Effect of antigen sensitization and challenge on oscillatory mechanics of the lung and pulmonary inflammation in obese carboxypeptidase E-deficient mice

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 307, Issue 6, 2014, Pages R621-R633

  Dahm, Paul H ^a   Richards, Jeremy B ^b   Karmouty Quintana, Harry ^a   Cromar, Kevin R ^c   Sur, Sanjiv ^d   Price, Roger E ^e   Malik, Farhan ^a   Spencer, Chantal Y ^e   Barreno, Ramon X ^a   Hashmi, Syed S ^a   Blackburn, Michael R ^a   Haque, Ikram U ^a   Johnston, Richard A ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d University of Texas Medical Branch School of Medicine   (United States)

^e BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Asthma; Atopic; Eosinophil; Interleukin 13; Ovalbumin

Indexed keywords

ANTIGEN; CARBOXYPEPTIDASE H; CHEMERIN; HORMONE PRECURSOR; INTERLEUKIN 13; INTERLEUKIN 18; INTERLEUKIN 4; NEUROPEPTIDE; OVALBUMIN; AUTACOID; BIOLOGICAL MARKER; IMMUNOGLOBULIN;

AIRWAY OBSTRUCTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTHMA; ATOPY; CONTROLLED STUDY; ENERGY EXPENDITURE; EOSINOPHIL; FEMALE; LUNG LAVAGE; LUNG MECHANICS; MACROPHAGE; MOUSE; NEUTROPHIL; NONHUMAN; OBESITY; OSCILLATION; PHENOTYPE; RESPIRATORY TRACT INFLAMMATION; SATIETY; SENSITIZATION; AIRWAY RESISTANCE; ANIMAL; ATOPIC; BLOOD; C57BL MOUSE; CYTOLOGY; DISEASE MODEL; ENZYMOLOGY; GENETICS; GENOTYPE; IMMUNOLOGY; KNOCKOUT MOUSE; LUNG; PATHOPHYSIOLOGY; PNEUMONIA; TIME;

ASTHMA; ATOPIC; EOSINOPHIL; INTERLEUKIN-13; OVALBUMIN;

AIRWAY OBSTRUCTION; AIRWAY RESISTANCE; ANIMALS; ANTIGENS; BIOLOGICAL MARKERS; BRONCHOALVEOLAR LAVAGE FLUID; CARBOXYPEPTIDASE H; DISEASE MODELS, ANIMAL; FEMALE; GENOTYPE; IMMUNOGLOBULINS; INFLAMMATION MEDIATORS; LUNG; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OBESITY; OVALBUMIN; PHENOTYPE; PNEUMONIA; TIME FACTORS;

EID: 84907147145     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00205.2014     Document Type: Article

References (85)

