Immunobiotic Lactobacillus rhamnosus strains differentially modulate antiviral immune response in porcine intestinal epithelial and antigen presenting cells

BMC Microbiology

Volumn 14, Issue 1, 2014, Pages

  Villena, Julio ^a,b   Chiba, Eriko ^a   Vizoso Pinto, Maria Guadalupe ^c   Tomosada, Yohsuke ^a   Takahashi, Takuya ^a   Ishizuka, Takamasa ^a   Aso, Hisashi ^a   Salva, Susana ^b   Alvarez, Susana ^b   Kitazawa, Haruki ^a  

^a TOHOKU UNIVERSITY   (Japan)

^b CENTRO DE REFERENCIA PARA LACTOBACILOS CERELA CONICET   (Argentina)

^c UNIVERSIDAD NACIONAL DE TUCUMÁN   (Argentina)

Author keywords

Antiviral immunity; Intestinal antigen presenting cells; Lactobacillus rhamnosus; PIE cells; Poly(I:C); TLR2

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 6; MESSENGER RNA; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE; HLA ANTIGEN CLASS 2; IMMUNOGLOBULIN RECEPTOR; IMMUNOLOGIC FACTOR; PROBIOTIC AGENT;

ADHERENT CELL; ANIMAL EXPERIMENT; ANTIGEN PRESENTING CELL; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENSITY GRADIENT CENTRIFUGATION; DIARRHEA; FLOW CYTOMETRY; GENE EXPRESSION; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; IMMUNOREGULATION; IN VITRO STUDY; INNATE IMMUNITY; INTESTINE CELL; INTESTINE EPITHELIUM CELL; LACTOBACILLUS RHAMNOSUS; MONOCULTURE; NONHUMAN; PROFESSIONAL KNOWLEDGE; SIGNAL TRANSDUCTION; SWINE; ANIMAL; BIOSYNTHESIS; CELL CULTURE; EPITHELIUM CELL; GENE EXPRESSION PROFILING; GENETICS; IMMUNOLOGY; PIG; VIROLOGY;

ANIMALS; ANTIGEN-PRESENTING CELLS; CELLS, CULTURED; CYTOKINES; EPITHELIAL CELLS; GENE EXPRESSION PROFILING; HISTOCOMPATIBILITY ANTIGENS CLASS II; IMMUNOLOGIC FACTORS; LACTOBACILLUS RHAMNOSUS; PROBIOTICS; RECEPTORS, IMMUNOLOGIC; SWINE;

EID: 84901672443     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-14-126     Document Type: Article

References (50)

