Recombinant probiotic expressing Listeria adhesion protein attenuates Listeria monocytogenes virulence in vitro

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Koo, Ok Kyung ^a,c   Amalaradjou, Mary Anne Roshni ^a   Bhunia, Arun K ^a,b  

^a PURDUE UNIVERSITY   (United States)

^b PURDUE UNIVERSITY   (United States)

^c UNIVERSITY OF ARKANSAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; LISTERIA ADHESION PROTEIN; PROBIOTIC AGENT; UNCLASSIFIED DRUG; RECOMBINANT DNA;

ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; CELL DAMAGE; CELL STRAIN CACO 2; COMPETITIVE ABILITY; CONTROLLED STUDY; CYTOTOXICITY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; LACTOBACILLUS PARACASEI; LISTERIA MONOCYTOGENES; MICROBIAL ATTENUATION; NONHUMAN; PROTEIN EXPRESSION; TIGHT JUNCTION; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION; CYTOLOGY; EPITHELIUM CELL; GENE EXPRESSION; GENETIC ENGINEERING; GENETICS; LISTERIA; METABOLISM; METHODOLOGY; MICROBIOLOGY; PATHOGENICITY; PERMEABILITY; PHYSIOLOGY;

LACTOBACILLUS PARACASEI; LISTERIA; LISTERIA MONOCYTOGENES;

BACTERIAL ADHESION; BACTERIAL PROTEINS; CACO-2 CELLS; DNA, RECOMBINANT; EPITHELIAL CELLS; GENE EXPRESSION; GENETIC ENGINEERING; HUMANS; LISTERIA; LISTERIA MONOCYTOGENES; PERMEABILITY; PROBIOTICS; TIGHT JUNCTIONS;

EID: 84855303451     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0029277     Document Type: Article

References (81)

