- Research article
- Open Access
A human RNA polymerase II subunit is encoded by a recently generated multigene family
- Sylvie Grandemange†1,
- Sophie Schaller†1,
- Shigeru Yamano1,
- Stanislas Du Manoir1,
- George V Shpakovski2,
- Marie-Geneviève Mattei3,
- Claude Kedinger1Email author and
- Marc Vigneron1
© Grandemange et al; licensee BioMed Central Ltd. 2001
- Received: 8 August 2001
- Accepted: 30 November 2001
- Published: 30 November 2001
The sequences encoding the yeast RNA polymerase II (RPB) subunits are single copy genes.
While those characterized so far for the human (h) RPB are also unique, we show that hRPB subunit 11 (hRPB11) is encoded by a multigene family, mapping on chromosome 7 at loci p12, q11.23 and q22. We focused on two members of this family, hRPB11a and hRPB11b: the first encodes subunit hRPB11a, which represents the major RPB11 component of the mammalian RPB complex ; the second generates polypeptides hRPB11bα and hRPB11bβ through differential splicing of its transcript and shares homologies with components of the hPMS2L multigene family related to genes involved in mismatch-repair functions (MMR). Both hRPB11a and b genes are transcribed in all human tissues tested. Using an inter-species complementation assay, we show that only hRPB11bα is functional in yeast. In marked contrast, we found that the unique murine homolog of RPB11 gene maps on chromosome 5 (band G), and encodes a single polypeptide which is identical to subunit hRPB11a.
The type hRPB11b gene appears to result from recent genomic recombination events in the evolution of primates, involving sequence elements related to the MMR apparatus.
- Multigene Family
- Differential Splice
- Recombinant Baculoviruses
- RPB11 Gene
- Lambda Clone
In eukaryotes, mRNAs are transcribed by RNA polymerase II (RPB). To date, most studies have focused on the yeast polymerases. Yeast RPB consists of 12 polypeptides ranging from 220 to 6 kDa [1–3]. Much less is known about the human (h) RPB, although the sequences encoding the subunits homologous to the yeast RPB have been determined. Complementation experiments have shown that many yeast subunits may be replaced in vivo by their human counterparts indicating a remarkable functional conservation through evolution [4–8]. This supports the view that the 3D structure of the yeast RPB [9, 10] can most likely be extended to other eukaryotic nuclear RPB molecules.
We have undertaken the characterisation of the human RPB subunits. All the subunit genes identified so far are unique: hRPB1 (Ac N° X74870-74) , hRPB2 (Ac N° AC068261), hRPB3 (Ac N° AC004382), hRPB4 (Ac N° U89387) , hRPB5 (Ac N° AC004151), hRPB6 (Ac N° AF006501) , hRPB7 (Ac N° U52427) , hRPB8 (Ac N° AJ252079-80), hRPB9 (Ac N° Z23102) , hRPB10α (Ac N° AJ252078), hRPB10β, (Ac N° Z47728-29) . The present report focuses on the hRPB11 gene which remained to be characterised.
It has been shown in many systems that the RPB11 subunit is able to heterodimerize with RPB3, evoking the alpha dimer in bacteria that directs the assembly of the two largest subunits of the RPB complex [16–22, 9, 10]. We show that human homologs of RPB11 are encoded by a multi-gene family. We shall refer to the previously identified human gene and cDNA encoding a protein homologous to yeast RPB11, as hRPB11a[23–25]. We have characterised additional members of this family and discuss their properties.
