Dengue Virus Perturbs Mitochondrial Morphodynamics to Dampen Innate Immune Responses

Cell Host and Microbe

Volumn 20, Issue 3, 2016, Pages 342-356

  Chatel Chaix, Laurent ^a   Cortese, Mirko ^a   Romero Brey, Inés ^a   Bender, Silke ^a   Neufeldt, Christopher John ^a   Fischl, Wolfgang ^a   Scaturro, Pietro ^a   Schieber, Nicole ^b   Schwab, Yannick ^b   Fischer, Bernd ^c   Ruggieri, Alessia ^a   Bartenschlager, Ralf ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

NONSTRUCTURAL PROTEIN 4B; DNM1L PROTEIN, HUMAN; GUANOSINE TRIPHOSPHATASE; MICROTUBULE ASSOCIATED PROTEIN; MITOCHONDRIAL PROTEIN; NS4B PROTEIN, FLAVIVIRUS; VIRAL PROTEIN;

ARTICLE; DENGUE VIRUS; ENDOPLASMIC RETICULUM; IMMUNE RESPONSE; INNATE IMMUNITY; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL MEMBRANE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRUS REPLICATION; ANTAGONISTS AND INHIBITORS; HOST PATHOGEN INTERACTION; IMMUNE EVASION; METABOLISM; MITOCHONDRION; PATHOGENICITY; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

DENGUE VIRUS; GTP PHOSPHOHYDROLASES; HOST-PATHOGEN INTERACTIONS; IMMUNE EVASION; IMMUNITY, INNATE; MICROSCOPY, ELECTRON, TRANSMISSION; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; VIRAL NONSTRUCTURAL PROTEINS;

EID: 84995550705     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2016.07.008     Document Type: Article

References (49)

