Molecular mechanism responsible for the priming of macrophage activation

Journal of Biological Chemistry

Volumn 288, Issue 6, 2013, Pages 3897-3906

  Deng, Hui ^a   Maitra, Urmila ^a   Morris, Matt ^a   Li, Liwu ^a  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENDOTOXINS; BODY WEIGHT; CHRONIC INFLAMMATORY DISEASE; HIGH DOSE; IN-VIVO; LOW DOSE; MACROPHAGE ACTIVATION; MOLECULAR MECHANISM; PHOSPHOINOSITIDE 3-KINASE; PROINFLAMMATORY; SHARP CONTRAST;

ENZYMES; MAMMALS;

MACROPHAGES;

AUTACOID; CELL PROTEIN; ESCHERICHIA COLI LIPOPOLYSACCHARIDE; INTERLEUKIN 6; INTERLEUKIN RECEPTOR ASSOCIATED KINASE 1; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOTRANSFERASE; SODIUM CHLORIDE; TOLL INTERACTING PROTEIN; TRANSCRIPTION FACTOR RELB; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL FUNCTION; CHROMATIN IMMUNOPRECIPITATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; IMMUNOLOGICAL TOLERANCE; IN VIVO STUDY; INFLAMMATION; MACROPHAGE ACTIVATION; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; SIGNAL TRANSDUCTION;

ANIMALS; CELL LINE; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION REGULATION; INFLAMMATION MEDIATORS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIPOPOLYSACCHARIDES; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MICE, MUTANT STRAINS; PHOSPHATIDYLINOSITOL 3-KINASES; TRANSCRIPTION FACTOR RELB;

EID: 84873620317     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.424390     Document Type: Article

References (66)

