The gut microbiota is increasingly recognised as a key-player in defining the health status of the gastrointestinal tract. Recently, we demonstrated that colonisation of healthy germfree mice with a conventional microbiota (conventionalisation) elicits temporal and region specific host-microbe communication responses that lead to the establishment of a microbiota-accommodating homeostatic state within 30 days. Here, the microbiota composition profiles, mucosal transcriptomes and plasma-analytes in germ-free and conventionalised C57/BL 6 J mice were assessed to decipher the features of the distinctive and pivotal events occurring four days after initiation of the conventionalisation process. The dominance of the microbial genera Helicobacter, Sphingomonas and Mucispirillum in the gut microbiota coincided with the transient mounting of proinflammatory responses in the mucosa and the transiently elevated levels of specific (inflammatory) cytokines and amines in plasma. The overrepresented microbes have previously been associated with the potential to cause disease under certain conditions, illustrating that conventionalisation proceeds through a transient state that resembles situations associated with dysbiosis. However, no overt mucosal inflammation was observed, suggesting a pivotal role of the overrepresented bacterial groups in priming and maturation of the immune system during the process of conventionalisation. These findings imply that the transiently elevated relative overgrowth of particular microbial genera functions as pivotal adjuvants to elicit the corresponding proinflammatory cascades, which precede the full maturation of the different arms of the immune system following these events and is required to achieve a microbiota-accommodating homeostasis in healthy animals.
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Akobeng, A.K., Miller, V., Thomas, A.G. and Richmond, K., 2000. Glutamine supplementation and intestinal permeability in Crohn's disease. Journal of Parenteral and Enteral Nutrition 24: 196.
'Glutamine supplementation and intestinal permeability in Crohn's disease ' () 24 Journal of Parenteral and Enteral Nutrition : 196.
Bellows, C.F. and Jaffe, B.M., 1999. Glutamine is essential for nitric oxide synthesis by murine macrophages. Journal of Surgical Research 86: 213-219.
'Glutamine is essential for nitric oxide synthesis by murine macrophages ' () 86 Journal of Surgical Research : 213 -219.
Berry, D., Schwab, C., Milinovich, G., Reichert, J., Ben Mahfoudh, K., Decker, T., Engel, M., Hai, B., Hainzl, E., Heider, S., Kenner, L., Müller, M., Rauch, I., Strobl, B., Wagner, M., Schleper, C., Urich, T. and Loy, A., 2012. Phylotype-level 16S rRNA analysis reveals new bacterial indicators of health state in acute murine colitis. ISME Journal 6: 2091-2106.
'Phylotype-level 16S rRNA analysis reveals new bacterial indicators of health state in acute murine colitis ' () 6 ISME Journal : 2091 -2106.
Bogomoletz, W.V., Williams, G.T. and Potet, F., 1987. HID-blue alcian (High iron diamine-alcian blue) and the histochemistry of mucins in colonic pathology - 20 years later. Gastroenterology and Clinical Biology 11: 865-868.
'HID-blue alcian (High iron diamine-alcian blue) and the histochemistry of mucins in colonic pathology - 20 years later ' () 11 Gastroenterology and Clinical Biology : 865 -868.
Chinen, T., Kobayashi, T., Ogata, H., Takaesu, G., Takaki, H., Hashimoto, M., Yagita, H., Nawata, H. and Yoshimura, A., 2006. Suppressor of cytokine signaling-1 regulates inflammatory bowel disease in which both IFN gamma and IL-4 are involved. Gastroenterology 130: 373-388.
'Suppressor of cytokine signaling-1 regulates inflammatory bowel disease in which both IFN gamma and IL-4 are involved ' () 130 Gastroenterology : 373 -388.
Chow, J. and Mazmanian, S.K., 2010. A pathobiont of the microbiota balances host colonisation and intestinal inflammation. Cell Host and Microbe 7: 265-276.
'A pathobiont of the microbiota balances host colonisation and intestinal inflammation ' () 7 Cell Host and Microbe : 265 -276.
Chow, J., Tang, H. and Mazmanian, S.K., 2011. Pathobionts of the gastrointestinal microbiota and inflammatory disease. Current Opinion in Immunology 23: 473-480.
'Pathobionts of the gastrointestinal microbiota and inflammatory disease ' () 23 Current Opinion in Immunology : 473 -480.
Duan, R.D. and Nilsson, A., 2009. Metabolism of sphingolipids in the gut and its relation to inflammation and cancer development. Progress in Lipid Research 48: 62-72.
