Skip to main content
SpringerLink
Log in

Atrial natriuretic factor-like immunoreactivity in spinal cord and in primary sensory neurons of spinal and trigeminal ganglia of guinea-pig: correlation with tachykinin immunoreactivity*

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

Atrial natriuretic factor (ANF) is a cardiac hormone with various functions in body homeostasis. It is also processed in the brain and in the peripheral nervous system where it appears to play a role as a neuromodulator. Little is known about the presence of ANF throughout the spinal cord of the guinea-pig. We therefore examined the distribution of ANF and its possible interrelation with primary sensory afferents in this species. Using enzyme- and fluorescence-immunohistochemistry on deparaffinized sections, ANF-like immunoreactivity was found to be present in nerve fibers in laminae I/II of the spinal cord and in neurons of spinal and trigeminal ganglia. Tachykinins and ANF coexisted in very few fibers of the spinal cord but did not coexist in primary sensory spinal or trigeminal neurons. Our results indicate that spinal ANF-immunoreactive fibers are of dual origin, primary sensory and non-primary sensory. The possibly heterogeneous source of the non-primary sensory ANF, its possible coexistence with other co-transmitters and functional implications are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Arendt RM, Stangl E, Zähringer J, Liebisch DC, Herz A (1985) Demonstration and characterization of alpha-human atrial natriuretic factor in human plasma. FEBS Lett 189:57–61

    Google Scholar 

  • Ballermann BJ, Brenner BM (1986) Role of atrial peptides in body fluid homeostasis. Circ Res 58:619–630

    Google Scholar 

  • Battaglia G, Rustioni A (1988) Coexistence of glutamate and substance P in dorsal root ganglion neurons of the rat and monkey. J Comp Neurol 277:302–314

    Google Scholar 

  • Bergey JL, Much DR, Kratunis V, Asaad M (1989) Effects of human ANF-(99–126) on sympathetic nerve function, hemodynamic parameters and plasma cGMP levels in anesthetized, ganglion-blocked dogs. Eur J Pharmacol 159:103–112

    Google Scholar 

  • Cantin M, Gutkowska J, Thibault G, Milne RW, Ledoux SC, Min-Li S, Chapeau C, Garcia R, Genest J (1984) Immunochemical localization of atrial natriuretic factor in the heart and salivary glands. Histochemistry 89:113–117

    Google Scholar 

  • Debinski W, Gutkowska J, Küchel O, Racz K, Buu NT, Cantin M, Genest J (1986) ANF-like peptide(s) in the peripheral autonomic system. Biochem Biophys Res Commun 134:279–284

    Google Scholar 

  • Debinski W, Kuchel O, Buu NT, Thibault G (1988) Atrial natriuretic factor in the spinal cord of normotensive and hypertensive rats. Peptides 9:1101–1105

    Google Scholar 

  • Forssmann WG (1986) Cardiac hormones. I. Review on the morphology, biochemistry, and molecular biology of the endocrine heart. Eur J Clin Invest 16:439–4151

    Google Scholar 

  • Forssmann WG, Birr C, Carlquist M, Christmann M, Finke R, Henschen A, Hock D, Kirchheim H, Kreye V, Lotspeich F, Metz J, Mutt V, Reinecke M (1984) The auricular myocardiocytes of the heart constitute an endocrine organ. Characterization of a porcine cardiac hormone, cardiodilatin-126. Cell Tisue Res 238:425–430

    Google Scholar 

  • Gardner DG, Deschepper CF, Ganong WF, Hane S, Fiddes J, Baxter JD, Lewicki J (1986) Extra-atrial expression of the gene for atrial natriuretic factor. Proc Natl Acad Sci USA 83:6697–6701

    Google Scholar 

  • Genest J, Cantin M (1986) Atrial natriuretic factor. In: Zanchetti A, Tarazi RC (eds) Handbook of Hypertension, Vol. 8, Pathophysiology of hypertension — Regulatory mechanisms, Elsevier, Amsterdam, pp 647–657

