Cellular stress amplifies TLR3/4-Induced CXCL1/2 gene transcription in mononuclear phagocytes via RIPK1

Journal of Immunology

Volumn 193, Issue 2, 2014, Pages 879-888

  Zhao, Chenyang ^a   Pavicic Jr , Paul G ^a   Datta, Shyamasree ^a   Sun, Dongxu ^a   Novotny, Michael ^a   Hamilton, Thomas A ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; CYTOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN KINASE; PROTEIN RIPK1; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL INFILTRATION; CELLULAR STRESS RESPONSE; ENVIRONMENTAL STRESS; ENZYME ACTIVATION; GENE AMPLIFICATION; GENE EXPRESSION; GENETIC TRANSCRIPTION; INTRACELLULAR SIGNALING; LIVER CELL; MOLECULAR MECHANICS; MONONUCLEAR PHAGOCYTE; MOUSE; NONHUMAN; PERITONEAL CAVITY; PERITONEUM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; UBIQUITINATION;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; BLOTTING, WESTERN; CELL LINE; CELLS, CULTURED; CHEMOKINE CXCL1; CHEMOKINE CXCL2; CYTOKINES; DIMETHYL SULFOXIDE; DNA-BINDING PROTEINS; GENE EXPRESSION; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELOID CELLS; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TOLL-LIKE RECEPTOR 3; TOLL-LIKE RECEPTOR 4; TRANSCRIPTION FACTORS; TUNICAMYCIN;

EID: 84904250820     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1303396     Document Type: Article

References (83)

1. Thorp, E., T. Iwawaki, M. Miura, and I. Tabas. 2011. A reporter for tracking the UPR in vivo reveals patterns of temporal and cellular stress during atherosclerotic progression. J. Lipid Res. 52: 1033-1038.
2. Kitamura, M. 2008. Endoplasmic reticulum stress and unfolded protein response in renal pathophysiology: Janus faces. Am. J. Physiol. Renal Physiol. 295: F323-F334.
3. Wang, S., and R. J. Kaufman. 2012. The impact of the unfolded protein response on human disease. J. Cell Biol. 197: 857-867.
4. Kaser, A., A. H. Lee, A. Franke, J. N. Glickman, S. Zeissig, H. Tilg, E. E. Nieuwenhuis, D. E. Higgins, S. Schreiber, L. H. Glimcher, and R. S. Blumberg. 2008. XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease. Cell 134: 743-756.
5. Zhang, K., and R. J. Kaufman. 2008. From endoplasmic-reticulum stress to the inflammatory response. Nature 454: 455-462.
6. Todd, D. J., A. H. Lee, and L. H. Glimcher. 2008. The endoplasmic reticulum stress response in immunity and autoimmunity. Nat. Rev. Immunol. 8: 663-674.
7. Martinon, F., and L. H. Glimcher. 2011. Regulation of innate immunity by signaling pathways emerging from the endoplasmic reticulum. Curr. Opin. Immunol. 23: 35-40.
8. Akira, S., S. Uematsu, and O. Takeuchi. 2006. Pathogen recognition and innate immunity. Cell 124: 783-801. (Pubitemid 43261452)
9. Bauer, S., T. Müller, and S. Hamm. 2009. Pattern recognition by Toll-like receptors. Adv. Exp. Med. Biol. 653: 15-34.
10. Bianchi, M. E. 2007. DAMPs, PAMPs and alarmins: all we need to know about danger. J. Leukoc. Biol. 81: 1-5. (Pubitemid 46028489)
11. Kawai, T., and S. Akira. 2006. TLR signaling. Cell Death Differ. 13: 816-825.
12. West, A. P., A. A. Koblansky, and S. Ghosh. 2006. Recognition and signaling by Toll-like receptors. Annu. Rev. Cell Dev. Biol. 22: 409-437.
13. Blasius, A. L., and B. Beutler. 2010. Intracellular Toll-like receptors. Immunity 32: 305-315.
14. Schröder, M., and R. J. Kaufman. 2005. The mammalian unfolded protein response. Annu. Rev. Biochem. 74: 739-789. (Pubitemid 40995523)
15. Shang, F., and A. Taylor. 2011. Ubiquitin-proteasome pathway and cellular responses to oxidative stress. Free Radic. Biol. Med. 51: 5-16.
16. Flynn, R. L., and L. Zou. 2011. ATR: a master conductor of cellular responses to DNA replication stress. Trends Biochem. Sci. 36: 133-140.
