1hx6 › Citations

The X-ray crystal structure of P3, the major coat protein of the lipid-containing bacteriophage PRD1, at 1.65 A resolution.

Benson SD, Bamford JK, Bamford DH, Burnett RM
Acta Crystallogr D Biol Crystallogr 58 39-59 (2002)
Cited: 30 times
EuropePMC logo PMID: 11752778

Abstract

P3 has been imaged with X-ray crystallography to reveal a trimeric molecule with strikingly similar characteristics to hexon, the major coat protein of adenovirus. The structure of native P3 has now been extended to 1.65 A resolution (R(work) = 19.0% and R(free) = 20.8%). The new high-resolution model shows that P3 forms crystals through hydrophobic patches solvated by 2-methyl-2,4-pentanediol molecules. It reveals details of how the molecule's high stability may be achieved through ordered solvent in addition to intra- and intersubunit interactions. Of particular importance is a 'puddle' at the top of the molecule containing a four-layer deep hydration shell that cross-links a complex structural feature formed by 'trimerization loops'. These loops also link subunits by extending over a neighbor to reach the third subunit in the trimer. As each subunit has two eight-stranded viral jelly rolls, the trimer has a pseudo-hexagonal shape to allow close packing in its 240 hexavalent capsid positions. Flexible regions in P3 facilitate these interactions within the capsid and with the underlying membrane. A selenometh-ionine P3 derivative, with which the structure was solved, has been refined to 2.2 A resolution (R(work) = 20.1% and R(free) = 22.8%). The derivatized molecule is essentially unchanged, although synchrotron radiation has the curious effect of causing it to rotate about its threefold axis. P3 is a second example of a trimeric 'double-barrel' protein that forms a stable building block with optimal shape for constructing a large icosahedral viral capsid. A major difference is that hexon has long variable loops that distinguish different adenovirus species. The short loops in P3 and the severe constraints of its various interactions explain why the PRD1 family has highly conserved coat proteins.

Reviews - 1hx6 mentioned but not cited (2)

  1. The Baltimore Classification of Viruses 50 Years Later: How Does It Stand in the Light of Virus Evolution? Koonin EV, Krupovic M, Agol VI. Microbiol Mol Biol Rev 85 e0005321 (2021)
  2. Superimposition of Viral Protein Structures: A Means to Decipher the Phylogenies of Viruses. Ravantti JJ, Martinez-Castillo A, Abrescia NGA. Viruses 12 E1146 (2020)

Articles - 1hx6 mentioned but not cited (6)

  1. Structure and host-cell interaction of SH1, a membrane-containing, halophilic euryarchaeal virus. Jäälinoja HT, Roine E, Laurinmäki P, Kivelä HM, Bamford DH, Butcher SJ. Proc Natl Acad Sci U S A 105 8008-8013 (2008)
  2. Familial relationships in hyperthermo- and acidophilic archaeal viruses. Happonen LJ, Redder P, Peng X, Reigstad LJ, Prangishvili D, Butcher SJ. J Virol 84 4747-4754 (2010)
  3. Virus found in a boreal lake links ssDNA and dsDNA viruses. Laanto E, Mäntynen S, De Colibus L, Marjakangas J, Gillum A, Stuart DI, Ravantti JJ, Huiskonen JT, Sundberg LR. Proc Natl Acad Sci U S A 114 8378-8383 (2017)
  4. Cellular homologs of the double jelly-roll major capsid proteins clarify the origins of an ancient virus kingdom. Krupovic M, Makarova KS, Koonin EV. Proc Natl Acad Sci U S A 119 e2120620119 (2022)
  5. Four principles to establish a universal virus taxonomy. Simmonds P, Adriaenssens EM, Zerbini FM, Abrescia NGA, Aiewsakun P, Alfenas-Zerbini P, Bao Y, Barylski J, Drosten C, Duffy S, Duprex WP, Dutilh BE, Elena SF, García ML, Junglen S, Katzourakis A, Koonin EV, Krupovic M, Kuhn JH, Lambert AJ, Lefkowitz EJ, Łobocka M, Lood C, Mahony J, Meier-Kolthoff JP, Mushegian AR, Oksanen HM, Poranen MM, Reyes-Muñoz A, Robertson DL, Roux S, Rubino L, Sabanadzovic S, Siddell S, Skern T, Smith DB, Sullivan MB, Suzuki N, Turner D, Van Doorslaer K, Vandamme AM, Varsani A, Vasilakis N. PLoS Biol 21 e3001922 (2023)
  6. Bacteriophage PRD1 as a nanoscaffold for drug loading. Duyvesteyn HME, Santos-Pérez I, Peccati F, Martinez-Castillo A, Walter TS, Reguera D, Goñi FM, Jiménez-Osés G, Oksanen HM, Stuart DI, Abrescia NGA. Nanoscale 13 19875-19883 (2021)


Reviews citing this publication (3)

  1. Adenovirus structure. Rux JJ, Burnett RM. Hum Gene Ther 15 1167-1176 (2004)
  2. Principles of virus structural organization. Prasad BV, Schmid MF. Adv Exp Med Biol 726 17-47 (2012)
  3. Membrane-containing viruses with icosahedrally symmetric capsids. Huiskonen JT, Butcher SJ. Curr Opin Struct Biol 17 229-236 (2007)

Articles citing this publication (19)

