SR-B1 Is a Silica Receptor that Mediates Canonical Inflammasome Activation

Cell Reports

Volumn 18, Issue 5, 2017, Pages 1298-1311

  Tsugita, Misato ^a   Morimoto, Nobuyuki ^a   Tashiro, Manabu ^a   Kinoshita, Kengo ^a   Nakayama, Masafumi ^a  

^a TOHOKU UNIVERSITY   (Japan)

Author keywords

fibrosis; IL 1 ; IL 1 ; SiO2; SR BI

Indexed keywords

INFLAMMASOME; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; LATEX; SCAVENGER RECEPTOR BI; SILICON DIOXIDE; TITANIUM DIOXIDE; TUMOR NECROSIS FACTOR; URATE; SCARB1 PROTEIN, MOUSE; SCAVENGER RECEPTOR; SCAVENGER RECEPTOR B;

ALPHA HELIX; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW DERIVED MACROPHAGE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; HUMAN; HUMAN CELL; INTERNALIZATION; LUNG ALVEOLUS MACROPHAGE; LUNG FIBROSIS; MONOCYTE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PHAGOCYTE; PNEUMONIA; SILICOSIS; SURFACE CHARGE; ANIMAL; C57BL MOUSE; CELL LINE; HEK293 CELL LINE; MACROPHAGE; METABOLISM; NIH 3T3 CELL LINE;

ANIMALS; CASPASE 1; CELL LINE; HEK293 CELLS; HUMANS; INFLAMMASOMES; MACROPHAGES; MICE; MICE, INBRED C57BL; MONOCYTES; NIH 3T3 CELLS; PNEUMONIA; RECEPTORS, SCAVENGER; SCAVENGER RECEPTORS, CLASS B; SILICON DIOXIDE;

EID: 85011710605     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2017.01.004     Document Type: Article

References (61)

