Summary.
To study the interaction between lipopolysaccharide and protein, a comparative approach was employed using seven Salmonella enterica serovar Typhimurium typing phages as the protein model systems. This interaction has been studied in detail in the Salmonella enterica serovar Typhimurium phage P22 system and involves only the viral tailspike protein. Similarity between these phages and phage P22 was monitored in this Report by assaying restriction endonuclease digestions, capsid size, reactivity to the P22 tailspike protein monoclonal antibody, mAb92, which reacts with the N-terminus of the P22 tail protein and the ability to produce a PCR fragment using primers made to the ends of the P22 tailspike gene. The data indicate that tailspike similarity exists between most of these phages and a scheme reclassifying them is presented and that the N-terminus of the P22 tailspike protein may be a motif for many phage systems and may serve as a aid in the taxonomy of phages. The data suggest a classification scheme in which the N-terminus of some tailspike proteins (head-binding region in some tail proteins) may play a critical element role in the classification of Salmonella viruses.
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References
HW Ackermann (2003) ArticleTitleBacteriophage observations and evolution. Res Microbiol 154 245–251 Occurrence Handle10.1016/S0923-2508(03)00067-6 Occurrence Handle12798228 Occurrence Handle1:CAS:528:DC%2BD3sXkt1ymur4%3D
ES Anderson LR Ward M De Saxe JDH De Sa (1977) ArticleTitleBacteriophage-typing designations of Salmonella typhimurium. J Hyg Camb 78 297–300 Occurrence Handle321679 Occurrence Handle1:STN:280:DyaE2s7kt1Cquw%3D%3D
H Brussow RW Hendrix (2003) ArticleTitlePhage genomics: small is beautiful. Cell 108 13–16
BR Callow (1959) ArticleTitleA new phage-typing scheme for Salmonella typhimurium. J Hyg 57 346–359 Occurrence Handle1:STN:280:DyaF3c7islChtA%3D%3D Occurrence Handle10.1017/S0022172400020209
S Casjens G Hatful R Hendrix (1992) ArticleTitleEvolution of dsDNA tailed-bacteriophage genomes. Semin Virol 3 383–397 Occurrence Handle1:CAS:528:DyaK3sXitV2jsb8%3D
SR Casjens EB Gilcrease DA Winn-Stapley P Schicklmaier H Schmieger ML Pedulla ME Ford JM Houtz GF Hatfull RW Hendrix (2005) ArticleTitleThe generalized transducing Salmonella bacteriophage ES18: complete genome sequence and DNA packaging strategy. J Bacteriol 187 1091–1104 Occurrence Handle10.1128/JB.187.3.1091-1104.2005 Occurrence Handle15659686 Occurrence Handle1:CAS:528:DC%2BD2MXhtFyisbs%3D
C Canchaya C Proux G Fournous A Bruttin H Brüssow (2003) ArticleTitleProphage genomics. Microbiol Mol Biol Rev 67 238–276 Occurrence Handle12794192 Occurrence Handle1:CAS:528:DC%2BD3sXlsVeht7k%3D
B Chen J King (1991) ArticleTitleThermal unfolding pathway for the thermostable P22 tailspike endorhamnosidase. Biochemistry 30 6260–6269 Occurrence Handle2059632 Occurrence Handle1:CAS:528:DyaK3MXktVent7g%3D
JE Chua PA Manning R Morona (1999) ArticleTitleThe Shigella flexneri bacteriophage Sf6 tailspike protein (TSP)/endorhamnosidase is related to the bacteriophage P22 TSP and has a motif common to exo- and endoglycanases, and C-5 epimerases. Microbiology 145 1649–1659 Occurrence Handle10439404 Occurrence Handle1:CAS:528:DyaK1MXkvFahtLk%3D Occurrence Handle10.1099/13500872-145-7-1649
