Structural Basis of the Novel S. pneumoniae Virulence Factor, GHIP, a Glycosyl Hydrolase 25 Participating in Host-Cell Invasion

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Niu, Siqiang ^a   Luo, Miao ^a   Tang, Jian ^a   Zhou, Hua ^a   Zhang, Yangli ^a   Min, Xun ^a   Cai, Xuefei ^a   Zhang, Wenlu ^a   Xu, Wenchu ^a   Li, Defeng ^b   Ding, Jingjin ^b   Hu, Yonglin ^b   Wang, Dacheng ^b   Huang, Ailong ^a   Yin, Yibin ^a   Wang, Deqiang ^a  

^a CHONGQING MEDICAL UNIVERSITY   (China)

^b INSTITUTE OF BIOPHYSICS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOSIDASE; N ACETYLGLUCOSAMINE; VIRULENCE FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL VIRULENCE; CELL INVASION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG TARGETING; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME SPECIFICITY; EPITHELIUM CELL; FEMALE; HOST CELL; HUMAN; HUMAN CELL; HYDROLYSIS; MOUSE; NASOPHARYNX; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN FOLDING; PROTEIN STRUCTURE; STREPTOCOCCUS PNEUMONIAE;

EID: 84880727233     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068647     Document Type: Article

References (57)