1. Can the world afford to save the lives of 6 million children each year? Bryce J, Black RE, Walker N, Bhutta ZA, Lawn JE, Steketee RW, Lancet 2005 365 9478 2193 2200 10.1016/S0140-6736(05)66777-3 15978927 (Pubitemid 40853912)
2. Global and regional burden of disease and risk factors, 2001: systematic analysis of population health data. Lopez AD, Mathers CD, Ezzati M, Jamison DT, Murray CJ, Lancet 2006 367 9524 1747 1757 10.1016/S0140-6736(06)68770-9 16731270 (Pubitemid 43767064)
3. Rotavirus and severe childhood diarrhea. Parashar UD, Gibson CJ, Bresee JS, Glass RI, Emerg Infect Dis 2006 12 2 304 306 10.3201/eid1202.050006 16494759
4. Rotaviruses: from pathogenesis to vaccination. Greenberg HB, Estes MK, Gastroenterology 2009 136 6 1939 1951 10.1053/j.gastro.2009.02.076 19457420
5. Remaining issues and challenges for rotavirus vaccine in preventing global childhood diarrheal morbidity and mortality. Tate JE, Patel MM, Cortese MM, Lopman BA, Gentsch JR, Fleming J, Steele AD, Parashar UD, Expert Rev Vaccines 2012 11 2 211 220 10.1586/erv.11.184 22309669
6. Rotavirus immune responses and correlates of protection. Angel J, Franco MA, Greenberg HB, Curr Opin Virol 2012 2 4 419 425 10.1016/j.coviro.2012.05.003 22677178
7. Efficacy of high-dose Lactobacillus rhamnosus GG in controlling acute watery diarrhea in Indian children: a randomized controlled trial. Basu S, Paul DK, Ganguly S, Chatterjee M, Chandra PK, J Clin Gastroenterol 2009 43 3 208 213 10.1097/MCG.0b013e31815a5780 18813028
8. Porcine small intestinal epithelial cell line (IPEC-J2) of rotavirus infection as a new model for the study of innate immune responses to rotaviruses and probiotics. Liu F, Li G, Wen K, Bui T, Cao D, Zhang Y, Yuan L, Viral Immunol 2010 23 2 135 149 10.1089/vim.2009.0088 20373994
9. Lactic acid bacteria efficiently protect human and animal intestinal epithelial and immune cells from enteric virus infection. Maragkoudakis PA, Chingwaru W, Gradisnik L, Tsakalidou E, Cencic A, Int J Food Microbiol 2010 141 Suppl 1 91 S97 20106541
10. Development of a fermented goats' milk containing Lactobacillus rhamnosus: in vivo study of health benefits. Salva S, Nunez M, Villena J, Ramon A, Font G, Alvarez S, J Sci Food Agric 2011 91 13 2355 2362 10.1002/jsfa.4467 21604277
11. Immunomodulatory activity of Lactobacillus rhamnosus strains isolated from goat milk: impact on intestinal and respiratory infections. Salva S, Villena J, Alvarez S, Int J Food Microbiol 2010 141 1-2 82 89 20395002
12. Probiotics for everyone! The novel immunobiotic Lactobacillus rhamnosus CRL1505 and the beginning of Social Probiotic Programs in Argentina. Villena J, Salva S, Nuñez M, Corzo J, Tolaba R, Faedda J, Font G, Alvarez S, Int J Biotechnol Wellness Industries 2012 In Press
13. Comparison of human metapneumovirus, respiratory syncytial virus and influenza A virus lower respiratory tract infections in hospitalized young children. Wolf DG, Greenberg D, Kalkstein D, Shemer-Avni Y, Givon-Lavi N, Saleh N, Goldberg MD, Dagan R, Pediatr Infect Dis J 2006 25 4 320 324 10.1097/01.inf.0000207395.80657.cf 16567983
14. Epidemiology of community-acquired pneumonia in children of Latin America and the Caribbean: a systematic review and meta-analysis. Gentile A, Bardach A, Ciapponi A, Garcia-Marti S, Aruj P, Glujovsky D, Calcagno JI, Mazzoni A, Colindres RE, Int J Infect Dis 2012 16 1 5 e15 10.1016/j.ijid.2011.09.013 22056731
15. Stimulation of macrophages by immunobiotic Lactobacillus strains: influence beyond the intestinal tract. Marranzino G, Villena J, Salva S, Alvarez S, Microbiol Immunol 2012 56 771 781 10.1111/j.1348-0421.2012.00495.x 22846065
16. Orally administered Lactobacillus rhamnosus modulates the respiratory immune response triggered by the viral pathogen-associated molecular pattern poly(I:C). Villena J, Chiba E, Tomosada Y, Salva S, Marranzino G, Kitazawa H, Alvarez S, BMC Immunol 2012 13 53 10.1186/1471-2172-13-53 22989047
