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Oxytocin-producing and vasopressin-producing eosinophils in the mouse spleen: immunohistochemical, immuno-electron-microscopic and in situ hybridization studies

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Abstract

Oxytocin-like and vasopressin-like immunoreactive cells, and the cells expressing mRNAs for these peptides in the spleen of the C57BL/6 mouse were studied by immunohistochemistry, immuno-electron microscopy and in situ hybridization. Immunoreactive cells were distributed mainly in the splenic cord and marginal zone, whereas there were few in the lymphocyte-packed periarteriolar-lymphoid sheath, lymphoid follicle and germinal center. More numerous vasopressin-positive cells were seen in the splenic cord. The colocalization of oxytocin-like and vasopressin-like immunoreactivity in the same cells was identified by the investigation of mirror sections. By the pre-embedding immuno-electron-microscopic method using antisera against oxytocin and vasopressin, immunopositive reaction products were localized in the matrix around the specific granules, small clear vesicles and mitochondrial membrane of the eosinophils. No immunoreactivity to these peptides was found within the specific granules of the eosinophils. In situ hybridization with synthetic oligonucleotide probes labeled with 32P revealed the presence of mRNAs for oxytocin and vasopressin in the cells of the spleen, the distribution of the mRNAs for these peptides being the same as that of immunopositive cells. These observations suggest that eosinophils synthesize both oxytocin and vasopressin and store them in the matrix. Possible differences in the mechanism of synthesis and storage of these peptides between peripheral eosinophils and hypothalamic neurons are discussed.

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References

  • Ang VTY, Jenkins JS (1984) Neurohypophysial hormones in the adrenal medulla. J Clin Endocrinol Metab 58:688–691

    Google Scholar 

  • Angeletti RH, Hickey WF (1987) Neuroendocrine cells within immune tissues. Ann NY Acad Sci 996:78–84

    Google Scholar 

  • Archer GT, Air G, Jackas M, Morell DB (1965) Studies on rat eosinophil peroxidase. Biochim Biophys Acta 99:96–101

    Google Scholar 

  • Bainton DF, Farquhar MG (1970) Segregation and packaging of granule enzymes in eosinophilic leukocytes. J Cell Biol 45:54–73

    Google Scholar 

  • Baldino F, O'Kane TM, Fitzpatrick-McElligott S, Wolfson B (1988) Coordinate hormonal and synaptic regulation of vasopressin messenger RNA. Science 241:978–981

    Google Scholar 

  • Clements JA, Funder JW (1986) Arginine vasopressin (AVP) and AVP-like immunoreactivity in peripheral tissues. Endocr Rev 7:449–460

    Google Scholar 

  • Cunningham ET, Sawchenko PE (1991) Reflex control of magnocellular vasopressin and oxytocin secretion. Trends Neurosci 14:406–411

    Google Scholar 

  • Davis LG, Arentzen R, Reid JM, Manning RW, Wolfson B, Lawrence KL, Baldino F (1986) Glucocorticoid-sensitive vasopressin mRNA levels in the paraventricular nucleus of the rat. Proc Natl Acad Sci USA 83:1145–1149

    Google Scholar 

  • Doris PA (1984) Vasopressin and central integrative processes. Neuroendocrinology 38:75–85

    Google Scholar 

  • Durack DT, Ackerman SJ, Loegering DA, Gleich GJ (1981) Purification of human eosinophil-derived neurotoxin. Proc Natl Acad Sci USA 78:5165–5169

    Google Scholar 

  • Elands J, Barberis C, Jard S (1988) [3H]-[Thr4,Gly7]OT: a highly selective ligand for central and peripheral OT receptors. Am J Physiol 254:E31-E38

    Google Scholar 

  • Elands J, Resink A, De Kloet ER (1990) Neurohypophyseal hormone receptors in the rat thymus, spleen, and lymphocytes. Endocrinology 126:2703–2710

    Google Scholar 

  • Felten DL, Felten SY, Carlson SL, Olschowka JA, Livnat S (1985) Noradrenergic and peptidergic innervation of lymphoid tissue. J Immunol 135:755s-765s