1. Acosta, E.G., Kumar, A., Bartenschlager, R., Revisiting dengue virus-host cell interaction: new insights into molecular and cellular virology. Adv. Virus Res. 88 (2014), 1–109.
2. Aguirre, S., Maestre, A.M., Pagni, S., Patel, J.R., Savage, T., Gutman, D., Maringer, K., Bernal-Rubio, D., Shabman, R.S., Simon, V., et al. DENV inhibits type I IFN production in infected cells by cleaving human STING. PLoS Pathog., 8, 2012, e1002934.
3. Bhatt, S., Gething, P.W., Brady, O.J., Messina, J.P., Farlow, A.W., Moyes, C.L., Drake, J.M., Brownstein, J.S., Hoen, A.G., Sankoh, O., et al. The global distribution and burden of dengue. Nature 496 (2013), 504–507.
4. Castanier, C., Garcin, D., Vazquez, A., Arnoult, D., Mitochondrial dynamics regulate the RIG-I-like receptor antiviral pathway. EMBO Rep. 11 (2010), 133–138.
5. Chan, D.C., Fusion and fission: interlinked processes critical for mitochondrial health. Annu. Rev. Genet. 46 (2012), 265–287.
6. Chan, Y.K., Gack, M.U., A phosphomimetic-based mechanism of dengue virus to antagonize innate immunity. Nat. Immunol. 17 (2016), 523–530.
7. Chatel-Chaix, L., Bartenschlager, R., Dengue virus- and hepatitis C virus-induced replication and assembly compartments: the enemy inside–caught in the web. J. Virol. 88 (2014), 5907–5911.
8. Chatel-Chaix, L., Fischl, W., Scaturro, P., Cortese, M., Kallis, S., Bartenschlager, M., Fischer, B., Bartenschlager, R., A Combined Genetic-Proteomic Approach Identifies Residues within Dengue Virus NS4B Critical for Interaction with NS3 and Viral Replication. J. Virol. 89 (2015), 7170–7186.
9. Chen, Y., Dorn, G.W. 2nd, PINK1-phosphorylated mitofusin 2 is a Parkin receptor for culling damaged mitochondria. Science 340 (2013), 471–475.
10. Chen, H., Detmer, S.A., Ewald, A.J., Griffin, E.E., Fraser, S.E., Chan, D.C., Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J. Cell Biol. 160 (2003), 189–200.
11. Dalrymple, N.A., Cimica, V., Mackow, E.R., Dengue Virus NS Proteins Inhibit RIG-I/MAVS Signaling by Blocking TBK1/IRF3 Phosphorylation: Dengue Virus Serotype 1 NS4A Is a Unique Interferon-Regulating Virulence Determinant. MBio, 6, 2015 e00553–15.
12. Friedman, J.R., Lackner, L.L., West, M., DiBenedetto, J.R., Nunnari, J., Voeltz, G.K., ER tubules mark sites of mitochondrial division. Science 334 (2011), 358–362.
13. Glauser, L., Sonnay, S., Stafa, K., Moore, D.J., Parkin promotes the ubiquitination and degradation of the mitochondrial fusion factor mitofusin 1. J. Neurochem. 118 (2011), 636–645.
14. Horner, S.M., Liu, H.M., Park, H.S., Briley, J., Gale, M. Jr., Mitochondrial-associated endoplasmic reticulum membranes (MAM) form innate immune synapses and are targeted by hepatitis C virus. Proc. Natl. Acad. Sci. USA 108 (2011), 14590–14595.
15. Kakumani, P.K., Ponia, S.S., Rajgokul, K.S., Sood, V., Chinnappan, M., Banerjea, A.C., Medigeshi, G.R., Malhotra, P., Mukherjee, S.K., Bhatnagar, R.K., Role of RNA interference (RNAi) in dengue virus replication and identification of NS4B as an RNAi suppressor. J. Virol. 87 (2013), 8870–8883.
16. Kim, S.J., Syed, G.H., Khan, M., Chiu, W.W., Sohail, M.A., Gish, R.G., Siddiqui, A., Hepatitis C virus triggers mitochondrial fission and attenuates apoptosis to promote viral persistence. Proc. Natl. Acad. Sci. USA 111 (2014), 6413–6418.
17. Knoops, K., Kikkert, M., Worm, S.H., Zevenhoven-Dobbe, J.C., van der Meer, Y., Koster, A.J., Mommaas, A.M., Snijder, E.J., SARS-coronavirus replication is supported by a reticulovesicular network of modified endoplasmic reticulum. PLoS Biol., 6, 2008, e226.
18. Korobova, F., Ramabhadran, V., Higgs, H.N., An actin-dependent step in mitochondrial fission mediated by the ER-associated formin INF2. Science 339 (2013), 464–467.
19. Leboucher, G.P., Tsai, Y.C., Yang, M., Shaw, K.C., Zhou, M., Veenstra, T.D., Glickman, M.H., Weissman, A.M., Stress-induced phosphorylation and proteasomal degradation of mitofusin 2 facilitates mitochondrial fragmentation and apoptosis. Mol. Cell 47 (2012), 547–557.
20. Lee, H., Yoon, Y., Mitochondrial fission: regulation and ER connection. Mol. Cells 37 (2014), 89–94.
21. Manor, U., Bartholomew, S., Golani, G., Christenson, E., Kozlov, M., Higgs, H., Spudich, J., Lippincott-Schwartz, J., A mitochondria-anchored isoform of the actin-nucleating spire protein regulates mitochondrial division. eLife, 4, 2015, e08828.
22. McLean, J.E., Wudzinska, A., Datan, E., Quaglino, D., Zakeri, Z., Flavivirus NS4A-induced autophagy protects cells against death and enhances virus replication. J. Biol. Chem. 286 (2011), 22147–22159.
23. Miller, S., Kastner, S., Krijnse-Locker, J., Bühler, S., Bartenschlager, R., The non-structural protein 4A of dengue virus is an integral membrane protein inducing membrane alterations in a 2K-regulated manner. J. Biol. Chem. 282 (2007), 8873–8882.
24. Muñoz-Jordan, J.L., Sánchez-Burgos, G.G., Laurent-Rolle, M., García-Sastre, A., Inhibition of interferon signaling by dengue virus. Proc. Natl. Acad. Sci. USA 100 (2003), 14333–14338.