Characterisation of human genomic sequences encoding RPB11-related proteins a and b
Accession numbers of RPB11 sequences
AJ277932 (exon 1)
AJ277928 (exon 2)
AJ277929 (exon 3)
AJ277930 (exon 4)
AJ277931 (exons 1–4)
AJ277736 (intron 4)
AJ277737 (intron 4)
AJ277738 (intron 4)
AC087420 (exons 1–4)
Differential splicing of hRPB11b transcripts
We characterised two types of cDNAs from HeLa cells corresponding to hRPB11b transcripts and differing by the presence or absence of exon 3: they were named hRPB11bα and hRPB11bβ, respectively (Fig. 1B, Table 1). The absence of exon 3 switches the reading frame of exon 4, thereby extending the coding sequence (CDS) of hRPB11bβ into an additional exon 5, identified in another genomic sequence (Ac N° AC004951).
Most of the human cDNAs and ESTs in the databases (Table 1) perfectly matched the cDNAs reconstituted from the exons of both hRPB11a and b genes, indicating that these sequences are transcribed in vivo. Exon 3 being present in all the genomic clones, we conclude that the hRPB11bβ cDNA is produced by differential splicing resulting in exon 3 skipping.
Three types of proteins are encoded by the hRPB11 genes
The hRPB11a gene yields one type of mRNA that encodes the hRPB11a protein which was previously identified as a subunit of the human RPB complexes in Western-blots of immunoprecipitated RPB ( and our unpublished data). We have presently identified two additional cDNAs, hRPB11bα and hRPB11bβ, as distinct members of the same family.
Strikingly, as predicted from their sequences, the hRPB11a, bα and bβ polypeptides have similar sizes: 117, 115 and 116 residues, with calculated M.W. of 13.3, 13, 12.7 kDa, respectively (Fig. 1C). The N-terminal part of hRPB11a subunit differs only from the hRPB11b polypeptide by the presence of an additional Lys encoded at the junction between exons 1 and 2. By contrast, the C-terminal portions of these polypeptides differ drastically: while exon 4 of hRPB11a encodes a hydrophilic 11-residue peptide, it generates a rather hydrophobic 10-residue peptide in the case of hRPB11bα (Fig. 1C); concerning hRPB11bβ, due to exon 3 skipping, an unrelated peptide, rich in Pro (16%), Ala (14.5%), Gln (9%), His (9%) and Cys (7%) residues, is produced.
hRPB11 maps to three distinct loci on human chromosome 7
We localised the hRPB11 genomic sequences on metaphasic chromosomes with a fluorescent genomic probe encompassing the conserved exons 1 to 3 of hRPB11a (see Fig. 1A), thus revealing both hRPB11a and b genomic sequences. 50 metaphases were analysed: 90 % showed specific signals on chromosome 7, at positions q11.23 and q22, and about 80% at position p12.
A unique mRPB11 gene maps on mouse chromosome 5
The hRPB11a and hRPB11b genomic sequences are transcribed in all human tissues tested
The proteins encoded by the three cDNAs exhibit specific interaction properties
Complementation experiments in budding yeast
hRPB11b genomic sequences share a domain with hPMS2L genes
A multigene family encodes the hRPB11 but not the mRPB11 subunit
Our results demonstrate the existence in the human genome of a family of sequences related to the hRPB11a gene. Three distinct loci were detected using these genomic sequences as a probe on human chromosome 7 (Fig. 1A). Four distinct genomic sequences, hRPB11a, hRPB11b, and two type b-related sequences not described here (Ac N°s AC004951 and AC004084), were identified. Quantitative PCR measurements of the genomic copy number of hRPB11 exon 3 suggested the presence of about twelve distinct hRPB11 sequences in the human haploid genome (not shown).
In sharp contrast, such a gene family does not exist in mouse. The mRPB11 gene is unique, maps to a unique locus at 5G which was previously identified as a region synthenic to the human locus 7q11.23 [27, 28] and encodes a single murine mRPB11 protein identical to hRPB11a. The amplification of these genomic sequences may therefore represent a recent evolutionary event, that may be restricted to the primates, including human and african green monkey, as both RPB11 b-type mRNAs were present in COS-7 and CV1 cells (not shown).
