DOI: 10.1128/jb.188.7.2715-2720.2006. Liberation of Zinc-Containing L31 (RpmE) from Ribosomes by Its Paralogous Gene Product, YtiA, in<i>Bacillus subtilis</i>

Liberation of Zinc-Containing L31 (RpmE) from Ribosomes by Its Paralogous Gene Product, YtiA, inBacillus subtilis

10.1128/jb.188.7.2715-2720.2006

Crossref journal-article

American Society for Microbiology

Journal of Bacteriology (235)

Abstract

ABSTRACTWe have found that alternative localization of two types of L31 ribosomal protein, RpmE and YtiA, is controlled by the intracellular concentration of zinc inBacillus subtilis. The detailed mechanisms for the alternation of L31 proteins under zinc-deficient conditions were previously unknown. To obtain further information about this regulatory mechanism, we have studied the stability of RpmE in vivo and the binding affinity of these proteins to ribosomes in vitro, and we have found that liberation of RpmE from ribosomes is triggered by the expression ofytiA, which is induced by the derepression of Zur under zinc-deficient conditions.

Bibliography

Akanuma, G., Nanamiya, H., Natori, Y., Nomura, N., & Kawamura, F. (2006). Liberation of Zinc-Containing L31 (RpmE) from Ribosomes by Its Paralogous Gene Product, YtiA, inBacillus subtilis. Journal of Bacteriology, 188(7), 2715â2720.

Authors 5

Genki Akanuma (first)
Hideaki Nanamiya (additional)
Yousuke Natori (additional)
Naofumi Nomura (additional)
Fujio Kawamura (additional)

References 20 Referenced 73

Eistetter, A. J., P. D. Butler, R. R. Traut, and T. G. Fanning. 1999. Characterization of Escherichia coli 50S ribosomal protein L31. FEMS Microbiol. Lett. 180 : 345-349. (10.1111/j.1574-6968.1999.tb08816.x) / FEMS Microbiol. Lett. (1999)
10.1128/JB.180.22.5815-5821.1998
10.1128/JB.184.23.6508-6514.2002
Hardy, S. J. S., C. G. Kurland, P. Voynow, and G. Mora. 1969. The ribosomal proteins of Eschericha coli. I. Purification of the 30S ribosomal proteins. Biochemistry 8 : 2897-2905. (10.1021/bi00835a031) / Biochemistry (1969)
Henne, A., H. Bruggemann, C. Raasch, A. Wiezer, T. Hartsch, H. Liesegang, A. Johann, T. Lienard, O. Gohl, R. Martinez-Arias, C. Jacobi, V. Starkuviene, S. Schlenczeck, S. Dencker, R. Huber, H. P. Klenk, W. Kramer, R. Merk, G. Gottschalk, and H. J. Fritz. 2004. The genome sequence of the extreme thermophile Thermus thermophilus. Nat. Biotechnol. 22 : 547-553. (10.1038/nbt956) / Nat. Biotechnol. (2004)
Herold, M., and K. H. Nierhaus. 1987. Incorporation of six additional proteins to complete the assembly map of the 50S subunit from Escherichia coli ribosomes. J. Biol. Chem. 262 : 8826-8833. (10.1016/S0021-9258(18)47489-3) / J. Biol. Chem. (1987)
10.1128/JB.186.16.5450-5459.2004
