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Mediators of Inflammation
Volume 2016, Article ID 3635809, 16 pages
http://dx.doi.org/10.1155/2016/3635809
Research Article

CCR9 Is a Key Regulator of Early Phases of Allergic Airway Inflammation

1CBRL, Ciudad de México, Mexico
2Departamento de Inmunología, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, 04510 Ciudad de México, Mexico
3Departamento de Patología Experimental, Instituto Nacional de Ciencias Médicas y Nutrición “Salvador Zubirán”, Tlalpan, 14080 Ciudad de México, Mexico

Received 9 May 2016; Accepted 7 August 2016

Academic Editor: Carolina T. Piñeiro

Copyright © 2016 C. López-Pacheco et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. “GINA Report, Global Strategy for Asthma Management and Prevention,” 2015.
  2. H. Y. Kim, R. H. Dekruyff, and D. T. Umetsu, “The many paths to asthma: phenotype shaped by innate and adaptive immunity,” Nature Immunology, vol. 11, no. 7, pp. 577–584, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. T. R. Myers and L. Tomasio, “Asthma: 2015 and beyond,” Respiratory Care, vol. 56, no. 9, pp. 1389–1407, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. F. D. Martinez and D. Vercelli, “Asthma,” The Lancet, vol. 382, no. 9901, pp. 1360–1372, 2013. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Masoli, D. Fabian, S. Holt, and R. Beasley, “The global burden of asthma,” Global Initiative for Asthma Reports, 2014. View at Google Scholar
  6. R. H. Dekruyff, S. Yu, H. Y. Kim, and D. T. Umetsu, “Innate immunity in the lung regulates the development of asthma,” Immunological Reviews, vol. 260, no. 1, pp. 235–248, 2014. View at Publisher · View at Google Scholar · View at Scopus
  7. J. W. Griffith, C. L. Sokol, and A. D. Luster, “Chemokines and chemokine receptors: positioning cells for host defense and immunity,” Annual Review of Immunology, vol. 32, pp. 659–702, 2014. View at Publisher · View at Google Scholar · View at Scopus
  8. J. E. Pease, “Asthma, allergy and chemokines,” Current Drug Targets, vol. 7, no. 1, pp. 3–12, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. B.-S. Youn, C. H. Kim, F. O. Smith, and H. E. Broxmeyer, “TECK, an efficacious chemoattractant for human thymocytes, uses GPR-9-6/CCR9 as a specific receptor,” Blood, vol. 94, no. 7, pp. 2533–2536, 1999. View at Google Scholar · View at Scopus
  10. M.-A. Wurbel, J.-M. Philippe, C. Nguyen et al., “The chemokine TECK is expressed by thymic and intestinal epithelial cells and attracts double- and single-positive thymocytes expressing the TECK receptor CCR9,” European Journal of Immunology, vol. 30, no. 1, pp. 262–271, 2000. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Uehara, A. Grinberg, J. M. Farber, and P. E. Love, “A role for CCR9 in T lymphocyte development and migration,” The Journal of Immunology, vol. 168, no. 6, pp. 2811–2819, 2002. View at Publisher · View at Google Scholar · View at Scopus
  12. E. J. Kunkel, J. J. Campbell, G. Haraldsen 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,” Journal of Experimental Medicine, vol. 192, no. 5, pp. 761–768, 2000. View at Publisher · View at Google Scholar · View at Scopus
  13. Y.-J. Jung, S.-Y. Woo, M. H. Jang et al., “Human eosinophils show chemotaxis to lymphoid chemokines and exhibit antigen-presenting-cell-like properties upon stimulation with IFN-γ, IL-3 and GM-CSF,” International Archives of Allergy and Immunology, vol. 146, no. 3, pp. 227–234, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. L. Y. Liu, N. N. Jarjour, W. W. Busse, and E. A. B. Kelly, “Chemokine receptor expression on human eosinophils from peripheral blood and bronchoalveolar lavage fluid after segmental antigen challenge,” Journal of Allergy and Clinical Immunology, vol. 112, no. 3, pp. 556–562, 2003. View at Publisher · View at Google Scholar · View at Scopus
  15. M. A. Gill, “The role of dendritic cells in asthma,” Journal of Allergy and Clinical Immunology, vol. 129, no. 4, pp. 889–901, 2012. View at Publisher · View at Google Scholar · View at Scopus
