Alteration of airway neuropeptide expression and development of airway hyperresponsiveness following respiratory syncytial virus infection

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 288, Issue 4 32-4, 2005, Pages

  Dakhama, Azzeddine ^a   Park, Jung Won ^a   Taube, Christian ^a   El Gazzar, Mohamed ^a   Kodama, Taku ^a   Miyahara, Nobuaki ^a   Takeda, Katsuyuki ^a   Kanehiro, Arihiko ^a   Balhorn, Annette ^a   Joetham, Anthony ^a   Loader, Joan E ^a   Larsen, Gary L ^a   Gelfand, Erwin W ^a  

^a NATIONAL JEWISH MEDICAL AND RESEARCH CENTER   (United States)

Author keywords

Animal model; Asthma; Calcitonin gene related peptide; Substance P

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; METHACHOLINE; NEUROKININ 1 RECEPTOR ANTAGONIST; NEUROPEPTIDE; SENDIDE; SUBSTANCE P; UNCLASSIFIED DRUG;

AIRWAY RESISTANCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRONCHUS HYPERREACTIVITY; CONTROLLED STUDY; ELECTRIC FIELD; ELECTROSTIMULATION; INFLAMMATION; MOUSE; NEUROMODULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; TISSUE DISTRIBUTION; TRACHEA MUSCLE; VIRUS INFECTION;

ANIMALS; ANTIEMETICS; CALCITONIN GENE-RELATED PEPTIDE; HUMANS; INFLAMMATION; LUNG; MICE; MICE, INBRED BALB C; PEPTIDE FRAGMENTS; PYRROLIDONECARBOXYLIC ACID; RECEPTORS, NEUROKININ-1; RESPIRATORY HYPERSENSITIVITY; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUS, HUMAN; SUBSTANCE P;

EID: 20144367691     PISSN: 10400605     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajplung.00143.2004     Document Type: Article

References (45)

