Previous Article | Next Article 
Molecular and Cellular Biology, January 2001, p. 467-475, Vol. 21, No. 2
0270-7306/01/$04.00+0 DOI: 10.1128/MCB.21.2.467-475.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Nucleic Acid Chaperone Activity of the ORF1 Protein
from the Mouse LINE-1 Retrotransposon
Sandra L.
Martin1,2,* and
Frederic D.
Bushman2
Department of Cellular and Structural
Biology, University of Colorado School of Medicine, Denver,
Colorado 80262,1 and Infectious Disease
Laboratory, The Salk Institute, La Jolla, California
920372
Received 26 July 2000/Returned for modification 11 September
2000/Accepted 22 October 2000
Non-LTR retrotransposons such as L1 elements are major components
of the mammalian genome, but their mechanism of replication is
incompletely understood. Like retroviruses and LTR-containing retrotransposons, non-LTR retrotransposons replicate by reverse transcription of an RNA intermediate. The details of cDNA priming and
integration, however, differ between these two classes. In retroviruses, the nucleocapsid (NC) protein has been shown to assist reverse transcription by acting as a "nucleic acid
chaperone," promoting the formation of the most stable duplexes
between nucleic acid molecules. A protein-coding region with an NC-like
sequence is present in most non-LTR retrotransposons, but no such
sequence is evident in mammalian L1 elements or other
members of its class. Here we investigated the ORF1 protein from mouse
L1 and found that it does in fact display nucleic acid chaperone
activities in vitro. L1 ORF1p (i) promoted annealing of complementary
DNA strands, (ii) facilitated strand exchange to form the most stable hybrids in competitive displacement assays, and (iii) facilitated melting of an imperfect duplex but stabilized perfect duplexes. These
findings suggest a role for L1 ORF1p in mediating nucleic acid strand
transfer steps during L1 reverse transcription.
*
Corresponding author. Mailing address: Department of
Cellular and Structural Biology, B111, University of Colorado School of
Medicine, 4200 E. Ninth Ave., Denver, CO 80262. Phone: (303) 315-6284. Fax: (303) 315-4729. E-mail: sandy.martin{at}uchsc.edu.
Molecular and Cellular Biology, January 2001, p. 467-475, Vol. 21, No. 2
0270-7306/01/$04.00+0 DOI: 10.1128/MCB.21.2.467-475.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Kano, H., Godoy, I., Courtney, C., Vetter, M. R., Gerton, G. L., Ostertag, E. M., Kazazian, H. H. Jr
(2009). L1 retrotransposition occurs mainly in embryogenesis and creates somatic mosaicism. Genes Dev.
23: 1303-1312
[Abstract]
[Full Text]
-
Khazina, E., Weichenrieder, O.
(2009). Non-LTR retrotransposons encode noncanonical RRM domains in their first open reading frame. Proc. Natl. Acad. Sci. USA
106: 731-736
[Abstract]
[Full Text]
-
Dong, C., Poulter, R. T., Han, J. S.
(2009). LINE-Like Retrotransposition in Saccharomyces cerevisiae. Genetics
181: 301-311
[Abstract]
[Full Text]
-
Martin, S. L., Bushman, D., Wang, F., Li, P. W.-L., Walker, A., Cummiskey, J., Branciforte, D., Williams, M. C.
(2008). A single amino acid substitution in ORF1 dramatically decreases L1 retrotransposition and provides insight into nucleic acid chaperone activity. Nucleic Acids Res
36: 5845-5854
[Abstract]
[Full Text]
-
Kirilyuk, A., Tolstonog, G. V., Damert, A., Held, U., Hahn, S., Lower, R., Buschmann, C., Horn, A. V., Traub, P., Schumann, G. G.
(2008). Functional endogenous LINE-1 retrotransposons are expressed and mobilized in rat chloroleukemia cells. Nucleic Acids Res
36: 648-665
[Abstract]
[Full Text]
-
Chung, T., Siol, O., Dingermann, T., Winckler, T.
(2007). Protein Interactions Involved in tRNA Gene-Specific Integration of Dictyostelium discoideum Non-Long Terminal Repeat Retrotransposon TRE5-A. Mol. Cell. Biol.
27: 8492-8501
[Abstract]
[Full Text]
-
Ichiyanagi, K., Nishihara, H., Duvernell, D. D., Okada, N.
