Impact of adiponectin deficiency on pulmonary responses to acute ozone exposure in mice

American Journal of Respiratory Cell and Molecular Biology

Volumn 43, Issue 4, 2010, Pages 487-497

  Zhu, Ming ^a   Hug, Christopher ^b   Kasahara, David I ^a   Johnston, Richard A ^a,c   Williams, Alison S ^a   Verbout, Norah G ^a   Si, Huiqing ^a   Jastrab, Jordan ^b   Srivastava, Amit ^b   Williams, Erin S ^a   Ranscht, Barbara ^d   Shore, Stephanie A ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

^d BURNHAM INSTITUTE   (United States)

Author keywords

Airway responsiveness; Bronchoalveolar lavage; Inflammation; Neutrophil; T cadherin

Indexed keywords

ADIPONECTIN; CADHERIN; INTERLEUKIN 6; METHACHOLINE; OZONE; CYTOKINE; ISOPROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ENZYME LINKED IMMUNOSORBENT ASSAY; GENOTYPE; LUNG LAVAGE; MOUSE; NEUTROPHIL; NONHUMAN; PNEUMONIA; PROTEIN DEFICIENCY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ANIMAL; BLOOD; BODY WEIGHT; C57BL MOUSE; CELL COUNT; CYTOLOGY; DRUG EFFECT; EXPOSURE; LUNG; METABOLISM; PATHOLOGY;

MUS;

ADIPONECTIN; ANIMALS; BODY WEIGHT; BRONCHOALVEOLAR LAVAGE FLUID; CADHERINS; CELL COUNT; CYTOKINES; INHALATION EXPOSURE; LUNG; MICE; MICE, INBRED C57BL; OZONE; PROTEIN ISOFORMS;

EID: 77958143481     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2009-0086OC     Document Type: Article

References (59)

