Dangerous liaisons between interleukin-6 cytokine and toll-like receptor families: A potent combination in inflammation and cancer

Cytokine and Growth Factor Reviews

Volumn 24, Issue 3, 2013, Pages 249-256

  Mansell, Ashley ^a   Jenkins, Brendan J ^a  

^a HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

Cancer; IL 6 family cytokines; Inflammation; STATs; TLRs

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 11; INTERLEUKIN 17; INTERLEUKIN 31; INTERLEUKIN 6; MYELOID DIFFERENTIATION FACTOR 88; STAT1 PROTEIN; STAT3 PROTEIN; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; AUTOCRINE EFFECT; AUTOIMMUNE DISEASE; CARCINOGENESIS; CHRONIC INFLAMMATION; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DENDRITIC CELL; HUMAN; IMMUNOMODULATION; INFLAMMATORY DISEASE; INNATE IMMUNITY; MACROPHAGE; METASTASIS; MOLECULAR PATHOLOGY; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TUMOR GROWTH; TUMOR VASCULARIZATION;

CANCER; IL-6 FAMILY CYTOKINES; INFLAMMATION; STATS; TLRS;

ANIMALS; CYTOKINES; HUMANS; INFLAMMATION; INTERLEUKIN-10; INTERLEUKIN-6; NEOPLASMS; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS;

EID: 84881258773     PISSN: 13596101     EISSN: 18790305     Source Type: Journal    
DOI: 10.1016/j.cytogfr.2013.03.007     Document Type: Article

References (94)