(2007). Acquisition of Endonuclease Specificity during Evolution of L1 Retrotransposon. Mol Biol Evol
24: 2009-2015
[Abstract]
[Full Text]
-
Januszyk, K., Li, P. W.-l., Villareal, V., Branciforte, D., Wu, H., Xie, Y., Feigon, J., Loo, J. A., Martin, S. L., Clubb, R. T.
(2007). Identification and Solution Structure of a Highly Conserved C-terminal Domain within ORF1p Required for Retrotransposition of Long Interspersed Nuclear Element-1. J. Biol. Chem.
282: 24893-24904
[Abstract]
[Full Text]
-
Garcia-Perez, J. L., Marchetto, M. C.N., Muotri, A. R., Coufal, N. G., Gage, F. H., O'Shea, K. S., Moran, J. V.
(2007). LINE-1 retrotransposition in human embryonic stem cells. Hum Mol Genet
16: 1569-1577
[Abstract]
[Full Text]
-
Garcia-Perez, J. L., Doucet, A. J., Bucheton, A., Moran, J. V., Gilbert, N.
(2007). Distinct mechanisms for trans-mediated mobilization of cellular RNAs by the LINE-1 reverse transcriptase. Genome Res
17: 602-611
[Abstract]
[Full Text]
-
Ichiyanagi, K., Nakajima, R., Kajikawa, M., Okada, N.
(2007). Novel retrotransposon analysis reveals multiple mobility pathways dictated by hosts. Genome Res
17: 33-41
[Abstract]
[Full Text]
-
An, W., Han, J. S., Wheelan, S. J., Davis, E. S., Coombes, C. E., Ye, P., Triplett, C., Boeke, J. D.
(2006). Active retrotransposition by a synthetic L1 element in mice. Proc. Natl. Acad. Sci. USA
103: 18662-18667
[Abstract]
[Full Text]
-
Christensen, S. M., Ye, J., Eickbush, T. H.
(2006). Eukaryotic Transposable Elements and Genome Evolution Special Feature: RNA from the 5' end of the R2 retrotransposon controls R2 protein binding to and cleavage of its DNA target site. Proc. Natl. Acad. Sci. USA
103: 17602-17607
[Abstract]
[Full Text]
-
Muckenfuss, H., Hamdorf, M., Held, U., Perkovic, M., Lower, J., Cichutek, K., Flory, E., Schumann, G. G., Munk, C.
(2006). APOBEC3 Proteins Inhibit Human LINE-1 Retrotransposition. J. Biol. Chem.
281: 22161-22172
[Abstract]
[Full Text]
-
Kubo, S., Seleme, M. d. C., Soifer, H. S., Perez, J. L. G., Moran, J. V., Kazazian, H. H. Jr., Kasahara, N.
(2006). L1 retrotransposition in nondividing and primary human somatic cells. Proc. Natl. Acad. Sci. USA
103: 8036-8041
[Abstract]
[Full Text]
-
Seleme, M. d. C., Vetter, M. R., Cordaux, R., Bastone, L., Batzer, M. A., Kazazian, H. H. Jr.
(2006). Extensive individual variation in L1 retrotransposition capability contributes to human genetic diversity. Proc. Natl. Acad. Sci. USA
103: 6611-6616
[Abstract]
[Full Text]
-
Lucchinetti, E., Feng, J., Silva, R. d., Tolstonog, G. V., Schaub, M. C., Schumann, G. G., Zaugg, M.
(2006). Inhibition of LINE-1 expression in the heart decreases ischemic damage by activation of Akt/PKB signaling. Physiol. Genomics
25: 314-324
[Abstract]
[Full Text]
-
Farkash, E. A., Kao, G. D., Horman, S. R., Prak, E. T. L.
(2006). Gamma radiation increases endonuclease-dependent L1 retrotransposition in a cultured cell assay. Nucleic Acids Res
34: 1196-1204
[Abstract]
[Full Text]
-
Li, P. W.-L., Li, J., Timmerman, S. L., Krushel, L. A., Martin, S. L.
(2006). The dicistronic RNA from the mouse LINE-1 retrotransposon contains an internal ribosome entry site upstream of each ORF: implications for retrotransposition. Nucleic Acids Res
34: 853-864
[Abstract]
[Full Text]
-
Babushok, D. V., Ostertag, E. M., Courtney, C. E., Choi, J. M., Kazazian, H. H. Jr.
(2006). L1 integration in a transgenic mouse model. Genome Res
16: 240-250
[Abstract]
[Full Text]
-
Khan, H., Smit, A., Boissinot, S.