  16. R. Elgueta, F. E. Sepulveda, F. Vilches et al., “Imprinting of CCR9 on CD4 T cells requires IL-4 signaling on mesenteric lymph node dendritic cells,” Journal of Immunology, vol. 180, no. 10, pp. 6501–6507, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. A. E. Rojas-López, G. Soldevila, S. Meza-Pérez et al., “CCR9+ T cells contribute to the resolution of the inflammatory response in a mouse model of intestinal amoebiasis,” Immunobiology, vol. 217, no. 8, pp. 795–807, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. J. A. MacLean, A. Sauty, A. D. Luster, J. M. Drazen, and G. T. De Sanctis, “Antigen-induced airway hyperresponsiveness, pulmonary eosinophilia, and chemokine expression in B cell-deficient mice,” American Journal of Respiratory Cell and Molecular Biology, vol. 20, no. 3, pp. 379–387, 1999. View at Publisher · View at Google Scholar · View at Scopus
  19. E. Mendez-Enriquez, Y. Melendez, F. Martinez et al., “CDIP-2, a synthetic peptide derived from chemokine (C-C motif) ligand 13 (CCL13), ameliorates allergic airway inflammation,” Clinical and Experimental Immunology, vol. 152, no. 2, pp. 354–363, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. M. Grob, P. Schmid-Grendelmeier, H. I. Joller-Jemelka et al., “Altered intracellular expression of the chemokines MIP-1α, MIP-1β and IL-8 by peripheral blood CD4+ and CD8+ T cells in mild allergic asthma,” Allergy, vol. 58, no. 3, pp. 239–245, 2003. View at Publisher · View at Google Scholar · View at Scopus
  21. L. Cohn, J. A. Elias, and G. L. Chupp, “Asthma: mechanisms of disease persistence and progression,” Annual Review of Immunology, vol. 22, pp. 789–815, 2004. View at Publisher · View at Google Scholar · View at Scopus
  22. E. A. Garcia-Zepeda, M. E. Rothenberg, R. T. Ownbey, J. Celestin, P. Leder, and A. D. Luster, “Human eotaxin is a specific chemoattractant for eosinophil cells and provides a new mechanism to explain tissue eosinophilia,” Nature Medicine, vol. 2, no. 4, pp. 449–456, 1996. View at Publisher · View at Google Scholar · View at Scopus
  23. E. A. Garcia-Zepeda, C. Combadiere, M. E. Rothenberg et al., “Human monocyte chemoattractant protein (MCP)-4 is a novel cc chemokine with activities on monocytes, eosinophils, and basophils induced in allergic and nonallergic inflammation that signals through the CC Chemokine receptors (CCR)-2 and -3,” Journal of Immunology, vol. 157, no. 12, pp. 5613–5626, 1996. View at Google Scholar · View at Scopus
  24. S. Ying, D. S. Robinson, Q. Meng et al., “C-C chemokines in allergen-induced late-phase cutaneous responses in atopic subjects: association of eotaxin with early 6-hour eosinophils, and of eotaxin-2 and monocyte chemoattractant protein-4 with the later 24-hour tissue eosinophilia, and relationship to basophils and other C-C chemokines (monocyte chemoattractant protein-3 and RANTES),” Journal of Immunology, vol. 163, no. 7, pp. 3976–3984, 1999. View at Google Scholar · View at Scopus
  25. T. Tomankova, E. Kriegova, and M. Liu, “Chemokine receptors and their therapeutic opportunities in diseased lung: far beyond leukocyte trafficking,” American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 308, no. 7, pp. L603–L618, 2015. View at Publisher · View at Google Scholar · View at Scopus
  26. R. Alam, J. York, M. Boyars et al., “Increased MCP-1, RANTES, and MIP-1α in bronchoalveolar lavage fluid of allergic asthmatic patients,” American Journal of Respiratory and Critical Care Medicine, vol. 153, no. 4, pp. 1398–1404, 1996. View at Publisher · View at Google Scholar · View at Scopus
  27. S. Mattoli, M. A. Stacey, G. Sun, A. Bellini, and M. Marini, “Eotaxin expression and eosinophilic inflammation in asthma,” Biochemical and Biophysical Research Communications, vol. 236, no. 2, pp. 299–301, 1997. View at Publisher · View at Google Scholar · View at Scopus
  28. J. E. Pease and T. J. Williams, “Eotaxin and asthma,” Current Opinion in Pharmacology, vol. 1, no. 3, pp. 248–253, 2001. View at Publisher · View at Google Scholar · View at Scopus
