Lactobacillus rhamnosus L34 and Lactobacillus casei L39 suppress Clostridium difficile-induced IL-8 production by colonic epithelial cells

BMC Microbiology

Volumn 14, Issue 1, 2014, Pages

  Boonma, Prapaporn ^a   Spinler, Jennifer K ^b,c   Venable, Susan F ^b,c   Versalovic, James ^b,c   Tumwasorn, Somying ^a  

^a CHULALONGKORN UNIVERSITY   (Thailand)

^b TEXAS CHILDREN S HOSPITAL   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Anti inflammatory; Clostridium difficile; IL 8; Lactobacillus; Probiotic

Indexed keywords

GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; MESSENGER RNA; METRONIDAZOLE; PROBIOTIC AGENT; PROTEIN C JUN; VANCOMYCIN;

ANTIFUNGAL RESISTANCE; ARTICLE; BACTERIAL VIABILITY; CELL VIABILITY; CLOSTRIDIUM DIFFICILE INFECTION; COLON MUCOSA; COLONY FORMING UNIT; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DOWN REGULATION; EPITHELIUM CELL; GENETIC TRANSCRIPTION; HEAT TOLERANCE; HT 29 CELL LINE; HUMAN; HUMAN CELL; IMMUNOMODULATION; LACTOBACILLUS CASEI; LACTOBACILLUS RHAMNOSUS; MINIMUM INHIBITORY CONCENTRATION; NEUTROPHIL COUNT; NONHUMAN; TREATMENT RESPONSE; ANTIBIOSIS; CELL LINE; IMMUNOLOGY; MICROBIOLOGY; PEPTOCLOSTRIDIUM DIFFICILE; PHYSIOLOGY; SECRETION (PROCESS);

CLOSTRIDIUM DIFFICILE; LACTOBACILLUS; LACTOBACILLUS CASEI; LACTOBACILLUS RHAMNOSUS;

ANTIBIOSIS; CELL LINE; CLOSTRIDIUM DIFFICILE; EPITHELIAL CELLS; HUMANS; INTERLEUKIN-8; LACTOBACILLUS CASEI; LACTOBACILLUS RHAMNOSUS; PROBIOTICS;

EID: 84903413896     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-14-177     Document Type: Article

References (73)

