Advertisement

Molecular Recognition of Ligands by Native Viruses and Virus-Like Particles as Studied by NMR Experiments

  • Christoph Rademacher
  • Thomas PetersEmail author
Chapter
Part of the Topics in Current Chemistry book series (TOPCURRCHEM, volume 273)

Abstract

Viral entry into host cells is a process that in the majority of cases is not understoodin its molecular details. The first step of viral entry is the recognition of cellular receptorson host cells by viruses, and although X-ray crystallography had yielded some spectacular resultsin individual cases, in general there is little data available to unravel the principles of virus–ligandrecognition at atomic resolution. Therefore, new techniques that uncover the molecular details ofthese recognition processes are needed. The investigation of virus–ligand interactions usingligand-based NMR techniques is an emerging field with the potential to substantially contribute toa deeper understanding of the molecular aspects of viral entry into host cells. Here, we givean overview that covers some of the systems studied so far. This comprises native viruses as wellas virus-like particles (VLPs). We will not address studies that have been performed with individualproteins that are not in a native environment. It turns out that STD NMR in particular has a greatpotential to shine light on the viral entry process as this technique requires only very moderateamounts of viruses or VLPs and corresponding ligands. As a further advantage, this approachis also applicable to ligands that bind to viruses with medium to low affinity. Therefore, STD NMRis extremely well suited for development of antiviral entry inhibitors utilizing fragment-based approacheswith low molecular weight compounds.

Entry inhibitors Ligand-based NMR Noroviruses Rabbit hemorrhagic disease virus Rhinoviruses STD NMR Virus–ligand interaction  

