Startseite Hepatitis C virus and autophagy
Artikel
Lizenziert
Nicht lizenziert Erfordert eine Authentifizierung

Hepatitis C virus and autophagy

  • Linya Wang und Jing-hsiung James Ou EMAIL logo
Veröffentlicht/Copyright: 29. Mai 2015
Biological Chemistry
Aus der Zeitschrift Biological Chemistry Band 396 Heft 11

Abstract

Autophagy is a catabolic process by which cells remove protein aggregates and damaged organelles for recycling. It can also be used by cells to remove intracellular microbial pathogens, including viruses, in a process known as xenophagy. However, many viruses have developed mechanisms to subvert this intracellular antiviral response and even use this pathway to support their own replications. Hepatitis C virus (HCV) is one such virus and is an important human pathogen that can cause severe liver diseases. Recent studies indicated that HCV could activate the autophagic pathway to support its replication. This review summarizes the current knowledge on the interplay between HCV and autophagy and how this interplay affects HCV replication and host innate immune responses.

Keywords: autolysosomes; autophagosomes; autophagy; hepatitis C virus; innate immunity; unfolded protein response
Corresponding author: Jing-hsiung James Ou, Department of Molecular Microbiology and Immunology, University of Southern California, Keck School of Medicine, Los Angeles, CA 90033, USA, e-mail:

Acknowledgments

This work is supported by National Institutes of Diabetes and Digestive and Kidney Diseases grants DK094652, DK100257 and National Cancer Institute CA177337.

References

Ait-Goughoulte, M., Kanda, T., Meyer, K., Ryerse, J.S., Ray, R.B., and Ray, R. (2008). Hepatitis C virus genotype 1a growth and induction of autophagy. J. Virol. 82, 2241–2249.10.1128/JVI.02093-07Suche in Google Scholar PubMed PubMed Central

Aweya, J.J., Mak, T.M., Lim, S.G., and Tan, Y.J. (2013). The p7 protein of the hepatitis C virus induces cell death differently from the influenza A virus viroporin M2. Virus Res. 172, 24–34.10.1016/j.virusres.2012.12.005Suche in Google Scholar PubMed PubMed Central

Bartenschlager, R. and Lohmann, V. (2000). Replication of hepatitis C virus. J. Gen. Virol. 81, 1631–1648.10.1053/bega.1999.0073Suche in Google Scholar

Chatterji, U., Bobardt, M., Tai, A., Wood, M., and Gallay, P.A. (2015). Cyclophilin and NS5A inhibitors, but not other anti-hepatitis C virus (HCV) agents, preclude HCV-mediated formation of double-membrane-vesicle viral factories. Antimicrob. Agents Chemother. 59, 2496–2507.10.1128/AAC.04958-14Suche in Google Scholar PubMed PubMed Central

Desai, M.M., Gong, B., Chan, T., Davey, R.A., Soong, L., Kolokoltsov, A.A., and Sun, J. (2011). Differential, type I interferon-mediated autophagic trafficking of hepatitis C virus proteins in mouse liver. Gastroenterology 141, 674–685, 685 e671–e676.10.1053/j.gastro.2011.04.060Suche in Google Scholar PubMed PubMed Central

Dreux, M., Gastaminza, P., Wieland, S.F., and Chisari, F.V. (2009). The autophagy machinery is required to initiate hepatitis C virus replication. Proc. Natl. Acad. Sci. USA 106, 14046–14051.10.1073/pnas.0907344106Suche in Google Scholar PubMed PubMed Central

Ferraris, P., Blanchard, E., and Roingeard, P. (2010). Ultrastructural and biochemical analyses of hepatitis C virus-associated host cell membranes. J. Gen. Virol. 91, 2230–2237.10.1099/vir.0.022186-0Suche in Google Scholar PubMed

Foy, E., Li, K., Sumpter, R., Jr., Loo, Y.M., Johnson, C.L., Wang, C., Fish, P.M., Yoneyama, M., Fujita, T., Lemon, S.M., et al. (2005). Control of antiviral defenses through hepatitis C virus disruption of retinoic acid-inducible gene-I signaling. Proc. Natl. Acad. Sci. USA 102, 2986–2991.10.1073/pnas.0408707102Suche in Google Scholar PubMed PubMed Central

Gomes, L.C. and Dikic, I. (2014). Autophagy in antimicrobial immunity. Mol. Cell 54, 224–233.10.1016/j.molcel.2014.03.009Suche in Google Scholar PubMed

