Systemic administration of TLR3 agonist induces IL-7 expression and IL-7-dependent CXCR3 ligand production in the lung

Journal of Leukocyte Biology

Volumn 93, Issue 3, 2013, Pages 413-425

  Jin, Jun O ^a   Yu, Qing ^a  

^a FORSYTH INSTITUTE   (United States)

Author keywords

Chemokine; Effector T cells; IFN ; M1 macrophage; NK cells; Poly I:C

Indexed keywords

ALPHA INTERFERON; CHEMOKINE RECEPTOR CXCR3; CXCL11 CHEMOKINE; CXCL9 CHEMOKINE; DOUBLE STRANDED RNA; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 12P40; INTERLEUKIN 17 RECEPTOR; INTERLEUKIN 23P19; INTERLEUKIN 7; MONOCYTE CHEMOTACTIC PROTEIN 1; NEUTRALIZING ANTIBODY; POLYINOSINIC POLYCYTIDYLIC ACID; TOLL LIKE RECEPTOR 3;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IMMUNOCOMPETENT CELL; INFLAMMATION; MOUSE; NATURAL KILLER CELL; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; UPREGULATION;

ANIMALS; CHEMOKINE CCL2; HOMEODOMAIN PROTEINS; IMMUNITY, CELLULAR; INTERFERON INDUCERS; INTERFERON-GAMMA; INTERLEUKIN-7; KILLER CELLS, NATURAL; LUNG; MACROPHAGES; MICE; MICE, KNOCKOUT; POLY I-C; RECEPTORS, CXCR3; T-LYMPHOCYTES; TOLL-LIKE RECEPTOR 3; UP-REGULATION;

EID: 84874529417     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.0712360     Document Type: Article

References (71)

