Full text in pdf format

 

Reverse transcriptases in bacteria: small RNAs as genetic vectors and biological modulators

 

 

M. Beljanski

Centre de Recherche Biologique - CERBIOL, 94200 Ivry-sur-Seine, France

 

 

ABSTRACT

In 1970, with my group at the Pasteur Institute in Paris, I observed that showdomycin resistant Escherichia coli cells excrete into their culture medium a small RNA, about 160 nucleotides long, rich in purine bases. This RNA transforms wild bacteria (E. coli and Agrobacterium tumefaciens) into transformants which exhibit new stable biochemical and physical characteristics. Thus A. tumefaciens once transformed by E. coil transforming RNA, partially or often totally loses its oncogenic potentialities and acquires new properties. It appeared that reverse transcriptase might give transforming RNA the means of integrating into the genome of the transformed organisms the modifications it vectored. We demonstrated (1971-1972) that bacterial reverse transcriptase was involved in this process. In the course of our studies on bacterial transformation, we devised a technique which led to the discovery, first of RNA free reverse transcriptase in bacteria, then of RNA-bound reverse transcriptase which is easily distinguishable from DNA- dependent-DNA polymerase. In 1989 several american scientists rediscovered reverse transcriptase in E. coli.

Keywords: Reverse transcriptases; Bacteria.

 

 

REFERENCES

Arsdell, S.W. Van, Donison, R.A., Bernstein, L.B., Weiner, A.M., Manser, T. and Gesteland, R.E (1981). Direct repeats flank three small nuclear RNA pseudogenes in the human genome. Cell 26: 11-17.

Beljanski, M. (1949). A propos du microdosage du ribose dans les acides nucléiques et leurs dérivés. Ann. Inst. Past. 76: 451-455.

Beljanski, M. (1972). Synthèse in vitro de l'ADN sur une matrice d'ARN par une transcriptase d'Escherichia coli. C.R. Acad. Sci. (Paris) 274: 2801-2804.

Beljanski, M. (1973). Séparation de la transcriptase inverse de l'ADN polymérase ADN dépendante. Analyse de l'ADN synthétisé sur le modèle de l'ARN transformant. C.R. Acad. Sci. (Paris) 276: 1625-1628.

Beljanski, M. and Beljanski, M.S. (1974). RNA-bound Reverse Transcriptase in Escherichia coli and in vitro synthesis of a complementary DNA. Biochem. Genet. 12: 163-180.

Beljanski, M. and Manigault, P. (1972). Genetic transformation of bacteria by RNA and loss of oncogenic power properties ofAgrobacterium tumefaciens. Transforming RNA as template for DNA synthesis. Sixth Miles International Symposium on Molecular Biology. (E Beers and R.C. Tilghamn, eds.). The Johns Hopkins University Press, Baltimore, pp. 81-97.

Beljanski, M. and Le Goff, L. (1986). Analysis of small RNA species: phylogenetic Trends. In: DNA Systematics (S.K. Dutta, eds.). Evolution. CRC Press Inc. Roca Raton Florida, pp. 81-104.

Beljanski, M. and Plawecki, M. (1973). Transforming RNA as a template directing RNA and DNA synthesis in bacteria. In: The role of RNA in Reproduction and Development (Niu and Segal, eds.). North Holland Publ. Co., pp. 203-224.

Beljanski, M. and Plawecki, M. (1975). Synthèse in vitro d'un ARN utilisé comme amorceur pour la réplication de l'ADN. C.R. Acad. Sci. (Paris) 278: 1413-1416, 280: 363-366.

Beljanski, M., Beljanski, M.S. and Bourgarel, P. (1971). ARN transformants porteurs de caractères héréditaires chez Escherichia coli showdomycino-resistant. C.R. Acad. Sci (Paris) 272: 2107-2110.

Beljanski, M., Beljanski, M.S. and Bourgarel, P. (1971). "Episome à ARN" porté par 1'ADN d'Escherichia coli sauvage et showdomycino-resistant. C.R. Acad. Sci. (Paris) 272: 2736-2739.

Beljanski, M., Bourgarel, P. and Beljanski, M.S. (1971). Drastic alteration of ribosomal RNA and ribosomal proteins in showdomycin-resistant Escherichia coll. Nat. Acad. Sci. (U.S.A.) 68: 491-495.

Beljanski, M., Beljanski, M.S., Manigault, P. and Bourgarel, P. (1972). Transformation of Agrobacterium tumefaciens into a non-oncogenic species by an Escherichia coli RNA. Proc. Nat. Acad. Sci. (U.S.A.) 69: 191-195.

Beljanski, M., Manigault, P., Beljanski, M.S. and Aaron-da Cunha, M.Y. (1974). Genetic transformation of Agrobacterium tumefaciens by RNA and nature of the tumor inducing principle. First Intern. Congress of the Intern. Assoc. of Microbiol. Sic. Tokyo LA.M.S., 1: 132-141.

Beljanski, M., Bourgarel, P. and Beljanski, M.S. (1978). Découpage des ARN ribosomiques d'Escherichia Coli par la ribonucléase U2 et transcription in vitro des ARN-fragments en ADN complémentaires. C.r Acad. Sci. (Paris) 286: 1825-1828.

Beljanski, M., Niu, L.C., Beljanski, M.S., Yan, S. and Niu, M.C. (1988). Iron stimulated RNA-dependent DNA polymerase activity from goldfish eggs. Cellular and Molecular Biology 34: 17-25.

Bernstein, L.B., Mount, S.M. and Weiner, A.M. (1983). Pseudogens for human small nuclear U3 appear to arise by integration of self-primed reverse transcripts of the RNA into new chromosomal sites. Cell 32: 461-472.

