The role of chemokines in shaping the balance between CD4+ T cell subsets and its therapeutic implications in autoimmune and cancer diseases

Frontiers in Immunology

Volumn 6, Issue NOV, 2015, Pages

  Karin, Nathan ^a   Wildbaum, Gizi ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

Cancer; Chemokines; CXCL10; CXCL11; CXCR3; EAE; Immunotherapy; T cell subsets

Indexed keywords

CELL ADHESION MOLECULE; CHEMOATTRACTANT; CHEMOKINE RECEPTOR CXCR3; CHEMOKINE RECEPTOR CXCR4; CXCL11 CHEMOKINE; CXCL9 CHEMOKINE; FORKHEAD TRANSCRIPTION FACTOR; FORKHEAD TRANSCRIPTION FACTOR 3; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 17; INTERLEUKIN 1BETA; IPILIMUMAB; NIVOLUMAB; PROGRAMMED DEATH 1 RECEPTOR; STROMAL CELL DERIVED FACTOR 1; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ALLERGIC ENCEPHALOMYELITIS; AUTOIMMUNE DISEASE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL FUNCTION; CELL MIGRATION; CELL PLASTICITY; CELL POLARIZATION; CLINICAL ASSESSMENT; GRAFT VERSUS HOST REACTION; HUMAN; INFLAMMATION; MYELOMA; NEOPLASM; NONHUMAN; PLASTICITY; REGULATORY T LYMPHOCYTE; SHORT SURVEY; TH1 TH2 BALANCE; TUMOR IMMUNITY;

EID: 84949556667     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2015.00609     Document Type: Short Survey

References (83)

