- Research article
- Open Access
Rice SUV3 is a bidirectional helicase that binds both DNA and RNA
© Tuteja et al.; licensee BioMed Central Ltd. 2014
- Received: 21 September 2014
- Accepted: 9 October 2014
- Published: 14 October 2014
Helicases play crucial role in almost all the nucleic acid metabolism including replication, repair, recombination, transcription, translation, ribosome biogenesis and splicing and these processes regulate plant growth and development. It is suggested that helicases play essential roles in stabilizing growth in plants under stress because their presence in the stress-induced ORFs has been identified. Moreover in a recent study we have reported that SUV3 helicase from Oryza sativa (OsSUV3) functions in salinity stress tolerance in transgenic rice by improving the antioxidant machinery. SUV3 helicase has been identified and characterized from yeast and human systems but the properties and functions of plant SUV3 are poorly understood.
In this study, the purification and extensive characterization of recombinant OsSUV3 protein (67 kDa) is presented. OsSUV3 binds to DNA and RNA and exhibits DNA as well as RNA-dependent ATPase activities. It also contains the characteristic DNA and RNA helicase activity. OsSUV3 can use mainly ATP or dATP as energy source for the unwinding activity and it cannot unwind the blunt-end duplex DNA substrate. It is interesting to note that OsSUV3 unwinds DNA in both the 5'-3' and 3'-5 directions and thus its activity is bipolar in vitro. The Km values of OsSUV3 are 0.51 nM and 0.95 nM for DNA helicase and RNA helicase, respectively.
This study is the first direct evidence to show the bipolar DNA helicase activity of OsSUV3 protein. The unique properties of OsSUV3 including its dual helicase activity imply that it could be a multifunctional protein involved in biologically significant process of DNA and RNA metabolisms. These results should make significant contribution towards better understanding of SUV3 protein in plants.
- Mitochondrial protein
- Oryza sativa
- Plant DNA and RNA helicases
Helicases are highly conserved ubiquitous motor proteins involved in almost all the nucleic acid metabolic processes. They unwind nucleic acid duplexes with affiliated NTP hydrolysis and play essential roles in replication, DNA repair, recombination, transcription, translation, pre-mRNA processing and RNA degradation . Helicases are crucial tools for machinery of the cell. Most helicases contain conserved helicase motifs which are grouped together for the enzymatic and other functions ,.
The product of the SUV3 (suppressor of Var 3) gene was first described in yeast Saccharomyces cerevisiae. This gene encodes a DNA/RNA helicase belonging to the Ski2 family of DExH/D-box helicases. The human nuclear SUV3 gene (SUPV3L1) encodes an NTP-dependent RNA/DNA helicase (SUV3p, hSUV3p), which is related to the DexH/D (Ski2p) super family. The gene has been conserved during evolution and is present in purple bacteria, plants, C. elegans, Drosophila, mammals and in all eukaryotes . In humans the hSUV3 protein is localized predominantly in the mitochondrial matrix . The human hSUV3 protein is also present in the cell nucleus and was found to have several interacting partners: HBXIP , BLM helicase, and WRN helicase . hSUV3p has been reported to unwind both DNA and RNA duplexes and DNA/RNA hybrids and its activity towards DNA is much stronger ,. It was reported that the hSUV3 helicase interacts with replication protein A and flap endonuclease 1 in the nucleus . The yeast SUV3 has been reported to be involved in RNA turnover, mtDNA replication and maintenance of mtDNA stability .