1. Kawai, T., Akira, S. (2010) The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 11, 373-384.
2. Arpaia, N., Barton, G. M. (2011) Toll-like receptors: key players in antiviral immunity. Curr. Opin. Virol. 1, 447-454.
3. Mills, K. H. (2011) TLR-dependent T cell activation in autoimmunity. Nat. Rev. Immunol. 11, 807-822.
4. Marshak-Rothstein, A. (2006) Toll-like receptors in systemic autoimmune disease. Nat. Rev. Immunol. 6, 823-835.
5. Alexopoulou, L., Holt, A. C., Medzhitov, R., Flavell, R. A. (2001) Recognition of double-stranded RNA and activation of NF-κB by Toll-like receptor Nature 413, 732-738.
6. Matsumoto, M., Oshiumi, H., Seya, T. (2011) Antiviral responses induced by the TLR3 pathway. Rev. Med. Virol. doi: 10.1002/rmv.680 [Epub ahead of print].
7. Guillot, L., Le Goffic, R., Bloch, S., Escriou, N., Akira, S., Chignard, M., Si-Tahar, M. (2005) Involvement of Toll-like receptor 3 in the immune response of lung epithelial cells to double-stranded RNA and influenza A virus. J. Biol. Chem. 280, 5571-5580.
8. Brentano, F., Schorr, O., Gay, R. E., Gay, S., Kyburz, D. (2005) RNA released from necrotic synovial fluid cells activates rheumatoid arthritis synovial fibroblasts via Toll-like receptor 3. Arthritis Rheum. 52, 2656-2665.
9. Tissari, J., Siren, J., Meri, S., Julkunen, I., Matikainen, S. (2005) IFN-α enhances TLR3-mediated antiviral cytokine expression in human endothelial and epithelial cells by up-regulating TLR3 expression. J. Immunol. 174, 4289-4294.
10. Malmgaard, L., Melchjorsen, J., Bowie, A. G., Mogensen, S. C., Paludan, S. R. (2004) Viral activation of macrophages through TLR-dependent and-independent pathways. J. Immunol. 173, 6890-6898.
11. Kumar, H., Koyama, S., Ishii, K. J., Kawai, T., Akira, S. (2008) Cutting edge: cooperation of IPS-1-and TRIF-dependent pathways in poly ICenhanced antibody production and cytotoxic T cell responses. J. Immunol. 180, 683-687.
12. Longhi, M. P., Trumpfheller, C., Idoyaga, J., Caskey, M., Matos, I., Kluger, C., Salazar, A. M., Colonna, M., Steinman, R. M. (2009) Dendritic cells require a systemic type I interferon response to mature and induce CD4+ Th1 immunity with poly IC as adjuvant. J. Exp. Med. 206, 1589-1602.
13. Seya, T., Matsumoto, M. (2009) The extrinsic RNA-sensing pathway for adjuvant immunotherapy of cancer. Cancer Immunol. Immunother. 58, 1175-1184.
14. Matsumoto, M., Seya, T. (2008) TLR3: interferon induction by doublestranded RNA including poly(I:C). Adv. Drug Deliv. Rev. 60, 805-812.
15. Ngoi, S. M., Tovey, M. G., Vella, A. T. (2008) Targeting poly(I: C) to the TLR3-independent pathway boosts effector CD8 T cell differentiation through IFN-α/β. J. Immunol. 181, 7670-7680.
16. Salem, M. L., Diaz-Montero, C. M., El-Naggar, S. A., Chen, Y., Moussa, O., Cole, D. J. (2009) The TLR3 agonist poly(I: C) targets CD8+ T cells and augments their antigen-specific responses upon their adoptive transfer into naive recipient mice. Vaccine 27, 549-557.
17. Ainai, A., Tashiro, M., Hasegawa, H. (2011) Cross-protective immunity against influenza virus infections induced by intranasal vaccination together with a TLR3-mucosal adjuvant. Hum. Vaccin. 7 (Suppl.), 174-182.
18. Wick, D. A., Martin, S. D., Nelson, B. H., Webb, J. R. (2011) Profound CD8+ T cell immunity elicited by sequential daily immunization with exogenous antigen plus the TLR3 agonist poly(I: C). Vaccine 29, 984-993.
19. Lang, K. S., Georgiev, P., Recher, M., Navarini, A. A., Bergthaler, A., Heikenwalder, M., Harris, N. L., Junt, T., Odermatt, B., Clavien, P. A., Pircher, H., Akira, S., Hengartner, H., Zinkernagel, R. M. (2006) Immunoprivileged status of the liver is controlled by Toll-like receptor 3 signaling. J. Clin. Invest. 116, 2456-2463.
20. Stowell, N. C., Seideman, J., Raymond, H. A., Smalley, K. A., Lamb, R. J., Egenolf, D. D., Bugelski, P. J., Murray, L. A., Marsters, P. A., Bunting, R. A., Flavell, R. A., Alexopoulou, L., San Mateo, L. R., Griswold, D. E., Sarisky, R. T., Mbow, M. L., Das, A. M. (2009) Long-term activation of TLR3 by poly(I: C) induces inflammation and impairs lung function in mice. Respir. Res. 10, 43.