1. Clostridium difficile colitis. Kelly CP, Pothoulakis C, LaMont JT, N Engl J Med 1994 330 4 257 262 10.1056/NEJM199401273300406 8043060 (Pubitemid 24034138)
2. Clostridium difficile infection. Kelly CP, LaMont JT, Annu Rev Med 1998 49 375 390 10.1146/annurev.med.49.1.375 9509270 (Pubitemid 28197461)
3. Effect of antibiotic therapy on human fecal microbiota and the relation to the development of Clostridium difficile. De La Cochetiere MF, Durand T, Lalande V, Petit JC, Potel G, Beaugerie L, Microb Ecol 2008 56 3 395 402 10.1007/s00248-007-9356-5 18209965
4. Clostridium difficile infection: new developments in epidemiology and pathogenesis. Rupnik M, Wilcox MH, Gerding DN, Nat Rev Microbiol 2009 7 7 526 536 10.1038/nrmicro2164 19528959
5. Clostridium difficile toxins: mechanism of action and role in disease. Voth DE, Ballard JD, Clin Microbiol Rev 2005 18 2 247 263 10.1128/CMR.18.2.247- 263.2005 15831824 (Pubitemid 40548293)
6. Glucosylation of small GTP-binding Rho proteins disrupts endothelial barrier function. Hippenstiel S, Tannert-Otto S, Vollrath N, Krull M, Just I, Aktories K, von Eichel-Streiber C, Suttorp N, Am J Physiol 1997 272 1 Pt 1 38 L43 9038900
7. Clostridium difficile toxins disrupt epithelial barrier function by altering membrane microdomain localization of tight junction proteins. Nusrat A, von Eichel-Streiber C, Turner JR, Verkade P, Madara JL, Parkos CA, Infect Immun 2001 69 3 1329 1336 10.1128/IAI.69.3.1329-1336.2001 11179295 (Pubitemid 32187577)
8. Mechanism of Clostridium difficile toxin A-induced apoptosis in T84 cells. Brito GA, Fujji J, Carneiro-Filho BA, Lima AA, Obrig T, Guerrant RL, J Infect Dis 2002 186 10 1438 1447 10.1086/344729 12404159 (Pubitemid 35286111)
9. Clostridium difficile toxin B is more potent than toxin A in damaging human colonic epithelium in vitro. Riegler M, Sedivy R, Pothoulakis C, Hamilton G, Zacherl J, Bischof G, Cosentini E, Feil W, Schiessel R, LaMont JT, Wenzl E, J Clin Invest 1995 95 5 2004 2011 10.1172/JCI117885 7738167
10. Effect of Clostridium difficile toxin A on human intestinal epithelial cells: induction of interleukin 8 production and apoptosis after cell detachment. Mahida YR, Makh S, Hyde S, Gray T, Borriello SP, Gut 1996 38 3 337 347 10.1136/gut.38.3.337 8675084 (Pubitemid 26075533)
11. Early functional effects of Clostridium difficile toxin A on human colonocytes. Branka JE, Vallette G, Jarry A, Bou-Hanna C, Lemarre P, Van PN, Laboisse CL, Gastroenterology 1997 112 6 1887 1894 10.1053/gast.1997.v112. pm9178681 9178681 (Pubitemid 27240775)
12. Differential expression and polarized secretion of CXC and CC chemokines by human intestinal epithelial cancer cell lines in response to Clostridium difficile toxin A. Kim JM, Kim JS, Jun HC, Oh YK, Song IS, Kim CY, Microbiol Immunol 2002 46 5 333 342 10.1111/j.1348-0421.2002.tb02704.x 12139393 (Pubitemid 34535007)
13. The enterotoxicity of Clostridium difficile toxins. Sun X, Savidge T, Feng H, Toxins (Basel) 2010 2 7 1848 1880 10.3390/toxins2071848 22069662
14. IL-8 secretion and neutrophil activation by HT-29 colonic epithelial cells. Kelly CP, Keates S, Siegenberg D, Linevsky JK, Pothoulakis C, Brady HR, Am J Physiol 1994 267 6 Pt 1 991 G997 7810667
15. The CXC-chemokine neutrophil-activating peptide-2 induces two distinct optima of neutrophil chemotaxis by differential interaction with interleukin-8 receptors CXCR-1 and CXCR-2. Ludwig A, Petersen F, Zahn S, Gotze O, Schroder JM, Flad HD, Brandt E, Blood 1997 90 11 4588 4597 9373270 (Pubitemid 27508465)
