Lactobacillus gasseri K7 modulates the blood cell transcriptome of conventional mice infected with Escherichia coli O157: H7

Journal of Applied Microbiology

Volumn 116, Issue 5, 2014, Pages 1282-1296

  Sagaya, F M ^a,b   Hacin, B ^c   Tompa, G ^c   Ihan, A ^d   Špela, Š ^d   Cerne M ^e   Hurrell, R F ^b   Matijasic B B ^c   Rogelj, I ^c   Vergeres G ^a  

^a AGROSCOPE   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY OF LJUBLJANA   (Slovenia)

^d Sandoz Company Biopharmaceuticals   (Slovenia)

^e Lek dd   (Slovenia)

Author keywords

Enterohemorrhagic escherichia coli; Lactobacillus gasseri; Transcriptomics

Indexed keywords

BLOOD; CYTOLOGY; GENE EXPRESSION; MAMMALS;

BLOOD CELLS; E. COLI; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ESCHERICHIA COLI O157:H7; GUT BACTERIA; IMMUNE CELLS; INTESTINAL BARRIERS; LACTOBACILLUS GASSERI; TRANSCRIPTOMES; TRANSCRIPTOMICS;

ESCHERICHIA COLI;

TRANSCRIPTOME; PROBIOTIC AGENT;

BACTERIUM; BIOMARKER; BLOOD; COLIFORM BACTERIUM; CYTOLOGY; GENE EXPRESSION; INFECTIOUS DISEASE; PROBIOTICS; RODENT; SIGNAL;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM DETECTION; BLOOD CELL; CONTROLLED STUDY; DOWN REGULATION; ESCHERICHIA COLI INFECTION; ESCHERICHIA COLI O157; FECES ANALYSIS; FEMALE; FOOD INTAKE; GENE EXPRESSION; HEMATOLOGICAL PARAMETERS; HYBRIDIZATION; INOCULATION; INTESTINE FLORA; LACTOBACILLUS GASSERI; MOUSE; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; ANIMAL; C57BL MOUSE; ESCHERICHIA COLI INFECTIONS; GASTROINTESTINAL TRACT; GENETICS; LACTOBACILLUS; MALE; METABOLISM; MICROBIOLOGY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; LACTOBACILLUS GASSERI; MUS;

ANIMALS; BLOOD CELLS; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI O157; FEMALE; GASTROINTESTINAL TRACT; LACTOBACILLUS; MALE; MICE; MICE, INBRED C57BL; PROBIOTICS; TRANSCRIPTOME;

EID: 84898415199     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.12440     Document Type: Article

References (56)

