Summary
With the use of several region-specific antisera and the peroxidase-antiperoxidase (PAP) technique, several regulatory polypeptides were localized in nerves of the kidney. Neuropeptide Y (NPY)- immunoreactivity (IR), neurotensin (NT)-IR and vasoactive intestinal polypeptide (VIP)-IR occurred at high densities in all segments of the renal arterial system forming a perivascular plexus. Furthermore, NT-IR nerves were particularly frequent at the juxtaglomerular apparatus (JGA). Calcitonin gene-related peptide (CGRP)-IR was mainly concentrated in nerves supplying the hilus arteries and the JGA. Substance P (SP)-IR was predominantly found in large varicosities close to large renal arterial vessels and in the vicinity of the JGA. Somatostatin (SOM)-IR was only observed in single varicosities located at the media-adventitia border of large renal hilus arteries. The peptidergic nerves are correlated to their ultrastructural counterpart. In addition, the distribution patterns and the frequency of the different types of renal peptidergic nerve fibres are evaluated and compared. The functional role of these neuropeptides and their origin within the efferent branch of this part of the peripheral autonomic nervous system is discussed. Furthermore, the implication of some of the neuropeptides studied in afferent renal innervation is also substantiated.
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References
Alm P, Alumets J, Brodin F, Håkanson R, Sjöberg NO, Nilsson G, Sundler F (1978) Peptidergic (substance P) nerves in the genitourinary tract. Neuroscience 3:419–425
Alm P, Alumets J, Håkanson R, Owman C, Sjöberg NO, Sundler F, Walles B (1980) Origin and distribution of VIP (vasoactive intestinal polypeptide)-nerves in the genitourinary tract. Cell Tissue Res 205:337–347
Amara SG, Jonas V, Rosenfeld MG, Ong ES, Evans RM (1982) Alternative RNA-processing in calcitonin gene expression generates mRNAs encoding different polypeptide products. Nature 298:240–244
Archelos T, Xiang JZ, Reinecke M, Lang RE (1988) Regulation of release and function of neuropeptides in the heart. J Cardiovase Pharmacol (in press)
Barajas L (1978) Innervatio of the renal cortex. Fed Proc 37:1192–1201
Barajas L, Sokolski KN, Lechago J (1983) Vasoactive intestinal polypeptide-immunoreactive nerves in the kidney. Neurosci Lett 43:263–269
Brain SD, Williams TJ, Tippins JR, Morris HR, MacIntyre J, (1985) Calcitonin gene-related peptide is a potent vasodilator. Nature 313:54–56
Burnweit C, Forssmann WG (1979) Somatostatinergic nerves in the cervical spinal cord of the monkey. Cell Tissue Res 200:83–90
Della NG, Papka RE, Furness JB, Costa M (1983) Vasoactive intestinal peptide-like immunoreactivity in nerves associated with the cardiovascular system of guinea-pigs. Neuroscience 9:605–619
Emson PC, De Quidt ME (1984) NPY—a new member of the pancreatic polypeptide family. Trends Neurosci 7:31–35
Ferguson M, Bell C (1985) Substance P-immunoreactive nerves in the rat kidney. Neurosci Lett 60:183–188
Forssmann WG, Reinecke M (1984) Organ-specific innervation by autonomic nerve fibers as revealed by electron microscopy and immunohistochemistry. In: Ratzenhofer M, Höfler H, Walter GF (eds) Frontiers in hormone research, vol 12 Karger, Basel, pp 59–73
Forssmann WG, Pickel V, Reinecke M, Hock D, Metz J (1981) Immunohistochemistry and immunocytochemistry of nervous tissue. In: Heym C, Forssmann WG (eds) Techniques in neuroanatomical research Springer, Berlin Heidelberg New York, pp 171–205
Forssmann WG, Hock D, Metz J (1982) Peptidergic innervation of the kidney. Neurosci Lett 10:S183
Gattone VH, Marfurt CF, Dallie S (1986) Extrinsic innervation of the rat kidney: a retrograde tracing study. Am J Physiol 250:F189-F196
Gorgas K, Reinecke M, Weihe E, Forssmann WG (1983) Neurotensin and substance P immunoreactive nerve endings in the guinea pig carotid sinus and their ultranstructural counterpart. Anat Embryol 167:347–354
Håkanson R, Sundler F, Uddman R (1982) Distribution and topography of peripheral VIP nerve fibers: functional implications. In: Said SI (ed) Vasoactive intestinal peptide: advances in peptide hormone research series. Raven Press, New York, pp 121–144
Hassall CJS, Burnstock G (1984) Neuropeptide Y-like immunore-activity in cultured intrinsic neurones of the heart. Neurosci Lett 52:111–115
Hock D, Forssmann WG (1984) Zur peptidergen Innervation der Niere. Verh Anat Ges 78:463–464
