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Article ; Online: Pregnancy is linked to faster epigenetic aging in young women.

Ryan, Calen P / Lee, Nanette R / Carba, Delia B / MacIsaac, Julie L / Lin, David T S / Atashzay, Parmida / Belsky, Daniel W / Kobor, Michael S / Kuzawa, Christopher W

Proceedings of the National Academy of Sciences of the United States of America

2024 Volume 121, Issue 16, Page(s) e2317290121

Abstract: A central prediction of evolutionary theory is that energy invested into reproduction comes at the expense of somatic maintenance and repair, accelerating biological aging. Supporting this prediction are findings that high fertility among women predicts ... ...

Abstract	A central prediction of evolutionary theory is that energy invested into reproduction comes at the expense of somatic maintenance and repair, accelerating biological aging. Supporting this prediction are findings that high fertility among women predicts shorter lifespan and poorer health later in life. However, biological aging is thought to begin before age-related health declines, limiting the applicability of morbidity and mortality for studying the aging process earlier in life. Here, we examine the relationship between reproductive history and biological aging in a sample of young (20 to 22yo) men and women from the Cebu Longitudinal Health and Nutrition Survey, located in the Philippines (n = 1,735). We quantify biological aging using six measures, collectively known as epigenetic clocks, reflecting various facets of cellular aging, health, and mortality risk. In a subset of women, we test whether longitudinal changes in gravidity between young and early-middle adulthood (25 to 31yo) are associated with changes in epigenetic aging during that time. Cross-sectionally, gravidity was associated with all six measures of accelerated epigenetic aging in women (n = 825). Furthermore, longitudinal increases in gravidity were linked to accelerated epigenetic aging in two epigenetic clocks (n = 331). In contrast, the number of pregnancies a man reported fathering was not associated with epigenetic aging among same-aged cohort men (n = 910). These effects were robust to socioecological, environmental, and immunological factors, consistent with the hypothesis that pregnancy accelerates biological aging and that these effects can be detected in young women in a high-fertility context.
MeSH term(s)	Pregnancy ; Male ; Humans ; Female ; Adult ; Philippines ; Aging/genetics ; Reproduction/genetics ; Cellular Senescence ; Epigenesis, Genetic ; DNA Methylation
Language	English
Publishing date	2024-04-08
Publishing country	United States
Document type	Journal Article
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
DOI	10.1073/pnas.2317290121
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Article ; Online: Enzymatic protein depalmitoylation by acyl protein thioesterases.

Lin, David T S / Conibear, Elizabeth

Biochemical Society transactions

2015 Volume 43, Issue 2, Page(s) 193–198

Abstract: Protein palmitoylation is a dynamic post-translational modification, where the 16-carbon fatty acid, palmitate, is added to cysteines of proteins to modulate protein sorting, targeting and signalling. Palmitate removal from proteins is mediated by acyl ... ...

Abstract	Protein palmitoylation is a dynamic post-translational modification, where the 16-carbon fatty acid, palmitate, is added to cysteines of proteins to modulate protein sorting, targeting and signalling. Palmitate removal from proteins is mediated by acyl protein thioesterases (APTs). Although initially identified as lysophospholipases, increasing evidence suggests APT1 and APT2 are the major APTs that mediate the depalmitoylation of diverse cellular substrates. Here, we describe the conserved functions of APT1 and APT2 across organisms and discuss the possibility that these enzymes are members of a larger family of depalmitoylation enzymes.
MeSH term(s)	Cysteine/genetics ; Cysteine/metabolism ; Drug Discovery ; Humans ; Lipoylation/genetics ; Palmitates/metabolism ; Protein Transport ; Thiolester Hydrolases/genetics ; Thiolester Hydrolases/metabolism
Chemical Substances	Palmitates ; LYPLA1 protein, human (EC 3.1.2.-) ; LYPLA2 protein, human (EC 3.1.2.-) ; Thiolester Hydrolases (EC 3.1.2.-) ; Cysteine (K848JZ4886)
Language	English
Publishing date	2015-04
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	184237-7
ISSN	1470-8752 ; 0300-5127
ISSN (online)	1470-8752
ISSN	0300-5127
DOI	10.1042/BST20140235
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Article ; Online: DNA methylation signatures of youth-onset type 2 diabetes and exposure to maternal diabetes.

