Re-visiting protein-centric two-tier classification of existing DNA-protein complexes

BMC Bioinformatics

Sony Malhotra¹  Ramanathan Sowdhamini¹ 

[1] National Centre for Biological Sciences (TIFR), UAS-GKVK Campus, Bellary Road, Bangalore, 560 065, India

关键词: Sequence searches;    Genome-wide survey;    DNA-protein interactions;    Classification;    DNA;   

Others  :  1088205
DOI  :  10.1186/1471-2105-13-165

 received in 2011-07-12, accepted in 2012-03-26,  发布年份 2012

【 摘 要 】

Background

Precise DNA-protein interactions play most important and vital role in maintaining the normal physiological functioning of the cell, as it controls many high fidelity cellular processes. Detailed study of the nature of these interactions has paved the way for understanding the mechanisms behind the biological processes in which they are involved. Earlier in 2000, a systematic classification of DNA-protein complexes based on the structural analysis of the proteins was proposed at two tiers, namely groups and families. With the advancement in the number and resolution of structures of DNA-protein complexes deposited in the Protein Data Bank, it is important to revisit the existing classification.

Results

On the basis of the sequence analysis of DNA binding proteins, we have built upon the protein centric, two-tier classification of DNA-protein complexes by adding new members to existing families and making new families and groups. While classifying the new complexes, we also realised the emergence of new groups and families. The new group observed was where β-propeller was seen to interact with DNA. There were 34 SCOP folds which were observed to be present in the complexes of both old and new classifications, whereas 28 folds are present exclusively in the new complexes. Some new families noticed were NarL transcription factor, Z-α DNA binding proteins, Forkhead transcription factor, AP2 protein, Methyl CpG binding protein etc.

Conclusions

Our results suggest that with the increasing number of availability of DNA-protein complexes in Protein Data Bank, the number of families in the classification increased by approximately three fold. The folds present exclusively in newly classified complexes is suggestive of inclusion of proteins with new function in new classification, the most populated of which are the folds responsible for DNA damage repair. The proposed re-visited classification can be used to perform genome-wide surveys in the genomes of interest for the presence of DNA-binding proteins. Further analysis of these complexes can aid in developing algorithms for identifying DNA-binding proteins and their family members from mere sequence information.

