Sigma-1 receptor regulates early steps of viral RNA replication at the onset of hepatitis C virus infection

Journal of Virology

Volumn 87, Issue 11, 2013, Pages 6377-6390

  Friesland, Martina ^a   Mingorance, Lidia ^a   Chung, Josan ^b   Chisari, Francis V ^b   Gastaminza, Pablo ^a  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; LIPID; SIGMA 1 OPIATE RECEPTOR; VIRUS RNA;

ARTICLE; CALCIUM SIGNALING; CELL LINE; CELL STRAIN HUH 7; CONTROLLED STUDY; DOWN REGULATION; ENDOPLASMIC RETICULUM; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; INFECTION SENSITIVITY; LIPID STORAGE; LIPID TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; RNA INTERFERENCE; RNA REPLICATION;

CELL LINE; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION, VIRAL; HEPACIVIRUS; HEPATITIS C; HUMANS; RECEPTORS, SIGMA; RNA, VIRAL; VIRUS REPLICATION;

EID: 84878198176     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03557-12     Document Type: Article

References (73)

1. Guidotti LG, Chisari FV. 2006. Immunobiology and pathogenesis of viral hepatitis. Annu. Rev. Pathol. 1:23-61.
2. Poordad F, McCone J, Jr, Bacon BR, Bruno S, Manns MP, Sulkowski MS, Jacobson IM, Reddy KR, Goodman ZD, Boparai N, DiNubile MJ, Sniukiene V, Brass CA, Albrecht JK, Bronowicki JP. 2011. Boceprevir for untreated chronic HCV genotype 1 infection. N. Engl. J. Med. 364: 1195-1206.
3. Jacobson IM, McHutchison JG, Dusheiko G, Di Bisceglie AM, Reddy KR, Bzowej NH, Marcellin P, Muir AJ, Ferenci P, Flisiak R, George J, Rizzetto M, Shouval D, Sola R, Terg RA, Yoshida EM, Adda N, Bengtsson L, Sankoh AJ, Kieffer TL, George S, Kauffman RS, Zeuzem S. 2011. Telaprevir for previously untreated chronic hepatitis C virus infection. N. Engl. J. Med. 364:2405-2416.
4. Otto GA, Puglisi JD. 2004. The pathway of HCV IRES-mediated translation initiation. Cell 119:369-380.
5. Moradpour D, Penin F, Rice CM. 2007. Replication of hepatitis C virus. Nat. Rev. Microbiol. 5:453-463.
6. Ploss A, Dubuisson J. 2012. New advances in the molecular biology of hepatitis C virus infection: towards the identification of new treatment targets. Gut 61(Suppl. 1):i25-i35.
7. Ploss A, Evans MJ. 2012. Hepatitis C virus host cell entry. Curr. Opin. Virol. 2:14-19.
8. Dubuisson J, Helle F, Cocquerel L. 2008. Early steps of the hepatitis C virus life cycle. Cell Microbiol. 10:821-827.
9. Miyanari Y, Atsuzawa K, Usuda N, Watashi K, Hishiki T, Zayas M, Bartenschlager R, Wakita T, Hijikata M, Shimotohno K. 2007. The lipid droplet is an important organelle for hepatitis C virus production. Nat. Cell Biol. 9:1089-1097.
10. Alvisi G, Madan V, Bartenschlager R. 2011. Hepatitis C virus and host cell lipids: an intimate connection. RNA Biol. 8:258-269.
11. Gastaminza P, Dryden KA, Boyd B, Wood MR, Law M, Yeager M, Chisari FV. 2010. Ultrastructural and biophysical characterization of hepatitis C virus particles produced in cell culture. J. Virol. 84:10999-11009.
12. Shimizu Y, Hishiki T, Ujino S, Sugiyama K, Funami K, Shimotohno K. 2011. Lipoprotein component associated with hepatitis C virus is essential for virus infectivity. Curr. Opin. Virol. 1:19-26.
