Heterophilic chemokine receptor interactions in chemokine signaling and biology

Experimental Cell Research

Volumn 317, Issue 5, 2011, Pages 655-663

  Kramp, Birgit K ^a   Sarabi, Alisina ^a   Koenen, Rory R ^a,b   Weber, Christian ^a,b,c  

^a UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c UNIVERSITY OF MUNICH   (Germany)

Author keywords

Chemokine; G protein coupled receptor; Immunology; Leukocyte; Multimerization; Signaling

Indexed keywords

CHEMOKINE; CHEMOKINE RECEPTOR; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR1; CHEMOKINE RECEPTOR CXCR2; CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR7; G PROTEIN COUPLED RECEPTOR;

HUMAN; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; REVIEW;

EID: 79952105905     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2010.11.014     Document Type: Review

References (69)

1. Zlotnik A., Yoshie O. Chemokines: a new classification system and their role in immunity. Immunity 2000, 12:121-127.
2. Proudfoot A.E., Power C.A., Hoogewerf A.J., Montjovent M.O., Borlat F., Offord R.E., Wells T.N. Extension of recombinant human RANTES by the retention of the initiating methionine produces a potent antagonist. J. Biol. Chem. 1996, 271:2599-2603.
3. Clore G.M., Gronenborn A.M. Three-dimensional structures of alpha and beta chemokines. FASEB J. 1995, 9:57-62.
4. Mayo K.H., Chen M.J. Human platelet factor 4 monomer-dimer-tetramer equilibria investigated by 1H NMR spectroscopy. Biochemistry 1989, 28:9469-9478.
5. Nesmelova I.V., Sham Y., Dudek A.Z., van Eijk L.I., Wu G., Slungaard A., Mortari F., Griffioen A.W., Mayo K.H. Platelet factor 4 and interleukin-8 CXC chemokine heterodimer formation modulates function at the quaternary structural level. J. Biol. Chem. 2005, 280:4948-4958.
6. Nesmelova I.V., Sham Y., Gao J., Mayo K.H. CXC and CC chemokines form mixed heterodimers: association free energies from molecular dynamics simulations and experimental correlations. J. Biol. Chem. 2008, 283:24155-24166.
7. 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.
8. Nasser M.W., Raghuwanshi S.K., Grant D.J., Jala V.R., Rajarathnam K., Richardson R.M. Differential activation and regulation of CXCR1 and CXCR2 by CXCL8 monomer and dimer. J. Immunol. 2009, 183:3425-3432.
9. Das S.T., Rajagopalan L., Guerrero-Plata A., Sai J., Richmond A., Garofalo R.P., Rajarathnam K. Monomeric and dimeric CXCL8 are both essential for in vivo neutrophil recruitment. PLoS ONE 2010, 5:e11754.
10. Veldkamp C.T., Seibert C., Peterson F.C., De la Cruz N.B., Haugner J.C., Basnet H., Sakmar T.P., Volkman B.F. Structural basis of CXCR4 sulfotyrosine recognition by the chemokine SDF-1/CXCL12. Sci. Signal. 2008, 1:ra4.
11. Weber C., Koenen R.R. Fine-tuning leukocyte responses: towards a chemokine 'interactome'. Trends Immunol. 2006, 27:268-273.
12. Guan E., Wang J., Norcross M.A. Identification of human macrophage inflammatory proteins 1alpha and 1beta as a native secreted heterodimer. J. Biol. Chem. 2001, 276:12404-12409.
13. 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.
14. Dudek A.Z., Nesmelova I., Mayo K., Verfaillie C.M., Pitchford S., Slungaard A. Platelet factor 4 promotes adhesion of hematopoietic progenitor cells and binds IL-8: novel mechanisms for modulation of hematopoiesis. Blood 2003, 101:4687-4694.
15. von Hundelshausen P., Koenen R.R., Sack M., Mause S.F., Adriaens W., Proudfoot A.E., Hackeng T.M., Weber C. Heterophilic interactions of platelet factor 4 and RANTES promote monocyte arrest on endothelium. Blood 2005, 105:924-930.
