Abstract
An avirulent, invasion plasmid insertion mutant of Shigella flexneri 5 (pHS1059) was restored to the virulence phenotype by transformation with a partial HindIII library of the wild-type invasion plasmid constructed in pBR322. Western immunoblot analysis of pHS1059 whole-cell lysates revealed that the synthesis of the invasion plasmid antigens VirG, IpaA, IpaB, IpaC, and IpaD was similar to that seen in the corresponding isogenic S. flexneri 5 virulent strain, M90T. IpaB and IpaC, however, were not present on the surface of pHS1059 as was found in M90T, suggesting that the transport or presentation of the IpaB and IpaC proteins onto the bacterial surface was defective in the mutant. pHS1059 was complemented by pWR266, which carried contiguous 1.2- and 4.1-kb HindIII fragments of the invasion plasmid. pHS1059(pWR266) cells were positive in the HeLa cell invasion assay as well as colony immunoblot and enzyme-linked immunosorbent assays, using monoclonal antibodies to IpaB and IpaC. These studies established that the antigens were expressed on the surface of the transformed bacteria. In addition, water extraction of pHS1059 and pHS1059(pWR266) whole cells, which can be used to remove IpaB and IpaC antigens from the surface of wild-type M90T bacteria, yielded significant amounts of these antigens from pHS1059(pWR266) but not from pHS1059. Minicell and DNA sequence analysis indicated that several proteins were encoded by pWR266, comprising the spa loci, which were mapped to a region approximately 18 kb upstream of the ipaBCDAR gene cluster. Subcloning and deletion analysis revealed that more than one protein was involved in complementing the Spa- phenotype in pHS1059. One of these proteins, Spa47, showed striking homology to ORF4 of the Bacillus subtilis flaA locus and the fliI gene sequence of Salmonella typhimurium, both of which bear strong resemblance to the alpha and beta subunits of bacterial, mitochondrial, and chloroplast proton-translocating F0F1 ATPases.
References
55
Referenced
146
-
Albertini , A. M. , T. Caramori , W. D. Crabb , F. Scoffone , and A. Galizzi . 1991 . TheflaA locus of Bacillus subtilis is part of a large operon coding for flagellar structures, motility functions, and an ATPase-like polypeptide . J. Bacteriol. 173 : 3573 - 3579 .
(
10.1128/JB.173.11.3573-3579.1991
) / J. Bacteriol. / TheflaA locus of Bacillus subtilis is part of a large operon coding for flagellar structures, motility functions, and an ATPase-like polypeptide by Albertini A. M. (1991) -
Ames , G. F. L. , and A. K. Joshi . 1990 . Energy coupling in bacterial periplasmic permeases . J. Bacteriol. 172 : 4133 - 4137 .
(
10.1128/JB.172.8.4133-4137.1990
) / J. Bacteriol. / Energy coupling in bacterial periplasmic permeases by Ames G. F. L. (1990) -
Andrews , G. P. , A. E. Hromockyj , C. Coker , and A. T. Maurelli . 1991 . Two novel virulence loci, mxiA and nmiB, in Shigella flexneri 2a facilitate excretion of invasion plasmid antigens . Infect. Immun. 59 : 1997 - 2005 .
(
10.1128/iai.59.6.1997-2005.1991
) / Infect. Immun. / Two novel virulence loci, mxiA and nmiB, in Shigella flexneri 2a facilitate excretion of invasion plasmid antigens by Andrews G. P. (1991) -
Baudry , B. , M. Kaczorek , and P. J. Sansonetti . 1988 . Nucleotide sequence of the invasion plasmid antigen B and C genes (ipaB and ipaC) of Shigella flexneri . Microb. Pathog. 4 : 345 - 357 .
