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Virology Journal
Published in: Virology Journal 1/2013

Open Access 01-12-2013 | Review

Multiscale perspectives of virus entry via endocytosis

Authors: Eric Barrow, Anthony V Nicola, Jin Liu

Published in: Virology Journal | Issue 1/2013

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Abstract

Most viruses take advantage of endocytic pathways to gain entry into host cells and initiate infections. Understanding of virus entry via endocytosis is critically important for the design of antiviral strategies. Virus entry via endocytosis is a complex process involving hundreds of cellular proteins. The entire process is dictated by events occurring at multiple time and length scales. In this review, we discuss and evaluate the available means to investigate virus endocytic entry, from both experimental and theoretical/numerical modeling fronts, and highlight the importance of multiscale features. The complexity of the process requires investigations at a systems biology level, which involves the combination of different experimental approaches, the collaboration of experimentalists and theorists across different disciplines, and the development of novel multiscale models.
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Literature
1.
2.
Fauci AS: Emerging and re-emerging infectious diseases: influenza as a prototype of the host-pathogen balancing act. Cell 2006, 124: 665-670. 10.1016/j.cell.2006.02.010PubMed
3.
Morens DM, Folkers GK, Fauci AS: Emerging infections: a perpetual challenge. Lancet Infect Dis 2008, 8: 710-719. 10.1016/S1473-3099(08)70256-1PubMedPubMedCentral
4.
Smith AE, Helenius A: How viruses enter animal cells. Science 2004, 304: 237-242. 10.1126/science.1094823PubMed
5.
Mercer J, Schelhaas M, Helenius A: Virus entry by Endocytosis. Annu Rev Biochem 2010, 79: 803-833. 10.1146/annurev-biochem-060208-104626PubMed
6.
Sieczkarski SB, Whittaker GR: Dissecting virus entry via endocytosis. J Gen Virol 2002, 83: 1535-1545.PubMed
7.
Pelkmans L, Helenius A: Insider information: what viruses tell us about endocytosis. Curr Opin Cell Biol 2003, 15: 414-422. 10.1016/S0955-0674(03)00081-4PubMed
8.
Marsh M, Helenius A: Virus entry: open sesame. Cell 2006, 124: 729-740. 10.1016/j.cell.2006.02.007PubMed
9.
Doherty GJ, McMahon HT: Mechanisms of endocytosis. Annu Rev Biochem 2009, 78: 857-902. 10.1146/annurev.biochem.78.081307.110540PubMed
10.
Ramanan V, Agrawal NJ, Liu J, Engles S, Toy R, Radhakrishnan R: Systems biology and physical biology of clathrin-mediated endocytosis. Integr Biol 2011, 3: 803-815. 10.1039/c1ib00036e
11.
Canton I, Battaglia G: Endocytosis at the nanoscale. Chem Soc Rev 2012, 41: 2718-2739. 10.1039/c2cs15309bPubMed
12.
Miyauchi K, Kim Y, Latinovic O, Morozov V, Melikyan GB: HIV enters cells via endocytosis and dynamin-dependent fusion with endosomes. Cell 2009, 137: 433-444. 10.1016/j.cell.2009.02.046PubMedPubMedCentral
13.
Mercer J, Helenius A: Virus entry by macropinocytosis. Nat Cell Biol 2009, 11: 510-520. 10.1038/ncb0509-510PubMed
14.
Nicola AV, Hou J, Major EO, Straus SE: Herpes simplex virus type 1 enters human epidermal keratinocytes, but not neurons, via a pH-dependent endocytic pathway. J Virol 2005, 79: 7609-7616. 10.1128/JVI.79.12.7609-7616.2005PubMedPubMedCentral
15.
Amstutz B, Gastaldelli M, Kalin S, Imelli N, Boucke K, Wandeler E, Mercer J, Hemmi S, Greber UF: Subversion of CtBP1-controlled macropinocytosis by human adenovirus serotype 3. EMBO J 2008, 27: 956-969. 10.1038/emboj.2008.38PubMedPubMedCentral
16.
