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Assembly, Engineering and Applications of Virus-Based Protein Nanoparticles

  • Mauricio G. MateuEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 940)

Abstract

Viruses and their protein capsids can be regarded as biologically evolved nanomachines able to perform multiple, complex biological functions through coordinated mechano-chemical actions during the infectious cycle. The advent of nanoscience and nanotechnology has opened up, in the last 10 years or so, a vast number of novel possibilities to exploit engineered viral capsids as protein-based nanoparticles for multiple biomedical, biotechnological or nanotechnological applications. This chapter attempts to provide a broad, updated overview on the self-assembly and engineering of virus capsids, and on applications of virus-based nanoparticles. Different sections provide outlines on: (i) the structure, functions and properties of virus capsids; (ii) general approaches for obtaining assembled virus particles; (iii) basic principles and events related to virus capsid self-assembly; (iv) genetic and chemical strategies for engineering virus particles; (v) some applications of engineered virus particles being developed; and (vi) some examples on the engineering of virus particles to modify their physical properties, in order to improve their suitability for different uses.

Keywords

Virus Virion Capsid Virus-like particle Virus capsid-based nanoparticle Capsid structure, function and properties Capsid proteins and building blocks Capsid assembly Protein engineering Chemical functionalization Phage display Capsid-based vaccines Gene therapy Virotherapy Targeted drug delivery Diagnostic imaging Nanobiosensors Inorganic nanoparticles Nanoscale materials Virus capsid stability 

Abbreviations

AAV

adeno-associated viruses

AFM

atomic force microscopy

BMV

brome mosaic virus

CA

capsid protein of HIV

CBB

capsid building block

CCMV

cowpea chlorotic mottle virus

CNT

classic nucleation theory

CP

capsid protein

CPMV

cowpea mosaic virus

CMV

cucumber mosaic virus

CPV

canine parvovirus

cryo-EM

cryo-electron microscopy

ds

double-stranded

EMDB

Electron Microscopy Database

FMDV

foot-and-mouth disease virus

FRET

Förster resonance energy transfer

HBV

hepatitis B virus

HCRSV

Hibiscus chlorotic ringspot virus

HIV

human immunodeficiency virus

HPV

human papillomavirus

HRV

human rhinovirus

HSV-1

herpes simplex virus type 1

MD

molecular dynamics

MRI

magnetic resonance imaging

MS

mass spectrometry

MVM

minute virus of mice

NP

nanoparticle

PCR

polymerase chain reaction

PDB

Protein Data Bank

PEG

polyethyleneglycol

RCNMV

red clover nechrotic mottle virus

SBMV

southern bean mosaic virus

ss

single-stranded

STNV

satellite tobacco necrosis virus

SV40

simian virus 40

TBSV

tomato bushy stunt virus

TMV

tobacco mosaic virus

VLP

virus-like particle

VP

viral (capsid) protein.

Notes

Acknowledgments

I gratefully acknowledge former and current collaborators and members of my group for their invaluable contributions to our studies on structure-properties-function relationships and engineering of virus particles, and Miguel Angel Fuertes for help with figures in this chapter. This work was funded by grants from MINECO/FEDER EU (BIO2012-37649 and BIO2015-69928-R) and by an institutional grant from Fundacion Ramon Areces. The author is an associate member of the Institute for Biocomputation and Physics of Complex Systems, Zaragoza, Spain.