13. Merz A, Long G, Hiet MS, Brugger B, Chlanda P, Andre P, Wieland F, Krijnse-Locker J, Bartenschlager R. 2011. Biochemical and morphological properties of hepatitis C virus particles and determination of their lipidome. J. Biol. Chem. 286:3018-3032.
14. den Boon JA, Diaz A, Ahlquist P. 2010. Cytoplasmic viral replication complexes. Cell Host Microbe 8:77-85.
15. Hsu NY, Ilnytska O, Belov G, Santiana M, Chen YH, Takvorian PM, Pau C, van der Schaar H, Kaushik-Basu N, Balla T, Cameron CE, Ehrenfeld E, van Kuppeveld FJ, Altan-Bonnet N. 2010. Viral reorganization of the secretory pathway generates distinct organelles for RNA replication. Cell 141:799-811.
16. Moradpour D, Gosert R, Egger D, Penin F, Blum HE, Bienz K. 2003. Membrane association of hepatitis C virus nonstructural proteins and identification of the membrane alteration that harbors the viral replication complex. Antiviral Res. 60:103-109.
17. Aizaki H, Lee KJ, Sung VM, Ishiko H, Lai MM. 2004. Characterization of the hepatitis C virus RNA replication complex associated with lipid rafts. Virology 324:450-461.
18. Miyanari Y, Hijikata M, Yamaji M, Hosaka M, Takahashi H, Shimotohno K. 2003. Hepatitis C virus non-structural proteins in the probable membranous compartment function in viral genome replication. J. Biol. Chem. 278:50301-50308.
19. El-Hage N, Luo G. 2003. Replication of hepatitis C virus RNA occurs in a membrane-bound replication complex containing nonstructural viral proteins and RNA. J. Gen. Virol. 84:2761-2769.
20. Hirata Y, Ikeda K, Sudoh M, Tokunaga Y, Suzuki A, Weng L, Ohta M, Tobita Y, Okano K, Ozeki K, Kawasaki K, Tsukuda T, Katsume A, Aoki Y, Umehara T, Sekiguchi S, Toyoda T, Shimotohno K, Soga T, Nishijima M, Taguchi R, Kohara M. 2012. Self-enhancement of hepatitis C virus replication by promotion of specific sphingolipid biosynthesis. PLoS Pathog. 8:e1002860. doi:10.1371/journal.ppat.1002860.
21. Paul D, Romero-Brey I, Gouttenoire J, Stoitsova S, Krijnse-Locker J, Moradpour D, Bartenschlager R. 2011. NS4B self-interaction through conserved C-terminal elements is required for the establishment of functional hepatitis C virus replication complexes. J. Virol. 85:6963-6976.
22. Romero-Brey I, Merz A, Chiramel A, Lee JY, Chlanda P, Haselman U, Santarella-Mellwig R, Habermann A, Hoppe S, Kallis S, Walther P, Antony C, Krijnse-Locker J, Bartenschlager R. 2012. Three-dimensional architecture and biogenesis of membrane structures associated with hepatitis C virus replication. PLoS Pathog. 8:e1003056. doi:10.1371/journal.ppat.1003056.
23. Reiss S, Rebhan I, Backes P, Romero-Brey I, Erfle H, Matula P, Kaderali L, Poenisch M, Blankenburg H, Hiet MS, Longerich T, Diehl S, Ramirez F, Balla T, Rohr K, Kaul A, Buhler S, Pepperkok R, Lengauer T, Albrecht M, Eils R, Schirmacher P, Lohmann V, Bartenschlager R. 2011. Recruitment and activation of a lipid kinase by hepatitis C virus NS5A is essential for integrity of the membranous replication compartment. Cell Host Microbe 9:32-45.
24. Berger KL, Kelly SM, Jordan TX, Tartell MA, Randall G. 2011. Hepatitis C virus stimulates the phosphatidylinositol 4-kinase III alpha-dependent phosphatidylinositol 4-phosphate production that is essential for its replication. J. Virol. 85:8870-8883.
