Identification of hnRNPH1, NF45, and C14orf166 as novel host interacting partners of the mature hepatitis C virus core protein

Journal of Proteome Research

Volumn 10, Issue 10, 2011, Pages 4522-4534

  Lee, Jun Wei ^a   Liao, Pao Chi ^a   Young, Kung Chia ^a,d   Chang, Christina L ^a   Chen, Steve S L ^b   Chang, Ting Tsung ^a,d   Lai, Ming Derg ^a,d   Wang, Shainn Wei ^a,c,d  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

^c NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^d NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

C14orf166; hepatitis C virus core; heterogeneous nuclear ribonucleoprotein H1; liquid chromatography mass spectrometry mass spectrometry; nuclear factor 45; proteomics

Indexed keywords

CORE PROTEIN; DEAD BOX POLYPEPTIDE 17 ISOFORM 1; HEAT SHOCK PROTEIN 70; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN H1; INTERLEUKIN ENHANCER BINDING FACTOR 2; MESSENGER RNA; PROTEIN; RIBOSOMAL PROTEIN L14; RIBOSOMAL PROTEIN L4; RIBOSOMAL PROTEIN L6; RIBOSOMAL PROTEIN P0; RIBOSOMAL PROTEIN S8; RPL14 PROTEIN; TUBULIN ALPHA 6; UNCLASSIFIED DRUG; VIMENTIN; ZINC FINGER PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS; CELL STRAIN HEK293; CELLULAR DISTRIBUTION; CYTOPLASM; GENE CONTROL; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; LIQUID CHROMATOGRAPHY; LIVER CELL CARCINOMA; MICROTUBULE; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEOMICS; RNA METABOLISM; VIRUS REPLICATION;

CHROMATOGRAPHY, LIQUID; GENE EXPRESSION REGULATION, VIRAL; GENOTYPE; HEK293 CELLS; HEPACIVIRUS; HEPATITIS C; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN GROUP F-H; HUMANS; MASS SPECTROMETRY; MICROSCOPY, CONFOCAL; NUCLEAR FACTOR 45 PROTEIN; PLASMIDS; TRANS-ACTIVATORS; VIRAL CORE PROTEINS; VIRUS REPLICATION;

HEPATITIS C VIRUS;

EID: 80053931214     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr200338d     Document Type: Article

References (58)

