Functional domains of the HK97 capsid maturation protease and the mechanisms of protein encapsidation

Journal of Molecular Biology

Volumn 425, Issue 15, 2013, Pages 2765-2781

  Duda, Robert L ^a   Oh, Bonnie ^a   Hendrix, Roger W ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

capsid maturation protein; targeting protein processsing; virus assembly

Indexed keywords

CAPSID PROTEIN; PROTEINASE;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIOPHAGE; BACTERIOPHAGE HK97; CARBOXY TERMINAL SEQUENCE; CATALYSIS; ENZYME ACTIVITY; ENZYME STRUCTURE; GENE INSERTION; IN VIVO STUDY; PRIORITY JOURNAL; PROTEIN DEGRADATION;

MIRIDAE;

EID: 84879937095     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2013.05.002     Document Type: Article

References (99)

1. H. Cheng, N. Shen, J. Pei, and N.V. Grishin Double-stranded DNA bacteriophage prohead protease is homologous to herpesvirus protease Protein Sci. 13 2004 2260 2269
2. J. Liu, and A. Mushegian Displacements of prohead protease genes in the late operons of double-stranded-DNA bacteriophages J. Bacteriol. 186 2004 4369 4375
3. L. Tong Viral proteases Chem. Rev. 102 2002 4609 4626
4. J.T. Hsu, H.C. Wang, G.W. Chen, and S.R. Shih Antiviral drug discovery targeting to viral proteases Curr. Pharm. Des. 12 2006 1301 1314
5. H. Steuber, and R. Hilgenfeld Recent advances in targeting viral proteases for the discovery of novel antivirals Curr. Top. Med. Chem. 10 2010 323 345
6. J.F. Conway, R.L. Duda, N. Cheng, R.W. Hendrix, and A.C. Steven Proteolytic and conformational control of virus capsid maturation: the bacteriophage HK97 system J. Mol. Biol. 253 1995 86 99
7. R.L. Duda, J. Hempel, H. Michel, J. Shabanowitz, D. Hunt, and R.W. Hendrix Structural transitions during bacteriophage HK97 head assembly J. Mol. Biol. 247 1995 618 635
8. R.L. Duda, K. Martincic, and R.W. Hendrix Genetic basis of bacteriophage HK97 prohead assembly J. Mol. Biol. 247 1995 636 647
9. R.L. Duda, K. Martincic, Z. Xie, and R.W. Hendrix Bacteriophage HK97 head assembly FEMS Microbiol. Rev. 17 1995 41 46
10. J. King, and S. Casjens Catalytic head assembling protein in virus morphogenesis Nature 251 1974 112 119
11. S. Casjens, and R.W. Hendrix Control mechanisms in dsDNA bacteriophage assembly R. Calendar, The Bacteriophages Vol. 1 1988 Plenum New York 15 91
12. R.A. Driedonks, and J. Caldentey Gene 20 product of bacteriophage T4 II. Its structural organization in prehead and bacteriophage J. Mol. Biol. 166 1983 341 360
13. R.A. Driedonks, A. Engel, B. tenHeggeler, and D. van Gene 20 product of bacteriophage T4 its purification and structure J. Mol. Biol. 152 1981 641 662
14. S. Casjens, and J. King P22 morphogenesis. I: catalytic scaffolding protein in capsid assembly J. Supramol. Struct. 2 1974 202 224
15. G.S. Roeder, and P.D. Sadowski Bacteriophage T7 morphogenesis: phage-related particles in cells infected with wild-type and mutant T7 phage Virology 76 1977 263 285
16. F.L. Homa, and J.C. Brown Capsid assembly and DNA packaging in herpes simplex virus Rev. Med. Virol. 7 1997 107 122
17. M.K. Showe, E. Isobe, and L. Onorato Bacteriophage T4 prehead proteinase I. Purification and properties of a bacteriophage enzyme which cleaves the capsid precursor proteins J. Mol. Biol. 107 1976 35 54
18. J.R. Chang, M.S. Spilman, C.M. Rodenburg, and T. Dokland Functional domains of the bacteriophage P2 scaffolding protein: identification of residues involved in assembly and protease activity Virology 384 2009 144 150
19. E. Medina, D. Wieczorek, E.M. Medina, Q. Yang, M. Feiss, and C.E. Catalano Assembly and maturation of the bacteriophage lambda procapsid: gpC is the viral protease J. Mol. Biol. 401 2010 813 830
