Chemokine receptor oligomerization: A further step toward chemokine function

Immunology Letters

Volumn 145, Issue 1-2, 2012, Pages 23-29

  Muñoz, Laura Martínez ^a   Holgado, Borja López ^a   Martínez A, Carlos ^a   Rodríguez Frade, José Miguel ^a   Mellado, Mario ^a  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

Author keywords

Chemokine receptors; GPCR; Oligomerization

Indexed keywords

CHEMOATTRACTANT; CHEMOKINE; CHEMOKINE RECEPTOR; CHEMOKINE RECEPTOR ANTAGONIST; CHEMOKINE RECEPTOR CCR; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CXCR; CHEMOKINE RECEPTOR CXCR4; CYTOKINE; CYTOKINE RECEPTOR; DECOY RECEPTOR; G PROTEIN COUPLED RECEPTOR; GLYCOSAMINOGLYCAN; HETERODIMER; HOMODIMER; OLIGOMER; UNCLASSIFIED DRUG;

ARTICLE; BIOLUMINESCENCE RESONANCE ENERGY TRANSFER; CELL MOTION; CELL SURFACE; COMPLEX FORMATION; ENDOTHELIUM CELL; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; IMMUNE RESPONSE; IN VIVO STUDY; LIGAND BINDING; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; STRUCTURE ANALYSIS; TARGET CELL;

EID: 84862162672     PISSN: 01652478     EISSN: 18790542     Source Type: Journal    
DOI: 10.1016/j.imlet.2012.04.012     Document Type: Review

References (91)