1. Shore SA, Johnston RA. Obesity and asthma. Pharmacol Ther 2006;110:83-102.
2. Ford ES. The epidemiology of obesity and asthma. J Allergy Clin Immunol 2005;115:897-909, quiz 910.
3. Alexeeff SE, Litonjua AA, Suh H, Sparrow D, Vokonas PS, Schwartz J. Ozone exposure and lung function: Effect modified by obesity and airways hyperresponsiveness in the VA Normative Aging Study. Chest 2007;132:1890-1897.
4. Bennett WD, Hazucha MJ, Folinsbee LJ, Bromberg PA, Kissling GE, London SJ. Acute pulmonary function response to ozone in young adults as a function of body mass index. Inhal Toxicol 2007;19:1147-1154.
5. Gent JF, Triche EW, Holford TR, Belanger K, Bracken MB, Beckett WS, Leaderer BP. Association of low-level ozone and fine particles with respiratory symptoms in children with asthma. JAMA 2003;290:1859-1867.
6. Tolbert PE, Mulholland JA, MacIntosh DL, Xu F, Daniels D, Devine OJ, Carlin BP, Klein M, Dorley J, Butler AJ, et al. Air quality and pediatric emergency room visits for asthma in Atlanta, Georgia, USA. Am J Epidemiol 2000;151:798-810.
7. Shore SA, Rivera-Sanchez YM, Schwartzman IN, Johnston RA. Responses to ozone are increased in obese mice. J Appl Physiol 2003;95:938-945.
8. 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 2006;290:L856-L865. (Pubitemid 43725047)
9. Johnston RA, Theman TA, Shore SA. Augmented responses to ozone in obese carboxypeptidase E-deficient mice. Am J Physiol Regul Integr Comp Physiol 2006;290:R126-R133.
10. Johnston RA, Theman TA, Lu FL, Terry RD, Williams ES, Shore SA. Diet-induced obesity causes innate airway hyperresponsiveness to methacholine and enhances ozone-induced pulmonary inflammation. J Appl Physiol 2008;104:1727-1735.
11. Kadowaki T, Yamauchi T, Kubota N. The physiological and pathophysiological role of adiponectin and adiponectin receptors in the peripheral tissues and CNS. FEBS Lett 2008;582:74-80. (Pubitemid 50012818)
12. Fantuzzi G. Adiponectin and inflammation: consensus and controversy. J Allergy Clin Immunol 2008;121:326-330.
13. Tsao TS, Murrey HE, Hug C, Lee DH, Lodish HF. Oligomerization state-dependent activation of NF-kappa B signaling pathway by adipocyte complement-related protein of 30 kDa (Acrp30). J Biol Chem 2002;277:29359-29362.
14. Schraw T, Wang ZV, Halberg N, Hawkins M, Scherer PE. Plasma adiponectin complexes have distinct biochemical characteristics. Endocrinology 2008;149:2270-2282.
15. Scherer PE. Adipose tissue: from lipid storage compartment to endocrine organ. Diabetes 2006;55:1537-1545.
16. Wolf AM, Wolf D, Rumpold H, Enrich B, Tilg H. Adiponectin induces the anti-inflammatory cytokines IL-10 and IL-1Ra in human leukocytes. Biochem Biophys Res Commun 2004;323:630-635.
17. Wulster-Radcliffe MC, Ajuwon KM, Wang J, Christian JA, Spurlock ME. Adiponectin differentially regulates cytokines in porcine macrophages. Biochem Biophys Res Commun 2004;316:924-929.
18. Ouchi N, Kihara S, Funahashi T, Matsuzawa Y, Walsh K. Obesity, adiponectin and vascular inflammatory disease. Curr Opin Lipidol 2003;14:561-566.
19. Shore SA, Terry RD, Flynt L, Xu A, Hug C. Adiponectin attenuates allergen-induced airway inflammation and hyperresponsiveness in mice. J Allergy Clin Immunol 2006;118:389-395. (Pubitemid 44142709)
20. Medoff BD, Okamoto Y, Leyton P, Weng M, Sandall BP, Raher MJ, Kihara S, Bloch KD, Libby P, Luster AD. Adiponectin deficiency increases allergic airway inflammation and pulmonary vascular remodeling. Am J Respir Cell Mol Biol 2009;41:397-406.
21. Yamauchi T, Kamon J, Ito Y, Tsuchida A, Yokomizo T, Kita S, Sugiyama T, Miyagishi M, Hara K, Tsunoda M, et al. Cloning of adiponectin receptors that mediate antidiabetic metabolic effects. Nature 2003;423:762-769.
22. Hug C, Wang J, Ahmad NS, Bogan JS, Tsao TS, Lodish HF. T-cadherin is a receptor for hexameric and high-molecular-weight forms of Acrp30/adiponectin. Proc Natl Acad Sci USA 2004;101:10308-10313.