Bishop, J.M. (1978). Retroviruses. Ann. Rev. Biochem. 47: 35-88.

Braun, A.C. (1951). Cellular autonomy in Crown-gall. Phytopath. 14: 963-972.

Buchman, A.R. and Berg, P. (1988). Comparison of Intron-Dependent and Intron-Independent gene expression. Molecular and Cellular Biology 8: 4395-4405.

Dhundale, A., Lampson, B., Fumichi, T., Inouye, M. and Inouye, S. (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.

Dutta, S.K., Beljanski, M. and Bourgarel, P. (1977). Endogenous RNA-bound RNA dependent DNA polymerase activity in Neurospora crassa. Exp. Mycology 1: 173-182.

Grabkina, O.A., Vorob'eva, N.V., Buneva, V.N., Nagibneva, I.N., Panfilova, Z.I., Romashchenko, A.G. and Serdyukova, N.A. (1983). Localization of RNA-dependent DNA polymerase complex with endogenous matrix and discrimination of RNA and DNA-dependent DNA synthesis by the alkylating -amide of dTTP in Escherichia coli cells. Molekulyarnaya Biologiya 17: 1019-1017.

Jagadeeswaran, P., Forget, B.G. and Weissman, S.M. (1981). Short Interspersed Repetitive DNA elements in Eucaryotes. Transposable DNA elements generated by reverse transcription of RNA Pol III Transcripts. Cell 26: 141-142.

Lampson, B.C., Sun, J., Hsu, Mei-Yin, Vallejo-Ramirez, J., Inouye, S. and Inouye, M. (1989). Reverse transcriptase in a clinical strain of Escherichia coli: Production of branched RNA-linked msDNA. Science 243: 1033-1038.

Le Goff, L., Aaron-da-Cunha, M.Y. and Beljanski, M. (1976). Un ARN extrait d'Agrobacterium tumefaciens souches oncogènes et non oncogènes, éléments indispensables à l'induction des tumeurs chez Datura stramonium. Canad. J. of Microbiol. 22: 694-701.

Le Goff, L. and Beljanski, M. (1979). Biologie Moléculaire - Stimulation de l'induction - ou inhibition du développement - des tumeurs de Crown-gall par des ARN-fragments U2. Interférence de l'auxine. C.R. Acad. Sci. (Paris) 288: 147-150.

Lim, D. and Mass, K. (1989). Reverse transcriptase-dependent synthesis of a covalently linked, branched DNA-RNA compound in E. coli B. Cell 56: 891-904.

Mizuno, T., Chou, M-Y. and Inouye, M. (1983). Regulation of gene expression by a small RNA transcript (mic RNA) in Escherichia coll. K-12. Proc. Japan Acad. 59: 335-338.

Needham, J. (1935). Chemical embryology. Ann. Rev. Biochem. 4: 435-448.

Nelson, J.A., Levy, J.A., and Leong, J.C. (1981). Human placentas contain a specific inhibitor of RNA-directed DNA polymerase. Proc. Nat. Acad. Sci. (U.S.A.) 78: 1670-1674.

Niu, M.C. (1981). The effect of mRNA on nuclear activity in developing system. In: The Role of RNA in Development and Reproduction (Niu, M.C. and Zhuang, H.H., eds.). Science Press, Beijing or Van Nostrand Reinhard New-York, pp. 415-433.

Niu, M.C., Xue, G.X., Niu, L.C. and Huang, H.Z. (1989). Transfer of information from mRNA to chromosomes by reverse transcription in early development of goldfish eggs. Cellular and Molecular Biology 35: 333-345

Poiesz, B.J., Ruscetti, F.W., Reitz, M.S., Kalyanaraman, V.S. and Gallo, R.C. (1981). Isolation of a new type C retrovirus (HTLV) in primary uncultured cells of a patient with sezary T-cell leukemia. Nature 294: 268-271.

Raff, R.A., Colot, H.V., Selvig, S.E. and Gross, P.R. (1972). Oogenetic origin of messenger RNA for embryonic synthesis of microtube proteins. Nature (Lond.) 235: 211-214.

Romashchenko, A.G., Vorob'eva, N.V., Kozhemyakina, N.N., Potapov, V.A., Sidel'nikova, N.P., Staroobrazova, M.G. and Salganik, R.I. (1977). RNA-dependent DNA polymerase of Escherichia coli. Separation of the enzyme from DNA polymerase I, purification and properties. Doklady Akademii Nauk SSSR 233: 734-737.

Schmid, C.W. and Jelinek, W.R. (1982). The alu family of dispersed repetitive sequences. Science 216: 1065-1069.

Shiba, T. and Saigo, K. (1983). Retrovirus like particles containing RNA homologous to the transposable element copia in Drosophila melanogaster. Nature 302: 119-124.

Temin, H.M. (1989a). Retrons in bacteria. Nature 339: 254-255.

Temin, H.M. (1989b). Retrocitation. Nature 342: 624.

Vannus, H. (1989). Reverse transcription in bacteria. Minireview. Cell 56: 721-724.

Vorob'eva, N.V., Nebrat, L.T., Potapov, V.A., Romashchenko, A.G., Salganik, R.I. and Yushkova, L.F. (1982). Reverse transcription of heterologous RNA with the help of RNA-dependent DNA polymerase of Escherichia coli. Molekulyarnaya Biologia 16: 977-983.

Zucchi, T.M.A.D., Passos Jr., G.A.S. and de Lucca, F.L. (1989). R.N.A. - Mediated genetic transformation in Aspergillus nidulans. Cellular and Molecular biology 35: 573-580.