25. Shulla A, Randall G. 2012. Hepatitis C virus-host interactions, replication, and viral assembly. Curr. Opin. Virol. 2:725-732.
26. Moriishi K, Matsuura Y. 2007. Host factors involved in the replication of hepatitis C virus. Rev. Med. Virol. 17:343-354.
27. Barbaro G, Di Lorenzo G, Asti A, Ribersani M, Belloni G, Grisorio B, Filice G, Barbarini G. 1999. Hepatocellular mitochondrial alterations in patients with chronic hepatitis C: ultrastructural and biochemical findings. Am. J. Gastroenterol. 94:2198-2205.
28. Quarato G, Scrima R, Agriesti F, Moradpour D, Capitanio N, Piccoli C. 2013. Targeting mitochondria in the infection strategy of the hepatitis C virus. Int. J. Biochem. Cell Biol. 45:156-166.
29. Piccoli C, Scrima R, Quarato G, D'Aprile A, Ripoli M, Lecce L, Boffoli D, Moradpour D, Capitanio N. 2007. Hepatitis C virus protein expression causes calcium-mediated mitochondrial bioenergetic dysfunction and nitro-oxidative stress. Hepatology 46:58-65.
30. Rizzuto R, Pinton P, Carrington W, Fay FS, Fogarty KE, Lifshitz LM, Tuft RA, Pozzan T. 1998. Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2 responses. Science 280:1763-1766.
31. de Brito OM, Scorrano L. 2010. An intimate liaison: spatial organization of the endoplasmic reticulum-mitochondria relationship. EMBO J. 29: 2715-2723.
32. Hayashi T, Su TP. 2007. Sigma-1 receptor chaperones at the ERmitochondrion interface regulate Ca(2+) signaling and cell survival. Cell 131:596-610.
33. Hayashi T, Su TP. 2003. Sigma-1 receptors (sigma(1) binding sites) form raft-like microdomains and target lipid droplets on the endoplasmic reticulum: roles in endoplasmic reticulum lipid compartmentalization and export. J. Pharmacol. Exp. Ther. 306:718-725.
34. Hayashi T, Su TP. 2004. Sigma-1 receptors at galactosylceramideenriched lipid microdomains regulate oligodendrocyte differentiation. Proc. Natl. Acad. Sci. U. S. A. 101:14949-14954.
35. Gastaminza P, Whitten-Bauer C, Chisari FV. 2010. Unbiased probing of the entire hepatitis C virus life cycle identifies clinical compounds that target multiple aspects of the infection. Proc. Natl. Acad. Sci. U. S. A. 107:291-296.
36. Zhong J, Gastaminza P, Cheng G, Kapadia S, Kato T, Burton DR, Wieland SF, Uprichard SL, Wakita T, Chisari FV. 2005. Robust hepatitis C virus infection in vitro. Proc. Natl. Acad. Sci. U. S. A. 102:9294-9299.
37. Zhong J, Gastaminza P, Chung J, Stamataki Z, Isogawa M, Cheng G, McKeating JA, Chisari FV. 2006. Persistent hepatitis C virus infection in vitro: coevolution of virus and host. J. Virol. 80:11082-11093.
38. Nakabayashi H, Taketa K, Miyano K, Yamane T, Sato J. 1982. Growth of human hepatoma cell lines with differentiated functions in chemically defined medium. Cancer Res. 42:3858-3863.
39. Graham FL, Smiley J, Russell WC, Nairn R. 1977. Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J. Gen. Virol. 36:59-74.
40. Pietschmann T, Kaul A, Koutsoudakis G, Shavinskaya A, Kallis S, Steinmann E, Abid K, Negro F, Dreux M, Cosset FL, Bartenschlager R. 2006. Construction and characterization of infectious intragenotypic and intergenotypic hepatitis C virus chimeras. Proc. Natl. Acad. Sci. U. S. A. 103:7408-7413.