Salama, Ola E / Hizon, Nikho / Del Vecchio, Melissa / Kolsun, Kurt / Fonseca, Mario A / Lin, David T S / Urtatiz, Oscar / MacIsaac, Julia L / Kobor, Michael S / Sellers, Elizabeth A C / Dolinsky, Vernon W / Dart, Allison B / Jones, Meaghan J / Wicklow, Brandy A

Clinical epigenetics

2024 Volume 16, Issue 1, Page(s) 65

Abstract: Objective: Youth-onset type 2 diabetes (T2D) is physiologically distinct from adult-onset, but it is not clear how the two diseases differ at a molecular level. In utero exposure to maternal type 2 diabetes (T2D) is known to be a specific risk factor ... ...

Abstract	Objective: Youth-onset type 2 diabetes (T2D) is physiologically distinct from adult-onset, but it is not clear how the two diseases differ at a molecular level. In utero exposure to maternal type 2 diabetes (T2D) is known to be a specific risk factor for youth-onset T2D. DNA methylation (DNAm) changes associated with T2D but which differ between youth- and adult-onset might delineate the impacts of T2D development at different ages and could also determine the contribution of exposure to in utero diabetes. Methods: We performed an epigenome-wide analysis of DNAm on whole blood from 218 youth with T2D and 77 normoglycemic controls from the iCARE (improving renal Complications in Adolescents with type 2 diabetes through REsearch) cohort. Associations were tested using multiple linear regression models while adjusting for maternal diabetes, sex, age, BMI, smoking status, second-hand smoking exposure, cell-type proportions and genetic ancestry. Results: We identified 3830 differentially methylated sites associated with youth T2D onset, of which 3794 were moderately (adjusted p-value < 0.05 and effect size estimate > 0.01) associated and 36 were strongly (adjusted p-value < 0.05 and effect size estimate > 0.05) associated. A total of 3725 of these sites were not previously reported in the EWAS Atlas as associated with T2D, adult obesity or youth obesity. Moreover, three CpGs associated with youth-onset T2D in the PFKFB3 gene were also associated with maternal T2D exposure (FDR < 0.05 and effect size > 0.01). This is the first study to link PFKFB3 and T2D in youth. Conclusion: Our findings support that T2D in youth has different impacts on DNAm than adult-onset, and suggests that changes in DNAm could provide an important link between in utero exposure to maternal diabetes and the onset of T2D.
MeSH term(s)	Humans ; Diabetes Mellitus, Type 2/genetics ; Female ; DNA Methylation/genetics ; Pregnancy ; Adolescent ; Male ; Prenatal Exposure Delayed Effects/genetics ; Epigenesis, Genetic/genetics ; Age of Onset ; Child ; Case-Control Studies ; Diabetes, Gestational/genetics ; Adult ; Epigenome/genetics
Language	English
Publishing date	2024-05-13
Publishing country	Germany
Document type	Journal Article
ZDB-ID	2553921-8
ISSN	1868-7083 ; 1868-7075
ISSN (online)	1868-7083
ISSN	1868-7075
DOI	10.1186/s13148-024-01675-1
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Optimized CRISPR-mediated gene knockin reveals FOXP3-independent maintenance of human Treg identity.

Lam, Avery J / Lin, David T S / Gillies, Jana K / Uday, Prakruti / Pesenacker, Anne M / Kobor, Michael S / Levings, Megan K

Cell reports

2021 Volume 36, Issue 5, Page(s) 109494

Abstract: Regulatory T cell (Treg) therapy is a promising curative approach for a variety of immune-mediated conditions. CRISPR-based genome editing allows precise insertion of transgenes through homology-directed repair, but its use in human Tregs has been ... ...

