Viglietti-Panzica C, Modica R, Polak JM (1990) The innervation of human teeth and gingival epithelium as revealed by means of an antiserum for protein gene product 9.5 (PGP 9.5). Am J Anat 189:146–154

    Article  PubMed  CAS  Google Scholar 

  • Redecker P, Grube D, Jahn R (1990) Immunohistochemical localization of synaptophysin (p38) in the pineal gland of the mongolian gerbil (Meriones unguiculatus). Anat Embryol (Berl) 181:433–440

    Article  CAS  Google Scholar 

  • Reiter RJ, Rudeen PK, Banks A, Rollag MD (1979) Acute effects of unilateral or bilateral superior cervical ganglionectomy on rat pineal N-acetyltransferase activity and melatonin content. Experientia 35:691–692

    Article  PubMed  CAS  Google Scholar 

  • Reuss S, Moller M (1986) Direct projections to the rat pineal gland via the stria medullaris thalami—an anterograde tracing study by use of horseradish peroxidase. Cell Tissue Res 244:691–694

    Article  PubMed  CAS  Google Scholar 

  • Reuss S, Moore RY (1989) Neuropeptide Y-containing neurons in the rat superior cervical ganglion: projections to the pineal gland. J Pineal Res 6:307–316

    Article  PubMed  CAS  Google Scholar 

  • Reuss S, Riemann R, Vollrath L (1992) Substance P-and calcitonin gene-related peptide-like immunoreactive neurons in the rat trigeminal ganglion with special reference to meningeal and pineal innervation. Acta Histochem 92:104–109

    PubMed  CAS  Google Scholar 

  • Rode J, Dhillon AP, Doran JF, Jackson P, Thompson RJ (1985) PGP 9.5, a new marker for human neuroendocrine tumours. Histopathology 9:147–158

    Article  PubMed  CAS  Google Scholar 

  • Romeo HE, Nohr D, Weihe E, Reuss S, Vollrath L (1991) Presence of protein gene product 9.5 immunoreactivity in nerve fibers and pinealocytes of rodent pineal gland: interrelationship with tyrosine hydroxylase and NPY immunoreactive fibers and influence of bilateral superior cervical ganglionectomy. Verh Anat Ges 86 [Anat Anz 172]:251

    Google Scholar 

  • Ronnekleiv OK, Kelly MJ (1984) Distribution of substance P neurons in the epithalamus of the rat. An immunohistochemical investigation. J Pineal Res 1:355–370

    Article  PubMed  CAS  Google Scholar 

  • Sasek CA, Zigmond RE (1989) Localization of vasoactive intestinal peptide-and peptide histidine isoleucine amide-like immunoreactivities in the rat superior cervical ganglion and its nerve trunks. J Comp Neurol 280:522–532

    Article  PubMed  CAS  Google Scholar 

  • Schneider T, Semm P, Vollrath L (1981) Ultrastructural observations on the central innervation of guinea-pig pineal gland. Cell Tissue Res 220:41–49

    Article  PubMed  CAS  Google Scholar 

  • Schon F, Allen JM, Yeats JC, Allen YS, Ballesta J, Polak JM, Kelly JS, Bloom SR (1985) Neuropeptide Y innervation of the rodent pineal gland and cerebral blood vessels. Neurosci Lett 57:65–71

    Article  PubMed  CAS  Google Scholar 

  • Schröder H (1986) Neuropeptide Y (NPY)-like immunoreactivity in peripheral and central nerve fibers of the golden hamster (Mesocricetus auratus) with special respect to pineal gland innervation. Histochemistry 85:321–325

    Article  PubMed  Google Scholar 

  • Schröder H, Vollrath L (1986) Neuropeptide Y (NPY)-like immunoreactivity in the guinea pig pineal organ. Neurosci Lett 63:285–289

    Article  PubMed  Google Scholar 

  • Schröder H, Weihe E, Nohr D, Vollrath L (1988) Immunohistochemical evidence for the presence of peptides derived from proenkephalin, prodynorphin and proopiomelanocortin in the guinea pig pineal gland. Histochemistry 88:333–341

    PubMed  Google Scholar 

  • Schröder H, Bendig A, Dahl D, Gröschel-Stewart U, Vollrath L (1990) Neuronal markers in the rodent pineal gland—an immunohistochemical investigation. Histochemistry 94:309–314

