Expression of tyrosine hydroxylase and neuropeptide tyrosine in mouse sympathetic airway-specific neurons under normal situation and allergic airway inflammation
Q. T. Dinh
Department of Internal Medicine,
Clinical Research Unit of Allergy and
Search for more papers by this authorC. Witt
Department of Pneumology, Charité School of Medicine, Humboldt University, Berlin, Germany
Search for more papers by this authorN. Frossard
INSERM U 425, Pulmonary Neuroimmunopharmacology, University of Strasbourg, Illkirch, Strasbourg, France
Search for more papers by this authorQ. T. Dinh
Department of Internal Medicine,
Clinical Research Unit of Allergy and
Search for more papers by this authorC. Witt
Department of Pneumology, Charité School of Medicine, Humboldt University, Berlin, Germany
Search for more papers by this authorN. Frossard
INSERM U 425, Pulmonary Neuroimmunopharmacology, University of Strasbourg, Illkirch, Strasbourg, France
Search for more papers by this authorSummary
Background The traditional neurotransmitter catecholamine and the neuropeptide tyrosine in sympathetic airway nerves have been proposed to be involved in the pathogenesis of airway diseases.
Objective The aim of the present study was to investigate the effect of allergic airway inflammation on the expression of catecholamine enzyme tyrosine hydroxylase (TH), neuropeptide tyrosine (NPY) and tachykinins in mouse sympathetic airway ganglia.
Methods Using neuronal tracing in combination with immunohistochemistry, the present study was designed to characterize TH, NPY and tachykinin profiles of superior cervical (SCG) and stellate ganglia after allergen challenge.
Results The vast majority of fast blue-labelled SCG neurons (allergen: 97.5±1.22% (mean±SEM) vs. controls: 94.5±1.48%, P=0.18) and stellate neurons (allergen: 95.3±1.01% vs. controls: 93.6±1.33%, P=0.34) were immunoreactive for TH. Of the TH immunoreactive and fast blue-labelled SCG neurons, 52.0±1.01% allergen vs. 51.2±3.58% controls (P=0.83) and stellate neurons, 57.3%±0.97 allergen vs. 56.4±1.65% controls (P=0.64) were positive for TH only but not NPY, whereas 45.3±1.05% allergen vs. 43.3±1.18% controls (P=0.47) of fast blue-labelled SCG neurons and 37.9±0.86% allergen vs. 37.1±1.24% controls (P=0.62) of fast blue-labelled stellate neurons were immunoreactive for both TH and NPY immunoreactivities. There was a trend of an increase, but not significant one, in the percentage of TH-/NPY-immunoreactive and fast blue-labelled neurons in allergen-treated animals in comparison with the controls. Tachykinins, however, were not expressed by sympathetic neurons and were also not induced in sympathetic neurons after allergen challenge.
Conclusion The present study indicates that allergic airway inflammation does not alter the expression of noradrenalin and NPY in sympathetic ganglia and also shows that sympathetic neurons do not respond to allergic airway inflammation with tachykinins induction. However, a participation of catecholamine and NPY in the pathogenesis of allergic airway inflammation cannot be excluded in the present study as a higher neurotransmitter output per neuron following allergen challenge could be possible.
References
- 1 De Jongste JC, Jongejan RC, Kerrebijn KF. Control of airway caliber by autonomic nerves in asthma and in chronic obstructive pulmonary disease. Am Rev Respir Dis 1991; 143: 1421–6.
- 2 Canning BJ, Fischer A. Neural regulation of airway smooth muscle tone. Respir Physiol 2001; 125: 113–27.
- 3 Belvisi MG, Miura M, Stretton D, Barnes PJ. Endogenous vasoactive intestinal peptide and nitric oxide modulate cholinergic neurotransmission in guinea-pig trachea. Eur J Pharmacol 1993; 231: 97–102.
- 4 Belvisi MG, Stretton CD, Yacoub M, Barnes PJ. Nitric oxide is the endogenous neurotransmitter of bronchodilator nerves in humans. Eur J Pharmacol 1992; 210: 221–2.
