Modulation of chemokine responses: Synergy and cooperativity

Frontiers in Immunology

Volumn 7, Issue MAY, 2016, Pages

  Proudfoot, Amanda E I ^a   Uguccioni, Mariagrazia ^b  

^a NOVIMMUNE SA   (Switzerland)

^b INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Switzerland)

Author keywords

Cell migration; Chemokines; Glycosaminoglycan; Oligomerization; Synergy

Indexed keywords

CHEMOKINE; CHEMOKINE RECEPTOR CCR7; CHEMOKINE RECEPTOR CXCR1; CHEMOKINE RECEPTOR CXCR4; CXCL3 CHEMOKINE; GLYCOSAMINOGLYCAN; PATHOGEN ASSOCIATED MOLECULAR PATTERN; SECONDARY LYMPHOID TISSUE CHEMOKINE; STROMAL CELL DERIVED FACTOR 1;

CELL MIGRATION ASSAY; COOPERATION; DRUG POTENTIATION; HEMATOPOIETIC CELL; HUMAN; INFLAMMATION; OLIGOMERIZATION; PERITONEAL CAVITY; SHORT SURVEY; TUMOR MICROENVIRONMENT;

EID: 84973582538     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2016.00183     Document Type: Short Survey

References (71)

1. Charo IF, Ransohoff RM. The many roles of chemokines and chemokine receptors in inflammation. N Engl J Med (2006) 354(6):610-21. doi:10.1056/NEJMra052723
2. 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):1-79. doi:10.1124/pr.113.007724
3. 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
4. Vacchini A, Locati M, Borroni EM. Overview and potential unifying themes of the atypical chemokine receptor family. J Leukoc Biol (2016). doi:10.1189/jlb.2MR1015-477R
5. Zlotnik A. Chemokines and cancer. Int J Cancer (2006) 119(9):2026-9. doi:10.1002/ijc.22024
6. Kiermaier E, Moussion C, Veldkamp CT, Gerardy-Schahn R, de Vries I, Williams LG, et al. Polysialylation controls dendritic cell trafficking by regulating chemokine recognition. Science (2016) 351(6269):186-90. doi:10.1126/science.aad0512
7. Hauser MA, Kindinger I, Laufer JM, Spate AK, Bucher D, Vanes SL, et al. Distinct CCR7 glycosylation pattern shapes receptor signaling and endocytosis to modulate chemotactic responses. J Leukoc Biol (2016). doi:10.1189/jlb.2VMA0915-432RR
8. Agace WW, Amara A, Roberts AI, Pablos JL, Thelen S, Uguccioni M, et al. Constitutive expression of stromal derived factor-1 by mucosal epithelia and its role in HIV transmission and propagation. Curr Biol (2000) 10(6):325-8. doi:10.1016/S0960-9822(00)00380-8
9. Manzo A, Paoletti S, Carulli M, Blades MC, Barone F, Yanni G, et al. Systematic microanatomical analysis of CXCL13 and CCL21 in situ production and progressive lymphoid organization in rheumatoid synovitis. Eur J Immunol (2005) 35(5):1347-59. doi:10.1002/eji.200425830
10. Mazzucchelli L, Blaser A, Kappeler A, Scharli P, Laissue JA, Baggiolini M, et al. BCA-1 is highly expressed in Helicobacter pylori-induced mucosa-associated lymphoid tissue and gastric lymphoma. J Clin Invest (1999) 104(10):R49-54. doi:10.1172/JCI7830
11. Smith JR, Braziel RM, Paoletti S, Lipp M, Uguccioni M, Rosenbaum JT. Expression of B-cell-attracting chemokine 1 (CXCL13) by malignant lymphocytes and vascular endothelium in primary central nervous system lymphoma. Blood (2003) 101(3):815-21. doi:10.1182/blood-2002-05-1576
12. Uguccioni M, Gionchetti P, Robbiani DF, Rizzello F, Peruzzo S, Campieri M, et al. Increased expression of IP-10, IL-8, MCP-1, and MCP-3 in ulcerative colitis. Am J Pathol (1999) 155(2):331-6. doi:10.1016/S0002-9440(10)65128-0
