Rapamycin decreases airway remodeling and hyperreactivity in a transgenic model of noninflammatory lung disease

Journal of Applied Physiology

Volumn 111, Issue 6, 2011, Pages 1760-1767

  Kramer, Elizabeth L ^a   Hardie, William D ^b   Mushaben, Elizabeth M ^a   Acciani, Thomas H ^a   Pastura, Patricia A ^a   Korfhagen, Thomas R ^a   Hershey, Gurjit Khurana ^c   Whitsett, Jeffrey A ^a   Le Cras, Timothy D ^a  

^a Section of Neonatology Perinatal and Pulmonary Biology   (United States)

^b Division of Pulmonary Medicine   (United States)

^c UNIVERSITY OF CINCINNATI   (United States)

Author keywords

Airway hyperresponsiveness; Airway smooth muscle; Epidermal growth factor receptor; Mammalian target of rapamycin; Transforming growth factor

Indexed keywords

EARLY GROWTH RESPONSE FACTOR 1; EGR1 PROTEIN, MOUSE; EPIDERMAL GROWTH FACTOR RECEPTOR; MESSENGER RNA; MTOR PROTEIN, MOUSE; RAPAMYCIN; TARGET OF RAPAMYCIN KINASE; TRANSFORMING GROWTH FACTOR ALPHA;

AIRWAY REMODELING; ANIMAL; ARTICLE; BIOLOGICAL MODEL; BRONCHUS HYPERREACTIVITY; DRUG EFFECT; GENETICS; LUNG DISEASE; METABOLISM; MOUSE; MOUSE MUTANT; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

AIRWAY REMODELING; ANIMALS; BRONCHIAL HYPERREACTIVITY; EARLY GROWTH RESPONSE PROTEIN 1; LUNG DISEASES; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MODELS, BIOLOGICAL; RECEPTOR, EPIDERMAL GROWTH FACTOR; RNA, MESSENGER; SIGNAL TRANSDUCTION; SIROLIMUS; TOR SERINE-THREONINE KINASES; TRANSFORMING GROWTH FACTOR ALPHA;

EID: 83655191503     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00737.2011     Document Type: Article

References (53)