16. von Hundelshausen P., Weber K.S., Huo Y., Proudfoot A.E., Nelson P.J., Ley K., Weber C. RANTES deposition by platelets triggers monocyte arrest on inflamed and atherosclerotic endothelium. Circulation 2001, 103:1772-1777.
17. Koenen R.R., von Hundelshausen P., Nesmelova I.V., Zernecke A., Liehn E.A., Sarabi A., Kramp B.K., Piccinini A.M., Paludan S.R., Kowalska M.A., Kungl A.J., Hackeng T.M., Mayo K.H., Weber C. Disrupting functional interactions between platelet chemokines inhibits atherosclerosis in hyperlipidemic mice. Nat. Med. 2009, 15:97-103.
18. Kuschert G.S., Coulin F., Power C.A., Proudfoot A.E., Hubbard R.E., Hoogewerf A.J., Wells T.N. Glycosaminoglycans interact selectively with chemokines and modulate receptor binding and cellular responses. Biochemistry 1999, 38:12959-12968.
19. Proudfoot A.E. The biological relevance of chemokine-proteoglycan interactions. Biochem. Soc. Trans. 2006, 34:422-426.
20. Hoogewerf A.J., Kuschert G.S., Proudfoot A.E., Borlat F., Clark-Lewis I., Power C.A., Wells T.N. Glycosaminoglycans mediate cell surface oligomerization of chemokines. Biochemistry 1997, 36:13570-13578.
21. Proudfoot A.E., Handel T.M., Johnson Z., Lau E.K., LiWang P., Clark-Lewis I., Borlat F., Wells T.N., Kosco-Vilbois M.H. Glycosaminoglycan binding and oligomerization are essential for the in vivo activity of certain chemokines. Proc. Natl Acad. Sci. USA 2003, 100:1885-1890.
22. Goger B., Halden Y., Rek A., Mosl R., Pye D., Gallagher J., Kungl A.J. Different affinities of glycosaminoglycan oligosaccharides for monomeric and dimeric interleukin-8: a model for chemokine regulation at inflammatory sites. Biochemistry 2002, 41:1640-1646.
23. Veldkamp C.T., Peterson F.C., Pelzek A.J., Volkman B.F. The monomer-dimer equilibrium of stromal cell-derived factor-1 (CXCL 12) is altered by pH, phosphate, sulfate, and heparin. Protein Sci. 2005, 14:1071-1081.
24. Murphy P.M., Baggiolini M., Charo I.F., Hebert C.A., Horuk R., Matsushima K., Miller L.H., Oppenheim J.J., Power C.A. International union of pharmacology. XXII. Nomenclature for chemokine receptors. Pharmacol. Rev. 2000, 52:145-176.
25. 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.
26. 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. USA 2007, 104:10859-10864.
27. Milligan G. G protein-coupled receptor dimerisation: molecular basis and relevance to function. Biochim. Biophys. Acta 2007, 1768:825-835.
28. White J.H., Wise A., Main M.J., Green A., Fraser N.J., Disney G.H., Barnes A.A., Emson P., Foord S.M., Marshall F.H. Heterodimerization is required for the formation of a functional GABA(B) receptor. Nature 1998, 396:679-682.
29. 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.
30. Liang Y., Fotiadis D., Filipek S., Saperstein D.A., Palczewski K., Engel A. Organization of the G protein-coupled receptors rhodopsin and opsin in native membranes. J. Biol. Chem. 2003, 278:21655-21662.
31. Liu R., Paxton W.A., Choe S., Ceradini D., Martin S.R., Horuk R., MacDonald M.E., Stuhlmann H., Koup R.A., Landau N.R. Homozygous defect in HIV-1 coreceptor accounts for resistance of some multiply-exposed individuals to HIV-1 infection. Cell 1996, 86:367-377.
32. Benkirane M., Jin D.Y., Chun R.F., Koup R.A., Jeang K.T. Mechanism of transdominant inhibition of CCR5-mediated HIV-1 infection by ccr5delta32. J. Biol. Chem. 1997, 272:30603-30606.
33. 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.