13. de Zeeuw D, Bekker P, Henkel E, Hasslacher C, Gouni-Berthold I, Mehling H, et al. The effect of CCR2 inhibitor CCX140-B on residual albuminuria in patients with type 2 diabetes and nephropathy: a randomised trial. Lancet Diabetes Endocrinol (2015) 3(9):687-96. doi:10.1016/S2213-8587(15)00261-2
14. Proudfoot AE, Power CA, Rommel C, Wells TN. Strategies for chemokine antagonists as therapeutics. Semin Immunol (2003) 15(1):57-65. doi:10.1016/S1044-5323(02)00128-8
15. Wells TN, Power CA, Shaw JP, Proudfoot AE. Chemokine blockers-therapeutics in the making? Trends Pharmacol Sci (2006) 27(1):41-7. doi:10.1016/j.tips.2005.11.001
16. Yokoyama W, Kohsaka H, Kaneko K, Walters M, Takayasu A, Fukuda S, et al. Abrogation of CC chemokine receptor 9 ameliorates collagen-induced arthritis of mice. Arthritis Res Ther (2014) 16(5):445. doi:10.1186/s13075-014-0445-9
17. Loos T, Dekeyzer L, Struyf S, Schutyser E, Gijsbers K, Gouwy M, et al. TLR ligands and cytokines induce CXCR3 ligands in endothelial cells: enhanced CXCL9 in autoimmune arthritis. Lab Invest (2006) 86(9):902-16. doi:10.1038/labinvest.3700453
18. Panzer U, Uguccioni M. Prostaglandin E2 modulates the functional responsiveness of human monocytes to chemokines. Eur J Immunol (2004) 34(12):3682-9. doi:10.1002/eji.200425226
19. Fulkerson PC, Zhu H, Williams DA, Zimmermann N, Rothenberg ME. CXCL9 inhibits eosinophil responses by a CCR3-and Rac2-dependent mechanism. Blood (2005) 106(2):436-43. doi:10.1182/blood-2005-02-0489
20. Fulkerson PC, Zimmermann N, Brandt EB, Muntel EE, Doepker MP, Kavanaugh JL, et al. Negative regulation of eosinophil recruitment to the lung by the chemokine monokine induced by IFN-gamma (Mig, CXCL9). Proc Natl Acad Sci U S A (2004) 101(7):1987-92. doi:10.1073/pnas.0308544100
21. Ogilvie P, Bardi G, Clark-Lewis I, Baggiolini M, Uguccioni M. Eotaxin is a natural antagonist for CCR2 and an agonist for CCR5. Blood (2001) 97(7):1920-4. doi:10.1182/blood.V97.7.1920
22. Ogilvie P, Paoletti S, Clark-Lewis I, Uguccioni M. Eotaxin-3 is a natural antagonist for CCR2 and exerts a repulsive effect on human monocytes. Blood (2003) 102(3):789-94. doi:10.1182/blood-2002-09-2773
23. Petkovic V, Moghini C, Paoletti S, Uguccioni M, Gerber B. Eotaxin-3/CCL26 is a natural antagonist for CC chemokine receptors 1 and 5. A human chemokine with a regulatory role. J Biol Chem (2004) 279(22):23357-63. doi:10.1074/jbc.M309283200
24. Petkovic V, Moghini C, Paoletti S, Uguccioni M, Gerber B. I-TAC/CXCL11 is a natural antagonist for CCR5. J Leukoc Biol (2004) 76(3):701-8. doi:10.1189/jlb.1103570
25. Gouwy M, Struyf S, Mahieu F, Put W, Proost P, Van Damme J. The unique property of the CC chemokine regakine-1 to synergize with other plasma-derived inflammatory mediators in neutrophil chemotaxis does not reside in its NH2-terminal structure. Mol Pharmacol (2002) 62(1):173-80. doi:10.1124/mol.62.1.173
26. Krug A, Uppaluri R, Facchetti F, Dorner BG, Sheehan KC, Schreiber RD, et al. IFN-producing cells respond to CXCR3 ligands in the presence of CXCL12 and secrete inflammatory chemokines upon activation. J Immunol (2002) 169(11):6079-83. doi:10.4049/jimmunol.169.11.6079