16. Clostridium difficile toxin A stimulates macrophage-inflammatory protein-2 production in rat intestinal epithelial cells. Castagliuolo I, Keates AC, Wang CC, Pasha A, Valenick L, Kelly CP, Nikulasson ST, LaMont JT, Pothoulakis C, J Immunol 1998 160 12 6039 6045 9637520 (Pubitemid 28298067)
17. IL-8 induces neutrophil chemotaxis predominantly via type I IL-8 receptors. Hammond ME, Lapointe GR, Feucht PH, Hilt S, Gallegos CA, Gordon CA, Giedlin MA, Mullenbach G, Tekamp-Olson P, J Immunol 1995 155 3 1428 1433 7636208
18. Discrete steps in binding and signaling of interleukin-8 with its receptor. Wu L, Ruffing N, Shi X, Newman W, Soler D, Mackay CR, Qin S, J Biol Chem 1996 271 49 31202 31209 10.1074/jbc.271.49.31202 8940121 (Pubitemid 26408564)
19. Neutrophil-activating peptides NAP-2 and IL-8 bind to the same sites on neutrophils but interact in different ways. Discrepancies in binding affinities, receptor densities, and biologic effects. Petersen F, Flad HD, Brandt E, J Immunol 1994 152 5 2467 2478 8133058 (Pubitemid 24097939)
20. [Ca2+]i changes and respiratory burst in human neutrophils and monocytes induced by NAP-1/interleukin-8, NAP-2, and gro/MGSA. Walz A, Meloni F, Clark-Lewis I, von Tscharner V, Baggiolini M, J Leukoc Biol 1991 50 3 279 286 1856598
21. Differential effects of neutrophil-activating peptide 1/IL-8 and its homologues on leukocyte adhesion and phagocytosis. Detmers PA, Powell DE, Walz A, Clark-Lewis I, Baggiolini M, Cohn ZA, J Immunol 1991 147 12 4211 4217 1721641
22. Functional modulation of human intestinal epithelial cell responses by Bifidobacterium infantis and Lactobacillus salivarius. O'Hara AM, O'Regan P, Fanning A, O'Mahony C, Macsharry J, Lyons A, Bienenstock J, O'Mahony L, Shanahan F, Immunology 2006 118 2 202 215 10.1111/j.1365-2567.2006.02358.x 16771855 (Pubitemid 43727425)
23. Mechanisms of action of probiotics: recent advances. Ng SC, Hart AL, Kamm MA, Stagg AJ, Knight SC, Inflamm Bowel Dis 2009 15 2 300 310 10.1002/ibd.20602 18626975
24. Meta-analysis of probiotics for the prevention of antibiotic associated diarrhea and the treatment of Clostridium difficile disease. McFarland LV, Am J Gastroenterol 2006 101 4 812 822 10.1111/j.1572-0241.2006.00465.x 16635227
25. Probiotics for the prevention and treatment of antibiotic-associated diarrhea: a systematic review and meta-analysis. Hempel S, Newberry SJ, Maher AR, Wang Z, Miles JN, Shanman R, Johnsen B, Shekelle PG, JAMA 2012 307 18 1959 1969 10.1001/jama.2012.3507 22570464
26. Prevention of beta-lactam-associated diarrhea by Saccharomyces boulardii compared with placebo. McFarland LV, Surawicz CM, Greenberg RN, Elmer GW, Moyer KA, Melcher SA, Bowen KE, Cox JL, Am J Gastroenterol 1995 90 3 439 448 7872284
27. A randomized placebo-controlled trial of Saccharomyces boulardii in combination with standard antibiotics for Clostridium difficile disease. McFarland LV, Surawicz CM, Greenberg RN, Fekety R, Elmer GW, Moyer KA, Melcher SA, Bowen KE, Cox JL, Noorani Z, Harrington G, Rubin M, Greenwald D, JAMA 1994 271 24 1913 1918 10.1001/jama.1994.03510480037031 8201735 (Pubitemid 24177098)
28. Recurrent Clostridium difficile diarrhoea. Kyne L, Kelly CP, Gut 2001 49 1 152 153 10.1136/gut.49.1.152 11413124 (Pubitemid 32601893)
29. Saccharomyces boulardii protease inhibits the effects of Clostridium difficile toxins A and B in human colonic mucosa. Castagliuolo I, Riegler MF, Valenick L, LaMont JT, Pothoulakis C, Infect Immun 1999 67 1 302 307 9864230 (Pubitemid 29021663)