To the best of our knowledge there are very few reports on plant SUV3. It was reported that nuclear-encoded Arabidopsis thaliana SUV3 (AtSUV3) is localized in Arabidopsis mitochondria and possesses ATPase activity . In a recent study we have reported that OsSUV3 dual helicase functions in salinity stress tolerance by maintaining photosynthesis and antioxidant machinery in rice (Oryza sativa L. cv. IR64) . Earlier we reported only presence of helicase and ATPase activities in the OsSUV3 protein but the detail characterization has not been reported yet. Here we report extensive characterization of OsSUV3 helicase. In this study a fresh batch of recombinant SUV3 protein from Oryza sativa (OsSUV3) was purified to homogeneity and characterized in detail using biochemical assays. ATPase assay in the presence of either DNA or RNA was performed and OsSUV3 exhibits ATP hydrolyzing properties. The OsSUV3 contains the DNA and RNA binding and DNA and RNA helicase activities. OsSUV3 exhibits bidirectional DNA unwinding activity and is unable to unwind the blunt-end DNA duplex substrate. The detailed OsSUV3 helicase kinetics was performed and the Km values are 0.51 and 0.95 nM for DNA helicase and RNA helicase, respectively. This study will be helpful in understanding the biochemical properties of OsSUV3 protein.
Purification of OsSUV3 protein
The expression clone corresponding to OsSUV3 was transformed into E. coli strain BL21 (DE3) pLysS and a fresh batch of his-tagged recombinant protein of 67 kDa (Additional file 1: Figure S1A) was purified as described earlier . The purified protein was confirmed by western blotting with anti-His antibodies (Additional file 1: Figure S1B). This purified protein was used for all the characterization as described in the following sections.
Characterization of ATPase activity of OsSUV3 protein
Characterization of DNA helicase activities of OsSUV3 protein
Almost all the helicases have specific nucleotide requirement and the hydrolysis of nucleotide is tightly coupled to unwinding activity. Therefore the helicase activity of OsSUV3 protein (300 nM) was measured with different nucleotide and deoxynucleotide triphosphates (NTPs and dNTPs). The activity was maximum in presence of ATP and dATP (Figure 2D, lanes 3 and 4, respectively). Although to some extent OsSUV3 also showed little unwinding activity in the presence of other dNTPs and NTPs such as UTP, dTTP, CTP, dCTP, GTP and dGTP (Figure 2D, lanes 1, 2, 5'8, respectively) but OsSUV3 did not show any unwinding activity in the absence of any NTP or dNTP (Figure 2D, lane C). The concentration requirement using ATP showed that the unwinding activity of OsSUV3 (300 nM) was maximal at 2.0 mM ATP concentration and it did not increase further on increasing the ATP concentration to 5.0 mM (Figure 2E, lane 4, 5 and 6, respectively). The specificity of OsSUV3 was further determined by checking its DNA unwinding activity with blunt-ended duplex DNA substrate. This substrate has same duplex length (17 base pair) and identical core sequence as the hanging tails substrate but had blunt ends so that as far as possible, any differences in efficiency of unwinding due to sequence differences could be eliminated. The results clearly indicate that OsSUV3 protein is unable to unwind the blunt-ended duplex substrate (Figure 2F, lanes 1-6).
Determination of direction of unwinding of OsSUV3 protein
Determination of RNA helicase activity of OsSUV3 protein
DNA and RNA binding activities of OsSUV3 protein
Determination of Kmand Vmaxfor the helicase activity of OsSUV3 protein
In a recent study we have reported that OsSUV3 protein contains the highest sequence homology to SUV3 protein from Arabidopsis thaliana, as compared to its yeast and human counterparts . AtSUV3 has been reported to be present in the mitochondria  therefore most likelyOsSUV3 is also present in mitochondria. In the present study we report the detailed biochemical characterization of OsSUV3 helicase. The results show that OsSUV3 exhibits DNA and RNA-dependent ATPase, DNA and RNA-binding and DNA and RNA unwinding activities. The results further show that OsSUV3 is a bipolar helicase capable of unwinding the DNA duplex in both the directions. Recently, the bipolar DNA helicase activity was also reported for pea p68 (Psp68) protein . The plant pea DNA helicase 47 (PDH47) was also reported as bipolar DNA helicase . Previously it has been reported that the some other non-plant helicases such as PfDH60, PfH45 and Dbp5/DDX19 homologue from human malaria parasite Plasmodium falciparum exhibit bipolar DNA helicase activity -. Some of the bacterial DNA helicases (PcrA and HerA) have also been reported as bipolar DNA helicases ,. In some of the previous studies it was suggested that hSUV3 moves in 5' to 3' direction  but some other results show that hSUV3 moves along the substrate in 3' to 5' direction .
