Immunization of mice with Lactobacillus casei expressing intimin fragments produces antibodies able to inhibit the adhesion of enteropathogenic Escherichia coli to cultivated epithelial cells

FEMS Immunology and Medical Microbiology

Volumn 54, Issue 2, 2008, Pages 245-254

  Ferreira, Patrícia C D ^a   Campos, Ivana B ^a   Abe, Cecília M ^a   Trabulsi, Luiz R ^b   Elias, Waldir P ^a   Ho, Paulo L ^a   Oliveira, Maria Leonor S ^a  

^a INSTITUTO BUTANTAN   (Brazil)

^b NONE

Author keywords

Enteropathogenic Escherichia coli (EPEC); Intimin; Lactobacillus casei

Indexed keywords

DNA FRAGMENT; INTIMIN; INTIMIN BETA; PROTEIN ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANTIGEN BINDING; ARTICLE; BACTERIAL STRAIN; CELL ADHESION; CONTROLLED STUDY; DRUG MECHANISM; ENTEROPATHOGENIC ESCHERICHIA COLI; EPITHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; IMMUNIZATION; IN VITRO STUDY; LACTOBACILLUS CASEI; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION;

ADHESINS, BACTERIAL; ANIMALS; ANTIBODIES, BACTERIAL; BACTERIAL ADHESION; CELLS, CULTURED; ENTEROPATHOGENIC ESCHERICHIA COLI; EPITHELIAL CELLS; ESCHERICHIA COLI PROTEINS; IMMUNITY, MUCOSAL; IMMUNIZATION; LACTOBACILLUS CASEI; MICE; RECOMBINANT PROTEINS;

EID: 53549086381     PISSN: 09288244     EISSN: 1574695X     Source Type: Journal    
DOI: 10.1111/j.1574-695X.2008.00471.x     Document Type: Article

References (61)