1. Arredouani, M., Yang, Z., Ning, Y., Qin, G., Soininen, R., Tryggvason, K., Kobzik, L., The scavenger receptor MARCO is required for lung defense against pneumococcal pneumonia and inhaled particles. J. Exp. Med. 200 (2004), 267–272.
2. Beamer, C.A., Holian, A., Scavenger receptor class A type I/II (CD204) null mice fail to develop fibrosis following silica exposure. Am. J. Physiol. Lung Cell. Mol. Physiol. 289 (2005), L186–L195.
3. Bouvard, D., Pouwels, J., De Franceschi, N., Ivaska, J., Integrin inactivators: balancing cellular functions in vitro and in vivo. Nat. Rev. Mol. Cell Biol. 14 (2013), 430–442.
4. Brauer, M., Avila-Casado, C., Fortoul, T.I., Vedal, S., Stevens, B., Churg, A., Air pollution and retained particles in the lung. Environ. Health Perspect. 109 (2001), 1039–1043.
5. Cai, L., Ji, A., de Beer, F.C., Tannock, L.R., van der Westhuyzen, D.R., SR-BI protects against endotoxemia in mice through its roles in glucocorticoid production and hepatic clearance. J. Clin. Invest. 118 (2008), 364–375.
6. Canton, J., Neculai, D., Grinstein, S., Scavenger receptors in homeostasis and immunity. Nat. Rev. Immunol. 13 (2013), 621–634.
7. Cassel, S.L., Eisenbarth, S.C., Iyer, S.S., Sadler, J.J., Colegio, O.R., Tephly, L.A., Carter, A.B., Rothman, P.B., Flavell, R.A., Sutterwala, F.S., The Nalp3 inflammasome is essential for the development of silicosis. Proc. Natl. Acad. Sci. USA 105 (2008), 9035–9040.
8. Cassel, S.L., Janczy, J.R., Bing, X., Wilson, S.P., Olivier, A.K., Otero, J.E., Iwakura, Y., Shayakhmetov, D.M., Bassuk, A.G., Abu-Amer, Y., et al. Inflammasome-independent IL-1β mediates autoinflammatory disease in Pstpip2-deficient mice. Proc. Natl. Acad. Sci. USA 111 (2014), 1072–1077.
9. Dostert, C., Pétrilli, V., Van Bruggen, R., Steele, C., Mossman, B.T., Tschopp, J., Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science 320 (2008), 674–677.
10. Flach, T.L., Ng, G., Hari, A., Desrosiers, M.D., Zhang, P., Ward, S.M., Seamone, M.E., Vilaysane, A., Mucsi, A.D., Fong, Y., et al. Alum interaction with dendritic cell membrane lipids is essential for its adjuvanticity. Nat. Med. 17 (2011), 479–487.
11. Franklin, B.S., Bossaller, L., De Nardo, D., Ratter, J.M., Stutz, A., Engels, G., Brenker, C., Nordhoff, M., Mirandola, S.R., Al-Amoudi, A., et al. The adaptor ASC has extracellular and ‘prionoid’ activities that propagate inflammation. Nat. Immunol. 15 (2014), 727–737.
12. Franklin, B.S., Mangan, M.S., Latz, E., Crystal formation in inflammation. Annu. Rev. Immunol. 34 (2016), 173–202.
13. Guo, H., Callaway, J.B., Ting, J.P., Inflammasomes: mechanism of action, role in disease, and therapeutics. Nat. Med. 21 (2015), 677–687.
14. Hamilton, R.F. Jr., Thakur, S.A., Mayfair, J.K., Holian, A., MARCO mediates silica uptake and toxicity in alveolar macrophages from C57BL/6 mice. J. Biol. Chem. 281 (2006), 34218–34226.
15. Haneklaus, M., O'Neill, L.A., NLRP3 at the interface of metabolism and inflammation. Immunol. Rev. 265 (2015), 53–62.
16. Heit, B., Kim, H., Cosío, G., Castaño, D., Collins, R., Lowell, C.A., Kain, K.C., Trimble, W.S., Grinstein, S., Multimolecular signaling complexes enable Syk-mediated signaling of CD36 internalization. Dev. Cell 24 (2013), 372–383.
17. Hemler, M.E., Tetraspanin functions and associated microdomains. Nat. Rev. Mol. Cell Biol. 6 (2005), 801–811.
18. Hoebe, K., Georgel, P., Rutschmann, S., Du, X., Mudd, S., Crozat, K., Sovath, S., Shamel, L., Hartung, T., Zähringer, U., Beutler, B., CD36 is a sensor of diacylglycerides. Nature 433 (2005), 523–527.
19. Hornung, V., Bauernfeind, F., Halle, A., Samstad, E.O., Kono, H., Rock, K.L., Fitzgerald, K.A., Latz, E., Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat. Immunol. 9 (2008), 847–856.
20. Huh, D., Matthews, B.D., Mammoto, A., Montoya-Zavala, M., Hsin, H.Y., Ingber, D.E., Reconstituting organ-level lung functions on a chip. Science 328 (2010), 1662–1668.
