Decreased levels of bisecting GlcNAc glycoforms of IgG are associated with human longevity
Markers for longevity that reflect the health condition and predict healthy aging are extremely scarce. Such markers are, however, valuable in aging research. It has been shown previously that the N-glycosylation pattern of human immunoglobulin G (IgG) is age-dependent. Here we investigate whether N...
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| creator | Ruhaak, L Renee Uh, Hae-Won Beekman, Marian Koeleman, Carolien A M Hokke, Cornelis H Westendorp, Rudi G J Wuhrer, Manfred Houwing-Duistermaat, Jeanine J Slagboom, P Eline Deelder, André M |
| description | Markers for longevity that reflect the health condition and predict healthy aging are extremely scarce. Such markers are, however, valuable in aging research. It has been shown previously that the N-glycosylation pattern of human immunoglobulin G (IgG) is age-dependent. Here we investigate whether N-linked glycans reflect early features of human longevity.
The Leiden Longevity Study (LLS) consists of nonagenarian sibling pairs, their offspring, and partners of the offspring serving as control. IgG subclass specific glycosylation patterns were obtained from 1967 participants in the LLS by MALDI-TOF-MS analysis of tryptic IgG Fc glycopeptides. Several regression strategies were applied to evaluate the association of IgG glycosylation with age, sex, and longevity. The degree of galactosylation of IgG decreased with increasing age. For the galactosylated glycoforms the incidence of bisecting GlcNAc increased as a function of age. Sex-related differences were observed at ages below 60 years. Compared to males, younger females had higher galactosylation, which decreased stronger with increasing age, resulting in similar galactosylation for both sexes from 60 onwards. In younger participants (60 years), decreased levels of non-galactosylated glycoforms containing a bisecting GlcNAc reflected early features of longevity.
We here describe IgG glycoforms associated with calendar age at all ages and the propensity for longevity before middle age. As modulation of IgG effector functions has been described for various IgG glycosylation features, a modulatory effect may be expected for the longevity marker described in this study. |
| doi_str_mv | 10.1371/journal.pone.0012566 |
| format | Article |
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The Leiden Longevity Study (LLS) consists of nonagenarian sibling pairs, their offspring, and partners of the offspring serving as control. IgG subclass specific glycosylation patterns were obtained from 1967 participants in the LLS by MALDI-TOF-MS analysis of tryptic IgG Fc glycopeptides. Several regression strategies were applied to evaluate the association of IgG glycosylation with age, sex, and longevity. The degree of galactosylation of IgG decreased with increasing age. For the galactosylated glycoforms the incidence of bisecting GlcNAc increased as a function of age. Sex-related differences were observed at ages below 60 years. Compared to males, younger females had higher galactosylation, which decreased stronger with increasing age, resulting in similar galactosylation for both sexes from 60 onwards. In younger participants (<60 years of age), but not in the older age group (>60 years), decreased levels of non-galactosylated glycoforms containing a bisecting GlcNAc reflected early features of longevity.
We here describe IgG glycoforms associated with calendar age at all ages and the propensity for longevity before middle age. As modulation of IgG effector functions has been described for various IgG glycosylation features, a modulatory effect may be expected for the longevity marker described in this study.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0012566</identifier><identifier>PMID: 20830288</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adult ; Age ; Age Factors ; Aged ; Aging ; Analysis ; Bayesian analysis ; Biochemistry/Structural Genomics ; Bioinformatics ; Calendars ; Centenarians ; Chemical Biology/Protein Chemistry and Proteomics ; Cloning ; Cytotoxicity ; Developmental Biology/Aging ; Developmental Biology/Molecular Development ; Enzymes ; Epidemiology ; Female ; Females ; Geriatrics ; Glycopeptides ; Glycoproteins ; Glycosylation ; Humans ; Immunoglobulin Fc Fragments - metabolism ; Immunoglobulin G ; Immunoglobulin G - metabolism ; Immunoglobulins ; Immunology ; Immunology/Immunomodulation ; Longevity ; Male ; Males ; Markers ; Mass spectrometry ; Medical statistics ; Middle Aged ; N-glycans ; Neutrophils ; Nonagenarian ; Offspring ; Oldest old people ; Parasitology ; Pedigree ; Plasma ; Polysaccharides ; Polysaccharides - metabolism ; Population ; Proteins ; Regression analysis ; Scientific imaging ; Sex ; Sex differences ; Studies</subject><ispartof>PloS one, 2010-09, Vol.5 (9), p.e12566-e12566</ispartof><rights>COPYRIGHT 2010 Public Library of Science</rights><rights>2010 Ruhaak et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Ruhaak et al. 2010</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c793t-f5c5350aa6e2b66202613c2bee77ea4a09df4cba47fca8c137154afa3bf934993</citedby><cites>FETCH-LOGICAL-c793t-f5c5350aa6e2b66202613c2bee77ea4a09df4cba47fca8c137154afa3bf934993</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2935362/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2935362/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79569,79570</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/20830288$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ruhaak, L