Skip to main content
Top
Published in: Gut Pathogens 1/2010

Open Access 01-12-2010 | Research

Pseudomonas fluorescens alters epithelial permeability and translocates across Caco-2/TC7 intestinal cells

Authors: Amar Madi, Pascal Svinareff, Nicole Orange, Marc GJ Feuilloley, Nathalie Connil

Published in: Gut Pathogens | Issue 1/2010

Login to get access

Abstract

Background

Pseudomonas fluorescens has long been considered as a psychrotrophic microorganism. Recently, we have shown that clinical strains of P. fluorescens (biovar 1) are able to adapt at a growth temperature of 37°C or above and induce a specific inflammatory response. Interestingly, a highly specific antigen of P. fluorescens, I2, is detected in the serum of patients with Crohn's disease but the possible role of this bacterium in the disease has not yet been explored. In the present study, we examined the ability of a psychrotrophic and a clinical strain of P. fluorescens to modulate the permeability of a Caco-2/TC7 intestinal epithelial model, reorganize the actin cytoskeleton, invade the target cells and translocate across the epithelium. The behaviour of these two strains was compared to that of the well known opportunistic pathogen P. aeruginosa PAO1.

Results

Both strains of P. fluorescens were found to decrease the transepithelial resistance (TER) of Caco-2/TC7 differentiated monolayers. This was associated with an increase in paracellular permeability and F-actin microfilaments rearrangements. Moreover, the invasion and translocation tests demonstrated that the two strains used in this study can invade and translocate across the differentiated Caco-2/TC7 cell monolayers.

