Unité de Génétique Moléculaire Animale, UMR1061 (Institut National de la Recherche Agronomique/Université de Limoges), Institut des Sciences de la Vie et de la Santé, Faculté des Sciences Limoges, Limoges, France;
Laboratoire de Génétique Biochimique et de Cytogénétique, UR339, Institut National de la Recherche Agronomique, Jouy-en-Josas, France;
Glycobiologie Institut National de la Santé et de la Recherche Médicale U504, Université Paris Sud XI, Villejuif, France
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Abstract |
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Introduction |
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We have previously shown that the present mammalian 6- and
3/4-fucosyltransferase genes might have been shaped owing to different molecular mechanisms, including exon shuffling (Javaud et al. 2000
), exonintron conversion, duplication (Wierinckx et al. 1999
), and point mutations (Dupuy et al. 1999
). A split exonintron structure is observed only for the coding sequence of the
6-fucosyltransferase gene family (FUT8), which is thought to be representative of the ancestor of the present fucosyltransferase genes (Oriol et al. 1999b). In contrast, the coding sequences of the other known fucosyltransferase gene families are monoexonic (Costache et al. 1997a, 1997b
), suggesting their possible emergence via a retrotransposition mechanism involving mature mRNAs. Indeed, by comparing the complete structure of bovine futb gene with those of its three human homologous FUT3, FUT5, and FUT6 counterparts (Oulmouden et al. 1997
; Wierinckx et al. 1999
), we identified inside the bovine gene an antisense reverse transcriptaselike sequence that we have proposed might be an indication of an ancient retrotransposition event.
To examine whether retrotransposition could mediate the fucosyltransferase gene's emergence in mammals, we established the genomic structures of bovine 2-fucosyltransferase genes and compared them with their human counterparts. The coding sequences of the three bovine
2-fucosyltransferase genes (bfut1, bfut2, and sec1) are fully active (Barreaud et al. 2000)
, as in rodents (Hitoshi et al. 1995, 1996
) and New World primates, while in humans, chimpanzees, and gorillas, only FUT1 (H) and FUT2 (Se) are fully expressed, and Sec1 is a pseudogene (Kelly et al. 1995
; Apoil et al. 2000
).
Here, we show that in mammals, a complex nonautonomous L1-retrotransposition event occurred within the locus of the 2-fucosyltransferase ancestor gene itself. Base mutations inducing premature stop codons in the Sec1 pseudogene (Apoil et al. 2000
) occurred secondarily in Catarrhini.
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Materials and Methods |
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Materials
The oligonucleotides used in this study are listed in table 1 . Before sequencing, all polymerase chain reaction (PCR) products were cloned into the pGEM-T Easy vector (Promega, Madison, Wis.). Bovine brain, heart, kidney, lung, and spleen mRNAs were obtained from CLONTECH (Palo Alto, Calif.). Intestine RNAs were prepared using TRIZOL Reagent (LifeTechnologies, Grand Island, N.Y.) according to the manufacturer's protocols.
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Rapid Amplification of 5' and 3' cDNA Ends (RACE)
The Marathon cDNA Amplification kit (CLONTECH) was used to obtain a library of adapter-ligated double-stranded cDNA from bovine brain, heart, intestine, kidney, lung, and spleen tissues. Poly(A)+ RNA (1 µg) was used as initial template. The 5' and 3' ends were amplified according to the protocol previously described by Barreaud et al. (2000)
using 2.5 µl of each library as a template. The sense oligonucleotides (AP1 and nested AP2) and the antisense oligonucleotides (RA1 and nested RA2, RA3 and nested RA4, RA5 and nested RA6) (table 1
) were used for 5'-end amplification of bfut1, bfut2, and sec1, respectively. For 3' ends, the antisense nucleotides were AP1 and AP2, and the sense nucleotides were FA1 and nested FA2 for bfut1 and FA3 and nested FA4 (table 1
) for bfut2 and sec1.
Final PCR products were analyzed on a 1.5% agarose gel, and then RACE fragments were gel-extracted (QIAquick, Qiagen), cloned into pGEM-T, and sequenced using T7 and pUCM13rev sequencing primers.
High-Density Membrane and BAC Library Screening
A 762-nt probe (Barreaud et al. 2000
) corresponding to a large part of the bfut2 catalytic domain was used to sample the high-density membranes. Probe (25 µg) was labeled with [
-32P]dCTP using the Multiprime DNA Labeling Systems Kit (Amersham) and purified to avoid unincorporated isotopes (QIAquick Nucleotide Removal Kit, Qiagen, Hilden, Germany) at a specific activity of 109 cpm/µg.