1. Amishima M, Munakata M, Nasuhara Y, Sato A, Takahashi T, Homma Y, Kawakami Y. Expression of epidermal growth factor and epidermal growth factor receptor immunoreactivity in the asthmatic human airway. Am J Respir Crit Care Med 157: 1907-1912, 1998.
2. Baroffio M, Barisione G, Crimi E, Brusasco V. Noninflammatory mechanisms of airway hyper-responsiveness in bronchial asthma: an overview. Ther Adv Respir Dis 3: 163-174, 2009.
3. Bates JH, Cojocaru A, Haverkamp HC, Rinaldi LM, Irvin CG. The synergistic interactions of allergic lung inflammation and intratracheal cationic protein. Am J Respir Crit Care Med 177: 261-268, 2008. (Pubitemid 351198368)
4. Bel EH. Clinical phenotypes of asthma. Curr Opin Pulm Med 10: 44-50, 2004. (Pubitemid 38045900)
5. Boxall C, Holgate ST, Davies DE. The contribution of transforming growth factor-beta and epidermal growth factor signalling to airway remodelling in chronic asthma. Eur Respir J 27: 208-229, 2006. (Pubitemid 43092684)
6. Brewster CE, Howarth PH, Djukanovic R, Wilson J, Holgate ST, Roche WR. Myofibroblasts and subepithelial fibrosis in bronchial asthma. Am J Respir Cell Mol Biol 3: 507-511, 1990.
7. Burgel PR, Nadel JA. Epidermal growth factor receptor-mediated innate immune responses and their roles in airway diseases. Eur Respir J 32: 1068-1081, 2008.
8. Burgel PR, Nadel JA. Roles of epidermal growth factor receptor activation in epithelial cell repair and mucin production in airway epithelium. Thorax 59: 992-996, 2004. (Pubitemid 39490787)
9. Corrigan CJ. Asthma refractory to glucocorticoids: the role of newer immunosuppressants. Am J Respir Med 1: 47-54, 2002. (Pubitemid 37038923)
10. Cox G, Thomson NC, Rubin AS, Niven RM, Corris PA, Siersted HC, Olivenstein R, Pavord ID, McCormack D, Chaudhuri R, Miller JD, Laviolette M. Asthma control during the year after bronchial thermoplasty. N Engl J Med 356: 1327-1337, 2007. (Pubitemid 46513298)
11. Eynott PR, Salmon M, Huang TJ, Oates T, Nicklin PL, Chung KF. Effects of cyclosporin A and a rapamycin derivative (SAR943) on chronic allergic inflammation in sensitized rats. Immunology 109: 461-467, 2003. (Pubitemid 36783273)
12. Fedorov IA, Wilson SJ, Davies DE, Holgate ST. Epithelial stress and structural remodelling in childhood asthma. Thorax 60: 389-394, 2005. (Pubitemid 40685821)
13. Fujitani Y, Trifilieff A. In vivo and in vitro effects of SAR 943, a rapamycin analogue, on airway inflammation and remodeling. Am J Respir Crit Care Med 167: 193-198, 2003. (Pubitemid 36076079)
14. Giordano A. Molecular basis of different outcomes for drug-eluting stents that release sirolimus or tacrolimus. Curr Opin Drug Discov Devel 13: 159-168, 2010.
15. Guertin DA, Sabatini DM. Defining the role of mTOR in cancer. Cancer Cell 12: 9-22, 2007. (Pubitemid 47001784)
16. Gupte GL, Mahadevan S, Clarke JR, Alton H, Beath SV. Sirolimusrelated pulmonary toxicity mimicking "asthma like" symptoms. World J Gastroenterol 13: 5151-5153, 2007. (Pubitemid 47527355)
17. Hardie WD, Bruno MD, Huelsman KM, Iwamoto HS, Carrigan PE, Leikauf GD, Whitsett JA, Korfhagen TR. Postnatal lung function and morphology in transgenic mice expressing transforming growth factoralpha. Am J Pathol 151: 1075-1083, 1997. (Pubitemid 27424317)
18. Hardie WD, Davidson C, Ikegami M, Leikauf GD, Le Cras TD, Prestridge A, Whitsett JA, Korfhagen TR. EGF receptor tyrosine kinase inhibitors diminish transforming growth factor-alpha-induced pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol 294: L1217-L1225, 2008.
19. Hardie WD, Kerlakian CB, Bruno MD, Huelsman KM, Wert SE, Glasser SW, Whitsett JA, Korfhagen TR. Reversal of lung lesions in transgenic transforming growth factor alpha mice by expression of mutant epidermal growth factor receptor. Am J Respir Cell Mol Biol 15: 499-508, 1996. (Pubitemid 126440577)
