Key elements of the RNAi pathway are regulated by hepatitis B virus replication and HBx acts as a viral suppressor of RNA silencing

Biochemical Journal

Volumn 462, Issue 2, 2014, Pages 347-358

  Chinnappan, Mahendran ^a   Singh, Avishek Kumar ^b   Kakumani, Pavan Kumar ^a   Kumar, Gautam ^a   Rooge, Sheetalnath Babasaheb ^b   Kumari, Anupama ^b   Varshney, Aditi ^b   Rastogi, Archana ^b   Singh, Ashok Kumar ^c   Sarin, Shiv Kumar ^b   Malhotra, Pawan ^a   Mukherjee, Sunil Kumar ^c   Bhatnagar, Raj Kamal ^a  

^a INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY ICGEB   (India)

^b INSTITUTE OF LIVER AND BILIARY SCIENCES   (India)

^c UNIVERSITY OF DELHI   (India)

Author keywords

Chronic hepatitis B (CHB); Dicer; Hepatitis B virus (HBV); Human dicing assay; RNA silencing suppressor

Indexed keywords

ADULT; ARGONAUTE PROTEINS; CELL LINE, TUMOR; FEMALE; HEK293 CELLS; HEPATITIS B VIRUS; HEPATITIS B, CHRONIC; HUMANS; LIVER; MALE; MUTATION; OPEN READING FRAMES; RIBONUCLEASE III; RNA INTERFERENCE; RNA, DOUBLE-STRANDED; RNA, MESSENGER; RNA, SMALL INTERFERING; TOBACCO; TRANS-ACTIVATORS; VIRUS REPLICATION; YOUNG ADULT;

EID: 84905900970     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20140316     Document Type: Article

References (60)