(
10.1016/0882-4010(88)90062-9
) / Microb. Pathog. / Nucleotide sequence of the invasion plasmid antigen B and C genes (ipaB and ipaC) of Shigella flexneri by Baudry B. (1988) -
Bernardini , M. L. , J. Mounier , H. d' Hauteville , M. Coquis Rondon , and P. J. Sansonetti . 1989 . Identification of icsA, a plasmid locus of Shigella flexneri that governs bacterial intra and intercellular spread through interaction with F actin . Proc. Natl. Acad. Sci. USA 86 : 3867 - 3871 .
(
10.1073/pnas.86.10.3867
) / Proc. Natl. Acad. Sci. USA / Identification of icsA, a plasmid locus of Shigella flexneri that governs bacterial intra and intercellular spread through interaction with F actin by Bernardini M. L. (1989) -
Blight , M. A. , and I. B. Holland . 1990 . Structure and function of hemolysin P, P glycoprotein and other members of a novel family of membrane translocators . Mol. Microbiol. 4 : 873 - 880 .
(
10.1111/j.1365-2958.1990.tb00660.x
) / Mol. Microbiol. / Structure and function of hemolysin P, P glycoprotein and other members of a novel family of membrane translocators by Blight M. A. (1990) -
Bowman , E. J. , K. Tenney , and B. J. Bowman . 1988 . Isolation of genes encoding the Neurospora vacuolar ATPase . J. Biol. Chem. 263 : 13994 - 14001 .
(
10.1016/S0021-9258(18)68175-X
) / J. Biol. Chem. / Isolation of genes encoding the Neurospora vacuolar ATPase by Bowman E. J. (1988) - Buysse J. M. A. T. Hartman N. Strockbine and M. M. Venkatesan. Submitted for publication.
-
Buysse , J. M. , C. K. Stover , E. V. Oaks , M. Venkatesan , and D. J. Kopecko . 1987 . Molecular cloning of invasion plasmid antigen (ipa) genes from Shigella fle-xneri: analysis of ipa gene products and genetic mapping . J. Bacteriol. 169 : 2561 - 2569 .
(
10.1128/JB.169.6.2561-2569.1987
) / J. Bacteriol. / Molecular cloning of invasion plasmid antigen (ipa) genes from Shigella fle-xneri: analysis of ipa gene products and genetic mapping by Buysse J. M. (1987) -
Buysse , J. M. , M. Venkatesan , J. A. Mills , and E. V. Oaks . 1990 . Molecular characterization of a transacting positive effector (ipaR) of invasion plasmid antigen synthesis in Shigella fle-xneri serotype 5 . Microb. Pathog. 8 : 197 - 211 .
(
10.1016/0882-4010(90)90047-T
) / Microb. Pathog. / Molecular characterization of a transacting positive effector (ipaR) of invasion plasmid antigen synthesis in Shigella fle-xneri serotype 5 by Buysse J. M. (1990) -
Cangelosi , G. A. , G. Martinetti , J. A. Leigh , C. C. Lee , C. Theines , and E. W. Nester . 1989 . Role of Agrobacterium tumefaciens ChvA protein in export of P-1,2-glucan . J. Bacteriol. 171 : 1609 - 1615 .
(
10.1128/jb.171.3.1609-1615.1989
) / J. Bacteriol. / Role of Agrobacterium tumefaciens ChvA protein in export of P-1,2-glucan by Cangelosi G. A. (1989) -
Dhar , R. , R. W. Ellis , T. Y. Shih , S. Oroszlan , B. Shapiro , J. Maizel , D. Lowy , and E. Scolnick . 1982 . Nucleotide sequence of the p21 transforming protein of Harvey murine sarcoma virus . Science 217 : 934 - 936 .
(
10.1126/science.6287572
) / Science / Nucleotide sequence of the p21 transforming protein of Harvey murine sarcoma virus by Dhar R. (1982) -
Dinari , G. , T. L. Hale , S. W. Austin , and S. B. Formal . 1987 . Local and systemic antibody responses to Shigella infection in rhesus monkeys . J. Infect. Dis. 155 : 1065 - 1069 .