34. Contento R.L., Molon B., Boularan C., Pozzan T., Manes S., Marullo S., Viola A. CXCR4-CCR5: a couple modulating T cell functions. Proc. Natl Acad. Sci. USA 2008, 105:10101-10106.
35. Sohy D., Yano H., de Nadai P., Urizar E., Guillabert A., Javitch J.A., Parmentier M., Springael J.Y. Hetero-oligomerization of CCR2, CCR5, and CXCR4 and the protean effects of "selective" antagonists. J. Biol. Chem. 2009, 284:31270-31279.
36. Babcock G.J., Farzan M., Sodroski J. Ligand-independent dimerization of CXCR4, a principal HIV-1 coreceptor. J. Biol. Chem. 2003, 278:3378-3385.
37. 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.
38. Chen C., Li J., Bot G., Szabo I., Rogers T.J., Liu-Chen L.Y. Heterodimerization and cross-desensitization between the mu-opioid receptor and the chemokine CCR5 receptor. Eur. J. Pharmacol. 2004, 483:175-186.
39. Suzuki S., Chuang L.F., Yau P., Doi R.H., Chuang R.Y. Interactions of opioid and chemokine receptors: oligomerization of mu, kappa, and delta with CCR5 on immune cells. Exp. Cell Res. 2002, 280:192-200.
40. Issafras H., Angers S., Bulenger S., Blanpain C., Parmentier M., Labbe-Jullie C., Bouvier M., Marullo S. Constitutive agonist-independent CCR5 oligomerization and antibody-mediated clustering occurring at physiological levels of receptors. J. Biol. Chem. 2002, 277:34666-34673.
41. Percherancier Y., Berchiche Y.A., Slight I., Volkmer-Engert R., Tamamura H., Fujii N., Bouvier M., Heveker N. Bioluminescence resonance energy transfer reveals ligand-induced conformational changes in CXCR4 homo- and heterodimers. J. Biol. Chem. 2005, 280:9895-9903.
42. 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.
43. Ayoub M.A., Couturier C., Lucas-Meunier E., Angers S., Fossier P., Bouvier M., Jockers R. Monitoring of ligand-independent dimerization and ligand-induced conformational changes of melatonin receptors in living cells by bioluminescence resonance energy transfer. J. Biol. Chem. 2002, 277:21522-21528.
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. Albizu L., Cottet M., Kralikova M., Stoev S., Seyer R., Brabet I., Roux T., Bazin H., Bourrier E., Lamarque L., Breton C., Rives M.L., Newman A., Javitch J., Trinquet E., Manning M., Pin J.P., Mouillac B., Durroux T. Time-resolved FRET between GPCR ligands reveals oligomers in native tissues. Nat. Chem. Biol. 2010, 6:587-594.
46. Margeta-Mitrovic M., Jan Y.N., Jan L.Y. A trafficking checkpoint controls GABA(B) receptor heterodimerization. Neuron 2000, 27:97-106.
47. Mellado M., Rodriguez-Frade J.M., Vila-Coro A.J., Fernandez S., Martin de Ana A., Jones D.R., Toran J.L., Martinez A.C. Chemokine receptor homo- or heterodimerization activates distinct signaling pathways. EMBO J. 2001, 20:2497-2507.
48. 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.
49. 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. USA 1999, 96:3628-3633.
50. Rodriguez-Frade J.M., Mellado M., Martinez A.C. Chemokine receptor dimerization: two are better than one. Trends Immunol. 2001, 22:612-617.
51. Vila-Coro A.J., Mellado M., Martin de Ana A., Lucas P., del Real G., Martinez A.C., Rodriguez-Frade J.M. HIV-1 infection through the CCR5 receptor is blocked by receptor dimerization. Proc. Natl Acad. Sci. USA 2000, 97:3388-3393.
52. Hernanz-Falcon P., Rodriguez-Frade J.M., Serrano A., Juan D., del Sol A., Soriano S.F., Roncal F., Gomez L., Valencia A., Martinez A.C., Mellado M. Identification of amino acid residues crucial for chemokine receptor dimerization. Nat. Immunol. 2004, 5:216-223.