1. Butcher E.C., Picker L.J. Lymphocyte homing and homeostasis. Science 1996, 272:60-66.
2. Gowans J.L., Knight E.J. The Route of Re-Circulation of Lymphocytes in the Rat. Proc R Soc Lond B Biol Sci 1964, 159:257-282.
3. von Andrian U.H., Mackay C.R. T-cell function and migration. Two sides of the same coin. N Engl J Med 2000, 343:1020-1034.
4. Springer T.A. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 1994, 76:301-314.
5. Rot A., von Andrian U.H. Chemokines in innate and adaptive host defense: basic chemokinese grammar for immune cells. Annu Rev Immunol 2004, 22:891-928.
6. Campbell R.N. Assessing the spread of engineered TMV. Science 1999, 286:903.
7. Cyster J.G. Chemokines and cell migration in secondary lymphoid organs. Science 1999, 286:2098-2102.
8. Rossi D., Zlotnik A. The biology of chemokines and their receptors. Annu Rev Immunol 2000, 18:217-242.
9. Clore G.M., Gronenborn A.M. Three-dimensional structures of alpha and beta chemokines. FASEB J 1995, 9:57-62.
10. Fernandez E.J., Lolis E. Structure, function, and inhibition of chemokines. Annu Rev Pharmacol Toxicol 2002, 42:469-499.
11. Mackay C.R. Chemokines: immunology's high impact factors. Nat Immunol 2001, 2:95-101.
12. Muller A., Homey B., Soto H., Ge N., Catron D., Buchanan M.E., et al. Involvement of chemokine receptors in breast cancer metastasis. Nature 2001, 410:50-56.
13. Strieter R.M. Chemokines: not just leukocyte chemoattractants in the promotion of cancer. Nat Immunol 2001, 2:285-286.
14. Proudfoot A.E. Chemokine receptors: multifaceted therapeutic targets. Nat Rev Immunol 2002, 2:106-115.
15. Alcami A. Viral mimicry of cytokines, chemokines and their receptors. Nat Rev Immunol 2003, 3:36-50.
16. Murphy P.M., Baggiolini M., Charo I.F., Hebert C.A., Horuk R., Matsushima K., et al. International union of pharmacology. XXII. Nomenclature for chemokine receptors. Pharmacol Rev 2000, 52:145-176.
17. Murdoch C., Finn A. Chemokine receptors and their role in inflammation and infectious diseases. Blood 2000, 95:3032-3043.
18. Littman D.R. Chemokine receptors: keys to AIDS pathogenesis. Cell 1998, 93:677-680.
19. el-Sawy T., Fahmy N.M., Fairchild R.L. Chemokines: directing leukocyte infiltration into allografts. Curr Opin Immunol 2002, 14:562-568.
20. Horuk R. Development and evaluation of pharmacological agents targeting chemokine receptors. Methods 2003, 29:369-375.
21. Proudfoot A.E., Power C.A., Rommel C., Wells T.N. Strategies for chemokine antagonists as therapeutics. Semin Immunol 2003, 15:57-65.
22. Wells T.N., Power C.A., Shaw J.P., Proudfoot A.E. Chemokine blockers--therapeutics in the making. Trends Pharmacol Sci 2006, 27:41-47.
23. Loetscher P., Seitz M., Baggiolini M., Moser B. Interleukin-2 regulates CC chemokine receptor expression and chemotactic responsiveness in T lymphocytes. J Exp Med 1996, 184:569-577.
24. Papadopoulos E.J., Sassetti C., Saeki H., Yamada N., Kawamura T., Fitzhugh D.J., et al. Fractalkine, a CX3C chemokine, is expressed by dendritic cells and is up-regulated upon dendritic cell maturation. Eur J Immunol 1999, 29:2551-2559.
25. Parks E., Strieter R.M., Lukacs N.W., Gauldie J., Hitt M., Graham F.L., et al. Transient gene transfer of IL-12 regulates chemokine expression and disease severity in experimental arthritis. J Immunol 1998, 160:4615-4619.
26. Johnson Z., Proudfoot A.E., Handel T.M. Interaction of chemokines and glycosaminoglycans: a new twist in the regulation of chemokine function with opportunities for therapeutic intervention. Cytokine Growth Factor Rev 2005, 16:625-636.
27. Jin H., Shen X., Baggett B.R., Kong X., LiWang P.J. The human CC chemokine MIP-1beta dimer is not competent to bind to the CCR5 receptor. J Biol Chem 2007, 282:27976-27983.
28. Rajarathnam K., Sykes B.D., Kay C.M., Dewald B., Geiser T., Baggiolini M., et al. Neutrophil activation by monomeric interleukin-8. Science 1994, 264:90-92.
29. Baltus T., Weber K.S., Johnson Z., Proudfoot A.E., Weber C. Oligomerization of RANTES is required for CCR1-mediated arrest but not CCR5-mediated transmigration of leukocytes on inflamed endothelium. Blood 2003, 102:1985-1988.