23. Ranscht B, Dours-Zimmermann MT. T-cadherin, a novel cadherin cell adhesion molecule in the nervous system lacks the conserved cytoplasmic region. Neuron 1991;7:391-402.
24. Hebbard LW, Garlatti M, Young LJ, Cardiff RD, Oshima RG, Ranscht B. T-cadherin supports angiogenesis and adiponectin association with the vasculature in a mouse mammary tumor model. Cancer Res 2008;68:1407-1416.
25. Takeuchi T, Misaki A, Fujita J, Sonobe H, Ohtsuki Y. T-cadherin (CDH13, H-cadherin) expression downregulated surfactant protein d in bronchioloalveolar cells. Virchows Arch 2001;438:370-375. (Pubitemid 32285362)
26. Summer R, Fiack CA, Ikeda Y, Sato K, Dwyer D, Ouchi N, Fine A, Farber HW, Walsh K. Adiponectin deficiency: a model of pulmonary hypertension associated with pulmonary vascular disease. Am J Physiol Lung Cell Mol Physiol 2009;297:L432-L438.
27. Maeda N, Shimomura I, Kishida K, Nishizawa H, Matsuda M, Nagaretani H, Furuyama N, Kondo H, Takahashi M, Arita Y, et al. Diet-induced insulin resistance in mice lacking adiponectin/Acrp30. Nat Med 2002;8:731-737.
28. Wong GW, Krawczyk SA, Kitidis-Mitrokostas C, Ge G, Spooner E, Hug C, Gimeno R, Lodish HF. Identification and characterization of CTRP9, a novel secreted glycoprotein, from adipose tissue that reduces serum glucose in mice and forms heterotrimers with adiponectin. FASEB J 2009;23:241-258.
29. Williams AS, Issa R, Leung SY, Nath P, Ferguson GD, Bennett BL, Adcock IM, Chung KF. Attenuation of ozone-induced airway inflammation and hyper-responsiveness by c-Jun NH2 terminal kinase inhibitor SP600125. J Pharmacol Exp Ther 2007;322:351-359.
30. Johnston RA, Mizgerd JP, Flynt L, Quinton LJ, Williams ES, Shore SA. Type I interleukin-1 receptor is required for pulmonary responses to subacute ozone exposure in mice. Am J Respir Cell Mol Biol 2007;37:477-484.
31. Summer R, Little FF, Ouchi N, Takemura Y, Aprahamian T, Dwyer D, Fitzsimmons K, Suki B, Parameswaran H, Fine A, et al. Alveolar macrophage activation and an emphysema-like phenotype in adiponectin-deficient mice. Am J Physiol Lung Cell Mol Physiol 2008;294:L1035-L1042.
32. Hantos Z, Daroczy B, Suki B, Nagy S, Fredberg JJ. Input impedance and peripheral inhomogeneity of dog lungs. J Appl Physiol 1992;72:168-178.
33. Hjoberg J, Shore S, Kobzik L, Okinaga S, Hallock A, Vallone J, Subramaniam V, De Sanctis GT, Elias JA, Drazen JM, et al. Expression of nitric oxide synthase-2 in the lungs decreases airway resistance and responsiveness. J Appl Physiol 2004;97:249-259. (Pubitemid 38802526)
34. Pillow JJ, Korfhagen TR, Ikegami M, Sly PD. Overexpression of TGF-alpha increases lung tissue hysteresivity in transgenic mice. J Appl Physiol 2001;91:2730-2734.
35. Lang JE, Williams ES, Mizgerd JP, Shore SA. Effect of obesity on pulmonary inflammation induced by acute ozone exposure: role of interleukin-6. Am J Physiol Lung Cell Mol Physiol 2008;294:L1013-L1020.
36. Johnston RA, Mizgerd JP, Shore SA. CXCR2 is essential for maximal neutrophil recruitment and methacholine responsiveness after ozone exposure. Am J Physiol Lung Cell Mol Physiol 2005;288:L61-L67.
37. Johnston RA, Schwartzman IN, Flynt L, Shore SA. Role of interleukin-6 in murine airway responses to ozone. Am J Physiol Lung Cell Mol Physiol 2005;288:L390-L397.
38. Zhao Q, Simpson LG, Driscoll KE, Leikauf GD. Chemokine regulation of ozone-induced neutrophil and monocyte inflammation. Am J Physiol 1998;274:L39-L46. (Pubitemid 128736045)
39. Robbesom AA, Versteeg EM, Veerkamp JH, van Krieken JH, Bulten HJ, Smits HT, Willems LN, van Herwaarden CL, Dekhuijzen PN, van Kuppevelt TH. Morphological quantification of emphysema in small human lung specimens: comparison of methods and relation with clinical data. Mod Pathol 2003;16:1-7.