17. Bakkenist, C. J., and M. B. Kastan. 2004. Initiating cellular stress responses. Cell 118: 9-17. (Pubitemid 38902810)
18. Hotamisligil, G. S. 2010. Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 140: 900-917.
19. Reuter, S., S. C. Gupta, M. M. Chaturvedi, and B. B. Aggarwal. 2010. Oxidative stress, inflammation, and cancer: how are they linked? Free Radic. Biol. Med. 49: 1603-1616.
20. Rath, E., and D. Haller. 2011. Inflammation and cellular stress: a mechanistic link between immune-mediated and metabolically driven pathologies. Eur. J. Nutr. 50: 219-233.
21. Kraskiewicz, H., and U. FitzGerald. 2012. InterfERing with endoplasmic reticulum stress. Trends Pharmacol. Sci. 33: 53-63.
22. Martinon, F. 2012. The endoplasmic reticulum: a sensor of cellular stress that modulates immune responses. Microbes Infect. 14: 1293-1300.
23. Li, Y., R. F. Schwabe, T. DeVries-Seimon, P. M. Yao, M. C. Gerbod-Giannone, A. R. Tall, R. J. Davis, R. Flavell, D. A. Brenner, and I. Tabas. 2005. Free cholesterol-loaded macrophages are an abundant source of tumor necrosis factor-alpha and interleukin-6: model of NF-k B- and map kinase-dependent inflammation in advanced atherosclerosis. J. Biol. Chem. 280: 21763-21772. (Pubitemid 40827824)
24. Goodall, J. C., C. Wu, Y. Zhang, L. McNeill, L. Ellis, V. Saudek, and J. S. Gaston. 2010. Endoplasmic reticulum stress-induced transcription factor, CHOP, is crucial for dendritic cell IL-23 expression. Proc. Natl. Acad. Sci. USA 107: 17698-17703.
25. DeLay, M. L., M. J. Turner, E. I. Klenk, J. A. Smith, D. P. Sowders, and R. A. Colbert. 2009. HLA-B27 misfolding and the unfolded protein response augment interleukin-23 production and are associated with Th17 activation in transgenic rats. Arthritis Rheum. 60: 2633-2643.
26. Smith, J. A., M. J. Turner, M. L. DeLay, E. I. Klenk, D. P. Sowders, and R. A. Colbert. 2008. Endoplasmic reticulum stress and the unfolded protein response are linked to synergistic IFN-β induction via X-box binding protein 1. Eur. J. Immunol. 38: 1194-1203.
27. Martinon, F., X. Chen, A. H. Lee, and L. H. Glimcher. 2010. TLR activation of the transcription factor XBP1 regulates innate immune responses in macrophages. Nat. Immunol. 11: 411-418.
28. Cusson-Hermance, N., S. Khurana, T. H. Lee, K. A. Fitzgerald, and M. A. Kelliher. 2005. Rip1 mediates the Trif-dependent Toll-like receptor 3- and 4-induced NF-κB activation but does not contribute to interferon regulatory factor 3 activation. J. Biol. Chem. 280: 36560-36566. (Pubitemid 41587731)
29. Meylan, E., K. Burns, K. Hofmann, V. Blancheteau, F. Martinon, M. Kelliher, and J. Tschopp. 2004. RIP1 is an essential mediator of Toll-like receptor 3-induced NF-κB activation. Nat. Immunol. 5: 503-507. (Pubitemid 38660462)
30. He, S., Y. Liang, F. Shao, and X. Wang. 2011. Toll-like receptors activate programmed necrosis in macrophages through a receptor-interacting kinase-3-mediated pathway. Proc. Natl. Acad. Sci. USA 108: 20054-20059.
31. Lee, A. H., N. N. Iwakoshi, K. C. Anderson, and L. H. Glimcher. 2003. Proteasome inhibitors disrupt the unfolded protein response in myeloma cells. Proc. Natl. Acad. Sci. USA 100: 9946-9951.
32. Mandal, P., and T. Hamilton. 2007. Signaling in lipopolysaccharide- induced stabilization of formyl peptide receptor 1 mRNA in mouse peritoneal macrophages. J. Immunol. 178: 2542-2548. (Pubitemid 46233456)
33. Ohmori, Y., and T. A. Hamilton. 1995. The interferon-stimulated response element and a κB site mediate synergistic induction of murine IP-10 gene transcription by IFN-γ and TNF-α. J. Immunol. 154: 5235-5244.
34. Ohmori, Y., J. Tebo, S. Nedospasov, and T. A. Hamilton. 1994. κB binding activity in a murine macrophage-like cell line. Sequence-specific differences in κB binding and transcriptional activation functions. J. Biol. Chem. 269: 17684-17690.