53. Wu B., Chien E.Y., Mol C.D., Fenalti G., Liu W., Katritch V., Abagyan R., Brooun A., Wells P., Bi F.C., Hamel D.J., Kuhn P., Handel T.M., Cherezov V., Stevens R.C. Structures of the CXCR4 chemokine GPCR with small-molecule and cyclic peptide antagonists. Science 2010.
54. 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.
55. 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.
56. Balabanian K., Lagane B., Infantino S., Chow K.Y., Harriague J., Moepps B., Arenzana-Seisdedos F., Thelen M., Bachelerie F. The chemokine SDF-1/CXCL12 binds to and signals through the orphan receptor RDC1 in T lymphocytes. J. Biol. Chem. 2005, 280:35760-35766.
57. Sierro F., Biben C., Martinez-Munoz L., Mellado M., Ransohoff R.M., Li M., Woehl B., Leung H., Groom J., Batten M., Harvey R.P., Martinez A.C., Mackay C.R., Mackay F. Disrupted cardiac development but normal hematopoiesis in mice deficient in the second CXCL12/SDF-1 receptor, CXCR7. Proc. Natl Acad. Sci. USA 2007, 104:14759-14764.
58. Naumann U., Cameroni E., Pruenster M., Mahabaleshwar H., Raz E., Zerwes H.G., Rot A., Thelen M. CXCR7 functions as a scavenger for CXCL12 and CXCL11. PLoS ONE 2010, 5:e9175.
59. Kryczek I., Lange A., Mottram P., Alvarez X., Cheng P., Hogan M., Moons L., Wei S., Zou L., Machelon V., Emilie D., Terrassa M., Lackner A., Curiel T.J., Carmeliet P., Zou W. CXCL12 and vascular endothelial growth factor synergistically induce neoangiogenesis in human ovarian cancers. Cancer Res. 2005, 65:465-472.
60. Grimm M.C., Ben-Baruch A., Taub D.D., Howard O.M., Resau J.H., Wang J.M., Ali H., Richardson R., Snyderman R., Oppenheim J.J. Opiates transdeactivate chemokine receptors: delta and mu opiate receptor-mediated heterologous desensitization. J. Exp. Med. 1998, 188:317-325.
61. Pello O.M., Martinez-Munoz L., Parrillas V., Serrano A., Rodriguez-Frade J.M., Toro M.J., Lucas P., Monterrubio M., Martinez A.C., Mellado M. Ligand stabilization of CXCR4/delta-opioid receptor heterodimers reveals a mechanism for immune response regulation. Eur. J. Immunol. 2008, 38:537-549.
62. Szabo I., Wetzel M.A., Zhang N., Steele A.D., Kaminsky D.E., Chen C., Liu-Chen L.Y., Bednar F., Henderson E.E., Howard O.M., Oppenheim J.J., Rogers T.J. Selective inactivation of CCR5 and decreased infectivity of R5 HIV-1 strains mediated by opioid-induced heterologous desensitization. J. Leukoc. Biol. 2003, 74:1074-1082.
63. Weber C. Far from the heart: receptor cross-talk in remote conditioning. Nat. Med. 2010, 16:760-762.
64. Braunersreuther V., Pellieux C., Pelli G., Burger F., Steffens S., Montessuit C., Weber C., Proudfoot A., Mach F., Arnaud C. Chemokine CCL5/RANTES inhibition reduces myocardial reperfusion injury in atherosclerotic mice. J. Mol. Cell. Cardiol. 2010, 48:789-798.
65. Liehn E.A., Merx M.W., Postea O., Becher S., Djalali-Talab Y., Shagdarsuren E., Kelm M., Zernecke A., Weber C. Ccr1 deficiency reduces inflammatory remodelling and preserves left ventricular function after myocardial infarction. J. Cell. Mol. Med. 2008, 12:496-506.
66. Koenen R.R., Weber C. Therapeutic targeting of chemokine interactions in atherosclerosis. Nat. Rev. Drug Discov. 2010, 9:141-153.
67. 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.
68. 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.
69. Szabo I., Chen X.H., Xin L., Adler M.W., Howard O.M., Oppenheim J.J., Rogers T.J. Heterologous desensitization of opioid receptors by chemokines inhibits chemotaxis and enhances the perception of pain. Proc. Natl Acad. Sci. USA 2002, 99:10276-10281.