1. Luster AD. Chemokines-chemotactic cytokines that mediate inflammation. N Engl J Med (1998) 338:436-45. doi: 10.1056/NEJM199802123380706.
2. Zlotnic A, Yoshei O. Chemokines: a new classification system and their role in immunity. Immunity (2000) 12:121-7. doi:10.1016/S1074-7613(00)80165-X.
3. Proudfoot AE. Chemokine receptors: multifaceted therapeutic targets. Nat Rev Immunol (2002) 2:106-15. doi:10.1038/nri722.
4. Stoolman LM. Adhesion molecules controlling lymphocyte migration. Cell (1989) 56:907-10. doi:10.1016/0092-8674(89)90620-X.
5. Elices MJ, Osborn L, Takada Y, Crouse C, Luhowskyj S, Hemler ME, et al. VCAM-1 on activated endothelium interacts with the leukocyte integrin VLA-4 at a site distinct from the VLA-4/fibronectin binding site. Cell (1990) 60:577-84. doi:10.1016/0092-8674(90)90661-W.
6. Osborn L. Leukocyte adhesion to endothelium in inflammation. Cell (1990) 62:3-6. doi:10.1016/0092-8674(90)90230-C.
7. Springer TA. Adhesion receptors of the immune system. Nature (1990) 346:425-34. doi:10.1038/346425a0.
8. Spertini O, Kansas GS, Munro JM, Griffin JD, Tedder TF. Regulation of leukocyte migration by activation of the leukocyte adhesion molecule-1 (LAM-1) selectin. Nature (1991) 349:691-4. doi:10.1038/349691a0.
9. Salomon I, Netzer N, Wildbaum G, Schif-Zuck S, Maor G, Karin N. Targeting the function of IFN-gamma-inducible protein 10 suppresses ongoing adjuvant arthritis. J Immunol (2002) 169:2685-93. doi:10.4049/jimmunol.169.5.2685.
10. Wildbaum G, Netzer N, Karin N. Plasmid DNA encoding IFN-gamma-inducible protein 10 redirects antigen-specific T cell polarization and suppresses experimental autoimmune encephalomyelitis. J Immunol (2002) 168:5885-92. doi:10.4049/jimmunol.168.11.5885.
11. Zohar Y, Wildbaum G, Novak R, Salzman AL, Thelen M, Alon R, et al. CXCL11-dependent induction of FOXP3-negative regulatory T cells suppresses autoimmune encephalomyelitis. J Clin Invest (2014) 124:2009-22. doi:10.1172/JCI71951.
12. Meiron M, Zohar Y, Anunu R, Wildbaum G, Karin N. CXCL12 (SDF-1alpha) suppresses ongoing experimental autoimmune encephalomyelitis by selecting antigen-specific regulatory T cells. J Exp Med (2008) 205:2643-55. doi:10.1084/jem.20080730.
13. Arend WP, Dayer JM. Inhibition of the production and effects of interleukin-1 and tumor necrosis factor alpha in rheumatoid arthritis. Arthritis Rheum (1995) 38:151-60. doi:10.1002/art.1780380202.
14. Feldmann M, Brennan FM, Foxwell BM, Maini RN. The role of TNF alpha and IL-1 in rheumatoid arthritis. Curr Dir Autoimmun (2001) 3:188-99. doi:10.1159/000060522.
15. Dayer JM, Krane SM. Anti-TNF-alpha therapy for ankylosing spondylitis-a specific or nonspecific treatment? N Engl J Med (2002) 346:1399-400. doi:10.1056/NEJM200205023461811.
16. Ogata H, Hibi T. Cytokine and anti-cytokine therapies for inflammatory bowel disease. Curr Pharm Des (2003) 9:1107-13. doi:10.2174/1381612033455035.
17. Mosmann TR, Cherwinski H, Bond MW, Giedlin MA, Coffman RL. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J Immunol (1986) 136:2348-57.
18. Stevens TL, Bossie A, Sanders VM, Fernandez-Botran R, Coffman RL, Mosmann TR, et al. Regulation of antibody isotype secretion by subsets of antigen-specific helper T cells. Nature (1988) 334:255-8. doi:10.1038/334255a0.
19. Mosmann TR, Coffman RL. Th1 and Th2 cells: different patterns of lymphokine secretion lead to different functional properties. Annu Rev Immunol (1989) 9:145-73. doi:10.1146/annurev.iy.07.040189.001045.
20. Zheng W, Flavell RA. The transcription factor GATA-3 is necessary and sufficient for Th2 cytokine gene expression in CD4 T cells. Cell (1997) 89:587-96. doi:10.1016/S0092-8674(00)80240-8.
21. Leonard JP, Waldburger KE, Goldman SJ. Prevention of experimental autoimmune encephalomyelitis by antibodies against interleukin 12. J Exp Med (1995) 181:381-6. doi:10.1084/jem.181.1.381.
22. Okamura H, Tsutsi H, Komatsu T, Yutsudo M, Hakura A, Tanimoto T, et al. Cloning of a new cytokine that induces IFN-gamma production by T cells. Nature (1995) 378:88-91. doi:10.1038/378088a0.
23. Wildbaum G, Youssef S, Grabie N, Karin N. Neutralizing antibodies to IFN-gamma-inducing factor prevent experimental autoimmune encephalomyelitis. J Immunol (1998) 161:6368-74.