(2006). Molecular evolution and tempo of amplification of human LINE-1 retrotransposons since the origin of primates. Genome Res
16: 78-87
[Abstract]
[Full Text]
-
Heras, S. R., Lopez, M. C., Garcia-Perez, J. L., Martin, S. L., Thomas, M. C.
(2005). The L1Tc C-Terminal Domain from Trypanosoma cruzi Non-Long Terminal Repeat Retrotransposon Codes for a Protein That Bears Two C2H2 Zinc Finger Motifs and Is Endowed with Nucleic Acid Chaperone Activity. Mol. Cell. Biol.
25: 9209-9220
[Abstract]
[Full Text]
-
Kulpa, D. A., Moran, J. V.
(2005). Ribonucleoprotein particle formation is necessary but not sufficient for LINE-1 retrotransposition. Hum Mol Genet
14: 3237-3248
[Abstract]
[Full Text]
-
Gilbert, N., Lutz, S., Morrish, T. A., Moran, J. V.
(2005). Multiple Fates of L1 Retrotransposition Intermediates in Cultured Human Cells. Mol. Cell. Biol.
25: 7780-7795
[Abstract]
[Full Text]
-
Christensen, S. M., Eickbush, T. H.
(2005). R2 Target-Primed Reverse Transcription: Ordered Cleavage and Polymerization Steps by Protein Subunits Asymmetrically Bound to the Target DNA. Mol. Cell. Biol.
25: 6617-6628
[Abstract]
[Full Text]
-
Zingler, N., Willhoeft, U., Brose, H.-P., Schoder, V., Jahns, T., Hanschmann, K.-M. O., Morrish, T. A., Lower, J., Schumann, G. G.
(2005). Analysis of 5' junctions of human LINE-1 and Alu retrotransposons suggests an alternative model for 5'-end attachment requiring microhomology-mediated end-joining. Genome Res
15: 780-789
[Abstract]
[Full Text]
-
Kajikawa, M., Ichiyanagi, K., Tanaka, N., Okada, N.
(2005). Isolation and Characterization of Active LINE and SINEs from the Eel. Mol Biol Evol
22: 673-682
[Abstract]
[Full Text]
-
Seleme, M. d. C., Disson, O., Robin, S.ép., Brun, C., Teninges, D., Bucheton, A.
(2005). In vivo RNA localization of I factor, a non-LTR retrotransposon, requires a cis-acting signal in ORF2 and ORF1 protein. Nucleic Acids Res
33: 776-785
[Abstract]
[Full Text]
-
Bennett, E. A., Coleman, L. E., Tsui, C., Pittard, W. S., Devine, S. E.
(2004). Natural Genetic Variation Caused by Transposable Elements in Humans. Genetics
168: 933-951
[Abstract]
[Full Text]
-
Ergun, S., Buschmann, C., Heukeshoven, J., Dammann, K., Schnieders, F., Lauke, H., Chalajour, F., Kilic, N., Stratling, W. H., Schumann, G. G.
(2004). Cell Type-specific Expression of LINE-1 Open Reading Frames 1 and 2 in Fetal and Adult Human Tissues. J. Biol. Chem.
279: 27753-27763
[Abstract]
[Full Text]
-
Goodier, J. L., Ostertag, E. M., Engleka, K. A., Seleme, M. C., Kazazian, H. H. Jr
(2004). A potential role for the nucleolus in L1 retrotransposition. Hum Mol Genet
13: 1041-1048
[Abstract]
[Full Text]
-
Cristofari, G., Ivanyi-Nagy, R., Gabus, C., Boulant, S., Lavergne, J.-P., Penin, F., Darlix, J.-L.
(2004). The hepatitis C virus Core protein is a potent nucleic acid chaperone that directs dimerization of the viral (+) strand RNA in vitro. Nucleic Acids Res
32: 2623-2631
[Abstract]
[Full Text]
-
Gabus, C., Mazroui, R., Tremblay, S., Khandjian, E. W., Darlix, J.-L.
(2004). The fragile X mental retardation protein has nucleic acid chaperone properties. Nucleic Acids Res
32: 2129-2137
[Abstract]
[Full Text]
-
Farley, A. H., Luning Prak, E. T., Kazazian, H. H. Jr
(2004). More active human L1 retrotransposons produce longer insertions. Nucleic Acids Res
32: 502-510
[Abstract]
[Full Text]
-
Matsumoto, T., Takahashi, H., Fujiwara, H.
(2004). Targeted Nuclear Import of Open Reading Frame 1 Protein Is Required for In Vivo Retrotransposition of a Telomere-Specific Non-Long Terminal Repeat Retrotransposon, SART1. Mol. Cell. Biol.
