SEC14L2 enables pan-genotype HCV replication in cell culture

Nature

Volumn 524, Issue 7566, 2015, Pages 471-475

  Saeed, Mohsan ^a   Andreo, Ursula ^a   Chung, Hyo Young ^a   Espiritu, Christine ^a   Branch, Andrea D ^b   Silva, Jose M ^b   Rice, Charles M ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TOCOPHEROL; COMPLEMENTARY DNA; PROTEIN; SEC14L2 PROTEIN; UNCLASSIFIED DRUG; ANTIOXIDANT; CARRIER PROTEIN; HOST FACTOR; LIPOPROTEIN; SEC14L2 PROTEIN, HUMAN; TRANSACTIVATOR PROTEIN; VIRUS RNA;

ADAPTIVE RADIATION; CELLS AND CELL COMPONENTS; GENE EXPRESSION; GENOME; GENOTYPE; INFECTIVITY; LIPID; METABOLISM; MUTATION; VIRUS; VITAMIN;

ARTICLE; BHK CELL LINE; CELL CULTURE; CELL FRACTIONATION; COLONY FORMATION; DELETION MUTANT; GENOTYPE; HEPATITIS C VIRUS; HEPATOCELLULAR CARCINOMA CELL LINE; HEPATOMA CELL; HUMAN; IN VITRO STUDY; LIPID PEROXIDATION; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; RNA REPLICATION; RNA VIRUS; VIRUS ISOLATION; VIRUS REPLICATION; BIOSYNTHESIS; CULTURE TECHNIQUE; GENE LIBRARY; GENETIC TRANSDUCTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEPACIVIRUS; LENTIVIRINAE; LIVER CELL CARCINOMA; METABOLISM; MUTATION; PHYSIOLOGY; REPLICON; SERUM; TUMOR CELL LINE; VIROLOGY; VIRUS GENOME;

HEPATITIS C VIRUS; LENTIVIRUS;

ANTIOXIDANTS; CARCINOMA, HEPATOCELLULAR; CARRIER PROTEINS; CELL CULTURE TECHNIQUES; CELL LINE, TUMOR; CELLS, CULTURED; GENE LIBRARY; GENOME, VIRAL; GENOTYPE; HEPACIVIRUS; HOST-DERIVED CELLULAR FACTORS; HUMANS; LENTIVIRUS; LIPID PEROXIDATION; LIPOPROTEINS; MUTATION; REPLICON; RNA, VIRAL; SERUM; TRANS-ACTIVATORS; TRANSDUCTION, GENETIC; VIRUS REPLICATION; VITAMIN E;

EID: 84940487299     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature14899     Document Type: Article

References (45)

