Surface-exposed histone-like protein A modulates adherence of Streptococcus gallolyticus to colon adenocarcinoma cells

Infection and Immunity

Volumn 77, Issue 12, 2009, Pages 5519-5527

  Boleij, Annemarie ^a   Schaeps, Renée M J ^a   De Kleijn, Stan ^a   Hermans, Peter W ^a   Glaser, Philippe ^b   Pancholi, Vijay ^c   Swinkels, Dorine W ^a   Tjalsma, Harold ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b INSTITUT PASTEUR   (France)

^c THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEPARAN SULFATE; HEPARIN BINDING PROTEIN; HISTONE; HISTONE LIKE PROTEIN A; LIPOTEICHOIC ACID; MEMBRANE PROTEIN; PROTEIN A; PROTEOHEPARAN SULFATE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BINDING AFFINITY; BINDING SITE; CANCER CELL; CELL STRAIN HCT116; CELL STRAIN HT29; CELL WALL; COLON ADENOCARCINOMA; CONTROLLED STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; STREPTOCOCCUS BOVIS; STREPTOCOCCUS GALLOLYTICUS;

ADHESINS, BACTERIAL; BACTERIAL ADHESION; BACTERIAL PROTEINS; CELL LINE, TUMOR; HEPARIN; HUMANS; MEMBRANE PROTEINS; PROTEIN BINDING; STREPTOCOCCUS BOVIS;

EID: 72449139059     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00384-09     Document Type: Article

References (44)

