Advertisement

Alkalinization of Icosahedral Non-enveloped Viral Capsid Interior Through Proton Channeling

  • Maria Marta Branda
  • Diego M. A. GuérinEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1215)

Abstract

Small icosahedral viruses have a compact capsid that apparently lacks holes through which solvents can be exchanged with the external milieu. However, due to the steric hindrance of amino acids, upon folding, capsid proteins form narrow cavities in which water and ions can be trapped. These occluded solvent molecules can form lines of water, called water wires, representing an arrangement with special features for proton conduction. In this chapter, we review the physico-chemical principles that permit proton conduction through protein cavities. We also describe how a combination of these elements found in an insect viral capsid can allow the virus to sense alkaline environments. Through this analysis, we stress the need to combine experimental and theoretical techniques when modeling complex biological systems.

Keywords

Proton diode Water wire pH sensing Grotthuss Triatoma virus 

Notes

Acknowledgements

We thank Dieter Blaas, Medical University of Vienna, Vienna Biocenter, A-1030, Austria, for critical reading and useful comments of the manuscript. MMB is a member of the CONICET research staff, Argentina, and she thanks a permit from the CONICET and UNS to do sabbatical stage at DMAG’s lab, Instituto Biofisika (CSIC, UPV/EHU). MMB thanks a traveling grant from the CYTED (216RT0506). This work was partially supported by a grant to DMAG from the Ministerio de Ciencia e Innovación (BFU2012-36241), and Gobierno Vasco (Elkartek KK-2017/00008), Spain.