- 5 Belvisi MG, Ward JK, Mitchell JA, Barnes PJ. Nitric oxide as a neurotransmitter in human airways. Arch Int Pharmacodyn Ther 1995; 329: 97–110.
- 6 Lacroix JS, Anggard A, Hokfelt T, O'Hare MM, Fahrenkrug J, Lundberg JM. Neuropeptide Y: presence in sympathetic and parasympathetic innervation of the nasal mucosa. Cell Tissue Res 1990; 259: 119–28.
- 7 Matran R. Neural control of lower airway vasculature. Involvement of classical transmitters and neuropeptides. Acta Physiol Scand 1991; 601 (Suppl.): 1–54.
- 8 Baraniuk JN, Silver PB, Kaliner MA, Barnes PJ. Neuropeptide Y is a vasoconstrictor in human nasal mucosa. J Appl Physiol 1992; 73: 1867–72.
- 9 Cervin A, Onnerfalt J, Edvinsson L, Grundemar L. Functional effects of neuropeptide Y receptors on blood flow and nitric oxide levels in the human nose. Am J Respir Crit Care Med 1999; 160: 1724–8.
- 10 Fischer A, Mayer B, Kummer W. Nitric oxide synthase in vagal sensory and sympathetic neurons innervating the guinea-pig trachea. J Auton Nerve Systems 1996; 56: 157–60.
- 11 Myers AC, Kajekar R, Undem BJ. Allergic inflammation-induced neuropeptide production in rapidly adapting afferent nerves in guinea pig airways. Am J Physiol Lung Cell Mol Physiol 2002; 282: 775–81.
- 12 Hunter DD, Myers AC, Undem BJ. Nerve growth factor-induced phenotypic switch in guinea pig airway sensory neurons. Am J Respir Crit Care Med 2000; 161: 1985–90.
- 13 Jonakait GM. Neural-immune interactions in sympathetic ganglia. Trends Neurosci 1993; 16: 419–23.
- 14 Pabst R. Animal models for asthma: controversial aspects and unsolved problems. Pathobiology 2002; 70: 252–4.
- 15 Springer J, Wagner S, Subramamiam A, McGregor GP, Groneberg DA, Fischer A. BDNF-overexpression regulates the reactivity of small pulmonary arteries to neurokinin A. Regul Pept 2004; 118: 19–23.
- 16 Kumar RK, Foster PS. Modeling allergic asthma in mice: pitfalls and opportunities. Am J Respir Cell Mol Biol 2002; 27: 267–72.
- 17 Rubio-Aliaga I, Frey I, Boll M et al. Targeted disruption of the peptide transporter Pept2 gene in mice defines its physiological role in the kidney. Mol Cell Biol 2003; 23: 3247–52.
- 18 Kerzel S, Path G, Nockher WA et al. Pan-neurotrophin receptor p75 contributes to neuronal hyperreactivity and airway inflammation in a murine model of experimental asthma. Am J Respir Cell Mol Biol 2003; 28: 170–8.
- 19 Fischer A, McGregor GP, Saria A, Philippin B, Kummer W. Induction of tachykinin gene and peptide expression in guinea pig nodose primary afferent neurons by allergic airway inflammation. J Clin Invest 1996; 98: 2284–91.
- 20 Fischer A, Mundel P, Mayer B, Preissler U, Philippin B, Kummer W. Nitric oxide synthase in guinea pig lower airway innervation. Neurosci Lett 1993; 149: 157–60.
- 21 Kummer W, Fischer A, Kurkowski R, Heym C. The sensory and sympathetic innervation of guinea-pig lung and trachea as studied by retrograde neuronal tracing and double-labelling immunohistochemistry. Neuroscience 1992; 49: 715–37.
- 22
Wallis D,
Watson AH,
Mo N.
Cardiac neurones of autonomic ganglia.
Microsc Res Technol
1996; 35: 69–79.
10.1002/(SICI)1097-0029(19960901)35:1<69::AID-JEMT6>3.0.CO;2-N CAS PubMed Web of Science® Google Scholar
- 23 Ganguly PK, Sherwood GR. Noradrenaline turnover and metabolism in myocardium following aortic constriction in rats. Cardiovasc Res 1991; 25: 579–85.
