Adenosine and inflammation: CD39 and CD73 are critical mediators in LPS-induced PMN trafficking into the lungs

FASEB Journal

Volumn 23, Issue 2, 2009, Pages 473-482

  Reutershan, Jörg ^a   Vollmer, Irene ^a   Stark, Stefanie ^a   Wagner, Rosalyn ^a   Ngamsri, Kristian Christos ^a   Eltzschig, Holger K ^a,b  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

Acute lung injury; ARDS; Chemotaxis; Migration; Neutrophil; PMN

Indexed keywords

5' NUCLEOTIDASE; ADENOSINE; APYRASE; CD39 ANTIGEN;

ARTICLE; CONTROLLED STUDY; GENE TARGETING; IN VIVO STUDY; INFLAMMATION; LUNG EDEMA; LUNG INJURY; MALE; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL;

5'-NUCLEOTIDASE; ADENOSINE; ANIMALS; ANTIGENS, CD; APYRASE; CELL MOVEMENT; GENE EXPRESSION REGULATION; INFLAMMATION; LIPOPOLYSACCHARIDES; LUNG DISEASES; MALE; MICE; MICE, KNOCKOUT; NEUTROPHILS; NUCLEOTIDASES; PHOSPHORYLATION; SOLUBILITY; TRANSCRIPTION, GENETIC;

MUS;

EID: 59649088866     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.08-119701     Document Type: Article

References (60)

