Atypical chemokine receptors and their roles in the resolution of the inflammatory response

Frontiers in Immunology

Volumn 7, Issue JUN, 2016, Pages

  Bonecchi, Raffaella ^a,b   Graham, Gerard J ^c  

^a HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^b HUMANITAS UNIVERSITY   (Italy)

^c UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Atypical receptors; Chemokines; Immunity; Inflammation; Scavenging

Indexed keywords

APOLIPOPROTEIN E; CHEMOKINE RECEPTOR; CHEMOKINE RECEPTOR CXCR4; CXCL13 CHEMOKINE; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; MITOGEN ACTIVATED PROTEIN KINASE; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN KINASE B; SECONDARY LYMPHOID TISSUE CHEMOKINE; VASCULOTROPIN;

ALLERGIC ENCEPHALOMYELITIS; ATHEROGENESIS; ATHEROSCLEROTIC PLAQUE; BIOAVAILABILITY; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; GENE; GENE ACKR1; GENE ACKR2; GENE ACKR3; GENE ACKR4; GENE EXPRESSION; GENE LOCUS; INFLAMMATION; LEUKOCYTE; LEUKOCYTE MIGRATION; MACROPHAGE; MOUSE; MOUSE MODEL; NEUTROPHIL; NONHUMAN; PERIPHERAL LYMPHOCYTE; REVIEW; RHEUMATOID ARTHRITIS; T LYMPHOCYTE; TH17 CELL;

EID: 84977519286     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2016.00224     Document Type: Review

References (73)

