Visualization of early infiuenza A virus trafficking in human dendritic cells using STED microscopy

PLoS ONE

Volumn 12, Issue 6, 2017, Pages

  Baharom, Faezzah ^a   Thomas, Oliver S ^a   Lepzien, Rico ^a   Mellman, Ira ^a   Chalouni, Cécile ^a   Smed Sörensen, Anna ^a  

^a NONE

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOPROTEIN; CORE PROTEIN; EARLY ENDOSOME ANTIGEN 1; HLA DR ANTIGEN; LAMP1 PROTEIN, HUMAN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN; NP PROTEIN, INFLUENZA A VIRUS; RNA BINDING PROTEIN; VESICULAR TRANSPORT PROTEIN;

ARTICLE; CELL ISOLATION; CELL MIGRATION; CONTROLLED STUDY; DENDRITIC CELL; ENDOSOME; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLUENZA A VIRUS; MICROSCOPY; MONOCYTE; STIMULATED EMISSION DEPLETION MICROSCOPY; VIRUS PARTICLE; VIRUS REPLICATION; EPITHELIUM CELL; GENETICS; HOST PATHOGEN INTERACTION; ISOLATION AND PURIFICATION; METABOLISM; PATHOGENICITY; ULTRASTRUCTURE; VIRION; VIROLOGY;

DENDRITIC CELLS; ENDOSOMES; EPITHELIAL CELLS; HLA-DR ANTIGENS; HOST-PATHOGEN INTERACTIONS; HUMANS; INFLUENZA A VIRUS; LYSOSOME-ASSOCIATED MEMBRANE GLYCOPROTEINS; MICROSCOPY; RNA-BINDING PROTEINS; VESICULAR TRANSPORT PROTEINS; VIRAL CORE PROTEINS; VIRION; VIRUS REPLICATION;

EID: 85020240243     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0177920     Document Type: Article

References (51)