Abstract	Regulatory T cell (Treg) therapy is a promising curative approach for a variety of immune-mediated conditions. CRISPR-based genome editing allows precise insertion of transgenes through homology-directed repair, but its use in human Tregs has been limited. We report an optimized protocol for CRISPR-mediated gene knockin in human Tregs with high-yield expansion. To establish a benchmark of human Treg dysfunction, we target the master transcription factor FOXP3 in naive and memory Tregs. Although FOXP3-ablated Tregs upregulate cytokine expression, effects on suppressive capacity in vitro manifest slowly and primarily in memory Tregs. Moreover, FOXP3-ablated Tregs retain their characteristic protein, transcriptional, and DNA methylation profile. Instead, FOXP3 maintains DNA methylation at regions enriched for AP-1 binding sites. Thus, although FOXP3 is important for human Treg development, it has a limited role in maintaining mature Treg identity. Optimized gene knockin with human Tregs will enable mechanistic studies and the development of tailored, next-generation Treg cell therapies.
MeSH term(s)	Base Sequence ; CRISPR-Cas Systems/genetics ; DNA Methylation/genetics ; DNA Repair ; Dependovirus/metabolism ; Forkhead Transcription Factors/metabolism ; Gene Knock-In Techniques ; Green Fluorescent Proteins/metabolism ; HEK293 Cells ; Humans ; Immunosuppression Therapy ; Interleukin-2/metabolism ; Lymphocyte Subsets/immunology ; Phenotype ; Plasmids/metabolism ; T-Lymphocytes, Regulatory/immunology ; Time Factors ; Transcription, Genetic ; Transgenes
Chemical Substances	FOXP3 protein, human ; Forkhead Transcription Factors ; Interleukin-2 ; Green Fluorescent Proteins (147336-22-9)
Language	English
Publishing date	2021-08-04
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2649101-1
ISSN	2211-1247 ; 2211-1247
ISSN (online)	2211-1247
ISSN	2211-1247
DOI	10.1016/j.celrep.2021.109494
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Article ; Online: Epigenetic age is associated with baseline and 3-year change in frailty in the Canadian Longitudinal Study on Aging.

Verschoor, Chris P / Lin, David T S / Kobor, Michael S / Mian, Oxana / Ma, Jinhui / Pare, Guillaume / Ybazeta, Gustavo

Clinical epigenetics

2021 Volume 13, Issue 1, Page(s) 163

Abstract: Background: The trajectory of frailty in older adults is important to public health; therefore, markers that may help predict this and other important outcomes could be beneficial. Epigenetic clocks have been developed and are associated with various ... ...

