CwpFM (EntFM) is a Bacillus cereus potential cell wall peptidase implicated in adhesion, biofilm formation, and virulence

Journal of Bacteriology

Volumn 192, Issue 10, 2010, Pages 2638-2642

  Tran, Seav Ly ^a   Guillemet, Elisabeth ^a   Gohar, Michel ^a   Lereclus, Didier ^a   Ramarao, Nalini ^a  

^a UMR1319 MICALIS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOTOXIN; ENT FM PROTEIN; ENTEROTOXIN; HEMOLYSIN; PEPTIDASE; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS CEREUS; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BIOFILM; CELL ADHESION; CELL MOTILITY; CELL SHAPE; CELL VACUOLE; CELL WALL; CONTROLLED STUDY; MACROPHAGE; NONHUMAN; PATHOGENESIS; PATHOGENICITY; PHENOTYPE; PLEIOTROPY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION;

ANIMALS; BACILLUS CEREUS; BACTERIAL ADHESION; BACTERIAL PROTEINS; BIOFILMS; CELL LINE; CELL WALL; HELA CELLS; HUMANS; MICE; MOTHS; PEPTIDE HYDROLASES; VIRULENCE;

BACILLUS CEREUS; BACTERIA (MICROORGANISMS);

EID: 77952088977     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01315-09     Document Type: Article

References (49)