1. Adu-Bobie J, Trabulsi LR, Carneiro-Sampaio MM, Dougan G Frankel G (1998) Identification of immunodominant regions within the C-terminal cell binding domain of intimin alpha and intimin beta from enteropathogenic Escherichia coli. Infect Immun 66 : 5643 5649.
2. Batchelor M, Prasannan S, Daniell S et al 2000) Structural basis for recognition of the translocated intimin receptor (Tir) by intimin from enteropathogenic Escherichia coli. EMBO J 19 : 2452 2464.
3. Bermudez-Humaran LG, Cortes-Perez NG, Lefevre F et al 2005) A novel mucosal vaccine based on live Lactococci expressing E7 antigen and IL-12 induces systemic and mucosal immune responses and protects mice against human papillomavirus type 16-induced tumors. J Immunol 175 : 7297 7302.
4. Bittencourt SA, Leal Mdo C Rivera J (1993) Diarrhea and growth among children under 18 months of age in Rio de Janeiro. Bull Pan Am Health Organ 27 : 135 144.
5. Blanco M, Schumacher S, Tasara T et al 2005) Serotypes, intimin variants and other virulence factors of eae positive Escherichia coli strains isolated from healthy cattle in Switzerland. Identification of a new intimin variant gene (eae-eta2). BMC Microbiol 5 : 23.
6. Camara LM, Carbonare SB, Silva ML Carneiro-Sampaio MM (1994) Inhibition of enteropathogenic Escherichia coli (EPEC) adhesion to HeLa cells by human colostrum: detection of specific sIgA related to EPEC outer-membrane proteins. Int Arch Allergy Immunol 103 : 307 310.
7. Campos IB, Darrieux M, Ferreira DM et al 2008) Nasal immunization of mice with Lactobacillus casei expressing the pneumococcal surface protein A: induction of antibodies, complement deposition and partial protection against Streptococcus pneumoniae challenge. Microb Infect 10 : 481 488.
8. Campos LC, Whittam TS, Gomes TA, Andrade JR Trabulsi LR (1994) Escherichia coli serogroup O111 includes several clones of diarrheagenic strains with different virulence properties. Infect Immun 62 : 3282 3288.
9. Canani RB, Cirillo P, Terrin G et al 2007) Probiotics for treatment of acute diarrhoea in children: randomised clinical trial of five different preparations. BMJ 335 : 340.
10. Carbonare CB, Carbonare SB Carneiro-Sampaio MM (2003) Early acquisition of serum and saliva antibodies reactive to enteropathogenic Escherichia coli virulence-associated proteins by infants living in an endemic area. Pediatr Allergy Immunol 14 : 222 228.
11. Cleary J, Lai LC, Shaw RK, Straatman-Iwanowska A, Donnenberg MS, Frankel G Knutton S (2004) Enteropathogenic Escherichia coli (EPEC) adhesion to intestinal epithelial cells: role of bundle-forming pili (BFP), EspA filaments and intimin. Microbiology 150 : 527 538.
12. Cravioto A, Tello A, Villafan H, Ruiz J, del Vedovo S Neeser JR (1991) Inhibition of localized adhesion of enteropathogenic Escherichia coli to HEp-2 cells by immunoglobulin and oligosaccharide fractions of human colostrum and breast milk. J Infect Dis 163 : 1247 1255.
13. Dean P, Maresca M Kenny B (2005) EPEC's weapons of mass subversion. Curr Opin Microbiol 8 : 28 34.
14. Dean P, Maresca M, Schuller S, Phillips AD Kenny B (2006) Potent diarrheagenic mechanism mediated by the cooperative action of three enteropathogenic Escherichia coli-injected effector proteins. Proc Natl Acad Sci USA 103 : 1876 1881.
15. Detmer A Glenting J (2006) Live bacterial vaccines - a review and identification of potential hazards. Microb Cell Fact 5 : 23.
16. Fagundes-Neto U de Andrade JA (1999) Acute diarrhea and malnutrition: lethality risk in hospitalized infants. J Am Coll Nutr 18 : 303 308.
17. Frankel G, Candy DC, Fabiani E et al 1995) Molecular characterization of a carboxy-terminal eukaryotic-cell-binding domain of intimin from enteropathogenic Escherichia coli. Infect Immun 63 : 4323 4328.
18. Frankel G, Phillips AD, Novakova M et al 1996) Intimin from enteropathogenic Escherichia coli restores murine virulence to a Citrobacter rodentium eaeA mutant: induction of an immunoglobulin A response to intimin and EspB. Infect Immun 64 : 5315 5325.
19. Frankel G, Phillips AD, Trabulsi LR, Knutton S, Dougan G Matthews S (2001) Intimin and the host cell - is it bound to end in Tir(s)? Trends Microbiol 9 : 214 218.
