Respiratory syncytial virus induces insensitivity to β-adrenergic agonists in mouse lung epithelium in vivo

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 293, Issue 2, 2007, Pages

  Davis, Ian C ^a,e   Xu, Anna ^b   Gao, Zhiqian ^a   Hickman Davis, Judy M ^a,e   Factor, Phillip ^b   Sullender, Wayne M ^c   Matalon, Sadis ^a,d  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b NewYork Presbyterian Hospital   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^e OHIO STATE UNIVERSITY   (United States)

Author keywords

CXCL8; G protein coupled receptor kinase 2; Paramyxovirus; Protein kinase C

Indexed keywords

12 (2 CYANOETHYL) 6,7,12,13 TETRAHYDRO 13 METHYL 5 OXOINDOLO[2,3 A]PYRROLO[3,4 C]CARBAZOLE; 2 [1 (3 DIMETHYLAMINOPROPYL) 3 INDOLYL] 3 (3 INDOLYL)MALEIMIDE; 8 BROMO CYCLIC AMP; ADENYLATE CYCLASE; BETA ADRENERGIC RECEPTOR; BETA ADRENERGIC RECEPTOR STIMULATING AGENT; CATECHOLAMINE; CYCLIC AMP DEPENDENT PROTEIN KINASE; FORSKOLIN; G PROTEIN COUPLED RECEPTOR KINASE 2; INTERLEUKIN 8; ISOPRENALINE; PROCATEROL; PROTEIN KINASE C INHIBITOR; PROTEIN KINASE C ZETA; SALMETEROL; TERBUTALINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CATECHOLAMINE BLOOD LEVEL; CONTROLLED STUDY; DRUG RESPONSE; DRUG SENSITIVITY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; FEMALE; LUNG ALVEOLUS EPITHELIUM; LUNG FLUID; MALE; MOUSE; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN DEGRADATION; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; RESPIRATORY TRACT INFECTION;

ADRENERGIC BETA-AGONISTS; ANIMALS; CATECHOLAMINES; CHEMOKINES, CXC; EXTRAVASCULAR LUNG WATER; FEMALE; FORSKOLIN; MALE; MICE; MICE, INBRED BALB C; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN KINASE INHIBITORS; PULMONARY ALVEOLI; RECEPTORS, ADRENERGIC, BETA-2; RESPIRATORY MUCOSA; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUS, HUMAN; SPECIFIC PATHOGEN-FREE ORGANISMS; TERBUTALINE;

EID: 34547646140     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00458.2006     Document Type: Article

References (49)