1. Blackard, J. T.; Kemmer, N.; Sherman, K. E. Extrahepatic replication of HCV: insights into clinical manifestations and biological consequences Hepatology 2006, 44, 15-22 (Pubitemid 44049134)
2. Sansonno, D.; Dammacco, F. Hepatitis C virus, cryoglobulinaemia, and vasculitis: immune complex relations Lancet Infect. Dis. 2005, 5, 227-36 (Pubitemid 40410068)
3. Boonstra, A.; van der Laan, L. J.; Vanwolleghem, T.; Janssen, H. L. Experimental models for hepatitis C viral infection Hepatology 2009, 50, 1646-55
4. Boni, S.; Lavergne, J. P.; Boulant, S.; Cahour, A. Hepatitis C virus core protein acts as a trans-modulating factor on internal translation initiation of the viral RNA J. Biol. Chem. 2005, 280, 17737-48 (Pubitemid 41389012)
5. Kang, S. M.; Choi, J. K.; Kim, S. J.; Kim, J. H.; Ahn, D. G.; Oh, J. W. Regulation of hepatitis C virus replication by the core protein through its interaction with viral RNA polymerase Biochem. Biophys. Res. Commun. 2009, 386, 55-9
6. Ait-Goughoulte, M.; Banerjee, A.; Meyer, K.; Mazumdar, B.; Saito, K.; Ray, R. B.; Ray, R. Hepatitis C virus core protein interacts with fibrinogen-beta and attenuates cytokine stimulated acute-phase response Hepatology 2010, 51, 1505-13
7. Kountouras, J.; Zavos, C.; Chatzopoulos, D. Apoptosis in hepatitis C J. Viral Hepat. 2003, 10, 335-42 (Pubitemid 37159417)
8. Tai, D. I.; Tsai, S. L.; Chen, Y. M.; Chuang, Y. L.; Peng, C. Y.; Sheen, I. S.; Yeh, C. T.; Chang, K. S.; Huang, S. N.; Kuo, G. C.; Liaw, Y. F. Activation of nuclear factor kappaB in hepatitis C virus infection: implications for pathogenesis and hepatocarcinogenesis Hepatology 2000, 31, 656-64 (Pubitemid 30118634)
9. Waggoner, S. N.; Hall, C. H. T.; Hahn, Y. S. HCV core protein interaction with gC1q receptor inhibits Th1 differentiation of CD4+ T cells via suppression of dendritic cell IL-12 production J. Leukoc. Biol. 2007, 82, 1407-19 (Pubitemid 350276952)
10. Simmonds, P.; Bukh, J.; Combet, C.; Deleage, G.; Enomoto, N.; Feinstone, S.; Halfon, P.; Inchauspe, G.; Kuiken, C.; Maertens, G.; Mizokami, M.; Murphy, D. G.; Okamoto, H.; Pawlotsky, J. M.; Penin, F.; Sablon, E.; Shin, I. T.; Stuyver, L. J.; Thiel, H. J.; Viazov, S.; Weiner, A. J.; Widell, A. Consensus proposals for a unified system of nomenclature of hepatitis C virus genotypes Hepatology 2005, 42, 962-73 (Pubitemid 41401136)
11. Tanaka, Y.; Hanada, K.; Mizokami, M.; Yeo, A. E.; Shih, J. W.; Gojobori, T.; Alter, H. J. Inaugural Article: A comparison of the molecular clock of hepatitis C virus in the United States and Japan predicts that hepatocellular carcinoma incidence in the United States will increase over the next two decades Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 15584-9 (Pubitemid 35403976)
12. Kato, T.; Date, T.; Murayama, A.; Morikawa, K.; Akazawa, D.; Wakita, T. Cell culture and infection system for hepatitis C virus Nat. Protoc. 2006, 1, 2334-9
13. Webster, D. P.; Klenerman, P.; Collier, J.; Jeffery, K. J. Development of novel treatments for hepatitis C Lancet Infect. Dis. 2009, 9, 108-17
14. Lo, S. Y.; Masiarz, F.; Hwang, S. B.; Lai, M. M.; Ou, J. H. Differential subcellular localization of hepatitis C virus core gene products Virology 1995, 213, 455-61
