Uncoating of human rhinoviruses

Reviews in Medical Virology

Volumn 20, Issue 5, 2010, Pages 281-297

  Fuchs, Renate ^a   Blaas, Dieter ^b  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

INTERCELLULAR ADHESION MOLECULE 1; LIPOSOME; PROTEIN VP1;

CELL MIGRATION; ENDOSOME; HUMAN; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; REVIEW; RHINOVIRUS; RNA VIRUS; VIRUS ENTRY;

CELL MEMBRANE; ENDOCYTOSIS; ENDOSOMES; HUMANS; MODELS, BIOLOGICAL; PROTEIN BINDING; RECEPTORS, VIRUS; RHINOVIRUS; RNA, VIRAL; VIRUS ATTACHMENT; VIRUS INTERNALIZATION;

EID: 77956625541     PISSN: 10529276     EISSN: 10991654     Source Type: Journal    
DOI: 10.1002/rmv.654     Document Type: Review

References (153)

1. Falanga A, Cantisani M, Pedone C, Galdiero S. Membrane fusion and fission: enveloped viruses. Protein Pept Lett 2009; 16: 751-759.
2. Harrison SC. Viral membrane fusion. Nat Struct Mol Biol 2008; 15: 690-698.
3. Mudhakir D, Harashima H. Learning from the viral journey: how to enter cells and how to overcome intracellular barriers to reach the nucleus. AAPS J 2009; 11: 65-77.
4. Banerjee M, Johnson JE. Activation, exposure and penetration of virally encoded, membrane-active polypeptides during non-enveloped virus entry. Curr Protein Pept Sci 2008; 9: 16-27.
5. Tsai B. Penetration of nonenveloped viruses into the cytoplasm. Annu Rev Cell Dev Biol 2007; 23: 23-43.
6. Prchla E, Plank C, Wagner E, Blaas D, Fuchs R. Virus-mediated release of endosomal content in vitro: different behavior of adenovirus and rhinovirus serotype 2. J Cell Biol 1995; 131: 111-123.
7. Odegard AL, Kwan MH, Walukiewicz HE, Banerjee M, Schneemann A, Johnson JE. Low endocytic pH and capsid protein autocleavage are critical components of Flock House virus cell entry. J Virol 2009; 83: 8628-8637.
8. Lee WM, Monroe SS, Rueckert RR. Role of maturation cleavage in infectivity of picornaviruses: activation of an infectosome. J Virol 1993; 67: 2110-2122.
9. Meier O, Greber UF. Adenovirus endocytosis. J Gene Med 2004; 6(Suppl 1): S152-S163.
10. Leopold PL, Crystal RG. Intracellular trafficking of adenovirus: many means to many ends. Adv Drug Deliv Rev 2007; 59: 810-821.
11. Wickham TJ, Filardo EJ, Cheresh DA, Nemerow GR. Integrin alpha v beta 5 selectively promotes adenovirus mediated cell membrane permeabilization. J Cell Biol 1994; 127: 257-264. (Pubitemid 2147586)
12. Whittaker GR, Kann M, Helenius A. Viral entry into the nucleus. Annu Rev Cell Dev Biol 2000; 16: 627-651.
13. Wagner E. Effects of membrane-active agents in gene delivery. J Controlled Release 1998; 53: 155-158.
14. Zauner W, Blaas D, Kuechler E, Wagner E. Rhinovirus-mediated endosomal release of transfection complexes. J Virol 1995; 69: 1085-1092.
15. Blumenthal R, Seth P, Willingham MC, Pastan I. pH-dependent lysis of liposomes by adenovirus. Biochemistry 1986; 25: 2231-2237.
16. Seth P. Mechanism of adenovirus-mediated endosome lysis: role of the intact adenovirus capsid structure. Biochem Biophys Res Commun 1994; 205: 1318-1324.
17. Gastaldelli M, Imelli N, Boucke K, Amstutz B, Meier O, Greber UF. Infectious adenovirus type 2 transport through early but not late endosomes. Traffic 2008; 9: 2265-2278.
18. Seth P, Willingham M, Pastan I. Adenovirus-dependent release of 51Cr from KB cells at an acidic pH. J Biol Chem 1984; 259: 14350-14353. (Pubitemid 15222247)
19. Everitt E, Rodriguez E. Adenovirus cellular receptor site recirculation of HeLa cells upon receptor-mediated endocytosis is not low pH-dependent. Arch Virol 1999; 144: 787-795.