References

  1. 1.
    Agbandje-McKenna M, McKenna R (eds) (2011) Structural virology. RSC Publishing, CambridgeGoogle Scholar
  2. 2.
    Mateu MG (ed) (2013) Structure and physics of viruses. Springer, DordrechtGoogle Scholar
  3. 3.
    Harrison SC (2007) Principles of virus structure. In: Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Strauss SE (eds) Fields virology, vol 1. Lippincott Williams & Wilkins, Philadelphia, pp 59–98Google Scholar
  4. 4.
    Johnson JE, Speir JA (2008) Principles of virus structure. In: Mahy BWJ, van Regenmortel MHV (eds) Encyclopedia of virology, vol 5. Elsevier, Oxford, pp 393–401CrossRefGoogle Scholar
  5. 5.
    Prasad BV, Schmid MF (2012) Principles of virus structural organization. Exp Med Virol 726:17–47Google Scholar
  6. 6.
    Acheson NH (2007) Fundamentals of molecular virology, 2nd edn. Wiley, HobokenGoogle Scholar
  7. 7.
    Flint SJ, Enquist LW, Racaniello VR, Skalka AM (2009) Principles of virology, 3rd edn. ASM Press, Washington, DCGoogle Scholar
  8. 8.
    Cann AJ (2012) Principles of molecular virology, 5th edn. Academic, WalthamGoogle Scholar
  9. 9.
    Caston JR (2013) The basic architectures of viruses. In: Mateu MG (ed) Structure and physics of viruses. Springer, Dordrecht, pp 53–75CrossRefGoogle Scholar
  10. 10.
    Chapman MS, Liljas L (2003) Structural folds of viral proteins. Adv Prot Chem 64:125–196CrossRefGoogle Scholar
  11. 11.
    Caspar DLD, Klug A (1962) Physical principles in the construction of regular viruses. Cold Spring Harbor Symp Quant Biol 27:1–24PubMedCrossRefGoogle Scholar
  12. 12.
    Johnson JE (1996) Functional implications of protein-protein interactions in icosahedral viruses. Proc Natl Acad Sci U S A 93:27–33PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Prevelige PE Jr (1998) Inhibiting virus-capsid assembly by altering the polymerisation pathway. Trends Biotechnol 16:61–65Google Scholar
  14. 14.
    San Martin C (2013) Structure and assembly of complex viruses. In: Mateu MG (ed) Structure and physics of viruses. Springer, Dordrecht, pp 329–360CrossRefGoogle Scholar
  15. 15.
    Sundquist WI, Kräusslich H-G (2012) HIV-1 assembly, budding, and maturation. Cold Spring Harb Perspect Med 2:a006924PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Rossmann MG, Rao VB (eds) (2012) Viral molecular machines, vol 726, Advances in experimental medicine and biology. Springer, New YorkGoogle Scholar
  17. 17.
    Risco C, Fernández de Castro I (2013) Virus morphogenesis in the cell: methods and observations. In: Mateu MG (ed) Structure and physics of viruses. Springer, Dordrecht, pp 417–440CrossRefGoogle Scholar
  18. 18.
    Mateu MG (2013) Assembly, stability and dynamics of virus capsids. Arch Biochem Biophys 531:65–79PubMedCrossRefGoogle Scholar
  19. 19.
    Alonso JM, Górzny ML, Bittner AM (2013) The physics of tobacco mosaic virus and virus-based devices in biotechnology. Trends Biotechnol 31:530–538PubMedCrossRefGoogle Scholar
  20. 20.
    Witz J, Brown F (2001) Structural dynamics, an intrinsic property of viral capsids. Arch Virol 146:2263–2274PubMedCrossRefGoogle Scholar
  21. 21.
    Johnson JE (2003) Virus particle dynamics. Adv Protein Chem 64:197–218PubMedCrossRefGoogle Scholar
  22. 22.
    Bothner B, Hilmer JK (2011) Probing viral capsids in solution. In: Agbandje-McKenna M, McKenna R (eds) Structural virology. RSC Publishing, Cambridge, pp 41–61Google Scholar
  23. 23.
    Katen S, Zlotnick A (2009) The thermodynamics of virus capsid assembly. Methods Enzymol 455:395–417PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Zlotnick A, Fane BA (2011) Mechanisms of icosahedral virus assembly. In: Agbandje-McKenna M, McKenna R (eds) Structural virology. RSC Publishing, Cambridge, pp 180–202Google Scholar