1. Bravo J., Heath J. Receptor recognition by gp130 cytokines. EMBO Journal 2000, 19:2399-2411.
2. Heinrich P., Behrmann I., Haan S., Hermanns H., Muller-Newen G., Schaper F. Principles of interleukin (IL)-6-type cytokine signaling and its regulation. Biochemical Journal 2003, 374:1-20.
3. Silver J., Hunter C. gp130 at the nexus of inflammation, autoimmunity, and cancer. Journal of Leukocyte Biology 2010, 88:1145-1156.
4. Rose-John S., Scheller J., Elson G., Jones S. Interleukin-6 biology is coordinated by membrane-bound and soluble receptors: role in inflammation and cancer. Journal of Leukocyte Biology 2006, 80:227-236.
5. Villarino A., Huang E., Hunter C. Understanding the pro- and anti-inflammatory properties of IL-27. Journal of Immunology 2004, 173:715-720.
6. Kawai T., Akira S. The role of pattern-recognition receptors in innate immunity: update on toll-like receptors. Nature Immunology 2010, 11:373-384.
7. Li X., Jiang S., Tapping R.I. Toll-like receptor signaling in cell proliferation and survival. Cytokine 2010, 49:1-9.
8. Hanahan D., Weinberg R.A. The hallmarks of cancer. Cell 2000, 100:57-70.
9. Pinto A., Morello S., Sorrentino R. Lung cancer and toll-like receptors. Cancer Immunology, Immunotherapy 2011, 60:1211-1220.
10. Rakoff-Nahoum S., Medzhitov R. Toll-like receptors and cancer. Nature Reviews Cancer 2009, 9:57-63.
11. Abdi J., Engels F., Garssen J., Redegeld F. The role of toll-like receptor mediated signaling in the pathogenesis of multiple myeloma. Critical Reviews in Oncology/Hematology 2011, 80:225-240.
12. Basith S., Manavalan B., Yoo T.H., Kim S.G., Choi S. Roles of toll-like receptors in cancer: a double-edged sword for defense and offense. Archives of Pharmacal Research 2012, 35:1297-1316.
13. Carvalho F.A., Aitken J.D., Vijay-Kumar M., Gewirtz A.T. Toll-like receptor-gut microbiota interactions: perturb at your own risk!. Annual Review of Physiology 2012, 74:177-198.
14. Takeuchi O., Hoshino K., Kawai T., Sanjo H., Takada H., Ogawa T., et al. Differential roles of TLR2 and TLR4 in recognition of gram-negative and gram-positive bacterial cell wall components. Immunity 1999, 11:443-451.
15. Jin M.S., Kim S.E., Heo J.Y., Lee M.E., Kim H.M., Paik S.G., et al. Crystal structure of the TLR1-TLR2 heterodimer induced by binding of a tri-acylated lipopeptide. Cell 2007, 130:1071-1082.
16. Guan Y., Ranoa D.R., Jiang S., Mutha S.K., Li X., Baudry J., et al. Human TLRs 10 and 1 share common mechanisms of innate immune sensing but not signaling. Journal of Immunology 2010, 184:5094-5103.
17. Poltorak A., He X., Smirnova I., Liu M.Y., Van Huffel C., Du X., et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 1998, 282:2085-2088.
18. Hayashi F., Smith K.D., Ozinsky A., Hawn T.R., Yi E.C., Goodlett D.R., et al. The innate immune response to bacterial flagellin is mediated by toll-like receptor 5. Nature 2001, 410:1099-1103.
19. Alexopoulou L., Holt A.C., Medzhitov R., Flavell R.A. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 2001, 413:732-738.
20. Heil F., Hemmi H., Hochrein H., Ampenberger F., Kirschning C., Akira S., et al. Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 2004, 303:1526-1529.
21. Lund J.M., Alexopoulou L., Sato A., Karow M., Adams N.C., Gale N.W., et al. Recognition of single-stranded RNA viruses by toll-like receptor 7. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:5598-5603.
22. Hemmi H., Takeuchi O., Kawai T., Kaisho T., Sato S., Sanjo H., et al. A toll-like receptor recognizes bacterial DNA. Nature 2000, 408:740-745.
23. Zhang D., Zhang G., Hayden M.S., Greenblatt M.B., Bussey C., Flavell R.A., et al. A toll-like receptor that prevents infection by uropathogenic bacteria. Science 2004, 303:1522-1526.
24. Yarovinsky F., Zhang D., Andersen J.F., Bannenberg G.L., Serhan C.N., Hayden M.S., et al. TLR11 activation of dendritic cells by a protozoan profilin-like protein. Science 2005, 308:1626-1629.
25. Erridge C. Endogenous ligands of TLR2 and TLR4: agonists or assistants?. Journal of Leukocyte Biology 2010, 87:989-999.
26. Netea M.G., Wijmenga C., O'Neill L.A. Genetic variation in toll-like receptors and disease susceptibility. Nature Immunology 2012, 13:535-542.
27. Takeuchi O., Akira S. Pattern recognition receptors and inflammation. Cell 2010, 140:805-820.
28. Abdelsadik A., Trad A. Toll-like receptors on the fork roads between innate and adaptive immunity. Human Immunology 2011, 72:1188-1193.