  29. C. E. Rose Jr., S.-S. J. Sung, and S. M. Fu, “Significant involvement of CCL2 (MCP-1) in inflammatory disorders of the lung,” Microcirculation, vol. 10, no. 3-4, pp. 273–288, 2003. View at Publisher · View at Google Scholar · View at Scopus
  30. N. W. Lukacs, A. L. Miller, and C. M. Hogaboam, “Chemokine receptors in asthma: searching for the correct immune targets,” Journal of Immunology, vol. 171, no. 1, pp. 11–15, 2003. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Isgrò, L. Bianchetti, M. A. Marini, A. Bellini, M. Schmidt, and S. Mattoli, “The C-C motif chemokine ligands CCL5, CCL11, and CCL24 induce the migration of circulating fibrocytes from patients with severe asthma,” Mucosal Immunology, vol. 6, no. 4, pp. 718–727, 2013. View at Publisher · View at Google Scholar · View at Scopus
  32. V. Provost, M.-C. Larose, A. Langlois, M. Rola-Pleszczynski, N. Flamand, and M. Laviolette, “CCL26/eotaxin-3 is more effective to induce the migration of eosinophils of asthmatics than CCL11/eotaxin-1 and CCL24/eotaxin-2,” Journal of Leukocyte Biology, vol. 94, no. 2, pp. 213–222, 2013. View at Publisher · View at Google Scholar · View at Scopus
  33. A. A. Humbles, B. Lu, D. S. Friend et al., “The murine CCR3 receptor regulates both the role of eosinophils and mast cells in allergen-induced airway inflammation and hyperresponsiveness,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 3, pp. 1479–1484, 2002. View at Publisher · View at Google Scholar · View at Scopus
  34. D. A. Wacker, J. B. Santella, III, D. S. Gardner et al., “CCR3 antagonists: A potential new therapy for the treatment of asthma. Discovery and structure-activity relationships,” Bioorganic and Medicinal Chemistry Letters, vol. 12, no. 13, pp. 1785–1789, 2002. View at Publisher · View at Google Scholar · View at Scopus
  35. L. Faustino, D. M. Da Fonseca, M. C. Takenaka et al., “Regulatory T cells migrate to airways via CCR4 and attenuate the severity of airway allergic inflammation,” Journal of Immunology, vol. 190, no. 6, pp. 2614–2621, 2013. View at Publisher · View at Google Scholar · View at Scopus
  36. P. Vijayanand, K. Durkin, G. Hartmann et al., “Chemokine receptor 4 plays a key role in T cell recruitment into the airways of asthmatic patients,” The Journal of Immunology, vol. 184, no. 8, pp. 4568–4574, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. M.-A. Wurbel, B. Malissen, and J. J. Campbell, “Complex regulation of CCR9 at multiple discrete stages of T cell development,” European Journal of Immunology, vol. 36, no. 1, pp. 73–81, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. K. A. Papadakis and S. R. Targan, “The role of chemokines and chemokine receptors in mucosal inflammation,” Inflammatory Bowel Diseases, vol. 6, no. 4, pp. 303–313, 2000. View at Google Scholar · View at Scopus
  39. L. Carramolino, A. Zaballos, L. Kremer et al., “Expression of CCR9 β-chemokine receptor is modulated in thymocyte differentiation and is selectively maintained in CD8+ T cells from secondary lymphoid organs,” Blood, vol. 97, no. 4, pp. 850–857, 2001. View at Publisher · View at Google Scholar · View at Scopus
  40. M.-A. Wurbel, M. Malissen, D. Guy-Grand et al., “Mice lacking the CCR9 CC-chemokine receptor show a mild impairment of early T- and B-cell development and a reduction in T-cell receptor γδ+ gut intraepithelial lymphocytes,” Blood, vol. 98, no. 9, pp. 2626–2632, 2001. View at Publisher · View at Google Scholar · View at Scopus
  41. M. Wendland, N. Czeloth, N. Mach et al., “CCR9 is a homing receptor for plasmacytoid dendritic cells to the small intestine,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 15, pp. 6347–6352, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. O. Pabst, L. Ohl, M. Wendland et al., “Chemokine receptor CCR9 contributes to the localization of plasma cells to the small intestine,” The Journal of Experimental Medicine, vol. 199, no. 3, pp. 411–416, 2004. View at Publisher · View at Google Scholar · View at Scopus