Abstract	Background: The trajectory of frailty in older adults is important to public health; therefore, markers that may help predict this and other important outcomes could be beneficial. Epigenetic clocks have been developed and are associated with various health-related outcomes and sociodemographic factors, but associations with frailty are poorly described. Further, it is uncertain whether newer generations of epigenetic clocks, trained on variables other than chronological age, would be more strongly associated with frailty than earlier developed clocks. Using data from the Canadian Longitudinal Study on Aging (CLSA), we tested the hypothesis that clocks trained on phenotypic markers of health or mortality (i.e., Dunedin PoAm, GrimAge, PhenoAge and Zhang in Nat Commun 8:14617, 2017) would best predict changes in a 76-item frailty index (FI) over a 3-year interval, as compared to clocks trained on chronological age (i.e., Hannum in Mol Cell 49:359-367, 2013, Horvath in Genome Biol 14:R115, 2013, Lin in Aging 8:394-401, 2016, and Yang Genome Biol 17:205, 2016). Results: We show that in 1446 participants, phenotype/mortality-trained clocks outperformed age-trained clocks with regard to the association with baseline frailty (mean = 0.141, SD = 0.075), the greatest of which is GrimAge, where a 1-SD increase in ΔGrimAge (i.e., the difference from chronological age) was associated with a 0.020 increase in frailty (95% CI 0.016, 0.024), or ~ 27% relative to the SD in frailty. Only GrimAge and Hannum (Mol Cell 49:359-367, 2013) were significantly associated with change in frailty over time, where a 1-SD increase in ΔGrimAge and ΔHannum 2013 was associated with a 0.0030 (95% CI 0.0007, 0.0050) and 0.0028 (95% CI 0.0007, 0.0050) increase over 3 years, respectively, or ~ 7% relative to the SD in frailty change. Conclusion: Both prevalence and change in frailty are associated with increased epigenetic age. However, not all clocks are equally sensitive to these outcomes and depend on their underlying relationship with chronological age, healthspan and lifespan. Certain clocks were significantly associated with relatively short-term changes in frailty, thereby supporting their utility in initiatives and interventions to promote healthy aging.
MeSH term(s)	Age Factors ; Aged ; Aged, 80 and over ; Aging/genetics ; Canada ; Cause of Death ; DNA Methylation/genetics ; Epigenesis, Genetic ; Female ; Frailty/genetics ; Frailty/mortality ; Genetic Variation ; Humans ; Longitudinal Studies ; Male ; Middle Aged ; Sociodemographic Factors ; Time Factors
Language	English
Publishing date	2021-08-23
Publishing country	Germany
Document type	Comparative Study ; Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2553921-8
ISSN	1868-7083 ; 1868-7075
ISSN (online)	1868-7083
ISSN	1868-7075
DOI	10.1186/s13148-021-01150-1
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Article ; Online: Tonic-signaling chimeric antigen receptors drive human regulatory T cell exhaustion.

Lamarche, Caroline / Ward-Hartstonge, Kirsten / Mi, Tian / Lin, David T S / Huang, Qing / Brown, Andrew / Edwards, Karlie / Novakovsky, Gherman E / Qi, Christopher N / Kobor, Michael S / Zebley, Caitlin C / Weber, Evan W / Mackall, Crystal L / Levings, Megan K

Proceedings of the National Academy of Sciences of the United States of America

2023 Volume 120, Issue 14, Page(s) e2219086120

Abstract: Regulatory T cell (Treg) therapy is a promising approach to improve outcomes in transplantation and autoimmunity. In conventional T cell therapy, chronic stimulation can result in poor in vivo function, a phenomenon termed exhaustion. Whether or not ... ...

Abstract	Regulatory T cell (Treg) therapy is a promising approach to improve outcomes in transplantation and autoimmunity. In conventional T cell therapy, chronic stimulation can result in poor in vivo function, a phenomenon termed exhaustion. Whether or not Tregs are also susceptible to exhaustion, and if so, if this would limit their therapeutic effect, was unknown. To "benchmark" exhaustion in human Tregs, we used a method known to induce exhaustion in conventional T cells: expression of a tonic-signaling chimeric antigen receptor (TS-CAR). We found that TS-CAR-expressing Tregs rapidly acquired a phenotype that resembled exhaustion and had major changes in their transcriptome, metabolism, and epigenome. Similar to conventional T cells, TS-CAR Tregs upregulated expression of inhibitory receptors and transcription factors such as PD-1, TIM3, TOX and BLIMP1, and displayed a global increase in chromatin accessibility-enriched AP-1 family transcription factor binding sites. However, they also displayed Treg-specific changes such as high expression of 4-1BB, LAP, and GARP. DNA methylation analysis and comparison to a CD8
MeSH term(s)	Humans ; Receptors, Chimeric Antigen ; T-Lymphocytes, Regulatory ; T-Cell Exhaustion ; Immunotherapy, Adoptive/methods ; Graft vs Host Disease ; Receptors, Antigen, T-Cell/genetics ; Receptors, Antigen, T-Cell/metabolism
Chemical Substances	Receptors, Chimeric Antigen ; Receptors, Antigen, T-Cell
Language	English
Publishing date	2023-03-27
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
DOI	10.1073/pnas.2219086120
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Article ; Online: An in vitro chronic damage model impairs inflammatory and regenerative responses in human colonoid monolayers.

