Cleavage of annexin A1 by ADAM10 during secondary necrosis generates a monocytic "find-me" signal

Journal of Immunology

Volumn 188, Issue 1, 2012, Pages 135-145

  Blume, Karin E ^a   Soeroes, Szabolcs ^a   Keppeler, Hildegard ^a   Stevanovic, Stefan ^a   Kretschmer, Dorothee ^a   Rautenberg, Maren ^a   Wesselborg, Sebastian ^a,b   Lauber, Kirsten ^a,c  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADAM10 ENDOPEPTIDASE; LIPOCORTIN 1;

AMINO TERMINAL SEQUENCE; APOPTOSIS; ARTICLE; CELL DEATH; CHEMOTAXIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; FLOW CYTOMETRY; FOLLOW UP; HUMAN; HUMAN CELL; MONOCYTE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN DOMAIN; SECONDARY NECROSIS; SUPERNATANT;

ADAM PROTEINS; AMYLOID PRECURSOR PROTEIN SECRETASES; ANNEXIN A1; CHEMOTACTIC FACTORS; CHEMOTAXIS; GENE KNOCKDOWN TECHNIQUES; HL-60 CELLS; HUMANS; JURKAT CELLS; MEMBRANE PROTEINS; MONOCYTES; NECROSIS; PROTEIN STRUCTURE, TERTIARY; PROTEOLYSIS; SIGNAL TRANSDUCTION; U937 CELLS;

EID: 84855414471     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1004073     Document Type: Article

References (46)

