Molecular Biology, Vol. 35, No. 6, 2001, pp. 874–882. Translated from Molekulyarnaya Biologiya, Vol. 35, No. 6, 2001, pp. 1023–1031. Original Russian Text Copyright © 2001 by Chaley, Korotkov.
UDC 577.212.3
Evolution of MIR Elements Located in the Coding Regions of Human Genome M. B. Chaley and E. V. Korotkov Center of Bioengineering, Russian Academy of Sciences, Moscow, 117312 Russia; E-mail:
[email protected] Received December 19, 2000
Abstract—A search for new members of the mammalian interspersed repeat (MIR) family has been done over the coding regions of human genome from GenBank-116. Only 254 nucleotide sequences contained MIRs in coding regions, of which 45 MIR copies were unknown before, including 17 that occurred in translated gene regions. The program developed by the authors has been demonstrated to surpass the CENSOR program in the search power. The evolution of the MIR copies located in translated regions of human genome is discussed. Key words: computer analysis, MIR elements, CORE-SINE family, evolution of translated gene regions, human genome
INTRODUCTION Repeated DNA sequences comprise a major part of eukaryotic genomes. Clarifying their origin, evolution, and influence on the host genome is of fundamental importance for the study of genomes [1]. The share of the repeats spreading by transposition in the human genome is more than 42% [2]. The transposition proceeds either by reverse transcription of the RNA mediator (reverse transposition or retroposition) or by excision of the DNA sequence and its insertion into a new site (DNA transposition) by enzyme transposase encoded by this DNA sequence. Most reversetransposed repeats belong either to short or long interspersed nuclear elements (SINEs or LINEs, respectively) or to retrovirus-like elements. SINEs are characterized by length of 100–400 bp and, as a rule, possess a complex structure of several units, one of which contains the promoter of RNA polymerase III responsible for transcriptional activity. LINEs vary from 3 to 8 kb and bear a gene for reverse transcriptase that also has endonuclease activity [3]. It is now generally accepted that transposition of SINEs involves the proteins encoded by the corresponding group of LINEs. SINEs have a tRNA-like structure at the 5' end and share a common 3'-terminal fragment with LINEs that is considered to be a binding site for reverse transcriptase [4, 5]. The examples of such a relationship between SINEs and LINEs are: SINE Bov-tA and LINE Bov-B from bovine genome, tortoise Pol III/SINE and turtle CR1-like LINE, and HpaI SINE and RSg-1 LINE in fishes [6]. Mammalian interspersed repeats (MIRs) are classical tRNA-like SINEs of 260 bp in length, whose sequences are substantially diverged, so that these
repeats were discovered by several authors mainly owing to their most conserved central part often called the “core” [7–10]. At the present time, the MIR structure is described in detail and consists of the conserved part containing the tRNA-like region from the 1st to the 80th base followed by the central domain, the core, of 65 bp and the variable part from the 146th to the 263rd base that displays similarity with the 3' ends of LINEs [6, 10]. The age of MIRs was first estimated at 130 million years, since MIRs occur in genomes of marsupials and ancient oviparous mammals [11, 12]. Analysis of similarity of the 3' ends revealed five MIR subfamilies in mammals [6]. The MIR consensus of placental mammals called Ter-1 coincides with that revealed earlier in humans [10]. Moreover, the comparison of the consensus sequences of tRNA-like SINEs from genomes of invertebrate animals, fishes, reptiles, and birds demonstrated the obvious similarity not only of their tRNA-like parts, but also of their cores [6]. This allowed one to consider the evolution of mammalian MIRs as part of