20. Brabec M, Schober D, Wagner E, et al. Opening of size-selective pores in endosomes during human rhinovirus serotype 2 in vivo uncoating monitored by single-organelle flow analysis. J Virol 2005; 79: 1008-1016.
21. Farr GA, Zhang LG, Tattersall P. Parvoviral virions deploy a capsid-tethered lipolytic enzyme to breach the endosomal membrane during cell entry. Proc Natl Acad Sci USA 2005; 102: 17148-17153. (Pubitemid 41692698)
22. Suikkanen S, Antila M, Jaatinen A, Vihinen-Ranta M, Vuento M. Release of canine parvovirus from endocytic vesicles. Virology 2003; 316: 267-280.
23. Mani B, Baltzer C, Valle N, Almendral JM, Kempf C, Ros C. Low pH-dependent endosomal processing of the incoming parvovirus minute virus of mice virion leads to externalization of the VP1 N-terminal sequence (N-VP1), N-VP2 cleavage, and uncoating of the full-length genome. J Virol 2006; 80: 1015-1024.
24. Bothner B, Dong X, Bibbs L, Johnson J, Siuzdak G. Evidence of viral capsid dynamics using limited proteolysis and mass spectrometry. J Biol Chem 1998; 273: 673-676. (Pubitemid 28049149)
25. Lewis JK, Bothner B, Smith TJ, Siuzdak G. Antiviral agent blocks breathing of the common cold virus. Proc Natl Acad Sci USA 1998; 95: 6774-6778.
26. Bong DT, Steinem C, Janshoff A, Johnson JE, Reza Ghadiri M. A highly membrane-active peptide in Flock House virus: implications for the mechanism of nodavirus infection. Chem Biol 1999; 6: 473-481.
27. Banerjee M, Khayat R, Walukiewicz HE, Odegard AL, Schneemann A, Johnson JE. Dissecting the functional domains of a nonenveloped virus membrane penetration peptide. J Virol 2009; 83: 6929-6933.
28. Maia LF, Soares MR, Valente AP, et al. Structure of a membrane-binding domain from a non-enveloped animal virus: insights into the mechanism of membrane permeability and cellular entry. J Biol Chem 2006; 281: 29278-29286.
29. Racaniello VR. The poliovirus receptor: a hook, or an unzipper? Structure 1996; 4: 769-773.
30. Hogle JM. Poliovirus cell entry: common structural themes in viral cell entry pathways. Annu Rev Microbiol 2002; 56: 677-702.
31. Tsang SK, McDermott BM, Racaniello VR, Hogle JM. Kinetic analysis of the effect of poliovirus receptor on viral uncoating: the receptor as a catalyst. J Virol 2001; 75: 4984-4989.
32. Fricks C, Hogle J. Cell-induced conformational change in poliovirus: externalization of the amino terminus of VP1 is responsible for liposome binding. J Virol 1990; 64: 1934-1945. (Pubitemid 20148434)
33. Tosteson MT, Chow M. Characterization of the ion channels formed by poliovirus in planar lipid membranes. J Virol 1997; 71: 507-511.
34. Danthi P, Tosteson M, Li QH, Chow M. Genome delivery and ion channel properties are altered in VP4mutants of poliovirus. J Virol 2003; 77: 5266-5274.
35. Krausslich HG, Holscher C, Reuer Q, Harber J, Wimmer E. Myristoylation of the poliovirus polyprotein is required for proteolytic processing of the capsid and for viral infectivity. J Virol 1990; 64: 2433-2436. (Pubitemid 20148498)
36. Marc D, Masson G, Girard M, Vanderwerf S. Lack of myristoylation of poliovirus capsid polypeptide Vp0 prevents the formation of virions or results in the assembly of noninfectious virus particles. J Virol 1990; 64: 4099-4107.
37. Marc D, Drugeon G, Haenni AL, Girard M, van der Werf S. Role of myristoylation of poliovirus capsid protein VP4 as determined by site-directed mutagenesis of its N-terminal sequence. EMBO J 1989; 8: 2661-2668. (Pubitemid 19273351)
38. Tuthill TJ, Bubeck D, Rowlands DJ, Hogle JM. Characterization of early steps in the poliovirus infection process: receptor-decorated liposomes induce conversion of the virus to membrane-anchored entry-intermediate particles. J Virol 2006; 80: 172-180.
