Microbiota matures colonic epithelium through a coordinated induction of cell cycle-related proteins in gnotobiotic rat
Previous studies have suggested that intestinal microbiota modulates colonic epithelium renewal. The objective of our work was to study the effects of microbiota on colonic epithelium structure and cell cycle-related proteins by using gnotobiotic rats. Colonic crypts and amount of cell cycle-related...
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| Veröffentlicht in: | American journal of physiology: Gastrointestinal and liver physiology 2010-08, Vol.299 (2), p.G348-G357 |
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| container_title | American journal of physiology: Gastrointestinal and liver physiology |
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| creator | Cherbuy, Claire Honvo-Houeto, Edith Bruneau, Aurélia Bridonneau, Chantal Mayeur, Camille Duée, Pierre-Henri Langella, Philippe Thomas, Muriel |
| description | Previous studies have suggested that intestinal microbiota modulates colonic epithelium renewal. The objective of our work was to study the effects of microbiota on colonic epithelium structure and cell cycle-related proteins by using gnotobiotic rats. Colonic crypts and amount of cell cycle-related proteins were compared between germ-free (GF), conventional (CV), and conventionalized rats by histochemistry and Western blot. Ki67 and proliferating cell nuclear antigen (PCNA) were used as surrogates for proliferative cells; p21(cip1) and p27(kip1) were markers of cell cycle arrest; anti- and proapoptotic proteins, Bcl2 and Bax, respectively, were also studied. We observed 40% increase of the crypt proliferative area 2 days after inoculation of GF rats with a complex microbiota. This recruitment of proliferative cells may account for the 30% increase of crypt depth observed between CV and GF rats. The hyperproliferative boost induced by microbiota was compensated by a fourfold increase of p21(cip1) and p27(kip1) involved in cell cycle arrest and a 30% drop of antiapoptotic Bcl2 protein while Bax was unchanged. Inductions of p21(cip1), p27(kip1), and PCNA protein were not paralleled by an increase of the corresponding mRNA. We also showed that p21(cip1) induction by microbiota was partially restored by Bacteroides thetaiotaomicron, Ruminococcus gnavus, and Clostridium paraputrificum. Colonization of the colon by a complex microbiota increases the crypt depth of colon epithelium. This event takes place in conjunction with a multistep process: a hyperproliferative boost accompanied by compensatory events as induction of p21(cip1) and p27(kip1) and decrease of Bcl2. |
| doi_str_mv | 10.1152/ajpgi.00384.2009 |
| format | Article |
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The objective of our work was to study the effects of microbiota on colonic epithelium structure and cell cycle-related proteins by using gnotobiotic rats. Colonic crypts and amount of cell cycle-related proteins were compared between germ-free (GF), conventional (CV), and conventionalized rats by histochemistry and Western blot. Ki67 and proliferating cell nuclear antigen (PCNA) were used as surrogates for proliferative cells; p21(cip1) and p27(kip1) were markers of cell cycle arrest; anti- and proapoptotic proteins, Bcl2 and Bax, respectively, were also studied. We observed 40% increase of the crypt proliferative area 2 days after inoculation of GF rats with a complex microbiota. This recruitment of proliferative cells may account for the 30% increase of crypt depth observed between CV and GF rats. The hyperproliferative boost induced by microbiota was compensated by a fourfold increase of p21(cip1) and p27(kip1) involved in cell cycle arrest and a 30% drop of antiapoptotic Bcl2 protein while Bax was unchanged. Inductions of p21(cip1), p27(kip1), and PCNA protein were not paralleled by an increase of the corresponding mRNA. We also showed that p21(cip1) induction by microbiota was partially restored by Bacteroides thetaiotaomicron, Ruminococcus gnavus, and Clostridium paraputrificum. Colonization of the colon by a complex microbiota increases the crypt depth of colon epithelium. This event takes place in conjunction with a multistep process: a hyperproliferative boost accompanied by compensatory events as induction of p21(cip1) and p27(kip1) and decrease of Bcl2.