Hyaluronan fragments promote inflammation by down-regulating the anti-inflammatory A2a receptor

American Journal of Respiratory Cell and Molecular Biology

Volumn 45, Issue 4, 2011, Pages 675-683

  Collins, Samuel L ^a   Black, Katharine E ^a   Chan Li, Yee ^a   Ahn, Young Hoon ^a   Cole, Philip A ^a   Powell, Jonathan D ^b   Horton, Maureen R ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Adenosine; Extracellular matrix; Hyaluronan; Inflammation; Macrophages

Indexed keywords

ADENOSINE A2A RECEPTOR; HERMES ANTIGEN; HYALURONIC ACID; PEPTIDE; PROTEIN KINASE C;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; EXTRACELLULAR MATRIX; GENE EXPRESSION; INFLAMMATION; MACROPHAGE FUNCTION; MOLECULAR WEIGHT; MOUSE; NONHUMAN; PROTEIN EXPRESSION; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION;

ANIMALS; ANTI-INFLAMMATORY AGENTS; ANTIGENS, CD44; CELL LINE; DISEASE MODELS, ANIMAL; DOWN-REGULATION; HYALURONIC ACID; INFLAMMATION MEDIATORS; LIPOPOLYSACCHARIDES; MACROPHAGES, ALVEOLAR; MACROPHAGES, PERITONEAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELOID DIFFERENTIATION FACTOR 88; PEPTIDE FRAGMENTS; PEPTIDES; PNEUMONIA; PROTEIN KINASE C; PROTEIN KINASE INHIBITORS; RECEPTOR, ADENOSINE A2A; RNA, MESSENGER; TIME FACTORS; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4;

EID: 80053644689     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2010-0387OC     Document Type: Article

References (46)