39. Bostina M, Bubeck D, Schwartz C, Nicastro D, Filman DJ, Hogle JM. Single particle cryoelectron tomography characterization of the structure and structural variability of poliovirus-receptor-membrane complex at 30 A resolution. J Struct Biol 2007; 160: 200-210.
40. Bubeck D, Filman DJ, Hogle JM. Cryo-electron microscopy reconstruction of a poliovirus-receptor-membrane complex. Nat Struct Mol Biol 2005; 12: 615-618. (Pubitemid 40980812)
41. Belnap DM, Filman DJ, Trus BL, et al. Molecular tectonic model of virus structural transitions: the putative cell entry states of poliovirus. J Virol 2000; 74: 1342-1354.
42. Ketterlinus R, Wiegers K. Mapping of antigenic domains in poliovirus VP1 involved in structural rearrangements during virus morphogenesis and antigenic alterations of the virion. Virology 1994; 204: 27-37.
43. Brandenburg B, Lee LY, Lakadamyali M, Rust MJ, Zhuang X, Hogle JM. Imaging poliovirus entry in live cells. PLoS Biol 2007; 5: e183.
44. Kronenberger P, Vrijsen R, Boeye A. Intracellular proteolysis of poliovirus eclipse particles is abortive. J Gen Virol 1994; 75: 573-580. (Pubitemid 24091813)
45. Kronenberger P, Schober D, Prchla E, Blaas D, Fuchs R. Use of free-flow electrophoresis for the analysis of cellular uptake of picornaviruses. Electrophoresis 1997; 18: 2531-2536.
46. Hughes JH, Chema S, Lin N, Conant RM, Hamparian VV. Acid lability of rhinoviruses: loss of C and D antigenicity after treatment at pH 3.0. J Immunol 1974; 112: 919-925.
47. Yin FH, Knight CG. In vivo and in vitro synthesis of human rhinovirus type 2 ribonucleic acid. J Virol 1972; 10: 93-98.
48. Rossmann M, Arnold E, Erickson J, et al. Structure of a human common cold virus and functional relationship to other picornaviruses. Nature 1985; 317: 145-153. (Pubitemid 16243130)
49. Verdaguer N, Blaas D, Fita I. Structure of human rhinovirus serotype 2 (HRV2). J Mol Biol 2000; 300: 1179-1194.
50. Palmenberg AC, Spiro D, Kuzmickas R, et al. Sequencing and analyses of all known human rhinovirus genomes reveal structure and evolution. Science 2009; 324: 55-59.
51. Heikkinen T, Jarvinen A. The common cold. Lancet 2003; 361: 51-59.
52. Hayden FG. Rhinovirus and the lower respiratory tract. Rev Med Virol 2004; 14: 17-31.
53. Peltola V, Waris M, Osterback R, Susi P, Hyypia T, Ruuskanen O. Clinical effects of rhinovirus infections. J Clin Virol 2008; 43: 411-414.
54. Fendrick AM. Viral respiratory infections due to rhinoviruses: current knowledge, new developments. Am J Ther 2003; 10: 193-202.
55. Colonno RJ, Condra JH, Mizutani S, Callahan PL, Davies ME, Murcko MA. Evidence for the direct involvement of the rhinovirus canyon in receptor binding. Proc Natl Acad Sci USA 1988; 85: 5449-5453.
56. Hughes JH, Thomas DC, Hamparian VV, Cramblett HG. Acid liability of rhinovirus type 14: effect of pH, time, and temperature. Proc Soc Exp Biol Med 1973; 144: 555-560.
57. Wisdom A, McWilliam Leitch EC, Gaunt E, Harvala H, Simmonds P. Screening respiratory samples for human rhinoviruses (HRV) and enteroviruses: comprehensive VP4/2-typing reveals high incidence and genetic diversity of HRV species C. J Clin Microbiol 2009; 47: 3958-3967.
