Epigenetic Research in Neuropsychiatric Disorders: the “Tissue Issue”

Bakulski, Kelly M.; Halladay, Alycia; Hu, Valerie W.; Mill, Jonathan; Fallin, M. Daniele

doi:10.1007/s40473-016-0083-4

Cited by 127Epigenetics and DNA MethylationGenetic Associations and EpidemiologyHealth, Environment, Cognitive Aging

Epigenetic Research in Neuropsychiatric Disorders: the “Tissue Issue”

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Bakulski, Kelly M., Halladay, Alycia, Hu, Valerie W., Mill, Jonathan, Fallin, M. Daniele·2016·Current Behavioral Neuroscience Reports

DOI 10.1007/s40473-016-0083-4PMC PMC5235359

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Abstract

Purpose of review Evidence has linked neuropsychiatric disorders with epigenetic marks as either a biomarker of disease, biomarker of exposure, or mechanism of disease processes. Neuropsychiatric epidemiologic studies using either target brain tissue or surrogate blood tissue each have methodological challenges and distinct advantages.Recent findings Brain tissue studies are challenged by small sample sizes of cases and controls, incomplete phenotyping, post-mortem timing, and cellular heterogeneity, but the use of a primary disease relevant tissue is critical. Blood-based studies have access to much larger sample sizes and more replication opportunities, as well as the potential for longitudinal measurements, both prior to onset and during the course of treatments. Yet, blood studies also are challenged by cell-type heterogeneity, and many question the validity of using peripheral tissues as a brain biomarker. Emerging evidence suggests that these limitations to blood-based epigenetic studies are surmountable, but confirmation in target tissue remains important.Summary Epigenetic mechanisms have the potential to help elucidate biology connecting experiential risk factors with neuropsychiatric disease manifestation. Cross-tissue studies as well as advanced epidemiologic methods should be employed to more effectively conduct neuropsychiatric epigenetic research.