These genomic sequences yield stable mRNAs
hRPB11a and hRPB11b transcripts were detected as stable mRNAs from 16 human tissues with, in some cases, a clear expression specificity, as shown by both Northern-blot (Fig. 3) and RT-PCR experiments (not shown). This is further confirmed by the fact that they have also been isolated from cDNA libraries from various tissues (see Table 1). The hRPB11bα and bβ CDS result from a differential splicing mechanism which we have not observed in any hRPB11a transcript. It is tempting therefore to speculate that a selective pressure maintains both isoforms of hRPB11b messenger RNAs.
Using specific antibodies, the hRPB11a protein was readily detected in extracts from either human tissues or cell lines . By contrast, the hRPB11bα or β proteins have not been detected so far, suggesting that their expression may be regulated at the translational level. We conclude that the hRPB11b proteins are either present at very low levels in these cells, or restricted to specific cell lines and/or situations that remain to be identified.
The hRPB11 proteins exhibit distinctive properties
Both hRPB11a and bα proteins were found to contact exclusively hRPB3 in coexpression assays, consistent with previous results (see Introduction). The yeast ScRPB3/ScRPB11 heterodimer has been modelled as an alpha-like dimer [29, 22], in which both C-terminal domains consist of two long alpha helices that cross each other and point toward the outside of the RPB complex [9, 10]. The hRPB11bα protein differs from hRPB11a at the very C-terminal end of this structure: its incorporation into the RPB complex instead of hRPB11a may therefore alter the interactions with the surrounding molecules. Despite this difference, both hRPB11a and bα can indeed integrate the RPB complex in vivo. We show that hRPB11bα is able to functionally replace ScRPB11 in the yeast RPB. Strikingly, the hRPB11a protein, known as a bona fide human RPB subunit, is not functional in yeast, whereas RPB11 of the distantly related fission yeast Schizosaccharomyces pombe can replace ScRPB11 in vivo . Why only hRPB11bα protein is functional in yeast may be related to the fact that its C-terminal domain exhibits a higher homology to the one of ScRPB11, both being rather hydrophobic, than the hydrophilic C-terminal domain of hRPB11a. The hRPB11bα protein may therefore be able to make, although weakly, critical contacts that the hRPB11a protein cannot make. These data point to a critical function of this C-terminal domain, that is encoded by a separate specific exon in mammals, in vivo.
The observation that the hRPB11bβ protein exhibits a completely distinct set of interactions with the other RPB subunits is presently difficult to integrate into the available model of the yeast RPB . It is possible that hRPB11bβ establishes multiple but transient contacts with various subunits during theRPB assembly and that these interactions are revealed in our binary protein binding assay.
How did evolution create the hRPB11b genomic sequences?
The b types of RPB11 genes may result from recombination events between a hRPB11a gene and at least two other genes, recruiting new exons 4 and 5, respectively. While the origin of exon 5 remains to be identified, exon 4 of hRPB11b is present in human PMS2L genes [31, 32] that have no known murine homolog. Although the function of these hPMS2L genes is still elusive, they share five coding exons with the PMS2 gene (b to f, Fig. 6) which plays a critical role in the mismatch repair (MMR) machinery and is located on human chromosome 7p22 [32, 33]. The hPMS2L and hRPB11 genes are located close to each other at positions 7p12, 7q11.23 and 7q22, supporting a recombinational origin [31, 32]. The primate specific hRPB11b gene products may provide a new link between the transcription and MMR machineries, together with the hPMS2L gene products. Thus, it will be of interest to explore the potential contribution of this species-specific gene rearrangement to the phenotypical differences between human and mice mutants which, when affected in their MMR activity, exhibit different types of tumors [34, 35]. Because of the presence of these primate-specific variants, drugs which are often tested in rodents may be mis-evaluated regarding their effects on human patients. The present findings indicate that more surprises may arise from studies of fundamental cellular processes, even in closely related species.
