A novel extracellular metallopeptidase domain shared by animal Host-Associated mutualistic and pathogenic microbes

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Nakjang, Sirintra ^a   Ndeh, Didier A ^a   Wipat, Anil ^a,b   Bolam, David N ^a   Hirt, Robert P ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCAN; HYALURONIDASE; METALLOPROTEINASE; MUCIN;

ARTICLE; BACTERIAL COLONIZATION; BACTEROIDES THETAIOTAOMICRON; BINDING AFFINITY; CELL ANCHORAGE; COMMENSAL; CONTROLLED STUDY; ENTAMOEBA HISTOLYTICA; ENZYME SUBSTRATE; EUKARYOTE; GENETIC TRAIT; HOST PATHOGEN INTERACTION; IN VITRO STUDY; INTESTINE FLORA; MICROBIAL ACTIVITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PROKARYOTE; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN TARGETING; SIGNAL TRANSDUCTION; SYMBIOSIS; TRICHOMONAS VAGINALIS; ADAPTATION; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; COMPARATIVE STUDY; DIGESTIVE SYSTEM; ENZYMOLOGY; GENETICS; HUMAN; INVERTEBRATE; MICROBIOLOGY; MOLECULAR GENETICS; PATHOLOGY; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY;

ANIMALIA; BACTEROIDES THETAIOTAOMICRON; EUKARYOTA; INVERTEBRATA; MAMMALIA; PROKARYOTA; VERTEBRATA;

ADAPTATION, BIOLOGICAL; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; DIGESTIVE SYSTEM; HOST-PATHOGEN INTERACTIONS; HUMANS; INVERTEBRATES; METALLOPROTEASES; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; SYMBIOSIS;

EID: 84856407458     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0030287     Document Type: Article

References (87)

1. Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, et al. (2007) The human microbiome project. Nature 449: 804-810.
2. Sekirov I, Russell SL, Antunes LC, Finlay BB, (2010) Gut microbiota in health and disease. Physiol Rev 90: 859-904.
3. Ehrlich GD, Hiller NL, Hu FZ, (2008) What makes pathogens pathogenic. Genome Biol 9: 225.
4. Lebeer S, Vanderleyden J, De Keersmaecker SC, (2010) Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens. Nat Rev Microbiol 8: 171-184.
5. Tseng TT, Tyler BM, Setubal JC, (2009) Protein secretion systems in bacterial-host associations, and their description in the Gene Ontology. BMC Microbiol 9 (Suppl 1): S2.
6. Pallen MJ, Wren BW, (2007) Bacterial pathogenomics. Nature 449: 835-842.
7. Linden SK, Sutton P, Karlsson NG, Korolik V, McGuckin MA, (2008) Mucins in the mucosal barrier to infection. Mucosal Immunol 1: 183-197.
8. Cone RA, (2005) Mucus. In: Mestecky J, Lamm ME, McGhee JR, Bienenstock J, Mayer L, editors. Mucosal Immunology. 3rd ed Burlington Elsevier pp. 49-72.
9. Johansson ME, Larsson JM, Hansson GC, (2011) The two mucus layers of colon are organized by the MUC2 mucin, whereas the outer layer is a legislator of host-microbial interactions. Proceedings of the National Academy of Sciences of the United States of America 108 (Suppl 1): 4659-4665.
10. Wiggins R, Hicks SJ, Soothill PW, Millar MR, Corfield AP, (2001) Mucinases and sialidases: their role in the pathogenesis of sexually transmitted infections in the female genital tract. Sex Transm Infect 77: 402-408.
11. Korbel JO, Doerks T, Jensen LJ, Perez-Iratxeta C, Kaczanowski S, et al. (2005) Systematic association of genes to phenotypes by genome and literature mining. PLoS Biol 3: e134.
12. Liu Y, Li J, Sam L, Goh CS, Gerstein M, et al. (2006) An integrative genomic approach to uncover molecular mechanisms of prokaryotic traits. PLoS Comput Biol 2: e159.
13. Read TD, Myers GS, Brunham RC, Nelson WC, Paulsen IT, et al. (2003) Genome sequence of Chlamydophila caviae (Chlamydia psittaci GPIC): examining the role of niche-specific genes in the evolution of the Chlamydiaceae. Nucleic Acids Research 31: 2134-2147.
14. O'Sullivan O, O'Callaghan J, Sangrador-Vegas A, McAuliffe O, Slattery L, et al. (2009) Comparative genomics of lactic acid bacteria reveals a niche-specific gene set. BMC Microbiology 9: 50.
15. Liolios K, Chen IM, Mavromatis K, Tavernarakis N, Hugenholtz P, et al. (2010) The Genomes On Line Database (GOLD) in 2009: status of genomic and metagenomic projects and their associated metadata. Nucleic Acids Res 38: D346-354.
16. Medini D, Serruto D, Parkhill J, Relman DA, Donati C, et al. (2008) Microbiology in the post-genomic era. Nat Rev Microbiol 6: 419-430.
17. Ellrott K, Jaroszewski L, Li W, Wooley JC, Godzik A, (2010) Expansion of the protein repertoire in newly explored environments: human gut microbiome specific protein families. PLoS Comput Biol 6: e1000798.
18. Clark CG, Alsmark UC, Tazreiter M, Saito-Nakano Y, Ali V, et al. (2007) Structure and content of the Entamoeba histolytica genome. Adv Parasitol 65: 51-190.
19. Loftus B, Anderson I, Davies R, Alsmark UC, Samuelson J, et al. (2005) The genome of the protist parasite Entamoeba histolytica. Nature 433: 865-868.
20. Carlton JM, Hirt RP, Silva JC, Delcher AL, Schatz M, et al. (2007) Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science 315: 207-212.
21. Carlton JM, Malik SB, Sullivan SA, Sicheritz-Ponten T, Tang P, et al. (2010) The genome of Trichomonas vaginalis. In: Clark CG, Johnson PJ, Adam RD, editors. Anaerobic Parasitic Protozoa: Genomics and Molecular Biology: Caister Academic Press pp. 45-77.
22. Alsmark UC, Sicheritz-Ponten T, Foster PG, Hirt RP, Embley TM, (2009) Horizontal gene transfer in eukaryotic parasites: a case study of Entamoeba histolytica and Trichomonas vaginalis. Methods Mol Biol 532: 489-500.
23. Hirt RP, Noel CJ, Sicheritz-Ponten T, Tachezy J, Fiori PL, (2007) Trichomonas vaginalis surface proteins: a view from the genome. Trends Parasitol 23: 540-547.
24. Noel CJ, Diaz N, Sicheritz-Ponten T, Safarikova L, Tachezy J, et al. (2010) Trichomonas vaginalis vast BspA-like gene family: evidence for functional diversity from structural organisation and transcriptomics. BMC Genomics 11: 99.
25. de Miguel N, Lustig G, Twu O, Chattopadhyay A, Wohlschlegel JA, et al. (2010) Proteome analysis of the surface of Trichomonas vaginalis reveals novel proteins and strain-dependent differential expression. Mol Cell Proteomics 9: 1554-1566.
26. Edman U, Meraz MA, Rausser S, Agabian N, (1990) Characterization of an immuno-dominant variable surface antigen from pathogenic and nonpathogenic Entamoeba histolytica. Journal of Experimental Medicine.
27. Marquay Markiewicz J, Syan S, Hon CC, Weber C, Faust D, et al. (2011) A Proteomic and Cellular Analysis of Uropods in the Pathogen Entamoeba histolytica. PLoS Negl Trop Dis 5: e1002.