    Article  PubMed  Google Scholar 

  • Semm P, Vollrath L (1980) Electrophysiological evidence for cireadian rhythmicity in mammalian pineal organ. J Neural Trans 47:181–190

    Article  CAS  Google Scholar 

  • Shiotani Y, Yamano M, Shiosaka S, Emson PC, Hillajard CJ, Girgis S, MacIntry I (1986) Distribution and origins of substance P (SP)-calcitonin gene related peptide (CGRP)-, vasoactive intestinal polypeptide (VIP)- and neuropeptide Y (NPY)-containing nerve fibers in the pineal gland of gerbils. Neurosci Lett 70:187–192

    Article  PubMed  CAS  Google Scholar 

  • Thompson RJ, Doran JF, Jackson P, Dhillon AP, Rode J (1983) PGP 9.5—a new marker for vertebrate neurons and neuroendocrine cells. Brain Res 278:224–228

    Article  PubMed  CAS  Google Scholar 

  • Vigh-Teichmann I, Vigh B, Gery I, Veen T van (1986) Different types of pinealocytes as revealed by immunoelectron microscopy of S-antigen and antiopsin binding sites in the pineal organ of toad, frog, headgehog and bat. Exp Biol 45:27–43

    PubMed  CAS  Google Scholar 

  • Vollrath L, Schröder H (1987) Neuronal properties of mammalian pinealocytes? In: Trentini GP, De Gaetani C, Pévet P (eds) Fundaentals and clinics in pineal research, vol 44. Raven, New York, pp 13–25

    Google Scholar 

  • Wang L, Hilliges M, Jernberg T, Wiegleb-Edström D, Johansson O (1990) Protein gene product 9.5 immunoreactive nerve fibres and cells in human skin. Cell Tissue Res 261:25–33

    Article  PubMed  CAS  Google Scholar 

  • Weihe E, Krekel J (1991) The neuroimmune connection in human tonsils. Brain Behav Immun 5:41–54

    Article  PubMed  CAS  Google Scholar 

  • Welsh MG, Ding JM, Buggy J, Terracio L (1991) Application of confocal laser scanning microscopy to the deep pineal gland and other neural tissues. Anat Rec 231:473–481

    Article  PubMed  CAS  Google Scholar 

  • Wilkinson KD, Lee K, Deshapande S, Duerksen-Hughes P, Boss JM, Pohl J (1989) The neuron-specific protein PGP 9.5 is a ubiquitin carboxyl-terminal hydrolase. Science 246:670–673

    Article  PubMed  CAS  Google Scholar 

  • Wilson POG, Barber PC, Hamid QA, Power BF, Dhillon AP, Rode J, Day INM, Thompson RJ, Polak JM (1988) The immunolocalization of protein gene product 9.5 using rabbit polyclonal and mouse monoclonal antibodies. Br J Exp Path 69:91–104

    CAS  Google Scholar 

  • Zentel HJ, Weihe E (1991) The neuro-B cell link of peptidergic innervation in the bursa Fabricii. Brain Behav Immun 5:132–147

    Article  PubMed  CAS  Google Scholar 

  • Zhang ET, Mikkelsen JD, Moller M (1991) Tyrosine hydroxylase-and neuropeptide Y-immunoreactive nerve fibers in the pineal complex of untreated rats and rats following removal of the superior cervical ganglia. Cell Tissue Res 265:63–71

    Article  PubMed  CAS  Google Scholar 

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  1. Anatomisches Institut, Johannes Gutenberg-Universität, Saarstrasse 19-21, W-6500, Mainz, Germany

    Horacio E. Romeo, Eberhard Weihe, Sabine Müller & Lutz Vollrath

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  1. Horacio E. Romeo
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  2. Eberhard Weihe
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  3. Sabine Müller
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  4. Lutz Vollrath
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Romeo, H.E., Weihe, E., Müller, S. et al. Protein gene product (PGP) 9.5 immunoreactivity in nerve fibres and pinealocytes of guinea-pig pineal gland: interrelationship with tyrosine-hydroxylase- and neuropeptide-Y-immunoreactive nerve fibres. Cell Tissue Res 271, 477–484 (1993). https://doi.org/10.1007/BF02913730

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  • DOI: https://doi.org/10.1007/BF02913730

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