Prehybridization was performed for 4 h at 42°C in a buffer containing 200 mM Na2PO4, 1 mM EDTA, 15 % (v/v) deionized formamide, 7% (w/v) SDS, 1% (w/v) BSA, and 0.2 mg/ml salmon sperm. After elimination of the prehybridization buffer, hybridization was performed at 42°C for at least 12 h in the same buffer but the salmon sperm replaced by the labeled probe. Membranes were washed twice for 25 min in 0.2 x SSC at 60°C and then subjected to autoradiography. Positive clones corresponding to a specific address of the organized BAC library were ordered to RZPD. DNA was prepared using the Nucleobond AX 100 Kit (Macherey-Nagel, Dürel, Germany) according to the manufacturer's protocol.
To characterize fucosyltransferase genes present in each BAC, PCR was done using different discriminating primer pairs: F1/R1, F2/R2, or F3/R3 for bfut1; F4/R4, F4/R5, or F5/R5 for bfut2; and F5/R5 or F6/R6 for sec1. The 10-µl reaction mixture contained 125 µM of each dNTP, 1.25 mM MgCl2, 0.5 U Taq DNA polymerase (Promega), 10 pmol of each primer, and 5 ng DNA. After 5 min at 94°C, 35 cycles were executed (30 s at 94°C, 30 s at annealing temperature [58°C for F2/R2, 60°C for F3/R3, 62°C for F5/R5, and 65°C for the other primer pairs], and 20 s at 72°C), followed by a final extension step of 5 min. The same primer pairs and PCR conditions were used to isolate a BAC from the LGBC library.
BAC Size Determination by Pulsed-Field Electrophoresis
Reaction mixture (20 µl) containing 500 ng DNA was digested by 5 U of NotI enzyme for 2 h and subsequently run on pulsed-field gel (22 h run time, switch time 315 s, 6 V/cm, 14°C, 1% agarose in 0.5 x TBE buffer). The BAC size estimation was determined using long-range and middle-range DNA molecular weight markers (Boehringer Mannheim).
Long-Range PCR
Gene fragments were amplified using the Expand Long Template PCR System (Boehringer Mannheim). The 50-µl reaction mixture contained 15 pmol of each primer, 2.6 U of DNA polymerase, 25 nmol of each dNTP, 50 ng of DNA, and 2.25 mM MgCl2. Amplifications were performed using the following cycling parameters: one cycle of denaturation at 94°C for 2 min, followed by 35 cycles of 30 s at 94°C, 30 s at 65°C, and 20 min at 68°C. The final polymerization step was extended to 7 min at 68°C.
DNA Sequence Analysis
Sequencing of cloned inserts was achieved using T7 and pUCM13rev (pEasy T-vector) sequencing primers, a dye terminal labeling chemistry kit (PRISM Ready Reaction Ampli Taq FS), and the ABI PRISM 310 Genetic Analyzer (Perkin Elmer, Norwalk, Colo.).
Sequencing of BAC extremities was performed according to the protocol described by Schibler et al. (1998)
using elongated SP6L and T7L primers for BAC isolated at LGBC (table 1
) or classic SP6 and T7 primers for BACs provided by RZPD, and 2.5 µg DNA. BAC3 extremity sequences were used to determine primer pairs (table 1
) to establish the BAC contig.
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Results |
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For sec1, two alternative 5' untranslated exons, Ea (290 bp) and Eb (213 bp), were found by PCR (AP2 and RA6 primers; table 1 ) in kidney (sec1; fig. 1 ). Only one PCR product (FA4 and AP2 primers; table 1 ) was obtained (432 bp) at the 3' end of sec1. A putative polyadenylation site (AAAAA) was identified. Altogether, these data show that the bovine sec1 was expressed as two transcripts differing only in their 5' UT regions. Transcript 1 (1,855 bp) and transcript 2 (1,779 bp) of sec1 corresponded to the alternative use of Ea or Eb, respectively.
Organization of the 2-Fucosyltransferase Gene Cluster
Several BACs from the RZPD library have been isolated with the specific bfut2 probe, synthesized as previously described (Barreaud et al. 2000
). To identify each
2-fucosyltransferase gene, specific primer pairs were designed (table 1
). They were also employed to screen the LGBC library from which we isolated the BAC 704F11 (BAC1; about 90 kb), which contained a cluster of the three
2-fucosyltransferase genes, as in humans (Reguigne-Arnould et al. 1995
). Moreover, in this BAC, we also found two other genes: CA11 and DBP. In the human species, CA11 appears to be located inside the
2-fucosyltransferase gene cluster, and DBP has been located in the same chromosome band, 19q13.3 (Lovejoy et al. 1998
). Lovejoy et al. (1998)
have shown that CA11 and Sec1 transcripts are in opposite orientations, suggesting an overlap between these genes and the following order: DBP, CA11, and Sec1.