(
10.1093/infdis/155.5.1065
) / J. Infect. Dis. / Local and systemic antibody responses to Shigella infection in rhesus monkeys by Dinari G. (1987) -
Felmlee , T. , S. Pellett , and R. A. Welch . 1985 . Nucleotide sequence of an Escherichia coli chromosomal hemolysin . J. Bacteriol. 163 : 94 - 105 .
(
10.1128/JB.163.1.94-105.1985
) / J. Bacteriol. / Nucleotide sequence of an Escherichia coli chromosomal hemolysin by Felmlee T. (1985) -
Fry , D. C. , S. A. Kuby , and A. S. Mildvan . 1986 . ATP-binding site of adenylate kinase: mechanistic implications of its homology with ras encoded p21, F1-ATPase, and other nucleotidebinding proteins . Proc. Natl. Acad. Sci. USA 83 : 907 - 911 .
(
10.1073/pnas.83.4.907
) / Proc. Natl. Acad. Sci. USA / ATP-binding site of adenylate kinase: mechanistic implications of its homology with ras encoded p21, F1-ATPase, and other nucleotidebinding proteins by Fry D. C. (1986) -
Futai , M. , T. Noumi , and M. Maeda . 1989 . ATP synthase (H+-ATPase): results by combined biochemical and molecular biological approaches. Annu . Rev. Biochem. 58 : 111 - 136 .
(
10.1146/annurev.bi.58.070189.000551
) / Rev. Biochem. / ATP synthase (H+-ATPase): results by combined biochemical and molecular biological approaches. Annu by Futai M. (1989) -
Gay , N. J. , and J. E. Walker . 1981 . The atp operon: nucleotide sequence of the region encoding the (x subunit of Escherichia coli ATP synthase . Nucleic Acids Res. 9 : 2187 - 2194 .
(
10.1093/nar/9.9.2187
) / Nucleic Acids Res. / The atp operon: nucleotide sequence of the region encoding the (x subunit of Escherichia coli ATP synthase by Gay N. J. (1981) -
Gerlach , J. H. , J. A. Endicott , P. F. Juranka , G. Henderson , F. Sarangi , K. L. Deuchars , and V. Ling . 1986 . Homology between P-glycoprotein and a bacterial hemolysin transport protein suggests a model for multidrug resistance . Nature (London) 324 : 485 - 489 .
(
10.1038/324485a0
) / Nature (London) / Homology between P-glycoprotein and a bacterial hemolysin transport protein suggests a model for multidrug resistance by Gerlach J. H. (1986) -
Gros , P. , J. Croop , and D. Housman . 1986 . Mammalian multidrug resistance gene: complete cDNA sequence indicates strong homology to bacterial transport proteins . Cell 47 : 371 - 380 .
(
10.1016/0092-8674(86)90594-5
) / Cell / Mammalian multidrug resistance gene: complete cDNA sequence indicates strong homology to bacterial transport proteins by Gros P. (1986) -
Hale , T. L. 1991 . Genetics of virulence in Shigella . Microbiol. Rev. 55 : 206 - 224 .
(
10.1128/MR.55.2.206-224.1991
) / Microbiol. Rev. / Genetics of virulence in Shigella by Hale T. L. (1991) -
Hesse , J. E. , L. Weiczorek , K. Altendorf , A. S. Reicin , E. Dorus , and W. Epstein . 1984 . Sequence homology between two membrane transport ATPases, the kdp ATPases of E. coli and the Ca"+ ATPase of sarcoplasmic reticulum . Proc. Natl. Acad. Sci. USA 81 : 4746 - 4751 .
(
10.1073/pnas.81.15.4746
) / Proc. Natl. Acad. Sci. USA / Sequence homology between two membrane transport ATPases, the kdp ATPases of E. coli and the Ca"+ ATPase of sarcoplasmic reticulum by Hesse J. E. (1984) -
Higgins , C. F. , P. D. Haag , K. Nikaido , F. Ardeshir , G. Garcia , and G. F. -L. Ames . 1982 . Complete nucleotide sequence and identification of membrane components of the histidine transport operon of S. typhimurium . Nature (London) 298 : 723 - 727 .
