Non-signaling chemokine receptors: Mechanism of action and role in vivo

Journal of Neuroimmunology

Volumn 198, Issue 1-2, 2008, Pages 14-19

  Bonecchi, Raffaella ^a,b   Borroni, Elena M ^a   Savino, Benedetta ^a,b   Buracchi, Chiara ^a   Mantovani, Alberto ^a,b   Locati, Massimo ^a,b  

^a HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

Author keywords

Chemokine; Decoy receptor; Inflammation; Scavenger receptor

Indexed keywords

CHEMOKINE RECEPTOR; CHEMOKINE RECEPTOR CCX CKR; D6 CHEMOKINE; DUFFY ANTIGEN RECEPTOR FOR CHEMOKINE;

ADAPTIVE IMMUNITY; ARTICLE; BINDING AFFINITY; CELL MIGRATION; ENDOTHELIUM CELL; IN VIVO STUDY; INNATE IMMUNITY; INTERNALIZATION; MEDIATOR; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; CELL MOVEMENT; HUMANS; IMMUNITY; MODELS, IMMUNOLOGICAL; RECEPTORS, CHEMOKINE;

EID: 47249115214     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2008.04.018     Document Type: Article

References (61)

1. Addison C.L., Belperio J.A., Burdick M.D., and Strieter R.M. Overexpression of the duffy antigen receptor for chemokines (DARC) by NSCLC tumor cells results in increased tumor necrosis. BMC Cancer 4 (2004) 28
2. Bandyopadhyay S., Zhan R., Chaudhuri A., Watabe M., Pai S.K., Hirota S., Hosobe S., Tsukada T., Miura K., Takano Y., Saito K., Pauza M.E., Hayashi S., Wang Y., Mohinta S., Mashimo T., Iiizumi M., Furuta E., and Watabe K. Interaction of KAI1 on tumor cells with DARC on vascular endothelium leads to metastasis suppression. Nat. Med. 12 (2006) 933-938
3. Blackburn P.E., Simpson C.V., Nibbs R.J., O'Hara M., Booth R., Poulos J., Isaacs N.W., and Graham G.J. Purification and biochemical characterization of the D6 chemokine receptor. Biochem. J. 379 (2004) 263-272
4. Bonecchi R., Locati M., Galliera E., Vulcano M., Sironi M., Fra A.M., Gobbi M., Vecchi A., Sozzani S., Haribabu B., Van Damme J., and Mantovani A. Differential recognition and scavenging of native and truncated macrophage-derived chemokine (MDC/CCL22) by the D6 decoy receptor. J. Immunol. 172 (2004) 4972-4976
5. Bonecchi, R., Borroni, E.M., Anselmo, A., Doni, A., Savino, B., Mirolo, M., Fabbri, M., Jala, V.R., Haribabu, B., Mantovani, A, Locati, M., in press. Regulation of D6 chemokine scavenging activity by ligand and Rab11-dependent surface upregulation. Blood.
6. Bonini J.A., Martin S.K., Dralyuk F., Roe M.W., Philipson L.H., and Steiner D.F. Cloning, expression, and chromosomal mapping of a novel human CC-chemokine receptor (CCR10) that displays high-affinity binding for MCP-1 and MCP-3. DNA Cell Biol. 16 (1997) 1249-1256
7. Charo I.F., and Ransohoff R.M. The many roles of chemokines and chemokine receptors in inflammation. N. Engl. J. Med. 354 (2006) 610-621
8. Chaudhuri A., Polyakova J., Zbrzezna V., Williams K., Gulati S., and Pogo A.O. Cloning of glycoprotein D cDNA, which encodes the major subunit of the Duffy blood group system and the receptor for the Plasmodium vivax malaria parasite. Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 10793-10797
9. Chaudhuri A., Rodriguez M., Zbrzezna V., Luo H., Pogo A.O., and Banerjee D. Induction of Duffy gene (FY) in human endothelial cells and in mouse. Cytokine 21 (2003) 137-148
10. Chitnis C.E., Chaudhuri A., Horuk R., Pogo A.O., and Miller L.H. The domain on the Duffy blood group antigen for binding Plasmodium vivax and P. knowlesi malarial parasites to erythrocytes. J. Exp. Med. 184 (1996) 1531-1536
