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Chapter 32 : Retrons

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Abstract:

This chapter describes the genetic element called "retron," which is responsible for multicopy single-stranded DNA (msDNA) synthesis, and the mechanism of msDNA synthesis. It discusses the retron mobility and the relationship between retrons and pathogenicity. Retrons responsible for the synthesis of msDNA consist of three essential genes: for the RNA-coding region, for the DNA-coding region, and for reverse transcriptase (RT). A study of the codon usage for RTs revealed an interesting difference between retrons of and . The codon usage for RTs of is very typical for this species, further supporting the notion that retrons in myxobacteria are genetic elements that already existed in the genome of an ancestral bacterium before individual myxobacterial species evolved. In contrast, the codon usage for RTs of is significantly different from the general codon usage of . Emerging infectious diseases (EID) are a major public health issue of this millennium. It has been suggested that more virulent bacterial pathogens could emerge through recent acquisition of virulence factors. Retrons may be associated with bacterial pathogenicity, because all pathogenic strains produce msDNA, whereas all nonpathogenic strains do not. Identification of the retron insertion site, biochemical and pathological characterization of retrons, effects of mutations in the retron on its pathogenicity, and characterization of open reading frames (ORFs) downstream of RT are expected to provide important insights into the function of retrons, their origins, and the pathogenicity of the persistent human disease.

Citation: Yamanaka K, Inouye S, Inoye M, Shimamoto T. 2002. Retrons, p 784-795. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch32

Key Concept Ranking

DNA Synthesis
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Genetic Elements
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Single-Stranded Satellite DNA
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Nucleotide Excision Repair
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Figures

Image of Figure 1
Figure 1

Biosynthesis of msDNA. (A) Arrangement of and genes in a retron. Inverted repeats, a1/a2 and b1/ b2, are indicated by arrows. The G residue, which is used for priming cDNA synthesis, is circled. (B) The biosynthetic pathway of msDNA. The region and can be expressed under separate promoters. The transcript from the region is folded by forming stem structures between a1 and a2 inverted repeats as shown. The branching G residue is circled. The G residue opposite the branching G residue and an A:Upair immediately upstream of the G/G are highly conserved. The dotted line indicates the direction of cDNA synthesis from the branching G residue. Thick lines in the mRNA transcript correspond to the RNA molecule (msdRNA) in the msDNA. Gray lines in the msDNA correspond to the DNA molecule.

Citation: Yamanaka K, Inouye S, Inoye M, Shimamoto T. 2002. Retrons, p 784-795. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch32
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Image of Figure 2
Figure 2

Structures of msDNAs from retrons: msDNA Ec48 from Mao et al. ( ), msDNA Ec67 from Lampson et al. ( ), msDNA Ec73 from Sun et al. ( ), msDNA Ec78 from Lima and Lim ( ), msDNA Ec83 from Lim ( ), msDNA Ec86 from Lim and Maas ( ), and msDNA Ec107 from Herzer et al. ( ).

Citation: Yamanaka K, Inouye S, Inoye M, Shimamoto T. 2002. Retrons, p 784-795. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch32
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Image of Figure 3
Figure 3

Alignment of all known RTs. Alignments were performed by visual examination of the sequences and adopted with some modifications from the previous report ( ). Identical residues are shaded in black and functionally similar residues are shaded in gray. Residues shaded in black are biased toward Ec73, if other residues are also identical in the same row. Structural assignments for α and β structures are from the X-ray structure of HIV-RT ( ). X and Y sequences are found in retron RTs and other non-LTR-RTs ( ). The highly conserved VTGL sequence is marked by closed circles on the top, where the domain exchanges were performed between RT Ec73 and RT Ec86, as described in the text. The residues marked with stars are three Asp residues only known to be invariant among all known RTs and involved to form the catalytic triad essential for DNA polymerase activity ( ).

Citation: Yamanaka K, Inouye S, Inoye M, Shimamoto T. 2002. Retrons, p 784-795. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch32
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Image of Figure 4
Figure 4

Models for a retron RT forming a complex with a substrate. (A) A substrate-HIV-RT complex. The structure is cited from the report by Kohlstaedt et al. ( ). However, P51 and the connection and RNase H domain of P66, which do not exist in the structure of retron RT, are shown by a dotted line. X and VTGL represent two unique domain existing only in retron RTs, and arrows indicate possible insertion sites of these domains. (B) The primer-template RNA molecule for msDNA is superimposed on A. (C) The recognition stem-loop structure interacts with the external part of the thumb as discussed in the text. In panels B and C, the recognition stem-loop structure is indicated by an arrow. The branching G residue is circled.

