Coronaviruses and arteriviruses display striking differences in their cyclophilin A-dependence during replication in cell culture

Virology

Volumn 517, Issue , 2018, Pages 148-156

  de Wilde, Adriaan H ^a   Zevenhoven Dobbe, Jessika C ^a   Beugeling, Corrine ^a   Chatterji, Udayan ^b   de Jong, Danielle ^a   Gallay, Philippe ^b   Szuhai, Karoly ^a   Posthuma, Clara C ^a   Snijder, Eric J ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Arterivirus; CRISPR Cas9; Cyclophilin; CypA; EAV; human coronavirus 229E; Knockout; MERS coronavirus

Indexed keywords

CYCLOPHILIN A;

ARTERIVIRUS; ARTERIVIRUS EQUINE ARTERITIS VIRUS; ARTICLE; BETACORONAVIRUS; CELL CULTURE; CONTROLLED STUDY; CORONAVIRINAE; CRISPR-CAS9 SYSTEM; HUMAN; HUMAN CELL; HUMAN CORONAVIRUS 229E; KARYOTYPING; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; SEQUENCE ANALYSIS; VIRUS CELL INTERACTION; VIRUS REPLICATION; VIRUS STRAIN; VIRUS TITRATION; WESTERN BLOTTING; ANIMAL; CELL LINE; HAMSTER; METABOLISM; PHYSIOLOGY; VIRUS CULTURE;

ANIMALS; ARTERIVIRUS; CELL LINE; CORONAVIRUS; CRICETINAE; CYCLOPHILIN A; HUMANS; VIRUS CULTIVATION; VIRUS REPLICATION;

EID: 85039413597     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2017.11.022     Document Type: Article

References (60)

