Dissociation of endotoxin tolerance and differentiation of alternatively activated macrophages

Journal of Immunology

Volumn 190, Issue 9, 2013, Pages 4763-4772

  Rajaiah, Rajesh ^a   Perkins, Darren J ^a   Polumuri, Swamy Kumar ^a   Zhao, Aiping ^a   Keegan, Achsah D ^a   Vogel, Stefanie N ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; GALACTOSAMINE; HISTONE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 4 RECEPTOR ALPHA; LIPOPOLYSACCHARIDE; MACROPHAGE DERIVED CHEMOKINE; MITOGEN ACTIVATED PROTEIN KINASE; MONOCYTE CHEMOTACTIC PROTEIN 1; STAT6 PROTEIN; THYMUS AND ACTIVATION REGULATED CHEMOKINE; TRICHOSTATIN A;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DEACETYLATION; ENDOTOXIN TOLERANCE; ENZYME ACTIVATION; GENE EXPRESSION PROFILING; IN VIVO STUDY; LETHALITY; MACROPHAGE ACTIVATION; MOLECULAR BIOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN BLOOD LEVEL; SIGNAL TRANSDUCTION; TOXICITY TESTING; WILD TYPE;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; ENDOTOXINS; IMMUNE TOLERANCE; INTERLEUKIN-13; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; NF-KAPPA B; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; STAT6 TRANSCRIPTION FACTOR; TRANSCRIPTOME;

EID: 84876807851     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1202407     Document Type: Article

References (67)

1. Beutler, B. 2004. Inferences, questions and possibilities in Toll-like receptor signalling. Nature 430: 257-263. (Pubitemid 38902439)
2. Medzhitov, R. 2001. Toll-like receptors and innate immunity. Nat. Rev. Immunol. 1: 135-145. (Pubitemid 33741967)
3. Daubeuf, B., J. Mathison, S. Spiller, S. Hugues, S. Herren, W. Ferlin, M. Kosco-Vilbois, H. Wagner, C. J. Kirschning, R. Ulevitch, and G. Elson. 2007. TLR4/MD-2 monoclonal antibody therapy affords protection in experimental models of septic shock. J. Immunol. 179: 6107-6114.
4. O'Neill, L. A. 2006. How Toll-like receptors signal: what we know and what we don't know. Curr. Opin. Immunol. 18: 3-9. (Pubitemid 43049641)
5. Beutler, B., and A. Poltorak. 2001. Sepsis and evolution of the innate immune response. Crit. Care. Med. 29(7 Suppl.): S2-6; discussion S6-7.
6. Biswas, S. K., and E. Lopez-Collazo. 2009. Endotoxin tolerance: new mechanisms, molecules and clinical significance. Trends Immunol. 30: 475-487.
7. Dobrovolskaia, M. A., and S. N. Vogel. 2002. Toll receptors, CD14, and macrophage activation and deactivation by LPS. Microbes Infect. 4: 903-914. (Pubitemid 34775232)
8. West, M. A., and W. Heagy. 2002. Endotoxin tolerance: A review. Crit. Care Med. 30: S64-S73. (Pubitemid 34131164)
9. Akira, S., and K. Takeda. 2004. Toll-like receptor signalling. Nat. Rev. Immunol. 4: 499-511. (Pubitemid 38931765)
10. Medvedev, A. E., K. M. Kopydlowski, and S. N. Vogel. 2000. Inhibition of lipopolysaccharide-induced signal transduction in endotoxin-tolerized mouse macrophages: dysregulation of cytokine, chemokine, and toll-like receptor 2 and 4 gene expression. J. Immunol. 164: 5564-5574. (Pubitemid 30389795)
11. Perkins, D. J., N. Qureshi, and S. N. Vogel. 2010. A Toll-like receptor-responsive kinase, protein kinase R, is inactivated in endotoxin tolerance through differential K63/K48 ubiquitination. MBio. 1: pii: e00239-10.