Rees, William D / Telkar, Nikita / Lin, David T S / Wong, May Q / Poloni, Chad / Fathi, Ayda / Kobor, Michael / Zachos, Nicholas C / Steiner, Theodore S

Cell reports

2022 Volume 38, Issue 3, Page(s) 110283

Abstract: Acute damage to the intestinal epithelium can be repaired via de-differentiation of mature intestinal epithelial cells (IECs) to a stem-like state, but there is a lack of knowledge on how intestinal stem cells function after chronic injury, such as in ... ...

Abstract	Acute damage to the intestinal epithelium can be repaired via de-differentiation of mature intestinal epithelial cells (IECs) to a stem-like state, but there is a lack of knowledge on how intestinal stem cells function after chronic injury, such as in inflammatory bowel disease (IBD). We developed a chronic-injury model in human colonoid monolayers by repeated rounds of air-liquid interface and submerged culture. We use this model to understand how chronic intestinal damage affects the ability of IECs to (1) respond to microbial stimulation, using the Toll-like receptor 5 (TLR5) agonist FliC and (2) regenerate and protect the epithelium from further damage. Repeated rounds of damage impair the ability of IECs to regrow and respond to TLR stimulation. We also identify mRNA expression and DNA methylation changes in genes associated with IBD and colon cancer. This methodology results in a human model of recurrent IEC injury like that which occurs in IBD.
MeSH term(s)	Cell Culture Techniques/methods ; Colonic Neoplasms ; DNA Methylation ; Humans ; Inflammatory Bowel Diseases ; Intestinal Mucosa/physiology ; Organoids/physiology ; Regeneration/physiology ; Stem Cells/physiology
Language	English
Publishing date	2022-01-19
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2649101-1
ISSN	2211-1247 ; 2211-1247
ISSN (online)	2211-1247
ISSN	2211-1247
DOI	10.1016/j.celrep.2021.110283
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Article: The Blood DNA Methylation Clock GrimAge Is a Robust Surrogate for Airway Epithelia Aging.

Hernandez Cordero, Ana I / Yang, Chen Xi / Li, Xuan / Yang, Julia / Shaipanich, Tawimas / MacIsaac, Julie L / Lin, David T S / Kobor, Michael S / Horvath, Steve / Man, Shu Fan Paul / Sin, Don D / Leung, Janice M

Biomedicines

2022 Volume 10, Issue 12

Abstract: One key feature of Chronic Obstructive Pulmonary Disease (COPD) is that its prevalence increases exponentially with age. DNA methylation clocks have become powerful biomarkers to detect accelerated aging in a variety of diseases and can help prognose ... ...

Abstract	One key feature of Chronic Obstructive Pulmonary Disease (COPD) is that its prevalence increases exponentially with age. DNA methylation clocks have become powerful biomarkers to detect accelerated aging in a variety of diseases and can help prognose outcomes in severe COPD. This study investigated which DNA methylation clock could best reflect airway epigenetic age when used in more accessible blood samples. Our analyses showed that out of six DNA methylation clocks investigated, DNAmGrimAge demonstrated the strongest correlation and the smallest difference between the airway epithelium and blood. Our findings suggests that blood DNAmGrimAge accurately reflects airway epigenetic age of individuals and that its elevation is highly associated with COPD.
Language	English
Publishing date	2022-12-01
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2720867-9
ISSN	2227-9059
ISSN	2227-9059
DOI	10.3390/biomedicines10123094
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Article ; Online: Sex differences in epigenetic age in Mediterranean high longevity regions.