Joseph, P., J. R. Fantino, M. L. Herbaud, and F. Denizot. 2001. Rapid orientated cloning in a shuttle vector allowing modulated gene expression in Bacillus subtilis. FEMS Microbiol. Lett. 205 : 91-97. (10.1111/j.1574-6968.2001.tb10930.x) / FEMS Microbiol. Lett. (2001)
10.1038/36786
Makarova, K. S., V. A. Ponomarev, and E. V. Koonin. 2001. Two C or not two C: recurrent disruption of Zn-ribbons, gene duplication, lineage-specific gene loss, and horizontal gene transfer in evolution of bacterial ribosomal proteins. Genome Biol. 2 : 0033.1-0033.14. / Genome Biol. (2001)
Murayama, R., G. Akanuma, Y. Makino, H. Nanamiya, and F. Kawamura. 2004. Spontaneous transformation and its use for genetic mapping in Bacillus subtilis. Biosci. Biotechnol. Biochem. 68 : 1672-1680. (10.1271/bbb.68.1672) / Biosci. Biotechnol. Biochem. (2004)
Nanamiya, H., G. Akanuma, Y. Natori, R. Murayama, S. Kosono, T. Kudo, K. Kobayashi, N. Ogasawara, S.-M. Park, K. Ochi, and F. Kawamura. 2004. Zinc is a key factor in controlling alternation of two types of L31 protein in the Bacillus subtilis ribosome. Mol. Microbiol. 52 : 273-283. (10.1111/j.1365-2958.2003.03972.x) / Mol. Microbiol. (2004)
Nanamiya, H., Y. Ohashi, K. Asai, S. Moriya, N. Ogasawara, M. Fujita, Y. Sadaie, and F. Kawamura. 1998. ClpC regulates the fate of a sporulation initiation sigma factor, σH protein, in Bacillus subtilis at elevated temperatures. Mol. Microbiol. 29 : 505-513. (10.1046/j.1365-2958.1998.00943.x) / Mol. Microbiol. (1998)
Nierhaus, K. H. 2004. Assembly of the prokaryotic ribosome, p. 85-105. In K. H. Nierhaus and D. N. Wilson (ed.), Protein synthesis and ribosome structure. Wiley-VCH Verlag GmbH, Weinheim, Germany. / Protein synthesis and ribosome structure (2004)
Outten, C. E., and T. V. O'Halloran. 2001. Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science 292 : 2488-2492. (10.1126/science.1060331) / Science (2001)
Panina, E. M., A. A. Mironov, and M. S. Gelfand. 2003. Comparative genomics of bacterial zinc regulons: enhanced ion transport, pathogenesis, and rearrangement of ribosomal proteins. Proc. Natl. Acad. Sci. USA 100 : 9912-9917. (10.1073/pnas.1733691100) / Proc. Natl. Acad. Sci. USA (2003)
Sambrook J. and D. W. Russell. 2001. Molecular cloning: a laboratory manual 3rd ed. Cold Spring Harbor Laboratory Press Cold Spring Harbor N.Y.
10.1016/0003-2697(87)90587-2
Toda, T., T. Tanaka, and M. Itaya. 1996. A method to invert DNA segments of the Bacillus subtilis 168 genome by recombination between two homologous sequences. Biosci. Biotechnol. Biochem. 60 : 773-778. (10.1271/bbb.60.773) / Biosci. Biotechnol. Biochem. (1996)
Yusupov, M. M., G. Z. Yusupova, K. Lieberman, T. N. Earnest, J. H. D. Cate, and H. F. Noller. 2001. Crystal structure of the ribosome at 5.5 Å resolution. Science 292 : 883-896. (10.1126/science.1060089) / Science (2001)