20. R.W. Hendrix, and R.L. Duda Bacteriophage HK97 head assembly: a protein ballet Adv. Virus Res. 50 1998 235 288
21. M.P. Popa, T.A. McKelvey, J. Hempel, and R.W. Hendrix Bacteriophage HK97 structure: wholesale covalent cross-linking between the major head shell subunits J. Virol. 65 1991 3227 3237
22. I. Gertsman, L. Gan, M. Guttman, K. Lee, J.A. Speir, and R.L. Duda An unexpected twist in viral capsid maturation Nature 458 2009 646 650
23. C. Helgstrand, W.R. Wikoff, R.L. Duda, R.W. Hendrix, J.E. Johnson, and L. Liljas The refined structure of a protein catenane: the HK97 bacteriophage capsid at 3.44 Å resolution J. Mol. Biol. 334 2003 885 899
24. W.R. Wikoff, L. Liljas, R.L. Duda, H. Tsuruta, R.W. Hendrix, and J.E. Johnson Topologically linked protein rings in the bacteriophage HK97 capsid Science 289 2000 2129 2133
25. R.L. Duda Protein chainmail: catenated protein in viral capsids Cell 94 1998 55 60
26. J.F. Conway, W.R. Wikoff, N. Cheng, R.L. Duda, R.W. Hendrix, J.E. Johnson, and A.C. Steven Virus maturation involving large subunit rotations and local refolding Science 292 2001 744 748
27. R.L. Duda, P.D. Ross, N. Cheng, B.A. Firek, R.W. Hendrix, J.F. Conway, and A.C. Steven Structure and energetics of encapsidated DNA in bacteriophage HK97 studied by scanning calorimetry and cryo-electron microscopy J. Mol. Biol. 391 2009 471 483
28. L. Gan, J.F. Conway, B.A. Firek, N. Cheng, R.W. Hendrix, and A.C. Steven Control of crosslinking by quaternary structure changes during bacteriophage HK97 maturation Mol. Cell 14 2004 559 569
29. L. Gan, J.A. Speir, J.F. Conway, G. Lander, N. Cheng, and B.A. Firek Capsid conformational sampling in HK97 maturation visualized by X-ray crystallography and cryo-EM Structure 14 2006 1655 1665
30. R. Lata, J.F. Conway, N. Cheng, R.L. Duda, R.W. Hendrix, and W.R. Wikoff Maturation dynamics of a viral capsid: visualization of transitional intermediate states Cell 100 2000 253 263
31. K.K. Lee, L. Gan, H. Tsuruta, R.W. Hendrix, R.L. Duda, and J.E. Johnson Evidence that a local refolding event triggers maturation of HK97 bacteriophage capsid J. Mol. Biol. 340 2004 419 433
32. K.K. Lee, L. Gan, H. Tsuruta, C. Moyer, J.F. Conway, and R.L. Duda Virus capsid expansion driven by the capture of mobile surface loops Structure 16 2008 1491 1502
33. P.D. Ross, N. Cheng, J.F. Conway, B.A. Firek, R.W. Hendrix, R.L. Duda, and A.C. Steven Crosslinking renders bacteriophage HK97 capsid maturation irreversible and effects an essential stabilization EMBO J. 24 2005 1352 1363
34. P.D. Ross, J.F. Conway, N. Cheng, L. Dierkes, B.A. Firek, and R.W. Hendrix A free energy cascade with locks drives assembly and maturation of bacteriophage HK97 capsid J. Mol. Biol. 364 2006 512 525
35. W.R. Wikoff, J.F. Conway, J. Tang, K.K. Lee, L. Gan, and N. Cheng Time-resolved molecular dynamics of bacteriophage HK97 capsid maturation interpreted by electron cryo-microscopy and X-ray crystallography J. Struct. Biol. 153 2006 300 306
36. J.M. Benevides, P. Bondre, R.L. Duda, R.W. Hendrix, and G.J. Thomas Jr. Domain structures and roles in bacteriophage HK97 capsid assembly and maturation Biochemistry 43 2004 5428 5436
37. J.F. Conway, N. Cheng, P.D. Ross, R.W. Hendrix, R.L. Duda, and A.C. Steven A thermally induced phase transition in a viral capsid transforms the hexamers, leaving the pentamers unchanged J. Struct. Biol. 158 2007 224 232
38. R.K. Huang, R. Khayat, K.K. Lee, I. Gertsman, R.L. Duda, R.W. Hendrix, and J.E. Johnson The Prohead-I structure of bacteriophage HK97: implications for scaffold-mediated control of particle assembly and maturation J. Mol. Biol. 408 2011 541 554