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Human studies to assess epigenetic modifications have been limited to measures made in blood cells or in post-mortem brain.
“Human studies to assess epigenetic modifications have been lim ited to measures made in blood cells or in post- mortem brain 115,116 .”
From Substance use disorders: a comprehensive update of classification, epidemiology, neurobiology, clinical aspects, treatment and prevention (2023) · cites this paper as [116]
The Introduction’s ‘Challenges of Brain-Based Research’ section discusses blood and post-mortem brain studies, but also identifies buccal and saliva samples as sources for epigenetic discovery in neuropsychiatric research. The claim that human measurements have been limited to blood cells or post-mortem brain therefore excludes sample types the paper explicitly discusses. (LLM, conf=0.89)
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Elucidating molecular changes in the human brain is made difficult by the timing of sample acquisition, cell type distribution between samples, cause of death, brain agonal state, sample handling, storage temperatures, and sample size.
“Elucidating molecular changes in the human brain is made difficult by the timing of sample acquisition, cell type distribution between samples, cause of death, and brain agonal state, as well as sample handling, storage temperatures, and sample size (Bakulski et al., 2016).”
From The Epigenetics of Anxiety Pathophysiology: A DNA Methylation and Histone Modification Focused Review (2023) · cites this paper as Bakulski et al., 2016
The Introduction’s “Challenges of Brain-Based Research” section identifies timing of acquisition, cell-type variation, small sample sizes, cause of death, and pre-mortem agonal state as limitations. It also calls for careful sampling and storage, but does not specifically identify storage temperatures as a difficulty. Page numbers were not available in our copy. (LLM, conf=0.87)
Experimental — accuracy not yet measured
Epigenetic studies so far have mostly relied on peripheral tissues, which precludes definite conclusions from being drawn regarding CNS processes.
“epigenetic studies so far have mostly (with the exception of investigations in post-mortem samples) relied on peripheral tissues, which precludes definite conclusions from being drawn regarding CNS processes.”
From The applied implications of epigenetics in anxiety, affective and stress-related disorders - A review and synthesis on psychosocial stress, psychotherapy and prevention (2020) · cites this paper as Bakulski, Halladay, Hu, Mill, & Fallin, 2016
The Introduction’s ‘Challenges of Blood-Based Neuropsychiatric Epigenetic Research’ section says blood findings require caution when inferring brain mechanisms, and the Abstract’s ‘Recent findings’ section says confirmation in brain tissue remains important. The paper does not establish that most studies relied on peripheral tissues; its ‘Utility of Brain Tissue’ section also says many studies used brain material. It treats peripheral-to-brain inference as limited, not categorically impossible. (LLM, conf=0.84)
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Enrichment of cis-regulatory gene expression SNPs and methylation quantitative trait loci among bipolar disorder susceptibility variants
Gamazon, E. R., Badner, J. A., Cheng, L., Zhang, C., Zhang, D., Cox, N. J., Gershon, E. S., Kelsoe, J. R., Greenwood, T. A., Nievergelt, C. M., et al. (2012) · Molecular Psychiatry · doi:10.1038/mp.2011.174 · Cited by 157 · see citing works
Brain connectivity in autism spectrum disorder
Mohammad-Rezazadeh, I., Frohlich, J., Loo, S. K., & Jeste, S. (2016) · Current Opinion in Neurology · doi:10.1097/wco.0000000000000301 · Cited by 153 · see citing works
DNA Methylation in Whole Blood: Uses and Challenges
Houseman, E. A., Kim, S., Kelsey, K. T., & Wiencke, J. K. (2015) · Current Environmental Health Reports · doi:10.1007/s40572-015-0050-3 · Cited by 147 · see citing works
Epigenetic dysregulation of SHANK3 in brain tissues from individuals with autism spectrum disorders
Zhu, L., Wang, X., Li, X.-L., Towers, A., Cao, X., Wang, P., Bowman, R., Yang, H., Goldstein, J., Li, Y.-J., et al. (2014) · Human Molecular Genetics · doi:10.1093/hmg/ddt547 · Cited by 147 · see citing works
Concordant and discordant DNA methylation signatures of aging in human blood and brain