  43. M.-A. Wurbel, M. G. McIntire, P. Dwyer, and E. Fiebiger, “CCL25/CCR9 interactions regulate large intestinal inflammation in a murine model of acute colitis,” PLoS ONE, vol. 6, no. 1, Article ID e16442, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. M.-A. Wurbel, S. Le Bras, M. Ibourk et al., “CCL25/CCR9 interactions are not essential for colitis development but are required for innate immune cell protection from chronic experimental murine colitis,” Inflammatory Bowel Diseases, vol. 20, no. 7, pp. 1165–1176, 2014. View at Publisher · View at Google Scholar · View at Scopus
  45. B. Eksteen and D. H. Adams, “GSK-1605786, a selective small-molecule antagonist of the CCR9 chemokine receptor for the treatment of Crohn's disease,” IDrugs, vol. 13, no. 7, pp. 472–481, 2010. View at Google Scholar · View at Scopus
  46. J. Rivera-Nieves, J. Ho, G. Bamias et al., “Antibody blockade of CCL25/CCR9 ameliorates early but not late chronic murine ileitis,” Gastroenterology, vol. 131, no. 5, pp. 1518–1529, 2006. View at Publisher · View at Google Scholar · View at Scopus
  47. J. D. Wermers, E. N. McNamee, M.-A. Wurbel, P. Jedlicka, and J. Riveranieves, “The chemokine receptor CCR9 is required for the T-cell-mediated regulation of chronic ileitis in mice,” Gastroenterology, vol. 140, no. 5, pp. 1526–1535, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. B. Li, Z. Wang, Y. Zhong, J. Lan, X. Li, and H. Lin, “CCR9–CCL25 interaction suppresses apoptosis of lung cancer cells by activating the PI3K/Akt pathway,” Medical Oncology, vol. 32, no. 3, pp. 66–75, 2015. View at Publisher · View at Google Scholar · View at Scopus
  49. H. J. Chen, R. Edwards, S. Tucci et al., “Chemokine 25-induced signaling suppresses colon cancer invasion and metastasis,” The Journal of Clinical Investigation, vol. 122, no. 9, pp. 3184–3196, 2012. View at Publisher · View at Google Scholar · View at Scopus
  50. P. Gupta, P. K. Sharma, H. Mir et al., “CCR9/CCL25 expression in non-small cell lung cancer correlates with aggressive disease and mediates key steps of metastasis,” Oncotarget, vol. 5, no. 20, pp. 10170–10179, 2014. View at Publisher · View at Google Scholar · View at Scopus
  51. Y.-J. Jung, S.-Y. Woo, M. H. Jang et al., “Human eosinophils show chemotaxis to lymphoid chemokines and exhibit antigen-presenting-cell-like properties upon stimulation with IFN-γ, IL-3 and GM-CSF,” International Archives of Allergy and Immunology, vol. 146, no. 3, pp. 227–234, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. M. V. Bautista, Y. Chen, V. S. Ivanova, M. K. Rahimi, A. M. Watson, and M. C. Rose, “IL-8 regulates mucin gene expression at the posttranscriptional level in lung epithelial cells,” Journal of Immunology, vol. 183, no. 3, pp. 2159–2166, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. S. Kim, C. Lewis, and J. A. Nadel, “CCL20/CCR6 feedback exaggerates epidermal growth factor receptor-dependent MUC5AC mucin production in human airway epithelial (NCI-H292) cells,” Journal of Immunology, vol. 186, no. 6, pp. 3392–3400, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. B. O. V. Shum, M. S. Rolph, and W. A. Sewell, “Mechanisms in allergic airway inflammation—lessons from studies in the mouse,” Expert Reviews in Molecular Medicine, vol. 10, no. 16, article e15, 2008. View at Publisher · View at Google Scholar · View at Scopus
  55. K. F. Chung, “Targeting the interleukin pathway in the treatment of asthma,” The Lancet, vol. 386, no. 9998, pp. 1086–1096, 2015. View at Publisher · View at Google Scholar · View at Scopus
  56. W. Al-Ramli, D. Préfontaine, F. Chouiali et al., “TH17-associated cytokines (IL-17A and IL-17F) in severe asthma,” Journal of Allergy and Clinical Immunology, vol. 123, no. 5, pp. 1185–1187, 2009. View at Publisher · View at Google Scholar · View at Scopus
  57. C. M. Hawrylowicz and A. O'Garra, “Potential role of interleukin-10-secreting regulatory T cells in allergy and asthma,” Nature Reviews Immunology, vol. 5, no. 4, pp. 271–283, 2005. View at Publisher · View at Google Scholar · View at Scopus
  58. M. Saraiva and A. O'Garra, “The regulation of IL-10 production by immune cells,” Nature Reviews Immunology, vol. 10, no. 3, pp. 170–181, 2010. View at Publisher · View at Google Scholar · View at Scopus