1. Kadioglu A, Weiser J, Paton JC, Andrew PW, (2008) The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nat Rev Microbiol 6: 288-301.
2. Mook-Kanamori BB, Geldhoff M, van der Poll T, van de Beek D, (2011) Pathogenesis and pathophysiology of pneumococcal meningitis. Clin Microbiol Rev 24: 557-591.
3. Hava DL, Camilli A, (2002) Large-scale identification of serotype 4 Streptococcus pneumoniae virulence factors. Mol Microbiol 45: 1389-1406.
4. Coutinho PM, Henrissat B (1999) Carbohydrate-active enzymes: an integrated database approach. In Recent Advances in Carbohydrate Bioengineering (Gilbert, H. J., Davies G, Henrissat B, Svensson B, eds.), 3-12, The Royal Society of Chemistry, Cambridge.
5. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B, (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 37: D233-238.
6. Rau A, Hogg T, Marquardt R, Hilgenfeld R, (2001) A new lysozyme fold crystal structure of the muramidase from Streptomyces coelicolor at 1.65 Å resolution. J Biol Chem 276: 31994-31999.
7. Wohlkönig A, Huet J, Looze Y, Wintjens R, (2010) Structural relationships in the lysozyme superfamily: significant evidence for glycoside hydrolase signature motifs. PLoS One 5: e15388.
8. Frias MJ, Melo-Cristino J, Ramirez M, (2009) The autolysin LytA contributes to efficient bacteriophage progeny release in Streptococcus pneumoniae. J Bacteriol 191: 5428-5440.
9. Mellroth P, Daniels R, Eberhardt A, Rönnlund D, Blom H, et al. (2012) LytA, the major autolysin of Streptococcus pneumoniae, requires access to the nascent peptidoglycan. J Biol Chem [Epub ahead of print].
10. Ramos-Sevillano E, Moscoso M, García P, García E, Yuste J, (2011) Nasopharyngeal colonization and invasive disease are enhanced by the cell wall hydrolases LytB and LytC of Streptococcus pneumoniae. PLoS One 6: e23626.
11. Pérez-Dorado I, Campillo NE, Monterroso B, Hesek D, Lee M, et al. (2007) Elucidation of the molecular recognition of bacterial cell wall by modular pneumococcal phage endolysin CPL-1. J Biol Chem 282: 24990-24999.
12. Hermoso JA, Monterroso B, Albert A, Galán B, Ahrazem O, et al. (2003) Structural basis for selective recognition of pneumococcal cell wall by modular endolysin from phage Cp-1. Structure 11: 1239-1249.
13. Pérez-Dorado I, González A, Morales M, Sanles R, Striker W, et al. (2012) Group A streptococcus adheres to pharyngeal epithelial cells with salivary proline-rich proteins via GrpE chaperone protein. Nat Struct Mol Biol 17: 576-581.
14. Hammerschmidt S, (2006) Adherence molecules of pathogenic pneumococci. Curr Opin Microbiol 9: 12-20.
15. Gamez G, Hammerschmidt S, (2012) Combat pneumococcal infections: adhesins as candidates for protein- based vaccine development. Curr Drug Targets 13: 323-337.
16. Bergmann S, Hammerschmidt S, (2006) Versatility of pneumococcal surface proteins. Microbiology 152: 295-303.
17. Bergmann S, Lang A, Rohde M, Agarwal V, Rennemeier C, et al. (2009) Integrin-linked kinase is required for vitronectin-mediated internalization of Streptococcus pneumoniae by host cells. J Cell Sci 122: 256-267.
18. Agarwal V, Asmat TM, Luo S, Jensch I, Zipfel PF, et al. (2010) Complement regulator Factor H mediates a two-step uptake of Streptococcus pneumoniae by human cells. J Biol Chem 285: 23486-23495.
19. Porter CJ, Schuch R, Pelzek AJ, Buckle AM, McGowan S, et al. (2007) The 1.6 A crystal structure of the catalytic domain of PlyB, a bacteriophage lysin active against Bacillus anthracis. J Mol Biol 366: 540-550.
20. Kim YG, Kim JH, Kim KJ, (2009) Crystal structure of the Salmonella enterica serovar typhimurium virulence factor SrfJ, a glycoside hydrolase family enzyme. J Bacteriol 191: 6550-6554.
21. Martinez-Fleites C, Korczynska JE, Davies GJ, Cope MJ, Turkenburg JP, et al. (2009) The crystal structure of a family GH25 lysozyme from Bacillus anthracis implies a neighboring-group catalytic mechanism with retention of anomeric configuration. Carbohydr Res 344: 1753-1757.
22. Song L, Zeng M, Liao W, Zhang L, Mo H, et al. (2006) Bmi-1 is a novel molecular marker of nasopharyngeal carcinoma progression and immortalizes primary human nasopharyngeal epithelial cells. Cancer Res. 66: 6225-6232.
23. Niu S, Luo M, Huang A, Yin Y, Wang D, (2010) Purification, crystallization and preliminary X-ray studies of the putative lysozyme SP0987 from Streptococcus pneumoniae. Acta Crystallogr Sect F Struct Biol Cryst Commun 66: 286-288.
24. Otwinowski Z, Minor W, (1997) Processing of X-ray Diffraction Data Collected in Oscillation Mode. Methods in Enzymology 276: 307-326.
25. Leslie AGW (1992) Recent changes to the MOSFLM package for processing film and image plate data. Joint CCP4 and ESF-EACMB newsletter on protein crystallography: Daresbury Laboratory, Warrington, UK.
26. Terwilliger TC, Berendzen J, (1999) Bayesian correlated MAD phasing. Acta Crystallogr D Biol Crystallogr 53: 571-579.
27. Terwilliger TC, (2000) Maximum likelihood density modification. Acta Crystallogr D Biol Crystallogr 56: 965-972.
28. Murshudov GN, Skubák P, Lebedev AA, Pannu NS, Steiner RA, et al. (2011) REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr D Biol Crystallogr 67: 355-367.
