CD11b/CD18 (Mac-1) is a novel surface receptor for extracellular double-stranded RNA to mediate cellular inflammatory responses

Journal of Immunology

Volumn 190, Issue 1, 2013, Pages 115-125

  Zhou, Hui ^a   Liao, Jieying ^a   Aloor, Jim ^a   Nie, Hui ^a   Wilson, Belinda C ^a   Fessler, Michael B ^a   Gao, Hui Ming ^a,b   Hong, Jau Shyong ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b NANJING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CD18 ANTIGEN; CYTOKINE; DOUBLE STRANDED RNA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; POLYINOSINIC POLYCYTIDYLIC ACID; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; TOLL LIKE RECEPTOR 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL SURFACE; CONTROLLED STUDY; CYTOKINE PRODUCTION; INFLAMMATION; INTERNALIZATION; LIVER; MALE; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN RNA BINDING; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, CD11B; ANTIGENS, CD18; CELL LINE; EXTRACELLULAR SPACE; INFLAMMATION; INFLAMMATION MEDIATORS; MACROPHAGE-1 ANTIGEN; MACROPHAGES, PERITONEAL; MALE; MICE; MICE, KNOCKOUT; NADPH OXIDASE; RNA, DOUBLE-STRANDED; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 3;

EID: 84871835926     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1202136     Document Type: Article

References (54)

1. Creagh, E. M., and L. A. O'Neill. 2006. TLRs, NLRs and RLRs: a trinity of pathogen sensors that co-operate in innate immunity. Trends Immunol. 27: 352- 357.
2. Jacobs, B. L., and J. O. Langland. 1996. When two strands are better than one: the mediators and modulators of the cellular responses to double-stranded RNA. Virology 219: 339-349. (Pubitemid 126407667)
3. Majde, J. A., N. Guha-Thakurta, Z. Chen, S. Bredow, and J. M. Krueger. 1998. Spontaneous release of stable viral double-stranded RNA into the extracellular medium by influenza virus-infected MDCK epithelial cells: implications for the viral acute phase response. Arch. Virol. 143: 2371-2380. (Pubitemid 29020111)
4. Carter, W. A., and E. De Clercq. 1974. Viral infection and host defense. Science 186: 1172-1178.
5. Majde, J. A. 2000. Viral double-stranded RNA, cytokines, and the flu. J. Interferon Cytokine Res. 20: 259-272. (Pubitemid 30169737)
6. DeWitte-Orr, S. J., S. E. Collins, C. M. Bauer, D. M. Bowdish, and K. L. Mossman. 2010. An accessory to the 'Trinity': SR-As are essential pathogen sensors of extracellular dsRNA, mediating entry and leading to subsequent type I IFN responses. PLoS Pathog. 6: e1000829.
7. Alexopoulou, L., A. C. Holt, R. Medzhitov, and R. A. Flavell. 2001. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413: 732-738. (Pubitemid 33009951)
8. Kanneganti, T. D., M. Body-Malapel, A. Amer, J. H. Park, J. Whitfield, L. Franchi, Z. F. Taraporewala, D. Miller, J. T. Patton, N. Inohara, and G. Núñez. 2006. Critical role for Cryopyrin/Nalp3 in activation of caspase-1 in response to viral infection and double-stranded RNA. J. Biol. Chem. 281: 36560-36568. (Pubitemid 46042123)
9. Kato, H., O. Takeuchi, E. Mikamo-Satoh, R. Hirai, T. Kawai, K. Matsushita, A. Hiiragi, T. S. Dermody, T. Fujita, and S. Akira. 2008. Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5. J. Exp. Med. 205: 1601-1610. (Pubitemid 351962024)
10. Liao, J. Y., S. A. Thakur, Z. B. Zalinger, K. E. Gerrish, and F. Imani. 2011. Inosine-containing RNA is a novel innate immune recognition element and reduces RSV infection. PLoS ONE 6: e26463.