30. Graham G.J., McKimmie C.S. Chemokine scavenging by D6: a movable feast. Trends Immunol 2006, 27:381-386.
31. Nibbs R., Graham G., Rot A. Chemokines on the move: control by the chemokine interceptors Duffy blood group antigen and D6. Semin Immunol 2003, 15:287-294.
32. Murphy P.M. The molecular biology of leukocyte chemoattractant receptors. Annu Rev Immunol 1994, 12:593-633.
33. Bayburt T.H., Vishnivetskiy S.A., McLean M.A., Morizumi T., Huang C.C., Tesmer J.J., et al. Monomeric rhodopsin is sufficient for normal rhodopsin kinase (GRK1) phosphorylation and arrestin-1 binding. J Biol Chem 2011, 286:1420-1428.
34. Ernst O.P., Gramse V., Kolbe M., Hofmann K.P., Heck M. Monomeric G protein-coupled receptor rhodopsin in solution activates its G protein transducin at the diffusion limit. Proc Natl Acad Sci U S A 2007, 104:10859-10864.
35. Kuszak A.J., Pitchiaya S., Anand J.P., Mosberg H.I., Walter N.G., Sunahara R.K. Purification and functional reconstitution of monomeric mu-opioid receptors: allosteric modulation of agonist binding by Gi2. J Biol Chem 2009, 284:26732-26741.
36. Hamatake M., Aoki T., Futahashi Y., Urano E., Yamamoto N., Komano J. Ligand-independent higher-order multimerization of CXCR4, a G-protein-coupled chemokine receptor involved in targeted metastasis. Cancer Sci 2009, 100:95-102.
37. Hernanz-Falcon P., Rodriguez-Frade J.M., Serrano A., Juan D., del Sol A., Soriano S.F., et al. Identification of amino acid residues crucial for chemokine receptor dimerization. Nat Immunol 2004, 5:216-223.
38. Percherancier Y., Berchiche Y.A., Slight I., Volkmer-Engert R., Tamamura H., Fujii N., et al. Bioluminescence resonance energy transfer reveals ligand-induced conformational changes in CXCR4 homo- and heterodimers. J Biol Chem 2005, 280:9895-9903.
39. Wang J., He L., Combs C.A., Roderiquez G., Norcross M.A. Dimerization of CXCR4 in living malignant cells: control of cell migration by a synthetic peptide that reduces homologous CXCR4 interactions. Mol Cancer Ther 2006, 5:2474-2483.
40. Wilson S., Wilkinson G., Milligan G. The CXCR1 and CXCR2 receptors form constitutive homo- and heterodimers selectively and with equal apparent affinities. J Biol Chem 2005, 280:28663-28674.
41. Wu B., Chien E.Y., Mol C.D., Fenalti G., Liu W., Katritch V., et al. Structures of the CXCR4 chemokine GPCR with small-molecule and cyclic peptide antagonists. Science 2010, 330:1066-1071.
42. Rodriguez-Frade J.M., Vila-Coro A.J., de Ana A.M., Albar J.P., Martinez A.C., Mellado M. The chemokine monocyte chemoattractant protein-1 induces functional responses through dimerization of its receptor CCR2. Proc Natl Acad Sci U S A 1999, 96:3628-3633.
43. Kenworthy A.K. Imaging protein-protein interactions using fluorescence resonance energy transfer microscopy. Methods 2001, 24:289-296.
44. Isik N., Hereld D., Jin T. Fluorescence resonance energy transfer imaging reveals that chemokine-binding modulates heterodimers of CXCR4 and CCR5 receptors. PLoS One 2008, 3:e3424.
45. Martinez Munoz L., Lucas P., Navarro G., Checa A.I., Franco R., Martinez A.C., et al. Dynamic regulation of CXCR1 and CXCR2 homo- and heterodimers. J Immunol 2009, 183:7337-7346.
46. Issafras H., Angers S., Bulenger S., Blanpain C., Parmentier M., Labbe-Jullie C., et al. Constitutive agonist-independent CCR5 oligomerization and antibody-mediated clustering occurring at physiological levels of receptors. J Biol Chem 2002, 277:34666-34673.
47. Bulenger S., Marullo S., Bouvier M. Emerging role of homo- and heterodimerization in G-protein-coupled receptor biosynthesis and maturation. Trends Pharmacol Sci 2005, 26:131-137.
48. Singer I.I., Scott S., Kawka D.W., Chin J., Daugherty B.L., DeMartino J.A., et al. CCR5, CXCR4, and CD4 are clustered and closely apposed on microvilli of human macrophages and T cells. J Virol 2001, 75:3779-3790.
49. Angers S., Salahpour A., Bouvier M. Dimerization: an emerging concept for G protein-coupled receptor ontogeny and function. Annu Rev Pharmacol Toxicol 2002, 42:409-435.
