Crossref journal-article
American Society for Microbiology
Journal of Bacteriology (235)
Abstract

An intracellular symbiont harbored by the aphid bacteriocyte, a specialized fat body cell, synthesizes in vivo substantially only one protein, symbionin, which is a member of the chaperonin-60 family of molecular chaperones. Nucleotide sequence determination of the symbionin region of the endosymbiont genome revealed that it contains the two-cistron operon sym. Just like the Escherichia coli groE operon, the sym operon was dually led by a heat shock and an ordinary promoter sequence. According to the nucleotide sequence, symbionin was 85.5% identical to GroEL of E. coli at the amino acid sequence level. SymS, another protein encoded in the sym operon, which is a member of chaperonin-10, was 79.6% identical to GroES. Complementation experiments with E. coli groE mutants showed that the chaperonin-10 and chaperonin-60 genes from the endosymbiont are expressed in E. coli and that they can function as molecular chaperones together with endogenous GroEL and GroES, respectively.

Bibliography

Ohtaka, C., Nakamura, H., & Ishikawa, H. (1992). Structures of chaperonins from an intracellular symbiont and their functional expression in Escherichia coli groE mutants. Journal of Bacteriology, 174(6), 1869–1874.

Authors 3
  1. C Ohtaka (first)
  2. H Nakamura (additional)
  3. H Ishikawa (additional)
References 34 Referenced 63
  1. Bochkareva , E. S. , N. M. Lissen , and A. S. Girshovich . 1988 . Transient association of newly synthesized unfolded proteins with the heat-shock GroEL protein . Nature (London) 336 : 254 - 257 . (10.1038/336254a0) / Nature (London) / Transient association of newly synthesized unfolded proteins with the heat-shock GroEL protein by Bochkareva E. S. (1988)
  2. Buchner P. 1965. Endosymbiosis of animals with plant microorganisms p. 297-332. Interscience Publishers Inc. New York.
  3. Fayet , O. , T. Ziegelhoffer , and C. Georgopoulos . 1989 . The groES and groEL heat shock gene products of Escherichia coli are essential for bacterial growth at all temperatures . J. Bacteriol. 171 : 1379 - 1385 . (10.1128/jb.171.3.1379-1385.1989) / J. Bacteriol. / The groES and groEL heat shock gene products of Escherichia coli are essential for bacterial growth at all temperatures by Fayet O. (1989)
  4. Goloubinoff , P. , J. T. Christeller , A. A. Gatenby , and G. H. Lorimer . 1989 . Reconstitution of active dimeric ribulose bisphosphate carboxylase from an unfolded state depends on two chaperonin proteins and Mg-ATP . Nature (London) 342 : 884 - 889 . (10.1038/342884a0) / Nature (London) / Reconstitution of active dimeric ribulose bisphosphate carboxylase from an unfolded state depends on two chaperonin proteins and Mg-ATP by Goloubinoff P. (1989)
  5. Goloubinoff , P. , A. A. Gatenby , and G. H. Lorimer . 1989 . GroE heat-shock proteins promote assembly of foreign prokaryotic ribulose bisphosphate carboxylase oligomers in Escherichia coli . Nature (London) 337 : 44 47. (10.1038/337044a0) / Nature (London) / GroE heat-shock proteins promote assembly of foreign prokaryotic ribulose bisphosphate carboxylase oligomers in Escherichia coli by Goloubinoff P. (1989)
  6. Gross A. C. D. B. Straus J. W. Erickson and T. Yura. 1990. The function and regulation of heat shock proteins in Eschenichia coli p. 167-190. In R. I. Morimoto A. Tissieres and C. Georgopoulos (ed.) Stress proteins in biology and medicine. Cold Spring Harbor Laboratory Cold Spring Harbor N.Y.