AJ Clark W Inwood T Cloutier TS Dillon (2001) ArticleTitleNucleotide sequence of coliphage HK620 and the evolution of lambdoid phages. J Bacteriol 311 657–679 Occurrence Handle1:CAS:528:DC%2BD3MXmtFGgtrc%3D
W Demczuk R Ahmed H-W Ackermann (2004) ArticleTitleMorphology of Salmonella enterica serovar Heidelberg typing phages. Can J Microbiol 50 873–875 Occurrence Handle10.1139/w04-075 Occurrence Handle15644903 Occurrence Handle1:CAS:528:DC%2BD2MXjtVantQ%3D%3D
W Demczuk R Ahmed H-W Ackermann (2003) ArticleTitlePhage-based typing scheme for Salmonella enterica serovar Heidelberg, a causative agent for food poisoning in Canada. J Clin Microbiol 41 4279–4284 Occurrence Handle10.1128/JCM.41.9.4279-4284.2003 Occurrence Handle12958257 Occurrence Handle1:CAS:528:DC%2BD3sXnvFaqtb8%3D
AT Dobbins M George SuffixJr DA Basham ME Ford JM Houtz ML Pedulla JG Lawrence GF Hatfull RW Hendrix (2004) ArticleTitleComplete genomic sequence of the virulent Salmonella bacteriophage SP6. J Bacteriol 186 1933–1944 Occurrence Handle10.1128/JB.186.7.1933-1944.2004 Occurrence Handle15028677 Occurrence Handle1:CAS:528:DC%2BD2cXivVylsrs%3D
A Freiberg R Morona L Van Den Bosch C Jung J Behlke N Carlin R Seckler U Baxa (2003) ArticleTitleThe tailspike protein of Shigella phage Sf6. A structural homolog of Salmonella phage P22 tailspike protein without sequence similarity in the b-helix domain. J Biol Chem 278 1542–1548 Occurrence Handle10.1074/jbc.M205294200 Occurrence Handle12424253 Occurrence Handle1:CAS:528:DC%2BD3sXisFyhsQ%3D%3D
B Friguet L Djavadi-Ohaniance C Haase-Pettingell J King ME Goldberg (1990) ArticleTitleProperties of monoclonal antibodies selected for probing the conformation of wild type and mutant forms of the P22 tailspike endorhamnosidase. J Biol Chem 265 10347–10351 Occurrence Handle2141331 Occurrence Handle1:CAS:528:DyaK3cXkvFeqt74%3D
B Friguet L Djavadi-Ohaniance J King ME Goldberg (1994) ArticleTitleIn vitro and ribosome-bound folding intermediates of P22 tailspike protein directed with monoclonal antibodies. J Biol Chem 269 15945–15949 Occurrence Handle7515066 Occurrence Handle1:CAS:528:DyaK2cXkt12mt7s%3D
DP Goldenberg PB Berget J King (1982) ArticleTitleMaturation of the tail spike endorhamnosidase of Salmonella phage P22. J Biol Chem 257 7864–7871 Occurrence Handle7045114 Occurrence Handle1:CAS:528:DyaL38Xks12is74%3D
M Greenberg J Dunlap R Villafane (1995) ArticleTitleIdentification of the tailspike protein from the Salmonella newington phage epsilon 34 and partial characterization of its phage-associated properties. J Struct Biol 115 283–289 Occurrence Handle10.1006/jsbi.1995.1053 Occurrence Handle8573470 Occurrence Handle1:CAS:528:DyaK28XhtVyit7g%3D
E Haggard-Ljungquist C Halling R Calendar (1992) ArticleTitleDNA sequences of the tail fiber genes of bacteriophage P2: evidence for horizontal transfer of tail fiber genes among unrelated bacteriophages. J Bacteriol 174 1462–1477 Occurrence Handle1531648 Occurrence Handle1:STN:280:DyaK387msFOhsg%3D%3D
