Lactobacillus rhamnosus GG Colonization in Early Life Ameliorates Inflammaging of Offspring by Activating SIRT1/AMPK/PGC-1α Pathway
Inflammaging refers to chronic, low-grade inflammation during aging, which contributes to the pathogenesis of age-related diseases. Studies have shown that probiotic intervention in the aging stage could delay aging-related disorders. However, whether the application of probiotics in early life coul...
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| description | Inflammaging refers to chronic, low-grade inflammation during aging, which contributes to the pathogenesis of age-related diseases. Studies have shown that probiotic intervention in the aging stage could delay aging-related disorders. However, whether the application of probiotics in early life could have antiaging effects on offspring was unknown. Here, we investigated the effects of Lactobacillus rhamnosus GG (LGG) colonization in early life on inflammaging of offspring. Pregnant mice with the same conception time were given LGG live bacteria (LC group) or LGG fixed bacteria (NC group) from the 18th day after pregnancy until natural birth. The progeny mice were treated with 107 cfu of live or fixed LGG for 0-5 days after birth, respectively. LGG colonization could be detected in the feces of 3-week offspring. The 16S rRNA sequencing analysis of 3-week-old offspring showed that colonization of LGG in early life could alter the composition and diversity of gut microbiota. Interestingly, the beneficial effects of LGG colonization in early life on the microbiota lasted to 8 months old. The abundance of longevity-related bacteria (Lactobacillus, Bifidobacterium, and Akkermansia muciniphila) increased significantly in the LGG colonization group. In addition, LGG colonization increased the abundance of short-chain fatty acid- (SCFA-) producing bacteria and the production of cecal SCFAs. LGG colonization in early life protected the intestinal barrier, enhanced antioxidant defense, attenuated epithelial cell DNA damage, and inhibited intestinal low-grade inflammation in 8-month-old progeny mice. Mechanically, LGG could upregulate Sirtuin1 (SIRT1)/Adenosine 5′-monophosphate-activated protein kinase (AMPK)/Peroxisome proliferator-activated receptor γ coactivator 1-α (PGC-1α) pathway and repress activation of nuclear factor-kappa B (NF-κB), while the protective effect of LGG was blunted after SIRT1 gene silencing. Together, LGG colonization in early life could ameliorate inflammaging of offspring, which would provide a new strategy for the prevention of age-related diseases. |
| doi_str_mv | 10.1155/2021/3328505 |
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Studies have shown that probiotic intervention in the aging stage could delay aging-related disorders. However, whether the application of probiotics in early life could have antiaging effects on offspring was unknown. Here, we investigated the effects of Lactobacillus rhamnosus GG (LGG) colonization in early life on inflammaging of offspring. Pregnant mice with the same conception time were given LGG live bacteria (LC group) or LGG fixed bacteria (NC group) from the 18th day after pregnancy until natural birth. The progeny mice were treated with 107 cfu of live or fixed LGG for 0-5 days after birth, respectively. LGG colonization could be detected in the feces of 3-week offspring. The 16S rRNA sequencing analysis of 3-week-old offspring showed that colonization of LGG in early life could alter the composition and diversity of gut microbiota. Interestingly, the beneficial effects of LGG colonization in early life on the microbiota lasted to 8 months old. The abundance of longevity-related bacteria (Lactobacillus, Bifidobacterium, and Akkermansia muciniphila) increased significantly in the LGG colonization group. In addition, LGG colonization increased the abundance of short-chain fatty acid- (SCFA-) producing bacteria and the production of cecal SCFAs. LGG colonization in early life protected the intestinal barrier, enhanced antioxidant defense, attenuated epithelial cell DNA damage, and inhibited intestinal low-grade inflammation in 8-month-old progeny mice. Mechanically, LGG could upregulate Sirtuin1 (SIRT1)/Adenosine 5′-monophosphate-activated protein kinase (AMPK)/Peroxisome proliferator-activated receptor γ coactivator 1-α (PGC-1α) pathway and repress activation of nuclear factor-kappa B (NF-κB), while the protective effect of LGG was blunted after SIRT1 gene silencing. Together, LGG colonization in early life could ameliorate inflammaging of offspring, which would provide a new strategy for the prevention of age-related diseases.