  1. Does common architecture reveal a viral lineage spanning all three domains of life? Benson SD, Bamford JK, Bamford DH, Burnett RM. Mol Cell 16 673-685 (2004)
  2. The structure and evolution of the major capsid protein of a large, lipid-containing DNA virus. Nandhagopal N, Simpson AA, Gurnon JR, Yan X, Baker TS, Graves MV, Van Etten JL, Rossmann MG. Proc Natl Acad Sci U S A 99 14758-14763 (2002)
  3. The structure of the human adenovirus 2 penton. Zubieta C, Schoehn G, Chroboczek J, Cusack S. Mol Cell 17 121-135 (2005)
  4. Constituents of SH1, a novel lipid-containing virus infecting the halophilic euryarchaeon Haloarcula hispanica. Bamford DH, Ravantti JJ, Rönnholm G, Laurinavicius S, Kukkaro P, Dyall-Smith M, Somerharju P, Kalkkinen N, Bamford JK. J Virol 79 9097-9107 (2005)
  5. Insights into the evolution of a complex virus from the crystal structure of vaccinia virus D13. Bahar MW, Graham SC, Stuart DI, Grimes JM. Structure 19 1011-1020 (2011)
  6. Membrane proteins modulate the bilayer curvature in the bacterial virus Bam35. Laurinmäki PA, Huiskonen JT, Bamford DH, Butcher SJ. Structure 13 1819-1828 (2005)
  7. The structure of the bacteriophage PRD1 spike sheds light on the evolution of viral capsid architecture. Merckel MC, Huiskonen JT, Bamford DH, Goldman A, Tuma R. Mol Cell 18 161-170 (2005)
  8. Binding of adenovirus capsid to dipalmitoyl phosphatidylcholine provides a novel pathway for virus entry. Balakireva L, Schoehn G, Thouvenin E, Chroboczek J. J Virol 77 4858-4866 (2003)
  9. The unique vertex of bacterial virus PRD1 is connected to the viral internal membrane. Strömsten NJ, Bamford DH, Bamford JK. J Virol 77 6314-6321 (2003)
  10. The receptor binding protein P2 of PRD1, a virus targeting antibiotic-resistant bacteria, has a novel fold suggesting multiple functions. Xu L, Benson SD, Butcher SJ, Bamford DH, Burnett RM. Structure 11 309-322 (2003)
  11. Length variations amongst protein domain superfamilies and consequences on structure and function. Sandhya S, Rani SS, Pankaj B, Govind MK, Offmann B, Srinivasan N, Sowdhamini R. PLoS One 4 e4981 (2009)
  12. Diffraction quality crystals of PRD1, a 66-MDa dsDNA virus with an internal membrane. Bamford JK, Cockburn JJ, Diprose J, Grimes JM, Sutton G, Stuart DI, Bamford DH. J Struct Biol 139 103-112 (2002)
  13. Automatic comparison and classification of protein structures. Ravantti J, Bamford D, Stuart DI. J Struct Biol 183 47-56 (2013)
  14. Generation of filamentous instead of icosahedral particles by repression of African swine fever virus structural protein pB438L. Epifano C, Krijnse-Locker J, Salas ML, Salas J, Rodríguez JM. J Virol 80 11456-11466 (2006)
  15. Identification of a ligand on the Wip1 bacteriophage highly specific for a receptor on Bacillus anthracis. Kan S, Fornelos N, Schuch R, Fischetti VA. J Bacteriol 195 4355-4364 (2013)
  16. Probing the ability of the coat and vertex protein of the membrane-containing bacteriophage PRD1 to display a meningococcal epitope. Huiskonen JT, Laakkonen L, Toropainen M, Sarvas M, Bamford DH, Bamford JK. Virology 310 267-279 (2003)
  17. Integral membrane protein P16 of bacteriophage PRD1 stabilizes the adsorption vertex structure. Jaatinen ST, Viitanen SJ, Bamford DH, Bamford JK. J Virol 78 9790-9797 (2004)
  18. Sequence and Structure Analysis of Distantly-Related Viruses Reveals Extensive Gene Transfer between Viruses and Hosts and among Viruses. Caprari S, Metzler S, Lengauer T, Kalinina OV. Viruses 7 5388-5409 (2015)
  19. Selenomethionine labeling of large biological macromolecular complexes: probing the structure of marine bacterial virus PM2. Kivelä HM, Abrescia NG, Bamford JK, Grimes JM, Stuart DI, Bamford DH. J Struct Biol 161 204-210 (2008)


Related citations provided by authors (4)

  1. Viral Evolution Revealed by Bacteriophage PRD1 and Human Adenovirus Coat Protein Structures. Benson SD, Bamford JK, Bamford DH, Burnett RM Cell 98 825-833 (1999)
  2. Crystallization of the Major Coat Protein of PRD1, a Bacteriophage with an Internal Membrane. Stewart PL, Ghosh S, Bamford DH, Burnett RM J. Mol. Biol. 230 349-352 (1993)
  3. Capsomer Proteins of Bacteriophage PRD1, a Bacterial Virus with a Membrane. Bamford JK, Bamford DH Virology 177 445-451 (1990)
  4. Type-specific Epitope Locations Revealed by X-ray Crystallographic Study of Adenovirus Type 5 Hexon. Rux JJ, Burnett RM Mol. Ther. 1 18-30 (2000)

Quick links