1. Argmann, C.A. and Auwerx, J. (2006) Collection of blood and plasma from the mouse. Curr Protoc Mol Biol Chapter 29, Unit 29A, 23.
2. Banchereau, R., Jordan-Villegas, A., Ardura, M., Mejias, A., Baldwin, N., Xu, H., Saye, E., Rossello-Urgell, J. et al. (2012) Host immune transcriptional profiles reflect the variability in clinical disease manifestations in patients with Staphylococcus aureus infections. PLoS ONE 7, e34390.
3. Bavaro, M.F. (2012) E. coli O157:H7 and other toxigenic strains: the curse of global food distribution. Curr Gastroenterol Rep 14, 317-323.
4. Borsutzky, S., Cazac, B.B., Roes, J. and Guzman, C.A. (2004) TGF-beta receptor signaling is critical for mucosal IgA responses. J Immunol 173, 3305-3309.
5. Cano, P.G. and Perdigon, G. (2003) Probiotics induce resistance to enteropathogens in a re-nourished mouse model. J Dairy Res 70, 433-440.
6. Conlan, J.W. and Perry, M.B. (1998) Susceptibility of three strains of conventional adult mice to intestinal colonization by an isolate of Escherichia coli O157:H7. Can J Microbiol 44, 800-805.
7. Corthesy, B. (2007) Roundtrip ticket for secretory IgA: role in mucosal homeostasis? J Immunol 178, 27-32.
8. Corthesy, B., Gaskins, H.R. and Mercenier, A. (2007) Cross-talk between probiotic bacteria and the host immune system. J Nutr 137, 781S-790S.
9. Dahan, S., Busuttil, V., Imbert, V., Peyron, J.F., Rampal, P. and Czerucka, D. (2002) Enterohemorrhagic Escherichia coli infection induces interleukin-8 production via activation of mitogen-activated protein kinases and the transcription factors NF-kappaB and AP-1 in T84 cells. Infect Immun 70, 2304-2310.
10. Dahlquist, K.D., Salomonis, N., Vranizan, K., Lawlor, S.C. and Conklin, B.R. (2002) GenMAPP, a new tool for viewing and analyzing microarray data on biological pathways. Nat Genet 31, 19-20.
11. Doniger, S.W., Salomonis, N., Dahlquist, K.D., Vranizan, K., Lawlor, S.C. and Conklin, B.R. (2003) MAPPFinder: using gene ontology and GenMAPP to create a global gene-expression profile from microarray data. Genome Biol 4, R7.
12. Duncan, L., Mai, V., Carter, A., Carlson, J., Borczyk, A. and Karmali, M. (1987) Outbreak of gastrointestinal disease. Can Dis Weekly Rep 13, 5-8.
13. Fagundes, C.T., Souza, D.G., Nicoli, J.R. and Teixeira, M.M. (2011) Control of host inflammatory responsiveness by indigenous microbiota reveals an adaptive component of the innate immune system. Microbes Infect 13, 1121-1132.
14. Foster, G.H. and Tesh, V.L. (2002) Shiga toxin 1-induced activation of c-Jun NH(2)-terminal kinase and p38 in the human monocytic cell line THP-1: possible involvement in the production of TNF-alpha. J Leukoc Biol 71, 107-114.
15. Fratamico, P.M., Sackitey, S.K., Wiedmann, M. and Deng, M.Y. (1995) Detection of Escherichia coli O157:H7 by multiplex PCR. J Clin Microbiol 33, 2188-2191.
16. Galdeano, C.M. and Perdigon, G. (2004) Role of viability of probiotic strains in their persistence in the gut and in mucosal immune stimulation. J Appl Microbiol 97, 673-681.
17. Gyles, C.L. (2007) Shiga toxin-producing Escherichia coli: an overview. J Anim Sci 85, E45-E62.
18. Ho, N.K., Hawley, S.P., Ossa, J.C., Mathieu, O., Tompkins, T.A., Johnson-Henry, K.C. and Sherman, P.M. (2013) Immune signalling responses in intestinal epithelial cells exposed to pathogenic Escherichia coli and lactic acid-producing probiotics. Benef Microbes 4, 195-209.
19. Irizarry, R.A., Bolstad, B.M., Collin, F., Cope, L.M., Hobbs, B. and Speed, T.P. (2003) Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 31, e15.
20. Jacoby, R.O., Fox, J.G. and Avisson, M. (2002) Biology and diseases of mice. In Laboratory Animal Medicine ed. Fox, J.G., Anderson, L.C., Loew, F.M. and Quimby, F.W. pp. 35-120. 2nd edn. New York: Academic Press.
21. Karpman, D., Connell, H., Svensson, M., Scheutz, F., Alm, P. and Svanborg, C. (1997) The role of lipopolysaccharide and Shiga-like toxin in a mouse model of Escherichia coli O157:H7 infection. J Infect Dis 175, 611-620.