1. Agaisse, H., M. Gominet, O. A. Økstad, A. B. Kolstø, and D. Lereclus. 1999. PlcR is a pleiotropic regulator of extracellular virulence factor gene expression in Bacillus thuringiensis. Mol. Microbiol. 32:1043-1053.
2. Andersson, A., P. E. Granum, and U. Ronner. 1998. The adhesion of Bacillus cereus spores to epithelial cells might be an additional virulence mechanism. Int. J. Food Microbiol. 39:93-99.
3. Andreeva, Z., V. Nesterenko, I. Yurkov, Z. I. Budarina, E. Sineva, and A. S. Solonin. 2006. Purification and cytotoxic properties of Bacillus cereus hemolysin II. Protein Express. Purif. 47:186-193.
4. Arnaout, M., R. Tamburro, S. Bodner, J. Sandlund, G. Rivera, and C. Pui. 1999. Bacillus cereus causing fulminant sepsis and hemolysis in two patients with acute leukemia. J. Pediatr. Hematol. Oncol. 21:431-435.
5. Asano, S., Y. Nukumizu, H. Bando, T. Iizuka, and T. Yamamoto. 1997. Cloning of novel enterotoxin genes from Bacillus cereus and Bacillus thuringiensis. Appl. Environ. Microbiol. 63:1054-1057.
6. Auger, S., E. Krin, S. Aymerich, and M. Gohar. 2006. Autoinducer 2 affects biofilm formation by Bacillus cereus. Appl. Environ. Microbiol. 72:937-941.
7. Auger, S., N. Ramarao, C. Faille, A. Fouet, S. Aymerich, and M. Gohar. 2009. Biofilms formation and cell surface properties among pathogenic and nonpathogenic strains of the Bacillus cereus group. Appl. Environ. Microbiol. 75:6616-6618.
8. Boonchai, N., S. Asano, H. Bando, and C. Wiwat. 2008. Study on cytotoxicity and nucleotide sequences of enterotoxin FM of Bacillus cereus isolated from various food sources. J. Med. Assoc. Thai. 91:1425-1432.
9. Bouillaut, L., N. Ramarao, C. Buisson, N. Gilois, M. Gohar, D. Lereclus, and C. Nilesen-LeRoux. 2005. FlhA influences Bacillus thuringiensis PlcR-regulated gene transcription, protein production, and virulence. Appl. Environ. Microbiol. 71:8903-8910.
10. Calabrese, D., and K. W. Nickerson. 1980. A comparison of protein crystal subunit sizes in Bacillus thuringiensis. Can. J. Microbiol. 26:1006-1010.
11. Callegan, M. C., S. T. Kane, D. C. Cochran, M. S. Gilmore, M. Gominet, and D. Lereclus. 2003. Relationship of PlcR-regulated factors to Bacillus endophthalmitis virulence. Infect. Immun. 71:3116-3124.
12. Callegan, M. C., S. T. Kane, D. C. Cochran, B. Novosad, M. S. Gilmore, M. Gominet, and D. Lereclus. 2005. Bacillus endophthalmitis: roles of bacterial toxins and motility during infection. Invest. Ophthalmol. Vis Sci. 46:3233-3238.
13. Costerton, J., P. Stewart, and E. Greenberg. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318-1322. (Pubitemid 29289651)
14. Fedhila, S., N. Daou, D. Lereclus, and C. Nielsen-LeRoux. 2006. Identification of Bacillus cereus internalin and other candidate virulence genes specifically induced during oral infection in insects. Mol. Microbiol. 62:339-355.
15. Fedhila, S., P. Nel, and D. Lereclus. 2002. The InhA2 metalloprotease of Bacillus thuringiensis strain 407 is required for pathogenicity in insects infected via the oral route. J. Bacteriol. 184:3296-3304.
16. Finney, D. J. 1971. Probit analysis. Cambridge University Press, London, England.
17. Fukushima, T., A. Afkham, S. Kurosawa, T. Tanabe, H. Yamamoto, and J. Sekiguchi. 2006. A new D, L-endopeptidase gene product, YojL (renamed CwlS), plays a role in cell separation with LytE and LytF in Bacillus subtilis. J. Bacteriol. 188:5541-5550. (Pubitemid 44157311)
18. Ghelardi, E., F. Celandroni, S. Salvetti, D. J. Beecher, M. Gominet, D. Lereclus, A. C. Wong, and S. Senesi. 2002. Requirement of flhA for swarming differentiation, flagellin export, and secretion of virulence-associated proteins in Bacillus thuringiensis. J. Bacteriol. 184:6424-6433. (Pubitemid 35332544)
19. Gohar, M., K. Faegri, S. Perchat, S. Ravnum, O. A. Økstad, M. Gominet, A. B. Kolstø, and D. Lereclus. 2008. The PlcR virulence regulon of Bacillus cereus. PLoS One 3:e2793.
20. Guillemet, E., C. Cadot, S. Tran, M. H. Guinebretière, D. Lereclus, and N. Ramarao. 2010. The InhA metalloproteases of B. cereus contribute concomitantly to virulence. J. Bacteriol. 192:286-294.
21. Guinebretière, M. H., V. Broussolle, and C. Nguyen-The. 2002. Enterotoxigenic profiles of food-poisoning and food-borne Bacillus cereus strains. J. Clin. Microbiol. 40:3053-3056.
22. Hall-Stoodley, L., and P. Stoodley. 2009. Evolving concepts in biofim infections. Cell. Microbiol. 11:1034-1043.
23. Hirst, R., B. Gosai, A. Rutman, C. Guerin, P. Nicotera, P. Andrew, and C. O'Callaghan. 2008. Streptococcus pneumoniae deficient in pneumolysin or autolysin has reduced virulence in meningitis. J. Infect. Dis. 1997:744-751.
24. Houry, A., R. Briandet, S. Aymerich, and M. Gohar. 2010. Motility and flagellum involvement in Bacillus cereus biofilm formation. Microbiology 156:1009-1018.
25. Hsieh, Y., S. Sheu, Y. Chen, and H. Tsen. 1999. Enterotoxigenic profiles and polymerase chain reaction detection of Bacillus cereus group cells and B. cereus strains from foods and food-borne ourbreaks. J. Appl. Microbiol. 87:481-490.
26. Hsueh, Y., E. Somers, D. Lereclus, and A. C. Wong. 2006. Biofilm formation by Bacillus cereus is influenced by PlcR, a pleiotropic regulator. Appl. Environ. Microbiol. 72:5089-5092.