12. van't Veer, C., P. S. van den Pangaart, M. A. van Zoelen, M. de Kruif, R. S. Birjmohun, E. S. Stroes, A. F. de Vos, and T. van der Poll. 2007. Induction of IRAK-M is associated with lipopolysaccharide tolerance in a human endo-toxemia model. J. Immunol. 179: 7110-7120.
13. Xiong, Y., and A. E. Medvedev. 2011. Induction of endotoxin tolerance in vivo inhibits activation of IRAK4 and increases negative regulators IRAK-M, SHIP-1, and A20. J. Leukoc. Biol. 90: 1141-1148.
14. Hotchkiss, R. S., C. M. Coopersmith, J. E. McDunn, and T. A. Ferguson. 2009. The sepsis seesaw: tilting toward immunosuppression. Nat. Med. 15: 496-497.
15. Stout, R. D., and J. Suttles. 2004. Functional plasticity of macrophages: reversible adaptation to changing microenvironments. J. Leukoc. Biol. 76: 509-513. (Pubitemid 39129080)
16. Gordon, S., and P. R. Taylor. 2005. Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 5: 953-964. (Pubitemid 41746764)
17. Gordon, S. 2003. Alternative activation of macrophages. Nat. Rev. Immunol. 3: 23-35. (Pubitemid 37328697)
18. Mantovani, A., S. Sozzani, M. Locati, P. Allavena, and A. Sica. 2002. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol. 23: 549-555. (Pubitemid 35223554)
19. Mosser, D. M. 2003. The many faces of macrophage activation. J. Leukoc. Biol. 73: 209-212. (Pubitemid 36158295)
20. Heller, N. M., X. Qi, I. S. Junttila, K. A. Shirey, S. N. Vogel, W. E. Paul, and A. D. Keegan. 2008. Type I IL-4Rs selectively activate IRS-2 to induce target gene expression in macrophages. Sci. Signal. 1: ra17.
21. Shirey, K. A., L. M. Pletneva, A. C. Puche, A. D. Keegan, G. A. Prince, J. C. Blanco, and S. N. Vogel. 2010. Control of RSV-induced lung injury by alternatively activated macrophages is IL-4R alpha-, TLR4-, and IFN-beta-de-pendent. Mucosal Immunol. 3: 291-300.
22. Stein, M., S. Keshav, N. Harris, and S. Gordon. 1992. Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. J. Exp. Med. 176: 287-292.
23. Raes, G., P. De Baetselier, W. Noël, A. Beschin, F. Brombacher, and G. Hassanzadeh Gh. 2002. Differential expression of FIZZ1 and Ym1 in alternatively versus classically activated macrophages. J. Leukoc. Biol. 71: 597-602.
24. Pena, O. M., J. Pistolic, D. Raj, C. D. Fjell, and R. E. Hancock. 2011. Endotoxin tolerance represents a distinctive state of alternative polarization (M2) in human mononuclear cells. J. Immunol. 186: 7243-7254.
25. Porta, C., M. Rimoldi, G. Raes, L. Brys, P. Ghezzi, D. Di Liberto, F. Dieli, S. Ghisletti, G. Natoli, P. De Baetselier, et al. 2009. Tolerance and M2 (alternative) macrophage polarization are related processes orchestrated by p50 nuclear factor kappaB. Proc. Natl. Acad. Sci. USA 106: 14978-14983.
26. Sekiya, T., M. Miyamasu, M. Imanishi, H. Yamada, T. Nakajima, M. Yamaguchi, T. Fujisawa, R. Pawankar, Y. Sano, K. Ohta, et al. 2000. Inducible expression of a Th2-type CC chemokine thymus-and activation-regulated chemokine by human bronchial epithelial cells. J. Immunol. 165: 2205-2213. (Pubitemid 30648752)
27. El Chartouni, C., and M. Rehli. 2010. Comprehensive analysis of TLR4-induced transcriptional responses in interleukin 4-primed mouse macrophages. Immu-nobiology 215: 780-787.