    Google Scholar 

  • Fuller PJ, Clements JA, Tregear GW, Nikolaidis I, Whitfeld PL, Funder JW (1985) Vasopressin-neurophysin II gene expression in the ovary: studies in Sprague-Dawley, Long-Evans and Brattleboro rats. J Endocrinol 105:317–321

    Google Scholar 

  • Geenen V, Legros JJ, Hazée-Hagelstein MT, Louis-Kohn F, Lecomte-Yerna MJ, Demoulin A, Franchimont P (1985) Release of immunoreactive oxytocin and neurophysin I by cultured luteinizing bovine granulosa cells. Acta Endocrinol 110:263–270

    Google Scholar 

  • Geenen V, Legros JJ, Franchimont P, Defresne MP, Boniver J, Ivell R, Richter D (1987) The thymus as a neuroendocrine organ: synthesis of vasopressin and oxytocin in human thymic epithelium. Ann NY Acad Sci 496:56–66

    Google Scholar 

  • Geenen V, Robert F, Defresne MP, Boniver J, Legros JJ, Franchimont P (1989) Neuroendocrinology of the thymus. Horm Res 31:81–84

    Google Scholar 

  • Gleich GJ, Loegering DA, Maldonado JE (1973) Identification of major basic protein in guinea pig eosinophil granules. J Exp Med 137:1459–1471

    Google Scholar 

  • Hanley MR, Benton HP, Lightman SL, Todd K, Bone EA, Fretten P, Palmer S, Kirk CJ, Michell RH (1984) A vasopressin-like peptide in the mammalian sympathetic nervous system. Nature 309:258–261

    Google Scholar 

  • Hawthorn J, Nussey SS, Henderson JR, Jenkins JS (1987) Immunohistochemical localization of oxytocin and vasopressin in the adrenal glands of rat, cow, hamster and guinea pig. Cell Tissue Res 250:1–6

    Google Scholar 

  • Ivell R, Brackett KH, Fields MJ, Richter D (1985) Ovulation triggers oxytocin gene expression in the bovine ovary. FEBS Lett 190:263–267

    Google Scholar 

  • Ivell R, Schmale H, Krisch B, Nahke P, Richter D (1986) Expression of a mutant vasopressin gene:differential polyadenylation and read through of the mRNA 3′ end in a frame-shift mutant. EMBO J 5:971–977

    Google Scholar 

  • Johnson HM, Torres BA (1985) Regulation of lymphokine production by arginine vasopressin and oxytocin: modulation of lymphocyte function by neurohypophyseal hormones. J Immunol 135:773s-775s

    Google Scholar 

  • Kai-Kai MA, Anderton BH, Keen P (1986) A quantitative analysis of the interrelationships between subpopulations of rat sensory neurons containing arginine vasopressin or oxytocin and those containing substance P, fluoride-resistant acid phosphatase or neurofilament protein. Neuroscience 18:475–486

    Google Scholar 

  • Kawata M, McCabe JT, Pfaff DW (1988) In situ hybridization histochemistry with oxytocin synthetic oligonucleotide: strategy for making the probe and its application. Brain Res Bull 20:693–697

    Google Scholar 

  • Kawata M, Yuri K, Kumamoto K (1990) In situ hybridization histochemistry with oligodeoxy nucleotide probe as a tool for the detection of neuropeptide mRNAs. Acta Histochem Cytochem 23:307–325

    Google Scholar 

  • Kawata M, McCabe JT, Chung SK, Dutt A, Yuri K, Hirakawa M, Kumamoto K, Hirayama Y, Pfaff DW (1991) The effect of progesterone on oxytocin messenger RNA in hypothalamic neurons of estrogen-treated female rats studied with quantitative in situ hybridization histochemistry. Biomed Res 12:405–415

    Google Scholar 

  • Kumamoto K, Ebara S, Matsuura T, Kawata M (1992) Distribution of oxytocin and vasopressin neurons in the diencephalon of the Japanese horseshoe bat, Rhinolophys ferrumequinum. Acta Anat 144:80–92