1. Bitko V, Barik S. Persistent activation of RelA by respiratory syncytial virus involves protein kinase C, underphosphorylated IkappaBbeta, and sequestration of protein phosphatase 2A by the viral phosphoprotein. J Virol 72: 5610-5618, 1998.
2. Buckner CK, Clayton DE, in-Shoka AA, Busse WW, Dick EC, Shult P. Parainfluenza 3 infection blocks the ability of a beta adrenergic receptor agonist to inhibit antigen-induced contraction of guinea pig isolated airway smooth muscle. J Clin Invest 67: 376-384, 1981.
3. Carstairs R, Nimmo AJ, Barnes PJ. Autoradiographic visualization of beta-adrenoreceptor subtypes in human lung. Am Rev Respir Dis 132: 541-547, 1985.
4. Davis IC, Lazarowski ER, Hickman-Davis JM, Fortenberry JA, Chen FP, Zhao X, Sorscher E, Graves LM, Sullender WM, Matalon S. Leflunomide prevents alveolar fluid clearance inhibition by respiratory syncytial virus. Am J Respir Crit Care Med 173: 673-682, 2006.
5. Davis IC, Sullender WM, Hickman-Davis JM, Lindsey JR, Matalon S. Nucleotide-mediated inhibition of alveolar fluid clearance in BALB/c mice after respiratory syncytial virus infection. Am J Physiol Lung Cell Mol Physiol 286: L112-L120, 2004.
6. Dhami GK, Ferguson SS. Regulation of metabotropic glutamate receptor signaling, desensitization and endocytosis. Pharmacol Ther 111: 260-271, 2006.
7. Factor P, Adir Y, Mutlu GM, Burhop J, Dumasius V. Effects of beta2-adrenergic receptor overexpression on alveolar epithelial active transport. J Allergy Clin Immunol 110: S242-S246, 2002.
8. Falsey AR, Hennessey PA, Formica MA, Cox C, Walsh EE. Respiratory syncytial virus infection in elderly and high-risk adults. N Engl J Med 352: 1749-1759, 2005.
9. Finney PA, Donnelly LE, Belvisi MG, Chuang TT, Birrell M, Harris A, Mak JC, Scorer C, Barnes PJ, Adcock IM, Giembycz MA. Chronic systemic administration of salmeterol to rats promotes pulmonary beta(2)-adrenoceptor desensitization and down-regulation of G(s alpha). Br J Pharmacol 132: 1261-1270, 2001.
10. Garat C, Carter EP, Matthay MA. New in situ mouse model to quantify alveolar epithelial fluid clearance. J Appl Physiol 84: 1763-1767, 1998.
11. Grunstein MM, Hakonarson H, Whelan R, Yu Z, Grunstein JS, Chuang S. Rhinovirus elicits proasthmatic changes in airway responsiveness independently of viral infection. J Allergy Clin Immunol 108: 997-1004, 2001.
12. Hammer J, Numa A, Newth CJ. Albuterol responsiveness in infants with respiratory failure caused by respiratory syncytial virus infection. J Pediatr 127: 485-490, 1995.
13. Hammer J, Numa A, Newth CJ. Acute respiratory distress syndrome caused by respiratory syncytial virus. Pediatr Pulmonol 23: 176-183, 1997.
14. Hardiman KM, McNicholas-Bevensee CM, Fortenberry J, Myles CT, Malik B, Eaton DC, Matalon S. Regulation of amiloride-sensitive Na(+) transport by basal nitric oxide. Am J Respir Cell Mol Biol 30: 720-728, 2004.
15. Hartling L, Wiebe N, Russell K, Patel H, Klassen TP. A meta-analysis of randomized controlled trials evaluating the efficacy of epinephrine for the treatment of acute viral bronchiolitis. Arch Pediatr Adolesc Med 157: 957-964, 2003.
16. Heijink IH, Vellenga E, Oostendorp J, de Monchy JG, Postma DS, Kauffman HF. Exposure to TARC alters 2-adrenergic receptor signaling in human peripheral blood T lymphocytes. Am J Physiol Lung Cell Mol Physiol 289: L53-L59, 2005.
17. Henry PJ, Rigby PJ, Mackenzie JS, Goldie RG. Effect of respiratory tract viral infection on murine airway beta-adrenoceptor function, distribution and density. Br J Pharmacol 104: 914-921, 1991.
18. Hickman-Davis JM, Nicholas-Bevensee C, Davis IC, Ma HP, Davis GC, Bosworth CA, Matalon S. Reactive species mediate inhibition of alveolar type II sodium transport during mycoplasma infection. Am J Respir Crit Care Med 173: 334-344, 2006.
19. Johnson M. Molecular mechanisms of beta(2)-adrenergic receptor function, response, and regulation. J Allergy Clin Immunol 117: 18-24, 2006.
20. Kellner JD, Ohlsson A, Gadomski AM, Wang EE. Efficacy of bronchodilator therapy in bronchiolitis. A meta-analysis. Arch Pediatr Adolesc Med 150: 1166-1172, 1996.
21. Liggett SB, Caron MG, Lefkowitz RJ, Hnatowich M. Coupling of a mutated form of the human beta 2-adrenergic receptor to Gi and Gs. Requirement for multiple cytoplasmic domains in the coupling process. J Biol Chem 266: 4816-4821, 1991.
22. Mantovani A. The chemokine system: redundancy for robust outputs. Immunol Today 20: 254-257, 1999.
23. Martinez-Sobrido L, Gitiban N, Fernandez-Sesma A, Cros J, Mertz SE, Jewell NA, Hammond S, Flano E, Durbin RK, Garcia-Sastre A, Durbin JE. Protection against respiratory syncytial virus by a recombinant Newcastle disease virus vector. J Virol 80: 1130-1139, 2006.
24. Matalon S, O'Brodovich H. Sodium channels in alveolar epithelial cells: molecular characterization, biophysical properties, and physiological significance. Annu Rev Physiol 61: 627-661, 1999.
25. Matthay MA, Folkesson HG, Clerici C. Lung epithelial fluid transport and the resolution of pulmonary edema. Physiol Rev 82: 569-600, 2002.