Dates

Type	When
Created	19 years, 5 months ago (March 17, 2006, 4:27 a.m.)
Deposited	1 year, 6 months ago (Feb. 3, 2024, 5:44 a.m.)
Indexed	1 year ago (Aug. 4, 2024, 4:41 a.m.)
Issued	19 years, 4 months ago (April 1, 2006)
Published	19 years, 4 months ago (April 1, 2006)
Published Print	19 years, 4 months ago (April 1, 2006)

Funders 0

None

BibTeX

@article{Akanuma_2006, title={Liberation of Zinc-Containing L31 (RpmE) from Ribosomes by Its Paralogous Gene Product, YtiA, inBacillus subtilis}, volume={188}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.188.7.2715-2720.2006}, DOI={10.1128/jb.188.7.2715-2720.2006}, number={7}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Akanuma, Genki and Nanamiya, Hideaki and Natori, Yousuke and Nomura, Naofumi and Kawamura, Fujio}, year={2006}, month=apr, pages={2715–2720} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2024,
        8,
        4
      ]
    ],
    "date-time": "2024-08-04T08:41:24Z",
    "timestamp": 1722760884602
  },
  "reference-count": 20,
  "publisher": "American Society for Microbiology",
  "issue": "7",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2006,
            4,
            1
          ]
        ],
        "date-time": "2006-04-01T00:00:00Z",
        "timestamp": 1143849600000
      },
      "content-version": "tdm",
      "delay-in-days": 0,
      "URL": "https://journals.asm.org/non-commercial-tdm-license"
    }
  ],
  "content-domain": {
    "domain": [
      "journals.asm.org"
    ],
    "crossmark-restriction": true
  },
  "published-print": {
    "date-parts": [
      [
        2006,
        4
      ]
    ]
  },
  "abstract": "<jats:title>ABSTRACT</jats:title><jats:p>We have found that alternative localization of two types of L31 ribosomal protein, RpmE and YtiA, is controlled by the intracellular concentration of zinc in<jats:italic>Bacillus subtilis</jats:italic>. The detailed mechanisms for the alternation of L31 proteins under zinc-deficient conditions were previously unknown. To obtain further information about this regulatory mechanism, we have studied the stability of RpmE in vivo and the binding affinity of these proteins to ribosomes in vitro, and we have found that liberation of RpmE from ribosomes is triggered by the expression of<jats:italic>ytiA</jats:italic>, which is induced by the derepression of Zur under zinc-deficient conditions.</jats:p>",
  "DOI": "10.1128/jb.188.7.2715-2720.2006",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2006,
        3,
        17
      ]
    ],
    "date-time": "2006-03-17T09:27:51Z",
    "timestamp": 1142587671000
  },
  "page": "2715-2720",
  "update-policy": "http://dx.doi.org/10.1128/asmj-crossmark-policy-page",
  "source": "Crossref",
  "is-referenced-by-count": 73,
  "title": "Liberation of Zinc-Containing L31 (RpmE) from Ribosomes by Its Paralogous Gene Product, YtiA, in<i>Bacillus subtilis</i>",
  "prefix": "10.1128",
  "volume": "188",
  "author": [
    {
      "given": "Genki",
      "family": "Akanuma",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Laboratory of Molecular Genetics and Frontier Project \u201cLife's Adaptation Strategies to Environmental Changes,\u201d Department of Life Science, College of Science, Rikkyo University, Toshima-ku, Tokyo 171-8501, Japan"
        }
      ]
    },
    {
      "given": "Hideaki",
      "family": "Nanamiya",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Laboratory of Molecular Genetics and Frontier Project \u201cLife's Adaptation Strategies to Environmental Changes,\u201d Department of Life Science, College of Science, Rikkyo University, Toshima-ku, Tokyo 171-8501, Japan"
        }
      ]
    },
    {
      "given": "Yousuke",
      "family": "Natori",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Laboratory of Molecular Genetics and Frontier Project \u201cLife's Adaptation Strategies to Environmental Changes,\u201d Department of Life Science, College of Science, Rikkyo University, Toshima-ku, Tokyo 171-8501, Japan"
        }
      ]
    },
    {
      "given": "Naofumi",
      "family": "Nomura",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Laboratory of Molecular Genetics and Frontier Project \u201cLife's Adaptation Strategies to Environmental Changes,\u201d Department of Life Science, College of Science, Rikkyo University, Toshima-ku, Tokyo 171-8501, Japan"
        }
      ]
    },
    {
      "given": "Fujio",