(
10.1038/298723a0
) / Nature (London) / Complete nucleotide sequence and identification of membrane components of the histidine transport operon of S. typhimurium by Higgins C. F. (1982) -
Higgins , C. F. , I. D. Hiles , G. P. C. Salmond , D. R. Gill , J. A. Downie , I. J. Evans , I. B. Holland , L. Gray , S. D. Buckel , A. W. Bell , and M. A. Hermodson . 1989 . A family of related ATP binding subunits coupled to many distinct biological processes in bacteria . Nature (London) 323 : 448 - 450 .
(
10.1038/323448a0
) / Nature (London) / A family of related ATP binding subunits coupled to many distinct biological processes in bacteria by Higgins C. F. (1989) -
Hromockyj , A. E. , and A. T. Maurelli . 1989 . Identification of Shigella invasion genes by inoculation of temperature regulated inv::lacZ operon fusions . Infect. Immun. 57 : 2963 - 2970 .
(
10.1128/IAI.57.10.2963-2970.1989
) / Infect. Immun. / Identification of Shigella invasion genes by inoculation of temperature regulated inv::lacZ operon fusions by Hromockyj A. E. (1989) -
Hyde , S. C. , P. Elmsley , M. J. Hartshorn , M. M. Mimmack , U. Gileadi , S. P. Pearce , M. P. Gallagher , D. R. Gill , R. E. Hubbard , and C. F. Higgins . 1990 . Structural model of ATPbinding proteins associated with cystic fibrosis, multidrug resistance and bacterial transport . Nature (London) 346 : 362 - 365 .
(
10.1038/346362a0
) / Nature (London) / Structural model of ATPbinding proteins associated with cystic fibrosis, multidrug resistance and bacterial transport by Hyde S. C. (1990) -
Krebbers , E. T. , I. M. Larrinua , L. Mcintosh , and L. Bogorad . 1982 . The maize chloroplast genes for the i and e subunits of the photosynthetic coupling factor CF1 are fused . Nucleic Acids Res. 10 : 4985 - 5002 .
(
10.1093/nar/10.16.4985
) / Nucleic Acids Res. / The maize chloroplast genes for the i and e subunits of the photosynthetic coupling factor CF1 are fused by Krebbers E. T. (1982) -
Kuby , S. A. , R. H. Palmieri , A. Frischat , A. H. Fischer , L. H. Wu , L. Maland , and M. Manship . 1984 . Studies on adenosine triphosphate transphosphorylases. Amino acid sequence of rabbit muscle ATP-AMP transphosphorylase . Biochemistry 23 : 2393 - 2399 .
(
10.1021/bi00306a012
) / Biochemistry / Studies on adenosine triphosphate transphosphorylases. Amino acid sequence of rabbit muscle ATP-AMP transphosphorylase by Kuby S. A. (1984) -
Kuchler , K. , R. E. Sterne , and J. Thorner . 1989 . Saccharomyces cerevisiae STE6 gene product: a novel pathway for protein export in eukaryotic cells . EMBO J. 8 : 3973 - 3984 .
(
10.1002/j.1460-2075.1989.tb08580.x
) / EMBO J. / Saccharomyces cerevisiae STE6 gene product: a novel pathway for protein export in eukaryotic cells by Kuchler K. (1989) -
Kumamoto , C. A. 1991 . Molecular chaperones and protein translocation across the Escherichia coli inner membrane . Mol. Microbiol. 5 : 19 - 22 .
