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PMID: 11470904 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

A conserved RNA structure (thi box) is involved in regulation of thiamin biosynthetic gene expression in bacteria.

Proceedings of the National Academy of Sciences of the United States of America ·Vol. 98 ·No. 17 ·2001-08-14 ·Pages 9736-41

Miranda-Ríos J, Navarro M, Soberón M

Abstract

The thiCOGE genes of Rhizobium etli code for enzymes involved in thiamin biosynthesis. These genes are transcribed with a 211-base untranslated leader that contains the thi box, a 38-base sequence highly conserved in the 5' regions of thiamin biosynthetic and transport genes of Gram-positive and Gram-negative organisms. A deletion analysis of thiC-lacZ fusions revealed an unexpected relationship between the degree of repression shown by the deleted derivatives and the length of the thiC sequences present in the transcript. Three regions were found to be important for regulation: (i) the thi box sequence, which is absolutely necessary for high-level expression of thiC; (ii) the region immediately upstream to the translation start codon of thiC, which can be folded into a stem-loop structure that would mask the Shine-Dalgarno sequence; and (iii) the proximal part of the coding region of thiC, which was shown to contain a putative Rho-independent terminator. A comparative phylogenetic analysis revealed a possible folding of the thi box sequence into a hairpin structure composed of a hairpin loop, two helices, and an interior loop. Our results show that thiamin regulation of gene expression involves a complex posttranscriptional mechanism and that the thi box RNA structure is indispensable for thiCOGE expression.