28. Marion S, Guillén N, (2006) Genomic and proteomic approaches highlight phagocytosis of living and apoptotic human cells by the parasite Entamoeba histolytica. International Journal for Parasitology 36: 131-139.
29. Okada M, Huston CD, Mann BJ, Petri WA Jr, Kita K, et al. (2005) Proteomic analysis of phagocytosis in the enteric protozoan parasite Entamoeba histolytica. Eukaryot Cell 4: 827-831.
30. Boraston AB, Bolam DN, Gilbert HJ, Davies GJ, (2004) Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem J 382: 769-781.
31. Guillen D, Sanchez S, Rodriguez-Sanoja R, (2010) Carbohydrate-binding domains: multiplicity of biological roles. Appl Microbiol Biotechnol 85: 1241-1249.
32. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, et al. (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 37: D233-238.
33. Sasaki Y, Ishikawa J, Yamashita A, Oshima K, Kenri T, et al. (2002) The complete genomic sequence of Mycoplasma penetrans, an intracellular bacterial pathogen in humans. Nucleic Acids Res 30: 5293-5300.
34. Brynestad S, Granum PE, (2002) Clostridium perfringens and foodborne infections. Int J Food Microbiol 74: 195-202.
35. Hunter S, Apweiler R, Attwood TK, Bairoch A, Bateman A, et al. (2009) InterPro: the integrative protein signature database. Nucleic Acids Res 37: D211-215.
36. Hooper NM, (1994) Families of zinc metalloproteases. FEBS letters 354: 1-6.
37. Lepore LS, Roelvink PR, Granados RR, (1996) Enhancin, the granulosis virus protein that facilitates nucleopolyhedrovirus (NPV) infections, is a metalloprotease. J Invertebr Pathol 68: 131-140.
38. Wang P, Granados RR, (1997) An intestinal mucin is the target substrate for a baculovirus enhancin. Proc Natl Acad Sci USA 94: 6977-6982.
39. Rawlings ND, Barrett AJ, Bateman A, (2010) MEROPS: the peptidase database. Nucleic Acids Res 38: D227-233.
40. Derrien M, Collado MC, Ben-Amor K, Salminen S, de Vos WM, (2008) The Mucin degrader Akkermansia muciniphila is an abundant resident of the human intestinal tract. Appl Environ Microbiol 74: 1646-1648.
41. Abbott DW, Eirín-López JM, Boraston AB, (2008) Insight into ligand diversity and novel biological roles for family 32 carbohydrate-binding modules. Mol Biol Evol 25: 155-167.
42. Gregg KJ, Finn R, Abbott DW, Boraston AB, (2008) Divergent modes of glycan recognition by a new family of carbohydrate-binding modules. J Biol Chem 283: 12604-12613.
43. Swiecicka I, (2008) Natural occurrence of Bacillus thuringiensis and Bacillus cereus in eukaryotic organisms: a case for symbiosis. Biocontrol Science and Technology 18: 221-239.
44. Mello LV, Chen X, Rigden DJ, (2010) Mining metagenomic data for novel domains: BACON, a new carbohydrate-binding module. FEBS Lett 584: 2421-2426.
45. Rigden DJ, Mello LV, Galperin MY, (2004) The PA14 domain, a conserved all-beta domain in bacterial toxins, enzymes, adhesins and signaling molecules. Trends Biochem Sci 29: 335-339.
46. Martens EC, Chiang HC, Gordon JI, (2008) Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont. Cell Host Microbe 4: 447-457.
47. Fang S, Wang L, Guo W, Zhang X, Peng D, et al. (2009) Bacillus thuringiensis bel protein enhances the toxicity of Cry1Ac protein to Helicoverpa armigera larvae by degrading insect intestinal mucin. Appl Environ Microbiol 75: 5237-5243.
48. Wang P, Granados RR, (2001) Molecular structure of the peritrophic membrane (PM): identification of potential PM target sites for insect control. Arch Insect Biochem Physiol 47: 110-118.
49. Pearson JP, Brownlee IA, (2005) Structure and function of mucosal surfaces. In: Nataro JP, Cohen PS, Mobley HLT, Weiser JN, editors. Colonization of mucosal surfaces Washington DC ASM Press pp. 3-16.
50. Auld DS, (1995) Removal and replacement of metal ions in metallopeptidases. Methods Enzymol 248: 228-242.
51. Szabady RL, Yanta JH, Halladin DK, Schofield MJ, Welch RA, (2011) TagA is a secreted protease of Vibrio cholerae that specifically cleaves mucin glycoproteins. Microbiology 157: 516-525.
52. Brockhausen I, Schachter H, Stanley P, (2009) O-GalNAc Glycans. In: Varki A, Cummings RD, Esko JD, Freeze HH, Stanley P, editors. Essentials of Glycobiology. 2nd ed Cold Spring Harbor Cold Spring Harbor Laboratory Press pp. 115-128.
53. Peterson KM, (2002) Expression of Vibrio cholerae virulence genes in response to environmental signals. Curr Issues Intest Microbiol 3: 29-38.
54. Parsot C, Taxman E, Mekalanos JJ, (1991) ToxR regulates the production of lipoproteins and the expression of serum resistance in Vibrio cholerae. Proc Natl Acad Sci U S A 88: 1641-1645.
55. Senderovich Y, Izhaki I, Halpern M, (2010) Fish as reservoirs and vectors of Vibrio cholerae. PLoS One 5: e8607.
56. Hazen TH, Pan L, Gu JD, Sobecky PA, (2010) The contribution of mobile genetic elements to the evolution and ecology of Vibrios. FEMS Microbiol Ecol 74: 485-499.
57. Kaper JB, Nataro JP, Mobley HL, (2004) Pathogenic Escherichia coli. Nat Rev Microbiol 2: 123-140.
