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Peptide-containing nerve fibers in the respiratory tract of the ferret

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Summary

The ferret is widely used in functional and neuromorphological studies on the respiratory tract. We have examined the occurrence and distribution of peptide-containing and adrenergic nerve fibers (using dopamine-β-hydroxylase as a marker). Adrenergic nerve fibers and fibers storing vasoactive intestinal peptide have a widespread distribution along the entire respiratory tract. Adrenergic nerve fibers were found in the lamina propria, as well as around blood vessels and glands and in smooth muscle. Nerve fibers storing vasoactive intestinal peptide occurred in the epithelium, the lamina propria, around blood vessels and glands, and among muscle bundles. Substance P-, neurokinin A- and calcitonin gene-related peptide-containing nerve fibers predominated beneath and within the epithelium along the entire respiratory tract. Neuropeptide Y-containing nerve fibers were prominent among smooth muscle bundles and around glands. The blood vessels in the wall of the airways were richly supplied with peptidecontaining nerve fibers and adrenergic fibers. Ganglia located over the outer or dorsal surface of the tracheal wall harbored vasoactive intestinal peptide-containing nerve cell bodies. Substance P and neurokinin A invariably coexisted in the same nerve fibers. Further, coexistence of substance P/neurokinin A and calcitonin gene-related peptide was observed in the nerve fibers associated with the epithelium. Vasoactive intestinal peptide, neuropeptide Y and occasionally also substance P coexisted in the population of nerve fibers associated with blood vessels and smooth muscle. Many adrenergic nerve fibers contained neuropeptide Y.

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References

  • Al-Hadithi BAK, Stauber V, Mitchell J (1988) The co-localization of substance P and VIP in cholinergic-type terminals of the rat parotid gland. J Anat 159:83–92

    Google Scholar 

  • Alumets J, Håkanson R, Sundler F, Chang K-J (1978) Leu-enkephalin-like material in nerves and enterochromaffin cells in the gut. Histochemistry 56:187–196

    Google Scholar 

  • Baker DG, Basbaum CB, Herbert D, Mitchell RA (1983) Transmission in airway ganglia of ferrets: Inhibition by norepinephrine. Neurosci Lett 41:139–143

    Google Scholar 

  • Baker DG, McDonald DM, Basbaum CB, Mitchell RA (1986) The architecture of nerves and ganglia of the ferret trachea as revealed by acetylcholinesterase histochemistry. J Comp Neurol 246:513–526

    Google Scholar 

  • Barber WH, Small PA (1977) Construction of an improved tracheal pouch in the ferret. Am Rev Respir Dis 115:165–169

    Google Scholar 

  • Barnes PJ (1987) Regulatory peptides in the respiratory system. Experientia 43:832–839

    Google Scholar 

  • Basbaum CB, Veki I, Brezina L, Nadel JA (1981) Tracheal submucosal gland serous cells stimulated in vitro with adrenergic and cholinergic agonists. Cell Tissue Res 220:481–488

    Google Scholar 

  • Borson DB, Chinn RA, Davis B, Nadel JA (1980) Adrenergic and cholinergic nerves mediate fluid secretion from tracheal glands of ferrets. J Appl Physiol 49:1027–1031

    Google Scholar 

  • Borson DB, Corrales R, Varsano S, Gold M, Viro N, Caughey G, Ramachandran J, Nadel JA (1987) Enkephalinase inhibitors potentiate substance P-induced secretion of 35SO4-macromolecules from ferret trachea. Exp Lung Res 12:21–36

    Google Scholar 

  • Cameron AR, Coburn RF (1982) Calcium dependence of the after hyperpolarization of type-A cells of the ferret paratracheal ganglion. Fed Proc 41:1356

    Google Scholar 

  • Cameron AR, Coburn RF (1984) Electrical and anatomic characteristics of cells of ferret paratracheal ganglion. Am J Physiol 24:450–458

    Google Scholar 

  • Cheung A, Polak JM, Bauer FE, Cadieux A, Christofides ND, Springall DR, Bloom SR (1985) Distribution of galanin immunoreactivity in the respiratory tract of pig, guinea-pig, rat and dog. Thorax 40:889–896

    Google Scholar 

  • Coburn RF (1984a) Neural coordination of excitation of ferret trachealis muscle. Am J Physiol 246:459–466

    Google Scholar 

  • Coburn RF (1984b) The anatomy of the ferret paratracheal parasympathetic nerve ganglion plexus. Exp Lung Res 7:1–9

    Google Scholar 

  • Costa M, Furness JB, Gibbins IL (1986) Chemical coding of enteric neurons. Prog in Brain Res 68:217–239

    Google Scholar 

  • Dahlström A, Fuxe K, Hökfelt T, Norberg K-A (1966) Adrenergic innervation of the bronchial muscle of the cat. Acta Physiol Scand 66:507–508

    Google Scholar 

  • Dey RD, Shannon WA Jr, Said SI (1981) Localization of VIP-immunoreactive nerves in airways and pulmonary vessels of dogs, cats and human subjects. Cell Tissue Res 220:231–238