  25. 25.
    Almendral JM (2013) Assembly of simple icosahedral viruses. In: Mateu MG (ed) Structure and physics of viruses. Springer, Dordrecht, pp 307–328CrossRefGoogle Scholar
  26. 26.
    Luque A, Reguera D (2013) Theoretical studies on assembly, physical stability and dynamics of viruses. In: Mateu MG (ed) Structure and physics of viruses. Springer, Dordrecht, pp 553–595CrossRefGoogle Scholar
  27. 27.
    Perlmutter JD, Hagan MF (2014) Mechanisms of virus assembly. Annu Rev Phys Chem 66:217–239PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Pattenden LK, Middelberg APJ, Niebert M, Lipin DI (2005) Towards the preparative and large-scale precision manufacture of virus-like particles. Trends Biotechnol 23:523–529PubMedCrossRefGoogle Scholar
  29. 29.
    Gurda BL, Agbandje-McKenna M (2011) Production and purification of viruses for structural studies. In: Agbandje-McKenna M, McKenna R (eds) Structural virology. RSC Publishing, Cambridge, pp 3–21Google Scholar
  30. 30.
    Lua LHL, Connors NK, Sainsbury F, Chuan YP, Wibowo N, Middleberg APJ (2013) Bioengineering virus-like particles as vaccines. Biotechnol Bioeng 111:425–440PubMedCrossRefGoogle Scholar
  31. 31.
    Glasgow J, Tullman-Ercek D (2014) Production and applications of engineered viral capsids. Appl Microbiol Biotechnol 98:5847–5858PubMedCrossRefGoogle Scholar
  32. 32.
    Evans DJ (1999) Reverse genetics of picornaviruses. Adv Virus Res 53:209–228PubMedCrossRefGoogle Scholar
  33. 33.
    Nagyova A, Subr Z (2007) Infectious full-length clones of plant viruses and their use for construction of viral vectors. Acta Virol 51:223–237PubMedGoogle Scholar
  34. 34.
    Yildiz I, Shukia S, Steinmetz NF (2011) Applications of viral nanoparticles in medicine. Curr Opin Biotechnol 22:901–908PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Saunders K, Lomonosoff GP (2013) Exploiting plant virus-derived components to achieve in planta expression and for templates for synthetic biology applications. New Phytol 200:16–26PubMedCrossRefGoogle Scholar
  36. 36.
    Palomares LA, Ramirez OT (2009) Challenges for the production of virus-like particles in insect cells: the case of rotavirus-like particles. Biochem Eng 45:158–167CrossRefGoogle Scholar
  37. 37.
    Bundy BC, Franciszkowitz MJ, Swartz JR (2008) Escherichia coli-based cell-free synthesis of virus-like particles. Biotechnol Bioeng 100:28–37PubMedCrossRefGoogle Scholar
  38. 38.
    Liu Z, Qiao J, Niu Z, Wang Q (2012) Natural supramolecular building blocks: from virus coat proteins to viral nanoparticles. Chem Soc Rev 41:6178–6194PubMedCrossRefGoogle Scholar
  39. 39.
    De la Escosura A, Nolte R, Cornelissen J (2009) Viruses and protein cages as nanoconainers and nanoreactors. J Mater Chem 19:2274–2278CrossRefGoogle Scholar
  40. 40.
    Bronstein LM (2011) Virus-based nanoparticles with inorganic cargo: what does the future hold? Small 12:1069–1618Google Scholar
  41. 41.
    Li F, Wang Q (2014) Fabrication of nanoarchitectures templated by virus-based nanoparticles: strategies and applications. Small 2:230–245CrossRefGoogle Scholar
  42. 42.
    Klug A (1999) The tobacco mosaic virus particle: structure and assembly. Philos Trans R Soc Lond B Biol Sci 354:531–535PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Tuma R, Tsuruta H, French KH, Prevelige PE (2008) Detection of intermediates and kinetic control during assembly of bacteriophage P22 procapsid. J Mol Biol 381:1395–1406PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Teschke CN, Parent KN (2010) Let the phage do the work: using the phage P22 coat protein structures as a framework to understand its folding and assembly mutants. Virology 401:119–130PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Uchida M, Klem MT, Allen M, Suci P, Flenniken M, Gillitzer E, Varpness Z, Liepold LO, Young M, Douglas T (2007) Biological containers: protein cages as multifunctional nanoplatforms. Adv Mater 19:1025–1042CrossRefGoogle Scholar
