A LINE-like transposable element in Drosophila, the I factor, encodes a protein with properties similar to those of retroviral nucleocapsids

EMBO Journal

Volumn 16, Issue 14, 1997, Pages 4448-4455

  Dawson, A ^a   Hartswood, E ^a   Paterson, T ^a   Finnegan, D J ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

DNA binding protein; Drosophila; Nucleocapsid; Retrotransposon; Transposable element

Indexed keywords

COMPLEMENTARY DNA; DNA; DNA BINDING PROTEIN; GAG PROTEIN; OLIGONUCLEOTIDE; RNA; RNA BINDING PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; DNA TRANSPOSITION; DROSOPHILA; ESCHERICHIA COLI; LEPIDOPTERA; MOLECULAR WEIGHT; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN RNA BINDING; PROTEIN STRUCTURE; RETROVIRUS; REVERSE TRANSCRIPTION; TRANSPOSON; VIRUS NUCLEOCAPSID;

ANIMALS; CROSS-LINKING REAGENTS; DNA TRANSPOSABLE ELEMENTS; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ESCHERICHIA COLI; GLUTARAL; MOLECULAR WEIGHT; NUCLEOCAPSID; OPEN READING FRAMES; RECOMBINANT PROTEINS; RNA-BINDING PROTEINS; SEQUENCE DELETION; SPODOPTERA;

ESCHERICHIA COLI; LEPIDOPTERA; SPODOPTERA; SPODOPTERA FRUGIPERDA; UNIDENTIFIED RETROVIRUS;

EID: 0030746164     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.14.4448     Document Type: Article

References (53)

