Mathematical model of viral kinetics in vitro estimates the number of E2-CD81 complexes necessary for hepatitis C virus entry

PLoS Computational Biology

Volumn 7, Issue 12, 2011, Pages

  Padmanabhan, Pranesh ^a   Dixit, Narendra M ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; CELL CULTURE; CELL PROLIFERATION; ESTIMATION; GROWTH KINETICS; VIRUSES;

CULTURE SYSTEMS; ENVELOPE PROTEINS; HEPATITIS C VIRUS; IN-VITRO; MODEL PREDICTION; QUANTITATIVE AGREEMENT; TARGET CELLS; TRI-PHASIC; VIRUS ENTRY; VIRUS INFECTION;

KINETICS;

CD81 ANTIGEN; GLYCOPROTEIN E2; GLYCOPROTEIN E2, HEPATITIS C VIRUS; VIRUS ENVELOPE PROTEIN;

ANTIGEN EXPRESSION; ARTICLE; BINDING AFFINITY; CELL CULTURE; CELL LEVEL; CELL PROLIFERATION; CONTROLLED STUDY; HEPATITIS C VIRUS; HEPATOMA CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; MATHEMATICAL MODEL; MICROBIAL KINETICS; MOLECULAR CLONING; NONHUMAN; PREDICTION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; VIRUS CELL INTERACTION; VIRUS ENTRY; BIOLOGICAL MODEL; CHEMISTRY; IMMUNOLOGY; KINETICS; METABOLISM;

HEPATITIS C VIRUS;

ANTIGENS, CD81; HEPACIVIRUS; HUMANS; KINETICS; MODELS, BIOLOGICAL; VIRAL ENVELOPE PROTEINS; VIRUS INTERNALIZATION;

EID: 84855295474     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002307     Document Type: Article

References (55)