The relative position of bfut1 was determined using sequence extremities of BAC3 that contain bfut2 and sec1. Finally, the analysis of the region including DBP, CA11, and Sec1 allowed us to determine the DBP, CA11, sec1, bfut2, and bfut1 order in the resulting bovine contig (fig. 2 ).
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Comparative Organization of Human and Bovine 2-Fucosyltransferase Genes
A BLAST search revealed evidence of homologies between the bovine sec1 sequence and several fragments of the human BAC AC008888 (fig. 3
). The human Sec1 pseudogene sequence published by Lowe and co-workers (Kelly et al. 1995
) matches with 99% identity along the BAC sequence with no gaps. In contrast, the bovine sec1 coding exon c was partitioned into three fragments of 102 bp (80% of identity), 1,031 bp (84% of identity), and 76 bp (73% of identity), respectively (fig. 3
). Moreover, high identity (84%) was observed between the human Sec1 sequence and the 1,010-bp fragment of bovine exon c. The untranslated bovine exons a and b match the human BAC sequence with 82% identity on 211 bp and 90% identity on 138 bp, respectively. Surprisingly, the order of bovine homologous exons on the corresponding human BAC sequences was a, c, b.
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When the described mutations in the human Sec1 pseudogene (Apoil et al. 2000
) are abolished, the existence of a putative TAG stop codon (nucleotide 1100) can be depicted, and a polyadenylated sequence (17 A) is observed about 800 bp downstream. Moreover, several short interspersed nucleotide elements (SINEs; Alu-type elements) can be identified at each of 5' and 3' ends (fig. 3 ).
The other 2-fucosyltransferase genes (FUT1 and FUT2) have been assigned to human BACs AC024740 and AC008888, respectively. As for the Sec1 pseudogene, polyadenylated sequences were identified at their 3' ends. Alu-like elements are also found in the 5' and 3' regions of these two genes. Unlike Sec1, bovine and human FUT1 and FUT2 coding sequences thoroughly match the human BAC genomic sequences.
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Discussion |
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In humans, gorillas, and chimpanzees, a pseudogene (Sec1) has also been cloned (Kelly et al. 1995
; Rouquier et al. 1995
; Apoil et al. 2000
), whereas in other mammals, such as rabbits (Hitoshi et al. 1995
) and bovines (Barreaud et al. 2000
), sec1 encodes a functional product. We show that in bovines, the three
2-fucosyltransferase genes have similar genomic DNA organizations characterized by a monoexonic coding sequence and various 5' UT exons (fig. 1
). The three bovine enzymes transfer fucose in
1
2 linkage to the terminal galactose (Barreaud et al. 2000
). Although this species has retained three
2-fucosyltransferase functional genes and expresses H antigen in exocrine secretions, it does not possess the H antigen either on endothelial cells or on red cells.
Expression of histo-blood antigens varies according to vertebrate species (Watkins 1995
). In some tissues, such as mucosa, these antigens are observed from amphibians to higher mammals, whereas in vascular endothelial cells, H antigen is restricted to humans, apes, and Old World monkeys (Catarrhini). During evolution, erythrocytes are the most recent cells which have acquired the H antigen observed only in humans and some anthropoid primates (Oriol et al. 1992
). On red cells of New World monkeys (Platyrrhini), lower primates (prosimii), and other nonprimate mammals, the H antigen is replaced by the
Gal antigen. The
Gal epitopes are abundantly expressed in these mammals (Galili et al. 1988
; Oriol et al. 1999a) and are synthesized by the
3GalT geneencoded enzyme (Joziasse et al. 1989, 1992
; Henion et al. 1994
; Strahan et al. 1995
). The Gal glycotope constitutes a major barrier for the possible use of xenogenic organs in humans (Oriol, Koren, and Cooper 1993
). Surprisingly, humans presenting an H antigen on endothelium and erythrocyte membranes possess the Sec1 pseudogene (Apoil et al. 2000)
and two inactive
3GalT pseudogenes (Joziasse et al. 1991
).