Citation: Yamanaka K, Inouye S, Inoye M, Shimamoto T. 2002. Retrons, p 784-795. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch32
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References

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1. Binder, S.,, A. M. Levitt,, J. J. Sacks,, and J. M. Hughes. 1999. Emerging infectious diseases: public health issues for the 21st century. Science 284: 1311 1313.
2. Dhundale, A.,, T. Furuichi,, S. Inouye,, and M. Inouye. 1985. Distribution of multicopy single-stranded DNA among Myxobacteria and related species. J. Bacteriol. 164: 914 917.
3. Dhundale, A.,, B. Lampson,, T. Furuichi,, M. Inouye,, and S. Inouye. 1987. Structure of msDNA from Myxococcus xanthus: evidence for a long, self-annealing RNA precursor for the covalently linked, branched RNA. Cell 51: 1105 1112.
4. Furuichi, T.,, A. Dhundale,, M. Inouye,, and S. Inouye. 1987. Branched RNA covalently linked to the 5′end of a singlestranded DNA in Stigmatella aurantiaca: structure of msDNA. Cell 48: 47 53.
5. Furuichi, T.,, M. Inouye,, and S. Inouye. 1987. Biosynthesis and structure of stable branched RNA covalently linked to the 5′end of multicopy single-stranded DNA of Stigmatella aurantiaca. Cell 48: 55 62.
6. Halling, C.,, R. Calendar,, G. E. Christie,, E. C. Dale,, G. Deho,, S. Finkel,, J. Flensburg,, D. Ghisotti,, M. L. Kahn,, K. B. Lane,, C. S. Lin,, B. H. Lindquist,, L. S. Pierson,, E. W. Six,, M. G. Sunshine,, and R. Ziermann. 1990. DNA sequence of satellite bacteriophage P4. Nucleic Acids Res. 18: 1649.
7. Herzer, P. J.,, S. Inouye,, and M. Inouye. 1992. Retron-Ec107 is inserted into the Escherichia coli genome by replacing a palindromic 34-bp intergenic sequence. Mol. Microbiol. 6: 345 354.
8. Herzer, P. J.,, S. Inouye,, M. Inouye,, and T. S. Whittam. 1990. Phylogenetic distribution of branched RNA-linked multicopy single-stranded DNA among natural isolates of Escherichia coli. J. Bacteriol. 172: 6175 6181.
9. Hsu, M.-Y.,, S. G. Eagle,, M. Inouye,, and S. Inouye. 1992. Cellfree synthesis of the branched RNA-linked msDNA from retron- Ec67 of Escherichia coli. J. Biol. Chem. 267: 13823 13829.
10. Hsu, M.-Y.,, M. Inouye,, and S. Inouye. 1990. Retron for the 67-base multicopy single-strandedDNA from Escherichia coli: a potential transposable element encoding both reverse transcriptase and Dam methylase functions. Proc. Natl. Acad. Sci. USA 87: 9454 9458.
11. Hsu, M.-Y.,, S. Inouye,, and M. Inouye. 1989. Structural requirements of the RNA precursor for the biosynthesis of the branched RNA-linked multicopy single-stranded DNA of Myxococcus xanthus. J. Biol. Chem. 264: 6214 6219.
12. Hsu, M.-Y.,, C. Xu,, M. Inouye,, and S. Inouye. 1992. Similarity between the Myxococcus xanthus and Stigmatella aurantiaca reverse transcriptase genes associated with multicopy, singlestranded DNA. J. Bacteriol. 174: 2384 2387.
13. Inouye, M.,, and S. Inouye. 1991. msDNA and bacterial reverse transcriptase. Annu. Rev. Microbiol. 45: 163 186.
14. Inouye, M.,, and S. Inouye. 1992. Retrons and multicopy single- stranded DNA. J. Bacteriol. 174: 2419 2424.
15. Inouye, S.,, P. J. Herzer,, and M. Inouye. 1990. Two independent retrons with highly diverse transcriptase in Myxococcus xanthus. Proc. Natl. Acad. Sci. USA 87: 942 945.
16. Inouye, S.,, M.-Y. Hsu,, S. Eagle,, and M. Inouye. 1989. Reverse transcriptase associated with the biosynthesis of the branched RNA-linked msDNA in Myxococcus xanthus. Cell 56: 709 717.
17. Inouye, S.,, M.-Y. Hsu,, A. Xu,, and M. Inouye. 1999. Highly specific recognition of primer RNA structures for 2′-OH priming reaction by bacterial reverse transcriptase. J. Biol. Chem. 274: 31236 31244.
18. Inouye, S.,, and M. Inouye. 1993. The retron: a bacterial retroelement required for the synthesis of msDNA. Curr. Opin. Genet. Dev. 3: 713 718.