1. Agrawal, N., Dasaradhi, P. V. N., Mohmmed, A., Malhotra, P., Bhatnagar, R. K. and Mukherjee, S. K. (2003) RNA interference: biology, mechanism, and applications. Microbiol. Mol. Biol. Rev. 67, 657-685 (Pubitemid 37549773)
2. Parameswaran, P., Sklan, E., Wilkins, C., Burgon, T., Samuel, M. A., Lu, R., Ansel, K. M., Heissmeyer, V., Einav, S. and Jackson, W. (2010) Six RNA viruses and forty-one hosts: viral small RNAs and modulation of small RNA repertoires in vertebrate and invertebrate systems. PLoS Pathog. 6, e1000764
3. Hamilton, A. J. and Baulcombe, D. C. (1999) A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286, 950-952
4. Lu, R., Maduro, M., Li, F., Li, H. W., Broitman-Maduro, G., Li, W. X. and Ding, S. W. (2005) Animal virus replication and RNAi-mediated antiviral silencing in Caenorhabditis elegans. Nature 436, 1040-1043 (Pubitemid 41191689)
5. Lee, Y. S., Nakahara, K., Pham, J. W., Kim, K., He, Z., Sontheimer, E. J. and Carthew, R. W. (2004) Distinct roles for Drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA silencing pathways. Cell 117, 69-81 (Pubitemid 38469899)
6. de Vries, W. and Berkhout, B. (2008) RNAi suppressors encoded by pathogenic human viruses. Int. J. Biochem. Cell Biol. 40, 2007-2012
7. Duan, C.-G., Fang, Y.-Y., Zhou, B.-J., Zhao, J.-H., Hou, W.-N., Zhu, H., Ding, S.-W. and Guo, H.-S. (2012) Suppression of Arabidopsis ARGONAUTE1-mediated slicing, transgene-induced RNA silencing, and DNA methylation by distinct domains of the Cucumber mosaic virus 2b protein. Plant Cell 24, 259-274
8. Kawai, T. and Akira, S. (2006) Innate immune recognition of viral infection. Nat. Immunol. 7, 131-137 (Pubitemid 43135878)
9. Pedersen, I. M., Cheng, G., Wieland, S., Volinia, S., Croce, C. M., Chisari, F. V. and David, M. (2007) Interferon modulation of cellular microRNAs as an antiviral mechanism. Nature 449, 919-922 (Pubitemid 47598616)
10. Li, Y., Lu, J., Han, Y., Fan, X. and Ding, S.-W. (2013) RNA interference functions as an antiviral immunity mechanism in mammals. Science 342, 231-234
11. Maillard, P. V., Ciaudo, C., Marchais, A., Li, Y., Jay, F., Ding, S. W. and Voinnet, O. (2013) Antiviral RNA interference in mammalian cells. Science 342, 235-238
12. Li, W.-X., Li, H., Lu, R., Li, F., Dus, M., Atkinson, P., Brydon, E. W. A., Johnson, K. L., Garcia-Sastre, A. and Ball, L. A. (2004) Interferon antagonist proteins of influenza and vaccinia viruses are suppressors of RNA silencing. Proc. Natl. Acad. Sci. U.S.A. 101, 1350-1355 (Pubitemid 38182692)
13. Wang, Y., Kato, N., Jazag, A., Dharel, N., Otsuka, M., Taniguchi, H., Kawabe, T. and Omata, M. (2006) Hepatitis C virus core protein is a potent inhibitor of RNA silencing-based antiviral response. Gastroenterology 130, 883-892 (Pubitemid 43374535)
14. Ji, J., Glaser, A., Wernli, M., Berke, J. M., Moradpour, D. and Erb, P. (2008) Suppression of short interfering RNA-mediated gene silencing by the structural proteins of hepatitis C virus. J. Gen. Virol. 89, 2761-2766
15. Karjee, S., Minhas, A., Sood, V., Ponia, S. S., Banerjea, A. C., Chow, V. T. K., Mukherjee, S. K. and Lal, S. K. (2010) The 7a accessory protein of severe acute respiratory syndrome coronavirus acts as an RNA silencing suppressor. J. Virol. 84, 10395-10401
16. Fabozzi, G., Nabel, C. S., Dolan, M. A. and Sullivan, N. J. (2011) Ebolavirus proteins suppress the effects of small interfering RNA by direct interaction with the mammalian RNA interference pathway. J. Virol. 85, 2512-2523
17. Kakumani, P. K., Ponia, S. S., Rajgokul, K. S., Sood, V., Chinnappan, M., Banerjea, A. C., Medigeshi, G., Malhotra, P., Mukherjee, S. K. and Bhatnagar, R. K. (2013) Role of RNAi in dengue viral replication and identification of NS4B as a RNAi suppressor. J. Virol. 87, 8870-8883
18. Feitelson, M. (1992) Hepatitis B virus infection and primary hepatocellular carcinoma. Clin. Microbiol. Rev. 5, 275-301
19. Schädler, S. and Hildt, E. (2009) HBV life cycle: entry and morphogenesis. Viruses 1, 185-209
20. Beck, J. and Nassal, M. (2007) Hepatitis B virus replication. World J. Gastroenterol. 13, 48