1. Blight, K. J., Kolykhalov, A. A. & Rice, C. M. Efficient initiation of HCV RNA replication in cell culture. Science 290, 1972-1974 (2000).
2. Saeed, M. et al. Efficient replication of genotype 3a and 4a hepatitis C virus replicons in human hepatoma cells. Antimicrob. Agents Chemother. 56, 5365-5373 (2012).
3. Kato, T, et al. Efficient replication of the genotype 2a hepatitis C virus subgenomic replicon. Gastroenterology 125, 1808-1817 (2003).
4. Mohd Hanafiah, K., Groeger, J., Flaxman, A. D. & Wiersma, S. T. Global epidemiology of hepatitis C virus infection: new estimates of age-specific antibody to HCV seroprevalence. Hepatology 57, 1333-1342 (2013).
5. Gottwein, J. M. et al. Novel infectious cDNA clones of hepatitis C virus genotype 3a (strain S52) and 4a (strain ED43): genetic analyses and in vivo pathogenesis studies. J. Virol. 84, 5277-5293 (2010).
6. Murayama, A. et al. The NS3 helicase and NS5B-to-3′X regions are important for efficient hepatitis C virus strain JFH-1 replication in Huh7 cells. J. Virol. 81, 8030-8040 (2007).
7. Murayama, A. et al. RNA polymerase activity and specific RNA structure are required for efficient HCV replication in cultured cells. PLoS Pathog. 6, e1000885 (2010).
8. Bukh, J. et al. Mutations that permit efficient replication of hepatitis C virus RNA in Huh-7 cells prevent productive replication in chimpanzees. Proc. Natl Acad. Sci. USA 99, 14416-14421 (2002).
9. Allen-Baume, V., Segui, B. & Cockcroft, S. Current thoughts on the phosphatidylinositol transfer protein family. FEBS Lett. 531, 74-80 (2002).
10. Aravind, L., Neuwald, A. F. & Ponting, C.P. Sec14p-like domains in NF1 and Dbl-like proteins indicate lipid regulation of Ras and Rho signaling. Curr. Biol. 9, R195-R197 (1999).
11. Kempná, P. et al. Cloning of novel human SEC14p-like proteins: ligand binding and functional properties. Free Radic. Biol. Med. 34, 1458-1472 (2003).
12. Jones, C. T. et al. Real-timeimaging of hepatitisCvirus infection using a fluorescent cell-based reporter system. Nature Biotechnol. 28, 167-171 (2010).
13. Farci, P. et al. Prevention of hepatitis C virus infection in chimpanzees by hyperimmune serumagainst the hypervariable region 1 of the envelope 2 protein. Proc. Natl Acad. Sci. USA 93, 15394-15399 (1996).
14. Washburn, M.L. et al. Ahumanized mouse model to study hepatitis C virus infection, immune response, and liver disease. Gastroenterology 140, 1334-1344 (2011).
15. Panagabko, C. et al. Ligand specificity in the CRAL-TRIO protein family. Biochemistry 42, 6467-6474 (2003).
16. Ni, J. et al. Tocopherol-associated protein suppresses prostate cancer cell growth by inhibition of the phosphoinositide 3-kinase pathway. Cancer Res. 65, 9807-9816 (2005).
17. Mokashi, V., Singh, D. K. & Porter, T. D. Supernatant protein factor stimulates HMG-CoA reductase in cell culture and in vitro. Arch. Biochem. Biophys. 433, 474-480 (2005).
18. Mokashi, V. & Porter, T. D. Supernatant protein factor requires phosphorylation and interaction with Golgi to stimulate cholesterol synthesis in hepatoma cells. Arch. Biochem. Biophys. 435, 175-181 (2005).
19. Neuzil, J., Dong, L. F., Wang, X. F. & Zingg, J. M. Tocopherol-associated protein-1 accelerates apoptosis induced by alpha-tocopheryl succinate in mesothelioma cells. Biochem. Biophys. Res. Commun. 343, 1113-1117 (2006).
20. Yamane, D. et al. Regulation of the hepatitis C virus RNA replicase by endogenous lipid peroxidation. Nature Med. 20, 927-935 (2014).
21. Yoshimoto, T. et al. Positive modulation of IL-12 signaling by sphingosine kinase 2 associating with the IL-12 receptor beta 1 cytoplasmic region. J. Immunol. 171, 1352-1359 (2003).
22. Poveda, E. et al. Update on hepatitis C virus resistance to direct-acting antiviral agents. Antiviral Res. 108, 181-191 (2014).
23. Lohmann, V. et al. Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science 285, 110-113 (1999).
