Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Overview
  • Published:

Chemokines: immunology's high impact factors

Nature Immunology volume 2, pages 95–101 (2001)Cite this article

Abstract

Chemokines facilitate leukocyte migration and positioning as well as other processes such as angiogenesis and leukocyte degranulation. The burgeoning knowledge on chemokines and their receptors has influenced many aspects of immunology, in part because cell migration is intimately related to leukocyte function. This overview assesses the impact that chemokines have had on our understanding of immunology and infectious diseases. These include the role of chemokines in leukocyte–endothelial cell interactions; dendritic cell function; T cell differentiation and function; inflammatory diseases; mucosal and subcutaneous immunity; and subversion of immune responses by viruses, including HIV-1. This knowledge heralds new opportunities for the manipulation of immune responses and the development of new anti-inflammatory therapies. It has also provided a new perspective on the functioning of the immune system.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Four of the important biological functions of chemokines.
Figure 2: A phylogenetic comparison of human chemoattractant receptors, list of representative ligands and generalized main biological roles.
Figure 3: Three major cytokine-chemokine-leukocyte systems for mammalian immune responses.

References

  1. Devreotes, P. N. & Zigmond, S. H. Chemotaxis in eukaryotic cells: a focus on leukocytes and dictyostelium. Ann. Rev. Biol. 4, 649–586 (1988).

    Article  CAS  Google Scholar 

  2. Zlotnik, A. & Yoshie, O. Chemokines: a new classification system and their role in immunity. Immunity 12, 121–127 (2000).

    Article  CAS  PubMed  Google Scholar 

  3. Yoshimura, T. et al. Purification of a human monocyte-derived neutrophil chemotactic factor that has peptide sequence similarity to other host defense cytokines. Proc. Natl Acad. Sci. USA 84, 9233–9237 (1987).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Rossi, D. & Zlotnik, A. The biology of chemokines and their receptors. Annu. Rev. Immunol. 18, 217–242 (2000).

    Article  CAS  PubMed  Google Scholar 

  5. Holmes, W. E., Lee, J., Kuang, W. J., Rice, G. C. & Wood, W. I. Structure and functional expression of a human interleukin-8 receptor. Science 253, 1278–1280 (1991).

    Article  CAS  PubMed  Google Scholar 

  6. Gerard, C. & Rollins, B. Chemokines in disease. Nature Immunol. 2, 108–115 (2001).

    Article  CAS  Google Scholar 

  7. Zou, Y. R., Kottmann, A. H., Kuroda, M., Taniuchi, I. & Littman, D. R. Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 393, 595–599 (1998).

    Article  CAS  PubMed  Google Scholar 

  8. Nagasawa, T. et al. Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature 382, 635–638 (1996).

    Article  CAS  PubMed  Google Scholar 

  9. Butcher, E. C. Leukocyte-endothelial cell recognition: three (or more) steps to specificity and diversity. Cell 67, 1033–1036 (1991).

    Article  CAS  PubMed  Google Scholar 

  10. Springer, T. A. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 76, 301–314 (1994).

    Article  CAS  PubMed  Google Scholar 

  11. Bargatze, R. F. & Butcher, E. C. Rapid G protein-regulated activation event involved in lymphocyte binding to high endothelial venules. J. Exp. Med. 178, 367–372 (1993).

    Article  CAS  PubMed  Google Scholar 

  12. Tanaka, Y. et al. T-cell adhesion induced by proteoglycan-immobilized cytokine MIP-1β. Nature 361, 79–82 (1993).

    Article  CAS  PubMed  Google Scholar 

  13. Kitayama, J., Mackay, C. R., Ponath, P. D. & Springer, T. A. The C-C chemokine receptor CCR3 participates in stimulation of eosinophil arrest on inflammatory endothelium in shear flow. J. Clin. Invest. 101, 2017–2024 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Gerszten, R. E. et al. MCP-1 and IL-8 trigger firm adhesion of monocytes to vascular endothelium under flow conditions. Nature 398, 718–723 (1999).

