The atypical chemokine receptor D6 controls macrophage efferocytosis and cytokine secretion during the resolution of inflammation

FASEB Journal

Volumn 26, Issue 9, 2012, Pages 3891-3900

  Pashover Schallinger, Ester ^a   Aswad, Miran ^a   Schif Zuck, Sagie ^a   Shapiro, Haim ^b   Singer, Pierre ^b   Ariel, Amiram ^a  

^a UNIVERSITY OF HAIFA   (Israel)

^b RABIN MEDICAL CENTER   (Israel)

Author keywords

Acute immune responses; Apoptotic cell clearance; Chemokine receptors; Leukocytes

Indexed keywords

CHEMOKINE RECEPTOR; CHEMOKINE RECEPTOR D6; INTERLEUKIN 1BETA; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; RANTES; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; EFFEROCYTOSIS; EX VIVO STUDY; IN VIVO STUDY; INCUBATION TIME; INFLAMMATION; MACROPHAGE; MEMBRANE BIOLOGY; MOUSE; NEUTROPHIL; NONHUMAN; PERITONEUM; PERITONITIS; POLYMORPHONUCLEAR CELL; PRIORITY JOURNAL; SENESCENCE; WILD TYPE;

ANIMALS; APOPTOSIS; CYTOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; MACROPHAGES; MICE; MICE, KNOCKOUT; NEUTROPHILS; PERITONITIS; RECEPTORS, CCR10;

ANIMALIA; MURINAE; MUS; RODENTIA;

EID: 84865747622     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-194894     Document Type: Article

References (45)