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Dimitrov DS (2004) Nat Rev Microbiol 2:109 CrossRefGoogle Scholar
  2. 2.
    Sieczkarski SB, Whittaker GR (2005) Curr Top Microbiol Immunol 285:1 CrossRefGoogle Scholar
  3. 3.
    Stewart PL, Dermody TS, Nemerow GR (2003) Adv Protein Chem 64:455 CrossRefGoogle Scholar
  4. 4.
    Baranowski E, Ruiz-Jarabo CM, Pariente N, Verdaguer N, Domingo E (2003) Adv Virus Res 62:19 CrossRefGoogle Scholar
  5. 5.
    Marsh M, Helenius A (2006) Cell 124:729 CrossRefGoogle Scholar
  6. 6.
    Damm EM, Pelkmans L (2006) Cell Microbiol 8:1219 CrossRefGoogle Scholar
  7. 7.
    Gagneux P, Cheriyan M, Hurtado-Ziola N, van der Linden EC, Anderson D, McClure H, Varki A, Varki NM (2003) J Biol Chem 278:48245 CrossRefGoogle Scholar
  8. 8.
    Baranowski E, Ruiz-Jarabo CM, Domingo E (2001) Science 292:1102 CrossRefGoogle Scholar
  9. 9.
    Flint SJ (2004) Principles of virology: molecular biology, pathogenesis, and control of animal viruses. ASM, Washington DC Google Scholar
  10. 10.
    Hogle JM (2002) Annu Rev Microbiol 56:677 CrossRefGoogle Scholar
  11. 11.
    Dormitzer PR, Nason EB, Prasad BV, Harrison SC (2004) Nature 430:1053 CrossRefGoogle Scholar
  12. 12.
    Vliegenthart GA, Gompper G (2006) Biophys J 91:834 CrossRefGoogle Scholar
  13. 13.
    Chow M, Basavappa R, Hogle JM (1997) The role of conformational transitions in poliovirus pathogenesis. In: Chiu W, Garcea R, Burnette R (eds) Structural biology of viruses. Oxford University Press, Oxford, pp 157–186 Google Scholar
  14. 14.
    Fox MP, Otto MJ, McKinlay MA (1986) Antimicrob Agents Chemother 30:110 CrossRefGoogle Scholar
  15. 15.
    Kim SS, Smith TJ, Chapman MS, Rossmann MC, Pevear DC, Dutko FJ, Felock PJ, Diana GD, McKinlay MA (1989) J Mol Biol 210:91 CrossRefGoogle Scholar
  16. 16.
    Smith TJ, Kremer MJ, Luo M, Vriend G, Arnold E, Kamer G, Rossmann MG, McKinlay MA, Diana GD, Otto MJ (1986) Science 233:1286 CrossRefGoogle Scholar
  17. 17.
    Tsang SK, Danthi P, Chow M, Hogle JM (2000) J Mol Biol 296:335 CrossRefGoogle Scholar
  18. 18.
    Phelps DK, Rossky PJ, Post CB (1998) J Mol Biol 276:331 CrossRefGoogle Scholar
  19. 19.
    Munch J, Standker L, Adermann K, Schulz A, Schindler M, Chinnadurai R, Pohlmann S, Chaipan C, Biet T, Peters T, Meyer B, Wilhelm D, Lu H, Jing W, Jiang S, Forssmann WG, Kirchhoff F (2007) Cell 129:263 CrossRefGoogle Scholar
  20. 20.
    O’Hara BM, Olson WC (2002) Curr Opin Pharmacol 2:523 CrossRefGoogle Scholar
  21. 21.
    Welch BD, Vandemark AP, Heroux A, Hill CP, Kay MS (2007) Proc Natl Acad Sci USA 104:16828 CrossRefGoogle Scholar
  22. 22.
    Bomsel M, Alfsen A (2003) Nat Rev Mol Cell Biol 4:57 CrossRefGoogle Scholar
  23. 23.
    The Scripps Research Institute (2007) Viperdb:Virus particle explorer. TSRI, La Jolla, CA. http://viperdb.scripps.edu . Last visited: 12 Dec 2007
  24. 24.
    Natarajan P, Lander GC, Shepherd CM, Reddy VS, Brooks CL III, Johnson JE (2005) Nat Rev Microbiol 3:809 CrossRefGoogle Scholar
  25. 25.
    Wall ME, Gallagher SC, Trewhella J (2000) Annu Rev Phys Chem 51:355 CrossRefGoogle Scholar
  26. 26.
    Rossmann MG, Morais MC, Leiman PG, Zhang W (2005) Structure 13:355 CrossRefGoogle Scholar
  27. 27.
    Meinhold L, Smith JC (2006) Proteins, p 941 Google Scholar
  28. 28.
    Verdaguer N, Fita I, Reithmayer M, Moser R, Blaas D (2004) Nat Struct Mol Biol 11:429 CrossRefGoogle Scholar
  29. 29.
    Fry EE, Lea SM, Jackson T, Newman JW, Ellard FM, Blakemore WE, Abu-Ghazaleh R, Samuel A, King AM, Stuart DI (1999) EMBO J 18:543 CrossRefGoogle Scholar
  30. 30.
    Xiao C, Bator-Kelly CM, Rieder E, Chipman PR, Craig A, Kuhn RJ, Wimmer E, Rossmann MG (2005) Structure 13:1019 CrossRefGoogle Scholar
  31. 31.
    Szymczyna BR, Gan L, Johnson JE, Williamson JR (2007) J Am Chem Soc 129:7867 CrossRefGoogle Scholar
  32. 32.