1. Blight, K.J., McKeating, J.A., Rice, C.M., Highly permissive cell lines for subgenomic and genomic hepatitis C virus RNA replication. J. Virol. 76 (2002), 13001–13014.
2. Braaten, D., Franke, E.K., Luban, J., Cyclophilin A is required for an early step in the life cycle of human immunodeficiency virus type 1 before the initiation of reverse transcription. J. Virol. 70 (1996), 3551–3560.
3. Bryans, J.T., Crowe, M.E., Doll, E.R., McCollum, W.H., Isolation of a filterable agent causing arteritis of horses and abortion by mares; its differentiation from the equine abortion (influenza) virus. Cornell Vet. 47 (1957), 3–41.
4. Carbajo-Lozoya, J., Ma-Lauer, Y., Malesevic, M., Theuerkorn, M., Kahlert, V., Prell, E., von Brunn, B., Muth, D., Baumert, T.F., Drosten, C., Fischer, G., von Brunn, A., Human coronavirus NL63 replication is cyclophilin A-dependent and inhibited by non-immunosuppressive cyclosporine A-derivatives including Alisporivir. Virus Res. 184C (2014), 44–53.
5. Carbajo-Lozoya, J., Muller, M.A., Kallies, S., Thiel, V., Drosten, C., von Brunn, A., Replication of human coronaviruses SARS-CoV, HCoV-NL63 and HCoV-229E is inhibited by the drug FK506. Virus Res. 165 (2012), 112–117.
6. Carlotti, F., Bazuine, M., Kekarainen, T., Seppen, J., Pognonec, P., Maassen, J.A., Hoeben, R.C., Lentiviral vectors efficiently transduce quiescent mature 3T3-L1 adipocytes. Mol. Ther.: J. Am. Soc. Gene Ther. 9 (2004), 209–217.
7. Cervantes-Barragan, L., Zust, R., Maier, R., Sierro, S., Janda, J., Levy, F., Speiser, D., Romero, P., Rohrlich, P.S., Ludewig, B., Thiel, V., Dendritic cell-specific antigen delivery by coronavirus vaccine vectors induces long-lasting protective antiviral and antitumor immunity. MBio 1 (2010), e00171–00110.
8. Chatterji, U., Bobardt, M., Selvarajah, S., Yang, F., Tang, H., Sakamoto, N., Vuagniaux, G., Parkinson, T., Gallay, P., The isomerase active site of cyclophilin A is critical for hepatitis C virus replication. J. Biol. Chem. 284 (2009), 16998–17005.
9. Cong, L., Ran, F.A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P.D., Wu, X., Jiang, W., Marraffini, L.A., Zhang, F., Multiplex genome engineering using CRISPR/Cas systems. Science 339 (2013), 819–823.
10. Davis, T.L., Walker, J.R., Campagna-Slater, V., Finerty, P.J., Paramanathan, R., Bernstein, G., MacKenzie, F., Tempel, W., Ouyang, H., Lee, W.H., Eisenmesser, E.Z., Dhe-Paganon, S., Structural and biochemical characterization of the human cyclophilin family of peptidyl-prolyl isomerases. PLoS Biol., 8, 2010, e1000439.
11. de Graaff, M.A., de Jong, D., Briaire-de Bruijn, I.H., Hogendoorn, P.C., Bovee, J.V., Szuhai, K., A translocation t(6;14) in two cases of leiomyosarcoma: Molecular cytogenetic and array-based comparative genomic hybridization characterization. Cancer Genet. 208 (2015), 537–544.
12. de Wilde, A.H., Falzarano, D., Zevenhoven-Dobbe, J.C., Beugeling, C., Fett, C., Martellaro, C., Posthuma, C.C., Feldmann, H., Perlman, S., Snijder, E.J., Alisporivir inhibits MERS- and SARS-coronavirus replication in cell culture, but not SARS-coronavirus infection in a mouse model. Virus Res. 228 (2017), 7–13.
13. de Wilde, A.H., Li, Y., van der Meer, Y., Vuagniaux, G., Lysek, R., Fang, Y., Snijder, E.J., van Hemert, M.J., Cyclophilin inhibitors block arterivirus replication by interfering with viral RNA synthesis. J. Virol. 87 (2013), 1454–1464.
14. de Wilde, A.H., Raj, V.S., Oudshoorn, D., Bestebroer, T.M., van Nieuwkoop, S., Limpens, R.W., Posthuma, C.C., van der Meer, Y., Barcena, M., Haagmans, B.L., Snijder, E.J., van den Hoogen, B.G., MERS-coronavirus replication induces severe in vitro cytopathology and is strongly inhibited by cyclosporin A or interferon-alpha treatment. J. Gen. Virol. 94 (2013), 1749–1760.
15. de Wilde, A.H., Snijder, E.J., Kikkert, M., van Hemert, M.J., Host factors in coronavirus replication. Curr. Top. Microbiol. Immunol., 2017.
16. de Wilde, A.H., Zevenhoven-Dobbe, J.C., van der Meer, Y., Thiel, V., Narayanan, K., Makino, S., Snijder, E.J., van Hemert, M.J., Cyclosporin A inhibits the replication of diverse coronaviruses. J. Gen. Virol. 92 (2011), 2542–2548.
17. de Wit, E., van Doremalen, N., Falzarano, D., Munster, V.J., SARS and MERS: recent insights into emerging coronaviruses. Nat. Rev. Microbiol. 14 (2016), 523–534.
18. den Boon, J.A., Snijder, E.J., Chirnside, E.D., de Vries, A.A., Horzinek, M.C., Spaan, W.J., Equine arteritis virus is not a togavirus but belongs to the coronaviruslike superfamily. J. Virol. 65 (1991), 2910–2920.