References

  1. 1.
    Hackett BA, Yasunaga A, Panda D, Tartell MA, Hopkins KC, Hensley SE, Cherry S (2015) RNASEK is required for internalization of diverse acid-dependent viruses. PNAS 112(25):7797–7802PubMedGoogle Scholar
  2. 2.
    Penkler DL, Jiwaji M, Domitrovic T, Short JR, Johnson JE, Dorrington RA (2016) Binding and entry of a non-enveloped T1/44 insect RNA virus is triggered by alkaline pH. Virology 498:277–287PubMedGoogle Scholar
  3. 3.
    Appell HM, Martin MM (1990) Gut redox conditions in herbivorous lepidopteran larvae. J Chem Ecol 16:3277–3290Google Scholar
  4. 4.
    Agirre J, Aloria K, Arizmendi JM, Iloro I, Elortza F, Marti GA, Neumann E, Rey FA, Guérin DMA (2011) Capsid protein identification and analysis of Triatoma Virus (TrV) mature virions and naturally occurring empty particles. Virology 409:91–101PubMedPubMedCentralGoogle Scholar
  5. 5.
    Czibener C, La Torre JL, Muscio OA, Ugalde RA, Scodeller EA (2000) Nucleotide sequence analysis of Triatoma virus shows that it is a member of a novel group of insect RNA viruses. J Gen Virol 81:1149–1154PubMedGoogle Scholar
  6. 6.
    Muscio OA, La Torre JL, Scodeller EA (1987) Small nonoccluded viruses from triatomine bug Triatoma infestans (Hemiptera: Reduviidae). J Invertebr Pathol 49:218–220PubMedGoogle Scholar
  7. 7.
    Snijder J, Uetrecht C, Rose RJ, Sanchez-Eugenia R, Marti GA, Agirre J, Guérin DMA, Wuite GJL, Heck AJR, Roos WH (2013) Probing the biophysical interplay between a viral genome and its capsid. Nat Chem 5:502–509Google Scholar
  8. 8.
    Bonning BC, Miller WA (2010) Dicistroviruses. Annu Rev Entomol 55:129–150PubMedGoogle Scholar
  9. 9.
    Squires G, Pous J, Agirre J, Rozas-Dennis GS, Costabel MD, Marti GA, Navaza J, Bressanelli S, Guérin DM, Rey FA (2013) Structure of the Triatoma virus capsid. Acta Crystallogr D Biol Crystallogr 69(6):1026–1037PubMedPubMedCentralGoogle Scholar
  10. 10.
    Viso J, Belelli PG, Machado M, González H, Pantano S, Amundarain MJ, Zamarreño F, Branda MM, Guérin DMA, Costabel MD (2018) Multiscale modelization in a small virus: mechanism of proton channeling and its role in triggering capsid disassembly. PLoS Comput Biol 14(4):e1006082.  https://doi.org/10.1371/journal.pcbi.1006082 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Eisenman G, Oberhauser A, Benzanilla F (1988) Ion selectivity and molecular structure of binding sites and channels in icosahedral viruses in the 21st Jerusalem Symposyum on quantum chemistry. In: Pullman A, Jortner J, Pullman B (eds) Transport through membrane: carriers, channels and pumps. Kluwer Academic, Dordrecht, pp 27–50Google Scholar
  12. 12.
    Silva AM, Cachau RE, Goldstein DJ (1987) Ion channels in southern bean mosaic virus capsid. Biophys J 52:595–592PubMedPubMedCentralGoogle Scholar
  13. 13.
    Jiang Y, Lee A, Chen J, Ruta V, Cadene M, Chait BT, Mackinnon R (2003) X-ray structure of a voltage dependent K+ channel. Nature 423:33–41Google Scholar
  14. 14.
    Hogle JM, Chow M, Filman DJ (1985) Three-dimensional structure of poliovirus at 2.9 A resolution. Science 229:1358–1365PubMedPubMedCentralGoogle Scholar
  15. 15.
    Rossmann MG, Arnold F, Erickson JW, Frankenberger EA, Grifith JP, Hecht HJ, Johnson JE, Kamer G, Luo M, Mosser AG, Rueckert RR, Sherry B, Vriend G (1985) Structure of a human common cold virus and functional relationship to other picornaviruses. Nature 317:145–153Google Scholar
  16. 16.
    Agmon N, Bakker HJ, Campen RK, Henchman RH, Pohl P, Roke S, Thämer M, Hassanali A (2016) Protons and hydroxide ions in aqueous systems. Chem Rev 116:7642–7672PubMedGoogle Scholar
  17. 17.