1. Ware, L. B., and Matthay, M. A. (2000) The acute respiratory distress syndrome. N. Engl. J. Med. 342, 1334-1349
2. Rubenfeld, G. D., Caldwell, E., Peabody, E., Weaver, J., Martin, D. P., Neff, M., Stern, E. J., and Hudson, L. D. (2005) Incidence and outcomes of acute lung injury. N. Engl. J. Med. 353, 1685-1693
3. Martin, T. R. (2002) Neutrophils and lung injury: getting it right. J. Clin. Invest. 110, 1603-1605
4. Belperio, J. A., Keane, M. P., Burdick, M. D., Londhe, V., Xue, Y. Y., Li, K., Phillips, R. J., and Strieter, R. M. (2002) Critical role for CXCR2 and CXCR2 ligands during the pathogenesis of ventilator-induced lung injury. J. Clin. Invest. 110, 1703-1716
5. Reutershan, J., Morris, M. A., Burcin, T. L., Smith, D. F., Chang, D., Saprito, M. S., and Ley, K. (2006) Critical role of endothelial CXCR2 in LPS-induced neutrophil migration into the lung. J. Clin. Invest. 116, 695-702
6. Reutershan, J., Stockton, R., Zarbock, A., Sullivan, G. W., Chang, D., Scott, D., Schwartz, M. A., and Ley, K. (2007) Blocking p21-activated kinase reduces lipopolysaccharide-induced acute lung injury by preventing polymorphonuclear leukocyte infiltration. Am. J. Respir. Crit. Care Med. 175, 1027-1035
7. Folkesson, H. G., Matthay, M. A., Hebert, C. A., and Broaddus, V. C. (1995) Acid aspiration-induced lung injury in rabbits is mediated by interleukin-8-dependent mechanisms. J. Clin. Invest. 96, 107-116
8. Fredholm, B. B. (2007) Adenosine, an endogenous distress signal, modulates tissue damage and repair. Cell Death Differ. 14, 1315-1323
9. Cronstein, B. N., Naime, D., and Ostad, E. (1993) The antiinflammatory mechanism of methotrexate. Increased adenosine release at inflamed sites diminishes leukocyte accumulation in an in vivo model of inflammation. J. Clin. Invest. 92, 2675-2682
10. Thiel, M., Chouker, A., Ohta, A., Jackson, E., Caldwell, C., Smith, P., Lukashev, D., Bittmann, I., and Sitkovsky, M. V. (2005) Oxygenation inhibits the physiological tissue-protecting mechanism and thereby exacerbates acute inflammatory lung injury. PLoS Biol. 3, e174
11. Ohta, A., and Sitkovsky, M. (2001) Role of G-protein-coupled adenosine receptors in downregulation of inflammation and protection from tissue damage. Nature 414, 916-920
12. Day, Y. J., Marshall, M. A., Huang, L., McDuffie, M. J., Okusa, M. D., and Linden, J. (2004) Protection from ischemic liver injury by activation of A2A adenosine receptors during reperfusion: inhibition of chemokine induction. Am. J. Physiol. Gastrointest. Liver Physiol. 286, G285-G293
13. Yang, Z., Day, Y. J., Toufektsian, M. C., Ramos, S. I., Marshall, M., Wang, X. Q., French, B. A., and Linden, J. (2005) Infarctsparing effect of A2A-adenosine receptor activation is due primarily to its action on lymphocytes. Circulation 111, 2190-2197
14. Yang, D., Koupenova, M., McCrann, D. J., Kopeikina, K. J., Kagan, H. M., Schreiber, B. M., and Ravid, K. (2008) The A2b adenosine receptor protects against vascular injury. Proc. Natl. Acad. Sci. U. S. A. 105, 792-796
15. Yang, D., Zhang, Y., Nguyen, H. G., Koupenova, M., Chauhan, A. K., Makitalo, M., Jones, M. R., St Hilaire, C., Seldin, D. C., Toselli, P., Lamperti, E., Schreiber, B. M., Gavras, H., Wagner, D. D., and Ravid, K. (2006) The A2B adenosine receptor protects against inflammation and excessive vascular adhesion. J. Clin. Invest. 116, 1913-1923
16. Eckle, T., Kohler, D., Lehmann, R., El Kasmi, K. C., and Eltzschig, H. K. (2008) Hypoxia-inducible factor-1 is central to cardioprotection: a new paradigm for ischemic preconditioning. Circulation 118, 166-175
17. Eckle, T., Krahn, T., Grenz, A., Kohler, D., Mittelbronn, M., Ledent, C., Jacobson, M. A., Osswald, H., Thompson, L. F., Unertl, K., and Eltzschig, H. K. (2007) Cardioprotection by ecto-5'-nucleotidase (CD73) and A2B adenosine receptors. Circulation 115, 1581-1590
18. Grenz, A., Osswald, H., Eckle, T., Yang, D., Zhang, H., Tran, Z. V., Klingel, K., Ravid, K., and Eltzschig, H. K. (2008) The reno-vascular A2B adenosine receptor protects the kidney from ischemia. PLoS Med. 5, e137
19. Eckle, T., Faigle, M., Grenz, A., Laucher, S., Thompson, L. F., and Eltzschig, H. K. (2008) A2B adenosine receptor dampens hypoxia-induced vascular leak. Blood 111, 2024-2035
20. Eltzschig, H. K., Ibla, J. C., Furuta, G. T., Leonard, M. O., Jacobson, K. A., Enjyoji, K., Robson, S. C., and Colgan, S. P. (2003) Coordinated adenine nucleotide phosphohydrolysis and nucleoside signaling in posthypoxic endothelium: role of ectonucleotidases and adenosine A2B receptors. J. Exp. Med. 198, 783-796