Mercer J, Helenius A: Vaccinia virus uses macropinocytosis and apoptotic mimicry to enter host cells. Science 2008, 320: 531-535. 10.1126/science.1155164PubMed
17.
Stang E, Kartenbeck J, Parton RG: Major histocompatibility complex class I molecules mediate association of SV40 with caveolae. Mol Biol Cell 1997, 8: 47-57.PubMedPubMedCentral
18.
Richterova Z, Liebl D, Horak M, Palkova Z, Stokrova J, Hozak P, Korb J, Forstova J: Caveolae are involved in the trafficking of mouse polyomavirus virions and artificial VP1 pseudocapsids toward cell nuclei. J Virol 2001, 75: 10880-10891. 10.1128/JVI.75.22.10880-10891.2001PubMedPubMedCentral
19.
Pelkmans L, Helenius A: Endocytosis via caveolae. Traffic 2002, 3: 311-320. 10.1034/j.1600-0854.2002.30501.xPubMed
20.
Sieczkarski SB, Whittaker GR: Influenza virus can enter and infect cells in the absence of clathrin-mediated endocytosis. J Virol 2002, 76: 10455-10464. 10.1128/JVI.76.20.10455-10464.2002PubMedPubMedCentral
21.
Lakadamyali M, Rust MJ, Zhuang XW: Endocytosis of influenza viruses. Microbes Infect 2004, 6: 929-936. 10.1016/j.micinf.2004.05.002PubMedPubMedCentral
22.
Rust MJ, Lakadamyali M, Zhang F, Zhuang XW: Assembly of endocytic machinery around individual influenza viruses during viral entry. Nat Struct Mol Biol 2004, 11: 567-573. 10.1038/nsmb769PubMedPubMedCentral
23.
Pelkmans L, Fava E, Grabner H, Hannus M, Habermann B, Krausz E, Zerial M: Genome-wide analysis of human kinases in clathrin- and caveolae/raft-mediated endocytosis. Nature 2005, 436: 78-86. 10.1038/nature03571PubMed
24.
Damm E-M, Pelkmans L: Systems biology of virus entry in mammalian cells. Cell Microbiol 2006, 8: 1219-1227. 10.1111/j.1462-5822.2006.00745.xPubMed
25.
Greber UF: Signalling in viral entry. Cell Mol Life Sci 2002, 59: 608-626. 10.1007/s00018-002-8453-3PubMed
26.
Gruenberg J: Viruses and endosome membrane dynamics. Curr Opin Cell Biol 2009, 21: 582-588. 10.1016/j.ceb.2009.03.008PubMed
27.
Mayor S, Pagano RE: Pathways of clathrin-independent endocytosis. Nat Rev Mol Cell Biol 2007, 8: 603-612. 10.1038/nrm2216PubMed
28.
Dales S: An electron microscope study of the early association between two mammalian viruses and their hosts. J Cell Biol 1962, 13: 303-322. 10.1083/jcb.13.2.303PubMedPubMedCentral
29.
Nicola AV, McEvoy AM, Straus SE: Roles for endocytosis and Low pH in herpes simplex virus entry into HeLa and chinese hamster ovary cells. J Virol 2003, 77: 5324-5332. 10.1128/JVI.77.9.5324-5332.2003PubMedPubMedCentral
30.
Brandenburg B, Zhuang X: Virus trafficking - learning from single-virus tracking. Nat Rev Microbiol 2007, 5: 197-208. 10.1038/nrmicro1615PubMedPubMedCentral
31.
Pelkmans L, Kartenbeck J, Helenius A: Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat Cell Biol 2001, 3: 473-483. 10.1038/35074539PubMed
32.
