1 Department of Applied Biological Science, Faculty of Science and Technology, Tokyo University of Science, 2641 Yamazaki, Noda-shi, Chiba-ken 278-8510, Japan
2 Department of Pathological Biochemistry, Medical Research Institute, Tokyo Medical and Dental University, Chiyoda-ku, Tokyo 101-0062, Japan
Correspondence
Kengo Sakaguchi
kengo{at}rs.noda.tus.ac.jp
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ABSTRACT |
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The GenBank accession number for the sequence of CcLIG4 is AB098474.
Present address: Department of Food Science and Human Nutrition, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.
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INTRODUCTION |
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We shall consider roles of DNA ligase IV from a slightly different point of view. Yeasts lacking DNA ligase IV and LIF1, which share sequence identity with mammalian XRCC4, are viable but their sporulation efficiency is reduced (Herrmann et al., 1998; Schar et al., 1997
). DNA ligase IV may play a role in meiosis.
During meiotic prophase I, chromosomes begin to condense, and they show thin thread-like structures in leptotene. Homologue paring is initiated in leptotene, and continues in zygotene. Fully synapsed homologues are observed in pachytene as thick thread-like structures. During meiotic prophase I, several DNA metabolic processes are associated with meiotic recombination (Allers & Lichten, 2001a; Hunter & Kleckner, 2001
; Paques & Haber, 1999
; Villeneuve & Hillers, 2001
). Meiotic recombination in yeast starts from meiosis-specific DSBs with formation of single-stranded DNA by exonuclease digestion. The single-strand portion invades the region having homologous sequences in the other allele. After single-ended strand invasion and initial repair synthesis, crossover and non-crossover pathways diverge (Allers & Lichten, 2001b
). In both crossover and non-crossover pathways, repair-type DNA synthesis occurs with the action of DNA polymerase and ligation by DNA ligase (Paques & Haber, 1999
; Villeneuve & Hillers, 2001
). DNA ligase IV may be an important element in the coordinated multi-enzymic processes of meiotic DNA metabolism.
For the purpose of this study, we chose to investigate the meiocytes of a basidiomycete, Coprinus cinereus. C. cinereus has been used as a genetic tool for studying mating type and sexual development (Brown & Casselton, 2001; Casselton, 2002
; Casselton & Olesnicky, 1998
; Kamada, 2002
; Kues, 2000
) and is well suited for studies on meiosis because of its synchronous meiotic cell cycle in the fruiting cap (Li et al., 1999
; Nara et al., 1999
; Pukkila et al., 1984
; Raju & Lu, 1970
). In this study, we cloned the DNA ligase IV cDNA of C. cinereus and characterized the recombinant protein, and then investigated its expression during meiotic development in detail by Northern blotting analyses, and by in situ hybridization of C. cinereus meiotic tissues. Based on these observations, the possible role(s) of C. cinereus DNA ligase IV during meiosis are discussed.
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METHODS |
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cDNA cloning of C. cinereus DNA ligase IV.
In order to isolate cDNA clones of C. cinereus DNA ligase IV (CcLIG4), two primers were synthesized corresponding to the amino acid motifs conserved among species: sense primer (5'-TGGATCGAGGAGAAGATGGAYGGNGANMG-3') and antisense primer (5'-TCGAGGTACTCGGGCTTGAYYTTNADCCA-3') (N=A, C, G or T; Y=C or T, M=A or C; D=A, G or T). These primers were used for PCR of cDNA generated from total RNA isolated from meiotic tissues of C. cinereus. The PCR product was used to screen the C. cinereus ZAP II cDNA library as described previously (Nara et al., 1999
). The DDBJ/EMBL/GenBank accession number of the nucleotide sequence reported in this paper is AB098474 for CcLIG4.
Search for the three-dimensional structure of C. cinereus DNA ligase IV.
A modelled 3D structure for CcLIG4 was calculated by the KabschSander method and visualized using Insight II (Molecular Simulation) (Guex & Peitsch, 1997; Peitsch, 1996
; Peitsch et al., 1995
).
Bacterial expression and purification of CcLIG4.
