CD16 regulates TRIF-dependent TLR4 response in human monocytes and their subsets

Journal of Immunology

Volumn 188, Issue 8, 2012, Pages 3584-3593

  Shalova, Irina N ^a   Kajiji, Tasneem ^a   Lim, Jyue Yuan ^a   Gómez Piña, Vanesa ^b   Fernández Ruíz, Irene ^b   Arnalich, Francisco ^b   Iau, Philip Tsau Choong ^c   López Collazo, Eduardo ^b   Wong, Siew Cheng ^a   Biswas, Subhra K ^a  

^a AGENCY FOR SCIENCE   (Singapore)

^b HOSPITAL UNIVERSITARIO LA PAZ   (Spain)

^c NATIONAL UNIVERSITY HEALTH SYSTEM   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; CD16 ANTIGEN; ENDOTOXIN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERFERON REGULATORY FACTOR 3; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 3; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; MYELOID DIFFERENTIATION FACTOR 88; PROTEIN KINASE SYK; RANTES; SMALL INTERFERING RNA; STAT1 PROTEIN; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1;

ANIMAL CELL; ANTIGEN EXPRESSION; ANTIGEN RECOGNITION; ARTICLE; CELL EXPANSION; CELL ISOLATION; CONTROLLED STUDY; GENE CONTROL; GENE EXPRESSION; GENE SILENCING; GRAM NEGATIVE BACTERIUM; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOREGULATION; INFLAMMATION; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEPSIS; SIGNAL TRANSDUCTION; UPREGULATION;

ADAPTIVE IMMUNITY; ADAPTOR PROTEINS, VESICULAR TRANSPORT; ADULT; ANIMALS; ENDOTOXINS; GENE EXPRESSION REGULATION; HUMANS; INTERFERONS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, INBRED C57BL; MIDDLE AGED; MONOCYTES; MYELOID DIFFERENTIATION FACTOR 88; PRIMARY CELL CULTURE; PROTEIN-TYROSINE KINASES; RECEPTORS, IGG; RNA, SMALL INTERFERING; SEPSIS; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; TOLL-LIKE RECEPTOR 4; TRANSFECTION;

EID: 84860337683     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1100244     Document Type: Article

References (69)