  46. 46.
    Casjens S (1997) Principles of virion structure, function and assembly. In: Chiu W, Burnett RM, Garcea RL (eds) Structural biology of viruses. Oxford University Press, New York, pp 3–37Google Scholar
  47. 47.
    Dokland T (1999) Scaffolding proteins and their role in viral assembly. Cell Mol Life Sci 56:580–603PubMedCrossRefGoogle Scholar
  48. 48.
    Fane BA, Prevelige PE Jr (2003) Mechanism of scaffolding-assisted viral assembly. Adv Protein Chem 64:259–299Google Scholar
  49. 49.
    Prevelige PE Jr, Fane BA (2012) Building the machines: scaffolding protein functions during bacteriophage morphogenesis. Adv Exp Med Virol 726:325–350Google Scholar
  50. 50.
    Johnson JE, Rueckert RR (1997) Packaging and release of the viral genome. In: Chiu W, Burnett RM, Garcea RL (eds) Structural biology of viruses. Oxford University Press, New York, pp 269–287Google Scholar
  51. 51.
    Larson SB, McPherson A (2001) Satellite mosaic virus RNA: structure and implications for assembly. Curr Opin Struct Biol 11:59–65PubMedCrossRefGoogle Scholar
  52. 52.
    Culver JN (2002) Tobacco mosaic virus assembly and disassembly: determinants in pathogenicity and resistance. Annu Rev Phytopathol 40:287–308PubMedCrossRefGoogle Scholar
  53. 53.
    Schneemann A (2006) The structural and functional role of RNA in icosahedral virus assembly. Annu Rev Microbiol 60:51–67PubMedCrossRefGoogle Scholar
  54. 54.
    Rao AL (2006) Genome packaging by spherical plant RNA viruses. Annu Rev Phytopathol 44:61–87PubMedCrossRefGoogle Scholar
  55. 55.
    Cuervo A, Daudén MI, Carrascosa JL (2013) Nucleic acid packaging in viruses. In: Mateu MG (ed) Structure and physics of viruses. Springer, Dordrecht, pp 361–394CrossRefGoogle Scholar
  56. 56.
    Rapaport DC (2014) Molecular dynamics simulation: a tool for exploration and discovery using simple models. J Phys Condens Matter 26:503104PubMedCrossRefGoogle Scholar
  57. 57.
    Rapaport DC (2010) Studies of reversible capsid shell growth. Phys Biol 7:045001PubMedCrossRefGoogle Scholar
  58. 58.
    Hida K, Hanes J, Ostermeier M (2007) Directed evolution for drug and nucleic acid delivery. Adv Drug Deliv Rev 59:1562–1578PubMedCrossRefGoogle Scholar
  59. 59.
    Fischlechner M, Donath E (2007) Viruses as building blocks for materials and devices. Angew Chem Int Ed 46:3184–3193CrossRefGoogle Scholar
  60. 60.
    Kehoe JW, Kay BK (2005) Filamentous phage display in the new millennium. Chem Rev 105:4056–4072PubMedCrossRefGoogle Scholar
  61. 61.
    Domingo E, Biebricher C, Eigen M, Holland J (2001) Quasispecies and RNA virus evolution: principles and consequences. Landes Bioscience, AustinGoogle Scholar
  62. 62.
    Arora PS, Kirshenbaum K (2004) Nano-tailoring: stitching alterations on viral coats. Chem Biol 11:418–420PubMedCrossRefGoogle Scholar
  63. 63.
    Strable E, Finn MG (2009) Chemical modification of viruses and virus-like particles. In: Manchester M, Steinmetz NF (eds) Viruses and nanotechnology. Curr Top Microbiol Immunol 327:1–21Google Scholar
  64. 64.
    Pokorski JK, Steinmetz NF (2011) The art of engineering viral nanoparticles. Mol Pharm 8:29–43PubMedCrossRefGoogle Scholar
  65. 65.
    Smith MT, Hawes AK, Bundy BC (2013) Reengineering viruses and virus-like particles through chemical functionalization strategies. Curr Opin Struct Biol 24:620–626Google Scholar
  66. 66.
