Structure and computational analysis of a novel protein with metallopeptidase-like and circularly permuted winged-helix-turn-helix domains reveals a possible role in modified polysaccharide biosynthesis

BMC Bioinformatics

Volumn 15, Issue 1, 2014, Pages

  Das, Debanu ^a,b   Murzin, Alexey G ^c   Rawlings, Neil D ^d,e   Finn, Robert D ^f   Coggill, Penelope ^d,e   Bateman, Alex ^e   Godzik, Adam ^a,g   Aravind, L ^h  

^a Joint Center for Structural Genomics   (United States)

^b SLAC NATIONAL ACCELERATOR LABORATORY   (United States)

^c MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^d WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^e WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^f HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^g BURNHAM INSTITUTE   (United States)

^h NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

CA_C2195; DUF2172; DUF4910; HTH_47; Peptidase; Structural genomics

Indexed keywords

BIOCHEMISTRY; BIOSYNTHESIS; CRYSTAL STRUCTURE;

CA_C2195; DUF2172; DUF4910; HTH_47; PEPTIDASE; STRUCTURAL GENOMICS;

PROTEINS;

BACTERIAL PROTEIN; METALLOPROTEINASE;

ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; CLOSTRIDIUM ACETOBUTYLICUM; ENZYMOLOGY; GENETICS; METABOLISM; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

BACTERIAL PROTEINS; CLOSTRIDIUM ACETOBUTYLICUM; CRYSTALLOGRAPHY, X-RAY; METALLOPROTEASES; MODELS, MOLECULAR; PROTEIN STRUCTURE, TERTIARY;

EID: 84899099152     PISSN: None     EISSN: 14712105     Source Type: Journal    
DOI: 10.1186/1471-2105-15-75     Document Type: Article

References (50)