    Article  CAS  PubMed  Google Scholar 

  15. Campbell, J. J. et al. Chemokines and the arrest of lymphocytes rolling under flow conditions. Science 279, 381–384 (1998).

    Article  CAS  PubMed  Google Scholar 

  16. Ponath, P. D. et al. Cloning of the human eosinophil chemoattractant, eotaxin. Expression, receptor binding, and functional properties suggest a mechanism for the selective recruitment of eosinophils. J. Clin. Invest. 97, 604–612 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Bleul, C. C., Schultze, J. L. & Springer, T. A. B lymphocyte chemotaxis regulated in association with microanatomic localization, differentiation state, and B cell receptor engagement. J. Exp. Med. 187, 753–762 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Bowman, E. P. et al. Developmental switches in chemokine response profiles during B cell differentiation and maturation. J. Exp. Med. 191, 1303–1318 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Guinamard, R., Okigaki, M., Schlessinger, J. & Ravetch, J. V. Absence of marginal zone B cells in Pyk-2–deficient mice defines their role in the humoral response. Nature Immunol. 1, 31–36 (2000).

    Article  CAS  Google Scholar 

  20. Bleul, C. C. & Boehm, T. Chemokines define distinct microenvironments in the developing thymus. Eur. J. Immunol. 30, 3371–3379 (2000).

    Article  CAS  PubMed  Google Scholar 

  21. Campbell, J. J., Pan, J. & Butcher, E. C. Cutting edge: developmental switches in chemokine responses during T cell maturation. J. Immunol. 163, 2353–2357 (1999).

    CAS  PubMed  Google Scholar 

  22. Sallusto, F., Mackay, C. R. & Lanzavecchia, A. The role of chemokine receptors in primary, effector, and memory immune responses. Annu. Rev. Immunol. 18, 593–620 (2000).

    Article  CAS  PubMed  Google Scholar 

  23. Campbell, J. et al. The chemokine receptor CCR4 in vascular recognition by cutaneous but not intestinal memory T cells. Nature 400, 776–780 (1999).

    Article  CAS  PubMed  Google Scholar 

  24. Bleul, C. C., Wu, L., Hoxie, J. A., Springer, T. A. & Mackay, C. R. The HIV coreceptors CXCR4 and CCR5 are differentially expressed and regulated on human T lymphocytes. Proc. Natl Acad. Sci. USA 94, 1925–1930 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Zabel, B. A. et al. Human G protein-coupled receptor GPR-9-6/CC chemokine receptor 9 is selectively expressed on intestinal homing T lymphocytes, mucosal lymphocytes, and thymocytes and is required for thymus-expressed chemokine-mediated chemotaxis. J. Exp. Med. 190, 1241–1256 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Sallusto, F., Mackay, C. R. & Lanzavecchia, A. Selective expression of the eotaxin receptor CCR3 by human T helper 2 cells. Science 277, 2005–2007 (1997).

    Article  CAS  PubMed  Google Scholar 

  27. Sallusto, F., Lenig, D., Forster, R., Lipp, M. & Lanzavecchia, A. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401, 708–712 (1999).

    Article  CAS  PubMed  Google Scholar 

  28. Dieu, M. C. et al. Selective recruitment of immature and mature dendritic cells by distinct chemokines expressed in different anatomic sites. J. Exp. Med. 188, 373–386 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Cook, D. N. et al. CCR6 mediates dendritic cell localization, lymphocyte homeostasis, and immune responses in mucosal tissue. Immunity 12, 495–503 (2000).

    Article  CAS  PubMed  Google Scholar 

  30. Sallusto, F. et al. Rapid and coordinated switch in chemokine receptor expression during dendritic cell maturation. Eur. J. Immunol. 28, 2760–2769 (1998).

    Article  CAS  PubMed  Google Scholar 

  31. Sozzani, S. et al. Differential regulation of chemokine receptors during dendritic cell maturation: a model for their trafficking properties. J. Immunol. 161, 1083–1086 (1998).