30. Saccharomyces boulardii inhibits ERK1/2 mitogen-activated protein kinase activation both in vitro and in vivo and protects against Clostridium difficile toxin A-induced enteritis. Chen X, Kokkotou EG, Mustafa N, Bhaskar KR, Sougioultzis S, O'Brien M, Pothoulakis C, Kelly CP, J Biol Chem 2006 281 34 24449 24454 10.1074/jbc.M605200200 16816386 (Pubitemid 44274218)
31. Lactobacillus delbrueckii ssp. bulgaricus B-30892 can inhibit cytotoxic effects and adhesion of pathogenic Clostridium difficile to Caco-2 cells. Banerjee P, Merkel GJ, Bhunia AK, Gut Pathog 2009 1 1 8 10.1186/1757-4749-1-8 19397787
32. Co-culture with potentially probiotic microorganisms antagonises virulence factors of Clostridium difficile in vitro. Trejo FM, Perez PF, De Antoni GL, Antonie Van Leeuwenhoek 2010 98 1 19 29 10.1007/s10482-010-9424-6 20232250
33. Draft genome sequences and description of Lactobacillus rhamnosus strains L31, L34, and L35. Boonma P, Spinler JK, Qin X, Jittaprasatsin C, Muzny DM, Doddapaneni H, Gibbs R, Petrosino J, Tumwasorn S, Versalovic J, Stand Genomic Sci 2014 In press
34. The granulocyte-macrophage colony-stimulating factor receptor: linking its structure to cell signaling and its role in disease. Hercus TR, Thomas D, Guthridge MA, Ekert PG, King-Scott J, Parker MW, Lopez AF, Blood 2009 114 7 1289 1298 10.1182/blood-2008-12-164004 19436055
35. Prolongation of survival of human polymorphonuclear neutrophils by granulocyte-macrophage colony-stimulating factor is caused by inhibition of programmed cell death. Brach MA, de Vos S, Gruss HJ, Herrmann F, Blood 1992 80 11 2920 2924 1280481
36. Differential regulation of neutrophil chemotaxis to IL-8 and fMLP by GM-CSF: lack of direct effect of oestradiol. Shen L, Smith JM, Shen Z, Hussey SB, Wira CR, Fanger MW, Immunology 2006 117 2 205 212 10.1111/j.1365-2567.2005. 02280.x 16423056
37. Treatment of Clostridium difficile-associated disease. Leffler DA, Lamont JT, Gastroenterology 2009 136 6 1899 1912 10.1053/j.gastro.2008.12.070 19457418
38. Clinical practice guidelines for Clostridium difficile infection in adults: 2010 update by the society for healthcare epidemiology of America (SHEA) and the infectious diseases society of America (IDSA). Cohen SH, Gerding DN, Johnson S, Kelly CP, Loo VG, McDonald LC, Pepin J, Wilcox MH, Infect Control Hosp Epidemiol 2010 31 5 431 455 10.1086/651706 20307191
39. Calcium regulation of GM-CSF by calmodulin-dependent kinase II phosphorylation of Ets1. Liu H, Grundstrom T, Mol Biol Cell 2002 13 12 4497 4507 10.1091/mbc.E02-03-0149 12475968 (Pubitemid 35471201)
40. NF-kappa B activation pathway is essential for the chemokine expression in intestinal epithelial cells stimulated with Clostridium difficile toxin A. Kim JM, Lee JY, Yoon YM, Oh YK, Youn J, Kim YJ, Scand J Immunol 2006 63 6 453 460 10.1111/j.1365-3083.2006.001756.x 16764699 (Pubitemid 43978860)
41. Epithelial cell I kappa B-kinase beta has an important protective role in Clostridium difficile toxin A-induced mucosal injury. Chae S, Eckmann L, Miyamoto Y, Pothoulakis C, Karin M, Kagnoff MF, J Immunol 2006 177 2 1214 1220 10.4049/jimmunol.177.2.1214 16818780 (Pubitemid 44036626)
42. Transcription factor AP-1 regulation by mitogen-activated protein kinase signal transduction pathways. Whitmarsh AJ, Davis RJ, J Mol Med (Berl) 1996 74 10 589 607 10.1007/s001090050063 8912180 (Pubitemid 26343761)
43. Breaking the cycle: treatment strategies for 163 cases of recurrent Clostridium difficile disease. McFarland LV, Elmer GW, Surawicz CM, Am J Gastroenterol 2002 97 7 1769 1775 10.1111/j.1572-0241.2002.05839.x 12135033 (Pubitemid 34761404)
44. Increasing risk of relapse after treatment of Clostridium difficile colitis in Quebec, Canada. Pepin J, Alary ME, Valiquette L, Raiche E, Ruel J, Fulop K, Godin D, Bourassa C, Clin Infect Dis 2005 40 11 1591 1597 10.1086/430315 15889355 (Pubitemid 40720808)