Further characterization reveals that OsSUV3 shows maximum DNA helicase activity only with ATP and dATP as compared to other NTPs/dNTPs. This characteristic was similar to previously reported pea DNA helicase 45 (PDH45)  and human DNA helicase II . The AtSUV3 was reported to be localized in A. thaliana mitochondria. The characterization of the N-terminal domain of AtSUV3 containing the characteristic DExH-box helicase motifs revealed that it exhibited a low RNA stimulated ATPase activity in vitro . Similar to OsSUV3 the hSUV3p is also reported to be associated with both the DNA and RNA helicase activities ,. Our results indicate that OsSUV3 has no DNA unwinding activity with blunt end substrate. Previous studies have also reported that human and yeast SUV3 require a single-stranded fragment to unwind and have no detectable activity towards blunt-ended substrates . It has been reported previously that hSUV3 interacts with the RPA (replication protein A) and FEN1 (flap endonuclease 1) which are RecQ helicase associated proteins. These observations suggest that even though SUV3 is considered a mitochondrial helicase but the physical and functional interactions between hSUV3 and RPA and FEN1 support the hypothesis that hSUV3 most likely plays an important role in nuclear DNA metabolism as well . In an interesting recent study it has been reported that hSUV3, polynucleotide phosphorylase and mitochondrial polyadenylation polymerase form a transient complex to modulate mitochondrial mRNA polyadenylated tail lengths in response to energetic changes .
The biochemical studies reported in this manuscript are the necessary first step to obtain new insights into enzyme function and regulation. Overall, this study is the first direct evidence to show the bipolar DNA helicase activity of OsSUV3 protein. This protein exhibits both the ATP-dependent DNA and RNA helicase activities and ssDNA/RNA-dependent ATPase activities which provide energy for its unwinding function. Since maintenance of mitochondrial DNA requires activity of RNA and DNA helicases, therefore the DNA and RNA helicase activity of OsSUV3 may be useful for mitochondrial RNA splicing, translation and genome maintenance. Through its RNA helicase property it may act as RNA chaperone to destabilize the inhibitory secondary structures especially during stress conditions in plants where secondary structures in RNA are common. Its bipolar DNA helicase activity could also be useful in normal functioning of the protein during the stress conditions. Overall these results suggest that OsSUV3 is most likely a multifunctional protein involved in diverse processes including nucleic acid metabolism and might be playing important roles in numerous physiological processes in plant.
Purification and characterization of OsSUV3
The cloning, expression and purification of OsSUV3 was done using the method described earlier . The GenBank accession number of OsSUV3 gene is GQ982584 (http://www.ncbi.nlm.nih.gov/nuccore/GQ982584) and the accession number of OsSUV3 protein sequence is ACX50964 (http://www.ncbi.nlm.nih.gov/protein/260800457). The purified protein was confirmed by SDS-PAGE analysis. This purified preparation was used for all of the enzyme assays.
The ATPase reaction was performed in the buffer (20 mM Tris–HCl, pH 8.0, 8 mM DTT, 1.0 mM MgCl2, 20 mM KCl and 16 μg/ml BSA) for 1 hour at 37°C in the presence of purified OsSUV3 and 10 ng of M13 mp19 ssDNA and a mixture of [γ-32P] ATP (~17 nM) and 1 mM cold ATP. The products were separated by thin layer chromatography (TLC) (33'35) and the plate was scanned on phosphoimager. The quantitation was done using IMAGE j/ geldoc software (http://rsbweb.nih.gov/ij/). For the concentration curve analysis different concentrations of OsSUV3 (from 10 to 240 nM) protein was used. The time course analysis was performed with a fixed concentration (180 nM) of OsSUV3 and time duration ranging from 10 to 90 minutes. The quantitation was done using IMAGE j/ geldoc software (http://rsbweb.nih.gov/ij/) and percentage of ATP hydrolysis was plotted as the bar diagram.