    Doherty PC, Turner SJ, Webby RG, Thomas PG (2006) Nat Immunol 7:449 CrossRefGoogle Scholar
  33. 33.
    Palese P (2004) Nat Med 10:S82 CrossRefGoogle Scholar
  34. 34.
    Matrosovich M, Tuzikov A, Bovin N, Gambaryan A, Klimov A, Castrucci MR, Donatelli I, Kawaoka Y (2000) J Virol 74:8502 CrossRefGoogle Scholar
  35. 35.
    Vines A, Wells K, Matrosovich M, Castrucci MR, Ito T, Kawaoka Y (1998) J Virol 72:7626 Google Scholar
  36. 36.
    Angata T, Varki A (2002) Chem Rev 102:439 CrossRefGoogle Scholar
  37. 37.
    Hanson JE, Sauter NK, Skehel JJ, Wiley DC (1992) Virology 189:525 CrossRefGoogle Scholar
  38. 38.
    von Itzstein M, Wu WY, Kok GB, Pegg MS, Dyason JC, Jin B, Van Phan T, Smythe ML, White HF, Oliver SW et al. (1993) Nature 363:418 CrossRefGoogle Scholar
  39. 39.
    Russell RJ, Haire LF, Stevens DJ, Collins PJ, Lin YP, Blackburn GM, Hay AJ, Gamblin SJ, Skehel JJ (2006) Nature 443:45 CrossRefGoogle Scholar
  40. 40.
    Sauter NK, Bednarski MD, Wurzburg BA, Hanson JE, Whitesides GM, Skehel JJ, Wiley DC (1989) Biochemistry 28:8388 CrossRefGoogle Scholar
  41. 41.
    Reibarkh M, Malia TJ, Wagner G (2006) J Am Chem Soc 128:2160 CrossRefGoogle Scholar
  42. 42.
    Semler BL, Wimmer E (2002) Molecular biology of picornaviruses. ASM, Washington DC Google Scholar
  43. 43.
    Tan WC (2005) Curr Opin Pulm Med 11:21 Google Scholar
  44. 44.
    Whitton JL, Cornell CT, Feuer R (2005) Nat Rev Microbiol 3:765 CrossRefGoogle Scholar
  45. 45.
    Modrow S, Falke D, Truyen U (2003) Molekulare Virologie. Spektrum Akad, Heidelberg Google Scholar
  46. 46.
    Staunton DE, Gaur A, Chan PY, Springer TA (1992) J Immunol 148:3271 Google Scholar
  47. 47.
    Andries K, Dewindt B, De Brabander M, Stokbroekx R, Janssen PA (1988) Arch Virol 101:155 CrossRefGoogle Scholar
  48. 48.
    Goncalves RB, Mendes YS, Soares MR, Katpally U, Smith TJ, Silva JL, Oliveira AC (2007) J Mol Biol 366:295 CrossRefGoogle Scholar
  49. 49.
    Lewis JK, Bothner B, Smith TJ, Siuzdak G (1998) Proc Natl Acad Sci USA 95:6774 CrossRefGoogle Scholar
  50. 50.
    Goncalves RB, Mendes YS, Soares MR, Katpally U, Smith TJ, Silva JL, Oliveira AC (2007) J Mol Biol 366:295 CrossRefGoogle Scholar
  51. 51.
    Korant BD, Lonberg-Holm K, Noble J, Stasny JT (1972) Virology 48:71 CrossRefGoogle Scholar
  52. 52.
    Lonberg-Holm K, Noble-Harvey J (1973) J Virol 12:819 Google Scholar
  53. 53.
    Benie AJ, Moser R, Baeuml E, Blaas D, Peters T (2003) J Am Chem Soc 125:14 CrossRefGoogle Scholar
  54. 54.
    Bella J, Kolatkar PR, Marlor CW, Greve JM, Rossmann MG (1998) Proc Natl Acad Sci USA 95:4140 CrossRefGoogle Scholar
  55. 55.
    Yamaya M, Sasaki H (2003) Viral Immunol 16:99 CrossRefGoogle Scholar
  56. 56.
    Hewat EA, Neumann E, Conway JF, Moser R, Ronacher B, Marlovits TC, Blaas D (2000) EMBO J 19:6317 CrossRefGoogle Scholar
  57. 57.
    Moser R, Snyers L, Wruss J, Angulo J, Peters H, Peters T, Blaas D (2005) Virology 338:259 CrossRefGoogle Scholar
  58. 58.
    Blacklow SC (2004) Nat Struct Mol Biol 11:388 CrossRefGoogle Scholar
  59. 59.
    Jeon H, Blacklow SC (2005) Annu Rev Biochem 74:535 CrossRefGoogle Scholar
  60. 60.
    Marionneau S, Cailleau-Thomas A, Rocher J, Le Moullac-Vaidye B, Ruvoen N, Clement M, Le Pendu J (2001) Biochimie 83:565 CrossRefGoogle Scholar
  61. 61.
    Le Pendu J, Marionneau S, Cailleau-Thomas A, Rocher J, Le Moullac-Vaidye B, Clement M (2001) Apmis 109:9 CrossRefGoogle Scholar
  62. 62.
    Hakomori S (1999) Biochim Biophys Acta 1473:247 CrossRefGoogle Scholar
  63. 63.
    Le Pendu J (2004) Adv Exp Med Biol 554:135 Google Scholar
  64. 64.
    Tan M, Jiang X (2005) Trends Microbiol 13:285 CrossRefGoogle Scholar
  65. 65.
    Ruvoen-Clouet N, Ganiere JP, Andre-Fontaine G, Blanchard D, Le Pendu J (2000) J Virol 74:11950 CrossRefGoogle Scholar
  66. 66.