Gregoire, I.P., Richetta, C., Meyniel-Schicklin, L., Borel, S., Pradezynski, F., Diaz, O., Deloire, A., Azocar, O., Baguet, J., Le Breton, M., et al. (2011). IRGM is a common target of RNA viruses that subvert the autophagy network. PLoS Pathog. 7, e1002422.10.1371/journal.ppat.1002422Suche in Google Scholar PubMed PubMed Central

Guevin, C., Manna, D., Belanger, C., Konan, K.V., Mak, P., and Labonte, P. (2010). Autophagy protein ATG5 interacts transiently with the hepatitis C virus RNA polymerase (NS5B) early during infection. Virology 405, 1–7.10.1016/j.virol.2010.05.032Suche in Google Scholar PubMed PubMed Central

Hetz, C. (2012). The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat. Rev. Mol. Cell. Biol. 13, 89–102.10.1038/nrm3270Suche in Google Scholar PubMed

Huang, H., Kang, R., Wang, J., Luo, G., Yang, W., and Zhao, Z. (2013). Hepatitis C virus inhibits AKT-tuberous sclerosis complex (TSC), the mechanistic target of rapamycin (MTOR) pathway, through endoplasmic reticulum stress to induce autophagy. Autophagy 9, 175–195.10.4161/auto.22791Suche in Google Scholar PubMed PubMed Central

Jounai, N., Takeshita, F., Kobiyama, K., Sawano, A., Miyawaki, A., Xin, K.Q., Ishii, K.J., Kawai, T., Akira, S., Suzuki, K., et al. (2007). The Atg5 Atg12 conjugate associates with innate antiviral immune responses. Proc. Natl. Acad. Sci. USA 104, 14050–14055.10.1073/pnas.0704014104Suche in Google Scholar PubMed PubMed Central

Joyce, M.A., Walters, K.A., Lamb, S.E., Yeh, M.M., Zhu, L.F., Kneteman, N., Doyle, J.S., Katze, M.G., and Tyrrell, D.L. (2009). HCV induces oxidative and ER stress, and sensitizes infected cells to apoptosis in SCID/Alb-uPA mice. PLoS Pathog. 5, e1000291.10.1371/journal.ppat.1000291Suche in Google Scholar PubMed PubMed Central

Ke, P.Y. and Chen, S.S. (2011). Activation of the unfolded protein response and autophagy after hepatitis C virus infection suppresses innate antiviral immunity in vitro. J. Clin. Invest. 121, 37–56.10.1172/JCI41474Suche in Google Scholar PubMed PubMed Central

Kim, S.J., Syed, G.H., and Siddiqui, A. (2013). Hepatitis C virus induces the mitochondrial translocation of Parkin and subsequent mitophagy. PLoS Pathog. 9, e1003285.10.1371/journal.ppat.1003285Suche in Google Scholar PubMed PubMed Central

Kim, S.J., Syed, G.H., Khan, M., Chiu, W.W., Sohail, M.A., Gish, R.G., and Siddiqui, A. (2014). Hepatitis C virus triggers mitochondrial fission and attenuates apoptosis to promote viral persistence. Proc. Natl. Acad. Sci. USA 111, 6413–6418.10.1073/pnas.1321114111Suche in Google Scholar PubMed PubMed Central

Levine, B. and Kroemer, G. (2008). Autophagy in the pathogenesis of disease. Cell 132, 27–42.10.1016/j.cell.2007.12.018Suche in Google Scholar PubMed PubMed Central

Li, X.D., Sun, L., Seth, R.B., Pineda, G., and Chen, Z.J. (2005). Hepatitis C virus protease NS3/4A cleaves mitochondrial antiviral signaling protein off the mitochondria to evade innate immunity. Proc. Natl. Acad. Sci. USA 102, 17717–17722.10.1073/pnas.0508531102Suche in Google Scholar PubMed PubMed Central

Li, S., Ye, L., Yu, X., Xu, B., Li, K., Zhu, X., Liu, H., Wu, X., and Kong, L. (2009). Hepatitis C virus NS4B induces unfolded protein response and endoplasmic reticulum overload response-dependent NF-κB activation. Virology 391, 257–264.10.1016/j.virol.2009.06.039Suche in Google Scholar PubMed

Li, X.D., Chiu, Y.H., Ismail, A.S., Behrendt, C.L., Wight-Carter, M., Hooper, L.V., and Chen, Z.J. (2011). Mitochondrial antiviral signaling protein (MAVS) monitors commensal bacteria and induces an immune response that prevents experimental colitis. Proc. Natl. Acad. Sci. USA 108, 17390–17395.10.1073/pnas.1107114108Suche in Google Scholar PubMed PubMed Central