1. Ali Azam, T., A. Iwata, A. Nishimura, S. Ueda, and A. Ishihama. 1999. Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J. Bacteriol. 181:6361-6370.
2. Boël, G., H. Jin, and V. Pancholi. 2005. Inhibition of cell surface export of group A streptococcal anchorless surface dehydrogenase affects bacterial adherence and antiphagocytic properties. Infect. Immun. 73:6237-6248.
3. Bootsma, H. J., M. Egmont-Petersen, and P. W. Hermans. 2007. Analysis of the in vitro transcriptional response of human pharyngeal epithelial cells to adherent Streptococcus pneumoniae: evidence for a distinct response to encapsulated strains. Infect. Immun. 75:5489-5499.
4. Cardin, A. D., and H. J. Weintraub. 1989. Molecular modeling of proteinglycosaminoglycan interactions. Arteriosclerosis 9:21-32.
5. Chhatwal, G. S. 2002. Anchorless adhesins and invasins of Gram-positive bacteria: a new class of virulence factors. Trends Microbiol. 10:205-208. (Pubitemid 34327804)
6. Corredoira, J., M. P. Alonso, A. Coira, E. Casariego, C. Arias, D. Alonso, J. Pita, A. Rodriguez, M. J. Lopez, and J. Varela. 2008. Characteristics of Streptococcus bovis endocarditis and its differences with Streptococcus viridans endocarditis. Eur. J. Clin. Microbiol. Infect. Dis. 27:285-291.
7. Courtney, H. S., C. von Hunolstein, J. B. Dale, M. S. Bronze, E. H. Beachey, and D. L. Hasty. 1992. Lipoteichoic acid and M protein: dual adhesins of group A streptococci. Microb. Pathog. 12:199-208.
8. Draing, C., S. Sigel, S. Deininger, S. Traub, R. Munke, C. Mayer, L. Hareng, T. Hartung, S. von Aulock, and C. Hermann. 2008. Cytokine induction by Gram-positive bacteria. Immunobiology 213:285-296.
9. Gandhi, N. S., and R. L. Mancera. 2008. The structure of glycosaminoglycans and their interactions with proteins. Chem. Biol. Drug Des. 72:455-482.
10. Guarner, F., and J. R. Malagelada. 2003. Gut flora in health and disease. Lancet 361:512-519.
11. Henry-Stanley, M. J., D. J. Hess, E. A. Erickson, R. M. Garni, and C. L. Wells. 2003. Role of heparan sulfate in interactions of Listeria monocytogenes with enterocytes. Med. Microbiol. Immunol. 192:107-115.
12. Henry-Stanley, M. J., D. J. Hess, S. L. Erlandsen, and C. L. Wells. 2005. Ability of the heparan sulfate proteoglycan syndecan-1 to participate in bacterial translocation across the intestinal epithelial barrier. Shock 24:571-576.
13. Herrero, I. A., M. S. Rouse, K. E. Piper, S. A. Alyaseen, J. M. Steckelberg, and R. Patel. 2002. Reevaluation of Streptococcus bovis endocarditis cases from 1975 to 1985 by 16S ribosomal DNA sequence analysis. J. Clin. Microbiol. 40:3848-3850.
14. Hess, D. J., M. J. Henry-Stanley, S. L. Erlandsen, and C. L. Wells. 2006. Heparan sulfate proteoglycans mediate Staphylococcus aureus interactions with intestinal epithelium. Med. Microbiol. Immunol. 195:133-141.
15. Hoen, B., C. Chirouze, C. H. Cabell, C. Selton-Suty, F. Duchene, L. Olaison, J. M. Miro, G. Habib, E. Abrutyn, S. Eykyn, Y. Bernard, F. Marco, and G. R. Corey. 2005. Emergence of endocarditis due to group D streptococci: findings derived from the merged database of the International Collaboration on Endocarditis. Eur. J. Clin. Microbiol. Infect. Dis. 24:12-16.
16. Jin, H., and V. Pancholi. 2006. Identification and biochemical characterization of a eukaryotic-type serine/threonine kinase and its cognate phosphatase in Streptococcus pyogenes: their biological functions and substrate identification. J. Mol. Biol. 357:1351-1372.
17. Kapczynski, D. R., R. J. Meinersmann, and M. D. Lee. 2000. Adherence of Lactobacillus to intestinal 407 cells in culture correlates with fibronectin binding. Curr. Microbiol. 41:136-141.
18. Katsube, T., S. Matsumoto, M. Takatsuka, M. Okuyama, Y. Ozeki, M. Naito, Y. Nishiuchi, N. Fujiwara, M. Yoshimura, T. Tsuboi, M. Torii, N. Oshitani, T. Arakawa, and K. Kobayashi. 2007. Control of cell wall assembly by a histone-like protein in mycobacteria. J. Bacteriol. 189:8241-8249. (Pubitemid 350178936)
19. Kim, N., D. L. Weeks, J. M. Shin, D. R. Scott, M. K. Young, and G. Sachs. 2002. Proteins released by Helicobacter pylori in vitro. J. Bacteriol. 184:6155-6162.
20. Klein, R. S., R. A. Recco, M. T. Catalano, S. C. Edberg, J. I. Casey, and N. H. Steigbigel. 1977. Association of Streptococcus bovis with carcinoma of the colon. N. Engl. J. Med. 297:800-802.
21. Lei, B., S. Mackie, S. Lukomski, and J. M. Musser. 2000. Identification and immunogenicity of group A streptococcus culture supernatant proteins. Infect. Immun. 68:6807-6818.