【 授权许可】

   
2012 Malhotra and Sowdhamini; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Luscombe NM, Austin SE, Berman HM, Thornton JM: An overview of the structures of protein-DNA complexes. Genome Biol 2000., 1reviews001.1-001.37
• [2]Mandel-Gutfreund Y, Schueler O, Margalit H: Comprehensive analysis of hydrogen bonds in regulatory protein DNA-complexes: in search of common principles. J Mol Biol 1995, 253:370-382.
• [3]Luscombe NM, Laskowski RA, Thornton JM: Amino acid–base interactions: a three-dimensional analysis of protein-DNA interactions at an atomic level. Nucleic Acids Res 2001, 29:2860-2874.
• [4]Reddy CK, Das A, Jayaram B: Do water molecules mediate protein-DNA recognition? J Mol Biol 2001, 314:619-632.
• [5]Harrison SC: A structural taxonomy of DNA-binding domains. Nature 1991, 353:715-719.
• [6]Ponomarenko JV, Bourne PE, Shindyalov IN: Building an automated classification of DNA-binding protein domains. Bioinformatics 2002, 18(Suppl 2):S192-201.
• [7]Prabakaran P, Siebers JG, Ahmad S, Gromiha MM, Singarayan MG, Sarai A: Classification of protein-DNA complexes based on structural descriptors. Structure 2006, 14:1355-1367.
• [8]Sen TZ, Kloczkowski A, Jernigan RL: A DNA-centric look at protein-DNA complexes. Structure 2006, 14:1341-1342.
• [9]Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE: The Protein Data Bank. Nucleic Acids Res 2000, 28:235-242.
• [10]Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402.
• [11]Marchler-Bauer A, Panchenko AR, Shoemaker BA, Thiessen PA, Geer LY, Bryant SH: CDD: a database of conserved domain alignments with links to domain three-dimensional structure. Nucleic Acids Res 2002, 30:281-283.
• [12]Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ: Multiple sequence alignment with Clustal X. Trends Biochem Sci 1998, 23:403-405.
• [13]Schmitt MP, Holmes RK: Iron-dependent regulation of diphtheria toxin and siderophore expression by the cloned Corynebacterium diphtheriae repressor gene dtxR in C. diphtheriae C7 strains. Infect Immun 1991, 59:1899-1904.
• [14]Schmitt MP, Predich M, Doukhan L, Smith I, Holmes RK: Characterization of an iron-dependent regulatory protein (IdeR) of Mycobacterium tuberculosis as a functional homolog of the diphtheria toxin repressor (DtxR) from Corynebacterium diphtheriae. Infect Immun 1995, 63:4284-4289.
• [15]Ito J, Braithwaite DK: Compilation and alignment of DNA polymerase sequences. Nucleic Acids Res 1991, 19:4045-4057.
• [16]Murzin AG, Brenner SE, Hubbard T, Chothia C: SCOP: a structural classification of proteins database for the investigation of sequences and structures. J Mol Biol 1995, 247:536-540.
• [17]Täubig H, Buchner A, Griebsch J: PAST: fast structure-based searching in the PDB. Nucleic Acids Res 2006, 34:W20-23.
• [18]Scrima A, Konícková R, Czyzewski BK, Kawasaki Y, Jeffrey PD, Groisman R, Nakatani Y, Iwai S, Pavletich NP, Thomä NH: Structural basis of UV DNA-damage recognition by the DDB1-DDB2 complex. Cell 2008, 135:1213-1223.
• [19]Iyaguchi D, Yao M, Watanabe N, Nishihira J, Tanaka I: DNA Recognition Mechanism of the ONECUT Homeodomain of Transcription Factor HNF-6. Structure 2007, 15:75-83.
• [20]Chi Y, Frantz JD, Oh B, Hansen L, Dhe-Paganon S, Shoelson SE: Diabetes mutations delineate an atypical POU domain in HNF-1alpha. Mol Cell 2002, 10:1129-1137.
• [21]Yousef MS, Matthews BW: Structural basis of Prospero-DNA interactionimplications for transcription regulationin developing cells. Structure 2005, 13:601-607.