24. Novick D, Kim SH, Fantuzzi G, Reznikov LL, Dinarello CA, Rubinstein M. Interleukin-18 binding protein: a novel modulator of the Th1 cytokine response. Immunity (1999) 10:127-36. doi:10.1016/S1074-7613(00)80013-8.
25. Schif-Zuck S, Westermann J, Netzer N, Zohar Y, Meiron M, Wildbaum G, et al. Targeted overexpression of IL-18 binding protein at the central nervous system overrides flexibility in functional polarization of antigen-specific Th2 cells. J Immunol (2005) 174:4307-15. doi:10.4049/jimmunol.174.7.4307.
26. Abbas AK, Murphy KM, Sher A. Functional diversity of helper T lymphocytes. Nature (1996) 383:787-93. doi:10.1038/383787a0.
27. Pedotti R, Mitchell D, Wedemeyer J, Karpuj M, Chabas D, Hattab EM, et al. An unexpected version of horror autotoxicus: anaphylactic shock to a self-peptide. Nat Immunol (2001) 2:216-22. doi:10.1038/85266.
28. Harrington LE, Hatton RD, Mangan PR, Turner H, Murphy TL, Murphy KM, et al. Interleukin 17-producing CD4(+) effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol (2005) 6(11):1123-32. doi:10.1038/ni1254.
29. Bettelli E, Korn T, Oukka M, Kuchroo VK. Induction and effector functions of T(H)17 cells. Nature (2008) 453:1051-7. doi:10.1038/nature07036.
30. Acosta-Rodriguez EV, Napolitani G, Lanzavecchia A, Sallusto F. Interleukins 1beta and 6 but not transforming growth factor-beta are essential for the differentiation of interleukin 17-producing human T helper cells. Nat Immunol (2007) 8:942-9. doi:10.1038/ni1496.
31. Chalmin F, Mignot G, Bruchard M, Chevriaux A, Vegran F, Hichami A, et al. Stat3 and Gfi-1 transcription factors control Th17 cell immunosuppressive activity via the regulation of ectonucleotidase expression. Immunity (2012) 36:362-73. doi:10.1016/j.immuni.2011.12.019.
32. Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science (2003) 299:1057-61. doi:10.1126/science.1079490.
33. Sakaguchi S. Naturally arising Foxp3-expressing CD25+CD4+ regulatory T cells in immunological tolerance to self and non-self. Nat Immunol (2005) 6:345-52. doi:10.1038/ni1178.
34. Sakaguchi S, Ono M, Setoguchi R, Yagi H, Hori S, Fehervari Z, et al. Foxp3+ CD25+ CD4+ natural regulatory T cells in dominant self-tolerance and autoimmune disease. Immunol Rev (2006) 212:8-27. doi:10.1111/j.0105-2896.2006.00427.x.
35. Shevach EM. Mechanisms of foxp3+ T regulatory cell-mediated suppression. Immunity (2009) 30:636-45. doi:10.1016/j.immuni.2009.04.010.
36. Wing K, Sakaguchi S. Regulatory T cells exert checks and balances on self tolerance and autoimmunity. Nat Immunol (2009) 11:7-13. doi:10.1038/ni.1818.
37. Chen W, Jin W, Hardegen N, Lei KJ, Li L, Marinos N, et al. Conversion of peripheral CD4+CD25-naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med (2003) 198:1875-86. doi:10.1084/jem.20030152.
38. Groux H, O'Garra A, Bigler M, Rouleau M, Antonenko S, De Vries JE, et al. A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature (1997) 389:737-42. doi:10.1038/39614.
39. Roncarolo MG, Gregori S, Battaglia M, Bacchetta R, Fleischhauer K, Levings MK. Interleukin-10-secreting type 1 regulatory T cells in rodents and humans. Immunol Rev (2006) 212:28-50. doi:10.1111/j.0105-2896.2006.00420.x.
40. Battaglia M, Stabilini A, Draghici E, Gregori S, Mocchetti C, Bonifacio E, et al. Rapamycin and interleukin-10 treatment induces T regulatory type 1 cells that mediate antigen-specific transplantation tolerance. Diabetes (2006) 55:40-9. doi:10.2337/diabetes.55.01.06.db05-0613.
41. Gagliani N, Magnani CF, Huber S, Gianolini ME, Pala M, Licona-Limon P, et al. Coexpression of CD49b and LAG-3 identifies human and mouse T regulatory type 1 cells. Nat Med (2013) 19:739-46. doi:10.1038/nm.3179.
42. Anderson CF, Oukka M, Kuchroo VJ, Sacks D. CD4(+)CD25(-)Foxp3(-) Th1 cells are the source of IL-10-mediated immune suppression in chronic cutaneous leishmaniasis. J Exp Med (2007) 204:285-97. doi:10.1084/jem.20061886.
43. Apetoh L, Quintana FJ, Pot C, Joller N, Xiao S, Kumar D, et al. The aryl hydrocarbon receptor interacts with c-Maf to promote the differentiation of type 1 regulatory T cells induced by IL-27. Nat Immunol (2010) 11:854-61. doi:10.1038/ni.1912.
44. Sun J, Dodd H, Moser EK, Sharma R, Braciale TJ. CD4+ T cell help and innate-derived IL-27 induce Blimp-1-dependent IL-10 production by antiviral CTLs. Nat Immunol (2011) 12:327-34. doi:10.1038/ni.1996.