35. Dai, Y., S. Datta, M. Novotny, and T. A. Hamilton. 2003. TGFβ inhibits LPS-induced chemokine mRNA stabilization. Blood 102: 1178-1185. (Pubitemid 36988020)
36. Ohmori, Y., S. Fukumoto, and T. A. Hamilton. 1995. Two structurally distinct κB sequence motifs cooperatively control LPS-induced KC gene transcription in mouse macrophages. J. Immunol. 155: 3593-3600.
37. Yu, M. C., C. H. Chen, X. Liang, L. Wang, C. R. Gandhi, J. J. Fung, L. Lu, and S. Qian. 2004. Inhibition of T-cell responses by hepatic stellate cells via B7-H1-mediated T-cell apoptosis in mice. Hepatology 40: 1312-1321. (Pubitemid 39657005)
38. Novotny, M., S. Datta, R. Biswas, and T. Hamilton. 2005. Functionally independent AU-rich sequence motifs regulate KC (CXCL1) mRNA. J. Biol. Chem. 280: 30166-30174. (Pubitemid 41216195)
39. Zhao, C., S. Datta, P. Mandal, S. Xu, and T. Hamilton. 2010. Stress-sensitive regulation of IFRD1 mRNA decay is mediated by an upstream open reading frame. J. Biol. Chem. 285: 8552-8562.
40. Arima, Y., M. Harada, D. Kamimura, J. H. Park, F. Kawano, F. E. Yull, T. Kawamoto, Y. Iwakura, U. A. Betz, G. Márquez, et al. 2012. Regional neural activation defines a gateway for autoreactive T cells to cross the blood-brain barrier. Cell 148: 447-457.
41. Pagano, M. B., M. A. Bartoli, T. L. Ennis, D. Mao, P. M. Simmons, R. W. Thompson, and C. T. Pham. 2007. Critical role of dipeptidyl peptidase I in neutrophil recruitment during the development of experimental abdominal aortic aneurysms. Proc. Natl. Acad. Sci. USA 104: 2855-2860. (Pubitemid 46327969)
42. Liu, Y. P., L. Zeng, A. Tian, A. Bomkamp, D. Rivera, D. Gutman, G. N. Barber, J. K. Olson, and J. A. Smith. 2012. Endoplasmic reticulum stress regulates the innate immunity critical transcription factor IRF3. J. Immunol. 189: 4630-4639.
43. Ea, C. K., and D. Baltimore. 2009. Regulation of NF-κB activity through lysine monomethylation of p65. Proc. Natl. Acad. Sci. USA 106: 18972-18977.
44. Yeretssian, G., R. G. Correa, K. Doiron, P. Fitzgerald, C. P. Dillon, D. R. Green, J. C. Reed, and M. Saleh. 2011. Non-apoptotic role of BID in inflammation and innate immunity. Nature 474: 96-99.
45. Zak, D. E., F. Schmitz, E. S. Gold, A. H. Diercks, J. J. Peschon, J. S. Valvo, A. Niemistö, I. Podolsky, S. G. Fallen, R. Suen, et al. 2011. Systems analysis identifies an essential role for SHANK-associated RH domain-interacting protein (SHARPIN) in macrophage Toll-like receptor 2 (TLR2) responses. Proc. Natl. Acad. Sci. USA 108: 11536-11541.
46. Zhang, K., and R. J. Kaufman. 2008. Identification and characterization of endoplasmic reticulum stress-induced apoptosis in vivo. Methods Enzymol. 442: 395-419.
47. Datta, S., R. Biswas, M. Novotny, P. G. Pavicic, Jr., T. Herjan, P. Mandal, and T. A. Hamilton. 2008. Tristetraprolin regulates CXCL1 (KC) mRNA stability. J. Immunol. 180: 2545-2552.
48. Lennarz, W. J. 1975. Lipid linked sugars in glycoprotein synthesis. Science 188: 986-991.
49. Lytton, J., M. Westlin, and M. R. Hanley. 1991. Thapsigargin inhibits the sarcoplasmic or endoplasmic reticulum Ca-ATPase family of calcium pumps. J. Biol. Chem. 266: 17067-17071. (Pubitemid 21907906)
50. Toshchakov, V., B. W. Jones, P. Y. Perera, K. Thomas, M. J. Cody, S. Zhang, B. R. Williams, J. Major, T. A. Hamilton, M. J. Fenton, and S. N. Vogel. 2002. TLR4, but not TLR2, mediates IFN-β-induced STAT1α/β- dependent gene expression in macrophages. Nat. Immunol. 3: 392-398. (Pubitemid 34308628)
51. Ohmori, Y., and T. A. Hamilton. 2001. Requirement for STAT1 in LPS-induced gene expression in macrophages. J. Leukoc. Biol. 69: 598-604. (Pubitemid 32294845)
52. Chen, L., S. Jarujaron, X. Wu, L. Sun, W. Zha, G. Liang, X. Wang, E. C. Gurley, E. J. Studer, P. B. Hylemon, et al. 2009. HIV protease inhibitor lopinavir-induced TNF-α and IL-6 expression is coupled to the unfolded protein response and ERK signaling pathways in macrophages. Biochem. Pharmacol. 78: 70-77.