1. Amrani Y, Martinet N, Bronner C. Potentiation by tumour necrosis factor-a of calcium signals induced by bradykinin and carbachol in human tracheal smooth muscle cells. Br J Pharmacol 114:4-5, 1995.
2. Barreno RX, Richards JB, Schneider DJ, Cromar KR, Nadas AJ, Hernandez CB, Hallberg LM, Price RE, Hashmi SS, Blackburn MR, Haque IU, Johnston RA. Endogenous osteopontin promotes ozone-induced neutrophil recruitment to the lungs and airway hyperresponsive-ness to methacholine. Am J Physiol Lung Cell Mol Physiol 305:L118-L129, 2013.
3. Barros LL, Souza-Machado A, Correa LB, Santos JS, Cruz C, Leite M, Castro L, Coelho AC, Almeida P, Cruz AA. Obesity and poor asthma control in patients with severe asthma. J Asthma 48:171-176, 2011.
4. Bates JH, Shardonofsky F, Stewart DE. The low-frequency dependence of respiratory system resistance and elastance in normal dogs. Respir Physiol 78:369-382, 1989.
5. Belke DD, Severson DL. Diabetes in mice with monogenic obesity:The db/db mouse and its use in the study of cardiac consequences. Methods Mol Biol 933:47-57, 2012.
6. Bohm M, Apel M, Sugawara K, Brehler R, Jurk K, Luger TA, Haas H, Paus R, Eiz-Vesper B, Walls AF, Ponimaskin E, Gehring M, Kapp A, Raap U. Modulation of basophil activity:A novel function of the neuropeptide a-melanocyte-stimulating hormone. J Allergy Clin Immunol 129:1085-1093, 2012.
7. Boring L, Gosling J, Cleary M, Charo IF. Decreased lesion formation in CCR2∼/∼mice reveals a role for chemokines in the initiation of atherosclerosis. Nature 394:894-897, 1998.
8. Brumpton B, Langhammer A, Romundstad P, Chen Y, Mai XM. General and abdominal obesity and incident asthma in adults:the HUNT study. Eur Respir J 41:323-329, 2013.
9. Bruun JM, Stallknecht B, Helge JW, Richelsen B. Interleukin-18 in plasma and adipose tissue:effects of obesity, insulin resistance, and weight loss. Eur J Endocrinol 157:465-471, 2007.
10. Bruun JM, Verdich C, Toubro S, Astrup A, Richelsen B. Association between measures of insulin sensitivity and circulating levels of interleu-kin-8, interleukin-6 and tumor necrosis factor-alpha. Effect of weight loss in obese men. Eur J Endocrinol 148:535-542, 2003.
11. Cain BM, Wang W, Beinfeld MC. Cholecystokinin (CCK) levels are greatly reduced in the brains but not the duodenums of Cpefat /Cpefat mice:a regional difference in the involvement of carboxypeptidase E (Cpe) in pro-CCK processing. Endocrinology 138:4034-4037, 1997.
12. Calixto MC, Lintomen L, Andre DM, Leiria LO, Ferreira D, Lellis-Santos C, Anhe GF, Bordin S, Landgraf RG, Antunes E. Metformin attenuates the exacerbation of the allergic eosinophilic inflammation in high fat-diet-induced obesity in mice. PLoS One 8:e76786, 2013.
13. Catalan V, Gomez-Ambrosi J, Rodriguez A, Ramirez B, Rotellar F, Valenti V, Silva C, Gil MJ, Salvador J, Fruhbeck G. Increased levels of chemerin and its receptor, chemokine-like receptor-1, in obesity are related to inflammation:tumor necrosis factor-alpha stimulates mRNA levels of chemerin in visceral adipocytes from obese patients. Surg Obes Relat Dis 9:306-314, 2013.
14. Cawley NX, Wetsel WC, Murthy SR, Park JJ, Pacak K, Loh YP. New roles of carboxypeptidase E in endocrine and neural function and cancer. Endocr Rev 33:216-253, 2012.
15. Cawley NX, Yanik T, Woronowicz A, Chang W, Marini JC, Loh YP. Obese carboxypeptidase E knockout mice exhibit multiple defects in peptide hormone processing contributing to low bone mineral density. Am J Physiol Endocrinol Metab 299:E189-E197, 2010.
16. Chen Y, Rennie D, Cormier Y, Dosman J. Atopy, obesity, and asthma in adults:the Humboldt study. J Agromedicine 14:222-227, 2009.