Conclusions

The present work shows for the first time, that P. fluorescens is able to alter the intestinal epithelial barrier function by disorganizing the F-actin microfilament network. Moreover, we reveal that independently of their origins, the two P. fluorescens strains can translocate across differentiated Caco-2/TC7 cell monolayers by using the transcellular pathway. These findings could, at least in part, explain the presence of the P. fluorescens specific I2 antigen in the serum of patients with Crohn's disease.
Appendix
Available only for authorised users
Literature
1.
go back to reference Chapalain A, Rossignol G, Lesouhaitier O, Merieau A, Gruffaz C, Guerillon J, Meyer JM, Orange N, Feuilloley MG: Comparative study of 7 fluorescent pseudomonad clinical isolates. Can J Microbiol. 2008, 54 (1): 19-27. 10.1139/W07-110.CrossRefPubMed Chapalain A, Rossignol G, Lesouhaitier O, Merieau A, Gruffaz C, Guerillon J, Meyer JM, Orange N, Feuilloley MG: Comparative study of 7 fluorescent pseudomonad clinical isolates. Can J Microbiol. 2008, 54 (1): 19-27. 10.1139/W07-110.CrossRefPubMed
2.
go back to reference Sperandio D, Rossignol G, Guerillon J, Connil N, Orange N, Feuilloley MG, Merieau A: Cell-associated hemolysis activity in the clinical strain of Pseudomonas fluorescens MFN1032. BMC Microbiol. 2010, 10: 124-10.1186/1471-2180-10-124.PubMedCentralCrossRefPubMed Sperandio D, Rossignol G, Guerillon J, Connil N, Orange N, Feuilloley MG, Merieau A: Cell-associated hemolysis activity in the clinical strain of Pseudomonas fluorescens MFN1032. BMC Microbiol. 2010, 10: 124-10.1186/1471-2180-10-124.PubMedCentralCrossRefPubMed
3.
go back to reference Madi A, Lakhdari O, Blottière HM, Guyard-Nicodème M, Le Roux K, Groboillot A, Svinareff P, Doré J, Orange N, Feuilloley MG, Connil N: The clinical Pseudomonas fluorescens MFN1032 strain exerts a cytotoxic effect on epithelial intestinal cells and induces Interleukin-8 via the AP-1 signaling pathway. BMC Microbiol. 2010, 10: 215-10.1186/1471-2180-10-215.PubMedCentralCrossRefPubMed Madi A, Lakhdari O, Blottière HM, Guyard-Nicodème M, Le Roux K, Groboillot A, Svinareff P, Doré J, Orange N, Feuilloley MG, Connil N: The clinical Pseudomonas fluorescens MFN1032 strain exerts a cytotoxic effect on epithelial intestinal cells and induces Interleukin-8 via the AP-1 signaling pathway. BMC Microbiol. 2010, 10: 215-10.1186/1471-2180-10-215.PubMedCentralCrossRefPubMed
5.
go back to reference McDonald MJ, Cooper TF, Beaumont HJ, Rainey PB: The distribution of fitness effects of new beneficial mutations in Pseudomonas fluorescens. Biol Lett. McDonald MJ, Cooper TF, Beaumont HJ, Rainey PB: The distribution of fitness effects of new beneficial mutations in Pseudomonas fluorescens. Biol Lett.
6.
go back to reference Rajmohan S, Dodd CE, Waites WM: Enzymes from isolates of Pseudomonas fluorescens involved in food spoilage. J Appl Microbiol. 2002, 93 (2): 205-213. 10.1046/j.1365-2672.2002.01674.x.CrossRefPubMed Rajmohan S, Dodd CE, Waites WM: Enzymes from isolates of Pseudomonas fluorescens involved in food spoilage. J Appl Microbiol. 2002, 93 (2): 205-213. 10.1046/j.1365-2672.2002.01674.x.CrossRefPubMed
7.
go back to reference Wei B, Huang T, Dalwadi H, Sutton CL, Bruckner D, Braun J: Pseudomonas fluorescens encodes the Crohn's disease-associated I2 sequence and T-cell superantigen. Infect Immun. 2002, 70 (12): 6567-6575. 10.1128/IAI.70.12.6567-6575.2002.PubMedCentralCrossRefPubMed Wei B, Huang T, Dalwadi H, Sutton CL, Bruckner D, Braun J: Pseudomonas fluorescens encodes the Crohn's disease-associated I2 sequence and T-cell superantigen. Infect Immun. 2002, 70 (12): 6567-6575. 10.1128/IAI.70.12.6567-6575.2002.PubMedCentralCrossRefPubMed