50. Samson M., Libert F., Doranz B.J., Rucker J., Liesnard C., Farber C.M., et al. Resistance to HIV-1 infection in caucasian individuals bearing mutant alleles of the CCR-5 chemokine receptor gene. Nature 1996, 382:722-725.
51. Chelli M., Alizon M. Determinants of the trans-dominant negative effect of truncated forms of the CCR5 chemokine receptor. J Biol Chem 2001, 276:46975-46982.
52. White J.H., Wise A., Main M.J., Green A., Fraser N.J., Disney G.H., et al. Heterodimerization is required for the formation of a functional GABA(B) receptor. Nature 1998, 396:679-682.
53. Fotiadis D., Liang Y., Filipek S., Saperstein D.A., Engel A., Palczewski K. Atomic-force microscopy: rhodopsin dimers in native disc membranes. Nature 2003, 421:127-128.
54. Sohy D., Yano H., de Nadai P., Urizar E., Guillabert A., Javitch J.A., et al. Hetero-oligomerization of CCR2, CCR5, and CXCR4 and the protean effects of selective antagonists. J Biol Chem 2009, 284:31270-31279.
55. de Juan D., Mellado M., Rodriguez-Frade J.M., Hernanz-Falcon P., Serrano A., del Sol A., et al. A framework for computational and experimental methods: identifying dimerization residues in CCR chemokine receptors. Bioinformatics 2005, 21(Suppl. 2):ii13-ii18.
56. El-Asmar L., Springael J.Y., Ballet S., Andrieu E.U., Vassart G., Parmentier M. Evidence for negative binding cooperativity within CCR5-CCR2b heterodimers. Mol Pharmacol 2005, 67:460-469.
57. Springael J.Y., Le Minh P.N., Urizar E., Costagliola S., Vassart G., Parmentier M. Allosteric modulation of binding properties between units of chemokine receptor homo- and hetero-oligomers. Mol Pharmacol 2006, 69:1652-1661.
58. Sohy D., Parmentier M., Springael J.Y. Allosteric transinhibition by specific antagonists in CCR2/CXCR4 heterodimers. J Biol Chem 2007, 282:30062-30069.
59. Gao P., Zhou X.Y., Yashiro-Ohtani Y., Yang Y.F., Sugimoto N., Ono S., et al. The unique target specificity of a nonpeptide chemokine receptor antagonist: selective blockade of two Th1 chemokine receptors CCR5 and CXCR3. J Leukoc Biol 2003, 73:273-280.
60. Damian M., Martin A., Mesnier D., Pin J.P., Baneres J.L. Asymmetric conformational changes in a GPCR dimer controlled by G-proteins. EMBO J 2006, 25:5693-5702.
61. Chabre M., Deterre P., Antonny B. The apparent cooperativity of some GPCRs does not necessarily imply dimerization. Trends Pharmacol Sci 2009, 30:182-187.
62. Thelen M., Munoz L.M., Rodriguez-Frade J.M., Mellado M. Chemokine receptor oligomerization: functional considerations. Curr Opin Pharmacol 2010, 10:38-43.
63. Babcock G.J., Farzan M., Sodroski J. Ligand-independent dimerization of CXCR4, a principal HIV-1 coreceptor. J Biol Chem 2003, 278:3378-3385.
64. Trettel F., Di Bartolomeo S., Lauro C., Catalano M., Ciotti M.T., Limatola C. Ligand-independent CXCR2 dimerization. J Biol Chem 2003, 278:40980-40988.
65. Chakera A., Seeber R.M., John A.E., Eidne K.A., Greaves D.R. The duffy antigen/receptor for chemokines exists in an oligomeric form in living cells and functionally antagonizes CCR5 signaling through hetero-oligomerization. Mol Pharmacol 2008, 73:1362-1370.
66. Jordan B.A., Devi L.A. G-protein-coupled receptor heterodimerization modulates receptor function. Nature 1999, 399:697-700.
67. Terrillon S., Bouvier M. Roles of G-protein-coupled receptor dimerization. EMBO Rep 2004, 5:30-34.
68. Gouwy M., Struyf S., Noppen S., Schutyser E., Springael J.Y., Parmentier M., et al. Synergy between coproduced CC and CXC chemokines in monocyte chemotaxis through receptor-mediated events. Mol Pharmacol 2008, 74:485-495.
69. Paoletti S., Petkovic V., Sebastiani S., Danelon M.G., Uguccioni M., Gerber B.O. A rich chemokine environment strongly enhances leukocyte migration and activities. Blood 2005, 105:3405-3412.
70. Koenen R.R., von Hundelshausen P., Nesmelova I.V., Zernecke A., Liehn E.A., Sarabi A., et al. Disrupting functional interactions between platelet chemokines inhibits atherosclerosis in hyperlipidemic mice. Nat Med 2009, 15:97-103.