1. Soehnlein O, Lindbom L. Phagocyte partnership during the onset and resolution of inflammation. Nat Rev Immunol (2010) 10:427-39. doi:10.1038/nri2779
2. Griffith JW, Sokol CL, Luster AD. Chemokines and chemokine receptors: positioning cells for host defense and immunity. Annu Rev Immunol (2014) 32:659-702. doi:10.1146/annurev-immunol-032713-120145
3. Zlotnik A, Yoshie O. Chemokines: a new classification system and their role in immunity. Immunity (2000) 12:121-7. doi:10.1016/S1074-7613(00)80165-X
4. Zlotnik A, Yoshie O, Nomiyama H. The chemokine and chemokine receptor superfamilies and their molecular evolution. Genome Biol (2006) 7:243. doi:10.1186/gb-2006-7-12-243
5. Mantovani A. The chemokine system: redundancy for robust outputs. Immunol Today (1999) 20:254-7. doi:10.1016/S0167-5699(99)01469-3
6. Bachelerie F, Ben-Baruch A, Burkhardt AM, Combadiere C, Farber JM, Graham GJ, et al. International Union of Pharmacology. LXXXIX. Update on the extended family of chemokine receptors and introducing a new nomenclature for atypical chemokine receptors. Pharmacol Rev (2014) 66:1-79. doi:10.1124/pr.113.007724
7. Muñoz LM, Lucas P, Holgado BL, Barroso R, Vega B, Rodríguez-Frade JM, et al. Receptor oligomerization: a pivotal mechanism for regulating chemokine function. Pharmacol Ther (2011) 131:351-8. doi:10.1016/j.pharmthera.2011.05.002
8. Zweemer AJM, Toraskar J, Heitman LH, Ijzerman AP. Bias in chemokine receptor signalling. Trends Immunol (2014) 35:243-52. doi:10.1016/j.it.2014.02.004
9. Steen A, Larsen O, Thiele S, Rosenkilde MM. Biased and g protein-independent signaling of chemokine receptors. Front Immunol (2014) 5:277. doi:10.3389/fimmu.2014.00277
10. Viola A, Luster AD. Chemokines and their receptors: drug targets in immunity and inflammation. Annu Rev Pharmacol Toxicol (2008) 48:171-97. doi:10.1146/annurev.pharmtox.48.121806.154841
11. Schall TJ, Proudfoot AE. Overcoming hurdles in developing successful drugs targeting chemokine receptors. Nat Rev Immunol (2011) 11:355-63. doi:10.1038/nri2972
12. Murphy PM, Tiffany HL. Cloning of complementary-DNA encoding a functional human interleukin-8 receptor. Science (1991) 253:1280-3. doi:10.1126/science.1891716
13. Serhan CN, Chiang N, Van Dyke TE. Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nat Rev Immunol (2008) 8:349-61. doi:10.1038/nri2294
14. Lee KM, Danuser R, Stein JV, Graham D, Nibbs RJ, Graham GJ. The chemokine receptors ACKR2 and CCR2 reciprocally regulate lymphatic vessel density. EMBO J (2014) 33:2564-80. doi:10.15252/embj.201488887
15. Ortega-Gómez A, Perretti M, Soehnlein O. Resolution of inflammation: an integrated view. EMBO Mol Med (2013) 5:661-74. doi:10.1002/emmm.201202382
16. Bachelerie F, Graham GJ, Locati M, Mantovani A, Murphy PM, Nibbs R, et al. New nomenclature for atypical chemokine receptors. Nat Immunol (2014) 15:207-8. doi:10.1038/ni.2812
17. Graham GJ, Locati M, Mantovani A, Rot A, Thelen M. The biochemistry and biology of the atypical chemokine receptors. Immunol Lett (2012) 145:30-8. doi:10.1016/j.imlet.2012.04.004
18. Nibbs RJB, Graham GJ. Immune regulation by atypical chemokine receptors. Nat Rev Immunol (2013) 13:815-29. doi:10.1038/nri3544
19. Chaudhuri A, Polyakova J, Zbrzezna V, Pogo AO, Hesselgesser J, Horuk R, et al. The major glycoprotein of the Duffy blood-group antigen (Gpd), which is the malarial plasmodium-vivax erythrocyte receptor is also a novel class of chemokine receptor and is present in brain, kidney, lung, thymus, and spleen. FASEB J (1994) 8:A1386-1386.
20. Novitzky-Basso I, Rot A. Duffy antigen receptor for chemokines (DARC) and its involvement in patterning and control of inflammatory chemokines. Front Immunol (2012) 3:266. doi:10.3389/fimmu.2012.00266
21. Rot A. Contribution of Duffy antigen to chemokine function. Cytokine Growth Factor Rev (2005) 16:687-94. doi:10.1016/j.cytogfr.2005.05.011
22. Nomiyama H, Osada N, Yoshie O. A family tree of vertebrate chemokine receptors for a unified nomenclature. Dev Comp Immunol (2011) 35:705-15. doi:10.1016/j.dci.2011.01.019