26. McAuley DF, Frank JA, Fang X, Matthay MA. Clinically relevant concentrations of beta2-adrenergic agonists stimulate maximal cyclic adenosine monophosphate-dependent airspace fluid clearance and decrease pulmonary edema in experimental acid-induced lung injury. Crit Care Med 32: 1470-1476, 2004.
27. McNamara PS, Ritson P, Selby A, Hart CA, Smyth RL. Bronchoalveolar lavage cellularity in infants with severe respiratory syncytial virus bronchiolitis. Arch Dis Child 88: 922-926, 2003.
28. Modl M, Eber E, Malle-Scheid D, Weinhandl E, Zach MS. Does bronchodilator responsiveness in infants with bronchiolitis depend on age? J Pediatr 147: 617-621, 2005.
29. Moepps B, Nuesseler E, Braun M, Gierschik P. A homolog of the human chemokine receptor CXCR1 is expressed in the mouse. Mol Immunol 43: 897-914, 2006.
30. Monick M, Staber J, Thomas K, Hunninghake G. Respiratory syncytial virus infection results in activation of multiple protein kinase C isoforms leading to activation of mitogen-activated protein kinase. J Immunol 166: 2681-2687, 2001.
31. Moore PE, Cunningham G, Calder MM, DeMatteo AD Jr, Peeples ME, Summar ML, Peebles RS Jr. Respiratory syncytial virus infection reduces beta2-adrenergic responses in human airway smooth muscle. Am J Respir Cell Mol Biol 35: 559-564, 2006.
32. Morgan EE, Stader SM, Hodnichak CM, Mavrich KE, Folkesson HG, Maron MB. Postreceptor defects in alveolar epithelial β-adrenergic signaling after prolonged isoproterenol infusion. Am J Physiol Lung Cell Mol Physiol 285: L578-L583, 2003.
33. Mutlu GM, Koch WJ, Factor P. Alveolar epithelial beta 2-adrenergic receptors: their role in regulation of alveolar active sodium transport. Am J Respir Crit Care Med 170: 1270-1275, 2004.
34. Penela P, Murga C, Ribas C, Tutor AS, Peregrin S, Mayor F Jr. Mechanisms of regulation of G protein-coupled receptor kinases (GRKs) and cardiovascular disease. Cardiovasc Res 69: 46-56, 2006.
35. Perkins GD, McAuley DF, Thickett DR, Gao F. The beta-agonist lung injury trial (BALTI): a randomized placebo-controlled clinical trial. Am J Respir Crit Care Med 173: 281-287, 2006.
36. Planes C, Leyvraz C, Uchida T, Angelova MA, Vuagniaux G, Hummler E, Matthay M, Clerici C, Rossier B. In vitro and in vivo regulation of transepithelial lung alveolar sodium transport by serine proteases. Am J Physiol Lung Cell Mol Physiol 288: L1099-L1109, 2005.
37. Power UF, Huss T, Michaud V, Plotnicky-Gilquin H, Bonnefoy JY, Nguyen TN. Differential histopathology and chemokine gene expression in lung tissues following respiratory syncytial virus (RSV) challenge of formalin-inactivated RSV- or BBG2Na-immunized mice. J Virol 75: 12421-12430, 2001.
38. Rose JJ, Foley JF, Murphy PM, Venkatesan S. On the mechanism and significance of ligand-induced internalization of human neutrophil chemokine receptors CXCR1 and CXCR2. J Biol Chem 279: 24372-24386, 2004.
39. Sakuma T, Gu X, Wang Z, Maeda S, Sugita M, Sagawa M, Osanai K, Toga H, Ware LB, Folkesson G, Matthay MA. Stimulation of alveolar epithelial fluid clearance in human lungs by exogenous epinephrine. Crit Care Med 34: 676-681, 2006.
40. Sakuma T, Hida M, Nambu Y, Osanai K, Toga H, Takahashi K, Ohya N, Inoue M, Watanabe Y. Beta1-adrenergic agonist is a potent stimulator of alveolar fluid clearance in hyperoxic rat lungs. Jpn J Pharmacol 85: 161-166, 2001.
41. San-Juan-Vergara H, Peeples ME, Lockey RF, Mohapatra SS. Protein kinase C-alpha activity is required for respiratory syncytial virus fusion to human bronchial epithelial cells. J Virol 78: 13717-13726, 2004.
42. Sartori C, Allemann Y, Duplain H, Lepori M, Egli M, Lipp E, Hutter D, Turini P, Hugli O, Cook S, Nicod P, Scherrer U. Salmeterol for the prevention of high-altitude pulmonary edema. N Engl J Med 346: 1631-1636, 2002.
43. Seeman P, Kapur S. Anesthetics inhibit high-affinity states of dopamine D2 and other G-linked receptors. Synapse 50: 35-40, 2003.
44. Smyth RL, Openshaw PJ. Bronchiolitis. Lancet 368: 312-322, 2006.
45. Ware LB, Matthay MA. Alveolar fluid clearance is impaired in the majority of patients with acute lung injury and the acute respiratory distress syndrome. Am J Respir Crit Care Med 163: 1376-1383, 2001.
46. Warshamana GS, Corti M, Brody AR. TNF-alpha, PDGF, and TGF-beta(1) expression by primary mouse bronchiolar-alveolar epithelial and mesenchymal cells: TNF-alpha induces TGF-beta(1). Exp Mol Pathol 71: 13-33, 2001.
47. Wechsler ME, Lehman E, Lazarus SC, Lemanske RF Jr, Boushey HA, Deykin A, Fahy JV, Sorkness CA, Chinchilli VM, Craig TJ, DiMango E, Kraft M, Leone F, Martin RJ, Peters SP, Szefler SJ, Liu W, Israel E. β-Adrenergic receptor polymorphisms and response to salmeterol. Am J Respir Crit Care Med 173: 519-526, 2006.
48. Zhang L, Peeples ME, Boucher RC, Collins PL, Pickles RJ. Respiratory syncytial virus infection of human airway epithelial cells is polarized, specific to ciliated cells, and without obvious cytopathology. J Virol 76: 5654-5666, 2002.
49. Zhang Y, Luxon BA, Casola A, Garofalo RP, Jamaluddin M, Brasier AR. Expression of respiratory syncytial virus-induced chemokine gene networks in lower airway epithelial cells revealed by cDNA microarrays. J Virol 75: 9044-9058, 2001.