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Epigenetics, hippocampal neurogenesis, and neuropsychiatric disorders: Unraveling the genome to understand the mind
Hsieh, J., & Eisch, A. J. (2010) · Neurobiology of Disease · doi:10.1016/j.nbd.2010.01.008 · Cited by 144 · see citing works
Increased DNA methylation status of the serotonin receptor 5HTR1A gene promoter in schizophrenia and bipolar disorder
Carrard, A., Salzmann, A., Malafosse, A., & Karege, F. (2011) · Journal of Affective Disorders · doi:10.1016/j.jad.2011.03.018 · Cited by 138 · see citing works
The Role of Epigenetics in Genetic and Environmental Epidemiology
Ladd‐Acosta, C., & Fallin, M. D. (2015) · Epigenomics · doi:10.2217/epi.15.102 · Cited by 137 · see citing works
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Infant siblings and the investigation of autism risk factors
Newschaffer, C. J., Croen, L., Fallin, M. D., Hertz‐Picciotto, I., Nguyen, D. V., Lee, N. L., Berry, C. A., Farzadegan, H., Hess, H. N., Landa, R. J., et al. (2012) · Journal of Neurodevelopmental Disorders · doi:10.1186/1866-1955-4-7 · Cited by 136 · see citing works
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Genome-Wide DNA Methylation Scan in Major Depressive Disorder
Sabunciyan, S., Aryee, M. J., Irizarry, R. A., Rongione, M. A., Webster, M. J., Kaufmann, W. E., Murakami, P. N., Lessard, A., Yolken, R. H., Feinberg, A. P., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0034451 · Cited by 132 · see citing works
Genome-wide Methylomic Analysis of Monozygotic Twins Discordant for Adolescent Depression
Dempster, E. L., Wong, C. C. Y., Lester, K. J., Burrage, J., Gregory, A. M., Mill, J. S., & Eley, T. C. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.04.013 · Cited by 132 · see citing works
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Large-scale hypomethylated blocks associated with Epstein-Barr virus–induced B-cell immortalizationPreprint
Hansen, K. D., Sabunciyan, S., Langmead, B., Nagy, N., Curley, R., Klein, G., Klein, E., Salamon, D., & Feinberg, A. P. (2013) · Genome Research · doi:10.1101/gr.157743.113 · Cited by 127 · see citing works
Predicting DNA methylation level across human tissues
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Epigenetic Studies of Psychosis: Current Findings, Methodological Approaches, and Implications for Postmortem Research
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Epigenetic epidemiology: Promises for public health research
Bakulski, K. M., & Fallin, M. D. (2014) · Environmental and Molecular Mutagenesis · doi:10.1002/em.21850 · Cited by 112 · see citing works
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Traumatic stress and human DNA methylation: A critical review
Vinkers, C. H., Kalafateli, A. L., Rutten, B. P., Kas, M. J., Kaminsky, Z., Turner, J. D., & Boks, M. P. (2015) · Epigenomics · doi:10.2217/epi.15.11 · Cited by 112 · see citing works
Measuring cell-type specific differential methylation in human brain tissue
Montaño, C., Irizarry, R. A., Kaufmann, W. E., Talbot, K., Gur, R. E., Feinberg, A. P., & Taub, M. A. (2013) · Genome biology · doi:10.1186/gb-2013-14-8-r94 · Cited by 110 · see citing works
Alterations in DNA methylation of Fkbp5 as a determinant of blood–brain correlation of glucocorticoid exposure
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Epigenetic mechanisms in schizophrenia
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Comprehensive DNA methylation analysis of peripheral blood cells derived from patients with first-episode schizophrenia
Nishioka, M., Bundo, M., Koike, S., Takizawa, R., Kakiuchi, C., Araki, T., Kasai, K., & Iwamoto, K. (2013) · Journal of Human Genetics · doi:10.1038/jhg.2012.140 · Cited by 101 · see citing works
Complex epigenetic regulation of Engrailed-2 (EN-2) homeobox gene in the autism cerebellum
James, S. J., Shpyleva, S., Melnyk, S., Pavliv, O., & Pogribny, I. P. (2013) · Translational Psychiatry · doi:10.1038/tp.2013.8 · Cited by 100 · see citing works
PTSD and DNA Methylation in Select Immune Function Gene Promoter Regions: A Repeated Measures Case-Control Study of U.S. Military Service Members
Rusiecki, J. A., Byrne, C., Galdzicki, Z., Srikantan, V., Chen, L., Poulin, M., Yan, L., & Baccarelli, A. (2013) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2013.00056 · Cited by 99 · see citing works