22. Liu, D., H. Yumoto, K. Hirota, K. Murakami, K. Takahashi, K. Hirao, T. Matsuo, K. Ohkura, H. Nagamune, and Y. Miyake. 2008. Histone-like DNA binding protein of Streptococcus intermedius induces the expression of proinflammatory cytokines in human monocytes via activation of ERK1/2 and JNK pathways. Cell. Microbiol. 10:262-276.
23. Pancholi, V., and G. S. Chhatwal. 2003. Housekeeping enzymes as virulence factors for pathogens. Int. J. Med. Microbiol. 293:391-401.
24. Pancholi, V., and V. A. Fischetti. 1998. Alpha-enolase, a novel strong plasmin(ogen) binding protein on the surface of pathogenic streptococci. J. Biol. Chem. 273:14503-14515.
25. Pancholi, V., and V. A. Fischetti. 1992. A major surface protein on group A streptococci is a glyceraldehyde-3-phosphate-dehydrogenase with multiple binding activity. J. Exp. Med. 176:415-426.
26. Pancholi, V., P. Fontan, and H. Jin. 2003. Plasminogen-mediated group A streptococcal adherence to and pericellular invasion of human pharyngeal cells. Microb. Pathog. 35:293-303.
27. Ramstein, J., N. Hervouet, F. Coste, C. Zelwer, J. Oberto, and B. Castaing. 2003. Evidence of a thermal unfolding dimeric intermediate for the Escherichia coli histone-like HU proteins: thermodynamics and structure. J. Mol. Biol. 331:101-121.
28. Rostand, K. S., and J. D. Esko. 1997. Microbial adherence to and invasion through proteoglycans. Infect. Immun. 65:1-8.
29. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed., vol.1. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
30. Schagger, H. 2006. Tricine-SDS-PAGE. Nat. Protoc. 1:16-22.
31. Schlegel, L., F. Grimont, M. D. Collins, B. Regnault, P. A. Grimont, and A. Bouvet. 2000. Streptococcus infantarius sp. nov., Streptococcus infantarius subsp. infantarius subsp. nov. and Streptococcus infantarius subsp. coli subsp. nov., isolated from humans and food. Int. J. Syst. Evol. Microbiol. 50:1425-1434.
32. Sela, S., M. J. Marouni, R. Perry, and A. Barzilai. 2000. Effect of lipoteichoic acid on the uptake of Streptococcus pyogenes by HEp-2 cells. FEMS Microbiol. Lett. 193:187-193.
33. Severin, A., E. Nickbarg, J. Wooters, S. A. Quazi, Y. V. Matsuka, E. Murphy, I. K. Moutsatsos, R. J. Zagursky, and S. B. Olmsted. 2007. Proteomic analysis and identification of Streptococcus pyogenes surface-associated proteins. J. Bacteriol. 189:1514-1522.
34. Sillanpaa, J., S. R. Nallapareddy, K. V. Singh, M. J. Ferraro, and B. E. Murray. 2008. Adherence characteristics of endocarditis-derived Streptococcus gallolyticus ssp. gallolyticus (Streptococcus bovis biotype I) isolates to host extracellular matrix proteins. FEMS Microbiol. Lett. 289:104-109.
35. Stinson, M. W., R. McLaughlin, S. H. Choi, Z. E. Juarez, and J. Barnard. 1998. Streptococcal histone-like protein: primary structure of hlpA and protein binding to lipoteichoic acid and epithelial cells. Infect. Immun. 66:259-265.
36. Tjalsma, H., L. Lambooy, P. W. Hermans, and D. W. Swinkels. 2008. Shedding & shaving: disclosure of proteomic expressions on a bacterial face. Proteomics 8:1415-1428.
37. Tjalsma, H., W. Pluk, L. P. van den Heuvel, W. H. Peters, R. Roelofs, and D. W. Swinkels. 2006. Proteomic inventory of "anchorless" proteins on the colon adenocarcinoma cell surface. Biochim. Biophys. Acta 1764:1607-1617.
38. Tjalsma, H., M. Scholler-Guinard, E. Lasonder, T. J. Ruers, H. L. Willems, and D. W. Swinkels. 2006. Profiling the humoral immune response in colon cancer patients: diagnostic antigens from Streptococcus bovis. Int. J. Cancer 119:2127-2135. (Pubitemid 44423671)
39. Tonnaer, E. L., T. G. Hafmans, T. H. Van Kuppevelt, E. A. Sanders, P. E. Verweij, and J. H. Curfs. 2006. Involvement of glycosaminoglycans in the attachment of pneumococci to nasopharyngeal epithelial cells. Microbes Infect. 8:316-322.
40. Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76:4350-4354.
41. Von Hunolstein, C., M. L. Ricci, and G. Orefici. 1993. Adherence of glucanpositive and glucan-negative strains of Streptococcus bovis to human epithelial cells. J. Med. Microbiol. 39:53-57.
42. Winters, B. D., N. Ramasubbu, and M. W. Stinson. 1993. Isolation and characterization of a Streptococcus pyogenes protein that binds to basal laminae of human cardiac muscle. Infect. Immun. 61:3259-3264.
43. Zhang, L., T. A. Ignatowski, R. N. Spengler, B. Noble, and M. W. Stinson. 1999. Streptococcal histone induces murine macrophages to produce interleukin-1 and tumor necrosis factor alpha. Infect. Immun. 67:6473-6477.
44. zur Hausen, H. 2006. Streptococcus bovis: causal or incidental involvement in cancer of the colon? Int. J. Cancer 119:xi-xii.