'Metabolism of sphingolipids in the gut and its relation to inflammation and cancer development ' () 48 Progress in Lipid Research : 62 -72.
El Aidy, S., Derrien, M., Merrifield, C.A., Levenez, F., Doré, J., Boekschoten, M.V., Dekker, J., Holmes, E., Zoetendal, E.G., Van Baarlen, P., Claus, S.P. and Kleerebezem, M., 2012a. Gut bacteria-host metabolic interplay during conventionalisation of the mouse germfree colon. ISME Journal 7: 743-755.
'Gut bacteria-host metabolic interplay during conventionalisation of the mouse germfree colon ' () 7 ISME Journal : 743 -755.
El Aidy, S., Kunze, W., Bienenstock, J. and Kleerebezem, M., 2012d. The microbiota and the gut-brain axis: insights from the temporal and spatial mucosal alterations during colonisation of the germfree mouse intestine. Beneficial Microbes 3: 251-259.
'The microbiota and the gut-brain axis: insights from the temporal and spatial mucosal alterations during colonisation of the germfree mouse intestine ' () 3 Beneficial Microbes : 251 -259.
El Aidy, S., Merrifield, C.A., Derrien, M., Van Baarlen, P., Hooiveld, G., Levenez, F., Doré, J., Dekker, J., Holmes, E., Claus, S.P, Reijngoud, D.J. and Kleerebezem, M., 2012b. The gut microbiota elicits a profound metabolic reorientation in the mouse jejunal mucosa during conventionalisation. Gut 62: 1306-1314.
'The gut microbiota elicits a profound metabolic reorientation in the mouse jejunal mucosa during conventionalisation ' () 62 Gut : 1306 -1314.
El Aidy, S., Van Baarlen, P., Derrien, Lindenbergh-Kortleve, D.J., Hooiveld, G., Levenez, F., Doré, J., Dekker, J., Samsom, J.N., Nieuwenhuis, E.E.S. and Kleerebezem, M., 2012c. Temporal and spatial interplay of microbiota and intestinal mucosa drive establishment of immune homeostasis in conventionalized mice. Mucosal Immunology 5: 567-579.
'Temporal and spatial interplay of microbiota and intestinal mucosa drive establishment of immune homeostasis in conventionalized mice ' () 5 Mucosal Immunology : 567 -579.
Elinav, E., Strowig, T., Kau, A.L., Henao-Mejia, J., Thaiss, C.A., Booth, C.J., Peaper, D.R., Bertin, J., Eisenbarth, S.C., Gordon, J.I. and Flavell, R.A., 2011. NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell 145: 745-757.
'NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis ' () 145 Cell : 745 -757.
Erdman, S.E., Rao, V.P., Poutahidis, T., Ihrig, M.M., Ge, Z., Feng, Y., Tomczak, M., Rogers, A.B., Horwitz, B.H. and Fox, J.G., 2003. CD4(+)CD25(+) regulatory lymphocytes require interleukin 10 to interrupt colon carcinogenesis in mice. Cancer Research 63: 6042-6050.
'CD4(+)CD25(+) regulatory lymphocytes require interleukin 10 to interrupt colon carcinogenesis in mice ' () 63 Cancer Research : 6042 -6050.
Erdman, S.E., Rao, V.P., Poutahidis, T., Rogers, A.B., Taylor, C.L., Jackson, E.A., Ge, Z., Lee, C.W., Schauer, D.B., Wogan, G.N., Tannenbaum, S.R. and Fox. J.G., 2009. Nitric oxide and TNF-alpha trigger colonic inflammation and carcinogenesis in Helicobacter hepaticus-infected, Rag2-deficient mice. Proceedings of the National Academy of Sciences of the USA 106: 1027-1032.
'Nitric oxide and TNF-alpha trigger colonic inflammation and carcinogenesis in Helicobacter hepaticus-infected, Rag2-deficient mice ' () 106 Proceedings of the National Academy of Sciences of the USA : 1027 -1032.
Garrett, W.S., Gallini, C.A., Yatsunenko, T., Michaud, M., DuBois, A., Delaney, M.L., Punit, S., Karlsson, M., Bry, L., Glickman, J.N., Gordon, J.I., Onderdonk, A.B. and Glimcher, L.H., 2010. Enterobacteriaceae act in concert with the gut microbiota to induce spontaneous and maternally transmitted colitis. Cell Host and Microbe 8: 292-300.