24: 105-122
[Abstract]
[Full Text]
-
Martin, S. L., Branciforte, D., Keller, D., Bain, D. L.
(2003). Trimeric structure for an essential protein in L1 retrotransposition. Proc. Natl. Acad. Sci. USA
100: 13815-13820
[Abstract]
[Full Text]
-
Biedler, J., Tu, Z.
(2003). Non-LTR Retrotransposons in the African Malaria Mosquito, Anopheles gambiae: Unprecedented Diversity and Evidence of Recent Activity. Mol Biol Evol
20: 1811-1825
[Abstract]
[Full Text]
-
Morales, J. F., Snow, E. T., Murnane, J. P.
(2003). Environmental factors affecting transcription of the human L1 retrotransposon. II. Stressors. Mutagenesis
18: 151-158
[Abstract]
[Full Text]
-
Kolosha, V. O., Martin, S. L.
(2003). High-affinity, Non-sequence-specific RNA Binding by the Open Reading Frame 1 (ORF1) Protein from Long Interspersed Nuclear Element 1 (LINE-1). J. Biol. Chem.
278: 8112-8117
[Abstract]
[Full Text]
-
Huang, Z.-S., Su, W.-H., Wang, J.-L., Wu, H.-N.
(2003). Selective Strand Annealing and Selective Strand Exchange Promoted by the N-terminal Domain of Hepatitis Delta Antigen. J. Biol. Chem.
278: 5685-5693
[Abstract]
[Full Text]
-
Kapitonov, V. V., Jurka, J.
(2003). The Esterase and PHD Domains in CR1-Like Non-LTR Retrotransposons. Mol Biol Evol
20: 38-46
[Abstract]
[Full Text]
-
Deininger, P. L., Batzer, M. A.
(2002). Mammalian Retroelements. Genome Res
12: 1455-1465
[Abstract]
[Full Text]
-
Esnault, C., Casella, J.-F., Heidmann, T.
(2002). A Tetrahymena thermophila ribozyme-based indicator gene to detect transposition of marked retroelements in mammalian cells. Nucleic Acids Res
30: e49-e49
[Abstract]
[Full Text]
-
Chambeyron, S., Bucheton, A., Busseau, I.
(2002). Tandem UAA Repeats at the 3'-End of the Transcript Are Essential for the Precise Initiation of Reverse Transcription of the I Factor in Drosophila melanogaster. J. Biol. Chem.
277: 17877-17882
[Abstract]
[Full Text]
-
Morales, J. F., Snow, E. T., Murnane, J. P.
(2002). Environmental factors affecting transcription of the human L1 retrotransposon. I. Steroid hormone-like agents. Mutagenesis
17: 193-200
[Abstract]
[Full Text]
-
Casaregola, S., Neuveglise, C., Bon, E., Gaillardin, C.
(2002). Ylli, a Non-LTR Retrotransposon L1 Family in the Dimorphic Yeast Yarrowia lipolytica. Mol Biol Evol
19: 664-677
[Abstract]
[Full Text]
-
Rashkova, S., Karam, S. E., Pardue, M.-L.
(2002). Element-specific localization of Drosophila retrotransposon Gag proteins occurs in both nucleus and cytoplasm. Proc. Natl. Acad. Sci. USA
99: 3621-3626
[Abstract]
[Full Text]
-
Arkhipova, I. R., Morrison, H. G.
(2001). From the Cover: Three retrotransposon families in the genome of Giardia lamblia: Two telomeric, one dead. Proc. Natl. Acad. Sci. USA
98: 14497-14502
[Abstract]
[Full Text]
-
Boissinot, S., Furano, A. V.
(2001). Adaptive Evolution in LINE-1 Retrotransposons. Mol Biol Evol
18: 2186-2194
[Abstract]
[Full Text]
-
Malik, H. S., Eickbush, T. H.
(2001). Phylogenetic Analysis of Ribonuclease H Domains Suggests a Late, Chimeric Origin of LTR Retrotransposable Elements and Retroviruses. Genome Res
11: 1187-1197
[Abstract]
[Full Text]
-
Monroy, M. A., Ruhl, D. D., Xu, X., Granner, D. K., Yaciuk, P., Chrivia, J. C.
(2001). Regulation of cAMP-responsive Element-binding Protein-mediated Transcription by the SNF2/SWI-related Protein, SRCAP. J. Biol. Chem.
276: 40721-40726
[Abstract]
[Full Text]