    Google Scholar 

  • Genest J, Cantin M (1987) Atrial natriuretic factor. Circulation 75[Suppl I]:I-118-I-125

    Google Scholar 

  • Glembotski CG, Wildey GM, Gibson TR (1985) Molecular forms of immunoreactive atrial natriuretic peptide in the rat hypothalamus and atrium. Biochem Biophys Res Commun 129:671–678

    Google Scholar 

  • Inagaki S, Kubota Y, Kito S, Kangawa K, Matsuo H (1986) Imunoreactive atrial natriuretic polypeptides in the adrenal medulla and sympathetic ganglia. Regul Pept 15:249–260

    Google Scholar 

  • Jirikowski GF, Back H, Forssmann WG, Stumpf WE (1986) Coexistence of atrial natriuretic factor (ANF) and oxytocin in neurons of the rat hypothalamus. Neuropeptides 8:243–249

    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 

  • Lange W, Lang RE, Basting C, Unger J (1989) Localization of atrial natriuretic peptide/cardiodilatin (ANP/CDD)-immunorectivity in the lacrimal gland of the domestic pig. Graefe's Arch Clin Exp Ophthalmol (to appear)

  • Lazure C, Ong H, McNicoll N, Netchitailo P, Chrétien M, De Léan A, Vaudry H (1988) The amino acid sequences of frog heart atrial natriuretic-like peptide and mammalian ANF are closely related. FEBS Lett 238:300–306

    Google Scholar 

  • Marumo F, Masuda T, Ando K (1987) Presence of the atrial natriuretic peptide in human cerebrospinal fluid. Biochem Biophys Res Commun 143:813–818

    Google Scholar 

  • Morii N, Nakao K, Itoh H, Shiono S, Yamada T, Sugawara A, Saito Y, Mukoyama M, Arai H, Sakamoto M, Imura H (1987) Atrial natriuretic polypeptide in spinal cord and autonomic ganglia. Biochem Biophys Res Commun 145:196–203

    Google Scholar 

  • Needleman P, Adams SP, Cole BR, Currie MG, Geller DM, Michener ML, Saper CB, Schwartz D, Standaert DG (1985) Atriopeptins as cardiac hormones. Hypertension 7:469–482

    Google Scholar 

  • Nohr D, Weihe E, Arendt RM (1989) Atrialer natriuretischer Faktor (ANF) im Rückenmark, der Medulla, Spinalund Trigeminalganglien des Meerschweinchens. Verh Anat Ges (to appear)

  • Pines W, Hurwitz S (1988) The effect of parathyroid hormone and atrial natriuretic peptide on cyclic nucleotide production and proliferation of avian epiphyseal growth plate chondroprogenitor cells. Endocrinology 123:360–366

    Google Scholar 

  • Quirion R (1988) Atrial natriuretic factors and the brain: an update. TINS 11:58–62

    Google Scholar 

  • Samson WK (1987) Atrial natriuretic factor and the central nervous system. Endocrinol Metab Clin North Am 16:145–161

    Google Scholar 

  • Saper CB, Standaert DG, Currie MG, Schwartz D, Geller DM, Needleman P (1985) Atriopeptin-immunoreactive neurons in the brain: presence in cardiovascular regulatory areas. Science 227:1047–1049

    Google Scholar 

  • Simonnet G, Allard M, Legendre P, Gabrion J, Vincent JD (1989) Characteristics and specific localization of receptors for atrial natriuretic peptides at non-neuronal cells in cultured mouse spinal cord cells. Neuroscience 29:189–199

    Google Scholar 

  • Skofitsch G, Jacobowitz DM, Eskay RL, Zamir N (1985) Distribution of atrial natriuretic factor-like immunoreactive neurons in the rat brain. Neuroscience 16:917–948

    Google Scholar 

  • Standaert DG, Saper CB, Needleman P (1985) Atriopeptin: potent hormone and potential neuromediator. TINS 8:509–511