45. Zhou L, Chong MM, Littman DR. Plasticity of CD4+ T cell lineage differentiation. Immunity (2009) 30:646-55. doi:10.1016/j.immuni.2009.05.001.
46. Joller N, Kuchroo VK. Good guys gone bad: exTreg cells promote autoimmune arthritis. Nat Med (2014) 20:15-7. doi:10.1038/nm.3439.
47. 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.
48. Blattermann S, Peters L, Ottersbach PA, Bock A, Konya V, Weaver CD, et al. A biased ligand for OXE-R uncouples Galpha and Gbetagamma signaling within a heterotrimer. Nat Chem Biol (2012) 8:631-8. doi:10.1038/nchembio.962.
49. Liu JJ, Horst R, Katritch V, Stevens RC, Wuthrich K. Biased signaling pathways in beta2-adrenergic receptor characterized by 19F-NMR. Science (2012) 335:1106-10. doi:10.1126/science.1215802.
50. Reiter E, Ahn S, Shukla AK, Lefkowitz RJ. Molecular mechanism of beta-arrestin-biased agonism at seven-transmembrane receptors. Annu Rev Pharmacol Toxicol (2012) 52:179-97. doi:10.1146/annurev.pharmtox.010909.105800.
51. Zimmerman B, Beautrait A, Aguila B, Charles R, Escher E, Claing A, et al. Differential beta-arrestin-dependent conformational signaling and cellular responses revealed by angiotensin analogs. Sci Signal (2012) 5:ra33. doi:10.1126/scisignal.2002522.
52. Karpus WJ, Lukacs NW, Mcrae BL, Strieter RM, Kunkel SL, Miller SD. An important role for the chemokine macrophage inflammatory protein-1 alpha in the pathogenesis of the T cell-mediated autoimmune disease, experimental autoimmune encephalomyelitis. J Immunol (1995) 155:5003-10.
53. Karpus WJ, Kennedy KJ. MIP-1alpha and MCP-1 differentially regulate acute and relapsing autoimmune encephalomyelitis as well as Th1/Th2 lymphocyte differentiation. J Leukoc Biol (1997) 62:681-7.
54. Karpus WJ, Kennedy KJ, Kunkel SL, Lukacs NW. Monocyte chemotactic protein 1 regulates oral tolerance induction by inhibition of T helper cell 1-related cytokines. J Exp Med (1998) 187:733-41. doi:10.1084/jem.187.5.733.
55. Youssef S, Wildbaum G, Maor G, Lanir N, Gour-Lavie A, Grabie N, et al. Long-lasting protective immunity to experimental autoimmune encephalomyelitis following vaccination with naked DNA encoding C-C chemokines. J Immunol (1998) 161:3870-9.
56. Youssef S, Wildbaum G, Karin N. Prevention of experimental autoimmune encephalomyelitis by MIP-1alpha and MCP-1 naked DNA vaccines. J Autoimmun (1999) 13:21-9. doi:10.1006/jaut.1999.0306.
57. Izikson L, Klein RS, Charo IF, Weiner HL, Luster AD. Resistance to experimental autoimmune encephalomyelitis in mice lacking the CC chemokine receptor (CCR)2. J Exp Med (2000) 192:1075-80. doi:10.1084/jem.192.7.1075.
58. Fife BT, Kennedy KJ, Paniagua MC, Lukacs NW, Kunkel SL, Luster AD, et al. CXCL10 (IFN-gamma-inducible protein-10) control of encephalitogenic CD4+ T cell accumulation in the central nervous system during experimental autoimmune encephalomyelitis. J Immunol (2001) 166:7617-24. doi:10.4049/jimmunol.166.12.7617.
59. Fukumoto N, Shimaoka T, Fujimura H, Sakoda S, Tanaka M, Kita T, et al. Critical roles of CXC chemokine ligand 16/scavenger receptor that binds phosphatidylserine and oxidized lipoprotein in the pathogenesis of both acute and adoptive transfer experimental autoimmune encephalomyelitis. J Immunol (2004) 173:1620-7. doi:10.4049/jimmunol.173.3.1620.
60. Mccandless EE, Wang Q, Woerner BM, Harper JM, Klein RS. CXCL12 limits inflammation by localizing mononuclear infiltrates to the perivascular space during experimental autoimmune encephalomyelitis. J Immunol (2006) 177:8053-64. doi:10.4049/jimmunol.177.11.8053.
61. 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.
62. Martinez FO, Sica A, Mantovani A, Locati M. Macrophage activation and polarization. Front Biosci (2008) 13:453-61. doi:10.2741/2692.
63. Karin N. The multiple faces of CXCL12 (SDF-1alpha) in the regulation of immunity during health and disease. J Leukoc Biol (2010) 88:463-73. doi:10.1189/jlb.0909602.
64. Samama P, Cotecchia S, Costa T, Lefkowitz RJ. A mutation-induced activated state of the beta 2-adrenergic receptor. Extending the ternary complex model. J Biol Chem (1993) 268:4625-36.