1. Gerke, V., C. E. Creutz, and S. E. Moss. 2005. Annexins: linking Ca2+ signalling to membrane dynamics. Nat. Rev. Mol. Cell Biol. 6: 449-461. (Pubitemid 40780557)
2. Perretti, M., and F. D'Acquisto. 2009. Annexin A1 and glucocorticoids as effectors of the resolution of inflammation. Nat. Rev. Immunol. 9: 62-70.
3. Liemann, S., and A. Lewit-Bentley. 1995. Annexins: a novel family of calcium-and membrane-binding proteins in search of a function. Structure 3: 233-237.
4. Liemann, S., and R. Huber. 1997. Three-dimensional structure of annexins. Cell. Mol. Life Sci. 53: 516-521. (Pubitemid 27374492)
5. Wang, W., and C. E. Creutz. 1992. Regulation of the chromaffin granule aggregating activity of annexin I by phosphorylation. Biochemistry 31: 9934-9939.
6. Rescher, U., V. Goebeler, A. Wilbers, and V. Gerke. 2006. Proteolytic cleavage of annexin 1 by human leukocyte elastase. Biochim. Biophys. Acta 1763: 1320-1324. (Pubitemid 44779860)
7. Vong, L., F. D'Acquisto, M. Pederzoli-Ribeil, L. Lavagno, R. J. Flower, V. Witko-Sarsat, and M. Perretti. 2007. Annexin 1 cleavage in activated neutrophils: a pivotal role for proteinase 3. J. Biol. Chem. 282: 29998-30004. (Pubitemid 350035249)
8. Gerke, V., and S. E. Moss. 2002. Annexins: from structure to function. Physiol. Rev. 82: 331-371. (Pubitemid 34654456)
9. Rescher, U., A. Danielczyk, A. Markoff, and V. Gerke. 2002. Functional activation of the formyl peptide receptor by a new endogenous ligand in human lung A549 cells. J. Immunol. 169: 1500-1504. (Pubitemid 34809196)
10. Solito, E., I. A. Romero, S. Marullo, F. Russo-Marie, and B. B. Weksler. 2000. Annexin 1 binds to U937 monocytic cells and inhibits their adhesion to microvascular endothelium: involvement of the alpha 4 beta 1 integrin. J. Immunol. 165: 1573-1581. (Pubitemid 30604594)
11. Byrne, A., and D. J. Reen. 2002. Lipopolysaccharide induces rapid production of IL-10 by monocytes in the presence of apoptotic neutrophils. J. Immunol. 168: 1968-1977. (Pubitemid 34135800)
12. Arur, S., U. E. Uche, K. Rezaul, M. Fong, V. Scranton, A. E. Cowan, W. Mohler, and D. K. Han. 2003. Annexin I is an endogenous ligand that mediates apoptotic cell engulfment. Dev. Cell 4: 587-598. (Pubitemid 36437564)
13. Fan, X., S. Krahling, D. Smith, P. Williamson, and R. A. Schlegel. 2004. Macrophage surface expression of annexins I and II in the phagocytosis of apoptotic lymphocytes. Mol. Biol. Cell 15: 2863-2872. (Pubitemid 38691874)
14. Blume, K. E., S. Soeroes, M. Waibel, H. Keppeler, S. Wesselborg, M. Herrmann, K. Schulze-Osthoff, and K. Lauber. 2009. Cell surface externalization of annexin A1 as a failsafe mechanism preventing inflammatory responses during secondary necrosis. J. Immunol. 183: 8138-8147.
15. Silva, M. T., A. do Vale, and N. M. dos Santos. 2008. Secondary necrosis in multicellular animals: an outcome of apoptosis with pathogenic implications. Apoptosis 13: 463-482.
16. Muñoz, L. E., K. Lauber, M. Schiller, A. A. Manfredi, and M. Herrmann. 2010. The role of defective clearance of apoptotic cells in systemic autoimmunity. Nat. Rev. Rheumatol. 6: 280-289.
17. Lauber, K., E. Bohn, S. M. Kröber, Y. J. Xiao, S. G. Blumenthal, R. K. Lindemann, P. Marini, C. Wiedig, A. Zobywalski, S. Baksh, et al. 2003. Apoptotic cells induce migration of phagocytes via caspase-3-mediated release of a lipid attraction signal. Cell 113: 717-730. (Pubitemid 36724936)
18. Lauber, K., H. A. Appel, S. F. Schlosser, M. Gregor, K. Schulze-Osthoff, and S. Wesselborg. 2001. The adapter protein apoptotic protease-activating factor-1 (Apaf-1) is proteolytically processed during apoptosis. J. Biol. Chem. 276: 29772-29781.
19. Berg, C. P., G. M. Stein, H. Keppeler, M. Gregor, S. Wesselborg, and K. Lauber. 2008. Apoptosis-associated antigens recognized by autoantibodies in patients with the autoimmune liver disease primary biliary cirrhosis. Apoptosis 13: 63-75.
20. Rabilloud, T., G. Carpentier, and P. Tarroux. 1988. Improvement and simplification of low-background silver staining of proteins by using sodium dithionite. Electrophoresis 9: 288-291.
21. Peter, C., M. Waibel, C. G. Radu, L. V. Yang, O. N. Witte, K. Schulze-Osthoff, S. Wesselborg, and K. Lauber. 2008. Migration to apoptotic "find-me" signals is mediated via the phagocyte receptor G2A. J. Biol. Chem. 283: 5296-5305.
22. Hakulinen, J., and J. Keski-Oja. 2006. ADAM10-mediated release of complement membrane cofactor protein during apoptosis of epithelial cells. J. Biol. Chem. 281: 21369-21376. (Pubitemid 44115476)
23. Chalaris, A., B. Rabe, K. Paliga, H. Lange, T. Laskay, C. A. Fielding, S. A. Jones, S. Rose-John, and J. Scheller. 2007. Apoptosis is a natural stimulus of IL6R shedding and contributes to the proinflammatory trans-signaling function of neutrophils. Blood 110: 1748-1755. (Pubitemid 47443884)
24. Movitz, C., C. Sjölin, and C. Dahlgren. 1999. Cleavage of annexin I in human neutrophils is mediated by a membrane-localized metalloprotease. Biochim. Biophys. Acta 1416: 101-108. (Pubitemid 29065428)
25. Hundhausen, C., D. Misztela, T. A. Berkhout, N. Broadway, P. Saftig, K. Reiss, D. Hartmann, F. Fahrenholz, R. Postina, V. Matthews, et al. 2003. The disintegrin-like metalloproteinase ADAM10 is involved in constitutive cleavage of CX3CL1 (fractalkine) and regulates CX3CL1-mediated cell-cell adhesion. Blood 102: 1186-1195. (Pubitemid 36988021)