Chen C, Zhuang X: Epsin 1 is a cargo-specific adaptor for the clathrin-mediated endocytosis of the influenza virus. Proc Natl Acad Sci USA 2008, 105: 11790-11795. 10.1073/pnas.0803711105PubMedPubMedCentral
33.
van der Schaar HM, Rust MJ, Chen C, van der Ende-Metselaar H, Wilschut J, Zhuang X, Smit JM: Dissecting the cell entry pathway of dengue virus by single-particle tracking in living cells. PLoS Pathog 2008, 4: e1000244. 10.1371/journal.ppat.1000244PubMedPubMedCentral
34.
Ewers H, Smith AE, Sbalzarini IF, Lilie H, Koumoutsakos P, Helenius A: Single-particle tracking of murine polyoma virus-like particles on live cells and artificial membranes. Proc Natl Acad Sci USA 2005, 102: 15110-15115. 10.1073/pnas.0504407102PubMedPubMedCentral
35.
Schelhaas M, Ewers H, Rajamaki M-L, Day PM, Schiller JT, Helenius A: Human papillomavirus type 16 entry: retrograde cell surface transport along actin-rich protrusions. PLoS Pathog 2008, 4: e1000148. 10.1371/journal.ppat.1000148PubMedPubMedCentral
36.
Brandenburg B, Lee LY, Lakadamyali M, Rust MJ, Zhuang X, Hogle JM: Imaging poliovirus entry in live cells. PLoS Biol 2007, 5: 1543-1555.
37.
Vaughan JC, Brandenburg B, Hogle JM, Zhuang X: Rapid actin-dependent viral motility in live cells. Biophys J 2009, 97: 1647-1656. 10.1016/j.bpj.2009.07.011PubMedPubMedCentral
38.
Huang B, Bates M, Zhuang X: Super-Resolution Fluorescence Microscopy. Annu Rev Biochem Volume 78 2009, 993-1016. Annual Review of Biochemistry
39.
Rust MJ, Bates M, Zhuang X: Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat Methods 2006, 3: 793-795. 10.1038/nmeth929PubMedPubMedCentral
40.
Betzig E, Patterson GH, Sougrat R, Lindwasser OW, Olenych S, Bonifacino JS, Davidson MW, Lippincott-Schwartz J, Hess HF: Imaging intracellular fluorescent proteins at nanometer resolution. Science 2006, 313: 1642-1645. 10.1126/science.1127344PubMed
41.
Gustafsson MGL: Nonlinear structured-illumination microscopy: wide-field fluorescence imaging with theoretically unlimited resolution. Proc Natl Acad Sci USA 2005, 102: 13081-13086. 10.1073/pnas.0406877102PubMedPubMedCentral
42.
Pereira CF, Rossy J, Owen DM, Mak J, Gaus K: HIV taken by STORM: super-resolution fluorescence microscopy of a viral infection. Virol J 2012, 9: 84. 10.1186/1743-422X-9-84PubMedPubMedCentral
43.
Rossman JS, Leser GP, Lamb RA: Filamentous influenza virus enters cells via macropinocytosis. J Virol 2012, 86: 10950-10960. 10.1128/JVI.05992-11PubMedPubMedCentral
44.
Subramaniam S, Bartesaghi A, Liu J, Bennett AE, Sougrat R: Electron tomography of viruses. Curr Opin Struct Biol 2007, 17: 596-602. 10.1016/j.sbi.2007.09.009PubMedPubMedCentral
45.
Grunewald K, Desai P, Winkler DC, Heymann JB, Belnap DM, Baumeister W, Steven AC: Three-dimensional structure of herpes simplex virus from cryo-electron tomography. Science 2003, 302: 1396-1398. 10.1126/science.1090284PubMed
46.
Forster F, Medalia O, Zauberman N, Baumeister W, Fass D: Retrovirus envelope protein complex structure in situ studied by cryo-electron tomography. Proc Natl Acad Sci USA 2005, 102: 4729-4734. 10.1073/pnas.0409178102PubMedPubMedCentral
47.