11. Choe H., Moore M.J., Owens C.M., Wright P.L., Vasilieva N., Li W., Singh A.P., Shakri R., Chitnis C.E., and Farzan M. Sulphated tyrosines mediate association of chemokines and Plasmodium vivax Duffy binding protein with the Duffy antigen/receptor for chemokines (DARC). Mol. Microbiol. 55 (2005) 1413-1422
12. Comerford I., Milasta S., Morrow V., Milligan G., and Nibbs R. The chemokine receptor CCX-CKR mediates effective scavenging of CCL19 in vitro. Eur. J. Immunol. 36 (2006) 1904-1916
13. Darbonne W.C., Rice G.C., Mohler M.A., Apple T., Hebert C.A., Valente A.J., and Baker J.B. Red blood cells are a sink for interleukin 8, a leukocyte chemotaxin. J. Clin. Invest. 88 (1991) 1362-1369
14. Dawson T.C., Lentsch A.B., Wang Z., Cowhig J.E., Rot A., Maeda N., and Peiper S.C. Exaggerated response to endotoxin in mice lacking the Duffy antigen/receptor for chemokines (DARC). Blood 96 (2000) 1681-1684
15. Du J., Luan J., Liu H., Daniel T.O., Peiper S., Chen T.S., Yu Y., Horton L.W., Nanney L.B., Strieter R.M., and Richmond A. Potential role for Duffy antigen chemokine-binding protein in angiogenesis and maintenance of homeostasis in response to stress. J. Leukoc. Biol. 71 (2002) 141-153
16. Fra A.M., Locati M., Otero K., Sironi M., Signorelli P., Massardi M.L., Gobbi M., Vecchi A., Sozzani S., and Mantovani A. Cutting edge: scavenging of inflammatory CC chemokines by the promiscuous putatively silent chemokine receptor D6. J. Immunol. 170 (2003) 2279-2282
17. Galliera E., Jala V.R., Trent J.O., Bonecchi R., Signorelli P., Lefkowitz R.J., Mantovani A., Locati M., and Haribabu B. beta -arrestin dependent constitutive internalization of the human chemokine decoy receptor D6. J. Biol. Chem. 279 (2004) 25590-25597
18. Gardner L., Patterson A.M., Ashton B.A., Stone M.A., and Middleton J. The human Duffy antigen binds selected inflammatory but not homeostatic chemokines. Biochem. Biophys. Res. Commun. 321 (2004) 306-312
19. Gosling J., Dairaghi D.J., Wang Y., Hanley M., Talbot D., Miao Z., and Schall T.J. Cutting edge: identification of a novel chemokine receptor that binds dendritic cell- and T cell-active chemokines including ELC, SLC, and TECK. J. Immunol. 164 (2000) 2851-2856
20. Hadley T.J., and Peiper S.C. From malaria to chemokine receptor: the emerging physiologic role of the Duffy blood group antigen. Blood 89 (1997) 3077-3091
21. Heinzel K., Benz C., and Bleul C.C. A silent chemokine receptor regulates steady-state leukocyte homing in vivo. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 8421-8426
22. Horton L.W., Yu Y., Zaja-Milatovic S., Strieter R.M., and Richmond A. Opposing roles of murine duffy antigen receptor for chemokine and murine CXC chemokine receptor-2 receptors in murine melanoma tumor growth. Cancer Res. 67 (2007) 9791-9799
23. Horuk R., Chitnis C.E., Darbonne W.C., Colby T.J., Rybicki A., Hadley T.J., and Miller L.H. A receptor for the malarial parasite Plasmodium vivax: the erythrocyte chemokine receptor. Science 261 (1993) 1182-1184
24. Horuk R., Martin A., Hesselgesser J., Hadley T., Lu Z.H., Wang Z.X., and Peiper S.C. The Duffy antigen receptor for chemokines: structural analysis and expression in the brain. J. Leukoc. Biol. 59 (1996) 29-38
25. Iiizumi M., Bandyopadhyay S., and Watabe K. Interaction of Duffy antigen receptor for chemokines and KAI1: a critical step in metastasis suppression. Cancer Res. 67 (2007) 1411-1414
26. 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. The chemokine receptor D6 limits the inflammatory response in vivo. Nat. Immunol. 6 (2005) 403-411