20. Hardie WD, Korfhagen TR, Sartor MA, Prestridge A, Medvedovic M, Le Cras TD, Ikegami M, Wesselkamper SC, Davidson C, Dietsch M, Nichols W, Whitsett JA, Leikauf GD. Genomic profile of matrix and vasculature remodeling in TGF-alpha induced pulmonary fibrosis. Am J Respir Cell Mol Biol 37: 309-321, 2007. (Pubitemid 350067610)
21. Hardie WD, Le Cras TD, Jiang K, Tichelaar JW, Azhar M, Korfhagen TR. Conditional expression of transforming growth factor-alpha in adult mouse lung causes pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol 286: L741-L749, 2004. (Pubitemid 38365059)
22. Hardie WD, Piljan-Gentle A, Dunlavy MR, Ikegami M, Korfhagen TR. Dose-dependent lung remodeling in transgenic mice expressing transforming growth factor-alpha. Am J Physiol Lung Cell Mol Physiol 281: L1088-L1094, 2001.
23. Hardt M, Chantaravisoot N, Tamanoi F. Activating mutations of TOR (target of rapamycin). Genes Cells 16: 141-151, 2011.
24. Harrison DE, Strong R, Sharp ZD, Nelson JF, Astle CM, Flurkey K, Nadon NL, Wilkinson JE, Frenkel K, Carter CS, Pahor M, Javors MA, Fernandez E, Miller RA. Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature 460: 392-395, 2009.
25. Holgate ST, Davies DE, Lackie PM, Wilson SJ, Puddicombe SM, Lordan JL. Epithelial-mesenchymal interactions in the pathogenesis of asthma. J Allergy Clin Immunol 105: 193-204, 2000. (Pubitemid 30109029)
26. Homer RJ, Elias JA. Airway remodeling in asthma: therapeutic implications of mechanisms. Physiology (Bethesda) 20: 28-35, 2005. (Pubitemid 40363368)
27. James AL, Hogg JC, Dunn LA, Pare PD. The use of the internal perimeter to compare airway size and to calculate smooth muscle shortening. Am Rev Respir Dis 138: 136-139, 1988.
28. Johnson PR, Roth M, Tamm M, Hughes M, Ge Q, King G, Burgess JK, Black JL. Airway smooth muscle cell proliferation is increased in asthma. Am J Respir Crit Care Med 164: 474-477, 2001. (Pubitemid 32778219)
29. Juvet SC, McCormack FX, Kwiatkowski DJ, Downey GP. Molecular pathogenesis of lymphangioleiomyomatosis: lessons learned from orphans. Am J Respir Cell Mol Biol 36: 398-408, 2007. (Pubitemid 46622997)
30. Kon OM, Kay AB. Anti-T cell strategies in asthma. Inflamm Res 48: 516-523, 1999. (Pubitemid 29495632)
31. Korfhagen TR, Le Cras TD, Davidson CR, Schmidt SM, Ikegami M, Whitsett JA, Hardie WD. Rapamycin prevents transforming growth factor-alpha induced pulmonary fibrosis. Am J Respir Cell Mol Biol 41: 562-572, 2009.
32. Kramer EL, Deutsch GH, Sartor MA, Hardie WD, Ikegami M, Korfhagen TR, Le Cras TD. Perinatal increases in TGF-disrupt the saccular phase of lung morphogenesis and cause remodeling: microarray analysis. Am J Physiol Lung Cell Mol Physiol 293: L314-L327, 2007. (Pubitemid 47205012)
33. Kramer EL, Mushaben EM, Pastura PA, Acciani TH, Deutsch GH, Khurana Hershey GK, Korfhagen TR, Hardie WD, Whitsett JA, Le Cras TD. Early growth response-1 suppresses epidermal growth factor receptor-mediated airway hyperresponsiveness and lung remodeling in mice. Am J Respir Cell Mol Biol 41: 415-425, 2009.
34. Krymskaya VP, Goncharova EA. PI3K/mTORC1 activation in hamartoma syndromes: therapeutic prospects. Cell Cycle 8: 403-413, 2009.
35. Krymskaya VP, Penn RB, Orsini MJ, Scott PH, Plevin RJ, Walker TR, Eszterhas AJ, Amrani Y, Chilvers ER, Panettieri RA Jr. Phosphatidylinositol 3-kinase mediates mitogen-induced human airway smooth muscle cell proliferation. Am J Physiol Lung Cell Mol Physiol 277: L65-L78, 1999. (Pubitemid 29356752)