Preparation of DNA helicase substrate and helicase assay
By using the standard strand displacement assay the helicase activity of OsSUV3 was determined using the partially duplex hanging tails substrate which consisted of a 32P-labelled 47-mer DNA oligodeoxynucleotide annealed to M13mp19 phage ssDNA. This oligodeoxynucleotide contains 15 base-pairs of non-complementary region at both 5' and 3' ends. Using T4 polynucleotide kinase (PNK) (5U) (New England Biolabs) in the standard PNK buffer (New England Biolabs) and 1.85'MBq of [γ-32P] ATP (specific activity 222 TBq/mmol)10 ng of the oligodeoxynucleotide was labeled at 5'-end at 37°C for one hour. Using 0.5'μg of single-stranded circular M13mp19 (+) phage DNA and standard annealing buffer (20 mM Tris–HCl, pH 7.5, 10 mM MgCl2, 100 mM NaCl, 1 mM DTT) the labeled oligodeoxynucleotide was annealed by heating at 95'C for 1 min, transferring immediately to 65'C for 2 min and then cooling slowly to room temperature. Using gel filtration through a Sepharose-4B column (Pharmacia, Sweden) the non-hybridized oligodeoxynucleotide was removed. The reaction mixture (10 μl) containing the 32P-labeled helicase substrate (1000°Cpm/10 μl) in appropriate buffer (20 mM Tris-HCl, pH 8.0, 8 mM DTT, 1.0 mM MgCl2, 20 mM KCl and 16 μg/ml BSA), and the purified protein OsSUV3 was incubated at 37°C for 60 min. The substrate and products were separated by electrophoresis on a non denaturing 12% or 15% (for the blunt end substrate) PAGE, dried, and the gel was scanned on phosphoimager and both the substrate and unwound DNA bands were quantified. The quantitation was done using IMAGE j/ geldoc software (http://rsbweb.nih.gov/ij/) and the percent unwinding was plotted as the bar diagram.
Preparation of RNA helicase substrate and unwinding assay
The RNA helicase substrate (RNA duplex) was prepared using the method described earlier . The RNA helicase substrate was prepared by using the RNA oligonucleotides synthesized from Primm srl (Milan, Italy): 13 mer 5'-AUAGCCUCAACCG-3' and 39 mer 5'-GGGAGAAAUCACUCGGUUGAGGCUAUCCGUAAAGCACGC-3'. Using five units of bacteriophage T4 polynucleotide kinase (NEB, England) about 10 ng of the 13-mer oligonucleotide was labeled at the 5'-end. This labeled oligonucleotide was then annealed with the 39-mer oligonucleotide using the standard procedure. The duplex RNA substrate was purified using the method described in the previous section. The RNA helicase assay (concentration and time course analysis) was done using the method described .
Preparation of blunt-ended DNA helicase substrate
The sequence of 17 mer oligodeoxynucleotide used for making the blunt-ended duplex substrate is as follows 5'-GTTTTCCCAGTCACGAC-3'. This was labeled at 5' end using the method described above and was annealed to its complementary oligodeoxynucleotide with the sequence 5'-GTCGTGACTGGGAAAAC-3'. The substrate was purified and used for the assay using the method described above.
Preparation of direction specific substrates
The substrate consisting of long linear M13mp19 ssDNA with short duplex ends for 3' to 5' unwinding was prepared by first 5'-end labeling of 32-mer oligodeoxynucleotide and then annealing with M13mp19 ssDNA as described above. The annealed substrate was digested with SmaI and purified by gel filtration through 1 ml of Sepharose-4B.For preparing a 5' to 3' direction-specific substrate, the oligodeoxynucleotide 32-mer (5'-TTCGAGCTCGGTACCCGGGGATCCTCTAGAGT-3') was first annealed to M13mp19 ssDNA using annealing buffer (20 mM Tris-HCl, pH 7.5, 10 mM MgCl2, 100 mM NaCl, 1 mM DTT) followed by labeling at 3'-OH end using standard buffer,5 units of DNA polymerase I (large fragment) and 50 μCurie [α-32P] dCTP at 23'C for 20 min. After increasing the dCTP to 50 mM using unlabelled dCTP the incubation was further continued for an additional 20 min at 23'C. The resulting duplex substrate was also digested with SmaI and purified by gel filtration through 1 ml Sepharose-4B.