1. Vazquez-Boland JA, Kuhn M, Berche P, Chakraborty T, Dominguez-Bernal G, et al. (2001) Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 14: 584-640.
2. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, et al. (2011) Foodborne illness acquired in the United States-major pathogens. Emerg Infect Dis 17: 7-15.
3. Culligan EP, Hill C, Sleator RD, (2009) Probiotics and gastrointestinal disease: successes, problems and future prospects. Gut Pathog 1: 19.
4. Oelschlaeger TA, (2010) Mechanisms of probiotic actions- A review. Int J Med Microbiol 300: 57-62.
5. Ferber D, (2010) From pigs to people: The emergence of a new superbug. Science 329: 1010-1011.
6. Cossart P, Sansonetti PJ, (2004) Bacterial invasion: The paradigms of enteroinvasive pathogens. Science 304: 242-248.
7. Freitag NE, Port GC, Miner MD, (2009) Listeria monocytogenes- from saprophyte to intracellular pathogen. Nat Rev Microbiol 7: 623-628.
8. Sleator RD, Watson D, Hill C, Gahan CG, (2009) The interaction between Listeria monocytogenes and the host gastrointestinal tract. Microbiology 155: 2463-2475.
9. Turner JR, (2009) Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 9: 799-809.
10. Collado MC, Gueimonde M, Sanz Y, Salminen S, (2006) Adhesion properties and competitive pathogen exclusion ability of bifidobacteria with acquired acid resistance. J Food Prot 69: 1675-1679.
11. Jagadeesan B, Koo OK, Kim KP, Burkholder KM, Mishra KK, et al. (2010) LAP, an alcohol acetaldehyde dehydrogenase enzyme in Listeria promotes bacterial adhesion to enterocyte-like Caco-2 cells only in pathogenic species. Microbiology-SGM 156: 2782-2795.
12. Jaradat ZW, Wampler JW, Bhunia AW, (2003) A Listeria adhesion protein-deficient Listeria monocytogenes strain shows reduced adhesion primarily to intestinal cell lines. Med Microbiol Immunol 192: 85-91.
13. Kim KP, Jagadeesan B, Burkholder KM, Jaradat ZW, Wampler JL, et al. (2006) Adhesion characteristics of Listeria adhesion protein (LAP)-expressing Escherichia coli to Caco-2 cells and of recombinant LAP to eukaryotic receptor Hsp60 as examined in a surface plasmon resonance sensor. FEMS Microbiol Lett 256: 324-332.
14. Wampler JL, Kim KP, Jaradat Z, Bhunia AK, (2004) Heat shock protein 60 acts as a receptor for the Listeria adhesion protein in Caco-2 cells. Infect Immun 72: 931-936.
15. Jagadeesan B, Fleishman Littlejohn AE, Amalaradjou MAR, Singh AK, Mishra KK, et al. (2011) N-Terminal Gly224- Gly411 domain in Listeria adhesion protein interacts with host receptor Hsp60. PLoS ONE 6: e20694.
16. Burkholder KM, Kim KP, Mishra KK, Medina S, Hahm BK, et al. (2009) Expression of LAP, a SecA2-dependent secretory protein, is induced under anaerobic environment. Microbes Infect 11: 859-867.
17. Jaradat ZW, Bhunia AK, (2002) Glucose and nutrient concentrations affect the expression of a 104-kilodalton Listeria adhesion protein in Listeria monocytogenes. Appl Environ Microbiol 68: 4876-4883.
18. Santiago NI, Zipf A, Bhunia AK, (1999) Influence of temperature and growth phase on expression of a 104-kilodalton Listeria adhesion protein in Listeria monocytogenes. Appl Environ Microbiol 65: 2765-2769.
19. Cossart P, Pizarro-Cerda J, Lecuit M, (2003) Invasion of mammalian cells by Listeria monocytogenes: functional mimicry to subvert cellular functions. Trends Cell Biol 13: 23-31.
20. Pentecost M, Kumaran J, Ghosh P, Amieva MR, (2010) Listeria monocytogenes Internalin B activates junctional endocytosis to accelerate intestinal invasion. PLoS Pathog 6: e1000900.
21. Burkholder KM, Bhunia AK, (2010) Listeria monocytogenes uses Listeria adhesion protein (LAP) to promote bacterial transepithelial translocation, and induces expression of LAP receptor Hsp60. Infect Immun 78: 5062-5073.
22. Salminen S, Nybom S, Meriluoto J, Collado MC, Vesterlund S, et al. (2010) Interaction of probiotics and pathogens--benefits to human health? Curr Opin Biotechnol 21: 157-167.