    Google Scholar 

  • Lim ATW, Lolait SJ, Barlow JW, Autelitano DJ, Toh BH, Boublik J, Abraham J, Johnston CI, Funder JW (1984) Immunoreactive arginine-vasopressin in Brattleboro rat ovary. Nature 310:61–64

    Google Scholar 

  • Markwick AJ, Lolait SJ, Funder JW (1986) Immunoreactive arginine vasopressin in the rat thymus. Endocrinology 119:1690–1696

    Google Scholar 

  • Mezey E, Seidah NG, Chretien M, Brownstein MJ (1986) Demonstration of the vasopressin associated glycopeptide in the brain and peripheral tissues of the Brattleboro rat. Neuropeptide 7:79–85

    Google Scholar 

  • Miller MA, Zoeller RT, Dorsa DM (1988) Detection of vasopressin messenger RNA in cells within the bed nucleus of the stria terminalis by in situ hybridization histochemistry. Neurosci Lett 94:264–268

    Google Scholar 

  • Moll UM, Lane BL, Robert F, Geenen V, Legros JJ (1988) The neuroendocrine thymus: abundant occurrence of oxytocin-, vasopressin-, and neurophysin-like peptides in epithelial cells. Histochemistry 89:385–390

    Google Scholar 

  • Nicolas JF, Reano A, Kaiserlian D, Thivolet J (1986) Epithelial cell heterogeneity in the guinea pig thymus: immunohistochemical characterization of four thymic epithelial subsets defined by monoclonal anti-keratin antibodies. Eur J Immunol 16:457–464

    Google Scholar 

  • Nojiri H, Sato M, Urano A (1985) In situ hybridization of the vasopressin mRNA in the rat hypothalamus by use of a synthetic oligonucleotide probe. Neurosci Lett 58:101–105

    Google Scholar 

  • Nussey SS, Ang VTY, Jenkins JS, Chowdrey HS, Bisset GW (1984) Brattleboro rat adrenal contains vasopressin. Nature 310:64–66

    Google Scholar 

  • Nussey SS, Prysor-Jones RA, Ang VTY, Jenkins JS (1986) Vasopressin and oxytocin modulate catecholamine secretion by isolated adrenal medulla cells. J Endocrinol 108 [Suppl]:121

    Google Scholar 

  • Ogasa T, Hashimoto K, Suemaru S, Kageyama J, Ota Z (1992) The magnocellular arginine-vasopressin mRNA responds differently to food deprivation between the supraoptic and paraventricular nuclei of the hypothalamus in adrenalectomized rats with low corticosterone replacement. Brain Res 583:45–53

    Google Scholar 

  • Olsson I, Venge P (1974) Cationic proteins of human granulocytes. II. Separation of the cationic proteins of the granules of leukemic myeloid cells. Blood 44:235–246

    Google Scholar 

  • Peters MS, Rodriguez M, Gleich GJ (1986) Localization of human eosinophil granule major basic protein, eosinophil cationic protein, and eosinophil-derived neurotoxin by immunoelectron microscopy. Lab Invest 574:656–662

    Google Scholar 

  • Peterson CGB, Venge P (1983) Purification and characterization of a new cationic protein—eosinophil protein-X (EPX)—from granules of human eosinophils. Immunology 50:19–26

    Google Scholar 

  • Pow DV, Morris JF (1989) Dendrites of hypothalamic magnocellular neurons release neurohypophysial peptides by exocytosis. Neuroscience 32:435–439

    Google Scholar 

  • Robert F, Geenen V, Schoenen J, Burgeon E, De Groote D, Defresne MP, Legros JJ, Franchimont P (1991) Colocalization of immunoreactive oxytocin, vasopressin and interleukin-1 in human thymic epithelial neuroendocrine cells. Brain Behav Immun 5:102–115

    Google Scholar 

  • Silverman A J, Zimmerman E A (1975) Ultrastructural immunocytochemical localization of neurophysin and vasopressin in the median eminence and posterior pituitary of the guinea pig. Cell Tissue Res 159:291–301