1. Levy, B. D., Clish, C. B., Schmidt, B., Gronert, K., and Serhan, C. N. (2001) Lipid mediator class switching during acute inflammation: signals in resolution. Nat. Immunol. 2, 612-619
2. Serhan, C. N., Brain, S. D., Buckley, C. D., Gilroy, D. W., Haslett, C., O'Neill, L. A., Perretti, M., Rossi, A. G., and Wallace, J. L. (2007) Resolution of inflammation: state of the art, definitions and terms. FASEB J. 21, 325-332
3. Majno, G, and Joris, I. (2004) Cells, Tissues, and Disease: Principles of General Pathology, 2nd Ed., Oxford University Press, New York
4. Rossi, A. G., and Haslett, C. (1998) Inflammation, cell injury, and apoptosis. In Pro-Inflammatory and Anti-Inflammatory Peptides, Vol. 117 (Said, S. I., ed.) pp 9-24, Marcel Dekker, New York
5. Fadok, V. A., Bratton, D. L., Konowal, A., Freed, P. W., Westcott, J. Y., and Henson, P. M. (1998) Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF. J. Clin. Invest. 101, 890-898
6. Savill, J., Dransfield, I., Gregory, C., and Haslett, C. (2002) A blast from the past: clearance of apoptotic cells regulates immune responses. Nat. Rev. Immunol. 2, 965-975
7. Hanayama, R., Tanaka, M., Miwa, K., Shinohara, A., Iwamatsu, A., and Nagata, S. (2002) Identification of a factor that links apoptotic cells to phagocytes. Nature 417, 182-187
8. Voll, R. E., Herrmann, M., Roth, E. A., Stach, C., Kalden, J. R., and Girkontaite, I. (1997) Immunosuppressive effects of apoptotic cells. Nature 390, 350-351
9. Ravichandran, K. S., and Lorenz, U. (2007) Engulfment of apoptotic cells: signals for a good meal. Nat. Rev. Immunol. 7, 964-974
10. Patel, V. A., Longacre, A., Hsiao, K., Fan, H., Meng, F., Mitchell, J. E., Rauch, J., Ucker, D. S., and Levine, J. S. (2006) Apoptotic cells, at all stages of the death process, trigger characteristic signaling events that are divergent from and dominant over those triggered by necrotic cells: Implications for the delayed clearance model of autoimmunity. J. Biol. Chem. 281, 4663-4670
11. Kim, S., Elkon, K. B., and Ma, X. (2004) Transcriptional suppression of interleukin-12 gene expression following phagocytosis of apoptotic cells. Immunity 21, 643-653
12. Byrne, A., and Reen, D. J. (2002) Lipopolysaccharide induces rapid production of IL-10 by monocytes in the presence of apoptotic neutrophils. J. Immunol. 168, 1968-1977
13. Huynh, M. L., Fadok, V. A., and Henson, P. M. (2002) Phosphatidylserine- dependent ingestion of apoptotic cells promotes TGF-beta1 secretion and the resolution of inflammation. J. Clin. Invest. 109, 41-50
14. Mitchell, S., Thomas, G., Harvey, K., Cottell, D., Reville, K., Berlasconi, G., Petasis, N. A., Erwig, L., Rees, A. J., Savill, J., Brady, H. R., and Godson, C. (2002) Lipoxins, aspirin-triggered epi-lipoxins, lipoxin stable analogues, and the resolution of inflammation: stimulation of macrophage phagocytosis of apoptotic neutrophils in vivo. J. Am. Soc. Nephrol. 13, 2497-2507
15. Freire-de-Lima, C. G., Xiao, Y. Q., Gardai, S. J., Bratton, D. L., Schiemann, W. P., and Henson, P. M. (2006) Apoptotic cells, through transforming growth factor-beta, coordinately induce anti-inflammatory and suppress pro-inflammatory eicosanoid and NO synthesis in murine macrophages. J. Biol. Chem. 281, 38376-38384
16. 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
17. Golpon, H. A., Fadok, V. A., Taraseviciene-Stewart, L., Scerbavicius, R., Sauer, C., Welte, T., Henson, P. M., and Voelkel, N. F. (2004) Life after corpse engulfment: phagocytosis of apoptotic cells leads to VEGF secretion and cell growth. FASEB J. 18, 1716-1718
18. Martinez, F. O., Helming, L., and Gordon, S. (2009) Alternative activation of macrophages: an immunologic functional perspective. Annu. Rev. Immunol. 27, 451-483
19. Weigert, A., Jennewein, C., and Brune, B. (2009) The liaison between apoptotic cells and macrophages - the end programs the beginning. Biol. Chem. 390, 379-390
20. Bystrom, J., Evans, I., Newson, J., Stables, M., Toor, I., van Rooijen, N., Crawford, M., Colville-Nash, P., Farrow, S., and Gilroy, D. W. (2008) Resolution-phase macrophages possess a unique inflammatory phenotype that is controlled by cAMP. Blood 112, 4117-4127
21. Schif-Zuck, S., Gross, N., Assi, S., Rostoker, R., Serhan, C. N., and Ariel, A. (2011) Saturated-efferocytosis generates pro-resolving CD11b(low) macrophages: Modulation by resolvins and glucocorticoids. Eur. J. Immunol. 41, 366-379
22. Rot, A., and von Andrian, U. H. (2004) Chemokines in innate and adaptive host defense: basic chemokinese grammar for immune cells. Annu. Rev. Immunol. 22, 891-928
23. D'Amico, G., Frascaroli, G., Bianchi, G., Transidico, P., Doni, A., Vecchi, A., Sozzani, S., Allavena, P., and Mantovani, A. (2000) Uncoupling of inflammatory chemokine receptors by IL-10: generation of functional decoys. Nat. Immunol. 1, 387-391
24. Jamieson, T., Cook, D. N., Nibbs, R. J., Rot, A., Nixon, C., McLean, P., Alcami, A., Lira, S. A., Wiekowski, M., and Graham, G. J. (2005) The chemokine receptor D6 limits the inflammatory response in vivo. Nat. Immunol. 6, 403-411