26. Ernst, S., C. Lange, A. Wilbers, V. Goebeler, V. Gerke, and U. Rescher. 2004. An annexin 1 N-terminal peptide activates leukocytes by triggering different members of the formyl peptide receptor family. J. Immunol. 172: 7669-7676. (Pubitemid 38747633)
27. Debret, R., H. El Btaouri, L. Duca, I. Rahman, S. Radke, B. Haye, J. M. Sallenave, and F. Antonicelli. 2003. Annexin A1 processing is associated with caspase-dependent apoptosis in BZR cells. FEBS Lett. 546: 195-202. (Pubitemid 36782410)
28. Waldhauer, I., D. Goehlsdorf, F. Gieseke, T. Weinschenk, M. Wittenbrink, A. Ludwig, S. Stevanovic, H. G. Rammensee, and A. Steinle. 2008. Tumor-associated MICA is shed by ADAM proteases. Cancer Res. 68: 6368-6376.
29. Kirkin, V., N. Cahuzac, F. Guardiola-Serrano, S. Huault, K. Lückerath, E. Friedmann, N. Novac, W. S. Wels, B. Martoglio, A. O. Hueber, and M. Zörnig. 2007. The Fas ligand intracellular domain is released by ADAM10 and SPPL2a cleavage in T-cells. Cell Death Differ. 14: 1678-1687. (Pubitemid 47278853)
30. Schulz, B., J. Pruessmeyer, T. Maretzky, A. Ludwig, C. P. Blobel, P. Saftig, and K. Reiss. 2008. ADAM10 regulates endothelial permeability and T-Cell transmigration by proteolysis of vascular endothelial cadherin. Circ. Res. 102: 1192-1201.
31. Anders, A., S. Gilbert, W. Garten, R. Postina, and F. Fahrenholz. 2001. Regulation of the alpha-secretase ADAM10 by its prodomain and proprotein convertases. FASEB J. 15: 1837-1839.
32. Lopez-Perez, E., Y. Zhang, S. J. Frank, J. Creemers, N. Seidah, and F. Checler. 2001. Constitutive alpha-secretase cleavage of the beta-amyloid precursor protein in the furin-deficient LoVo cell line: involvement of the pro-hormone convertase 7 and the disintegrin metalloprotease ADAM10. J. Neurochem. 76: 1532-1539. (Pubitemid 32198257)
33. Le Gall, S. M., P. Bobé, K. Reiss, K. Horiuchi, X. D. Niu, D. Lundell, D. R. Gibb, D. Conrad, P. Saftig, and C. P. Blobel. 2009. ADAMs 10 and 17 represent differentially regulated components of a general shedding machinery for membrane proteins such as transforming growth factor alpha, L-selectin, and tumor necrosis factor alpha. Mol. Biol. Cell 20: 1785-1794.
34. Orrenius, S., B. Zhivotovsky, and P. Nicotera. 2003. Regulation of cell death: the calcium-apoptosis link. Nat. Rev. Mol. Cell Biol. 4: 552-565. (Pubitemid 36773407)
35. Rosengarth, A., and H. Luecke. 2003. A calcium-driven conformational switch of the N-terminal and core domains of annexin A1. J. Mol. Biol. 326: 1317-1325. (Pubitemid 36269076)
36. Smith, S. F., T. D. Tetley, A. Guz, and R. J. Flower. 1990. Detection of lipocortin 1 in human lung lavage fluid: lipocortin degradation as a possible proteolytic mechanism in the control of inflammatory mediators and inflammation. Environ. Health Perspect. 85: 135-144. (Pubitemid 20315292)
37. Perretti, M., A. Ahluwalia, J. G. Harris, N. J. Goulding, and R. J. Flower. 1993. Lipocortin-1 fragments inhibit neutrophil accumulation and neutrophil-dependent edema in the mouse. A qualitative comparison with an anti-CD11b monoclonal antibody. J. Immunol. 151: 4306-4314. (Pubitemid 23298764)
38. Gastardelo, T. S., A. S. Damazo, J. Dalli, R. J. Flower, M. Perretti, and S. M. Oliani. 2009. Functional and ultrastructural analysis of annexin A1 and its receptor in extravasating neutrophils during acute inflammation. Am. J. Pathol. 174: 177-183.
39. Facio, F. N., Jr., A. A. Sena, L. P. Araujo, G. E.Mendes, I. Castro, M. A. Luz, L. Yu, S. M. Oliani, and E. A. Burdmann. 2011. Annexin 1 mimetic peptide protects against renal ischemia/reperfusion injury in rats. J. Mol. Med. (Berl). 89: 51-63.
40. Scannell, M., M. B. Flanagan, A. deStefani, K. J. Wynne, G. Cagney, C. Godson, and P. Maderna. 2007. Annexin-1 and peptide derivatives are released by apoptotic cells and stimulate phagocytosis of apoptotic neutrophils by macrophages. J. Immunol. 178: 4595-4605. (Pubitemid 46492412)
41. Walther, A., K. Riehemann, and V. Gerke. 2000. A novel ligand of the formyl peptide receptor: annexin I regulates neutrophil extravasation by interacting with the FPR. Mol. Cell 5: 831-840.
42. Gavins, F. N., P. Sawmynaden, B. E. Chatterjee, and M. Perretti. 2005. A twist in anti-inflammation: annexin 1 acts via the lipoxin A4 receptor. Prostaglandins Leukot. Essent. Fatty Acids 73: 211-219. (Pubitemid 41253478)
43. Hayhoe, R. P., A. M. Kamal, E. Solito, R. J. Flower, D. Cooper, and M. Perretti. 2006. Annexin 1 and its bioactive peptide inhibit neutrophil- endothelium interactions under flow: indication of distinct receptor involvement. Blood 107: 2123-2130. (Pubitemid 43289398)
44. Movitz, C., L. Brive, K. Hellstrand, M. J. Rabiet, and C. Dahlgren. 2010. The annexin I sequence gln(9)-ala(10)-trp(11)-phe(12) is a core structure for interaction with the formyl peptide receptor 1. J. Biol. Chem. 285: 14338-14345.
45. D'Acquisto, F., M. Perretti, and R. J. Flower. 2008. Annexin-A1: a pivotal regulator of the innate and adaptive immune systems. Br. J. Pharmacol. 155: 152-169.
46. Yang, Y., M. Leech, P. Hutchinson, S. R. Holdsworth, and E. F. Morand. 1997. Antiinflammatory effect of lipocortin 1 in experimental arthritis. Inflammation 21: 583-596. (Pubitemid 28026329)