In vitro DNA/RNA binding assay
The DNA-binding assay was performed by using the end-labeled DNA oligodeoxynucleotide of 32 bases with the sequence 5'-TTCGAGCTCGGTACCCGGGGATCCTCTAGAGT-3'. BSA (1 μg) and different amounts of OsSUV3 were dot-blotted on pre-charged PVDF membrane and the membrane was incubated in blocking buffer which contained 25'mM NaCl, 10 mM MgCl2, 10 mM HEPES, 0.1 mM EDTA, 1 mM DTT and 3% BSA. The membrane was incubated for 2 hour in binding buffer containing 10 pmol of 32P-labeled DNA oligodeoxynucleotide after blocking. After binding, the membrane was washed thrice with binding buffer and exposed for autoradiography. Increasing amounts of OsSUV3 were dot-blotted on another precharged PVDF membrane to check for loading of proteins. This membrane was blocked with blocking buffer (1% BSA in TBS) for 1 hour at room temperature and probed for a further 1 hour with alkaline phosphatase conjugated anti-his antibody (Sigma Chemical Co) (St. Louis, MO, USA) in same buffer. The blot was washed and developed using standard protocol. The RNA binding activity was assayed using the similar method but the labeled RNA oligonucleotide with the sequence 13 mer 5'-AUAGCCUCAACC-G-3' used for making the RNA substrate was used for the assay.
Determination of Km and Vmax
Helicase assay reactions for OsSUV3 were performed using the substrate of different concentrations (5'40 nM) in a standard reaction buffer (20 mM Tris-HCl, pH 8.0, 8 mM DTT, 1.0 mM MgCl2, 20 mM KCl and 16 μg/ml BSA). Using ImageJ software (http://rsbweb.nih.gov/ij/) the amount of dsDNA and unwound ssDNA was quantified from the autoradiogram and used for the Km and Vmax calculations.
Availability of supporting data
Name of the open access repository: NCBI (National Center for Biotechnology Information)
Link to the dataset for OsSUV3 gene: http://www.ncbi.nlm.nih.gov/nuccore/GQ982584
Link to the dataset for OsSUV3 protein: http://www.ncbi.nlm.nih.gov/protein/260800457
NT gratefully acknowledges the help of Drs. Pawan Umate and Maryam Sarwat in the initial stages of the work, and Dr Dipesh Trivedi for his help in protein purification. Work on plant helicases and abiotic stress tolerance in NT's laboratory is partially supported by the Department of Biotechnology (DBT), Government of India. We do not have any conflict of interest to declare.
