Neuropeptides
Volume 44, Issue 5 , Pages 399-406 , October 2010

Involvement of preprotachykinin A gene-encoded peptides and the neurokinin 1 receptor in endotoxin-induced murine airway inflammation

  • Zsuzsanna Helyes

      Affiliations

    • Department of Pharmacology and Pharmacotherapy, University of Pécs, Hungary
    • Corresponding Author InformationCorresponding author. Address: Department of Pharmacology and Pharmacotherapy, Faculty of Medicine, University of Pécs, H-7624 Pécs, Szigeti u. 12, Hungary. Tel.: +36 72 536 001/5591; fax: +36 72 536 218.
    • ,
  • Krisztián Elekes

      Affiliations

    • Department of Pharmacology and Pharmacotherapy, University of Pécs, Hungary
    • ,
  • Katalin Sándor

      Affiliations

    • Department of Pharmacology and Pharmacotherapy, University of Pécs, Hungary
    • ,
  • István Szitter

      Affiliations

    • Department of Pharmacology and Pharmacotherapy, University of Pécs, Hungary
    • ,
  • László Kereskai

      Affiliations

    • Department of Pathology, University of Pécs, Hungary
    • ,
  • Erika Pintér

      Affiliations

    • Department of Pharmacology and Pharmacotherapy, University of Pécs, Hungary
    • ,
  • Ágnes Kemény

      Affiliations

    • Department of Pharmacology and Pharmacotherapy, University of Pécs, Hungary
    • ,
  • János Szolcsányi

      Affiliations

    • Department of Pharmacology and Pharmacotherapy, University of Pécs, Hungary
    • ,
  • Lynn McLaughlin

      Affiliations

    • School of Biomedical Sciences, Liverpool University, Liverpool, UK
    • ,
  • Sylvia Vasiliou

      Affiliations

    • School of Biomedical Sciences, Liverpool University, Liverpool, UK
    • ,
  • Anja Kipar

      Affiliations

    • School of Veterinary Science, University of Liverpool, UK
    • ,
  • Andreas Zimmer

      Affiliations

    • Institute of Molecular Psychiatry, University of Bonn, Germany
    • ,
  • Stephen P. Hunt

      Affiliations

    • Research Department of Cell and Developmental Biology, University College London, UK
    • ,
  • James P. Stewart

      Affiliations

    • School of Infection and Host Defence, University of Liverpool, UK
    • ,
  • John P. Quinn

      Affiliations

    • School of Biomedical Sciences, Liverpool University, Liverpool, UK

Received 5 February 2010 ,Accepted 28 May 2010.