27. Vanbervliet B, Bendriss-Vermare N, Massacrier C, Homey B, de Bouteiller O, Briere F, et al. The inducible CXCR3 ligands control plasmacytoid dendritic cell responsiveness to the constitutive chemokine stromal cell-derived factor 1 (SDF-1)/CXCL12. J Exp Med (2003) 198(5):823-30. doi:10.1084/jem.20020437
28. Gouwy M, Struyf S, Berghmans N, Vanormelingen C, Schols D, Van Damme J. CXCR4 and CCR5 ligands cooperate in monocyte and lymphocyte migration and in inhibition of dual-tropic (R5/X4) HIV-1 infection. Eur J Immunol (2011) 41(4):963-73. doi:10.1002/eji.201041178
29. Gouwy M, Struyf S, Noppen S, Schutyser E, Springael JY, Parmentier M, et al. Synergy between coproduced CC and CXC chemokines in monocyte chemotaxis through receptor-mediated events. Mol Pharmacol (2008) 74(2):485-95. doi:10.1124/mol.108.045146
30. Mellado M, Rodriguez-Frade JM, Vila-Coro AJ, Fernandez S, Martin de AA, Jones DR, et al. Chemokine receptor homo-or heterodimerization activates distinct signaling pathways. EMBO J (2001) 20(10):2497-507. doi:10.1093/emboj/20.10.2497
31. Cecchinato V, D'Agostino G, Raeli L, Uguccioni M. Chemokine interaction with synergy-inducing molecules: fine tuning modulation of cell trafficking. J Leukoc Biol (2015). doi:10.1189/jlb.1MR1015-457R
32. Paoletti S, Petkovic V, Sebastiani S, Danelon MG, Uguccioni M, Gerber BO. A rich chemokine environment strongly enhances leukocyte migration and activities. Blood (2005) 105(9):3405-12. doi:10.1182/blood-2004-04-1648
33. Sebastiani S, Danelon G, Gerber B, Uguccioni M. CCL22-induced responses are powerfully enhanced by synergy inducing chemokines via CCR4: evidence for the involvement of first beta-strand of chemokine. Eur J Immunol (2005) 35(3):746-56. doi:10.1002/eji.200525800
34. Kuscher K, Danelon G, Paoletti S, Stefano L, Schiraldi M, Petkovic V, et al. Synergy-inducing chemokines enhance CCR2 ligand activities on monocytes. Eur J Immunol (2009) 39(4):1118-28. doi:10.1002/eji.200838906
35. Venetz D, Ponzoni M, Schiraldi M, Ferreri AJ, Bertoni F, Doglioni C, et al. Perivascular expression of CXCL9 and CXCL12 in primary central nervous system lymphoma: T-cell infiltration and positioning of malignant B cells. Int J Cancer (2010) 127(10):2300-12. doi:10.1002/ijc.25236
36. Gijsbers K, Gouwy M, Struyf S, Wuyts A, Proost P, Opdenakker G, et al. GCP-2/CXCL6 synergizes with other endothelial cell-derived chemokines in neutrophil mobilization and is associated with angiogenesis in gastrointestinal tumors. Exp Cell Res (2005) 303(2):331-42. doi:10.1016/j.yexcr.2004.09.027
37. Gouwy M, Schiraldi M, Struyf S, Van Damme J, Uguccioni M. Possible mechanisms involved in chemokine synergy fine tuning the inflammatory response. Immunol Lett (2012) 145(1-2):10-4. doi:10.1016/j.imlet.2012.04.005
38. Koenen RR, von Hundelshausen P, Nesmelova IV, Zernecke A, Liehn EA, Sarabi A, et al. Disrupting functional interactions between platelet chemokines inhibits atherosclerosis in hyperlipidemic mice. Nat Med (2009) 15(1):97-103. doi:10.1038/nm.1898
39. von Hundelshausen P, Koenen RR, Sack M, Mause SF, Adriaens W, Proudfoot AE, et al. Heterophilic interactions of platelet factor 4 and RANTES promote monocyte arrest on endothelium. Blood (2005) 105(3):924-30. doi:10.1182/blood-2004-06-2475
40. Weber C, Koenen RR. Fine-tuning leukocyte responses: towards a chemokine 'interactome'. Trends Immunol (2006) 27(6):268-73. doi:10.1016/j.it.2006.04.002