17. Intestinal epithelial cells as a source of inflammatory cytokines and chemokines. Stadnyk AW, Can J Gastroenterol 2002 16 4 241 246 11981577 (Pubitemid 34727590)
18. Innate immune recognition of viral infection. Kawai T, Akira S, Nat Immun 2006 7 2 131 137 10.1038/ni1303 (Pubitemid 43135878)
19. MDA5/RIG-I and virus recognition. Takeuchi O, Akira S, Curr Opin Immunol 2008 20 1 17 22 10.1016/j.coi.2008.01.002 18272355
20. Innate immunity to virus infection. Takeuchi O, Akira S, Immunol Rev 2009 227 1 75 86 10.1111/j.1600-065X.2008.00737.x 19120477
21. Immunobiotic Lactobacillus jensenii Modulates the Toll-Like Receptor 4-Induced Inflammatory Response via Negative Regulation in Porcine Antigen-Presenting Cells. Villena J, Suzuki R, Fujie H, Chiba E, Takahashi T, Tomosada Y, Shimazu T, Aso H, Ohwada S, Suda Y, Ikegami S, Itoh H, Alvarez S, Saito T, Kitazawa H, Clin Vaccine Immunol 2012 19 7 1038 1053 10.1128/CVI.00199-12 22573738
22. Immunobiotic lactic acid bacteria beneficially regulate immune response triggered by poly(I:C) in porcine intestinal epithelial cells. Hosoya S, Villena J, Shimazu T, Tohno M, Fujie H, Chiba E, Shimosato T, Aso H, Suda Y, Kawai Y, Saito T, Alvarez S, Ikegami S, Itoh H, Kitazawa H, Vet Res 2011 42 1 111 10.1186/1297-9716-42-111 22046952
23. Advanced application of porcine intestinal epithelial cells for the selection of immunobiotics modulating toll-like receptor 3-mediated inflammation. Hosoya S, Villena J, Chiba E, Shimazu T, Suda Y, Aso H, Saito T, Kitazawa H, J Microbiol Immunol Infect 2013 46 6 474 478 10.1016/j.jmii.2012.04. 005 22727542
24. Toll-like receptor 4 and cytokine expression involved in functional immune response in an originally established porcine intestinal epitheliocyte cell line. Moue M, Tohno M, Shimazu T, Kido T, Aso H, Saito T, Kitazawa H, Biochim Biophys Acta 2008 1780 2 134 144 10.1016/j.bbagen.2007.11.006 18082146
25. Intestinal epithelia activate anti-viral signaling via intracellular sensing of rotavirus structural components. Frias AH, Vijay-Kumar M, Gentsch JR, Crawford SE, Carvalho FA, Estes MK, Gewirtz AT, Mucosal Immunol 2010 3 6 622 632 10.1038/mi.2010.39 20664578
26. Pathogen recognition by innate immunity and its signaling. Akira S, Proc Jpn Acad Ser B Phys Biol Sci 2009 85 4 143 156 10.2183/pjab.85.143 19367086
27. Innate immunity and adjuvants. Akira S, Philos Trans R Soc Lond B Biol Sci 2011 366 1579 2748 2755 10.1098/rstb.2011.0106 21893536
28. Toll-like receptors and RNA helicases: two parallel ways to trigger antiviral responses. Meylan E, Tschopp J, Mol Cell 2006 22 5 561 569 10.1016/j.molcel.2006.05.012 16762830 (Pubitemid 43817607)
29. Transcriptional signaling by double-stranded RNA: role of TLR3. Sen GC, Sarkar SN, Cytokine Growth Factor Rev 2005 16 1 1 14 10.1016/j.cytogfr.2005.01. 006 15733829 (Pubitemid 40279114)
30. Rotavirus-induced IFN-beta promotes anti-viral signaling and apoptosis that modulate viral replication in intestinal epithelial cells. Frias AH, Jones RM, Fifadara NH, Vijay-Kumar M, Gewirtz AT, Innate immunity 2012 18 2 294 306 10.1177/1753425911401930 21733977
31. Role of interferon in homologous and heterologous rotavirus infection in the intestines and extraintestinal organs of suckling mice. Feng N, Kim B, Fenaux M, Nguyen H, Vo P, Omary MB, Greenberg HB, J Virol 2008 82 15 7578 7590 10.1128/JVI.00391-08 18495762 (Pubitemid 352031225)
32. Rotavirus NSP1 inhibits expression of type I interferon by antagonizing the function of interferon regulatory factors IRF3, IRF5, and IRF7. Barro M, Patton JT, J Virol 2007 81 9 4473 4481 10.1128/JVI.02498-06 17301153 (Pubitemid 46668645)
33. Non-pathogenic bacteria elicit a differential cytokine response by intestinal epithelial cell/leucocyte co-cultures. Haller D, Bode C, Hammes WP, Pfeifer AM, Schiffrin EJ, Blum S, Gut 2000 47 1 79 87 10.1136/gut.47.1.79 10861268 (Pubitemid 30430415)
34. Role of intestinal epithelial cells in immune effects mediated by gram-positive probiotic bacteria: involvement of toll-like receptors. Vinderola G, Matar C, Perdigon G, Clin Diagn Lab Immunol 2005 12 9 1075 1084 16148174 (Pubitemid 41324539)