Epigenetic Signatures as Biomarkers of Exposure
Ladd‐Acosta, C. (2015) · Current Environmental Health Reports · doi:10.1007/s40572-015-0051-2 · Cited by 98 · see citing works
Obesity Weighs down Memory through a Mechanism Involving the Neuroepigenetic Dysregulation of Sirt1
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An Update on the Epigenetics of Psychotic Diseases and Autism
Abdolmaleky, H. M., Zhou, J., & Thiagalingam, S. (2015) · Epigenomics · doi:10.2217/epi.14.85 · Cited by 75 · see citing works
The effects of pH on DNA methylation state: In vitro and post-mortem brain studies
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Prenatal mercury concentration is associated with changes in DNA methylation at TCEANC2 in newborns
Bakulski, K. M., Lee, H., Feinberg, J. I., Wells, E. M., Brown, S. C., Herbstman, J. B., Witter, F. R., Halden, R. U., Caldwell, K. L., Mortensen, M. E., et al. (2015) · International Journal of Epidemiology · doi:10.1093/ije/dyv032 · Cited by 65 · see citing works
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Epigenetic signaling in schizophrenia
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Psychological factors and DNA methylation of genes related to immune/inflammatory system markers: the VA Normative Aging Study
Kim, D. J., Kubzansky, L. D., Baccarelli, A., Sparrow, D., Spiro, A., Tarantini, L., Cantone, L., Vokonas, P., & Schwartz, J. D. (2016) · BMJ Open · doi:10.1136/bmjopen-2015-009790 · Cited by 58 · see citing works
The Expression of the Suicide-Associated Gene SKA2 Is Decreased in the Prefrontal Cortex of Suicide Victims but Not of Nonsuicidal Patients
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iPSC-derived neurons as a higher-throughput readout for autism: promises and pitfalls
Prilutsky, D., Palmer, N., Smedemark-Margulies, N., Schlaeger, T. M., Margulies, D. M., & Kohane, I. S. (2013) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2013.11.004 · Cited by 48 · see citing works
Profiling of Childhood Adversity-Associated DNA Methylation Changes in Alcoholic Patients and Healthy Controls
Zhang, H., Wang, F., Kranzler, H. R., Zhao, H., & Gelernter, J. E. (2013) · PLoS ONE · doi:10.1371/journal.pone.0065648 · Cited by 48 · see citing works
Methylomic analysis of monozygotic twins discordant for childhood psychotic symptoms
Fisher, H. L., Murphy, T. M., Arseneault, L., Caspi, A., Moffitt, T. E., Viana, J. F., Hannon, E. J., Pidsley, R., Burrage, J., Dempster, E. L., et al. (2015) · Epigenetics · doi:10.1080/15592294.2015.1099797 · Cited by 46 · see citing works
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Altered DNA methylation of glucose transporter 1 and glucose transporter 4 in patients with major depressive disorder
Kahl, K. G., Georgi, K., Bleich, S., Muschler, M., Hillemacher, T., Hilfiker-Kleinert, D., Schweiger, U., Ding, X., Kotsiari, A., & Frieling, H. (2016) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2016.02.002 · Cited by 44 · see citing works
A Longitudinal Study ofBDNFPromoter Methylation and Depression in Breast Cancer
Kang, H., Kim, J., Kim, S.-Y., Kim, S., Shin, I., Kim, H. R., Park, M. H., Shin, M., Yoon, J.-H., & Yoon, J. (2015) · Psychiatry Investigation · doi:10.4306/pi.2015.12.4.523 · Cited by 39 · see citing works
Epigenetics and addiction
Cadet, J., McCoy, M., & Jayanthi, S. (2016) · Clinical Pharmacology & Therapeutics · doi:10.1002/cpt.345 · Cited by 31 · see citing works
Tissue-specific patterns of allelically-skewed DNA methylation
Marzi, S. J., Meaburn, E. L., Dempster, E. L., Lunnon, K., Paya-Cano, J. L., Smith, R. G., Volta, M., Troakes, C., Schalkwyk, L. C., & Mill, J. S. (2016) · Epigenetics · doi:10.1080/15592294.2015.1127479 · Cited by 27 · see citing works
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Leukocyte DNA as Surrogate for the Evaluation of Imprinted Loci Methylation in Mammary Tissue DNA
Barault, L., Ellsworth, R. E., Harris, H. R., Valente, A. L., Shriver, C. D., & Michels, K. B. (2013) · PLoS ONE · doi:10.1371/journal.pone.0055896 · Cited by 19 · see citing works
Comparative DNA methylation among females with neurodevelopmental disorders and seizures identifies TAC1 as a MeCP2 target gene
Aldinger, K. A., Plummer, J., & Levitt, P. R. (2013) · Journal of Neurodevelopmental Disorders · doi:10.1186/1866-1955-5-15 · Cited by 13 · see citing works