MeSH Terms
5' Untranslated Regions/chemistry,genetics,metabolism Bacterial Proteins/biosynthesis,genetics Escherichia coli/genetics Gene Expression Regulation, Bacterial/drug effects,genetics Genome, Bacterial Lac Operon Models, Genetic Nucleic Acid Conformation Operon RNA, Bacterial/chemistry,genetics,metabolism RNA, Messenger/genetics,metabolism Recombinant Fusion Proteins/biosynthesis Regulatory Sequences, Nucleic Acid Rhizobium/genetics Sequence Deletion Structure-Activity Relationship Thiamine/biosynthesis,pharmacology
Chemicals
5' Untranslated Regions Bacterial Proteins RNA, Bacterial RNA, Messenger Recombinant Fusion Proteins ThiC protein, Bacteria Thiamine
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Miranda-Ríos J
Departamento de Microbiología Molecular, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Morelos. [email protected]
Navarro M
Soberón M
References (44)
44 references, click to expand
  1. Making ends meet: a model for RNA splicing in fungal mitochondria.
    Nature. 1982 Dec 23;300(5894):719-24 PMID: 6757759
  2. Coupled changes in translation and transcription during cobalamin-dependent regulation of btuB expression in Escherichia coli.
    J Bacteriol. 1998 Dec;180(24):6719-28 PMID: 9852020
  3. thiK and thiL loci of Escherichia coli.
    J Bacteriol. 1982 Aug;151(2):708-17 PMID: 6284709
  4. Thiamine pyrophosphate (TPP) negatively regulates transcription of some thi genes of Salmonella typhimurium.
    J Bacteriol. 1996 May;178(9):2533-8 PMID: 8626319
  5. Comparison of fungal mitochondrial introns reveals extensive homologies in RNA secondary structure.
    Biochimie. 1982 Oct;64(10):867-81 PMID: 6817818
  6. Multiple transcribed elements control expression of the Escherichia coli btuB gene.
    J Bacteriol. 1997 Jun;179(12):4039-42 PMID: 9190822
  7. An adenosyl-cobalamin (coenzyme-B12)-repressed translational enhancer in the cob mRNA of Salmonella typhimurium.
    Mol Microbiol. 2001 Mar;39(6):1585-94 PMID: 11260475
  8. Characterization of thiI, a new gene involved in thiazole biosynthesis in Salmonella typhimurium.
    J Bacteriol. 1997 Jul;179(13):4399-402 PMID: 9209060
  9. Cobalamin (coenzyme B12): synthesis and biological significance.
    Annu Rev Microbiol. 1996;50:137-81 PMID: 8905078
  10. Characterization of thiL, encoding thiamin-monophosphate kinase, in Salmonella typhimurium.
    J Biol Chem. 1997 Jun 20;272(25):15702-7 PMID: 9188462
  11. Vitamin B12 repression of the btuB gene in Salmonella typhimurium is mediated via a translational control which requires leader and coding sequences.
    Mol Microbiol. 1997 Jan;23(1):35-42 PMID: 9004218
  12. Transcribed sequences of the Escherichia coli btuB gene control its expression and regulation by vitamin B12.
    Proc Natl Acad Sci U S A. 1991 Feb 15;88(4):1479-83 PMID: 1847525
  13. Nucleotide sequence of a yeast tyrosine transfer RNA.
    Science. 1966 Jul 29;153(3735):531-4 PMID: 5938777
  14. Adenosylcobalamin inhibits ribosome binding to btuB RNA.
    Proc Natl Acad Sci U S A. 2000 Jun 20;97(13):7190-5 PMID: 10852957
  15. Repression of synthesis of the vitamin B12 receptor in Escherichia coli.
    J Bacteriol. 1978 Dec;136(3):1050-7 PMID: 363685
  16. Thiamin biosynthesis in Escherichia coli. Identification of ThiS thiocarboxylate as the immediate sulfur donor in the thiazole formation.
    J Biol Chem. 1998 Jun 26;273(26):16555-60 PMID: 9632726
  17. Promoters in the nodulation region of the Rhizobium leguminosarum Sym plasmid pRL1JI.
    Plant Mol Biol. 1987 Jan;9(1):27-39 PMID: 24276795
  18. Cloning and characterization of a gene from Escherichia coli encoding a transketolase-like enzyme that catalyzes the synthesis of D-1-deoxyxylulose 5-phosphate, a common precursor for isoprenoid, thiamin, and pyridoxol biosynthesis.
    Proc Natl Acad Sci U S A. 1998 Mar 3;95(5):2105-10 PMID: 9482846
  19. Gene organization and primary structure of a ribosomal RNA operon from Escherichia coli.
    J Mol Biol. 1981 May 15;148(2):107-27 PMID: 7028991
  20. Vitamin B12 repression of the cob operon in Salmonella typhimurium: translational control of the cbiA gene.
    Mol Microbiol. 1994 Aug;13(3):541-53 PMID: 7527895
  21. Thiamin biosynthesis in prokaryotes.
    Arch Microbiol. 1999 Apr;171(5):293-300 PMID: 10382260
  22. Expression pattern of Rhizobium etli ccmIEFH genes involved in c-type cytochrome maturation.
    Gene. 2000 May 30;250(1-2):149-57 PMID: 10854788
  23. STAB-SD: a Shine-Dalgarno sequence in the 5' untranslated region is a determinant of mRNA stability.
    Mol Microbiol. 1996 May;20(3):633-43 PMID: 8736542
  24. Secondary structure model for 23S ribosomal RNA.
    Nucleic Acids Res. 1981 Nov 25;9(22):6167-89 PMID: 7031608
  25. A positive selection vector for cloning of long polymerase chain reaction fragments based on a lethal mutant of the crp gene of Escherichia coli.
    Anal Biochem. 1998 Mar 15;257(2):203-9 PMID: 9514792
  26. RNA aptamers to the peptidyl transferase inhibitor chloramphenicol.
    Chem Biol. 1997 Nov;4(11):833-43 PMID: 9384530
  27. A conserved RNA structure element involved in the regulation of bacterial riboflavin synthesis genes.
    Trends Genet. 1999 Nov;15(11):439-42 PMID: 10529804
  28. Effect of ermC leader region mutations on induced mRNA stability.
    J Bacteriol. 1991 Jun;173(12):3732-40 PMID: 1711026
  29. Regulation of cobalamin biosynthetic operons in Salmonella typhimurium.
    J Bacteriol. 1987 May;169(5):2251-8 PMID: 3032913
  30. Phylogenetic comparative analysis and the secondary structure of ribonuclease P RNA--a review.
    Gene. 1989 Oct 15;82(1):65-75 PMID: 2479592
  31. Structural genes for thiamine biosynthetic enzymes (thiCEFGH) in Escherichia coli K-12.
    J Bacteriol. 1993 Feb;175(4):982-92 PMID: 8432721
  32. thiBPQ encodes an ABC transporter required for transport of thiamine and thiamine pyrophosphate in Salmonella typhimurium.
    J Biol Chem. 1998 Apr 10;273(15):8946-50 PMID: 9535878
  33. Cobalamin (vitamin B12) repression of the Cob operon in Salmonella typhimurium requires sequences within the leader and the first translated open reading frame.
    Mol Microbiol. 1992 Mar;6(6):743-9 PMID: 1374146
  34. 5S RNA secondary structure.
    Nature. 1975 Aug 7;256(5517):505-7 PMID: 808733
  35. Secondary structure model for bacterial 16S ribosomal RNA: phylogenetic, enzymatic and chemical evidence.
    Nucleic Acids Res. 1980 May 24;8(10):2275-93 PMID: 6159576
  36. Identification and characterization of an operon in Salmonella typhimurium involved in thiamine biosynthesis.
    J Bacteriol. 1997 Aug;179(15):4894-900 PMID: 9244280
  37. Conserved structural and regulatory regions in the Salmonella typhimurium btuB gene for the outer membrane vitamin B12 transport protein.
    Res Microbiol. 1992 Jun;143(5):459-66 PMID: 1448622
  38. Rhizobium phaseoli symbiotic mutants with transposon Tn5 insertions.
    J Bacteriol. 1984 Apr;158(1):148-55 PMID: 6325385
  39. Saccharomyces cerevisiae has a U1-like small nuclear RNA with unexpected properties.
    Science. 1987 Sep 18;237(4821):1484-7 PMID: 3306922
  40. Identification of a thiamin-dependent synthase in Escherichia coli required for the formation of the 1-deoxy-D-xylulose 5-phosphate precursor to isoprenoids, thiamin, and pyridoxol.
    Proc Natl Acad Sci U S A. 1997 Nov 25;94(24):12857-62 PMID: 9371765
  41. Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure.
    J Mol Biol. 1999 May 21;288(5):911-40 PMID: 10329189
  42. Self-cleavage of plus and minus RNAs of a virusoid and a structural model for the active sites.
    Cell. 1987 Apr 24;49(2):211-20 PMID: 2436805
  43. Expression of thiamin biosynthetic genes (thiCOGE) and production of symbiotic terminal oxidase cbb3 in Rhizobium etli.
    J Bacteriol. 1997 Nov;179(22):6887-93 PMID: 9371431
  44. High-resolution molecular discrimination by RNA.
    Science. 1994 Mar 11;263(5152):1425-9 PMID: 7510417
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
DOI
10.1073/pnas.161168098
Email
[email protected]
Published
2001-08-14
Epub
2001-00-24
Pages
9736-41
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC55522
Subset
IM
Corrections
CommentIn
PMID: 11504932
External Links
PubMed source DOI: 10.1073/pnas.161168098 PMC Full Text View journal details
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