  59. P. J. Barnes, “Cytokine modulators as novel therapies for asthma,” Annual Review of Pharmacology and Toxicology, vol. 42, pp. 81–98, 2002. View at Publisher · View at Google Scholar · View at Scopus
  60. D. F. Choy, K. M. Hart, L. A. Borthwick et al., “TH2 and TH17 inflammatory pathways are reciprocally regulated in asthma,” Science Translational Medicine, vol. 7, no. 301, pp. 301ra129–301ra129, 2015. View at Publisher · View at Google Scholar
  61. Y. Wei, B. Liu, J. Sun et al., “Regulation of Th17/Treg function contributes to the attenuation of chronic airway inflammation by icariin in ovalbumin-induced murine asthma model,” Immunobiology, vol. 220, no. 6, pp. 789–797, 2015. View at Publisher · View at Google Scholar · View at Scopus
  62. H. Nakamura, A. D. Luster, H. Tateno et al., “IL-4 differentially regulates eotaxin and MCP-4 in lung epithelium and circulating mononuclear cells,” American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 281, no. 5, pp. L1288–L1302, 2001. View at Google Scholar · View at Scopus
  63. M. E. Banwell, N. S. Tolley, T. J. Williams, and T. J. Mitchell, “Regulation of human eotaxin-3/CCL26 expression: modulation by cytokines and glucocorticoids,” Cytokine, vol. 17, no. 6, pp. 317–323, 2002. View at Publisher · View at Google Scholar · View at Scopus
  64. Y. Motomura, H. Morita, K. Moro et al., “Basophil-derived interleukin-4 controls the function of natural helper cells, a member of ILC2s, in lung inflammation,” Immunity, vol. 40, no. 5, pp. 758–771, 2014. View at Publisher · View at Google Scholar · View at Scopus
  65. W. Ito, M. Tanimoto, K. Ono et al., “Growth factors temporally associate with airway responsiveness and inflammation in allergen-exposed mice,” International Archives of Allergy and Immunology, vol. 145, no. 4, pp. 324–339, 2008. View at Publisher · View at Google Scholar · View at Scopus
  66. K. Bloemen, S. Verstraelen, R. Van Den Heuvel, H. Witters, I. Nelissen, and G. Schoeters, “The allergic cascade: review of the most important molecules in the asthmatic lung,” Immunology Letters, vol. 113, no. 1, pp. 6–18, 2007. View at Publisher · View at Google Scholar · View at Scopus
  67. J. Kim, A. C. Merry, J. A. Nemzek, G. L. Bolgos, J. Siddiqui, and D. G. Remick, “Eotaxin represents the principal eosinophil chemoattractant in a novel murine asthma model induced by house dust containing cockroach allergens,” Journal of Immunology, vol. 167, no. 5, pp. 2808–2815, 2001. View at Publisher · View at Google Scholar · View at Scopus
  68. J.-A. Gonzalo, C. M. Lloyd, L. Kremer et al., “Eosinophil recruitment to the lung in a murine model of allergic inflammation. The role of T cells, chemokines, and adhesion receptors,” The Journal of Clinical Investigation, vol. 98, no. 10, pp. 2332–2345, 1996. View at Publisher · View at Google Scholar · View at Scopus
  69. P. C. Fulkerson, N. Zimmermann, L. M. Hassman, F. D. Finkelman, and M. E. Rothenberg, “Pulmonary chemokine expression is coordinately regulated by STAT1, STAT6, and IFN-δ,” Journal of Immunology, vol. 173, no. 12, pp. 7565–7574, 2004. View at Publisher · View at Google Scholar · View at Scopus
  70. A. P. Vicari, D. J. Figueroa, J. A. Hedrick et al., “TECK: a novel CC chemokine specifically expressed by thymic dendritic cells and potentially involved in T cell development,” Immunity, vol. 7, no. 2, pp. 291–301, 1997. View at Publisher · View at Google Scholar · View at Scopus
  71. A. Ericsson, K. Kotarsky, M. Svensson, M. Sigvardsson, and W. Agace, “Functional characterization of the CCL25 promoter in small intestinal epithelial cells suggests a regulatory role for caudal-related homeobox (Cdx) transcription factors,” The Journal of Immunology, vol. 176, no. 6, pp. 3642–3651, 2006. View at Publisher · View at Google Scholar · View at Scopus
  72. T. Nabe, C. L. Zindl, W. J. Yong et al., “Induction of a late asthmatic response associated with airway inflammation in mice,” European Journal of Pharmacology, vol. 521, no. 1–3, pp. 144–155, 2005. View at Publisher · View at Google Scholar · View at Scopus