      "family": "Kawamura",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Laboratory of Molecular Genetics and Frontier Project \u201cLife's Adaptation Strategies to Environmental Changes,\u201d Department of Life Science, College of Science, Rikkyo University, Toshima-ku, Tokyo 171-8501, Japan"
        }
      ]
    }
  ],
  "member": "235",
  "reference": [
    {
      "key": "e_1_3_2_2_2",
      "doi-asserted-by": "crossref",
      "first-page": "345",
      "DOI": "10.1111/j.1574-6968.1999.tb08816.x",
      "volume": "180",
      "year": "1999",
      "unstructured": "Eistetter, A. J., P. D. Butler, R. R. Traut, and T. G. Fanning. 1999. Characterization of Escherichia coli 50S ribosomal protein L31. FEMS Microbiol. Lett. 180 : 345-349.",
      "journal-title": "FEMS Microbiol. Lett."
    },
    {
      "key": "e_1_3_2_3_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.180.22.5815-5821.1998"
    },
    {
      "key": "e_1_3_2_4_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.184.23.6508-6514.2002"
    },
    {
      "key": "e_1_3_2_5_2",
      "doi-asserted-by": "crossref",
      "first-page": "2897",
      "DOI": "10.1021/bi00835a031",
      "volume": "8",
      "year": "1969",
      "unstructured": "Hardy, S. J. S., C. G. Kurland, P. Voynow, and G. Mora. 1969. The ribosomal proteins of Eschericha coli. I. Purification of the 30S ribosomal proteins. Biochemistry 8 : 2897-2905.",
      "journal-title": "Biochemistry"
    },
    {
      "key": "e_1_3_2_6_2",
      "doi-asserted-by": "crossref",
      "first-page": "547",
      "DOI": "10.1038/nbt956",
      "volume": "22",
      "year": "2004",
      "unstructured": "Henne, A., H. Bruggemann, C. Raasch, A. Wiezer, T. Hartsch, H. Liesegang, A. Johann, T. Lienard, O. Gohl, R. Martinez-Arias, C. Jacobi, V. Starkuviene, S. Schlenczeck, S. Dencker, R. Huber, H. P. Klenk, W. Kramer, R. Merk, G. Gottschalk, and H. J. Fritz. 2004. The genome sequence of the extreme thermophile Thermus thermophilus. Nat. Biotechnol. 22 : 547-553.",
      "journal-title": "Nat. Biotechnol."
    },
    {
      "key": "e_1_3_2_7_2",
      "doi-asserted-by": "crossref",
      "first-page": "8826",
      "DOI": "10.1016/S0021-9258(18)47489-3",
      "volume": "262",
      "year": "1987",
      "unstructured": "Herold, M., and K. H. Nierhaus. 1987. Incorporation of six additional proteins to complete the assembly map of the 50S subunit from Escherichia coli ribosomes. J. Biol. Chem. 262 : 8826-8833.",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_3_2_8_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.186.16.5450-5459.2004"
    },
    {
      "key": "e_1_3_2_9_2",
      "doi-asserted-by": "crossref",
      "first-page": "91",
      "DOI": "10.1111/j.1574-6968.2001.tb10930.x",
      "volume": "205",
      "year": "2001",
      "unstructured": "Joseph, P., J. R. Fantino, M. L. Herbaud, and F. Denizot. 2001. Rapid orientated cloning in a shuttle vector allowing modulated gene expression in Bacillus subtilis. FEMS Microbiol. Lett. 205 : 91-97.",
      "journal-title": "FEMS Microbiol. Lett."
    },
    {
      "key": "e_1_3_2_10_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/36786"
    },
    {
      "key": "e_1_3_2_11_2",
      "first-page": "0033.1",
      "volume": "2",
      "year": "2001",
      "unstructured": "Makarova, K. S., V. A. Ponomarev, and E. V. Koonin. 2001. Two C or not two C: recurrent disruption of Zn-ribbons, gene duplication, lineage-specific gene loss, and horizontal gene transfer in evolution of bacterial ribosomal proteins. Genome Biol. 2 : 0033.1-0033.14.",
      "journal-title": "Genome Biol."
    },
    {
      "key": "e_1_3_2_12_2",
      "doi-asserted-by": "crossref",
      "first-page": "1672",
      "DOI": "10.1271/bbb.68.1672",
      "volume": "68",
      "year": "2004",
      "unstructured": "Murayama, R., G. Akanuma, Y. Makino, H. Nanamiya, and F. Kawamura. 2004. Spontaneous transformation and its use for genetic mapping in Bacillus subtilis. Biosci. Biotechnol. Biochem. 68 : 1672-1680.",
      "journal-title": "Biosci. Biotechnol. Biochem."
    },
    {
      "key": "e_1_3_2_13_2",
      "doi-asserted-by": "crossref",
      "first-page": "273",
      "DOI": "10.1111/j.1365-2958.2003.03972.x",
      "volume": "52",
      "year": "2004",
      "unstructured": "Nanamiya, H., G. Akanuma, Y. Natori, R. Murayama, S. Kosono, T. Kudo, K. Kobayashi, N. Ogasawara, S.-M. Park, K. Ochi, and F. Kawamura. 2004. Zinc is a key factor in controlling alternation of two types of L31 protein in the Bacillus subtilis ribosome. Mol. Microbiol. 52 : 273-283.",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "e_1_3_2_14_2",
      "doi-asserted-by": "crossref",