41. Hamel DJ, Sielaff I, Proudfoot AE, Handel TM. Chapter 4. Interactions of chemokines with glycosaminoglycans. Methods Enzymol (2009) 461:71-102. doi:10.1016/S0076-6879(09)05404-4
42. Kuschert GSV, Coulin F, Power CA, Proudfoot AEI, Hubbard RE, Hoogewerf AJ, et al. Glycosaminoglycans interact selectively with chemokines and modulate receptor binding and cellular responses. Biochemistry (1999) 38(39):12959-68. doi:10.1021/bi990711d
43. Rot A. Neutrophil attractant/activation protein-1 (interleukin-8) induces in vitro neutrophil migration by haptotactic mechanism. Eur J Immunol (1993) 23:303-6. doi:10.1002/eji.1830230150
44. Proudfoot AE, Handel TM, Johnson Z, Lau EK, LiWang P, Clark-Lewis I, et al. Glycosaminoglycan binding and oligomerization are essential for the in vivo activity of certain chemokines. Proc Natl Acad Sci U S A (2003) 100(4):1885-90. doi:10.1073/pnas.0334864100
45. Gangavarapu P, Rajagopalan L, Kolli D, Guerrero-Plata A, Garofalo RP, Rajarathnam K. The monomer-dimer equilibrium and glycosaminoglycan interactions of chemokine CXCL8 regulate tissue-specific neutrophil recruitment. J Leukoc Biol (2012) 91(2):259-65. doi:10.1189/jlb.0511239
46. Tanino Y, Coombe DR, Gill SE, Kett WC, Kajikawa O, Proudfoot AE, et al. Kinetics of chemokine-glycosaminoglycan interactions control neutrophil migration into the airspaces of the lungs. J Immunol (2010) 184(5):2677-85. doi:10.4049/jimmunol.0903274
47. Verkaar F, van OJ, van der Lee MM, van Lith LH, Watts AO, Rops AL, et al. Chemokine cooperativity is caused by competitive glycosaminoglycan binding. J Immunol (2014) 192(8):3908-14. doi:10.4049/jimmunol.1302159
48. Islam SA, Ling MF, Leung J, Shreffler WG, Luster AD. Identification of human CCR8 as a CCL18 receptor. J Exp Med (2013) 210(10):1889-98. doi:10.1084/jem.20130240
49. Krohn SC, Bonvin P, Proudfoot AE. CCL18 exhibits a regulatory role through inhibition of receptor and glycosaminoglycan binding. PLoS One (2013) 8(8):e72321. doi:10.1371/journal.pone.0072321
50. Adage T, Konya V, Weber C, Strutzmann E, Fuchs T, Zankl C, et al. Targeting glycosaminoglycans in the lung by an engineered CXCL8 as a novel therapeutic approach to lung inflammation. Eur J Pharmacol (2015) 748:83-92. doi:10.1016/j.ejphar.2014.12.019
51. Campanella GS, Grimm J, Manice LA, Colvin RA, Medoff BD, Wojtkiewicz GR, et al. Oligomerization of CXCL10 is necessary for endothelial cell presentation and in vivo activity. J Immunol (2006) 177(10):6991-8. doi:10.4049/jimmunol.177.10.6991
52. Das ST, Rajagopalan L, Guerrero-Plata A, Sai J, Richmond A, Garofalo RP, et al. Monomeric and dimeric CXCL8 are both essential for in vivo neutrophil recruitment. PLoS One (2010) 5(7):e11754. doi:10.1371/journal.pone.0011754
53. Rajarathnam K, Sykes BD, Kay CM, Dewald B, Geiser T, Baggiolini M, et al. Neutrophil activation by monomeric interleukin-8. Science (1994) 264(5155):90-2. doi:10.1126/science.8140420
54. Dyer DP, Salanga CL, Volkman BF, Kawamura T, Handel TM. The dependence of chemokine-glycosaminoglycan interactions on chemokine oligomerization. Glycobiology (2016) 26(3):312-26. doi:10.1093/glycob/cwv100
55. Joseph PR, Mosier PD, Desai UR, Rajarathnam K. Solution NMR characterization of chemokine CXCL8/IL-8 monomer and dimer binding to glycosaminoglycans: structural plasticity mediates differential binding interactions. Biochem J (2015) 472(1):121-33. doi:10.1042/BJ20150059