• [22]Tawaramoto MS, Park S, Tanaka Y, Nureki O, Kurumizaka H, Yokoyama S: Crystal structure of the human centromere protein B (CENP-B) dimerization domain at 1.65-A resolution. J Biol Chem 2003, 278:51454-51461.
• [23]Orth P, Schnappinger D, Hillen W, Saenger W, Hinrichs W: Structural basis of gene regulation by the tetracycline inducible Tet repressor-operator system. Nat Struct Biol 2000, 7:215-219.
• [24]Schumacher MA, Miller MC, Grkovic S, Brown MH, Skurray RA, Brennan RG: Structural basis for cooperative DNA binding by two dimers of the multidrug-binding protein QacR. EMBO J 2002, 21:1210-1218.
• [25]Itou H, Watanabe N, Yao M, Shirakihara Y, Tanaka I: Crystal structures of the multidrug binding repressor Corynebacterium glutamicum CgmR in complex with inducers and with an operator. J Molecular Biol 2010, 403:174-184.
• [26]Komori H, Matsunaga F, Higuchi Y, Ishiai M, Wada C, Miki K: Crystal structure of a prokaryotic replication initiator protein bound to DNA at 2.6 A resolution. EMBO J 1999, 18:4597-4607.
• [27]Schumacher MA, Funnell BE: Structures of ParB bound to DNA reveal mechanism of partition complex formation. Nature 2005, 438:516-519.
• [28]Williams CE, Grotewold E: Differences between plant and animal Myb domains are fundamental for DNA binding activity, and chimeric Myb domains have novel DNA binding specificities. J Biol Chem 1997, 272:563-571.
• [29]König B, Müller JJ, Lanka E, Heinemann U: Crystal structure of KorA bound to operator DNA: insight into repressor cooperation in RP4 gene regulation. Nucleic Acids Res 2009, 37:1915-1924.
• [30]Shen A, Higgins DE, Panne D: Recognition of at-rich DNA binding sites by the MogR repressor. Structure 2009, 17:769-777.
• [31]Lee KS, Bumbaca D, Kosman J, Setlow P, Jedrzejas MJ: Structure of a protein–DNA complex essential for DNA protection in spores of Bacillus species. Proc Nat Acad Sci 2008, 105:2806.
• [32]Lane WJ, Darst SA: The structural basis for promoter -35 element recognition by the group IV sigma factors. PLoS Biol 2006, 4:e269.
• [33]Fuhrmann J, Schmidt A, Spiess S, Lehner A, Turgay K, Mechtler K, Charpentier E, Clausen T: McsB is a protein Arginine Kinase that Phosphorylates and inhibits the heat-shock regulator CtsR. Science 2009, 324:1323-1327.
• [34]McGeehan JE, Streeter SD, Thresh SJ, Ball N, Ravelli RB, Kneale GG: Structural analysis of the genetic switch that regulates the expression of restriction-modification genes. Nucleic Acids Res 2008, 36:4778.
• [35]Fujikawa N, Kurumizaka H, Nureki O, Terada T, Shirouzu M, Katayama T, Yokoyama S: Structural basis of replication origin recognition by the DnaA protein. Nucleic Acids Res 2003, 31:2077-2086.
• [36]Zhao H, Msadek T, Zapf J, Madhusudan , Hoch JA, Varughese KI: DNA complexed structure of the key transcription factor initiating development in sporulating bacteria. Structure 2002, 10:1041-1050.
• [37]Khare D, Ziegelin G, Lanka E, Heinemann U: Sequence-specific DNA binding determined by contacts outside the helix-turn-helix motif of the ParB homolog KorB. Nat Struct Mol Biol 2004, 11:656-663.
• [38]He C, Hus J, Sun LJ, Zhou P, Norman DPG, Dötsch V, Wei H, Gross JD, Lane WS, Wagner G, Verdine GL: A methylation-dependent electrostatic switch controls DNA repair and transcriptional activation by E. coli ada. Mol Cell 2005, 20:117-129.