  7. Gupta , S. R. , J. D. Picketts , and S. Ahmad . 1989 . A novel ubiquitous protein 'chaperonin' supports the endosymbiotic origin of mitochondrion and plant chloroplast . Biochem. Biophys. Res. Commun. 163 : 780 - 787 . (10.1016/0006-291X(89)92290-0) / Biochem. Biophys. Res. Commun. / A novel ubiquitous protein 'chaperonin' supports the endosymbiotic origin of mitochondrion and plant chloroplast by Gupta S. R. (1989)
  8. Hara , E. , T. Fukatsu , K. Kakeda , M. Kengaku , C. Ohtaka , and H. Ishikawa . 1990 . The predominant protein in an aphid endosymbiont is homologous to an E. coli heat shock protein . Symbiosis 8 : 271 - 283 . / Symbiosis / The predominant protein in an aphid endosymbiont is homologous to an E. coli heat shock protein by Hara E. (1990)
  9. Hara , E. , and H. Ishikawa . 1990 . Purification and partial characterization of symbionin, an aphid endosymbiont-specific protein . Insect Biochem. 20 : 421 - 427 . (10.1016/0020-1790(90)90063-Z) / Insect Biochem. / Purification and partial characterization of symbionin, an aphid endosymbiont-specific protein by Hara E. (1990)
  10. Harrison , C. P. , A. E. Douglas , and A. F. G. Dixon . 1989 . A rapid method to isolate symbiotic bacteria from aphids . J. Invertebr. Pathol. 53 : 427 - 428 . (10.1016/0022-2011(89)90110-9) / J. Invertebr. Pathol. / A rapid method to isolate symbiotic bacteria from aphids by Harrison C. P. (1989)
  11. Hemmingsen , S. M. , C. Woolford , S. M. van der Vies , K. Tilly , D. T. Dennis , C. P. Georgopoulos , R. W. Hendrix , and R. J. Ellis . 1988 . Homologous plant and bacterial proteins chaperone oligomeric protein assembly . Nature (London) 333 : 330 - 334 . (10.1038/333330a0) / Nature (London) / Homologous plant and bacterial proteins chaperone oligomeric protein assembly by Hemmingsen S. M. (1988)
  12. Ishikawa , H. 1982 . Host-symbiont interactions in the protein synthesis in the pea aphid, Acyrthosiphon pisum . Insect Biochem. 12 : 613 - 622 . (10.1016/0020-1790(82)90048-8) / Insect Biochem. / Host-symbiont interactions in the protein synthesis in the pea aphid, Acyrthosiphon pisum by Ishikawa H. (1982)
  13. Ishikawa , H. 1984 . Characterization of the protein species synthesized in vivo and in vitro by an aphid endosymbiont . Insect Biochem. 14 : 417 - 425 . (10.1016/0020-1790(84)90098-2) / Insect Biochem. / Characterization of the protein species synthesized in vivo and in vitro by an aphid endosymbiont by Ishikawa H. (1984)
  14. Ishikawa , H. , and M. Yamaji . 1985 . Symbionin, an aphid endosymbiont-specific protein. I. Production of insects deficient in symbiont . Insect Biochem. 15 : 165 - 174 . (10.1016/0020-1790(85)90004-6) / Insect Biochem. / Symbionin, an aphid endosymbiont-specific protein. I. Production of insects deficient in symbiont by Ishikawa H. (1985)
  15. Jindal , S. , A. K. Dudani , B. Singh , C. B. Harley , and R. Y. Gupta . 1989 . Primary structure of a human mitochondrial protein homologous to the bacterial and plant chaperonins and to the 65-kilodalton mycobacterial antigen . Mol. Cell. Biol. 9 : 2279 - 2283 . / Mol. Cell. Biol. / Primary structure of a human mitochondrial protein homologous to the bacterial and plant chaperonins and to the 65-kilodalton mycobacterial antigen by Jindal S. (1989)
  16. Kakeda , K. , and H. Ishikawa . 1991 . Molecular chaperone produced by an intracellular symbiont . J. Biochem. 110 : 583 - 587 . (10.1093/oxfordjournals.jbchem.a123623) / J. Biochem. / Molecular chaperone produced by an intracellular symbiont by Kakeda K. (1991)