Renee</creatorcontrib><creatorcontrib>Uh, Hae-Won</creatorcontrib><creatorcontrib>Beekman, Marian</creatorcontrib><creatorcontrib>Koeleman, Carolien A M</creatorcontrib><creatorcontrib>Hokke, Cornelis H</creatorcontrib><creatorcontrib>Westendorp, Rudi G J</creatorcontrib><creatorcontrib>Wuhrer, Manfred</creatorcontrib><creatorcontrib>Houwing-Duistermaat, Jeanine J</creatorcontrib><creatorcontrib>Slagboom, P Eline</creatorcontrib><creatorcontrib>Deelder, André M</creatorcontrib><title>Decreased levels of bisecting GlcNAc glycoforms of IgG are associated with human longevity</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Markers for longevity that reflect the health condition and predict healthy aging are extremely scarce. Such markers are, however, valuable in aging research. It has been shown previously that the N-glycosylation pattern of human immunoglobulin G (IgG) is age-dependent. Here we investigate whether N-linked glycans reflect early features of human longevity.
The Leiden Longevity Study (LLS) consists of nonagenarian sibling pairs, their offspring, and partners of the offspring serving as control. IgG subclass specific glycosylation patterns were obtained from 1967 participants in the LLS by MALDI-TOF-MS analysis of tryptic IgG Fc glycopeptides. Several regression strategies were applied to evaluate the association of IgG glycosylation with age, sex, and longevity. The degree of galactosylation of IgG decreased with increasing age. For the galactosylated glycoforms the incidence of bisecting GlcNAc increased as a function of age. Sex-related differences were observed at ages below 60 years. Compared to males, younger females had higher galactosylation, which decreased stronger with increasing age, resulting in similar galactosylation for both sexes from 60 onwards. In younger participants (<60 years of age), but not in the older age group (>60 years), decreased levels of non-galactosylated glycoforms containing a bisecting GlcNAc reflected early features of longevity.
We here describe IgG glycoforms associated with calendar age at all ages and the propensity for longevity before middle age. As modulation of IgG effector functions has been described for various IgG glycosylation features, a modulatory effect may be expected for the longevity marker described in this study.</description><subject>Adult</subject><subject>Age</subject><subject>Age Factors</subject><subject>Aged</subject><subject>Aging</subject><subject>Analysis</subject><subject>Bayesian analysis</subject><subject>Biochemistry/Structural Genomics</subject><subject>Bioinformatics</subject><subject>Calendars</subject><subject>Centenarians</subject><subject>Chemical Biology/Protein Chemistry and Proteomics</subject><subject>Cloning</subject><subject>Cytotoxicity</subject><subject>Developmental Biology/Aging</subject><subject>Developmental Biology/Molecular 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people</subject><subject>Parasitology</subject><subject>Pedigree</subject><subject>Plasma</subject><subject>Polysaccharides</subject><subject>Polysaccharides - metabolism</subject><subject>Population</subject><subject>Proteins</subject><subject>Regression analysis</subject><subject>Scientific imaging</subject><subject>Sex</subject><subject>Sex 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levels of bisecting GlcNAc glycoforms of IgG are associated with human longevity</title><author>Ruhaak, L Renee ; Uh, Hae-Won ; Beekman, Marian ; Koeleman, Carolien A M ; Hokke, Cornelis H ; Westendorp, Rudi G J ; Wuhrer, Manfred ; Houwing-Duistermaat, Jeanine J ; Slagboom, P Eline ; Deelder, André M</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c793t-f5c5350aa6e2b66202613c2bee77ea4a09df4cba47fca8c137154afa3bf934993</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2010</creationdate><topic>Adult</topic><topic>Age</topic><topic>Age Factors</topic><topic>Aged</topic><topic>Aging</topic><topic>Analysis</topic><topic>Bayesian analysis</topic><topic>Biochemistry/Structural Genomics</topic><topic>Bioinformatics</topic><topic>Calendars</topic><topic>Centenarians</topic><topic>Chemical Biology/Protein Chemistry and Proteomics</topic><topic>Cloning</topic><topic>Cytotoxicity</topic><topic>Developmental 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Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ruhaak, L Renee</au><au>Uh, Hae-Won</au><au>Beekman, Marian</au><au>Koeleman, Carolien A M</au><au>Hokke, Cornelis H</au><au>Westendorp, Rudi G J</au><au>Wuhrer, Manfred</au><au>Houwing-Duistermaat, Jeanine J</au><au>Slagboom, P Eline</au><au>Deelder, André M</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Decreased levels of bisecting GlcNAc glycoforms of IgG are associated with human longevity</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2010-09-07</date><risdate>2010</risdate><volume>5</volume><issue>9</issue><spage>e12566</spage><epage>e12566</epage><pages>e12566-e12566</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Markers for longevity that reflect the health condition and predict healthy aging are extremely scarce. Such markers are, however, valuable in aging research. It has been shown previously that the N-glycosylation pattern of human immunoglobulin G (IgG) is age-dependent. Here we investigate whether N-linked glycans reflect early features of human longevity.