23. Ng SC, Hart AL, Kamm MA, Stagg AJ, Knight SC, (2009) Mechanisms of action of probiotics: Recent advances. Inflamm Bowel Dis 15: 300-310.
24. Servin AL, Coconnier MH, (2003) Adhesion of probiotic strains to the intestinal mucosa and interaction with pathogens. Best Pract Res Clin Gastroenterol 17: 741-754.
25. Thomas DJ, Husmann RJ, Villamar M, Winship TR, Buck RH, et al. (2011) Lactobacillus rhamnosus HN001 attenuates allergy development in a pig model. PLoS ONE 6: e16577.
26. Hebert C, Weber SG, (2011) Common approaches to the control of multidrug-resistant organisms other than methicillin-resistant Staphylococcus aureus (MRSA). Infect Dis Clin North Am 25: 181-200.
27. Liu Z, Shen T, Zhang P, Ma Y, Qin H, (2011) Lactobacillus plantarum surface layer adhesive protein protects intestinal epithelial cells against tight junction injury induced by enteropathogenic Escherichia coli. Mol Biol Reports 38: 3471-3480.
28. Di Giacinto C, Marinaro M, Sanchez M, Strober W, Boirivant M, (2005) Probiotics ameliorate recurrent Th1-mediated murine colitis by inducing IL-10 and IL-10-dependent TGF-beta-bearing regulatory cells. J Immunol 174: 3237-3246.
29. Cook SI, Sellin JH, (1998) Review article: short chain fatty acids in health and disease. Aliment Pharmacol Ther 12: 499-507.
30. Delcenserie V, Martel D, Lamoureux M, Amiot J, Boutin Y, et al. (2008) Immunomodulatory effects of probiotics in the intestinal tract. Curr Issues Mol Biol 10: 37-53.
31. Fukushima Y, Kawata Y, Hara H, Terada A, Mitsuoka T, (1998) Effect of a probiotic formula on intestinal immunoglobulin A production in healthy children. Int J Food Microbiol 42: 39-44.
32. Granato D, Perotti F, Masserey I, Rouvet M, Golliard M, et al. (1999) Cell surface-associated lipoteichoic acid acts as an adhesion factor for attachment of Lactobacillus johnsonii La1 to human enterocyte-like Caco-2 cells. Appl Environ Microbiol 65: 1071-1077.
33. Coconnier MH, Bernet MF, Kerneis S, Chauviere G, Fourniat J, et al. (1993) Inhibition of adhesion of enteroinvasive pathogens to human intestinal Caco-2 cells by Lactobacillus acidophilus strain LB decreases bacterial invasion. FEMS Microbiol Lett 110: 299-305.
34. Sanchez B, Bressollier P, Urdaci MC, (2008) Exported proteins in probiotic bacteria: adhesion to intestinal surfaces, host immunomodulation and molecular cross-talking with the host. FEMS Immunol Med Microbiol 54: 1-17.
35. Neeser JR, Granato D, Rouvet M, Servin A, Teneberg S, et al. (2000) Lactobacillus johnsonii La1 shares carbohydrate-binding specificities with several enteropathogenic bacteria. Glycobiology 10: 1193-1199.
36. Medellin-Pena MJ, Griffiths MW, (2009) Effect of molecules secreted by Lactobacillus acidophilus strain La-5 on Escherichia coli O157:H7 colonization. Appl Environ Microbiol 75: 1165-1172.
37. Banerjee P, Merkel GJ, Bhunia AK, (2009) Lactobacillus delbrueckii ssp. bulgaricus B-30892 can inhibit cytotoxic effects and adhesion of pathogenic Clostridium difficile to Caco-2 cells. Gut Pathog 1: 8.
38. Sleator RD, Hill C, (2007) Patho-biotechnology; using bad bugs to make good bugs better. Sci Prog 90: 1-14.
39. Barrett KE, (2010) Building better bugs to deliver biologics in intestinal inflammation. Gut 59: 427-428.
40. Wells J, (2011) Mucosal vaccination and therapy with genetically modified lactic acid bacteria. Annual Review of Food Science and Technology 2: 423-445.
41. Oliveira ML, Monedero V, Miyaji EN, Leite LC, Lee Ho P, et al. (2003) Expression of Streptococcus pneumoniae antigens, PsaA (pneumococcal surface antigen A) and PspA (pneumococcal surface protein A) by Lactobacillus casei. FEMS Microbiol Lett 227: 25-31.
42. Paton AW, Jennings MP, Morona R, Wang H, Focareta A, et al. (2005) Recombinant probiotics for treatment and prevention of enterotoxigenic Escherichia coli diarrhea. Gastroenterology 128: 1219-1228.