    Garcea RL, Gissmann L (2004) Virus-like particles as vaccines and vessels for the delivery of small molecules. Curr Opin Biotechnol 15:513–517PubMedCrossRefGoogle Scholar
  67. 67.
    Douglas T, Young M (2006) Viruses: making friends with old foes. Science 312:873–875PubMedCrossRefGoogle Scholar
  68. 68.
    Steinmetz NF, Evans D (2007) Utilisation of plant viruses in bionanotechnology. Org Biomol Chem 5:2891–2902PubMedCrossRefGoogle Scholar
  69. 69.
    Young M, Willits D, Uchida M, Douglas T (2008) Plant viruses as biotemplates for materials and their use in nanotechnology. Annu Rev Phytopathol 46:361–384PubMedCrossRefGoogle Scholar
  70. 70.
    Steinmetz NF, Lin T, Lomonosoff GP, Johnson JE (2009) Structure-based engineering of an icosahedral virus for nanomedicine and nanotechnology. In: Manchester M, Steinmetz NF (eds) Viruses and nanotechnology. Curr Top Microbiol Immunol 327:23–58Google Scholar
  71. 71.
    Flenniken ML, Uchida M, Liepold LO, Kang S, Young MJ, Douglas T (2009) A library of cage architectures as nanomaterials. In: Manchester M, Steinmetz NF (eds) Viruses and nanotechnology. Curr Top Microbiol Immunol 327:71–93Google Scholar
  72. 72.
    Mateu MG (2011) Virus engineering: functionalization and stabilization. Protein Eng Des Sel 24:53–63PubMedCrossRefGoogle Scholar
  73. 73.
    Dedeo MT, Finley DT, Francis MB (2011) Viral capsids as self-assembling templates for new materials. Prog Mol Biol Transl Sci 103:353–392PubMedCrossRefGoogle Scholar
  74. 74.
    Lee S-Y, Lim J-S, Harris MT (2012) Synthesis and applications of virus-based hybrid nanomaterials. Biotechnol Bioeng 109:16–30PubMedCrossRefGoogle Scholar
  75. 75.
    Bittner AM, Alonso JM, Górzny ML, Wege C (2013) Nanoscale science and technology with plant viruses and bacteriophages. In: Mateu MG (ed) Structure and physics of viruses. Springer, Dordrecht, pp 667–702CrossRefGoogle Scholar
  76. 76.
    van Kan-Davelaar HE, van Hest JCM, Cornelissen JJLM, Koay MST (2014) Using viruses as nanomedicines. Br J Pharmacol 171:4001–4009PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Paschke M (2006) Phage display systems and their applications. Appl Microbiol Biotechnol 70:2–11PubMedCrossRefGoogle Scholar
  78. 78.
    Carnazza S, Guglielmino S (2010) Phage display as a tool for synthetic biology, Nanotechnology science and technology series. Nova Science Publications, New YorkGoogle Scholar
  79. 79.
    Cardinale D, Carette N, Michon T (2012) Virus scaffolds as enzyme nano-carriers. Trends Biotechnol 30:369–376PubMedCrossRefGoogle Scholar
  80. 80.
    Roy P, Noad R (2008) Virus-like particles as a vaccine delivery system. Hum Vaccin 4:5–8PubMedCrossRefGoogle Scholar
  81. 81.
    Jennings GT, Bachmann MF (2008) The coming of age of virus-like particle vaccines. Biol Chem 389:521–536PubMedCrossRefGoogle Scholar
  82. 82.
    Roldao A, Mellado MC, Castilho LR, Carrondo MJ, Alves PM (2010) Virus-like particles as particulate vaccines. Expert Rev Vaccines 9:1149–1176PubMedCrossRefGoogle Scholar
  83. 83.
    Plummer EM, Manchester M (2011) Viral nanoparticles and virus-like particles: platforms for contemporary vaccine design. Wiley Interdiscip Rev Nanomed Nanobiotechnol 3:174–196PubMedCrossRefGoogle Scholar
  84. 84.
    Barcena J, Blanco E (2013) Design of novel vaccines based on virus-like particles or chimeric virions. In: Mateu MG (ed) Structure and physics of viruses. Springer, Dordrecht, pp 631–665CrossRefGoogle Scholar
  85. 85.
    Wang D, Gao G (2014) State-of-the-art human gene therapy. Part I. Gene delivery technologies. Discov Med 18:67–77PubMedPubMedCentralGoogle Scholar
  86. 86.
    Wang D, Gao G (2014) State-of-the-art human gene therapy. Part II. Gene therapy strategies and clinical applications. Discov Med 18:151–161PubMedPubMedCentralGoogle Scholar