1. Morris, M., and Li, L. (2012) Molecular mechanisms responsible for the reduced expression of cholesterol transporters from macrophages by low-dose endotoxin. Arch. Immunol. Ther. Exp. 60, 13-18
2. Scheifele, D. W., Olsen, E. M., and Pendray, M. R. (1985) Endotoxinemia and thrombocytopenia during neonatal necrotizing enterocolitis. Am. J. Clin. Pathol. 83, 227-229
3. Dofferhoff, A. S., Nijland, J. H., de Vries-Hospers, H. G., Mulder, P. O., Weits, J., and Bom, V. J. (1991) Effects of different types and combinations of antimicrobial agents on endotoxin release from gram-negative bacteria: an in-vitro and in-vivo study. Scand. J. Infect. Dis. 23, 745-754
4. West, M. A., and Heagy, W. (2002) Endotoxin tolerance: a review. Crit. Care Med. 30, S64-73
5. Zhang, X., and Morrison, D. C. (1993) Lipopolysaccharide-induced selective priming effects on tumor necrosis factor a and nitric oxide production in mouse peritoneal macrophages. J. Exp. Med. 177, 511-516
6. Henricson, B. E., Manthey, C. L., Perera, P. Y., Hamilton, T. A., and Vogel, S. N. (1993) Dissociation of lipopolysaccharide (LPS)-inducible gene expression in murine macrophages pretreated with smooth LPS versus monophosphoryl lipid A. Infect. Immun. 61, 2325-2333
7. Hirohashi, N., and Morrison, D. C. (1996) Low-dose lipopolysaccharide (LPS) pretreatment of mouse macrophages modulates LPS-dependent in-terleukin-6 production in vitro. Infect. Immun. 64, 1011-1015
8. Cani, P. D., Bibiloni, R., Knauf, C, Waget, A., Neyrinck, A. M., Delzenne, N. M., and Burcelin, R. (2008) Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 57, 1470-1481
9. Goto, T., Edén, S., Nordenstam, G., Sundh, V., Svanborg-Edén, C., and Mattsby-Baltzer, I. (1994) Endotoxin levels in sera of elderly individuals. Clin. Diagn. Lab. Immunol. 1, 684-688
10. Ancuta, P., Kamat, A., Kunstman, K. J., Kim, E. Y., Autissier, P., Wurcel, A., Zaman, T., Stone, D., Mefford, M., Morgello, S., Singer, E. J., Wolinsky, S. M., and Gabuzda, D. (2008) Microbial translocation is associated with increased monocyte activation and dementia in AIDS patients. PLoS One 3, e2516
11. Szeto, C.C, Kwan, B. C, Chow, K.M., Lai, K.B., Chung, K. Y., Leung, C.B., and Li, P. K. (2008) Endotoxemia is related to systemic inflammation and atherosclerosis in peritoneal dialysis patients. Clin. J. Am. Soc. Nephrol. 3, 431-436
12. Rao, R. (2009) Endotoxemia and gut barrier dysfunction in alcoholic liver disease. Hepatology 50, 638-644
13. De Gaudio, A. R., Rinaldi, S., Chelazzi, C, and Borracci, T. (2009) Pathophysiology of sepsis in the elderly: clinical impact and therapeutic considerations. Curr. Drug Targets 10, 60-70
14. Zahr, F., Genovese, E., Mathier, M., Shullo, M., Lockard, K., Zomak, R., McNamara, D., Toyoda, Y., Kormos, R. L., and Teuteberg, J. J. (2011) Obese patients and mechanical circulatory support: weight loss, adverse events, and outcomes. Ann. Thorac. Surg. 92, 1420-1426
15. Strandberg, L., Verdrengh, M., Enge, M., Andersson, N, Amu, S., Onnheim, K., Benrick, A., Brisslert, M., Bylund, J., Bokarewa, M., Nilsson, S., and Jansson, J. O. (2009) Mice chronically fed high-fat diet have increased mortality and disturbed immune response in sepsis. PLoS One 4, e7605
16. Turnbull, I. R., Clark, A. T., Stromberg, P. E., Dixon, D. J., Woolsey, C. A., Davis, C. G., Hotchkiss, R. S., Buchman, T. G., and Coopersmith, C. M. (2009) Effects of aging on the immunopathologic response to sepsis. Crit. Care Med. 37, 1018-1023
17. Chen, P., Li, J., Barnes, J., Kokkonen, G. C, Lee, J. C, and Liu, Y. (2002) Restraint of proinflammatory cytokine biosynthesis by mitogen-activated protein kinase phosphatase-1 in lipopolysaccharide-stimulated macrophages. J. Immunol. 169, 6408-6416