    Moss SR, Turner SL, Trout RC, White PJ, Hudson PJ, Desai A, Armesto M, Forrester NL, Gould EA (2002) J Gen Virol 83:2461 Google Scholar
  67. 67.
    Capucci L, Fusi P, Lavazza A, Pacciarini ML, Rossi C (1996) J Virol 70:8614 Google Scholar
  68. 68.
    Thiel HJ, Konig M (1999) Vet Microbiol 69:55 CrossRefGoogle Scholar
  69. 69.
    Tan M, Huang P, Meller J, Zhong W, Farkas T, Jiang X (2003) J Virol 77:12562 CrossRefGoogle Scholar
  70. 70.
    Jiang X, Wang M, Graham DY, Estes MK (1992) J Virol 66:6527 Google Scholar
  71. 71.
    Jiang X, Matson DO, Ruiz-Palacios GM, Hu J, Treanor J, Pickering LK (1995) J Clin Microbiol 33:1452 Google Scholar
  72. 72.
    Jiang X, Zhong WM, Farkas T, Huang PW, Wilton N, Barrett E, Fulton D, Morrow R, Matson DO (2002) Arch Virol 147:119 CrossRefGoogle Scholar
  73. 73.
    Ewers H, Smith AE, Sbalzarini IF, Lilie H, Koumoutsakos P, Helenius A (2005) Proc Natl Acad Sci USA 102:15110 CrossRefGoogle Scholar
  74. 74.
    Cao S, Lou Z, Tan M, Chen Y, Liu Y, Zhang Z, Zhang XC, Jiang X, Li X, Rao Z (2007) J Virol 81:5949 CrossRefGoogle Scholar
  75. 75.
    Angulo J, Rademacher C, Biet T, Benie AJ, Blume A, Peters H, Palcic M, Parra F, Peters T (2006) Methods Enzymol 416:12 CrossRefGoogle Scholar
  76. 76.
    Kalk A, Berendsen HJC (1976) J Magn Reson 24:343 Google Scholar
  77. 77.
    Andree PJ (1978) J Magn Reson 29:419 Google Scholar
  78. 78.
    Peng JW, Moore J, Abdul-Manan N (2004) Prog Nucl Magn Reson Spectr 44:225 CrossRefGoogle Scholar
  79. 79.
    Slichter CP (1996) Principles of magnetic resonance. Springer, Berlin, Heidelberg, New York Google Scholar
  80. 80.
    Ishima R, Shibata S, Akasaka K (1991) J Magn Reson 91:455 Google Scholar
  81. 81.
    Tan M, Jiang X (2007) Expert Rev Mol Med 9:1 CrossRefGoogle Scholar
  82. 82.
    Estes MK, Prasad BV, Atmar RL (2006) Curr Opin Infect Dis 19:467 CrossRefGoogle Scholar
  83. 83.
    Siebenga JJ, Vennema H, Renckens B, de Bruin E, van der Veer B, Siezen RJ, Koopmans M (2007) J Virol 81:9932 CrossRefGoogle Scholar
  84. 84.
    Farkas T, Nakajima S, Sugieda M, Deng X, Zhong W, Jiang X (2005) J Clin Microbiol 43:657 CrossRefGoogle Scholar
  85. 85.
    Gallimore CI, Lewis D, Taylor C, Cant A, Gennery A, Gray JJ (2004) J Clin Virol 30:196 CrossRefGoogle Scholar
  86. 86.
    Nilsson M, Hedlund KO, Thorhagen M, Larson G, Johansen K, Ekspong A, Svensson L (2003) J Virol 77:13117 CrossRefGoogle Scholar
  87. 87.
    Lindesmith L, Moe C, Marionneau S, Ruvoen N, Jiang X, Lindblad L, Stewart P, Le Pendu J, Baric R (2003) Nat Med 9:548 CrossRefGoogle Scholar
  88. 88.
    Chakravarty S, Hutson AM, Estes MK, Prasad BV (2005) J Virol 79:554 CrossRefGoogle Scholar
  89. 89.
    Huang P, Farkas T, Zhong W, Tan M, Thornton S, Morrow AL, Jiang X (2005) J Virol 79:6714 CrossRefGoogle Scholar
  90. 90.
    Tan M, Hegde RS, Jiang X (2004) J Virol 78:6233 CrossRefGoogle Scholar
  91. 91.
    Feng X, Jiang X (2007) Antimicrob Agents Chemother 51:324 CrossRefGoogle Scholar
  92. 92.
    Hajduk PJ, Greer J (2007) Nat Rev Drug Discov 6:211 CrossRefGoogle Scholar
  93. 93.
    Verdaguer N, Blaas D, Fita I (2000) J Mol Biol 300:1179 CrossRefGoogle Scholar
  94. 94.
    Stierand K, Rarey M (2007) Chem Med Chem 2:853 Google Scholar
  95. 95.
    Rarey M, Kramer B, Lengauer T, Klebe G (1996) J Mol Biol 261:470 CrossRefGoogle Scholar
  96. 96.
    Wang R, Lai L, Wang S (2002) J Comput Aided Mol Des 16:11 CrossRefGoogle Scholar
  97. 97.
    Mayer M, Meyer B (2001) J Am Chem Soc 123:6108 CrossRefGoogle Scholar
  98. 98.
    Freeman R, Hill HDW (1971) J Chem Phys 54:3367 CrossRefGoogle Scholar
  99. 99.
    Jayalakshmi V, Krishna NR (2002) J Magn Reson 155:106 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2008

Authors and Affiliations

  1. 1.Institute of ChemistryUniversity of LuebeckLuebeckGermany

Personalised recommendations