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Substance use disorders: a comprehensive update of classification, epidemiology, neurobiology, clinical aspects, treatment and prevention
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Candidate biomarkers in psychiatric disorders: state of the field
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Epigenetics at the crossroads between genes, environment and resilience in anxiety disorders
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Systematic evaluation and validation of reference and library selection methods for deconvolution of cord blood DNA methylation data
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Epigenetic biomarkers: Current strategies and future challenges for their use in the clinical laboratory
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Childhood maltreatment and DNA methylation: A systematic review
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Annual Research Review: Perspectives on progress in <scp>ADHD</scp> science – from characterization to cause
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Genetics and epigenetics of autism: A Review
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Prenatal epigenetics diets play protective roles against environmental pollution
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Case-control meta-analysis of blood DNA methylation and autism spectrum disorder
Andrews, S. V., Sheppard, B. K., Windham, G. C., Schieve, L. A., Schendel, D., Croen, L., Chopra, P., Alisch, R. S., Newschaffer, C. J., Warren, S. T., et al. (2018) · Molecular Autism · doi:10.1186/s13229-018-0224-6 · Cited by 104 · see citing works
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Integrating DNA Methylation Measures of Biological Aging into Social Determinants of Health Research
Raffington, L., & Belsky, D. W. (2022) · Current Environmental Health Reports · doi:10.1007/s40572-022-00338-8 · Cited by 94 · see citing works
Blood DNA methylation as a potential biomarker of dementia: A systematic review
Fransquet, P. D., Lacaze, P., Saffery, R., McNeil, J., Woods, R., & Ryan, J. (2018) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2017.10.002 · Cited by 96 · see citing works
DNA methylation and antipsychotic treatment mechanisms in schizophrenia: Progress and future directions
Ovenden, E. S., McGregor, N. W., Emsley, R. A., & Warnich, L. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.10.004 · Cited by 85 · see citing works
Present and future challenges for the investigation of transgenerational epigenetic inheritance
Fallet, M., Blanc, M., Criscio, M. D., Antczak, P., Engwall, M., Guerrero‐Bosagna, C., Rüegg, J., & Keiter, S. H. (2023) · Environment International · doi:10.1016/j.envint.2023.107776 · Cited by 83 · see citing works
Cross-tissue integration of genetic and epigenetic data offers insight into autism spectrum disorder
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Epigenetics applied to psychiatry: Clinical opportunities and future challenges
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The role of epigenetic modifications in neurodevelopmental disorders: A systematic review
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Considerations toward an epigenetic and common pathways theory of mental disorder.
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Epigenetics of Schizophrenia
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Epigenomics of Major Depressive Disorders and Schizophrenia: Early Life Decides
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Exploring a causal role of DNA methylation in the relationship between maternal vitamin B12 during pregnancy and child’s IQ at age 8, cognitive performance and educational attainment: a two-step Mendelian randomization study
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Characterization of cross-tissue genetic-epigenetic effects and their patterns in schizophrenia
Lin, D., Chen, J., Perrone‐Bizzozero, N. I., Bustillo, J., Du, Y., Calhoun, V. D., & Liu, J. (2018) · Genome Medicine · doi:10.1186/s13073-018-0519-4 · Cited by 58 · see citing works
Variation in DNA methylation of the oxytocin receptor gene predicts children's resilience to prenatal stress
Milaniak, I., Cecil, C. A. M., Barker, E. D., Relton, C. L., Gaunt, T. R., McArdle, W. L., & Jaffee, S. R. (2017) · Development and Psychopathology · doi:10.1017/s0954579417001316 · Cited by 57 · see citing works
Can epigenetics shine a light on the biological pathways underlying major mental disorders?
Alameda, L., Trotta, G., Quigley, H., Rodriguez, V., Gadelrab, R., Dwir, D., Dempster, E., Wong, C. C. Y., & Forti, M. D. (2022) · Psychological Medicine · doi:10.1017/s0033291721005559 · Cited by 60 · see citing works
