Histone acetylome-wide associations in immune cells from individuals with active Mycobacterium tuberculosis infection.

Acetylation Adult Chromatin Cohort Studies Female Genetic Association Studies Granulocytes / immunology Histones / genetics Humans Longitudinal Studies Male Monocytes / immunology Mycobacterium tuberculosis / immunology Proof of Concept Study Quantitative Trait Loci Singapore South Africa THP-1 Cells Tuberculosis / genetics Young Adult

Journal

Nature microbiology
ISSN: 2058-5276
Titre abrégé: Nat Microbiol
Pays: England
ID NLM: 101674869

Informations de publication

Date de publication:
02 2022
Historique:
received: 16 09 2021
accepted: 14 12 2021
pubmed: 2 2 2022
medline: 23 2 2022
entrez: 1 2 2022
Statut: ppublish

Résumé

Host cell chromatin changes are thought to play an important role in the pathogenesis of infectious diseases. Here we describe a histone acetylome-wide association study (HAWAS) of an infectious disease, on the basis of genome-wide H3K27 acetylation profiling of peripheral blood granulocytes and monocytes from persons with active Mycobacterium tuberculosis (Mtb) infection and healthy controls. We detected >2,000 differentially acetylated loci in either cell type in a Singapore Chinese discovery cohort (n = 46), which were validated in a subsequent multi-ethnic Singapore cohort (n = 29), as well as a longitudinal cohort from South Africa (n = 26), thus demonstrating that HAWAS can be independently corroborated. Acetylation changes were correlated with differential gene expression. Differential acetylation was enriched near potassium channel genes, including KCNJ15, which modulates apoptosis and promotes Mtb clearance in vitro. We performed histone acetylation quantitative trait locus (haQTL) analysis on the dataset and identified 69 candidate causal variants for immune phenotypes among granulocyte haQTLs and 83 among monocyte haQTLs. Our study provides proof-of-principle for HAWAS to infer mechanisms of host response to pathogens.

Identifiants

DOI: 10.1038/s41564-021-01049-w PMID: 35102304 PMC: PMC9439955
pubmed: 35102304
doi: 10.1038/s41564-021-01049-w
pii: 10.1038/s41564-021-01049-w
pmc: PMC9439955
doi:

Substances chimiques

Chromatin 0
Histones 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

312-326

Subventions

Organisme : Medical Research Council
ID : FC0012018
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 203135
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 104803
Pays : United Kingdom
Organisme : NIAID NIH HHS
ID : U01 AI115940
Pays : United States
Organisme : Wellcome Trust
ID : FC0012018
Pays : United Kingdom
Organisme : Cancer Research UK
ID : FC0012018
Pays : United Kingdom
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : NIDA NIH HHS
ID : R01 DA015302
Pays : United States

Commentaires et corrections

Type : CommentIn
Type : ErratumIn

Informations de copyright

© 2022. The Author(s), under exclusive licence to Springer Nature Limited.