• [39]Ha SC, Kim D, Hwang HY, Rich A, Kim YG, Kim KK: The crystal structure of the second Z-DNA binding domain of human DAI (ZBP1) in complex with Z-DNA reveals an unusual binding mode to Z-DNA. Proc Nat Acad Sci 2008, 105:20671.
• [40]Ha SC, Lokanath NK, Van Quyen D, Wu CA, Lowenhaupt K, Rich A, Kim Y, Kim KK: A poxvirus protein forms a complex with left-handed Z-DNA: crystal structure of a Yatapoxvirus Zalpha bound to DNA. Proc Natl Acad Sci USA 2004, 101:14367-14372.
• [41]Schumacher MA, Lau AOT, Johnson PJ: Structural basis of core promoter recognition in a primitive eukaryote. Cell 2003, 115:413-424.
• [42]Yokoyama K, Ishijima SA, Koike H, Kurihara C, Shimowasa A, Kabasawa M, Kawashima T, Suzuki M: Feast/famine regulation by transcription factor FL11 for the survival of the Hyperthermophilic Archaeon Pyrococcus OT3. Structure 2007, 15:1542-1554.
• [43]Huang N, De Ingeniis J, Galeazzi L, Mancini C, Korostelev YD, Rakhmaninova AB, Gelfand MS, Rodionov DA, Raffaelli N, Zhang H: Structure and function of an ADPRibose- dependent transcriptional regulator of NAD metabolism. Structure 2009, 17:939-951.
• [44]Cherney LT, Cherney MM, Garen CR, Lu GJ, James MN: Crystal structure of the arginine repressor protein in complex with the DNA operator from Mycobacterium tuberculosis. J Mol Biol 2008, 384:1330-1340.
• [45]Garnett JA, Marincs F, Baumberg S, Stockley PG, Phillips SEV: Structure and function of the arginine repressor-operator complex from Bacillus subtilis. J Mol Biol 2008, 379:284-298.
• [46]Gajiwala KS, Chen H, Cornille F, Roques BP, Reith W, Mach B, Burley SK: Structure of the winged-helix protein hRFX1 reveals a new mode of DNA binding. Nature 2000, 403:916-921.
• [47]Blanco AG, Sola M, Gomis-Rüth FX, Coll M: Tandem DNA recognition by PhoB, a two-component signal transduction transcriptional activator. Structure 2002, 10:701-713.
• [48]Watanabe S, Kita A, Kobayashi K, Miki K: Crystal structure of the [2Fe-2S] oxidativestress sensor SoxR bound to DNA. Proc Natl Acad Sci USA 2008, 105:4121-4126.
• [49]Schumacher MA, Hurlburt BK, Brennan RG: Crystal structures of SarA, a pleiotropic regulator of virulence genes in S. aureus. Nature 2001, 409:215-219.
• [50]Sabogal A, Lyubimov AY, Corn JE, Berger JM, Rio DC: THAP proteins target specific DNA sites through bipartite recognition of adjacent major and minor grooves. Nat Struct Mol Biol 2009, 17:117-123.
• [51]Bates DL, Chen Y, Kim G, Guo L, Chen L: Crystal structures of multiple GATA zinc fingers bound to DNA reveal new insights into DNA recognition and self-association by GATA. J. Mol. Biol 2008, 381:1292-1306.
• [52]Cohen SX, Moulin M, Hashemolhosseini S, Kilian K, Wegner M, M\üller CW: Structure of the GCM domain–DNA complex: a DNA-binding domain with a novel fold and mode of target site recognition. EMBO J 2003, 22:1835-1845.
• [53]Schumacher MA: The Structure of a CREB bZIPmiddle dotSomatostatin CRE complex reveals the basis for selective dimerization and divalent cation-enhanced DNA Binding. J Bioll Chem 2000, 275:35242-35247.
• [54]Fujii Y, Shimizu T, Toda T, Yanagida M, Hakoshima T: Structural basis for the diversity of DNA recognition by bZIP transcription factors. Nat Struct Mol Biol 2000, 7:889-893.
• [55]Kurokawa H, Motohashi H, Sueno S, Kimura M, Takagawa H, Kanno Y, Yamamoto M, Tanaka T: Structural Basis of Alternative DNA Recognition by Maf Transcription Factors. Mol Cell Biol 2009, 29:6232-6244.