39. Z. Xie, and R.W. Hendrix Assembly in vitro of bacteriophage HK97 proheads J. Mol. Biol. 253 1995 74 85
40. L. Baird, B. Lipinska, S. Raina, and C. Georgopoulos Identification of the Escherichia coli sohB gene, a multicopy suppressor of the HtrA (DegP) null phenotype J. Bacteriol. 173 1991 5763 5770
41. X. Qiu, C.A. Janson, J.S. Culp, S.B. Richardson, C. Debouck, W.W. Smith, and S.S. Abdel-Meguid Crystal structure of varicella-zoster virus protease Proc. Natl Acad. Sci. USA 94 1997 2874 2879
42. H.S. Shieh, R.G. Kurumbail, A.M. Stevens, R.A. Stegeman, E.J. Sturman, and J.Y. Pak Three-dimensional structure of human cytomegalovirus protease Nature 383 1996 279 282
43. L. Tong, C. Qian, M.J. Massariol, P.R. Bonneau, M.G. Cordingley, and L. Lagace A new serine-protease fold revealed by the crystal structure of human cytomegalovirus protease Nature 383 1996 272 275
44. P. Forrer, and R. Jaussi High-level expression of soluble heterologous proteins in the cytoplasm of Escherichia coli by fusion to the bacteriophage lambda head protein D Gene 224 1998 45 52
45. H. Iwai, P. Forrer, A. Pluckthun, and P. Guntert NMR solution structure of the monomeric form of the bacteriophage lambda capsid stabilizing protein gpD J. Biomol. NMR 31 2005 351 356
46. F. Yang, P. Forrer, Z. Dauter, J.F. Conway, N. Cheng, and M.E. Cerritelli Novel fold and capsid-binding properties of the lambda-phage display platform protein gpD Nat. Struct. Biol. 7 2000 230 237
47. L.J. McGuffin, K. Bryson, and D.T. Jones The PSIPRED protein structure prediction server Bioinformatics 16 2000 404 405
48. A. Lupas, M. Van Dyke, and J. Stock Predicting coiled coils from protein sequences Science 252 1991 1162 1164
49. Y. Li, J.F. Conway, N. Cheng, A.C. Steven, R.W. Hendrix, and R.L. Duda Control of virus assembly: HK97 "Whiffleball" mutant capsids without pentons J. Mol. Biol. 348 2005 167 182
50. M.K. Showe, and L.W. Black Assembly core of bacteriophage T4: an intermediate in head formation Nat. New Biol. 242 1973 70 75
51. A. Tsugita, L.W. Black, and M.K. Showe Protein cleavage during virus assembly: characterization of cleavage in T4 phage J. Mol. Biol. 98 1975 217 225
52. L.W. Black, and C. Ahmad-Zadeh Internal proteins of bacteriophage T4D: their characterization and relation to head structure and assembly J. Mol. Biol. 57 1971 71 92
53. M.B. Streiff, S. Iida, and T.A. Bickle Expression and proteolytic processing of the darA antirestriction gene product of bacteriophage P1 Virology 157 1987 167 171
54. B.V. Prasad, P.E. Prevelige, E. Marietta, R.O. Chen, D. Thomas, J. King, and W. Chiu Three-dimensional transformation of capsids associated with genome packaging in a bacterial virus J. Mol. Biol. 231 1993 65 74
55. R.A. Nelson, B.E. Reilly, and D.L. Anderson Morphogenesis of bacteriophage phi 29 of Bacillus subtilis: preliminary isolation and characterization of intermediate particles of the assembly pathway J. Virol. 19 1976 518 532
56. A. Droge, M.A. Santos, A.C. Stiege, J.C. Alonso, R. Lurz, T.A. Trautner, and P. Tavares Shape and DNA packaging activity of bacteriophage SPP1 procapsid: protein components and interactions during assembly J. Mol. Biol. 296 2000 117 132
57. M. Sutter, D. Boehringer, S. Gutmann, S. Gunther, D. Prangishvili, and M.J. Loessner Structural basis of enzyme encapsulation into a bacterial nanocompartment Nat. Struct. Mol. Biol. 15 2008 939 947
58. F. Akita, K.T. Chong, H. Tanaka, E. Yamashita, N. Miyazaki, and Y. Nakaishi The crystal structure of a virus-like particle from the hyperthermophilic archaeon Pyrococcus furiosus provides insight into the evolution of viruses J. Mol. Biol. 368 2007 1469 1483