22. Kouadjo, K.E., Nishida, Y., Cadrin-Girard, J.F., Yoshioka, M. and St-Amand, J. (2007) Housekeeping and tissue-specific genes in mouse tissues. BMC Genomics 8, 127.
23. Krishnan, K., Salomonis, N. and Guo, S. (2008) Identification of Spt5 target genes in zebrafish development reveals its dual activity in vivo. PLoS ONE 3, e3621.
24. Ledesma, M.A., Ochoa, S.A., Cruz, A., Rocha-Ramirez, L.M., Mas-Oliva, J., Eslava, C.A., Giron, J.A. and Xicohtencatl-Cortes, J. (2010) The hemorrhagic coli pilus (HCP) of Escherichia coli O157:H7 is an inducer of proinflammatory cytokine secretion in intestinal epithelial cells. PLoS ONE 5, e12127.
25. Matijasic, B.B. and Rogelj, I. (2000) Lactobacillus K7-a new candidate for a probiotic strain. Food Technol. Biotech. 38, 113-119.
26. Matijasic, B.B., Stojkovic, S., Salobir, J., Malovrh, S. and Rogelj, I. (2004) Evaluation of the Lactobacillus gasseri K7 and LF221 strains in weaned piglets for their possible probiotic use and their detection in the faeces. Anim Res 53, 35-44.
27. Matijasic, B.B., Narat, M., Zoric, P.M. and Rogelj, I. (2006a) Ability of Lactobacillus gasseri K 7 to inhibit Escherichia coli adhesion in vitro on Caco-2 cells and ex vivo on pigs' jejunal tissue. Int J Food Microbiol 107, 92-96.
28. Matijasic, B.B., Stojkovic, S. and Rogelj, I. (2006b) Survival and in vivo adhesion of human isolates Lactobacillus gasseri LF221 and K7 in weaned piglets and their effects on coliforms, clostridia and lactobacilli viable counts in faeces and mucosa. J Dairy Res 73, 417-422.
29. Matijasic, B.B., Rajsp, K.M., Perko, B. and Rogelj, I. (2007) Inhibition of Clostridium tyrobutyricum in cheese by Lactobacillus gasseri. Int Dairy J 17, 157-166.
30. Mogna, L., Del, P.M., Deidda, F., Nicola, S., Soattini, L., Debiaggi, R., Sforza, F., Strozzi, G. et al. (2012) Assessment of the in vitro inhibitory activity of specific probiotic bacteria against different Escherichia coli strains. J Clin Gastroenterol 46(Suppl), S29-S32.
31. Mohawk, K.L. and O'Brien, A.D. (2011) Mouse models of Escherichia coli O157:H7 infection and shiga toxin injection. J Biomed Biotechnol 2011, 258185.
32. Moist, L.M., Sontrop, J.M., Garg, A.X., Clark, W.F., Suri, R.S., Salvadori, M., Gratton, R.J. and Macnab, J. (2009) Risk of pregnancy-related hypertension within five years of exposure to bacteria-contaminated drinking water. Kidney Int Suppl, S47-S49.
33. Nau, G.J., Richmond, J.F., Schlesinger, A., Jennings, E.G., Lander, E.S. and Young, R.A. (2002) Human macrophage activation programs induced by bacterial pathogens. Proc Natl Acad Sci USA 99, 1503-1508.
34. Ng, S.C., Hart, A.L., Kamm, M.A., Stagg, A.J. and Knight, S.C. (2009) Mechanisms of action of probiotics: recent advances. Inflamm Bowel Dis 15, 300-310.
35. Ottenhoff, T.H., Dass, R.H., Yang, N., Zhang, M.M., Wong, H.E., Sahiratmadja, E., Khor, C.C., Alisjahbana, B. et al. (2012) Genome-wide expression profiling identifies type 1 interferon response pathways in active tuberculosis. PLoS ONE 7, e45839.
36. Paturi, G., Phillips, M., Jones, M. and Kailasapathy, K. (2007) Immune enhancing effects of Lactobacillus acidophilus LAFTI L10 and Lactobacillus paracasei LAFTI L26 in mice. Int J Food Microbiol 115, 115-118.
37. Phillips, A.D., Navabpour, S., Hicks, S., Dougan, G., Wallis, T. and Frankel, G. (2000) Enterohaemorrhagic Escherichia coli O157:H7 target Peyer's patches in humans and cause attaching/effacing lesions in both human and bovine intestine. Gut 47, 377-381.
38. Poirier, K., Faucher, S.P., Beland, M., Brousseau, R., Gannon, V., Martin, C., Harel, J. and Daigle, F. (2008) Escherichia coli O157:H7 survives within human macrophages: global gene expression profile and involvement of the Shiga toxins. Infect Immun 76, 4814-4822.
39. Putaala, H., Barrangou, R., Leyer, G.J., Ouwehand, A.C., Hansen, E.B., Romero, D.A. and Rautonen, N. (2010) Analysis of the human intestinal epithelial cell transcriptional response to Lactobacillus acidophilus, Lactobacillus salivarius, Bifidobacterium lactis and Escherichia coli. Benef Microbes 1, 283-295.