The human genome contains a family of genes that includes the gene (hRPB11a) encoding subunit 11 of the hRPB complex. Strikingly, such a family does not exist in the murine genome which contains a unique gene (mRPB11) encoding a protein which is identical to hRPB11a. Our observations strongly suggest that the hRPB11b genes have been engineered by evolution in the primate genomes to produce proteins with novel properties, required only under specific circumstances, the nature and role of which remain to be identified.
Cloning of genomic sequences
Strains and plasmids
# MATa/MATα ura3-52 his3-Δ200 leu2-3, leu2-112 lys2-Δ201 ade2-101 RPB11/rpb11-Δ1::HIS
# MATa/MATα ura3-52 his3-Δ200 leu2-3, leu2-112 lys2-Δ201 ade2-101 RPB11/rpb11-Δ1::HIS 3trp1-Δ63
# MATa ura3-52 his3-Δ200 leu2-3, leu2-112 lys2-Δ201 ade2-101 trp1-Δ63 rpb11-Δ1::HIS3 [pRP11/8-RPB11] (Offspring of YGVS-074 used for complementation assays)
# URA3 CEN ARS ScRPB11 EcoRI/SacI into pRS416 
# Partial Sau3AI genomic fragment in pBSK (Stratagene), containing exon 1 and 2 from hRPB11a gene
# Partial Sau3AI genomic fragment (19.6 kb) in pBSK (Stratagene), containing exons 1 to 4 from hRPB11b gene
# Partial Sau3AI genomic fragment (16.5 kb) in pBSK (Stratagene), containing exons 1 to 4 from mRPB11 gene
# Partial Sau3AI genomic fragment (17.7 kb) in pBSK (Stratagene), containing exons 1 to 4 from mRPB11 gene
# RT-PCR cloning of hRPB11a CDS in pBSK. The CDS can be excised using the unique Nhe I and Spe I sites
# RT-PCR cloning of hRPB11bα CDS in pCRII (Invitrogen). The CDS can be excised using Nhe I and Spe l
# RT-PCR cloning of hRPB11bβ CDS in pCRII. The CDS can be excised using the flanking EcoRI sites
# PCR cloning of ScRPB11 CDS from pRP11/8-RPB11 in pCRII. The CDS can be excised using Nhe I and Spe l
# 2μORI, TRP1, PGK promoter 
# Cloning of the Eco RI fragment of pCRII-ScRPB11 into the Eco RI site of pGEN
# Cloning of the Nhe I-Xba I fragment of pBSK-hRPB11a into the Nhe I site of pGEN
# Cloning of the Nhe I-Spe I fragment of pCRII-hRPB11bα into the Nhe I site of pGEN
# Cloning of the Eco RI fragment of pCRII-hRPB11bβ into the Eco RI site of pGEN
# Cloning of the Nhe I-Xba I fragment of pBSK-hRPB11a into the Xba I site of pVL1393 (PharMingen)
# Cloning of the Nhe I-Spe I fragment of pCRII-hRPB11bα into the Xba I site of pVL1393 (PharMingen)
# Cloning of the Nhe I-Spe I fragment of pCRII-hRPB11bβ into the Xba I site of pVL1393 (PharMingen)
A mouse SV129 D3 genomic library was similarly generated from mouse ES cells in lambda GEM12, yielding a library of about 2.5 106 independent phages, equivalent to 10 murine genomes. About 1.2 106 clones were screened as described above for the human genomic library. 26 positive clones were obtained. A Southern-blot analysis was performed on 12 independent clones (not shown) that revealed an identical restriction pattern indicating that they corresponded to a unique gene sequence. For further sequence analysis, the DNA inserts of two independent phages were excised using the flanking Not I restriction sites and subcloned in the unique Not I site of pBSK yielding pBSK-mRPB11-gen1 and pBSK-mRPB11-gen2, respectively (Table 2). Both of these genomic sequences were identical to the sequence that is present in the database (Ac N° AC087420).