The coding region of CcLIG4 (residues 11025) was expressed as thioredoxin-tagged fusion protein using pET32-a expression vector (Novagen) at NcoI and XhoI sites. Recombinant CcLIG4 thioredoxin-tagged (Trx) fusion protein (Trx-CcLIG4) was produced in Escherichia coli BL21 (DE3) (Novagen) by growing the E. coli in 100 ml 2xYT medium containing 50 µg ampicillin ml-1. The cells were grown to an OD600 of 0·6 at 37 °C, then IPTG was added to a final concentation of 1 mM. The cells were harvested after 20 h at 16 °C by centrifugation at 5000 r.p.m. for 10 min. The cell pellets were resuspended in 5 ml ice-cold binding buffer (20 mM Tris/HCl pH 7·9, 0·5 M NaCl, 5 mM imidazole, 0·1 % NP-40) and sonicated five times (20 kHz, 30 s). The supernatant was loaded on a Ni+-NTA column and eluted with 1 M imidazole in lysis buffer. The fraction containing Trx-CcLIG4 was dialysed against buffer A (50 mM Tris/HCl pH 7·5, 1 mM EDTA, 10 %, v/v, glycerol, 0·1 % NP-40) and used in a subsequent experiment.
Enzyme assays.
Assays of DNA ligase activity were performed as described previously (Matsuda et al., 1996; Teraoka et al., 1993
) with minor modifications. Adenylation was performed in a 20 µl reaction mixture containing 60 mM Tris/HCl (pH 7·8), 10 mM MgCl2, 5 mM DTT, 50 µg BSA ml-1 and 1 µCi [
-32P]ATP (3000 Ci mmol-1; 110 TBq mmol-1) and 2 µl of the ligase fraction. NaPPi treatment was carried out in the presence of 0·05 mM NaPPi in the reaction buffer. Reactions were incubated for 10 min at room temperature, and then terminated by the addition of SDS-PAGE sample buffer. Adenylated proteins were resolved by SDS-PAGE.
Nick-ligation reactions were performed using a (dT)16 substrate, which was 5'-end-labelled using T4 polynucleotide kinase and [-32P]ATP (6000 Ci mmol-1; 220 TBq mmol-1). The radiolabelled (dT)16 was hybridized with poly(dA) or poly(rA) (Amersham) as described previously (Tomkinson et al., 1991
). Ligation reactions were performed in a 10 µl volume containing 1 ng DNA substrate, 60 mM Tris/HCl (pH 7·8), 10 mM MgCl2, 5 mM DTT, 50 µg BSA ml-1 for 10 min at 37 °C, and then the mixture was rapidly chilled to 0 °C. The ligation products were separated on denaturing 20 % polyacrylamide 8 M urea gels. NaPPi treatment was performed in the presence of 0·5 mM NaPPi in the reaction buffer.
DSB ligation reactions were performed using a linearized pUC119 DNA with BamHI or SmaI as described previously (Matsuda et al., 1996).
Northern analysis.
RNA was prepared from C. cinereus using Trizol reagent (Invitrogen) according to the manufacturer's protocol. The RNA samples were separated on 1·2 % agarose-formaldehyde gels; 20 µg total RNA sample was loaded in each lane. The agarose gel was stained with ethidium bromide and blotted overnight in 20x SSPE to a Hybond-N+ membrane (Amersham). The membrane was fixed with alkali and carefully rinsed with 2x SSPE, and RNA was immobilized to the membrane and hybridized with 32P-labelled probe as described previously (Hamada et al., 2002).
Effect of MMS on vegetative mycelium.
For examination of CcLIG4 mRNA levels, 300 ml aliquots of liquid YMG medium were inoculated with small pieces of C. cinereus mycelium tissue. After 2 days of growth at 37 °C with shaking, the tissue was harvested onto filter paper by filtration through a Buchner funnel. Untreated samples (after 0 h MMS treatment) were immediately frozen in liquid N2 and the rest of the tissues were returned to 500 ml YMG medium containing 0·01 % MMS. Total RNA was isolated from vegetative dikaryotic mycelium after 06 h of MMS treatment and analysed by Northern hybridization as described above.
Preparation of riboprobes and in situ hybridization.
In situ hybridization of meiotic C. cinereus tissues was performed as described previously (Hamada et al., 2002). Riboprobes for in situ hybridization were labelled with digoxigenin-11-rUTP using a DIG RNA Labelling Kit (Boehringer Mannheim) according to the manufacturer's protocol. The riboprobes were made using the cDNAs corresponding to amino acids 1626 for CcLIG4 shown in Fig. 1
(A). The riboprobes were subjected to mild alkaline hydrolysis by heating at 60 °C for 53 min in 0·2 M carbonate/bicarbonate buffer and used at a concentration of 2 mg ml-1. The fruiting caps were fixed overnight at 4 °C with a mixture of 4 % (w/v) paraformaldehyde and 0·25 % (v/v) glutaraldehyde in 50 mM sodium phosphate buffer (pH 7·2). The fixed tissues were dehydrated in a series of xylene and ethanol and embedded in paraffin. The embedded tissues were sectioned at a thickness of 5 µm, and placed on microscope slides precoated with poly-L-lysine. The sections were deparaffinized with xylene and rehydrated through a graded ethanol series. They were subsequently pretreated with 10 mg proteinase K ml-1 in 100 mM Tris/HCl pH 7·5 and 50 mM EDTA at 37 °C for 30 min, dehydrated in a graded ethanol series, and dried under vacuum for 2 h. Hybridization and detection of the hybridized riboprobes were performed as described previously (Hamada et al., 2002
).