43. Focareta A, Paton JC, Morona R, Cook J, Paton AW, (2006) A recombinant probiotic for treatment and prevention of cholera. Gastroenterology 130: 1688.
44. Corthesy B, Boris S, Isler P, Grangette C, Mercenier A, (2005) Oral Immunization of mice with lactic acid bacteria producing Helicobacter pylori urease B subunit partially protects against challenge with Helicobacter felis. J Infect Dis 192: 1441-1449.
45. Liu X, Lagenaur LA, Lee PP, Xu Q, (2008) Engineering of a human vaginal Lactobacillus strain for surface expression of two-domain CD4 molecules. Appl Environ Microbiol 74: 4626-4635.
46. 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.
47. Kaushik JK, Kumar A, Duary RK, Mohanty AK, Grover S, et al. (2009) Functional and probiotic attributes of an indigenous isolate of Lactobacillus plantarum. Plos One 4: 11.
48. FAO/WHO, (2002) Guidelines for the evaluation of probiotics in food. London, Ontario.
49. Maassen CB, Laman JD, den Bak-Glashouwer MJ, Tielen FJ, van Holten-Neelen JC, et al. (1999) Instruments for oral disease-intervention strategies: recombinant Lactobacillus casei expressing tetanus toxin fragment C for vaccination or myelin proteins for oral tolerance induction in multiple sclerosis. Vaccine 17: 2117-2128.
50. Pouwels PH, Vriesema A, Martinez B, Tielen FJ, Seegers JF, et al. (2001) Lactobacilli as vehicles for targeting antigens to mucosal tissues by surface exposition of foreign antigens. Methods Enzymol 336: 369-389.
51. Koo OK, Aroonnual A, Bhunia AK, (2011) Human heat shock protein 60 receptor coated paramagnetic beads show improved capture of Listeria monocytogenes in presence of other Listeria in food J Appl Microbiol 111: 93-104.
52. Koo OK, (2010) Listeria adhesion protein and heat shock protein 60: application in pathogenic Listeria detection and implication in listeriosis prevention. West Lafayette Purdue University.
53. Banerjee P, Bhunia AK, (2009) Mammalian cell-based biosensors for pathogens and toxins. Trends Biotechnol 27: 179-188.
54. Keeney KM, Finlay BB, (2011) Enteric pathogen exploitation of the microbiota-generated nutrient environment of the gut. Curr Opin Microbiol 14: 92-98.
55. Fishman JA, Issa NC, (2010) Infection in organ transplantation: Risk factors and evolving patterns of infection. Infect Dis Clin North America 24: 273-283.
56. Bodey GP, (2005) Managing infections in the immunocompromised patient. Clin Infect Dis 40: S239.
57. Vanderpool C, Yan F, Polk DB, (2008) Mechanisms of probiotic action: Implications for therapeutic applications in inflammatory bowel diseases. Inflam Bowel Dis 14: 1585-1596.
58. Candela M, Perna F, Carnevali P, Vitali B, Ciati R, et al. (2008) Interaction of probiotic Lactobacillus and Bifidobacterium strains with human intestinal epithelial cells: adhesion properties, competition against enteropathogens and modulation of IL-8 production. Int J Food Microbiol 125: 286-292.
59. Xu H, Jeong HS, Lee HY, Ahn J, (2009) Assessment of cell surface properties and adhesion potential of selected probiotic strains. Lett Appl Microbiol 49: 434-442.
60. Gueimonde M, Margolles A, de los Reyes-Gavilan CG, Salminen S, (2007) Competitive exclusion of enteropathogens from human intestinal mucus by Bifidobacterium strains with acquired resistance to bile--a preliminary study. Int J Food Microbiol 113: 228-232.
61. Corr S, Li Y, Riedel CU, O'Toole PW, Hill C, et al. (2007) Bacteriocin production as a mechanism for the antiinfective activity of Lactobacillus salivarius UCC118. Proc Nat Acad Sci U S A 104: 7617-7621.
62. Chen X, Xu J, Shuai J, Chen J, Zhang Z, et al. (2007) The S-layer proteins of Lactobacillus crispatus strain ZJ001 is responsible for competitive exclusion against Escherichia coli O157:H7 and Salmonella typhimurium. Int J Food Microbiol 115: 307-312.
63. Lee YK, Puong KY, Ouwehand AC, Salminen S, (2003) Displacement of bacterial pathogens from mucus and Caco-2 cell surface by lactobacilli. J Med Microbiol 52: 925-930.