19. Favreau, D.J., Meessen-Pinard, M., Desforges, M., Talbot, P.J., Human coronavirus-induced neuronal programmed cell death is cyclophilin d dependent and potentially caspase dispensable. J. Virol. 86 (2012), 81–93.
20. Gorbalenya, A.E., Enjuanes, L., Ziebuhr, J., Snijder, E.J., Nidovirales: evolving the largest RNA virus genome. Virus Res. 117 (2006), 17–37.
21. Gosert, R., Kanjanahaluethai, A., Egger, D., Bienz, K., Baker, S.C., RNA replication of mouse hepatitis virus takes place at double-membrane vesicles. J. Virol. 76 (2002), 3697–3708.
22. Hagemeijer, M.C., Vonk, A.M., Monastyrska, I., Rottier, P.J., de Haan, C.A., Visualizing coronavirus RNA synthesis in time by using click chemistry. J. Virol. 86 (2012), 5808–5816.
23. Hamre, D., Procknow, J.J., A new virus isolated from the human respiratory tract. Proceedings of the Society for Experimental biology and medicine. Soc. Exp. Biol. Med. 121 (1966), 190–193.
24. Harding, M.W., Handschumacher, R.E., Speicher, D.W., Isolation and amino acid sequence of cyclophilin. J. Biol. Chem. 261 (1986), 8547–8555.
25. Hatziioannou, T., Perez-Caballero, D., Cowan, S., Bieniasz, P.D., Cyclophilin interactions with incoming human immunodeficiency virus type 1 capsids with opposing effects on infectivity in human cells. J. Virol. 79 (2005), 176–183.
26. Holtkamp, D.J., Kliebenstein, J.B., Neumann, E.J., Assessment of the economic impact of porcine reproductive and respiratory syndrome virus on United States pork producers. JSHAP 21 (2013), 72–84.
27. Hopkins, S., Gallay, P.A., The role of immunophilins in viral infection. Biochim. Biophys. Acta 1850 (2015), 2103–2110.
28. Kim, Y., Lee, C., Porcine epidemic diarrhea virus induces caspase-independent apoptosis through activation of mitochondrial apoptosis-inducing factor. Virology 460–461 (2014), 180–193.
29. Knoops, K., Barcena, M., Limpens, R.W., Koster, A.J., Mommaas, A.M., Snijder, E.J., Ultrastructural characterization of arterivirus replication structures: reshaping the endoplasmic reticulum to accommodate viral RNA synthesis. J. Virol. 86 (2012), 2474–2487.
30. Knoops, K., Kikkert, M., van den 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.
31. Lin, C.M., Saif, L.J., Marthaler, D., Wang, Q., Evolution, antigenicity and pathogenicity of global porcine epidemic diarrhea virus strains. Virus Res. 226 (2016), 20–39.
32. Lin, Y.C., Boone, M., Meuris, L., Lemmens, I., Van Roy, N., Soete, A., Reumers, J., Moisse, M., Plaisance, S., Drmanac, R., Chen, J., Speleman, F., Lambrechts, D., Van de Peer, Y., Tavernier, J., Callewaert, N., Genome dynamics of the human embryonic kidney 293 lineage in response to cell biology manipulations. Nat. Commun., 5, 2014, 4767.
33. Maier, H.J., Hawes, P.C., Cottam, E.M., Mantell, J., Verkade, P., Monaghan, P., Wileman, T., Britton, P., Infectious bronchitis virus generates spherules from zippered endoplasmic reticulum membranes. MBio 4 (2013), e00801–e00813.
34. Mertens, F., Johansson, B., Fioretos, T., Mitelman, F., The emerging complexity of gene fusions in cancer. Nat. Rev. Cancer 15 (2015), 371–381.
35. Nakabayashi, H., Taketa, K., Miyano, K., Yamane, T., Sato, J., Growth of human hepatoma cells lines with differentiated functions in chemically defined medium. Cancer Res. 42 (1982), 3858–3863.
36. Naoumov, N.V., Cyclophilin inhibition as potential therapy for liver diseases. J. Hepatol. 61 (2014), 1166–1174.
37. Nedialkova, D.D., Gorbalenya, A.E., Snijder, E.J., Arterivirus Nsp1 modulates the accumulation of minus-strand templates to control the relative abundance of viral mRNAs. PLoS Pathog., 6, 2010, e1000772.
38. Neuman, B.W., Joseph, J.S., Saikatendu, K.S., Serrano, P., Chatterjee, A., Johnson, M.A., Liao, L., Klaus, J.P., Yates, J.R. 3rd, Wuthrich, K., Stevens, R.C., Buchmeier, M.J., Kuhn, P., Proteomics analysis unravels the functional repertoire of coronavirus nonstructural protein 3. J. Virol. 82 (2008), 5279–5294.
39. Nga, P.T., Parquet Mdel, C., Lauber, C., Parida, M., Nabeshima, T., Yu, F., Thuy, N.T., Inoue, S., Ito, T., Okamoto, K., Ichinose, A., Snijder, E.J., Morita, K., Gorbalenya, A.E., Discovery of the first insect nidovirus, a missing evolutionary link in the emergence of the largest RNA virus genomes. PLoS Pathog., 7, 2011, e1002215.
40. Nigro, P., Pompilio, G., Capogrossi, M.C., Cyclophilin A: a key player for human disease. Cell Death Dis., 4, 2013, e888.