1. Scarselli E, Ansuini H, Cerino R, Roccasecca RM, Acali S, et al. (2002) The human scavenger receptor class B type I is a novel candidate receptor for the hepatitis C virus. EMBO J 21: 5017-5025.
2. Pileri P, Uematsu Y, Campagnoli S, Galli G, Falugi F, et al. (1998) Binding of hepatitis C virus to CD81. Science 282: 938-941.
3. Cormier EG, Tsamis F, Kajumo F, Durso RJ, Gardner JP, et al. (2004) CD81 is an entry coreceptor for hepatitis C virus. Proc Natl Acad Sci U S A 101: 7270-7274.
4. Evans MJ, von Hahn T, Tscherne DM, Syder AJ, Panis M, et al. (2007) Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 446: 801-805.
5. Ploss A, Evans MJ, Gaysinskaya VA, Panis M, You H, et al. (2009) Human occludin is a hepatitis C virus entry factor required for infection of mouse cells. Nature 457: 882-886.
6. Law M, Maruyama T, Lewis J, Giang E, Tarr AW, et al. (2008) Broadly neutralizing antibodies protect against hepatitis C virus quasispecies challenge. Nat Med 14: 25-27.
7. Dorner M, Horwitz JA, Robbins JB, Barry WT, Feng Q, et al. (2011) A genetically humanized mouse model for hepatitis C virus infection. Nature 474: 208-211.
8. Fafi-Kremer S, Fofana I, Soulier E, Carolla P, Meuleman P, et al. (2010) Viral entry and escape from antibody-mediated neutralization influence hepatitis C virus reinfection in liver transplantation. J Exp Med 207: 2019-2031.
9. Krieger SE, Zeisel MB, Davis C, Thumann C, Harris HJ, et al. (2009) Inhibition of hepatitis C virus infection by anti-claudin-1 antibodies is mediated by neutralization of E2-CD81-claudin-1 associations. Hepatology 51: 1144-1157.
10. Harris HJ, Davis C, Mullins JGL, Hu K, Goodall M, et al. (2010) Claudin association with CD81 defines hepatitis C virus entry. J Biol Chem 285: 21092-21102.
11. Lemon SM, McKeating JA, Pietschmann T, Frick DN, Glenn JS, et al. (2010) Development of novel therapies for hepatitis C. Antivir Res 86: 79-92.
12. Zeisel MB, Fofana I, Fafi-Kremer S, Baumert TF, (2011) Hepatitis C virus entry into hepatocytes: Molecular mechanisms and targets for antiviral therapies. J Hepatol 54: 566-576.
13. Koutsoudakis G, Herrmann E, Kallis S, Bartenschlager R, Pietschmann T, (2007) The level of CD81 cell surface expression is a key determinant for productive entry of hepatitis C virus into host cells. J Virol 81: 588-598.
14. Tscherne DM, Evans MJ, von Hahn T, Jones CT, Stamataki Z, et al. (2007) Superinfection exclusion in cells infected with hepatitis C virus. J Virol 81: 3693-3703.
15. Zhong J, Gastaminza P, Chung J, Stamataki Z, Isogawa M, et al. (2006) Persistent hepatitis C virus infection in vitro: coevolution of virus and host. J Virol 80: 11082-11093.
16. Kapadia SB, Barth H, Baumert T, McKeating JA, Chisari FV, (2007) Initiation of hepatitis C virus infection is dependent on cholesterol and cooperativity between CD81 and scavenger receptor B type I. J Virol 81: 374-383.
17. Brazzoli M, Bianchi A, Filippini S, Weiner A, Zhu Q, et al. (2008) CD81 is a central regulator of cellular events required for hepatitis C virus infection of human hepatocytes. J Virol 82: 8316-8329.
18. Zhang YY, Zhang BH, Ishii K, Liang TJ, (2010) Novel function of CD81 in controlling hepatitis C virus replication. J Virol 84: 3396-3407.
19. Magnus C, Rusert P, Bonhoeffer S, Trkola A, Regoes RR, (2009) Estimating the stoichiometry of human immunodeficiency virus entry. J Virol 83: 1523-1531.
20. Mulampaka SN, Dixit NM, (2011) Estimating the threshold surface density of gp120-CCR5 complexes necessary for HIV-1 envelope-mediated cell-cell fusion. PLoS One 6: e19941.
21. Neumann AU, Lam NP, Dahari H, Gretch DR, Wiley TE, et al. (1998) Hepatitis C viral dynamics in vivo and the antiviral efficacy of interferon-alpha therapy. Science 282: 103-107.
22. Zeuzem S, Herrmann E, Lee JH, Fricke J, Neumann AU, et al. (2001) Viral kinetics in patients with chronic hepatitis C treated with standard or peginterferon alpha-2a. Gastroenterology 120: 1438-1447.
23. Herrmann E, Lee JH, Marinos G, Modi M, Zeuzem S, (2003) Effect of ribavirin on hepatitis C viral kinetics in patients treated with pegylated interferon. Hepatology 37: 1351-1358.
24. Dixit NM, Layden-Almer JE, Layden TJ, Perelson AS, (2004) Modelling how ribavirin improves interferon response rates in hepatitis C virus infection. Nature 432: 922-924.
25. Dahari H, Ribeiro RM, Perelson AS, (2007) Triphasic decline of hepatitis C virus RNA during antiviral therapy. Hepatology 46: 16-21.
26. Colombatto P, Ciccorossi P, Maina AM, Civitano L, Oliveri F, et al. (2008) Early and accurate prediction of peg-IFNs/ribavirin therapy outcome in the individual patient with chronic hepatitis C by modeling the dynamics of the infected cells. Clin Pharmacol Ther 84: 212-215.
27. Rong L, Dahari H, Ribeiro RM, Perelson AS, (2010) Rapid emergence of protease inhibitor resistance in hepatitis C virus. Sci Transl Med 2: 30ra32.