Accelerated aging in the brain, epigenetic aging in blood, and polygenic risk for schizophrenia
Teeuw, J., Ori, A. P. S., Brouwer, R. M., de Zwarte, S. M. C., Schnack, H. G., Pol, H. E. H., & Ophoff, R. A. (2021) · Schizophrenia Research · doi:10.1016/j.schres.2021.04.005 · Cited by 52 · see citing works
The role of Toll‐like receptors in neuropsychiatric disorders: Immunopathology, treatment, and management
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Psychotherapy and Genetic Neuroscience: An Emerging Dialog
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Exposure to different early-life stress experiences results in differentially altered DNA methylation in the brain and immune system
Catale, C., Bussone, S., Iacono, L. L., Viscomi, M. T., Palacios, D., Troisi, A., & Carola, V. (2020) · Neurobiology of Stress · doi:10.1016/j.ynstr.2020.100249 · Cited by 54 · see citing works
Cell Types in Environmental Epigenetic Studies: Biological and Epidemiological Frameworks
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Challenges in the analysis of epigenetic biomarkers in clinical samples
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Metals Exposures and DNA Methylation: Current Evidence and Future Directions
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Epigenome-Wide Meta-Analysis of Prenatal Maternal Stressful Life Events and Newborn DNA Methylation
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Monoamine Oxidase A Gene Methylation and Its Role in Posttraumatic Stress Disorder: First Evidence from the South Eastern Europe (SEE)-PTSD Study
Ziegler, C., Wolf, C., Schiele, M. A., Bojić, E. F., Kučukalić, S., Dzananovic, E. S., Uka, A. G., Hoxha, B., Haxhibeqiri, V., Haxhibeqiri, S., et al. (2017) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyx111 · Cited by 43 · see citing works
Integrating -Omics Approaches into Human Population-Based Studies of Prenatal and Early-Life Exposures
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The Epigenetics of Anxiety Pathophysiology: A DNA Methylation and Histone Modification Focused Review
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Socially Stratified Epigenetic Profiles Are Associated With Cognitive Functioning in Children and Adolescents
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Linking Prenatal Environmental Exposures to Lifetime Health with Epigenome-Wide Association Studies: State-of-the-Science Review and Future Recommendations
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Autism-Associated DNA Methylation at Birth From Multiple Tissues Is Enriched for Autism Genes in the Early Autism Risk Longitudinal Investigation
Bakulski, K. M., Dou, J., Feinberg, J. I., Aung, M. T., Ladd‐Acosta, C., Volk, H. E., Newschaffer, C. J., Croen, L., Hertz‐Picciotto, I., Levy, S. E., et al. (2021) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.775390 · Cited by 35 · see citing works
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Social Epigenomics: Are we at an Impasse?
Non, A. L. (2021) · Epigenomics · doi:10.2217/epi-2020-0136 · Cited by 35 · see citing works
Epigenetics applied to child and adolescent mental health: Progress, challenges and opportunities
Cecil, C. A. M., Neumann, A., & Walton, E. (2022) · JCPP Advances · doi:10.1002/jcv2.12133 · Cited by 33 · see citing works
Utility of DNA Methylation as a Biomarker in Aging and Alzheimer’s Disease
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Authors: Bakulski, K. M., Halladay, A., Hu, V. W., Mill, J., & Fallin, M. D.
Affiliations: University of Michigan (US)
Rutgers, The State University of New Jersey (US)
George Washington University (US)
King's College London (GB)
Johns Hopkins University (US)
Corresponding author: Fallin, M. Daniele
ORCID: Bakulski, Kelly M.
Halladay, Alycia
Hu, Valerie W.
Mill, Jonathan
Fallin, M. Daniele
Venue: Current Behavioral Neuroscience Reports
Publisher: Springer Science and Business Media LLC
Published: 2016-08-02
Volume: 3
Issue: 3
Pages: 264-274
ISSN: 2196-2979 (ISSN-L)
DOI: 10.1007/s40473-016-0083-4
PMC: PMC5235359
OpenAlex: W2505166506
Cited by: 127
References: 111
Citations by year: 2026: 5 · 2025: 7 · 2024: 12 · 2023: 13 · 2022: 25 · 2021: 13 · 2020: 15 · 2019: 11 · 2018: 14 · 2017: 12
FWCI: 6.37
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Current Behavioral Neuroscience Reports (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Environmental Health Sciences (ES017646, ES023061)
Medical Research Council (MRC; MR/K013807/1)
National Institutes of Health (AG036039)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Health, Environment, Cognitive Aging
Keywords: epigenetics, neuropsychiatric disorders, blood-based biomarkers, brain tissue, surrogate tissue, cellular heterogeneity, postmortem brain, risk factors

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