45. Clostridium difficile-more difficult than ever. Kelly CP, LaMont JT, N Engl J Med 2008 359 18 1932 1940 10.1056/NEJMra0707500 18971494
46. Risk factors for recurrence of Clostridium difficile infection: effect of vancomycin-resistant enterococci colonization. Choi HK, Kim KH, Lee SH, Lee SJ, J Korean Med Sci 2011 26 7 859 864 10.3346/jkms.2011.26.7.859 21738336
47. Fidaxomicin versus vancomycin for Clostridium difficile infection. Louie TJ, Miller MA, Mullane KM, Weiss K, Lentnek A, Golan Y, Gorbach S, Sears P, Shue YK, N Engl J Med 2011 364 5 422 431 10.1056/NEJMoa0910812 21288078
48. Fidaxomicin versus vancomycin for infection with Clostridium difficile in Europe, Canada, and the USA: a double-blind, non-inferiority, randomised controlled trial. Cornely OA, Crook DW, Esposito R, Poirier A, Somero MS, Weiss K, Sears P, Gorbach S, Lancet Infect Dis 2012 12 4 281 289 10.1016/S1473- 3099(11)70374-7 22321770
49. Predictors of first recurrence in Clostridium difficile-associated disease. A study of 306 patients hospitalized in a Romanian tertiary referral center. Lupse M, Flonta M, Cioara A, Filipescu I, Todor N, J Gastrointestin Liver Dis 2013 22 4 397 403 24369321
50. Treatment of recurrent Clostridium difficile colitis with Lactobacillus GG. Biller JA, Katz AJ, Flores AF, Buie TM, Gorbach SL, J Pediatr Gastroenterol Nutr 1995 21 2 224 226 10.1097/00005176-199508000-00016 7472911
51. Lactobacillus plantarum 299v for the treatment of recurrent Clostridium difficile-associated diarrhoea: a double-blind, placebo-controlled trial. Wullt M, Hagslatt ML, Odenholt I, Scand J Infect Dis 2003 35 6-7 365 367 12953945 (Pubitemid 37038627)
52. Interaction of lactic acid bacteria with the gut immune system. Perdigon G, Maldonado Galdeano C, Valdez JC, Medici M, Eur J Clin Nutr 2002 56 Suppl 4 21 S26 12556943
53. Human mucosal in vivo transcriptome responses to three lactobacilli indicate how probiotics may modulate human cellular pathways. van Baarlen P, Troost F, van der Meer C, Hooiveld G, Boekschoten M, Brummer RJ, Kleerebezem M, Proc Natl Acad Sci U S A 2010 108 Suppl 1 4562 4569 20823239
54. Inhibition of Escherichia coli O157:H7 attachment by interactions between lactic acid bacteria and intestinal epithelial cells. Kim Y, Kim SH, Whang KY, Kim YJ, Oh S, J Microbiol Biotechnol 2008 18 7 1278 1285 18667857
55. Probiotics for the prevention of antibiotic-associated diarrhea and Clostridium difficile infection among hospitalized patients: systematic review and meta-analysis. Pattani R, Palda VA, Hwang SW, Shah PS, Open Med 2013 7 2 56 e67 24348885
56. Commensal-derived probiotics as anti-inflammatory agents. Versalovic J, Iyer C, Ping Lin Y, Huang Y, Dobrogosz W, Microb Ecol Health Dis 2008 20 86 93 10.1080/08910600802106491
57. Clostridial toxins: sensing a target in a hostile gut environment. Oezguen N, Power TD, Urvil P, Feng H, Pothoulakis C, Stamler JS, Braun W, Savidge TC, Gut Microbes 2012 3 1 35 41 10.4161/gmic.19250 22356854
58. Anti-inflammatory activity of probiotic Bifidobacterium: enhancement of IL-10 production in peripheral blood mononuclear cells from ulcerative colitis patients and inhibition of IL-8 secretion in HT-29 cells. Imaoka A, Shima T, Kato K, Mizuno S, Uehara T, Matsumoto S, Setoyama H, Hara T, Umesaki Y, World J Gastroenterol 2008 14 16 2511 2516 10.3748/wjg.14.2511 18442197 (Pubitemid 352037738)
59. Molecular mechanism of interleukin-8 gene expression. Mukaida N, Okamoto S, Ishikawa Y, Matsushima K, J Leukoc Biol 1994 56 5 554 558 7525815 (Pubitemid 24348811)