27. Kashiwazaki M., Tanaka T., Kanda H., Ebisuno Y., Izawa D., Fukuma N., Akimitsu N., Sekimizu K., Monden M., and Miyasaka M. A high endothelial venule-expressing promiscuous chemokine receptor DARC can bind inflammatory, but not lymphoid, chemokines and is dispensable for lymphocyte homing under physiological conditions. Int. Immunol. 15 (2003) 1219-1227
28. Klein D.E., Nappi V.M., Reeves G.T., Shvartsman S.Y., and Lemmon M.A. Argos inhibits epidermal growth factor receptor signalling by ligand sequestration. Nature 430 (2004) 1040-1044
29. Lee J.S., Frevert C.W., Wurfel M.M., Peiper S.C., Wong V.A., Ballman K.K., Ruzinski J.T., Rhim J.S., Martin T.R., and Goodman R.B. Duffy antigen facilitates movement of chemokine across the endothelium in vitro and promotes neutrophil transmigration in vitro and in vivo. J. Immunol. 170 (2003) 5244-5251
30. Lentsch A.B. The Duffy antigen/receptor for chemokines (DARC) and prostate cancer. A role as clear as black and white?. Faseb J. 16 (2002) 1093-1095
31. Liu L., Graham G.J., Damodaran A., Hu T., Lira S.A., Sasse M., Canasto-Chibuque C., Cook D.N., and Ransohoff R.M. Cutting edge: the silent chemokine receptor D6 is required for generating T cell responses that mediate experimental autoimmune encephalomyelitis. J. Immunol. 177 (2006) 17-21
32. Luster A.D. Chemokines-chemotactic cytokines that mediate inflammation. N. Engl. J. Med. 338 (1998) 436-445
33. Mantovani A. The chemokine system: redundancy for robust outputs. Immunol. Today 20 (1999) 254-257
34. Mantovani A., Locati M., Vecchi A., Sozzani S., and Allavena P. Decoy receptors: a strategy to regulate inflammatory cytokines and chemokines. Trends Immunol. 22 (2001) 328-336
35. 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. Protection against inflammation- and autoantibody-caused fetal loss by the chemokine decoy receptor D6. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 2319-2324
36. 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. Increased inflammation in mice deficient for the chemokine decoy receptor D6. Eur. J. Immunol. 35 (2005) 1342-1346
37. McCulloch C.V., Morrow V., Milasta S., Comerford I., Milligan G., Graham G.J., Isaacs N.W., and Nibbs R.J. Multiple roles for the carboxy-terminal tail of the chemokine scavenger D6. J. Biol. Chem. 283 (2008) 7972-7982
38. McKimmie C.S., and Graham G.J. Leucocyte expression of the chemokine scavenger D6. Biochem. Soc. Trans. 34 (2006) 1002-1004
39. Middleton J., Neil S., Wintle J., Clark-Lewis I., Moore H., Lam C., Auer M., Hub E., and Rot A. Transcytosis and surface presentation of IL-8 by venular endothelial cells. Cell 91 (1997) 385-395
40. Miller L.H., Mason S.J., Clyde D.F., and McGinniss M.H. The resistance factor to Plasmodium vivax in blacks. The Duffy-blood-group genotype, FyFy. N. Engl. J. Med. 295 (1976) 302-304
41. Murphy P.M. The molecular biology of leukocyte chemoattractant receptors. Annu. Rev. Immunol. 12 (1994) 593-633
42. Neil S.J., Aasa-Chapman M.M., Clapham P.R., Nibbs R.J., McKnight A., and Weiss R.A. The promiscuous CC chemokine receptor D6 is a functional coreceptor for primary isolates of human immunodeficiency virus type 1 (HIV-1) and HIV-2 on astrocytes. J. Virol. 79 (2005) 9618-9624
43. Neote K., Mak J.Y., Kolakowski Jr. L.F., and Schall T.J. Functional and biochemical analysis of the cloned Duffy antigen: identity with the red blood cell chemokine receptor. Blood 84 (1994) 44-52
44. Nibbs R.J., Gilchrist D.S., King V., Ferra A., Forrow S., Hunter K.D., and Graham G.J. The atypical chemokine receptor D6 suppresses the development of chemically induced skin tumors. J. Clin. Invest. 117 (2007) 1884-1892