40. Flo C, Lopes FD, Kasahara DI, Silva AC, Jesus RC, Rivero DH, Saldiva PH, Martins MA, Jacob-Filho W. Effects of exercise training on papain-induced pulmonary emphysema in Wistar rats. J Appl Physiol 2006;100:281-285. (Pubitemid 43671119)
41. Schmittgen TD, Zakrajsek BA, Mills AG, Gorn V, Singer MJ, Reed MW. Quantitative reverse transcription-polymerase chain reaction to study mRNA decay: comparison of endpoint and real-time methods. Anal Biochem 2000;285:194-204.
42. Johnston RA, Theman TA, Terry RD, Williams ES, Shore SA. Pulmonary responses to acute ozone exposure in fasted mice: effect of leptin administration. J Appl Physiol 2007;102:149-156.
43. Last JA, Gohil K, Mathrani VC, Kenyon NJ. Systemic responses to inhaled ozone in mice: cachexia and down-regulation of liver xenobiotic metabolizing genes. Toxicol Appl Pharmacol 2005;208:117-126.
44. Hattori Y, Hattori S, Akimoto K, Nishikimi T, Suzuki K, Matsuoka H, Kasai K. Globular adiponectin activates nuclear factor-kappaB and activating protein-1 and enhances angiotensin II-induced proliferation in cardiac fibroblasts. Diabetes 2007;56:804-808. (Pubitemid 46348485)
45. Ehling A, Schaffler A, Herfarth H, Tarner IH, Anders S, Distler O, Paul G, Distler J, Gay S, Scholmerich J, et al. The potential of adiponectin in driving arthritis. J Immunol 2006;176:4468-4478.
46. Tsatsanis C, Zacharioudaki V, Androulidaki A, Dermitzaki E, Charalampopoulos I, Minas V, Gravanis A, Margioris AN. Adiponectin induces TNF-alpha and IL-6 in macrophages and promotes tolerance to itself and other pro-inflammatory stimuli. Biochem Biophys Res Commun 2005;335:1254-1263.
47. Ogunwobi OO, Beales IL. Adiponectin stimulates proliferation and cytokine secretion in colonic epithelial cells. Regul Pept 2006;134:105-113.
48. Miller M, Cho JY, Pham A, Ramsdell J, Broide DH. Adiponectin and functional adiponectin receptor 1 are expressed by airway epithelial cells in chronic obstructive pulmonary disease. J Immunol 2009;182:684-691.
49. Wert SE. Does adiponectin play a role in pulmonary emphysema? Am J Physiol Lung Cell Mol Physiol 2008;294:L1032-L1034.
50. 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 2004;96:2019-2027.
51. 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 2007;102:221-230.
52. Podgorski A, Sosnowski TR, Gradon L. Deactivation of the pulmonary surfactant dynamics by toxic aerosols and gases. J Aerosol Med 2001;14:455-466.
53. Kierstein S, Poulain FR, Cao Y, Grous M, Mathias R, Kierstein G, Beers MF, Salmon M, Panettieri RA Jr, Haczku A. Susceptibility to ozone-induced airway inflammation is associated with decreased levels of surfactant protein D. Respir Res 2006;7:85.
54. Wang Y, Lam KS, Xu JY, Lu G, Xu LY, Cooper GJ, Xu A. Adiponectin inhibits cell proliferation by interacting with several growth factors in an oligomerization dependent manner. J Biol Chem 2005;280:18341-18347.
55. Masaie H, Oritani K, Yokota T, Takahashi I, Shirogane T, Ujiie H, Ichii M, Saitoh N, Maeda T, Tanigawa R, et al. Adiponectin binds to chemokines via the globular head and modulates interactions between chemokines and heparan sulfates. Exp Hematol 2007;35:947-956. (Pubitemid 46802989)
56. Takemura Y, Ouchi N, Shibata R, Aprahamian T, Kirber MT, Summer RS, Kihara S, Walsh K. Adiponectin modulates inflammatory reactions via calreticulin receptor-dependent clearance of early apoptotic bodies. J Clin Invest 2007;117:375-386.
57. Scherer PE, Williams S, Fogliano M, Baldini G, Lodish HF. A novel serum protein similar to C1q, produced exclusively in adipocytes. J Biol Chem 1995;270:26746-26749.
58. Mehta D, Malik AB. Signaling mechanisms regulating endothelial permeability. Physiol Rev 2006;86:279-367.
59. Shibata R, Sato K, Kumada M, Izumiya Y, Sonoda M, Kihara S, Ouchi N, Walsh K. Adiponectin accumulates in myocardial tissue that has been damaged by ischemia-reperfusion injury via leakage from the vascular compartment. Cardiovasc Res 2007;74:471-479.