      "first-page": "505",
      "DOI": "10.1046/j.1365-2958.1998.00943.x",
      "volume": "29",
      "year": "1998",
      "unstructured": "Nanamiya, H., Y. Ohashi, K. Asai, S. Moriya, N. Ogasawara, M. Fujita, Y. Sadaie, and F. Kawamura. 1998. ClpC regulates the fate of a sporulation initiation sigma factor, \u03c3H protein, in Bacillus subtilis at elevated temperatures. Mol. Microbiol. 29 : 505-513.",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "e_1_3_2_15_2",
      "first-page": "85",
      "year": "2004",
      "unstructured": "Nierhaus, K. H. 2004. Assembly of the prokaryotic ribosome, p. 85-105. In K. H. Nierhaus and D. N. Wilson (ed.), Protein synthesis and ribosome structure. Wiley-VCH Verlag GmbH, Weinheim, Germany.",
      "journal-title": "Protein synthesis and ribosome structure"
    },
    {
      "key": "e_1_3_2_16_2",
      "doi-asserted-by": "crossref",
      "first-page": "2488",
      "DOI": "10.1126/science.1060331",
      "volume": "292",
      "year": "2001",
      "unstructured": "Outten, C. E., and T. V. O'Halloran. 2001. Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science 292 : 2488-2492.",
      "journal-title": "Science"
    },
    {
      "key": "e_1_3_2_17_2",
      "doi-asserted-by": "crossref",
      "first-page": "9912",
      "DOI": "10.1073/pnas.1733691100",
      "volume": "100",
      "year": "2003",
      "unstructured": "Panina, E. M., A. A. Mironov, and M. S. Gelfand. 2003. Comparative genomics of bacterial zinc regulons: enhanced ion transport, pathogenesis, and rearrangement of ribosomal proteins. Proc. Natl. Acad. Sci. USA 100 : 9912-9917.",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "e_1_3_2_18_2",
      "unstructured": "Sambrook J. and D. W. Russell. 2001. Molecular cloning: a laboratory manual 3rd ed. Cold Spring Harbor Laboratory Press Cold Spring Harbor N.Y."
    },
    {
      "key": "e_1_3_2_19_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0003-2697(87)90587-2"
    },
    {
      "key": "e_1_3_2_20_2",
      "doi-asserted-by": "crossref",
      "first-page": "773",
      "DOI": "10.1271/bbb.60.773",
      "volume": "60",
      "year": "1996",
      "unstructured": "Toda, T., T. Tanaka, and M. Itaya. 1996. A method to invert DNA segments of the Bacillus subtilis 168 genome by recombination between two homologous sequences. Biosci. Biotechnol. Biochem. 60 : 773-778.",
      "journal-title": "Biosci. Biotechnol. Biochem."
    },
    {
      "key": "e_1_3_2_21_2",
      "doi-asserted-by": "crossref",
      "first-page": "883",
      "DOI": "10.1126/science.1060089",
      "volume": "292",
      "year": "2001",
      "unstructured": "Yusupov, M. M., G. Z. Yusupova, K. Lieberman, T. N. Earnest, J. H. D. Cate, and H. F. Noller. 2001. Crystal structure of the ribosome at 5.5 \u00c5 resolution. Science 292 : 883-896.",
      "journal-title": "Science"
    }
  ],
  "container-title": "Journal of Bacteriology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://journals.asm.org/doi/pdf/10.1128/JB.188.7.2715-2720.2006",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://journals.asm.org/doi/pdf/10.1128/JB.188.7.2715-2720.2006",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2024,
        2,
        3
      ]
    ],
    "date-time": "2024-02-03T10:44:57Z",
    "timestamp": 1706957097000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://journals.asm.org/doi/10.1128/JB.188.7.2715-2720.2006"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2006,
        4
      ]
    ]
  },
  "references-count": 20,
  "journal-issue": {
    "issue": "7",
    "published-print": {
      "date-parts": [
        [
          2006,
          4
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1128/JB.188.7.2715-2720.2006"
  ],
  "URL": "http://dx.doi.org/10.1128/JB.188.7.2715-2720.2006",
  "relation": {},
  "ISSN": [
    "0021-9193",
    "1098-5530"
  ],
  "subject": [],
  "container-title-short": "J Bacteriol",
  "published": {
    "date-parts": [
      [
        2006,
        4
      ]
    ]
  },
  "assertion": [
    {
      "value": "2005-10-28",
      "order": 0,
      "name": "received",
      "label": "Received",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    },
    {
      "value": "2006-01-13",
      "order": 1,
      "name": "accepted",
      "label": "Accepted",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    },
    {
      "value": "2020-12-20",
      "order": 2,
      "name": "published",
      "label": "Published",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    }
  ]
}