56. Hoogewerf AJ, Kuschert GSV, Proudfoot AEI, Borlat F, Clark-Lewis I, Power CA, et al. Glycosaminoglycans mediate cell surface oligomerization of chemokines. Biochemistry (1997) 36:13570-8. doi:10.1021/bi971125s
57. Monneau Y, Arenzana-Seisdedos F, Lortat-Jacob H. The sweet spot: how GAGs help chemokines guide migrating cells. J Leukoc Biol (2015). doi:10.1189/jlb.3MR0915-440R
58. Tarbell JM, Cancel LM. The glycocalyx and its significance in human medicine. J Intern Med (2016). doi:10.1111/joim.12465
59. Taylor KR, Gallo RL. Glycosaminoglycans and their proteoglycans: host-associated molecular patterns for initiation and modulation of inflammation. FASEB J (2006) 20(1):9-22. doi:10.1096/fj.05-4682rev
60. Johnson Z, Schwarz M, Power CA, Wells TN, Proudfoot AE. Multi-faceted strategies to combat disease by interference with the chemokine system. Trends Immunol (2005) 26(5):268-74. doi:10.1016/j.it.2005.03.001
61. Springael JY, Urizar E, Parmentier M. Dimerization of chemokine receptors and its functional consequences. Cytokine Growth Factor Rev (2005) 16(6):611-23. doi:10.1016/j.cytogfr.2005.05.005
62. Thelen M, Munoz LM, Rodriguez-Frade JM, Mellado M. Chemokine receptor oligomerization: functional considerations. Curr Opin Pharmacol (2010) 10(1):38-43. doi:10.1016/j.coph.2009.09.004
63. Corbisier J, Gales C, Huszagh A, Parmentier M, Springael JY. Biased signaling at chemokine receptors. J Biol Chem (2015) 290(15):9542-54. doi:10.1074/jbc.M114.596098
64. Back M, Weber C, Lutgens E. Regulation of atherosclerotic plaque inflammation. J Intern Med (2015) 278(5):462-82. doi:10.1111/joim.12367
65. Alard JE, Ortega-Gomez A, Wichapong K, Bongiovanni D, Horckmans M, Megens RT, et al. Recruitment of classical monocytes can be inhibited by disturbing heteromers of neutrophil HNP1 and platelet CCL5. Sci Transl Med (2015) 7(317):317ra196. doi:10.1126/scitranslmed.aad5330
66. Schiraldi M, Raucci A, Munoz LM, Livoti E, Celona B, Venereau E, et al. HMGB1 promotes recruitment of inflammatory cells to damaged tissues by forming a complex with CXCL12 and signaling via CXCR4. J Exp Med (2012) 209(3):551-63. doi:10.1084/jem.20111739
67. Venereau E, Casalgrandi M, Schiraldi M, Antoine DJ, Cattaneo A, De Marchis F, et al. Mutually exclusive redox forms of HMGB1 promote cell recruitment or proinflammatory cytokine release. J Exp Med (2012) 209(9):1519-28. doi:10.1084/jem.20120189
68. Venereau E, Schiraldi M, Uguccioni M, Bianchi ME. HMGB1 and leukocyte migration during trauma and sterile inflammation. Mol Immunol (2013) 55(1):76-82. doi:10.1016/j.molimm.2012.10.037
69. Ortega-Gomez A, Perretti M, Soehnlein O. Resolution of inflammation: an integrated view. EMBO Mol Med (2013) 5(5):661-74. doi:10.1002/emmm.201202382
70. Campana L, Bosurgi L, Bianchi ME, Manfredi AA, Rovere-Querini P. Requirement of HMGB1 for stromal cell-derived factor-1/CXCL12-dependent migration of macrophages and dendritic cells. J Leukoc Biol (2009) 86(3):609-15. doi:10.1189/jlb.0908576
71. Solari R, Pease JE, Begg M. Chemokine receptors as therapeutic targets: why aren't there more drugs? Eur J Pharmacol (2015) 746:363-7. doi:10.1016/j.ejphar.2014.06.060