28. Rong L, Perelson AS, (2010) Treatment of hepatitis C virus infection with interferon and small molecule direct antivirals: viral kinetics and modeling. Crit Rev Immunol 30: 131-148.
29. Adiwijaya BS, Herrmann E, Hare B, Kieffer T, Lin C, et al. (2010) A multi-variant, viral dynamic model of genotype 1 HCV to assess the in vivo evolution of protease-inhibitor resistant variants. PLoS Comput Biol 6: e1000745.
30. Guedj J, Perelson AS, (2011) Second-phase hepatitis C virus RNA decline during telaprevir-based therapy increases with drug effectiveness: Implications for treatment duration. Hepatology 53: 1801-1808.
31. Hsu CS, Hsu SJ, Chen HC, Tseng TC, Liu CH, et al. (2011) Association of IL28B gene variations with mathematical modeling of viral kinetics in chronic hepatitis C patients with IFN plus ribavirin therapy. Proc Natl Acad Sci U S A 108: 3719-3724.
32. Walters KA, Syder AJ, Lederer SL, Diamond DL, Paeper B, et al. (2009) Genomic analysis reveals a potential role for cell cycle perturbation in HCV-mediated apoptosis of cultured hepatocytes. PLoS Pathog 5: e1000269.
33. DebRoy S, Kribs-Zaleta C, Mubayi A, Cardona-Melendez GM, Medina-Rios L, et al. (2010) Evaluating treatment of hepatitis C for hemolytic anemia management. Mathematical Biosciences 225: 141-155.
34. Krishnan SM, Dixit NM, (2011) Ribavirin-induced anemia in hepatitis C virus patients undergoing combination therapy. PLoS Comput Biol 7: e1001072.
35. Wakita T, Pietschmann T, Kato T, Date T, Miyamoto M, et al. (2005) Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med 11: 791-796.
36. Zhong J, Gastaminza P, Cheng G, Kapadia S, Kato T, et al. (2005) Robust hepatitis C virus infection in vitro. Proc Natl Acad Sci U S A 102: 9294-9299.
37. Lindenbach BD, Evans MJ, Syder AJ, Wölk B, Tellinghuisen TL, et al. (2005) Complete replication of hepatitis C virus in cell culture. Science 309: 623-626.
38. Ploss A, Khetani SR, Jones CT, Syder AJ, Trehan K, et al. (2010) Persistent hepatitis C virus infection in microscale primary human hepatocyte cultures. Proc Natl Acad Sci U S A 107: 3141-3145.
39. Guedj J, Neumann AU, (2010) Understanding hepatitis C viral dynamics with direct-acting antiviral agents due to the interplay between intracellular replication and cellular infection dynamics. J Theor Biol 267: 330-340.
40. Dahari H, Ribeiro RM, Rice CM, Perelson AS, (2007) Mathematical modeling of subgenomic hepatitis C virus replication in Huh-7 cells. J Virol 81: 750-760.
41. Dahari H, Sainz B Jr, Perelson AS, Uprichard SL, (2009) Modeling subgenomic hepatitis C virus RNA kinetics during treatment with alpha interferon. J Virol 83: 6383-6390.
42. Hofmann WP, Zeuzem S, (2011) A new standard of care for the treatment of chronic HCV infection. Nat Rev Gastroenterol Hepatol 8: 257-264.
43. Nakajima H, Cocquerel L, Kiyokawa N, Fujimoto J, Levy S, (2005) Kinetics of HCV envelope proteins' interaction with CD81 large extracellular loop. Biochem Biophys Res Commun 328: 1091-1100.
44. Baksh MM, Kussrow AK, Mileni M, Finn MG, Bornhop DJ, (2011) Label-free quantification of membrane-ligand interactions using backscattering interferometry. Nat Biotechnol 29: 357-360.
45. Flint M, Von Hahn T, Zhang J, Farquhar M, Jones CT, et al. (2006) Diverse CD81 proteins support hepatitis C virus infection. J Virol 80: 11331-11342.
46. Rocha-Perugini V, Lavie M, Delgrange D, Canton J, Pillez A, et al. (2009) The association of CD81 with tetraspanin-enriched microdomains is not essential for hepatitis C virus entry. BMC Microbiol 9: 111.
47. Brimacombe CL, Grove J, Meredith LW, Hu K, Syder AJ, et al. (2011) Neutralizing antibody resistant hepatitis C virus cell-to-cell transmission. J Virol 85: 596-605.
48. Kannan RP, Hensley LL, Evers LE, Lemon SM, McGivern DR, (2011) Hepatitis C virus infection causes cell cycle arrest at the level of initiation of mitosis. J Virol 85: 7989-8001.
49. Beauchemin CAA, McSharry JJ, Drusano GL, Nguyen JT, Went GT, et al. (2008) Modeling amantadine treatment of influenza A virus in vitro. J Theor Biol 254: 439-451.
50. Sabahi A, Marsh KA, Dahari H, Corcoran P, Lamora JM, et al. (2010) The rate of hepatitis C virus infection initiation in vitro is directly related to particle density. Virology 407: 110-119.
51. Bell GI, (1978) Models for the specific adhesion of cells to cells. Science 200: 618-627.
52. Wu J, Fang Y, Zarnitsyna VI, Tolentino TP, Dustin ML, et al. (2008) A coupled diffusion-kinetics model for analysis of contact-area FRAP experiment. Biophys J 95: 910-919.
53. Yu X, Qiao M, Atanasov I, Hu Z, Kato T, et al. (2007) Cryo-electron microscopy and three-dimensional reconstructions of hepatitis C virus particles. Virology 367: 126-134.
54. Sougrat R, Bartesaghi A, Lifson JD, Bennett AE, Bess JW, et al. (2007) Electron tomography of the contact between T cells and SIV/HIV-1: implications for viral entry. PLoS Pathog 3: e63.
55. Zhang J, Randall G, Higginbottom A, Monk P, Rice CM, et al. (2004) CD81 is required for hepatitis C virus glycoprotein-mediated viral infection. J Virol 78: 1448-1455.