Transgenic expression of human S100A12 induces structural airway abnormalities and limited lung inflammation in a mouse model of allergic inflammation

Clinical and Experimental Allergy

Volumn 41, Issue 6, 2011, Pages 878-889

  Hofmann Bowman, M A ^a   Heydemann, A ^a   Gawdzik, J ^a   Shilling, R A ^a   Camoretti Mercado, B ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Airway remodelling; Animal models; Apoptosis; Calgranulins; Inflammation; RAGE; Smooth muscle

Indexed keywords

BIOLOGICAL MARKER; CALCIUM BINDING PROTEIN; CALGRANULIN; CASPASE 3; FAS ANTIGEN; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; OVALBUMIN; PROTEIN S 100; PROTEIN S100A12; UNCLASSIFIED DRUG;

AIRWAY; ALLERGIC ASTHMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; BRONCHUS; CONTROLLED STUDY; ENZYME ACTIVATION; EOSINOPHILIA; INFLAMMATION; LUNG FUNCTION; LUNG LAVAGE; MOUSE; MUCUS; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMOOTH MUSCLE; TRANSGENIC MOUSE; WILD TYPE;

AIRWAY REMODELING; ANIMALS; APOPTOSIS; BRONCHOALVEOLAR LAVAGE FLUID; BRONCHOCONSTRICTION; CHEMOKINES; DISEASE MODELS, ANIMAL; HUMANS; HYPERSENSITIVITY; IMMUNITY, HUMORAL; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MYOCYTES, SMOOTH MUSCLE; OVALBUMIN; PNEUMONIA; RESPIRATORY MUCOSA; RESPIRATORY SYSTEM; S100 PROTEINS;

EID: 79955760681     PISSN: 09547894     EISSN: 13652222     Source Type: Journal    
DOI: 10.1111/j.1365-2222.2011.03714.x     Document Type: Article

References (50)