59. K. Namba, K. Hagiwara, H. Tanaka, Y. Nakaishi, K.T. Chong, and E. Yamashita Expression and molecular characterization of spherical particles derived from the genome of the hyperthermophilic euryarchaeote Pyrococcus furiosus J. Biochem. 138 2005 193 199
60. J.A. Lengyel, R.N. Goldstein, M. Marsh, M.G. Sunshine, and R. Calendar Bacteriophage P2 head morphogenesis: cleavage of the major capsid protein Virology 53 1973 1 23
61. O.J. Marvik, P. Sharma, T. Dokland, and B.H. Lindqvist Bacteriophage P2 and P4 assembly: alternative scaffolding proteins regulate capsid size Virology 200 1994 702 714
62. M.W. Lubbers, N.R. Waterfield, T.P. Beresford, R.W. Le Page, and A.W. Jarvis Sequencing and analysis of the prolate-headed lactococcal bacteriophage c2 genome and identification of the structural genes Appl. Environ. Microbiol. 61 1995 4348 4356
63. G. Effantin, N. Figueroa-Bossi, G. Schoehn, L. Bossi, and J.F. Conway The tripartite capsid gene of Salmonella phage Gifsy-2 yields a capsid assembly pathway engaging features from HK97 and lambda Virology 402 2010 355 365
64. M. McClelland, K.E. Sanderson, J. Spieth, S.W. Clifton, P. Latreille, and L. Courtney Complete genome sequence of Salmonella enterica serovar Typhimurium LT2 Nature 413 2001 852 856
65. J.E. Shaw, and H. Murialdo Morphogenetic genes C and Nu3 overlap in bacteriophage lambda Nature 283 1980 30 35
66. T. Ziegelhoffer, P. Yau, G.N. Chandrasekhar, J. Kochan, C. Georgopoulos, and H. Murialdo The purification and properties of the scaffolding protein of bacteriophage lambda J. Biol. Chem. 267 1992 455 461
67. C. Georgopoulos, K. Tilly, and S. Casjens Lambdoid phage head assembly R.W. Hendrix, J.W. Roberts, F.W. Stahl, R.A. Weisberg, Lambda II 1983 Cold Spring Harbor Laboratory Cold Spring Harbor, New York 279 303
68. F.Y. Liu, and B. Roizman The herpes simplex virus 1 gene encoding a protease also contains within its coding domain the gene encoding the more abundant substrate J. Virol. 65 1991 5149 5156
69. W.W. Newcomb, F.L. Homa, D.R. Thomsen, Z. Ye, and J.C. Brown Cell-free assembly of the herpes simplex virus capsid J. Virol. 68 1994 6059 6063
70. V.G. Preston, M.F. al-Kobaisi, I.M. McDougall, and F.J. Rixon The herpes simplex virus gene UL26 proteinase in the presence of the UL26.5 gene product promotes the formation of scaffold-like structures J. Gen. Virol. 75 1994 2355 2366
71. D.J. McGeoch, M.A. Dalrymple, A.J. Davison, A. Dolan, M.C. Frame, and D. McNab The complete DNA sequence of the long unique region in the genome of herpes simplex virus type 1 J. Gen. Virol. 69 1988 1531 1574
72. L.W. Black, M.K. Showe, and A.C. Steven Morphogenesis of the T4 head J. Karam, Molecular Biology of Bacteriophage T4 1994 ASM Press Washington, DC 518 558
73. V.B. Rao, and L.W. Black Structure and assembly of bacteriophage T4 head Virol. J. 7 2010 356
74. J.M. Mullaney, and L.W. Black Capsid targeting sequence targets foreign proteins into bacteriophage T4 and permits proteolytic processing J. Mol. Biol. 261 1996 372 385
75. T. Dokland Scaffolding proteins and their role in viral assembly Cell. Mol. Life Sci. 56 1999 580 603
76. S. Wang, P. Palasingam, R.H. Nokling, B.H. Lindqvist, and T. Dokland In vitro assembly of bacteriophage P4 procapsids from purified capsid and scaffolding proteins Virology 275 2000 133 144
77. G.J. Morgan, G.F. Hatfull, S. Casjens, and R.W. Hendrix Bacteriophage Mu genome sequence: analysis and comparison with Mu-like prophages in Haemophilus, Neisseria and Deinococcus J. Mol. Biol. 317 2002 337 359
78. M.K. Showe, E. Isobe, and L. Onorato Bacteriophage T4 prehead proteinase. II. Its cleavage from the product of gene 21 and regulation in phage-infected cells J. Mol. Biol. 107 1976 55 69