8.
go back to reference Sutton CL, Kim J, Yamane A, Dalwadi H, Wei B, Landers C, Targan SR, Braun J: Identification of a novel bacterial sequence associated with Crohn's disease. Gastroenterology. 2000, 119 (1): 23-31. 10.1053/gast.2000.8519.CrossRefPubMed Sutton CL, Kim J, Yamane A, Dalwadi H, Wei B, Landers C, Targan SR, Braun J: Identification of a novel bacterial sequence associated with Crohn's disease. Gastroenterology. 2000, 119 (1): 23-31. 10.1053/gast.2000.8519.CrossRefPubMed
9.
go back to reference Dalwadi H, Wei B, Kronenberg M, Sutton CL, Braun J: The Crohn's disease-associated bacterial protein I2 is a novel enteric t cell superantigen. Immunity. 2001, 15 (1): 149-158. 10.1016/S1074-7613(01)00164-9.CrossRefPubMed Dalwadi H, Wei B, Kronenberg M, Sutton CL, Braun J: The Crohn's disease-associated bacterial protein I2 is a novel enteric t cell superantigen. Immunity. 2001, 15 (1): 149-158. 10.1016/S1074-7613(01)00164-9.CrossRefPubMed
10.
go back to reference Hugot JP, Alberti C, Berrebi D, Bingen E, Cezard JP: Crohn's disease: the cold chain hypothesis. Lancet. 2003, 362 (9400): 2012-2015. 10.1016/S0140-6736(03)15024-6.CrossRefPubMed Hugot JP, Alberti C, Berrebi D, Bingen E, Cezard JP: Crohn's disease: the cold chain hypothesis. Lancet. 2003, 362 (9400): 2012-2015. 10.1016/S0140-6736(03)15024-6.CrossRefPubMed
11.
go back to reference Yap AS, Mullin JM, Stevenson BR: Molecular analyses of tight junction physiology: insights and paradoxes. J Membr Biol. 1998, 163 (3): 159-167. 10.1007/s002329900380.CrossRefPubMed Yap AS, Mullin JM, Stevenson BR: Molecular analyses of tight junction physiology: insights and paradoxes. J Membr Biol. 1998, 163 (3): 159-167. 10.1007/s002329900380.CrossRefPubMed
12.
go back to reference Baumgart DC, Dignass AU: Intestinal barrier function. Curr Opin Clin Nutr Metab Care. 2002, 5 (6): 685-694. 10.1097/00075197-200211000-00012.CrossRefPubMed Baumgart DC, Dignass AU: Intestinal barrier function. Curr Opin Clin Nutr Metab Care. 2002, 5 (6): 685-694. 10.1097/00075197-200211000-00012.CrossRefPubMed
13.
go back to reference Tsukita S, Furuse M, Itoh M: Structural and signalling molecules come together at tight junctions. Curr Opin Cell Biol. 1999, 11 (5): 628-633. 10.1016/S0955-0674(99)00016-2.CrossRefPubMed Tsukita S, Furuse M, Itoh M: Structural and signalling molecules come together at tight junctions. Curr Opin Cell Biol. 1999, 11 (5): 628-633. 10.1016/S0955-0674(99)00016-2.CrossRefPubMed
14.
go back to reference Ma TY, Hollander D, Tran LT, Nguyen D, Hoa N, Bhalla D: Cytoskeletal regulation of Caco-2 intestinal monolayer paracellular permeability. J Cell Physiol. 1995, 164 (3): 533-545. 10.1002/jcp.1041640311.CrossRefPubMed Ma TY, Hollander D, Tran LT, Nguyen D, Hoa N, Bhalla D: Cytoskeletal regulation of Caco-2 intestinal monolayer paracellular permeability. J Cell Physiol. 1995, 164 (3): 533-545. 10.1002/jcp.1041640311.CrossRefPubMed
15.
go back to reference Madara JL: Tight junction dynamics: is paracellular transport regulated?. Cell. 1988, 53 (4): 497-498. 10.1016/0092-8674(88)90562-4.CrossRefPubMed Madara JL: Tight junction dynamics: is paracellular transport regulated?. Cell. 1988, 53 (4): 497-498. 10.1016/0092-8674(88)90562-4.CrossRefPubMed