(
10.1111/j.1365-2958.1991.tb01821.x
) / Mol. Microbiol. / Molecular chaperones and protein translocation across the Escherichia coli inner membrane by Kumamoto C. A. (1991) -
Lett , M. , C. Sasakawa , N. Okada , T. Sakai , S. Makino , M. Yamada , K. Komatsu , and M. Yoshikawa . 1989 . virG, a plasmidcoded virulence gene of Shigella flexneri: identification of the VirG protein and determination of the complete coding sequence . J. Bacteriol. 171 : 353 - 359 .
(
10.1128/jb.171.1.353-359.1989
) / J. Bacteriol. / virG, a plasmidcoded virulence gene of Shigella flexneri: identification of the VirG protein and determination of the complete coding sequence by Lett M. (1989) -
Makino , S. , C. Sasakawa , K. Kamata , T. Kurata , and M. Yoshikawa . 1986 . A genetic determinant required for continuous reinfection of adjacent cells on a large plasmid in S. flexneri 2a . Cell 46 : 551 - 555 .
(
10.1016/0092-8674(86)90880-9
) / Cell / A genetic determinant required for continuous reinfection of adjacent cells on a large plasmid in S. flexneri 2a by Makino S. (1986) -
Maurelli , A. T. , B. Baudry , H. d' Hauteville , T. L. Hale , and P. J. Sansonetti . 1985 . Cloning of plasmid DNA sequences involved in invasion of HeLa cells by Shigella flexneri . Infect. Immun. 49 : 164 - 171 .
(
10.1128/IAI.49.1.164-171.1985
) / Infect. Immun. / Cloning of plasmid DNA sequences involved in invasion of HeLa cells by Shigella flexneri by Maurelli A. T. (1985) -
Mills , J. A. , J. M. Buysse , and E. V. Oaks . 1988 . Shigella flexneri invasion plasmid antigens B and C: epitope location and characterization with monoclonal antibodies . Infect. Immun. 56 : 2933 - 2941 .
(
10.1128/IAI.56.11.2933-2941.1988
) / Infect. Immun. / Shigella flexneri invasion plasmid antigens B and C: epitope location and characterization with monoclonal antibodies by Mills J. A. (1988) -
Oaks , E. V. , T. L. Hale , and S. B. Formal . 1986 . Serum immune response to Shigella protein antigens in rhesus monkeys and humans infected with Shigella species . Infect. Immun. 53 : 57 - 63 .
(
10.1128/IAI.53.1.57-63.1986
) / Infect. Immun. / Serum immune response to Shigella protein antigens in rhesus monkeys and humans infected with Shigella species by Oaks E. V. (1986) -
Ohta , S. , H. Tomura , K. Matsuda , and Y. Kagawa . 1988 . Gene structure of the human mitochondrial adenosine triphosphate synthase ,B subunit . J. Biol. Chem. 263 : 11257 - 11262 .
(
10.1016/S0021-9258(18)37950-X
) / J. Biol. Chem. / Gene structure of the human mitochondrial adenosine triphosphate synthase ,B subunit by Ohta S. (1988) -
Pal , T. P. , T. L. Hale , and S. B. Formal . 1989 . Characterization of virulence marker antigens of Shigella spp. and enteroinvasive Escherichia coli . J. Clin. Microbiol. 27 : 561 - 563 .
(
10.1128/JCM.27.3.561-563.1989
) / J. Clin. Microbiol. / Characterization of virulence marker antigens of Shigella spp. and enteroinvasive Escherichia coli by Pal T. P. (1989) -
Pearson , W. , and D. Lipman . 1985 . Rapid and sensitive protein similarity searches . Science 227 : 1435 - 1441 .
(
10.1126/science.2983426
) / Science / Rapid and sensitive protein similarity searches by Pearson W. (1985) -
Randall , L. L. , and S. J. S. Hardy . 1986 . Correlation of competence for export with lack of tertiary structure of the mature species: a study in vivo of maltose binding protein in E. coli . Cell 46 : 921 - 928 .