28. McIntire, F. C., H. W. Sievert, G. H. Barlow, R. A. Finley, and A. Y. Lee. 1967. Chemical, physical, biological properties of a lipopolysaccharide from Escher-ichia coli K-235. Biochemistry 6: 2363-2372.
29. Salkowski, C. A., K. Kopydlowski, J. Blanco, M. J. Cody, R. McNally, and S. N. Vogel. 1999. IL-12 is dysregulated in macrophages from IRF-1 and IRF-2 knockout mice. J. Immunol. 163: 1529-1536. (Pubitemid 29352776)
30. Medvedev, A. E., J. C. Blanco, N. Qureshi, and S. N. Vogel. 1999. Limited role of ceramide in lipopolysaccharide-mediated mitogen-activated protein kinase activation, transcription factor induction, and cytokine release. J. Biol. Chem. 274: 9342-9350.
31. Polumuri, S. K., V. Y. Toshchakov, and S. N. Vogel. 2007. Role of phosphatidylinositol-3 kinase in transcriptional regulation of TLR-induced IL-12 and IL-10 by Fc gamma receptor ligation in murine macrophages. J. Immunol. 179: 236-246. (Pubitemid 46986539)
32. Goerdt, S., O. Politz, K. Schledzewski, R. Birk, A. Gratchev, P. Guillot, N. Hakiy, C. D. Klemke, E. Dippel, V. Kodelja, and C. E. Orfanos. 1999. Alternative versus classical activation of macrophages. Pathobiology 67: 222-226. (Pubitemid 30135909)
33. Martinez, F. O., A. Sica, A. Mantovani, and M. Locati. 2008. Macrophage activation and polarization. Front. Biosci. 13: 453-461. (Pubitemid 351599757)
34. Ziegler-Heitbrock, L. 2001. The p50-homodimer mechanism in tolerance to LPS. J. Endotoxin Res. 7: 219-222. (Pubitemid 32894576)
35. Kobayashi, K., L. D. Hernandez, J. E. Galán, C. A. Janeway, Jr., R. Medzhitov, and R. A. Flavell. 2002. IRAK-M is a negative regulator of Toll-like receptor signaling. Cell 110: 191-202. (Pubitemid 34876547)
36. 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)
37. Carmody, R. J., and Y. H. Chen. 2007. Nuclear factor-kappaB: activation and regulation during toll-like receptor signaling. Cell. Mol. Immunol. 4: 31-41.
38. Xiong, Y., F. Qiu, W. Piao, C. Song, L. M. Wahl, and A. E. Medvedev. 2011. Endotoxin tolerance impairs IL-1 receptor-associated kinase (IRAK) 4 and TGF-beta-activated kinase 1 activation, K63-linked polyubiquitination and assembly of IRAK1, TNF receptor-associated factor 6, and IkappaB kinase gamma and increases A20 expression. J. Biol. Chem. 286: 7905-7916.
39. Chen, X., M. El Gazzar, B. K. Yoza, and C. E. McCall. 2009. The NF-kappaB factor RelB and histone H3 lysine methyltransferase G9a directly interact to generate epigenetic silencing in endotoxin tolerance. J. Biol. Chem. 284: 27857-27865.
40. Qin, H., K. L. Roberts, S. A. Niyongere, Y. Cong, C. O. Elson, and E. N. Benveniste. 2007. Molecular mechanism of lipopolysaccharide-induced SOCS-3 gene expression in macrophages and microglia. J. Immunol. 179: 5966-5976.