</description><identifier>ISSN: 1942-0900</identifier><identifier>EISSN: 1942-0994</identifier><identifier>DOI: 10.1155/2021/3328505</identifier><identifier>PMID: 34804363</identifier><language>eng</language><publisher>United States: Hindawi</publisher><subject>Aging ; AMP-Activated Protein Kinases - genetics ; AMP-Activated Protein Kinases - metabolism ; Animals ; Animals, Newborn ; Antibodies ; Colon ; Feces ; Female ; Gastrointestinal Microbiome ; Gene Expression Regulation - drug effects ; Inflammation - microbiology ; Inflammation - pathology ; Inflammation - prevention & control ; Intestines - drug effects ; Intestines - microbiology ; Lactobacillus rhamnosus - physiology ; Male ; Mice ; Mice, Inbred C57BL ; Microbiota ; NF-kappa B - genetics ; NF-kappa B - metabolism ; Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha - genetics ; Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha - metabolism ; Pregnancy ; Probiotics - administration & dosage ; Proteins ; Sirtuin 1 - genetics ; Sirtuin 1 - metabolism ; Vagina</subject><ispartof>Oxidative medicine and cellular longevity, 2021, Vol.2021 (1), p.3328505-3328505</ispartof><rights>Copyright © 2021 Tianyu Liu et al.</rights><rights>Copyright © 2021 Tianyu Liu et al. This is an open access article distributed under the Creative Commons Attribution License (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. https://creativecommons.org/licenses/by/4.0</rights><rights>Copyright © 2021 Tianyu Liu et al. 2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c448t-f545c08d78115a23f0d72e41572f450b6129562414b111f164a8bc7c855ddbd93</citedby><cites>FETCH-LOGICAL-c448t-f545c08d78115a23f0d72e41572f450b6129562414b111f164a8bc7c855ddbd93</cites><orcidid>0000-0002-4702-9711 ; 0000-0002-8410-7715 ; 0000-0002-0147-7826</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8601837/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8601837/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,4024,27923,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34804363$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Mendoza-Núñez, Víctor M.</contributor><contributor>Víctor M Mendoza-Núñez</contributor><creatorcontrib>Liu, Tianyu</creatorcontrib><creatorcontrib>Song, Xueli</creatorcontrib><creatorcontrib>An, Yaping</creatorcontrib><creatorcontrib>Wu, Xuemei</creatorcontrib><creatorcontrib>Zhang, Wanru</creatorcontrib><creatorcontrib>Li, Jia</creatorcontrib><creatorcontrib>Sun, Yue</creatorcontrib><creatorcontrib>Jin, Ge</creatorcontrib><creatorcontrib>Liu, Xiang</creatorcontrib><creatorcontrib>Guo, Zixuan</creatorcontrib><creatorcontrib>Wang, Bangmao</creatorcontrib><creatorcontrib>Lei, Ping</creatorcontrib><creatorcontrib>Cao, Hailong</creatorcontrib><title>Lactobacillus rhamnosus GG Colonization in Early Life Ameliorates Inflammaging of Offspring by Activating SIRT1/AMPK/PGC-1α Pathway</title><title>Oxidative medicine and cellular longevity</title><addtitle>Oxid Med Cell Longev</addtitle><description>Inflammaging refers to chronic, low-grade inflammation during aging, which contributes to the pathogenesis of age-related diseases. Studies have shown that probiotic intervention in the aging stage could delay aging-related disorders. However, whether the application of probiotics in early life could have antiaging effects on offspring was unknown. Here, we investigated the effects of Lactobacillus rhamnosus GG (LGG) colonization in early life on inflammaging of offspring. Pregnant mice with the same conception time were given LGG live bacteria (LC group) or LGG fixed bacteria (NC group) from the 18th day after pregnancy until natural birth. The progeny mice were treated with 107 cfu of live or fixed LGG for 0-5 days after birth, respectively. LGG colonization could be detected in the feces of 3-week offspring. The 16S rRNA sequencing analysis of 3-week-old offspring showed that colonization of LGG in early life could alter the composition and diversity of gut microbiota. Interestingly, the beneficial effects of LGG colonization in early life on the microbiota lasted to 8 months old. The abundance of longevity-related bacteria (Lactobacillus, Bifidobacterium, and Akkermansia muciniphila) increased significantly in the LGG colonization group. In addition, LGG colonization increased the abundance of short-chain fatty acid- (SCFA-) producing bacteria and the production of cecal SCFAs. LGG colonization in early life protected the intestinal barrier, enhanced antioxidant defense, attenuated epithelial cell DNA damage, and inhibited intestinal low-grade inflammation in 8-month-old progeny mice. Mechanically, LGG could upregulate Sirtuin1 (SIRT1)/Adenosine 5′-monophosphate-activated protein kinase (AMPK)/Peroxisome proliferator-activated receptor γ coactivator 1-α (PGC-1α) pathway and repress activation of nuclear factor-kappa B (NF-κB), while the protective effect of LGG was blunted after SIRT1 gene silencing. Together, LGG colonization in early life could ameliorate inflammaging of offspring, which would provide a new strategy for the prevention of age-related diseases.