The cDNA fragments were amplified by RT-PCR from total HeLa cell RNA using the appropriate primers and inserted in either pBSK or PCRII vectors. In each case, unique restriction sites were introduced in front of the ATG and after the stop codons. Several independent clones of each cDNA were sequenced. Restriction fragments spanning the complete coding sequences (CDS) were then transferred to various expression vectors (Table 2).
Localisation on human chromosomes by FISH
Human metaphase spreads were hybridised using as a probe the biotinylated 4.5 kb fragment encompassing hRPB11a exons 1 to 3 that was amplified using the TaKaRa system (BIO Whittaker Europe SPRL) [36, 37].
Mouse metaphase spreads were analysed as described using as probes the pBSK-mRPB11-gen1 and 2 plasmid DNAs, that were labelled using green and red fluorescent nucleotide derivatives respectively, and mixed for hybridization .
Recombinant baculoviruses and GST-pulldown
pVL1393-hRPB11bα and -hRPB11bβ transfer vectors (Table 2) were recombined with linearized baculovirus DNA (BaculoGold DNA, PharMingen) in Sf9 cells. The recombinant viruses were plaque-purified and expression of the proteins was verified by Western-blot analysis using specific mouse monoclonal antibodies. The other recombinant baculoviruses and the conditions for GST-pulldown assays have been described previously . The glutathione-sepharose beads were washed with PBS buffer containing 0.65 M NaCI and 1% Nonidet P-40.
Three 32P-end-labelled oligonucleotides specific to hRPB11 a, bα and bβ mRNAs, respectively, were used to probe MTN human blots I and II (Clonetech) of poly A+ mRNA from 16 normal human tissues (2 μg of each). The probe for hRPB11a was derived from the corresponding exon 4. The probe for hRPB11bα was derived from the junction between the corresponding exons 3 and 4. The probe for hRPB11bβ was derived from the junction between exons 2 and 4 of the hRPB11b gene.
Complementation in Saccharomyces cerevisiae
Yeast was grown on YPD or SD standard media. The ability of pGEN derivatives, expressing various proteins, to rescue the lethal phenotype conferred by the rpb11::HIS3 allele was assayed by plasmid shuffling. The YGVS-072 strain (Table 2) was transformed with the pGEN derivatives using a DMSO treatment protocol and plated on SD medium supplemented with adenine (20 mg/l), leucine (30 mg/l) and lysine (30 mg/l). Trp+ transformants were transferred twice to 5-fluoro-orotic acid plates and monitored for their ability to grow at 28°C. The viable clones were then grown on YPD liquid medium and the doubling time during exponential growth was determined from absorbance at 600 nm.
We thank Charlotte Hauss for technical assistance, Jean-Marie Gamier for the human and mouse genomic libraries, Isabelle Kolb-Cheynel for baculovirus and the DNA sequencing, oligonucleotide and peptide synthesis facilities. We also thank Bruno Chatton, Yann-Gaël Gangloff and Hélène Boeuf for helpfull discussions. This work was supported by the Association pour la Recherche sur Ie Cancer (ARC 9479), and the Ligue Nationale contre Ie Cancer. G.V.S acknowledges the support from the University Louis Pasteur of Strasbourg and the Russian Foundation for Basic Research (Grant N° 01-04-49741).