  17. Kohara , Y. , K. Akiyama , and K. Isono . 1987 . The physical map of the whole E. coli chromosome: application of a new strategy for rapid analysis and sorting of a large genomic library . Cell 50 : 495 - 508 . (10.1016/0092-8674(87)90503-4) / Cell / The physical map of the whole E. coli chromosome: application of a new strategy for rapid analysis and sorting of a large genomic library by Kohara Y. (1987)
  18. Kusukawa , N. , T. Yura , C. Ueguchi , Y. Akdyama , and K. Ito . 1989 . Effects of mutations in heat-shock genesgroES andgroEL on protein export in Escherichia coli . EMBO J. 8 : 3517 - 3521 . (10.1002/j.1460-2075.1989.tb08517.x) / EMBO J. / Effects of mutations in heat-shock genesgroES andgroEL on protein export in Escherichia coli by Kusukawa N. (1989)
  19. Lecker , S. , R Lill , T. Ziegelhoffer , C. Georgopoulos , P. J. Baisford , Jr. , C. A. Kumamoto , and W. Wickner . 1989 . Three pure chaperone proteins of Escherichia coli-SecB, trigger factor and GroEL-form soluble complexes with precursor proteins in vitro . EMBO J. 8 : 2703 - 2709 . (10.1002/j.1460-2075.1989.tb08411.x) / EMBO J. / Three pure chaperone proteins of Escherichia coli-SecB, trigger factor and GroEL-form soluble complexes with precursor proteins in vitro by Lecker S. (1989)
  20. Lubben , H. T. , A. A. Gatenby , G. K. Donaldson , G. H. Lolimer , and P. V. Viltanen . 1990 . Identification of a groES-like chaperonin in mitochondria that facilitates protein folding . Proc. Natl. Acad. Sci. USA 87 : 7683 - 7687 . (10.1073/pnas.87.19.7683) / Proc. Natl. Acad. Sci. USA / Identification of a groES-like chaperonin in mitochondria that facilitates protein folding by Lubben H. T. (1990)
  21. McCarthy , J. E. G. 1988 . Expression of unc genes in Escherichia coli . J. Bioenerg. Biomembr. 20:.19-39. (10.1007/BF00762136) / J. Bioenerg. Biomembr. 20:.19-39. / Expression of unc genes in Escherichia coli by McCarthy J. E. G. (1988)
  22. Morioka M. and H. Ishikawa. Mutualism based on stress: selective synthesis and phosphorylation of stress protein by an intracellular symbiont. J. Biochem. in press.
  23. McMullin , T. W. , and R. L. Hailberg . 1988 . A highly evolutionarily conserved mitochondrial protein is structurally related to the protein encoded by the Escherichia coli groEL gene . Mol. Cell. Biol. 8 : 371 - 380 . / Mol. Cell. Biol. / A highly evolutionarily conserved mitochondrial protein is structurally related to the protein encoded by the Escherichia coli groEL gene by McMullin T. W. (1988)
  24. Neidhardt , F. C. , R. A. Van Bogelen , and V. Vaughn . 1984 . The genetics and regulation of heat-shock proteins. Annu . Rev. Genet. 18 : 295 - 329 . (10.1146/annurev.ge.18.120184.001455) / Rev. Genet. / The genetics and regulation of heat-shock proteins. Annu by Neidhardt F. C. (1984)
  25. Ohtaka , C. , and H. Ishikawa . 1991 . Effects of heat-treatment on the symbiotic system of an aphid mycetocyte . Symbiosis 11 : 19 - 30 . / Symbiosis / Effects of heat-treatment on the symbiotic system of an aphid mycetocyte by Ohtaka C. (1991)
  26. Picketts , D. J. , C. S. K. Mayanil , and R. S. Gupta . 1989 . Molecular cloning of a Chinese hamster mitochondrial protein related to the "chaperonin " family of bacterial and plant J. Biol. Chem. 264 : 12001 - 12008 . (10.1016/S0021-9258(18)80166-1) / J. Biol. Chem. / Molecular cloning of a Chinese hamster mitochondrial protein related to the "chaperonin by Picketts D. J. (1989)
  27. Reading , D. S. , R. L. Hallberg , and A. M. Myers . 1989 . Characterization of the yeast HSP60 gene coding for a mitochondrial assembly factor . Nature (London) 337 : 655 - 659 . (10.1038/337655a0) / Nature (London) / Characterization of the yeast HSP60 gene coding for a mitochondrial assembly factor by Reading D. S. (1989)
  28. Sambrook J. E. F. Fritsch and T. Maniatis. 1989. Molecular cloning: a laboratory manual p. 15.3-15.31. Cold Spring Harbor Laboratory Cold Spring Harbor N.Y.