15. Suzuki, R.; Sakamoto, S.; Tsutsumi, T.; Rikimaru, A.; Tanaka, K.; Shimoike, T.; Moriishi, K.; Iwasaki, T.; Mizumoto, K.; Matsuura, Y.; Miyamura, T.; Suzuki, T. Molecular determinants for subcellular localization of hepatitis C virus core protein J. Virol. 2005, 79, 1271-81 (Pubitemid 40053909)
16. Yasui, K.; Wakita, T.; Tsukiyama-Kohara, K.; Funahashi, S. I.; Ichikawa, M.; Kajita, T.; Moradpour, D.; Wands, J. R.; Kohara, M. The native form and maturation process of hepatitis C virus core protein J. Virol. 1998, 72, 6048-55 (Pubitemid 28283394)
17. McLauchlan, J. Properties of the hepatitis C virus core protein: a structural protein that modulates cellular processes J. Viral Hepat. 2000, 7, 2-14 (Pubitemid 30139846)
18. Ai, L. S.; Lee, Y. W.; Chen, S. S. L. Characterization of hepatitis C virus core protein multimerization and membrane envelopment: revelation of a cascade of core-membrane interactions J. Virol. 2009, 83, 9923-39
19. Cristofari, G.; Ivanyi-Nagy, R.; Gabus, C.; Boulant, S.; Lavergne, J. P.; Penin, F.; Darlix, J. L. The hepatitis C virus Core protein is a potent nucleic acid chaperone that directs dimerization of the viral (+) strand RNA in vitro Nucleic Acids Res. 2004, 32, 2623-31 (Pubitemid 38854816)
20. Klein, K. C.; Dellos, S. R.; Lingappa, J. R. Identification of residues in the hepatitis C virus core protein that are critical for capsid assembly in a cell-free system J. Virol. 2005, 79, 6814-26 (Pubitemid 40677314)
21. Majeau, N.; Gagne, V.; Boivin, A.; Bolduc, M.; Majeau, J. A.; Ouellet, D.; Leclerc, D. The N-terminal half of the core protein of hepatitis C virus is sufficient for nucleocapsid formation J. Gen. Virol. 2004, 85 (Pt 4) 971-81 (Pubitemid 38489562)
22. Duvignaud, J. B.; Savard, C.; Fromentin, R.; Majeau, N.; Leclerc, D.; Gagne, S. M. Structure and dynamics of the N-terminal half of hepatitis C virus core protein: an intrinsically unstructured protein Biochem. Biophys. Res. Commun. 2009, 378, 27-31
23. Maillard, P.; Lavergne, J. P.; Siberil, S.; Faure, G.; Roohvand, F.; Petres, S.; Teillaud, J. L.; Budkowska, A. Fc gamma receptor-like activity of hepatitis C virus core protein J. Biol. Chem. 2004, 279, 2430-7 (Pubitemid 38114226)
24. Namboodiri, A. M.; Budkowska, A.; Nietert, P. J.; Pandey, J. P. Fc gamma receptor-like hepatitis C virus core protein binds differentially to IgG of discordant Fc (GM) genotypes Mol. Immunol. 2007, 44, 3805-8 (Pubitemid 46817663)
25. Yeh, C. T.; Lo, S. Y.; Dai, D. I.; Tang, J. H.; Chu, C. M.; Liaw, Y. F. Amino acid substitutions in codons 9-11 of hepatitis C virus core protein lead to the synthesis of a short core protein product J. Gastroenterol. Hepatol. 2000, 15, 182-91
26. Ruster, B.; Zeuzem, S.; Krump-Konvalinkova, V.; Berg, T.; Jonas, S.; Severin, K.; Roth, W. K. Comparative sequence analysis of the core- and NS5-region of hepatitis C virus from tumor and adjacent non-tumor tissue J. Med. Virol. 2001, 63, 128-34 (Pubitemid 32142269)
27. Shirakura, M.; Murakami, K.; Ichimura, T.; Suzuki, R.; Shimoji, T.; Fukuda, K.; Abe, K.; Sato, S.; Fukasawa, M.; Yamakawa, Y.; Nishijima, M.; Moriishi, K.; Matsuura, Y.; Wakita, T.; Suzuki, T.; Howley, P. M.; Miyamura, T.; Shoji, I. E6AP ubiquitin ligase mediates ubiquitylation and degradation of hepatitis C virus core protein J. Virol. 2007, 81, 1174-85 (Pubitemid 46167839)
28. Suzuki, R.; Tamura, K.; Li, J.; Ishii, K.; Matsuura, Y.; Miyamura, T.; Suzuki, T. Ubiquitin-mediated degradation of hepatitis C virus core protein is regulated by processing at its carboxyl terminus Virology 2001, 280, 301-9 (Pubitemid 34165360)