common evolution of a CORE-SINE repeat family bearing a generic CORE-SINE that has spread by borrowing reverse transcriptase from different LINE families (by addition of the 3' end containing the binding site for this enzyme) [13]. The similarity observed between Ter-1 and the SINE consensus sequences of fishes, reptiles, and birds testifies to the occurrence of CORE-SINEs 300–400 million years ago. The remarkable similarity between the central regions of Ter-1 and OR2 SINE of octopuses suggests that CORE-SINEs age about 550 million years [13, 14]. In addition to the origination and spreading of MIRs, there is another aspect of the repeat evolution,
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Table 1. MIRs missed by the CENSOR program [22] during the search among the primate nucleotide sequences from GenBank-112 (the list is an addition to that from Repbase http://charon.girinst.org/server/arc). I, inverted complementary MIR copy; D, MIR copy in direct orientation; symbol * marks MIR copies in untranslated parts of exons GenBank accession number AB000462* AB000462* AB012922* AB015201* AB015201 AB015201 AF127916* AJ006835* D63710* L04193* L39874* M22898* M37815* M86360* M86360 M86360 M86360 M86360 U29926* U65416* U67092* U70065* U92316* X54156* X77738* Y09764* Y09764 AB007921 AF050154 AF050154 AF050154 AF050154 AF069489 AJ004799 AJ004799 AJ004799 AL021808 AL021808 M12523 M12523 M68516 M68516 M68516 M68516 M68516 M68516 M68516
MIR consensus coordinates 77 108 73 78 77 59 150 208 30 57 118 131 60 80 62 114 61 77 11 24 8 74 87 131 21 112 34 23 66 39 81 2 80 77 1 70 15 6 148 16 6 23 77 105 36 66 133
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4927 4552 574 1511 1754 2907 6203 1869 2296 919 828 483 2043 8795 9961 10,137 5599 2925 2625 11,715 532 13,003 425 19,068 13,250 10,388 4608 3199 12,956 17,039 29,630 17,518 3402 29,652 9745 8962 5759 61,573 11,813 9000 366 1383 2240 4581 4757 13,280 14,305 2001
4981 4609 645 1664 1797 3010 6279 1908 2426 1002 953 549 2132 8873 10,077 10,176 5666 2991 2741 11,771 589 13,053 484 19,134 13,337 10,515 4668 3396 13,122 17,151 29,689 17,607 3446 29,780 9797 9039 5824 61,616 11,921 9183 508 1482 2347 4682 4859 13,354 14,408
Significance
Orientation
7.03 7.31 8.95 9.20 7.65 9.62 7.44 7.20 7.83 8.47 7.79 7.09 7.74 7.59 8.74 7.85 7.09 7.01 7.42 7.14 8.13 7.73 7.76 7.10 9.24 8.07 7.36 11.12 7.73 7.44 7.11 8.45 7.29 8.20 7.26 8.66 7.72 8.49 8.48 9.49 7.57 8.14 9.16 8.19 8.00 8.92 7.02
I I D D D I D I I I D D D D D I I I I D D D I D I I I I D D D I D D I I D I I I D D D D D D I
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Table 1. (Contd.) GenBank accession number M68516 M68519 U07563 U07563 U07563 U07563 U72965 U92283 X03833 X03833 X03833 X87344 X87344 X87344 X87344 Y07848 Y07848 Y07848 Y07848 Y07848
MIR consensus coordinates 13 20 100 174 23 161 67 34 66 33 39 69 90 31 62 114 80 73 27 93
132 140 217 248 160 253 168 93 154 135 142 237 253 145 149 195 123 120 124 205
MIR coordinates in GenBank 3075 680 42,018 61,644 51,564 41,946 279 2838 10,895 8292 5281 164,894 191,639 102,713 98,354 14,240 55,043 67,311 66,097 13,559
Significance
Orientation
7.37 7.52 7.15 7.54 7.06 7.08 9.66 7.57 7.50 8.59 9.89 10.70 8.08 7.26 7.94 7.09 7.03 7.69 8.01 7.42
I I D I I I I I D I I D I I I D D D I I
3184 813 42,139 61,719 51,693 41,946 381 2898 10,984 8390 5381 165,047 191,793 102,827 98,439 14,317 55,084 67,358 66,193 13,671
Table 2. Unknown human MIRs revealed in coding untranslated regions of nucleotide sequences from GenBank-116 (asterisked) and in noncoding regions of the sample of 254 sequences (see text). A list of new MIRs has been split into Table 1 and Table 2 to compare the efficiencies of our program and CENSOR [22] GenBank accession number AB018563* AB020851* AF077754* AF157816 AF157816* AF157816* D31646* M55683* M69135* AF130343 AF130343 AF130343 AF157814 AF157814 AF157814 AL008723 L42239