29. Fukata M., Abreu M.T. Role of toll-like receptors in gastrointestinal malignancies. Oncogene 2008, 27:234-243.
30. Marques R., Boneca I.G. Expression and functional importance of innate immune receptors by intestinal epithelial cells. Cellular and Molecular Life Sciences 2011, 68:3661-3673.
31. Yu L., Chen S. Toll-like receptors expressed in tumor cells: targets for therapy. Cancer Immunology, Immunotherapy 2008, 57:1271-1278.
32. Amit I., Garber M., Chevrier N., Leite A.P., Donner Y., Eisenhaure T., et al. Unbiased reconstruction of a mammalian transcriptional network mediating pathogen responses. Science 2009, 326:257-263.
33. Gilchrist M., Thorsson V., Li B., Rust A.G., Korb M., Roach J.C., et al. Systems biology approaches identify ATF3 as a negative regulator of toll-like receptor 4. Nature 2006, 441:173-178.
34. Nilsson R., Bajic V.B., Suzuki H., di Bernardo D., Bjorkegren J., Katayama S., et al. Transcriptional network dynamics in macrophage activation. Genomics 2006, 88:133-142.
35. Bode J.G., Ehlting C., Haussinger D. The macrophage response towards LPS and its control through the p38(MAPK)-STAT3 axis. Cellular Signalling 2012, 24:1185-1194.
36. Dong C., Davis R.J., Flavell R.A. MAP kinases in the immune response. Annual Review of Immunology 2002, 20:55-72.
37. Vermeulen L., De Wilde G., Notebaert S., Vanden Berghe W., Haegeman G. Regulation of the transcriptional activity of the nuclear factor-kappaB p65 subunit. Biochemical Pharmacology 2002, 64:963-970.
38. Balkwill F.R., Mantovani A. Cancer-related inflammation: common themes and therapeutic opportunities. Seminars in Cancer Biology 2012, 22:33-40.
39. Kim S., Karin M. Role of TLR2-dependent inflammation in metastatic progression. Annals of the New York Academy of Sciences 2011, 1217:191-206.
40. Mantovani A., Allavena P., Sica A., Balkwill F. Cancer-related inflammation. Nature 2008, 454:436-444.
41. Pidgeon G.P., Harmey J.H., Kay E., Da Costa M., Redmond H.P., Bouchier-Hayes D.J. The role of endotoxin/lipopolysaccharide in surgically induced tumor growth in a murine model of metastatic disease. British Journal of Cancer 1999, 81:1311-1317.
42. Harmey J.H., Bucana C.D., Lu W., Byrne A.M., McDonnell S., Lynch C., et al. Lipopolysaccharide-induced metastatic growth is associated with increased angiogenesis, vascular permeability and tumor cell invasion. International Journal of Cancer 2002, 101:415-422.
43. Jego G., Bataille R., Geffroy-Luseau A., Descamps G., Pellat-Deceunynck C. Pathogen-associated molecular patterns are growth and survival factors for human myeloma cells through toll-like receptors. Leukemia 2006, 20:1130-1137.
44. Bohnhorst J., Rasmussen T., Moen S.H., Flottum M., Knudsen L., Borset M., et al. Toll-like receptors mediate proliferation and survival of multiple myeloma cells. Leukemia 2006, 20:1138-1144.
45. Naugler W.E., Sakurai T., Kim S., Maeda S., Kim K., Elsharkawy A.M., et al. Gender disparity in liver cancer due to sex differences in MyD88-dependent IL-6 production. Science 2007, 317:121-124.
46. Rakoff-Nahoum S., Medzhitov R. Regulation of spontaneous intestinal tumorigenesis through the adaptor protein MyD88. Science 2007, 317:124-127.
47. Swann J.B., Vesely M.D., Silva A., Sharkey J., Akira S., Schreiber R.D., et al. Demonstration of inflammation-induced cancer and cancer immunoediting during primary tumorigenesis. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:652-656.
48. Adachi O., Kawai T., Takeda K., Matsumoto M., Tsutsui H., Sakagami M., et al. Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 1998, 9:143-150.
49. Kim S., Takahashi H., Lin W.W., Descargues P., Grivennikov S., Kim Y., et al. Carcinoma-produced factors activate myeloid cells through TLR2 to stimulate metastasis. Nature 2009, 457:102-106.
50. West X., Malinin N.L., Merkulova A.A., Tischenko M., Kerr B.A., Borden E.C., et al. Oxidative stress induces angiogenesis by activating TLR2 with novel endogenous ligands. Nature Medicine 2010, 467:972-976.
51. Yang H., Cui B., Liu H.Z., Mi S., Yan J., Yan H.M., et al. Blocking TLR2 activity attenuates pulmonary metastases of tumor. PLoS ONE 2009, 4:e6520.
52. Huang B., Zhao J., Shen S., Li H., He K.L., Shen G.X., et al. Listeria monocytogenes promotes tumor growth via tumor cell toll-like receptor 2 signaling. Cancer Research 2007, 67:4346-4352.
53. Shcheblyakov D., Logunov D., Rakovskaya I., Shmarov M., Naroditsky B., Ginzburg A. Triggering of toll-like receptor-2 in mouse myelomonocytic leukaemia cells WEHI-3B leads to the suppression of apoptosis and promotes tumor progression in vivo. Acta Naturae 2011, 3:83-93.