- Sentenac A: Eukaryotic RNA polymerases. CRC Crit Rev Biochem. 1985, 18: 31-90.View ArticlePubMedGoogle Scholar
- Young RA: RNA polymerase II. Annu Rev Biochem. 1991, 60: 689-715. 10.1146/annurev.biochem.60.1.689View ArticlePubMedGoogle Scholar
- Thuriaux P, Sentenac A: The molecular and cellular biology of the yeast saccharomyces: gene expression. In: Transcriptional regulation Edited by McKnight SL, Yamamoto KR, vol. 2, Cold Spring Harbor Lab. Press ed. pp. 1–48. New-York: Cold Spring Harbor Lab. Press;. 1992, 1-48.Google Scholar
- Shpakovski GV, Acker J, Wintzerith M, Lacroix JF, Thuriaux P, Vigneron M: Four subunits that are shared by the three classes of RNA polymerase are functionally interchangeable between Homo sapiens and Saccharomyces cerevisiae. Mol. Cell Biol. 1995, 15: 4702-4710.PubMed CentralView ArticlePubMedGoogle Scholar
- Mckune K, Moore PA, Hull MW, Woychik NA: Six human RNA polymerase subunits functionally substitute for their yeast counterparts. Mol. Cell Biol. 1995, 15: 6895-6900.PubMed CentralView ArticlePubMedGoogle Scholar
- Khazak V, Sadhale PP, Woychik NA, Brent R, Golemis EA: Human RNA polymerase II subunit hsRPB7 functions in yeast and influences stress survival and cell morphology. Mol. Biol. Cell. 1995, 6: 759-775.PubMed CentralView ArticlePubMedGoogle Scholar
- Khazak V, Estojak J, Cho H, Majors J, Sonoda G, Testa JR, Golemis EA: Analysis of the interaction of the novel RNA polymerase II subunit hsRPB4 with its partner hsRPB7 and with pol II. Mol. Cell Biol. 1998, 18: 1935-1945.PubMed CentralView ArticlePubMedGoogle Scholar
- Schaller S, Grandemange S, Shpakovski GV, Golemis EA, Kedinger C, Vigneron M: Interactions between the full complement of human RNA polymerase II subunits. FEBS Lett. 1999, 461: 253-257. 10.1016/S0014-5793(99)01441-6View ArticlePubMedGoogle Scholar
- Cramer P, Bushnell DA, Fu J, Gnatt AL, Maier-Davis B, Thompson NE, Burgess RR, Edwards AM, David PR, Kornberg RD: Architecture of RNA polymerase II and implications for the transcription mechanism. Science. 2000, 288: 640-649. 10.1126/science.288.5466.640View ArticlePubMedGoogle Scholar
- Cramer P, Bushnell DA, Kornberg RD: Structural basis of transcription: RNA polymerase II at 2.8 angstrom resolution. Science. 2001, 292: 1863-1876. 10.1126/science.1059493View ArticlePubMedGoogle Scholar
- Mita K, Tsuji H, Morimyo M, Takahashi E, Nenoi M, Ichimura S, Yamauchi M, Hongo E, Hayashi A: The human gene encoding the largest subunit of RNA polymerase II. Gene. 1995, 159: 285-286. 10.1016/0378-1119(95)00081-GView ArticlePubMedGoogle Scholar
- Pusch C, Wang Z, Roe B, Blin N: Genomic structure of the RNA polymerase II small subunit (hRPB14.4) locus (POLRF) and mapping to 22q13.1 by sequence identity. Genomics. 1996, 34: 440-442. 10.1006/geno.1996.0312View ArticlePubMedGoogle Scholar
- Schoen TJ, Chandrasekharappa SC, Guru SC, Mazuruk K, Chader GJ, Rodriguez IR: Human gene for the RNA polymerase II seventh subunit (hsRPB7): structure, expression and chromosomal localization. Biochim Biophys Acta. 1997, 1353: 39-49. 10.1016/S0167-4781(97)00041-9View ArticlePubMedGoogle Scholar
- Acker J, Wintzerith M, Vigneron M, Kedinger C: Structure of the gene encoding the 14.5 kDa subunit of human RNA polymerase II. Nucleic Acids Res. 1993, 21: 5345-5350.PubMed CentralView ArticlePubMedGoogle Scholar