29. Potterton E, Briggs P, Turkenburg M, Dodson E, (2003) A graphical user interface to the CCP4 program suite. Crystallogr D Biol Crystallogr 59: 1131-1137.
30. Laskowski RA, MacArthur MW, Moss DS, Thornton JM, (1993) PROCHECK: a program to check the stereochemical quality of protein structures J. Appl. Cryst 26: 283-291.
31. DeLano WL (2004) The PyMOL user's manual. San Carlos, CA: Delano Scientific.
32. Nanjo F, Sakai K, Usui T, (1988) p-Nitrophenyl Penta-N-Acetyl-β- Chitopentaoside as a Novel Synthetic Substrate for the Colorimetric Assay of Lysozyme. J. Biochem 104: 255-258.
33. Eberhardt A, Wu LJ, Errington J, Vollmer W, Veening JW, (2009) Cellular localization of choline-utilization proteins in Streptococcus pneumoniae using novel fluorescent reporter systems. Mol Microbiol 74: 395-408.
34. Wu K, Zhang X, Shi J, Li N, Li D, et al. (2010) Immunization with a combination of three pneumococcal proteins confers additive and broad protection against Streptococcus pneumoniae Infections in Mice. Infect Immun 78: 1276-1283.
35. Blue CE, Mitchell TJ, (2003) Contribution of a response regulator to the virulence of Streptococcus pneumoniae is strain dependent. Infect Immun 71: 4405-4413.
36. Kafka D, Ling E, Feldman G, Benharroch D, Voronov E, et al. (2008) Contribution of IL-1 to resistance to Streptococcus pneumoniae infection. Int Immunol 20: 1139-1146.
37. Pracht D, Elm C, Gerber J, Bergmann S, Rohde M, et al. (2005) PavA of Streptococcus pneumoniae modulates adherence, invasion, and meningeal inflammation. Infect Immun 73: 2680-2869.
38. Bergmann S, Lang A, Rohde M, Agarwal V, Rennemeier C, et al. (2009) Integrin-linked kinase is required for vitronectin-mediated internalization of Streptococcus pneumoniae by host cells. J Cell Sci 122: 256-267.
39. Velanker SS, Ray SS, Gokhale RS, Suma S, Balaram H, et al. (1997) Triosephosphate isomerase from Plasmodium falciparum: the crystal structure provides insights into antimalarial drug design. Structure 5: 751-761.
40. Stenberg K, Lindqvist Y, (1997) Three-dimensional structures of glycolate oxidase with bound active-site inhibitors. Protein Sci 6: 1009-1015.
41. Ramasubbu N, Thomas LM, Ragunath C, Kaplan JB, (2005) Structural Analysis of Dispersin B, a Biofilm-releasing Glycoside Hydrolase from the Periodontopathogen Actinobacillus actinomycetemcomitans. J Mol Biol 349: 475-486.
42. Holm L, Rosenström P, (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res 38: W545-549.
43. Zoll S, Pätzold B, Schlag M, Götz F, Kalbacher H, et al. (2010) Structural basis of cell wall cleavage by a staphylococcal autolysin. PLoS Pathog 6: e1000807.
44. Obita T, Ueda T, Imoto T, (2003) Solution structure and activity of mouse lysozyme M. Cell Mol Life Sci. 60: 176-184.
45. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, et al. (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31: 3497-3500.
46. Nagano N, Hutchinson EG, Thornton JM, (1999) Barrel structures in proteins: automatic identification and classification including a sequence analysis of TIM barrels. Protein Sci 8: 2072-2084.
47. Vijayabaskar MS, Vishveshwara S, (2012) Insights into the Fold Organization of TIM Barrel from Interaction Energy Based Structure Networks. PLoS Comput Biol 8: e1002505.
48. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, et al. (2012) The Pfam protein families database. Nucleic Acids Res 40: D290-D301.
49. Frolet C, Beniazza M, Roux L, Gallet B, Noirclerc-Savoye M, et al. (2010) New adhesin functions of surface-exposed pneumococcal proteins. BMC Microbiol 10: 190.
50. Wang L, Lin M, (2008) A novel cell wall-anchored peptidoglycan hydrolase (autolysin), IspC, essential for Listeria monocytogenes virulence: genetic and proteomic analysis. Microbiology 154: 1900-1913.
51. Cabanes D, Dussurget O, Dehoux P, Cossart P, (2004) Auto, a surface associated autolysin of Listeria monocytogenes required for entry into eukaryotic cells and virulence. Mol Microbiol 51: 1601-1614.
52. Milohanic E, Jonquieres R, Cossart P, Berche P, Gaillard JL, (2001) The autolysin Ami contributes to the adhesion of Listeria monocytogenes to eukaryotic cells via its cell wall anchor. Mol Microbiol 39: 1212-1224.
53. Klug D, Wallet F, Kacet S, Courcol RJ, (2003) Involvement of Adherence and Adhesion Staphylococcus epidermidis Genes in Pacemaker Lead-Associated Infections. J Clin Microbiol 41: 3348-3350.
54. Feldman C, Cockeran R, Jedrzejas MJ, Mitchell TJ, Anderson R, (2007) Hyaluronidase augments pneumolysin-mediated injury to human ciliated epithelium. Int J Infect Dis 11: 11-15.
55. Uchiyama S, Carlin AF, Khosravi A, Weiman S, Banerjee A, et al. (2009) The surface-anchored NanA protein promotes pneumococcal brain endothelial cell invasion. J Exp Med 206: 1845-1852.
56. Parker D, Soong G, Planet P, Brower J, Ratner AJ, Prince A, (2009) The NanA neuraminidase of Streptococcus pneumoniae is involved in biofilm formation. Infect Immun 77: 3722-3730.
57. Gut H, King SJ, Walsh MA, (2008) Structural and functional studies of Streptococcus pneumoniae neuraminidase B: An intramolecular trans-sialidase. FEBS Lett 582: 3348-3352.