1. Amara SG, Jonas V, Rosenfeld MG, Ong ES, and Evans RM. Alternative RNA processing in calcitonin gene expression generates mRNAs encoding different polypeptide products. Nature 298: 240-244, 1982.
2. Auais A, Adkins B, Napchan G, and Piedimonte G. Immunomodulatory effects of sensory nerves during respiratory syncytial virus infection in rats. Am J Physiol Lung Cell Mol Physiol 285: L105-L113, 2003.
3. Barnes PJ. Neurogenic inflammation and asthma. J Asthma 29: 165-180, 1992.
4. Barnes PJ, Baraniuk JN, and Belvisi MG. Neuropeptides in the respiratory tract. Part I. Am Rev Respir Dis 144: 1187-1198, 1991.
5. Bramley AM, Vitalis TZ, Wiggs BR, and Hegele RG. Effects of respiratory syncytial virus persistence on airway responsiveness and inflammation in guinea-pigs. Eur Respir J 14: 1061-1067, 1999.
6. Carucci JA, Ignatius R, Wei Y, Cypess AM, Schaer DA, Pope M, Steinman RM, and Mojsov S. Calcitonin gene-related peptide decreases expression of HLA-DR and CD86 by human dendritic cells and dampens dendritic cell-driven T cell-proliferative responses via the type I calcitonin gene-related peptide receptor. J Immunol 164: 3494-3499, 2000.
7. Choi RC, Yung LY, Dong TT, Wan DC, Wong YH, and Tsim KW. The calcitonin gene-related peptide-induced acetylcholinesterase synthesis in cultured chick myotubes is mediated by cyclic AMP. J Neurochem 71: 152-160, 1998.
8. Colasurdo GN, Hemming VG, Prince GA, Gelfand AS, Loader JE, and Larsen GL. Human respiratory syncytial virus produces prolonged alterations of neural control in airways of developing ferrets. Am J Respir Crit Care Med 157: 1506-1511, 1998.
9. Colasurdo GN, Hemming VG, Prince GA, Loader JE, Graves JP, and Larsen GL. Human respiratory syncytial virus affects nonadrenergic noncholinergic inhibition in cotton rat airways. Am J Physiol Lung Cell Mol Physiol 268: L1006-L1011, 1995.
10. Colasurdo GN, Loader JE, Graves JP, and Larsen GL. Modulation of acetylcholine release in rabbit airways in vitro. Am J Physiol Lung Cell Mol Physiol 268: L432-L437, 1995.
11. Dakhama A, Balhorn A, Taube C, Alvarez AG, Kodama T, Miyahara N, Joetham A, Takeda K, and Gelfand EW. Calcitonin gene-related peptide inhibits antigen-specific T-cell activation and subsequent development of a primary allergic immune response. J Allergy Clin Immunol 111: S290, 2003.
12. Dakhama A, Hegele RG, Laflamme G, Israel-Assayag E, and Cormier Y. Common respiratory viruses in lower airways of patients with acute hypersensitivity pneumonitis. Am J Respir Crit Care Med 159: 1316-1322, 1999.
13. Dakhama A, Kanehiro A, Makela MJ, Loader JE, Larsen GL, and Gelfand EW. Regulation of airway hyperresponsiveness by calcitonin gene-related peptide in allergen sensitized and challenged mice. Am J Respir Crit Care Med 165: 1137-1144, 2002.
14. De Giorgio R, Tazzari PL, Barbara G, Stanghellini V, and Corinaldesi R. Detection of substance P immunoreactivity in human peripheral leukocytes. J Neuroimmunol 82: 175-181, 1998.
15. Di Angelantonio S, Giniatullin R, Costa V, Sokolova E, and Nistri A. Modulation of neuronal nicotinic receptor function by the neuropeptides CGRP and substance P on autonomic nerve cells. Br J Pharmacol 139: 1061-1073, 2003.
16. Hakonarson H and Grunstein MM. Regulation of second messengers associated with airway smooth muscle contraction and relaxation. Am J Respir Crit Care Med 158: S115-S122, 1998.
17. Hall CB. Respiratory syncytial virus: a continuing culprit and conundrum. J Pediatr 135: 2-7, 1999.
18. Haynes LM, Tonkin J, Anderson LJ, and Tripp RA. Neutralizing anti-F glycoprotein and anti-substance P antibody treatment effectively reduces infection and inflammation associated with respiratory syncytial virus infection. J Virol 76: 6873-6881, 2002.
19. Ho WZ, Lai JP, Zhu XH, Uvaydova M, and Douglas SD. Human monocytes and macrophages express substance P and neurokinin-1 receptor. J Immunol 159: 5654-5660, 1997.
20. Jacoby DB. Virus-induced asthma attacks. JAMA 287: 755-761, 2002.
21. Joos GP and Geppetti P. Neural mechanisms in asthma. Eur Respir Mon 23: 138-163, 2003.
22. King KA, Hu C, Rodriguez MM, Romaguera R, Jiang X, and Piedimonte G. Exaggerated neurogenic inflammation and substance P receptor upregulation in RSV-infected weanling rats. Am J Respir Cell Mol Biol 24: 101-107, 2001.
23. Lai JP, Douglas SD, and Ho WZ. Human lymphocytes express substance P and its receptor. J Neuroimmunol 86: 80-86, 1998.