Cyrklaff M, Risco C, Fernandez JJ, Jimenez MV, Esteban M, Baumeister W, Carrascosa JL: Cryo-electron tomography of vaccinia virus. Proc Natl Acad Sci USA 2005, 102: 2772-2777. 10.1073/pnas.0409825102PubMedPubMedCentral
48.
Zanetti G, Briggs JAG, Gruenewald K, Sattentau QJ, Fuller SD: Cryo-electron tomographic structure of an immunodeficiency virus envelope complex in situ. PLoS Pathog 2006, 2: e83. 10.1371/journal.ppat.0020083PubMedPubMedCentral
49.
Zhu P, Liu J, Bess J, Chertova E, Lifson JD, Grise H, Ofek GA, Taylor KA, Roux KH: Distribution and three-dimensional structure of AIDS virus envelope spikes. Nature 2006, 441: 847-852. 10.1038/nature04817PubMed
50.
Harris A, Cardone G, Winkler DC, Heymann JB, Brecher M, White JM, Steven AC: Influenza virus pleiomorphy characterized by cryoelectron tomography. Proc Natl Acad Sci USA 2006, 103: 19123-19127. 10.1073/pnas.0607614103PubMedPubMedCentral
51.
Bharat TAM, Noda T, Riches JD, Kraehling V, Kolesnikova L, Becker S, Kawaoka Y, Briggs JAG: Structural dissection of Ebola virus and its assembly determinants using cryo-electron tomography. Proc Natl Acad Sci USA 2012, 109: 4275-4280.PubMedPubMedCentral
52.
Iwasaki K, Omura T: Electron tomography of the supramolecular structure of virus-infected cells. Curr Opin Struct Biol 2010, 20: 632-639. 10.1016/j.sbi.2010.08.007PubMed
53.
Sougrat R, Bartesaghi A, Lifson JD, Bennett AE, Bess JW, Zabransky DJ, Subramaniam S: Electron tomography of the contact between T cells and SIV/HIV-1: implications for viral entry. PLoS Pathog 2007, 3: 571-581.
54.
Maurer UE, Sodeik B, Gruenewald K: Native 3D intermediates of membrane fusion in herpes simplex virus 1 entry. Proc Natl Acad Sci USA 2008, 105: 10559-10564. 10.1073/pnas.0801674105PubMedPubMedCentral
55.
Peng L, Ryazantsev S, Sun R, Zhou ZH: Three-dimensional visualization of gammaherpesvirus life cycle in host cells by electron tomography. Structure 2010, 18: 47-58. 10.1016/j.str.2009.10.017PubMedPubMedCentral
56.
Cyrklaff M, Linaroudis A, Boicu M, Chlanda P, Baumeister W, Griffiths G, Krijnse-Locker J: Whole cell cryo-electron tomography reveals distinct disassembly intermediates of vaccinia virus. PLoS One 2007, 2: e420. 10.1371/journal.pone.0000420PubMedPubMedCentral
57.
Welsch S, Kolesnikova L, Kraehling V, Riches JD, Becker S, Briggs JAG: Electron tomography reveals the steps in filovirus budding. PLoS Pathog 2010, 6: e1000875. 10.1371/journal.ppat.1000875PubMedPubMedCentral
58.
Grove J, Marsh M: The cell biology of receptor-mediated virus entry. J Cell Biol 2011, 195: 1071-1082. 10.1083/jcb.201108131PubMedPubMedCentral
59.
Willis SH, Rux AH, Peng C, Whitbeck JC, Nicola AV, Lou H, Hou WF, Salvador L, Eisenberg RJ, Cohen GH: Examination of the kinetics of herpes simplex virus glycoprotein D binding to the herpesvirus entry mediator, using surface plasmon resonance. J Virol 1998, 72: 5937-5947.PubMedPubMedCentral
60.