</description><subject>Aging</subject><subject>AMP-Activated Protein Kinases - genetics</subject><subject>AMP-Activated Protein Kinases - metabolism</subject><subject>Animals</subject><subject>Animals, Newborn</subject><subject>Antibodies</subject><subject>Colon</subject><subject>Feces</subject><subject>Female</subject><subject>Gastrointestinal Microbiome</subject><subject>Gene Expression Regulation - drug effects</subject><subject>Inflammation - microbiology</subject><subject>Inflammation - pathology</subject><subject>Inflammation - prevention & control</subject><subject>Intestines - drug effects</subject><subject>Intestines - microbiology</subject><subject>Lactobacillus rhamnosus - physiology</subject><subject>Male</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Microbiota</subject><subject>NF-kappa B - genetics</subject><subject>NF-kappa B - metabolism</subject><subject>Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha - genetics</subject><subject>Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha - metabolism</subject><subject>Pregnancy</subject><subject>Probiotics - administration & dosage</subject><subject>Proteins</subject><subject>Sirtuin 1 - genetics</subject><subject>Sirtuin 1 - metabolism</subject><subject>Vagina</subject><issn>1942-0900</issn><issn>1942-0994</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>RHX</sourceid><sourceid>EIF</sourceid><sourceid>8G5</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><recordid>eNp9kc1uEzEURkcIREthxxpZYoMEQ_w749kgRVEbIoIaQVlbHo-duPLYxZ5pFdZ9IV6EZ8IhIQIWrHyvfHR0P31F8RzBtwgxNsEQowkhmDPIHhSnqKG4hE1DHx5nCE-KJyldQ1gRTNHj4oRQDimpyGlxv5RqCK1U1rkxgbiRvQ8pT_M5mAUXvP0mBxs8sB6cy-i2YGmNBtNeOxuiHHQCC2-c7Hu5tn4NggGXxqSbuFvaLZiqwd5mQ94-Lz5docn04-rDZDWflejHd7CSw-ZObp8Wj4x0ST87vGfFl4vzq9n7cnk5X8ymy1JRyofSMMoU5F3Nc3CJiYFdjTVFrMaGMthWCDesyglpixAyqKKSt6pWnLGua7uGnBXv9t6bse11p7QfonQiH9vLuBVBWvH3j7cbsQ63glcQcVJnwauDIIavo06D6G1S2jnpdRiTwBWEHGPGeEZf_oNehzH6HO8XBSteYZKpN3tKxZBS1OZ4DIJiV6_Y1SsO9Wb8xZ8BjvDvPjPweg9srO_knf2_7ieJF6yd</recordid><startdate>2021</startdate><enddate>2021</enddate><creator>Liu, Tianyu</creator><creator>Song, Xueli</creator><creator>An, Yaping</creator><creator>Wu, Xuemei</creator><creator>Zhang, Wanru</creator><creator>Li, Jia</creator><creator>Sun, Yue</creator><creator>Jin, Ge</creator><creator>Liu, Xiang</creator><creator>Guo, Zixuan</creator><creator>Wang, Bangmao</creator><creator>Lei, Ping</creator><creator>Cao, Hailong</creator><general>Hindawi</general><general>Hindawi Limited</general><scope>RHU</scope><scope>RHW</scope><scope>RHX</scope><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>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BENPR</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>K9.</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>MBDVC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-4702-9711</orcidid><orcidid>https://orcid.org/0000-0002-8410-7715</orcidid><orcidid>https://orcid.org/0000-0002-0147-7826</orcidid></search><sort><creationdate>2021</creationdate><title>Lactobacillus rhamnosus GG Colonization in Early Life Ameliorates Inflammaging of Offspring by Activating SIRT1/AMPK/PGC-1α Pathway</title><author>Liu, Tianyu ; Song, Xueli ; An, Yaping ; Wu, Xuemei ; Zhang, Wanru ; Li, Jia ; Sun, Yue ; Jin, Ge ; Liu, Xiang ; Guo, Zixuan ; Wang, Bangmao ; Lei, Ping ; Cao, Hailong</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c448t-f545c08d78115a23f0d72e41572f450b6129562414b111f164a8bc7c855ddbd93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Aging</topic><topic>AMP-Activated Protein Kinases - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Oxidative medicine and cellular longevity</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Liu, Tianyu</au><au>Song, Xueli</au><au>An, Yaping</au><au>Wu, Xuemei</au><au>Zhang, Wanru</au><au>Li, Jia</au><au>Sun, Yue</au><au>Jin, Ge</au><au>Liu, Xiang</au><au>Guo, Zixuan</au><au>Wang, Bangmao</au><au>Lei, Ping</au><au>Cao, Hailong</au><au>Mendoza-Núñez, Víctor M.