41. Kronke J, Kittler R, Buchholz F, Windisch MP, Pietschmann T, Bartenschlager R, Frese M. 2004. Alternative approaches for efficient inhibition of hepatitis C virus RNA replication by small interfering RNAs. J. Virol. 78:3436-3446.
42. Dull T, Zufferey R, Kelly M, Mandel RJ, Nguyen M, Trono D, Naldini L. 1998. A third-generation lentivirus vector with a conditional packaging system. J. Virol. 72:8463-8471.
43. Bartosch B, Dubuisson J, Cosset FL. 2003. Infectious hepatitis C virus pseudo-particles containing functional E1-E2 envelope protein complexes. J. Exp. Med. 197:633-642.
44. Steinmann E, Brohm C, Kallis S, Bartenschlager R, Pietschmann T. 2008. Efficient trans-encapsidation of hepatitis C virus RNAs into infectious virus-like particles. J. Virol. 82:7034-7046.
45. Lohmann V, Hoffmann S, Herian U, Penin F, Bartenschlager R. 2003. Viral and cellular determinants of hepatitis C virus RNA replication in cell culture. J. Virol. 77:3007-3019.
46. Gastaminza P, Cheng G, Wieland S, Zhong J, Liao W, Chisari FV. 2008. Cellular determinants of hepatitis C virus assembly, maturation, degradation, and secretion. J. Virol. 82:2120-2129.
47. Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9:671-675.
48. Dreux M, Gastaminza P, Wieland SF, Chisari FV. 2009. The autophagy machinery is required to initiate hepatitis C virus replication. Proc. Natl. Acad. Sci. U. S. A. 106:14046-14051.
49. Chomczynski P, Sacchi N. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159.
50. Garaigorta U, Chisari FV. 2009. Hepatitis C virus blocks interferon ef-fector function by inducing protein kinase R phosphorylation. Cell Host Microbe 6:513-522.
51. Bolte S, Cordelieres FP. 2006. A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc. 224:213-232.
52. Costes SV, Daelemans D, Cho EH, Dobbin Z, Pavlakis G, Lockett S. 2004. Automatic and quantitative measurement of protein-protein colocalization in live cells. Biophys. J. 86:3993-4003.
53. van Steensel B, van Binnendijk EP, Hornsby CD, van der Voort HT, Krozowski ZS, de Kloet ER, van Driel R. 1996. Partial colocalization of glucocorticoid and mineralocorticoid receptors in discrete compartments in nuclei of rat hippocampus neurons. J. Cell Sci. 109:787-792.
54. Hayashi T, Fujimoto M. 2010. Detergent-resistant microdomains determine the localization of sigma-1 receptors to the endoplasmic reticulummitochondria junction. Mol. Pharmacol. 77:517-528.
55. Hayashi T, Su TP. 2004. Sigma-1 receptor ligands: potential in the treatment of neuropsychiatric disorders. CNS Drugs 18:269-284.
56. Pietschmann T, Lohmann V, Rutter G, Kurpanek K, Bartenschlager R. 2001. Characterization of cell lines carrying self-replicating hepatitis C virus RNAs. J. Virol. 75:1252-1264.
57. Wakita T, Pietschmann T, Kato T, Date T, Miyamoto M, Zhao Z, Murthy K, Habermann A, Krausslich HG, Mizokami M, Bartenschlager R, Liang TJ. 2005. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat. Med. 11:791-796.
58. Gastaminza P, Pitram SM, Dreux M, Krasnova LB, Whitten-Bauer C, Dong J, Chung J, Fokin VV, Sharpless KB, Chisari FV. 2011. Antiviral stilbene 1,2-diamines prevent initiation of hepatitis C viral RNA replication at the outset of infection. J. Virol. 85:5513-5523.
59. Hayashi T, Su TP. 2003. Intracellular dynamics of sigma-1 receptors (sigma(1) binding sites) in NG108-15 cells. J. Pharmacol. Exp. Ther. 306: 726-733.