1. World Health Organization. The top 10 causes of death-Fact sheet no. 310 2014 [cited 2016 30 August 2016]. http://www.who.int/mediacentre/factsheets/fs310/en/]
2. Glezen WP. Emerging infections: pandemic influenza. Epidemiol Rev. 1996;18(1):64-76.
3. Yewdell J, Garcia-Sastre A. Influenza virus still surprises. Curr Opin Microbiol. 2002;5(4):414-8.
4. Hilleman MR, Flatley FJ, Anderson SA, Luecking ML, Levinson DJ. Distribution and significance of Asian and other influenza antibodies in the human population. N Engl J Med. 1958;258(20):969-74.
5. Doherty PC, Topham DJ, Tripp RA, Cardin RD, Brooks JW, Stevenson PG. Effector CD4+ and CD8+ T-cell mechanisms in the control of respiratory virus infections. Immunol Rev. 1997;159:105-17.
6. Bhardwaj N, Bender A, Gonzalez N, Bui LK, Garrett MC, Steinman RM. Influenza virus-infected dendritic cells stimulate strong proliferative and cytolytic responses from human CD8+ T cells. J Clin Invest. 1994;94(2):797-807.
7. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature. 1998;392(6673):245-52.
8. Mercer J, Greber UF. Virus interactions with endocytic pathways in macrophages and dendritic cells. Trends Microbiol. 2013;21(8):380-8.
9. van de Sandt CE, Kreijtz JH, Rimmelzwaan GF. Evasion of influenza A viruses from innate and adaptive immune responses. Viruses. 2012;4(9):1438-76.
10. Herter S, Osterloh P, Hilf N, Rechtsteiner G, Hohfeld J, Rammensee HG, et al. Dendritic cell aggresome-like-induced structure formation and delayed antigen presentation coincide in influenza virus-infected dendritic cells. Journal of immunology. 2005;175(2):891-8.
11. Smed-Sorensen A, Chalouni C, Chatterjee B, Cohn L, Blattmann P, Nakamura N, et al. Influenza A virus infection of human primary dendritic cells impairs their ability to cross-present antigen to CD8 T cells. PLoS Pathog. 2012;8(3):e1002572. Epub 2012/03/14. PubMed Central PMCID: PMC3297599.
12. Mellman I, Steinman RM. Dendritic cells: specialized and regulated antigen processing machines. Cell. 2001;106(3):255-8. Epub 2001/08/18.
13. Trombetta ES, Mellman I. Cell biology of antigen processing in vitro and in vivo. Annu Rev Immunol. 2005;23:975-1028.
14. Trombetta ES, Ebersold M, Garrett W, Pypaert M, Mellman I. Activation of lysosomal function during dendritic cell maturation. Science. 2003;299(5611):1400-3.
15. Vyas JM, Van der Veen AG, Ploegh HL. The known unknowns of antigen processing and presentation. Nat Rev Immunol. 2008;8(8):607-18.
16. Edinger TO, Pohl MO, Stertz S. Entry of influenza A virus: host factors and antiviral targets. J Gen Virol. 2014;95(Pt 2):263-77.
17. Yoshimura A, Ohnishi S. Uncoating of influenza virus in endosomes. J Virol. 1984;51(2):497-504.
18. Matlin KS, Reggio H, Helenius A, Simons K. Infectious entry pathway of influenza virus in a canine kidney cell line. J Cell Biol. 1981;91(3 Pt 1):601-13.
19. Harrison SC. Viral membrane fusion. Nat Struct Mol Biol. 2008;15(7):690-8.
20. Hamilton BS, Whittaker GR, Daniel S. Influenza virus-mediated membrane fusion: determinants of hemagglutinin fusogenic activity and experimental approaches for assessing virus fusion. Viruses. 2012;4(7):1144-68.
21. Sieczkarski SB, Whittaker GR. Differential requirements of Rab5 and Rab7 for endocytosis of influenza and other enveloped viruses. Traffic. 2003;4(5):333-43.
22. Edinger TO, Pohl MO, Yanguez E, Stertz S. Cathepsin W Is Required for Escape of Influenza A Virus from Late Endosomes. MBio. 2015;6(3):e00297.
23. Dias A, Bouvier D, Crepin T, McCarthy AA, Hart DJ, Baudin F, et al. The cap-snatching endonuclease of influenza virus polymerase resides in the PA subunit. Nature. 2009;458(7240):914-8.
24. Savina A, Amigorena S. Phagocytosis and antigen presentation in dendritic cells. Immunol Rev. 2007;219:143-56.
25. Lakadamyali M, Rust MJ, Babcock HP, Zhuang X. Visualizing infection of individual influenza viruses. Proc Natl Acad Sci U S A. 2003;100(16):9280-5.
26. Willig KI, Harke B, Medda R, Hell SW. STED microscopy with continuous wave beams. Nat Methods. 2007;4(11):915-8.
27. Colberg-Poley AM, Patterson GH, Salka K, Bhuvanendran S, Yang D, Jaiswal JK. Superresolution imaging of viral protein trafficking. Med Microbiol Immunol. 2015;204(3):449-60.
28. Hell SW, Wichmann J. Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy. Opt Lett. 1994;19(11):780-2.