16.
go back to reference Maeda S, Hsu LC, Liu H, Bankston LA, Iimura M, Kagnoff MF, Eckmann L, Karin M: Nod2 mutation in Crohn's disease potentiates NF-kappaB activity and IL-1beta processing. Science. 2005, 307 (5710): 734-738. 10.1126/science.1103685.CrossRefPubMed Maeda S, Hsu LC, Liu H, Bankston LA, Iimura M, Kagnoff MF, Eckmann L, Karin M: Nod2 mutation in Crohn's disease potentiates NF-kappaB activity and IL-1beta processing. Science. 2005, 307 (5710): 734-738. 10.1126/science.1103685.CrossRefPubMed
17.
go back to reference Bras AM, Ketley JM: Transcellular translocation of Campylobacter jejuni across human polarised epithelial monolayers. FEMS Microbiol Lett. 1999, 179 (2): 209-215. 10.1016/S0378-1097(99)00413-9.CrossRefPubMed Bras AM, Ketley JM: Transcellular translocation of Campylobacter jejuni across human polarised epithelial monolayers. FEMS Microbiol Lett. 1999, 179 (2): 209-215. 10.1016/S0378-1097(99)00413-9.CrossRefPubMed
18.
go back to reference Walker RI, Schmauder-Chock EA, Parker JL, Burr D: Selective association and transport of Campylobacter jejuni through M cells of rabbit Peyer's patches. Can J Microbiol. 1988, 34 (10): 1142-1147. 10.1139/m88-201.CrossRefPubMed Walker RI, Schmauder-Chock EA, Parker JL, Burr D: Selective association and transport of Campylobacter jejuni through M cells of rabbit Peyer's patches. Can J Microbiol. 1988, 34 (10): 1142-1147. 10.1139/m88-201.CrossRefPubMed
19.
go back to reference Burini JF, Gugi B, Merieau A, Guespin-Michel JF: Lipase and acidic phosphatase from the psychrotrophic bacterium Pseudomonas fluorescens: two enzymes whose synthesis is regulated by the growth temperature. FEMS Microbiol Lett. 1994, 122 (1-2): 13-18. 10.1111/j.1574-6968.1994.tb07136.x.CrossRefPubMed Burini JF, Gugi B, Merieau A, Guespin-Michel JF: Lipase and acidic phosphatase from the psychrotrophic bacterium Pseudomonas fluorescens: two enzymes whose synthesis is regulated by the growth temperature. FEMS Microbiol Lett. 1994, 122 (1-2): 13-18. 10.1111/j.1574-6968.1994.tb07136.x.CrossRefPubMed
20.
go back to reference Chantret I, Rodolosse A, Barbat A, Dussaulx E, Brot-Laroche E, Zweibaum A, Rousset M: Differential expression of sucrase-isomaltase in clones isolated from early and late passages of the cell line Caco-2: evidence for glucose-dependent negative regulation. J Cell Sci. 1994, 107 (Pt 1): 213-225.PubMed Chantret I, Rodolosse A, Barbat A, Dussaulx E, Brot-Laroche E, Zweibaum A, Rousset M: Differential expression of sucrase-isomaltase in clones isolated from early and late passages of the cell line Caco-2: evidence for glucose-dependent negative regulation. J Cell Sci. 1994, 107 (Pt 1): 213-225.PubMed
21.
go back to reference Lynch T, Livingstone S, Buenaventura E, Lutter E, Fedwick J, Buret AG, Graham D, DeVinney R: Vibrio parahaemolyticus disruption of epithelial cell tight junctions occurs independently of toxin production. Infect Immun. 2005, 73 (3): 1275-1283. 10.1128/IAI.73.3.1275-1283.2005.PubMedCentralCrossRefPubMed Lynch T, Livingstone S, Buenaventura E, Lutter E, Fedwick J, Buret AG, Graham D, DeVinney R: Vibrio parahaemolyticus disruption of epithelial cell tight junctions occurs independently of toxin production. Infect Immun. 2005, 73 (3): 1275-1283. 10.1128/IAI.73.3.1275-1283.2005.PubMedCentralCrossRefPubMed
22.