65. Luttrell LM, Ferguson SSNG, Daaka Y, Miller WE, Maudsley S, Della Rocca GJ, et al. Arrestin-dependent formation of 2 adrenergic receptor-Src protein kinase complexes. Science (1999) 283:655-61. doi:10.1126/science.283.5402.655.
66. Frigerio S, Junt T, Lu B, Gerard C, Zumsteg U, Hollander GA, et al. Beta cells are responsible for CXCR3-mediated T-cell infiltration in insulitis. Nat Med (2002) 8:1414-20. doi:10.1038/nm1202-792.
67. Liu L, Huang D, Matsui M, He TT, Hu T, Demartino J, et al. Severe disease, unaltered leukocyte migration, and reduced IFN-gamma production in CXCR3-/-mice with experimental autoimmune encephalomyelitis. J Immunol (2006) 176:4399-409. doi:10.4049/jimmunol.176.7.4399.
68. Gazzaniga S, Bravo AI, Guglielmotti A, Van Rooijen N, Maschi F, Vecchi A, et al. Targeting tumor-associated macrophages and inhibition of MCP-1 reduce angiogenesis and tumor growth in a human melanoma xenograft. J Invest Dermatol (2007) 127:2031-41. doi:10.1038/sj.jid.5700827.
69. Loberg RD, Ying C, Craig M, Day LL, Sargent E, Neeley C, et al. Targeting CCL2 with systemic delivery of neutralizing antibodies induces prostate cancer tumor regression in vivo. Cancer Res (2007) 67:9417-24. doi:10.1158/0008-5472.CAN-07-1286.
70. Youssef S, Maor G, Wildbaum G, Grabie N, Gour-Lavie A, Karin N. C-C chemokine-encoding DNA vaccines enhance breakdown of tolerance to their gene products and treat ongoing adjuvant arthritis. J Clin Invest (2000) 106:361-71. doi:10.1172/JCI9109.
71. Izhak L, Wildbaum G, Zohar Y, Anunu R, Klapper L, Elkeles A, et al. A novel recombinant fusion protein encoding a 20-amino acid residue of the third extracellular (E3) domain of CCR2 neutralizes the biological activity of CCL2. J Immunol (2009) 183:732-9. doi:10.4049/jimmunol.0802746.
72. Sapir Y, Vitenshtein A, Barsheshet Y, Zohar Y, Wildbaum G, Karin N. A fusion protein encoding the second extracellular domain of CCR5 arrests chemokine-induced cosignaling and effectively suppresses ongoing experimental autoimmune encephalomyelitis. J Immunol (2010) 185:2589-99. doi:10.4049/jimmunol.1000666.
73. 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.
74. Khan A, Greenman J, Archibald SJ. Small molecule CXCR4 chemokine receptor antagonists: developing drug candidates. Curr Med Chem (2007) 14:2257-77. doi:10.2174/092986707781696618.
75. Hamid O, Robert C, Daud A, Hodi FS, Hwu WJ, Kefford R, et al. Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma. N Engl J Med (2013) 369:134-44. doi:10.1056/NEJMoa1305133.
76. Brahmer JR, Tykodi SS, Chow LQ, Hwu WJ, Topalian SL, Hwu P, et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med (2012) 366:2455-65. doi:10.1056/NEJMoa1200694.
77. Hodi FS, O'Day SJ, Mcdermott DF, Weber RW, Sosman JA, Haanen JB, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med (2010) 363:711-23. doi:10.1056/NEJMoa1003466.
78. Wolchok JD, Kluger H, Callahan MK, Postow MA, Rizvi NA, Lesokhin AM, et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med (2013) 369:122-33. doi:10.1056/NEJMoa1302369.
79. Barash U, Zohar Y, Wildbaum G, Beider K, Nagler A, Karin N, et al. Heparanase enhances myeloma progression via CXCL10 down regulation. Leukemia (2014) 28(11):2178-87. doi:10.1038/leu.2014.121.
80. Barreira Da Silva R, Laird ME, Yatim N, Fiette L, Ingersoll MA, Albert ML. Dipeptidylpeptidase 4 inhibition enhances lymphocyte trafficking, improving both naturally occurring tumor immunity and immunotherapy. Nat Immunol (2015) 16:850-8. doi:10.1038/ni.3201.
81. Iellem A, Mariani M, Lang R, Recalde H, Panina-Bordignon P, Sinigaglia F, et al. Unique chemotactic response profile and specific expression of chemokine receptors CCR4 and CCR8 by CD4(+)CD25(+) regulatory T cells. J Exp Med (2001) 194:847-53. doi:10.1084/jem.194.6.847.
82. Coghill JM, Fowler KA, West ML, Fulton LM, Van Deventer H, Mckinnon KP, et al. CC chemokine receptor 8 potentiates donor Treg survival and is critical for the prevention of murine graft-versus-host disease. Blood (2013) 122:825-36. doi:10.1182/blood-2012-06-435735.
83. Hoelzinger DB, Smith SE, Mirza N, Dominguez AL, Manrique SZ, Lustgarten J. Blockade of CCL1 inhibits T regulatory cell suppressive function enhancing tumor immunity without affecting T effector responses. J Immunol (2010) 184:6833-42. doi:10.4049/jimmunol.0904084.