58. Lau SK, Yip CC, Tsoi HW, et al. Clinical features and complete genome characterization of a distinct human rhinovirus (HRV) genetic cluster, probably representing a previously undetected HRV species, HRV-C, associated with acute respiratory illness in children. J Clin Microbiol 2007; 45: 3655-3664.
59. Vlasak M, Roivainen M, Reithmayer M, et al. The minor receptor group of human rhinovirus (HRV) includes HRV23 and HRV25, but the presence of a lysine in the VP1 HI loop is not sufficient for receptor binding. J Virol 2005; 79: 7389-7395.
60. Uncapher CR, Dewitt CM, Colonno RJ. The major and minor group receptor families contain all but one human rhinovirus serotype. Virology 1991; 180: 814-817.
61. Reischl A, Reithmayer M, Winsauer G, Moser R, Gosler I, Blaas D. Viral evolution toward change in receptor usage: adaptation of a major group human rhinovirus to grow in ICAM-1-negative cells. J Virol 2001; 75: 9312-9319.
62. Vlasak M, Goesler I, Blaas D. Human rhinovirus type 89 variants use heparan sulfate proteoglycan for cell attachment. J Virol 2005; 79: 5963-5970. (Pubitemid 40617202)
63. Khan AG, Pichler J, Rosemann A, Blaas D. Human rhinovirus type 54 infection via heparan sulfate is less efficient and strictly dependent on low endosomal pH. J Virol 2007; 81: 4625-4632.
64. McErlean P, Shackelton LA, Andrews E, et al. Distinguishing molecular features and clinical characteristics of a putative new rhinovirus species, human rhinovirus C (HRV C). PLoS ONE 2008; 3: e1847.
65. Pitkaranta A, Puhakka T, Makela MJ, Ruuskanen O, Carpen O, Vaheri A. Detection of rhinovirus RNAin middle turbinate of patients with common colds by in situ hybridization. J Med Virol 2003; 70: 319-323. (Pubitemid 36520646)
66. Arruda E, Boyle TR, Winther B, Pevear DC, Gwaltney JM, Jr, Hayden FG. Localization of human rhinovirus replication in the upper respiratory tract by in situ hybridization. J Infect Dis 1995; 171: 1329-1333.
67. Gern JE, Galagan DM, Jarjour NN, Dick EC, Busse WW. Detection of rhinovirus RNA in lower airway cells during experimentally induced infection. Am J Respir Crit Care Med 1997; 155: 1159-1161.
68. Bardin PG, Johnston SL, Sanderson G, et al. Detection of rhinovirus infection of the nasal mucosa by oligonucleotide in situ hybridization. Am J Respir Cell Mol Biol 1994; 10: 207-213.
69. Wright PF, Deatly AM, Karron RA, et al. Comparison of results of detection of rhinovirus by PCR and viral culture in human nasal wash specimens from subjects with and without clinical symptoms of respiratory illness. J Clin Microbiol 2007; 45: 2126-2129.
70. Mosser AG, Brockman-Schneider R, Amineva S, et al. Similar frequency of rhinovirus-infectible cells in upper and lower airway epithelium. J Infect Dis 2002; 185: 734-743.
71. de Arruda Er, Mifflin TE, Gwaltney JM, Jr, Winther B, Hayden FG. Localization of rhinovirus replication in vitro with in situ hybridization. J Med Virol 1991; 34: 38-44.
72. Winther B, Greve JM, Gwaltney JM, et al. Surface expression of intercellular adhesion molecule 1 on epithelial cells in the human adenoid. J Infect Diseases 1997; 176: 523-525.
73. Winther B, Arruda E, Witek TJ, et al. Expression of ICAM-1 in nasal epithelium and levels of soluble ICAM-1 in nasal lavage fluid during human experimental rhinovirus infection. Arch Otolaryngol Head Neck Surg 2002; 128: 131-136. (Pubitemid 34132166)
74. Jakiela B, Brockman-Schneider R, Amineva S, Lee WM, Gern JE. Basal cells of differentiated bronchial epithelium are more susceptible to rhinovirus infection. Am J Respir Cell Mol Biol 2008; 38: 517-523.
75. Lopez-Souza N, Dolganov G, Dubin R, et al. Resistance of differentiated human airway epithelium to infection by rhinovirus. Am J Physiol Lung Cell Mol Physiol 2004; 286: L373-L381.