'Enterobacteriaceae act in concert with the gut microbiota to induce spontaneous and maternally transmitted colitis ' () 8 Cell Host and Microbe : 292 -300.
Garrett, W.S., Punit, S., Gallini, C.A., Michaud, M., Zhang, D., Sigrist, K.S., Lord, G.M., Glickman, J.N. and Glimcher, L.H., 2009. Colitis-associated colorectal cancer driven by T-bet deficiency in dendritic cells. Cancer Cell 16: 208-219.
'Colitis-associated colorectal cancer driven by T-bet deficiency in dendritic cells ' () 16 Cancer Cell : 208 -219.
Hakansson, A. and Molin, G., 2011. Gut microbiota and inflammation. Nutrients 3: 637-682.
'Gut microbiota and inflammation ' () 3 Nutrients : 637 -682.
Heuschkel, R.B., MacDonald, T.T., Monteleone, G., Bajaj-Elliott, M., Smith, J.A. and Pender, S.L.F., 2000. Imbalance of stromelysin-1 and TIMP-1 in the mucosal lesions of children with inflammatory bowel disease. Gut 47: 57-62.
'Imbalance of stromelysin-1 and TIMP-1 in the mucosal lesions of children with inflammatory bowel disease ' () 47 Gut : 57 -62.
Kinjyo, I., Hanada, T., Inagaki-Ohara, K., Mori, H., Aki, D., Ohishi, M., Yoshida, H., Kubo, M. and Yoshimura, A., 2002. SOCS1/JAB is a negative regulator of LPS-induced macrophage activation. Immunity 17: 583-591.
'SOCS1/JAB is a negative regulator of LPS-induced macrophage activation ' () 17 Immunity : 583 -591.
Lindén, S.K., Sutton, P., Karlsson, N.G., Korolik, V. and McGuckin, M.A., 2008. Mucins in the mucosal barrier to infection. Mucosal Immunology 1: 183-197.
'Mucins in the mucosal barrier to infection ' () 1 Mucosal Immunology : 183 -197.
Macpherson, A.J., Geuking, M.B. and McCoy, K.D., 2005. Immune responses that adapt the intestinal mucosa to commensal intestinal bacteria. Immunology 115: 153-162.
'Immune responses that adapt the intestinal mucosa to commensal intestinal bacteria ' () 115 Immunology : 153 -162.
Mai, V., Young, C.M., Ukhanova, M., Wang, X., Sun, Y., Casella, G., Theriaque, D., Li, N., Sharma, R., Hudak, M. and Neu, J., 2011. Fecal microbiota in premature infants prior to necrotizing enterocolitis. PLoS ONE 6: e20647.
'Fecal microbiota in premature infants prior to necrotizing enterocolitis ' () 6 PLoS ONE : e20647.
Manco, M., Putignani, L. and Bottazzo, G.F., 2010. Gut microbiota, lipopolysaccharides, and innate immunity in the pathogenesis of obesity and cardiovascular risk. Endocrine Reviews 31: 817-844.
'Gut microbiota, lipopolysaccharides, and innate immunity in the pathogenesis of obesity and cardiovascular risk ' () 31 Endocrine Reviews : 817 -844.
Mattner, J., Debord, K.L., Ismail, N., Goff, R.D., Cantu III, C., Zhou, D., Saint-Mezard, P., Wang, V., Gao, Y., Yin, N., Hoebe, K., Schneewind, O., Walker, D., Beutler, B., Teyton, L., Savage, P.B. and Bendelac, A., 2005. Exogenous and endogenous glycolipid antigens activate NKT cells during microbial infections. Nature 434: 525-529.
'Exogenous and endogenous glycolipid antigens activate NKT cells during microbial infections ' () 434 Nature : 525 -529.
Morrow, A.L., Lagomarcino, A.J., Schibler, K.R., Taft, D.H., Yu, Z., Wang, B., Altaye, M., Wagner, M., Gevers, D., Ward, D.V., Kennedy, M.A., Huttenhower, C. and Newburg, D.S., 2013. Early microbial and metabolomic signatures predict later onset of necrotizing enterocolitis in preterm infants. Microbiome 1: 13.
'Early microbial and metabolomic signatures predict later onset of necrotizing enterocolitis in preterm infants ' () 1 Microbiome : 13.
Nishimura, M., Kuboi, Y., Muramoto, K., Kawano, T. and Imai, T., 2009. Chemokines as novel therapeutic targets for inflammatory bowel disease. Annals of the New York Academy of Sciences 1173: 350-356.