  29. Sanger , F. , S. Nicklen , and A. R. Coulson . 1977 . DNA sequencing with chain-terminating inhibitors . Proc. Natl. Acad. Sci. USA 74 : 5463 - 5467 . (10.1073/pnas.74.12.5463) / Proc. Natl. Acad. Sci. USA / DNA sequencing with chain-terminating inhibitors by Sanger F. (1977)
  30. Tilly , K. , and C. Georgopoulos . 1982 . Evidence that two Eschenichia coli groE morphogenetic gene products interact in vivo . J. Bacteriol. 149 : 1082 - 1088 . (10.1128/JB.149.3.1082-1088.1982) / J. Bacteriol. / Evidence that two Eschenichia coli groE morphogenetic gene products interact in vivo by Tilly K. (1982)
  31. Tilly , K. , H. Munaldo , and C. Georgopoulos . 1981 . Identification of a second Escherichia coli groE gene whose product is necessary for bacteriophage morphogenesis . Proc. Natl. Acad. Sci. USA 78 : 1629 - 1633 . (10.1073/pnas.78.3.1629) / Proc. Natl. Acad. Sci. USA / Identification of a second Escherichia coli groE gene whose product is necessary for bacteriophage morphogenesis by Tilly K. (1981)
  32. Unterman , M. B. , P. Bauman , and L. D. McLean . 1989 . Pea aphid symbiont relationships established by analysis of 16S rRNAs . J. Bacteriol. 171 : 2970 - 2974 . (10.1128/jb.171.6.2970-2974.1989) / J. Bacteriol. / Pea aphid symbiont relationships established by analysis of 16S rRNAs by Unterman M. B. (1989)
  33. Webb , R. , K. J. Reddy , and L. A. Sherman . 1990 . Regulation and sequence of the Synechococcus sp. strain PCC7942groESL operon, encoding a cyanobacterial chaperonin . J. Bacteriol. 172 : 5079 - 5088 . (10.1128/JB.172.9.5079-5088.1990) / J. Bacteriol. / Regulation and sequence of the Synechococcus sp. strain PCC7942groESL operon, encoding a cyanobacterial chaperonin by Webb R. (1990)
  34. Zhou , Y. , N. Kusukawa , A. C. Erickson , C. A. Gross , and T. Yura . 1988 . Isolation and characterization of Escherichia coli mutants that lack the heat shock sigma factor (32) . J. Bacteriol. 179 : 3640 - 3644 . (10.1128/JB.170.8.3640-3649.1988) / J. Bacteriol. / Isolation and characterization of Escherichia coli mutants that lack the heat shock sigma factor (32) by Zhou Y. (1988)
Dates
Type When
Created 8 years, 9 months ago (Nov. 4, 2016, 3:52 p.m.)
Deposited 4 years, 1 month ago (July 29, 2021, 1:49 p.m.)
Indexed 1 month ago (July 24, 2025, 7:14 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)
Funders 0

None

@article{Ohtaka_1992, title={Structures of chaperonins from an intracellular symbiont and their functional expression in Escherichia coli groE mutants}, volume={174}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.174.6.1869-1874.1992}, DOI={10.1128/jb.174.6.1869-1874.1992}, number={6}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Ohtaka, C and Nakamura, H and Ishikawa, H}, year={1992}, month=mar, pages={1869–1874} }