29. Schermelleh L, Heintzmann R, Leonhardt H. A guide to super-resolution fluorescence microscopy. J Cell Biol. 2010;190(2):165-75.
30. Blom H, Brismar H. STED microscopy: increased resolution for medical research? J Intern Med. 2014;276(6):560-78.
31. Baharom F, Thomas S, Bieder A, Hellmer M, Volz J, Sandgren KJ, et al. Protection of Human Myeloid Dendritic Cell Subsets against Influenza A Virus Infection Is Differentially Regulated upon TLR Stimulation. Journal of immunology. 2015.
32. van der Walt S, Schonberger JL, Nunez-Iglesias J, Boulogne F, Warner JD, Yager N, et al. scikit-image: image processing in Python. PeerJ. 2014;2:e453.
33. Fontana J, Steven AC. Influenza virus-mediated membrane fusion: Structural insights from electron microscopy. Arch Biochem Biophys. 2015;581:86-97.
34. Kramer B, Pelchen-Matthews A, Deneka M, Garcia E, Piguet V, Marsh M. HIV interaction with endosomes in macrophages and dendritic cells. Blood Cells Mol Dis. 2005;35(2):136-42.
35. Garcia E, Pion M, Pelchen-Matthews A, Collinson L, Arrighi JF, Blot G, et al. HIV-1 trafficking to the dendritic cell-T-cell infectious synapse uses a pathway of tetraspanin sorting to the immunological synapse. Traffic. 2005;6(6):488-501.
36. Schoonderwoert V, Dijkstra R, Luckinavicius G, Kobler O, van der Voort H. Huygens STED Deconvolution Increases Signal-To-Noise and Image Resolution towards 22 nm. Microscopy Today. 2013;21(06):38-44.
37. Sandgren KJ, Smed-Sorensen A, Forsell MN, Soldemo M, Adams WC, Liang F, et al. Human plasmacytoid dendritic cells efficiently capture HIV-1 envelope glycoproteins via CD4 for antigen presentation. Journal of immunology. 2013;191(1):60-9.
38. Cohn L, Chatterjee B, Esselborn F, Smed-Sorensen A, Nakamura N, Chalouni C, et al. Antigen delivery to early endosomes eliminates the superiority of human blood BDCA3+ dendritic cells at cross presentation. J Exp Med. 2013;210(5):1049-63.
39. Chatterjee B, Smed-Sorensen A, Cohn L, Chalouni C, Vandlen R, Lee BC, et al. Internalization and endosomal degradation of receptor-bound antigens regulate the efficiency of cross presentation by human dendritic cells. Blood. 2012;120(10):2011-20.
40. Zhou Z, Xue Q, Wan Y, Yang Y, Wang J, Hung T. Lysosome-Associated membrane glycoprotein 3 is involved in influenza A virus replication in human lung epithelial (A549) cells. Virol J. 2011;8:384.
41. de Vries E, Tscherne DM, Wienholts MJ, Cobos-Jimenez V, Scholte F, Garcia-Sastre A, et al. Dissection of the influenza A virus endocytic routes reveals macropinocytosis as an alternative entry pathway. PLoS Pathog. 2011;7(3):e1001329.
42. Banerjee I, Miyake Y, Nobs SP, Schneider C, Horvath P, Kopf M, et al. Influenza A virus uses the aggresome processing machinery for host cell entry. Science. 2014;346(6208):473-7.
43. Lee BL, Barton GM. Trafficking of endosomal Toll-like receptors. Trends Cell Biol. 2014;24(6):360-9
44. Nair-Gupta P, Baccarini A, Tung N, Seyffer F, Florey O, Huang Y, et al. TLR signals induce phagosomal MHC-I delivery from the endosomal recycling compartment to allow cross-presentation. Cell. 2014;158(3):506-21.
45. Watts C, West MA, Zaru R. TLR signalling regulated antigen presentation in dendritic cells. Curr Opin Immunol. 2010;22(1):124-30.
46. Segura E, Touzot M, Bohineust A, Cappuccio A, Chiocchia G, Hosmalin A, et al. Human inflammatory dendritic cells induce Th17 cell differentiation. Immunity. 2013;38(2):336-48.
47. Schmid S, Fuchs R, Kielian M, Helenius A, Mellman I. Acidification of endosome subpopulations in wild-Type Chinese hamster ovary cells and temperature-sensitive acidification-defective mutants. J Cell Biol. 1989;108(4):1291-300.
48. Gujuluva CN, Kundu A, Murti KG, Nayak DP. Abortive replication of influenza virus A/WSN/33 in HeLa229 cells: defective viral entry and budding processes. Virology. 1994;204(2):491-505.
49. Short KR, Brooks AG, Reading PC, Londrigan SL. The fate of influenza A virus after infection of human macrophages and dendritic cells. J Gen Virol. 2012;93(Pt 11):2315-25.
50. Spadaro F, Lapenta C, Donati S, Abalsamo L, Barnaba V, Belardelli F, et al. IFN-Alpha enhances cross-presentation in human dendritic cells by modulating antigen survival, endocytic routing, and processing. Blood. 2012;119(6):1407-17.
51. Fernandez-Sesma A, Marukian S, Ebersole BJ, Kaminski D, Park MS, Yuen T, et al. Influenza virus evades innate and adaptive immunity via the NS1 protein. J Virol. 2006;80(13):6295-304.