58. Money P, Kelly AF, Gould SW, Denholm-Price J, Threlfall EJ, et al. (2010) Cattle, weather and water: mapping Escherichia coli O157:H7 infections in humans in England and Scotland. Environ Microbiol 12: 2633-2644.
59. Sonnenburg ED, Zheng H, Joglekar P, Higginbottom SK, Firbank SJ, et al. (2010) Specificity of polysaccharide use in intestinal bacteroides species determines diet-induced microbiota alterations. Cell 141: 1241-1252.
60. Xu J, Mahowald MA, Ley RE, Lozupone CA, Hamady M, et al. (2007) Evolution of symbiotic bacteria in the distal human intestine. PLoS Biol 5: e156.
61. Farthing MJ, (2006) Treatment options for the eradication of intestinal protozoa. Nat Clin Pract Gastroenterol Hepatol 3: 436-445.
62. Hobbs MM, Seña AC, Swygard H, Schwekke JR, (2007) Trichomonas vaginalis and trichomononisasis. In: Holmes K, Sparling S, Stamm W, Piot P, Wasserheit J, editors. Sexually transmitted diseases. 4th ed McGraw-Hill Professional pp. 771-794.
63. Davis PH, Chen M, Zhang X, Clark CG, Townsend RR, et al. (2009) Proteomic comparison of Entamoeba histolytica and Entamoeba dispar and the role of E. histolytica alcohol dehydrogenase 3 in virulence. PLoS Negl Trop Dis 3: e415.
64. Pereira-Neves A, Benchimol M, (2007) Phagocytosis by Trichomonas vaginalis: new insights. Biol Cell 99: 87-101.
65. de Groot PW, Klis FM, (2008) The conserved PA14 domain of cell wall-associated fungal adhesins governs their glycan-binding specificity. Mol Microbiol 68: 535-537.
66. Songer JG, (2010) Clostridia as agents of zoonotic disease. Vet Microbiol 140: 399-404.
67. Qin X, Evans JD, Aronstein KA, Murray KD, Weinstock GM, (2006) Genome sequences of the honey bee pathogens Paenibacillus larvae and Ascosphaera apis. Insect Mol Biol 15: 715-718.
68. Heermann R, Fuchs TM, (2008) Comparative analysis of the Photorhabdus luminescens and the Yersinia enterocolitica genomes: uncovering candidate genes involved in insect pathogenicity. BMC Genomics 9: 40.
69. Zhang JC, Sun L, Nie QH, (2010) Botulism, where are we now? Clin Toxicol (Phila) 48: 867-879.
70. Brun E, Moriaud F, Gans P, Blackledge MJ, (1997) Solution structure of the cellulose-binding domain of the Endoglucanase Z secreted by Erwinia chrysanthemi. Biochemistry.
71. Ikegami T, Okada T, Hashimoto M, Seino S, (2000) Solution structure of the chitin-binding domain of Bacillus circulans WL-12 chitinase A1. Journal of Biological Chemistry.
72. Antúnez K, Anido M, Schlapp G, Evans JD, Zunino P, (2009) Characterization of secreted proteases of Paenibacillus larvae, potential virulence factors involved in honeybee larval infection. J Invertebr Pathol 102: 129-132.
73. Stenfors Arnesen LP, Fagerlund A, Granum PE, (2008) From soil to gut: Bacillus cereus and its food poisoning toxins. FEMS Microbiol Rev 32: 579-606.
74. Wilkinson M, McInerney JO, Hirt RP, Foster PG, Embley TM, (2007) Of clades and clans: terms for phylogenetic relationships in unrooted trees. Trends in ecology & evolution 22: 114-115.
75. Goulas T, Arolas JL, Gomis-Ruth FX, (2011) Structure, function and latency regulation of a bacterial enterotoxin potentially derived from a mammalian adamalysin/ADAM xenolog. Proc Natl Acad Sci U S A 108: 1856-1861.
76. Cerda-Costa N, Guevara T, Karim AY, Ksiazek M, Nguyen KA, et al. (2011) The structure of the catalytic domain of Tannerella forsythia karilysin reveals it is a bacterial xenologue of animal matrix metalloproteinases. Mol Microbiol 79: 119-132.
77. Vilcinskas A, (2010) Coevolution between pathogen-derived proteinases and proteinase inhibitors of host insects. Virulence 1: 206-214.
78. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
79. Finn RD, Mistry J, Tate J, Coggill P, Heger A, et al. (2010) The Pfam protein families database. Nucleic Acids Res 38: D211-222.
80. Gouy M, Guindon S, Gascuel O, (2010) SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27: 221-224.
81. Dyrlovbendtsen J, (2004) Improved Prediction of Signal Peptides: SignalP 3.0. Journal of Molecular Biology 340: 783-795.
82. Krogh A, Larsson B, von Heijne G, Sonnhammer ELL, (2001) Predicting transmembrane protein topology with a hidden markov model: application to complete genomes. Journal of Molecular Biology 305: 567-580.
83. Kall L, Krogh A, Sonnhammer EL, (2005) An HMM posterior decoder for sequence feature prediction that includes homology information. Bioinformatics 21 (Suppl 1): i251-257.
84. Söding J, Biegert A, Lupas AN, (2005) The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Research 33: W244-248.
85. Frickey T, Lupas A, (2004) CLANS: a Java application for visualizing protein families based on pairwise similarity. Bioinformatics 20: 3702-3704.
86. Bolam DN, Xie H, Pell G, Hogg D, Galbraith G, et al. (2004) X4 modules represent a new family of carbohydrate-binding modules that display novel properties. J Biol Chem 279: 22953-22963.
87. Letunic I, Bork P, (2011) Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic acids research.