20. Galdeano CM Perdigon G (2006) The probiotic bacterium Lactobacillus casei induces activation of the gut mucosal immune system through innate immunity. Clin Vaccine Immunol 13 : 219 226.
21. Gansheroff LJ, Wachtel MR O'Brien AD (1999) Decreased adherence of enterohemorrhagic Escherichia coli to HEp-2 cells in the presence of antibodies that recognize the C-terminal region of intimin. Infect Immun 67 : 6409 6417.
22. Gomes TA, Rassi V, MacDonald KL et al 1991) Enteropathogens associated with acute diarrheal disease in urban infants in São Paulo, Brazil. J Infect Dis 164 : 331 337.
23. Grangette C, Muller-Alouf H, Hols P, Goudercourt D, Delcour J, Turneer M Mercenier A (2004) Enhanced mucosal delivery of antigen with cell wall mutants of lactic acid bacteria. Infect Immun 72 : 2731 2737.
24. Guerrant RL, Kosek M, Moore S, Lorntz B, Brantley R Lima AA (2002) Magnitude and impact of diarrheal diseases. Arch Med Res 33 : 351 355.
25. Hanniffy SB, Carter AT, Hitchin E Wells JM (2007) Mucosal delivery of a pneumococcal vaccine using Lactococcus lactis affords protection against respiratory infection. J Infect Dis 195 : 185 193.
26. Huang JS, Bousvaros A, Lee JW, Diaz A Davidson EJ (2002) Efficacy of probiotic use in acute diarrhea in children: a meta-analysis. Dig Dis Sci 47 : 2625 2634.
27. Ito K, Iida M, Yamazaki M et al 2007) Intimin types determined by heteroduplex mobility assay of intimin gene (eae)-positive Escherichia coli strains. J Clin Microbiol 45 : 1038 1041.
28. Kajikawa A, Satoh E, Leer RJ, Yamamoto S Igimi S (2007) Intragastric immunization with recombinant Lactobacillus casei expressing flagellar antigen confers antibody-independent protective immunity against Salmonella enterica serovar Enteritidis. Vaccine 25 : 3599 3605.
29. Kane M (1998) Unsafe injections. Bull World Health Organ 76 : 99 100.
30. Kaper JB, Nataro JP Mobley HL (2004) Pathogenic Escherichia coli. Nat Rev Microbiol 2 : 123 140.
31. Kenny B (2002) Enteropathogenic Escherichia coli (EPEC) - a crafty subversive little bug. Microbiology 148 : 1967 1978.
32. Kosek M, Bern C Guerrant RL (2003) The global burden of diarrhoeal disease, as estimated from studies published between 1992 and 2000. Bull World Health Organ 81 : 197 204.
33. Leblanc J, Fliss I Matar C (2004) Induction of a humoral immune response following an Escherichia coli O157:H7 infection with an immunomodulatory peptidic fraction derived from Lactobacillus helveticus-fermented milk. Clin Diagn Lab Immunol 11 : 1171 1181.
34. Levine MM, Bergquist EJ, Nalin DR, Waterman DH, Hornick RB, Young CR Sotman S (1978) Escherichia coli strains that cause diarrhoea but do not produce heat-labile or heat-stable enterotoxins and are non-invasive. Lancet 1 : 1119 1122.
35. Loureiro I, Frankel G, Adu-Bobie J, Dougan G, Trabulsi LR Carneiro-Sampaio MM (1998) Human colostrum contains IgA antibodies reactive to enteropathogenic Escherichia coli virulence-associated proteins: intimin, BfpA, EspA, and EspB. J Pediatr Gastroenterol Nutr 27 : 166 171.
36. Luo Y, Frey EA, Pfuetzner RA et al 2000) Crystal structure of enteropathogenic Escherichia coli intimin-receptor complex. Nature 405 : 1073 1077.
37. McDaniel TK, Jarvis KG, Donnenberg MS Kaper JB (1995) A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc Natl Acad Sci USA 92 : 1664 1668.
38. McGraw EA, Li J, Selander RK Whittam TS (1999) Molecular evolution and mosaic structure of alpha, beta, and gamma intimins of pathogenic Escherichia coli. Mol Biol Evol 16 : 12 22.
39. Miyake M, Hanajima M, Matsuzawa T, Kobayashi C, Minami M, Abe A Horiguchi Y (2005) Binding of intimin with Tir on the bacterial surface is prerequisite for the barrier disruption induced by enteropathogenic Escherichia coli. Biochem Biophys Res Commun 337 : 922 927.
40. Mohamadzadeh M, Olson S, Kalina WV et al 2005) Lactobacilli activate human dendritic cells that skew T cells toward T helper 1 polarization. Proc Natl Acad Sci USA 102 : 2880 2885.
41. Mundy R, Schuller S, Girard F, Fairbrother JM, Phillips AD Frankel G (2007) Functional studies of intimin in vivo and ex vivo: implications for host specificity and tissue tropism. Microbiology 153 : 959 967.