'Chemokines as novel therapeutic targets for inflammatory bowel disease ' () 1173 Annals of the New York Academy of Sciences : 350 -356.
O’Connor, S.M., Taylor, C.E. and Hughes, J.M., 2006. Emerging infectious determinants of chronic diseases. Emerging Infectious Diseases 12: 1051-1057.
'Emerging infectious determinants of chronic diseases ' () 12 Emerging Infectious Diseases : 1051 -1057.
Palmer, R., 2011. Fecal matters. Nature Medicine 17: 150-152.
'Fecal matters ' () 17 Nature Medicine : 150 -152.
Palmer, R.M., Ashton, D.S. and Moncada, S., 1988. Vascular endothelial cells synthesize nitric oxide from L-arginine. Nature 333: 664-666.
'Vascular endothelial cells synthesize nitric oxide from L-arginine ' () 333 Nature : 664 -666.
Parker, N., Tsai, H.H., Ryder, S.D., Raouf, A.H. and Rhodes, J.M., 1995. Increased rate of sialylation of colonic mucin by cultured ulcerative colitis mucosal explants. Digestion 56: 52-56.
'Increased rate of sialylation of colonic mucin by cultured ulcerative colitis mucosal explants ' () 56 Digestion : 52 -56.
Rajilić-Stojanović, M., Heilig, H.G., Molenaar, D., Kajander, K., Surakka, A., Smidt, H. and De Vos, W.M., 2009. Development and application of the human intestinal tract chip, a phylogenetic microarray: analysis of universally conserved phylotypes in the abundant microbiota of young and elderly adults. Environmental Microbiolology 11: 1736-1751.
'Development and application of the human intestinal tract chip, a phylogenetic microarray: analysis of universally conserved phylotypes in the abundant microbiota of young and elderly adults ' () 11 Environmental Microbiolology : 1736 -1751.
Raouf, A.H., Tsai, H.H., Parker, N., Hoffman, J., Walker, R.J. and Rhodes, J.M., 1992. Sulphation of colonic and rectal mucin in inflammatory bowel disease: reduced sulphation of rectal mucus in ulcerative colitis. Clinical Science 83: 623-626.
'Sulphation of colonic and rectal mucin in inflammatory bowel disease: reduced sulphation of rectal mucus in ulcerative colitis ' () 83 Clinical Science : 623 -626.
Robertson, B.R., O’Rourke, J.L., Neilan, B.A., Vandamme, P., On, S.L., Fox, J.G. and Lee, A., 2005. Mucispirillum schaedleri gen. nov., sp. nov., a spiral-shaped bacterium colonizing the mucus layer of the gastrointestinal tract of laboratory rodents. International Journal of Systematic and Evolutionary Microbiology 55: 1199-1204.
'Mucispirillum schaedleri gen. nov., sp. nov., a spiral-shaped bacterium colonizing the mucus layer of the gastrointestinal tract of laboratory rodents ' () 55 International Journal of Systematic and Evolutionary Microbiology : 1199 -1204.
Singh, U.P., Venkataraman, C., Singh, R. and Lillard Jr., J.W., 2007. CXCR3 axis: role in inflammatory bowel disease and its therapeutic implication. Endocrine, Metabolic and Immune Disorders - Drug Targets 7: 111-123.
'CXCR3 axis: role in inflammatory bowel disease and its therapeutic implication ' () 7 Endocrine, Metabolic and Immune Disorders - Drug Targets : 111 -123.
Spicer, S.S., 1965. Diamine methods for differentiating mucosubstances histochemically. Journal of Histochemistry and Cytochemistry 13: 211-234.
'Diamine methods for differentiating mucosubstances histochemically ' () 13 Journal of Histochemistry and Cytochemistry : 211 -234.
Stepankova, R., Powrie, F., Kofronova, O., Kozakova, H., Hudcovic, T., Hrncir, T., Uhlig, H., Read, S., Rehakova, Z., Benada, O., Heczko, P., Strus, M., Bland, P. and Tlaskalova-Hogenova, H., 2007. Segmented filamentous bacteria in a defined bacterial cocktail induce intestinal inflammation in SCID mice reconstituted with CD45RB(high) CD4+ T cells. Inflammatory Bowel Disease 13: 1202-1211.
'Segmented filamentous bacteria in a defined bacterial cocktail induce intestinal inflammation in SCID mice reconstituted with CD45RB(high) CD4+ T cells ' () 13 Inflammatory Bowel Disease : 1202 -1211.