36. Krymskaya VP, Snow J, Cesarone G, Khavin I, Goncharov DA, Lim PN, Veasey SC, Ihida-Stansbury K, Jones PL, Goncharova EA. mTOR is required for pulmonary arterial vascular smooth muscle cell proliferation under chronic hypoxia. FASEB J 25: 1922-1933, 2011.
37. Lange P, Parner J, Vestbo J, Schnohr P, Jensen G. A 15-year follow-up study of ventilatory function in adults with asthma. N Engl J Med 339: 1194-1200, 1998.
38. Laplante M, Sabatini DM. mTOR signaling at a glance. J Cell Sci 122: 3589-3594, 2009.
39. Le Cras TD, Acciani TH, Mushaben EM, Kramer EL, Pastura PA, Hardie WD, Korfhagen TR, Sivaprasad U, Ericksen M, Gibson AM, Holtzman MJ, Whitsett JA, Khurana Hershey GK. Epithelial EGF receptor signaling mediates airway hyperreactivity and remodeling in a mouse model of chronic asthma. Am J Physiol Lung Cell Mol Physiol 300: L414-L421, 2011.
40. Le Cras TD, Hardie WD, Deutsch GH, Albertine KH, Ikegami M, Whitsett JA, Korfhagen TR. Transient induction of TGF-alpha disrupts lung morphogenesis, causing pulmonary disease in adulthood. Am J Physiol Lung Cell Mol Physiol 287: L718-L729, 2004. (Pubitemid 39249385)
41. Le Cras TD, Hardie WD, Fagan K, Whitsett JA, Korfhagen TR. Disrupted pulmonary vascular development and pulmonary hypertension in transgenic mice overexpressing transforming growth factor-alpha. Am J Physiol Lung Cell Mol Physiol 285: L1046-L1054, 2003. (Pubitemid 37310094)
42. McCormack FX, Inoue Y, Moss J, Singer LG, Strange C, Nakata K, Barker AF, Chapman JT, Brantly ML, Stocks JM, Brown KK, Lynch JP, Goldberg HJ, Young LR, Kinder BW, Downey GP, Sullivan EJ, Colby TV, McKay RT, Cohen MM, Korbee L, Taveira-Dasilva AM, Lee HS, Krischer JP, Trapnell BC. Efficacy and safety of sirolimus in lymphangioleiomyomatosis. N Engl J Med 364: 1595-1606, 2011.
43. Panettieri RA Jr. Effects of corticosteroids on structural cells in asthma and chronic obstructive pulmonary disease. Proc Am Thorac Soc 1: 231-234, 2004.
44. Pavord ID, Cox G, Thomson NC, Rubin AS, Corris PA, Niven RM, Chung KF, Laviolette M. Safety and efficacy of bronchial thermoplasty in symptomatic, severe asthma. Am J Respir Crit Care Med 176: 1185-1191, 2007. (Pubitemid 350256471)
45. Payne D, Bush A. Phenotype-specific treatment of difficult asthma in children. Paediatr Respir Rev 5: 116-123, 2004. (Pubitemid 38701810)
46. Perl AK, Zhang L, Whitsett JA. Conditional expression of genes in the respiratory epithelium in transgenic mice: cautionary notes and toward building a better mouse trap. Am J Respir Cell Mol Biol 40: 1-3, 2009.
47. Pham PT, Pham PC, Danovitch GM, Ross DJ, Gritsch HA, Kendrick EA, Singer J, Shah T, Wilkinson AH. Sirolimus-associated pulmonary toxicity. Transplantation 77: 1215-1220, 2004. (Pubitemid 38580300)
48. Powell JD, Delgoffe GM. The mammalian target of rapamycin: linking T cell differentiation, function, and metabolism. Immunity 33: 301-311, 2010.
49. Sarbassov DD, Ali SM, Sengupta S, Sheen JH, Hsu PP, Bagley AF, Markhard AL, Sabatini DM. Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol Cell 22: 159-168, 2006.
50. Saunders RN, Metcalfe MS, Nicholson ML. Rapamycin in transplantation: a review of the evidence. Kidney Int 59: 3-16, 2001. (Pubitemid 32055209)
51. Schiele TM, Leibig M, Rieber J, Konig A, Krotz F, Sohn HY, Klauss V. Five-year clinical follow-up after sirolimus-eluting stent implantation for the treatment of coronary in-stent restenosis. Coron Artery Dis 22: 188-193, 2011.
52. Stevenson EC, Turner G, Heaney LG, Schock BC, Taylor R, Gallagher T, Ennis M, Shields MD. Bronchoalveolar lavage findings suggest two different forms of childhood asthma. Clin Exp Allergy 27: 1027-1035, 1997. (Pubitemid 27421831)
53. Urso DL, Vincenzo D, Pignataro E, Acri P, Cucinotta G. Diagnosis and treatment of refractory asthma. Eur Rev Med Pharmacol Sci 12: 315-320, 2008.