RW Hendrix GF Hatfull MC Smith (2003) ArticleTitleBacteriophages with tails: chasing their origins and evolution. Res Microbiol 154 253–257 Occurrence Handle10.1016/S0923-2508(03)00068-8 Occurrence Handle12798229 Occurrence Handle1:CAS:528:DC%2BD3sXkt1ymur8%3D
RW Hendrix MCM Smith RN Burns ME Ford GF Hatfull (1999) ArticleTitleEvolutionary relationships among diverse bacteriophages and prophages: All the world’s a phage. Proc Natl Acad Sci 96 2192–2197 Occurrence Handle10.1073/pnas.96.5.2192 Occurrence Handle10051617 Occurrence Handle1:CAS:528:DyaK1MXhvVSqsbg%3D
Jain M, Evans MS, King J, Clark PL (2005) Monoclonal antibody epitope mapping describes tailspike b-helix folding and aggregation intermediates. J Biol Chem (in press)
JG Lawrence GF Hatfull RW Hendrix (2002) ArticleTitleImbroglios of viral taxonomy: genetic exchange and failings of phenetic approaches. J Bacteriol 184 4891–4905 Occurrence Handle10.1128/JB.184.17.4891-4905.2002 Occurrence Handle12169615 Occurrence Handle1:CAS:528:DC%2BD38Xmt12ns74%3D
JE Lohr F Chen RT Hill (2005) ArticleTitleGenomic analysis of bacteriophage φJL001: insights into its interaction with a sponge-associated alpha-proteobacterium. Appl Envir Microbiol 71 1598–1609 Occurrence Handle1:CAS:528:DC%2BD2MXisVOitr0%3D
S Miller B Schuler R Seckler (1998) ArticleTitlePhage P22 tailspike protein: removal of head-binding domain unmasks effects of folding mutations on native-state thermal stability. Protein Sci 7 2223–2232 Occurrence Handle9792111 Occurrence Handle1:CAS:528:DyaK1cXntVSlsLk%3D Occurrence Handle10.1002/pro.5560071021
S Miller B Schuler R Seckler (1998) ArticleTitleA reversibly unfolding fragment of P22 tailspike protein with native structure: the isolated beta-helix domain. Biochemistry 37 9160–9168 Occurrence Handle9636063 Occurrence Handle1:CAS:528:DyaK1cXjsFegur8%3D
M Muniesa J Recktenwald M Bielaszewska H Karch H Schmidt (2000) ArticleTitleCharacterization of a shiga toxin 2e-converting bacteriophage from an Escherichia coli strain of human origin. Infect Immun 68 4850–4855 Occurrence Handle10.1128/IAI.68.9.4850-4855.2000 Occurrence Handle10948096 Occurrence Handle1:CAS:528:DC%2BD3cXmtVelur8%3D
MN Neely DI Friedman (1998) ArticleTitleFunctional and genetic analysis of regulatory regions of coliphage H-19B: location of shiga-like toxin and lysis genes suggest a role of phage functions in toxin release. Mol Microbiol 28 1255–1267 Occurrence Handle10.1046/j.1365-2958.1998.00890.x Occurrence Handle9680214 Occurrence Handle1:CAS:528:DyaK1cXktl2itLY%3D
D Nelson (2004) ArticleTitlePhage Taxonomy: We Agree to Disagree. J Bacteriol 186 7029–7031 Occurrence Handle15489416 Occurrence Handle1:CAS:528:DC%2BD2cXptVKnsLk%3D
ML Pedulla ME Ford T Karthikeyan JM Houtz RW Hendrix GF Hatfull AR Poteete EB Gilcrease DA Winn-Stapley SR Casjens (2003) ArticleTitleCorrected sequence of the bacteriophage P22 genome. J Bacteriol 185 1475–1477 Occurrence Handle10.1128/JB.185.4.1475-1477.2003 Occurrence Handle12562822 Occurrence Handle1:CAS:528:DC%2BD3sXhtFKnsLs%3D