25. Martinez de la Torre, Y., Buracchi, C., Borroni, E. M., Dupor, J., Bonecchi, R., Nebuloni, M., Pasqualini, F., Doni, A., Lauri, E., Agostinis, C., Bulla, R., Cook, D. N., Haribabu, B., Meroni, P., Rukavina, D., Vago, L., Tedesco, F., Vecchi, A., Lira, S. A., Locati, M., and Mantovani, A. (2007) Protection against inflammation- and autoantibody-caused fetal loss by the chemokine decoy receptor D6. Proc. Natl. Acad. Sci. U. S. A. 104, 2319-2324
26. Ariel, A., Fredman, G., Sun, Y. P., Kantarci, A., Van Dyke, T. E., Luster, A. D., and Serhan, C. N. (2006) Apoptotic neutrophils and T cells sequester chemokines during immune response resolution through modulation of CCR5 expression. Nat. Immunol. 7, 1209-1216
27. Amano, H., Morimoto, K., Senba, M., Wang, H., Ishida, Y., Kumatori, A., Yoshimine, H., Oishi, K., Mukaida, N., and Nagatake, T. (2004) Essential contribution of monocyte chemoattractant protein-1/C-C chemokine ligand-2 to resolution and repair processes in acute bacterial pneumonia. J. Immunol. 172, 398-409
28. Mantovani, A., Bonecchi, R., and Locati, M. (2006) Tuning inflammation and immunity by chemokine sequestration: decoys and more. Nat. Rev. Immunol. 6, 907-918
29. Nibbs, R. J., McLean, P., McCulloch, C., Riboldi-Tunnicliffe, A., Blair, E., Zhu, Y., Isaacs, N., and Graham, G. J. (2009) Structure-function dissection of D6, an atypical scavenger receptor. Methods Enzymol. 460, 245-261
30. Bonecchi, R., Borroni, E. M., Anselmo, A., Doni, A., Savino, B., Mirolo, M., Fabbri, M., Jala, V. R., Haribabu, B., Mantovani, A., and Locati, M. (2008) Regulation of D6 chemokine scavenging activity by ligand- and Rab11-dependent surface up-regulation. Blood 112, 493-503
31. McKimmie, C. S., Fraser, A. R., Hansell, C., Gutierrez, L., Philipsen, S., Connell, L., Rot, A., Kurowska-Stolarska, M., Carreno, P., Pruenster, M., Chu, C. C., Lombardi, G., Halsey, C., McInnes, I. B., Liew, F. Y., Nibbs, R. J., and Graham, G. J. (2008) Hemopoietic cell expression of the chemokine decoy receptor D6 is dynamic and regulated by GATA1. J. Immunol. 181, 8171-8181
32. Bellingan, G. J., Caldwell, H., Howie, S. E., Dransfield, I., and Haslett, C. (1996) In vivo fate of the inflammatory macrophage during the resolution of inflammation: inflammatory macrophages do not die locally, but emigrate to the draining lymph nodes. J. Immunol. 157, 2577-2585
33. 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
34. Martinez de la Torre, Y., Locati, M., Buracchi, C., Dupor, J., Cook, D. N., Bonecchi, R., Nebuloni, M., Rukavina, D., Vago, L., Vecchi, A., Lira, S. A., and Mantovani, A. (2005) Increased inflammation in mice deficient for the chemokine decoy receptor D6. Eur. J. Immunol. 35, 1342-1346
35. Hartl, D., Krauss-Etschmann, S., Koller, B., Hordijk, P. L., Kuijpers, T. W., Hoffmann, F., Hector, A., Eber, E., Marcos, V., Bittmann, I., Eickelberg, O., Griese, M., and Roos, D. (2008) Infiltrated neutrophils acquire novel chemokine receptor expression and chemokine responsiveness in chronic inflammatory lung diseases. J. Immunol. 181, 8053-8067
36. Kowolenko, M., Keese, C. R., Lawrence, D. A., and Giaever, I. (1990) Measurement of macrophage adherence and spreading with weak electric fields. J. Immunol. Methods 127, 71-77
37. Bordon, Y., Hansell, C. A., Sester, D. P., Clarke, M., Mowat, A. M., and Nibbs, R. J. (2009) The atypical chemokine receptor D6 contributes to the development of experimental colitis. J. Immunol. 182, 5032-5040
38. Lee, K. M., McKimmie, C. S., Gilchrist, D. S., Pallas, K. J., Nibbs, R. J., Garside, P., McDonald, V., Jenkins, C., Ransohoff, R., Liu, L., Milling, S., Cerovic, V., and Graham, G. J. (2011) D6 facilitates cellular migration and fluid flow to lymph nodes by suppressing lymphatic congestion. Blood 118, 6220-6229
39. Liu, L., Graham, G. J., Damodaran, A., Hu, T., Lira, S. A., Sasse, M., Canasto-Chibuque, C., Cook, D. N., and Ransohoff, R. M. (2006) Cutting edge: the silent chemokine receptor D6 is required for generating T cell responses that mediate experimental autoimmune encephalomyelitis. J. Immunol. 177, 17-21
40. Gordon, S., and Martinez, F. O. (2010) Alternative activation of macrophages: mechanism and functions. Immunity 32, 593-604
41. Di Liberto, D., Locati, M., Caccamo, N., Vecchi, A., Meraviglia, S., Salerno, A., Sireci, G., Nebuloni, M., Caceres, N., Cardona, P. J., Dieli, F., and Mantovani, A. (2008) Role of the chemokine decoy receptor D6 in balancing inflammation, immune activation, and antimicrobial resistance in Mycobacterium tuberculosis infection. J. Exp. Med. 205, 2075-2084
42. Whitehead, G. S., Wang, T., DeGraff, L. M., Card, J. W., Lira, S. A., Graham, G. J., and Cook, D. N. (2007) The chemokine receptor D6 has opposing effects on allergic inflammation and airway reactivity. Am. J. Respir. Crit. Care Med. 175, 243-249
43. Vetrano, S., Borroni, E. M., Sarukhan, A., Savino, B., Bonecchi, R., Correale, C., Arena, V., Fantini, M., Roncalli, M., Malesci, A., Mantovani, A., Locati, M., and Danese, S. (2010) The lymphatic system controls intestinal inflammation and inflammation-associated colon cancer through the chemokine decoy receptor D6. Gut 59, 197-206
44. Allen, S. J., Crown, S. E., and Handel, T. M. (2007) Chemokine: receptor structure, interactions, and antagonism. Annu. Rev. Immunol. 25, 787-820
45. Erwig, L. P., and Henson, P. M. (2007) Immunological consequences of apoptotic cell phagocytosis. Am. J. Pathol. 171, 2-8