76. Suzuki T, Yamaya M, Sekizawa K, et al. Bafilomycin A(1) inhibits rhinovirus infection in human airway epithelium: effects on endosome and ICAM-1. Am J Physiol Lung Cell Mol Physiol 2001; 280: L1115-L1127.
77. Suzuki T, Yamaya M, Kamanaka M, et al. Sasaki H. Type 2 rhinovirus infection of cultured human tracheal epithelial cells: role of LDL receptor. Am J Physiol Lung Cell Mol Physiol 2001; 280: L409-L420. (Pubitemid 33780201)
78. Khan AG, Pickl-Herk A, Gajdzik L, Marlovits T, Fuchs R, Blaas D. Human rhinovirus 14 enters RD cells expressing ICAM-1 by a non-clathrin, noncaveolin dependent pathway. J Virol 2010; Feb 3 [epub ahead of print] (in press).
79. DeTulleo L, Kirchhausen T. The clathrin endocytic pathway in viral infection. EMBO J 1998; 17: 4585-4593.
80. Grunert H, Wolf K, Langner K, Sawitzky D, Habermehl K, Zeichhardt H. Internalization of human rhinovirus 14 into HeLa and ICAM-1-transfected BHK cells. Med Microbiol Immunol Berl 1997; 186: 1-9.
81. Casasnovas M, Springer TA. Kinetics and thermodynamics of virus binding to receptor. Studies with rhinovirus, intercellular adhesion molecule-1 (ICAM-1), and surface plasmon resonance. J Biol Chem 1995; 270: 13216-13224.
82. Hoover-Litty H, Greve JM. Formation of rhinovirus-soluble ICAM-1 complexes and conformational changes in the virion. J Virol 1993; 67: 390-397. (Pubitemid 23003002)
83. Giranda V, Heinz B, Oliveira M, et al. Acid-induced structural changes in human rhinovirus 14: possible role in uncoating. Proc Natl Acad Sci USA 1992; 89: 10213-10217.
84. Skern T, Torgersen H, Auer H, Kuechler E, Blaas D. Human rhinovirus mutants resistant to low pH. Virology 1991; 183: 757-763.
85. Arruda E, Crump CE, Hayden FG. In vitro selection of human rhinovirus relatively resistant to soluble intercellular adhesion molecule-1. Antimicrob Agents Chemother 1994; 38: 66-70.
86. Nurani G, Lindqvist B, Casasnovas JM. Receptor priming of major group human rhinoviruses for uncoating and entry at mild low-pH environments. J Virol 2003; 77: 11985-11991.
87. Crump CE, Arruda E, Hayden FG. In vitro inhibitory activity of soluble ICAM-1 for the numbered serotypes of human rhinovirus. Antiviral Chem Chemother 1993; 4: 323-327.
88. Register RB, Uncapher CR, Naylor AM, Lineberger DW, Colonno RJ. Human-murine chimeras of ICAM-1 identify amino acid residues critical for rhinovirus and antibody binding. J Virol 1991; 65: 6589-6596.
89. Laine P, Blomqvist S, Savolainen C, Andries K, Hovi T. Alignment of capsid protein VP1 sequences of all human rhinovirus prototype strains: conserved motifs and functional domains. J Gen Virol 2006; 87: 129-138.
90. Olson NH, Kolatkar PR, Oliveira MA, et al. Structure of a human rhinovirus complexed with its receptor molecule. Proc Natl Acad Sci USA 1993; 90: 507-511.
91. Kolatkar PR, Bella J, Olson NH, Bator CM, Baker TS, Rossmann MG. Structural studies of two rhinovirus serotypes complexed with fragments of their cellular receptor. EMBO J 1999; 18: 6249-6259. (Pubitemid 29533229)
92. Casasnovas JM. The dynamics of receptor recognition by human rhinoviruses. Trends Microbiol 2000; 8: 251-254.
93. Xing L, Casasnovas JM, Cheng RH. Structural analysis of human rhinovirus complexed with ICAM-1 reveals the dynamics of receptor-mediated virus uncoating. J Virol 2003; 77: 6101-6107.
94. Hewat EA, Neumann E, Blaas D. The concerted conformational changes during human rhinovirus 2 uncoating. Mol Cell 2002; 10: 317-326. (Pubitemid 35007346)
95. Hewat EA, Blaas D. Cryoelectron microscopy analysis of the structural changes associated with human rhinovirus type 14 uncoating. J Virol 2004; 78: 2935-2942.