21. Patole, P. S., Grone, H. J., Segerer, S., Ciubar, R., Belemezova, E., Henger, A., Kretzler, M., Schlondorff, D., Anders, H. J. (2005) Viral double-stranded RNA aggravates lupus nephritis through Toll-like receptor 3 on glomerular mesangial cells and antigen-presenting cells. J. Am. Soc. Nephrol. 16, 1326-1338.
22. Lacotte, S., Brun, S., Muller, S., Dumortier, H. (2009) CXCR3, inflammation, and autoimmune diseases. Ann. N. Y. Acad. Sci. 1173, 310-317.
23. Groom, J. R., Luster, A. D. (2011) CXCR3 ligands: redundant, collaborative and antagonistic functions. Immunol. Cell Biol. 89, 207-215.
24. Groom, J. R., Luster, A. D. (2011) CXCR3 in T cell function. Exp. Cell. Res. 317, 620-631.
25. Sawa, Y., Arima, Y., Ogura, H., Kitabayashi, C., Jiang, J. J., Fukushima, T., Kamimura, D., Hirano, T., Murakami, M. (2009) Hepatic interleukin-7 expression regulates T cell responses. Immunity 30, 447-457.
26. Park, J. H., Adoro, S., Guinter, T., Erman, B., Alag, A. S., Catalfamo, M., Kimura, M. Y., Cui, Y., Lucas, P. J., Gress, R. E., Kubo, M., Hennighausen, L., Feigenbaum, L., Singer, A. (2010) Signaling by intrathymic cytokines, not T cell antigen receptors, specifies CD8 lineage choice and promotes the differentiation of cytotoxic-lineage T cells. Nat. Immunol. 11, 257-264.
27. Mackall, C. L., Fry, T. J., Gress, R. E. (2011) Harnessing the biology of IL-7 for therapeutic application. Nat. Rev. Immunol. 11, 330-342.
28. Sprent, J., Surh, C. D. (2011) Normal T cell homeostasis: the conversion of naive cells into memory-phenotype cells. Nat. Immunol. 12, 478-484.
29. Lee, L. F., Axtell, R., Tu, G. H., Logronio, K., Dilley, J., Yu, J., Rickert, M., Han, B., Evering, W., Walker, M. G., Shi, J., de Jong, B. A., Killestein, J., Polman, C. H., Steinman, L., Lin, J. C. (2011) IL-7 promotes T(H)1 development and serum IL-7 predicts clinical response to interferon-β in multiple sclerosis. Sci. Transl. Med. 3, 93ra68.
30. Pellegrini, M., Calzascia, T., Toe, J. G., Preston, S. P., Lin, A. E., Elford, A. R., Shahinian, A., Lang, P. A., Lang, K. S., Morre, M., Assouline, B., Lahl, K., Sparwasser, T., Tedder, T. F., Paik, J. H., DePinho, R. A., Basta, S., Ohashi, P. S., Mak, T. W. (2011) IL-7 engages multiple mechanisms to overcome chronic viral infection and limit organ pathology. Cell 144, 601-613.
31. Hartgring, S. A., Bijlsma, J. W., Lafeber, F. P., van Roon, J. A. (2006) Interleukin-7 induced immunopathology in arthritis. Ann. Rheum. Dis. 65 (Suppl 3), iii69-iii74.
32. Hartgring, S. A., Willis, C. R., Alcorn, D., Nelson, L. J., Bijlsma, J. W., Lafeber, F. P., van Roon, J. A. (2010) Blockade of the interleukin-7 receptor inhibits collagen-induced arthritis and is associated with reduction of T cell activity and proinflammatory mediators. Arthritis Rheum. 62, 2716-2725.
33. Pellegrini, M., Calzascia, T., Elford, A. R., Shahinian, A., Lin, A. E., Dissanayake, D., Dhanji, S., Nguyen, L. T., Gronski, M. A., Morre, M., Assouline, B., Lahl, K., Sparwasser, T., Ohashi, P. S., Mak, T. W. (2009) Adjuvant IL-7 antagonizes multiple cellular and molecular inhibitory networks to enhance immunotherapies. Nat. Med. 15, 528-536.
34. Kim, H. R., Hwang, K. A., Park, S. H., Kang, I. (2008) IL-7 and IL-15: biology and roles in T-cell immunity in health and disease. Crit. Rev. Immunol. 28, 325-339.
35. Churchman, S. M., Ponchel, F. (2008) Interleukin-7 in rheumatoid arthritis. Rheumatology (Oxford) 47, 753-759.
36. Totsuka, T., Kanai, T., Nemoto, Y., Makita, S., Okamoto, R., Tsuchiya, K., Watanabe, M. (2007) IL-7 Is essential for the development and the persistence of chronic colitis. J. Immunol. 178, 4737-4748.
37. Witte, P. L., Frantsve, L. M., Hergott, M., Rahbe, S. M. (1993) Cytokine production and heterogeneity of primary stromal cells that support B lymphopoiesis. Eur. J. Immunol. 23, 1809-1817.