27. Ivanova, N., A. Sorokin, I. Anderson, N. Galleron, B. Candelon, V. Kapatral, A. Bhattacharyya, G. Reznik, N. Mikhailova, A. Lapidus, L. Chu, M. Mazur, E. Goltsman, N. Larsen, M. D'Souza, T. Walunas, Y. Grechkin, G. Pusch, R. Haselkorn, M. Fonstein, S. D. Ehrlich, R. Overbeek, and N. Kyrpides. 2003. Genome sequence of Bacillus cereus and comparative analysis with Bacillus anthracis. Nature 423:87-91.
28. Kajimura, J., T. Fujlwara, S. Yamada, Y. Suzawa, T. Nishida, Oyamada, I. Y. Hayashi, J. Yamagishi, H. Komatsuzawa, and M. Sugai. 2005. Identification and molecular characterization of an N-acetylmuramyl-L-alanine amidase Sle1 involved in cell separation of Staphylococcus aureus. Mol. Microbiol. 58:1087-1101. (Pubitemid 41667227)
29. Lereclus, D., O. Arantes, J. Chaufaux, and M.-M. Lecadet. 1989. Transformation and expression of a cloned ∂-endotoxin gene in Bacillus thuringiensis. FEMS Microbiol. Lett. 60:211-218.
30. Lereclus, D., M. Vallade, J. Chaufaux, O. Arantes, and S. Rambaud. 1992. Expansion of insecticidal host range of Bacillus thuringiensis by in vivo genetic recombination. Biotechnology 10:418-421.
31. Lindbäck, T., O. A. Økstad, A. L. Rishovd, and A. B. Kolstø. 1999. Insertional inactivation of hblC encoding the L2 component of Bacillus cereus ATCC 14579 haemolysin BL strongly reduces enterotoxigenic activity, but not the haemolytic activity against human erythrocytes. Microbiology 145:3139-3146.
32. Lövgren, A., M.-Y. Zhang, A. Engström, and R. Landén. 1993. Identification of two expressed flagellin genes in the insect pathogen Bacillus thuringiensis subsp. alesti. J. Gen. Microbiol. 139:21-30. (Pubitemid 23060056)
33. Margot, P., M. Wahlen, A. Gholamhoseinian, P. Piggot, and D. Karamata. 1998. The lytE gene of Bacillus subtilis 168 encodes a cell wall hydrolase. J. Bacteriol. 180:749-752.
34. Miller, J. M., J. G. Hair, M. Hebert, L. Hebert, F. J. Roberts, and R. S. Weyant. 1997. Fulminating bacteremia and pneumonia due to Bacillus cereus. J. Clin. Microbiol. 35:504-507.
35. Minnaard, J., V. Lievin-Le Moal, M. H. Coconnier, A. L. Servin, and P. F. Pérez. 2004. Disassembly of F-actin cytoskeleton after interaction of Bacillus cereus with fully differentiated human intestinal Caco-2 cells. Infect. Immun. 72:3106-3112.
36. Ngamwongsatit, P., W. Buasri, P. Puianariyanon, C. Pulsrikarn, M. Ohba, A. Assavanig, and W. Panbangreb. 2008. Broad distribution of enterotoxin genes (hblCDA, nheABC, cytK, and entFM) among Bacillus thuringiensis and Bacillus cereus as shown by novel primers. Int. J. Food Microbiol. 121:352-356.
37. Pan, Y., F. J. Breidt, and S. Kathariou. 2006. Resistance of Listeria monocytogenes biofilms to sanitizing agents in a simulated food processing environment. Appl. Environ. Microbiol. 72:7711-7717.
38. Qin, Z. O., Y. L. Yang, Y. Zhu, T. Tolker-Nielsen, S. Molin, and D. Qu. 2007. Role of autolysin-mediated DNA release in biofilm formation of Staphylococcus epidermis. Microbiology 153:2083-2092.
39. Ramarao, N., and D. Lereclus. 2006. Adhesion and cytotoxicity of Bacillus cereus and Bacillus thuringiensis to epithelial cells are FlhA and PlcR dependent, respectively. Microbes Infect. 8:1483-1491.
40. Ramarao, N., and D. Lereclus. 2005. The InhA1 metalloprotease allows spores of the B. cereus group to escape macrophages. Cell. Microbiol. 7:1357-1364.
41. Salamitou, S., F. Ramisse, M. Brehélin, D. Bourguet, N. Gilois, M. Gominet, E. Hernandez, and D. Lereclus. 2000. The plcR regulon is involved in the opportunistic properties of Bacillus thuringiensis and Bacillus cereus in mice and insects. Microbiology 146:2825-2832.
42. Shinagawa, K., J. Sugiyama, T. Terada, N. Matsusaka, and S. Sugii. 1991. Improved methods for purification of an enterotoxin produced by Bacillus cereus. FEMS Microbiol. Lett. 80:1-6.
43. Smith, T. J., S. Blackman, and S. Foster. 2000. Autolysins of Bacillus subtilis: multiple enzymes with multiple functions. Microbiology 146:249-262. (Pubitemid 30099199)
44. Stenfors Arnesen, L., A. Fagerlund, and P. Granum. 2008. From soil to gut: Bacillus cereus and its food poisoning toxins. FEMS Microbiol. Rev. 32:579-606.
45. VanDyke, D. J., J. Wu, S. M. Logan, J. F. Kelly, S. Mizuno, S. I. Alzawa, and K. F. Jarrell. 2 April 2009, . Identification of genes involved in the assembly and attachment of a novel flagellinN-linked tetrasaccharide important for motility in the archaeon Methanococcus maripaludis. Mol. Microbiol. [Epub ahead of print.] doi:10.1111/j.1365-2958.2009.06671.x.
46. Vollmer, W., B. Joris, P. Charlier, and S. Foster. 2008. Bacterial peptidoglycan (murein) hydrolases. FEMS Microbiol. Rev. 32:259-286.
47. Wang, L., and M. Lin. 2008. A novel cell-wall anchored peptidoglycan hydrolase (autolysin), IspC, essential for Listeria monocytogenes virulence: genetic and proteomic analysis. Microbiology 154:1900-1913.
48. Wijman, J., P. de Leeuw, R. Moezelaar, M. Zwietering, and T. Abee. 2007. Air-liquid interface biofilms of Bacillus cereus: formation, sporulation and dispersion. Appl. Environ. Microbiol. 73:1481-1488.
49. Zhang, M.-Y., A. Lövgren, M. G. Low, and R. Landén. 1993. Characterization of an avirulent pleiotropic mutant of the insect pathogen Bacillus thuringiensis: reduced expression of flagellin and phospholipases. Infect. Immun. 61:4947-4954.