期刊论文详细信息
BMC Microbiology
Immunobiotic Lactobacillus rhamnosus strains differentially modulate antiviral immune response in porcine intestinal epithelial and antigen presenting cells
Haruki Kitazawa2  Susana Alvarez3  Susana Salva3  Hisashi Aso1  Takamasa Ishizuka2  Takuya Takahashi2  Yohsuke Tomosada2  Maria Guadalupe Vizoso-Pinto4  Eriko Chiba2  Julio Villena3 
[1] Cell Biology Laboratory, Graduate School of Agricultural Science, Tohoku University, Sendai 981-8555, Japan;Food and Feed Immunology Group, Laboratory of Animal Products Chemistry, Graduate School of Agricultural Science, Tohoku University, Sendai 981-8555, Japan;Laboratory of Immunobiotechnology, Reference Centre for Lactobacilli (CERELA-CONICET), Tucuman, Argentina;INSIBIO-CONICET, Biomedical Department, Faculty of Medicine, National University of Tucumán, Tucumán, Argentina
关键词: TLR2;    Intestinal antigen presenting cells;    PIE cells;    Antiviral immunity;    Poly(I:C);    Lactobacillus rhamnosus;   
Others  :  1141085
DOI  :  10.1186/1471-2180-14-126
 received in 2013-05-06, accepted in 2014-05-07,  发布年份 2014
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【 摘 要 】

Background

Previous findings suggested that Lactobacillus rhamnosus CRL1505 is able to increase resistance of children to intestinal viral infections. However, the intestinal cells, cytokines and receptors involved in the immunoregulatory effect of this probiotic strain have not been fully characterized.

Results

We aimed to gain insight into the mechanisms involved in the immunomodulatory effect of the CRL1505 strain and therefore evaluated in vitro the crosstalk between L. rhamnosus CRL1505, porcine intestinal epithelial cells (IECs) and antigen presenting cells (APCs) from swine Peyer’s patches in order to deepen our knowledge about the mechanisms, through which this strain may help preventing viral diarrhoea episodes. L. rhamnosus CRL1505 was able to induce IFN–α and –β in IECs and improve the production of type I IFNs in response to poly(I:C) challenge independently of Toll-like receptor (TLR)-2 or TLR9 signalling. In addition, the CRL1505 strain induced mRNA expression of IL-6 and TNF-α via TLR2 in IECs. Furthermore, the strain significantly increased surface molecules expression and cytokine production in intestinal APCs. The improved Th1 response induced by L. rhamnosus CRL1505 was triggered by TLR2 signalling and included augmented expression of MHC-II and co-stimulatory molecules and expression of IL-1β, IL-6, and IFN-γ in APCs. IL-10 was also significantly up-regulated by CRL1505 in APCs.

Conclusions

It was recently reviewed the emergence of TLR agonists as new ways to transform antiviral treatments by introducing panviral therapeutics with less adverse effects than IFN therapies. The use of L. rhamnosus CRL1505 as modulator of innate immunity and inductor of antiviral type I IFNs, IFN-γ, and regulatory IL-10 clearly offers the potential to overcome this challenge.