11. Liu, L., I. Botos, Y. Wang, J. N. Leonard, J. Shiloach, D. M. Segal, and D. R. Davies. 2008. Structural basis of toll-like receptor 3 signaling with doublestranded RNA. Science 320: 379-381. (Pubitemid 351555661)
12. Town, T., D. Jeng, L. Alexopoulou, J. Tan, and R. A. Flavell. 2006. Microglia recognize double-stranded RNA via TLR3. J. Immunol. 176: 3804-3812. (Pubitemid 43364029)
13. Wright, S. D., and M. T. Jong. 1986. Adhesion-promoting receptors on human macrophages recognize Escherichia coli by binding to lipopolysaccharide. J. Exp. Med. 164: 1876-1888. (Pubitemid 17217970)
14. Zhang, D., X. Hu, L. Qian, S. H. Chen, H. Zhou, B. Wilson, D. S. Miller, and J. S. Hong. 2011. Microglial MAC1 receptor and PI3K are essential in mediating b-amyloid peptide-induced microglial activation and subsequent neurotoxicity. J. Neuroinflammation 8: 3.
15. Gao, H. M., H. Zhou, F. Zhang, B. C. Wilson, W. Kam, and J. S. Hong. 2011. HMGB1 acts on microglia Mac1 to mediate chronic neuroinflammation that drives progressive neurodegeneration. J. Neurosci. 31: 1081-1092.
16. Ho, M. K., and T. A. Springer. 1982. Mac-1 antigen: quantitative expression in macrophage populations and tissues, and immunofluorescent localization in spleen. J. Immunol. 128: 2281-2286. (Pubitemid 12086524)
17. Solovjov, D. A., E. Pluskota, and E. F. Plow. 2005. Distinct roles for the alpha and beta subunits in the functions of integrin alphaMbeta2. J. Biol. Chem. 280: 1336-1345.
18. Hynes, R. O. 2002. Integrins: bidirectional, allosteric signaling machines. Cell 110: 673-687. (Pubitemid 35283958)
19. Morrison, T. E., J. D. Simmons, and M. T. Heise. 2008. Complement receptor 3 promotes severe ross river virus-induced disease. J. Virol. 82: 11263-11272.
20. Benimetskaya, L., J. D. Loike, Z. Khaled, G. Loike, S. C. Silverstein, L. Cao, J. el Khoury, T. Q. Cai, and C. A. Stein. 1997. Mac-1 (CD11b/CD18) is an oligodeoxynucleotide-binding protein. Nat. Med. 3: 414-420. (Pubitemid 27145683)
21. Perera, P. Y., T. N. Mayadas, O. Takeuchi, S. Akira, M. Zaks-Zilberman, S. M. Goyert, and S. N. Vogel. 2001. CD11b/CD18 acts in concert with CD14 and Toll-like receptor (TLR) 4 to elicit full lipopolysaccharide and taxolinducible gene expression. J. Immunol. 166: 574-581. (Pubitemid 32038479)
22. Sumpter, R., Jr., Y. M. Loo, E. Foy, K. Li, M. Yoneyama, T. Fujita, S. M. Lemon, and M. Gale, Jr. 2005. Regulating intracellular antiviral defense and permissiveness to hepatitis C virus RNA replication through a cellular RNA helicase, RIG-I. J. Virol. 79: 2689-2699. (Pubitemid 40270547)
23. Feng, Z., M. Cerveny, Z. Yan, and B. He. 2007. The VP35 protein of Ebola virus inhibits the antiviral effect mediated by double-stranded RNA-dependent protein kinase PKR. J. Virol. 81: 182-192. (Pubitemid 44975159)
24. Limmon, G. V., M. Arredouani, K. L. McCann, R. A. Corn Minor, L. Kobzik, and F. Imani. 2008. Scavenger receptor class-A is a novel cell surface receptor for double-stranded RNA. FASEB J. 22: 159-167.
25. Loike, J. D., and S. C. Silverstein. 1983. A fluorescence quenching technique using trypan blue to differentiate between attached and ingested glutaraldehydefixed red blood cells in phagocytosing murine macrophages. J. Immunol. Methods 57: 373-379. (Pubitemid 13116752)
26. Zhou, H., F. Zhang, S. H. Chen, D. Zhang, B. Wilson, J. S. Hong, and H. M. Gao. 2012. Rotenone activates phagocyte NADPH oxidase by binding to its membrane subunit gp91phox. Free Radic. Biol. Med. 52: 303-313.
