The activity of CCL18 is principally mediated through interaction with glycosaminoglycans

Frontiers in Immunology

Volumn 4, Issue JUL, 2013, Pages

  Krohn, Sonja ^a   Garin, Alexandre ^a   Gabay, Cem ^b,c   Proudfoot, Amanda E I ^a  

^a MERCK SERONO S A   (Switzerland)

^b GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^c UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

Author keywords

BBXB motif; CCL18; Chemokines; Evasin; Glycosaminoglycan; Synovial fluid

Indexed keywords

BINDING PROTEIN; CC CHEMOKINE LIGAND 18; CHEMOKINE; CHEMOKINE RECEPTOR CCR3; EVASIN 1; EVASIN 4; GLYCOSAMINOGLYCAN; HEPARIN; IODINE 125; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ARTICLE; B LYMPHOCYTE; BINDING ASSAY; BREAST CANCER; CD8+ T LYMPHOCYTE; CELL DENSITY; CELL PROLIFERATION ASSAY; CHEMOTAXIS ASSAY; CONTROLLED STUDY; EOSINOPHIL; FLOW CYTOMETRY; GEL PERMEATION CHROMATOGRAPHY; HUMAN; HUMAN CELL; LEUKOCYTE; POLYMERASE CHAIN REACTION; PROTEIN ANALYSIS; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; SIGNAL TRANSDUCTION; SURFACE ENHANCED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; T LYMPHOCYTE;

EID: 84883665201     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2013.00193     Document Type: Article

References (50)