    Google Scholar 

  • Sofroniew MV (1985) Vasopressin, oxytocin and their related neurophysins. In: Björklund A, Hökfelt T (eds) Handbook of chemical neuroanatomy, vol 4. Elsevier, Amsterdam New York Oxford, pp 93–165

    Google Scholar 

  • Soranzo L, Ganem Y, Chatelet F, Launay JM, Roland J (1992) Bombesin-like immunoreactivity in eosinophils. A light and electron microscopic study: effect of fixatives and cross-reactivity with various compounds. Biol Cell 75:69–81

    Google Scholar 

  • Swann RW, O'Shaughnessy PJ, Birkett SD, Wathes DC, Porter DG, Pickering BT (1984) Biosynthesis of oxytocin in the corpus luteum. FEBS Lett 174:262–266

    Google Scholar 

  • Thibonnier M, Snajdar RM, Rapp JP (1986) Characterization of vasopressin receptors of rat urinary bladder and spleen. Am J Physiol 251:H115-H120

    Google Scholar 

  • Torres BA, Johnson HM (1988) Arginine vasopressin (AVP) replacement of helper cell requirement in IFN-γ production. J Immunol 140:2179–2183

    Google Scholar 

  • Uhl GR, Zingg HH, Habener JF (1985) Vasopressin mRNA in situ hybridization: localization and regulation studied with oligonucleotide cDNA probes in normal and Brattleboro rat hypothalamus. Proc Natl Acad Sci USA 82:5555–5559

    Google Scholar 

  • Vandesande F, Dierickx K (1975) Identification of the vasopressin producing and of the oxytocin producing neurons in the hypothalamic neurosecretory system of the rat. Cell Tissue Res 164:153–162

    Google Scholar 

  • Vandesande F, Dierickx K, DeMay J (1977) The origin of the vasopressinergic and oxytocinergic fibers of the external region of the median eminence of the rat hypophysis. Cell Tissue Res 180:443–452

    Google Scholar 

  • Wekerle H, Ketelsen UP (1980) Thymic nurse cells Ia-bearing epithelium involved in T-lymphocyte differentiation? Nature 283:402–404

    Google Scholar 

  • Weller PF, Goetzel EJ, Austen KF (1980) Identification of human eosinophil lysophospholipase as the constituent of Charcot-Leyden crystals. Proc Natl Acad Sci USA 77:7740–7743

    Google Scholar 

  • Wiemann M, Ehret G (1993) Subcellular localization of immunoreactive oxytocin within thymic epithelial cells of the male mouse. Cell Tissue Res 273:79–87

    Google Scholar 

  • Wolfson B, Manning RW, Davis LG, Arentzen R, Baldino F Jr (1985) Co-localization of corticotropin releasing factor and vasopressin mRNA in neurons after adrenalectomy. Nature 315:59–61

    Google Scholar 

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Authors and Affiliations

  1. Department of Anatomy, Meiji College of Oriental Medicine, Hiyoshi-cho, Funai-gun, 629-03, Kyoto, Japan

    Kenzo Kumamoto & Tadao Matsuura

  2. Department of Immunology and Microbiology, Meiji College of Oriental Medicine, Hiyoshi-cho, Funai-gun, 629-03, Kyoto, Japan

    Takashi Amagai

  3. Department of Anatomy, Kyoto Prefectural University of Medicine, Kawaramachi-Hirokoji, Kamigyo-ku, 602, Kyoto, Japan

    Mitsuhiro Kawata

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  1. Kenzo Kumamoto
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  2. Tadao Matsuura
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  3. Takashi Amagai
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  4. Mitsuhiro Kawata
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Kumamoto, K., Matsuura, T., Amagai, T. et al. Oxytocin-producing and vasopressin-producing eosinophils in the mouse spleen: immunohistochemical, immuno-electron-microscopic and in situ hybridization studies. Cell Tissue Res 281, 1–10 (1995). https://doi.org/10.1007/BF00307953

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  • DOI: https://doi.org/10.1007/BF00307953

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