38. Alves, N. L., Richard-Le Goff, O., Huntington, N. D., Sousa, A. P., Ribeiro, V. S., Bordack, A., Vives, F. L., Peduto, L., Chidgey, A., Cumano, A., Boyd, R., Eberl, G., Di Santo, J. P. (2009) Characterization of the thymic IL-7 niche in vivo. Proc. Natl. Acad. Sci. USA 106, 1512-1517.
39. Marrack, P., Bender, J., Hildeman, D., Jordan, M., Mitchell, T., Murakami, M., Sakamoto, A., Schaefer, B. C., Swanson, B., Kappler, J. (2000) Homeostasis of α β TCR+ T cells. Nat. Immunol. 1, 107-111.
40. Mazzucchelli, R. I., Warming, S., Lawrence, S. M., Ishii, M., Abshari, M., Washington, A. V., Feigenbaum, L., Warner, A. C., Sims, D. J., Li, W. Q., Hixon, J. A., Gray, D. H., Rich, B. E., Morrow, M., Anver, M. R., Cherry, J., Naf, D., Sternberg, L. R., McVicar, D. W., Farr, A. G., Germain, R. N., Rogers, K., Jenkins, N. A., Copeland, N. G., Durum, S. K. (2009) Visualization and identification of IL-7 producing cells in reporter mice. PLoS One 4, e7637.
41. Heufler, C., Topar, G., Grasseger, A., Stanzl, U., Koch, F., Romani, N., Namen, A. E., Schuler, G. (1993) Interleukin 7 is produced by murine and human keratinocytes. J. Exp. Med. 178, 1109-1114.
42. Watanabe, M., Ueno, Y., Yajima, T., Iwao, Y., Tsuchiya, M., Ishikawa, H., Aiso, S., Hibi, T., Ishii, H. (1995) Interleukin 7 is produced by human intestinal epithelial cells and regulates the proliferation of intestinal mucosal lymphocytes. J. Clin. Invest. 95, 2945-2953.
43. Ma, A., Koka, R., Burkett, P. (2006) Diverse functions of IL-2, IL-15, and IL-7 in lymphoid homeostasis. Annu. Rev. Immunol. 24, 657-679.
44. Mazzucchelli, R., Durum, S. K. (2007) Interleukin-7 receptor expression: intelligent design. Nat. Rev. Immunol. 7, 144-154.
45. Shalapour, S., Deiser, K., Sercan, O., Tuckermann, J., Minnich, K., Willimsky, G., Blankenstein, T., Hammerling, G. J., Arnold, B., Schuler, T. (2010) Commensal microflora and interferon-γ promote steady-state interleukin-7 production in vivo. Eur. J. Immunol. 40, 2391-2400
46. Oshima, S., Nakamura, T., Namiki, S., Okada, E., Tsuchiya, K., Okamoto, R., Yamazaki, M., Yokota, T., Aida, M., Yamaguchi, Y., Kanai, T., Handa, H., Watanabe, M. (2004) Interferon regulatory factor 1 (IRF-1) and IRF-2 distinctively up-regulate gene expression and production of interleukin-7 in human intestinal epithelial cells. Mol. Cell. Biol. 24, 6298-6310.
47. Sawa, S., Kamimura, D., Jin, G. H., Morikawa, H., Kamon, H., Nishihara, M., Ishihara, K., Murakami, M., Hirano, T. (2006) Autoimmune arthritis associated with mutated interleukin (IL)-6 receptor gp130 is driven by STAT3/IL-7-dependent homeostatic proliferation of CD4+ T cells. J. Exp. Med. 203, 1459-1470.
48. Ritter, M., Mennerich, D., Weith, A., Seither, P. (2005) Characterization of Toll-like receptors in primary lung epithelial cells: strong impact of the TLR3 ligand poly(I:C) on the regulation of Toll-like receptors, adaptor proteins and inflammatory response. J. Inflamm. 2, 16.
49. Honda, K., Yanai, H., Negishi, H., Asagiri, M., Sato, M., Mizutani, T., Shimada, N., Ohba, Y., Takaoka, A., Yoshida, N., Taniguchi, T. (2005) IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 434, 772-777.
50. Goldrath, A. W., Sivakumar, P. V., Glaccum, M., Kennedy, M. K., Bevan, M. J., Benoist, C., Mathis, D., Butz, E. A. (2002) Cytokine requirements for acute and basal homeostatic proliferation of naive and memory CD8+ T cells. J. Exp. Med. 195, 1515-1522.
51. Kaech, S. M., Tan, J. T., Wherry, E. J., Konieczny, B. T., Surh, C. D., Ahmed, R. (2003) Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat. Immunol. 4, 1191-1198.
52. Sudo, T., Nishikawa, S., Ohno, N., Akiyama, N., Tamakoshi, M., Yoshida, H. (1993) Expression and function of the interleukin 7 receptor in murine lymphocytes. Proc. Natl. Acad. Sci. USA 90, 9125-9129.
53. Deshmane, S. L., Kremlev, S., Amini, S., Sawaya, B. E. (2009) Monocyte chemoattractant protein-1 (MCP-1): an overview. J. Interferon Cytokine Res. 29, 313-326.
54. Bracke, K. R., Demedts, I. K., Joos, G. F., Brusselle, G. G. (2007) CCchemokine receptors in chronic obstructive pulmonary disease. Inflamm. Allergy Drug Targets 6, 75-79.