45. Nibbs R.J., Kriehuber E., Ponath P.D., Parent D., Qin S., Campbell J.D., Henderson A., Kerjaschki D., Maurer D., Graham G.J., and Rot A. The beta-chemokine receptor D6 is expressed by lymphatic endothelium and a subset of vascular tumors. Am. J. Pathol. 158 (2001) 867-877
46. Nibbs R.J., Wylie S.M., Pragnell I.B., and Graham G.J. Cloning and characterization of a novel murine beta chemokine receptor, D6. Comparison to three other related macrophage inflammatory protein-1alpha receptors, CCR-1, CCR-3, and CCR-5. J. Biol. Chem. 272 (1997) 12495-12504
47. Nibbs R.J., Wylie S.M., Yang J., Landau N.R., and Graham G.J. Cloning and characterization of a novel promiscuous human beta-chemokine receptor D6. J. Biol. Chem. 272 (1997) 32078-32083
48. Nibbs R.J., Yang J., Landau N.R., Mao J.H., and Graham G.J. LD78beta, a non-allelic variant of human MIP-1alpha (LD78alpha), has enhanced receptor interactions and potent HIV suppressive activity. J. Biol. Chem. 274 (1999) 17478-17483
49. Peiper S.C., Wang Z.X., Neote K., Martin A.W., Showell H.J., Conklyn M.J., Ogborne K., Hadley T.J., Lu Z.H., Hesselgesser J., et al. The Duffy antigen/receptor for chemokines (DARC) is expressed in endothelial cells of Duffy negative individuals who lack the erythrocyte receptor. J. Exp. Med. 181 (1995) 1311-1317
50. Proudfoot A.E. Chemokine receptors: multifaceted therapeutic targets. Nat. Rev. Immunol. 2 (2002) 106-115
51. Rios M., Chaudhuri A., Mallinson G., Sausais L., Gomensoro-Garcia A.E., Hannon J., Rosenberger S., Poole J., Burgess G., Pogo O., and Reid M. New genotypes in Fy(a-b-) individuals: nonsense mutations (Trp to stop) in the coding sequence of either FY A or FY B. Br. J. Haematol. 108 (2000) 448-454
52. Rollins B.J. Chemokines. Blood 90 (1997) 909-928
53. Rot A. Contribution of Duffy antigen to chemokine function. Cytokine Growth Factor Rev. 16 (2005) 687-694
54. Segerer S., Bohmig G.A., Exner M., Colin Y., Cartron J.P., Kerjaschki D., Schlondorff D., and Regele H. When renal allografts turn DARC. Transplantation 75 (2003) 1030-1034
55. Shen H., Schuster R., Stringer K.F., Waltz S.E., and Lentsch A.B. The Duffy antigen/receptor for chemokines (DARC) regulates prostate tumor growth. Faseb J. 20 (2006) 59-64
56. Tournamille C., Filipe A., Wasniowska K., Gane P., Lisowska E., Cartron J.P., Colin Y., and Le Van Kim C. Structure-function analysis of the extracellular domains of the Duffy antigen/receptor for chemokines: characterization of antibody and chemokine binding sites. Br. J. Haematol. 122 (2003) 1014-1023
57. Townson J.R., and Nibbs R.J. Characterization of mouse CCX-CKR, a receptor for the lymphocyte-attracting chemokines TECK/mCCL25, SLC/mCCL21 and MIP-3beta/mCCL19: comparison to human CCX-CKR. Eur. J. Immunol. 32 (2002) 1230-1241
58. Wang J., Ou Z.L., Hou Y.F., Luo J.M., Shen Z.Z., Ding J., and Shao Z.M. Enhanced expression of Duffy antigen receptor for chemokines by breast cancer cells attenuates growth and metastasis potential. Oncogene 25 (2006) 7201-7211
59. Weber M., Blair E., Simpson C.V., O'Hara M., Blackburn P.E., Rot A., Graham G.J., and Nibbs R.J. The chemokine receptor D6 constitutively traffics to and from the cell surface to internalize and degrade chemokines. Mol. Biol. Cell 15 (2004) 2492-2508
60. Wessels J.M., Linton N.F., Croy B.A., and Tayade C. A review of molecular contrasts between arresting and viable porcine attachment sites. Am. J. Reprod. Immunol. 58 (2007) 470-480
61. Xu L., Ashkenazi A., and Chaudhuri A. Duffy antigen/receptor for chemokines (DARC) attenuates angiogenesis by causing senescence in endothelial cells. Angiogenesis 10 (2007) 307-318