24. Wose Kinge, C. N. et al. Hepatitis C virus genotype 5a subgenomic replicons for evaluation of direct-acting antiviral agents. Antimicrob. Agents Chemother. 58, 5386-5394 (2014).
25. Liehl, P. et al. Host-cell sensors for Plasmodium activate innate immunity against liver-stage infection. Nature Med. 20, 47-53 (2014).
26. Yanagi, M., Purcell, R. H., Emerson, S. U. & Bukh, J. Hepatitis C virus: an infectious molecular clone of a secondmajor genotype (2a) and lack of viability of intertypic 1a and 2a chimeras. Virology 262, 250-263 (1999).
27. Lohmann, V., Korner, F., Dobierzewska, A. & Bartenschlager, R. Mutations in hepatitis C virus RNAs conferring cell culture adaptation. J. Virol. 75, 1437-1449 (2001).
28. Blight, K. J., McKeating, J. A., Marcotrigiano, J. & Rice, C. M. Efficient replication of hepatitis C virus genotype 1a RNAs in cell culture. J. Virol. 77, 3181-3190 (2003).
29. Shimakami, T. et al. Protease inhibitor-resistant hepatitis C virus mutants with reduced fitness from impaired production of infectious virus. Gastroenterology 140, 667-675 (2011).
30. Wakita, T. et al. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nature Med. 11, 791-796 (2005).
31. Lindenbach, B. D. et al. Complete replication of hepatitis C virus in cell culture. Science 309, 623-626 (2005).
32. Marukian, S. et al. Cell culture-produced hepatitisCvirus doesnot infect peripheral blood mononuclear cells. Hepatology 48, 1843-1850 (2008).
33. Fukuhara, T. et al. Expression of microRNA miR-122 facilitates an efficient replication in nonhepatic cells upon infection with hepatitis C virus. J. Virol. 86, 7918-7933 (2012).
34. Rodriguez-Barrueco, R., Marshall, N. & Silva, J. M. Pooled shRNA screenings: experimental approach. Methods Mol. Biol. 980, 353-370 (2013).
35. Yi, Z. et al. Identification and characterization of the host protein DNAJC14 as a broadly active flavivirus replication modulator. PLoS Pathog. 7, e1001255 (2011).
36. Schoggins, J. W. et al. Dengue reporter viruses reveal viral dynamics in interferon receptor-deficient mice and sensitivity to interferon effectors in vitro. Proc. Natl Acad. Sci. USA 109, 14610-14615 (2012).
37. Suthar, M. S., Shabman, R., Madric, K., Lambeth, C. & Heise, M. T. Identification of adultmouse neurovirulence determinants of the Sindbis virus strain AR86. J. Virol. 79, 4219-4228 (2005).
38. Shabman, R.S. et al. Differential induction of type I interferon responses inmyeloid dendritic cells bymosquito and mammalian-cell-derived alphaviruses. J. Virol. 81, 237-247 (2007).
39. Bredenbeek, P. J. et al. A stable full-length yellow fever virus cDNA clone and the role of conserved RNA elements in flavivirus replication. J. Gen. Virol. 84, 1261-1268 (2003).
40. Kinney, R. M. et al. Constructionof infectious cDNA clones for dengue 2 virus: strain 16681 and its attenuated vaccine derivative, strain PDK-53. Virology 230, 300-308 (1997).
41. Chung, H. Y., Gu, M., Buehler, E., MacDonald, M. R. & Rice, C. M. Seed sequencematched controls reveal limitations of small interfering RNA knockdown in functional and structural studies of hepatitis C virus NS5A-MOBKL1B interaction. J. Virol. 88, 11022-11033 (2014).
42. Cristea, I. M., Williams, R., Chait, B. T. & Rout, M. P. Fluorescent proteins as proteomic probes. Mol. Cell. Proteomics 4, 1933-1941 (2005).
43. Pan, M. et al. Lipid peroxidation and oxidant stress regulate hepatic apolipoprotein B degradation and VLDL production. J. Clin. Invest. 113, 1277-1287 (2004).
44. Scheel, T. K. et al. Analysis of functional differences between hepatitisC virusNS5A of genotypes 1-7 in infectious cell culture systems. PLoS Pathog. 8, e1002696 (2012).
45. Maqbool, M. A. et al. Regulation of hepatitis C virus replication by nuclear translocation of nonstructural 5A protein and transcriptional activation of host genes. J. Virol. 87, 5523-5539 (2013).