40. Raghavachari, N., Xu, X., Munson, P.J. and Gladwin, M.T. (2009) Characterization of whole blood gene expression profiles as a sequel to globin mRNA reduction in patients with sickle cell disease. PLoS ONE 4, e6484.
41. Ramilo, O., Allman, W., Chung, W., Mejias, A., Ardura, M., Glaser, C., Wittkowski, K.M., Piqueras, B. et al. (2007) Gene expression patterns in blood leukocytes discriminate patients with acute infections. Blood 109, 2066-2077.
42. Rogelj, I. and Matijasic, B.B. (2006) Lactobacillus gasseri LF221 and K7 - from isolation to application. Biologia 61, 761-769.
43. Rosner, B. (2011) Fundamentals of Biostatistics. 7th edn. Boston, MA: Brooks/Cole.
44. Roxas, J.L., Koutsouris, A., Bellmeyer, A., Tesfay, S., Royan, S., Falzari, K., Harris, A., Cheng, H. et al. (2010) Enterohemorrhagic E. coli alters murine intestinal epithelial tight junction protein expression and barrier function in a Shiga toxin independent manner. Lab Invest 90, 1152-1168.
45. Ryan, C.A., Tauxe, R.V., Hosek, G.W., Wells, J.G., Stoesz, P.A., McFadden, H.W. Jr, Smith, P.W., Wright, G.F. et al. (1986) Escherichia coli O157:H7 diarrhea in a nursing home: clinical, epidemiological, and pathological findings. J Infect Dis 154, 631-638.
46. Savkovic, S.D., Villanueva, J., Turner, J.R., Matkowskyj, K.A. and Hecht, G. (2005) Mouse model of enteropathogenic Escherichia coli infection. Infect Immun 73, 1161-1170.
47. Schwan, W.R., Kugler, S., Schuller, S., Kopecko, D.J. and Goebel, W. (1996) Detection and characterization by differential PCR of host eukaryotic cell genes differentially transcribed following uptake of intracellular bacteria. Infect Immun 64, 91-99.
48. Sheil, B., McCarthy, J., O'Mahony, L., Bennett, M.W., Ryan, P., Fitzgibbon, J.J., Kiely, B., Collins, J.K. et al. (2004) Is the mucosal route of administration essential for probiotic function? Subcutaneous administration is associated with attenuation of murine colitis and arthritis. Gut 53, 694-700.
49. Shu, Q. and Gill, H.S. (2002) Immune protection mediated by the probiotic Lactobacillus rhamnosus HN001 (DR20) against Escherichia coli O157:H7 infection in mice. FEMS Immunol Med Microbiol 34, 59-64.
50. Shu, Q., Zhou, S.J., Rutherfurd, K.J., Birtles, M.J., Prasad, J., Gopal, P.K. and Gill, H.S. (1999) Probiotic lactic acid bacteria (Lactobacillus acidophilus HN017, Lactobacillus rhamnosus HN001 and Bifidobacterium lactis HN019) have no adverse effects on the health of mice. Int Dairy J 9, 831-836.
51. Taguchi, H., Takahashi, M., Yamaguchi, H., Osaki, T., Komatsu, A., Fujioka, Y. and Kamiya, S. (2002) Experimental infection of germ-free mice with hyper-toxigenic enterohaemorrhagic Escherichia coli O157:H7, strain 6. J Med Microbiol 51, 336-343.
52. Torriani, S., Zapparoli, G. and Dellaglio, F. (1999) Use of PCR-based methods for rapid differentiation of Lactobacillus delbrueckii subsp. bulgaricus and L. delbrueckii subsp. lactis. Appl Environ Microbiol 65, 4351-4356.
53. Treven, P., Turkova, K., Trmcic, A., Obermajer, T., Rogelj, I. and Matijasic, B.B. (2013) Detection and quantification of probiotic strain Lactobacillus gasseri K7 in faecal samples by targeting bacteriocin genes. Folia Microbiol (Praha) 58, 623-630.
54. Wadolkowski, E.A., Burris, J.A. and O'Brien, A.D. (1990) Mouse model for colonization and disease caused by enterohemorrhagic Escherichia coli O157:H7. Infect Immun 58, 2438-2445.
55. Wang, X., Nie, J., Jia, Z., Feng, M., Zheng, Z., Chen, W., Li, X., Peng, W. et al. (2010) Impaired TGF-beta signalling enhances peritoneal inflammation induced by E. coli in rats. Nephrol Dial Transplant 25, 399-412.
56. Zhong, J. and Kyriakis, J.M. (2007) Dissection of a signaling pathway by which pathogen-associated molecular patterns recruit the JNK and p38 MAPKs and trigger cytokine release. J Biol Chem 282, 24246-24254.