21. Eltzschig, H. K., Thompson, L. F., Karhausen, J., Cotta, R. J., Ibla, J. C., Robson, S. C., and Colgan, S. P. (2004) Endogenous adenosine produced during hypoxia attenuates neutrophil accumulation: coordination by extracellular nucleotide metabolism. Blood 104, 3986-3992
22. Eckle, T., Grenz, A., Laucher, S., and Eltzschig, H. K. (2008) A2B adenosine receptor signaling attenuates acute lung injury by enhancing alveolar fluid clearance in mice. J. Clin. Invest. 118, 3301-3315.
23. Eckle, T., Fullbier, L., Wehrmann, M., Khoury, J., Mittelbronn, M., Ibla, J., Rosenberger, P., and Eltzschig, H. K. (2007) Identification of ectonucleotidases CD39 and CD73 in innate protection during acute lung injury. J. Immunol. 178, 8127-8137
24. Reutershan, J., Cagnina, R. E., Chang, D., Linden, J., and Ley, K. (2007) Therapeutic anti-inflammatory effects of myeloid cell adenosine receptor A2a stimulation in lipopolysaccharide-in-duced lung injury. J. Immunol. 179, 1254-1263
25. Eltzschig, H. K., Macmanus, C. F., and Colgan, S. P. (2008) Neutrophils as sources of extracellular nucleotides: functional consequences at the vascular interface. Trends Cardiovasc. Med. 18, 103-107
26. Eltzschig, H. K., Abdulla, P., Hoffman, E., Hamilton, K. E., Daniels, D., Schonfeld, C., Loffler, M., Reyes, G., Duszenko, M., Karhausen, J., Robinson, A., Westerman, K. A., Coe, I. R., and Colgan, S. P. (2005) HIF-1-dependent repression of equilibrative nucleoside transporter (ENT) in hypoxia. J. Exp. Med. 202, 1493-1505
27. Hart, M. L., Henn, M., Kohler, D., Kloor, D., Mittelbronn, M., Gorzolla, I. C., Stahl, G. L., and Eltzschig, H. K. (2008) Role of extracellular nucleotide phosphohydrolysis in intestinal ischemiareperfusion injury. FASEB J. 22, 2784-2797
28. Van Linden, A., and Eltzschig, H. K. (2007) Role of pulmonary adenosine during hypoxia: extracellular generation, signaling and metabolism by surface adenosine deaminase/CD26. Expert. Opin. Biol. Ther. 7, 1437-1447
29. Sitkovsky, M., and Lukashev, D. (2005) Regulation of immune cells by local-tissue oxygen tension: HIF1 alpha and adenosine receptors. Nat. Rev. Immunol. 5, 712-721
30. Sitkovsky, M. V., Lukashev, D., Apasov, S., Kojima, H., Koshiba, M., Caldwell, C., Ohta, A., and Thiel, M. (2004) Physiological control of immune response and inflammatory tissue damage by hypoxia-inducible factors and adenosine A2A receptors. Annu. Rev. Immunol. 22, 657-682
31. Linden, J. (2005) Adenosine in tissue protection and tissue regeneration. Mol. Pharmacol. 67, 1385-1387
32. Volmer, J. B., Thompson, L. F., and Blackburn, M. R. (2006) Ecto-5′ -nucleotidase (CD73)-mediated adenosine production is tissue protective in a model of bleomycin-induced lung injury. J. Immunol. 176, 4449-4458
33. Enjyoji, K., Sevigny, J., Lin, Y., Frenette, P. S., Christie, P. D., Esch, J. S., 2nd, Imai, M., Edelberg, J. M., Rayburn, H., Lech, M., Beeler, D. L., Csizmadia, E., Wagner, D. D., Robson, S. C., and Rosenberg, R. D. (1999) Targeted disruption of cd39/ATP diphosphohydrolase results in disordered hemostasis and thromboregulation. Nat. Med. 5, 1010-1017
34. Thompson, L. F., Eltzschig, H. K., Ibla, J. C., Van De Wiele, C. J., Resta, R., Morote-Garcia, J. C., and Colgan, S. P. (2004) Crucial role for ecto-5′ -nucleotidase (CD73) in vascular leakage during hypoxia. J. Exp. Med. 200, 1395-1405
35. Stark, M. A., Huo, Y., Burcin, T. L., Morris, M. A., Olson, T. S., and Ley, K. (2005) Phagocytosis of apoptotic neutrophils regulates granulopoiesis via IL-23 and IL-17. Immunity 22, 285-294
36. Pfaffl, M. W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45
37. Reutershan, J., Basit, A., Galkina, E. V., and Ley, K. (2005) Sequential recruitment of neutrophils into lung and bronchoalveolar lavage fluid in LPS-induced acute lung injury. Am. J. Physiol. Lung Cell. Mol. Physiol. 289, L807-L815
38. Reutershan, J., Chang, D., Hayes, J. K., and Ley, K. (2006) Protective effects of isoflurane pretreatment in endotoxininduced lung injury. Anesthesiology 104, 511-517
39. Green, T. P., Johnson, D. E., Marchessault, R. P., and Gatto, C. W. (1988) Transvascular flux and tissue accrual of Evans blue: effects of endotoxin and histamine. J. Lab. Clin. Med. 111, 173-183
40. Peng, X., Hassoun, P. M., Sammani, S., McVerry, B. J., Burne, M. J., Rabb, H., Pearse, D., Tuder, R. M., and Garcia, J. G. (2004) Protective effects of sphingosine 1-phosphate in murine endotoxin-induced inflammatory lung injury. Am. J. Respir. Crit. Care Med. 169, 1245-1251
41. Wangle, F., Patel, M., Razavi, H. M., Weicker, S., Joseph, M. G., McCormack, D. G., and Mehta, S. (2002) Role of inducible nitric oxide synthase in pulmonary microvascular protein leak in murine sepsis. Am. J. Respir. Crit. Care Med. 165, 1634-1639