1. Takahama Y. Journey through the thymus: stromal guides for T-cell development and selection. Nat Rev Immunol (2006) 6:127-35. doi:10.1038/nri1781
2. Murooka TT, Wong MM, Rahbar R, Majchrzak-Kita B, Proudfoot AE, Fish EN. CCL5-CCR5-mediated apoptosis in T cells: requirement for glycosaminoglycan binding and CCL5 aggregation. J Biol Chem (2006) 281:25184-94. doi:10.1074/jbc. M603912200
3. Zou YR, Kottmann AH, Kuroda M, Taniuchi I, Littman DR. Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature (1998) 393:595-9. doi:10.1038/31269
4. Strieter RM, Polverini PJ, Kunkel SL, Arenberg DA, Burdick MD, Kasper J, et al. The functional role of the ELR motif in CXC chemokine-mediated angiogenesis. J Biol Chem (1995) 270:27348-57. doi:10.1074/jbc.270.45.27348
5. O'Hayre M, Salanga CL, Handel TM, Allen SJ. Chemokines and cancer: migration, intracellular signalling and intercellular communication in the microenvironment. Biochem J (2008) 409:635-49. doi:10.1042/BJ20071493
6. Zlotnik A. Chemokines and cancer. Int J Cancer (2006) 119:2026-9. doi:10.1002/ijc.22024
7. Nibbs RJ, Salcedo TW, Campbell JD, Yao XT, Li Y, Nardelli B, et al. C-C chemokine receptor 3 antagonism by the beta-chemokine macrophage inflammatory protein 4, a property strongly enhanced by an amino-terminal alanine-methionine swap. J Immunol (2000) 164:1488-97.
8. Chen J, Yao Y, Gong C, Yu F, Su S, Chen J, et al. CCL18 from tumor-associated macrophages promotes breast cancer metastasis via PITPNM3. Cancer Cell (2011) 19:541-55. doi:10.1016/j.ccr.2011.02.006
9. Lev S, Hernandez J, Martinez R, Chen A, Plowman G, Schlessinger J. Identification of a novel family of targets of PYK2 related to Drosophila retinal degeneration B (rdgB) protein. Mol. Cell Biol. (1999) 19:2278-88.
10. Adema GJ, Hartgers F, Verstraten R, de Vries E, Marland G, Menon S, et al. A dendritic-cell-derived C-C chemokine that preferentially attracts naive T cells. Nature (1997) 387:713-7. doi:10.1038/42716
11. Hieshima K, Imai T, Baba M, Shoudai K, Ishizuka K, Nakagawa T, et al. A novel human CC chemokine PARC that is most homologous to macrophageinflammatory protein-1 alpha/LD78 alpha and chemotactic for T lymphocytes, but not for monocytes. J Immunol (1997) 159:1140-9.
12. Schutyser E, Struyf S, Proost P, Opdenakker G, Laureys G, Verhasselt B, et al. Identification of biologically active chemokine isoforms from ascitic fluid and elevated levels of CCL18/pulmonary and activation-regulated chemokine in ovarian carcinoma. J Biol Chem (2002) 277:24584-93. doi:10.1074/jbc. M112275200
13. Lindhout E, Vissers JL, Hartgers FC, Huijbens RJ, Scharenborg NM, Figdor CG, et al. The dendritic cell-specific CC-chemokine DC-CK1 is expressed by germinal center dendritic cells and attracts CD38-negative mantle zone B lymphocytes. J Immunol (2001) 166:3284-9.
14. Mortier A, Van Damme J, Proost P. Regulation of chemokine activity by posttranslational modification. Pharmacol Ther (2008) 120:197-217. doi:10.1016/j.pharmthera.2008.08.006
15. Berahovich RD, Miao Z, Wang Y, Premack B, Howard MC, Schall TJ. Proteolytic activation of alternative CCR1 ligands in inflammation. J Immunol (2005) 174:7341-51.
16. Schutyser E, Struyf S, Wuyts A, Put W, Geboes K, Grillet B, et al. Selective induction of CCL18/PARC by staphylococcal enterotoxins in mononuclear cells and enhanced levels in septic and rheumatoid arthritis. Eur J Immunol (2001) 31:3755-62. doi:10.1002/1521-4141(200112)31:12L<3755::AID-IMMU3755>3.0.CO;2-O
17. Proudfoot AEI, Borlat F. Purification of recombinant chemokines from E. coli. Methods Mol Biol (2000) 138:75-87.
18. Deruaz M, Frauenschuh A, Alessandri AL, Dias JM, Coelho FM, Russo RC, et al. Ticks produce highly selective chemokine binding proteins with antiinflammatory activity. J Exp Med (2008) 205:2019-31. doi:10.1084/jem.20072689
19. Frauenschuh A, Power CA, Deruaz M, Ferreira BR, Silva JS, Teixeira MM, et al. Molecular cloning and characterization of a highly selective chemokine-binding protein from the tick Rhipicephalus sanguineus. J Biol Chem (2007) 282:27250-8. doi:10.1074/jbc. M704706200
20. Severin IC, Gaudry JP, Johnson Z, Kungl A, Jansma A, Gesslbauer B, et al. Characterization of the chemokine CXCL11-heparin interaction suggests two different affinities for glycosaminoglycans. J Biol Chem (2010) 285:17713-24. doi:10.1074/jbc. M109.082552
21. Severin IC, Souza AL, Davis JH, Musolino N, Mack M, Power CA, et al. Properties of 7ND-CCL2 are modulated upon fusion to Fc. Protein Eng Des Sel (2012) 25:213-22. doi:10.1093/protein/gzs008
22. Zimmermann N, Conkright JJ, Rothenberg ME. CC chemokine receptor-3 undergoes prolonged ligand-induced internalization. J Biol Chem (1999) 274:12611-8. doi:10.1074/jbc.274.18.12611
23. Trickett A, Kwan YL. T cell stimulation and expansion using anti-CD3/CD28 beads. J Immunol Methods (2003) 275:251-5. doi:10.1016/S0022-1759(03)00010-3
24. Favre-Kontula L, Sattonnet-Roche P, Magnenat E, Proudfoot AE, Boschert U, Xenarios I, et al. Detection and identification of plasma proteins that bind Glial- CAM using ProteinChip arrays, SELDI-TOF MS, and nano-LC MS/MS. Proteomics (2008) 8:378-88. doi:10.1002/pmic.200700564
25. Schraufstatter I, Takamori H, Sikora L, Sriramarao P, Discipio RG. Eosinophils and monocytes produce pulmonary and activation-regulated chemokine, which activates cultured monocytes/macrophages. Am J Physiol Lung Cell Mol Physiol (2004) 286:L494-501. doi:10.1152/ajplung.00323.2002
