Examining the immunoepigenetic-gut microbiome axis in the context of self-esteem among Native Hawaiians and other Pacific Islanders

Becerra, Celyna Y.; Wells, Riley; Kunihiro, Braden; Lee, Rosa H.; Umeda, Lesley; Allan, Nina; Rubas, Noelle; McCracken, Trevor A.; Nunokawa, Chandler K. L.; Lee, Ming-Hao; Pidlaoan, Felix Gerard S.; Phankitnirondorn, Krit; Dye, Christian K.; Yamamoto, Brennan Y; Peres, Rafael; Juárez, Rubén; Maunakea, Alika K.

doi:10.3389/fgene.2023.1125217

Cited by 7 publications

(8 citation statements)

References 68 publications

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“…HMGB-1 levels may be influenced by the gut microbiome, which is known to regulation inflammation and immune response to viral infections. In addition, microbial metabolites like SCFAs impact health generally, with implications to vaccine effectiveness [ 5 , 6 ]. SCFAs produced by the gut microbiome include butyrate, acetate, and propionate which support the energy needs in maintaining B-cells through increasing glycolysis, fatty acid synthesis, and oxidation [ 26 ].…”

Section: Discussionmentioning

confidence: 99%

“…As an important modulator of the immune system, the gut microbiome may play a significant role in influencing vaccine effectiveness [ 4 , 5 , 6 ]. An imbalance in the gut microbiome resulting in increased inflammation may contribute to a decrease in the effectiveness of a vaccine through damage to the mucosal layer or general cellular damage [ 4 ].…”

Section: Introductionmentioning

confidence: 99%

“…Butyrate is a prominent SCFA that increases mucosal immunity, improves intestinal barrier integrity, and has been observed to have anti-inflammatory properties. Butyrate production is also associated with health outcomes such as reduced obesity and improved brain function [ 5 , 6 , 8 ].…”

Section: Introductionmentioning

confidence: 99%

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Immuno-Microbial Signature of Vaccine-Induced Immunity against SARS-CoV-2

Umeda,

Torres,

Kunihiro

et al. 2024

Vaccines

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Although vaccines address critical public health needs, inter-individual differences in responses are not always considered in their development. Understanding the underlying basis for these differences is needed to optimize vaccine effectiveness and ultimately improve disease control. In this pilot study, pre- and post-antiviral immunological and gut microbiota features were characterized to examine inter-individual differences in SARS-CoV-2 mRNA vaccine response. Blood and stool samples were collected before administration of the vaccine and at 2-to-4-week intervals after the first dose. A cohort of 14 adults was separated post hoc into two groups based on neutralizing antibody levels (high [HN] or low [LN]) at 10 weeks following vaccination. Bivariate correlation analysis was performed to examine associations between gut microbiota, inflammation, and neutralization capacity at that timepoint. These analyses revealed significant differences in gut microbiome composition and inflammation states pre-vaccination, which predicted later viral neutralization capacity, with certain bacterial taxa, such as those in the genus Prevotella, found at higher abundance in the LN vs HN group that were also negatively correlated with a panel of inflammatory factors such as IL-17, yet positively correlated with plasma levels of the high mobility group box 1 (HMGB-1) protein at pre-vaccination. In particular, we observed a significant inverse relationship (Pearson = −0.54, p = 0.03) between HMGB-1 pre-vaccination and neutralization capacity at 10 weeks post-vaccination. Consistent with known roles as mediators of inflammation, our results altogether implicate HMGB-1 and related gut microbial signatures as potential biomarkers in predicting SARS-CoV-2 mRNA vaccine effectiveness measured by the production of viral neutralization antibodies.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Immuno-Microbial Signature of Vaccine-Induced Immunity against SARS-CoV-2

Umeda,

Torres,

Kunihiro

et al. 2024

Vaccines

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“…Bacterial populations in a host can affect epigenetic regulation and correlate with clinical outcomes: gut microbial dysbiosis leads to inflammation, decrease in SCFA, and increased risk of inflammatory bowel disease IBD) [ 63 ]. A study evaluating self-esteem in patients with type 2 diabetes noted similar gut microbiome profiles, inflammatory profiles, and regions of differential methylation in participants with low self-esteem [ 64 ]. When we looked at associations with the level of Bacteroidaceae abundance and epigenetic changes, we found one particular DMR that varied between high vs. low abundance.…”

Section: Discussionmentioning

confidence: 99%

Impact of Maternal Mediterranean-Type Diet Adherence on Microbiota Composition and Epigenetic Programming of Offspring

Sasaki,

Kawamura,

Okuno

et al. 2023

Nutrients

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Understanding how maternal diet affects in utero neonatal gut microbiota and epigenetic regulation may provide insight into disease origins and long-term health. The impact of Mediterranean diet pattern adherence (MDA) on fetal gut microbiome and epigenetic regulation was assessed in 33 pregnant women. Participants completed a validated food frequency questionnaire in each trimester of pregnancy; the alternate Mediterranean diet (aMED) score was applied. Umbilical cord blood, placental tissue, and neonatal meconium were collected from offspring. DNA methylation patterns were probed using the Illumnia EPICarray Methylation Chip in parturients with high versus low MDA. Meconium microbial abundance in the first 24 h after birth was identified using 16s rRNA sequencing and compared among neonates born to mothers with high and low aMED scores. Twenty-one mothers were classified as low MDA and 12 as high MDA. Pasteurellaceae and Bacteroidaceae trended towards greater abundance in the high-MDA group, as well as other short-chain fatty acid-producing species. Several differentially methylated regions varied between groups and overlapped gene regions including NCK2, SNED1, MTERF4, TNXB, HLA-DPB, BAG6, and LMO3. We identified a beneficial effect of adherence to a Mediterranean diet on fetal in utero development. This highlights the importance of dietary counseling for mothers and can be used as a guide for future studies of meconium and immuno-epigenetic modulation.

