Nimbus (BgI): An active non-LTR retrotransposon of the Schistosoma mansoni snail host Biomphalaria glabrata

International Journal for Parasitology

Volumn 37, Issue 12, 2007, Pages 1307-1318

  Raghavan, Nithya ^a   Tettelin, Hervé ^b   Miller, André ^a   Hostetler, Jessica ^b   Tallon, Luke ^b   Knight, Matty ^a  

^a BIOMEDICAL RESEARCH INSTITUTE   (United States)

^b J CRAIG VENTER INSTITUTE   (United States)

Author keywords

Biomphlaria glabrata; I clade; Mobile genetic element; Nimbus (BgI); Non LTR retrotransposon; Reverse transcriptase; Schistosoma mansoni

Indexed keywords

DNA FRAGMENT;

CHROMOSOME; DISEASE CONTROL; DISEASE TRANSMISSION; ENDEMIC SPECIES; FLY; MOLECULAR ANALYSIS; NEOTROPICAL REGION; NUCLEIC ACID; PHYLOGENETICS; SCHISTOSOMIASIS; SNAIL;

ARTICLE; ARTIFICIAL CHROMOSOME; BIOMPHALARIA GLABRATA; CLADISTICS; CONTROLLED STUDY; GENE; GENE DELETION; GENE IDENTIFICATION; GENE SEQUENCE; GENETIC TRANSFORMATION; HOST; LONG TERMINAL REPEAT; NIMBUS GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHYLOGENY; PROTEIN DOMAIN; RETROPOSON; SCHISTOSOMA MANSONI; SEQUENCE ANALYSIS;

ANIMALS; BIOMPHALARIA; CHROMOSOMES, ARTIFICIAL, BACTERIAL; DNA, HELMINTH; GENES, HELMINTH; GENOME; HUMANS; MOLECULAR SEQUENCE DATA; POLYMERASE CHAIN REACTION; RETROELEMENTS; RNA-DIRECTED DNA POLYMERASE; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS; SEQUENCE ANALYSIS, DNA; TERMINAL REPEAT SEQUENCES; TRANSGENES;

AEDES AEGYPTI; ASCIDIA; BACTERIA (MICROORGANISMS); BASOMMATOPHORA; BIOMPHALARIA GLABRATA; CIONA INTESTINALIS; GASTROPODA; SCHISTOSOMA MANSONI;

EID: 34548041151     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2007.04.002     Document Type: Article

References (58)

