Administration of Lactobacillus rhamnosus GG (LGG) has been reported to be therapeutically effective against acute secretory diarrhoea resulting from the structural and functional intestinal mucosal lesions induced by rotavirus infection; however, the underlying mechanisms remain to be completely elucidated. Because Toll-like receptor 3 (TLR3) plays a key role in the innate immune responses following the recognition of rotavirus, the present study examined whether LGG influences TLR3 gene expression in murine small intestine ex vivo and in vivo. We employed cultured intestinal organoids derived from small intestinal crypts as an ex vivo tissue model. LGG supplementation increased TLR3 mRNA levels in the intestinal organoids, as estimated by quantitative real-time polymerase chain reaction. Likewise, single and 7-day consecutive daily administrations of LGG increased TLR3 mRNA levels in the small intestine of C57BL/6N mice. The mRNA levels of other TLRs were not substantially altered both ex vivo and in vivo. In addition, LGG supplementation increased the mRNA levels of an antiviral type 1 interferon, interferon-α (IFN-α), and a neutrophil chemokine, CXCL1, upon stimulation with a synthetic TLR3 ligand, poly(I:C) in the intestinal organoids. LGG administration did not alter IFN-α and CXCL1 mRNA levels in the small intestine in vivo. Supplementation of other bacterial strains, Bifidobacterium bifidum and Lactobacillus paracasei, failed to increase TLR3 and poly(I:C)-stimulated CXCL1 mRNA levels ex vivo. We propose that upregulation of TLR3 gene expression may play a pivotal role in the therapeutic efficacy of LGG against rotavirus-associated diarrhoea. In addition, we demonstrated that intestinal organoids may be a promising ex vivo tissue model for investigating host-pathogen interactions and the antiviral action of probiotics in the intestinal epithelium.
Purchase
Buy instant access (PDF download and unlimited online access):
Institutional Login
Log in with Open Athens, Shibboleth, or your institutional credentials
Personal login
Log in with your brill.com account
Abreu, M.T., Fukata, M. and Arditi, M., 2005. TLR signaling in the gut in health and disease. Journal of Immunology 174: 4453-4460.
'TLR signaling in the gut in health and disease ' () 174 Journal of Immunology : 4453 -4460.
Alexopoulou, L., Holt, A.C., Medzhitov, R. and Flavell, R.A., 2001. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413: 732-738.
'Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3 ' () 413 Nature : 732 -738.
Basu, S., Paul, D.K., Ganguly, S., Chatterjee, M. and Chandra, P.K., 2009. Efficacy of high-dose Lactobacillus rhamnosus GG in controlling acute watery diarrhea in Indian children: a randomized controlled trial. Journal of Clinical Gastroenterology 43: 208-213.
'Efficacy of high-dose Lactobacillus rhamnosus GG in controlling acute watery diarrhea in Indian children: a randomized controlled trial ' () 43 Journal of Clinical Gastroenterology : 208 -213.
Estes, M.K. and Morris, A.P., 1999. A viral enterotoxin. A new mechanism of virus-induced pathogenesis. Advances in Experimental Medicine and Biology 473: 73-82.
'A viral enterotoxin ' () 473 Advances in Experimental Medicine and Biology : 73 -82.
Feng, N.G., Jaimes, M.C., Lazarus, N.H., Monak, D. and Zhang, C.Q., 2006. Redundant role of chemokines CCL25/TECK and CCL28/MEC in IgA+ plasmablast recruitment to the intestinal lamina propria after RV infection. Journal of Immunology 176: 5749-5759.
'Redundant role of chemokines CCL25/TECK and CCL28/MEC in IgA+ plasmablast recruitment to the intestinal lamina propria after RV infection ' () 176 Journal of Immunology : 5749 -5759.
Finkbeiner, S.R., Zeng, X.L., Utama, B., Atmar, R.L., Shroyer, N.F. and Estes, M.K., 2012. Stem cell-derived human intestinal organoids as an infection model for rotaviruses. mBio 3: e00159-12.
'Stem cell-derived human intestinal organoids as an infection model for rotaviruses ' () 3 mBio : e00159 -12.
Foulke-Abel, J., In, J., Kovbasnjuk, O., Zachos, N.C., Ettayebi, K., Blutt, S.E., Hyser, J.M., Zeng, X.L., Crawford, S.E., Broughman, J.R., Estes, M.K. and Donowitz, M., 2014. Human enteroids as an ex-vivo model of host-pathogen interactions in the gastrointestinal tract. Experimental Biology and Medicine 239: 1124-1134.