26. Ganju RK, Brubaker SA, Meyer J, Dutt P, Yang Y, Qin S, et al. The alpha-chemokine, stromal cell-derived factor-1alpha, binds to the transmembrane G-proteincoupled CXCR-4 receptor and activates multiple signal transduction pathways. J Biol Chem (1998) 273:23169-75. doi:10.1074/jbc.273.36.23169
27. 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) 74:485-95. doi:10.1124/mol.108.045146
28. Déruaz M, Bonvin P, Severin I, Johnson Z, Krohn S, Power C, et al. A tick-derived chemokine binding protein with broad selectivity can be modified for therapeutic use in pre-clinical studies. FEBS (in press).
29. Krohn SC, Bonvin P, Proudfoot AEI. CCL18 exhibits a regulatory role through inhibition of receptor and glycosaminoglycan binding. PLoS ONE (in press).
30. Capila I, Linhardt RJ. Heparin-protein interactions. Angew Chem Int Ed Engl (2002) 41:391-412. doi:10.1002/1521-3773(20020201)41:3<390::AIDANIE390> 3.0.CO;2-B
31. Graham GJ, Wilkinson PC, Nibbs RJ, Lowe S, Kolset SO, Parker A, et al. Uncoupling of stem cell inhibition from monocyte chemoattraction in MIP-1alpha by mutagenesis of the proteoglycan binding site. EMBO J (1996) 15:6506-15.
32. Koopmann W, Krangel MS. Identification of a glycosaminoglycan-binding site in chemokine macrophage inflammatory protein-1alpha. J Biol Chem (1997) 272:10103-9. doi:10.1074/jbc.272.15.10103
33. Koopmann W, Ediriwickrema C, Krangel MS. Structure and function of the glycosaminoglycan binding site of chemokine macrophage-inflammatory protein-1 beta. J Immunol (1999) 163:2120-7.
34. Martin L, Blanpain C, Garnier P, Wittamer V, Parmentier M, Vita C. Structural and functional analysis of the RANTES-glycosaminoglycans interactions. Biochemistry (2001) 40:6303-18. doi:10.1021/bi002670n
35. Proudfoot AEI, Fritchley S, Borlat F, Shaw JP, Vilbois F, Zwahlen C, et al. The BBXB motif of RANTES is the principal site for heparin binding and controls receptor selectivity. J Biol Chem (2001) 276:10620-6. doi:10.1074/jbc. M010867200
36. Kuschert GS, Coulin F, Power CA, Proudfoot AE, Hubbard RE, Hoogewerf AJ, et al. Glycosaminoglycans interact selectively with chemokines and modulate receptor binding and cellular responses. Biochemistry (1999) 38:12959-68. doi:10.1021/bi990711d
37. Tasaki Y, Fukuda S, Iio M, Miura R, Imai T, Sugano S, et al. Chemokine PARC gene (SCYA18) generated by fusion of two MIP-1alpha/LD78alpha-like genes. Genomics (1999) 55:353-7. doi:10.1006/geno.1998.5670
38. de Nadai P, Charbonnier AS, Chenivesse C, Senechal S, Fournier C, Gilet J, et al. Involvement of CCL18 in allergic asthma. J Immunol (2006) 176:6286-93.
39. Gunther C, Bello-Fernandez C, Kopp T, Kund J, Carballido-Perrig N, Hinteregger S, et al. CCL18 is expressed in atopic dermatitis and mediates skin homing of human memory T cells. J Immunol (2005) 174:1723-8.
40. Chang Y, de Nadai P, Azzaoui I, Morales O, Delhem N, Vorng H, et al. The chemokine CCL18 generates adaptive regulatory T cells from memory CD4+ T cells of healthy but not allergic subjects. FASEB J (2010) 24:5063-72. doi:10.1096/fj.10-162560
41. Azzaoui I, Yahia SA, Chang Y, Vorng H, Morales O, Fan Y, et al. CCL18 differentiates dendritic cells in tolerogenic cells able to prime regulatory T cells in healthy subjects. Blood (2011) 118:3549-58. doi:10.1182/blood-2011-02-338780
42. Jiang Y, Valente AJ, Williamson MJ, Zhang L, Graves DT. Post-translational modification of a monocyte-specific chemoattractant synthesized by glioma, osteosarcoma, and vascular smooth muscle cells. J Biol Chem (1990) 265:18318-21.
43. Jiang Y, Tabak LA, Valente AJ, Graves DT. Initial characterization of the carbohydrate structure of MCP-1. Biochem Biophys Res Commun (1991) 178:1400-4. doi:10.1016/0006-291X(91)91049-I
44. Proost P, Loos T, Mortier A, Schutyser E, Gouwy M, Noppen S, et al. Citrullination of CXCL8 by peptidylarginine deiminase alters receptor usage, prevents proteolysis, and dampens tissue inflammation. J Exp Med (2008) 205:2085-97. doi:10.1084/jem.20080305
45. Loos T, Mortier A, Gouwy M, Ronsse I, Put W, Lenaerts JP, et al. Citrullination of CXCL10 and CXCL11 by peptidylarginine deiminase: a naturally occurring posttranslational modification of chemokines
46. Molon B, Ugel S, Del Pozzo F, Soldani C, Zilio S, Avella D, et al. Chemokine nitration prevents intratumoral infiltration of antigen-specific T cells. J Exp Med (2011) 208:1949-62. doi:10.1084/jem.20101956
47. Atamas SP, Luzina IG, Choi J, Tsymbalyuk N, Carbonetti NH, Singh IS, et al. Pulmonary and activation-regulated chemokine stimulates collagen production in lung fibroblasts. Am J Respir Cell Mol Biol (2003) 29:743-9. doi:10.1165/rcmb.2003-0078OC
48. Schraufstatter IU, Zhao M, Khaldoyanidi SK, Discipio RG. The chemokine CCL18 causes maturation of cultured monocytes to macrophages in the M2 spectrum. Immunology (2012) 135:287-98. doi:10.1111/j.1365-2567.2011.03541.x
49. Taub DD, Turcovski-Corrales SM, Key ML, Longo DL, Murphy WJ. Chemokines and T lymphocyte activation. I. Beta chemokines costimulate human T lymphocyte activation in vitro. J Immunol (1996) 156:2095-103.
50. Dantas-Torres F, Figueredo LA, Brandao-Filho SP. Rhipicephalus sanguineus (Acari: Ixodidae), the brown dog tick, parasitizing humans in Brazil. Rev Soc Bras Med Trop (2006) 39:64-7. doi:10.1590/S0037-86822006000100012