    Google Scholar 

  • Dey RD, Hoffpaur J, Said SI (1988) Co-localization of vasoactive intestinal peptide- and substance P-containing nerves in cat bronchi. Neuroscience 24:275–281

    Google Scholar 

  • Ekblad E, Håkanson R, Sundler F (1984) VIP and PHI coexist with an NPY-like peptide in intramural neurones of the small intestine. Regul Pept 10:47–55

    Google Scholar 

  • Ekblad E, Rökaeus Å, Håkanson R, Sundler F (1985) Galanin nerve fibers in the rat gut: distribution, origin and projections. Neuroscience 16:355–363

    Google Scholar 

  • Gabella G (1987) Innervation of airway smooth muscle: fine structure. Annu Rev Physiol 49:583–594

    Google Scholar 

  • Gibbins IL, Furness JB, Costa M (1987) Pathway — specific patterns of the coexistence of substance P, calcitonin gene-related peptide, cholecystokinin and dynorphin in neurons of the dorsal root ganglia of the guinea-pig. Cell Tissue Res 248:417–437

    Google Scholar 

  • Grunditz T, Håkanson R, Rerup C, Sundler F, Uddman R (1984) Neuropeptide Y in the thyroid gland: neuronal localization and enhancement of stimulated thyroid hormone secretion. Endocrinology 115:1537–1542

    Google Scholar 

  • Grunditz T, Håkanson R, Hedge G, Rerup C, Sundler F, Uddman R (1986) Peptide histidine isoleucine amide stimulates thyroid hormone secretion and coexists with vasoactive intestinal polypeptide in intrathyroid nerve fibers from laryngeal ganglia. Endocrinology 118:783–790

    Google Scholar 

  • Grunditz T, Ekman R, Håkanson R, Sundler F, Uddman R (1988) Neuropeptide Y and vasoactive intestinal peptide coexist in thyroid nerve fibers emanating from the thyroid ganglion. Regul Pept 23:193–208

    Google Scholar 

  • Håkanson R, Sundler F, Mogimzadeh E, Leander S (1983) Peptide containing nerve fibers in the airways: distribution and functional implications. Eur J Respir Dis [Suppl] 64:115–140

    Google Scholar 

  • Kyle H, Widdicombe JG (1987) The effects of peptides and mediaors on mucus secretion rate and smooth muscle tone in the ferret trachea. Agents Actions 22:86–90

    Google Scholar 

  • Laitinen LA, Eränkö L, Laitinen A, Panula P, Tervo K, Tervo T (1982) Substance P immunoreaction in the pulmonary tissue. Bull Int Union Tuberc 57:52

    Google Scholar 

  • Leah JD, Cameron AR, Kelly WL, Snow PS (1985) Coexistence of peptide immunoreactivity in sensory neurons of the cat. Neuroscience 16:683–690

    Google Scholar 

  • Lorén I, Alumets J, Håkanson R, Sundler F (1979) Distribution of gastrin and CCK-like peptides in rat brain. Immunocytochemical study. Histochemistry 59:249–257

    Google Scholar 

  • Lundberg JM, Terenius L, Hökfelt T, Martling C-R, Tatemoto K, Mutt V, Polak J, Bloom SR, Goldstein M (1982) Neuropeptide Y (NPY)-like immunoreactivity in peripheral noradreneric neurons and effects of NPY on sympathetic function. Acta Physiol Scand 116:477–480

    Google Scholar 

  • Lundberg JM, Hökfelt T, Martling C-R, Saria A, Cuello C (1984) Substance P-immunoreactive sensory nerves in the lower respiratory tract of various mammals including man. Cell Tissue Res 235:251–261

    Google Scholar 

  • Lundberg JM, Franco-Cereceda A, Hua X-Y, Hökfelt T, Fischer J (1985) Co-existence of substance P and calcitonin gene-related peptide immunoreactivities in sensory nerves in relation to cardiovascular and bronchoconstrictor effects of capsaicin. Eur J Pharmacol 108:315–319

    Google Scholar 

  • Martling C-R, Saria A, Fischer J, Hökfelt T, Lundberg JM (1988) Calcitonin gene-related peptide and the lung: neuronal coexistence with substance P, release by capsaicin and vasodilatory effect. Regul Pept 20:125–139

    Google Scholar 

  • Morris JL, Gibbins JL, Furness JB, Costa M, Murphy R (1985) Co-localization of neuropeptide Y, vasoactive intestinal polypeptide and dynorphin in non-adrenergic axons of the guineaig uterine artery. Neurosci Lett 62:31–37

    Google Scholar 

  • Peatfield AC, Barnes PJ, Bracher C, Nadel JA, Davis B (1983) Vasoactive intestinal peptide stimulates tracheal submucosal gland secretion in ferret. Am Rev Respir Dis 128:89–93

    Google Scholar 

  • Polak JM, Bloom SR (1982) Distribution of regulatory peptides in the respiratory tract of man and mammals. In: Bloom SR, Polak JM, Lindenlaub E (eds) Systemic role of regulatory peptides. FK Schattauer Verlag, Stuttgart, pp 241–269