  87. 87.
    Waehler R, Russell SJ, Curiel DT (2007) Engineered targeted viral vectors for gene therapy. Nat Rev 8:573–587CrossRefGoogle Scholar
  88. 88.
    Wang J, Faust SM, Rabinowitz JE (2011) The next step in gene delivery: molecular engineering of adeno-associated virus serotypes. J Mol Cell Cardiol 50:793–802PubMedCrossRefGoogle Scholar
  89. 89.
    Bartel MA, Weinstein JR, Schaffer DV (2012) Directed evolution of novel adeno-associated viruses for therapeutic gene delivery. Gene Ther 19:694–700PubMedCrossRefGoogle Scholar
  90. 90.
    Kotterman MA, Schaffer DV (2014) Engineering adeno-associated viruses for clinical gene therapy. Nat Rev 15:445–451CrossRefGoogle Scholar
  91. 91.
    Russell SJ, Peng K-W (2007) Viruses as anticancer drugs. Trends Pharmacol Sci 28:326–333PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Alemany R (2012) Design of improved oncolytic adenoviruses. Adv Cancer Res 115:93–114PubMedCrossRefGoogle Scholar
  93. 93.
    Miest TS, Cattaneo R (2014) New viruses for cancer therapy: meeting clinical needs. Nat Rev 12:23–34Google Scholar
  94. 94.
    Moradpour Z, Ghasemian A (2011) Modified phages: novel antimicrobial agents to combat infectious diseases. Biotechnol Adv 29:732–738PubMedCrossRefGoogle Scholar
  95. 95.
    Farr R, Choi DS, Lee S-W (2014) Phage-based nanomaterials for biomedical applications. Acta Biomater 10:1741–1750PubMedCrossRefGoogle Scholar
  96. 96.
    Manchester M, Singh P (2006) Virus-based nanoparticles (VNPs): platform technologies for diagnostic imaging. Adv Drug Deliv Rev 58:1505–1522PubMedCrossRefGoogle Scholar
  97. 97.
    Singh R, Kostarelos K (2009) Designer adenoviruses for nanomedicine and nanodiagnostics. Trends Biotechnol 27:220–229PubMedCrossRefGoogle Scholar
  98. 98.
    Ma Y, Nolte RJM, Cornelissen JJLM (2012) Virus-based nanocarriers for drug delivery. Adv Drug Deliv Rev 64:811–825PubMedCrossRefGoogle Scholar
  99. 99.
    Wen AM, Rambhia PH, French RH, Steinmetz NF (2013) Design rules for nanomedical engineering: from physical virology to the applications of virus-based materials in medicine. J Biol Phys 39:301–325PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Soto CM, Ratna BR (2010) Virus hybrids as nanomaterials for biotechnology. Curr Opin Biotechnol 21:426–438PubMedCrossRefGoogle Scholar
  101. 101.
    Lee JW, Song J, Hwang MP, Lee KH (2013) Nanoscale bacteriophage biosensors beyond phage display. Int J Nanomed 8:3917–3925CrossRefGoogle Scholar
  102. 102.
    Park JS, Cho MK, Lee EJ, Ahn KY, Jung JH, Cho Y, Han SS, Kim YK, Lee J (2009) A highly sensitive and selective diagnostic assay based on virus nanoparticles. Nat Nanotech 4:259–264CrossRefGoogle Scholar
  103. 103.
    Stephanopoulos N, Carrico ZM, Francis MB (2009) Nanoscale integration of sensitizing chromophores and porphyrins with bacteriophage MS2. Angew Chem Int Ed 48:9498–9502CrossRefGoogle Scholar
  104. 104.
    Everts M, Saini V, Leddon JL, Kok RJ, Stoff-Khalili M, Preuss MA, Millican CL, Perkins G, Brown JM, Bagaria H, Nikles DE, Johnson DT, Zharov VP, Curiel DT (2006) Covalently linked Au nanoparticles to a viral vector: potential for combined phototermal and gene cancer therapy. Nano Lett 6:587–591PubMedCrossRefGoogle Scholar
  105. 105.
    Merzlyak A, Indrakanti S, Lee SW (2009) Genetically engineered nanofiber-like viruses for tissue regenerating materials. Nano Lett 9:846–852PubMedCrossRefGoogle Scholar
  106. 106.
    Culver JM, Dawson WO, Plonk K, Stubbs G (1995) Site-directed mutagenesis confirms the involvement of carboxylate groups in the disassembly of tobacco mosaic virus. Virology 206:724–730PubMedCrossRefGoogle Scholar