'Human enteroids as an ex-vivo model of host-pathogen interactions in the gastrointestinal tract ' () 239 Experimental Biology and Medicine : 1124 -1134.
Guandalini, S., Pensabene, L., Zikri, M.A., Dias, J.A., Casali, L.G., Hoekstra, H., Kolacek, S., Massar, K., Micetic-Turk, D., Papadopoulou, A., De Sousa, J.S., Sandhu, B., Szajewska, H. and Weizman, Z., 2000. Lactobacillus GG administered in oral rehydration solution to children with acute diarrhea: a multicenter European trial. Journal of Pediatric Gastroenterology and Nutrition 30: 54-60.
'Lactobacillus GG administered in oral rehydration solution to children with acute diarrhea: a multicenter European trial ' () 30 Journal of Pediatric Gastroenterology and Nutrition : 54 -60.
Hill, C., Guarner, F., Reid, G., Gibson, G.R., Merenstein, D.J., Pot, B., Morelli, L., Canani, R.B., Flint, H.J., Salminen, S., Calder, P.C. and Sanders, M.E., 2014. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nature Reviews, Gastroenterology and Hepatology 11: 506-514.
'The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic ' () 11 Nature Reviews, Gastroenterology and Hepatology : 506 -514.
Imaizumi, T., Aizawa, T., Segawa, C., Shimada, M., Tsuruga, K., Kawaguchi, S., Matsumiya, T., Yoshida, H., Joh, K. and Tanaka, H., 2014. Toll-like receptor 3 signalling contributes to the expression of a neutrophil chemoattractant, CXCL1 in human mesangial cells. Clinical and Experimental Nephrology 19: 761-770.
'Toll-like receptor 3 signalling contributes to the expression of a neutrophil chemoattractant, CXCL1 in human mesangial cells ' () 19 Clinical and Experimental Nephrology : 761 -770.
Isolauri, E., 2004. The role of probiotics in paediatrics. Current Paediatrics 14: 104-109.
'The role of probiotics in paediatrics ' () 14 Current Paediatrics : 104 -109.
Kaila, M., Isolauri, E., Saxelin, M., Arvilommi, H. and Vesikari, T., 1995. Viable versus inactivated Lactobacillus strain GG in acute RV diarrhea. Archives of Disease in Childhood 72: 51-53.
'Viable versus inactivated Lactobacillus strain GG in acute RV diarrhea ' () 72 Archives of Disease in Childhood : 51 -53.
Kawai, T. and Akira, S., 2006. TLR signaling. Cell Death and Differentiation 13: 816-825.
'TLR signaling ' () 13 Cell Death and Differentiation : 816 -825.
Kovbasnjuk, O., Zachos, N.C., In, J., Foulke-Abel, J., Ettayebi, K., Hyser, J.M., Broughman, J.R., Zeng, X.L., Middendorp, S., De Jonge, H.R., Estes, M.K. and Donowitz, M., 2013. Human enteroids: preclinical models of non-inflammatory diarrhoea. Stem Cell Research and Therapy 4 Suppl. 1: S3.
'Human enteroids: preclinical models of non-inflammatory diarrhoea ' () 1 Stem Cell Research and Therapy 4 Suppl : S3.
Liévin-Le Moal, V. and Servin, A.L., 2014. Anti-infective activities of Lactobacillus strains in the human intestinal microbiota: from probiotics to gastrointestinal anti- infectious biotherapeutic agents. Clinical Microbiology Reviews 27: 167-199.
'Anti-infective activities of Lactobacillus strains in the human intestinal microbiota: from probiotics to gastrointestinal anti- infectious biotherapeutic agents ' () 27 Clinical Microbiology Reviews : 167 -199.
Liu, F., Li, G., Wen, K., Bui, T., Cao, D., Zhang, Y. and Yuan, L., 2010. 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 Immunology 23: 135-149.
'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 ' () 23 Viral Immunology : 135 -149.
Majamaa, H., Isolauri, E., Saxelin, M. and Vesikari, T., 1995. Lactic acid bacteria in the treatment of acute rotavirus gastroenteritis. Journal of Pediatric Gastroenterology and Nutrition 20: 333-338.
'Lactic acid bacteria in the treatment of acute rotavirus gastroenteritis ' () 20 Journal of Pediatric Gastroenterology and Nutrition : 333 -338.
