CLEC5A-mediated enhancement of the inflammatory response in myeloid cells contributes to influenza virus pathogenicity in vivo

Journal of Virology

Volumn 91, Issue 1, 2017, Pages

  Teng, Ooiean ^a,b   Chen, Szu Ting ^c   Hsu, Tsui Ling ^d   Sia, Sin Fun ^b   Cole, Suzanne ^b   Valkenburg, Sophie A ^a,b   Hsu, Tzu Yun ^c   Zheng, Jian Teddy ^b   Tu, Wenwei ^b   Bruzzone, Roberto ^a,b   Peiris, Joseph Sriyal Malik ^a,b   Hsieh, Shie Liang ^c,d,e   Yen, Hui Ling ^b  

^a HKU PASTEUR RESEARCH CENTRE   (Hong Kong)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c NATIONAL YANG MING UNIVERSITY   (Taiwan)

^d GENOMICS RESEARCH CENTER   (Taiwan)

^e TAIPEI VETERANS GENERAL HOSPITAL   (Taiwan)

Author keywords

C type lectins; CLEC5A; Influenza virus; Macrophages; Spleen tyrosine kinase (Syk)

Indexed keywords

ALPHA INTERFERON; DECTIN 5; DOUBLE STRANDED RNA; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INFLUENZA VIRUS HEMAGGLUTININ; LECTIN; MESSENGER RNA; MONOCLONAL ANTIBODY; PROTEIN TYROSINE KINASE INHIBITOR; TOLL LIKE RECEPTOR 3; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; ANTIBODY; CELL SURFACE RECEPTOR; CLEC5A PROTEIN, HUMAN; CXCL10 PROTEIN, MOUSE; HEMAGGLUTININ, HUMAN INFLUENZA A VIRUS; ISOPROTEIN; PROTEIN BINDING; SMALL INTERFERING RNA; TLR3 PROTEIN, MOUSE;

ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CELL INFILTRATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IN VIVO STUDY; INFLAMMATION; INFLUENZA A VIRUS (H5N1); INFLUENZA VIRUS; INOCULATION; LENTIVIRINAE; MACROPHAGE; MOUSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SURVIVAL RATE; UPREGULATION; VIRUS PARTICLE; VIRUS RECOMBINANT; VIRUS REPLICATION; VIRUS VIRULENCE; WILD TYPE; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INFLUENZA A VIRUS (H1N1); KNOCKOUT MOUSE; LUNG; LUNG ALVEOLUS MACROPHAGE; METABOLISM; MORTALITY; ORTHOMYXOVIRUS INFECTION; PATHOGENICITY; PRIMARY CELL CULTURE; SURVIVAL ANALYSIS; VIROLOGY;

ANIMALS; ANTIBODIES; CHEMOKINE CXCL10; GENE EXPRESSION REGULATION; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HOST-PATHOGEN INTERACTIONS; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H5N1 SUBTYPE; INTERFERON-ALPHA; LECTINS, C-TYPE; LENTIVIRUS; LUNG; MACROPHAGES; MACROPHAGES, ALVEOLAR; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; ORTHOMYXOVIRIDAE INFECTIONS; PRIMARY CELL CULTURE; PROTEIN BINDING; PROTEIN ISOFORMS; RECEPTORS, CELL SURFACE; RNA, SMALL INTERFERING; SURVIVAL ANALYSIS; TOLL-LIKE RECEPTOR 3; TUMOR NECROSIS FACTOR-ALPHA;

EID: 85008150063     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01813-16     Document Type: Article

References (53)