Hökfelt T, Kellerth JO, Nilsson G, Pernow B (1975) Experimental immunohistochemical studies on the localization and distribution of substance P in cat primary sensory neurons. Brain Res 100:235–252
Hökfelt T, Schultzberg M, Elde R, Nilsson G, Terenius L, Said S, Goldstein M (1978) Peptide neurons in peripheral tissues including the urinary tract: immunohistochemical studies. Acta. Pharmacol Toxicol 43 (Suppl II):79–89
Larsson LI, Fahrenkrug J, Schaffalitzky de Muckadell OB (1977) Vasoactive intestinal polypeptide occurs in nerves of the female genitourinary tract. Science 197:1374–1375
Lembeck F, Donnerer J, Colpaert FC (1981) Increase of substance P in primary afferent nerves during chronic pain. Neuropeptides 1:175–180
Lundberg JM, Saria A, Franco-Cereceda A, Hökfelt T, Terenius L, Goldstein M (1985) Differential effects of reserpine and 6-hydroxydopamine on neuropeptide Y (NPY) and noradrenalin in peripheral neurons. Naunyn Schmiedebergs Arch Pharmacol 328:331–340
Pernow B (1983) Substance P. Pharmacol. Rev 35:85–141
Porter JP, Ganong WF (1988) VIP and renin secretion. In: Said S (ed) Vasoactive intestinal peptide and related peptides. Ann NY Acad Sci (in press)
Porter JP, Reid IA, Said SI, Ganong WF (1983) Stimulation of renin secretion by vasoactive intestinal peptide. Am J Physiol 234:F306-F310
Porter JP, Said SI, Ganong WF (1984) Vasoactive intestinal peptide stimulates renin secretion in vitro: evidence for a direct action of the peptide on the renal juxtaglomerular cells. Neuroendocrinology 36:404–408
Quirion R, Gaudreau P, St-Pierre S, Rioux F (1982) Localization of neurotensin binding sites in rat kidney. Peptides 3:765–769
Reinecke M (1985) Neurotensin. Immunohistochemical localization in central and peripheral nervous system and in endocrine cells and its functional role as neurotransmitter and endocrine hormone Prog Histochem Cytochem 16:1–175
Reinecke M (1987a) Neurotensin in the human fallopian tube: immunohistochemical localization and effects of synthetic neurotensin on motor activity in vitro. Neurosci Lett 73:220–224
Reinecke M (1987b) Substance P is a vasoactive hormone in the atlantic hagfish Myxine glutinosa (Cyclostomata). Gen Comp Endocrinol 66:291–296
Reinecke M, Forssmann WG (1988) Peptidergic innervation of the coronary vessels. In: Burnstock G, Griffiths S (eds) Nonadrenergic non-cholinergic innervation. CRC Press, Bocca Raton
Reinecke M, Schlüter P, Yanaihara N, Forssmann WG (1981) VIP immunoreactivity in enteric nerves and endocrine cells of the vertebrate gut. Peptides 2 (Suppl 2):149–156
Rioux F, Kérouac R, St-Pierre S (1982) Analysis of the biphasic depressor-pressor effect and tachycardia caused by neurotensin in ganglion-blocked rats. Neuropeptides 3:361–172
Rosenfeld MG, Mermod JJ, Amara SG, Swanson IW, Sawchenko PE, Rivier J, Vale WW, Evans RM (1983) Production of a novel neuropeptide encoded by the calcitonin gene via tissuespecific RNA processing. Nature 304:129–135
Saria A, Lundberg JM, Hua X, Lembeck F (1983) Capsaicin-induced substance P release and sensory control of vascular permeability in the guinea pig ureter. Neurosci Lett 41:167–172
Sternberger LA (1979) Immunocytochemistry. Prentice-Hall, Englewood Cliffs, NJ
Tuchscherer MM, Seybold VS (1985) Immunohistochemical studies of substance P, cholecystokinin-octapeptide and somatostatin in dorsal root ganglia of the rat. Neuroscience 14:593–605
Wharton J, Gulbenkian S, Mulderry PK, Ghatei MA, McGregor GP, Bloom SR, Polak J (1986) Capsaicin induces a depletion of calcitonin gene-related peptide (CGRP-immunoreactive nerves in the cardiovascular system of the guinea pig and rat. J Auton Nerv Syst 16:289–309
Wiesenfeld-Hallin Z, Hökfelt T, Lundberg JM, Forssmann WG, Reinecke M, Tschopp FA, Fischer J (1984) Immunoreactive calcitonin gene-related peptide and substance P coexist in sensory neurones and interact in spinal bahavioral responses. Neurosci Lett 52:199–204
Zanchetti A, Stella A, Golin R, Genovesi S (1984) Neural control of the kidney-are there reno-renal reflexes? Clin Exp Hypertens [A] 6:275–286
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Dedicated to Prof. Dr. T.H. Schiebler on the occasion of his 65th birthday
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Reinecke, M., Forssmann, W.G. Neuropeptide (neuropeptide Y, neurotensin, vasoactive intestinal polypeptide, substance P, calcitonin gene-related peptide, somatostatin) immunohistochemistry and ultrastructure of renal nerves. Histochemistry 89, 1–9 (1988). https://doi.org/10.1007/BF00496578
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DOI: https://doi.org/10.1007/BF00496578