96. Lonberg-Holm K, Yin FH. Antigenic determinants of infective and inactivated human rhinovirus type 2. J Virol 1973; 12: 114-123.
97. Schober D, Kronenberger P, Prchla E, Blaas D, Fuchs R. Major and minor receptor group human rhinoviruses penetrate from endosomes by different mechanisms. J Virol 1998; 72: 1354-1364. (Pubitemid 28116921)
98. Lonberg-Holm K, Korant BD. Early interaction of rhinoviruses with host cells. J Virol 1972; 9: 29-40.
99. Springer TA. Adhesion receptors of the immune system. Nature 1990; 346: 425-434.
100. Xiao C, Bator-Kelly CM, Rieder E, et al. The crystal structure of coxsackievirus A21 and its interaction with ICAM-1. Structure 2005; 13: 1019-1033.
101. Xing L, Tjarnlund K, Lindqvist B, et al. Distinct cellular receptor interactions in poliovirus and rhinoviruses. EMBO J 2000; 19: 1207-1216.
102. Strickland DK, Gonias SL, Argraves WS. Diverse roles for the LDL receptor family. Trends Endocrinol Metab 2002; 13: 66-74.
103. Schneider WJ, Nimpf J. LDL receptor relatives at the crossroad of endocytosis and signaling. Cell Mol Life Sci 2003; 60: 892-903. (Pubitemid 36735120)
104. Snyers L, Zwickl H, Blaas D. Human rhinovirus type 2 is internalized by clathrin-mediated endocytosis. J Virol 2003; 77: 5360-5369.
105. Bayer N, Schober D, Huttinger M, Blaas D, Fuchs R. Inhibition of clathrin-dependent endocytosis has multiple effects on human rhinovirus serotype 2 cell entry. J Biol Chem 2001; 276: 3952-3962. (Pubitemid 33645860)
106. Huber M, Brabec M, Bayer N, Blaas D, Fuchs R. Elevated endosomal pH in HeLa cells overexpressing mutant dynamin can affect infection by pH-sensitive viruses. Traffic 2001; 2: 727-736.
107. Dreschers S, Franz P, Dumitru C, Wilker B, Jahnke K, Gulbins E. Infections with human rhinovirus induce the formation of distinct functional membrane domains. Cell Physiol Biochem 2007; 20: 241-254.
108. Grassme H, Riehle A, Wilker B, Gulbins E. Rhinoviruses infect human epithelial cells via ceramide-enriched membrane platforms. J Biol Chem 2005; 280: 26256-26262. (Pubitemid 41022223)
109. Bayer N, Schober D, Prchla E, Murphy RF, Blaas D, Fuchs R. Effect of bafilomycin A1 and nocodazole on endocytic transport in HeLa cells: implications for viral uncoating and infection. J Virol 1998; 72: 9645-9655.
110. Brabec M, Blaas D, Fuchs R. Wortmannin delays transfer of human rhinovirus serotype 2 to late endocytic compartments. Biochem Biophys Res Commun 2006; 348: 741-749.
111. Konecsni T, Berka U, Pickl-Herk A, et al. Low pH triggered beta-propeller switch of the low-density lipoprotein receptor assists rhinovirus infection. J Virol 2009; 83: 10922-10930.
112. Prchla E, Kuechler E, Blaas D, Fuchs R. Uncoating of human rhinovirus serotype 2 from late endosomes. J Virol 1994; 68: 3713-3723. (Pubitemid 24177396)
113. Baravalle G, Schober D, Huber M, Bayer N, Murphy RF, Fuchs R. Transferrin recycling and dextran transport to lysosomes is differentially affected by bafilomycin, nocodazole, and low temperature. Cell Tissue Res 2005; 320: 99-113.
114. Hofer F, Gruenberger M, Kowalski H, et al. Members of the low densitylipoprotein receptor family mediate cell entry of a minor-group common cold virus. Proc Nat Acad Sci USA 1994; 91: 1839-1842.