42. Grenz, A., Zhang, H., Hermes, M., Eckle, T., Klingel, K., Huang, D. Y., Muller, C. E., Robson, S. C., Osswald, H., and Eltzschig, H. K. (2007) Contribution of E-NTPDase1 (CD39) to renal protection from ischemia-reperfusion injury. FASEB J. 21, 2863-287
43. Kohler, D., Eckle, T., Faigle, M., Grenz, A., Mittelbronn, M., Laucher, S., Hart, M. L., Robson, S. C., Muller, C. E., and Eltzschig, H. K. (2007) CD39/ectonucleoside triphosphate diphosphohydrolase 1 provides myocardial protection during cardiac ischemia/reperfusion injury. Circulation 116, 1784-1794
44. Muller, C. E., Iqbal, J., Baqi, Y., Zimmermann, H., Rollich, A., and Stephan, H. (2006) Polyoxometalates-a new class of potent ecto-nucleoside triphosphate diphosphohydrolase (NTPDase) inhibitors. Bioorg. Med. Chem. Lett. 16, 5943-5947
45. Olson, T. S., Singbartl, K., and Ley, K. (2002) L-selectin is required for fMLP- but not C5a-induced margination ofneutrophils in pulmonary circulation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 282, R1245-R1252
46. Grenz, A., Zhang, H., Eckle, T., Mittelbronn, M., Wehrmann, M., Kohle, C., Kloor, D., Thompson, L. F., Osswald, H., and Eltzschig, H. K. (2007) Protective role of ecto-5′-nucleotidase (CD73) in renal ischemia. J.Am. Soc. Nephrol. 18, 833-845
47. Mills, J. H., Thompson, L. F., Mueller, C., Waickman, A. T., Jalkanen, S., Niemela, J., Airas, L., and Bynoe, M. S. (2008) CD73 is required for efficient entry of lymphocytes into the central nervous system during experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. U. S. A. 105, 9325-9330
48. Eltzschig, H. K., Eckle, T., Mager, A., Kuper, N., Karcher, C., Weissmuller, T., Boengler, K., Schulz, R., Robson, S. C., and Colgan, S. P. (2006) ATP release from activated neutrophils occurs via connexin 43 and modulates adenosine-dependent endothelial cell function. Circ. Res. 99, 1100-1108
49. Eckle, T., Fullbier, L., Grenz, A., and Eltzschig, H. K. (2008) Usefulness of pressure controlled ventilation at high inspiratory pressures to induce acute lung injury in mice. Am. J. Physiol. Lung Cell. Mol. Physiol. 295, L718-L724
50. Synnestvedt, K., Furuta, G. T., Comerford, K. M., Louis, N., Karhausen, J., Eltzschig, H. K., Hansen, K. R., Thompson, L. F., and Colgan, S. P. (2002) Ecto-5′-nucleotidase (CD73) regulation by hypoxia-inducible factor-1 mediates permeability changes in intestinal epithelia. J. Clin. Invest. 110, 993-1002
51. Chunn, J. L., Molina, J. G., Mi, T., Xia, Y., Kellems, R. E., and Blackburn, M. R. (2005) Adenosine-dependent pulmonary fibrosis in adenosine deaminase-deficient mice. J. Immunol. 175, 1937-1946
52. Sun, C.-X., Young, H. W., Molina, J. G., Volmer, J. B., Schnermann, J., and Blackburn, M. R. (2005) A protective role for the A1 adenosine receptor in adenosine-dependent pulmonary injury. J. Clin. Invest. 115, 35-43
53. Sun, C. X., Zhong, H., Mohsenin, A., Morschl, E., Chunn, J. L., Molina, J. G., Belardinelli, L., Zeng, D., and Blackburn, M. R. (2006) Role of A(2B) adenosine receptor signaling in adenosinedependent pulmonary inflammation and injury. J. Clin. Invest. 116, 2173-2182
54. Blackburn, M. R. (2003) Too much of a good thing: adenosine overload in adenosine-deaminase-deficient mice. Trends Pharmacol. Sci. 24, 66-70
55. Sun, C. X., Zhong, H., Mohsenin, A., Morschl, E., Chunn, J. L., Molina, J. G., Belardinelli, L., Zeng, D., and Blackburn, M. R. (2006) Role of A2B adenosine receptor signaling in adenosine-dependent pulmonary inflammation and injury. J. Clin. Invest. 116, 2173-2182
56. Driver, A. G., Kukoly, C. A., Ali, S., and Mustafa, S. J. (1993) Adenosine in bronchoalveolar lavage fluid in asthma. Am. Rev. Respir. Dis. 148, 91-97
57. Huszar, E., Vass, G., Vizi, E., Csoma, Z., Barat, E., Molnar Vilagos, G., Herjavecz, I., and Horvath, I. (2002) Adenosine in exhaled breath condensate in healthy volunteers and in patients with asthma. Eur. Respir. J. 20, 1393-1398
58. Fozard, J. R., and Hannon, J. P. (1999) Adenosine receptor ligands: potential as therapeutic agents in asthma and COPD. Pulm. Pharmacol. Ther. 12, 111-114
59. Blackburn, M. R., Volmer, J. B., Thrasher, J. L., Zhong, H., Crosby, J. R., Lee, J. J., and Kellems, R. E. (2000) Metabolic consequences of adenosine deaminase deficiency in mice are associated with defects in alveogenesis, pulmonary inflammation, and airway obstruction. J. Exp. Med. 192, 159-170
60. Hart, M. L., Kohler, D., Eckle, T., Kloor, D., Stahl, G. L., and Eltzschig, H. K. (2008) Direct treatment of mouse or human blood with soluble 5′-nucleotidase inhibits platelet aggregation. Arterioscler. Thromb. Vasc. Biol. 28, 1477-1483