C Proux D van Sinderen J Suarez P Garcia V Ladero GF Fitzgerald F Desiere H Brussow (2002) ArticleTitleThe dilemma of phage taxonomy illustrated by comparative genomics of Sfi21-like siphoviridae in lactic acid bacteria. J Bacteriol 184 6026–6036 Occurrence Handle10.1128/JB.184.21.6026-6036.2002 Occurrence Handle12374837 Occurrence Handle1:CAS:528:DC%2BD38XotVKisL4%3D
CJ Salgado M Zayas R Villafane (2004) ArticleTitleSimilarity between two different Salmonella phages: Salmonella enterica serovar typhimurium phage P22 and Salmonella enterica serovar anatum var. 15+ phage ɛ34. Virus Genes 29 87–98 Occurrence Handle10.1023/B:VIRU.0000032792.86188.fb Occurrence Handle15215687 Occurrence Handle1:CAS:528:DC%2BD2cXltVOnt7g%3D
RT Sauer W Krovatin AR Poteete PB Berget (1982) ArticleTitlePhage P22 tail protein: gene and amino acid sequence. Biochem 2 5811–5815
P Schicklmaier T Wieland H Schmieger (1999) ArticleTitleMolecular characterization and module composition of P22-related Salmonella phage genomes. J Biotech 73 185–194 Occurrence Handle10.1016/S0168-1656(99)00120-0 Occurrence Handle1:CAS:528:DyaK1MXlt1Sisb0%3D
P Schicklmaier H Schmieger (1997) ArticleTitleSequence comparison of the genes for immunity, DNA replication and cell lysis of the P22-related phages ES18 and L. Gene 195 93–100 Occurrence Handle10.1016/S0378-1119(97)00182-0 Occurrence Handle9300826 Occurrence Handle1:CAS:528:DyaK2sXksFagtLo%3D
H Schmieger (1999) ArticleTitleMolecular survey of the Salmonella phage typing system of Anderson. J Bacteriol 181 1630–1635 Occurrence Handle10049397 Occurrence Handle1:CAS:528:DyaK1MXhslWrtb8%3D
D Scholl S Adhya CR Merril (2002) ArticleTitleBacteriophage SP6 is closely related to phages K1-5, K5, and K1E but encodes a tail protein very similar to that of the distantly related P22. J Bacteriol 184 2833–2836 Occurrence Handle10.1128/JB.184.10.2833-2836.2002 Occurrence Handle11976314 Occurrence Handle1:CAS:528:DC%2BD38XjtlGqu7o%3D
D Scholl J Kieleczawa P Kemp J Rush CC Richardson RC Merril S Adhya IJ Molineux (2004) ArticleTitleGenomic analysis of bacteriophages SP6 and K1-5, an estranged subgroup of the T7 supergroup. J Mol Biol 335 1151–1171 Occurrence Handle10.1016/j.jmb.2003.11.035 Occurrence Handle14729334 Occurrence Handle1:CAS:528:DC%2BD2cXjtVChug%3D%3D
B Schuler R Rachel R Seckler (1999) ArticleTitleFormation of fibrous aggregates from a non-native intermediate: the isolated P22 tailspike beta-helix domain. J Biol Chem 274 18589–18596 Occurrence Handle10.1074/jbc.274.26.18589 Occurrence Handle10373469 Occurrence Handle1:CAS:528:DyaK1MXktF2qtrg%3D
S Steinbacher U Baxa S Miller A Weintraub R Seckler R Huber (1996) ArticleTitleCrystal structure of phage P22 tailspike protein complexed with Salmonella sp. O-antigen receptors. Proc Natl Acad Sci 93 10584–10588 Occurrence Handle10.1073/pnas.93.20.10584 Occurrence Handle8855221 Occurrence Handle1:CAS:528:DyaK28XmtVOlsLY%3D
S Steinbacher S Miller U Baxa N Budisa A Weintraub R Seckler R Huber (1997) ArticleTitlePhage P22 tailspike protein: crystal structure of the head-binding domain at 2.3 A, fully refined structure of the endorhamnosidase at 1.56A resolution, and the molecular basis of O-antigen recognition and cleavage. J Mol Biol 267 865–880 Occurrence Handle10.1006/jmbi.1997.0922 Occurrence Handle9135118 Occurrence Handle1:CAS:528:DyaK2sXivFWmu74%3D