1. Aksoy, S., Williams, S., Chang, S. and Richards, F.F. (1990) SLACS retrotransposon from Trypanosoma brucei gambiense is similar to mammalian LINEs. Nucleic Acids Res., 18, 785-792.
2. Aronoff, R., Hajjar, A.M. and Linial, M.L. (1993) Avian retroviral RNA encapsidation: re-examination of functional 5′ RNA sequences and the role of nucleocapsid Cys-His motifs. J. Virol., 67, 178-188.
3. Berg, J.M. (1990) Zinc fingers and other metal-binding domains. J. Biol. Chem., 265, 6513-6516.
4. Boeke, J.D. and Corces, V.G. (1989) Transcription and reverse transcription of retrotransposons. Annu. Rev. Microbiol., 43, 403-434.
5. Bouhidel, K., Terzian, C. and Pinon, H. (1994) The full-length transcript of the I factor, a LINE element of Drosophila melanogaster, is a potential bicistronic RNA messenger. Nucleic Acids Res., 12, 2370-2374.
6. Bucheton, A. (1990) I transposable elements and I-R hybrid dysgenesis in Drosophila. Trends Genet., 6, 16-21.
7. Bucheton, A., Paro, R., Sang, H., Pelisson, A. and Finnegan, D.J. (1984) The molecular basis of I-R hybrid dysgenesis in Drosophila melanogaster: identification, cloning and properties of the I factor. Cell, 38, 153-163.
8. Cambareri, E.B., Helber, J. and Kinsey, J.A. (1994) Tadl-1, an active LINE-like element of Neurospora crassa. Mol. Gen. Genet., 242, 658-665.
9. Chaboissier, M.-C., Busseau, I., Prosser, J., Finnegan, D.J. and Bucheton, A. (1990) Identification of a potential RNA intermediate for transposition of the LINE-like element I factor in Drosophila melanogasler. EMBO J., 9, 3557-3563.
10. D'Ambrosio, E., Waitzkins, S.D., Witney, F.R., Salemme, A. and Furano, A.V. (1986) Structure of the highly repeated long interspersed repetitive DNA family (LINE or L1Rn) of the rat. Mol. Cell. Biol., 6, 411-424.
11. Demers, G.W., Matunis, M.J. and Hardison, R.C. (1989) The L1 family of long interspersed repetitive DNA in rabbits: sequence, copy number, conserved open reading frames, and similarity to keratin. J. Mol. Evol., 29, 3-19.
12. Di Nocera, P. (1988) Close relationship between non-viral retroposons in Drosophila melanogaster. Nucleic Acids Res., 16, 4041-4052.
13. Di Nocera, P.P. and Casari, G. (1987) Related polypeptides are encoded by Drosophila F elements, I factors, and mammalian L1 sequences. Proc. Natl Acad. Sci. USA, 84, 5483-5487.
14. Dombroski, B.A., Mathias, S.L., Nanthakumar, E., Scott, A.F. and Kazazian, H.H. (1991) Isolation of an active human transposable element. Science, 254, 1805-1808.
15. Dongmei, D.L., Korman, M.K., Jakubczak, J.L. and Eickbush, T.H. (1993) Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: a mechanism for non-LTR retrotransposition. Cell, 72, 595-605.
16. Dorfman, T., Luban, J., Goff, S.P., Haseltine, W.A. and Gottlinger, H.G. (1993) Mapping of functionally important residues of a cysteine-histidine box in the human immunodeficiency virus Type 1 nucleocapsid protein. J. Virol., 67, 6159-6169.
17. Fawcett, D.H., Lister, C.K., Kellett, E. and Finnegan, D.J. (1986) Transposable elements controlling I-R hybrid dysgenesis in D. melanogaster are similar to mammalian LINEs. Cell, 47, 1007-1015.
18. Feng, Q., Moran, J.V., Kazazian, H.H. and Boeke, J.D. (1996) Human L1 retrotransposon encodes a conserved endonuclease required for retrotransposition. Cell, 87, 905-916.
19. Finnegan, D.J. (1989) The I factor and I-R hybrid dysgenesis in Drosophila melanogaster. In Berg, D.E. and Howe, M.M. (eds), Mobile DNA. American Society for Microbiology, Washington, DC, pp. 503-517.
20. Franck, A., Guilley, H., Jonard, C., Richards, K. and Hirth, L. (1980) Nucleotide sequence of cauliflower mosaic virus DNA. Cell, 21, 285-294.
21. Franke, E.K., Yuan, H.E.H., Leigh Bossolt, K., Goff, S.P. and Luban, J. (1994) Specificity and sequence requirements for interactions between various retroviral Gag proteins. J. Virol., 68, 5300-5305.
22. Gabriel, A. and Boeke, J.D. (1991) Reverse transcriptase encoded by a retrotransposon from the trypanosomid Crithidia fasciculata. Proc. Natl Acad. Sci. USA, 88, 9794-9798.
23. Gabriel, A., Yen, T.J., Schwartz, D.C., Smith, C.L., Boeke, J.D., Sollner-Webb, B. and Cleveland, D.W. (1990) A rapidly rearranging retrotransposon within the miniexon gene locus of Crithidia fasciculata. Mol. Cell. Biol., 10, 615-624.
24. George, J.A., Burke, W.D. and Eickbush, T.H. (1996) Analysis of the 5′ junctions of R2 insertions with the 28S gene: implications for non-LTR retrotransposition. Genetics. 142, 853-863.
25. Hohjoh, H. and Singer, M.F. (1996) Cytoplasmic ribonucleoprotein complexes containing human LINE-1 protein and RNA. EMBO J., 3, 630-639.
26. Hutchison, C.A. III, Hardies, S.C., Loeb, D.D., Sehee, W.R. and Edgell, M.H. (1989) LINEs and related retroposons: long interspersed repeated sequences in the eucaryotic genome. In Berg, D.E. and Howe, M.M. (eds), Mobile DNA. American Society for Microbiology, Washington, DC, pp. 593-617.
27. Jakubczak, J.J., Xiong, Y. and Eickbush, T.H. (1990) Type I (R1) and type II (R2) ribosomal DNA insertions of Drosophila melanogaster are retrotransposable elements closely related to those of Bombyx mori. J. Mol. Biol., 212, 37-52.