27. Cary, L. A., and J. L. Guan. 1999. Focal adhesion kinase in integrin-mediated signaling. Front. Biosci. 4: D102-D113.
28. Moissoglu, K., and M. A. Schwartz. 2006. Integrin signalling in directed cell migration. Biol. Cell 98: 547-555. (Pubitemid 44383371)
29. Schymeinsky, J., A. Mócsai, and B. Walzog. 2007. Neutrophil activation via beta2 integrins (CD11/CD18): molecular mechanisms and clinical implications. Thromb. Haemost. 98: 262-273.
30. Anderson, K. E., K. B. Boyle, K. Davidson, T. A. Chessa, S. Kulkarni, G. E. Jarvis, A. Sindrilaru, K. Scharffetter-Kochanek, O. Rausch, L. R. Stephens, and P. T. Hawkins. 2008. CD18-dependent activation of the neutrophil NADPH oxidase during phagocytosis of Escherichia coli or Staphylococcus aureus is regulated by class III but not class I or II PI3Ks. Blood 112: 5202-5211.
31. Araki, N., M. T. Johnson, and J. A. Swanson. 1996. A role for phosphoinositide 3-kinase in the completion of macropinocytosis and phagocytosis by macrophages. J. Cell Biol. 135: 1249-1260. (Pubitemid 27014597)
32. Fujioka, Y., M. Tsuda, T. Hattori, J. Sasaki, T. Sasaki, T. Miyazaki, and Y. Ohba. 2011. The Ras-PI3K signaling pathway is involved in clathrinindependent endocytosis and the internalization of influenza viruses. PLoS ONE 6: e16324.
33. Zhang, F., L. Qian, P. M. Flood, J. S. Shi, J. S. Hong, and H. M. Gao. 2010. Inhibition of IkappaB kinase-beta protects dopamine neurons against lipopolysaccharide- induced neurotoxicity. J. Pharmacol. Exp. Ther. 333: 822-833.
34. Steer, S. A., J. M. Moran, B. S. Christmann, L. B. Maggi, Jr., and J. A. Corbett. 2006. Role of MAPK in the regulation of double-stranded RNA- and encephalomyocarditis virus-induced cyclooxygenase-2 expression by macrophages. J. Immunol. 177: 3413-3420. (Pubitemid 44277862)
35. Saleh, M. C., R. P. van Rij, A. Hekele, A. Gillis, E. Foley, P. H. O'Farrell, and R. Andino. 2006. The endocytic pathway mediates cell entry of dsRNA to induce RNAi silencing. Nat. Cell Biol. 8: 793-802. (Pubitemid 44151582)
36. Matsumoto, M., and T. Seya. 2008. TLR3: interferon induction by doublestranded RNA including poly(I:C). Adv. Drug Deliv. Rev. 60: 805-812.
37. Prantner, D., T. Darville, and U. M. Nagarajan. 2010. Stimulator of IFN gene is critical for induction of IFN-beta during Chlamydia muridarum infection. J. Immunol. 184: 2551-2560.
38. Cox, D., M. Brennan, and N. Moran. 2010. Integrins as therapeutic targets: lessons and opportunities. Nat. Rev. Drug Discov. 9: 804-820.