18. Harada, K., Isse, K., Sato, Y., Ozaki, S., and Nakanuma, Y. (2006) Endotoxin tolerance in human intrahepatic biliary epithelial cells is induced by upregulation of IRAK-M. Liver Int. 26, 935-942
19. Chen, X., El Gazzar, M., Yoza, B. K., and McCall, C. E. (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
20. Salojin, K. V., Owusu, I. B., Millerchip, K. A., Potter, M., Platt, K. A., and Oravecz, T. (2006) Essential role of MAPK phosphatase-1 in the negative control of innate immune responses. J. Immunol. 176, 1899-1907
21. Kobayashi, K., Hernandez, L. D., Galán, J. E., Janeway, C. A., Jr., Medzhi-tov, R., and Flavell, R. A. (2002) IRAK-M is a negative regulator of Toll-like receptor signaling. Cell 110, 191-202
22. Chaurasia, B., Mauer, J., Koch, L., Goldau, J., Kock, A. S., and Brüning, J. C. (2010) Phosphoinositide-dependent kinase 1 provides negative feedback inhibition to Toll-like receptor-mediated NF-KB activation in macro-phages. Mol. Cell Biol. 30, 4354-4366
23. Zacharioudaki, V., Androulidaki, A., Arranz, A., Vrentzos, G., Margioris, A. N, and Tsatsanis, C. (2009) Adiponectin promotes endotoxin tolerance in macrophages by inducing IRAK-M expression. J. Immunol. 182, 6444-6451
24. Medina, E. A., Morris, I. R., and Berton, M. T. (2010) Phosphatidylinositol 3-kinase activation attenuates the TLR2-mediated macrophage proinflammatory cytokine response to Francisella tularensis live vaccine strain. J. Immunol. 185, 7562-7572
25. Zhu, Q. Y., Liu, Q., Chen, J. X., Lan, K., and Ge, B. X. (2010) MicroRNA-101 targets MAPK phosphatase-1 to regulate the activation of MAPKs in macrophages. J. Immunol. 185, 7435-7442
26. Noubir, S., Hmama, Z., and Reiner, N. E. (2004) Dual receptors and distinct pathways mediate interleukin-1 receptor-associated kinase degradation in response to lipopolysaccharide. Involvement of CD14/TLR4, CR3, and phosphatidylinositol 3-kinase. J. Biol. Chem. 279, 25189-25195
27. Maitra, U., Gan, L., Chang, S., and Li, L. (2011) Low-dose endotoxin induces inflammation by selectively removing nuclear receptors and activating CCAAT/enhancer-binding protein 8. J. Immunol. 186, 4467-4473
28. Liu, B., Yang, Y., Qiu, Z., Staron, M., Hong, F., Li, Y., Wu, S., Li, Y., Hao, B., Bona, R., Han, D., and Li, Z. (2010) Folding of Toll-like receptors by the HSP90 paralogue gp96 requires a substrate-specific cochaperone. Nat. Commun. 1, 79
29. Zhang, X., and Morrison, D. C. (1993) Lipopolysaccharide structure-function relationship in activation versus reprogramming of mouse peritoneal macrophages. J. Leukoc. Biol. 54, 444-450
30. Deng, J. C, Cheng, G., Newstead, M. W., Zeng, X., Kobayashi, K., Flavell, R. A., and Standiford, T. J. (2006) Sepsis-induced suppression of lung innate immunity is mediated by IRAK-M. J. Clin. Invest. 116, 2532-2542
31. Androulidaki, A., Iliopoulos, D., Arranz, A., Doxaki, C, Schworer, S., Zacharioudaki, V., Margioris, A. N, Tsichlis, P. N, and Tsatsanis, C. (2009) The kinase Akt1 controls macrophage response to lipopolysaccharide by regulating microRNAs. Immunity 31, 220-231
32. Martin, M., Rehani, K., Jope, R. S., and Michalek, S. M. (2005) Toll-like receptor-mediated cytokine production is differentially regulated by glycogen synthase kinase 3. Nat. Immunol. 6, 777-784
33. Gustin, J. A., Korgaonkar, C K., Pincheira, R., Li, Q., and Donner, D. B. (2006) Akt regulates basal and induced processing of NF-KB2 (p100) to p52. J. Biol. Chem. 281, 16473-16481
34. Xia, Y., Pauza, M. E., Feng, L., and Lo, D. (1997) RelB regulation of chemo-kine expression modulates local inflammation. Am. J. Pathol. 151, 375-387
35. Yoza, B. K., Hu, J. Y., Cousart, S. L., Forrest, L. M., and McCall, C E. (2006) Induction of RelB participates in endotoxin tolerance. J. Immunol. 177, 4080-4085