- 24 Fuller BC, Sumner AD, Kutzler MA, Ruiz-Velasco V. A novel approach employing ultrasound guidance for percutaneous cardiac muscle injection to retrograde label rat stellate ganglion neurons. Neurosci Lett 2004; 363: 252–6.
- 25 Larsson K, Hjemdahl P. Sympatho-adrenal activity is assessed in patients with asthma by measurements of catecholamines and neuropeptide Y-like immunoreactivity (NPY-LI) in venous plasma. Pulm Pharmacol 1989; 2: 167–8.
- 26 Barnes PJ. Neural control of human airways in health and disease. Am Rev Respir Dis 1986; 134: 1289–314.
- 27 Franco-Cereceda A, Matran R, Alving K, Lundberg JM. Sympathetic vascular control of the laryngeo-tracheal, bronchial and pulmonary circulation in the pig: evidence for non-adrenergic mechanisms involving neuropeptide Y. Acta Physiol Scand 1995; 155: 193–204.
- 28 Fujiwara H, Kurihara N, Hirata K, Ohta K, Kanazawa H, Takeda T. Effect of neuropeptide Y on human bronchus and its modulation of neutral endopeptidase. J Allergy Clin Immunol 1993; 92: 89–94.
- 29 Uddman R, Sundler F, Emson P. Occurrence and distribution of neuropeptide-Y-immunoreactive nerves in the respiratory tract and middle ear. Cell Tissue Res 1984; 237: 321–7.
- 30
Ind PW.
Role of the sympathetic nervous system and endogenous catecholamines in the regulation of the airways smooth muscle tone. In:
D Raebum,
M Gymbiecz, eds.
Airways smooth muscle: structure, innervation and neurotransmission. Basel: Birkhauser Verlag, 1994; 29–41.
10.1007/978-3-0348-7558-5_2 Google Scholar
- 31 Sheppard MN, Polak JM, Allen JM, Bloom SR. Neuropeptide tyrosine (NPY): a newly discovered peptide is present in the mammalian respiratory tract. Thorax 1984; 39: 326–30.
- 32 Goldie RG, Paterson JW, Lulich KM. Adrenoceptors in airway smooth muscle. Pharmacol Ther 1990; 48: 295–322.
- 33 Malis DD, Grouzmann E, Morel DR, Mutter M, Lacroix JS. Influence of TASP-V, a novel neuropeptide Y (NPY) Y2 agonist, on nasal and bronchial responses evoked by histamine in anaesthetized pigs and in humans. Br J Pharmacol 1999; 126: 989–96.
- 34
Grundemar L.
Multiple receptors and multiple actions. In:
L Grundemar,
SR Bloom, eds.
Neuropeptide Y and drug development. London: Academic Press, 1997; 1–14.
10.1016/B978-012304990-2/50002-0 Google Scholar
- 35 Gerald C, Walker MW, Criscione L et al. A receptor subtype involved in neuropeptide-Y-induced food intake. Nature 1996; 382: 168–71.
- 36 Nakamura M, Sakanaka C, Aoki Y et al. Identification of two isoforms of mouse neuropeptide Y-Y1 receptor generated by alternative splicing. Isolation, genomic structure, and functional expression of the receptors. J Biol Chem 1995; 270: 30102–10.
- 37
Nakamura M,
Yokoyama M,
Watanabe H,
Matsumoto T.
Molecular cloning, organization and localization of the gene for the mouse neuropeptide Y-Y5 receptor.
Biochim Biophys Acta
1997; 4: 83–9.
10.1016/S0005-2736(97)00131-4 Google Scholar
- 38 Heppt W, Peiser C, Cryer A et al. Innervation of human nasal mucosa in environmentally triggered hyperreflectoric rhinitis. J Occup Environ Med 2002; 44: 924–9.
- 39 Groneberg DA, Heppt W, Cryer A et al. Toxic rhinitis-induced changes of human nasal mucosa innervation. Toxicol Pathol 2003; 31: 326–31.
- 40 Groneberg DA, Heppt W, Welker P et al. Aspirin-sensitive rhinitis-associated changes in upper airway innervation. Eur Respir J 2003; 22: 986–91.