29. Kang, S. M.; Shin, M. J.; Kim, J. H.; Oh, J. W. Proteomic profiling of cellular proteins interacting with the hepatitis C virus core protein Proteomics 2005, 5, 2227-37
30. Matto, M.; Rice, C. M.; Aroeti, B.; Glenn, J. S. Hepatitis C virus core protein associates with detergent-resistant membranes distinct from classical plasma membrane rafts J. Virol. 2004, 78, 12047-53 (Pubitemid 39390789)
31. Okamoto, K.; Mori, Y.; Komoda, Y.; Okamoto, T.; Okochi, M.; Takeda, M.; Suzuki, T.; Moriishi, K.; Matsuura, Y. Intramembrane processing by signal peptide peptidase regulates the membrane localization of hepatitis C virus core protein and viral propagation J. Virol. 2008, 82, 8349-61
32. Drakas, R.; Prisco, M.; Baserga, R. A modified tandem affinity purification tag technique for the purification of protein complexes in mammalian cells Proteomics 2005, 5, 132-7 (Pubitemid 40189645)
33. Beard, M. R.; Abell, G.; Honda, M.; Carroll, A.; Gartland, M.; Clarke, B.; Suzuki, K.; Lanford, R.; Sangar, D. V.; Lemon, S. M. An infectious molecular clone of a Japanese genotype 1b hepatitis C virus Hepatology 1999, 30, 316-24 (Pubitemid 29300603)
34. Kato, T.; Matsumura, T.; Heller, T.; Saito, S.; Sapp, R. K.; Murthy, K.; Wakita, T.; Liang, T. J. Production of infectious hepatitis C virus of various genotypes in cell cultures J. Virol. 2007, 81, 4405-11 (Pubitemid 46668637)
35. Blight, K. J.; McKeating, J. A.; Rice, C. M. Highly permissive cell lines for subgenomic and genomic hepatitis C virus RNA replication J. Virol. 2002, 76, 13001-14 (Pubitemid 35386984)
36. Cristea, I. M.; Williams, R.; Chait, B. T.; Rout, M. P. Fluorescent proteins as proteomic probes Mol. Cell. Proteomics 2005, 4, 1933-41 (Pubitemid 41830187)
37. Chang, Y. H.; Wu, C. C.; Chang, K. P.; Yu, J. S.; Chang, Y. C.; Liao, P. C. Cell secretome analysis using hollow fiber culture system leads to the discovery of CLIC1 protein as a novel plasma marker for nasopharyngeal carcinoma J. Proteome Res. 2009, 8, 5465-74
38. Perkins, D. N.; Pappin, D. J.; Creasy, D. M.; Cottrell, J. S. Probability-based protein identification by searching sequence databases using mass spectrometry data Electrophoresis 1999, 20, 3551-67 (Pubitemid 30007252)
39. Li, K.; Prow, T.; Lemon, S. M.; Beard, M. R. Cellular response to conditional expression of hepatitis C virus core protein in Huh7 cultured human hepatoma cells Hepatology 2002, 35, 1237-46 (Pubitemid 34454021)
40. Fang, C. Y.; Yi, Z. G.; Liu, F.; Lan, S. Y.; Wang, J. D.; Lu, H. J.; Yang, P. Y.; Yuan, Z. H. Proteome analysis of human liver carcinoma Huh7 cells harboring hepatitis C virus subgenomic replicon Proteomics 2006, 6, 519-527 (Pubitemid 43208031)
41. Jablonski, J. A.; Caputi, M. Role of cellular RNA processing factors in human immunodeficiency virus type 1 mRNA metabolism, replication, and infectivity J. Virol. 2009, 83, 981-92
42. Isken, O.; Baroth, M.; Grassmann, C. W.; Weinlich, S.; Ostareck, D. H.; Ostareck-Lederer, A.; Behrens, S. E. Nuclear factors are involved in hepatitis C virus RNA replication RNA 2007, 13, 1675-92 (Pubitemid 47481676)
43. Merrill, M. K.; Gromeier, M. The double-stranded RNA binding protein 76:NF45 heterodimer inhibits translation initiation at the rhinovirus type 2 internal ribosome entry site J. Virol. 2006, 80, 6936-42 (Pubitemid 44025192)