Milne RSB, Hanna SL, Rux AH, Willis SH, Cohen GH, Eisenberg RJ: Function of herpes simplex virus type 1 gD mutants with different receptor-binding affinities in virus entry and fusion. J Virol 2003, 77: 8962-8972. 10.1128/JVI.77.16.8962-8972.2003PubMedPubMedCentral
61.
Alessandrini A, Facci P: AFM: a versatile tool in biophysics. Meas Sci Technol 2005, 16: R65-R92. 10.1088/0957-0233/16/6/R01
62.
Alessandrini A, Facci P: Unraveling lipid/protein interaction in model lipid bilayers by atomic force microscopy. J Mol Recognit 2011, 24: 387-396. 10.1002/jmr.1083PubMed
63.
Ovalle-Garcia E, Torres-Heredia JJ, Antillon A, Ortega-Blake I: Simultaneous determination of the elastic properties of the lipid bilayer by atomic force microscopy: bending, tension, and adhesion. J Phys Chem B 2011, 115: 4826-4833. 10.1021/jp111985zPubMed
64.
Cross SE, Jin Y-S, Rao J, Gimzewski JK: Nanomechanical analysis of cells from cancer patients. Nat Nanotechnol 2007, 2: 780-783. 10.1038/nnano.2007.388PubMed
65.
Iyer S, Gaikwad RM, Subba-Rao V, Woodworth CD, Sokolov I: Atomic force microscopy detects differences in the surface brush of normal and cancerous cells. Nat Nanotechnol 2009, 4: 389-393. 10.1038/nnano.2009.77PubMedPubMedCentral
66.
Wirtz D, Konstantopoulos K, Searson PC: The physics of cancer: the role of physical interactions and mechanical forces in metastasis. Nat Rev Cancer 2011, 11: 512-522. 10.1038/nrc3080PubMedPubMedCentral
67.
McDougal JS, Kennedy MS, Sligh JM, Cort SP, Mawle A, Nicholson JKA: Binding of HTLV-III/LAV to T4$^{+}$ T cells by a complex of the 110K viral protein and the T4 molecule. Science 1986, 231: 382-385. 10.1126/science.3001934PubMed
68.
Lasky LA, Nakamura G, Smith DH, Fennie C, Shimasaki C, Patzer E, Berman P, Gregory T, Capon DJ: Delineation of a region of the human immunodeficiency virus type 1 gp120 glycoprotein critical for interaction with the CD4 receptor. Cell 1987, 50: 975-985. 10.1016/0092-8674(87)90524-1PubMed
69.
Chang MI, Panorchan P, Dobrowsky TM, Tseng Y, Wirtz D: Single-molecule analysis of human immunodeficiency virus type 1 gp120-receptor interactions in living cells. J Virol 2005, 79: 14748-14755. 10.1128/JVI.79.23.14748-14755.2005PubMedPubMedCentral
70.
Dobrowsky TM, Zhou Y, Sun SX, Siliciano RF, Wirtz D: Monitoring early fusion dynamics of human immunodeficiency virus type 1 at single-molecule resolution. J Virol 2008, 82: 7022-7033. 10.1128/JVI.00053-08PubMedPubMedCentral
71.
van Effenterre D, Roux D: Adhesion of colloids on a cell surface in competition for mobile receptors. Europhys Lett 2003, 64: 543-549. 10.1209/epl/i2003-00268-x
72.
Gao HJ, Shi WD, Freund LB: Mechanics of receptor-mediated endocytosis. Proc Natl Acad Sci USA 2005, 102: 9469-9474. 10.1073/pnas.0503879102PubMedPubMedCentral
73.
Aoyama Y, Kanamori T, Nakai T, Sasaki T, Horiuchi S, Sando S, Niidome T: Artificial viruses and their application to gene delivery. Size-controlled gene coating with glycocluster nanoparticles. J Am Chem Soc 2003, 125: 3455-3457. 10.1021/ja029608tPubMed
74.