1. Wu J, Kobayashi M, Sousa EA et al. Differential proteomic analysis of bronchoalveolar lavage fluid in asthmatics following segmental antigen challenge. Mol Cell Proteomics 2005; 4:1251-64.
2. Heizmann CW, Ackermann GE, Galichet A. Pathologies involving the S100 proteins and RAGE. Subcell Biochem 2007; 45:93-138.
3. Foell D, Kane D, Bresnihan B et al. Expression of the pro-inflammatory protein S100A12 (EN-RAGE) in rheumatoid and psoriatic arthritis. Rheumatology (Oxford) 2003; 42:1383-9.
4. Foell D, Kucharzik T, Kraft M et al. Neutrophil derived human S100A12 (EN-RAGE) is strongly expressed during chronic active inflammatory bowel disease. Gut 2003; 52:847-53.
5. Foell D, Ichida F, Vogl T et al. S100A12 (EN-RAGE) in monitoring Kawasaki disease. Lancet 2003; 361:1270-2.
6. Yang Z, Yan WX, Cai H et al. S100A12 provokes mast cell activation: a potential amplification pathway in asthma and innate immunity. J Allergy Clin Immunol 2007; 119:106-14.
7. Lorenz E, Muhlebach MS, Tessier PA et al. Different expression ratio of S100A8/A9 and S100A12 in acute and chronic lung diseases. Respir Med 2008; 102:567-73.
8. Hofmann MA, Drury S, Fu C et al. RAGE mediates a novel proinflammatory axis: a central cell surface receptor for S100/calgranulin polypeptides. Cell 1999; 97:889-901.
9. Vogl T, Tenbrock K, Ludwig S et al. Mrp8 and Mrp14 are endogenous activators of Toll-like receptor 4, promoting lethal, endotoxin-induced shock. Nat Med 2007; 13:1042-9.
10. Brett J, Schmidt AM, Yan SD et al. Survey of the distribution of a newly characterized receptor for advanced glycation end products in tissues. Am J Pathol 1993; 143:1699-712.
11. Demling N, Ehrhardt C, Kasper M, Laue M, Knels L, Rieber EP. Promotion of cell adherence and spreading: a novel function of RAGE, the highly selective differentiation marker of human alveolar epithelial type I cells. Cell Tissue Res 2006; 323:475-88.
12. Yan SF, Ramasamy R, Schmidt AM. The receptor for advanced glycation endproducts (RAGE) and cardiovascular disease. Expert Rev Mol Med 2009; 11:e9.
13. Harja E, Bu DX, Hudson BI et al. Vascular and inflammatory stresses mediate atherosclerosis via RAGE and its ligands in apoE-/- mice. J Clin Invest 2008; 118:183-94.
14. Englert JM, Hanford LE, Kaminski N et al. A role for the receptor for advanced glycation end products in idiopathic pulmonary fibrosis. Am J Pathol 2008; 172:583-91.
15. van Zoelen MA, Schouten M, de Vos AF et al. The receptor for advanced glycation end products impairs host defense in pneumococcal pneumonia. J Immunol 2009; 182:4349-56.
16. Fuellen G, Nacken W, Sorg C, Kerkhoff C. Computational searches for missing orthologs: the case of S100A12 in mice. OMICS 2004; 8:334-40.
17. Solway J, Seltzer J, Samaha FF et al. Structure and expression of a smooth muscle cell-specific gene, SM22 alpha. J Biol Chem 1995; 270:13460-9.
18. Hofmann Bowman M, Wilk J, Heydemann A et al. S100A12 mediates aortic wall remodeling and aortic aneurysm. Circ Res 2010; 106:145-54.
19. Tong J, Bandulwala HS, Clay BS et al. Fas-positive T cells regulate the resolution of airway inflammation in a murine model of asthma. J Exp Med 2006; 203:1173-84.
20. Heydemann A, Huber JM, Demonbreun A, Hadhazy M, McNally EM. Genetic background influences muscular dystrophy. Neuromuscul Disord 2005; 15:601-9.
21. Noori F, Abduljawad S, Suffin DM et al. Mounier-Kuhn syndrome: a case report. Lung 2010; 188:353-4.
22. Hardaker EL, Bacon AM, Carlson K et al. Regulation of TNF-alpha- and IFN-gamma-induced CXCL10 expression: participation of the airway smooth muscle in the pulmonary inflammatory response in chronic obstructive pulmonary disease. FASEB J 2004; 18:191-3.
23. Clarke DL, Clifford RL, Jindarat S et al. TNF-alpha and IFN-gamma synergistically enhance transcriptional activation of CXCL10 in human airway smooth muscle cells via STAT-1, NF-kappaB, and the transcriptional coactivator CREB-binding protein. J Biol Chem 285:29101-10.
24. Jinquan T, Jing C, Jacobi HH et al. CXCR3 expression and activation of eosinophils: role of IFN-gamma-inducible protein-10 and monokine induced by IFN-gamma. J Immunol 2000; 165:1548-56.
25. Medoff BD, Sauty A, Tager AM et al. IFN-gamma-inducible protein 10 (CXCL10) contributes to airway hyperreactivity and airway inflammation in a mouse model of asthma. J Immunol 2002; 168:5278-86.