17. Coyle AJ, Wagner K, Bertrand C, Tsuyuki S, Bews J, Heusser C. Central role of immunoglobulin (Ig) E in the induction of lung eosinophil infiltration and T helper 2 cell cytokine production:Inhibition by a non-anaphylactogenic anti-IgE antibody. J Exp Med 183:1303-1310, 1996.
18. Delporte ML, El Mkadem SA, Quisquater M, Brichard SM. Leptin treatment markedly increased plasma adiponectin but barely decreased plasma resistin of ob/ob mice. Am J Physiol Endocrinol Metab 287:E446-E453, 2004.
19. Desai D, Newby C, Symon FA, Haldar P, Shah S, Gupta S, Bafadhel M, Singapuri A, Siddiqui S, Woods J, Herath A, Anderson IK, Bradding P, Green R, Kulkarni N, Pavord I, Marshall RP, Sousa AR, May RD, Wardlaw AJ, Brightling CE. Elevated sputum interleukin-5 and submucosal eosinophilia in obese individuals with severe asthma. Am J Respir Crit Care Med 188:657-663, 2013.
20. Dixon AE, Pratley RE, Forgione PM, Kaminsky DA, Whittaker-Leclair LA, Griffes LA, Garudathri J, Raymond D, Poynter ME, Bunn JY, Irvin CG. Effects of obesity and bariatric surgery on airway hyperresponsiveness, asthma control, and inflammation. J Allergy Clin Immunol 128:508-515, 2011.
21. Etori M, Yonekubo K, Sato E, Mizukami K, Hirahara K, Karasuy-ama H, Maeda H, Yamashita M. Melanocortin receptors 1 and 5 might mediate inhibitory effects of a-melanocyte-stimulating hormone on antigen-induced chronic allergic skin inflammation in IgE transgenic mice. J Invest Dermatol 132:1925-1927, 2012.
22. Eum SY, Maghni K, Hamid Q, Eidelman DH, Campbell H, Isogai S, Martin JG. Inhibition of allergic airways inflammation and airway hyperresponsiveness in mice by dexamethasone:Role of eosinophils, IL-5, eotaxin, and IL-13. J Allergy Clin Immunol 111:1049-1061, 2003.
23. Eum SY, Maghni K, Tolloczko B, Eidelman DH, Martin JG. IL-13 may mediate allergen-induced hyperresponsiveness independently of IL-5 or eotaxin by effects on airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 288:L576-L584, 2005.
24. Field AE, Coakley EH, Must A, Spadano JL, Laird N, Dietz WH, Rimm E, Colditz GA. Impact of overweight on the risk of developing common chronic diseases during a 10-year period. Arch Intern Med 161:1581-1586, 2001.
25. Fredrickson TN, Harris AW. Atlas of Mouse Hematopathology. Singapore:Harwood Academic Publishers, 2000.
26. Garthwaite TL, Martinson DR, Tseng LF, Hagen TC, Menahan LA. A longitudinal hormonal profile of the genetically obese mouse. Endocrinology 107:671-676, 1980.
27. Griesenbach U, Munkonge FM, Sumner-Jones S, Holder E, Smith SN, Boyd AC, Gill DR, Hyde SC, Porteous D, Alton EW, UK Cystic Fibrosis Gene Therapy Consortium. Assessment of CFTR function after gene transfer in vitro and in vivo. Methods Mol Biol 433:229-242, 2008.
28. Hamada K, Suzaki Y, Goldman A, Ning YY, Goldsmith C, Palecanda A, Coull B, Hubeau C, Kobzik L. Allergen-independent maternal transmission of asthma susceptibility. J Immunol 170:1683-1689, 2003.
29. Hamelmann E, Takeda K, Haczku A, Cieslewicz G, Shultz L, Hamid Q, Xing Z, Gauldie J, Gelfand EW. Interleukin (IL)-5 but not immunoglobulin E reconstitutes airway inflammation and airway hyperresponsive-ness in IL-4-deficient mice. Am J Respir Cell Mol Biol 23:327-334, 2000.
30. Hantos Z, Daroczy B, Suki B, Nagy S, Fredberg JJ. Input impedance and peripheral inhomogeneity of dog lungs. J Appl Physiol 72:168-178, 1992.
31. Hartney JM, Robichaud A. Assessment of airway hyperresponsiveness in mouse models of allergic lung disease using detailed measurements of respiratory mechanics. Methods Mol Biol 1032:205-217, 2013.