36. Weih, F., Warr, G., Yang, H., and Bravo, R. (1997) Multifocal defects in immune responses in RelB-deficient mice. J. Immunol. 158, 5211-5218
37. Swantek, J. L., Tsen, M. F., Cobb, M. H, and Thomas, J. A. (2000) IL-1 receptor-associated kinase modulates host responsiveness to endotoxin. J. Immunol. 164, 4301-4306
38. Didierlaurent, A., Brissoni, B., Velin, D., Aebi, N, Tardivel, A., Käslin, E., Sirard, J. C, Angelov, G., Tschopp, J., and Burns, K. (2006) Tollip regulates proinflammatory responses to interleukin-1 and lipopolysaccharide. Mol. Cell Biol. 26, 735-742
39. Neumann, M., Klar, S., Wilisch-Neumann, A., Hollenbach, E., Kavuri, S., Leverkus, M., Kandolf, R., Brunner-Weinzierl, M. C, and Klingel, K. (2011) Glycogen synthase kinase-3/3 is a crucial mediator of signal-induced RelB degradation. Oncogene 30, 2485-2492
40. Dinarello, C. A. (2011) Interleukin-1 in the pathogenesis and treatment of inflammatory diseases. Blood 117, 3720-3732
41. Suzuki, K., Murtuza, B., Beauchamp, J. R., Brand, N. J., Barton, P. J., Varela-Carver, A., Fukushima, S., Coppen, S. R., Partridge, T. A., and Yacoub, M. H. (2004) Role of interleukin-1/3 in acute inflammation and graft death after cell transplantation to the heart. Circulation 110, II219-224
42. Maedler, K., Schumann, D. M., Sauter, N, Ellingsgaard, H, Bosco, D., Baertschiger, R., Iwakura, Y., Oberholzer, J., Wollheim, C. B., Gauthier, B. R., and Donath, M. Y. (2006) Low concentration of interleukin-1/3 induces FLICE-inhibitory protein-mediated β-cell proliferation in human pancreatic islets. Diabetes 55, 2713-2722
43. Mantzoros, C. S., Magkos, F., Brinkoetter, M., Sienkiewicz, E., Dardeno, T. A., Kim, S. Y., Hamnvik, O. P., and Koniaris, A. (2011) Leptin in human physiology and pathophysiology. Am. J. Physiol. Endocrinol. Metab. 301, E567-584
44. Boura-Halfon, S., and Zick, Y. (2009) Phosphorylation of IRS proteins, insulin action, and insulin resistance. Am. J. Physiol. Endocrinol. Metab. 296, E581-591
45. Medvedev, A. E., Lentschat, A., Kuhns, D. B., Blanco, J. C, Salkowski, C, Zhang, S., Arditi, M., Gallin, J. I., and Vogel, S. N. (2003) Distinct mutations in IRAK-4 confer hyporesponsiveness to lipopolysaccharide and interleukin-1 in a patient with recurrent bacterial infections. J. Exp. Med. 198, 521-531
46. Biswas, S. K., and Lopez-Collazo, E. (2009) Endotoxin tolerance: new mechanisms, molecules and clinical significance. Trends Immunol. 30, 475-487
47. Li, L., Cousart, S., Hu, J., and McCall, C. E. (2000) Characterization of interleukin-1 receptor-associated kinase in normal and endotoxin-toler-ant cells. J. Biol. Chem. 275, 23340-23345
48. Ni, M., MacFarlane, A. W., 4th, Toft, M., Lowell, C. A., Campbell, K. S., and Hamerman, J. A. (2012) B-cell adaptor for PI3K (BCAP) negatively regulates Toll-like receptor signaling through activation of PI3K. Proc. Natl. Acad. Sci. U.S.A. 109, 267-272
49. Terragni, J., Graham, J. R., Adams, K. W., Schaffer, M. E., Tullai, J. W., and Cooper, G. M. (2008) Phosphatidylinositol 3-kinase signaling in proliferating cells maintains an anti-apoptotic transcriptional program mediated by inhibition of FOXO and non-canonical activation of NFKB transcription factors. BMC Cell Biol. 9, 6
50. Lochner, M., Peduto, L., Cherrier, M., Sawa, S., Langa, F., Varona, R., Riethmacher, D., Si-Tahar, M., Di Santo, J. P., and Eberl, G. (2008) In vivo equilibrium of proinflammatory IL-17+ and regulatory IL-10+ Foxp3+ ROR7t+ T cells. J. Exp. Med. 205, 1381-1393
51. Zhou, L., Lopes, J. E., Chong, M. M., Ivanov, I.I., Min, R., Victora, G. D., Shen, Y., Du, J., Rubtsov, Y. P., Rudensky, A. Y., Ziegler, S. F., and Littman, D. R. (2008) TGF-β-induced Foxp3 inhibits T(H)17 cell differentiation by antagonizing RORyt function. Nature 453, 236-240