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“… 41 Monocyte purity was verified from 50 000 cell aliquots per sample using flow cytometry as described previously. 42 , 43 An enrichment success threshold was set at more than 65% monocytes to limit DNA methylation variability caused by cell-type heterogeneity. 43 …”

Section: Methodsmentioning

confidence: 99%

Socioeconomic Status, Lifestyle, and DNA Methylation Age Among Racially and Ethnically Diverse Adults

Maunakea,

Phankitnirundorn,

Peres

et al. 2024

JAMA Netw Open

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ImportanceVariation in DNA methylation at specific loci estimates biological age, which is associated with morbidity, mortality, and social experiences. Aging estimates known as epigenetic clocks, including the Dunedin Pace of Aging Calculated From the Epigenome (DunedinPACE), were trained on data predominately from individuals of European ancestry; however, limited research has explored DunedinPACE in underrepresented populations experiencing health disparities.ObjectiveTo investigate associations of neighborhood and individual sociobehavioral factors with biological aging in a racially and ethnically diverse population.Design, Setting, and ParticipantsThis cohort study, part of the Multiethnic Cohort study conducted from May 1993 to September 1996 to examine racial and ethnic disparities in chronic diseases, integrated biospecimen and self-reported data collected between April 2004 and November 2005 from healthy Hawaii residents aged 45 to 76 years. These participants self-identified as of Japanese American, Native Hawaiian, or White racial and ethnic background. Data were analyzed from January 2022 to May 2024.Main Outcomes and MeasuresDNA methylation data were generated from monocytes enriched from cryopreserved lymphocytes and used to derive DunedinPACE scores from November 2017 to June 2021. Neighborhood social economic status (NSES) was estimated from 1990 US Census Bureau data to include factors such as educational level, occupation, and income. Individual-level factors analyzed included educational level, body mass index (BMI), physical activity (PA), and diet quality measured by the Healthy Eating Index (HEI). Linear regression analysis of DunedinPACE scores was used to examine their associations with NSES and sociobehavioral variables.ResultsA total of 376 participants were included (113 [30.1%] Japanese American, 144 [38.3%] Native Hawaiian, and 119 [31.6%] White; 189 [50.3%] were female). Mean (SE) age was 57.81 (0.38) years. Overall, mean (SE) DunedinPACE scores were significantly higher among females than among males (1.28 [0.01] vs 1.25 [0.01]; P = .005); correlated negatively with NSES (R = −0.09; P = .08), HEI (R = −0.11; P = .03), and educational attainment (R = −0.15; P = .003) and positively with BMI (R = 0.31; P &lt; .001); and varied by race and ethnicity. Native Hawaiian participants exhibited a higher mean (SE) DunedinPACE score (1.31 [0.01]) compared with Japanese American (1.25 [0.01]; P &lt; .001) or White (1.22 [0.01]; P &lt; .001) participants. Controlling for age, sex, HEI, BMI, and NSES, linear regression analyses revealed a negative association between educational level and DunedinPACE score among Japanese American (β, −0.005 [95% CI, −0.013 to 0.002]; P = .03) and Native Hawaiian (β, −0.003 [95% CI, −0.011 to 0.005]; P = .08) participants, yet this association was positive among White participants (β, 0.007; 95% CI, −0.001 to 0.015; P = .09). Moderate to vigorous PA was associated with lower DunedinPACE scores only among Native Hawaiian participants (β, −0.006; 95% CI, −0.011 to −0.001; P = .005), independent of NSES.Conclusions and RelevanceIn this study of a racially and ethnically diverse sample of 376 adults, low NSES was associated with a higher rate of biological aging measured by DunedinPACE score, yet individual-level factors such as educational level and physical activity affected this association, which varied by race and ethnicity. These findings support sociobehavioral interventions in addressing health inequities.

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Examining the immunoepigenetic-gut microbiome axis in the context of self-esteem among Native Hawaiians and other Pacific Islanders

Cited by 7 publications

References 68 publications

Immuno-Microbial Signature of Vaccine-Induced Immunity against SARS-CoV-2

Immuno-Microbial Signature of Vaccine-Induced Immunity against SARS-CoV-2

Impact of Maternal Mediterranean-Type Diet Adherence on Microbiota Composition and Epigenetic Programming of Offspring

Socioeconomic Status, Lifestyle, and DNA Methylation Age Among Racially and Ethnically Diverse Adults

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