- Acker J, Murroni O, Mattei MG, Kedinger C, Vigneron M: The gene (POLR2L) encoding the hRPB7.6 subunit of human RNA polymerase. Genomics. 1996, 32: 86-90. 10.1006/geno.1996.0079View ArticlePubMedGoogle Scholar
- Lalo D, Carles C, Sentenac A, Thuriaux P: Interactions between three common subunits of yeast RNA polymerases I and III. Proc. Natl. Acad. Sci. U.S.A. 1993, 90: 5524-5528.PubMed CentralView ArticlePubMedGoogle Scholar
- Woychik NA, Young RA: RNA polymerase II subunit RPB10 is essential for yeast cell viability. J Biol Chem. 1993, 268: 12230-PubMedGoogle Scholar
- Larkin RM, Guilfoyle TJ: Reconstitution of yeast and Arabidopsis RNA polymerase alpha-like subunit heterodimers. J. Biol. Chem. 1997, 272: 12824-12830. 10.1074/jbc.272.19.12824View ArticlePubMedGoogle Scholar
- Fanciulli M, Bruno T, Di Padova M, De Angelis R, Lovari S, Floridi A, Passananti C: The interacting RNA polymerase II subunits, hRPB11 and hRPB3, are coordinately expressed in adult human tissues and down-regulated by doxorubicin. FEBS Lett. 1998, 427: 236-240. 10.1016/S0014-5793(98)00431-1View ArticlePubMedGoogle Scholar
- Yasui K, Ishiguro A, Ishihama A: Location of subunit-subunit contact sites on RNA polymerase II subunit 3 from the fission yeast Schizosaccharomyces pombe. Biochemistry. 1998, 37: 5542-5548. 10.1021/bi972939bView ArticlePubMedGoogle Scholar
- Eloranta JJ, Kato A, Teng MS, WeinzierI RO: In vitro assembly of an archaeal D-L-N RNA polymerase subunit complex reveals a eukaryote-like structural arrangement. Nucleic Acids Res. 1998, 26: 5562-5567. 10.1093/nar/26.24.5562PubMed CentralView ArticlePubMedGoogle Scholar
- Zhang G, Campbell EA, Minakhin L, Richter C, Severinov K, Darst SA: Crystal structure of Thermus aquaticus core RNA polymerase at 3.3 A resolution. Cell. 1999, 98: 811-824. 10.1016/S0092-8674(00)81515-9View ArticlePubMedGoogle Scholar
- Pati UK: Human RNA polymerase II subunit hRPB14 is homologous to yeast RNA polymerase I, II, and III subunits (AC19 and RPB11) and is similar to a portion of the bacterial RNA polymerase alpha subunit. Gene. 1994, 145: 289-292. 10.1016/0378-1119(94)90022-1View ArticlePubMedGoogle Scholar
- Acker J, de Graaff M, Cheynel I, Khazak V, Kedinger C, Vigneron M: Interactions between the human RNA polymerase II subunits. J. Biol. Chem. 1997, 272: 16815-16821. 10.1074/jbc.272.27.16815View ArticlePubMedGoogle Scholar
- Fanciulli M, Bruno T, Cerboni C, Bonetto F, lacobini C, Frati L, Piccoli M, Floridi A, Santoni A, Punturieri A: Cloning of a novel human RNA polymerase II subunit downregulated by doxorubicin: New potential mechanisms of drug related toxicity. FEBS Lett. 1996, 384: 48-52. 10.1016/0014-5793(96)00277-3View ArticlePubMedGoogle Scholar
- Nishi Y, Yamamoto K, Yao Y, Yamamoto M, Nogi Y, Matsuo H, Muramatsu M: Isolation and characterization of cDNA encoding mouse RNA polymerase II subunit RPB14. Gene. 1997, 187: 165-170. 10.1016/S0378-1119(96)00739-1View ArticlePubMedGoogle Scholar
- O'Brien SJ, Menotti-Raymond M, Murphy WJ, Nash WG, Wienberg J, Stanyon R, Copeland NG, Jenkins NA, Womack JE, Marshall Graves JA: The promise of comparative genomics in mammals. Science. 1999, 286: 458-462. 10.1126/science.286.5439.458View ArticlePubMedGoogle Scholar