1. Adema C.M., Luo M., Hanelt B., Hertel L.A., Marshall J.J., Zhang S., DeJong R.J., Kim H., Kudrna D., Wing R.W., Soderlund C., Knight M., Lewis F.A., Caldeira R.L., Jannotti-Passos L.K., Carvalho O.S., and Loker E.S. A bacterial artificial chromosome library for Biomphalaria glabrata, intermediate snail host of Schistosoma mansoni. Mem. Inst. Oswaldo Cruz 101 Suppl. I (2006) 167-177
2. Altschul S.F., Gish W., Miller W., Myers E.W., and Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 215 (1990) 403-410
3. Apweiler R., Attwood T.K., Bairoch A., Bateman A., Birney E., Biswas M., Bucher P., Cerutti L., Corpet F., Croning M.D., Durbin R., Falquet L., Fleischmann W., Gouzy J., Hermjakob H., Hulo N., Jonassen I., Kahn D., Kanapin A., Karavidopoulou Y., Lopez R., Marx B., Mulder N.J., Oinn T.M., Pagni M., Servant F., Sigrist C.J., and Zdobnov E. The InterPro database, an integrated documentation resource for protein families, domains and functional sites. Nucleic Acids Res. 29 (2001) 37-40
4. Berezikov E., Bucheton A., and Busseau I. A search for reverse transcriptase-coding sequences reveals new non-LTR retrotransposons in the genome of Drosophila melanogaster. Genome Biol. 1 (2000) RESEARCH0012. Epub 2000
5. Bouchut A., Coustau C., Gourbal B., and Mitta G. Compatibility in the Biomphalaria glabrata/Echinostoma caproni model: new candidate genes evidenced by a suppressive subtractive hybridization approach. Parasitology 134 (2007) 575-588 Epub 2006
6. Boulo V., Cadoret J.P., Shike H., Shimizu C., Miyanohara A., and Burns J.C. Infection of cultured embryo cells of the pacific oyster, Crassostrea gigas, by pantropic retroviral vectors. In Vitro Cell. Dev. Biol. Anim. 36 (2000) 395-399
7. Brindley P.J., Laha T., and McManus D.P. Loukas A. Mobile genetic elements colonizing the genomes of metazoan parasites. Trends Parasitol. 19 (2003) 79-87 review
8. Busseau I., Chaboissier M.C., Pelisson A., and Bucheton A. I factors in Drosophila melanogaster: transposition under control. Genetica 93 (1994) 101-116 review
9. Charlesworth B., Sniegowski P., and Stephan W. The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371 (1994) 215-220
10. Coates C.J., Jasinskiene N., Miyashiro L., and James A.A. Mariner transposition and transformation of the yellow fever mosquito, Aedes aegypti. Proc. Natl. Acad. Sci. USA 95 (1998) 3748-3751
11. Craig N.L. In: Craig N.L., Craigie R., Gellert M., and Lambowitz A. (Eds). Mobile DNA II (2002), ASM Press Publishers, Washington, DC 3-11
12. Cribb T.H., Bray R.A., and Littlewood D.T. The nature and evolution of the association among digeneans, molluscs and fishes. Int. J. Parasitol. 31 (2001) 997-1011
13. Dawson A., Hartswood E., Paterson T., and Finnegan D.J. A LINE-like transposable element in Drosophila, the I factor, encodes a protein with properties similar to those of retroviral nucleocapsids. EMBO J. 16 (1997) 4448-4455
14. Dejong R.J., Morgan J.A., Wilson W.D., Al-Jaser M.H., Appleton C.C., Coulibaly G., D'Andrea P.S., Doenhoff M.J., Haas W., Idris M.A., Magalhaes L.A., Mone H., Mouahid G., Mubila L., Pointier J.P., Webster J.P., Zanotti-Magalhaes E.M., Paraense W.L., Mkoji G.M., and Loker E.S. Phylogeography of Biomphalaria glabrata and B. pfeifferi, important intermediate hosts of Schistosoma mansoni in the New and Old World tropics. Mol. Ecol. 12 (2003) 3041-3056
15. Devereux J., Haeberli P., and Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 12 (1984) 387-395
16. Dewilde S., Winnepenninckx B., Arndt M.H., Nascimento D.G., Santoro M.M., Knight M., Miller A.N., Kerlavage A.R., Geoghagen N., Van Marck E., Liu L.X., Weber R.E., and Moens L. characterisation of the myoglobin and its coding gene of the mollusc Biomphalaria glabrata. J. Biol. Chem. 273 (1998) 13583-13592