1. Altschul SF, Madden TL, Schaffer 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(17):3389-3402. 10.1093/nar/25.17.3389, 146917, 9254694.
2. Dessailly BH, Nair R, Jaroszewski L, Fajardo JE, Kouranov A, Lee D, Fiser A, Godzik A, Rost B, Orengo C. PSI-2: structural genomics to cover protein domain family space. Structure 2009, 17(6):869-881. 10.1016/j.str.2009.03.015, 2920419, 19523904.
3. Norvell JC, Berg JM. Update on the protein structure initiative. Structure 2007, 15(12):1519-1522. 10.1016/j.str.2007.11.004, 18073099.
4. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer EL, Tate J, Punta M. Pfam: the protein families database. Nucleic Acids Res 2014, 42(1):D222-D230.
5. Rowsell S, Pauptit RA, Tucker AD, Melton RG, Blow DM, Brick P. Crystal structure of carboxypeptidase G2, a bacterial enzyme with applications in cancer therapy. Structure 1997, 5(3):337-347. 10.1016/S0969-2126(97)00191-3, 9083113.
6. Bitto E, Bingman CA, Wesenberg GE, McCoy JG, Phillips GN. Structure of aspartoacylase, the brain enzyme impaired in Canavan disease. Proc Natl Acad Sci USA 2007, 104(2):456-461. 10.1073/pnas.0607817104, 1766406, 17194761.
7. Rawlings ND, Barrett AJ. Introduction: metallopeptidases and their clans. Handbook of Proteolytic Enzymes 2013, 325-370. Amsterdam: Elsevier, Rawlings ND, Salvesen GS, 3.
8. Auld DS. Catalytic Mechanisms for metallopeptidases. Handbook of Proteolytic Enzymes 2013, 370-396. Amsterdam: Elsevier, Rawlings ND, Salvesen GS, 3.
9. Rawlings ND, Barrett AJ, Bateman A. MEROPS: the database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res 2012, 40(Database issue):D343-D350. 3245014, 22086950.
10. Hermann JC, Marti-Arbona R, Fedorov AA, Fedorov E, Almo SC, Shoichet BK, Raushel FM. Structure-based activity prediction for an enzyme of unknown function. Nature 2007, 448(7155):775-779. 10.1038/nature05981, 2254328, 17603473.
11. Das D, Lee WS, Grant JC, Chiu HJ, Farr CL, Vance J, Klock HE, Knuth MW, Miller MD, Elsliger MA, Deacon AM, Godzik A, Lesley SA, Kornfeld S, Wilson IA. Structure and function of the DUF2233 domain in bacteria and in the human mannose 6-phosphate uncovering enzyme. J biol Chem 2013, 288(23):16789-16799. 10.1074/jbc.M112.434977, 23572527.
12. Das D, Hervé M, Feuerhelm J, Farr CL, Chiu HJ, Elsliger MA, Knuth MW, Klock HE, Miller MD, Godzik A, Lesley SA, Deacon AM, Mengin-Lecreulx D, Wilson IA. Structure and function of the first full-length murein peptide ligase (Mpl) cell wall recycling protein. PLoS One 2011, 6(3):e17624. 10.1371/journal.pone.0017624, 3060825, 21445265.
13. Das D, Moiani D, Axelrod HL, Miller MD, McMullan D, Jin KK, Abdubek P, Astakhova T, Burra P, Carlton D, Chiu HJ, Clayton T, Deller MC, Duan L, Ernst D, Feuerhelm J, Grant JC, Grzechnik A, Grzechnik SK, Han GW, Jaroszewski L, Klock HE, Knuth MW, Kozbial P, Krishna SS, Kumar A, Marciano D, Morse AT, Nigoghossian E, Okach L, et al. Crystal structure of the first eubacterial Mre11 nuclease reveals novel features that may discriminate substrates during DNA repair. J Mol Biol 2010, 397(3):647-663. 10.1016/j.jmb.2010.01.049, 2839085, 20122942.
14. Das D, Hyun H, Lou Y, Yokota H, Kim R, Kim SH. Crystal structure of a novel single-stranded DNA binding protein from Mycoplasma pneumoniae. Proteins 2007, 67(3):776-782. 10.1002/prot.21340, 17348019.
15. Shin DH, Hou J, Chandonia JM, Das D, Choi IG, Kim R, Kim SH. Structure-based inference of molecular functions of proteins of unknown function from Berkeley Structural Genomics Center. J Struct Funct Genomics 2007, 8(2-3):99-105.
16. Goodacre NF, Gerloff DL, Uetz P. Protein domains of unknown function are essential in bacteria. mBio 2013, 5(1):e00744-13. doi:10.1128/mBio.00744-13, 3884060, 24381303.
17. Diederichs K, Karplus PA. Improved R-factors for diffraction data analysis in macromolecular crystallography. Nat Struct Biol 1997, 4(4):269-275. 10.1038/nsb0497-269, 9095194.
18. Cruickshank DW. Remarks about protein structure precision. Acta Crystallogr D Biol Crystallogr 1999, 55(Pt 3):583-601.
19. Weiss MS, Hilgenfeld R. On the use of the merging R factor as a quality indicator for X-ray data. J Appl Crystallogr 1997, 30:203-205.
20. Weiss MS, Metzner HJ, Hilgenfeld R. Two non-proline cis peptide bonds may be important for factor XIII function. FEBS Lett 1998, 423(3):291-296. 10.1016/S0014-5793(98)00098-2, 9515726.
21. Krissinel E, Henrick K. Inference of macromolecular assemblies from crystalline state. J Mol Biol 2007, 372(3):774-797. 10.1016/j.jmb.2007.05.022, 17681537.
22. Krissinel E, Henrick K. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr D Biol Crystallogr 2004, 60(Pt 12 Pt 1):2256-2268.
23. Aravind L, Anantharaman V, Balaji S, Babu MM, Iyer LM. The many faces of the helix-turn-helix domain: transcription regulation and beyond. FEMS Microbiol Rev 2005, 29(2):231-262.
24. Andreeva A, Howorth D, Chandonia JM, Brenner SE, Hubbard TJ, Chothia C, Murzin AG. Data growth and its impact on the SCOP database: new developments. Nucleic Acids Res 2008, 36(Database issue):D419-D425. 2238974, 18000004.
25. Botelho TO, Guevara T, Marrero A, Arede P, Fluxa VS, Reymond JL, Oliveira DC, Gomis-Ruth FX. Structural and functional analyses reveal that Staphylococcus aureus antibiotic resistance factor HmrA is a zinc-dependent endopeptidase. J Biol Chem 2011, 286(29):25697-25709. 10.1074/jbc.M111.247437, 3138305, 21622555.