1. Everitt AR, Clare S, Pertel T, John SP, Wash RS, Smith SE, Chin CR, Feeley EM, Sims JS, Adams DJ, Wise HM, Kane L, Goulding D, Digard P, Anttila V, Baillie JK, Walsh TS, Hume DA, Palotie A, Xue Y, Colonna V, Tyler-Smith C, Dunning J, Gordon SB, GenISIS Investigators, MOSAIC Investigators, Smyth RL, Openshaw PJ, Dougan G, Brass AL, Kellam P. 2012. IFITM3 restricts the morbidity and mortality associated with influenza. Nature 484:519-523. https://doi.org/10.1038/nature10921.
2. Haller O, Staeheli P, Schwemmle M, Kochs G. 2015. Mx GTPases: dynamin-like antiviral machines of innate immunity. Trends Microbiol 23:154-163. https://doi.org/10.1016/j.tim.2014.12.003.
3. Fukuyama S, Kawaoka Y. 2011. The pathogenesis of influenza virus infections: the contributions of virus and host factors. Curr Opin Immunol 23:481-486. https://doi.org/10.1016/j.coi.2011.07.016.
4. Kash JC, Taubenberger JK. 2015. The role of viral, host, and secondary bacterial factors in influenza pathogenesis. Am J Pathol 185:1528-1536. https://doi.org/10.1016/j.ajpath.2014.08.030.
5. Iwasaki A, Pillai PS. 2014. Innate immunity to influenza virus infection. Nat Rev Immunol 14:315-328. https://doi.org/10.1038/nri3665.
6. Guillot L, Le Goffic R, Bloch S, Escriou N, Akira S, Chignard M, Si-Tahar M. 2005 Involvement of toll-like receptor 3 in the immune response of lung epithelial cells to double-stranded RNA and influenza A virus. J Biol Chem 280:5571-5580. https://doi.org/10.1074/jbc.M410592200.
7. Lund JM, Alexopoulou L, Sato A, Karow M, Adams NC, Gale NW, Iwasaki A, Flavell RA. 2004. Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc Natl Acad Sci U S A 101:5598-5603. https://doi.org/10.1073/pnas.0400937101.
8. Diebold SS, Kaisho T, Hemmi H, Akira S, Reis e Sousa C. 2004. Innate antiviral responses by means of TLR7-mediated recognition of singlestranded RNA. Science 303:1529-1531. https://doi.org/10.1126/science.1093616.
9. Lee SM, Kok KH, Jaume M, Cheung TK, Yip TF, Lai JC, Guan Y, Webster RG, Jin DY, Peiris JS. 2014. Toll-like receptor 10 is involved in induction of innate immune responses to influenza virus infection. Proc Natl Acad Sci U S A 111:3793-3798. https://doi.org/10.1073/pnas.1324266111.
10. Pichlmair A, Schulz O, Tan CP, Naslund TI, Liljestrom P, Weber F, Reis e Sousa C. 2006. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5'-phosphates. Science 314:997-1001. https://doi.org/10.1126/science.1132998.
11. Allen IC, Scull MA, Moore CB, Holl EK, McElvania-TeKippe E, Taxman DJ, Guthrie EH, Pickles RJ, Ting JP. 2009. The NLRP3 inflammasome mediates in vivo innate immunity to influenza A virus through recognition of viral RNA. Immunity 30:556-565. https://doi.org/10.1016/j.immuni.2009.02.005.
12. Ichinohe T, Lee HK, Ogura Y, Flavell R, Iwasaki A. 2009. Inflammasome recognition of influenza virus is essential for adaptive immune responses. J Exp Med 206:79-87. https://doi.org/10.1084/jem.20081667.
13. Lupfer C, Thomas PG, Anand PK, Vogel P, Milasta S, Martinez J, Huang G, Green M, Kundu M, Chi H, Xavier RJ, Green DR, Lamkanfi M, Dinarello CA, Doherty PC, Kanneganti TD. 2013. Receptor interacting protein kinase 2-mediated mitophagy regulates inflammasome activation during virus infection. Nat Immunol 14:480-488. https://doi.org/10.1038/ni.2563.
14. Lupfer C, Thomas PG, Kanneganti TD. 2014. Nucleotide oligomerization and binding domain 2-dependent dendritic cell activation is necessary for innate immunity and optimal CD8+ T cell responses to influenza A virus infection. J Virol 88:8946-8955. https://doi.org/10.1128/JVI.01110-14.