    CAS  PubMed  Google Scholar 

  32. Adema, G. J. et al. A dendritic-cell-derived C-C chemokine that preferentially attracts naive T cells. Nature 387, 713–717 (1997).

    Article  CAS  PubMed  Google Scholar 

  33. Sallusto, F. & Lanzavecchia, A. Mobilizing dendritic cells for tolerance, priming, and chronic inflammation. J. Exp. Med. 189, 611–614 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Heath, W. R., Kurts, C., Miller, J. F. A. P. & R., C. F. Cross–tolerance: A pathway for inducing tolerance to peripheral tissue antigens. J. Exp. Med. 187, 1549–1553 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Moser, B. & Loetscher, P. Lymphocyte traffic control by chemokines. Nature Immunol. 2, 123–128 (2001).

    Article  CAS  Google Scholar 

  36. Cyster, J. G. Chemokines and cell migration in secondary lymphoid organs. Science 286, 2098–2102 (1999).

    Article  CAS  PubMed  Google Scholar 

  37. Mackay, C. R. Follicular homing T helper cells and the Th1/Th2 paradigm. J. Exp. Med. 192, 31–34 (2000).

    Article  Google Scholar 

  38. Gunn, M. D. et al. Mice lacking expression of secondary lymphoid organ chemokine have defects in lymphocyte homing and dendritic cell localization. J. Exp. Med. 189, 451–460 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Forster, R. et al. A putative chemokine receptor, BLR1, directs B cell migration to defined lymphoid organs and specific anatomic compartments of the spleen. Cell 87, 1037–1047 (1996).

    Article  CAS  PubMed  Google Scholar 

  40. Forster, R. et al. CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell 99, 23–33 (1999).

    Article  CAS  PubMed  Google Scholar 

  41. Ansel, K. M. et al. A chemokine-driven positive feedback loop organizes lymphoid follicles. Nature 406, 309–314 (2000).

    Article  CAS  PubMed  Google Scholar 

  42. Yoshie, O., Imai, T. & Nomiyama, H. Novel lymphocyte-specific CC chemokines and their receptors. J. Leukoc. Biol. 62, 634–644 (1997).

    Article  CAS  PubMed  Google Scholar 

  43. Sallusto, F., Lanzavecchia, A. & Mackay, C. R. Chemokines and chemokine receptors in T-cell priming and Th1/Th2- mediated responses. Immunol. Today 19, 568–574 (1998).

    Article  CAS  PubMed  Google Scholar 

  44. Warnock, R. A. et al. The role of chemokines in the microenvironmental control of T versus B cell arrest in Peyer's patch high endothelial venules. J. Exp. Med. 191, 77–88 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Gunn, M. D. et al. A chemokine expressed in lymphoid high endothelial venules promotes the adhesion and chemotaxis of naive T lymphocytes. Proc. Natl Acad. Sci. USA 95, 258–263 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Stein, J. V. et al. The CC chemokine thymus-derived chemotactic agent 4 (TCA-4, secondary lymphoid tissue chemokine, 6Ckine, exodus-2) triggers lymphocyte function-associated antigen 1-mediated arrest of rolling T lymphocytes in peripheral lymph node high endothelial venules. J. Exp. Med. 191, 61–76 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Gunn, M. D. et al. A B-cell-homing chemokine made in lymphoid follicles activates Burkitt's lymphoma receptor-1. Nature 391, 799–803 (1998).

    Article  CAS  PubMed  Google Scholar 

  48. Ngo, V. N. et al. Lymphotoxin α/β and tumor necrosis factor are required for stromal cell expression of homing chemokines in B and T cell areas of the spleen. J. Exp. Med. 189, 403–412 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Ansel, K. M., McHeyzer-Williams, L. J., Ngo, V. N., McHeyzer-Williams, M. G. & Cyster, J. G. In vivo-activated CD4 T cells upregulate CXC chemokine receptor 5 and reprogram their response to lymphoid chemokines. J. Exp. Med. 190, 1123–1134 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Schaerli, P. et al. CXCR5 expression defines follicular homing T cells with B cell helper function. J. Exp. Med. 192, 1553–1562 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Breitfeld, D. et al. Follicular B helper T cells express CXCR5, localize to B cell follicles and support immunoglobulin production. J. Exp. Med.. 192, 1545–1552 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Li, L. et al. Effects of Th2 cytokines on chemokine expression in the lung: IL-13 potently induces eotaxin expression by airway epithelial cells. J. Immunol. 162, 2477–2487 (1999).