• [56]Longo A, Guanga GP, Rose RB: Crystal Structure of E47−NeuroD1/Beta2 bHLH Domain−DNA Complex: Heterodimer Selectivity and DNA Recognition. Biochemistry 2008, 47:218-229.
• [57]Bradley CM, Ronning DR, Ghirlando R, Craigie R, Dyda F: Structural basis for DNA bridging by barrier-to-autointegration factor. Nat Struct Mol Biol 2005, 12:935-936.
• [58]Albert A, Muñoz-Espín D, Jiménez M, Asensio JL, Hermoso JA, Salas M, Meijer WJJ: Structural basis for membrane anchorage of viral phi29 DNA during replication. J Biol Chem 2005, 280:42486-42488.
• [59]Lindner SE, De Silva EK, Keck JL, Llinás M: Structural determinants of DNA binding by a P. falciparum ApiAP2 transcriptional regulator. J Mol Biol 2010, 395:558-567.
• [60]Sidote DJ, Barbieri CM, Wu T, Stock AM: Structure of the Staphylococcus aureus AgrA LytTR domain bound to DNA reveals a beta fold with an unusual mode of binding. Structure 2008, 16:727-735.
• [61]Schumacher MA, Glover TC, Brzoska AJ, Jensen SO, Dunham TD, Skurray RA, Firth N: Segrosome structure revealed by a complex of ParR with centromere DNA. Nature 2007, 450:1268-1271.
• [62]Zhou Y, Larson JD, Bottoms CA, Arturo EC, Henzl MT, Jenkins JL, Nix JC, Becker DF, Tanner JJ: Structural basis of the transcriptional regulation of the proline utilization regulon by multifunctional PutA. J Mol Biol 2008, 381:174-188.
• [63]Min J, Pavletich NP: Recognition of DNA damage by the Rad4 nucleotide excision repair protein. Nature 2007, 449:570-575.
• [64]Walker JR, Corpina RA, Goldberg J: Structure of the Ku heterodimer bound to DNA and its implications for double-strand break repair. Nature 2001, 412:607-614.
• [65]Ho KL, McNae IW, Schmiedeberg L, Klose RJ, Bird AP, Walkinshaw MD: MeCP2 Binding to DNA Depends upon Hydration at Methyl-CpG. Mol Cell 2008, 29:525-531.
• [66]Badia D, Camacho A, Pérez-Lago L, Escandon C, Salas M, Coll M: The Structure of Phage 29 Transcription Regulator p4-DNA Complex Reveals an N-Hook Motif for DNA Binding. Mol cell 2006, 22:73-81.
• [67]Metz AH, Hollis T, Eichman BF: DNA damage recognition and repair by 3-methyladenine DNA glycosylase I (TAG). EMBO J 2007, 26:2411-2420.
• [68]Spiegel PC, Chevalier B, Sussman D, Turmel M, Lemieux C, Stoddard BL: The structure of I-CeuI homing endonuclease: Evolving asymmetric DNA recognition from a symmetric protein scaffold. Structure 2006, 14:869-880.
• [69]Shen BW, Landthaler M, Shub DA, Stoddard BL: DNA binding and cleavage by the HNH homing endonuclease I-HmuI. J Mol Biol 2004, 342:43-56.
• [70]Frei C, Gasser SM: RecQ-like helicases: the DNA replication checkpoint connection. J Cell Sci 2000, 113(Pt 15):2641-2646.
• [71]Faucher F, Wallace SS, Doublié S: The C-terminal lysine of Ogg2 DNA glycosylases is a major molecular determinant for guanine/8-oxoguanine distinction. J Mol Biol 2010, 397:46-56.
• [72]Hashimoto H, Shimizu T, Imasaki T, Kato M, Shichijo N, Kita K, Sato M: Crystal structures of type II restriction endonuclease EcoO109I and its complex with cognate DNA. J Biol Chem 2005, 280:5605-5610.
• [73]Newman M, Murray-Rust J, Lally J, Rudolf J, Fadden A, Knowles PP, White MF, McDonald NQ: Structure of an XPF endonuclease with and without DNA suggests a model for substrate recognition. EMBO J 2005, 24:895-905.
• [74]Biertümpfel C, Yang W, Suck D: Crystal structure of T4 endonuclease VII resolving a Holliday junction. Nature 2007, 449:616-620.