Nakai T, Kanamori T, Sando S, Aoyama Y: Remarkably size-regulated cell invasion by artificial viruses. Saccharide-dependent self-aggregation of glycoviruses and its consequences in glycoviral gene delivery. J Am Chem Soc 2003, 125: 8465-8475. 10.1021/ja035636fPubMed
75.
Osaki F, Kanamori T, Sando S, Sera T, Aoyama Y: A quantum dot conjugated sugar ball and its cellular uptake on the size effects of endocytosis in the subviral region. J Am Chem Soc 2004, 126: 6520-6521. 10.1021/ja048792aPubMed
76.
Yi X, Shi X, Gao H: Cellular uptake of elastic nanoparticles. Phys Rev Lett 2011, 107: 098101.PubMed
77.
Sun SX, Wirtz D: Mechanics of enveloped virus entry into host cells. Biophys J 2006, 90: L10-L12. 10.1529/biophysj.105.074203PubMedPubMedCentral
78.
Li L, Liu X, Zhou Y, Wang J: On resistance to virus entry into host cells. Biophys J 2012, 102: 2230-2233. 10.1016/j.bpj.2012.03.066PubMedPubMedCentral
79.
Decuzzi P, Ferrari M: The role of specific and non-specific interactions in receptor-mediated endocytosis of nanoparticles. Biomaterials 2007, 28: 2915-2922. 10.1016/j.biomaterials.2007.02.013PubMed
80.
Decuzzi P, Ferrari M: The receptor-mediated endocytosis of nonspherical particles. Biophys J 2008, 94: 3790-3797. 10.1529/biophysj.107.120238PubMedPubMedCentral
81.
Zhang S, Li J, Lykotrafitis G, Bao G, Suresh S: Size-dependent endocytosis of nanoparticles. Adv Mater 2009, 21: 419-424. 10.1002/adma.200801393PubMedPubMedCentral
82.
Yuan H, Huang C, Zhang S: Virus-inspired design principles of nanoparticle-based bioagents. PLoS One 2010, 5: e13495. 10.1371/journal.pone.0013495PubMedPubMedCentral
83.
Yuan H, Zhang S: Effects of particle size and ligand density on the kinetics of receptor-mediated endocytosis of nanoparticles. Appl Phys Lett 2010, 96: 033704. 10.1063/1.3293303
84.
English TJ, Hammer DA: Brownian adhesive dynamics (BRAD) for simulating the receptor-mediated binding of viruses. Biophys J 2004, 86: 3359-3372. 10.1529/biophysj.103.027813PubMedPubMedCentral
85.
English TJ, Hammer DA: The effect of cellular receptor diffusion on receptor-mediated viral binding using brownian adhesive dynamics (BRAD) simulations. Biophys J 2005, 88: 1666-1675. 10.1529/biophysj.104.047043PubMedPubMedCentral
86.
Trister AD, Hammer DA: Role of gp120 trimerization on HIV binding elucidated with brownian adhesive dynamics. Biophys J 2008, 95: 40-53. 10.1529/biophysj.107.118430PubMedPubMedCentral
87.
Dobrowsky TM, Daniels BR, Siliciano RF, Sun SX, Wirtz D: Organization of cellular receptors into a nanoscale junction during HIV-1 adhesion. PLoS Comput Biol 2010, 6: e1000855. 10.1371/journal.pcbi.1000855PubMedPubMedCentral
88.
Liu J, Weller GER, Zern B, Ayyaswamy PS, Eckmann DM, Muzykantov VR, Radhakrishnan R: Computational model for nanocarrier binding to endothelium validated using in vivo, in vitro, and atomic force microscopy experiments. Proc Natl Acad Sci USA 2010, 107: 16530-16535. 10.1073/pnas.1006611107PubMedPubMedCentral
89.