    CAS  PubMed  Google Scholar 

  53. Shinkai, A. et al. A novel human CC chemokine, eotaxin-3, which is expressed in IL-4- stimulated vascular endothelial cells, exhibits potent activity toward eosinophils. J. Immunol. 163, 1602–1610 (1999).

    CAS  PubMed  Google Scholar 

  54. Ying, S. et al. Enhanced expression of eotaxin and CCR3 mRNA and protein in atopic asthma. Association with airway hyperresponsiveness and predominant co-localization of eotaxin mRNA to bronchial epithelial and endothelial cells. Eur. J. Immunol. 27, 3507–3516 (1997).

    Article  CAS  PubMed  Google Scholar 

  55. Sallusto, F., Lenig, D., Mackay, C. R. & Lanzavecchia, A. Flexible programs of chemokine receptor expression on human polarized T helper 1 and 2 lymphocytes. J. Exp. Med. 187, 875–883 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Heath, H. et al. Chemokine receptor usage by human eosinophils. The importance of CCR3 demonstrated using an antagonistic monoclonal antibody. J. Clin. Invest. 99, 178–184 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Uguccioni, M. et al. High expression of the chemokine receptor CCR3 in human blood basophils. Role in activation by eotaxin, MCP-4, and other chemokines. J. Clin. Invest. 100, 1137–1143 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Ochi, H. et al. T helper cell type 2 cytokine-mediated comitogenic responses and CCR3 expression during differentiation of human mast cells in vitro. J. Exp. Med. 190, 267–280 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Zingoni, A. et al. The chemokine receptor CCR8 is preferentially expressed in Th2 but not Th1 cells. J. Immunol. 161, 547–551 (1998).

    CAS  PubMed  Google Scholar 

  60. Lloyd, C. M. et al. CC chemokine receptor (CCR)3/eotaxin is followed by CCR4/monocyte-derived chemokine in mediating pulmonary T helper lymphocyte type 2 recruitment after serial antigen challenge in vivo. J. Exp. Med. 191, 265–274 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Bonecchi, R. et al. Differential expression of chemokine receptors and chemotactic responsiveness of type 1 T helper cells (Th1s) and Th2s. J. Exp. Med. 187, 129–134 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Randolph, D. A., Huang, G., Carruthers, C. J., Bromley, L. E. & Chaplin, D. D. The role of CCR7 in TH1 and TH2 cell localization and delivery of B cell help in vivo. Science 286, 2159–2162 (1999).

    Article  CAS  PubMed  Google Scholar 

  63. Loetscher, P. et al. CCR5 is characteristic of Th1 lymphocytes. Nature 391, 344–345 (1998).

    Article  CAS  PubMed  Google Scholar 

  64. Balashov, K. E., Rottman, J. B., Weiner, H. L. & Hancock, W. W. CCR5(+) and CXCR3(+) T cells are increased in multiple sclerosis and their ligands MIP-1α and IP-10 are expressed in demyelinating brain lesions. Proc. Natl Acad. Sci. USA 96, 6873–6878 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Sauty, A. et al. The T cell-specific CXC chemokines IP-10, Mig, and I-TAC are expressed by activated human bronchial epithelial cells. J. Immunol. 162, 3549–3558 (1999).

    CAS  PubMed  Google Scholar 

  66. Qin, S. et al. The chemokine receptors CXCR3 and CCR5 mark subsets of T cells associated with certain inflammatory reactions. J. Clin. Invest. 101, 746–754 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Luther, S. A., Lopez, T., Bai, W., Hanahan, D. & Cyster, J. G. BLC expression in pancreatic islets causes B cell recruitment and lymphotoxin-dependent lymphoid neogenesis. Immunity 12, 471–481 (2000).