Suzuki, Y., Suda, T., Furuhashi, K., Suzuki, M., Fujie, M., Hahimoto, D., Nakamura, Y., Inui, N., Nakamura, H. and Chida, K., 2010. Increased serum kynurenine/tryptophan ratio correlates with disease progression in lung cancer. Lung Cancer 67: 361-365.
'Increased serum kynurenine/tryptophan ratio correlates with disease progression in lung cancer ' () 67 Lung Cancer : 361 -365.
Walker, A., Sanderson, J., Churcher, C., Parkes, G., Hudspith, B., Rayment, N., Brostoff, J., Parkhill, J., Dougan, G. and Petrovska, L., 2011. High-throughput clone library analysis of the mucosa-associated microbiota reveals dysbiosis and differences between inflamed and non-inflamed regions of the intestine in inflammatory bowel disease. BMC Microbiology 11: 7.
'High-throughput clone library analysis of the mucosa-associated microbiota reveals dysbiosis and differences between inflamed and non-inflamed regions of the intestine in inflammatory bowel disease ' () 11 BMC Microbiology : 7.
Wang, D., Pezo, R.C., Corner, G., Sison, C., Lesser, M.L., Shenoy, S.M., Mariadason, J.M., Singer, R.H. and Augenlicht L.H., 2010. Altered dynamics of intestinal cell maturation in Apc1638N/+ mice. Cancer Research 70: 5348-5357.
'Altered dynamics of intestinal cell maturation in Apc1638N/+ mice ' () 70 Cancer Research : 5348 -5357.
Wu, G.Y., 1998. Intestinal mucosal amino acid catabolism. Journal of Nutrition 128: 1249-1252.
'Intestinal mucosal amino acid catabolism ' () 128 Journal of Nutrition : 1249 -1252.
Zeissig, S., Kaser, A., Dougan, S.K., Nieuwenhuis, E.E. and Blumberg, R.S., 2007. Role of NKT cells in the digestive system. III. Role of NKT cells in intestinal immunity. American Journal of Physiology - Gastrointestinal and Liver Physiology 29: G1101-G1105.
'Role of NKT cells in the digestive system III. Role of NKT cells in intestinal immunity ' () 29 American Journal of Physiology - Gastrointestinal and Liver Physiology : G1101 -G1105.
Zhao, J., Kim, K.D., Yang, X., Auh, S., Fu, Y.X. and Tang H., 2008. Hyper innate responses in neonates lead to increased morbidity and mortality after infection. Proceedings of the National Academy of Sciences of the USA 105: 7528-7533.
'Hyper innate responses in neonates lead to increased morbidity and mortality after infection ' () 105 Proceedings of the National Academy of Sciences of the USA : 7528 -7533.
All Time | Past 365 days | Past 30 Days | |
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The gut microbiota is increasingly recognised as a key-player in defining the health status of the gastrointestinal tract. Recently, we demonstrated that colonisation of healthy germfree mice with a conventional microbiota (conventionalisation) elicits temporal and region specific host-microbe communication responses that lead to the establishment of a microbiota-accommodating homeostatic state within 30 days. Here, the microbiota composition profiles, mucosal transcriptomes and plasma-analytes in germ-free and conventionalised C57/BL 6 J mice were assessed to decipher the features of the distinctive and pivotal events occurring four days after initiation of the conventionalisation process. The dominance of the microbial genera Helicobacter, Sphingomonas and Mucispirillum in the gut microbiota coincided with the transient mounting of proinflammatory responses in the mucosa and the transiently elevated levels of specific (inflammatory) cytokines and amines in plasma. The overrepresented microbes have previously been associated with the potential to cause disease under certain conditions, illustrating that conventionalisation proceeds through a transient state that resembles situations associated with dysbiosis. However, no overt mucosal inflammation was observed, suggesting a pivotal role of the overrepresented bacterial groups in priming and maturation of the immune system during the process of conventionalisation. These findings imply that the transiently elevated relative overgrowth of particular microbial genera functions as pivotal adjuvants to elicit the corresponding proinflammatory cascades, which precede the full maturation of the different arms of the immune system following these events and is required to achieve a microbiota-accommodating homeostasis in healthy animals.
All Time | Past 365 days | Past 30 Days | |
---|---|---|---|
Abstract Views | 283 | 202 | 20 |
Full Text Views | 63 | 56 | 15 |
PDF Views & Downloads | 21 | 12 | 0 |