S Steinbacher S Miller U Baxa A Weintraub R Seckler (1997) ArticleTitleInteraction of Salmonella phage P22 with its O-Antigen receptor studied by x-ray crystallography. Biol Chem 378 337–343 Occurrence Handle9165091 Occurrence Handle1:CAS:528:DyaK2sXjtVOqs78%3D Occurrence Handle10.1515/bchm.1997.378.3-4.337
S Steinbacher R Seckler S Miller B Streipe R Huber B Reinemer (1994) ArticleTitleCrystal structure of P22 tailspike protein: interdigitated subunits in a thermostable trimer. Science 265 383–386 Occurrence Handle8023158 Occurrence Handle1:CAS:528:DyaK2cXlslegsL8%3D
A Sulakvelidze Z Alavidze JG Morris SuffixJr (2001) ArticleTitleBacteriophage therapy. Antimicrob Agents Chemother 45 649–659 Occurrence Handle10.1128/AAC.45.3.649-659.2001 Occurrence Handle11181338 Occurrence Handle1:CAS:528:DC%2BD3MXhsFWgt78%3D
WC Summers (2001) ArticleTitleBacteriophage therapy. Ann Rev Microbiol 55 437–451 Occurrence Handle1:CAS:528:DC%2BD3MXnslKjtL0%3D Occurrence Handle10.1146/annurev.micro.55.1.437
C Vander Byl AM Kropinski (2000) ArticleTitleSequence of the genome of Salmonella bacteriophage P22. J Bacteriol 182 6472–6481 Occurrence Handle11053393 Occurrence Handle1:CAS:528:DC%2BD3cXnvVGgsrw%3D
R Villafane J King (1988) ArticleTitleNature and distribution of sites of temperature-sensitive folding mutations in the gene for the P22 tailspike polypeptide chain. J Mol Biol 204 607–619 Occurrence Handle10.1016/0022-2836(88)90359-2 Occurrence Handle3225847 Occurrence Handle1:CAS:528:DyaL1MXptVygtg%3D%3D
R Villafane A Fleming C Haase-Pettingell (1994) ArticleTitleIsolation of suppressor of temperature-sensitive folding mutations. J Bacteriol 176 137–142 Occurrence Handle8282689 Occurrence Handle1:CAS:528:DyaK2cXntF2hsg%3D%3D
PR Weigele E Scanlon J King (2003) ArticleTitleHomotrimeric, ß-stranded viral adhesins and tail proteins. J Bacteriol 185 4022–4030 Occurrence Handle10.1128/JB.185.14.4022-4030.2003 Occurrence Handle12837775 Occurrence Handle1:CAS:528:DC%2BD3sXlsFahs7c%3D
C Werts V Michel M Hofnung A Charbit (1994) ArticleTitleAdsorption of bacteriophage lambda on the LamB protein of Escherichia coli K-12: point mutations in gene J of lambda responsible for extended host range. J Bacteriol 176 941–947 Occurrence Handle8106335 Occurrence Handle1:CAS:528:DyaK2cXitl2qs74%3D
C Westwater LM Kasman DA Schofield PA Werner JW Dolan MG Schmidt JS Norris (2003) ArticleTitleUse of genetically engineered phage to deliver antimicrobial agents to bacteria: an alternative therapy for treatment of bacterial infection. Antimicrob Agents Chemother 47 1301–1307 Occurrence Handle10.1128/AAC.47.4.1301-1307.2003 Occurrence Handle12654662 Occurrence Handle1:CAS:528:DC%2BD3sXivVSnu7Y%3D
Zayas M, Martinez JL, Villafane R (2005) The identification of the Salmonella phage ɛ34 tailspike gene (in preparation)
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Villafane, R., Costa, S., Ahmed, R. et al. Conservation of the N-terminus of some phage tail proteins. Arch Virol 150, 2609–2621 (2005). https://doi.org/10.1007/s00705-005-0597-7
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DOI: https://doi.org/10.1007/s00705-005-0597-7