- Tanner NK, Linder P: DExD/H box RNA helicases: from generic motors to specific dissociation functions. Mol Cell. 2001, 8: 251-262. 10.1016/S1097-2765(01)00329-X.View ArticlePubMedGoogle Scholar
- Tuteja N, Tuteja R: Prokaryotic and eukaryotic DNA helicases. Essential molecular motor proteins for cellular machinery. Eur J Biochem. 2004, 271: 1835-1848. 10.1111/j.1432-1033.2004.04093.x.View ArticlePubMedGoogle Scholar
- Tuteja N, Tuteja R: Unraveling DNA helicases: Motif, structure, mechanism and function. Eur J Biochem. 2004, 271: 1849-1863. 10.1111/j.1432-1033.2004.04094.x.View ArticlePubMedGoogle Scholar
- Stepien PP, Margossian SP, Landsman D, Butow RA: The yeast nuclear gene SUV3 affecting mitochondrial post-transcriptional processes encodes a putative ATP-dependent RNA helicase. Proc Natl Acad Sci U S A. 1992, 89: 6813-6817. 10.1073/pnas.89.15.6813.PubMed CentralView ArticlePubMedGoogle Scholar
- Dmochowska A, Kalita K, Krawczyk M, Golik P, Mroczek K, Lazowska J, Stepien PP, Bartnik E: A human putative SUV3-like RNA helicase is conserved between Rhodobacter and all eukaryotes. Acta Biochim Pol. 1999, 46: 155-162.PubMedGoogle Scholar
- Minczuk M, Piwowarski J, Papworth MA, Awiszus K, Schalinski S, Dziembowski A, Dmochowska A, Bartnik E, Tokatlidis K, Stepien PP, Borowski P: Localisation of the human hSUV3p helicase in the mitochondrial matrix and its preferential unwinding of dsDNA. Nucleic Acids Res. 2002, 30: 5074-5086. 10.1093/nar/gkf647.PubMed CentralView ArticlePubMedGoogle Scholar
- Minczuk M, Mroczek S, Pawlak SD, Stepien PP: Human ATP-dependent RNA/DNA helicase hSUV3p interacts with the cofactor of survivin HBXIP. FEBS J. 2005, 272: 5008-5019. 10.1111/j.1742-4658.2005.04910.x.View ArticlePubMedGoogle Scholar
- Pereira M, Mason P, Szczesny RJ, Maddukuri L, Dziwura S, Jedrzejczak R, Paul E, Wojcik A, Dybczynska L, Tudek B, Bartnik E, Klysik J, Bohr VA, Stepien P: Interaction of human SUV3 RNA/DNA helicase with BLM helicase; loss of the SUV3 gene results in mouse embryonic lethality. Mech Ageing Dev. 2007, 128: 609-617. 10.1016/j.mad.2007.09.001.View ArticlePubMedGoogle Scholar
- Shu Z, Vijayakumar S, Chen CF, Chen PL, Lee WH: Purified human SUV3p exhibits multiple-substrate unwinding activity upon conformational change. Biochemistry. 2004, 43: 4781-4790. 10.1021/bi0356449.View ArticlePubMedGoogle Scholar
- Veno ST, Kulikowicz T, Pestana C, Stepien PP, Stevnsner T, Bohr VA: The human SUV3 helicase interacts with replication protein A and flap endonuclease 1 in the nucleus. Biochem J. 2011, 440: 293-300. 10.1042/BJ20100991.PubMed CentralView ArticlePubMedGoogle Scholar
- Guo XE, Chen C-F, Ding-Hwa D, Wang DD, Modrek AS, Phan VH, Lee WH, Chen PL: Uncoupling the roles of the SUV3 helicase in maintenance of mitochondrial genome stability and RNA degradation. J Biol Chem. 2011, 286: 38783-3894. 10.1074/jbc.M111.257956.PubMed CentralView ArticlePubMedGoogle Scholar
- Gagliardi D, Kuhn J, Spadinger U, Brennicke A, Leaver CJ, Binder S: An RNA helicase (AtSUV3) is present in Arabidopsis thaliana mitochondria. FEBS Lett. 1999, 458: 337-342. 10.1016/S0014-5793(99)01168-0.View ArticlePubMedGoogle Scholar
- Tuteja N, Sahoo RK, Garg B, Tuteja N: OsSUV3 dual helicase functions in salinity stress tolerance by maintaining photosynthesis and antioxidant machinery in rice (Oryza sativa L. cv. IR64). Plant J. 2013, 76: 115-127.PubMedGoogle Scholar