32. Hirai T, McKeown KA, Gomes RF, Bates JH. Effects of lung volume on lung and chest wall mechanics in rats. J Appl Physiol 86:16-21, 1999.
33. Holguin F, Bleecker ER, Busse WW, Calhoun WJ, Castro M, Erzurum SC, Fitzpatrick AM, Gaston B, Israel E, Jarjour NN, Moore WC, Peters SP, Yonas M, Teague WG, Wenzel SE. Obesity and asthma:An association modified by age of asthma onset. J Allergy Clin Immunol 127:1486-1493, 2011.
34. Holguin F, Comhair SA, Hazen SL, Powers RW, Khatri SS, Bleecker ER, Busse WW, Calhoun WJ, Castro M, Fitzpatrick AM, Gaston B, Israel E, Jarjour NN, Moore WC, Peters SP, Teague WG, Chung KF, Erzurum SC, Wenzel SE. An association between L-arginine/asymmetric dimethyl arginine balance, obesity, and the age of asthma onset phenotype. Am J Respir Crit Care Med 187:153-159, 2013.
35. JAX Research Systems. New Cpe fat mouse model for diabetes and obesity research. In:JAX Notes. Bar Harbor, ME:The Jackson Laboratory, 2002.
36. Johnston RA, Theman TA, Lu FL, Terry RD, Williams ES, Shore SA. Diet-induced obesity causes innate airway hyperresponsiveness to meth-acholine and enhances ozone-induced pulmonary inflammation. J Appl Physiol 104:1727-1735, 2008.
37. Johnston RA, Theman TA, Shore SA. Augmented responses to ozone in obese carboxypeptidase E-deficient mice. Am J Physiol Regul Integr Comp Physiol 290:R126-R133, 2006.
38. Johnston RA, Zhu M, Hernandez CB, Williams ES, Shore SA. Onset of obesity in carboxypeptidase E-deficient mice and effect on airway responsiveness and pulmonary responses to ozone. J Appl Physiol 108:1812-1819, 2010.
39. Johnston RA, Zhu M, Rivera-Sanchez YM, Lu FL, Theman TA, Flynt L, Shore SA. Allergic airway responses in obese mice. Am J Respir Crit Care Med 176:650-658, 2007.
40. Juel CT, Ulrik CS. Obesity and asthma:Impact on severity, asthma control, and response to therapy. Respir Care 58:867-873, 2013.
41. Koga H, Miyahara N, Fuchimoto Y, Ikeda G, Waseda K, Ono K, Tanimoto Y, Kataoka M, Gelfand EW, Tanimoto M, Kanehiro A. Inhibition of neutrophil elastase attenuates airway hyperresponsiveness and inflammation in a mouse model of secondary allergen challenge:neutrophil elastase inhibition attenuates allergic airway responses. Respir Res 14:8, 2013.
42. Komakula S, Khatri S, Mermis J, Savill S, Haque S, Rojas M, Brown L, Teague GW, Holguin F. Body mass index is associated with reduced exhaled nitric oxide and higher exhaled 8-isoprostanes in asthmatics. Respir Res 8:32, 2007.
43. Kudo M, Melton AC, Chen C, Engler MB, Huang KE, Ren X, Wang Y, Bernstein X, Li JT, Atabai K, Huang X, Sheppard D. IL-17A produced by afj T cells drives airway hyper-responsiveness in mice and enhances mouse and human airway smooth muscle contraction. Nat Med 18:547-554, 2012.
44. Kumar RK, Herbert C, Foster PS. The “classical”ovalbumin challenge model of asthma in mice. Curr Drug Targets 9:485-494, 2008.
45. Lack G, Oshiba A, Bradley KL, Loader JE, Amran D, Larsen GL, Gelfand EW. Transfer of immediate hypersensitivity and airway hyperresponsiveness by IgE-positive B cells. Am J Respir Crit Care Med 152:1765-1773, 1995.
46. Lang JE, Hossain J, Smith K, Lima JJ. Asthma severity, exacerbation risk, and controller treatment burden in underweight and obese children. J Asthma 49:456-463, 2012.
47. Lefort J, Nahori MA, Ruffie C, Vargaftig BB, Pretolani M. In vivo neutralization of eosinophil-derived major basic protein inhibits antigen-induced bronchial hyperreactivity in sensitized guinea pigs. J Clin Invest 97:1117-1121, 1996.
48. Leibel RL, Chung WK, Chua SC Jr. The molecular genetics of rodent single gene obesities. J Biol Chem 272:31937-31940, 1997.
