DOI: 10.1111/j.1365-2958.1989.tb00198.x. Analysis of the <i>yopA</i> gene encoding the Yop1 virulence determinants of <i>Yersinia</i> spp.

Analysis of the yopA gene encoding the Yop1 virulence determinants of Yersinia spp.

10.1111/j.1365-2958.1989.tb00198.x

Crossref journal-article

Wiley

Molecular Microbiology (311)

Abstract

SummaryThe Yop proteins of Yersinia are important virulence determinants. The Yop1 protein sequences of Yersinia pestis, Yersinia pseudotuberculosis, and two Yersinia enterocolitica serotypes, O:3 and O:8, deduced from the nucleotide sequences of the corresponding yopA genes, were compared. Most differences were found in the hydrophilic domains of the proteins, whereas the hydrophobic domains were conserved. The amino acid sequences revealed a signal sequence 25 amino acids long. No cysteine residues were present, even though Yop1 forms a polymeric structure.The transcription startpoint of yop4 was determined by primer extension. The coding region and transcription startpoint were separated by a leader sequence 270 nucleotides long. The yopA promoter sequence of Y. pestis is identical to the corresponding sequence of Y. pseudotuberculosis and transcription studies revealed that this promoter is active in Y. pestis. Thus, the inability of Y. pestis to express the Yop1 protein is due to a single base pair deletion In the coding region of the yopA gene of Y. pestis (Rosqvist et al., 1988).

Bibliography

Skurnik, M., & WolfâWatz, H. (1989). Analysis of the yopA gene encoding the Yop1 virulence determinants of Yersinia spp. Molecular Microbiology, 3(4), 517â529. Portico.