54. Yang H.Z., Cui B., Liu H.Z., Mi S., Yan J., Yan H.M., et al. Blocking TLR2 activity attenuates pulmonary metastases of tumor. PLoS ONE 2009, 4:e6520.
55. Tye H., Kennedy C., Najdovska M., McLeod L., McCormack W., Hughes N., et al. STAT3-driven upregulation of TLR2 promotes gastric tumorigenesis independent of tumor inflammation. Cancer Cell 2012, 22:466-478.
56. Drucker C., Gewiese J., Malchow S., Scheller J., Rose-John S. Impact of interleukin-6 classic- and trans-signaling on liver damage and regeneration. Journal of Autoimmunity 2010, 34:29-37.
57. Mihara M., Hashizume M., Yoshida H., Suzuki M., Shiina M. IL-6/IL-6 receptor system and its role in physiological and pathological conditions. Clinical Science (London) 2012, 122:143-159.
58. Sims N., Walsh N. GP130 cytokines and bone remodelling in health and disease. BMB Reports 2010, 43:513-523.
59. Garbers C., Hermanns H., Schaper F., Müller-Newen G., Grötzinger J., Rose-John S., et al. Plasticity and cross-talk of interleukin 6-type cytokines. Cytokine and Growth Factor Reviews 2012, 23:85-97.
60. Dreuw A., Radtke S., Pflanz S., Lippok B., Heinrich P., Hermanns H. Characterization of the signaling capacities of the novel gp130-like cytokine receptor. Journal of Biological Chemistry 2004, 279:36112-36120.
61. Gerhartz C., Heesel B., Sasse J., Hemmann U., Landgraf C., Schneider-Mergener J., et al. Differential activation of acute phase response factor/STAT3 and STAT1 via the cytoplasmic domain of the interleukin 6 signal transducer gp130. I. Definition of a novel phosphotyrosine motif mediating STAT1 activation. Journal of Biological Chemistry 1996, 271:12991-12998.
62. Takahashi-Tezuka M., Yoshida Y., Fukada T., Ohtani T., Yamanaka Y., Nishida K., et al. Gab1 acts as an adapter molecule linking the cytokine receptor gp130 to ERK mitogen-activated protein kinase. Molecular and Cellular Biology 1998, 18:4109-4117.
63. Nicholson S.E., De Souza D., Fabri L.J., Corbin J., Willson T.A., Zhang J.G., et al. Suppressor of cytokine signaling-3 preferentially binds to the SHP-2- binding site on the shared cytokine receptor subunit gp130. Proceedings of the National Academy of Sciences of the United States of America 2000, 97:6493-6498.
64. Krebs D.L., Hilton D.J. SOCS proteins: negative regulators of cytokine signaling. Journal of Cell Science 2001, 19:378-387.
65. Mosley B., De Imus C., Friend D., Boiani N., Thoma B., Park L., et al. Dual oncostatin M (OSM) receptors. Cloning and characterization of an alternative signaling subunit conferring OSM-specific receptor activation. Journal of Biological Chemistry 1996, 271:32635-32643.
66. Schuster B., Kovaleva M., Sun Y., Regenhard P., Matthews V., Grötzinger J., et al. Signaling of human ciliary neurotrophic factor (CNTF) revisited. The interleukin-6 receptor can serve as an alpha-receptor for CTNF. Journal of Biological Chemistry 2003, 278:9528-9535.
67. Jones S., Scheller J., Rose-John S. Therapeutic strategies for the clinical blockade of IL-6/gp130 signaling. Journal of Clinical Investigation 2011, 121:3375-3383.
68. Zhang J., Wu H., Wang L., Tian Y., Zhang J., Wu H. Expression and significance of TLR4 and HIF-1alpha in pancreatic ductal adenocarcinoma. World Journal of Gastroenterology 2010, 16:2881-2888.
69. Ellmark P., Ingvarsson J., Carlsson A., Lundin B.S., Wingren C., Borrebaeck CA Identification of protein expression signatures associated with Helicobacter pylori infection and gastric adenocarcinoma using recombinant antibody microarrays. Molecular and Cellular Proteomics 2006, 5:1638-1646.
70. Ernst M., Najdovska M., Grail D., Lundgren-May T., Buchert M., Tye H., et al. STAT3 and STAT1 mediate IL-11-dependent and inflammation-associated gastric tumorigenesis in gp130 receptor mutant mice. Journal of Clinical Investigation 2008, 118:1727-1738.
71. Bollrath J., Phesse T., von Burstin V., Putoczki T., Bennecke M., Bateman T., et al. gp130-mediated Stat3 activation in enterocytes regulates cell survival and cell-cycle progression during colitis-associated tumorigenesis. Cancer Cell 2009, 15:91-102.
72. Gu D., Fan Q., Zhang X., Xie J. A role for transcription factor STAT3 signaling in oncogene smoothened-driven carcinogenesis. Journal of Biological Chemistry 2012, 287:38356-38366.
