Annexin A1 regulates neutrophil clearance by macrophages in the mouse bone marrow

FASEB Journal

Volumn 26, Issue 1, 2012, Pages 387-396

  Dalli, Jesmond ^a   Jones, Carla P ^b   Cavalcanti, Danielle M ^a,c   Farsky, Sandra H ^c   Perretti, Mauro ^a   Rankin, Sara M ^b  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

CXCR4; Neutrophil homeostasis

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; LIPOCORTIN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BAGG ALBINO MOUSE; BONE MARROW; CONTROLLED STUDY; MACROPHAGE; MALE; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; WILD TYPE;

ANIMALS; ANNEXIN A1; BONE MARROW; CELL AGING; CHEMOTAXIS; GENE EXPRESSION; HOMEOSTASIS; MACROPHAGES, PERITONEAL; MALE; MICE; MICE, INBRED BALB C; MICE, MUTANT STRAINS; NEUTROPHILS; PHAGOCYTOSIS; RECEPTORS, CXCR4;

MUS;

EID: 84855415055     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-182089     Document Type: Article

References (49)

1. Summers, C., Rankin, S. M., Condliffe, A. M., Singh, N., Peters, A. M., and Chilvers, E. R. (2010) Neutrophil kinetics in health and disease. Trends Immunol. 31, 318-324
2. Mauer, A. M., Athens, J. W., Ashenbrucker, H., Cartwright, G. E., and Wintrobe, M. M. (1960) Leukokinetic studies. Ii. A method for labeling granulocytes in vitro with radioactive diisopropylfluorophosphate (Dfp). J. Clin. Invest. 39, 1481-1486
3. Bicknell, S., van Eeden, S., Hayashi, S., Hards, J., English, D., and Hogg, J. C. (1994) A non-radioisotopic method for tracing neutrophils in vivo using 5′-bromo-2′-deoxyuridine. Am. J. Respir. Cell Mol. Biol. 10, 16-23
4. Furze, R. C., and Rankin, S. M. (2008) The role of the bone marrow in neutrophil clearance under homeostatic conditions in the mouse. FASEB J. 22, 3111-3119
5. Lovas, K., Knudsen, E., Iversen, P. O., and Benestad, H. B. (1996) Sequestration patterns of transfused rat neutrophilic granulocytes under normal and inflammatory conditions. Eur. J. Haematol. 56, 221-229 (Pubitemid 26156659)
6. Rankin, S. M. (2010) The bone marrow: a site of neutrophil clearance. J. Leukoc. Biol. 88, 241-251
7. Saverymuttu, S. H., Peters, A. M., Keshavarzian, A., Reavy, H. J., and Lavender, J. P. (1985) The kinetics of 111indium distribution following injection of 111indium labelled autologous granulocytes in man. Br. J. Haematol. 61, 675-685 (Pubitemid 16231520)
8. Suratt, B. T., Young, S. K., Lieber, J., Nick, J. A., Henson, P. M., and Worthen, G. S. (2001) Neutrophil maturation and activation determine anatomic site of clearance from circulation. Am. J. Physiol. Lung Cell. Mol. Physiol. 281, L913-L921
9. Thakur, M. L., Lavender, J. P., Arnot, R. N., Silvester, D. J., and Segal, A. W. (1977) Indium-111-labeled autologous leukocytes in man. J. Nucl. Med. 18, 1014-1021
10. Burdon, P. C., Martin, C., and Rankin, S. M. (2008) Migration across the sinusoidal endothelium regulates neutrophil mobilization in response to ELR + CXC chemokines. Br. J. Haematol. 142, 100-108 (Pubitemid 351783141)
11. Nagase, H., Miyamasu, M., Yamaguchi, M., Imanishi, M., Tsuno, N. H., Matsushima, K., Yamamoto, K., Morita, Y., and Hirai, K. (2002) Cytokine-mediated regulation of CXCR4 expression in human neutrophils. J. Leukoc. Biol. 71, 711-717
12. Martin, C., Burdon, P. C., Bridger, G., Gutierrez-Ramos, J. C., Williams, T. J., and Rankin, S. M. (2003) Chemokines acting via CXCR2 and CXCR4 control the release of neutrophils from the bone marrow and their return following senescence. Immunity 19, 583-593 (Pubitemid 37311439)
13. Sadahira, Y., and Mori, M. (1999) Role of the macrophage in erythropoiesis. Pathol. Int. 49, 841-848
14. Osmond, D. G., Rico-Vargas, S., Valenzona, H., Fauteux, L., Liu, L., Janani, R., Lu, L., and Jacobsen, K. (1994) Apoptosis and macrophage-mediated cell deletion in the regulation of B lymphopoiesis in mouse bone marrow. Immunol. Rev. 142, 209-230
15. Fox, S., Leitch, A. E., Duffin, R., Haslett, C., and Rossi, A. G. (2010) Neutrophil apoptosis: relevance to the innate immune response and inflammatory disease. J. Innate Immun. 2, 216-227