• [75]Sukackaite R, Grazulis S, Bochtler M, Siksnys V: The recognition domain of the BpuJI restriction endonuclease in complex with cognate DNA at 1.3-A resolution. J Mol Biol 2008, 378:1084-1093.
• [76]Deibert M, Grazulis S, Janulaitis A, Siksnys V, Huber R: Crystal structure of MunI restriction endonuclease in complex with cognate DNA at 1.7 A resolution. EMBO J 1999, 18:5805-5816.
• [77]van der Woerd MJ, Pelletier JJ, Xu S, Friedman AM: Restriction enzyme BsoBI-DNA complex: a tunnel for recognition of degenerate DNA sequences and potential histidine catalysis. Structure 2001, 9:133-144.
• [78]Newman M, Lunnen K, Wilson G, Greci J, Schildkraut I, Phillips SE: Crystal structure of restriction endonuclease BglI bound to its interrupted DNA recognition sequence. EMBO J 1998, 17:5466-5476.
• [79]Deibert M, Grazulis S, Sasnauskas G, Siksnys V, Huber R: Structure of the tetrameric restriction endonuclease NgoMIV in complex with cleaved DNA. Nat Struct Biol 2000, 7:792-799.
• [80]Huai Q, Colandene JD, Topal MD, Ke H: Structure of NaeI-DNA complex reveals dual-mode DNA recognition and complete dimer rearrangement. Nat Struct Biol 2001, 8:665-669.
• [81]Campbell EA, Muzzin O, Chlenov M, Sun JL, Olson CA, Weinman O, Trester-Zedlitz ML, Darst SA: Structure of the bacterial RNA polymerase promoter specificity sigma subunit. Mol Cell 2002, 9:527-539.
• [82]Hickman AB, Ronning DR, Perez ZN, Kotin RM, Dyda F: The nuclease domain of adeno-associated virus rep coordinates replication initiation using two distinct DNA recognition interfaces. Mol Cell 2004, 13:403-414.
• [83]Pascal JM, O'Brien PJ, Tomkinson AE, Ellenberger T: Human DNA ligase I completely encircles and partially unwinds nicked DNA. Nature 2004, 432:473-478.
• [84]Brissett NC, Pitcher RS, Juarez R, Picher AJ, Green AJ, Dafforn TR, Fox GC, Blanco L, Doherty AJ: Structure of a NHEJ polymerase-mediated DNA synaptic complex. Science 2007, 318:456-459.
• [85]Nandakumar J, Nair PA, Shuman S: Last stop on the road to repair: structure of E. coli DNA ligase bound to nicked DNA-adenylate. Mol Cell 2007, 26:257-271.
• [86]Dürr H, Körner C, Müller M, Hickmann V, Hopfner K: X-ray structures of the Sulfolobus solfataricus SWI2/SNF2 ATPase core and its complex with DNA. Cell 2005, 121:363-373.
• [87]Vanamee ES, Viadiu H, Kucera R, Dorner L, Picone S, Schildkraut I, Aggarwal AK: A view of consecutive binding events from structures of tetrameric endonuclease SfiI bound to DNA. EMBO J 2005, 24:4198-4208.
• [88]Kaus-Drobek M, Czapinska H, Sokołowska M, Tamulaitis G, Szczepanowski RH, Urbanke C, Siksnys V, Bochtler M: Restriction endonuclease MvaI is a monomer that recognizes its target sequence asymmetrically. Nucleic Acids Res 2007, 35:2035-2046.
• [89]Löwe J, Ellonen A, Allen MD, Atkinson C, Sherratt DJ, Grainge I: Molecular mechanism of sequence-directed DNA loading and translocation by FtsK. Mol Cell 2008, 31:498-509.
• [90]Golovenko D, Manakova E, Tamulaitiene G, Grazulis S, Siksnys V: Structural mechanisms for the 5'-CCWGG sequence recognition by the N- and C-terminal domains of EcoRII. Nucleic Acids Res 2009, 37:6613-6624.
• [91]Lambert AR, Sussman D, Shen B, Maunus R, Nix J, Samuelson J, Xu S, Stoddard BL: Structures of the rare-cutting restriction endonuclease NotI reveal a unique metal binding fold involved in DNA binding. Structure 2008, 16:558-569.
• [92]Georgescu RE, Kim S, Yurieva O, Kuriyan J, Kong X, O'Donnell M: Structure of a sliding clamp on DNA. Cell 2008, 132:43-54.