49. Leiter EH, Kintner J, Flurkey K, Beamer WG, Naggert JK. Physiologic and endocrinologic characterization of male sex-biased diabetes in C57BLKS/J mice congenic for the fat mutation at the carboxypeptidease E locus. Endocrine 10:57-66, 1999.
50. Leone N, Courbon D, Berr C, Barberger-Gateau P, Tzourio C, Alperovitch A, Zureik M. Abdominal obesity and late-onset asthma:cross-sectional and longitudinal results:the 3C study. Obesity (Silver Spring) 20:628-635, 2012.
51. Li P, Tiwari HK, Lin WY, Allison DB, Chung WK, Leibel RL, Yi N, Liu N. Genetic association analysis of 30 genes related to obesity in a European American population. Int J Obes 38:724-729, 2014.
52. Lu FL, Johnston RA, Flynt L, Theman TA, Terry RD, Schwartzman IN, Lee A, Shore SA. Increased pulmonary responses to acute ozone exposure in obese db/db mice. Am J Physiol Lung Cell Mol Physiol 290:L856-L865, 2006.
53. Marchesini G, Moscatiello S, Di Domizio S, Forlani G. Obesity-associated liver disease. J Clin Endocrinol Metab 93:S74-S80, 2008.
54. Martins IJ, Tran JM, Redgrave TG. Food restriction normalizes chylomicron remnant metabolism in murine models of obesity as assessed by a novel stable isotope breath test. J Nutr 132:176-181, 2002.
55. Mehlhop PD, van de Rijn M, Goldberg AB, Brewer JP, Kurup VP, Martin TR, Oettgen HC. Allergen-induced bronchial hyperreactivity and eosinophilic inflammation occur in the absence of IgE in a mouse model of asthma. Proc Natl Acad Sci USA 94:1344-1349, 1997.
56. Miyamoto S, Shikata K, Miyasaka K, Okada S, Sasaki M, Kodera R, Hirota D, Kajitani N, Takatsuka T, Kataoka HU, Nishishita S, Sato C, Funakoshi A, Nishimori H, Uchida HA, Ogawa D, Makino H. Chole-cystokinin plays a novel protective role in diabetic kidney through antiinflammatory actions on macrophage:Anti-inflammatory effect of chole-cystokinin. Diabetes 61:897-907, 2012.
57. Moore WC, Meyers DA, Wenzel SE, Teague WG, Li H, Li X, D’Agostino R Jr, Castro M, Curran-Everett D, Fitzpatrick AM, Gaston B, Jarjour NN, Sorkness R, Calhoun WJ, Chung KF, Comhair SA, Dweik RA, Israel E, Peters SP, Busse WW, Erzurum SC, Bleecker ER, National Heart, Lung, and Blood Institute’s Severe Asthma Research Program. Identification of asthma phenotypes using cluster analysis in the Severe Asthma Research Program. Am J Respir Crit Care Med 181:315-323, 2010.
58. Morimoto LM, White E, Chen Z, Chlebowski RT, Hays J, Kuller L, Lopez AM, Manson J, Margolis KL, Muti PC, Stefanick ML, McTi-ernan A. Obesity, body size, and risk of postmenopausal breast cancer:the Women’s Health Initiative (United States). Cancer Causes Control 13:741-751, 2002.
59. Musaad S, Haynes EN. Biomarkers of obesity and subsequent cardiovascular events. Epidemiol Rev 29:98-114, 2007.
60. Naggert JK, Fricker LD, Varlamov O, Nishina PM, Rouille Y, Steiner DF, Carroll RJ, Paigen BJ, Leiter EH. Hyperproinsulinaemia in obese fat/fat mice associated with a carboxypeptidase E mutation which reduces enzyme activity. Nat Genet 10:135-142, 1995.
61. O’Donnell DE, O’Donnell CD, Webb KA, Guenette JA. Respiratory consequences of mild-to-moderate obesity:Impact on exercise performance in health and in chronic obstructive pulmonary disease. Pulm Med 2012:818925, 2012.
62. Ogden CL, Carroll MD, Kit BK, Flegal KM. Prevalence of obesity in the United States, 2009-2010. NCHS Data Brief 1-8, 2012.
63. Pillow JJ, Korfhagen TR, Ikegami M, Sly PD. Overexpression of TGF-a increases lung tissue hysteresivity in transgenic mice. J Appl Physiol 91:2730-2734, 2001.
64. Rivera-Sanchez YM, Johnston RA, Schwartzman IN, Valone J, Silverman ES, Fredberg JJ, Shore SA. Differential effects of ozone on airway and tissue mechanics in obese mice. J Appl Physiol 96:2200-2206, 2004.