60. Shi ST, Lee KJ, Aizaki H, Hwang SB, Lai MM. 2003. Hepatitis C virus RNA replication occurs on a detergent-resistant membrane that cofractionates with caveolin-2. J. Virol. 77:4160-4168.
61. Piccoli C, Quarato G, Ripoli M, D'Aprile A, Scrima R, Cela O, Boffoli D, Moradpour D, Capitanio N. 2009. HCV infection induces mitochondrial bioenergetic unbalance: causes and effects. Biochim. Biophys. Acta 1787:539-546.
62. Ando T, Imamura H, Suzuki R, Aizaki H, Watanabe T, Wakita T, Suzuki T. 2012. Visualization and measurement of ATP levels in living cells replicating hepatitis C virus genome RNA. PLoS Pathog. 8:e1002561. doi:10.1371/journal.ppat.1002561.
63. Diamond DL, Syder AJ, Jacobs JM, Sorensen CM, Walters KA, Proll SC, McDermott JE, Gritsenko MA, Zhang Q, Zhao R, Metz TO, Camp DG, II, Waters KM, Smith RD, Rice CM, Katze MG. 2010. Temporal proteome and lipidome profiles reveal hepatitis C virus-associated reprogramming of hepatocellular metabolism and bioenergetics. PLoS Pathog. 6:e1000719. doi:10.1371/journal.ppat.1000719.
64. Tsai SY, Rothman RK, Su TP. 2012. Insights into the Sigma-1 receptor chaperone's cellular functions: a microarray report. Synapse 66:42-51.
65. Marriott KS, Prasad M, Thapliyal V, Bose HS. 2012. Sigma-1 receptor at the mitochondrial associated ER-membrane is responsible for mitochondrial metabolic regulation. J. Pharmacol. Exp. Ther. 343:578-586.
66. Hayashi T, Su TP. 2010. Cholesterol at the endoplasmic reticulum: roles of the sigma-1 receptor chaperone and implications thereof in human diseases. Subcell. Biochem. 51:381-398.
67. Horner SM, Liu HM, Park HS, Briley J, Gale M, Jr. 2011. Mitochondrial-associated endoplasmic reticulum membranes (MAM) form innate immune synapses and are targeted by hepatitis C virus. Proc. Natl. Acad. Sci. U. S. A. 108:14590-14595.
68. Sumpter R, Jr, Loo YM, Foy E, Li K, Yoneyama M, Fujita T, Lemon SM, Gale M, Jr. 2005. Regulating intracellular antiviral defense and permissiveness to hepatitis C virus RNA replication through a cellular RNA helicase, RIG-I. J. Virol. 79:2689-2699.
69. Schon EA, Area-Gomez E. 2012. Mitochondria-associated ER membranes in Alzheimer disease. Mol. Cell Neurosci. 24:S1044-7431(12)00127-3. doi:10.1016/j.mcn.2012.07.011.
70. Hayashi T, Su T. 2005. The sigma receptor: evolution of the concept in neuropsychopharmacology. Curr. Neuropharmacol. 3:267-280.
71. Diaz JL, Zamanillo D, Corbera J, Baeyens JM, Maldonado R, Pericas MA, Vela JM, Torrens A. 2009. Selective sigma-1 (sigma1) receptor antagonists: emerging target for the treatment of neuropathic pain. Cent. Nerv. Syst. Agents Med. Chem. 9:172-183.
72. Ablordeppey SY, Fischer JB, Glennon RA. 2000. Is a nitrogen atom an important pharmacophoric element in sigma ligand binding? Bioorg. Med. Chem. 8:2105-2111.
73. Amer MS, McKeown L, Tumova S, Liu R, Seymour VA, Wilson LA, Naylor J, Reenhalgh K, Hou B, Majeed Y, Turner P, Sedo A, O'Regan DJ, Li J, Bon RS, Porter KE, Beech DJ. 20132. Inhibition of endothelial cell Ca(2+) entry and transient receptor potential channels by Sigma-1 receptor ligands. Br. J. Pharmacol. 168:1445-1455.