Engelbrecht, Hannah-Ruth / Merrill, Sarah M / Gladish, Nicole / MacIsaac, Julie L / Lin, David T S / Ecker, Simone / Chrysohoou, Christina A / Pes, Giovanni M / Kobor, Michael S / Rehkopf, David H

Frontiers in aging

2022 Volume 3, Page(s) 1007098

Abstract: Sex differences in aging manifest in disparities in disease prevalence, physical health, and lifespan, where women tend to have greater longevity relative to men. However, in the Mediterranean Blue Zones of Sardinia (Italy) and Ikaria (Greece) are ... ...

Abstract	Sex differences in aging manifest in disparities in disease prevalence, physical health, and lifespan, where women tend to have greater longevity relative to men. However, in the Mediterranean Blue Zones of Sardinia (Italy) and Ikaria (Greece) are regions of centenarian abundance, male-female centenarian ratios are approximately one, diverging from the typical trend and making these useful regions in which to study sex differences of the oldest old. Additionally, these regions can be investigated as examples of healthy aging relative to other populations. DNA methylation (DNAm)-based predictors have been developed to assess various health biomarkers, including biological age, Pace of Aging, serum interleukin-6 (IL-6), and telomere length. Epigenetic clocks are biological age predictors whose deviation from chronological age has been indicative of relative health differences between individuals, making these useful tools for interrogating these differences in aging. We assessed sex differences between the Horvath, Hannum, GrimAge, PhenoAge, Skin and Blood, and Pace of Aging predictors from individuals in two Mediterranean Blue Zones and found that men displayed positive epigenetic age acceleration (EAA) compared to women according to all clocks, with significantly greater rates according to GrimAge (β = 3.55;
Language	English
Publishing date	2022-11-23
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	3076785-4
ISSN	2673-6217 ; 2673-6217
ISSN (online)	2673-6217
ISSN	2673-6217
DOI	10.3389/fragi.2022.1007098
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Article ; Online: The immune factors driving DNA methylation variation in human blood.

Bergstedt, Jacob / Azzou, Sadoune Ait Kaci / Tsuo, Kristin / Jaquaniello, Anthony / Urrutia, Alejandra / Rotival, Maxime / Lin, David T S / MacIsaac, Julia L / Kobor, Michael S / Albert, Matthew L / Duffy, Darragh / Patin, Etienne / Quintana-Murci, Lluís

Nature communications

2022 Volume 13, Issue 1, Page(s) 5895

Abstract: Epigenetic changes are required for normal development, yet the nature and respective contribution of factors that drive epigenetic variation in humans remain to be fully characterized. Here, we assessed how the blood DNA methylome of 884 adults is ... ...

Abstract	Epigenetic changes are required for normal development, yet the nature and respective contribution of factors that drive epigenetic variation in humans remain to be fully characterized. Here, we assessed how the blood DNA methylome of 884 adults is affected by DNA sequence variation, age, sex and 139 factors relating to life habits and immunity. Furthermore, we investigated whether these effects are mediated or not by changes in cellular composition, measured by deep immunophenotyping. We show that DNA methylation differs substantially between naïve and memory T cells, supporting the need for adjustment on these cell-types. By doing so, we find that latent cytomegalovirus infection drives DNA methylation variation and provide further support that the increased dispersion of DNA methylation with aging is due to epigenetic drift. Finally, our results indicate that cellular composition and DNA sequence variation are the strongest predictors of DNA methylation, highlighting critical factors for medical epigenomics studies.
MeSH term(s)	Adult ; Aging/genetics ; DNA Methylation ; Epigenesis, Genetic ; Epigenomics/methods ; Humans ; Immunologic Factors
Chemical Substances	Immunologic Factors
Language	English
Publishing date	2022-10-06
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-022-33511-6
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