【 授权许可】

   
2014 Villena et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Bryce J, Black RE, Walker N, Bhutta ZA, Lawn JE, Steketee RW: Can the world afford to save the lives of 6 million children each year? Lancet 2005, 365(9478):2193-2200.
  • [2]Lopez AD, Mathers CD, Ezzati M, Jamison DT, Murray CJ: Global and regional burden of disease and risk factors, 2001: systematic analysis of population health data. Lancet 2006, 367(9524):1747-1757.
  • [3]Parashar UD, Gibson CJ, Bresee JS, Glass RI: Rotavirus and severe childhood diarrhea. Emerg Infect Dis 2006, 12(2):304-306.
  • [4]Greenberg HB, Estes MK: Rotaviruses: from pathogenesis to vaccination. Gastroenterology 2009, 136(6):1939-1951.
  • [5]Tate JE, Patel MM, Cortese MM, Lopman BA, Gentsch JR, Fleming J, Steele AD, Parashar UD: Remaining issues and challenges for rotavirus vaccine in preventing global childhood diarrheal morbidity and mortality. Expert Rev Vaccines 2012, 11(2):211-220.
  • [6]Angel J, Franco MA, Greenberg HB: Rotavirus immune responses and correlates of protection. Curr Opin Virol 2012, 2(4):419-425.
  • [7]Basu S, Paul DK, Ganguly S, Chatterjee M, Chandra PK: Efficacy of high-dose Lactobacillus rhamnosus GG in controlling acute watery diarrhea in Indian children: a randomized controlled trial. J Clin Gastroenterol 2009, 43(3):208-213.
  • [8]Liu F, Li G, Wen K, Bui T, Cao D, Zhang Y, Yuan L: 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. Viral Immunol 2010, 23(2):135-149.
  • [9]Maragkoudakis PA, Chingwaru W, Gradisnik L, Tsakalidou E, Cencic A: Lactic acid bacteria efficiently protect human and animal intestinal epithelial and immune cells from enteric virus infection. Int J Food Microbiol 2010, 141(Suppl 1):S91-S97.
  • [10]Salva S, Nunez M, Villena J, Ramon A, Font G, Alvarez S: Development of a fermented goats' milk containing Lactobacillus rhamnosus: in vivo study of health benefits. J Sci Food Agric 2011, 91(13):2355-2362.
  • [11]Salva S, Villena J, Alvarez S: Immunomodulatory activity of Lactobacillus rhamnosus strains isolated from goat milk: impact on intestinal and respiratory infections. Int J Food Microbiol 2010, 141(1–2):82-89.
  • [12]Villena J, Salva S, Nuñez M, Corzo J, Tolaba R, Faedda J, Font G, Alvarez S: Probiotics for everyone! The novel immunobiotic Lactobacillus rhamnosus CRL1505 and the beginning of Social Probiotic Programs in Argentina. Int J Biotechnol Wellness Industries 2012. In Press
  • [13]Wolf DG, Greenberg D, Kalkstein D, Shemer-Avni Y, Givon-Lavi N, Saleh N, Goldberg MD, Dagan R: Comparison of human metapneumovirus, respiratory syncytial virus and influenza A virus lower respiratory tract infections in hospitalized young children. Pediatr Infect Dis J 2006, 25(4):320-324.
  • [14]Gentile A, Bardach A, Ciapponi A, Garcia-Marti S, Aruj P, Glujovsky D, Calcagno JI, Mazzoni A, Colindres RE: Epidemiology of community-acquired pneumonia in children of Latin America and the Caribbean: a systematic review and meta-analysis. Int J Infect Dis 2012, 16(1):e5-e15.
  • [15]Marranzino G, Villena J, Salva S, Alvarez S: Stimulation of macrophages by immunobiotic Lactobacillus strains: influence beyond the intestinal tract. Microbiol Immunol 2012, 56:771-781.
  • [16]Villena J, Chiba E, Tomosada Y, Salva S, Marranzino G, Kitazawa H, Alvarez S: Orally administered Lactobacillus rhamnosus modulates the respiratory immune response triggered by the viral pathogen-associated molecular pattern poly(I:C). BMC Immunol 2012, 13:53. BioMed Central Full Text
  • [17]Stadnyk AW: Intestinal epithelial cells as a source of inflammatory cytokines and chemokines. Can J Gastroenterol 2002, 16(4):241-246.
  • [18]Kawai T, Akira S: Innate immune recognition of viral infection. Nat Immun 2006, 7(2):131-137.
  • [19]Takeuchi O, Akira S: MDA5/RIG-I and virus recognition. Curr Opin Immunol 2008, 20(1):17-22.
  • [20]Takeuchi O, Akira S: Innate immunity to virus infection. Immunol Rev 2009, 227(1):75-86.
  • [21]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: Immunobiotic Lactobacillus jensenii Modulates the Toll-Like Receptor 4-Induced Inflammatory Response via Negative Regulation in Porcine Antigen-Presenting Cells. Clin Vaccine Immunol 2012, 19(7):1038-1053.
  • [22]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: Immunobiotic lactic acid bacteria beneficially regulate immune response triggered by poly(I:C) in porcine intestinal epithelial cells. Vet Res 2011, 42(1):111. BioMed Central Full Text
  • [23]Hosoya S, Villena J, Chiba E, Shimazu T, Suda Y, Aso H, Saito T, Kitazawa H: Advanced application of porcine intestinal epithelial cells for the selection of immunobiotics modulating toll-like receptor 3-mediated inflammation. J Microbiol Immunol Infect 2013, 46(6):474-478.
  • [24]Moue M, Tohno M, Shimazu T, Kido T, Aso H, Saito T, Kitazawa H: Toll-like receptor 4 and cytokine expression involved in functional immune response in an originally established porcine intestinal epitheliocyte cell line. Biochim Biophys Acta 2008, 1780(2):134-144.