21. Rawat, S., Clippinger, A. J. and Bouchard, M. J. (2012) Modulation of apoptotic signaling by the hepatitis B virus X protein. Viruses 4, 2945-2972
22. Wang, Y., Lu, Y., Toh, S. T., Sung, W.-K., Tan, P., Chow, P., Chung, A. Y. F., Jooi, L. L. P. and Lee, C. G. L. (2010) Lethal-7 is down-regulated by the hepatitis B virus x protein and targets signal transducer and activator of transcription 3. J. Hepatol. 53, 57-66
23. Wu, G., Yu, F., Xiao, Z., Xu, K., Xu, J., Tang, W., Wang, J. and Song, E. (2011) Hepatitis B virus X protein downregulates expression of the miR-16 family in malignant hepatocytes in vitro. Brit. J. Cancer 105, 146-153.
24. Hayes, C. N., Akamatsu, S., Tsuge, M., Miki, D., Akiyama, R., Abe, H., Ochi, H., Hiraga, N., Imamura, M. and Takahashi, S. (2012) Hepatitis B virus-specific miRNAs and argonaute2 play a role in the viral life cycle. PLoS ONE 7, e47490
25. Blum, H. E., Galun, E., Liang, T. J., von Weizsacker, F. and Wands, J. R. (1991) Naturally occurring missense mutation in the polymerase gene terminating hepatitis B virus replication. J. Virol. 65, 1836-1842
26. Blum, H. E., Zhang, Z.-S., Galun, E., Von Weizsacker, F., Garner, B., Liang, T. J. and Wands, J. R. (1992) Hepatitis B virus X protein is not central to the viral life cycle in vitro. J. Virol. 66, 1223-1227
27. Singh, G., Popli, S., Hari, Y., Malhotra, P., Mukherjee, S. and Bhatnagar, R. K. (2009) Suppression of RNA silencing by Flock house virus B2 protein is mediated through its interaction with the PAZ domain of Dicer. FASEB J. 23, 1845-1857
28. Meister, G., Landthaler, M., Patkaniowska, A., Dorsett, Y., Teng, G. and Tuschl, T. (2004) Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol. Cell 15, 185-197 (Pubitemid 38950966)
29. Han, J., Pedersen, J. S., Kwon, S. C., Belair, C. D., Kim, Y.-K., Yeom, K.-H., Yang, W.-Y., Haussler, D., Blelloch, R. and Kim, V. N. (2009) Posttranscriptional crossregulation between Drosha and DGCR8. Cell 136, 75-84
30. Laras, A., Koskinas, J., Dimou, E., Kostamena, A. and Hadziyannis, S. J. (2006) Intrahepatic levels and replicative activity of covalently closed circular hepatitis B virus DNA in chronically infected patients. Hepatology 44, 694-702 (Pubitemid 44433726)
31. Coley, W., Van Duyne, R., Carpio, L., Guendel, I., Kehn-Hall, K., Chevalier, S., Narayanan, A., Luu, T., Lee, N. and Klase, Z. (2010) Absence of DICER in monocytes and its regulation by HIV-1. J. Biol. Chem. 285, 31930-31943
32. Jani, D., Nagarkatti, R., Beatty, W., Angel, R., Slebodnick, C., Andersen, J., Kumar, S. and Rathore, D. (2008) HDP-a novel heme detoxification protein from the malaria parasite. PLoS Pathog. 4, e1000053
33. Berkhout, B. and Haasnoot, J. (2006) The interplay between virus infection and the cellular RNA interference machinery. FEBS Lett. 580, 2896-2902 (Pubitemid 43744478)
34. Wu, Z., Zhu, Y., Bisaro, D. M. and Parris, D. S. (2009) Herpes simplex virus type 1 suppresses RNA-induced gene silencing in mammalian cells. J. Virol. 83, 6652-6663
35. Matskevich, A. A. and Moelling, K. (2007) Dicer is involved in protection against influenza A virus infection. J. Gen. Vir. 88, 2627-2635 (Pubitemid 47555013)
36. Roth, B. M., Pruss, G. J. and Vance, V. B. (2004) Plant viral suppressors of RNA silencing. Virus Res. 102, 97-108 (Pubitemid 38447254)
37. Murakami, S., Cheong, J. and Kaneko, S. (1994) Human hepatitis virus X gene encodes a regulatory domain that represses transactivation of X protein. J. Biol. Chem. 269, 15118-15123 (Pubitemid 24198356)
38. Parashar Misra, K., Mukherji, A. and Kumar, V. (2004) The conserved amino-terminal region (amino acids 1-20) of the hepatitis B virus X protein shows a transrepression function. Virus Res. 105, 157-165 (Pubitemid 39207938)
39. Jiang, J. and Tang, H. (2010) Mechanism of inhibiting type I interferon induction by hepatitis B virus X protein. Protein Cell 1, 1106-1117
40. Kumar, V., Jayasuryan, N. and Kumar, R. (1996) A truncated mutant (residues 58-140) of the hepatitis B virus X protein retains transactivation function. Proc. Natl. Acad. Sci. U.S.A. 93, 5647-5652 (Pubitemid 26159506)