- Tuteja N, Tarique M, Banu MSA, Ahmad M, Tuteja R: Pisum sativum p68 DEAD-box protein is ATP-dependent RNA helicase and unique bipolar DNA helicase. Plant Mol Biol. 2014, 85: 639-651. 10.1007/s11103-014-0209-6.View ArticlePubMedGoogle Scholar
- Vashisht AA, Pradhan A, Tuteja R, Tuteja N: Cold- and salinity stress-induced bipolar pea DNA helicase 47 is involved in protein synthesis and stimulated by phosphorylation with protein kinase C. Plant J. 2005, 44: 76-87. 10.1111/j.1365-313X.2005.02511.x.View ArticlePubMedGoogle Scholar
- Pradhan A, Chauhan VS, Tuteja R: A novel `DEAD-box' DNA helicase from Plasmodium falciparum is homologous to p68. Mol Biochem Parasitol. 2005, 140: 55-60. 10.1016/j.molbiopara.2004.12.004.View ArticlePubMedGoogle Scholar
- Pradhan A, Chauhan VS, Tuteja R: Plasmodium falciparum DNA helicase 60 is a schizont stage specific, bipolar and dual helicase stimulated by PKC phosphorylation. Mol Biochem Parasitol. 2005, 144: 133-141. 10.1016/j.molbiopara.2005.08.006.View ArticlePubMedGoogle Scholar
- Pradhan A, Tuteja R: Bipolar, dual Plasmodium falciparum helicase 45 expressed in the intraerythrocytic developmental cycle is required for parasite growth. J Mol Biol. 2007, 373: 268-281. 10.1016/j.jmb.2007.07.056.View ArticlePubMedGoogle Scholar
- Mehta J, Tuteja R: A novel dual Dbp5/DDX19 homologue from Plasmodium falciparum requires Q motif for activity. Mol Biochem Parasitol. 2011, 176: 58-63. 10.1016/j.molbiopara.2010.12.003.View ArticlePubMedGoogle Scholar
- Anand SP, Khan SA: Structure-specific DNA binding and bipolar helicase activities of PcrA. Nucleic Acids Res. 2004, 32: 3190-3197. 10.1093/nar/gkh641.PubMed CentralView ArticlePubMedGoogle Scholar
- Constantinesco F, Forterre P, Koonin EV, Aravind L, Elie CA: A bipolar DNA helicase gene, herA, clusters with rad50, mre11 and nurA genes in thermophilic archaea. Nucleic Acids Res. 2004, 32: 1439-1447. 10.1093/nar/gkh283.PubMed CentralView ArticlePubMedGoogle Scholar
- Pham XH, Reddy MK, Ehtesham NZ, Matta B, Tuteja N: A DNA helicase from Pisum sativum is homologous to translation initiation factor and stimulates topoisomerase I activity. Plant J. 2000, 24: 219-229. 10.1046/j.1365-313x.2000.00869.x.View ArticlePubMedGoogle Scholar
- Tuteja N, Tuteja R, Ochem A, Taneja P, Huang NW, Simoncsits A, Susic S, Rahman K, Marusic L, Chen J, Zhang J, Wang S, Pongor S, Falaschi A: Human DNA helicase II: a novel DNA unwinding enzyme identified as the Ku autoantigen. EMBO J. 1994, 13: 4991-5001.PubMed CentralPubMedGoogle Scholar
- Szczesny RJ, Wojcik MA, Borowski LS, Szewczyk MJ, Skrok MM, Golik P, Stepien PP: Yeast and human mitochondrial helicases. Biochim Biophys Acta. 1829, 2013: 842-853.Google Scholar
- Wang D-H, Guo XE, Modrek AS, Chen C-F, Chen P-L, Lee W-H: Helicase SUV3, polynucleotide phosphorylase, and mitochondrial polyadenylation polymerase form a transient complex to modulate mitochondrial mRNA polyadenylated tail lengths in response to energetic changes. J Biol Chem. 2014, 289: 16727-16735. 10.1074/jbc.M113.536540.PubMed CentralView ArticlePubMedGoogle Scholar
- Tarique M, Ahmad M, Ansari A, Tuteja R: Plasmodium falciparum DOZI, an RNA helicase interacts with eIF4E. Gene. 2013, 522: 46-59. 10.1016/j.gene.2013.03.063.View ArticlePubMedGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.