52. Hong, T., Xing, J., Li, L., and Tyson, J. (2011) A mathematical model for the reciprocal differentiation of T helper 17 cells and induced regulatory T cells. PLoS Comput. Biol. 7, e1002122
53. Stewart, C. R., Stuart, L. M., Wilkinson, K., van Gils, J. M., Deng, J., Halle, A., Rayner, K. J., Boyer, L., Zhong, R., Frazier, W. A., Lacy-Hulbert, A., El Khoury, J., Golenbock, D. T., and Moore, K. J. (2010) CD36 ligands promote sterile inflammation through assembly of a Toll-like receptor 4 and 6 heterodimer. Nat. Immunol. 11, 155-161
54. Vogel, S. N., English, K. E., Fertsch, D., and Fultz, M. J. (1983) Differential modulation of macrophage membrane markers by interferon: analysis of Fc and C3b receptors, Mac-1 and Ia antigen expression. J. Interferon Res. 3, 153-160
55. Han, C., Jin, J., Xu, S., Liu, H., Li, N., and Cao, X. (2010) Integrin CD11b negatively regulates TLR-triggered inflammatory responses by activating Syk and promoting degradation of MyD88 and TRIF via Cbl-b. Nat. Immunol. 11, 734-742
56. Li, S., Strelow, A., Fontana, E. J., and Wesche, H. (2002) IRAK-4: a novel member of the IRAK family with the properties of an IRAK-kinase. Proc. Natl. Acad. Sci. U.S.A. 99, 5567-5572
57. Gan, L., and Li, L. (2010) Interleukin-1 receptor-associated kinase-1 (IRAK-1) functionally associates with PKCe and VASP in the regulation of macrophage migration. Mol. Immunol. 47, 1278-1282
58. Medvedev, A. E., Piao, W., Shoenfelt, J., Rhee, S. H, Chen, H, Basu, S., Wahl, L. M., Fenton, M. J., and Vogel, S. N. (2007) Role of TLR4 tyrosine phosphorylation in signal transduction and endotoxin tolerance. J. Biol. Chem. 282, 16042-16053
59. Ernst, M., Inglese, M., Scholz, G. M., Harder, K. W., Clay, F. J., Bozinovski, S., Waring, P., Darwiche, R., Kay, T., Sly, P., Collins, R., Turner, D., Hibbs, M. L., Anderson, G. P., and Dunn, A. R. (2002) Constitutive activation of the SRC family kinase Hck results in spontaneous pulmonary inflammation and an enhanced innate immune response. J. Exp. Med. 196, 589-604
60. Xi, C. X., Xiong, F., Zhou, Z., Mei, L., and Xiong, W. C. (2010) PYK2 interacts with MyD88 and regulates MyD88-mediated NF-KB activation in macrophages. J. Leukoc. Biol. 87, 415-423
61. Laird, M. H., Rhee, S. H., Perkins, D. J., Medvedev, A. E., Piao, W., Fenton, M. J., and Vogel, S. N. (2009) TLR4/MyD88/PI3K interactions regulate TLR4 signaling. J. Leukoc. Biol. 85, 966-977
62. Lee, J.Y., Chiu, Y. H., Asara, J., and Cantley, L. C. (2011) Inhibition of PI3K binding to activators by serine phosphorylation of PI3K regulatory subunit p85a Src homology-2 domains. Proc. Natl. Acad. Sci. U.S.A. 108, 14157-14162
63. Li, T., Hu, J., and Li, L. (2004) Characterization of Tollip protein upon lipopolysaccharide challenge. Mol. Immunol. 41, 85-92
64. Burns, K., Clatworthy, J., Martin, L., Martinon, F., Plumpton, C, Masch-era, B., Lewis, A., Ray, K., Tschopp, J., and Volpe, F. (2000) Tollip, a new component of the IL-1RI pathway, links IRAK to the IL-1 receptor. Nat. Cell Biol. 2, 346-351
65. Bosisio, D., Polentarutti, N., Sironi, M., Bernasconi, S., Miyake, K., Webb, G. R., Martin, M. U., Mantovani, A., and Muzio, M. (2002) Stimulation of toll-like receptor 4 expression in human mononuclear phagocytes by in-terferon-7: a molecular basis for priming and synergism with bacterial lipopolysaccharide. Blood 99, 3427-3431
66. Hu, X., Paik, P. K., Chen, J., Yarilina, A., Kockeritz, L., Lu, T. T., Woodgett, J. R., and Ivashkiv, L. B. (2006) IFN-7 suppresses IL-10 production and synergizes with TLR2 by regulating GSK3 and CREB/AP-1 proteins. Immunity 24, 563-574