41. Zhang, Z., Torii, N., Furusaka, A., Malayaman, N., Hu, Z. and Liang, T. J. (2000) Structural and functional characterization of interaction between hepatitis B virus X protein and the proteasome complex. J. Biol. Chem. 275, 15157-15165 (Pubitemid 30337239)
42. Park, N. H., Song, I. H. and Chung, Y.-H. (2007) Molecular pathogenesis of hepatitis-B-virus-associated hepatocellular carcinoma. Gut Liver 1, 101-117
43. Tang, H., Oishi, N., Kaneko, S. and Murakami, S. (2006) Molecular functions and biological roles of hepatitis B virus x protein. Cancer Sci. 97, 977-983 (Pubitemid 44322542)
44. Neuveut, C., Wei, Y. and Buendia, M. A. (2010) Mechanisms of HBV-related hepatocarcinogenesis. J. Hepatol. 52, 594-604
45. Bivalkar-Mehla, S., Vakharia, J., Mehla, R., Abreha, M., Kanwar, J. R., Tikoo, A. and Chauhan, A. (2011) Viral RNA silencing suppressors (RSS): novel strategy of viruses to ablate the host RNA interference (RNAi) defense system. Virus Res. 155, 1-9
46. Li, W. X. and Ding, S. W. (2011) Viral suppressors of RNA silencing. Curr. Opin. Biotech. 12, 150-154
47. Skalsky, R. L. and Cullen, B. R. (2010) Viruses, microRNAs, and host interactions. Ann. Rev. Microbiol. 64, 123
48. Glazov, E. A., Kongsuwan, K., Assavalapsakul, W., Horwood, P. F., Mitter, N. and Mahony, T. J. (2009) Repertoire of bovine miRNA and miRNA-like small regulatory RNAs expressed upon viral infection. PLoS ONE 4, e6349
49. Ren, M., Qin, D., Li, K., Qu, J., Wang, L., Wang, Z., Huang, A. and Tang, H. (2012) Correlation between hepatitis B virus protein and microRNA processor Drosha in cells expressing HBV. Antivir. Res. 94, 225-231
50. Jaronczyk, K., Carmichael, J. and Hobman, T. (2005) Exploring the functions of RNA interference pathway proteins: some functions are more RISCy than others? Biochem. J. 387, 561-571 (Pubitemid 40685689)
51. Lin, R.-J., Lin, Y.-C., Chen, J., Kuo, H.-H., Chen, Y.-Y., Diccianni, M. B., London, W. B., Chang, C.-H. and Alice, L. Y. (2010) microRNA signature and expression of Dicer and Drosha can predict prognosis and delineate risk groups in neuroblastoma. Cancer Res. 70, 7841-7850
52. Pampalakis, G., Diamandis, E. P., Katsaros, D. and Sotiropoulou, G. (2010) Down-regulation of dicer expression in ovarian cancer tissues. Clin. Biochem. 43, 324-327
53. Dedes, K. J., Natrajan, R., Lambros, M. B., Geyer, F. C., Lopez-Garcia, M. A., Savage, K., Jones, R. L. and Reis-Filho, J. S. (2011) Down-regulation of the miRNA master regulators Drosha and Dicer is associated with specific subgroups of breast cancer. Eur. J. Cancer. 47, 138-150
54. Torres, A., Torres, K., Paszkowski, T., Jodlowska-Jedrych, B., Radomanski, T., Ksiazek, A. and Maciejewski, R. (2011) Major regulators of microRNAs biogenesis Dicer and Drosha are down-regulated in endometrial cancer. Tumor Biol. 32, 769-776
55. Diaz-Garcia, C. V., Agudo-Lopez, A., Perez, C., Lopez-Martin, J. A., Rodriguez-Peralto, J. L., de Castro, J., Cortijo, A., Martinez-Villanueva, M., Iglesias, L. and Garcia-Carbonero, R. (2013) DICER1, DROSHA and miRNAs in patients with non-small cell lung cancer: implications for outcomes and histologic classification. Carcinogenesis 34, 1031-1038
56. Inchley, C. S., Sonerud, T., Fjaerli, H. O. and Nakstad, B. (2011) Reduced Dicer expression in the cord blood of infants admitted with severe respiratory syncytial virus disease. BMC Infect. Dis. 11, 59
57. Gale, Jr, M. and Katze, M. G. (1998) Molecular mechanisms of interferon resistance mediated by viral-directed inhibition of PKR, the interferon-induced protein kinase. Pharmacol. Ther. 78, 29-46 (Pubitemid 28178928)
58. Chendrimada, T. P., Gregory, R. I., Kumaraswamy, E., Norman, J., Cooch, N., Nishikura, K. and Shiekhattar, R. (2005) TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing. Nature 436, 740-744 (Pubitemid 41117280)
59. Wu, Q., Wang, X. and Ding, S.-W. (2010) Viral suppressors of RNA-based viral immunity: host targets. Cell. Host Microb. 8, 12-15
60. Rui, E., de Moura, P. R. and Kobarg, J. (2001) Expression of deletion mutants of the hepatitis B virus protein HBx in E. coli and characterization of their RNA binding activities. Virus Res. 74, 59-73 (Pubitemid 32168194)