35. Comparative study of the protective capacity against Salmonella infection between probiotic and nonprobiotic Lactobacilli. Castillo NA, de Moreno de LeBlanc A, MG C, Perdigon G, J Appl Microbiol 2013 114 3 861 876 10.1111/jam.12074 23163296
36. Dynamic imaging of dendritic cell extension into the small bowel lumen in response to epithelial cell TLR engagement. Chieppa M, Rescigno M, Huang AY, Germain RN, J Exp Med 2006 203 13 2841 2852 10.1084/jem.20061884 17145958 (Pubitemid 46026162)
37. Selected commensal-related bacteria and Toll-like receptor 3 agonist combinatorial codes synergistically induce interleukin-12 production by dendritic cells to trigger a T helper type 1 polarizing programme. Baba N, Samson S, Bourdet-Sicard R, Rubio M, Sarfati M, Immunology 2009 128 1 Suppl 523 e531 19740313
38. Lactobacilli differentially modulate expression of cytokines and maturation surface markers in murine dendritic cells. Christensen HR, Frokiaer H, Pestka JJ, J Immunol 2002 168 1 171 178 10.4049/jimmunol.168.1.171 11751960 (Pubitemid 34014116)
39. Bacterial probiotic modulation of dendritic cells. Drakes M, Blanchard T, Czinn S, Infect Immun 2004 72 6 3299 3309 10.1128/IAI.72.6.3299-3309.2004 15155633 (Pubitemid 38697752)
40. Lactobacillus acidophilus induces virus immune defence genes in murine dendritic cells by a Toll-like receptor-2-dependent mechanism. Weiss G, Rasmussen S, Zeuthen LH, Nielsen BN, Jarmer H, Jespersen L, Frokiaer H, Immunology 2010 131 2 268 281 10.1111/j.1365-2567.2010.03301.x 20545783
41. Interferon gamma and interleukin 1, but not interferon alfa, inhibit rotavirus entry into human intestinal cell lines. Bass DM, Gastroenterology 1997 113 1 81 89 10.1016/S0016-5085(97)70083-0 9207265 (Pubitemid 27281761)
42. Early transcriptional response in the jejunum of germ-free piglets after oral infection with virulent rotavirus. Hulst M, Kerstens H, de Wit A, Smits M, van der Meulen J, Niewold T, Arch Virol 2008 153 7 1311 1322 10.1007/s00705-008-0118-6 18523839
43. Recognition of double-stranded RNA by TLR3 induces severe small intestinal injury in mice. Zhou R, Wei H, Sun R, Tian Z, J Immunol 2007 178 7 4548 4556 10.4049/jimmunol.178.7.4548 17372013 (Pubitemid 46492407)
44. Differential alteration in intestinal epithelial cell expression of toll-like receptor 3 (TLR3) and TLR4 in inflammatory bowel disease. Cario E, Podolsky DK, Infect Immun 2000 68 12 7010 7017 10.1128/IAI.68.12.7010-7017.2000 11083826 (Pubitemid 32463415)
45. The probiotic bacterium Lactobacillus casei induces activation of the gut mucosal immune system through innate immunity. Galdeano CM, Perdigon G, Clin Vaccine Immunol 2006 13 2 219 226 10.1128/CVI.13.2.219-226.2006 16467329 (Pubitemid 43383790)
46. Lactobacilli activate human dendritic cells that skew T cells toward T helper 1 polarization. Mohamadzadeh M, Olson S, Kalina WV, Ruthel G, Demmin GL, Warfield KL, Bavari S, Klaenhammer TR, Proc Natl Acad Sci U S A 2005 102 8 2880 2885 10.1073/pnas.0500098102 15710900 (Pubitemid 40299885)
47. Differential Toll-like receptor recognition and induction of cytokine profile by Bifidobacterium breve and Lactobacillus strains of probiotics. Plantinga TS, van Maren WW, van Bergenhenegouwen J, Hameetman M, Nierkens S, Jacobs C, de Jong DJ, Joosten LA, van't Land B, Garssen J, Clin Vaccine Immunol 2011 18 4 621 628 10.1128/CVI.00498-10 21288993
48. Epithelial crosstalk at the microbiota-mucosal interface. Wells JM, Rossi O, Meijerink M, van Baarlen P, Proc Natl Acad Sci USA 2010 108 (supple. 1) 4607 4614 pnas.1000092107: 1-8 20826446
49. Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Abreu MT, Nat Rev Immunol 2010 10 2 131 144 10.1038/nri2707 20098461
50. Regulators of innate immunity as novel targets for panviral therapeutics. Es-Saad S, Tremblay N, Baril M, Lamarre D, Curr Opin Virol 2012 2 5 622 628 10.1016/j.coviro.2012.08.009 23017246