    Article  CAS  PubMed  Google Scholar 

  68. Gu, L. et al. Control of TH2 polarization by the chemokine monocyte chemoattractant protein-1. Nature 404, 407–411 (2000).

    Article  CAS  PubMed  Google Scholar 

  69. Lukacs, N. W. et al. C-C chemokines differentially alter interleukin-4 production from lymphocytes. Am. J. Pathol. 150, 1861–1868 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Kunkel, E. J. et al. Lymphocyte CC chemokine receptor 9 and epithelial thymus-expressed chemokine (TECK) expression distinguish the small intestinal immune compartment: Epithelial expression of tissue-specific chemokines as an organizing principle in regional immunity. J. Exp. Med. 192, 761–768 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Morales, J. et al. CTACK, a skin-associated chemokine that preferentially attracts skin-homing memory T cells. Proc. Natl Acad. Sci. USA 96, 14470–14475 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Homey, B. et al. Cutting edge: the orphan chemokine receptor G protein-coupled receptor-2 (GPR-2, CCR10) binds the skin-associated chemokine CCL27 (CTACK/ALP/ILC). J. Immunol. 164, 3465–3470 (2000).

    Article  CAS  PubMed  Google Scholar 

  73. Huang, Y. et al. The role of a mutant CCR5 allele in HIV-1 transmission and disease progression. Nature Med. 2, 1240–1243 (1996).

    Article  CAS  PubMed  Google Scholar 

  74. Berger, E. A., Murphy, P. M. & Farber, J. M. Chemokine receptors as HIV-1 coreceptors: roles in viral entry, tropism, and disease. Annu. Rev. Immunol. 17, 657–700 (1999).

    Article  CAS  PubMed  Google Scholar 

  75. Moore, J. P. Coreceptors: implications for HIV pathogenesis and therapy. Science 276, 51–52 (1997).

    Article  CAS  PubMed  Google Scholar 

  76. Murphy, P. M. Viral exploitation and subversion of the immune system through chemokine mimicry. Nature Immunol. 2,159–166 (2001).

    Article  CAS  Google Scholar 

  77. Lalani, A. S. et al. Use of chemokine receptors by poxviruses. Science 286, 1968–1971 (1999).

    Article  CAS  PubMed  Google Scholar 

  78. Lin, C. L. et al. Macrophage-tropic HIV Induces and Exploits Dendritic Cell Chemotaxis. J. Exp. Med. 192, 587–594 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Sozzani, S. et al. The viral chemokine macrophage inflammatory protein-II is a selective Th2 chemoattractant. Blood 92, 4036–4039 (1998).

    CAS  PubMed  Google Scholar 

  80. Kledal, T. N. et al. A broad-spectrum chemokine antagonist encoded by Kaposi's sarcoma- associated herpes virus. Science 277, 1656–1659 (1997).

    Article  CAS  PubMed  Google Scholar 

  81. Boshoff, C. et al. Angiogenic and HIV-inhibitory functions of KSHV-encoded chemokines. Science 278, 290–294 (1997).

    Article  CAS  PubMed  Google Scholar 

  82. McDermott, D. H. et al. CCR5 promoter polymorphism and HIV-1 disease progression. Multicenter AIDS Cohort Study (MACS). Lancet 352, 866–870 (1998).

    Article  CAS  PubMed  Google Scholar 

  83. Blanpain, C. et al. Multiple nonfunctional alleles of CCR5 are frequent in various human populations. Blood 96, 1638–1645 (2000).

    CAS  PubMed  Google Scholar 

  84. Wu, L. et al. CCR5 levels and expression pattern correlate with infectability by macrophage-tropic HIV-1, in vitro. J. Exp. Med. 185, 1681–1691 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Gomez-Reino, J. J. et al. Association of rheumatoid arthritis with a functional chemokine receptor, CCR5. Arthritis Rheum. 42, 989–992 (1999).