79. E. Hintermann, and A. Kuhn Bacteriophage T4 gene 21 encodes two proteins essential for phage maturation Virology 189 1992 474 482
80. U.K. Laemmli Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 1970 680 685
81. C.L. Bair, D. Rifat, and L.W. Black Exclusion of glucosyl- hydroxymethylcytosine DNA containing bacteriophages is overcome by the injected protein inhibitor IPI* J. Mol. Biol. 366 2007 779 789
82. H. Rohrer, W. Zillig, and R. Mailhammer ADP-ribosylation of DNA-dependent RNA polymerase of Escherichia coli by an NAD +: protein ADP-ribosyltransferase from bacteriophage T4 Eur. J. Biochem. 60 1975 227 238
83. Y.R. Hong, and L.W. Black Protein folding studies in vivo with a bacteriophage T4 expression-packaging-processing vector that delivers encapsidated fusion proteins into bacteria Virology 194 1993 481 490
84. Y.R. Hong, and L.W. Black An expression-packaging-processing vector which selects and maintains 7-kb DNA inserts in the blue T4 phage genome Gene 136 1993 193 198
85. Y.R. Hong, J.M. Mullaney, and L.W. Black Protection from proteolysis using a T4::T7-RNAP phage expression-packaging-processing system Gene 162 1995 5 11
86. J.M. Mullaney, and L.W. Black GFP:HIV-1 protease production and packaging with a T4 phage expression-packaging processing system Biotechniques 25 1998 1008 1012
87. J.M. Mullaney, and L.W. Black Activity of foreign proteins targeted within the bacteriophage T4 head and prohead: implications for packaged DNA structure J. Mol. Biol. 283 1998 913 929
88. J.M. Mullaney, R.B. Thompson, Z. Gryczynski, and L.W. Black Green fluorescent protein as a probe of rotational mobility within bacteriophage T4 J. Virol. Methods 88 2000 35 40
89. D.P. Patterson, P.E. Prevelige, and T. Douglas Nanoreactors by programmed enzyme encapsulation inside the capsid of the bacteriophage P22 ACS Nano 6 2012 5000 5009
90. S. Kang, M. Uchida, A. O'Neil, R. Li, P.E. Prevelige, and T. Douglas Implementation of p22 viral capsids as nanoplatforms Biomacromolecules 11 2010 2804 2809
91. I.J. Minten, L.J. Hendriks, R.J. Nolte, and J.J. Cornelissen Controlled encapsulation of multiple proteins in virus capsids J. Am. Chem. Soc. 131 2009 17771 17773
92. J.K. Rhee, M. Hovlid, J.D. Fiedler, S.D. Brown, F. Manzenrieder, and H. Kitagishi Colorful virus-like particles: fluorescent protein packaging by the Qbeta capsid Biomacromolecules 12 2011 3977 3981
93. F.P. Seebeck, K.J. Woycechowsky, W. Zhuang, J.P. Rabe, and D. Hilvert A simple tagging system for protein encapsulation J. Am. Chem. Soc. 128 2006 4516 4517
94. C. Fan, S. Cheng, Y. Liu, C.M. Escobar, C.S. Crowley, and R.E. Jefferson Short N-terminal sequences package proteins into bacterial microcompartments Proc. Natl Acad. Sci. USA 107 2010 7509 7514
95. J.A. Thomas, S.T. Weintraub, W. Wu, D.C. Winkler, N. Cheng, A.C. Steven, and L.W. Black Extensive proteolysis of head and inner body proteins by a morphogenetic protease in the giant Pseudomonas aeruginosa phage phiKZ Mol. Microbiol. 84 2012 324 339
96. B. Keller, and T.A. Bickle The nucleotide sequence of gene 21 of bacteriophage T4 coding for the prohead protease Gene 49 1986 245 251
97. F.W. Studier, A.H. Rosenberg, J.J. Dunn, and J.W. Dubendorff Use of T7 RNA polymerase to direct expression of cloned genes Methods Enzymol. 185 1990 60 89
98. R.F. Lathe, M.P. Kieny, D. Schmitt, P. Curtis, and J.P. Lecocq M13 bacteriophage vectors for the expression of foreign proteins in Escherichia coli: the rabies glycoprotein J. Mol. Appl. Genet. 2 1984 331 342
99. G. Dreyfuss, S.A. Adam, and Y.D. Choi Physical change in cytoplasmic messenger ribonucleoproteins in cells treated with inhibitors of mRNA transcription Mol. Cell. Biol. 4 1984 415 423