28. Jensen, S., Cavarec, L., Gassama, M.-P. and Heidmann, T. (1995) Defective I elements introduced into Drosophila as transgenes can regulate reactivity and prevent I-R hybrid dysgenesis. Mol. Gen. Genet., 248, 381-390.
29. Klikova, M., Rhee, S.S., Hunter, E. and Rumil, T. (1995) Efficient in vivo and in vitro assembly of retroviral capsids from gag precursor proteins expressed in bacteria. J. Virol., 69, 1093-1098.
30. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
31. Lapadat-Tapolsky, M.H., Do Rocquigny, D., van Gent, B., Roques, B. and Plasterk, R. (1993) Interaction between HIV-1 nucleocapsid protein and viral DNA may have important functions in the viral life cycle. Nucleic Acids Res., 21, 831-839.
32. Leeton, P.R.J. and Smyth, D.R. (1993) An abundant LINE-like element amplified in the genome of Lilium speciosum. Mol. Gen. Genet., 237, 97-104.
33. Loeb, D.D., Padgett, R.W., Hardies, S.C., Sheher, W.R., Comer, M.B., Edgell, M.H. and Hutchison, C.A. (1986) The sequence of a large L1Md element reveals a tandemly repeated 5′ end and several features found in retrotransposons. Mol. Cell. Biol., 6, 168-182.
34. Luan, D.D. and Eickbush, T.H. (1995) RNA template requirements for target DNA-primed reverse transcription by the R2 retrotransposable element. Mol. Cell. Biol., 15, 3882-3891.
35. Luschnig, C., Hess, M., Pusch, O., Brookman, J. and Bachmir, A. (1995) The gag homologue of retrotransposon Ty1 assembles into spherical particles in Escherichia coli. Eur. J. Biochem., 228, 739-744.
36. Martin, S.L. (1991) Ribonucleoprotein particles with LINE-1 RNA in mouse embryonal carcinoma cells. Mol. Cell. Biol., 11, 4804-4807.
37. Mathias, M.L., Scott, A.F., Kazazian, H.H., Boeke, J.D. and Gabriel, A. (1991) Reverse transcriptase encoded by a human transposable element. Science, 254, 1808-1810.
38. McLean, C., Bucheton, A. and Finnegan, D.J. (1993) The 5′ end of the I factor, a LINE-like retrotransposon of Drosophila, contains an internal promoter and sequences that regulate expression. Mol. Cell. Biol., 13, 1042-1050.
39. Medhora, M., Mruyama, K. and Hartl, D.L. (1991) Molecular and functional analysis of the mariner mutator element Mos 1 in Drosophila. Genetics, 128, 311-318.
40. O'Hare, K., Alley, M.R.K., Cullingford, T.E., Driver, A. and Sanderson, M.J. (1991) DNA sequence of the Doc retroposon in the while-one mutant of Drosophila melanogaster and of secondary insertions in the phenotypically altered derivatives white-honey and white-eosin. Mol. Gen. Genet., 225, 17-24.
41. Pelisson, A. and Bregliano, J.-C. (1987) Evidence for rapid limitation of the I element copy number in a genome submitted to several generations of I-R hybrid dysgenesis in Drosophila melanogaster. Mol. Gen. Genet., 207, 306-313.
42. Pelisson, A., Song, S.U., Prud'homme, N., Smith, P.A., Bucheton, A. and Corces, V.G. (1994) Gypsy transposition correlates with the production of a retroviral envelope-like protein under tissue specific control of the Drosophila flamenco gene. EMBO J., 13, 4401-1411.
43. Primagii, A.F., Mizrokhi, L.J. and Ilyin, Y.V. (1988) The Drosophila mobile element jockey belongs to LINEs and contains coding sequences homologous to some retroviral proteins. Gene, 70, 253-262.
44. Pritchard, M.A., Dura, J.-M., Pelisson, A., Bucheton, A. and Finnegan, D.J. (1988) A cloned I-factor is fully functional in Drosophila melanogaster. Mol. Gen. Genet., 214, 533-540.
45. Schwartz-Sommer, Z., Leclercq, L., Gobel, F. and Saedler, H. (1987) Cin4, an insert altering the structure of the A1 gene in Zea mays exhibits properties of non-viral retrotransposons. EMBO J., 6, 3873-3880.
46. Singer, M.F. and Skowronski, J. (1985) Making sense out of LINES: long interspersed repeat sequences in mammalian genomes. Trends Biochem. Sci., 10, 119-122.
47. Song, S.U., Kurkulos, M., Gerasimova, T., Boeke, J.D. and Corces, V.G. (1994) An env-like protein encoded by a Drosophila retroelement: evidence that gypsy is an infectious retrovirus. Genes Dev., 8, 2046-2057.
48. Studier, W.F., Rosenberg, A.H., Dunn, J.J. and Dubendorff, J.W. (1990) Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol., 185, 60-89.
49. Thomsen, D.R., Meyer, A.L. and Post, L.E. (1992) Expression of feline leukaemia virus gp95 and gag proteins and assembly into virus-like particles using the baculovirus expression vector system. J. Gen. Virol., 73, 1819-1824.
50. Tsuchihashi, Z. and Brown, P.O. (1994) DNA strand exchange and selective DNA annealing promoted by the Human Immunodeficiency Virus Type 1 nucleocapsid protein. J. Virol., 68, 5863-5870.
51. Udomkit, A., Forbes, S., Dalgleish, G. and Finnegan, D.J. (1995) BS a novel LINE-like element in Drosophila melanogaster. Nucleic Acids Res., 23, 1354-1358.
52. Udomkit, A., Forbes, S., Arkhipova, L. McLean, C. and Finnegan, D.J. (1996) Control of expression of the I factor, a LINE-like transposable element in Drosophila melanogaster. EMBO J., 15, 3174-3181.
53. Wright, D.A., Ke, N., Smalle, B.M., Goodman, H.M. and Voytas, D.F. (1996) Multiple non-LTR retrotransposons in the genome of Arabidopsis thaliana. Genetics, 142, 569-578.