24. Larsen GL, Renz H, Loader JE, Bradley KL, and Gelfand EW. Airway response to electrical field stimulation in sensitized inbred mice. Passive transfer of increased responsiveness with peribronchial lymph nodes. J Clin Invest 89: 747-752, 1992.
25. Lundberg JM, Hokfelt T, Martling CR, Saria A, and Cuello C. Substance P-immunoreactive sensory nerves in the lower respiratory tract of various mammals including man. Cell Tissue Res 235: 251-261, 1984.
26. Martinez FD. Respiratory syncytial virus bronchiolitis and the pathogenesis of childhood asthma. Pediatr Infect Dis J 22: S76-S82, 2003.
27. Martling CR. Sensory nerves containing tachykinins and CGRP in the lower airways. Functional implications for bronchoconstriction, vasodilatation, and protein extravasation. Acta Physiol Scand Suppl 563: 1-57, 1987.
28. Matteoli M, Haimann C, Torri-Tarelli F, Polak JM, Ceccarelli B, and De Camilli P. Differential effect of α-latrotoxin on exocytosis from small synaptic vesicles and from large dense-core vesicles containing calcitonin gene-related peptide at the frog neuromuscular junction. Proc Natl Acad Sci USA 85: 7366-7370, 1988.
29. Metwali A, Blum AM, Ferraris L, Klein JS, Fiocchi C, and Weinstock JV. Eosinophils within the healthy or inflamed human intestine produce substance P and vasoactive intestinal peptide. J Neuroimmunol 52: 69-78, 1994.
30. Miles K, Greengard P, and Huganir RL. Calcitonin gene-related peptide regulates phosphorylation of the nicotinic acetylcholine receptor in rat myotubes. Neuron 2: 1517-1524, 1989.
31. Mulle C, Benoit P, Pinset C, Roa M, and Changeux JP. Calcitonin gene-related peptide enhances the rate of desensitization of the nicotinic acetylcholine receptor in cultured mouse muscle cells. Proc Natl Acad Sci USA 85: 5728-5732, 1988.
32. Sakurada T, Manome Y, Tan-No K, Sakurada S, Ohba M, Kisara K, and Terenius L. A selective and extremely potent antagonist of the neurokinin-1 receptor. Regul Pept 46: 326-328, 1993.
33. Scheuermann DW. Morphology and cytochemistry of the endocrine epithelial system in the lung. Int Rev Cytol 106: 35-88, 1987.
34. Schwarze J, Hamelmann E, Bradley KL, Takeda K, and Gelfand EW. Respiratory syncytial virus infection results in airway hyperresponsiveness and enhanced airway sensitization to allergen. J Clin Invest 100: 226-233, 1997.
35. Sigurs N, Bjarnason R, Sigurbergsson F, and Kjellman B. Respiratory syncytial virus bronchiolitis in infancy is an important risk factor for asthma and allergy at age 7. Am J Respir Crit Care Med 161: 1501-1507, 2000.
36. Sly PD and Hibbert ME. Childhood asthma following hospitalization with acute viral bronchiolitis in infancy. Pediatr Pulmonol 7: 153-158, 1989.
37. Stein RT, Sherrill D, Morgan WJ, Holberg CJ, Halonen M, Taussig LM, Wright AL, and Martinez FD. Respiratory syncytial virus in early life and risk of wheeze and allergy by age 13 years. Lancet 354: 541-545, 1999.
38. Takeda K, Hamelmann E, Joetham A, Shultz LD, Larsen GL, Irvin CG, and Gelfand EW. Development of eosinophilic airway inflammation and airway hyperresponsiveness in mast cell-deficient mice. J Exp Med 186: 449-454, 1997.
39. Tripp RA, Barskey A, Goss L, and Anderson LJ. Substance P receptor expression on lymphocytes is associated with the immune response to respiratory syncytial virus infection. J Neuroimmunol 129: 141-153, 2002.
40. Tripp RA, Moore D, Winter J, and Anderson LJ. Respiratory syncytial virus infection and G and/or SH protein expression contribute to substance P, which mediates inflammation and enhanced pulmonary disease in BALB/c mice. J Virol 74: 1614-1622, 2000.
41. Undem BJ and Carr MJ. The role of nerves in asthma. Curr Allergy Asthma Rep 2: 159-165, 2002.
42. Verastegui C, Prada Oliveira A, Fernandez-Vivero J, Romero A, and de Castro JM. Calcitonin gene-related peptide immunoreactivity in adult mouse lung. Eur J Histochem 41: 119-126, 1997.
43. Wang F, Millet I, Bottomly K, and Vignery A. Calcitonin gene-related peptide inhibits interleukin 2 production by murine T lymphocytes. J Biol Chem 267: 21052-21057, 1992.
44. Watson N, Maclagan J, and Barnes PJ. Endogenous tachykinins facilitate transmission through parasympathetic ganglia in guinea-pig trachea. Br J Pharmacol 109: 751-759, 1993.
45. Webber SE, Lim JC, and Widdicombe JG. The effects of calcitonin gene-related peptide on submucosal gland secretion and epithelial albumin transport in the ferret trachea in vitro. Br J Pharmacol 102: 79-84, 1991.