41. Oudshoorn, D., van der Hoeven, B., Limpens, R.W., Beugeling, C., Snijder, E.J., Barcena, M., Kikkert, M., Antiviral innate immune response interferes with the formation of replication-associated membrane structures induced by a positive-strand RNA virus. MBio, 2016, 7.
42. Pedersen, K.W., van der, M.Y., Roos, N., Snijder, E.J., Open reading frame 1a-encoded subunits of the arterivirus replicase induce endoplasmic reticulum-derived double-membrane vesicles which carry the viral replication complex. J. Virol. 73 (1999), 2016–2026.
43. Pfefferle, S., Schopf, J., Kogl, M., Friedel, C.C., Muller, M.A., Carbajo-Lozoya, J., Stellberger, T., von Dall'armi, E., Herzog, P., Kallies, S., Niemeyer, D., Ditt, V., Kuri, T., Zust, R., Pumpor, K., Hilgenfeld, R., Schwarz, F., Zimmer, R., Steffen, I., Weber, F., Thiel, V., Herrler, G., Thiel, H.J., Schwegmann-Wessels, C., Pohlmann, S., Haas, J., Drosten, C., von Brunn, A., The SARS-coronavirus-host interactome: identification of cyclophilins as target for pan-coronavirus inhibitors. PLoS Pathog., 7, 2011, e1002331.
44. Sanjana, N.E., Shalem, O., Zhang, F., Improved vectors and genome-wide libraries for CRISPR screening. Nat. Methods 11 (2014), 783–784.
45. Snijder, E.J., Kikkert, M., Fang, Y., Arterivirus molecular biology and pathogenesis. J. Gen. Virol. 94 (2013), 2141–2163.
46. Szuhai, K., Tanke, H.J., COBRA: combined binary ratio labeling of nucleic-acid probes for multi-color fluorescence in situ hybridization karyotyping. Nat. Protoc. 1 (2006), 264–275.
47. Tanaka, Y., Sato, Y., Osawa, S., Inoue, M., Tanaka, S., Sasaki, T., Suppression of feline coronavirus replication in vitro by cyclosporin A. Vet. Res., 43, 2012, 41.
48. Tanaka, Y., Sato, Y., Sasaki, T., Feline coronavirus replication is affected by both cyclophilin A and cyclophilin B. J. Gen. Virol. 98 (2017), 190–200.
49. Ulasli, M., Verheije, M.H., de Haan, C.A., Reggiori, F., Qualitative and quantitative ultrastructural analysis of the membrane rearrangements induced by coronavirus. Cell. Microbiol. 12 (2010), 844–861.
50. van Boheemen, S., de Graaf, M., Lauber, C., Bestebroer, T.M., Raj, V.S., Zaki, A.M., Osterhaus, A.D., Haagmans, B.L., Gorbalenya, A.E., Snijder, E.J., Fouchier, R.A., Genomic characterization of a newly discovered coronavirus associated with acute respiratory distress syndrome in humans. MBio 3 (2012), e00473–00412.
51. van der Hoeven, B., Oudshoorn, D., Koster, A.J., Snijder, E.J., Kikkert, M., Barcena, M., Biogenesis and architecture of arterivirus replication organelles. Virus Res. 220 (2016), 70–90.
52. van Hemert, M.J., de Wilde, A.H., Gorbalenya, A.E., Snijder, E.J., The in vitro RNA synthesizing activity of the isolated arterivirus replication/transcription complex is dependent on a host factor. J. Biol. Chem. 283 (2008), 16525–16536.
53. van Hemert, M.J., van den Worm, S.H., Knoops, K., Mommaas, A.M., Gorbalenya, A.E., Snijder, E.J., SARS-coronavirus replication/transcription complexes are membrane-protected and need a host factor for activity in vitro. PLoS Pathog., 4, 2008, e1000054.
54. van Kasteren, P.B., Beugeling, C., Ninaber, D.K., Frias-Staheli, N., van Boheemen, S., Garcia-Sastre, A., Snijder, E.J., Kikkert, M., Arterivirus and nairovirus ovarian tumor domain-containing Deubiquitinases target activated RIG-I to control innate immune signaling. J. Virol. 86 (2012), 773–785.
55. von Brunn, A., Editorial overview: engineering for viral resistance. Curr. Opin. Virol. 14, 2015 (v-vii).
56. von Brunn, A., Ciesek, S., von Brunn, B., Carbajo-Lozoya, J., Genetic deficiency and polymorphisms of cyclophilin A reveal its essential role for Human Coronavirus 229E replication. Curr. Opin. Virol. 14 (2015), 56–61.
57. Wilkens, L., Hammer, C., Glombitza, S., Muller, D.E., Hepatocellular and cholangiolar carcinoma-derived cell lines reveal distinct sets of chromosomal imbalances. Pathobiology 79 (2012), 115–126.
58. Zaki, A.M., van Boheemen, S., Bestebroer, T.M., Osterhaus, A.D., Fouchier, R.A., Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N. Engl. J. Med. 367 (2012), 1814–1820.
59. Zhong, Y., Tan, Y.W., Liu, D.X., Recent progress in studies of arterivirus- and coronavirus-host interactions. Viruses 4 (2012), 980–1010.
60. Zust, R., Cervantes-Barragan, L., Habjan, M., Maier, R., Neuman, B.W., Ziebuhr, J., Szretter, K.J., Baker, S.C., Barchet, W., Diamond, M.S., Siddell, S.G., Ludewig, B., Thiel, V., Ribose 2′-O-methylation provides a molecular signature for the distinction of self and non-self mRNA dependent on the RNA sensor Mda5. Nat. Immunol. 12 (2011), 137–143.