65. Saia RS, Bertozi G, Mestriner FL, Antunes-Rodrigues J, Queiroz Cunha F, Carnio EC. Cardiovascular and inflammatory response to cholecystokinin during endotoxemic shock. Shock 39:104-113, 2013.
66. Shao J, Yamashita H, Qiao L, Friedman JE. Decreased Akt kinase activity and insulin resistance in C57BL/KsJ-Leprdb /db mice. J Endocrinol 167:107-115, 2000.
67. Shen FS, Loh YP. Intracellular misrouting and abnormal secretion of adrenocorticotropin and growth hormone in Cpefat mice associated with a carboxypeptidase E mutation. Proc Natl Acad Sci USA 94:5314-5319, 1997.
68. Shore SA, Johnston RA. Obesity and asthma. Pharmacol Ther 110:83-102, 2006.
69. Shore SA, Lang JE, Kasahara DI, Lu FL, Verbout NG, Si H, Williams ES, Terry RD, Lee A, Johnston RA. Pulmonary responses to subacute ozone exposure in obese vs. lean mice. J Appl Physiol 107:1445-1452, 2009.
70. Shore SA, Rivera-Sanchez YM, Schwartzman IN, Johnston RA. Responses to ozone are increased in obese mice. J Appl Physiol 95:938–945, 2003.
71. Shore SA, Schwartzman IN, Mellema MS, Flynt L, Imrich A, Johnston RA. Effect of leptin on allergic airway responses in mice. J Allergy Clin Immunol 115:103–109, 2005.
72. Shore SA, Terry RD, Flynt L, Xu A, Hug C. Adiponectin attenuates allergen-induced airway inflammation and hyperresponsiveness in mice. J Allergy Clin Immunol 118:389–395, 2006.
73. Sideleva O, Suratt BT, Black KE, Tharp WG, Pratley RE, Forgione P, Dienz O, Irvin CG, Dixon AE. Obesity and asthma:An inflammatory disease of adipose tissue not the airway. Am J Respir Crit Care Med 186:598–605, 2012.
74. Tomioka S, Bates JH, Irvin CG. Airway and tissue mechanics in a murine model of asthma:alveolar capsule vs. forced oscillations. J Appl Physiol 93:263–270, 2002.
75. Tomita T, Doull V, Pollock HG, Krizsan D. Pancreatic islets of obese hyperglycemic mice (ob/ob). Pancreas 7:367–375, 1992.
76. van Veen IH, Ten Brinke A, Sterk PJ, Rabe KF, Bel EH. Airway inflammation in obese and nonobese patients with difficult-to-treat asthma. Allergy 63:570–574, 2008.
77. Wagers S, Lundblad LK, Ekman M, Irvin CG, Bates JH. The allergic mouse model of asthma:normal smooth muscle in an abnormal lung? J Appl Physiol 96:2019–2027, 2004.
78. Wagers SS, Haverkamp HC, Bates JH, Norton RJ, Thompson-Figueroa JA, Sullivan MJ, Irvin CG. Intrinsic and antigen-induced airway hyperresponsiveness are the result of diverse physiological mechanisms. J Appl Physiol 102:221–230, 2007.
79. Williams AS, Chen L, Kasahara DI, Si H, Wurmbrand AP, Shore SA. Obesity and airway responsiveness:Role of TNFR2. Pulm Pharmacol Ther 26:444–454, 2013.
80. World Health Organization. World Health Statistics 2013. Geneva, Switzerland:WHO Press, 2013.
81. Yamagata S, Tomita K, Sato R, Niwa A, Higashino H, Tohda Y. Interleukin-18-deficient mice exhibit diminished chronic inflammation and airway remodelling in ovalbumin-induced asthma model. Clin Exp Immunol 154:295–304, 2008.
82. Yu ZW, Zhang JH. Effect of inhaled budesonide on surfactant protein expression in asthmatic mice. Allergy Asthma Proc 29:486–492, 2008.
83. Zerah F, Harf A, Perlemuter L, Lorino H, Lorino AM, Atlan G. Effects of obesity on respiratory resistance. Chest 103:1470–1476, 1993.
84. Zhu M, Williams AS, Chen L, Wurmbrand AP, Williams ES, Shore SA. Role of TNFR1 in the innate airway hyperresponsiveness of obese mice. J Appl Physiol 113:1476–1485, 2012.
85. Zhu Z, Enhorning G, Zheng T, Chen Q, Chen NY, Homer R, Elias JA. Interleukin-13 induces surfactant function abnormality in the murine lung. Chest 123:375S-376S, 2003.