1. Laurent TC. Functions of hyaluronan. Ann Rheum Dis 1995;54:429.
2. Scheibner KA, Lutz MA, Boodoo S, Fenton MJ, Powell JD, Horton MR. Hyaluronan fragments act as an endogenous danger signal by engaging TLR2. J Immunol 2006;177:1272-1281. (Pubitemid 44036633)
3. McKee C, Penno M, Cowman M, Burdick M, Strieter R, Bao C, Noble P. Hyaluronan (HA) fragments induce chemokine gene expression in alveolar macrophages: the role of HA size and CD44. J Clin Invest 1996;98:2403-2413. (Pubitemid 26394217)
4. Boodoo S, Spannhake EW, Powell JD, Horton MR. Differential regulation of hyaluronan-induced IL-8 and IP-10 in airway epithelial cells. Am J Physiol 2006;291:L479-L486. (Pubitemid 44343725)
5. Powell JD, Horton MR. Threat matrix: low-molecular-weight hyaluronan (HA) as a danger signal. Immunol Res 2005;31:207-218. (Pubitemid 40628958)
6. Mascarenhas MM, Day RM, Ochoa CD, Choi WI, Yu L, Ouyang B, Garg HG, Hales CA, Quinn DA. Low molecular weight hyaluronan from stretched lung enhances interleukin-8 expression. Am J Respir Cell Mol Biol 2004;30:51-60. (Pubitemid 38085258)
7. Hodge-Dufour J, Noble PW, Horton MR, Bao C, Wysoka M, Burdick MD, Strieter RM, Trinchieri G, Pure E. Induction of IL-12 and chemokines by hyaluronan requires adhesion-dependent priming of resident but not elicited macrophages. J Immunol 1997;159:2492-2500. (Pubitemid 127681045)
8. Horton MR, McKee CM, Bao C, Liao F, Farber JM, Hodge-DuFour J, Pure E, Oliver BL, Wright TM, Noble PW. Hyaluronan fragments synergize with interferon-gamma to induce the C-X-C chemokines MIG and interferon-inducible protein-10 in mouse macrophages. J Biol Chem 1998;52:35088-35094. (Pubitemid 29028210)
9. Horton MR, Olman MA, Bao C, White KE, Choi AM, Chin BY, Noble PW, Lowenstein CJ. Regulation of plasminogen activator inhibitor-1 and urokinase by hyaluronan fragments in mouse macrophages. Am J Physiol 2000;279:L707-L715.
10. Horton MR, Shapiro S, Bao C, Lowenstein CJ, Noble PW. Induction and regulation of macrophage metalloelastase by hyaluronan fragments in mouse macrophages. J Immunol 1999;162:4171-4176. (Pubitemid 29314803)
11. McKee CM, Lowenstein CJ, Horton MR, Wu J, Bao C, Chin BY, Choi AM, Noble PW. Hyaluronan fragments induce nitric-oxide synthase in murine macrophages through a nuclear factor kappaB-dependent mechanism. J Biol Chem 1997;272:8013-8018. (Pubitemid 27137366)
12. Dubyak GR, el-Moatassim C. Signal transduction via P2-purinergic receptors for extracellular ATP and other nucleotides. Am J Physiol 1993;265:C577-C606.
13. Ohta A, Sitkovsky M. Role of G-protein-coupled adenosine receptors in downregulation of inflammation and protection from tissue damage. Nature 2001;414:916-920. (Pubitemid 34024743)
14. Khoa ND, Montesinos MC, Reiss AB, Delano D, Awadallah N, Cronstein BN. Inflammatory cytokines regulate function and expression of adenosine A(2a) receptors in human monocytic THP-1 cells. J Immunol 2001;167:4026-4032. (Pubitemid 32910848)
15. Stiles GL. Adenosine receptors. J Biol Chem 1992;267:6451-6454.
16. Montminy M. Transcriptional regulation by cyclic amp. Annu Rev Biochem 1997;66:807-822. (Pubitemid 27274675)
17. Aronoff DM, Canetti C, Serezani CH, Luo M, Peters-Golden M. Cutting edge: macrophage inhibition by cyclic AMP (cAMP): differential roles of protein kinase a and exchange protein directly activated by cAMP-1. J Immunol 2005;174:595-599. (Pubitemid 40094248)
18. Scheibner KA, Boodoo S, Collins S, Black KE, Chan-Li Y, Zarek P, Powell JD, Horton MR. The adenosine a2a receptor inhibits matrix induced inflammation in a novel fashion. Am J Respir Cell Mol Biol 2009;40:251-259.
19. Mummert DI, Takashima A, Ellinger L, Mummert ME. Involvement of hyaluronan in epidermal langerhans cell maturation and migration in vivo. J Dermatol Sci 2003;33:91-97. (Pubitemid 37315901)
20. Jiang D, Liang J, Fan J, Yu S, Chen S, Luo Y, Prestwich GD, Mascarenhas MM, Garg HG, Quinn DA, et al. Regulation of lung injury and repair by Toll-like receptors and hyaluronan. Nat Med 2005;11:1173-1179. (Pubitemid 43093664)
21. Davis IC, Xu A, Gao Z, Hickman-Davis JM, Factor P, Sullender WM, Matalon S. Respiratory syncytial virus induces insensitivity to beta-adrenergic agonists in mouse lung epithelium in vivo. Am J Physiol 2007;293:L281-L289. (Pubitemid 47205007)
22. Noble PW, McKee CM, Cowman M, Shin HS. Hyaluronan fragments activate an NF-κB/IκBα autoregulatory loop in murine macrophages. J Exp Med 1996;183:2373-2378. (Pubitemid 26158930)
23. Kim Y, Lee YS, Choe J, Lee H, Kim YM, Jeoung D. CD44-epidermal growth factor receptor interaction mediates hyaluronic acid-promoted cell motility by activating protein kinase c signaling involving Akt, Rac1, Phox, reactive oxygen species, focal adhesion kinase, and MMP-2. J Biol Chem 2008;283:22513-22528.
24. + Tregs resolve experimental lung injury in mice and are present in humans with acute lung injury. J Clin Invest 2009;119:2898-2913.