References 

  1. Advenier C, Lagente V, Boichot E. The role of tachykinin receptor antagonists in the prevention of bronchial hyper responsiveness, airway inflammation and cough. Eur. Respir. J. 1997;10:1892–1906
  2. Barnes PJ. Neurogenic inflammation in airways and its modulation. Arch. Int. Pharmacodyn. Ther. 1990;303:67–82
  3. Barnes PJ. Potential novel therapies for chronic obstructive pulmonary disease. Novartis. Found. Symp. 2001;234:255–267
  4. Colasurdo GN, Loader JE, Graves JP, Larsen GL. Modulation of acetylcholine release in rabbit airways in vitro. Am. J. Physiol. 1995;268:L432–L437
  5. De Felipe C, Herrero JF, O’Brien JA, Palmer JA, Doyle CA, Smith AJ, et al. Altered nociception, analgesia and aggression in mice lacking the receptor for substance P. Nature. 1998;392:394–397
  6. DeRose V, Robbins RA, Snider RM, Spurzem JR, Thiele GM, Rennard SI, et al. Substance P increases neutrophil adhesion to bronchial epithelial cells. J. Immunol. 1994;152:1339–1346
  7. De Swert KO, Bracke KR, Demoor T, Brusselle GG, Joos GF. Role of the tachykinin NK1 receptor in a murine model of cigarette smoke-induced pulmonary inflammation. Respir. Res. 2009;10:37–44
  8. Dib M, Zsengeller Z, Mitsialis A, Lu B, Craig S, Gerard C, et al. A paradoxical protective role for the proinflammatory peptide substance P receptor (NK1R) in acute hyperoxic lung injury. Am. J. Physiol. Lung Cell Mol. Physiol. 2009;297:L687–L697
  9. Elekes K, Helyes Z, Nemeth J, Sandor K, Pozsgai G, Kereskai L, et al. Role of capsaicin-sensitive afferents and sensory neuropeptides in endotoxin-induced airway inflammation and consequent bronchial hyperreactivity in the mouse. Regul. Pept. 2007;141:44–54
  10. Frossard N, Advenier C. Tachykinin receptors and the airways. Life Sci. 1991;49:1941–1953
  11. Groneberg DA, Harrison S, Dinh QT, Geppetti P, Fischer A. Tachykinins in the respiratory tract. Curr. Drug Targets. 2006;7:1005–1010
  12. Hastings RH, Hua XY. Expression of calcitonin gene-related peptide by cultured rat alveolar type II cells. Am. J. Respir. Cell Mol. Biol. 1995;13:563–569
  13. Helyes Zs, Elekes K, Nemeth J, Pozsgai G, Sandor K, Kereskai L, et al. Role of transient receptor potential vanilloid 1 receptors in endotoxin-induced airway inflammation in the mouse. Am. J. Physiol. Lung Cell Mol. Physiol. 2007;292:L1173–L1181
  14. Helyes Z, Pinter E, Sandor K, Elekes K, Banvolgyi A, Keszthelyi D, et al. Impaired defense mechanism against inflammation, hyperalgesia, airway hyperreactivity in somatostatin 4 receptor gene-deleted mice. Proc. Natl. Acad. Sci. USA. 2009;106:13088–13093
  15. Joos GF, De Swert KO, Pauwels RA. Airway inflammation and tachykinins: prospects for the development of tachykinin receptor antagonists. Eur. J. Pharmacol. 2001;429:239–250
  16. Kraneveld AD, Nijkamp FP. Tachykinins and neuro-immune interactions in asthma. Int. Immunopharmacol. 2001;1:1629–1650
  17. Kurtz MM, Wang R, Clements MK, Cascieri MA, Austin CP, Cunningham BR, et al. Identification, localization and receptor characterization of novel mammalian substance P-like peptides. Gene. 2002;296:205–212
  18. Ladenius AR, Folkerts G, van der Linde HJ, Nijkamp FP. Potentiation by viral respiratory infection of ovalbumin-induced guinea-pig tracheal hyperresponsiveness: role for tachykinins. Br. J. Pharmacol. 1995;115:1048–1052
  19. Lagente V, Advenier C. Tachykinins and airway function. Pulm. Pharmacol. Ther. 1998;11:331–340
  20. Laird JM, Olivar T, Roza C, De Felipe C, Hunt SP, Cervero F. Deficits in visceral pain and hyperalgesia of mice with a disruption of the tachykinin NK1 receptor gene. Neuroscience. 2000;98:345–352
  21. Lefort J, Motreff L, Vargaftig BB. Airway administration of Escherichia coli endotoxin to mice induces glucocorticosteroid-resistant bronchoconstriction and vasopermeation. Am. J. Respir. Cell Mol. Biol. 2001;24:345–351
  22. Li W, Hou L, Hua Z, Wang X. Interleukin-1beta induces beta-calcitonin gene-related peptide secretion in human type II alveolar epithelial cells. FASEB J. 2004;18:1603–1605
  23. Lundberg JM. Tachykinins, sensory nerves, and asthma-an overview. Can. J. Physiol. Pharmacol. 1995;73:908–914
  24. Maggi CA. Tachykinins and calcitonin gene-related peptide (CGRP) as co- transmitters released from peripheral endings of sensory nerves. Prog. Neurobiol. 1995;45:1–98
  25. Maggi CA, Schwartz TW. The dual nature of the tachykinin NK1 receptor. Trends Pharmacol. Sci. 1997;18:351–355
  26. Nelson DA, Bost KL. Non-neuronal mammalian tachykinin expression. Front Biosci. 2004;9:2166–2176