MIR consensus coordinates 67 86 48 84 105 77 6 92 49 22 80 13 58 108 110 32 119
191 256 187 142 138 143 142 230 140 187 191 91 183 143 142 135 190
MIR coordinates in GenBank 660 560 823 588 3858 4052 1158 1595 622 222,303 173,811 169,455 4513 6003 1906 3281 841
their influence on the host genome. Unlike the Alu elements, whose role in the genome has been well studied [15, 16], very little is known about the conse-
Significance
Orientation
8.95 8.84 9.17 7.27 7.08 9.11 7.43 7.95 7.90 7.25 7.81 7.08 7.01 7.11 7.49 7.73 8.28
I D I D D I I I I I I I D D I I D
779 737 954 642 3891 4117 1279 1727 712 222,477 173,920 169,535 4632 6038 1937 3379 910
quences of the MIR insertion. A few reports about the sites of alternative splicing and the polyadenylation signals arising with the MIR insertion yet allow no MOLECULAR BIOLOGY
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conclusions about the general character of such cases [17]. Although the prevalence of MIRs in the transcribed DNA regions may be a result of their use, together with the Alu elements, for suppressing the translation inhibition in response to cell stress [2]. An interesting hypothesis has been suggested recently about a role of the MIR conserved sequences revealed in orthologous gene loci [18]. When occurring in the 5' and 3' untranslated regions (UTRs), MIRs may be involved in the fine mechanism regulating the life time of the mRNA transcript. The heteroduplexes corresponding to the sense and antisense MIR transcripts appear to be the structures recognized by proteins specific to double-stranded RNA, which destabilize mRNA [19]. Recently, SINEs were used as unique characters to infer the phylogeny of the present organisms [20]. Since MIRs are highly diverged, they are frequently identified as characteristic repeats unique for a given species, being indeed members of a family common for all vertebrates, and so may mislead one about the evolutionary divergence of species groups [21]. The possible mistakes could be easily avoided by the use of computer analysis allowing identification of even very ancient diverged MIR copies. Revealing both relatively new and very old MIR copies would build the most complete evolutionary picture of this interesting but still insufficiently studied repeat family. The occurrence of repeats in nucleotide sequences, including MIRs, may be tested by the CENSOR program [22] (http://www.girinst.org). A list of repeats revealed by this program among the nucleotide sequences of primates from GenBank-112 is available at http://charon.girinst.org/server/arc. An original program for repeat search has been recently developed by our group by combining the use of the weighted position matrix and a method of dynamic programming to achieve the optimal alignment [14]. The program allows the search for highly diverged MIR copies containing insertions and deletions. Results have been obtained corroborating a common ancestor repeat family in fishes, birds, and mammals, mentioned above as the CORE-SINE family [6, 13]. In the present work, a search for MIRs in the coding regions of human genome from GenBank-116 has been done by the program developed by us. MIRs have been determined in coding regions of 254 nucleotide sequences (see GenBank accession numbers in Appendix). For this sample, all newly revealed MIR copies have been described both for translated and untranslated gene regions, as well as for noncoding DNA regions. RESULTS AND DISCUSSION A search for MIRs in the sample of nucleotide sequences from the human genome (see appendix) by MOLECULAR BIOLOGY