15. de Jong MD, Simmons CP, Thanh TT, Hien VM, Smith GJ, Chau TN, Hoang DM, Chau NV, Khanh TH, Dong VC, Qui PT, Cam BV, Ha Do Q, Guan Y, Peiris JS, Chinh NT, Hien TT, Farrar J. 2006. Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat Med 12:1203-1207. https://doi.org/10.1038/nm1477.
16. Cheung CY, Poon LL, Lau AS, Luk W, Lau YL, Shortridge KF, Gordon S, Guan Y, Peiris JS. 2002. Induction of proinflammatory cytokines in human macrophages by influenza A (H5N1) viruses: a mechanism for the unusual severity of human disease? Lancet 360:1831-1837. https://doi.org/10.1016/S0140-6736(02)11772-7.
17. Perrone LA, Plowden JK, Garcia-Sastre A, Katz JM, Tumpey TM. 2008. H5N1 and 1918 pandemic influenza virus infection results in early and excessive infiltration of macrophages and neutrophils in the lungs of mice. PLoS Pathog 4:e1000115. https://doi.org/10.1371/journal.ppat.1000115.
18. Gao R, Bhatnagar J, Blau DM, Greer P, Rollin DC, Denison AM, Deleon-Carnes M, Shieh WJ, Sambhara S, Tumpey TM, Patel M, Liu L, Paddock C, Drew C, Shu Y, Katz JM, Zaki SR. 2013. Cytokine and chemokine profiles in lung tissues from fatal cases of 2009 pandemic influenza A (H1N1): role of the host immune response in pathogenesis. Am J Pathol 183: 1258-1268. https://doi.org/10.1016/j.ajpath.2013.06.023.
19. Wang Z, Zhang A, Wan Y, Liu X, Qiu C, Xi X, Ren Y, Wang J, Dong Y, Bao M, Li L, Zhou M, Yuan S, Sun J, Zhu Z, Chen L, Li Q, Zhang Z, Zhang X, Lu S, Doherty PC, Kedzierska K, Xu J. 2014. Early hypercytokinemia is associated with interferon-induced transmembrane protein-3 dysfunc-tion and predictive of fatal H7N9 infection. Proc Natl Acad Sci U S A 111:769-774. https://doi.org/10.1073/pnas.1321748111.
20. Drummond RA, Brown GD. 2013. Signalling C-type lectins in antimicrobial immunity. PLoS Pathog 9:e1003417. https://doi.org/10.1371/journal.ppat.1003417.
21. Iborra S, Sancho D. 2015. Signalling versatility following self and non-self sensing by myeloid C-type lectin receptors. Immunobiology 220: 175-184. https://doi.org/10.1016/j.imbio.2014.09.013.
22. Sancho D, Reis e Sousa C. 2012. Signaling by myeloid C-type lectin receptors in immunity and homeostasis. Annu Rev Immunol 30:491-529. https://doi.org/10.1146/annurev-immunol-031210-101352.
23. Herre J, Marshall AS, Caron E, Edwards AD, Williams DL, Schweighoffer E, Tybulewicz V, Reis e Sousa C, Gordon S, Brown GD. 2004. Dectin-1 uses novel mechanisms for yeast phagocytosis in macrophages. Blood 104: 4038-4045. https://doi.org/10.1182/blood-2004-03-1140.
24. Leibundgut-Landmann S, Osorio F, Brown GD, Reis e Sousa C. 2008. Stimulation of dendritic cells via the dectin-1/Syk pathway allows priming of cytotoxic T-cell responses. Blood 112:4971-4980. https://doi.org/10.1182/blood-2008-05-158469.
25. Graham LM, Gupta V, Schafer G, Reid DM, Kimberg M, Dennehy KM, Hornsell WG, Guler R, Campanero-Rhodes MA, Palma AS, Feizi T, Kim SK, Sobieszczuk P, Willment JA, Brown GD. 2012. The C-type lectin receptor CLECSF8 (CLEC4D) is expressed by myeloid cells and triggers cellular activation through Syk kinase. J Biol Chem 287:25964-25974. https://doi.org/10.1074/jbc.M112.384164.
26. Chen ST, Lin YL, Huang MT, Wu MF, Cheng SC, Lei HY, Lee CK, Chiou TW, Wong CH, Hsieh SL. 2008. CLEC5A is critical for dengue-virusinduced lethal disease. Nature 453:672-676. https://doi.org/10.1038/nature07013.
27. Wu MF, Chen ST, Yang AH, Lin WW, Lin YL, Chen NJ, Tsai IS, Li L, Hsieh SL. 2013. CLEC5A is critical for dengue virus-induced inflammasome activation in human macrophages. Blood 121:95-106. https://doi.org/10.1182/blood-2012-05-430090.