21. Kayagaki, N., Stowe, I.B., Lee, B.L., O'Rourke, K., Anderson, K., Warming, S., Cuellar, T., Haley, B., Roose-Girma, M., Phung, Q.T., et al. Caspase-11 cleaves gasdermin D for non-canonical inflammasome signalling. Nature 526 (2015), 666–671.
22. Kinoshita, K., Nakamura, H., eF-site and PDBjViewer: database and viewer for protein functional sites. Bioinformatics 20 (2004), 1329–1330.
23. Kitamura, T., Koshino, Y., Shibata, F., Oki, T., Nakajima, H., Nosaka, T., Kumagai, H., Retrovirus-mediated gene transfer and expression cloning: powerful tools in functional genomics. Exp. Hematol. 31 (2003), 1007–1014.
24. Krieger, M., Scavenger receptor class B type I is a multiligand HDL receptor that influences diverse physiologic systems. J. Clin. Invest. 108 (2001), 793–797.
25. Kusaka, T., Nakayama, M., Nakamura, K., Ishimiya, M., Furusawa, E., Ogasawara, K., Effect of silica particle size on macrophage inflammatory responses. PLoS ONE, 9, 2014, e92634.
26. Lagassé, H.A., Anidi, I.U., Craig, J.M., Limjunyawong, N., Poupore, A.K., Mitzner, W., Scott, A.L., Recruited monocytes modulate malaria-induced lung injury through CD36-mediated clearance of sequestered infected erythrocytes. J. Leukoc. Biol. 99 (2016), 659–671.
27. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., et al. Clustal W and Clustal X version 2.0. Bioinformatics 23 (2007), 2947–2948.
28. Latz, E., Xiao, T.S., Stutz, A., Activation and regulation of the inflammasomes. Nat. Rev. Immunol. 13 (2013), 397–411.
29. Leung, C.C., Yu, I.T., Chen, W., Silicosis. Lancet 379 (2012), 2008–2018.
30. Lukens, J.R., Gurung, P., Vogel, P., Johnson, G.R., Carter, R.A., McGoldrick, D.J., Bandi, S.R., Calabrese, C.R., Vande Walle, L., Lamkanfi, M., Kanneganti, T.D., Dietary modulation of the microbiome affects autoinflammatory disease. Nature 516 (2014), 246–249.
31. Martinon, F., Pétrilli, V., Mayor, A., Tardivel, A., Tschopp, J., Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 440 (2006), 237–241.
32. Merget, R., Bauer, T., Küpper, H.U., Philippou, S., Bauer, H.D., Breitstadt, R., Bruening, T., Health hazards due to the inhalation of amorphous silica. Arch. Toxicol. 75 (2002), 625–634.
33. Miyanishi, M., Tada, K., Koike, M., Uchiyama, Y., Kitamura, T., Nagata, S., Identification of Tim4 as a phosphatidylserine receptor. Nature 450 (2007), 435–439.
34. Moreno, T., Reche, C., Rivas, I., Cruz Minguillón, M., Martins, V., Vargas, C., Buonanno, G., Parga, J., Pandolfi, M., Brines, M., et al. Urban air quality comparison for bus, tram, subway and pedestrian commutes in Barcelona. Environ. Res. 142 (2015), 495–510.
35. Nakayama, M., Underhill, D.M., Petersen, T.W., Li, B., Kitamura, T., Takai, T., Aderem, A., Paired Ig-like receptors bind to bacteria and shape TLR-mediated cytokine production. J. Immunol. 178 (2007), 4250–4259.
36. Nakayama, M., Akiba, H., Takeda, K., Kojima, Y., Hashiguchi, M., Azuma, M., Yagita, H., Okumura, K., Tim-3 mediates phagocytosis of apoptotic cells and cross-presentation. Blood 113 (2009), 3821–3830.
37. Neculai, D., Schwake, M., Ravichandran, M., Zunke, F., Collins, R.F., Peters, J., Neculai, M., Plumb, J., Loppnau, P., Pizarro, J.C., et al. Structure of LIMP-2 provides functional insights with implications for SR-BI and CD36. Nature 504 (2013), 172–176.
38. Nel, A., Xia, T., Mädler, L., Li, N., Toxic potential of materials at the nanolevel. Science 311 (2006), 622–627.
39. Ng, G., Sharma, K., Ward, S.M., Desrosiers, M.D., Stephens, L.A., Schoel, W.M., Li, T., Lowell, C.A., Ling, C.C., Amrein, M.W., Shi, Y., Receptor-independent, direct membrane binding leads to cell-surface lipid sorting and Syk kinase activation in dendritic cells. Immunity 29 (2008), 807–818.
40. Nishi, C., Toda, S., Segawa, K., Nagata, S., Tim4- and MerTK-mediated engulfment of apoptotic cells by mouse resident peritoneal macrophages. Mol. Cell. Biol. 34 (2014), 1512–1520.
41. Ploss, A., Evans, M.J., Gaysinskaya, V.A., Panis, M., You, H., de Jong, Y.P., Rice, C.M., Human occludin is a hepatitis C virus entry factor required for infection of mouse cells. Nature 457 (2009), 882–886.