Maragkoudakis, P.A., Chingwaru, W., Gradisnik, L., Tsakalidou, E. and Cencic, A., 2010. Lactic acid bacteria efficiently protect human and animal intestinal epithelial and immune cells from enteric virus infection. International Journal of Food Microbiology 141 Suppl. 1: S91-S97.
'Lactic acid bacteria efficiently protect human and animal intestinal epithelial and immune cells from enteric virus infection ' () 1 International Journal of Food Microbiology 141 Suppl. : S91 -S97.
Matsumoto, M. and Seya, T., 2008. TLR3: interferon induction by double-stranded RNA including poly(I:C). Advanced Drug Delivery Reviews 60: 805-812.
'TLR3: interferon induction by double-stranded RNA including poly(I:C) ' () 60 Advanced Drug Delivery Reviews : 805 -812.
Pant, A.R., Graham, S.M., Allen, S.J., Harikul, S., Sabchareon, A., Cuevas, L. and Hart, C.A., 1996. Lactobacillus GG and acute diarrhoea in young children in the tropics. Journal of Tropical Pediatrics 42: 162-165.
'Lactobacillus GG and acute diarrhoea in young children in the tropics ' () 42 Journal of Tropical Pediatrics : 162 -165.
Pott, J., Stockinger, S., Torow, N., Smoczek, A., Lindner, C., McInerney, G., Bäckhed, F., Baumann, U., Pabst, O., Bleich, A. and Hornef, M.W., 2012. Age-dependent TLR3 expression of the intestinal epithelium contributes to rotavirus susceptibility. PLoS Pathogens 8: e1002670.
'Age-dependent TLR3 expression of the intestinal epithelium contributes to rotavirus susceptibility ' () 8 PLoS Pathogens : e1002670.
Rautanen, T., Isolauri, E., Salo, E. and Vesikari, T., 1998. Management of acute diarrhoea with low osmolarity oral rehydration solutions and Lactobacillus strain GG. Archives of Disease in Childhood 79: 157-160.
'Management of acute diarrhoea with low osmolarity oral rehydration solutions and Lactobacillus strain GG ' () 79 Archives of Disease in Childhood : 157 -160.
Saavedra, J.M., Bauman, N.A., Oung, I., Perman, J.A. and Yolken, R.H., 1994. Feeding of Bifidobacterium bifidum and Streptococcus thermophilus to infants in hospital for prevention of diarrhoea and shedding of rotavirus. The Lancet 344: 1046-1049.
'Feeding of Bifidobacterium bifidum and Streptococcus thermophilus to infants in hospital for prevention of diarrhoea and shedding of rotavirus ' () 344 The Lancet : 1046 -1049.
Sarker, S.A., Sultana, S., Fuchs, G.J., Alam, N.H., Azim, T., Brüssow, H. and Hammarström, L., 2005. Lactobacillus paracasei strain ST11 has no effect on rotavirus but ameliorates the outcome of nonrotavirus diarrhea in children from Bangladesh. Pediatrics 116: e221-e228.
'Lactobacillus paracasei strain ST11 has no effect on rotavirus but ameliorates the outcome of nonrotavirus diarrhea in children from Bangladesh ' () 116 Pediatrics : e221 -e228.
Sato, A., Iizuka, M., Nakagomi, O., Suzuki, M., Horie, Y., Konno, S., Hirasawa, F., Sasaki, K., Shindo, K. and Watanabe, S., 2006. Rotavirus double-stranded RNA induces apoptosis and diminishes wound repair in rat intestinal epithelial cells. Journal of Gastroenterology and Hepatology 21: 521-530.
'Rotavirus double-stranded RNA induces apoptosis and diminishes wound repair in rat intestinal epithelial cells ' () 21 Journal of Gastroenterology and Hepatology : 521 -530.
Sato, T., Vries, R.G., Snippert, H.J., Van de Wetering, M., Barker, N., Stange, D.E., Van Es, J.H., Abo, A., Kujala, P., Peters, P.J. and Clevers, H., 2009. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459: 262-265.
'Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche ' () 459 Nature : 262 -265.
Sugata, K., Taniguchi, K., Yui, A., Miyake, F. and Suqa, S., 2008. Analysis of rotavirus antigenemia and extra-intestinal manifestation in children with rotavirus gastroenteritis. Pediatrics 122: 329-397.
'Analysis of rotavirus antigenemia and extra-intestinal manifestation in children with rotavirus gastroenteritis ' () 122 Pediatrics : 329 -397.