1. 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.
2. Deans, K. J., M. Haley, C. Natanson, P. Q. Eichacker, and P. C. Minneci. 2005. Novel therapies for sepsis: a review. J. Trauma 58: 867-874. (Pubitemid 40592766)
3. Biswas, S. K., and E. Lopez-Collazo. 2009. Endotoxin tolerance: new mechanisms, molecules and clinical significance. Trends Immunol. 30: 475-487.
4. Adib-Conquy, M., and J. M. Cavaillon. 2009. Compensatory anti-inflammatory response syndrome. Thromb. Haemost. 101: 36-47.
5. Wilson, C. S., S. C. Seatter, J. L. Rodriguez, J. Bellingham, L. Clair, and M. A. West. 1997. In vivo endotoxin tolerance: impaired LPS-stimulated TNF release of monocytes from patients with sepsis, but not SIRS. J. Surg. Res. 69: 101-106. (Pubitemid 27265834)
6. Draisma, A., P. Pickkers, M. P. Bouw, and J. G. van der Hoeven. 2009. Development of endotoxin tolerance in humans in vivo. Crit. Care Med. 37: 1261-1267.
7. Munoz, C., J. Carlet, C. Fitting, B. Misset, J. P. Blériot, and J. M. Cavaillon. 1991. Dysregulation of in vitro cytokine production by monocytes during sepsis. J. Clin. Invest. 88: 1747-1754.
8. Escoll, P., C. del Fresno, L. García, G. Vallés, M. J. Lendínez, F. Arnalich, and E. López-Collazo. 2003. Rapid up-regulation of IRAK-M expression following a second endotoxin challenge in human monocytes and in monocytes isolated from septic patients. Biochem. Biophys. Res. Commun. 311: 465-472. (Pubitemid 37340100)
9. Monneret, G., F. Venet, A. Pachot, and A. Lepape. 2008. Monitoring immune dysfunctions in the septic patient: a new skin for the old ceremony. Mol. Med. 14: 64-78. (Pubitemid 351356886)
10. Beutler, B. 2002. TLR4 as the mammalian endotoxin sensor. Curr. Top. Microbiol. Immunol. 270: 109-120. (Pubitemid 35448156)
11. Poltorak, A., X. He, I. Smirnova, M. Y. Liu, C. Van Huffel, X. Du, D. Birdwell, E. Alejos, M. Silva, C. Galanos, et al. 1998. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282: 2085-2088. (Pubitemid 29001265)
12. Medzhitov, R., P. Preston-Hurlburt, and C. A. Janeway, Jr. 1997. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388: 394-397. (Pubitemid 27334820)
13. Akira, S. 2009. Innate immunity to pathogens: diversity in receptors for microbial recognition. Immunol. Rev. 227: 5-8.
14. 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)
15. Kawai, T., O. Adachi, T. Ogawa, K. Takeda, and S. Akira. 1999. Unresponsiveness of MyD88-deficient mice to endotoxin. Immunity 11: 115-122. (Pubitemid 29359962)
16. Björkbacka, H., K. A. Fitzgerald, F. Huet, X. Li, J. A. Gregory, M. A. Lee, C. M. Ordija, N. E. Dowley, D. T. Golenbock, and M. W. Freeman. 2004. The induction of macrophage gene expression by LPS predominantly utilizes Myd88-independent signaling cascades. Physiol. Genomics 19: 319-330. (Pubitemid 40039937)
17. 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)
18. 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)
19. Fan, H., and J. A. Cook. 2004. Molecular mechanisms of endotoxin tolerance. J. Endotoxin Res. 10: 71-84.
20. Medvedev, A. E., A. Lentschat, L. M. Wahl, D. T. Golenbock, and S. N. Vogel. 2002. Dysregulation of LPS-induced Toll-like receptor 4-MyD88 complex formation and IL-1 receptor-associated kinase 1 activation in endotoxin-tolerant cells. J. Immunol. 169: 5209-5216. (Pubitemid 35217192)
21. Biswas, S. K., and V Tergaonkar. 2007. Myeloid differentiation factor 88-independent Toll-like receptor pathway: Sustaining inflammation or promoting tolerance? Int. J. Biochem. Cell Biol. 39: 1582-1592. (Pubitemid 47096712)
22. Biswas, S. K., P. Bist, M. K. Dhillon, T. Kajiji, C. Del Fresno, M. Yamamoto, E. Lopez-Collazo, S. Akira, and V Tergaonkar. 2007. Role for MyD88independent, TRIF pathway in lipid A/TLR4-induced endotoxin tolerance. J. Immunol. 179: 4083-4092.
23. + dendritic cells for immune T cell areas. Cell 143: 416-429.
24. Geissmann, F, S. Gordon, D. A. Hume, A. M. Mowat, and G J. Randolph. 2010. Unravelling mononuclear phagocyte heterogeneity. Nat. Rev. Immunol. 10: 453-460.
25. Gordon, S., and P. R. Taylor. 2005. Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 5: 953-964. (Pubitemid 41746764)
26. 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)
27. + and CD16-monocyte subsets. BMC Genomics 10: 403.
28. Auffray, C, M. H. Sieweke, and F. Geissmann. 2009. Blood monocytes: development, heterogeneity, and relationship with dendritic cells. Annu. Rev. Immunol. 27: 669-692.