53. Zeng, L., Y. P. Liu, H. Sha, H. Chen, L. Qi, and J. A. Smith. 2010. XBP-1 couples endoplasmic reticulum stress to augmented IFN-β induction via a cisacting enhancer in macrophages. J. Immunol. 185: 2324-2330.
54. Zhang, P., B. C. McGrath, J. Reinert, D. S. Olsen, L. Lei, S. Gill, S. A. Wek, K. M. Vattem, R. C. Wek, S. R. Kimball, et al. 2002. The GCN2 eIF2α kinase is required for adaptation to amino acid deprivation in mice. Mol. Cell. Biol. 22: 6681-6688.
55. Menu, P., A. Mayor, R. Zhou, A. Tardivel, H. Ichijo, K. Mori, and J. Tschopp. 2012. ER stress activates the NLRP3 inflammasome via an UPR-independent pathway. Cell Death Dis. 3: e261.
56. Ea, C. K., L. Deng, Z. P. Xia, G. Pineda, and Z. J. Chen. 2006. Activation of IKK by TNFα requires site-specific ubiquitination of RIP1 and polyubiquitin binding by NEMO. Mol. Cell 22: 245-257.
57. Christofferson, D. E., Y. Li, and J. Yuan. 2014. Control of life-or-death decisions by RIP1 kinase. Annu. Rev. Physiol. 76: 129-150.
58. Vandenabeele, P., W. Declercq, F. Van Herreweghe, and T. Vanden Berghe. 2010. The role of the kinases RIP1 and RIP3 in TNF-induced necrosis. Sci. Signal. 3: re4.
59. Festjens, N., T. Vanden Berghe, S. Cornelis, and P. Vandenabeele. 2007. RIP1, a kinase on the crossroads of a cell's decision to live or die. Cell Death Differ. 14: 400-410.
60. Meylan, E., and J. Tschopp. 2005. The RIP kinases: crucial integrators of cellular stress. Trends Biochem. Sci. 30: 151-159. (Pubitemid 40332531)
61. Lee, T. H., J. Shank, N. Cusson, and M. A. Kelliher. 2004. The kinase activity of Rip1 is not required for tumor necrosis factor-α-induced IκB kinase or p38 MAP kinase activation or for the ubiquitination of Rip1 by Traf2. J. Biol. Chem. 279: 33185-33191. (Pubitemid 39062963)
62. Ofengeim, D., and J. Yuan. 2013. Regulation of RIP1 kinase signalling at the crossroads of inflammation and cell death. Nat. Rev. Mol. Cell Biol. 14: 727-736.
63. Boone, D. L., E. E. Turer, E. G. Lee, R. C. Ahmad, M. T. Wheeler, C. Tsui, P. Hurley, M. Chien, S. Chai, O. Hitotsumatsu, et al. 2004. The ubiquitin-modifying enzyme A20 is required for termination of Toll-like receptor responses. Nat. Immunol. 5: 1052-1060. (Pubitemid 41057725)
64. Cullen, S. P., C. M. Henry, C. J. Kearney, S. E. Logue, M. Feoktistova, G. A. Tynan, E. C. Lavelle, M. Leverkus, and S. J. Martin. 2013. Fas/CD95-induced chemokines can serve as "find-me" signals for apoptotic cells. Mol. Cell 49: 1034-1048.
65. Cai, Q., H. Sun, Y. Peng, J. Lu, Z. Nikolovska-Coleska, D. McEachern, L. Liu, S. Qiu, C. Y. Yang, R. Miller, et al. 2011. A potent and orally active antagonist (SM-406/AT-406) of multiple inhibitor of apoptosis proteins (IAPs) in clinical development for cancer treatment. J. Med. Chem. 54: 2714-2726.
66. Hamilton, T. A. 2002. Molecular basis of macrophage activation: from gene expression to phenotypic diversity. In The Macrophage, 2nd ed. C. Lewis, and B. Burke, eds. Oxford University Press, Oxford, U.K., p. 73-102.