Liu J, Agrawal NJ, Calderon A, Ayyaswamy PS, Eckmann DM, Radhakrishnan R: Multivalent binding of nanocarrier to endothelial cells under shear flow. Biophys J 2011, 101: 319-326. 10.1016/j.bpj.2011.05.063PubMedPubMedCentral
90.
Liu J, Bradley R, Eckmann DM, Ayyaswamy PS, Radhakrishnan R: Multiscale modeling of functionalized nanocarriers in targeted drug delivery. Curr Nanosci 2011, 7: 727-735. 10.2174/157341311797483826PubMedPubMedCentral
91.
Ramakrishnan N, Kumar PBS, Ipsen JH: Monte Carlo simulations of fluid vesicles with in-plane orientational ordering. Phys Rev E 2010, 81: 041922.
92.
Liu J, Tourdot R, Ramanan V, Agrawal NJ, Radhakrishanan R: Mesoscale simulations of curvature-inducing protein partitioning on lipid bilayer membranes in the presence of mean curvature fields. Mol Phys 2012, 110: 1127-1137. 10.1080/00268976.2012.664661PubMedPubMedCentral
93.
Vacha R, Martinez-Veracoechea FJ, Frenkel D: Receptor-mediated endocytosis of nanoparticles of various shapes. Nano Lett 2011, 11: 5391-5395. 10.1021/nl2030213PubMed
94.
Shi X, von dem Bussche A, Hurt RH, Kane AB, Gao H: Cell entry of one-dimensional nanomaterials occurs by tip recognition and rotation. Nat Nanotechnol 2011, 6: 714-719. 10.1038/nnano.2011.151PubMedPubMedCentral
95.
Yue T, Zhang X: Molecular understanding of receptor-mediated membrane responses to ligand-coated nanoparticles. Soft Matter 2011, 7: 9104-9112. 10.1039/c1sm05398a
96.
Li Y, Yue T, Yang K, Zhang X: Molecular modeling of the relationship between nanoparticle shape anisotropy and endocytosis kinetics. Biomaterials 2012, 33: 4965-4973. 10.1016/j.biomaterials.2012.03.044PubMed
97.
Ding H-m, Ma Y-q: Role of physicochemical properties of coating ligands in receptor-mediated endocytosis of nanoparticles. Biomaterials 2012, 33: 5798-5802. 10.1016/j.biomaterials.2012.04.055PubMed
98.
Yue T, Zhang X: Molecular modeling of the pathways of vesicle-membrane interaction. Soft Matter 2013, 9: 559-569. 10.1039/c2sm26940f
99.
Teissier E, Penin F, Pecheur E-I: Targeting cell entry of enveloped viruses as an antiviral strategy. Molecules 2011, 16: 221-250.
100.
O’Connell ST, Thompson PA: Molecular dynamics-continuum hybrid computations: a tool for studying complex fluid flows. Phys Rev E 1995, 52: R5792-R5795. 10.1103/PhysRevE.52.R5792
101.
Hadjiconstaninou NG, Patera AT: Heterogeneous atomistic-continuum representations for dense fluid systems. Int J Mod Phys C 1997, 8: 967-976. 10.1142/S0129183197000837
102.
Flekkoy EG, Wagner G, Feder J: Hybrid model for combined particle and continuum dynamics. Europhys Lett 2000, 52: 271-276. 10.1209/epl/i2000-00434-8
103.
Engquist B, Li X, Ren W, Vanden-Eijnden E, E W: Heterogeneous multiscale methods: A review. Commun Comput Phys 2007, 2: 367-450.
104.
Liu J, Chen SY, Nie XB, Robbins MO: A continuum-atomistic simulation of heat transfer in micro- and nano-flows. J Comput Phys 2007, 227: 279-291. 10.1016/j.jcp.2007.07.014
Metadata
Title
Multiscale perspectives of virus entry via endocytosis
Authors
Eric Barrow
Anthony V Nicola
Jin Liu
Publication date
01-12-2013
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2013
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/1743-422X-10-177

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