16. McColl, A., Bournazos, S., Franz, S., Perretti, M., Morgan, B. P., Haslett, C., and Dransfield, I. (2009) Glucocorticoids induce protein S-dependent phagocytosis of apoptotic neutrophils by human macrophages. J. Immunol. 183, 2167-2175
17. Takahashi, K., Naito, M., and Takeya, M. (1996) Development and heterogeneity of macrophages and their related cells through their differentiation pathways. Pathol. Int. 46, 473-485 (Pubitemid 26299464)
18. Naito, M., Umeda, S., Yamamoto, T., Moriyama, H., Umezu, H., Hasegawa, G., Usuda, H., Shultz, L. D., and Takahashi, K. (1996) Development, differentiation, and phenotypic heterogeneity of murine tissue macrophages. J. Leukoc. Biol. 59, 133-138 (Pubitemid 26098611)
19. Gorgani, N. N., Ma, Y., and Clark, H. F. (2008) Gene signatures reflect the marked heterogeneity of tissue-resident macrophages. Immunol. Cell Biol. 86, 246-254 (Pubitemid 351430801)
20. Jitkaew, S., Witasp, E., Zhang, S., Kagan, V. E., and Fadeel, B. (2009) Induction of caspase- and reactive oxygen species-independent phosphatidylserine externalization in primary human neutrophils: role in macrophage recognition and engulfment. J. Leukoc. Biol. 85, 427-437
21. Kobayashi, N., Karisola, P., Pena-Cruz, V., Dorfman, D. M., Jinushi, M., Umetsu, S. E., Butte, M. J., Nagumo, H., Chernova, I., Zhu, B., Sharpe, A. H., Ito, S., Dranoff, G., Kaplan, G. G., Casasnovas, J. M., Umetsu, D. T., Dekruyff, R. H., and Freeman, G. J. (2007) TIM-1 and TIM-4 glycoproteins bind phosphatidylserine and mediate uptake of apoptotic cells. Immunity 27, 927-940 (Pubitemid 50014866)
22. Greenberg, M. E., Sun, M., Zhang, R., Febbraio, M., Silverstein, R., and Hazen, S. L. (2006) Oxidized phosphatidylserine-CD36 interactions play an essential role in macrophage-dependent phagocytosis of apoptotic cells. J. Exp. Med. 203, 2613-2625 (Pubitemid 44833338)
23. Bottcher, A., Gaipl, U. S., Furnrohr, B. G., Herrmann, M., Girkontaite, I., Kalden, J. R., and Voll, R. E. (2006) Involvement of phosphatidylserine, alphavbeta3, CD14, CD36, and complement C1q in the phagocytosis of primary necrotic lymphocytes by macrophages. Arthritis Rheum. 54, 927-938
24. Savill, J., Hogg, N., Ren, Y., and Haslett, C. (1992) Thrombospondin cooperates with CD36 and the vitronectin receptor in macrophage recognition of neutrophils undergoing apoptosis. J. Clin. Invest. 90, 1513-1522
25. Fadok, V. A., Savill, J. S., Haslett, C., Bratton, D. L., Doherty, D. E., Campbell, P. A., and Henson, P. M. (1992) Different populations of macrophages use either the vitronectin receptor or the phosphatidylserine receptor to recognize and remove apoptotic cells. J. Immunol. 149, 4029-4035 (Pubitemid 23068888)
26. Fan, X., Krahling, S., Smith, D., Williamson, P., and Schlegel, R. A. (2004) Macrophage surface expression of annexins I and II in the phagocytosis of apoptotic lymphocytes. Mol. Biol. Cell 15, 2863-2872 (Pubitemid 38691874)
27. Yona, S., Buckingham, J. C., Perretti, M., and Flower, R. J. (2004) Stimulus-specific defect in the phagocytic pathways of annexin 1 null macrophages. Br. J. Pharmacol. 142, 890-898 (Pubitemid 38998102)
28. Perretti, M., and D'Acquisto, F. (2009) Annexin A1 and glucocorticoids as effectors of the resolution of inflammation. Nat. Rev. Immunol. 9, 62-70
29. Lim, L. H., Solito, E., Russo-Marie, F., Flower, R. J., and Perretti, M. (1998) Promoting detachment of neutrophils adherent to murine postcapillary venules to control inflammation: effect of lipocortin 1. Proc. Natl. Acad. Sci. U. S. A. 95, 14535-14539 (Pubitemid 28549402)
30. Chatterjee, B. E., Yona, S., Rosignoli, G., Young, R. E., Nourshargh, S., Flower, R. J., and Perretti, M. (2005) Annexin 1-deficient neutrophils exhibit enhanced transmigration in vivo and increased responsiveness in vitro. J. Leukoc. Biol. 78, 639-646 (Pubitemid 41292086)