    Google Scholar 

  • Standaert DG, Needleman P, Day ML, Weigand R, Krause JE (1988) Expression of the gene for preproatriopeptin in the central nervous system of the rat. Mol Brain Res 4:7–13

    Google Scholar 

  • Swanson LW (1987) The hypothalamus. In: Björklund A, Hökfelt T, Swanson LW (eds) Handbook of chemical neuroanatomy, Vol. 5, Integrated systems of the CNS, Part I, Elsevier, Amsterdam, pp 1–125

    Google Scholar 

  • Tainio H, Vaalasti A, Rechardt L (1987) The distribution of substance P-, CGRP-, galaninand ANP-like immunoreactive nerves in human sweat glands. J Histochem 19:375–380

    Google Scholar 

  • Ueda S, Minamino N, Sudoh T, Kangawa K, Matruo H (1988) Regional distribution of immunoreactive brain natriuretic peptide in porcine brain and spinal cord. Biochem Biophys Res Commun 155:733–739

    Google Scholar 

  • Vollmar AM, Schulz R (1988) Evidence for the presence of ANPprecursor material in the rat thymus. Biochem Biophys Res Commun 155:700–708

    Google Scholar 

  • Vollmar AM, Mytzka C, Arendt RM, Schulz R (1988) Atrial natriuretic peptide in bovine corpus luteum. Endocrinology 123:762–767

    Google Scholar 

  • Weihe E (1989) Neuropeptides in primary sensory neurons. In: Zenker W, Neuhuber W (eds) The primary sensory neuron — a survey of recent morpho-functional aspects. Plenum Press, New York

    Google Scholar 

  • Weihe E, Hartschuh W (1988) Multiple peptides in cutaneous nerves: regulators under physiological conditions and a pathogenic role in skin disease? Semin Dermatol 7:284–300

    Google Scholar 

  • Weihe E, Arendt RM, Nohr D, Liebisch BC, Herz A (1987) Immunohistochemical and radioimmunological evidence for the presence of ANF-like immunoreactivity in sensory afferents of guinea-pig. Neuroscience 22 [Suppl] 788

    Google Scholar 

  • Weihe E, Nohr D, Hartschuh W (1988a) Immunohistochemical evidence for a co-transmitter role of opioid peptides in primary sensory neurons. Prog Brain Res 74:189–199

    Google Scholar 

  • Weihe E, Nohr D, Hartschuh W, Gauweiler B, Fink T (1988b) Multiplicity of opioidergic pathways related to cardiovascular innervation: differential contribution of all three opioid precurors. In: Stumpe KO, Kraft K (eds) Opioid peptides and blood pressure control, Springer, Berlin Heidelberg New York, pp 27–49

    Google Scholar 

  • Zamir N, Skofitsch G, Eskay R, Jacobowitz DM (1986) Distribution of immunoreactive atrial natriuretic peptides in the central nervous system of the rat. Brain Res 365:105–111

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Anatomical Institute, Johannes Gutenberg-University, Mainz, Germany

    Donatus Nohr, Eberhard Weihe & Hans J. Zentel

  2. Medical Clinic, University of Munich, München, Germany

    Rainer M. Arendt

Authors
  1. Donatus Nohr
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eberhard Weihe
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hans J. Zentel
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rainer M. Arendt
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Preliminary aspects of this study have been reported at the 2nd World Congress of Neuroscience in Budapest (Weihe et al. 1987) and at the Versammlung der Anatomischen Gesellschaft in Zürich (Nohr et al. 1989)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nohr, D., Weihe, E., Zentel, H.J. et al. Atrial natriuretic factor-like immunoreactivity in spinal cord and in primary sensory neurons of spinal and trigeminal ganglia of guinea-pig: correlation with tachykinin immunoreactivity*. Cell Tissue Res. 258, 387–392 (1989). https://doi.org/10.1007/BF00239459

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00239459

Key words

Search

Navigation