73. DiDonato J.A., Mercurio F., Karin M. NF-kappaB and the link between inflammation and cancer. Immunological Reviews 2012, 246:379-400.
74. Bollrath J., Greten F. IKK/NF-kappaB and STAT3 pathways: central signaling hubs in inflammation-mediated tumor promotion and metastasis. EMBO Reports 2009, 10:1314-1319.
75. Yoshimura A. Signal transduction of inflammatory cytokines and tumor development. Cancer Science 2006, 97:439-447.
76. Yang J., Liao X., Agarwal M.K., Barnes L., Auron P.E., Stark G.R. Unphosphorylated STAT3 accumulates in response to IL-6 and activates transcription by binding to NFkappaB. Genes and Development 2007, 21:1396-1408.
77. Hu X., Chakravarty S.D., Ivashkiv L.B. Regulation of interferon and toll-like receptor signaling during macrophage activation by opposing feedforward and feedback inhibition mechanisms. Immunological Reviews 2008, 226:41-56.
78. Nguyen H., Chatterjee-Kishore M., Jiang Z., Qing Y., Ramana C.V., Bayes J., et al. IRAK-dependent phosphorylation of Stat1 on serine 727 in response to interleukin-1 and effects on gene expression. Journal of Interferon and Cytokine Research 2003, 23:183-192.
79. Rhee S.H., Jones B.W., Toshchakov V., Vogel S.N., Fenton M.J. Toll-like receptors 2 and 4 activate STAT1 serine phosphorylation by distinct mechanisms in macrophages. Journal of Biological Chemistry 2003, 278:22506-22512.
80. Schroder K., Spille M., Pilz A., Lattin J., Bode K.A., Irvine K.M., et al. Differential effects of CpG DNA on IFN-beta induction and STAT1 activation in murine macrophages versus dendritic cells: alternatively activated STAT1 negatively regulates TLR signaling in macrophages. Journal of Immunology 2007, 179:3495-3503.
81. Khoo J.J., Forster S., Mansell A. Toll-like receptors as interferon-regulated genes and their role in disease. Journal of Interferon and Cytokine Research 2011, 31:13-25.
82. Jenkins B.J., Grail D., Nheu T., Najdovska M., Wang B., Waring P., et al. Hyperactivation of Stat3 in gp130 mutant mice promotes gastric hyperproliferation and desensitizes TGF-beta signaling. Nature Medicine 2005, 11:845-852.
83. Greenhill C.J., Rose-John S., Lissilaa R., Ferlin W., Ernst M., Hertzog P.J., et al. IL-6 trans-signaling modulates TLR4-dependent inflammatory responses via STAT3. Journal of Immunology 2011, 186:1199-1208.
84. Greenhill C.J., Gould J., Ernst M., Jarnicki A., Hertzog P.J., Mansell A., et al. LPS hypersensitivity of gp130 mutant mice is independent of elevated haemopoietic TLR4 signaling. Immunology and Cell Biology 2012, 90:559-563.
85. Kim T.H., Choi S.E., Ha E.S., Jung J.G., Han S.J., Kim H.J., et al. IL-6 induction of TLR-4 gene expression via STAT3 has an effect on insulin resistance in human skeletal muscle. Acta Diabetologica 2011.
86. Fessler M.B., Rudel L.L., Brown J.M. Toll-like receptor signaling links dietary fatty acids to the metabolic syndrome. Current Opinion in Lipidology 2009, 20:379-385.
87. Guzzo C., Ayer A., Basta S., Banfield B.W., Gee K. IL-27 enhances LPS-induced proinflammatory cytokine production via upregulation of TLR4 expression and signaling in human monocytes. Journal of Immunology 2012, 188:864-873.
88. Inoue K., Takano H., Yanagisawa R., Sakurai M., Shimada A., Morita T., et al. Role of interleukin-6 in toll-like receptor 4 and 2 expressions induced by lipopolysaccharide in the lung. Immunopharmacology and Immunotoxicology 2007, 29:63-68.
89. Bollrath J., Greten F.R. IKK/NF-kappaB and STAT3 pathways: central signaling hubs in inflammation-mediated tumor promotion and metastasis. EMBO Reports 2009, 10:1314-1319.
90. Schroder K., Irvine K.M., Taylor M.S., Bokil N.J., Le Cao K.A., Masterman K.A., et al. Conservation and divergence in toll-like receptor 4-regulated gene expression in primary human versus mouse macrophages. Proceedings of the National Academy of Sciences of the United States of America 2012, 109:E944-E953.
91. de Jong M., Maina T. Of mice and humans: are they the same? Implications in cancer translational research. Journal of Nuclear Medicine 2012, 51:501-504.
92. Libby P., Ridker P.M., Hansson G.K. Progress and challenges in translating the biology of atherosclerosis. Nature 2011, 473:317-325.
93. Sharpless N.E., Depinho R.A. The mighty mouse: genetically engineered mouse models in cancer drug development. Nature Reviews Drug Discovery 2006, 5:741-754.
94. van der Worp H.B., Howells D.W., Sena E.S., Porritt M.J., Rewell S., O'Collins V., et al. Can animal models of disease reliably inform human studies?. PLoS Medicine 2010, 7:e1000245.