26. Yui S, Nakatani Y, Mikami M. Calprotectin (S100A8/S100A9), an inflammatory protein complex from neutrophils with a broad apoptosis-inducing activity. Biol Pharm Bull 2003; 26:753-60.
27. Ghavami S, Kerkhoff C, Chazin WJ et al. S100A8/9 induces cell death via a novel, RAGE-independent pathway that involves selective release of Smac/DIABLO and Omi/HtrA2. Biochim Biophys Acta 2008; 1783:297-311.
28. Tsoporis JN, Izhar S, Leong-Poi H, Desjardins JF, Huttunen HJ, Parker TG. S100B interaction with the receptor for advanced glycation end products (RAGE): a novel receptor-mediated mechanism for myocyte apoptosis postinfarction. Circ Res 2010; 106:93-101.
29. Morbini P, Villa C, Campo I, Zorzetto M, Inghilleri S, Luisetti M. The receptor for advanced glycation end products and its ligands: a new inflammatory pathway in lung disease? Mod Pathol 2006; 19:1437-45.
30. Cookson WO, Ubhi B, Lawrence R et al. Genetic linkage of childhood atopic dermatitis to psoriasis susceptibility loci. Nat Genet 2001; 27:372-3.
31. Sharma M, Mehla K, Batra J, Ghosh B. Association of a chromosome 1q21 locus in close proximity to a late cornified envelope-like proline-rich 1 (LELP1) gene with total serum IgE levels. J Hum Genet 2007; 52:378-83.
32. Rammes A, Roth J, Goebeler M, Klempt M, Hartmann M, Sorg C. Myeloid-related protein (MRP) 8 and MRP14, calcium-binding proteins of the S100 family, are secreted by activated monocytes via a novel, tubulin-dependent pathway. J Biol Chem 1997; 272:9496-502.
33. Kheradmand F, Corry DB. Discovery of novel markers in allergic lung inflammation through proteomic-based technologies. Expert Rev Proteomics 2008; 5:9-12.
34. Halayko AJ, Ghavami S. S100A8/A9: a mediator of severe asthma pathogenesis and morbidity? Can J Physiol Pharmacol 2009; 87:743-55.
35. Hershenson MB, Brown M, Camoretti-Mercado B, Solway J. Airway smooth muscle in asthma. Annu Rev Pathol 2008; 3:523-55.
36. Ebina M, Takahashi T, Chiba T, Motomiya M. Cellular hypertrophy and hyperplasia of airway smooth muscles underlying bronchial asthma. A 3-D morphometric study. Am Rev Respir Dis 1993; 148:720-6.
37. Panettieri RA Jr, Kotlikoff MI, Gerthoffer WT et al. Airway smooth muscle in bronchial tone, inflammation, and remodeling: basic knowledge to clinical relevance. Am J Respir Crit Care Med 2008; 177:248-52.
38. Camoretti-Mercado B. Targeting the airway smooth muscle for asthma treatment. Transl Res 2009; 154:165-74.
39. Waern I, Jonasson S, Hjoberg J et al. Mouse mast cell protease 4 is the major chymase in murine airways and has a protective role in allergic airway inflammation. J Immunol 2009; 183:6369-76.
40. Greenlee KJ, Corry DB, Engler DA et al. Proteomic identification of in vivo substrates for matrix metalloproteinases 2 and 9 reveals a mechanism for resolution of inflammation. J Immunol 2006; 177:7312-21.
41. Bozinovski S, Cross M, Vlahos R et al. S100A8 chemotactic protein is abundantly increased, but only a minor contributor to LPS-induced, steroid resistant neutrophilic lung inflammation in vivo. J Proteome Res 2005; 4:136-45.
42. Calvo FQ, Fillet M, de Seny D et al. Biomarker discovery in asthma-related inflammation and remodeling. Proteomics 2009; 9:2163-70.
43. Xu YD, Cui JM, Wang Y et al. The early asthmatic response is associated with glycolysis, calcium binding and mitochondria activity as revealed by proteomic analysis in rats. Respir Res 2010; 11:107.
44. Wong WS, Zhao J. Proteome analysis of chronically inflamed lungs in a mouse chronic asthma model. Int Arch Allergy Immunol 2008; 147:179-89.
45. Kumar RK, Foster PS. Murine model of chronic human asthma. Immunol Cell Biol 2001; 79:141-4.
46. Shinagawa K, Kojima M. Mouse model of airway remodeling: strain differences. Am J Respir Crit Care Med 2003; 168:959-67.
47. Hofmann Bowman MA, Gawdzik J, Bukhari U et al. S100A12 in vascular smooth muscle accelerates vascular calcification in apolipoprotein E-null mice by activating an osteogenic gene regulatory program. Arterioscler Thromb Vasc Biol 2011; 31:337-44.
48. Hudson BI, Carter AM, Harja E et al. Identification, classification, and expression of RAGE gene splice variants. FASEB J 2008; 22:1572-80.
49. Ma W, Lee SE, Guo J et al. RAGE ligand upregulation of VEGF secretion in ARPE-19 cells. Invest Ophthalmol Vis Sci 2007; 48:1355-61.
50. Goyette J, Yan WX, Yamen E et al. Pleiotropic roles of S100A12 in coronary atherosclerotic plaque formation and rupture. J Immunol 2009; 183:593-603.