28. Ling MT, Tu W, Han Y, Mao H, Chong WP, Guan J, Liu M, Lam KT, Law HK, Peiris JS, Takahashi K, Lau YL. 2012. Mannose-binding lectin contributes to deleterious inflammatory response in pandemic H1N1 and avian H9N2 infection. J Infect Dis 205:44-53. https://doi.org/10.1093/infdis/jir691.
29. Hartshorn KL, Crouch EC, White MR, Eggleton P, Tauber AI, Chang D, Sastry K. 1994. Evidence for a protective role of pulmonary surfactant protein D (SP-D) against influenza A viruses. J Clin Investig 94:311-319. https://doi.org/10.1172/JCI117323.
30. Hansen S, Selman L, Palaniyar N, Ziegler K, Brandt J, Kliem A, Jonasson M, Skjoedt MO, Nielsen O, Hartshorn K, Jorgensen TJ, Skjodt K, Holmskov U. 2010. Collectin 11 (CL-11, CL-K1) is a MASP-1/3-associated plasma collectin with microbial-binding activity. J Immunol 185:6096-6104. https://doi.org/10.4049/jimmunol.1002185.
31. Yang ML, Chen YH, Wang SW, Huang YJ, Leu CH, Yeh NC, Chu CY, Lin CC, Shieh GS, Chen YL, Wang JR, Wang CH, Wu CL, Shiau AL. 2011. Galectin-1 binds to influenza virus and ameliorates influenza virus pathogenesis. J Virol 85:10010-10020. https://doi.org/10.1128/JVI.00301-11.
32. Andersen O, Vilsgaard Ravn K, Juul Sorensen I, Jonson G, Holm Nielsen E, Svehag SE. 1997. Serum amyloid P component binds to influenza A virus haemagglutinin and inhibits the virus infection in vitro. Scand J Immunol 46:331-337. https://doi.org/10.1046/j.1365-3083.1997.d01-147.x.
33. Londrigan SL, Turville SG, Tate MD, Deng YM, Brooks AG, Reading PC. 2011 N-linked glycosylation facilitates sialic acid-independent attachment and entry of influenza A viruses into cells expressing DC-SIGN or L-SIGN. J Virol 85:2990-3000. https://doi.org/10.1128/JVI.01705-10.
34. Ng WC, Liong S, Tate MD, Irimura T, Denda-Nagai K, Brooks AG, Londrigan SL, Reading PC. 2014. The macrophage galactose-type lectin can function as an attachment and entry receptor for influenza virus. J Virol 88:1659-1672. https://doi.org/10.1128/JVI.02014-13.
35. Reading PC, Miller JL, Anders EM. 2000. Involvement of the mannose receptor in infection of macrophages by influenza virus. J Virol 74: 5190-5197. https://doi.org/10.1128/JVI.74.11.5190-5197.2000.
36. Upham JP, Pickett D, Irimura T, Anders EM, Reading PC. 2010. Macrophage receptors for influenza A virus: role of the macrophage galactosetype lectin and mannose receptor in viral entry. J Virol 84:3730-3737. https://doi.org/10.1128/JVI.02148-09.
37. Chen ST, Liu RS, Wu MF, Lin YL, Chen SY, Tan DT, Chou TY, Tsai IS, Li L, Hsieh SL. 2012. CLEC5A regulates Japanese encephalitis virus-induced neuroinflammation and lethality. PLoS Pathog 8:e1002655. https://doi.org/10.1371/journal.ppat.1002655.
38. Mok KP, Wong CH, Cheung CY, Chan MC, Lee SM, Nicholls JM, Guan Y, Peiris JS. 2009. Viral genetic determinants of H5N1 influenza viruses that contribute to cytokine dysregulation. J Infect Dis 200:1104-1112. https://doi.org/10.1086/605606.
39. Hui KP, Lee SM, Cheung CY, Ng IH, Poon LL, Guan Y, Ip NY, Lau AS, Peiris JS. 2009. Induction of proinflammatory cytokines in primary human macrophages by influenza A virus (H5N1) is selectively regulated by IFN regulatory factor 3 and p38 MAPK. J Immunol 182:1088-1098. https://doi.org/10.4049/jimmunol.182.2.1088.
40. Bakker AB, Baker E, Sutherland GR, Phillips JH, Lanier LL. 1999. Myeloid DAP12-associating lectin (MDL)-1 is a cell surface receptor involved in the activation of myeloid cells. Proc Natl Acad Sci U S A 96:9792-9796. https://doi.org/10.1073/pnas.96.17.9792.
41. Cheung R, Shen F, Phillips JH, McGeachy MJ, Cua DJ, Heyworth PG, Pierce RH. 2011. Activation of MDL-1 (CLEC5A) on immature myeloid cells triggers lethal shock in mice. J Clin Investig 121:4446-4461. https://doi.org/10.1172/JCI57682.