go back to reference Kubler I, Koslowski MJ, Gersemann M, Fellermann K, Beisner J, Becker S, Rothfuss K, Herrlinger KR, Stange EF, Wehkamp J: Influence of standard treatment on ileal and colonic antimicrobial defensin expression in active Crohn's disease. Aliment Pharmacol Ther. 2009, 30 (6): 621-633. 10.1111/j.1365-2036.2009.04070.x.CrossRefPubMed Kubler I, Koslowski MJ, Gersemann M, Fellermann K, Beisner J, Becker S, Rothfuss K, Herrlinger KR, Stange EF, Wehkamp J: Influence of standard treatment on ileal and colonic antimicrobial defensin expression in active Crohn's disease. Aliment Pharmacol Ther. 2009, 30 (6): 621-633. 10.1111/j.1365-2036.2009.04070.x.CrossRefPubMed
23.
go back to reference Picot L, Mezghani-Abdelmoula S, Chevalier S, Merieau A, Lesouhaitier O, Guerillon J, Cazin L, Orange N, Feuilloley MG: Regulation of the cytotoxic effects of Pseudomonas fluorescens by growth temperature. Res Microbiol. 2004, 155 (1): 39-46. 10.1016/j.resmic.2003.09.014.CrossRefPubMed Picot L, Mezghani-Abdelmoula S, Chevalier S, Merieau A, Lesouhaitier O, Guerillon J, Cazin L, Orange N, Feuilloley MG: Regulation of the cytotoxic effects of Pseudomonas fluorescens by growth temperature. Res Microbiol. 2004, 155 (1): 39-46. 10.1016/j.resmic.2003.09.014.CrossRefPubMed
24.
go back to reference Picot L, Abdelmoula SM, Merieau A, Leroux P, Cazin L, Orange N, Feuilloley MG: Pseudomonas fluorescens as a potential pathogen: adherence to nerve cells. Microbes Infect. 2001, 3 (12): 985-995. 10.1016/S1286-4579(01)01462-9.CrossRefPubMed Picot L, Abdelmoula SM, Merieau A, Leroux P, Cazin L, Orange N, Feuilloley MG: Pseudomonas fluorescens as a potential pathogen: adherence to nerve cells. Microbes Infect. 2001, 3 (12): 985-995. 10.1016/S1286-4579(01)01462-9.CrossRefPubMed
25.
go back to reference Donnarumma G, Buommino E, Fusco A, Paoletti I, Auricchio L, Tufano MA: Effect of temperature on the shift of Pseudomonas fluorescens from an environmental microorganism to a potential human pathogen. Int J Immunopathol Pharmacol. 23 (1): 227-234. Donnarumma G, Buommino E, Fusco A, Paoletti I, Auricchio L, Tufano MA: Effect of temperature on the shift of Pseudomonas fluorescens from an environmental microorganism to a potential human pathogen. Int J Immunopathol Pharmacol. 23 (1): 227-234.
26.
go back to reference Vikstrom E, Tafazoli F, Magnusson KE: Pseudomonas aeruginosa quorum sensing molecule N-(3 oxododecanoyl)-l-homoserine lactone disrupts epithelial barrier integrity of Caco-2 cells. FEBS Lett. 2006, 580 (30): 6921-6928. 10.1016/j.febslet.2006.11.057.CrossRefPubMed Vikstrom E, Tafazoli F, Magnusson KE: Pseudomonas aeruginosa quorum sensing molecule N-(3 oxododecanoyl)-l-homoserine lactone disrupts epithelial barrier integrity of Caco-2 cells. FEBS Lett. 2006, 580 (30): 6921-6928. 10.1016/j.febslet.2006.11.057.CrossRefPubMed
27.
go back to reference Dahan S, Dalmasso G, Imbert V, Peyron JF, Rampal P, Czerucka D: Saccharomyces boulardii interferes with enterohemorrhagic Escherichia coli-induced signaling pathways in T84 cells. Infect Immun. 2003, 71 (2): 766-773. 10.1128/IAI.71.2.766-773.2003.PubMedCentralCrossRefPubMed Dahan S, Dalmasso G, Imbert V, Peyron JF, Rampal P, Czerucka D: Saccharomyces boulardii interferes with enterohemorrhagic Escherichia coli-induced signaling pathways in T84 cells. Infect Immun. 2003, 71 (2): 766-773. 10.1128/IAI.71.2.766-773.2003.PubMedCentralCrossRefPubMed
28.