44. Sakamoto, S.; Aoki, K.; Higuchi, T.; Todaka, H.; Morisawa, K.; Tamaki, N.; Hatano, E.; Fukushima, A.; Taniguchi, T.; Agata, Y. The NF90-NF45 complex functions as a negative regulator in the microRNA processing pathway Mol. Cell. Biol. 2009, 29, 3754-69
45. Zhao, G.; Shi, L.; Qiu, D.; Hu, H.; Kao, P. N. NF45/ILF2 tissue expression, promoter analysis, and interleukin-2 transactivating function Exp. Cell Res. 2005, 305, 312-23 (Pubitemid 40467579)
46. Cui, Y.; Wu, J.; Zong, M.; Song, G.; Jia, Q.; Jiang, J.; Han, J. Proteomic profiling in pancreatic cancer with and without lymph node metastasis Int. J. Cancer 2009, 124, 1614-21
47. Howng, S. L.; Hsu, H. C.; Cheng, T. S.; Lee, Y. L.; Chang, L. K.; Lu, P. J.; Hong, Y. R. A novel ninein-interaction protein, CGI-99, blocks ninein phosphorylation by GSK3beta and is highly expressed in brain tumors FEBS Lett. 2004, 566, 162-8
48. Ariumi, Y.; Kuroki, M.; Abe, K.; Dansako, H.; Ikeda, M.; Wakita, T.; Kato, N.; DDX3 DEAD-box, RNA helicase is required for hepatitis C virus RNA replication J. Virol. 2007, 81, 13922-6 (Pubitemid 350247885)
49. Parent, R.; Qu, X.; Petit, M. A.; Beretta, L. The heat shock cognate protein 70 is associated with hepatitis C virus particles and modulates virus infectivity Hepatology 2009, 49, 1798-809
50. Roohvand, F.; Maillard, P.; Lavergne, J. P.; Boulant, S.; Walic, M.; Andreo, U.; Goueslain, L.; Helle, F.; Mallet, A.; McLauchlan, J.; Budkowska, A. Initiation of hepatitis C virus infection requires the dynamic microtubule network: role of the viral nucleocapsid protein J. Biol. Chem. 2009, 284, 13778-91
51. Rocak, S.; Linder, P. DEAD-box proteins: the driving forces behind RNA metabolism Nat. Rev. Mol. Cell Biol. 2004, 5, 232-41 (Pubitemid 38325804)
52. Lai, C. K.; Jeng, K. S.; Machida, K.; Lai, M. M. Hepatitis C virus egress and release depend on endosomal trafficking of core protein J. Virol. 2010, 84, 11590-8
53. Shavinskaya, A.; Boulant, S.; Penin, F.; McLauchlan, J.; Bartenschlager, R. The lipid droplet binding domain of hepatitis C virus core protein is a major determinant for efficient virus assembly J. Biol. Chem. 2007, 282, 37158-69
54. Mogensen, M. M.; Malik, A.; Piel, M.; Bouckson-Castaing, V.; Bornens, M. Microtubule minus-end anchorage at centrosomal and non-centrosomal sites: the role of ninein J. Cell Sci. 2000, 113 (Pt 17) 3013-23
55. Zhang, J.; Yamada, O.; Yoshida, H.; Iwai, T.; Araki, H. Autogenous translational inhibition of core protein: implication for switch from translation to RNA replication in hepatitis C virus Virology 2002, 293, 141-50
56. Graber, T. E.; Baird, S. D.; Kao, P. N.; Mathews, M. B.; Holcik, M. NF45 functions as an IRES trans-acting factor that is required for translation of cIAP1 during the unfolded protein response Cell Death Differ. 2010, 17, 719-29
57. Huang, Y. S.; Dai, Y.; Yu, X. F.; Bao, S. Y.; Yin, Y. B.; Tang, M.; Hu, C. X. Microarray analysis of microRNA expression in hepatocellular carcinoma and non-tumorous tissues without viral hepatitis J. Gastroenterol. Hepatol. 2008, 23, 87-94 (Pubitemid 350265207)
58. Varnholt, H.; Drebber, U.; Schulze, F.; Wedemeyer, I.; Schirmacher, P.; Dienes, H. P.; Odenthal, M. MicroRNA gene expression profile of hepatitis C virus-associated hepatocellular carcinoma Hepatology 2008, 47, 1223-32 (Pubitemid 351547908)