</description><identifier>ISSN: 0193-1857</identifier><identifier>EISSN: 1522-1547</identifier><identifier>DOI: 10.1152/ajpgi.00384.2009</identifier><identifier>PMID: 20466941</identifier><identifier>CODEN: APGPDF</identifier><language>eng</language><publisher>United States: American Physiological Society</publisher><subject>Adaptation, Physiological ; Animals ; Antigens ; Blotting, Western ; Cell Cycle ; Cell Cycle Proteins - biosynthesis ; Cell Proliferation ; Colon ; Colon - growth & development ; Colon - metabolism ; Colon - microbiology ; Colon - physiology ; Cyclin-Dependent Kinase Inhibitor p21 - metabolism ; Cyclin-Dependent Kinase Inhibitor p27 - metabolism ; Germ-Free Life ; Histocytochemistry ; Intestinal Mucosa - growth & development ; Intestinal Mucosa - metabolism ; Intestinal Mucosa - microbiology ; Intestinal Mucosa - physiology ; Life Sciences ; Male ; Metagenome ; Physiology ; Proteins ; Proto-Oncogene Proteins c-bcl-2 - metabolism ; Rats ; Rats, Inbred F344 ; Rodents</subject><ispartof>American journal of physiology: Gastrointestinal and liver physiology, 2010-08, Vol.299 (2), p.G348-G357</ispartof><rights>Copyright American Physiological Society Aug 2010</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c359t-666bc72d07b6a2ddd2d35dc4c9419fdbfda18e2ef88b9df59e8ca72b1f8c97353</citedby><cites>FETCH-LOGICAL-c359t-666bc72d07b6a2ddd2d35dc4c9419fdbfda18e2ef88b9df59e8ca72b1f8c97353</cites><orcidid>0000-0003-1147-524X ; 0000-0002-3088-4199 ; 0000-0002-7608-3274</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,3026,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/20466941$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.inrae.fr/hal-02662198$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Cherbuy, Claire</creatorcontrib><creatorcontrib>Honvo-Houeto, Edith</creatorcontrib><creatorcontrib>Bruneau, Aurélia</creatorcontrib><creatorcontrib>Bridonneau, Chantal</creatorcontrib><creatorcontrib>Mayeur, Camille</creatorcontrib><creatorcontrib>Duée, Pierre-Henri</creatorcontrib><creatorcontrib>Langella, Philippe</creatorcontrib><creatorcontrib>Thomas, Muriel</creatorcontrib><title>Microbiota matures colonic epithelium through a coordinated induction of cell cycle-related proteins in gnotobiotic rat</title><title>American journal of physiology: Gastrointestinal and liver physiology</title><addtitle>Am J Physiol Gastrointest Liver Physiol</addtitle><description>Previous studies have suggested that intestinal microbiota modulates colonic epithelium renewal. The objective of our work was to study the effects of microbiota on colonic epithelium structure and cell cycle-related proteins by using gnotobiotic rats. Colonic crypts and amount of cell cycle-related proteins were compared between germ-free (GF), conventional (CV), and conventionalized rats by histochemistry and Western blot. Ki67 and proliferating cell nuclear antigen (PCNA) were used as surrogates for proliferative cells; p21(cip1) and p27(kip1) were markers of cell cycle arrest; anti- and proapoptotic proteins, Bcl2 and Bax, respectively, were also studied. We observed 40% increase of the crypt proliferative area 2 days after inoculation of GF rats with a complex microbiota. This recruitment of proliferative cells may account for the 30% increase of crypt depth observed between CV and GF rats. The hyperproliferative boost induced by microbiota was compensated by a fourfold increase of p21(cip1) and p27(kip1) involved in cell cycle arrest and a 30% drop of antiapoptotic Bcl2 protein while Bax was unchanged. Inductions of p21(cip1), p27(kip1), and PCNA protein were not paralleled by an increase of the corresponding mRNA. We also showed that p21(cip1) induction by microbiota was partially restored by Bacteroides thetaiotaomicron, Ruminococcus gnavus, and Clostridium paraputrificum. Colonization of the colon by a complex microbiota increases the crypt depth of colon epithelium. This event takes place in conjunction with a multistep process: a hyperproliferative boost accompanied by compensatory events as induction of p21(cip1) and p27(kip1) and decrease of Bcl2.</description><subject>Adaptation, Physiological</subject><subject>Animals</subject><subject>Antigens</subject><subject>Blotting, Western</subject><subject>Cell Cycle</subject><subject>Cell Cycle Proteins - biosynthesis</subject><subject>Cell Proliferation</subject><subject>Colon</subject><subject>Colon - growth & development</subject><subject>Colon - metabolism</subject><subject>Colon - microbiology</subject><subject>Colon - physiology</subject><subject>Cyclin-Dependent Kinase Inhibitor p21 - metabolism</subject><subject>Cyclin-Dependent Kinase Inhibitor p27 - metabolism</subject><subject>Germ-Free Life</subject><subject>Histocytochemistry</subject><subject>Intestinal Mucosa - growth & development</subject><subject>Intestinal Mucosa - metabolism</subject><subject>Intestinal Mucosa - microbiology</subject><subject>Intestinal