- Kumar S, Gadagkar SR, Filipski A, Gu X: Determination of the number of conserved chromosomal segments between species. Genetics. 2001, 157: 1387-1395.PubMed CentralPubMedGoogle Scholar
- Tan Q, Linask KL, Ebright RH, Woychik NA: Activation mutants in yeast RNA polymerase II subunit RPB3 provide evidence for a structurally conserved surface required for activation in eukaryotes and bacteria. Dev. 2000, 14: 339-348.Google Scholar
- Shpakovski GV, Gadal O, Labarre-Mariotte S, Lebedenko EN, Miklos I, Sakurai H, Proshkin SA, Van Mullem V, Ishihama A, Thuriaux P: Functional conservation of RNA polymerase II in fission and budding yeasts. J Mol Biol. 2000, 295: 1119-1127. 10.1006/jmbi.1999.3399View ArticlePubMedGoogle Scholar
- Horii A, Han HJ, Sasaki S, Shimada M, Nakamura Y: Cloning, characterization and chromosomal assignment of the human genes homologous to yeast PMS1, a member of mismatch repair genes. Biochem Biophys Res Commun. 1994, 204: 1257-1264. 10.1006/bbrc.1994.2598View ArticlePubMedGoogle Scholar
- Nicolaides NC, Carter KC, Shell BK, Papadopoulos N, Vogelstein B, Kinzler KW: Genomic organization of the human PMS2 gene family. Genomics. 1995, 30: 195-206. 10.1006/geno.1995.9885View ArticlePubMedGoogle Scholar
- Kolodner RD, Marsischky GT: Eukaryotic DNA mismatch repair. Curr Opin Genet Dev. 1999, 9: 89-96. 10.1016/S0959-437X(99)80013-6View ArticlePubMedGoogle Scholar
- Prolla TA, Baker SM, Harris AC, Tsao JL, Yao X, Bronner CE, Zheng B, Gordon M, Reneker J, Arnheim N, Shibata D, Bradley A, Liskay RM: Tumour susceptibility and spontaneous mutation in mice deficient in Mlh1, Pms1 and Pms2 DNA mismatch repair. Nat Genet. 1998, 18: 276-279. 10.1038/ng0398-276View ArticlePubMedGoogle Scholar
- Rosty C, Briere J, Cellier C, Delabesse E, Carnot F, Barbier JP, Laurent-Puig P: Association of a duodenal follicular lymphoma and hereditary nonpolyposis colorectal cancer. Mod Pathol. 2000, 13: 586-590. 10.1038/modpathol.3880100View ArticlePubMedGoogle Scholar
- Pinkel D, Straume T, Gray JW: Cytogenetic analysis using quantitative, high-sensitivity, fluorescence hybridization. Proc NatI Acad Sci USA. 1986, 83: 2934-2938.View ArticleGoogle Scholar
- Lemieux N, Dutrillaux B, Viegas-Pequignot E: A simple method for simultaneous R- or G-banding and fluorescence in situ hybridization of small single-copy genes. Cytogenet Cell Genet. 1992, 59: 311-312.View ArticlePubMedGoogle Scholar
- Hopfner R, Mousli M, Garnier JM, Redon R, du Manoir S, Chatton B, Ghyselinck N, Oudet P, Bronner C: Genomic structure and chromosomal mapping of the gene coding for ICBP90, a protein involved in the regulation of the topoisomerase llalpha gene expression. Gene. 2001, 266: 15-23. 10.1016/S0378-1119(01)00371-7View ArticlePubMedGoogle Scholar
- Woychik NA, McKune K, Lane WS, Young RA: Yeast RNA polymerase II subunit RPB11 is related to a subunit shared by RNA polymerase I and III. Gene Expr. 1993, 3: 77-82.PubMedGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article: verbatim copying and redistribution of this article are permitted in all media for any purpose, provided this notice is preserved along with the article's original URL.