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RESULTS |
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The two carboxyl-terminal tandem BRCT domains, widely preserved in DNA ligase IV among eukaryotes, were also present in CcLIG4 (Fig. 1A). CcLIG4 had an inserted sequence, located between the tandem BRCT domains, which showed no sequence identity to the other eukaryotic counterparts of DNA ligase IV. The inserted sequence was composed of 95 amino acids from amino acid residues 810 to 904 (Fig. 1A
). Interestingly, the features of the inserted sequence in CcLIG4 were very similar to those of CcPCNA described previously (Hamada et al., 2002
). CcPCNA had an inserted sequence of 110 amino acids from amino acid residues 195 to 305 (Fig. 2
A). Although the inserted sequences of CcLIG4 and CcPCNA had no sequence identity, they shared some common features: the length (about 100 amino acids), the amino acid composition (rich in aspartic acid and glutamic acid), and the isoelectric point (about 4) (Fig. 2B
). The percentages of aspartic and glutamic acids in the inserted sequences of CcLIG4 and CcPCNA were 20·0 % and 19·0 %, and 21·4 % and 22·3 %, respectively. The inserted sequence of CcPCNA was rich in lysine (20·5 %), but that of CcLIG4 was not (5·3 %) (Fig. 2B
).
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Modelling of the three-dimensional structure of CcLIG4
The three-dimensional structure of the CcLIG4 catalytic core and that of two BRCT domains were obtained by computer analysis. The crystal 3D structure of the bacteriophage T7 DNA ligase catalytic core (Subramanya et al., 1996) and that of human DNA ligase III
BRCT domain (Krishnan et al., 2001
) have been reported. These enabled us to predict the 3D structures of CcLIG4 using the KabschSander method and Insight II (Molecular Simulation). Fig. 3
shows the computer-simulated possible structure of CcLIG4 catalytic core and that of two BRCT domains. The catalytic core (I258 to A584) and two BRCT domains (V667 to K759, A931 to E1021) were very similar to their eukaryotic counterparts. The inserted sequence of 810904 amino acid residues (DE-rich peptide site), which was present between two BRCT domains, must protrude beyond the tandem BRCT domains, although we could not simulate this because the other DNA ligase IVs have no such DE-rich peptide site. In humans, the region between the tandem BRCT domains has been shown to bind to XRCC4 (Grawunder et al., 1998
).
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Fig. 5 shows the substrate-specificities for the nick-ligation. (dT)16/poly(dA) was ligated, and activated by ATP (Fig. 5A
), indicating that it is an ATP-dependent DNA ligase. In the absence of ATP, CcLIG4 had nick-ligation activity, and this activity was suppressed by treatment with NaPPi (compare lanes 3 and 5 in Fig. 5A
), indicating that CcLIG4 was pre-adenylated by endogenous ATP. In the presence of 1 mM ATP and 0·5 mM NaPPi (lane 6), ATP was in greater excess than NaPPi and stimulated CcLIG4 (compare lanes 5 and 6 in Fig. 5A
). However, the ligase activity in lane 6 was lower than in the absence of NaPPi (lane 4). Fig. 5(B)
shows the nick-ligation activity on (dT)16/poly(rA), which is known as a substrate for human or Arabidopsis DNA ligase IV, but not for Sacch. cerevisiae (Robins & Lindahl, 1996
; Schar et al., 1997
; West et al., 2000
). The results were almost the same as for (dT)16/poly(dA), except that the activity was weaker. On the other hand, human DNA ligase III and Arabidopsis DNA ligase IV used (rA)/poly(dT) (Robins & Lindahl, 1996
; Tomkinson & Mackey, 1998
; West et al., 2000
), but CcLIG4 did not (data not shown). Overall, the substrate specificity of CcLIG4 was similar to that of human DNA ligase IV.