41. Kobayashi, M., M. N. Kweon, H. Kuwata, R. D. Schreiber, H. Kiyono, K. Takeda, and S. Akira. 2003. Toll-like receptor-dependent production of IL-12p40 causes chronic enterocolitis in myeloid cell-specific Stat3-deficient mice. J. Clin. Invest. 111: 1297-1308. (Pubitemid 36554700)
42. Dasgupta, P., S. P. Chapoval, E. P. Smith, and A. D. Keegan. 2011. Transfer of in vivo primed transgenic T cells supports allergic lung inflammation and FIZZ1 and Ym1 production in an IL-4Ra and STAT6 dependent manner. BMC Immunol. 12: 60.
43. Ford, A. Q., N. M. Heller, L. Stephenson, M. R. Boothby, and A. D. Keegan. 2009. An atopy-associated polymorphism in the ectodomain of the IL-4R(alpha) chain (V50) regulates the persistence of STAT6 phosphorylation. J. Immunol. 183: 1607-1616.
44. Strahl, B. D., and C. D. Allis. 2000. The language of covalent histone modifications. Nature 403: 41-45. (Pubitemid 30038513)
45. Foster, S. L., D. C. Hargreaves, and R. Medzhitov. 2007. Gene-specific control of inflammation by TLR-induced chromatin modifications. Nature 447: 972-978. (Pubitemid 46975746)
46. Nusinzon, I., and C. M. Horvath. 2005. Unexpected roles for deacetylation in interferon-and cytokine-induced transcription. J. Interferon Cytokine Res. 25: 745-748. (Pubitemid 43068485)
47. Henricson, B. E., W. R. Benjamin, and S. N. Vogel. 1990. Differential cytokine induction by doses of lipopolysaccharide and monophosphoryl lipid A that result in equivalent early endotoxin tolerance. Infect. Immun. 58: 2429-2437. (Pubitemid 20228221)
48. Shnyra, A., R. Brewington, A. Alipio, C. Amura, and D. C. Morrison. 1998. Reprogramming of lipopolysaccharide-primed macrophages is controlled by a counterbalanced production of IL-10 and IL-12. J. Immunol. 160: 3729-3736. (Pubitemid 28176074)
49. Zhang, X., and D. C. Morrison. 1993. Lipopolysaccharide structure-function relationship in activation versus reprogramming of mouse peritoneal macrophages. J. Leukoc. Biol. 54: 444-450. (Pubitemid 23347844)
50. Cuschieri, J., J. Billigren, and R. V. Maier. 2006. Endotoxin tolerance attenuates LPS-induced TLR4 mobilization to lipid rafts: a condition reversed by PKC activation. J. Leukoc. Biol. 80: 1289-1297. (Pubitemid 44911046)
51. Nomura, F., S. Akashi, Y. Sakao, S. Sato, T. Kawai, M. Matsumoto, K. Nakanishi, M. Kimoto, K. Miyake, K. Takeda, and S. Akira. 2000. Cutting edge: endotoxin tolerance in mouse peritoneal macrophages correlates with down-regulation of surface toll-like receptor 4 expression. J. Immunol. 164: 3476-3479. (Pubitemid 30169796)
52. Piao, W., C. Song, H. Chen, M. A. Diaz, L. M. Wahl, K. A. Fitzgerald, L. Li, and A. E. Medvedev. 2009. Endotoxin tolerance dysregulates MyD88-and Toll/IL-1R domain-containing adapter inducing IFN-beta-dependent pathways and increases expression of negative regulators of TLR signaling. J. Leukoc. Biol. 86: 863-875.