    Chaplin MF (2018) Structure and properties of water in its various states. In: Maurice PA (ed) Encyclopedia of water: science, technology, and society. Wiley (in press)Google Scholar
  18. 18.
    Marx D, Tuckerman ME, Hutter J, Parrinello M (1999) The nature of the hydrated excess proton in water. Nature 397(6720):601–604Google Scholar
  19. 19.
    Agmon N (2000) Mechanism of hydroxide mobility. Chem Phys Lett 319:247–252Google Scholar
  20. 20.
    Asthagiri D, Pratt LR, Kress JD, Gomez MA (2003) The hydration state of OH (aq). Chem Phys Lett 380:530–535Google Scholar
  21. 21.
    Wraight CA (2006) Chance and design-proton transfer in water, channels and bioenergetic proteins. Biochim Biophys Acta 1757:886–912PubMedGoogle Scholar
  22. 22.
    Light TS, Licht S, Bevilacqua AC, Morash KR (2005) The fundamental conductivity and resistivity of water. Electrochem Solid-State Lett 8(1):16–19Google Scholar
  23. 23.
    Lehninger AL, Nelson DL, Cox MM (2005) Lehninger principles of biochemistry, 4th edn. WH Freeman, New York, p 46Google Scholar
  24. 24.
    Chung LW, Sameera WMC, Ramozzi R, Page AJ, Hatanaka M, Petrova GP, Harris TV, Li X, Ke Z, Liu F, Li H-B, Ding L, Morokuma K (2015) The ONIOM method and its applications. Chem Rev 115:5678–5796PubMedPubMedCentralGoogle Scholar
  25. 25.
    Simonson T, Carlsson J, Case DA (2004) Proton binding to proteins: pKa calculations with explicit and implicit solvent models. JACS 126:4167–4180Google Scholar
  26. 26.
    Cukierman SL (2006) Et tu, Grotthuss! and other unfinished stories. Biochim Biophys Acta Bioenerg 1757:876–885Google Scholar
  27. 27.
    de Grotthuss CJT (1806) Sur la décomposition de l’eau et des corps qu’elle tient en dissolution à l’aide de l’électricité galvanique (On the decomposition of water and of the bodies that it holds in solution by means of galvanic electricity). Ann Chim LVIII:54–74Google Scholar
  28. 28.
    Ceriotti M, Cuny J, Parrinello M, Manolopoulos DE (2013) Nuclear quantum effects and hydrogen bond fluctuations in water. Proc Natl Acad Sci 110:15591–15596PubMedGoogle Scholar
  29. 29.
    Hassanali A, Giberti F, Cuny J, Kühne TD, Parrinello M (2013) Proton transfer through the water gossamer. PNAS 110(34):13723–13728PubMedGoogle Scholar
  30. 30.
    Ruscic B (2013) Active thermochemical tables: water and water dimer. J Phys Chem A 117:11940–11953PubMedGoogle Scholar
  31. 31.
    Ch’ng LC, Samanta AK, Czakó G, Bowman JM, Reisler H (2012) Experimental and theoretical investigations of energy transfer and hydrogen-bond breaking in the water dimer. JACS 134:15430–15435Google Scholar
  32. 32.
    Riccardi D, Koňig P, Prat-Resina X, Yu H, Elstner M, Frauenheim T, Cui Q (2006) Proton holes in long-range proton transfer reactions in solution and enzymes: a theoretical analysis. JACS 128:16302–16311Google Scholar
  33. 33.
    Gordalla B, Müller MB, Frimmel FH (2007) The physicochemical properties of water and their relevance for life. In: Lozán JL, Grassl H, Hupfer P, Menzel L, Schönwiese C-D (eds) Global change: enough water for all? Wissenschaftliche Auswertungen, Hamburg. www.klima-warnsignale.uni-hamburg.de Google Scholar
  34. 34.
    Rasaiah JC, Garde S, Hummer G (2008) Water in nonpolar confinement: from nanotubes to proteins and beyond. Annu Rev Phys Chem 59:713–740PubMedGoogle Scholar
  35. 35.
    Beckstein O, Sansom MS (2003) Liquid–vapor oscillations of water in hydrophobic nanopores. Proc Natl Acad Sci U S A 100:7063–7068PubMedPubMedCentralGoogle Scholar
  36. 36.
    Hummer G, Rasaiah JC, Noworyta JP (2001) Water conduction through the hydrophobic channel of a carbon nanotube. Nature 414:188–190Google Scholar
  37. 37.