- 41 Kroesen S, Lang S, Fischer-Colbrie R, Klimaschewski L. Plasticity of neuropeptide Y in the rat superior cervical ganglion in response to nerve lesion. Neuroscience 1997; 78: 251–8.
- 42 Chan RK, Sawchenko PE. Differential time- and dose-related effects of haemorrhage on tyrosine hydroxylase and neuropeptide Y mRNA expression in medullary catecholamine neurons. Eur J Neurosci 1998; 10: 3747–58.
- 43 Rutkoski NJ, Lerant AA, Nolte CM, Westberry J, Levenson CW. Regulation of neuropeptide Y in the rat amygdala following unilateral olfactory bulbectomy. Brain Res 2002; 951: 69–76.
- 44 Sun Y, Zigmond RE. Involvement of leukemia inhibitory factor in the increases in galanin and vasoactive intestinal peptide mRNA and the decreases in neuropeptide Y and tyrosine hydroxylase mRNA in sympathetic neurons after axotomy. J Neurochem 1996; 67: 1751–60.
- 45 Ji RR, Zhang X, Wiesenfeld-Hallin Z, Hokfelt T. Expression of neuropeptide Y and neuropeptide Y (Y1) receptor mRNA in rat spinal cord and dorsal root ganglia following peripheral tissue inflammation. J Neurosci 1994; 14: 6423–34.
- 46 Lacroix JS, Mosimann BL. Attenuation of allergen-evoked nasal responses by local pretreatment with exogenous neuropeptide Y in atopic patients. J Allergy Clin Immunol 1996; 98: 611–6.
- 47 Lacroix JS, Ricchetti AP, Morel D, Mossimann B, Waeber B, Grouzmann E. Intranasal administration of neuropeptide Y in man: systemic absorption and functional effects. Br J Pharmacol 1996; 118: 2079–84.
- 48 Stretton CD, Barnes PJ. Modulation of cholinergic neurotransmission in guinea-pig trachea by neuropeptide Y. Br J Pharmacol 1988; 93: 672–8.
- 49 Stretton CD, Belvisi MG, Barnes PJ. Neuropeptide Y modulates non-adrenergic, non-cholinergic neural bronchoconstriction in vivo and in vitro. Neuropeptides 1990; 17: 163–70.
- 50 Cardell LO, Uddman R, Edvinsson L. Low plasma concentrations of VIP and elevated levels of other neuropeptides during exacerbations of asthma. Eur Respir J 1994; 7: 2169–73.
- 51 Chanez P, Springall D, Vignola AM et al. Bronchial mucosal immunoreactivity of sensory neuropeptides in severe airway diseases. Am J Respir Crit Care Med 1998; 158: 985–90.
- 52 Undem BJ, Hunter DD, Liu M, Haak-Frendscho M, Oakragly A, Fischer A. Allergen-induced sensory neuroplasticity in airways. Int Arch Allergy Immunol 1999; 118: 150–3.
- 53 Ding M, Hart RP, Jonakait GM. Tumor necrosis factor-alpha induces substance P in sympathetic ganglia through sequential induction of interleukin-1 and leukemia inhibitory factor. J Neurobiol 1995; 28: 445–54.
- 54 Shadiack AM, Carlson CD, Ding M, Hart RP, Jonakait GM. Lipopolysaccharide induces substance P in sympathetic ganglia via ganglionic interleukin-1 production. J Neuroimmunol 1994; 49: 51–8.
- 55 Shadiack AM, Hart RP, Carlson CD, Jonakait GM. Interleukin-1 induces substance P in sympathetic ganglia through the induction of leukemia inhibitory factor (LIF). J Neurosci 1993; 13: 2601–9.
- 56 Rao MS, Sun Y, Vaidyanathan U, Landis SC, Zigmond RE. Regulation of substance P is similar to that of vasoactive intestinal peptide after axotomy or explantation of the rat superior cervical ganglion. J Neurobiol 1993; 24: 571–80.
- 57 Hart RP, Shadiack AM, Jonakait GM. Substance P gene expression is regulated by interleukin-1 in cultured sympathetic ganglia. J Neurosci Res 1991; 29: 282–91.