Liang, C., Lee, J.S., Inn, K.S., Gack, M.U., Li, Q., Roberts, E.A., Vergne, I., Deretic, V., Feng, P., Akazawa, C., et al. (2008). Beclin1-binding UVRAG targets the class C Vps complex to coordinate autophagosome maturation and endocytic trafficking. Nat. Cell Biol. 10, 776–87.10.1038/ncb1740Suche in Google Scholar PubMed PubMed Central

Matsunaga, K., Saitoh, T., Tabata, K., Omori, H., Satoh, T., Kurotori, N., Maejima, I., Shirahama-Noda, K., Ichimura, T., Isobe, T., et al. (2009). Two Beclin 1-binding proteins, Atg14L and Rubicon, reciprocally regulate autophagy at different stages. Nat. Cell Biol. 11, 385–396.10.1038/ncb1846Suche in Google Scholar PubMed

Mizui, T., Yamashina, S., Tanida, I., Takei, Y., Ueno, T., Sakamoto, N., Ikejima, K., Kitamura, T., Enomoto, N., Sakai, T., et al. (2010). Inhibition of hepatitis C virus replication by chloroquine targeting virus-associated autophagy. J. Gastroenterol. 45, 195–203.10.1007/s00535-009-0132-9Suche in Google Scholar PubMed PubMed Central

Mohl, B.P., Tedbury, P.R., Griffin, S., and Harris, M. (2012). Hepatitis C virus-induced autophagy is independent of the unfolded protein response. J. Virol. 86, 10724–10732.10.1128/JVI.01667-12Suche in Google Scholar PubMed PubMed Central

Moradpour, D., Penin, F., and Rice, C.M. (2007). Replication of hepatitis C virus. Nat. Rev. Microbiol. 5, 453–463.10.1038/nrmicro1645Suche in Google Scholar PubMed

Paul, D., Hoppe, S., Saher, G., Krijnse-Locker, J., and Bartenschlager, R. (2013). Morphological and biochemical characterization of the membranous hepatitis C virus replication compartment. J. Virol. 87, 10612–10627.10.1128/JVI.01370-13Suche in Google Scholar PubMed PubMed Central

Quan, M., Liu, S., Li, G., Wang, Q., Zhang, J., Zhang, M., Li, M., Gao, P., Feng, S., and Cheng, J. (2014). A functional role for NS5ATP9 in the induction of HCV NS5A-mediated autophagy. J. Viral Hepat. 21, 405–415.10.1111/jvh.12155Suche in Google Scholar PubMed

Rautou, P.E., Cazals-Hatem, D., Feldmann, G., Mansouri, A., Grodet, A., Barge, S., Martinot-Peignoux, M., Duces, A., Bieche, I., Lebrec, D., et al. (2011). Changes in autophagic response in patients with chronic hepatitis C virus infection. Am. J. Pathol. 178, 2708–2715.10.1016/j.ajpath.2011.02.021Suche in Google Scholar PubMed PubMed Central

Romero-Brey, I., Merz, A., Chiramel, A., Lee, J.Y., Chlanda, P., Haselman, U., Santarella-Mellwig, R., Habermann, A., Hoppe, S., Kallis, S., et al. (2012). Three-dimensional architecture and biogenesis of membrane structures associated with hepatitis C virus replication. PLoS Pathog. 8, e1003056.10.1371/journal.ppat.1003056Suche in Google Scholar PubMed PubMed Central

Shepard, C.W., Finelli, L., and Alter, M.J. (2005). Global epidemiology of hepatitis C virus infection. Lancet Infect. Dis. 5, 558–567.10.1016/S1473-3099(05)70216-4Suche in Google Scholar

Shinohara, Y., Imajo, K., Yoneda, M., Tomeno, W., Ogawa, Y., Kirikoshi, H., Funakoshi, K., Ikeda, M., Kato, N., Nakajima, A., et al. (2013). Unfolded protein response pathways regulate Hepatitis C virus replication via modulation of autophagy. Biochem. Biophys. Res. Commun. 432, 326–332.10.1016/j.bbrc.2013.01.103Suche in Google Scholar PubMed PubMed Central

Shrivastava, S., Raychoudhuri, A., Steele, R., Ray, R., and Ray, R.B. (2011). Knockdown of autophagy enhances the innate immune response in hepatitis C virus-infected hepatocytes. Hepatology 53, 406–414.10.1002/hep.24073Suche in Google Scholar PubMed PubMed Central