go back to reference Rossignol G, Sperandio D, Guerillon J, Duclairoir Poc C, Soum-Soutera E, Orange N, Feuilloley MG, Merieau A: Phenotypic variation in the Pseudomonas fluorescens clinical strain MFN1032. Res Microbiol. 2009, 160 (5): 337-344. 10.1016/j.resmic.2009.04.004.CrossRefPubMed Rossignol G, Sperandio D, Guerillon J, Duclairoir Poc C, Soum-Soutera E, Orange N, Feuilloley MG, Merieau A: Phenotypic variation in the Pseudomonas fluorescens clinical strain MFN1032. Res Microbiol. 2009, 160 (5): 337-344. 10.1016/j.resmic.2009.04.004.CrossRefPubMed
29.
go back to reference Lepage P, Seksik P, Sutren M, de la Cochetiere MF, Jian R, Marteau P, Dore J: Biodiversity of the mucosa-associated microbiota is stable along the distal digestive tract in healthy individuals and patients with IBD. Inflamm Bowel Dis. 2005, 11 (5): 473-480. 10.1097/01.MIB.0000159662.62651.06.CrossRefPubMed Lepage P, Seksik P, Sutren M, de la Cochetiere MF, Jian R, Marteau P, Dore J: Biodiversity of the mucosa-associated microbiota is stable along the distal digestive tract in healthy individuals and patients with IBD. Inflamm Bowel Dis. 2005, 11 (5): 473-480. 10.1097/01.MIB.0000159662.62651.06.CrossRefPubMed
30.
go back to reference Kazmierczak BI, Mostov K, Engel JN: Epithelial cell polarity alters Rho-GTPase responses to Pseudomonas aeruginosa. Mol Biol Cell. 2004, 15 (2): 411-419. 10.1091/mbc.E03-08-0559.PubMedCentralCrossRefPubMed Kazmierczak BI, Mostov K, Engel JN: Epithelial cell polarity alters Rho-GTPase responses to Pseudomonas aeruginosa. Mol Biol Cell. 2004, 15 (2): 411-419. 10.1091/mbc.E03-08-0559.PubMedCentralCrossRefPubMed
31.
go back to reference Schneeberger EE, Lynch RD: The tight junction: a multifunctional complex. Am J Physiol Cell Physiol. 2004, 286 (6): C1213-1228. 10.1152/ajpcell.00558.2003.CrossRefPubMed Schneeberger EE, Lynch RD: The tight junction: a multifunctional complex. Am J Physiol Cell Physiol. 2004, 286 (6): C1213-1228. 10.1152/ajpcell.00558.2003.CrossRefPubMed
32.
go back to reference Frankel FR, Tucker RW, Bruce J, Stenberg R: Fibroblasts and macrophages of mice with the Chediak-Higashi-like syndrome have microtubules and actin cables. J Cell Biol. 1978, 79 (2 Pt 1): 401-408. 10.1083/jcb.79.2.401.CrossRefPubMed Frankel FR, Tucker RW, Bruce J, Stenberg R: Fibroblasts and macrophages of mice with the Chediak-Higashi-like syndrome have microtubules and actin cables. J Cell Biol. 1978, 79 (2 Pt 1): 401-408. 10.1083/jcb.79.2.401.CrossRefPubMed
33.
go back to reference Puthenedam M, Williams PH, Lakshmi BS, Balakrishnan A: Modulation of tight junction barrier function by outer membrane proteins of enteropathogenic Escherichia coli: role of F-actin and junctional adhesion molecule-1. Cell Biol Int. 2007, 31 (8): 836-844. 10.1016/j.cellbi.2007.01.036.CrossRefPubMed Puthenedam M, Williams PH, Lakshmi BS, Balakrishnan A: Modulation of tight junction barrier function by outer membrane proteins of enteropathogenic Escherichia coli: role of F-actin and junctional adhesion molecule-1. Cell Biol Int. 2007, 31 (8): 836-844. 10.1016/j.cellbi.2007.01.036.CrossRefPubMed
34.
go back to reference Watson CJ, Hoare CJ, Garrod DR, Carlson GL, Warhurst G: Interferon-gamma selectively increases epithelial permeability to large molecules by activating different populations of paracellular pores. J Cell Sci. 2005, 118 (Pt 22): 5221-5230. 10.1242/jcs.02630.CrossRefPubMed Watson CJ, Hoare CJ, Garrod DR, Carlson GL, Warhurst G: Interferon-gamma selectively increases epithelial permeability to large molecules by activating different populations of paracellular pores. J Cell Sci. 2005, 118 (Pt 22): 5221-5230. 10.1242/jcs.02630.CrossRefPubMed