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Table 3. Summarized data about the structural composition of MIRs listed in Tables 1 and 2. The structural composition has been determined in accordance with the MIR consensus coordinates. The subdivision into structural parts corresponds to [6]; parts of less than 10 bp were not taken into account MIR structural composition
MIR copy number
Noncoding genomic regions tRNA-like region 4 tRNA-like region + core 20 tRNA-like region + core + variable 9 region core 9 core + variable region 11 variable region 3 Total: 56 Untranslated coding gene regions tRNA-like region 2 tRNA-like region + core 6 tRNA-like region + core + variable 3 region core 7 core + variable region 8 variable region 2 Total: 28 Summarized data for noncoding and untranslated genomic regions tRNA-like region 6 tRNA-like region + core 26 tRNA-like region + core + variable 12 region core 17 core + variable region 18 variable region 5 Total: 84
the new program [14] revealed the MIR sequences unknown before (Tables 1–4). The comparison of the search results with those obtained by the CENSOR program with nucleotide sequences of primates from GenBank-112 (http://charon.girinst.org/server/arc) demonstrated that only three MIRs revealed by CENSOR were missed by our program, while 67 MIR copies were found additionally (Table 1). In general, analysis of the sample of 254 nucleotide sequences of human genome from GenBank-116 (see Appendix) revealed 101 MIR sequences unknown before (Tables 1, 2, 4). The numbers mentioned above testify to the more efficient MIR identification due to the original search algorithm developed by us [14]. The CENSOR pro-
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Table 4. MIRs in translated gene regions. The translation phase indicates the shift of the beginning and the end of the revealed MIR fragment relative the gene reading frame GenBank accession number AB002315 AB0050381 AB0059891 AB007921* AF017109 AF020192* AF039196 AF0812492 AF0812502 AF161702* AL050256 L192673 S76476* U00115* U63127* U729673* U793023 X034734 Z976304 Z21943*
MIR consensus coordinates 24 11 11 21 22 11 2 10 10 21 206 65 84 14 1 60 37 28 28 14
64 42 42 80 71 42 66 45 45 65 251 139 142 70 96 149 132 59 59 70
MIR coordinates in GenBank 2586 1179 1058 116 1544 1070 2559 1189 917 867 475 1540 1675 2147 1147 690 779 739 13,782 1904
2627 1208 1088 174 1589 1099 2620 1222 951 909 520 1614 1732 2198 1238 779 872 770 13,813 1955
Significance
Orientation
Translation phase
7.04 7.03 7.03 8.18 7.18 7.03 8.49 7.22 7.22 7.26 7.62 10.39 8.54 7.29 8.56 11.33 10.81 7.12 7.12 7.29
I I I D I I I I I I D I I I D D I I I I
2–2 1–2 1–2 1–0 1–0 1–1 0–2 1–0 1–0 2–0 1–2 0–0 0–1 1–0 0–2 0–0 1–2 2–1 2–1 1–2
Sequences similar to 25-hydroxyvitamin D3 1α-hydroxylase gene. Sequences similar to genes for the short and long isoforms of protein MRVI1. 3 Sequences are also deposited in Repbase (http://charon.girinst.org/server/arc) with the following coordinates: L19267: MIR consensus: 65–39, GenBank: 1540–1614; U72967: MIR consensus: 81–149, GenBank: 711–779; U79302: MIR consensus: 37–128, GenBank: 783–873. 4 Sequences similar to histone H1(0) gene. * Known proteins whose translation has been experimentally proved. 1 2
gram [22] is based on homologous alignment of an analyzed sequence with an original query sequence, in particular, with the consensus sequence for a repeat family. Our program combines the dynamic alignment with the use of the position-specific matrix preliminarily deduced for MIRs. The weight of each base in a certain position of the presumed MIR sequence is computed from a large sample of known MIRs, which is especially essential taking into account the considerable divergence of MIR copies. As a result, the search power of the program has been substantially increased. The MIR copies located in translated gene regions are the least studied part of the family. Although MIRs were found in different human genes before, of the 13 MIRs revealed in exons only one MIR copy was located in a translated gene part [23]. The occurrence of MIRs in nontranslated gene regions has been discussed very recently [18]. The conservatism of MIRs