25. Wang Q, Teder P, Judd NP, Noble PW, Doerschuk CM. CD44 deficiency leads to enhanced neutrophil migration and lung injury in escherichia coli pneumonia in mice. Am J Pathol 2002;161:2219-2228. (Pubitemid 35434866)
26. Day YJ, Huang L, McDuffie MJ, Rosin DL, Ye H, Chen JF, Schwarzschild MA, Fink JS, Linden J, Okusa MD. Renal protection from ischemia mediated by A2a adenosine receptors on bone marrow-derived cells. J Clin Invest 2003;112:883-891. (Pubitemid 38063746)
27. Teder P, Vandivier RW, Jiang D, Liang J, Cohn L, Pure E, Henson PM, Noble PW. Resolution of lung inflammation by CD44. Science 2002;296:155-158. (Pubitemid 34280077)
28. Zhao H, Leu SW, Shi L, Dedaj R, Zhao G, Garg HG, Shen L, Lien E, Fitzgerald KA, Shiedlin A, et al. TLR4 is a negative regulator in noninfectious lung inflammation. J Immunol 2010;184:5308-5314.
29. Bjermer L, Eklund A, Blaschke E. Bronchoalveolar lavage fibronectin in patients with sarcoidosis: Correlation to hyaluronan and disease activity. Eur Respir J 1991;4:965-971.
30. Riise GC AS, Larsson S, Enander I, Jones I, Larsson P, Andersson B. Bronchial inflammation in chronic bronchitis assessed by measurement of cell products in bronchial lavage fluid. Thorax 1995;50:360-365.
31. Nedvetzki S, Gonen E, Assayag N, Reich R, Williams RO, Thurmond RL, Huang JF, Neudecker BA, Wang FS, Turley EA, et al. RHAMM, a receptor for hyaluronan-mediated motility, compensates for CD44 in inflamed CD44-knockout mice: a different interpretation of redundancy. Proc Natl Acad Sci USA 2004;101:18081-18086. (Pubitemid 40054077)
32. Bartolazzi A, Peach R, Aruffo A, Stamenkovic I. Interaction between CD44 and hyaluronate is directly implicated in the regulation of tumor development. J Exp Med 1994;180:53-66. (Pubitemid 24181055)
33. Lesley J, Hyman R, Kincade P. CD44 and its interaction with extracellular matrix. Adv Immunol 1993;54:271-335. (Pubitemid 23289255)
34. Termeer C, Benedix F, Sleeman J, Fieber C, Voith U, Ahrens T, Miyake K, Freudenberg M, Galanos C, Simon JC. Oligosaccharides of hyaluronan activate dendritic cells via Toll-like receptor 4. J Exp Med 2002;195:99-111. (Pubitemid 34074500)
35. Chunn JL, Young HW, Banerjee SK, Colasurdo GN, Blackburn MR. Adenosine-dependent airway inflammation and hyperresponsiveness in partially adenosine deaminase-deficient mice. J Immunol 2001;167:4676-4685. (Pubitemid 32954349)
36. Chunn JL, Mohsenin A, Young HW, Lee CG, Elias JA, Kellems RE, Blackburn MR. Partially adenosine deaminase-deficient mice develop pulmonary fibrosis in association with adenosine elevations. Am J Physiol 2006;290:L579-L587. (Pubitemid 43725103)
37. Chunn JL, Molina JG, Mi T, Xia Y, Kellems RE, Blackburn MR. Adenosine-dependent pulmonary fibrosis in adenosine deaminase-deficient mice. J Immunol 2005;175:1937-1946. (Pubitemid 41023101)
38. Sun CX, Young HW, Molina JG, Volmer JB, Schnermann J, Blackburn MR. A protective role for the A1 adenosine receptor in adenosine-dependent pulmonary injury. J Clin Invest 2005;115:35-43. (Pubitemid 40385503)
39. Blackburn MR, Lee CG, Young HW, Zhu Z, Chunn JL, Kang MJ, Banerjee SK, Elias JA. Adenosine mediates IL-13-induced inflammation and remodeling in the lung and interacts in an IL-13-adenosine amplification pathway. J Clin Invest 2003;112:332-344. (Pubitemid 38063762)
40. Liu X, Ostrom RS, Insel PA. cAMP-elevating agents and adenylyl cyclase overexpression promote an antifibrotic phenotype in pulmonary fibroblasts. Am J Physiol Cell Physiol 2004;286:C1089-C1099. (Pubitemid 38506924)
41. Zhong H, Belardinelli L, Maa T, Zeng D. Synergy between A2b adenosine receptors and hypoxia in activating human lung fibroblasts. Am J Respir Cell Mol Biol 2005;32:2-8. (Pubitemid 40053298)
42. Allen-Gipson DS, Wong J, Spurzem JR, Sisson JH, Wyatt TA. Adenosine A2a receptors promote adenosine-stimulated wound healing in bronchial epithelial cells. Am J Physiol 2006;290:L849-L855. (Pubitemid 43725046)
43. Zhong H, Wu Y, Belardinelli L, Zeng D. A2b adenosine receptors induce IL-19 from bronchial epithelial cells, resulting in TNF-{alpha} increase. Am J Respir Cell Mol Biol 2006;35:587-592. (Pubitemid 44706432)
44. Bonneau O, Wyss D, Ferretti S, Blaydon C, Stevenson CS, Trifilieff A. Effect of adenosine A2a receptor activation in murine models of respiratory disorders. Am J Physiol 2006;290:L1036-L1043. (Pubitemid 43725066)
45. Chan ES, Montesinos MC, Fernandez P, Desai A, Delano DL, Yee H, Reiss AB, Pillinger MH, Chen JF, Schwarzschild MA, et al. Adenosine A(2a) receptors play a role in the pathogenesis of hepatic cirrhosis. Br J Pharmacol 2006;148:1144-1155. (Pubitemid 44223020)
46. Hasko G, Xu DZ, Lu Q, Nemeth ZH, Jabush J, Berezina TL, Zaets SB, Csoka B, Deitch EA. Adenosine A2a receptor activation reduces lung injury in trauma/hemorrhagic shock. Crit Care Med 2006;34:1119-1125.