17. Eickbush T.H. Transposing without ends: the non-LTR retrotransposable elements. New Biol. 4 (1992) 430-440 review
18. Eickbush T.H. Origin and evolutionary relationship of retroelements. In: Morse S.S. (Ed). Evolutionary Biology of Viruses (1994), Raven Press, NY 121-157
19. Fanning T.G., and Singer M.F. LINE-1: a mammalian transposable element. Biochim. Biophys. Acta 910 (1987) 203-212 review
20. Fawcett D.H., Lister C.K., Kellett E., and Finnegan D.J. Transposable elements controlling I-R hybrid dysgenesis in D. melanogaster are similar to mammalian LINEs. Cell 47 (1986) 1007-1015
21. Fedoroff N.V. Transposable elements as a molecular evolutionary force. Ann. NY. Acad. Sci. 870 (1999) 251-264 review
22. Feng Q., Schumann G., and Boeke J.D. Retrotransposon R1Bm endonuclease cleaves the target sequence. Proc. Natl. Acad. Sci. USA 95 (1998) 2083-2088
23. Finnegan D.J. Eukaryotic transposable elements and genome evolution. Trends Genet. 5 (1989) 103-107 review
24. Finnegan D.J. Transposable elements: how non-LTR retrotransposons do it. Curr. Biol. 7 (1997) R245-R248 review
25. Gaffney P.M., Pierce J.C., Mackinley A.G., Titchen D.A., and Glenn W.K. Pearl, a novel family of putative transposable elements in bivalve mollusks. J. Mol. Evol. 56 (2003) 308-316
26. Gregory T.R. Genome size estimates for two important freshwater molluscs, the zebra mussel (Dreissena polymorpha) and the schistosomiasis vector snail (Biomphalaria glabrata). Genome 46 (2003) 841-844
27. Han J.S., and Boeke J.D. A highly active synthetic mammalian retrotransposon. Nature 429 (2004) 314-318
28. Han J.S., Szak S.T., and Boeke J.D. Transcriptional disruption by the L1 retrotransposon and implications for mammalian transcriptomes. Nature 429 (2004) 268-274
29. Jasinskiene N., Coates C.J., Benedict M.Q., Cornel A.J., Rafferty C.S., James A.A., and Collins F.H. Stable transformation of the yellow fever mosquito, Aedes aegypti, with the Hermes element from the housefly. Proc. Natl. Acad. Sci. USA 95 (1998) 3743-3747
30. Katz R.A., and Jentoft J.E. What is the role of the cys-his motif in retroviral nucleocapsid (NC) proteins?. Bioessays 11 (1989) 176-181
31. Kidwell M.G., and Wattam A.R. An important step forward in the genetic manipulation of mosquito vectors of human disease. Proc. Natl. Acad. Sci. USA 95 (1998) 3349-3350
32. Kimmel B.E., ole-MoiYoi O.K., and Young J.R. Ingi, a 5.2-kb dispersed sequence element from Trypanosoma brucei that carries half of a smaller mobile element at either end and has homology with mammalian LINEs. Mol. Cell. Biol. 7 (1987) 1465-1475
33. Knight M., Miller A., Raghavan N., Richards C., and Lewis F. Identification of a repetitive element in the snail Biomphalaria glabrata: relationship to the reverse transcriptase-encoding sequence in LINE-1 transposons. Gene 118 (1992) 181-187
34. Knight M., Miller A.N., Geoghagen N.S.M., Lewis F.A., and Kerlavage A.R. Expressed sequence tags (ESTs) of Biomphalaria glabrata, an intermediate snail host of Schistosoma mansoni: use in the identification of RFLP markers. Malacologia 39 (1998) 175-182
35. Lebens M., Sun J.B., Czerkinsky C., and Holmgren J. Current status and future prospects for a vaccine against schistosomiasis. Expert Rev. Vaccines 3 (2004) 315-328 review
36. Lockyer A.E., Noble L.R., Rollinson D., and Jones C.S. Schistosoma mansoni: resistant specific infection-induced gene expression in Biomphalaria glabrata identified by fluorescent-based differential display. Exp. Parasitol. 107 (2004) 97-104
37. Luan D.D., Korman M.H., Jakubczak J.L., and Eickbush T.H. Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: a mechanism for non-LTR retrotransposition. Cell 72 (1993) 595-605