23. Schnabel RB, Baumert J, Barbalic M, Dupuis J, Ellinor PT, Durda P, et al. Duffy antigen receptor for chemokines (Darc) polymorphism regulates circulating concentrations of monocyte chemoattractant protein-1 and other inflammatory mediators. Blood (2010) 115:5289-99. doi:10.1182/blood-2009-05-221382
24. Mangalmurti NS, Xiong Z, Hulver M, Ranganathan M, Liu XH, Oriss T, et al. Loss of red cell chemokine scavenging promotes transfusion-related lung inflammation. Blood (2009) 113:1158-66. doi:10.1182/blood-2008-07-166264
25. Howes RE, Patil AP, Piel FB, Nyangiri OA, Kabaria CW, Gething PW, et al. The global distribution of the Duffy blood group. Nat Commun (2011) 2:266. doi:10.1038/ncomms1265
26. Hansell CAH, Hurson CE, Nibbs RJB. DARC and D6: silent partners in chemokine regulation? Immunol Cell Biol (2011) 89:197-206. doi:10.1038/icb.2010.147
27. Pruenster M, Mudde L, Bombosi P, Dimitrova S, Zsak M, Middleton J, et al. The Duffy antigen receptor for chemokines transports chemokines and supports their promigratory activity. Nat Immunol (2009) 10:101-8. doi:10.1038/ni.1675
28. Lee JS, Wurfel MM, Matute-Bello G, Frevert CW, Rosengart MR, Ranganathan M, et al. The duffy antigen modifies systemic and local tissue chemokine responses following lipopolysaccharide stimulation. J Immunol (2006) 177:8086-94. doi:10.4049/jimmunol.177.11.8086
29. Lee JS, Frevert CW, Wurfel MM, Peiper SC, Wong VA, Ballman KK, et al. Duffy antigen facilitates movement of chemokine across the endothelium in vitro and promotes neutrophil transmigration in vitro and in vivo. J Immunol (2003) 170:5244-51. doi:10.4049/jimmunol.170.10.5244
30. Zarbock A, Bishop J, Müller H, Schmolke M, Buschmann K, Van Aken H, et al. Chemokine homeostasis vs. chemokine presentation during severe acute lung injury: the other side of the Duffy antigen receptor for chemokines. Am J Physiol Lung Cell Mol Physiol (2010) 298:L462-71. doi:10.1152/ajplung.00224.2009
31. Zarbock A, Schmolke M, Bockhorn SG, Scharte M, Buschmann K, Ley K, et al. The Duffy antigen receptor for chemokines in acute renal failure: a facilitator of renal chemokine presentation. Crit Care Med (2007) 35:2156-63. doi:10.1097/01.CCM.0000280570.82885.32
32. Rundle CH, Mohan S, Edderkaoui B. Duffy antigen receptor for chemokines regulates post-fracture inflammation. PLoS One (2013) 8:e77362. doi:10.1371/journal.pone.0077362
33. Wan W, Liu Q, Lionakis MS, Marino AP, Anderson SA, Swamydas M, et al. Atypical chemokine receptor 1 deficiency reduces atherogenesis in ApoE-knockout mice. Cardiovasc Res (2015) 106(3):478-87. doi:10.1093/cvr/cvv124
34. Zimmerman PA, Ferreira MU, Howes RE, Mercereau-Puijalon O. Chapter two-red blood cell polymorphism and susceptibility to Plasmodium vivax. In: Hay SI, Baird JK, editors. Advances in Parasitology. Cambridge, MA: Academic Press (2013). p. 27-76.
35. Lee KM, Nibbs RJB, Graham GJ. D6: the 'crowd controller' at the immune gateway. Trends Immunol (2013) 34:7-12. doi:10.1016/j.it.2012.08.001
36. Fra AM, Locati M, Otero K, Sironi M, Signorelli P, Massardi ML, et al. Cutting edge: scavenging of inflammatory CC chemokines by the promiscuous putatively silent chemokine receptor D6. J Immunol (2003) 170:2279-82. doi:10.4049/jimmunol.170.5.2279
37. Weber M, Blair E, Simpson CV, O'Hara M, Blackburn PE, Rot A, et al. The chemokine receptor D6 constitutively traffics to and from the cell surface to internalize and degrade chemokines. Mol Biol Cell (2004) 15:2492-508. doi:10.1091/mbc. E03-09-0634
38. Bonecchi R, Borroni EM, Anselmo A, Doni A, Savino B, Mirolo M, et al. Regulation of D6 chemokine scavenging activity by ligand-and Rab11-dependent surface up-regulation. Blood (2008) 112:493-503. doi:10.1182/blood-2007-08-108316
39. Borroni EM, Cancellieri C, Vacchini A, Benureau Y, Lagane B, Bachelerie F, et al. β-arrestin-dependent activation of the cofilin pathway is required for the scavenging activity of the atypical chemokine receptor D6. Sci Signal (2013) 6:ra30. doi:10.1126/scisignal.2003627