Mucosa - physiology</subject><subject>Life Sciences</subject><subject>Male</subject><subject>Metagenome</subject><subject>Physiology</subject><subject>Proteins</subject><subject>Proto-Oncogene Proteins c-bcl-2 - metabolism</subject><subject>Rats</subject><subject>Rats, Inbred F344</subject><subject>Rodents</subject><issn>0193-1857</issn><issn>1522-1547</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2010</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkctvEzEQxi0EoqFw54QsLhWHTf1-HKuKUqQgLuVseW1v4mh3HWxvUf97nKT0wGmkmd988_gA-IjRGmNOru3-sI1rhKhia4KQfgVWLU06zJl8DVYIa9phxeUFeFfKHiHECcZvwQVBTAjN8Ar8-RFdTn1M1cLJ1iWHAl0a0xwdDIdYd2GMywTrLqdlu4O2FVP2cbY1eBhnv7ga0wzTAF0YR-ie3Bi6HMZT_ZBTDXEuDYTbOdXTnCacbX0P3gx2LOHDc7wEv-6-Ptzed5uf377f3mw6R7munRCid5J4JHthifeeeMq9Y64trwffD95iFUgYlOq1H7gOyllJejwopyXl9BJ8Oevu7GgOOU42P5lko7m_2ZhjDhEhCNbqETf26sy2vX8voVQzxXI8y84hLcVIprSiEotGfv6P3Kclz-0QIyljklOGGoTOUHtwKTkML_MxMkf7zMk-c7LPHO1rLZ-edZd-Cv6l4Z9f9C_Y7Jjs</recordid><startdate>20100801</startdate><enddate>20100801</enddate><creator>Cherbuy, Claire</creator><creator>Honvo-Houeto, Edith</creator><creator>Bruneau, Aurélia</creator><creator>Bridonneau, Chantal</creator><creator>Mayeur, Camille</creator><creator>Duée, Pierre-Henri</creator><creator>Langella, Philippe</creator><creator>Thomas, Muriel</creator><general>American Physiological Society</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>1XC</scope><orcidid>https://orcid.org/0000-0003-1147-524X</orcidid><orcidid>https://orcid.org/0000-0002-3088-4199</orcidid><orcidid>https://orcid.org/0000-0002-7608-3274</orcidid></search><sort><creationdate>20100801</creationdate><title>Microbiota matures colonic epithelium through a coordinated induction of cell cycle-related proteins in gnotobiotic rat</title><author>Cherbuy, Claire ; 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The objective of our work was to study the effects of microbiota on colonic epithelium structure and cell cycle-related proteins by using gnotobiotic rats. Colonic crypts and amount of cell cycle-related proteins were compared between germ-free (GF), conventional (CV), and conventionalized rats by histochemistry and Western blot. Ki67 and proliferating cell nuclear antigen (PCNA) were used as surrogates for proliferative cells; p21(cip1) and p27(kip1) were markers of cell cycle arrest; anti- and proapoptotic proteins, Bcl2 and Bax, respectively, were also studied. We observed 40% increase of the crypt proliferative area 2 days after inoculation of GF rats with a complex microbiota. This recruitment of proliferative cells may account for the 30% increase of crypt depth observed between CV and GF rats. The hyperproliferative boost induced by microbiota was compensated by a fourfold increase of p21(cip1) and p27(kip1) involved in cell cycle arrest and a 30% drop of antiapoptotic Bcl2 protein while Bax was unchanged. Inductions of p21(cip1), p27(kip1), and PCNA protein were not paralleled by an increase of the corresponding mRNA. We also showed that p21(cip1) induction by microbiota was partially restored by Bacteroides thetaiotaomicron, Ruminococcus gnavus, and Clostridium paraputrificum. Colonization of the colon by a complex microbiota increases the crypt depth of colon epithelium. This event takes place in conjunction with a multistep process: a hyperproliferative boost accompanied by compensatory events as induction of p21(cip1) and p27(kip1) and decrease of Bcl2.</abstract><cop>United States</cop><pub>American Physiological Society</pub><pmid>20466941</pmid><doi>10.1152/ajpgi.00384.2009</doi><orcidid>https://orcid.org/0000-0003-1147-524X</orcidid><orcidid>https://orcid.org/0000-0002-3088-4199</orcidid><orcidid>https://orcid.org/0000-0002-7608-3274</orcidid></addata></record> |
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| subjects | Adaptation, Physiological Animals Antigens Blotting, Western Cell Cycle Cell Cycle Proteins - biosynthesis Cell Proliferation Colon Colon - growth & development Colon - metabolism Colon - microbiology Colon - physiology Cyclin-Dependent Kinase Inhibitor p21 - metabolism Cyclin-Dependent Kinase Inhibitor p27 - metabolism Germ-Free Life Histocytochemistry Intestinal Mucosa - growth & development Intestinal Mucosa - metabolism Intestinal Mucosa - microbiology Intestinal Mucosa - physiology Life Sciences Male Metagenome Physiology Proteins Proto-Oncogene Proteins c-bcl-2 - metabolism Rats Rats, Inbred F344 Rodents |
| title | Microbiota matures colonic epithelium through a coordinated induction of cell cycle-related proteins in gnotobiotic rat |
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