Shrivastava, S., Bhanja Chowdhury, J., Steele, R., Ray, R., and Ray, R.B. (2012). Hepatitis C virus upregulates Beclin1 for induction of autophagy and activates mTOR signaling. J. Virol. 86, 8705–8712.10.1128/JVI.00616-12Suche in Google Scholar PubMed PubMed Central

Simonsen, A. and Tooze, S.A. (2009). Coordination of membrane events during autophagy by multiple class III PI3-kinase complexes. J. Cell Biol. 186, 773–782.10.1083/jcb.200907014Suche in Google Scholar PubMed PubMed Central

Sir, D., Chen, W.L., Choi, J., Wakita, T., Yen, T.S., and Ou, J.H. (2008). Induction of incomplete autophagic response by hepatitis C virus via the unfolded protein response. Hepatology 48, 1054–1061.10.1002/hep.22464Suche in Google Scholar PubMed PubMed Central

Sir, D., Kuo, C.F., Tian, Y., Liu, H.M., Huang, E.J., Jung, J.U., Machida, K., and Ou, J.H. (2012). Replication of hepatitis C virus RNA on autophagosomal membranes. J. Biol. Chem. 287, 18036–18043.10.1074/jbc.M111.320085Suche in Google Scholar PubMed PubMed Central

Stone, M., Jia, S., Heo, W.D., Meyer, T., and Konan, K.V. (2007). Participation of rab5, an early endosome protein, in hepatitis C virus RNA replication machinery. J. Virol. 81, 4551–4563.10.1128/JVI.01366-06Suche in Google Scholar PubMed PubMed Central

Su, W.C., Chao, T.C., Huang, Y.L., Weng, S.C., Jeng, K.S., and Lai, M.M. (2011). Rab5 and class III phosphoinositide 3-kinase Vps34 are involved in hepatitis C virus NS4B-induced autophagy. J. Virol. 85, 10561–10571.10.1128/JVI.00173-11Suche in Google Scholar PubMed PubMed Central

Sun, Q., Westphal, W., Wong, K.N., Tan, I., and Zhong, Q. (2010). Rubicon controls endosome maturation as a Rab7 effector. Proc. Natl. Acad. Sci. USA 107, 19338–19343.10.1073/pnas.1010554107Suche in Google Scholar PubMed PubMed Central

Taguwa, S., Kambara, H., Fujita, N., Noda, T., Yoshimori, T., Koike, K., Moriishi, K., and Matsuura, Y. (2011). Dysfunction of autophagy participates in vacuole formation and cell death in cells replicating hepatitis C virus. J. Virol. 85, 13185–13194.10.1128/JVI.06099-11Suche in Google Scholar PubMed PubMed Central

Tanida, I., Fukasawa, M., Ueno, T., Kominami, E., Wakita, T., and Hanada, K. (2009). Knockdown of autophagy-related gene decreases the production of infectious hepatitis C virus particles. Autophagy 5, 937–945.10.4161/auto.5.7.9243Suche in Google Scholar PubMed

Tardif, K.D., Mori, K., and Siddiqui, A. (2002). Hepatitis C virus subgenomic replicons induce endoplasmic reticulum stress activating an intracellular signaling pathway. J. Virol. 76, 7453–7459.10.1128/JVI.76.15.7453-7459.2002Suche in Google Scholar PubMed PubMed Central

Tardif, K.D., Waris, G., and Siddiqui, A. (2005). Hepatitis C virus, ER stress, and oxidative stress. Trends Microbiol. 13, 159–163.10.1016/j.tim.2005.02.004Suche in Google Scholar PubMed

Tellinghuisen, T.L., Evans, M.J., von Hahn, T., You, S., and Rice, C.M. (2007). Studying hepatitis C virus: making the best of a bad virus. J. Virol. 81, 8853–8867.10.1128/JVI.00753-07Suche in Google Scholar PubMed PubMed Central

Vescovo, T., Romagnoli, A., Perdomo, A.B., Corazzari, M., Ciccosanti, F., Alonzi, T., Nardacci, R., Ippolito, G., Tripodi, M., Garcia-Monzon, C., et al. (2012). Autophagy protects cells from HCV-induced defects in lipid metabolism. Gastroenterology 142, 644–653, e643.10.1053/j.gastro.2011.11.033Suche in Google Scholar PubMed

Wang, M. and Kaufman, R.J. (2014). The impact of the endoplasmic reticulum protein-folding environment on cancer development. Nat. Rev. Cancer 14, 581–597.10.1038/nrc3800Suche in Google Scholar PubMed