40. McKimmie CS, Singh MD, Hewit K, Lopez-Franco O, Le Brocq M, Rose-John S, et al. An analysis of the function and expression of D6 on lymphatic endothelial cells. Blood (2013) 121:3768-77. doi:10.1182/blood-2012-04-425314
41. Graham GJ, Locati M. Regulation of the immune and inflammatory responses by the 'atypical' chemokine receptor D6. J Pathol (2013) 229:168-75. doi:10.1002/path.4123
42. Graham GJ. D6 and the atypical chemokine receptor family: novel regulators of immune and inflammatory processes. Eur J Immunol (2009) 39:342-51. doi:10.1002/eji.200838858
43. Martinez de la Torre Y, Locati M, Buracchi C, Dupor J, Cook DN, Bonecchi R, et al. Increased inflammation in mice deficient for the chemokine decoy receptor D6. Eur J Immunol (2005) 35:1342-6. doi:10.1002/eji.200526114
44. Bordon Y, Hansell CA, Sester DP, Clarke M, Mowat AM, Nibbs RJ. The atypical chemokine receptor D6 contributes to the development of experimental colitis. J Immunol (2009) 182:5032-40. doi:10.4049/jimmunol.0802802
45. Vetrano S, Borroni EM, Sarukhan A, Savino B, Bonecchi R, Correale C, et al. The lymphatic system controls intestinal inflammation and inflammation-associated colon cancer through the chemokine decoy receptor D6. Gut (2010) 59:197-206. doi:10.1136/gut.2009.183772
46. Whitehead GS, Wang T, DeGraffLM, Card JW, Lira SA, Graham GJ, et al. The chemokine receptor D6 has opposing effects on allergic inflammation and airway reactivity. Am J Respir Crit Care Med (2007) 175:243-9. doi:10.1164/rccm.200606-839OC
47. Madigan J, Freeman DJ, Menzies F, Forrow S, Nelson SM, Young A, et al. Chemokine scavenger D6 is expressed by trophoblasts and aids the survival of mouse embryos transferred into allogeneic recipients. J Immunol (2010) 184:3202-12. doi:10.4049/jimmunol.0902118
48. Martinez de la Torre Y, Buracchi C, Borroni EM, Dupor J, Bonecchi R, Nebuloni M, et al. Protection against inflammation-and autoantibody-caused fetal loss by the chemokine decoy receptor D6. Proc Natl Acad Sci U S A (2007) 104:2319-24. doi:10.1073/pnas.0607514104
49. Cochain C, Auvynet C, Poupel L, Vilar J, Dumeau E, Richart A, et al. The chemokine decoy receptor D6 prevents excessive inflammation and adverse ventricular remodeling after myocardial infarction. Arterioscler Thromb Vasc Biol (2012) 32:2206-13. doi:10.1161/ATVBAHA.112.254409
50. Di Liberto D, Locati M, Caccamo N, Vecchi A, Meraviglia S, Salerno A, et al. Role of the chemokine decoy receptor D6 in balancing inflammation, immune activation, and antimicrobial resistance in Mycobacterium tuberculosis infection. J Exp Med (2008) 205:2075-84. doi:10.1084/jem.20070608
51. Liu L, Graham GJ, Damodaran A, Hu T, Lira SA, Sasse M, et al. Cutting edge: the silent chemokine receptor d6 is required for generating T cell responses that mediate experimental autoimmune encephalomyelitis. J Immunol (2006) 177:17-21. doi:10.4049/jimmunol.177.1.17
52. Zheng S, Coventry S, Cai L, Powell DW, Jala VR, Haribabu B, et al. Renal protection by genetic deletion of the atypical chemokine receptor ACKR2 in diabetic OVE mice. J Diabetes Res (2016) 2016:11. doi:10.1155/2016/5362506
53. Hansell CAH, MacLellan LM, Oldham RS, Doonan J, Chapple KJ, Anderson EJ, et al. The atypical chemokine receptor ACKR2 suppresses Th17 responses to protein autoantigens. Immunol Cell Biol (2015) 93:167-76. doi:10.1038/icb.2014.90
54. Rot A, McKimmie C, Burt CL, Pallas KJ, Jamieson T, Pruenster M, et al. Cell-autonomous regulation of neutrophil migration by the D6 chemokine decoy receptor. J Immunol (2013) 190:6450-6. doi:10.4049/jimmunol.1201429
55. Pashover-Schallinger E, Aswad M, Schif-Zuck S, Shapiro H, Singer P, Ariel A. The atypical chemokine receptor D6 controls macrophage efferocytosis and cytokine secretion during the resolution of inflammation. FASEB J (2012) 26:3891-900. doi:10.1096/fj.11-194894
56. Nibbs RJ, Gilchrist DS, King V, Ferra A, Forrow S, Hunter KD, et al. The atypical chemokine receptor D6 suppresses the development of chemically induced skin tumors. J Clin Invest (2007) 117:1884-92. doi:10.1172/JCI30068