71. Crown S.E., Yu Y., Sweeney M.D., Leary J.A., Handel T.M. Heterodimerization of CCR2 chemokines and regulation by glycosaminoglycan binding. J Biol Chem 2006, 281:25438-25446.
72. Mellado M., Rodriguez-Frade J.M., Vila-Coro A.J., Fernandez S., Martin de Ana A., Jones D.R., et al. Chemokine receptor homo- or heterodimerization activates distinct signaling pathways. EMBO J 2001, 20:2497-2507.
73. Contento R.L., Molon B., Boularan C., Pozzan T., Manes S., Marullo S., et al. CXCR4-CCR5: a couple modulating T cell functions. Proc Natl Acad Sci U S A 2008, 105:10101-10106.
74. Molon B., Gri G., Bettella M., Gomez-Mouton C., Lanzavecchia A., Martinez A.C., et al. T cell costimulation by chemokine receptors. Nat Immunol 2005, 6:465-471.
75. Naumann U., Cameroni E., Pruenster M., Mahabaleshwar H., Raz E., Zerwes H.G., et al. CXCR7 functions as a scavenger for CXCL12 and CXCL11. PLoS One 2010, 5:e9175.
76. Levoye A., Balabanian K., Baleux F., Bachelerie F., Lagane B. CXCR7 heterodimerizes with CXCR4 and regulates CXCL12-mediated G protein signaling. Blood 2009, 113:6085-6093.
77. Sanchez-Alcaniz J.A., Haege S., Mueller W., Pla R., Mackay F., Schulz S., et al. Cxcr7 controls neuronal migration by regulating chemokine responsiveness. Neuron 2011, 69:77-90.
78. Sierro F., Biben C., Martinez-Munoz L., Mellado M., Ransohoff R.M., 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, 104:14759-14764.
79. Pello O.M., Martinez-Munoz L., Parrillas V., Serrano A., Rodriguez-Frade J.M., Toro M.J., et al. Ligand stabilization of CXCR4/delta-opioid receptor heterodimers reveals a mechanism for immune response regulation. Eur J Immunol 2008, 38:537-549.
80. Parenty G., Appelbe S., Milligan G. CXCR2 chemokine receptor antagonism enhances DOP opioid receptor function via allosteric regulation of the CXCR2-DOP receptor heterodimer. Biochem J 2008, 412:245-256.
81. Rodriguez-Frade J.M., Vila-Coro A.J., Martin A., Nieto M., Sanchez-Madrid F., Proudfoot A.E., et al. Similarities and differences in RANTES- and (AOP)-RANTES-triggered signals: implications for chemotaxis. J Cell Biol 1999, 144:755-765.
82. Vila-Coro A.J., Mellado M., Martin de Ana A., Lucas P., del Real G., Martinez A.C., et al. HIV-1 infection through the CCR5 receptor is blocked by receptor dimerization. Proc Natl Acad Sci U S A 2000, 97:3388-3393.
83. Hammad M.M., Kuang Y.Q., Yan R., Allen H., Dupre D.J. Na+/H+ exchanger regulatory factor-1 is involved in chemokine receptor homodimer CCR5 internalization and signal transduction but does not affect CXCR4 homodimer or CXCR4-CCR5 heterodimer. J Biol Chem 2010, 285:34653-34664.
84. Vila-Coro A.J., Rodriguez-Frade J.M., Martin De Ana A., Moreno-Ortiz M.C., Martinez A.C., Mellado M. The chemokine SDF-1alpha triggers CXCR4 receptor dimerization and activates the JAK/STAT pathway. FASEB J 1999, 13:1699-1710.
85. Toth P.T., Ren D., Miller R.J. Regulation of CXCR4 receptor dimerization by the chemokine SDF-1alpha and the HIV-1 coat protein gp120: a fluorescence resonance energy transfer (FRET) study. J Pharmacol Exp Ther 2004, 310:8-17.
86. Luker K.E., Gupta M., Luker G.D. Imaging chemokine receptor dimerization with firefly luciferase complementation. FASEB J 2009, 23:823-834.
87. Kalatskaya I., Berchiche Y.A., Gravel S., Limberg B.J., Rosenbaum J.S., Heveker N. AMD3100 is a CXCR7 ligand with allosteric agonist properties. Mol Pharmacol 2009, 75:1240-1247.
88. Mellado M., Rodriguez-Frade J.M., Vila-Coro A.J., de Ana A.M., Martinez A.C. Chemokine control of HIV-1 infection. Nature 1999, 400:723-724.
89. Rodriguez-Frade J.M., del Real G., Serrano A., Hernanz-Falcon P., Soriano S.F., Vila-Coro A.J., et al. Blocking HIV-1 infection via CCR5 and CXCR4 receptors by acting in trans on the CCR2 chemokine receptor. EMBO J 2004, 23:66-76.
90. Gouldson P.R., Dean M.K., Snell C.R., Bywater R.P., Gkoutos G., Reynolds C.A. Lipid-facing correlated mutations and dimerization in G-protein coupled receptors. Protein Eng 2001, 14:759-767.
91. Wang J., Alvarez R., Roderiquez G., Guan E., Norcross M.A. Constitutive association of cell surface CCR5 and CXCR4 in the presence of CD4. J Cell Biochem 2004, 93:753-760.