Wen, K., Tin, C., Wang, H., Yang, X., Li, G., Giri-Rachman, E., Kocher, J., Bui, T., Clark-Deener, S. and Yuan, L., 2014. Probiotic Lactobacillus rhamnosus GG enhanced Th1 cellular immunity but did not affect antibody responses in a human gut microbiota transplanted neonatal gnotobiotic pig model. PLoS One 9: e94504.
'Probiotic Lactobacillus rhamnosus GG enhanced Th1 cellular immunity but did not affect antibody responses in a human gut microbiota transplanted neonatal gnotobiotic pig model ' () 9 PLoS One : e94504.
Wilson, S.S., Tocchi, A., Holly, M.K., Parks, W.C. and Smith, J.G., 2015. A small intestinal organoid model of non-invasive enteric pathogen-epithelial cell interactions. Mucosal Immunology 8: 352-361.
'A small intestinal organoid model of non-invasive enteric pathogen-epithelial cell interactions ' () 8 Mucosal Immunology : 352 -361.
Yin, Y., Bijvelds, M., Dang, W., Xu, L., Van der Eijk, A.A., Knipping, K., Tuysuz, N., Dekkers, J.F., Wang, Y., De Jonge, J., Sprengers, D., Van der Laan, L.J., Beekman, J.M., Ten Berge, D., Metselaar, H.J., De Jonge, H., Koopmans, M.P., Peppelenbosch, M.P. and Pan, Q., 2015. Modeling rotavirus infection and antiviral therapy using primary intestinal organoids. Antiviral Research 123: 120-131.
'Modeling rotavirus infection and antiviral therapy using primary intestinal organoids ' () 123 Antiviral Research : 120 -131.
Yu, S. and Gao, N., 2015. Compartmentalizing intestinal epithelial cell toll-like receptors for immune surveillance. Cellular and Molecular Life Sciences 72: 3343-3353.
'Compartmentalizing intestinal epithelial cell toll-like receptors for immune surveillance ' () 72 Cellular and Molecular Life Sciences : 3343 -3353.
Zhou, R., Wei, H., Sun, R. and Tian, Z., 2007. Recognition of double-stranded RNA by TLR3 induces severe small intestinal injury in mice. Journal of Immunology 178: 4548-4556.
'Recognition of double-stranded RNA by TLR3 induces severe small intestinal injury in mice ' () 178 Journal of Immunology : 4548 -4556.
| All Time | Past 365 days | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 589 | 273 | 27 |
| Full Text Views | 59 | 5 | 0 |
| PDF Views & Downloads | 27 | 3 | 0 |
Administration of Lactobacillus rhamnosus GG (LGG) has been reported to be therapeutically effective against acute secretory diarrhoea resulting from the structural and functional intestinal mucosal lesions induced by rotavirus infection; however, the underlying mechanisms remain to be completely elucidated. Because Toll-like receptor 3 (TLR3) plays a key role in the innate immune responses following the recognition of rotavirus, the present study examined whether LGG influences TLR3 gene expression in murine small intestine ex vivo and in vivo. We employed cultured intestinal organoids derived from small intestinal crypts as an ex vivo tissue model. LGG supplementation increased TLR3 mRNA levels in the intestinal organoids, as estimated by quantitative real-time polymerase chain reaction. Likewise, single and 7-day consecutive daily administrations of LGG increased TLR3 mRNA levels in the small intestine of C57BL/6N mice. The mRNA levels of other TLRs were not substantially altered both ex vivo and in vivo. In addition, LGG supplementation increased the mRNA levels of an antiviral type 1 interferon, interferon-α (IFN-α), and a neutrophil chemokine, CXCL1, upon stimulation with a synthetic TLR3 ligand, poly(I:C) in the intestinal organoids. LGG administration did not alter IFN-α and CXCL1 mRNA levels in the small intestine in vivo. Supplementation of other bacterial strains, Bifidobacterium bifidum and Lactobacillus paracasei, failed to increase TLR3 and poly(I:C)-stimulated CXCL1 mRNA levels ex vivo. We propose that upregulation of TLR3 gene expression may play a pivotal role in the therapeutic efficacy of LGG against rotavirus-associated diarrhoea. In addition, we demonstrated that intestinal organoids may be a promising ex vivo tissue model for investigating host-pathogen interactions and the antiviral action of probiotics in the intestinal epithelium.
| All Time | Past 365 days | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 589 | 273 | 27 |
| Full Text Views | 59 | 5 | 0 |
| PDF Views & Downloads | 27 | 3 | 0 |