38. Malik H.S., Burke W.D., and Eickbush T.H. The age and evolution of non-LTR retrotransposable elements. Mol. Biol. Evol. 16 (1999) 793-805
39. Maniatis T., Fritsch E.F., and Sambrook J. Molecular Cloning, A Laboratory Manual (1982), Cold Spring Harbor Laboratory, Cold Spring Harbor, New York
40. Martin F., Maranon C., Olivares M., Alonso C., and Lopez MC. characterisation of a non-long terminal repeat retrotransposon cDNA (L1Tc) from Trypanosoma cruzi: homology of the first ORF with the ape family of DNA repair enzymes. J. Mol. Biol. 247 (1995) 49-59
41. Miller A.N., Raghavan N., FitzGerald P.C., Lewis F.A., and Knight M. Differential gene expression in haemocytes of the snail Biomphalaria glabrata: effects of Schistosoma mansoni infection. Int. J. Parasitol. 31 (2001) 687-696
42. Muotri A.R., Chu V.T., Marchetto M.C., Deng W., Moran J.V., and Gage F.H. Somatic mosaicism in neuronal precursor cells mediated by L1 retrotransposition. Nature 435 (2005) 903-910
43. Newton W.L. The establishment of a strain of Australorbis glabratus which combines albinism and high susceptibility to infection with Schistosoma mansoni. J. Parasitol. 41 (1955) 526-528
44. Paraense W., and Correa L. Variation in susceptibility of populations of Australorbis glabratus to a strain of Schistosoma mansoni. Rev. Inst. Med.Trop. Sao Paulo 5 (1963) 15-22
45. Pearce E.J. Progress towards a vaccine for schistosomiasis. Acta Trop. 86 (2003) 309-313 review
46. Permanyer J., Gonzàlez-Duarte R., and Albalat R. The non-LTR retrotransposons in Ciona intestinalis: new insights into the evolution of chordate genomes. Genome Biol. 4 (2003) R73
47. Permanyer J., Albalat R., and Gonzàlez-Duarte R. Getting closer to a pre-vertebrate genome: the non-LTR retrotransposons of Branchiostoma floridae. Int. J. Biol. Sci. 2 (2006) 48-53
48. Perrière G., and Gouy M. WWW-Query: An on-line retrieval system for biological sequence banks. Biochimie 78 (1996) 364-369
49. Raghavan N., Miller A.N., Gardner M., FitzGerald P.C., Kerlavage A.R., Johnston D.A., Lewis F.A., and Knight M. Comparative gene analysis of Biomphalaria glabrata haemocytes pre- and post-exposure to miracidia of Schistosoma mansoni. Mol. Biochem. Parasitol. 126 (2003) 181-191
50. Raghavan N., and Knight M. The snail (Biomphalaria glabrata) genome project. Trends Parasitol. 22 (2006) 148-151
51. Rice P., Longden I., and Bleasby A. EMBOSS: the European molecular biology open software suite. Trends Genet. 16 (2000) 276-277
52. Rowling, J.K., 1998. Harry Potter and the Sorcerer's Stone. Scholastic, Arthur A. Levine Books, USA.
53. Scott A.F., Schmeckpeper B.J., Comey C.T., Abdelrazik M., O'Hara B., Rossiter J.P., Cooley T., Heath P., Smith K.D., and Margolet L. Origin of the human L1 elements: proposed progenitor genes deduced from a consensus DNA sequence. Genomics 1 (1987) 113-125
54. Stewart G., Furst A., and Avdalovic N. Transverse alternating field electrophoresis (TAFE). Biotechniques 6 (1988) 68-73
55. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., and Higgins D.G. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25 (1997) 4876-4882
56. Tran M.H., Pearson M.S., Bethony J.M., Smyth D.J., Jones M.K., Duke M., Don T.A., McManus D.P., Correa-Oliveira R., and Loukas A. Tetraspanins on the surface of Schistosoma mansoni are protective antigens against schistosomiasis. Nat. Med. 12 (2006) 835-840 Epub. 2006, Jun 18
57. Tu Z., and Hill J.J. MosquI, a novel family of mosquito retrotransposons distantly related to the Drosophila I factors, may consist of elements of more than one origin. Mol. Biol. Evol. 16 (1999) 1675-1686
58. Zhang S.M., Adema C.M., Kepler T.B., and Loker E.S. Diversification of Ig superfamily genes in an invertebrate. Science 305 (2004) 251-254