    Aryal P, Sansom MSP, Tucker SJ (2015) Hydrophobic gating in ion channels. J Mol Biol 427:121–130PubMedGoogle Scholar
  38. 38.
    Karahka ML, Kreuzer HJ (2013) Charge transport along proton wires. Biointerphases 8(13):1–9Google Scholar
  39. 39.
    Miyake T, Rolandi M (2016) Grotthuss mechanisms: from proton transport in proton wires to bioprotonic devices. J Phys Condens Matter 28(023001):1–11Google Scholar
  40. 40.
    Zhou J, Sharp LL, Tang HL, Lloyd SA, Billings S, Braun TF, Blair DF (1998) Function of protonatable residues in the flagellar motor of Escherichia coli: a critical role for Asp 32 of MotB. J Bacteriol 180:2729–2735PubMedPubMedCentralGoogle Scholar
  41. 41.
    Baudry J, Tajkhorshid E, Molnar F, Phillips J, Schulten K (2001) Molecular dynamics study of bacteriorhodopsin and the purple membrane. J Phys Chem B 105:905–918Google Scholar
  42. 42.
    Bondar AN, Baudry J, Suhai S, Fischer S, Smith JC (2008) Key role of active site wáter molecules in bacteriorhodopsin proton-transfer reactions. J Phys Chem B 112:14729–14741PubMedGoogle Scholar
  43. 43.
    Kandt C, Schlitter J, Gerwert K (2004) Dynamics of water molecules in the bacteriorhodopsin trimer in explicit lipid/water environment. Biophys J 86:705–717PubMedPubMedCentralGoogle Scholar
  44. 44.
    Wolf S, Freier E, Potschies M, Hofmann E, Gerwert K (2010) Directional proton transfer in membrane proteins achieved through protonated protein-bound water molecules: a proton diode. Angew Chem Int Ed 49:6889–6893Google Scholar
  45. 45.
    Chernyshev A, Armstrong KM, Cukierman S (2003) Proton transfer in gramicidin channels is modulated by the thickness of monoglyceride bilayers. Biophys J 84(1):238–250PubMedPubMedCentralGoogle Scholar
  46. 46.
    Aksimentiev A, Balabin IA, Fillingame RH, Schulten K (2004) Insights into the molecular mechanism of rotation in the Fo sector of ATP synthase. Biophys J 86:1332–1344PubMedPubMedCentralGoogle Scholar
  47. 47.
    Gianti E, Carnevale V, de Grado WF, Klein ML, Fiorin G (2015) Hydrogen-bonded water molecules in the M2 channel of the influenza A virus guide the binding preferences of ammonium-based inhibitors. J Phys Chem B 119:1173–1183PubMedGoogle Scholar
  48. 48.
    Liang R, Li H, Swanson JMJ, Voth GA (2014) Multiscale simulation reveals a multifaceted mechanism of proton permeation through the influenza A M2 proton channel. PNAS 111(26):9396–9401PubMedGoogle Scholar
  49. 49.
    Moffat JC, Vijayvergiya V, Gao PF, Cross TA, Woodbury DJ, Busath DD (2008) Proton transport through influenza a virus M2 protein reconstituted in vesicles. Biophys J 94:434–445PubMedGoogle Scholar
  50. 50.
    Maupin CM, Castillo N, Taraphder S, Tu C, McKenna R, Silverman DN, Voth GA (2011) Chemical rescue of enzymes: proton transfer in mutants of human carbonic anhydrase II. JACS 133:6223–6234Google Scholar
  51. 51.
    Lee HJ, Svahn E, Swanson JMJ, Lepp H, Voth GA, Brzezinski P, Gennis RB (2010) Intricate role of water in proton transport through cytochrome C oxidase. JACS 132:16225–16239Google Scholar
  52. 52.
    Xu J, Voth GA (2005) Computer simulation of explicit proton translocation in cytochrome C oxidase: the D pathway. PNAS 102(19):6795–6800PubMedGoogle Scholar
  53. 53.
    Zhao H, Sheng S, Hong Y, Zeng H (2014) Proton gradient-induced water transport mediated by water wires inside narrow aquapores of aquafoldamer molecules. JACS 136:14270–14276Google Scholar
  54. 54.
    Muñoz-Santiburcio D, Marx D (2016) On the complex structural diffusion of proton holes in nanoconfined alkaline solutions within slit pores. Nat Commun 7(12625):1–9Google Scholar
  55. 55.
    Matsuki Y, Iwamoto M, Mita K, Shigemi K, Matsunaga S, Oiki S (2016) Rectified proton Grotthuss conduction across a long water-wire in the test nanotube of the polytheonamide B channel. JACS 138:4168–4177Google Scholar
  56. 56.
    Tunuguntla RH, Allen FI, Kim K, Belliveau A, Noy A (2016) Ultrafast proton transport in sub-1-nm diameter carbon nanotube porins. Nat Nanotechnol 11:639–644PubMedGoogle Scholar
  57. 57.
    Hsu CH, Sehgal OP, Pickett EE (1976) Stabilizing effect of divalent metal ions on virions of southern bean mosaic virus. Virology 69:587–595PubMedGoogle Scholar
  58. 58.
    Hull R (1978) The stabilization of the particles of turnip rosette virus. III. Divalent cations. Virology 89(2):418–422PubMedGoogle Scholar
  59. 59.
    Abad-Zapatero C, Abdel-Meguid SS, Johnson JE, Leslie AGW, Rayment I, Rossmann MG, Suck D, Tsukihara T (1980) Structure of southern bean mosaic virus at 2.8 resolution. Nature 286:33–39PubMedPubMedCentralGoogle Scholar
  60. 60.
    Harrison SC, Olson AJ, Schutt CE, Winkler FK, Bricogne G (1978) Tomato bushy stunt at 2.9 resolution. Nature 276:368–373PubMedPubMedCentralGoogle Scholar
  61. 61.
    Abdel-Meguid SS, Yamane T, Fukuyama K, Rossmann MG (1981) The location of calcium ions in southern bean mosaic virus. Virology 114:81–85PubMedGoogle Scholar
  62. 62.
    Olson AJ, Bricogne G, Harrison SC (1983) Structure of tomato bushy stunt virus IV. The virus particle at 2.9 E resolution. J Mol Biol 171:61–93PubMedGoogle Scholar
  63. 63.
    Robinson IK, Harrison SC (1982) Structure of the expanded state of tomato bushy stunt virus. Nature 297:563–568Google Scholar
  64. 64.
    Montelius I, Liljas L, Unge T (1990) Sequential removal of Ca2+ from satellite tobacco necrosis virus. Crystal structure of two EDTA-treated forms. J Mol Biol 212:331–343PubMedGoogle Scholar
  65. 65.
    Kim S, Smith TJ, Chapman MS, Rossmann MG, Pevear DC, Dutko FJ, Felock PJ, Diana GD, McKinlay MA (1989) The crystal structure of human rhinovirus serotype 1A (HRV1A). J Mol Biol 210:91–111PubMedGoogle Scholar
  66. 66.
    Hadfield AT, Lee WM, Zhao R, Oliveira MA, Minor I, Rueckert RR, Rossmann MG (1997) The refined structure of human rhinovirus 16 at 2.15 Å resolution: implications for the viral life cycle. Structure 5:427–441PubMedGoogle Scholar
  67. 67.
    Oliveira MA, Zhao R, Lee WM, Kremer MJ, Minor I, Rueckert RR, Diana GD, Pevear DC, Dutko FJ, McKinlay MA, Rossmann MG (1993) The structure of human rhinovirus 16. Structure 1:51–68PubMedGoogle Scholar
  68. 68.
    Zhao R, Pevear DC, Kremer MJ, Giranda VL, Kofron JA, Kuhn RJ, Rossmann MG (1996) Human rhinovirus 3 at 3.0 Å resolution. Structure 4:1205–1220PubMedGoogle Scholar
  69. 69.
    Filman DJ, Syed R, Chow M, Macadam AJ, Minor PD, Hogle JM (1989) Structural factors that control conformational transitions and serotype specificity in type 3 poliovirus. EMBO J 8(5):1567–1579PubMedPubMedCentralGoogle Scholar
  70. 70.
    Muckelbauer JK, Kremer M, Minor I, Diana G, Dutko FJ, Groarke J, Pevear DC, Rossmann MG (1995) The structure of coxsackievirus B3 at 3.5 Å resolution. Structure 3:653–667PubMedGoogle Scholar
  71. 71.
    Tate J, Liljas L, Scotti P, Christian P, Lin T, Johnson JE (1999) The crystal structure of cricket paralysis virus: the first view of a new virus family. Nat Struct Biol 6:765–774PubMedGoogle Scholar
  72. 72.
    Spurny R, Přidal A, Pálková L, Khanh Tran Kiem H, de Miranda JR, Plevka P (2017) Virion structure of black queen cell virus, a common honeybee pathogen. J Virol 91(6):e02100–e02116.  https://doi.org/10.1128/JVI.02100-16 CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Unge T, Montelius I, Liljas L, Öfverstedt L-G (1986) The EDTA-treated expanded satellite tobacco necrosis virus: biochemical properties and crystallisation. Virology 152:207–218PubMedGoogle Scholar
  74. 74.
    Zhao R, Hadfield AT, Kremer MJ, Rossmann MG (1997) Cations in human rhinoviruses. Virology 227:13–23PubMedGoogle Scholar
  75. 75.
    Kalko SG, Cachau RE, Silva AM (1992) Ion channels in icosahedral virus: a comparative analysis of the structures and binding sites at their five-fold axes. Biophys J 63:1133–1145PubMedPubMedCentralGoogle Scholar
  76. 76.
    Martín-González N, Guérin Darvas SM, Durana A, Marti GA, Guérin DMA, de Pablo PJ (2018) Exploring the role of genome and structural ions in preventing viral capsid collapse during dehydration. J Phys Condens Matter 30(10):104001.  https://doi.org/10.1088/1361-648X/aaa944 CrossRefPubMedGoogle Scholar
  77. 77.
    Cherny VV, Morgan D, Musset B, Chaves G, Smith SME, DeCoursey TE (2015) Tryptophan 207 is crucial to the unique properties of the human voltage-gated proton channel, hHV1. J Gen Physiol 146(5):343–356PubMedPubMedCentralGoogle Scholar
  78. 78.
    DeCoursey TE, Morgan D, Musset B, Cherny VV (2016) Insights into the structure and function of HV1 from a meta-analysis of mutation studies. J Gen Physiol 148(2):97–118PubMedPubMedCentralGoogle Scholar
  79. 79.
    Castillo K, Pupo A, Baez-Nieto D, Contreras GF, Morera FJ, Neely A, Latorre R, Gonzalez C (2015) Voltage-gated proton (Hv1) channels, a singular voltage sensing domain. FEBS Lett 589:3471–3478PubMedGoogle Scholar
  80. 80.
    Agirre J, Goret G, LeGoff M, Sánchez-Eugenia R, Marti GA, Navaza J, Guérin DMA, Neumann E (2013) Cryo-electron microscopy reconstructions of Triatoma virus particles: a clue to unravel genome delivery and capsid disassembly. J Gen Virol 94(Pt 5):1058–1068PubMedGoogle Scholar
  81. 81.
    Li Q, Yafal AG, Lee YM, Hogle J, Chow M (1994) Poliovirus neutralization by antibodies to internal epitopes of VP4 and VP1 results from reversible exposure of these sequences at physiological temperature. J Virol 68:3965–3970PubMedPubMedCentralGoogle Scholar
  82. 82.
    Broo K, Wei J, Marshall D, Brown F, Smith TJ, Johnson JE, Schneemann A, Siuzdak G (2001) Viral capsid mobility: a dynamic conduit for inactivation. PNAS 98(5):2274–2277PubMedGoogle Scholar
  83. 83.
    Kremser L, Petsch M, Blaas D, Kenndler E (2004) Labeling of capsid proteins and genomic RNA of human rhinovirus with two different fluorescent dyes for selective detection by capillary electrophoresis. Anal Chem 76(24):7360–7365PubMedGoogle Scholar
  84. 84.
    Yuan H, Li P, Ma X, Lu Z, Sun P, Bai X, Zhang J, Bao H, Cao Y, Li D et al (2017) The pH stability of foot-and-mouth disease virus. Virol J 14:233PubMedPubMedCentralGoogle Scholar
  85. 85.
    Acharya R et al (2010) Structure and mechanism of proton transport through the transmembrane tetrameric M2 protein bundle of the influenza A virus. Proc Natl Acad Sci U S A 107:15075–15080PubMedPubMedCentralGoogle Scholar
  86. 86.
    Thomaston JL, Alfonso-Prieto M, Woldeyes RA, Fraser JS, Klein ML, Fiorin G, DeGrado WF (2015) High-resolution structures of the M2 channel from influenza A virus reveal dynamic pathways for proton stabilization and transduction. Proc Natl Acad Sci USA 112(46):14260–14265PubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Departamento de FísicaUniversidad Nacional del Sur (DF-UNS), and GRUMASICA, IFISUR (UNS/CONICET)Bahía BlancaArgentina
  2. 2.Present address: Instituto de Física Aplicada (INFAP, CONICET-UNSL)Ciudad de San LuisArgentina
  3. 3.Department of Biochemistry and Molecular BiologyInstituto Biofisika (UPV/EHU, CSIC), University of the Basque Country (EHU)LeioaSpain

Personalised recommendations