29. Ingersoll, M. A, R. Spanbroek, C. Lottaz, E. L. Gautier, M. Frankenberger, R. Hoffmann, R. Lang, M. Haniffa, M. Collin, F. Tacke, et al. 2010. Comparison of gene expression profiles between human and mouse monocyte subsets. Blood 115: e10-e19.
30. Zhao, C, H. Zhang, W. C. Wong, X. Sem, H. Han, S. M. Ong, Y. C. Tan, W. H. Yeap, C. S. Gan, K. Q. Ng, et al. 2009. Identification of novel functional differences in monocyte subsets using proteomic and transcriptomic methods. J. Proteome Res. 8: 4028-4038.
31. + subpopulation. Immunol. Today 17: 424-428. (Pubitemid 26278368)
32. Auffray, C, D. Fogg, M. Garfa, G. Elain, O. Join-Lambert, S. Kayal, S. Sarnacki, A. Cumano, G. Lauvau, and F. Geissmann. 2007. Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science 317: 666-670. (Pubitemid 47229966)
33. Nahrendorf, M., F K. Swirski, E. Aikawa, L. Stangenberg, T. Wurdinger, J. L. Figueiredo, P. Libby, R. Weissleder, and M. J. Pittet. 2007. The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J. Exp. Med. 204: 3037-3047. (Pubitemid 350179569)
34. Mortellaro, A., S. C. Wong, J. Fric, and P. Ricciardi-Castagnoli. 2010. The need to identify myeloid dendritic cell progenitors in human blood. Trends Immunol. 31: 18-23.
35. Ingersoll, M. A, R. Spanbroek, C. Lottaz, E. L. Gautier, M. Frankenberger, R. Hoffmann, R. Lang, M. Haniffa, M. Collin, F. Tacke, et al. 2010. Comparison of gene expression profiles between human and mouse monocyte subsets. [Published erratum appears in 2010 Blood 116: 857.] Blood 115: e10-e19.
36. ++ monocytes are a major source of TNF. J. Immunol. 168: 3536-3542. (Pubitemid 34250422)
37. Cros, J., N. Cagnard, K. Woollard, N. Patey, S. Y Zhang, B. Senechal, A. Puel, S. K. Biswas, D. Moshous, C. Picard, et al. 2010. Human CD14 monocytes patrol and sense nucleic acids and viruses via TLR7 and TLR8 receptors. Immunity 33: 375-386.
38. + monocytes are main producers of IL10. Scand. J. Immunol. 67: 152-159.
39. Wong, K. L., J. J. Tai, W. C. Wong, H. Han, X. Sem, W. H. Yeap, P. Kourilsky, and S. C. Wong. 2011. Gene expression profiling reveals the defining features of the classical, intermediate, and nonclassical human monocyte subsets. Blood 118: e16-e31.
40. + blood monocytes is expanded in sepsis patients. Blood 82: 3170-3176. (Pubitemid 23334947)
41. Tomita, K., S. Lim, T. Hanazawa, O. Usmani, R. Stirling, K. F Chung, P. J. Barnes, and I. M. Adcock. 2002. Attenuated production of intracellular IL-10 and IL-12 in monocytes from patients with severe asthma. Clin. Immunol. 102: 258-266. (Pubitemid 34259259)
42. + monocytes in critically ill cardiac surgery patients. Inflammation 22: 367-379. (Pubitemid 28376853)
43. Kim, W. K., Y Sun, H. Do, P. Autissier, E. F Halpern, M. Piatak, Jr., J. D. Lifson, T. H. Burdo, M. S. McGrath, and K. Williams. 2009. Monocyte heterogeneity underlying phenotypic changes in monocytes according to SIV disease stage. J. Leukoc. Biol. 87: 557-567.
44. + monocytes in the course of sepsis in neonates and small children: monitoring and functional studies. Scand. J. Immunol. 55: 629-638. (Pubitemid 34535555)
45. Nimmerjahn, F., and J. V. Ravetch. 2008. Fcg receptors as regulators of immune responses. Nat. Rev. Immunol. 8: 34-47.
46. 1992. American College of Chest Physicians/Society of Critical Care Medicine Consensus Conference: definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. Crit. Care Med. 20: 864-874.
47. Biswas, S. K., L. Gangi, S. Paul, T. Schioppa, A. Saccani, M. Sironi, B. Bottazzi, A. Doni, B. Vincenzo, F. Pasqualini, et al. 2006. A distinct and unique transcriptional program expressed by tumor-associated macrophages (defective NFkB and enhanced IRF-3/STAT1 activation). Blood 107: 2112-2122. (Pubitemid 43289397)
48. Pinheiro da Silva, F., M. Aloulou, D. Skurnik, M. Benhamou, A. Andremont, I. T. Velasco, M. Chiamolera, J. S. Verbeek, P. Launay, and R. C. Monteiro. 2007. CD16 promotes Escherichia coli sepsis through an FcR g inhibitory pathway that prevents phagocytosis and facilitates inflammation. Nat. Med. 13: 1368-1374. (Pubitemid 350073597)
49. Uggla, C. K., M. Geisberg, M. Jondal, and R. W. Knowles. 1989. Agonistic effects of anti-CD2 and anti-CD16 antibodies on human natural killer killing. Scand. J. Immunol. 29: 507-515. (Pubitemid 19144308)
50. Perussia, B., and G. Trinchieri. 1984. Antibody 3G8, specific for the human neutrophil Fc receptor, reacts with natural killer cells. J. Immunol. 132: 1410-1415. (Pubitemid 14154569)