42. Pozzi, R., De Berardis, B., Paoletti, L., Guastadisegni, C., Inflammatory mediators induced by coarse (PM2.5-10) and fine (PM2.5) urban air particles in RAW 264.7 cells. Toxicology 183 (2003), 243–254.
43. Prabhudas, M., Bowdish, D., Drickamer, K., Febbraio, M., Herz, J., Kobzik, L., Krieger, M., Loike, J., Means, T.K., Moestrup, S.K., et al. Standardizing scavenger receptor nomenclature. J. Immunol. 192 (2014), 1997–2006.
44. Py, B.F., Kim, M.S., Vakifahmetoglu-Norberg, H., Yuan, J., Deubiquitination of NLRP3 by BRCC3 critically regulates inflammasome activity. Mol. Cell 49 (2013), 331–338.
45. Py, B.F., Jin, M., Desai, B.N., Penumaka, A., Zhu, H., Kober, M., Dietrich, A., Lipinski, M.M., Henry, T., Clapham, D.E., Yuan, J., Caspase-11 controls interleukin-1β release through degradation of TRPC1. Cell Rep. 6 (2014), 1122–1128.
46. Rigotti, A., Trigatti, B.L., Penman, M., Rayburn, H., Herz, J., Krieger, M., A targeted mutation in the murine gene encoding the high density lipoprotein (HDL) receptor scavenger receptor class B type I reveals its key role in HDL metabolism. Proc. Natl. Acad. Sci. USA 94 (1997), 12610–12615.
47. Rothlin, C.V., Carrera-Silva, E.A., Bosurgi, L., Ghosh, S., TAM receptor signaling in immune homeostasis. Annu. Rev. Immunol. 33 (2015), 355–391.
48. Sali, A., Blundell, T.L., Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234 (1993), 779–815.
49. Schroder, K., Tschopp, J., The inflammasomes. Cell 140 (2010), 821–832.
50. Sheedy, F.J., Grebe, A., Rayner, K.J., Kalantari, P., Ramkhelawon, B., Carpenter, S.B., Becker, C.E., Ediriweera, H.N., Mullick, A.E., Golenbock, D.T., et al. CD36 coordinates NLRP3 inflammasome activation by facilitating intracellular nucleation of soluble ligands into particulate ligands in sterile inflammation. Nat. Immunol. 14 (2013), 812–820.
51. Shi, J., Zhao, Y., Wang, K., Shi, X., Wang, Y., Huang, H., Zhuang, Y., Cai, T., Wang, F., Shao, F., Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature 526 (2015), 660–665.
52. Thakur, S.A., Hamilton, R.F. Jr., Holian, A., Role of scavenger receptor a family in lung inflammation from exposure to environmental particles. J. Immunotoxicol. 5 (2008), 151–157.
53. Thakur, S.A., Beamer, C.A., Migliaccio, C.T., Holian, A., Critical role of MARCO in crystalline silica-induced pulmonary inflammation. Toxicol. Sci. 108 (2009), 462–471.
54. Tschopp, J., Schroder, K., NLRP3 inflammasome activation: The convergence of multiple signalling pathways on ROS production?. Nat. Rev. Immunol. 10 (2010), 210–215.
55. Underhill, D.M., Goodridge, H.S., Information processing during phagocytosis. Nat. Rev. Immunol. 12 (2012), 492–502.
56. Wen, H., Miao, E.A., Ting, J.P., Mechanisms of NOD-like receptor-associated inflammasome activation. Immunity 39 (2013), 432–441.
57. WHO (2007). Elimination of silicosis. GOHNET news letter, 1-20: http://www.who.int/occupational_health/publications/newsletter/gohnet12e.pdf.
58. Yagnik, D.R., Hillyer, P., Marshall, D., Smythe, C.D., Krausz, T., Haskard, D.O., Landis, R.C., Noninflammatory phagocytosis of monosodium urate monohydrate crystals by mouse macrophages. Implications for the control of joint inflammation in gout. Arthritis Rheum. 43 (2000), 1779–1789.
59. Yalaoui, S., Huby, T., Franetich, J.F., Gego, A., Rametti, A., Moreau, M., Collet, X., Siau, A., van Gemert, G.J., Sauerwein, R.W., et al. Scavenger receptor BI boosts hepatocyte permissiveness to Plasmodium infection. Cell Host Microbe 4 (2008), 283–292.
60. Yazdi, A.S., Guarda, G., Riteau, N., Drexler, S.K., Tardivel, A., Couillin, I., Tschopp, J., Nanoparticles activate the NLR pyrin domain containing 3 (Nlrp3) inflammasome and cause pulmonary inflammation through release of IL-1α and IL-1β. Proc. Natl. Acad. Sci. USA 107 (2010), 19449–19454.
61. Zona, L., Lupberger, J., Sidahmed-Adrar, N., Thumann, C., Harris, H.J., Barnes, A., Florentin, J., Tawar, R.G., Xiao, F., Turek, M., et al. HRas signal transduction promotes hepatitis C virus cell entry by triggering assembly of the host tetraspanin receptor complex. Cell Host Microbe 13 (2013), 302–313.