53. Dobrovolskaia, M. A., A. E. Medvedev, K. E. Thomas, N. Cuesta, V. Toshchakov, T. Ren, M. J. Cody, S. M. Michalek, N. R. Rice, and S. N. Vogel. 2003. Induction of in vitro reprogramming by Toll-like receptor (TLR)2 and TLR4 agonists in murine macrophages: effects of TLR "homotolerance" versus "heterotolerance" on NF-kappa B signaling pathway components. J. Immunol. 170: 508-519. (Pubitemid 36026178)
54. Ziegler-Heitbrock, H. W., A. Wedel, W. Schraut, M. Ströbel, P. Wendelgass, T. Sternsdorf, P. A. Bäuerle, J. G. Haas, and G. Riethmüller. 1994. Tolerance to lipopolysaccharide involves mobilization of nuclear factor kappa B with predominance of p50 homodimers. J. Biol. Chem. 269: 17001-17004. (Pubitemid 24204013)
55. Chen, J., and L. B. Ivashkiv. 2010. IFN-g abrogates endotoxin tolerance by facilitating Toll-like receptor-induced chromatin remodeling. Proc. Natl. Acad. Sci. USA 107: 19438-19443.
56. Iwasaki, A., and R. Medzhitov. 2004. Toll-like receptor control of the adaptive immune responses. Nat. Immunol. 5: 987-995. (Pubitemid 41057715)
57. Qualls, J. E., G. Neale, A. M. Smith, M. S. Koo, A. A. DeFreitas, H. Zhang, G. Kaplan, S. S. Watowich, and P. J. Murray. 2010. Arginine usage in mycobacteria-infected macrophages depends on autocrine-paracrine cytokine signaling. Sci. Signal. 3: ra62.
58. Jenkins, S. J., D. Ruckerl, P. C. Cook, L. H. Jones, F. D. Finkelman, N. van Rooijen, A. S. MacDonald, and J. E. Allen. 2011. Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science 332: 1284-1288.
59. Carmody, R. J., Q. Ruan, S. Palmer, B. Hilliard, and Y. H. Chen. 2007. Negative regulation of toll-like receptor signaling by NF-kappaB p50 ubiquitination blockade. Science 317: 675-678. (Pubitemid 47229968)
60. Liddiard, K., J. S. Welch, J. Lozach, S. Heinz, C. K. Glass, and D. R. Greaves. 2006. Interleukin-4 induction of the CC chemokine TARC (CCL17) in murine macrophages is mediated by multiple STAT6 sites in the TARC gene promoter. BMC Mol. Biol. 7: 45.
61. Katz, Y., and R. C. Strunk. 1990. Enhanced synthesis of factor B induced by tumor necrosis factor in human skin fibroblasts is decreased by IL-4. J. Immunol. 144: 4675-4680. (Pubitemid 20224102)
62. Cox, G. W., U. Chattopadhyay, J. J. Oppenheim, and L. Varesio. 1991. IL-4 inhibits the costimulatory activity of IL-2 or picolinic acid but not of lipo-polysaccharide on IFN-gamma-treated macrophages. J. Immunol. 147: 3809-3814.
63. Levings, M. K., and J. W. Schrader. 1999. IL-4 inhibits the production of TNF-alpha and IL-12 by STAT6-dependent and-independent mechanisms. J. Immunol. 162: 5224-5229. (Pubitemid 29307127)
64. Kelly-Welch, A. E., E. M. Hanson, M. R. Boothby, and A. D. Keegan. 2003. Interleukin-4 and interleukin-13 signaling connections maps. Science 300: 1527-1528. (Pubitemid 36686713)
65. de Waal Malefyt, R., J. Abrams, B. Bennett, C. G. Figdor, and J. E. de Vries. 1991. Interleukin 10(IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J. Exp. Med. 174: 1209-1220.
66. Fiorentino, D. F., A. Zlotnik, T. R. Mosmann, M. Howard, and A. O'Garra. 1991. IL-10 inhibits cytokine production by activated macrophages. J. Immunol. 147: 3815-3822.
67. Berg, D. J., R. Kühn, K. Rajewsky, W. Müller, S. Menon, N. Davidson, G. Grünig, and D. Rennick. 1995. Interleukin-10 is a central regulator of the response to LPS in murine models of endotoxic shock and the Shwartzman reaction but not endotoxin tolerance. J. Clin. Invest. 96: 2339-2347.