31. Damazo, A. S., Yona, S., D'Acquisto, F., Flower, R. J., Oliani, S. M., and Perretti, M. (2005) Critical protective role for annexin 1 gene expression in the endotoxemic murine microcirculation. Am. J. Pathol. 166, 1607-1617 (Pubitemid 40734384)
32. El Kebir, D., Jozsef, L., and Filep, J. G. (2008) Opposing regulation of neutrophil apoptosis through the formyl peptide receptor-like 1/lipoxin A4 receptor: implications for resolution of inflammation. J. Leukoc. Biol. 84, 600-606
33. Maderna, P., Yona, S., Perretti, M., and Godson, C. (2005) Modulation of phagocytosis of apoptotic neutrophils by supernatant from dexamethasone-treated macrophages and annexin-derived peptide Ac(2-26). J. Immunol. 174, 3727-3733 (Pubitemid 40354084)
34. Scannell, M., Flanagan, M. B., deStefani, A., Wynne, K. J., Cagney, G., Godson, C., and Maderna, P. (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)
35. Solito, E., Kamal, A., Russo-Marie, F., Buckingham, J. C., Marullo, S., and Perretti, M. (2003) A novel calcium-dependent proapoptotic effect of annexin 1 on human neutrophils. FASEB J. 17, 1544-1546
36. Yona, S., Heinsbroek, S. E., Peiser, L., Gordon, S., Perretti, M., and Flower, R. J. (2006) Impaired phagocytic mechanism in annexin 1 null macrophages. Br. J. Pharmacol. 148, 469-477 (Pubitemid 43882083)
37. Pederzoli-Ribeil, M., Maione, F., Cooper, D., Al-Kashi, A., Dalli, J., Perretti, M., and D'Acquisto, F. (2010) Design and characterization of a cleavage-resistant Annexin A1 mutant to control inflammation in the microvasculature. Blood 116, 4288-4296
38. Hannon, R., Croxtall, J. D., Getting, S. J., Roviezzo, F., Yona, S., Paul-Clark, M. J., Gavins, F. N., Perretti, M., Morris, J. F., Buckingham, J. C., and Flower, R. J. (2003) Aberrant inflammation and resistance to glucocorticoids in annexin 1-/- mouse. FASEB J. 17, 253-255
39. Dalli, J., Norling, L. V., Renshaw, D., Cooper, D., Leung, K. Y., and Perretti, M. (2008) Annexin 1 mediates the rapid antiinflammatory effects of neutrophil-derived microparticles. Blood 112, 2512-2519
40. Godson, C., Mitchell, S., Harvey, K., Petasis, N. A., Hogg, N., and Brady, H. R. (2000) Cutting edge: lipoxins rapidly stimulate nonphlogistic phagocytosis of apoptotic neutrophils by monocyte-derived macrophages. J. Immunol. 164, 1663-1667 (Pubitemid 30108713)
41. Jung, T., Hohn, A., and Grune, T. (2010) Lipofuscin: detection and quantification by microscopic techniques. Methods Mol. Biol. 594, 173-193
42. Pitchford, S. C., Furze, R. C., Jones, C. P., Wengner, A. M., and Rankin, S. M. (2009) Differential mobilization of subsets of progenitor cells from the bone marrow. Cell Stem Cell 4, 62-72
43. Wolach, B., van der Laan, L. J., Maianski, N. A., Tool, A. T., van Bruggen, R., Roos, D., and Kuijpers, T. W. (2007) Growth factors G-CSF and GM-CSF differentially preserve chemotaxis of neutrophils aging in vitro. Exp. Hematol. 35, 541-550 (Pubitemid 46427962)
44. Whyte, M. K., Meagher, L. C., MacDermot, J., and Haslett, C. (1993) Impairment of function in aging neutrophils is associated with apoptosis. J. Immunol. 150, 5124-5134 (Pubitemid 23150380)
45. Schwab, J. M., Chiang, N., Arita, M., and Serhan, C. N. (2007) Resolvin E1 and protectin D1 activate inflammation-resolution programmes. Nature 447, 869-874 (Pubitemid 46920139)
46. Furze, R. C., and Rankin, S. M. (2008) Neutrophil mobilization and clearance in the bone marrow. Immunology 125, 281-288
47. Gastardelo, T. S., Damazo, A. S., Dalli, J., Flower, R. J., Perretti, M., and Oliani, S. M. (2009) Functional and ultrastructural analysis of annexin A1 and its receptor in extravasating neutrophils during acute inflammation. Am. J. Pathol. 174, 177-183
48. Damazo, A. S., Yona, S., Flower, R. J., Perretti, M., and Oliani, S. M. (2006) Spatial and temporal profiles for anti-inflammatory gene expression in leukocytes during a resolving model of peritonitis. J. Immunol. 176, 4410-4418 (Pubitemid 44264421)
49. Kamal, A. M., Flower, R. J., and Perretti, M. (2005) An overview of the effects of annexin 1 on cells involved in the inflammatory process. Mem. Inst. Oswaldo Cruz 100(Suppl. 1), 39-47