19. Inouye, S.,, and M. Inouye. 1996. Structure, function and evolution of bacterial reverse transcriptase. Virus Genes 11: 81 94.
20. Inouye, S.,, M. G. Sunshine,, E. W. Six,, and M. Inouye. 1991. Retronphage R73: an E. coli phage that contains a retroelement and integrates into a tRNA gene. Science 252: 969 971.
21. Jacobo-Molina, A.,, J. Ding,, R. G. Nanni,, A. D. Clark, Jr.,, X. Lu,, C. Tanillo,, R. L. Williams,, G. Kamer,, A. L. Ferris,, P. Clark,, A. Hizi,, S. H. Hughes,, and E. Arnold. 1993. Crystal structure of human immunodeficiency virus type 1 reverse transcriptase complexed with double-stranded DNA. Proc. Natl. Acad. Sci. USA 90: 6320 6324.
22. Kawaguchi, T.,, P. J. Herzer,, S. Inouye,, and M. Inouye. 1992. Sequence diversity of the 1.3-kb retron (retron-Ec107) among three distinct phylogenetic groups of Escherichia coli. Mol. Microbiol. 6: 355 361.
23. Kohlstaedt, L. A.,, J. Wang,, J. M. Friedman,, P. A. Rice,, and T. A. Steitz. 1992. Crystal structure at 3.5A resolution of HIV- 1 reverse transcriptase complexed with an inhibitor. Science 256: 1783 1790.
24. Lampson, B. C.,, M. Inouye,, and S. Inouye. 1991. Survey of multicopy single-stranded DNAs and reverse transcriptase genes among natural isolates of Myxococcus xanthus. J. Bacteriol. 173: 5363 5370.
24.a. Lampson, B. C.,, and S. A. Rice. 1997. Repetitive sequences found in the chromosome of the myxobacterium Nannocystis exedens are similar to msDNA: a possible retrotransposition event in bacteria. Mol. Microbiol. 23: 813 823.
25. Lampson, B. C.,, J. Sun,, M.-Y. Hsu,, J. Vallejo-Ramirez,, S. Inouye,, and M. Inouye. 1989. Reverse transcriptase in a clinical strain of E. coli: its requirement for the production of branched RNA-linked msDNA. Science 243: 1033 1038.
26. Legault, P.,, J. Li,, J. Mogridge,, L. E. Kay,, and J. Greenblatt. 1998. NMR structure of the bacteriophage lambda N peptide/ box B RNA complex: recognition of a GNRA fold by an arginine- rich motif. Cell 93: 289 299.
27. Li, B. H.,, A. Ebbert,, and R. Bockrath. 1999. Transcriptionmodulated repair in E. coli evident with UV-induced mutation spectra in supF. J. Mol. Biol. 294: 35 48.
28. Lim, D. 1991. Structure of two retrons of Escherichia coli and their common chromosomal insertion site. Mol. Microbiol. 5: 1863 1872.
29. Lim, D. 1992. Structure and biosynthesis of unbranched multicopy single-stranded DNA by reverse transcriptase in a clinical Escherichia coli isolate. Mol. Microbiol. 6: 3531 3542.
30. Lim, D.,, and W. K. Maas. 1989. Reverse transcriptase-dependent synthesis of a covalently linked, branched DNA-RNA compound in E. coli B. Cell 56: 891 904.
31. Lima, T. M.,, and D. Lim. 1997. A novel retron that produces RNA-less msDNA in Escherichia coli using reverse transcriptase. Plasmid 38: 25 33.
32. Maas, W. K.,, C. Wang,, T. Lima,, A. Hoch,, and D. Lim. 1996. Multicopy single-stranded DNA od Escherichia coli enhances mutation and recombination frequencies by titrating MutS protein. Mol. Microbiol. 19: 505 509.
33. Maas, W. K.,, C. Wang,, T. Lima,, G. Zubay,, and D. Lim. 1994. Multicopy single-stranded DNAs with mismatched base pair are mutagenic in Escherichia coli. Mol. Microbiol. 14: 437 441.
34. Mao, J. R.,, M. Inouye,, and S. Inouye. 1996. An unusual bacterial reverse transcriptase having LVDD in the YXDD box from Escherichia coli. Biochem. Biophys. Res. Commun. 227: 489 493.
35. Mao, J. R.,, S. Inouye,, and M. Inouye. 1996. Enhancement of frame-shift mutation by the overproduction of msDNA in Escherichia coli. FEMS Microbiol. Lett. 144: 109 115.
36. Mao, J. R.,, S. Inouye,, and M. Inouye. 1997. msDNA-Ec48, the smallest multicopy single-stranded DNA from Escherichia coli. J. Bacteriol. 179: 7865 7868.