    Google Scholar 

  • Rush RA, Geffen LB (1980) Dopamine-β-hydroxylase in health and disease. CRC Crit Rev Clin Lab Sci 12:261–265

    Google Scholar 

  • Sheppard MN, Polak JM, Allen JM, Bloom SR (1984) Neuropeptide tyrosine (NPY): a newly discovered peptide is present in mammalian respiratory tract. Thorax 39:326–330

    Google Scholar 

  • Sundler F, Alumets J, Brodin E, Dahlberg K, Nilsson G (1977a) Perivascular substance P-immunoreactive nerves in tracheobronchial tissue. In: Euler US von, Pernow B (eds) Substance P. Raven Press, New York, pp 271–273

    Google Scholar 

  • Sundler F, Håkanson R, Hammer RA, Alumets J, Carraway R, Leeman SE, Zimmerman EA (1977b) Immunohistochemical localization of neurotensin in endocrine cells of the gut. Cell Tissue Res 178:313–321

    Google Scholar 

  • Sundler F, Brodin E, Ekblad E, Håkanson R, Uddman R (1985) Sensory nerve fibers: distribution of substance P, neurokinin A and calcitonin gene-related peptide. In: Håkanson R, Sundler F (eds) Tachykinin antagonists. Elsevier, Amsterdam, pp 3–14

    Google Scholar 

  • Sundler F, Håkanson R, Ekblad E, Uddman R, Wahlestedt C (1986) Neuropeptide Y in the peripheral adrenergic and enteric nervous systems. Int Rev Cytol 102:243–269

    Google Scholar 

  • Sundler F, Ekblad E, Grunditz T, Håkanson R, Luts A, Uddman R (1989) NPY in peripheral non-adrenergic neurons. In: Mutt V, Hökfelt T, Fuxe K (eds) Nobel Symposium XIV: neuropeptide Y. Raven Press, New York, in press

    Google Scholar 

  • Tramu G, Pillez A, Leonardelli J (1978) An efficient method of antibody elution for the successive or simultaneous localization of two antigens by immunocytochemistry. J Histochem Cytochem 26:322–324

    Google Scholar 

  • Uddman R, Alumets J, Densert O, Håkanson R, Sundler F (1978) Occurrence and distribution of VIP nerves in the nasal mucosa and tracheobronchial wall. Acta Otolaryngol (Stockh) 86:443–448

    Google Scholar 

  • Uddman R, Malm L, Sundler F (1980) The origin of vasoactive intestinal polypeptide (VIP) nerves in the feline nasal mucosa. Acta Otolaryngol (Stockh) 89:152–156

    Google Scholar 

  • Uddman R, Malm L, Sundler F (1981) Peptide containing nerves in the nasal mucosa. Rhinology 19:75–79

    Google Scholar 

  • Uddman R, Moghimzadeh E, Sundler F (1984a) Occurrence and distribution of GRP-immunoreactive nerve fibers in the respiratory tract. Arch Otorhinolaryngol 239:145–151

    Google Scholar 

  • Uddman R, Sundler F, Emson P (1984b) Occurrence and distribution of neuropeptide Y-immunoreactive nerves in the respiratory tract and middle ear. Cell Tissue Res 237:321–327

    Google Scholar 

  • Uddman R, Luts A, Sundler F (1985b) Occurrence and distribution of calcitonin gene-related peptide in the mammalian respiratory tract and middle ear. Cell Tissue Res 241:551–555

    Google Scholar 

  • Yanaihara N, Yanaihara L, Mochizuki T, Imura K, Fujita T, Iwanaga T (1981) Immunoreactive GRP. Peptides 2 (Suppl 2) 185–192

    Google Scholar 

  • Webber SE (1988) The effects of peptide histidine isoleucine and neuropeptide Y on mucus volume output from the ferret trachea. Br J Pharmacol 95:49–54

    Google Scholar 

  • Webber SE, Widdicombe JG (1987a) The effect of vasoactive intestinal peptide on mucus secretion from the ferret in vitro trachea. J Physiol (Lond) 384:65

    Google Scholar 

  • Webber SE, Widdicombe JG (1987b) The effect of vasoactive intestinal peptide on smooth muscle tone and mucus secretion from the ferret trachea. Br J Pharmacol 91:139–148

    Google Scholar 

  • Webber SE, Tatar M, Breen M, Widdicombe JG (1987) The effects of PHI and NPY on the volume output of mucus from the ferret in vitro trachea. Br Eur Phys 23:363

    Google Scholar 

  • Wharton J, Polak JM, Bloom SR, Will JA, Pearse AGE (1979) Substance P-like immunoreactive nerves in mammalian lung. Invest Cell Pathol 2:3–10

    Google Scholar 

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Luts, A., Sundler, F. Peptide-containing nerve fibers in the respiratory tract of the ferret. Cell Tissue Res. 258, 259–267 (1989). https://doi.org/10.1007/BF00239446

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