42. Nakazato G, Gyles C, Ziebell K et al 2004) Attaching and effacing Escherichia coli isolated from dogs in Brazil: characteristics and serotypic relationship to human enteropathogenic E. coli (EPEC). Vet Microbiol 101 : 269 277.
43. Nataro JP Kaper JB (1998) Diarrheagenic Escherichia coli. Clin Microbiol Rev 11 : 142 201.
44. Nunes EB, Saridakis HO, Irino K Pelayo JS (2003) Genotypic and phenotypic characterization of attaching and effacing Escherichia coli (AEEC) isolated from children with and without diarrhoea in Londrina, Brazil. J Med Microbiol 52 : 499 504.
45. Oliveira ML, Areas AP, Campos IB et al 2006) Induction of systemic and mucosal immune response and decrease in Streptococcus pneumoniae colonization by nasal inoculation of mice with recombinant lactic acid bacteria expressing pneumococcal surface antigen A. Microb Infect 8 : 1016 1024.
46. Oliveira ML, Areas AP Ho PL (2007) Intranasal vaccines for protection against respiratory and systemic bacterial infections. Expert Rev Vaccines 6 : 419 429.
47. Palmeira P, Yu Ito L, Arslanian C Carneiro-Sampaio MM (2007) Passive immunity acquisition of maternal anti-enterohemorrhagic Escherichia coli (EHEC) O157:H7 IgG antibodies by the newborn. Eur J Pediatr 166 : 413 419.
48. Pant N, Marcotte H, Brussow H, Svensson L Hammarstrom L (2007) Effective prophylaxis against rotavirus diarrhea using a combination of Lactobacillus rhamnosus GG and antibodies. BMC Microbiol 7 : 86.
49. Penteado AS, Ugrinovich LA, Blanco J et al 2002) Serobiotypes and virulence genes of Escherichia coli strains isolated from diarrheic and healthy rabbits in Brazil. Vet Microbiol 89 : 41 51.
50. Ramachandran V, Brett K, Hornitzky MA, Dowton M, Bettelheim KA, Walker MJ Djordjevic SP (2003) Distribution of intimin subtypes among Escherichia coli isolates from ruminant and human sources. J Clin Microbiol 41 : 5022 5032.
51. Regua-Mangia AH, Gomes TA, Vieira MA, Andrade JR, Irino K Teixeira LM (2004) Frequency and characteristics of diarrhoeagenic Escherichia coli strains isolated from children with and without diarrhoea in Rio de Janeiro, Brazil. J Infect 48 : 161 167.
52. Rosa AC, Mariano AT, Pereira AM, Tibana A, Gomes TA Andrade JR (1998) Enteropathogenicity markers in Escherichia coli isolated from infants with acute diarrhoea and healthy controls in Rio de Janeiro, Brazil. J Med Microbiol 47 : 781 790.
53. Scaletsky IC, Fabbricotti SH, Silva SO, Morais MB Fagundes-Neto U (2002) HEp-2-adherent Escherichia coli strains associated with acute infantile diarrhea, Sao Paulo, Brazil. Emerg Infect Dis 8 : 855 858.
54. Sherman PM, Johnson-Henry KC, Yeung HP, Ngo PS, Goulet J Tompkins TA (2005) Probiotics reduce enterohemorrhagic Escherichia coli O157:H7- and enteropathogenic E. coli O127:H6-induced changes in polarized T84 epithelial cell monolayers by reducing bacterial adhesion and cytoskeletal rearrangements. Infect Immun 73 : 5183 5188.
55. Sinclair JF, Dean-Nystrom EA O'Brien AD (2006) The established intimin receptor Tir and the putative eucaryotic intimin receptors nucleolin and beta1 integrin localize at or near the site of enterohemorrhagic Escherichia coli O157:H7 adherence to enterocytes in vivo. Infect Immun 74 : 1255 1265.
56. Sobel J, Gomes TA, Ramos RT, Hoekstra M, Rodrigue D, Rassi V Griffin PM (2004) Pathogen-specific risk factors and protective factors for acute diarrheal illness in children aged 12-59 months in São Paulo, Brazil. Clin Infect Dis 38 : 1545 1551.
57. Tarr CL Whittam TS (2002) Molecular evolution of the intimin gene in O111 clones of pathogenic Escherichia coli. J Bacteriol 184 : 479 487.
58. Trabulsi LR, Keller R Tardelli Gomes TA (2002) Typical and atypical enteropathogenic Escherichia coli. Emerg Infect Dis 8 : 508 513.
59. Wells JM Mercenier A (2008) Mucosal delivery of therapeutic and prophylactic molecules using lactic acid bacteria. Nat Rev Microbiol 6 : 349 362.
60. Wu CM Chung TC (2007) Mice protected by oral immunization with Lactobacillus reuteri secreting fusion protein of Escherichia coli enterotoxin subunit protein. FEMS Immunol Med Microbiol 50 : 354 365.
61. Zhang WL, Kohler B, Oswald E et al 2002) Genetic diversity of intimin genes of attaching and effacing Escherichia coli strains. J Clin Microbiol 40 : 4486 4492.