39. Beller, D. I., T. A. Springer, and R. D. Schreiber. 1982. Anti-Mac-1 selectively inhibits the mouse and human type three complement receptor. J. Exp. Med. 156: 1000-1009. (Pubitemid 12036266)
40. Wright, S. D., P. E. Rao, W. C. Van Voorhis, L. S. Craigmyle, K. Iida, M. A. Talle, E. F. Westberg, G. Goldstein, and S. C. Silverstein. 1983. Identification of the C3bi receptor of human monocytes and macrophages by using monoclonal antibodies. Proc. Natl. Acad. Sci. USA 80: 5699-5703. (Pubitemid 14249895)
41. van Spriel, A. B., H. H. van Ojik, A. Bakker, M. J. Jansen, and J. G. van de Winkel. 2003. Mac-1 (CD11b/CD18) is crucial for effective Fc receptormediated immunity to melanoma. Blood 101: 253-258. (Pubitemid 36025915)
42. Fällman, M., R. Andersson, and T. Andersson. 1993. Signaling properties of CR3 (CD11b/CD18) and CR1 (CD35) in relation to phagocytosis of complementopsonized particles. J. Immunol. 151: 330-338. (Pubitemid 23206998)
43. Anderson, D. C., and T. A. Springer. 1987. Leukocyte adhesion deficiency: an inherited defect in the Mac-1, LFA-1, and p150,95 glycoproteins. Annu. Rev. Med. 38: 175-194.
44. Lee, J. O., P. Rieu, M. A. Arnaout, and R. Liddington. 1995. Crystal structure of the A domain from the alpha subunit of integrin CR3 (CD11b/CD18). Cell 80: 631-638.
45. Makranz, C., G. Cohen, A. Baron, L. Levidor, T. Kodama, F. Reichert, and S. Rotshenker. 2004. Phosphatidylinositol 3-kinase, phosphoinositide-specific phospholipase-Cgamma and protein kinase-C signal myelin phagocytosis mediated by complement receptor-3 alone and combined with scavenger receptor- AI/II in macrophages. Neurobiol. Dis. 15: 279-286. (Pubitemid 38296759)
46. Colonna, M. 2007. TLR pathways and IFN-regulatory factors: to each its own. Eur. J. Immunol. 37: 306-309. (Pubitemid 46915569)
47. Bsibsi, M., J. J. Bajramovic, M. H. Vogt, E. van Duijvenvoorden, A. Baghat, C. Persoon-Deen, F. Tielen, R. Verbeek, I. Huitinga, B. Ryffel, et al. 2010. The microtubule regulator stathmin is an endogenous protein agonist for TLR3. J. Immunol. 184: 6929-6937.
48. Matsumoto, M., S. Kikkawa, M. Kohase, K. Miyake, and T. Seya. 2002. Establishment of a monoclonal antibody against human Toll-like receptor 3 that blocks double-stranded RNA-mediated signaling. Biochem. Biophys. Res. Commun. 293: 1364-1369. (Pubitemid 34681026)
49. Matsumoto, M., H. Oshiumi, and T. Seya. 2011. Antiviral responses induced by the TLR3 pathway. Rev. Med. Virol. 21: 67-77.
50. Gonzalez-Dosal, R., K. A. Horan, S. H. Rahbek, H. Ichijo, Z. J. Chen, J. J. Mieyal, R. Hartmann, and S. R. Paludan. 2011. HSV infection induces production of ROS, which potentiate signaling from pattern recognition receptors: role for S-glutathionylation of TRAF3 and 6. PLoS Pathog. 7: e1002250.
51. Hu, S., W. S. Sheng, S. J. Schachtele, and J. R. Lokensgard. 2011. Reactive oxygen species drive herpes simplex virus (HSV)-1-induced proinflammatory cytokine production by murine microglia. J. Neuroinflammation 8: 123.
52. Liu, T., S. Castro, A. R. Brasier, M. Jamaluddin, R. P. Garofalo, and A. Casola. 2004. Reactive oxygen species mediate virus-induced STAT activation: role of tyrosine phosphatases. J. Biol. Chem. 279: 2461-2469. (Pubitemid 38114229)
53. Yu, M., J. Lam, B. Rada, T. L. Leto, and S. J. Levine. 2011. Double-stranded RNA induces shedding of the 34-kDa soluble TNFR1 from human airway epithelial cells via TLR3-TRIF-RIP1-dependent signaling: roles for dual oxidase 2- and caspase-dependent pathways. J. Immunol. 186: 1180-1188.
54. Jamaluddin, M., B. Tian, I. Boldogh, R. P. Garofalo, and A. R. Brasier. 2009. Respiratory syncytial virus infection induces a reactive oxygen species-MSK1- phospho-Ser-276 RelA pathway required for cytokine expression. J. Virol. 83: 10605-10615.