57. Burns JM, Summers BC, Wang Y, Melikian A, Berahovich R, Miao Z, et al. A novel chemokine receptor for SDF-1 and I-TAC involved in cell survival, cell adhesion, and tumor development. J Exp Med (2006) 203:2201-13. doi:10.1084/jem.20052144
58. Rajagopal S, Kim J, Ahn S, Craig S, Lam CM, Gerard NP, et al. Beta-arrestin-but not G protein-mediated signaling by the "decoy" receptor CXCR7. Proc Natl Acad Sci U S A (2010) 107:628-32. doi:10.1073/pnas.0912852107
59. Levoye A, Balabanian K, Baleux F, Bachelerie F, Lagane B. CXCR7 heterodimerizes with CXCR4 and regulates CXCL12-mediated G protein signaling. Blood (2009) 113:6085-93. doi:10.1182/blood-2008-12-196618
60. Sebastian JS, Guillaume V, Darren G, Lars H. Collective cell migration guided by dynamically maintained gradients. Phys Biol (2011) 8:045004. doi:10.1088/1478-3975/8/4/045004
61. Haege S, Einer C, Thiele S, Mueller W, Nietzsche S, Lupp A, et al. CXC chemokine receptor 7 (CXCR7) regulates CXCR4 protein expression and capillary tuft development in mouse kidney. PLoS One (2012) 7:e42814. doi:10.1371/journal.pone.0042814
62. Sierro F, Biben C, Martinez-Munoz L, Mellado M, RansohoffRM, Li M, et al. Disrupted cardiac development but normal hematopoiesis in mice deficient in the second CXCL12/SDF-1 receptor, CXCR7. Proc Natl Acad Sci U S A (2007) 104:14759-64. doi:10.1073/pnas.0702229104
63. Zhu Y, Matsumoto T, Nagasawa T, Mackay F, Murakami F. Chemokine signaling controls integrity of radial glial scaffold in developing spinal cord and consequential proper position of boundary cap cells. J Neurosci (2015) 35:9211-24. doi:10.1523/JNEUROSCI.0156-15.2015
64. Werner L, Elad H, Brazowski E, Tulchinsky H, Vigodman S, Kopylov U, et al. Reciprocal regulation of CXCR4 and CXCR7 in intestinal mucosal homeostasis and inflammatory bowel disease. J Leukoc Biol (2011) 90:583-90. doi:10.1189/jlb.0111101
65. Chatterjee M, von Ungern-Sternberg SN, Seizer P, Schlegel F, Büttcher M, Sindhu NA, et al. Platelet-derived CXCL12 regulates monocyte function, survival, differentiation into macrophages and foam cells through differential involvement of CXCR4-CXCR7. Cell Death Dis (2015) 6:e1989. doi:10.1038/cddis.2015.233
66. Maksym RB, Tarnowski M, Grymula K, Tarnowska J, Wysoczynski M, Liu R, et al. The role of stromal-derived factor-1-CXCR7 axis in development and cancer. Eur J Pharmacol (2009) 625:31-40. doi:10.1016/j.ejphar.2009.04.071
67. Watanabe K, Penfold ME, Matsuda A, Ohyanagi N, Kaneko K, Miyabe Y, et al. Pathogenic role of CXCR7 in rheumatoid arthritis. Arthritis Rheum (2010) 62:3211-20. doi:10.1002/art.27650
68. Cruz-Orengo L, Holman DW, Dorsey D, Zhou L, Zhang P, Wright M, et al. CXCR7 influences leukocyte entry into the CNS parenchyma by controlling abluminal CXCL12 abundance during autoimmunity. J Exp Med (2011) 208:327-39. doi:10.1084/jem.20102010
69. Banisadr G, Podojil JR, Miller SD, Miller RJ. Pattern of CXCR7 gene expression in mouse brain under normal and inflammatory conditions. J Neuroimmune Pharmacol (2016) 11:26-35. doi:10.1007/s11481-015-9616-y
70. Comerford I, Milasta S, Morrow V, Milligan G, Nibbs R. The chemokine receptor CCX-CKR mediates effective scavenging of CCL19 in vitro. Eur J Immunol (2006) 36:1904-16. doi:10.1002/eji.200535716
71. Ulvmar MH, Werth K, Braun A, Kelay P, Hub E, Eller K, et al. The atypical chemokine receptor CCRL1 shapes functional CCL21 gradients in lymph nodes. Nat Immunol (2014) 15:623-30. doi:10.1038/ni.2889
72. Comerford I, Nibbs RJ, Litchfield W, Bunting M, Harata-Lee Y, Haylock-Jacobs S, et al. The atypical chemokine receptor CCX-CKR scavenges homeostatic chemokines in circulation and tissues and suppresses Th17 responses. Blood (2010) 116:4130-40. doi:10.1182/blood-2010-01-264390
73. Singh MD, King V, Baldwin H, Burden D, Thorrat A, Holmes S, et al. Elevated expression of the chemokine-scavenging receptor D6 is associated with impaired lesion development in psoriasis. Am J Pathol (2012) 181:1158-64. doi:10.1016/j.ajpath.2012.06.042