25. Muñoz-Jordán, J.L., Laurent-Rolle, M., Ashour, J., Martínez-Sobrido, L., Ashok, M., Lipkin, W.I., García-Sastre, A., Inhibition of alpha/beta interferon signaling by the NS4B protein of flaviviruses. J. Virol. 79 (2005), 8004–8013.
26. Naghdi, S., Hajnoczky, G., VDAC2-specific cellular functions and the underlying structure. Biochim. Biophys. Acta., 2016, 10.1016/j.bbamcr.2016.04.020 Published online April 23, 2016.
27. Olichon, A., Baricault, L., Gas, N., Guillou, E., Valette, A., Belenguer, P., Lenaers, G., Loss of OPA1 perturbates the mitochondrial inner membrane structure and integrity, leading to cytochrome c release and apoptosis. J. Biol. Chem. 278 (2003), 7743–7746.
28. Onoguchi, K., Onomoto, K., Takamatsu, S., Jogi, M., Takemura, A., Morimoto, S., Julkunen, I., Namiki, H., Yoneyama, M., Fujita, T., Virus-infection or 5’ppp-RNA activates antiviral signal through redistribution of IPS-1 mediated by MFN1. PLoS Pathog., 6, 2010, e1001012.
29. Otera, H., Wang, C., Cleland, M.M., Setoguchi, K., Yokota, S., Youle, R.J., Mihara, K., Mff is an essential factor for mitochondrial recruitment of Drp1 during mitochondrial fission in mammalian cells. J. Cell Biol. 191 (2010), 1141–1158.
30. Paul, D., Bartenschlager, R., Architecture and biogenesis of plus-strand RNA virus replication factories. World J. Virol. 2 (2013), 32–48.
31. Poston, C.N., Krishnan, S.C., Bazemore-Walker, C.R., In-depth proteomic analysis of mammalian mitochondria-associated membranes (MAM). J. Proteomics 79 (2013), 219–230.
32. Pyakurel, A., Savoia, C., Hess, D., Scorrano, L., Extracellular regulated kinase phosphorylates mitofusin 1 to control mitochondrial morphology and apoptosis. Mol. Cell 58 (2015), 244–254.
33. Shi, C.S., Qi, H.Y., Boularan, C., Huang, N.N., Abu-Asab, M., Shelhamer, J.H., Kehrl, J.H., SARS-coronavirus open reading frame-9b suppresses innate immunity by targeting mitochondria and the MAVS/TRAF3/TRAF6 signalosome. J. Immunol. 193 (2014), 3080–3089.
34. Smirnova, E., Shurland, D.L., Ryazantsev, S.N., van der Bliek, A.M., A human dynamin-related protein controls the distribution of mitochondria. J. Cell Biol. 143 (1998), 351–358.
35. Smirnova, E., Griparic, L., Shurland, D.L., van der Bliek, A.M., Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Mol. Biol. Cell 12 (2001), 2245–2256.
36. Strack, S., Cribbs, J.T., Allosteric modulation of Drp1 mechanoenzyme assembly and mitochondrial fission by the variable domain. J. Biol. Chem. 287 (2012), 10990–11001.
37. Sun, L., Xing, Y., Chen, X., Zheng, Y., Yang, Y., Nichols, D.B., Clementz, M.A., Banach, B.S., Li, K., Baker, S.C., Chen, Z., Coronavirus papain-like proteases negatively regulate antiviral innate immune response through disruption of STING-mediated signaling. PLoS ONE, 7, 2012, e30802.
38. van Vliet, A.R., Verfaillie, T., Agostinis, P., New functions of mitochondria associated membranes in cellular signaling. Biochim. Biophys. Acta 1843 (2014), 2253–2262.
39. Vance, J.E., MAM (mitochondria-associated membranes) in mammalian cells: lipids and beyond. Biochim. Biophys. Acta 1841 (2014), 595–609.
40. Welsch, S., Miller, S., Romero-Brey, I., Merz, A., Bleck, C.K., Walther, P., Fuller, S.D., Antony, C., Krijnse-Locker, J., Bartenschlager, R., Composition and three-dimensional architecture of the dengue virus replication and assembly sites. Cell Host Microbe 5 (2009), 365–375.
41. Westaway, E.G., Mackenzie, J.M., Kenney, M.T., Jones, M.K., Khromykh, A.A., Ultrastructure of Kunjin virus-infected cells: colocalization of NS1 and NS3 with double-stranded RNA, and of NS2B with NS3, in virus-induced membrane structures. J. Virol. 71 (1997), 6650–6661.
42. World Health Organization. Dengue: Guidelines for Diagnosis,Treatment, Prevention and Control. 2009, World Health Organization.
43. Xia, M., Gonzalez, P., Li, C., Meng, G., Jiang, A., Wang, H., Gao, Q., Debatin, K.M., Beltinger, C., Wei, J., Mitophagy enhances oncolytic measles virus replication by mitigating DDX58/RIG-I-like receptor signaling. J. Virol. 88 (2014), 5152–5164.
44. Xie, X., Zou, J., Wang, Q.Y., Shi, P.Y., Targeting dengue virus NS4B protein for drug discovery. Antiviral Res. 118 (2015), 39–45.
45. Yasukawa, K., Oshiumi, H., Takeda, M., Ishihara, N., Yanagi, Y., Seya, T., Kawabata, S., Koshiba, T., Mitofusin 2 inhibits mitochondrial antiviral signaling. Sci. Signal., 2, 2009, ra47.
46. Yoshizumi, T., Ichinohe, T., Sasaki, O., Otera, H., Kawabata, S., Mihara, K., Koshiba, T., Influenza A virus protein PB1-F2 translocates into mitochondria via Tom40 channels and impairs innate immunity. Nat. Commun., 5, 2014, 4713.
47. Yu, C.Y., Chang, T.H., Liang, J.J., Chiang, R.L., Lee, Y.L., Liao, C.L., Lin, Y.L., Dengue virus targets the adaptor protein MITA to subvert host innate immunity. PLoS Pathog., 8, 2012, e1002780.
48. Yu, C.Y., Liang, J.J., Li, J.K., Lee, Y.L., Chang, B.L., Su, C.I., Huang, W.J., Lai, M.M., Lin, Y.L., Dengue Virus Impairs Mitochondrial Fusion by Cleaving Mitofusins. PLoS Pathog., 11, 2015, e1005350.
49. Ziviani, E., Tao, R.N., Whitworth, A.J., Drosophila parkin requires PINK1 for mitochondrial translocation and ubiquitinates mitofusin. Proc. Natl. Acad. Sci. USA 107 (2010), 5018–5023.