55. Culley, F. J. (2009) Natural killer cells in infection and inflammation of the lung. Immunology 128, 151-163.
56. McCartney, S., Vermi, W., Gilfillan, S., Cella, M., Murphy, T. L., Schreiber, R. D., Murphy, K. M., Colonna, M. (2009) Distinct and complementary functions of MDA5 and TLR3 in poly(I: C)-mediated activation of mouse NK cells. J. Exp. Med. 206, 2967-2976.
57. Kim, K. D., Zhao, J., Auh, S., Yang, X., Du, P., Tang, H., Fu, Y. X. (2007) Adaptive immune cells temper initial innate responses. Nat. Med. 13, 1248-1252.
58. Schmidt, K. N., Leung, B., Kwong, M., Zarember, K. A., Satyal, S., Navas, T. A., Wang, F., Godowski, P. J. (2004) APC-independent activation of NK cells by the Toll-like receptor 3 agonist double-stranded RNA. J. Immunol. 172, 138-143.
59. Lauzon, N. M., Mian, F., MacKenzie, R., Ashkar, A. A. (2006) The direct effects of Toll-like receptor ligands on human NK cell cytokine production and cytotoxicity. Cell. Immunol. 241, 102-112.
60. Baccala, R., Hoebe, K., Kono, D. H., Beutler, B., Theofilopoulos, A. N. (2007) TLR-dependent and TLR-independent pathways of type I interferon induction in systemic autoimmunity. Nat. Med. 13, 543-551.
61. Takeuchi, O., Akira, S. (2008) MDA5/RIG-I and virus recognition. Curr. Opin. Immunol. 20, 17-22.
62. Kato, H., Takeuchi, O., Sato, S., Yoneyama, M., Yamamoto, M., Matsui, K., Uematsu, S., Jung, A., Kawai, T., Ishii, K. J., Yamaguchi, O., Otsu, K., Tsujimura, T., Koh, C. S., Reise Sousa, C., Matsuura, Y., Fujita, T., Akira, S. (2006) Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441, 101-105.
63. Wang, Q., Miller, D. J., Bowman, E. R., Nagarkar, D. R., Schneider, D., Zhao, Y., Linn, M. J., Goldsmith, A. M., Bentley, J. K., Sajjan, U. S., Hershenson, M. B. (2011) MDA5 and TLR3 initiate pro-inflammatory signaling pathways leading to rhinovirus-induced airways inflammation and hyperresponsiveness. PLoS Pathog. 7, e1002070.
64. Andersson, A., Srivastava, M. K., Harris-White, M., Huang, M., Zhu, L., Elashoff, D., Strieter, R. M., Dubinett, S. M., Sharma, S. (2011) Role of CXCR3 ligands in IL-7/IL-7R α-Fc-mediated antitumor activity in lung cancer. Clin. Cancer Res. 17, 3660-3672.
65. Andersson, A., Yang, S. C., Huang, M., Zhu, L., Kar, U. K., Batra, R. K., Elashoff, D., Strieter, R. M., Dubinett, S. M., Sharma, S. (2009) IL-7 promotes CXCR3 ligand-dependent T cell antitumor reactivity in lung cancer. J. Immunol. 182, 6951-6958.
66. Martinez, F. O., Helming, L., Gordon, S. (2009) Alternative activation of macrophages: an immunologic functional perspective. Annu. Rev. Immunol. 27, 451-483.
67. Martinez, F. O., Gordon, S., Locati, M., Mantovani, A. (2006) Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J. Immunol. 177, 7303-7311.
68. Sica, A., Bronte, V. (2007) Altered macrophage differentiation and immune dysfunction in tumor development. J. Clin. Invest. 117, 1155-1166.
69. Pettersen, J. S., Fuentes-Duculan, J., Suarez-Farinas, M., Pierson, K. C., Pitts-Kiefer, A., Fan, L., Belkin, D. A., Wang, C. Q., Bhuvanendran, S., Johnson-Huang, L. M., Bluth, M. J., Krueger, J. G., Lowes, M. A., Carucci, J. A. (2011) Tumor-associated macrophages in the cutaneous SCC microenvironment are heterogeneously activated. J. Invest. Dermatol. 131, 1322-1330.
70. Zhou, Z. H., Han, Y., Wei, T., Aras, S., Chaturvedi, P., Tyler, S., Rani, M. R., Ransohoff, R. M. (2001) Regulation of monocyte chemoattractant protein (MCP)-1 transcription by interferon-gamma (IFN-γ) in human astrocytoma cells: postinduction refractory state of the gene, governed by its upstream elements. FASEB J. 15, 383-392.
71. Van der Velden, V. H., Verheggen, M. M., Bernasconi, S., Sozzani, S., Naber, B. A., van der Linden-van Beurden, C. A., Hoogsteden, H. C., Mantovani, A., Versnel, M. (1998) Interleukin-1β and interferon-γ differentially regulate release of monocyte chemotactic protein-1 and interleukin-8 by human bronchial epithelial cells. Eur. Cytokine Netw. 9, 269-277.