115. Oka K, Ishimura-Oka K, Chu MJ, et al. Mouse very-low- density-lipoprotein receptor (VLDLR) cDNA cloning, tissue-specific expression and evolutionary relationship with the low-density-lipoprotein receptor. Eur J Biochem 1994; 224: 975-982. (Pubitemid 24288861)
116. Konecsni T, Kremser L, Snyers L, et al. Twelve receptor molecules attach per viral particle of human rhinovirus serotype 2 via multiple modules. FEBS Lett 2004; 568: 99-104.
117. Moser R, Snyers L, Wruss J, et al. Neutralization of a common cold virus by concatemers of the third ligand binding module of the VLDL-receptor strongly depends on the number of modules. Virology 2005; 338: 259-269.
118. Wruss J, Runzler D, Steiger C, Chiba P, Kohler G, Blaas D. Attachment of VLDL receptors to an icosahedral virus along the 5-fold symmetry axis: multiple binding modes evidenced by fluorescence correlation spectroscopy. Biochemistry 2007; 46: 6331-6339. (Pubitemid 46842876)
119. Laschober C, Wruss J, Blaas D, Szymanski WW, Allmaier G. Gas-phase electrophoretic molecular mobility analysis of size and stoichiometry of complexes of a common cold virus with antibody and soluble receptor molecules. Anal Chem 2008; 80: 2261-2264.
120. Rankl C, Kienberger F, Wildling L, et al. Multiple receptors involved in human rhinovirus attachment to live cells. Proc Natl Acad Sci USA 2008; 105: 17778-17783.
121. Querol-Audi J, Konecsni T, Pous J, et al. Minor group human rhinovirus-receptor interactions: geometry of multimodular attachment and basis of recognition. FEBS Lett 2009; 583: 235-240.
122. Wruss J, Pollheimer PD, Meindl I, et al. Conformation of Receptor Adopted upon Interaction with Virus Revealed by Site-Specific Fluorescence Quenchers and FRET Analysis. J Am Chem Soc 2009; 131: 5478-5482.
123. Verdaguer N, Fita I, Reithmayer M, Moser R, Blaas D. X-ray structure of a minor group human rhinovirus bound to a fragment of its cellular receptor protein. Nat Struct Mol Biol 2004; 11: 429-434.
124. Nicodemou A, Petsch M, Konecsni T, et al. Rhinovirus- stabilizing activity of artificial VLDL-receptor variants defines a new mechanism for virus neutralization by soluble receptors. FEBS Lett 2005; 579: 5507-5511. (Pubitemid 41455622)
125. Rudenko G, Henry L, Henderson K, et al. Structure of the LDL receptor extracellular domain at endosomal pH. Science 2002; 298: 2353-2358.
126. Rudenko G, Deisenhofer J. The low-density lipoprotein receptor: ligands, debates and lore. Curr Opin Struct Biol 2003; 13: 683-689.
127. Brabec M, Baravalle G, Blaas D, Fuchs R. Conformational changes, plasma membrane penetration, and infection by human rhinovirus type 2: role of receptors and low pH. J Virol 2003; 77: 5370-5377. (Pubitemid 36460951)
128. Baravalle G, Brabec M, Snyers L, Blaas D, Fuchs R. Human rhinovirus type 2-antibody complexes enter and infect cells via Fc-gamma receptor IIB1. J Virol 2004; 78: 2729-2737.
129. Berka U, Khan A, Blaas D, Fuchs R. Human rhinovirus type 2 uncoating at the plasma membrane is not affected by a pH gradient but is affected by the membrane potential. J Virol 2009; 83: 3778-3787.
130. Brabec-Zaruba M, Pfanzagl B, Blaas D, Fuchs R. Site of human rhinovirus RNA uncoating revealed by fluorescent in situ hybridization. J Virol 2009; 83: 3770-3777.
131. Neubauer C, Frasel L, Kuechler E, Blaas D. Mechanism of entry of human rhinovirus 2 into HeLa cells. Virology 1987; 158: 255-258.
132. Beglova N, Jeon H, Fisher C, Blacklow SC. Structural features of the low-density lipoprotein receptor facilitating ligand binding and release. Biochem Soc Trans 2004; 32: 721-723. (Pubitemid 39524362)
133. Beglova N, Jeon H, Fisher C, Blacklow SC. Cooperation between fixed and low pH-inducible interfaces controls lipoprotein release by the LDL receptor. Mol Cell 2004; 16: 281-292.