With the aim of elucidating the switch between the Gal and the H antigens, we compared the
2-fucosyltransferase gene cluster organizations in the bovine and human species. The human Sec1 pseudogene presents several characteristics of a nonautonomous retrotransposon. It is associated with numerous Alu-type elements, possesses a polyA tail and, moreover, lacks protein-coding capacity. The mobilization of such a processed pseudogene requires a cellular source of reverse transcriptase that is most likely encoded by retrotransposition-competent long interspersed nuclear elements, such as LINEs or L1 (Kazazian and Moran 1998
). In this way, it is thought that proteins that are derived from retrotransposition-competent L1 act on Alu and cellular mRNA to induce their retrotransposition (Mathias et al. 1991
), probably by a target-primed reverse transcription mediated by an enzyme which also possesses an endonuclease activity (Jurka 1997
). Interestingly, retrotransposition events of ancestral Sec1 mRNA might have occurred at the locus of the ancestor of the Sec1 gene. Indeed, comparative studies of bovine and human Sec1 loci (fig. 3
) show that the ancestral gene depicted at the retrotransposition site has conserved a coding sequence split in several exons.
The Sec1-like family presents higher evolutionary rates than the FUT2-like family due to accumulation of mutations in the Sec1 pseudogene such as premature stop codons (Apoil et al. 2000
). Such mutations are also observed in some Old World monkeys, but until now no Sec1 transcript has been found in these species or in healthy human tissues. Described as responsible for pseudogene appearance, these mutations alone do not explain the absence of transcription. We hypothesize that a DNA rearrangement at the Sec1 locus occurred during and/or after the retrotransposition event in humans. However, in human ovarian cancer cells, two distinct Sec1 transcripts (EST D87946 and D87947) were found (Koda et al. 1997
). They reveal how the ancestral Sec1 gene was split in several coding exons (fig. 3
), as we have previously seen for the
6-fucosyltransferase genes (Oriol et al. 1999b; Javaud et al. 2000
). They also support a putative rearrangement at the Sec1 locus based on the shift of a DNA fragment including a 71-bp ancestral exon. As a consequence, we found that the orientations of the human 71-bp fragment and bovine exon b are opposite. Today, it is difficult to determine if the inactivating mutations or the rearrangement of the Sec1 gene was the first event that occurred. Nevertheless, the occurrence of a previous gene-inactivating rearrangement is known to have facilitated the implantation of subsequent mutations.
In human ovarian cancer cells, we postulate that Sec1 transcription is likely due to a new translocation event surrounding the 71-bp fragment. It could restore a primitive gene organization, including a promoter region compatible with the transcription.
A model for 2-fucosyltransferase gene cluster evolution and Sec1 inactivation is proposed (fig. 4
). Comparative analyses of bfut1 and bfut2 coding sequences with their human genomic counterparts do not show any intron. This suggests that bovine and human genes both result from retrotransposition events of mature mRNA products. We show that bovine and human Sec1 genes were shaped by the same mechanism of L1-reduced retrotransposition of exons. Moreover, in humans, we also show that a subsequent shuffling sequence of the putative promoter region (fig. 4
) might have led to the inactivation of Sec1 gene expression, a datum consistent with the fact that until now no Sec1 transcript had been depicted in normal human tissues.
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The two human genes and the pseudogene are located within a 100-kb region on chromosome 19q13.3 (Reguigne-Arnould et al. 1995
; Rouquier et al. 1995
). Also, the three bovine genes are organized in a cluster within a 60-kb region on the bovine chromosome 18q24 (data not shown). Phylogeny and gene cluster organization favor the hypothesis that they originated from duplication events of retrotransposed Sec1 mRNA. Due to the high identity between Sec1 and FUT2 sequences, we postulate that the duplication event at the origin of FUT2 and Sec1 genes occurred after the separation of the FUT1 gene from the common evolutionary trunk.
Recently, Joziasse and Oriol (1999)
proposed an evolution model for the
3GalT family in Catarrhini. Duplication of the ancestral gene and subsequent divergent evolution led to the ABO blood group genes and the
3GalT gene (Saitou and Yamamoto 1997
). Later,
3GalT was inactivated by multiple mutations, leading to the HGT-10 pseudogene located in the HSA9 (Larsen et al. 1990b
). Unlike the Sec1 retrotransposition which occurred at the same HSA19 locus (this paper), a second processed pseudogene, HGT-2, resulting from HGT-10 mRNA reverse transcription, was inserted on HSA12.
Interestingly, in Catarrhini, Sec1 and 3GalT genes, whose products act on the same terminal galactose, have been inactivated in parallel. Nevertheless, it is premature to conclude that their inactivation promoted the emergence of ABO blood-group genes.
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Acknowledgements |
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Footnotes |
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1 Keywords: 2-Fucosyltransferase
retrotransposition
pseudogene
gene cluster
Mammalian
2 Address for correspondence and reprints: Jean-Michel Petit, Unité de Génétique Moléculaire Animale, UMR1061 (Institut National de la Recherche Agronomique/Université de Limoges), Institut des Sciences de la Vie et de la Santé, Faculté des Sciences Limoges, 87060 Limoges Cedex, France. jean-michel.petit{at}unilim.fr
.
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