Authors 2

M. Skurnik (first)
H. Wolf‐Watz (additional)

References 50 Referenced 155

10.1093/genetics/39.4.440 / Genetics / Segregation of new lysogenic types during groth of doubly lysogenic strain derived from Escherichia coli K12 by Appleyard R.K. (1954)
{'key': 'e_1_2_1_3_1', 'volume-title': 'Current Protocols in Molecular Biology', 'author': 'Ausubel F.M.', 'year': '1987'} / Current Protocols in Molecular Biology by Ausubel F.M. (1987)
10.1128/IAI.48.3.782-786.1985
10.1016/0147-619X(81)90019-6
{'key': 'e_1_2_1_6_1', 'first-page': '1525', 'article-title': 'The replication, partition, and yop regulation of the pYV plasmids are highly conserved in Yersinia enterocolitica and pseudotuberculosis', 'volume': '134', 'author': 'Biot T.', 'year': '1988', 'journal-title': 'J Gen Microbiol'} / J Gen Microbiol / The replication, partition, and yop regulation of the pYV plasmids are highly conserved in Yersinia enterocolitica and pseudotuberculosis by Biot T. (1988)
10.1016/0378-1119(77)90000-2
10.1128/iai.56.2.343-348.1988 / Infect Immun / Identification and mapping of the temperature‐inducible plasmid‐encoded proteins of Yersinia by Bölin I. (1988)
10.1128/iai.37.2.506-512.1982
10.1128/iai.48.1.234-240.1985 / Infect Immun / Expression of temperature‐inducible outer membrane proteins of Yersinia by Bölin I. (1985)
10.1128/iai.43.1.72-78.1984 / Infect Immun / Molecular cloning of the temperature‐inducible outer membrane protein of Yersinia pseudotuberculosis by Bölin I. (1984)
10.1016/S0092-8674(85)80033-7
{'key': 'e_1_2_1_13_1', 'first-page': '1594', 'article-title': 'Comparison of specificity of recognition sites of adenine and cytosine DNA methylases of Yersinia pestis EV 76 with that of dam and dcm methylases of E. coli', 'volume': '49', 'author': 'Demidova G.V.', 'year': '1984', 'journal-title': 'Biokthimiya'} / Biokthimiya / Comparison of specificity of recognition sites of adenine and cytosine DNA methylases of Yersinia pestis EV 76 with that of dam and dcm methylases of E. coli by Demidova G.V. (1984)
10.1093/nar/12.1Part1.387
{'key': 'e_1_2_1_15_1', 'first-page': '6', 'article-title': 'Quasi end labeling in M13 dideoxy sequence analysis', 'volume': '4', 'author': 'Duncan C.H.', 'year': '1985', 'journal-title': 'NEN Product News'} / NEN Product News / Quasi end labeling in M13 dideoxy sequence analysis by Duncan C.H. (1985)
10.1016/0022-2836(78)90297-8
10.1128/IAI.27.2.682-685.1980
10.1128/iai.28.3.1044-1047.1980
{'key': 'e_1_2_1_19_1', 'first-page': '1302', 'volume-title': 'Escherichia coli and Salmonella typhimurium. Cellular and Molecular Biology', 'author': 'Gold L.', 'year': '1987'} / Escherichia coli and Salmonella typhimurium. Cellular and Molecular Biology by Gold L. (1987)
10.1093/nar/14.1.273
10.1093/nar/11.9.2943
10.1111/j.1574-6968.1987.tb01978.x
10.1016/0378-1119(84)90153-7
{'key': 'e_1_2_1_24_1', 'first-page': '181', 'article-title': 'The antigenic index: a novel algorithm for rapidly predicting antigenic determinants', 'volume': '4', 'author': 'Jameson B.A.', 'year': '1988', 'journal-title': 'Comput Appl Biosci'} / Comput Appl Biosci / The antigenic index: a novel algorithm for rapidly predicting antigenic determinants by Jameson B.A. (1988)
10.1128/iai.47.2.561-566.1985 / Infect Immun / Temperature‐inducibie surface fibrillae associated with the virulence plasmid of Yersinia enterocolitica and Yersinia pseudotuberculosis by Kapperud G. (1985)
10.1128/iai.55.9.2247-2254.1987 / Infect Immun / Plasmid‐mediated surface fibrillae of Yersinia pseudotuberculosis and Yersinia enterocolitica: relationship to the outer membrane protein YOP1 and possible importance for pathogenesis by Kapperud G. (1987)
10.1016/0022-2836(82)90515-0
{'key': 'e_1_2_1_28_1', 'first-page': '145', 'volume-title': 'Biochemistry', 'author': 'Lehninger A.L.', 'year': '1976'} / Biochemistry by Lehninger A.L. (1976)
10.1111/j.1475-4754.1982.tb01001.x
10.1128/iai.41.3.921-930.1983 / Infect Immun / Plasmid‐mediated and temperature‐regulated surface properties of Yersinia enterocolitica by Martinez R.J. (1983)
10.1016/0092-8674(80)90639-X
10.1093/nar/9.2.309
10.1016/0378-1119(83)90040-9
10.1146/annurev.mi.39.100185.003151
{'key': 'e_1_2_1_35_1', 'first-page': '123', 'volume-title': 'Gene Function in Procaryotes', 'author': 'Platt T.', 'year': '1983'} / Gene Function in Procaryotes by Platt T. (1983)
10.1128/JB.148.3.877-883.1981
10.1128/iai.31.2.775-782.1981 / Intect Immun / Characterization of plasmids and plasmid‐associated determinants of Yersinia enterocolitica pathogenesis by Portnoy D.A. (1981)
10.1128/IAI.43.1.108-114.1984
10.1016/0147-619X(86)90062-4
10.1038/334522a0
10.1146/annurev.ge.08.120174.001535
10.1016/0006-291X(62)90341-8
10.1128/iai.47.1.183-190.1985 / Infect Immun / Expression of antigens encoded by the virulence plasmid of Yersinia enterocolitca under different growth conditions by Skurnik M. (1985)
10.1128/JB.158.3.1033-1036.1984
{'key': 'e_1_2_1_45_1', 'first-page': '355', 'volume-title': 'Protein‐Carbohydrate Interactions in Biological Systems', 'author': 'Skurnik M.', 'year': '1986'} / Protein‐Carbohydrate Interactions in Biological Systems by Skurnik M. (1986)
10.3109/00365548609032347
10.1038/newbio246040a0
10.1128/iai.33.3.870-876.1981 / Infect Immun / Plasmids in Yersinia enterocolitica serotypes O:3 and O:9: correlation with epithelial cell adherence in vitro by Vesikari T. (1981)
10.1128/IAI.48.1.241-243.1985
10.1002/j.1460-2075.1985.tb03732.x
10.1038/283224a0

Dates

Type	When
Created	18 years, 10 months ago (Oct. 27, 2006, 4:58 p.m.)
Deposited	1 year, 10 months ago (Oct. 22, 2023, 3:59 a.m.)
Indexed	1 week ago (Aug. 28, 2025, 8:53 a.m.)
Issued	36 years, 5 months ago (April 1, 1989)
Published	36 years, 5 months ago (April 1, 1989)
Published Online	18 years, 10 months ago (Oct. 27, 2006)
Published Print	36 years, 5 months ago (April 1, 1989)

Funders 0

None

BibTeX

@article{Skurnik_1989, title={Analysis of the yopA gene encoding the Yop1 virulence determinants of Yersinia spp.}, volume={3}, ISSN={1365-2958}, url={http://dx.doi.org/10.1111/j.1365-2958.1989.tb00198.x}, DOI={10.1111/j.1365-2958.1989.tb00198.x}, number={4}, journal={Molecular Microbiology}, publisher={Wiley}, author={Skurnik, M. and Wolf‐Watz, H.}, year={1989}, month=apr, pages={517–529} }

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