and of their flanking regions has been noticed in orthologous gene loci. It is possible that some MIR insertions into genes were fixed by natural selection and are used for regulation of the RNA transcript life time. The cases when MIRs were determined in translated gene regions have not really been analyzed until now. Table 3 contains data about the structure of new MIRs found by us in noncoding regions of the sample of 254 human sequences and in untranslated coding gene regions from GenBank, which were obtained by comparison of the revealed repeats with the MIR consensus (see Tables 1, 2). The occurrence of the MIR core flanked by highly truncated (more than by half) fragments of the tRNA-like and variable parts prevails for the untranslated coding regions, while the structure comprising the tRNA-like part and the core is characteristic for the noncoding regions. MOLECULAR BIOLOGY
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Box A
Box B
Alignment (according to the consensus) of the MIR sequences revealed in translated gene regions. Two consensus sequences are shown: the upper one from Repbase (http://www.girinst.org), the lower one inferred from the position weight matrix and used in this work to search for new MIRs. The consensus sequences differ in 16 positions, half of which are transitions. The inserted nucleotides are in bold. MIRs appear in the order of their GenBank accession numbers. The MIR coordinates are in Table 4. I and D designate the complementary inverted and direct MIR copies, respectively. The inverted MIR copies are shown in the form of their direct counterparts. For the MIR sequence with an accession number U72967, only a part in the translated gene region is indicated. Boxes A and B of the split promoter for RNA polymerase III are enclosed in rectangles with the consensus sequences shown above. A filled bar marks the central part, the core; hatched bars indicate the tRNA-like part and the LINE-like variable region. The MIR structural composition is the same as in [6].
The translated MIR copies, most of which were new-found, have been considered by us separately. Table 4 contains data about the GenBank sequences where the translated MIR copies were found; three of them were known earlier (L19267, U72967, and U79302). The translated MIR copies correspond to 17 proteins, 10 of which were predicted only theoretically. The figure shows the alignment of MIRs found in translated gene regions; the sequences appear in the same order as in Table 4. Obviously, the tRNA-like MIR parts are observed in most cases, the core fragments occur only in 4 out of 17 MIR copies, and in one case, a MIR copy is represented by a fragment of the 3'-terminal variable region originating from the 3' end of L2 (LINE2) repeat [6]. MOLECULAR BIOLOGY
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Unfortunately, we have no definite answer to the question whether the revealed sequences are fragments of MIRs or ancient copies of tRNA genes. However, as an argument in favor of MIRs, it is possible to presume why mainly the tRNA-like part of the inserted MIR copy was conserved during the evolution of a translated gene region. Table 3 summarizes the data about the structural composition of the MIRs listed in Tables 1 and 2. The most frequently occurring MIR structure consists of the tRNA-like region and the core that is the most conserved part of human MIRs [13]. Such a structure appears to possess the greatest potential for transposition. The tRNA-like part bearing the RNA polymerase III promoter assisted the efficient transcription of the DNA frag-
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Figure. (Contd.)