Wang, J., Kang, R., Huang, H., Xi, X., Wang, B., Wang, J., and Zhao, Z. (2014). Hepatitis C virus core protein activates autophagy through EIF2AK3 and ATF6 UPR pathway- mediated MAP1LC3B and ATG12 expression. Autophagy 10, 766–784.10.4161/auto.27954Suche in Google Scholar PubMed PubMed Central

Wang, L., Tian, Y., and Ou, J.H. (2015). HCV induces the expression of Rubicon and UVRAG to temporally regulate the maturation of autophagosomes and viral replication. PLoS Pathog. 11, e1004764.10.1371/journal.ppat.1004764Suche in Google Scholar PubMed PubMed Central

Youle, R.J. and Narendra, D.P. (2011). Mechanisms of mitophagy. Nat. Rev. Mol. Cell. Biol. 12, 9–14.10.1038/nrm3028Suche in Google Scholar PubMed PubMed Central

Zheng, Y., Gao, B., Ye, L., Kong, L., Jing, W., Yang, X., Wu, Z., and Ye, L. (2005). Hepatitis C virus non-structural protein NS4B can modulate an unfolded protein response. J. Microbiol. 43, 529–536.Suche in Google Scholar

Received: 2015-5-2
Accepted: 2015-5-26
Published Online: 2015-5-29
Published in Print: 2015-11-1

©2015 by De Gruyter

Artikel in diesem Heft

  1. Frontmatter
  2. Reviews
  3. Defects of corneocyte structural proteins and epidermal barrier in atopic dermatitis
  4. C-reactive protein and inflammation: conformational changes affect function
  5. Biogenesis of mitochondrial outer membrane proteins, problems and diseases
  6. Hepatitis C virus and autophagy
  7. Minireviews
  8. The glucocorticoid receptor in inflammatory processes: transrepression is not enough
  9. Red blood cells in Rett syndrome: oxidative stress, morphological changes and altered membrane organization
  10. Research Articles/Short Communications
  11. Membranes, Lipids, Glycobiology
  12. High β-glucosidase (GBA) activity not attributable to GBA1 and GBA2 in live normal and enzyme-deficient fibroblasts may emphasise the role of additional GBAs
  13. Cell Biology and Signaling
  14. Exogenous hydrogen sulfide exhibits anti-cancer effects though p38 MAPK signaling pathway in C6 glioma cells
  15. Novel Techniques
  16. Impact of food components during in vitro digestion of silver nanoparticles on cellular uptake and cytotoxicity in intestinal cells
  17. A simple and highly sensitive method of measuring heme oxygenase activity
https://doi.org/10.1515/hsz-2015-0172
Schlagwörter für diesen Artikel
autolysosomes; autophagosomes; autophagy; hepatitis C virus; innate immunity; unfolded protein response

Artikel in diesem Heft

  1. Frontmatter
  2. Reviews
  3. Defects of corneocyte structural proteins and epidermal barrier in atopic dermatitis
  4. C-reactive protein and inflammation: conformational changes affect function
  5. Biogenesis of mitochondrial outer membrane proteins, problems and diseases
  6. Hepatitis C virus and autophagy
  7. Minireviews
  8. The glucocorticoid receptor in inflammatory processes: transrepression is not enough
  9. Red blood cells in Rett syndrome: oxidative stress, morphological changes and altered membrane organization
  10. Research Articles/Short Communications
  11. Membranes, Lipids, Glycobiology
  12. High β-glucosidase (GBA) activity not attributable to GBA1 and GBA2 in live normal and enzyme-deficient fibroblasts may emphasise the role of additional GBAs
  13. Cell Biology and Signaling
  14. Exogenous hydrogen sulfide exhibits anti-cancer effects though p38 MAPK signaling pathway in C6 glioma cells
  15. Novel Techniques
  16. Impact of food components during in vitro digestion of silver nanoparticles on cellular uptake and cytotoxicity in intestinal cells
  17. A simple and highly sensitive method of measuring heme oxygenase activity
Jetzt anmelden und 20% sparen
Institutioneller Zugang
Wie funktioniert Authentifizierung?
Haben Sie eine Idee, wie wir unsere Website verbessern können?
Bitte schreiben Sie uns.
© 2025 De Gruyter Brill
Heruntergeladen am 23.11.2025 von https://www.degruyterbrill.com/document/doi/10.1515/hsz-2015-0172/html?lang=de
Button zum nach oben scrollen