64. Wine E, Gareau MG, Johnson-Henry K, Sherman PM, (2009) Strain-specific probiotic (Lactobacillus helveticus) inhibition of Campylobacter jejuni invasion of human intestinal epithelial cells. FEMS Microbiol Lett 300: 146-152.
65. Botes M, Loos B, van Reenen CA, Dicks LM, (2008) Adhesion of the probiotic strains Enterococcus mundtii ST4SA and Lactobacillus plantarum 423 to Caco-2 cells under conditions simulating the intestinal tract, and in the presence of antibiotics and anti-inflammatory medicaments. Arch Microbiol 190: 573-584.
66. Holck A, Naes H, (1992) Cloning, sequencing and expression of the gene encoding the cell-envelope-associated proteinase from Lactobacillus paracasei subsp. paracasei NCDO 151. J Gen Microbiol 138: 1353-1364.
67. Kruger C, Hu Y, Pan Q, Marcotte H, Hultberg A, et al. (2002) In situ delivery of passive immunity by lactobacilli producing single-chain antibodies. Nat Biotechnol 20: 702-706.
68. Koo OK, Liu Y, Shuaib S, Bhattacharya S, Ladisch MR, et al. (2009) Targeted capture of pathogenic bacteria using a mammalian cell receptor coupled with dielectrophoresis on a biochip. Anal Chem 81: 3094-3101.
69. Gaillard JL, Berche P, Mounier J, Richard S, Sansonetti P, (1987) In vitro model of penetration and intracellular growth of Listeria monocytogenes in the human enterocyte-like cell line Caco-2. Infect Immun 55: 2822-2829.
70. Menon A, Shroyer ML, Wampler JL, Chawan CB, Bhunia AK, (2003) In vitro study of Listeria monocytogenes infection to murine primary and human transformed B cells. Comp Immunol Microbiol Infect Dis 26: 157-174.
71. Innocentin S, Guimaraes V, Miyoshi A, Azevedo V, Langella P, et al. (2009) Lactococcus lactis expressing either Staphylococcus aureus fibronectin-binding protein A or Listeria monocytogenes internalin A can efficiently internalize and deliver DNA in human epithelial cells. Appl Environ Microbiol 75: 4870-4878.
72. Liong MT, (2008) Safety of probiotics: translocation and infection. Nutr Rev 66: 192-202.
73. Pavan S, Desreumaux P, Mercenier A, (2003) Use of mouse models to evaluate the persistence, safety, and immune modulation capacities of lactic acid bacteria. Clin Diagn Lab Immunol 10: 696-701.
74. Resta-Lenert S, Barrett KE, (2006) Probiotics and commensals reverse TNF-alpha- and IFN-gamma-induced dysfunction in human intestinal epithelial cells. Gastroenterology 130: 731-746.
75. Schaumburg J, Diekmann O, Hagendorff P, Bergmann S, Rohde M, et al. (2004) The cell wall subproteome of Listeria monocytogenes. Proteomics 4: 2991-3006.
76. Yamada F, Ueda F, Ochiai Y, Mochizuki M, Shoji H, et al. (2006) Invasion assay of Listeria monocytogenes using Vero and Caco-2 cells. J Microbiol Methods 66: 96-103.
77. Pizarro-Cerda J, Jonquieres R, Gouin E, Vandekerckhove J, Garin J, et al. (2002) Distinct protein patterns associated with Listeria monocytogenes InlA- or InlB-phagosomes. Cell Microbiol 4: 101-115.
78. Cruz N, Qi L, Alvarez X, Berg RD, Deitch EA, (1994) The Caco-2 cell monolayer system as an in vitro model for studying bacterial-enterocyte interactions and bacterial translocation. J Burn Care Rehabil 15: 207-212.
79. Alemka A, Clyne M, Shanahan F, Tompkins T, Corcionivoschi N, et al. (2010) Probiotic colonization of the adherent mucus layer of HT29MTXE12 cells attenuates Campylobacter jejuni virulence properties. Infect Immun 78: 2812-2822.
80. Fukuhara S, Sakurai A, Sano H, Yamagishi A, Somekawa S, et al. (2005) Cyclic AMP potentiates vascular endothelial cadherin-mediated cell-cell contact to enhance endothelial barrier function through an epac-rap1 signaling pathway. Mol Cell Biol 25: 136-146.
81. Banerjee P, Lenz D, Robinson JP, Rickus JL, Bhunia AK, (2008) A novel and simple cell-based detection system with a collagen-encapsulated B-lymphocyte cell line as a biosensor for rapid detection of pathogens and toxins. Lab Invest 88: 196-206.