The Leiden Longevity Study (LLS) consists of nonagenarian sibling pairs, their offspring, and partners of the offspring serving as control. IgG subclass specific glycosylation patterns were obtained from 1967 participants in the LLS by MALDI-TOF-MS analysis of tryptic IgG Fc glycopeptides. Several regression strategies were applied to evaluate the association of IgG glycosylation with age, sex, and longevity. The degree of galactosylation of IgG decreased with increasing age. For the galactosylated glycoforms the incidence of bisecting GlcNAc increased as a function of age. Sex-related differences were observed at ages below 60 years. Compared to males, younger females had higher galactosylation, which decreased stronger with increasing age, resulting in similar galactosylation for both sexes from 60 onwards. In younger participants (<60 years of age), but not in the older age group (>60 years), decreased levels of non-galactosylated glycoforms containing a bisecting GlcNAc reflected early features of longevity.
We here describe IgG glycoforms associated with calendar age at all ages and the propensity for longevity before middle age. As modulation of IgG effector functions has been described for various IgG glycosylation features, a modulatory effect may be expected for the longevity marker described in this study.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>20830288</pmid><doi>10.1371/journal.pone.0012566</doi><tpages>e12566</tpages><oa>free_for_read</oa></addata></record> |
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| language | eng |
| recordid | cdi_plos_journals_1292285704 |
| source | Public Library of Science (PLoS) Journals Open Access; MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Adult Age Age Factors Aged Aging Analysis Bayesian analysis Biochemistry/Structural Genomics Bioinformatics Calendars Centenarians Chemical Biology/Protein Chemistry and Proteomics Cloning Cytotoxicity Developmental Biology/Aging Developmental Biology/Molecular Development Enzymes Epidemiology Female Females Geriatrics Glycopeptides Glycoproteins Glycosylation Humans Immunoglobulin Fc Fragments - metabolism Immunoglobulin G Immunoglobulin G - metabolism Immunoglobulins Immunology Immunology/Immunomodulation Longevity Male Males Markers Mass spectrometry Medical statistics Middle Aged N-glycans Neutrophils Nonagenarian Offspring Oldest old people Parasitology Pedigree Plasma Polysaccharides Polysaccharides - metabolism Population Proteins Regression analysis Scientific imaging Sex Sex differences Studies |
| title | Decreased levels of bisecting GlcNAc glycoforms of IgG are associated with human longevity |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-21T18%3A16%3A27IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Decreased%20levels%20of%20bisecting%20GlcNAc%20glycoforms%20of%20IgG%20are%20associated%20with%20human%20longevity&rft.jtitle=PloS%20one&rft.au=Ruhaak,%20L%20Renee&rft.date=2010-09-07&rft.volume=5&rft.issue=9&rft.spage=e12566&rft.epage=e12566&rft.pages=e12566-e12566&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0012566&rft_dat=%3Cgale_plos_%3EA473863833%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1292285704&rft_id=info:pmid/20830288&rft_galeid=A473863833&rft_doaj_id=oai_doaj_org_article_254679fc5da44461af61d94e662aee7f&rfr_iscdi=true |