(
10.1016/0092-8674(86)90074-7
) / Cell / Correlation of competence for export with lack of tertiary structure of the mature species: a study in vivo of maltose binding protein in E. coli by Randall L. L. (1986) -
Sancar , A. , C. Stachlek , W. Konigsberg , and W. D. Rupp . 1980 . Sequences of the recA gene and protein . Proc. Natl. Acad. Sci. USA 77 : 2611 - 2615 .
(
10.1073/pnas.77.5.2611
) / Proc. Natl. Acad. Sci. USA / Sequences of the recA gene and protein by Sancar A. (1980) -
Saraste , M. , N. J. Gay , A. Eberle , M. J. Runswick , and J. E. Walker . 1986 . The atp operon: nucleotide sequence of the genes for the -y, P and £ subunits of Escherichia coli ATP synthase . Nucleic Acids Res. 9 : 5287 - 5296 .
(
10.1093/nar/9.20.5287
) / Nucleic Acids Res. / The atp operon: nucleotide sequence of the genes for the -y, P and £ subunits of Escherichia coli ATP synthase by Saraste M. (1986) -
Sasakawa , C. , K. Kamata , T. Sakai , S. Makino , M. Yamada , N. Okada , and M. Yoshikawa . 1988 . Virulence-associated genetic regions comprising 31 kilobases of the 230-kilobase plasmid in Shigella flexneri 2a J . Bacteriol. 170 : 2480 - 2484 .
(
10.1128/JB.170.6.2480-2484.1988
) / Bacteriol. / Virulence-associated genetic regions comprising 31 kilobases of the 230-kilobase plasmid in Shigella flexneri 2a J by Sasakawa C. (1988) -
Schnaitman , C. A. 1970 . Protein composition of the cell wall and cytoplasmic membrane of Eschenichia coli . J. Bacteriol. 104 : 890 - 901 .
(
10.1128/jb.104.2.890-901.1970
) / J. Bacteriol. / Protein composition of the cell wall and cytoplasmic membrane of Eschenichia coli by Schnaitman C. A. (1970) -
Shea , C. M. , and M. A. MacIntosh . 1991 . Nucleotide sequence and genetic organization of the ferric enterobactin transport system: homology to other periplasmic binding protein-dependent systems in Escherichia coli . Mol. Microbiol. 5 : 1415 - 1428 .
(
10.1111/j.1365-2958.1991.tb00788.x
) / Mol. Microbiol. / Nucleotide sequence and genetic organization of the ferric enterobactin transport system: homology to other periplasmic binding protein-dependent systems in Escherichia coli by Shea C. M. (1991) -
Smith , P. K. , R. I. Krohn , G. T. Hermanson , A. K. Mallia , F. H. Gartner , M. D. Provenzano , E. K. Fujimoto , N. M. Goeke , B. J. Olson , and D. C. Kienk . 1985 . Measurement of protein using bicinchonic acid . Anal. Biochem. 150 : 76 - 85 .
(
10.1016/0003-2697(85)90442-7
) / Anal. Biochem. / Measurement of protein using bicinchonic acid by Smith P. K. (1985) -
Takeda , M. , A. Vassarotti , and M. G. Douglas . 1985 . Nuclear genes encoding the yeast mitochondrial adenosine triphosphatase complex . J. Biol. Chem. 260 : 15458 - 15465 .
(
10.1016/S0021-9258(17)36276-2
) / J. Biol. Chem. / Nuclear genes encoding the yeast mitochondrial adenosine triphosphatase complex by Takeda M. (1985) -
Tennent , J. M. , F. Lindberg , and S. Nomark 1990 . Integrity of Escherichia coli P pili during biogenesis: properties and role of Pap J. Mol. Microbiol. 4 : 747 - 758 .
(
10.1111/j.1365-2958.1990.tb00645.x
) / J. Mol. Microbiol. / Integrity of Escherichia coli P pili during biogenesis: properties and role of Pap by Tennent J. M. (1990) -
Tobe , T. , S. Nagai , N. Okada , B. Adler , M. Yoshi , and C. Sasakawa . 1991 . Temperature regulation of invasion genes in Shigella flexneri is controlled through the transcriptional activation of the virB gene on the large plasmid . Mol. Microbiol. 5 : 887 - 893 .