  27. Ng SW, Zhang H, Hedge A, Bhatia M. Role of preprotachykinin-A gene-products on multiple organ injury in LPS-induced endotoxinaemia. J. Leuk. Biol. 2008;83:288–296
  28. Okamoto T, Gohil K, Finkelstein EI, Bove P, Akaike T, van den der Vliet A. Multiple contributing roles for NOS2 in LPS-induced acute airway inflammation in mice. Am. J. Physiol. Lung Cell Mol. Physiol. 2004;286:198–209
  29. Oslund KL, Hyde DM, Putney LF, Alfaro MF, Walby WF, Tyler NK, et al. Activation of neurokinin-1 receptors during ozone inhalation contributes to epithelial injury and repair. Am. J. Respir. Cell Mol. Biol. 2008;39:279–288
  30. Page NM. Hemokinins and endokinins. Cell Mol. Life Sci. 2004;61:1652–1663
  31. Page NM. New challenges in the study of the mammalian tachykinins. Peptides. 2005;26:1356–1368
  32. Page NM. Characterization of the gene structures, precursor processing and pharmacology of the endokinin peptides. Vascul. Pharmacol. 2006;45:200–208
  33. Page NM, Bell NJ, Gardiner SM, Manyonda IT, Brayley KJ, Strange PG, et al. Characterization of the endokinins: human tachykinins with cardiovascular activity. Proc. Natl. Acad. Sci. USA. 2003;100:6245–6250
  34. Ping-Chia L, Ju L, Yu-Ching L, Li-Ching C, Wen-Chung C. Substance P scavenger enhances antioxidant defenses and prevents prothrombotic effects on the rat lung after acute exposure to oil smoke. J. Biomed. Sci. 2009;16:58–64
  35. Prado CM, Leick-Maldonado EA, Miyamoto L, Yano LM, Kasahara DI, Martins MA, et al. Capsaicin-sensitive nerves and neurokinins modulate non-neuronal nNOS expression in lung. Respir. Physiol. Neurobiol. 2008;160:37–44
  36. Regoli D, Boudon A, Fauchere JL. Receptors and antagonists for substance P and related peptides. Pharmacol. Rev. 1994;46:551–599
  37. Rennick RE, Loesch A, Burnstock G. Endothelin, vasopressin, and substance P like immunoreactivity in cultured and intact epithelium from rabbit trachea. Thorax. 1992;47:1044–1049
  38. Rocksen D, Ekstrand-Hammarstrom B, Johansson L, Bucht A. Vitamin E reduces transendothelial migration of neutrophils and prevents lung injury in endotoxin-induced airway inflammation. Am. J. Respir. Cell Mol. Biol. 2003;28:199–207
  39. Savov JD, Gavett SH, Brass DM, Costa DL, Schwartz DA. Neutrophils play a critical role in development of LPS-induced airway disease. Am. J. Physiol. Lung Cell Mol. Physiol. 2002;283:L952–L962
  40. Springer J, Geppetti P, Fischer A, Groneberg DA. Calcitonin gene-related peptide as inflammatory mediator. Pulm. Pharmacol. Ther. 2003;16:121–130
  41. Stewart JP, Kipar A, Cox H, Payne C, Vasiliou S, Quinn JP. Induction of tachykinin production in airway epithelia in response to viral infection. PLoS. One. 2008;3:e1673
  42. Szolcsanyi, J., 1996. Neurogenic inflammation: reevaluation of axon reflex theory. In: Geppetti, P., Holzer, P. (Eds.), Neurogenic Inflammation. pp. 33–42.
  43. Szolcsanyi J, Bartho L. Capsaicin-sensitive non-cholinergic excitatory innervation of the guinea-pig tracheobronchial smooth muscle. Neurosci. Lett. 1982;34:247–251
  44. Tsuchida H, Takahashi S, Nosaka E, Kuraya T, Yamashita M, Morimoto K. Novel triple neurokinin receptor antagonist CS-003 inhibits respiratory disease models in guinea pigs. Eur. J. Pharmacol. 2008;596:153–159
  45. Vargaftig BB. Modifications of experimental bronchopulmonary hyperresponsiveness. Am. J. Respir. Crit. Care Med. 1997;156:S97–102
  46. Veron M, Guenon I, Nenan S, Emonds-Alt X, Advenier C, Lagente V, et al. Interactions of tachykinin receptor antagonists with lipopolysaccharide-induced airway inflammation in mice. Clin. Exp. Pharmacol. Physiol. 2004;31:634–640
  47. Xu J, Xu F, Barrett E. Metalloelastase in lungs and alveolar macrophages is modulated by extracellular substance P in mice. Am. J. Physiol. Lung. Cell Mol. Physiol. 2008;295:L162–L170
  48. Zeldin DC, Wohlford-Lenane C, Chulada P, Bradbury JA, Scarborough PE, Roggli V, et al. Airway inflammation and responsiveness in prostaglandin H synthase-deficient mice exposed to bacterial lipopolysaccharide. Am. J. Respir. Cell Mol. Biol. 2001;25:457–465
  49. Zhang JJ, Yoshida H, Chao L, Chao J. Human adrenomedullin gene delivery protects against cardiac hypertrophy, fibrosis, and renal damage in hypertensive dahl salt- sensitive rats. Hum. Gene Ther. 2000;11:1817–1827
  50. Zimmer A, Zimmer AM, Baffi J, Usdin T, Reynolds K, König M, et al. Hypoalgesia in mice with a targeted deletion of the tachykinin 1 gene. Proc. Natl. Acad. Sci. USA. 1998;95:2630–2635

PII: S0143-4179(10)00064-8

doi: 10.1016/j.npep.2010.05.004

Neuropeptides
Volume 44, Issue 5 , Pages 399-406 , October 2010

Article Tools

* Image Usage & Resolution