ment of about 150 bp in length. The core function is probably to facilitate the exchange with the 3' ends of the actively retroposed LINEs [13]. The core is capable of binding with a ribonucleoprotein particle containing reverse transcriptase, which recognizes the actively retroposed LINE in the same manner [24, 25]. Moreover, during reverse transcription, the LINE RNA region containing the binding site for reverse transcriptase could join with the core 3' end, resulting in a new retroposon family [13]. Being inserted into the translated gene region, the MIR core could have given rise to interactions with various ribonucleoproteins unfavorable for translation and, therefore, underwent considerable divergence. The 3' ends of MIRs in translated gene regions also underwent the same
strong divergence since they contained the reverse transcriptase binding sites [4, 5]. This may explain why MIRs in translated gene regions rarely contain the cores or the 3'-terminal variable regions (see figure). As to the tRNA-like parts of MIRs in translated regions, the A and B boxes of the split promoter are clearly unfit to be recognized by RNA polymerase III because of their strong divergence and nucleotide deletions. The nucleotide sequences located between the boxes are quite conserved, probably, since their transcripts lack any active role. We also made an attempt to find a regularity in how the revealed MIR copies fit a translation frame, by considering the so-called translation phases of the MOLECULAR BIOLOGY
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EVOLUTION OF MIRs APPENDIX. GenBank accession numbers of the human genome sequences containing MIRs in coding gene regions. AB000462 AB002315 AB002455 AB002456 AB002457 AB002458 AB002459 AB002460 AB002461 AB002462 AB005038 AB005989 AB007921 AB010813 AB010814 AB010815 AB010816 AB010817 AB010818 AB010819 AB010820 AB010821 AB010822 AB012922 AB015201 AB015202 AB018255 AB018563 AB020337 AB020812 AB020813 AB020814 AB020815 AB020816 AB020817 AB020818 AB020819 AB020820 AB020821 AB020822 AB020823 AB020824 AB020825 AB020826 AB020827 AB020828 AB020829 AB020830 AB020831 AB020832 AB020833 AB020834 AB020835
AB020836 AB020837 AB020838 AB020839 AB020840 AB020841 AB020842 AB020843 AB020844 AB020845 AB020846 AB020847 AB020848 AB020849 AB020850 AB020851 AB025272 AB025273 AB025274 AF014958 AF017109 AF020192 AF023674 AF025999 AF026001 AF039196 AF050154 AF055575 AF069489 AF077754 AF081249 AF081250 AF083105 AF118141 AF127916 AF130343 AF157810 AF157811 AF157812 AF157813 AF157814 AF157815 AF157816 AF161702 AJ002305 AJ004799 AJ006835 AJ011600 AJ011601 AJ011602 AL008723 AL021808 AL050256
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D31641 D31642 D31643 D31644 D31645 D31646 D43967 D61690 D61691 D61692 D61693 D61694 D61695 D63710 D83402 L04193 L13748 L13749 L13750 L13751 L13752 L13753 L13754 L13755 L13756 L19267 L21756 L35930 L39874 L42237 L42238 L42239 L42240 L42241 L42242 L42243 L42323 M12523 M14752 M22897 M22898 M27318 M33208 M33209 M33210 M37815 M55683 M68516 M68519 M69130 M69131 M69132 M69133 Vol. 35
M69134 M69135 M86360 S76476 S81601 U00115 U02632 U07563 U09384 U09937 U11058 U11717 U13913 U14176 U14179 U23767 U28963 U29901 U29902 U29903 U29904 U29905 U29906 U29907 U29908 U29909 U29910 U29911 U29912 U29913 U29914 U29915 U29916 U29917 U29918 U29919 U29920 U29921 U29922 U29923 U29924 U29925 U29926 U29927 U29928 U29929 U29930 U29931 U29932 U31201 U63127 U65416 U67092 No. 6
U68159 U68160 U68161 U68162 U70065 U72959 U72961 U72962 U72963 U72964 U72965 U72966 U72967 U72968 U72969 U79121 U79302 U82972 U92283 U92316 U92317 U94788 U97500 U97501 U97502 X03473 X03833 X05850 X15377 X16416 X54156 X57025 X60152 X77738 X85116 X85117 X87344 Y07848 Y09764 Z21943 Z67743 Z97630