134. Gamper N, Stockand JD, Shapiro MS. The use of Chinese hamster ovary (CHO) cells in the study of ion channels. J Pharmacol Toxicol Methods 2005; 51: 177-185.
135. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch 1981; 391: 85-100. (Pubitemid 11012976)
136. Zsembery A, Jessner W, Sitter G, Spirli C, Strazzabosco M, Graf J. Correction of CFTR malfunction and stimulation of Ca-activated Cl channels restore HCO3- secretion in cystic fibrosis bile ductular cells. Hepatology 2002; 35: 95-104.
137. Katpally U, Fu TM, Freed DC, Casimiro DR, Smith TJ. Antibodies to the buried N terminus of rhinovirus VP4 exhibit cross-serotypic neutralization. J Virol 2009; 83: 7040-7048.
138. Davis MP, Bottley G, Beales LP, Killington RA, Rowlands DJ, Tuthill TJ. Recombinant VP4 of human rhinovirus induces permeability in model membranes. J Virol 2008; 82: 4169-4174.
139. Paredes AM, Ferreira D, Horton M, et al. Conformational changes in Sindbis virions resulting from exposure to low pH and interactions with cells suggest that cell penetration may occur at the cell surface in the absence of membrane fusion. Virology 2004; 324: 373-386.
140. Wang G, Hernandez R, Weninger K, Brown DT. Infection of cells by Sindbis virus at low temperature. Virology 2007; 362: 461-467. (Pubitemid 46678148)
141. Hernandez R, Paredes A. Sindbis virus as a model for studies of conformational changes in a metastable virus and the role of conformational changes in in vitro antibody neutralisation. Rev Med Virol 2009; 19: 257-272.
142. Lonberg Holm K, Gosser LB, Shimshick EJ. Interaction of liposomes with subviral particles of poliovirus type 2 and rhinovirus type 2. J Virol 1976; 19: 746-749.
143. Bilek G, Kremser L, Wruss J, Blaas D, Kenndler E. Mimicking early events of virus infection: capillary electrophoretic analysis of virus attachment to receptor-decorated liposomes. Anal Chem 2007; 79: 1620-1625.
144. Weiss VU, Bilek G, Pickl-Herk A, Blaas D, Kenndler E. Mimicking virus attachment to host cells employing liposomes: analysis by chip electrophoresis. Electrophoresis 2009; 30: 2123-2128.
145. Evilevitch A, Lavelle L, Knobler CM, Raspaud E, Gelbart WM. Osmotic pressure inhibition of DNA ejection from phage. Proc Natl Acad Sci USA 2003; 100: 9292-9305. (Pubitemid 37033922)
146. Kienberger F, Zhu R, Moser R, Blaas D, Hinterdorfer P. Monitoring RNA release from human rhinovirus by dynamic force microscopy. J Virol 2004; 78: 3203-3209.
147. Kuznetsov YG, Daijogo S, Zhou J, Semler BL, McPherson A. Atomic force microscopy analysis of icosahedral virus RNA. J Mol Biol 2005; 347: 41-52.
148. Palmenberg AC, Sgro JY. Topological organization of picornaviral genomes: statistical prediction of RNA structural signals. Seminars Virol 1997; 8: 231-241.
149. Reisdorph N, Thomas JJ, Katpally U, et al. Human rhinovirus capsid dynamics is controlled by canyon flexibility. Virology 2003; 314: 34-44. (Pubitemid 37153299)
150. Wang L, Smith DL. Capsid structure and dynamics of a human rhinovirus probed by hydrogen exchange mass spectrometry. Protein Sci 2005; 14: 1661-1672.
151. Roenhorst JW, Verduin BJ, Goldbach RW. Virusribosome complexes from cell-free translation systems supplemented with cowpea chlorotic mottle virus particles. Virology 1989; 168: 138-146.
152. Carrillo-Tripp M, Shepherd CM, Borelli IA, et al. VIPERdb2: an enhanced and web API enabled relational database for structural virology. Nucleic Acids Res 2009; 37: D436-D442.
153. Bayer N, Prchla E, Schwab M, Blaas D, Fuchs R. Human rhinovirus HRV14 uncoats from early endosomes in the presence of bafilomycin. FEBS Lett. 1999; 463: 175-178. (Pubitemid 30001742)