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DISCUSSION |
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In this study, we cloned and characterized the C. cinereus DNA ligase IV (CcLIG4) cDNA, and investigated the expression of CcLIG4 during meiotic development. Although CcLIG4 had sequence identity to DNA ligase IV from other eukaryotes, CcLIG4 contained an inserted sequence that had no sequence identity to other DNA ligases IV. The inserted sequence was very similar to the sequence inserted into exon IV of the C. cinereus PCNA gene (CcPCNA) we reported previously (Hamada et al., 2002). The role of the inserted sequence is unknown, but it may be a transposon or virus vestige after spread by infection in C. cinereus. The computer-simulated 3D structure suggests that the inserted sequence does not interfere with the structure of the catalytic core and tandem BRCT domains of CcLIG4. It must protrude beyond the tandem BRCT domains. In the human form, the region between the tandem BRCT domains has been shown to bind to XRCC4 (Grawunder et al., 1998
), so the inserted sequence may have some influence on the process by which XRCC4 binds to the region. DNA ligase IV forms a stable complex with XRCC4 and its protein is almost undetectable in a cell line lacking the XRCC4 gene (Bryans et al., 1999
). In C. cinereus, recombinant CcLIG4 protein has strong activity without XRCC4 compared to human DNA ligase IV (Y. Ichijima & H. Teraoka, unpublished data). CcLIG4 may have a function without XRCC4 in vivo. So far, XRCC4 in C.cinereus has not been reported.
Meiotic expression of CcLIG4
Northern blotting showed that CcLIG4 is expressed significantly in the leptotene and zygotene stages of the meiotic cell cycle. Although DNA ligase IV is an important element of DNA NHEJ pathways, it has been suggested that the NHEJ pathway is inhibited during the meiotic cell cycle. In mammalian meiotic cells, the Ku protein levels are much lower than in somatic cells, apparently reducing the capacity of the cells to carry out NHEJ and alternatively promoting homologous recombination (Goedecke et al., 1999). Taking this report into consideration, CcLIG4 may be involved not only in the NHEJ pathway of DSB repair, but also in meiotic recombination.
The other DSB repair proteins also function in meiotic recombination (Keeney, 2001; Martini & Keeney, 2002
), and C. cinereus homologues of DSB process proteins, for example Spo11, Mre11 and Rad50, have been found and relationships to meiotic recombination have been reported (Celerin et al., 2000
; Gerecke & Zolan, 2000
; Merino et al., 2000
; Ramesh & Zolan, 1995
). DNA ligase IV is possibly an important element in the coordinated multienzymic processes of meiotic recombination in relation to Spo11, Mre11 and Rad50.
In many organisms, Spo11-dependent DSBs are required for meiotic recombination pathways. In yeast and mouse, Spo11-dependent DSBs are formed in the leptotene stage (Roeder, 1997; Mahadevaiah et al., 2001
). Also in C. cinereus, ionizing radiation at the leptotene stage rescues spo11-1 mutation (Celerin et al., 2000
). Therefore, Spo11-dependent DSBs are expected in the leptotene stage in C. cinereus. After DSB formation, single-stranded DNA is generated by exonuclease digestion with Mre11 and Rad50. The single-strand portion invades the region having homologous sequences in the other allele (single-ended invasion, SEI) (Paques & Haber, 1999
; Villeneuve & Hillers, 2001
). The crossover and non-crossover pathways diverge soon after SEI. In the crossover pathway, double Holliday junction (DHJ) intermediates followed by SEI give rise mainly to crossover recombinants. Most noncrossover recombinants arise earlier via different pathways without any DHJ intermediate (Allers & Lichten, 2001b
). In the meiotic chromosome structure, recombination nodules (early and late) are observed as dense structures associated with syneptonemal complexes. It has been suggested that early nodules which are present during the zygotene and early pachytene stages mark the site of SEI, and mostly lead to noncrossover recombinants. Late nodules are thought to contain DHJ intermediates, subsequently resolving as crossover recombinants during mid and late pachytene stages (Zickler & Kleckner, 1999
; Allers & Lichten, 2001b
).
Northern blotting showed CcLIG4 to be expressed significantly in the leptotene and zygotene stages. In the current meiotic recombination model described above, we speculate that DNA ligase IV may ligate the synthesized strand to complete the noncrossover pathway in the zygotene and early pachytene stages, before crossover recombination is consummated. On the other hand, there is also a possibility that DNA ligase IV relates to crossover recombination in mid and late pachytene. Mammalian DNA ligase III is thought to have a role in meiotic recombination in the latter part of the pachytene stage (Chen et al., 1995
). In C. cinereus, predicted to lack DNA ligase III, CcLIG4 may play a similar role during meiosis, although there is no direct evidence of any relation to crossover or noncrossover pathways at this time.
CcLIG4-deficient mutants are required for further information, and more detailed investigation of the phenotype of the mutants is necessary, including studies on the genetic recombination frequency and morphology of the synaptinemal complex. A project to knock out the gene has been tried and further studies on conditional mutants of CcLIG4 would directly address the question of how CcLIG4 plays roles during meiosis.
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ACKNOWLEDGEMENTS |
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Received 19 February 2003;
revised 29 April 2003;
accepted 8 May 2003.
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