    Article  CAS  PubMed  Google Scholar 

  86. Sellebjerg, F., Madsen, H. O., Jensen, C. V., Jensen, J. & Garred, P. CCR5 Δ32, matrix metalloproteinase-9 and disease activity in multiple sclerosis. J. Neuroimmunol. 102, 98–106 (2000).

    Article  CAS  PubMed  Google Scholar 

  87. Teuscher, C. et al. Sequence polymorphisms in the chemokines Scya1 (TCA-3), Scya2 (monocyte chemoattractant protein (MCP)-1), and Scya12 (MCP-5) are candidates for eae7, a locus controlling susceptibility to monophasic remitting/nonrelapsing experimental allergic encephalomyelitis. J. Immunol. 163, 2262–2266 (1999).

    CAS  PubMed  Google Scholar 

  88. Cameron, M. J. et al. Differential expression of CC chemokines and the CCR5 receptor in the pancreas is associated with progression to type I diabetes. J. Immunol. 165, 1102–1110 (2000).

    Article  CAS  PubMed  Google Scholar 

  89. Strieter, R. M. et al. “The good, the bad, and the ugly.” The role of chemokines in models of human disease. J. Immunol. 156, 3583–3586 (1996).

    CAS  PubMed  Google Scholar 

  90. Baba, M. et al. A small-molecule, nonpeptide CCR5 antagonist with highly potent and selective anti-HIV-1 activity. Proc. Natl Acad. Sci. USA 96, 5698–5703 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Baggiolini, M. & Moser, B. Blocking chemokine receptors. J. Exp. Med. 186, 1189–1191 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Murphy, P. M. et al. International union of pharmacology. XXII. Nomenclature for chemokine receptors. Pharmacol. Rev. 52, 145–176 (2000).

    CAS  PubMed  Google Scholar 

  93. Gonzalo, J. A. et al. The coordinated action of CC chemokines in the lung orchestrates allergic inflammation and airway hyperresponsiveness. J. Exp. Med. 188, 157–167 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Dabbagh, K. et al. Local blockade of allergic airway hyperreactivity and inflammation by the poxvirus-derived pan-CC-chemokine inhibitor vCCI. J. Immunol. 165, 3418–3422 (2000).

    Article  CAS  PubMed  Google Scholar 

  95. Gu, L. et al. Absence of monocyte chemoattractant protein-1 reduces atherosclerosis in low density lipoprotein receptor-deficient mice. Mol. Cell 2, 275–281 (1998).

    Article  CAS  PubMed  Google Scholar 

  96. Boring, L., Gosling, J., Cleary, M. & Charo, I. F. Decreased lesion formation in CCR2−/− mice reveals a role for chemokines in the initiation of atherosclerosis. Nature 394, 894–897 (1998).

    Article  CAS  PubMed  Google Scholar 

  97. Gosling, J. et al. MCP-1 deficiency reduces susceptibility to atherosclerosis in mice that overexpress human apolipoprotein B. J. Clin. Invest. 103, 773–778 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Tesch, G. H., Maifert, S., Schwarting, A., Rollins, B. J. & Kelley, V. R. Monocyte chemoattractant protein 1-dependent leukocytic infiltrates are responsible for autoimmune disease in MRL-Fas(lpr) mice. J. Exp. Med. 190, 1813–1824 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Gao, W. et al. Targeting of the chemokine receptor CCR1 suppresses development of acute and chronic cardiac allograft rejection. J. Clin. Invest. 105, 35–44 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Supported by the Glazebrook Trust and the Cooperative Research Center for Asthma.

Author information

Authors and Affiliations

  1. Garvan Institute of Medical Research, 384 Victoria St., Darlinghurst, 2010, NSW, Australia

    Charles R. Mackay

Authors
  1. Charles R. Mackay
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mackay, C. Chemokines: immunology's high impact factors. Nat Immunol 2, 95–101 (2001). https://doi.org/10.1038/84298

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/84298

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing