Mechanism of Membranous Tunnelling Nanotube Formation in Viral Genome Delivery

PLoS Biology

Volumn 11, Issue 9, 2013, Pages

  Peralta, Bibiana ^a   Gil Carton, David ^a   Castaño Díez, Daniel ^b   Bertin, Aurelie ^c   Boulogne, Claire ^c   Oksanen, Hanna M ^d   Bamford, Dennis H ^d   Abrescia, Nicola G A ^a,e  

^a INSTITUTO DE SALUD CARLOS III   (Spain)

^b UNIVERSITY OF BASEL   (Switzerland)

^c INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

^d UNIVERSITY OF HELSINKI   (Finland)

^e BASQUE FOUNDATION FOR SCIENCE   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA; NANOTUBE;

ANTIBODY LABELING; ARTICLE; BACTERIAL MEMBRANE; BACTERIOPHAGE PRD1; CONTROLLED STUDY; CRYSTALLOGRAPHY; DNA PACKAGING; ELECTRON MICROSCOPY; ELECTRON TOMOGRAPHY; GENE TRANSLOCATION; MOLECULAR DYNAMICS; MORPHOLOGY; NONHUMAN; OSMOLARITY; POLYMERIZATION; PROTEIN CONFORMATION; PROTEIN INTERACTION; PROTEIN LIPID INTERACTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; VIRAL GENE DELIVERY SYSTEM; VIRION; VIRUS CAPSID; VIRUS GENOME;

BACTERIOPHAGE PRD1; CAPSID; CELL MEMBRANE; DNA, VIRAL; GENOME, VIRAL; MICROSCOPY, ELECTRON; NANOTUBES; SALMONELLA TYPHIMURIUM; VIRAL TAIL PROTEINS; VIRUS INTEGRATION;

EID: 84884543692     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001667     Document Type: Article

References (59)

1. Harrison SC, (2008) Viral membrane fusion. Nat Struct Mol Biol 15: 690-698.
2. Kadlec J, Loureiro S, Abrescia NG, Stuart DI, Jones IM, (2008) The postfusion structure of baculovirus gp64 supports a unified view of viral fusion machines. Nat Struct Mol Biol 15: 1024-1030.
3. Hu B, Margolin W, Molineux IJ, Liu J, (2013) The bacteriophage t7 virion undergoes extensive structural remodeling during infection. Science 339: 576-579.
4. Olia AS, Prevelige PE Jr, Johnson JE, Cingolani G, (2011) Three-dimensional structure of a viral genome-delivery portal vertex. Nat Struct Mol Biol 18: 597-603.
5. Liu X, Zhang Q, Murata K, Baker ML, Sullivan MB, et al. (2010) Structural changes in a marine podovirus associated with release of its genome into Prochlorococcus. Nat Struct Mol Biol 17: 830-836.
6. Oliveira L, Cuervo A, Tavares P, (2010) Direct interaction of the bacteriophage SPP1 packaging ATPase with the portal protein. J Biol Chem 285: 7366-7373.
7. Leiman PG, Chipman PR, Kostyuchenko VA, Mesyanzhinov VV, Rossmann MG, (2004) Three-dimensional rearrangement of proteins in the tail of bacteriophage T4 on infection of its host. Cell 118: 419-429.
8. Abrescia NG, Cockburn JJ, Grimes JM, Sutton GC, Diprose JM, et al. (2004) Insights into assembly from structural analysis of bacteriophage PRD1. Nature 432: 68-74.
9. Cockburn JJ, Abrescia NG, Grimes JM, Sutton GC, Diprose JM, et al. (2004) Membrane structure and interactions with protein and DNA in bacteriophage PRD1. Nature 432: 122-125.
10. Benson SD, Bamford JK, Bamford DH, Burnett RM, (1999) Viral evolution revealed by bacteriophage PRD1 and human adenovirus coat protein structures. Cell 98: 825-833.
11. Zhang X, Sun S, Xiang Y, Wong J, Klose T, et al. (2012) Structure of Sputnik, a virophage, at 3.5-A resolution. Proc Natl Acad Sci U S A 109: 18431-18436.
12. Abrescia NG, Grimes JM, Kivela HM, Assenberg R, Sutton GC, et al. (2008) Insights into virus evolution and membrane biogenesis from the structure of the marine lipid-containing bacteriophage PM2. Mol Cell 31: 749-761.
13. Khayat R, Tang L, Larson ET, Lawrence CM, Young M, et al. (2005) Structure of an archaeal virus capsid protein reveals a common ancestry to eukaryotic and bacterial viruses. Proc Natl Acad Sci U S A 102: 18944-18949.
14. Bowman BR, Baker ML, Rixon FJ, Chiu W, Quiocho FA, (2003) Structure of the herpesvirus major capsid protein. EMBO J 22: 757-765.
15. Nandhagopal N, Simpson AA, Gurnon JR, Yan X, Baker TS, et al. (2002) The structure and evolution of the major capsid protein of a large, lipid-containing DNA virus. Proc Natl Acad Sci U S A 99: 14758-14763.
16. Roberts MM, White JL, Grutter MG, Burnett RM, (1986) Three-dimensional structure of the adenovirus major coat protein hexon. Science 232: 1148-1151.
17. Abrescia NG, Bamford DH, Grimes JM, Stuart DI, (2012) Structure unifies the viral universe. Annu Rev Biochem 81: 795-822.
18. Bamford DH, Burnett RM, Stuart DI, (2002) Evolution of viral structure. Theor Popul Biol 61: 461-470.
19. Stromsten NJ, Bamford DH, Bamford JK, (2003) The unique vertex of bacterial virus PRD1 is connected to the viral internal membrane. J Virol 77: 6314-6321.
20. Karhu NJ, Ziedaite G, Bamford DH, Bamford JK, (2007) Efficient DNA packaging of bacteriophage PRD1 requires the unique vertex protein P6. J Virol 81: 2970-2979.
21. Gowen B, Bamford JK, Bamford DH, Fuller SD, (2003) The tailless icosahedral membrane virus PRD1 localizes the proteins involved in genome packaging and injection at a unique vertex. J Virol 77: 7863-7871.
22. Ziedaite G, Kivela HM, Bamford JK, Bamford DH, (2009) Purified membrane-containing procapsids of bacteriophage PRD1 package the viral genome. J Mol Biol 386: 637-647.
23. Huiskonen JT, Manole V, Butcher SJ, (2007) Tale of two spikes in bacteriophage PRD1. Proc Natl Acad Sci U S A 104: 6666-6671.
24. Jaatinen ST, Viitanen SJ, Bamford DH, Bamford JK, (2004) Integral membrane protein P16 of bacteriophage PRD1 stabilizes the adsorption vertex structure. J Virol 78: 9790-9797.
25. Xu L, Benson SD, Butcher SJ, Bamford DH, Burnett RM, (2003) The receptor binding protein P2 of PRD1, a virus targeting antibiotic-resistant bacteria, has a novel fold suggesting multiple functions. Structure 11: 309-322.
26. Zhang X, Xiang Y, Dunigan DD, Klose T, Chipman PR, et al. (2011) Three-dimensional structure and function of the Paramecium bursaria chlorella virus capsid. Proc Natl Acad Sci U S A 108: 14837-14842.
27. Cherrier MV, Kostyuchenko VA, Xiao C, Bowman VD, Battisti AJ, et al. (2009) An icosahedral algal virus has a complex unique vertex decorated by a spike. Proc Natl Acad Sci U S A 106: 11085-11089.
28. Xiao C, Kuznetsov YG, Sun S, Hafenstein SL, Kostyuchenko VA, et al. (2009) Structural studies of the giant mimivirus. PLoS Biol 7: e92 doi:10.1371/journal.pbio.1000092.
29. Zauberman N, Mutsafi Y, Halevy DB, Shimoni E, Klein E, et al. (2008) Distinct DNA exit and packaging portals in the virus Acanthamoeba polyphaga mimivirus. PLoS Biol 6: e114 doi:10.1371/journal.pbio.0060114.
30. Grahn AM, Daugelavicius R, Bamford DH, (2002) Sequential model of phage PRD1 DNA delivery: active involvement of the viral membrane. Mol Microbiol 46: 1199-1209.
31. Bamford D, Mindich L, (1982) Structure of the lipid-containing bacteriophage PRD1: disruption of wild-type and nonsense mutant phage particles with guanidine hydrochloride. J Virol 44: 1031-1038.
32. Kimura S, Hase K, Ohno H, (2012) Tunneling nanotubes: emerging view of their molecular components and formation mechanisms. Exp Cell Res 318: 1699-1706.
33. Gurke S, Barroso JF, Gerdes HH, (2008) The art of cellular communication: tunneling nanotubes bridge the divide. Histochem Cell Biol 129: 539-550.
34. San Martin C, Huiskonen JT, Bamford JK, Butcher SJ, Fuller SD, et al. (2002) Minor proteins, mobile arms and membrane-capsid interactions in the bacteriophage PRD1 capsid. Nat Struct Biol 9: 756-763.
35. Castano-Diez D, Kudryashev M, Arheit M, Stahlberg H, (2012) Dynamo: a flexible, user-friendly development tool for subtomogram averaging of cryo-EM data in high-performance computing environments. J Struct Biol 178: 139-151.
36. Happonen LJ, Oksanen E, Liljeroos L, Goldman A, Kajander T, Butcher SJ, (2013) The structure of the NTPase that powers DNA packaging into Sulfolobus turreted icosahedral virus 2. J Virol 87: 8388-8398.
37. Daugelavicius R, Bamford JK, Bamford DH, (1997) Changes in host cell energetics in response to bacteriophage PRD1 DNA entry. J Bacteriol 179: 5203-5210.
38. Lim HWG, Wortis M, Mukhopadhyay R, (2002) Stomatocyte-discocyte-echinocyte sequence of the human red blood cell: evidence for the bilayer- couple hypothesis from membrane mechanics. Proc Natl Acad Sci U S A 99: 16766-16769.
39. Sakashita A, Urakami N, Ziherl P, Imai M, (2012) Three-dimensional analysis of lipid vesicle transformations. Soft Matter 8: 8569-8581.
40. Li Y, Lipowsky R, Dimova R, (2011) Membrane nanotubes induced by aqueous phase separation and stabilized by spontaneous curvature. Proc Natl Acad Sci U S A 108: 4731-4736.
41. Derenyi I, Koster G, Van Duijn MM, Czovek A, Dogterom M, et al. (2007) Membrane nanotubes. In: H. LInke AM, editor. Controlled nanoscale motion, lect notes phys. Berlin Heidelberg: Springer-Verlag. pp. 141-159.
42. Stachowiak JC, Hayden CC, Sasaki DY, (2010) Steric confinement of proteins on lipid membranes can drive curvature and tubulation. Proc Natl Acad Sci U S A 107: 7781-7786.
43. Zimmerberg J, Kozlov MM, (2006) How proteins produce cellular membrane curvature. Nat Rev Mol Cell Biol 7: 9-19.
44. Grahn AM, Daugelavicius R, Bamford DH, (2002) The small viral membrane-associated protein P32 is involved in bacteriophage PRD1 DNA entry. J Virol 76: 4866-4872.
45. Jaatinen ST, Happonen LJ, Laurinmaki P, Butcher SJ, Bamford DH, (2008) Biochemical and structural characterisation of membrane-containing icosahedral dsDNA bacteriophages infecting thermophilic Thermus thermophilus. Virology 379: 10-19.
46. Aalto AP, Bitto D, Ravantti JJ, Bamford DH, Huiskonen JT, et al. (2012) Snapshot of virus evolution in hypersaline environments from the characterization of a membrane-containing Salisaeta icosahedral phage 1. Proc Natl Acad Sci U S A 109: 7079-7084.
47. Jaalinoja HT, Roine E, Laurinmaki P, Kivela HM, Bamford DH, et al. (2008) Structure and host-cell interaction of SH1, a membrane-containing, halophilic euryarchaeal virus. Proc Natl Acad Sci U S A 105: 8008-8013.
48. Jaakkola ST, Penttinen RK, Vilen ST, Jalasvuori M, Ronnholm G, et al. (2012) Closely related archaeal Haloarcula hispanica icosahedral viruses HHIV-2 and SH1 have nonhomologous genes encoding host recognition functions. J Virol 86: 4734-4742.
49. Fu CY, Johnson JE, (2012) Structure and cell biology of archaeal virus STIV. Curr Opin Virol 2: 122-127.
50. Bahar MW, Graham SC, Stuart DI, Grimes JM, (2011) Insights into the evolution of a complex virus from the crystal structure of vaccinia virus d13. Structure 19: 1011-1020.
51. Salas ML, Andres G, (2013) African swine fever virus morphogenesis. Virus Res 173: 29-41.
52. Mindich L, Bamford D, McGraw T, Mackenzie G, (1982) Assembly of bacteriophage PRD1: particle formation with wild-type and mutant viruses. J Virol 44: 1021-1030.
53. McDonald KL, Auer M, (2006) High-pressure freezing, cellular tomography, and structural cell biology. Biotechniques 41: 137, 139, 141 passim.
54. Mastronarde DN, (2005) Automated electron microscope tomography using robust prediction of specimen movements. J Struct Biol 152: 36-51.
55. Agulleiro JI, Fernandez JJ, (2011) Fast tomographic reconstruction on multicore computers. Bioinformatics 27: 582-583.
56. Kremer JR, Mastronarde DN, McIntosh JR, (1996) Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116: 71-76.
57. Sorzano CO, Marabini R, Velazquez-Muriel J, Bilbao-Castro JR, Scheres SH, et al. (2004) XMIPP: a new generation of an open-source image processing package for electron microscopy. J Struct Biol 148: 194-204.
58. Fernandez JJ, Li S, (2003) An improved algorithm for anisotropic nonlinear diffusion for denoising cryo-tomograms. J Struct Biol 144: 152-161.
59. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, et al. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25: 1605-1612.