51. Kramer, P. R., V. Winger, and J. Reuben. 2009. PI3K limits TNF-α production in CD16-activated monocytes. Eur. J. Immunol. 39: 561-570.
52. Darby, C., R. L. Geahlen, and A. D. Schreiber. 1994. Stimulation of macrophage FcgRIIIA activates the receptor-associated protein tyrosine kinase Syk and induces phosphorylation of multiple proteins including p95Vav and p62/GAPassociated protein. J. Immunol. 152: 5429-5437.
53. del Fresno, C., F. García-Rio, V. Gómez-Piña, A. Soares-Schanoski, I. Fernández-Ruíz, T. Jurado, T. Kajiji, C. Shu, E. Marín, A. Gutierrez del Arroyo, et al. 2009. Potent phagocytic activity with impaired antigen presentation identifying lipopolysaccharide- tolerant human monocytes: demonstration in isolated monocytes from cystic fibrosis patients. J. Immunol. 182: 6494-6507.
54. Gerber, J. S., and D. M. Mosser. 2001. Stimulatory and inhibitory signals originating from the macrophage Fcg receptors. Microbes Infect. 3: 131-139. (Pubitemid 32209330)
55. Anderson, C. F., and D. M. Mosser. 2002. A novel phenotype for an activated macrophage: the type 2 activated macrophage. J. Leukoc. Biol. 72: 101-106.
56. Abrahams, V. M., G. Cambridge, P. M. Lydyard, and J. C. Edwards. 2000. Induction of tumor necrosis factor a production by adhered human monocytes: a key role for Fg receptor type IIIa in rheumatoid arthritis. Arthritis Rheum. 43: 608-616. (Pubitemid 30394953)
57. Pinheiro da Silva, F., M. Aloulou, M. Benhamou, and R. C. Monteiro. 2008. Inhibitory ITAMs: a matter of life and death. Trends Immunol. 29: 366-373.
58. Dhodapkar, K. M., D. Banerjee, J. Connolly, A. Kukreja, E. Matayeva, M. C. Veri, J. V. Ravetch, R. M. Steinman, and M. V. Dhodapkar. 2007. Selective blockade of the inhibitory Fcg receptor (FcgRIIB) in human dendritic cells and monocytes induces a type I interferon response program. J. Exp. Med. 204: 1359-1369. (Pubitemid 46919874)
59. Zanoni, I., R. Ostuni, L. R. Marek, S. Barresi, R. Barbalat, G. M. Barton, F. Granucci, and J. C. Kagan. 2011. CD14 controls the LPS-induced endocytosis of Toll-like receptor 4. Cell 147: 868-880.
60. Schaaf, B., K. Luitjens, T. Goldmann, T. van Bremen, F. Sayk, C. Dodt, K. Dalhoff, and D. Droemann. 2009. Mortality in human sepsis is associated with downregulation of Toll-like receptor 2 and CD14 expression on blood monocytes. Diagn. Pathol. 4: 12.
61. Covert, M. W., T. H. Leung, J. E. Gaston, and D. Baltimore. 2005. Achieving stability of lipopolysaccharide-induced NF-κB activation. Science 309: 1854-1857. (Pubitemid 41325095)
62. Mantovani, A., A. Sica, S. Sozzani, P. Allavena, A. Vecchi, and M. Locati. 2004. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 25: 677-686. (Pubitemid 39457982)
63. Cavaillon, J. M., and M. Adib-Conquy. 2006. Bench-to-bedside review: endotoxin tolerance as a model of leukocyte reprogramming in sepsis. Crit. Care 10: 233.
64. Chang, E. Y., B. Guo, S. E. Doyle, and G. Cheng. 2007. Cutting edge: involvement of the type I IFN production and signaling pathway in lipopolysaccharide-induced IL-10 production. J. Immunol. 178: 6705-6709. (Pubitemid 46847391)
65. Häcker, H., V. Redecke, B. Blagoev, I. Kratchmarova, L. C. Hsu, G. G. Wang, M. P. Kamps, E. Raz, H. Wagner, G. Häcker, et al. 2006. Specificity in Toll-like receptor signalling through distinct effector functions of TRAF3 and TRAF6. Nature 439: 204-207. (Pubitemid 43083141)
66. Wu, J., J. C. Edberg, P. B. Redecha, V. Bansal, P. M. Guyre, K. Coleman, J. E. Salmon, and R. P. Kimberly. 1997. A novel polymorphism of FcgRIIIa (CD16) alters receptor function and predisposes to autoimmune disease. J. Clin. Invest. 100: 1059-1070. (Pubitemid 27386289)
67. Todd, I., P. M. Radford, L. Ziegler-Heitbrock, A. M. Ghaemmaghami, R. J. Powell, and P. J. Tighe. 2007. Elevated CD16 expression by monocytes from patients with tumor necrosis factor receptor-associated periodic syndrome. Arthritis Rheum. 56: 4182-4188. (Pubitemid 350262346)
68. + monocytes in peripheral blood and synovium: correlation with joint destruction in rheumatoid arthritis. Arthritis Rheum. 43: 1233-1243. (Pubitemid 30416308)
69. Andreu, P., M. Johansson, N. I. Affara, F. Pucci, T. Tan, S. Junankar, L. Korets, J. Lam, D. Tawfik, D. G. DeNardo, et al. 2010. FcRg activation regulates inflammation-associated squamous carcinogenesis. Cancer Cell 17: 121-134.