67. Hamilton, T., X. Li, M. Novotny, P. G. Pavicic, Jr., S. Datta, C. Zhao, J. Hartupee, and D. Sun. 2012. Cell type- and stimulus-specific mechanisms for post-transcriptional control of neutrophil chemokine gene expression. J. Leukoc. Biol. 91: 377-383.
68. Mahadevan, N. R., J. Rodvold, H. Sepulveda, S. Rossi, A. F. Drew, and M. Zanetti. 2011. Transmission of endoplasmic reticulum stress and proinflammation from tumor cells to myeloid cells. Proc. Natl. Acad. Sci. USA 108: 6561-6566.
69. Zhang, K., X. Shen, J. Wu, K. Sakaki, T. Saunders, D. T. Rutkowski, S. H. Back, and R. J. Kaufman. 2006. Endoplasmic reticulum stress activates cleavage of CREBH to induce a systemic inflammatory response. Cell 124: 587-599. (Pubitemid 43199443)
70. Janssens, S., A. Tinel, S. Lippens, and J. Tschopp. 2005. PIDD mediates NF-κB activation in response to DNA damage. Cell 123: 1079-1092. (Pubitemid 41785422)
71. Ando, K., J. L. Kernan, P. H. Liu, T. Sanda, E. Logette, J. Tschopp, A. T. Look, J. Wang, L. Bouchier-Hayes, and S. Sidi. 2012. PIDD death-domain phosphorylation by ATM controls prodeath versus prosurvival PIDDosome signaling. Mol. Cell 47: 681-693.
72. Yamamoto, M., S. Sato, H. Hemmi, K. Hoshino, T. Kaisho, H. Sanjo, O. Takeuchi, M. Sugiyama, M. Okabe, K. Takeda, and S. Akira. 2003. Role of adaptor TRIF in the MyD88-independent Toll-like receptor signaling pathway. Science 301: 640-643. (Pubitemid 36927946)
73. Anderson, P. 2008. Post-transcriptional control of cytokine production. Nat. Immunol. 9: 353-359. (Pubitemid 351405104)
74. Kitamura, M. 2011. Control of NF-κB and inflammation by the unfolded protein response. Int. Rev. Immunol. 30: 4-15.
75. Deng, J., P. D. Lu, Y. Zhang, D. Scheuner, R. J. Kaufman, N. Sonenberg, H. P. Harding, and D. Ron. 2004. Translational repression mediates activation of nuclear factor κB by phosphorylated translation initiation factor 2. Mol. Cell. Biol. 24: 10161-10168. (Pubitemid 39507856)
76. Jiang, H. Y., S. A. Wek, B. C. McGrath, D. Scheuner, R. J. Kaufman, D. R. Cavener, and R. C. Wek. 2003. Phosphorylation of the alpha subunit of eukaryotic initiation factor 2 is required for activation of NF-κB in response to diverse cellular stresses. Mol. Cell. Biol. 23: 5651-5663. (Pubitemid 36951330)
77. Gordon, S., and P. R. Taylor. 2005. Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 5: 953-964. (Pubitemid 41746764)
78. Geissmann, F., S. Jung, and D. R. Littman. 2003. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19: 71-82. (Pubitemid 36859902)
79. Sunderkötter, C., T. Nikolic, M. J. Dillon, N. Van Rooijen, M. Stehling, D. A. Drevets, and P. J. Leenen. 2004. Subpopulations of mouse blood monocytes differ in maturation stage and inflammatory response. J. Immunol. 172: 4410-4417. (Pubitemid 38375256)
80. Auffray, C., M. H. Sieweke, and F. Geissmann. 2009. Blood monocytes: development, heterogeneity, and relationship with dendritic cells. Annu. Rev. Immunol. 27: 669-692.
81. Platt, A. M., C. C. Bain, Y. Bordon, D. P. Sester, and A. M. Mowat. 2010. An independent subset of TLR expressing CCR2-dependent macrophages promotes colonic inflammation. J. Immunol. 184: 6843-6854.
82. Tsuji, H., N. Mukaida, A. Harada, S. Kaneko, E. Matsushita, Y. Nakanuma, H. Tsutsui, H. Okamura, K. Nakanishi, Y. Tagawa, et al. 1999. Alleviation of lipopolysaccharide-induced acute liver injury in Propionibacterium acnesprimed IFN-γ-deficient mice by a concomitant reduction of TNF-α, IL-12, and IL-18 production. J. Immunol. 162: 1049-1055. (Pubitemid 29035433)
83. Lukens, J. R., P. Vogel, G. R. Johnson, M. A. Kelliher, Y. Iwakura, M. Lamkanfi, and T. D. Kanneganti. 2013. RIP1-driven autoinflammation targets IL-1α independently of inflammasomes and RIP3. Nature 498: 224-227.