  107. 107.
    Ellard FM, Drew J, Blakemore WE, Stuart DI, King AMQ (1999) Evidence for the role of His-142 of protein 1C in the acid-induced disassembly of foot-and-mouth disease virus capsids. J Gen Virol 80:1911–1918PubMedCrossRefGoogle Scholar
  108. 108.
    Martín-Acebes MA, Vázquez-Calvo A, Rincón V, Mateu MG, Sobrino F (2011) A single amino acid substitution in the capsid of foot-and-mouth disease virus can increase acid resistance. J Virol 85:2733–2740PubMedCrossRefGoogle Scholar
  109. 109.
    Ashcroft AE, Lago H, Macedo JM, Horn WT, Stonehouse NJ, Stockley PG (2005) Engineering thermal stability in RNA phage capsids via disulphide bonds. J Nanosci Nanotechnol 5:2034–2041PubMedCrossRefGoogle Scholar
  110. 110.
    Porta C, Kotecha A, Burman A, Jackson T, Ren J, Loureiro S, Jones IM, Fry EE, Stuart DI, Charleston B (2013) Rational engineering of recombinant picornavirus capsids to produce safe, protective vaccine antigen. PLoS Pathog 9:e1003255PubMedPubMedCentralCrossRefGoogle Scholar
  111. 111.
    Mateo R, Luna E, Rincón V, Mateu MG (2008) Engineering viable foot-and-mouth disease viruses with increased thermostability as a step in the development of improved vaccines. J Virol 82:12232–12240PubMedPubMedCentralCrossRefGoogle Scholar
  112. 112.
    Rincón V, Rodríguez-Huete A, López-Argüello S, Ibarra-Molero B, Sanchez-Ruiz JM, Harmsen MM, Mateu MG (2014) Identification of the structural basis of thermal lability of a virus provide a rationale for improved vaccines. Structure 22:1560–1570PubMedCrossRefGoogle Scholar
  113. 113.
    Ivanovska IL et al (2004) Bacteriophage capsids: tough nanoshells with complex elastic properties. Proc Natl Acad Sci U S A 101:7600–7605PubMedPubMedCentralCrossRefGoogle Scholar
  114. 114.
    Roos WH, Wuite GJL (2009) Nanoindentation studies reveal material properties of viruses. Adv Mater 21:1187–1192CrossRefGoogle Scholar
  115. 115.
    Roos WH, Bruinsma R, Wuite GJL (2010) Physical virology. Nat Phys 6:733–743CrossRefGoogle Scholar
  116. 116.
    Mateu MG (2012) Mechanical properties of viruses analyzed by atomic force microscopy: a virological perspective. Virus Res 168:1–22PubMedCrossRefGoogle Scholar
  117. 117.
    De Pablo PJ, Mateu MG (2013) Mechanical properties of viruses. In: Mateu MG (ed) Structure and physics of viruses. Springer, Dordrecht, pp 519–551CrossRefGoogle Scholar
  118. 118.
    Michel JP, Ivanovska IL, Gibbons MM, Klug WS, Knobler CM, Wuite GJL, Schmidt CF (2006) Nanoindentation studies of full and empty viral capsids and the effects of protein mutations on elasticity and strength. Proc Natl Acad Sci U S A 103:6184–6189PubMedPubMedCentralCrossRefGoogle Scholar
  119. 119.
    Carrasco C, Castellanos M, de Pablo PJ, Mateu MG (2008) Manipulation of the mechanical properties of a virus by protein engineering. Proc Natl Acad Sci U S A 105:4150–4155PubMedPubMedCentralCrossRefGoogle Scholar
  120. 120.
    Castellanos M, de Pablo PJ, Mateu MG (2012) Mechanical elasticity as a physical signature of conformational dynamics in a virus particle. Proc Natl Acad Sci U S A 109:12028–12033PubMedPubMedCentralCrossRefGoogle Scholar
  121. 121.
    Castellanos M, Carrillo PJP, Mateu MG (2015) Quantitatively probing propensity for structural transitions in engineered virus nanoparticles by single-molecule mechanical analysis. Nanoscale 7:5654–5664PubMedCrossRefGoogle Scholar

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© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Centro de Biología Molecular “Severo Ochoa” (CSIC-UAM)Universidad Autónoma de MadridMadridSpain
  2. 2.Department of Molecular BiologyUniversidad Autónoma de MadridMadridSpain

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