  • [25]Frias AH, Vijay-Kumar M, Gentsch JR, Crawford SE, Carvalho FA, Estes MK, Gewirtz AT: Intestinal epithelia activate anti-viral signaling via intracellular sensing of rotavirus structural components. Mucosal Immunol 2010, 3(6):622-632.
  • [26]Akira S: Pathogen recognition by innate immunity and its signaling. Proc Jpn Acad Ser B Phys Biol Sci 2009, 85(4):143-156.
  • [27]Akira S: Innate immunity and adjuvants. Philos Trans R Soc Lond B Biol Sci 2011, 366(1579):2748-2755.
  • [28]Meylan E, Tschopp J: Toll-like receptors and RNA helicases: two parallel ways to trigger antiviral responses. Mol Cell 2006, 22(5):561-569.
  • [29]Sen GC, Sarkar SN: Transcriptional signaling by double-stranded RNA: role of TLR3. Cytokine Growth Factor Rev 2005, 16(1):1-14.
  • [30]Frias AH, Jones RM, Fifadara NH, Vijay-Kumar M, Gewirtz AT: Rotavirus-induced IFN-beta promotes anti-viral signaling and apoptosis that modulate viral replication in intestinal epithelial cells. Innate immunity 2012, 18(2):294-306.
  • [31]Feng N, Kim B, Fenaux M, Nguyen H, Vo P, Omary MB, Greenberg HB: Role of interferon in homologous and heterologous rotavirus infection in the intestines and extraintestinal organs of suckling mice. J Virol 2008, 82(15):7578-7590.
  • [32]Barro M, Patton JT: Rotavirus NSP1 inhibits expression of type I interferon by antagonizing the function of interferon regulatory factors IRF3, IRF5, and IRF7. J Virol 2007, 81(9):4473-4481.
  • [33]Haller D, Bode C, Hammes WP, Pfeifer AM, Schiffrin EJ, Blum S: Non-pathogenic bacteria elicit a differential cytokine response by intestinal epithelial cell/leucocyte co-cultures. Gut 2000, 47(1):79-87.
  • [34]Vinderola G, Matar C, Perdigon G: Role of intestinal epithelial cells in immune effects mediated by gram-positive probiotic bacteria: involvement of toll-like receptors. Clin Diagn Lab Immunol 2005, 12(9):1075-1084.
  • [35]Castillo NA, de Moreno de LeBlanc A, MG C, Perdigon G: Comparative study of the protective capacity against Salmonella infection between probiotic and nonprobiotic Lactobacilli. J Appl Microbiol 2013, 114(3):861-876.
  • [36]Chieppa M, Rescigno M, Huang AY, Germain RN: Dynamic imaging of dendritic cell extension into the small bowel lumen in response to epithelial cell TLR engagement. J Exp Med 2006, 203(13):2841-2852.
  • [37]Baba N, Samson S, Bourdet-Sicard R, Rubio M, Sarfati M: 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. Immunology 2009, 128(1 Suppl):e523-e531.
  • [38]Christensen HR, Frokiaer H, Pestka JJ: Lactobacilli differentially modulate expression of cytokines and maturation surface markers in murine dendritic cells. J Immunol 2002, 168(1):171-178.
  • [39]Drakes M, Blanchard T, Czinn S: Bacterial probiotic modulation of dendritic cells. Infect Immun 2004, 72(6):3299-3309.
  • [40]Weiss G, Rasmussen S, Zeuthen LH, Nielsen BN, Jarmer H, Jespersen L, Frokiaer H: Lactobacillus acidophilus induces virus immune defence genes in murine dendritic cells by a Toll-like receptor-2-dependent mechanism. Immunology 2010, 131(2):268-281.
  • [41]Bass DM: Interferon gamma and interleukin 1, but not interferon alfa, inhibit rotavirus entry into human intestinal cell lines. Gastroenterology 1997, 113(1):81-89.
  • [42]Hulst M, Kerstens H, de Wit A, Smits M, van der Meulen J, Niewold T: Early transcriptional response in the jejunum of germ-free piglets after oral infection with virulent rotavirus. Arch Virol 2008, 153(7):1311-1322.
  • [43]Zhou R, Wei H, Sun R, Tian Z: Recognition of double-stranded RNA by TLR3 induces severe small intestinal injury in mice. J Immunol 2007, 178(7):4548-4556.
  • [44]Cario E, Podolsky DK: Differential alteration in intestinal epithelial cell expression of toll-like receptor 3 (TLR3) and TLR4 in inflammatory bowel disease. Infect Immun 2000, 68(12):7010-7017.
  • [45]Galdeano CM, Perdigon G: The probiotic bacterium Lactobacillus casei induces activation of the gut mucosal immune system through innate immunity. Clin Vaccine Immunol 2006, 13(2):219-226.
  • [46]Mohamadzadeh M, Olson S, Kalina WV, Ruthel G, Demmin GL, Warfield KL, Bavari S, Klaenhammer TR: Lactobacilli activate human dendritic cells that skew T cells toward T helper 1 polarization. Proc Natl Acad Sci U S A 2005, 102(8):2880-2885.
  • [47]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: Differential Toll-like receptor recognition and induction of cytokine profile by Bifidobacterium breve and Lactobacillus strains of probiotics. Clin Vaccine Immunol 2011, 18(4):621-628.
  • [48]Wells JM, Rossi O, Meijerink M, van Baarlen P: Epithelial crosstalk at the microbiota–mucosal interface. Proc Natl Acad Sci USA 2010, 108((supple. 1)):4607-4614. pnas.1000092107: 1-8
  • [49]Abreu MT: Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nat Rev Immunol 2010, 10(2):131-144.
  • [50]Es-Saad S, Tremblay N, Baril M, Lamarre D: Regulators of innate immunity as novel targets for panviral therapeutics. Curr Opin Virol 2012, 2(5):622-628.
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