26. Schilling S, Cynis H, von Bohlen A, Hoffmann T, Wermann M, Heiser U, Buchholz M, Zunkel K, Demuth HU. Isolation, catalytic properties, and competitive inhibitors of the zinc-dependent murine glutaminyl cyclase. Biochemistry 2005, 44(40):13415-13424. 10.1021/bi051142e, 16201766.
27. Cheng Y, Zak O, Aisen P, Harrison SC, Walz T. Structure of the human transferrin receptor-transferrin complex. Cell 2004, 116(4):565-576. 10.1016/S0092-8674(04)00130-8, 14980223.
28. Luo X, Hofmann K. The protease-associated domain: a homology domain associated with multiple classes of proteases. Trends Biochem Sci 2001, 26(3):147-148. 10.1016/S0968-0004(00)01768-0, 11246007.
29. Finn RD, Clements J, Eddy SR. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 2011, 39(Web Server issue):W29-W37. 3125773, 21593126.
30. Liu S, Widom J, Kemp CW, Crews CM, Clardy J. Structure of human methionine aminopeptidase-2 complexed with fumagillin. Science 1998, 282(5392):1324-1327.
31. Aravind L. Guilt by association: contextual information in genome analysis. Genome Res 2000, 10(8):1074-1077. 10.1101/gr.10.8.1074, 10958625.
32. Huynen M, Snel B, Lathe W, Bork P. Predicting protein function by genomic context: quantitative evaluation and qualitative inferences. Genome Res 2000, 10(8):1204-1210. 10.1101/gr.10.8.1204, 310926, 10958638.
33. Overbeek R, Begley T, Butler RM, Choudhuri JV, Chuang HY, Cohoon M, de Crécy-Lagard V, Diaz N, Disz T, Edwards R, Fonstein M, Frank ED, Gerdes S, Glass EM, Goesmann A, Hanson A, Iwata-Reuyl D, Jensen R, Jamshidi N, Krause L, Kubal M, Larsen N, Linke B, McHardy AC, Meyer F, Neuweger H, Olsen G, Olson R, Osterman A, Portnoy V, et al. The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res 2005, 33(17):5691-5702. 10.1093/nar/gki866, 1251668, 16214803.
34. Kall L, Krogh A, Sonnhammer EL. Advantages of combined transmembrane topology and signal peptide prediction--the Phobius web server. Nucleic Acids Res 2007, 35(Web Server issue):W429-W432. 1933244, 17483518.
35. Petersen TN, Brunak S, von Heijne G, Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 2011, 8(10):785-786. 10.1038/nmeth.1701, 21959131.
36. Klock HE, Koesema EJ, Knuth MW, Lesley SA. Combining the polymerase incomplete primer extension method for cloning and mutagenesis with microscreening to accelerate structural genomics efforts. Proteins 2008, 71(2):982-994. 10.1002/prot.21786, 18004753.
37. Lesley SA, Kuhn P, Godzik A, Deacon AM, Mathews I, Kreusch A, Spraggon G, Klock HE, McMullan D, Shin T, Vincent J, Robb A, Brinen LS, Miller MD, McPhillips TM, Miller MA, Scheibe D, Canaves JM, Guda C, Jaroszewski L, Selby TL, Elsliger MA, Wooley J, Taylor SS, Hodgson KO, Wilson IA, Schultz PG, Stevens RC. Structural genomics of the Thermotoga maritima proteome implemented in a high-throughput structure determination pipeline. Proc Natl Acad Sci USA 2002, 99(18):11664-11669. 10.1073/pnas.142413399, 129326, 12193646.
38. Elsliger MA, Deacon AM, Godzik A, Lesley SA, Wooley J, Wuthrich K, Wilson IA. The JCSG high-throughput structural biology pipeline. Acta Crystallogr Sect F: Struct Biol Cryst Commun 2010, 66(Pt 10):1137-1142. 2954196, 20944202.
39. McPhillips TM, McPhillips SE, Chiu HJ, Cohen AE, Deacon AM, Ellis PJ, Garman E, Gonzalez A, Sauter NK, Phizackerley RP, Soltis SM, Kuhn P. Blu-Ice and the Distributed Control System: software for data acquisition and instrument control at macromolecular crystallography beamlines. J Synchrotron Radiat 2002, 9(Pt 6):401-406.
40. Collaborative Computing Project The CCP4 suite: programs for protein crystallography. Acta Crystallogr. Sect. D Biol. Crystallogr 1994, 50:760-763. Collaborative Computing Project.
41. Collaborative Computing Project N The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 1994, 50(Pt 5):760-763. Collaborative Computing Project N.
42. Sheldrick GM. A short history of SHELX. Acta Crystallogr A 2008, 64(Pt 1):112-122.
43. Vonrhein C, Blanc E, Roversi P, Bricogne G. Automated structure solution with autoSHARP. Methods Mol Biol 2007, 364:215-230.
44. Langer G, Cohen SX, Lamzin VS, Perrakis A. Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat Protoc 2008, 3(7):1171-1179. 10.1038/nprot.2008.91, 2582149, 18600222.
45. Winn MD, Murshudov GN, Papiz MZ. Macromolecular TLS refinement in REFMAC at moderate resolutions. Methods Enzymol 2003, 374:300-321.
46. Emsley P, Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 2004, 60(Pt 12 Pt 1):2126-2132.
47. Ashkenazy H, Erez E, Martz E, Pupko T, Ben-Tal N. ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res 2010, 38(Web Server issue):W529-W533. 2896094, 20478830.
48. DeLano WL. The PyMOL Molecular Graphics System 2008, Palo Alto, CA, USA: DeLano Scientific LLC.
49. Laskowski RA. PDBsum new things. Nucleic Acids Res 2009, 37(Database issue):D355-D359. 2686501, 18996896.
50. Schaffer AA, Wolf YI, Ponting CP, Koonin EV, Aravind L, Altschul SF. IMPALA: matching a protein sequence against a collection of PSI-BLAST-constructed position-specific score matrices. Bioinformatics 1999, 15(12):1000-1011. 10.1093/bioinformatics/15.12.1000, 10745990.