35.
go back to reference Macutkiewicz C, Carlson G, Clark E, Dobrindt U, Roberts I, Warhurst G: Characterisation of Escherichia coli strains involved in transcytosis across gut epithelial cells exposed to metabolic and inflammatory stress. Microbes Infect. 2008, 10 (4): 424-431. 10.1016/j.micinf.2008.01.001.CrossRefPubMed Macutkiewicz C, Carlson G, Clark E, Dobrindt U, Roberts I, Warhurst G: Characterisation of Escherichia coli strains involved in transcytosis across gut epithelial cells exposed to metabolic and inflammatory stress. Microbes Infect. 2008, 10 (4): 424-431. 10.1016/j.micinf.2008.01.001.CrossRefPubMed
36.
go back to reference Finlay BB, Falkow S: Salmonella interactions with polarized human intestinal Caco-2 epithelial cells. J Infect Dis. 1990, 162 (5): 1096-1106.CrossRefPubMed Finlay BB, Falkow S: Salmonella interactions with polarized human intestinal Caco-2 epithelial cells. J Infect Dis. 1990, 162 (5): 1096-1106.CrossRefPubMed
37.
go back to reference Fleiszig SM, Zaidi TS, Fletcher EL, Preston MJ, Pier GB: Pseudomonas aeruginosa invades corneal epithelial cells during experimental infection. Infect Immun. 1994, 62 (8): 3485-3493.PubMedCentralPubMed Fleiszig SM, Zaidi TS, Fletcher EL, Preston MJ, Pier GB: Pseudomonas aeruginosa invades corneal epithelial cells during experimental infection. Infect Immun. 1994, 62 (8): 3485-3493.PubMedCentralPubMed
38.
go back to reference Mezghani-Abdelmoula S, Khemiri A, Lesouhaitier O, Chevalier S, Orange N, Cazin L, Feuilloley MG: Sequential activation of constitutive and inducible nitric oxide synthase (NOS) in rat cerebellar granule neurons by Pseudomonas fluorescens and invasive behaviour of the bacteria. Microbiol Res. 2004, 159 (4): 355-363. 10.1016/j.micres.2004.08.003.CrossRefPubMed Mezghani-Abdelmoula S, Khemiri A, Lesouhaitier O, Chevalier S, Orange N, Cazin L, Feuilloley MG: Sequential activation of constitutive and inducible nitric oxide synthase (NOS) in rat cerebellar granule neurons by Pseudomonas fluorescens and invasive behaviour of the bacteria. Microbiol Res. 2004, 159 (4): 355-363. 10.1016/j.micres.2004.08.003.CrossRefPubMed
39.
go back to reference Kim SH, Wei CI: Invasiveness and intracellular growth of multidrug-resistant Salmonella and other pathogens in Caco-2 cells. J Food Sci. 2007, 72 (2): M72-78. 10.1111/j.1750-3841.2006.00268.x.CrossRefPubMed Kim SH, Wei CI: Invasiveness and intracellular growth of multidrug-resistant Salmonella and other pathogens in Caco-2 cells. J Food Sci. 2007, 72 (2): M72-78. 10.1111/j.1750-3841.2006.00268.x.CrossRefPubMed
40.
go back to reference Baker NT, Graham LL: Campylobacter fetus translocation across Caco-2 cell monolayers. Microb Pathog. 2010, 49 (5): 260-272. 10.1016/j.micpath.2010.06.008.CrossRefPubMed Baker NT, Graham LL: Campylobacter fetus translocation across Caco-2 cell monolayers. Microb Pathog. 2010, 49 (5): 260-272. 10.1016/j.micpath.2010.06.008.CrossRefPubMed
Metadata
Title
Pseudomonas fluorescens alters epithelial permeability and translocates across Caco-2/TC7 intestinal cells
Authors
Amar Madi
Pascal Svinareff
Nicole Orange
Marc GJ Feuilloley
Nathalie Connil
Publication date
01-12-2010
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2010
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/1757-4749-2-16

Other articles of this Issue 1/2010

Gut Pathogens 1/2010 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.