42. Yamamoto N, Takeshita K, Shichijo M, Kokubo T, Sato M, Nakashima K, Ishimori M, Nagai H, Li YF, Yura T, Bacon KB. 2003. The orally available spleen tyrosine kinase inhibitor 2-[7-(3, 4-dimethoxyphenyl)-imidazo[1, 2-c]pyrimidin-5-ylamino]nicotinamide dihydrochloride (BAY 61-3606) blocks antigen-induced airway inflammation in rodents. J Pharmacol Exp Ther 306:1174-1181. https://doi.org/10.1124/jpet.103.052316.
43. Schroder K, Irvine KM, Taylor MS, Bokil NJ, Le Cao KA, Masterman KA, Labzin LI, Semple CA, Kapetanovic R, Fairbairn L, Akalin A, Faulkner GJ, Baillie JK, Gongora M, Daub CO, Kawaji H, McLachlan GJ, Goldman N, Grimmond SM, Carninci P, Suzuki H, Hayashizaki Y, Lenhard B, Hume DA, Sweet MJ. 2012. Conservation and divergence in Toll-like receptor 4-regulated gene expression in primary human versus mouse macrophages. Proc Natl Acad Sci U S A 109:E944-E953. https://doi.org/10.1073/pnas.1110156109.
44. Schneemann M, Schoedon G, Hofer S, Blau N, Guerrero L, Schaffner A. 1993 Nitric oxide synthase is not a constituent of the antimicrobial armature of human mononuclear phagocytes. J Infect Dis 167: 1358-1363. https://doi.org/10.1093/infdis/167.6.1358.
45. Aoki N, Kimura Y, Kimura S, Nagato T, Azumi M, Kobayashi H, Sato K, Tateno M. 2009. Expression and functional role of MDL-1 (CLEC5A) in mouse myeloid lineage cells. J Leukoc Biol 85:508-517.
46. Ichinohe T, Pang IK, Iwasaki A. 2010. Influenza virus activates inflammasomes via its intracellular M2 ion channel. Nat Immunol 11:404-410. https://doi.org/10.1038/ni.1861.
47. Ramirez-Ortiz ZG, Prasad A, Griffith JW, Pendergraft WF, III, Cowley GS, Root DE, Tai M, Luster AD, El Khoury J, Hacohen N, Means TK. 2015. The receptor TREML4 amplifies TLR7-mediated signaling during antiviral responses and autoimmunity. Nat Immunol 16:495-504. https://doi.org/10.1038/ni.3143.
48. Pothlichet J, Meunier I, Davis BK, Ting JP, Skamene E, von Messling V, Vidal SM. 2013. Type I IFN triggers RIG-I/TLR3/NLRP3-dependent inflammasome activation in influenza A virus infected cells. PLoS Pathog 9:e1003256. https://doi.org/10.1371/journal.ppat.1003256.
49. Leung YH, Nicholls JM, Ho CK, Sia SF, Mok CK, Valkenburg SA, Cheung P, Hui KP, Chan RW, Guan Y, Akira S, Peiris JS. 2014. Highly pathogenic avian influenza A H5N1 and pandemic H1N1 virus infections have different phenotypes in Toll-like receptor 3 knockout mice. J Gen Virol 95:1870-1879. https://doi.org/10.1099/vir.0.066258-0.
50. Le Goffic R, Balloy V, Lagranderie M, Alexopoulou L, Escriou N, Flavell R, Chignard M, Si-Tahar M. 2006. Detrimental contribution of the Toll-like receptor (TLR)3 to influenza A virus-induced acute pneumonia. PLoS Pathog 2:e53. https://doi.org/10.1371/journal.ppat.0020053.
51. Nefkens I, Garcia JM, Ling CS, Lagarde N, Nicholls J, Tang DJ, Peiris M, Buchy P, Altmeyer R. 2007. Hemagglutinin pseudotyped lentiviral particles: characterization of a new method for avian H5N1 influenza sero-diagnosis. J Clin Virol 39:27-33. https://doi.org/10.1016/j.jcv.2007.02.005.
52. Hoffmann E, Neumann G, Kawaoka Y, Hobom G, Webster RG. 2000. A DNA transfection system for generation of influenza A virus from eight plasmids. Proc Natl Acad Sci U S A 97:6108-6113. https://doi.org/10.1073/pnas.100133697.
53. Li S, Liu C, Klimov A, Subbarao K, Perdue ML, Mo D, Ji Y, Woods L, Hietala S, Bryant M. 1999. Recombinant influenza A virus vaccines for the pathogenic human A/Hong Kong/97 (H5N1) viruses. J Infect Dis 179: 1132-1138. https://doi.org/10.1086/314713.