(
10.1111/j.1365-2958.1991.tb00762.x
) / Mol. Microbiol. / Temperature regulation of invasion genes in Shigella flexneri is controlled through the transcriptional activation of the virB gene on the large plasmid by Tobe T. (1991) - Turbyfill K. R. and E. V. Oaks. Unpublished data.
- Venkatesan M. and J. M. Buysse. Unpublished data.
- Venkatesan M. E. V. Oaks and J. M. Buysse. 1990. Abstr. Univ. Alabama-Birmingham Conf. Microb. Adhesion Invasion p. 32.
-
Venkatesan , M. M. , J. M. Buysse , and D. J. Kopecko . 1988 . Characterization of invasion plasmid antigen genes (ipaBCD) from Shigella flexneri . Proc. Natl. Acad. Sci. USA 85 : 9317 - 9321 .
(
10.1073/pnas.85.23.9317
) / Proc. Natl. Acad. Sci. USA / Characterization of invasion plasmid antigen genes (ipaBCD) from Shigella flexneri by Venkatesan M. M. (1988) -
Vogler , A. P. , M. Homma , V. M. Irikura , and R. M. Macnab . 1991 . Salmonella typhimurium mutants defective in flagellar filament regrowth and sequence similarity of Flil to FoF1, vacuolar, and archaebacterial ATPase subunits . J. Bacteriol. 173 : 3564 - 3572 .
(
10.1128/JB.173.11.3564-3572.1991
) / J. Bacteriol. / Salmonella typhimurium mutants defective in flagellar filament regrowth and sequence similarity of Flil to FoF1, vacuolar, and archaebacterial ATPase subunits by Vogler A. P. (1991) -
Walker , J. E. , M. Saraste , M. J. Runswick , and N. J. Gay . 1982 . Distantly related sequences in the a and P-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold . EMBO J. 1 : 945 - 951 .
(
10.1002/j.1460-2075.1982.tb01276.x
) / EMBO J. / Distantly related sequences in the a and P-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold by Walker J. E. (1982) -
Warrick , H. M. , and J. A. Spudich . 1987 . Myosin structure and function in cell motility. Annu . Rev. Cell Biol. 3 : 379 - 421 .
(
10.1146/annurev.cb.03.110187.002115
) / Rev. Cell Biol. / Myosin structure and function in cell motility. Annu by Warrick H. M. (1987) -
Watanabe , H. , and A. Nakamura . 1986 . Identification of Shigella sonnei form I plasmid genes necessary for cell invasion and their conservation among Shigella species and enteroinvasive Escherichia coli . Infect. Immun. 53 : 352 - 358 .
(
10.1128/IAI.53.2.352-358.1986
) / Infect. Immun. / Identification of Shigella sonnei form I plasmid genes necessary for cell invasion and their conservation among Shigella species and enteroinvasive Escherichia coli by Watanabe H. (1986)
Dates
Type | When |
---|---|
Created | 8 years, 9 months ago (Nov. 4, 2016, 3:52 p.m.) |
Deposited | 4 years ago (July 29, 2021, 1:49 p.m.) |
Indexed | 1 year, 7 months ago (Jan. 18, 2024, 12:27 a.m.) |
Issued | 33 years, 5 months ago (March 1, 1992) |
Published | 33 years, 5 months ago (March 1, 1992) |
Published Print | 33 years, 5 months ago (March 1, 1992) |
@article{Venkatesan_1992, title={Surface presentation of Shigella flexneri invasion plasmid antigens requires the products of the spa locus}, volume={174}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.174.6.1990-2001.1992}, DOI={10.1128/jb.174.6.1990-2001.1992}, number={6}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Venkatesan, M M and Buysse, J M and Oaks, E V}, year={1992}, month=mar, pages={1990–2001} }