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beginning and the end of the revealed MIRs (see Table 4). The translation phase of the MIR beginning shows the shift of the first MIR coordinate relative to the codon nucleotides in the translation frame. Digits 0, 1, and 2 designate that the beginning of the revealed MIR fragment coincides with the codon beginning or is shifted by one or two nucleotides, respectively, to the right. For the translation phase of the MIR end, digits 0, 1, and 2 indicate that the MIR end coincides with the third, first, or second codon nucleotides, respectively. The phases for the beginning and the end of MIR translation are hyphenated to each other in the last column of Table 4. As follows from these data, the insertion of MIRs into translated gene regions had no preferable position relative the reading frame and occurred randomly. The present work demonstrates the substantially more efficient method of searching for repeated sequences in a genome [14]. For the sample of 254 sequences from GenBank-116, 56 new MIR copies have been revealed in noncoding regions of human genome and 45 new MIRs, in coding regions. The patterns of evolutionary divergence of MIRs differ for untranslated and translated exon regions. The central part of MIR, the core, is mainly conserved in untranslated regions, while the translated MIR copies have undergone directed divergence of the cores and the 3'terminal variable domains in order to suppress their possible ribonucleoprotein-binding activity. The most conserved MIR region is the 5'-terminal tRNA-like part, whose split promoter for RNA polymerase III also underwent directed divergence, probably, to suppress undesired transcription. REFERENCES 1. Jurka, J., Curr. Opin. Struct. Biol., 1998, vol. 8, pp. 333– 337. 2. Smit, A.F.A., Curr. Opin. Genet. Dev., 1999, vol. 9, pp. 657–663. 3. Smit, A.F.A., Curr. Opin. Genet. Dev., 1996, vol. 6, pp. 743–748. 4. Ohshima, K., Hamada, M., Terai, Y., and Okada, N., Mol. Cell. Biol., 1996, vol. 16, pp. 3756–3764. 5. Okada, N. and Hamada, M., J. Mol. Evol., 1997, vol. 44 (suppl. 1), pp. S52–S56. 6. Gilbert, N. and Labuda, D., Proc. Natl. Acad. Sci. USA, 1999, vol. 96, pp. 2869–2874. 7. Donehower, L.A., Slagle, B.L., Wilde, M., Darlington, G., and Butel, J.S., Nucleic Acids Res., 1989, vol. 17, pp. 699–710. 8. Bancroft, J.D., Schaefer, L.A., and Degen, S.J.F., Gene, 1990, vol. 95, pp. 253–260. 9. Korotkov, E.V., Mol. Biol., 1991, vol. 25, pp. 250–263. 10. Smit, A.F.A. and Riggs, A.D., Nucleic Acids Res., 1995, vol. 23, pp. 98–102. 11. Jurka, J., Zietkiewicz, E., and Labuda, D., Nucleic Acids Res., 1995, vol. 23, pp. 170–175.
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12. Korotkov, E.V., Izv. Akad. Nauk, Ser. Biol., 1992, no. 4, pp. 660–672. 13. Gilbert, N. and Labuda, D., J. Mol. Biol., 2000, vol. 298, pp. 365–377. 14. Korotkov, E.V., Korotkova, M.A., and Rudenko, V.M., Mol. Biol., 2000, vol. 34, pp. 553–559. 15. Britten, R.J., Proc. Natl. Acad. Sci. USA, 1996, vol. 93, pp. 9374–9377. 16. Molecular intelligence unit in the impact of short interspersed elements (SINEs) on the host genome, Maraia, R.J., Ed., Springer–Verlag, 1995. 17. Murnane, J.P. and Morales, J.F., Nucleic Acids Res., 1995, vol. 23, pp. 2837–2839. 18. Hughes, D.C., Trends Genet., 2000, vol. 16, pp. 60–62.
19. Lipman, D., Nucleic Acids Res., 1997, vol. 25, pp. 3580– 3583. 20. Miyamoto, M., Curr. Biol., 1999, vol. 9, pp. R816– R819. 21. Buchanan, F., Crawford, A., Strobeck, C., Plasboll, P., and Plante, Y., Animal Genet., 1999, vol. 30, pp. 47–50. 22. Jurka, J., Klonowski, P., Dagman, V., and Pelton, P., Comp. Chem., 1996, vol. 20, pp. 119–122. 23. Tulko, J.S., Korotkov, E.V., and Phoenix, D.A., DNA Seq., 1997, vol. 8, pp. 31–38. 24. Deragon, J.M., Sinnet, D., and Labuda, D., EMBO J., 1990, vol. 9, pp. 3363–3368. 25. Sinett, D., Richer, C., Deragon, J.M., and Labuda, D., J. Mol. Biol., 1992, vol. 226, pp. 689–706.
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