60. Effects of transcription factor activator protein-1 on interleukin-8 expression and enteritis in response to Clostridium difficile toxin A. Lee JY, Park HR, Oh YK, Kim YJ, Youn J, Han JS, Kim JM, J Mol Med 2007 85 12 1393 1404 10.1007/s00109-007-0237-7 17639289 (Pubitemid 350234093)
61. Live Lactobacillus rhamnosus [corrected] is essential for the inhibitory effect on tumor necrosis factor alpha-induced interleukin-8 expression. Ma D, Forsythe P, Bienenstock J, Infect Immun 2004 72 9 5308 5314 10.1128/IAI.72.9. 5308-5314.2004 15322027 (Pubitemid 39223418)
62. Saccharomyces boulardii interferes with Shigella pathogenesis by postinvasion signaling events. Mumy KL, Chen X, Kelly CP, McCormick BA, Am J Physiol Gastrointest Liver Physiol 2008 294 3 599 G609 10.1152/ajpgi.00391.2007 18032477 (Pubitemid 351468759)
63. Saccharomyces boulardii interferes with enterohemorrhagic Escherichia coli-induced signaling pathways in T84 cells. Dahan S, Dalmasso G, Imbert V, Peyron JF, Rampal P, Czerucka D, Infect Immun 2003 71 2 766 773 10.1128/IAI.71.2.766-773.2003 12540556 (Pubitemid 36150770)
64. Saccharomyces boulardii prevents TNF-alpha-induced apoptosis in EHEC-infected T84 cells. Dalmasso G, Loubat A, Dahan S, Calle G, Rampal P, Czerucka D, Res Microbiol 2006 157 5 456 465 10.1016/j.resmic.2005.11.007 16487684 (Pubitemid 43833214)
65. Saccharomyces boulardii produces a soluble anti-inflammatory factor that inhibits NF-KB-mediated IL-8 gene expression. Sougioultzis S, Simeonidis S, Bhaskar KR, Chen X, Anton PM, Keates S, Pothoulakis C, Kelly CP, Biochem Biophys Res Commun 2006 343 1 69 76 10.1016/j.bbrc.2006.02.080 16529714
66. Soluble proteins produced by probiotic bacteria regulate intestinal epithelial cell survival and growth. Yan F, Cao H, Cover TL, Whitehead R, Washington MK, Polk DB, Gastroenterology 2007 132 2 562 575 10.1053/j.gastro. 2006.11.022 17258729 (Pubitemid 46274659)
67. Histamine derived from probiotic Lactobacillus reuteri suppresses TNF via modulation of PKA and ERK signaling. Thomas CM, Hong T, van Pijkeren JP, Hemarajata P, Trinh DV, Hu W, Britton RA, Kalkum M, Versalovic J, PLoS One 2012 7 2 31951 10.1371/journal.pone.0031951 22384111
68. Fecal microbiota transplantation for relapsing Clostridium difficile infection in 26 patients: methodology and results. Kelly CR, de Leon L, Jasutkar N, J Clin Gastroenterol 2012 46 2 145 149 10.1097/MCG.0b013e318234570b 22157239
69. Fecal transplant against relapsing Clostridium difficile-associated diarrhea in 32 patients. Jorup-Ronstrom C, Hakanson A, Sandell S, Edvinsson O, Midtvedt T, Persson AK, Norin E, Scand J Gastroenterol 2012 47 5 548 552 10.3109/00365521.2012.672587 22468996
70. Rapid detection of Clostridium difficile in feces by real-time PCR. Belanger SD, Boissinot M, Clairoux N, Picard FJ, Bergeron MG, J Clin Microbiol 2003 41 2 730 734 10.1128/JCM.41.2.730-734.2003 12574274 (Pubitemid 36184188)
71. NCCLS, Methods for Antimicrobial Susceptibility Testing of Anaerobic Bacteria; Approved Standard-Sixth Edition 940 West Valley Road, Suite 1400, Wayne, Pennsylvania19087-1898 USA: NCCLS NCCLS document M11-A6 [ISBN 1-56238-517-8]. 2004
72. Lactobacillus saerimneri and Lactobacillus ruminis: novel human-derived probiotic strains with immunomodulatory activities. Taweechotipatr M, Iyer C, Spinler JK, Versalovic J, Tumwasorn S, FEMS Microbiol Lett 2009 293 1 65 72 10.1111/j.1574-6968.2009.01506.x 19222575
73. A new mathematical model for relative quantification in real-time RT-PCR. Pfaffl MW, Nucleic Acids Res 2001 29 9 45 10.1093/nar/29.9.e45 11328886