</au><au>Víctor M Mendoza-Núñez</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Lactobacillus rhamnosus GG Colonization in Early Life Ameliorates Inflammaging of Offspring by Activating SIRT1/AMPK/PGC-1α Pathway</atitle><jtitle>Oxidative medicine and cellular longevity</jtitle><addtitle>Oxid Med Cell Longev</addtitle><date>2021</date><risdate>2021</risdate><volume>2021</volume><issue>1</issue><spage>3328505</spage><epage>3328505</epage><pages>3328505-3328505</pages><issn>1942-0900</issn><eissn>1942-0994</eissn><abstract>Inflammaging refers to chronic, low-grade inflammation during aging, which contributes to the pathogenesis of age-related diseases. Studies have shown that probiotic intervention in the aging stage could delay aging-related disorders. However, whether the application of probiotics in early life could have antiaging effects on offspring was unknown. Here, we investigated the effects of Lactobacillus rhamnosus GG (LGG) colonization in early life on inflammaging of offspring. Pregnant mice with the same conception time were given LGG live bacteria (LC group) or LGG fixed bacteria (NC group) from the 18th day after pregnancy until natural birth. The progeny mice were treated with 107 cfu of live or fixed LGG for 0-5 days after birth, respectively. LGG colonization could be detected in the feces of 3-week offspring. The 16S rRNA sequencing analysis of 3-week-old offspring showed that colonization of LGG in early life could alter the composition and diversity of gut microbiota. Interestingly, the beneficial effects of LGG colonization in early life on the microbiota lasted to 8 months old. The abundance of longevity-related bacteria (Lactobacillus, Bifidobacterium, and Akkermansia muciniphila) increased significantly in the LGG colonization group. In addition, LGG colonization increased the abundance of short-chain fatty acid- (SCFA-) producing bacteria and the production of cecal SCFAs. LGG colonization in early life protected the intestinal barrier, enhanced antioxidant defense, attenuated epithelial cell DNA damage, and inhibited intestinal low-grade inflammation in 8-month-old progeny mice. Mechanically, LGG could upregulate Sirtuin1 (SIRT1)/Adenosine 5′-monophosphate-activated protein kinase (AMPK)/Peroxisome proliferator-activated receptor γ coactivator 1-α (PGC-1α) pathway and repress activation of nuclear factor-kappa B (NF-κB), while the protective effect of LGG was blunted after SIRT1 gene silencing. Together, LGG colonization in early life could ameliorate inflammaging of offspring, which would provide a new strategy for the prevention of age-related diseases.</abstract><cop>United States</cop><pub>Hindawi</pub><pmid>34804363</pmid><doi>10.1155/2021/3328505</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0002-4702-9711</orcidid><orcidid>https://orcid.org/0000-0002-8410-7715</orcidid><orcidid>https://orcid.org/0000-0002-0147-7826</orcidid><oa>free_for_read</oa></addata></record> |
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| identifier | ISSN: 1942-0900 |
| ispartof | Oxidative medicine and cellular longevity, 2021, Vol.2021 (1), p.3328505-3328505 |
| issn | 1942-0900 1942-0994 |
| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_8601837 |
| source | MEDLINE; PubMed Central Open Access; EZB-FREE-00999 freely available EZB journals; Wiley Online Library (Open Access Collection); PubMed Central; Alma/SFX Local Collection |
| subjects | Aging AMP-Activated Protein Kinases - genetics AMP-Activated Protein Kinases - metabolism Animals Animals, Newborn Antibodies Colon Feces Female Gastrointestinal Microbiome Gene Expression Regulation - drug effects Inflammation - microbiology Inflammation - pathology Inflammation - prevention & control Intestines - drug effects Intestines - microbiology Lactobacillus rhamnosus - physiology Male Mice Mice, Inbred C57BL Microbiota NF-kappa B - genetics NF-kappa B - metabolism Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha - genetics Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha - metabolism Pregnancy Probiotics - administration & dosage Proteins Sirtuin 1 - genetics Sirtuin 1 - metabolism Vagina |
| title | Lactobacillus rhamnosus GG Colonization in Early Life Ameliorates Inflammaging of Offspring by Activating SIRT1/AMPK/PGC-1α Pathway |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-18T20%3A15%3A39IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Lactobacillus%20rhamnosus%20GG%20Colonization%20in%20Early%20Life%20Ameliorates%20Inflammaging%20of%20Offspring%20by%20Activating%20SIRT1/AMPK/PGC-1%CE%B1%20Pathway&rft.jtitle=Oxidative%20medicine%20and%20cellular%20longevity&rft.au=Liu,%20Tianyu&rft.date=2021&rft.volume=2021&rft.issue=1&rft.spage=3328505&rft.epage=3328505&rft.pages=3328505-3328505&rft.issn=1942-0900&rft.eissn=1942-0994&rft_id=info:doi/10.1155/2021/3328505&rft_dat=%3Cproquest_pubme%3E2600068623%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2600068623&rft_id=info:pmid/34804363&rfr_iscdi=true |