37. Mao, J. R.,, M. Shimada,, S. Inouye,, and M. Inouye. 1995. Gene regulation by antisense DNA produced in vivo. J. Biol. Chem. 270: 19684 19687.
38. Miao, E. A.,, and S. I. Miller. 1999. Bacteriophages in the evolution of pathogen-host interactions. Proc. Natl. Acad. Sci. USA 96: 9452 9454.
39. Miller, V. L.,, and J. J. Mekalanos. 1988. A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J. Bacteriol. 170: 2575 2583.
40. Mirochnitchenko, O.,, S. Inouye,, and M. Inouye. 1994. Production of single-stranded DNA in mammalian cells by means of a bacterial retron. J. Biol. Chem. 269: 2380 2383.
41. Mirold, S.,, W. Rabsch,, M. Rohde,, S. Stender,, H. Tshäpe,, H. Rü ssmann,, E. Igure,, and W. Hardt. 1999. Isolation of a temperate bacteriophage encoding the type III effector protein SopE from an epidemic Salmonella typhimurium strain. Proc. Natl. Acad. Sci. USA 96: 9845 9850.
42. Miyata, S.,, A. Oshima,, S. Inouye,, and M. Inouye. 1992. In vitro production of a stable single-stranded cDNA in Saccharomyces cerevisiae by means of a bacterial retron. Proc. Natl. Acad. Sci. USA 89: 5735 5739.
43. Rice, S. A.,, and B. C. Lampson. 1993. Diversity of retron elements in population of a Rhizobia and other Gram-negative bacteria. J. Bacteriol. 175: 4250 4254.
44. Rice, S. A.,, and B. C. Lampson. 1995. Phylogenetic comparison of retron elements among the myxobacteria: evidence for vertical inheritance. J. Bacteriol. 177: 37 45.
45. Roberts, D.,, B. C. Hoopers,, W. R. McClure,, and N. Kleckner. 1985. IS10 transposition is regulated by DNA adenine methylation. Cell 43: 117 130.
46. Shimamoto, T.,, M.-Y. Hsu,, S. Inouye,, and M. Inouye. 1993. Reverse transcriptase from bacterial retrons require specific secondary structures at the 5′-end of the template for the cDNA priming reaction. J. Biol. Chem. 268: 2684 2692.
47. Shimamoto, T.,, H. Kawanishi,, T. Tsuchiya,, S. Inouye,, and M. Inouye. 1998. In vitro synthesis of multicopy single-stranded DNA, using separate primer and template RNAs, by Escherichia coli reverse transcriptase. J. Bacteriol. 180: 2999 3002.
48. Shimamoto, T.,, M. Shimada,, M. Inouye,, and S. Inouye. 1995. The role of ribonuclease H in multicopy single-stranded DNA synthesis in retron-Ec73 and retron-Ec107 of Escherichia coli. J. Bacteriol. 177: 264 267.
49. Shimamoto, T.,, M. Inouye,, and S. Inouye. 1995. The formation of the 2′,5′-phosphodiester linkage in the cDNA priming reaction by bacterial reverse transcriptase in a cell-free system. J. Biol. Chem. 270: 581 588.
50. Shimamoto, T.,, M. Kobayashi,, T. Tsuchiya,, S. Shinoda,, H. Kawakami,, S. Inouye,, and M. Inouye. 1999. A retroelement in Vibrio cholerae. Mol. Microbiol. 34: 631 632.
51. Steitz, T. A. 1999. DNA polymerase: structural diversity and common mechanisms. J. Biol. Chem. 274: 17395 17398.
52. Sun, J.,, P. J. Herzer,, M. P. Weinstein,, B. C. Lampson,, M. Inouye,, and S. Inouye. 1989. Extensive diversity of branched- RNA-linked multicopy single-stranded DNAs in clinical strains of Escherichia coli. Proc. Natl. Acad. Sci. USA 86: 7208 7212.
53. Sun, J.,, M. Inouye,, and S. Inouye. 1991. Association of a retroelement with a P4-like cryptic prophage (retronphage ϕR73) integrated into the selenocysteinyl tRNA gene of Escherichia coli. J. Bacteriol. 173: 4171 4181.
54. Temin, H. M. 1989. Retrons in bacteria. Nature 339: 254 255.
55. Viswanathan, M.,, M. Inouye,, and S. Inouye. 1989. Myxococcus xanthus msDNA-Mx162 exists as a complex with proteins. J. Biol. Chem. 264: 13665 13671.
56. Waldor, M. K.,, and J. J. Mekalanos. 1996. Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272: 1910 1914.
57. Yee, T.,, T. Furuichi,, S. Inouye,, and M. Inouye. 1984. Multicopy single-stranded DNA isolated from a Gram-negative bacterium Myxococcus xanthus. Cell 38: 203 209.

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