Références

WHO World Health Statistics 2016: Monitoring Health for the SDGs http://www.who.int/gho/publications/world_health_statistics/2016/en/ (2016).
Behar, S. M., Divangahi, M. & Remold, H. G. Evasion of innate immunity by Mycobacterium tuberculosis: is death an exit strategy? Nat. Rev. Microbiol. 8, 668–674 (2010).
pubmed: 20676146 pmcid: 3221965 doi: 10.1038/nrmicro2387
Kumar, D. et al. Genome-wide analysis of the host intracellular network that regulates survival of Mycobacterium tuberculosis. Cell 140, 731–743 (2010).
pubmed: 20211141 doi: 10.1016/j.cell.2010.02.012
Berry, M. P. R. et al. An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis. Nature 466, 973–977 (2010).
pubmed: 20725040 pmcid: 3492754 doi: 10.1038/nature09247
Blankley, S. et al. A 380-gene meta-signature of active tuberculosis compared with healthy controls. Eur. Respir. J. 47, 1873–1876 (2016).
pubmed: 27076596 pmcid: 4892351 doi: 10.1183/13993003.02121-2015
Kaforou, M. et al. Detection of tuberculosis in HIV-infected and -uninfected African adults using whole blood RNA expression signatures: a case-control study. PLoS Med. 10, e1001538 (2013).
pubmed: 24167453 pmcid: 3805485 doi: 10.1371/journal.pmed.1001538
Novakovic, B. et al. β-glucan reverses the epigenetic state of LPS-induced immunological tolerance. Cell 167, 1354–1368.e14 (2016).
pubmed: 27863248 pmcid: 5927328 doi: 10.1016/j.cell.2016.09.034
Russ, B. E. et al. Distinct epigenetic signatures delineate transcriptional programs during virus-specific CD8+ T cell differentiation. Immunity 41, 853–865 (2014).
pubmed: 25517617 pmcid: 4479393 doi: 10.1016/j.immuni.2014.11.001
Saeed, S. et al. Epigenetic programming during monocyte to macrophage differentiation and trained innate immunity. Science 345, 1251086 (2014).
pubmed: 25258085 pmcid: 4242194 doi: 10.1126/science.1251086
Esterhuyse, M. M. et al. Epigenetics and proteomics join transcriptomics in the quest for tuberculosis biomarkers. mBio 6, e01187-15 (2015).
pubmed: 26374119 pmcid: 4600108 doi: 10.1128/mBio.01187-15
Roadmap Epigenomics ConsortiumIntegrative analysis of 111 reference human epigenomes. Nature 518, 317–330 (2015).
pmcid: 4530010 doi: 10.1038/nature14248
Consortium, T. E. P. An integrated encyclopedia of DNA elements in the human genome. Nature 489, 57–74 (2012).
doi: 10.1038/nature11247
Kumar, V. et al. Uniform, optimal signal processing of mapped deep-sequencing data. Nat. Biotechnol. 31, 615–622 (2013).
pubmed: 23770639 doi: 10.1038/nbt.2596
Sun, W. et al. Histone acetylome-wide association study of autism spectrum disorder. Cell 167, 1385–1397.e11 (2016).
pubmed: 27863250 doi: 10.1016/j.cell.2016.10.031
Klein, H.-U. et al. Epigenome-wide study uncovers large-scale changes in histone acetylation driven by tau pathology in aging and Alzheimer’s human brains. Nat. Neurosci. 22, 37–46 (2019).
pubmed: 30559478 doi: 10.1038/s41593-018-0291-1
Marzi, S. J. et al. A histone acetylome-wide association study of Alzheimer’s disease identifies disease-associated H3K27ac differences in the entorhinal cortex. Nat. Neurosci. 21, 1618–1627 (2018).
pubmed: 30349106 doi: 10.1038/s41593-018-0253-7
Spurrell, C. H. et al. Genome-wide fetalization of enhancer architecture in heart disease. Preprint at bioRxiv https://doi.org/10.1101/591362 (2019).
Tan W. L. W. et al. Epigenomes of human hearts reveal new genetic variants relevant for cardiac disease and phenotype. Circ. Res. 127, 761–777 (2020).
doi: 10.1161/CIRCRESAHA.120.317254
Chen, L. et al. Genetic drivers of epigenetic and transcriptional variation in human immune cells. Cell 167, 1398–1414.e24 (2016).
pubmed: 27863251 pmcid: 5119954 doi: 10.1016/j.cell.2016.10.026
Kim, B.-H., Shenoy, A. R., Kumar, P., Bradfield, C. J. & MacMicking, J. D. IFN-inducible GTPases in host defense. Cell Host Microbe 12, 432–444 (2012).
pubmed: 23084913 pmcid: 3490204 doi: 10.1016/j.chom.2012.09.007
McLean, C. Y. et al. GREAT improves functional interpretation of cis-regulatory regions. Nat. Biotechnol. 28, 495–501 (2010).
pubmed: 20436461 pmcid: 4840234 doi: 10.1038/nbt.1630
Eden, E., Navon, R., Steinfeld, I., Lipson, D. & Yakhini, Z. GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics 10, 48 (2009).
pubmed: 19192299 pmcid: 2644678 doi: 10.1186/1471-2105-10-48
Donovan, M. L., Schultz, T. E., Duke, T. J. & Blumenthal, A. Type I interferons in the pathogenesis of tuberculosis: molecular drivers and immunological consequences. Front. Immunol. 8, 1633 (2017).
pubmed: 29230217 pmcid: 5711827 doi: 10.3389/fimmu.2017.01633
Festen, E. A. M. et al. A meta-analysis of genome-wide association scans identifies IL18RAP, PTPN2, TAGAP, and PUS10 as shared risk loci for Crohn’s disease and celiac disease. PLoS Genet. 7, e1001283 (2011).
pubmed: 21298027 pmcid: 3029251 doi: 10.1371/journal.pgen.1001283
Burgon, J. et al. Serum and glucocorticoid-regulated kinase 1 regulates neutrophil clearance during inflammation resolution. J. Immunol. 192, 1796–1805 (2014).
pubmed: 24431232 doi: 10.4049/jimmunol.1300087
Daniel, J., Maamar, H., Deb, C., Sirakova, T. D. & Kolattukudy, P. E. Mycobacterium tuberculosis uses host triacylglycerol to accumulate lipid droplets and acquires a dormancy-like phenotype in lipid-loaded macrophages. PLoS Pathog. 7, e1002093 (2011).
pubmed: 21731490 pmcid: 3121879 doi: 10.1371/journal.ppat.1002093
Heinz, S. et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38, 576–589 (2010).
pubmed: 20513432 pmcid: 2898526 doi: 10.1016/j.molcel.2010.05.004
Hnisz, D. et al. Super-enhancers in the control of cell identity and disease. Cell 155, 934–947 (2013).
pubmed: 24119843 doi: 10.1016/j.cell.2013.09.053
Pott, S. & Lieb, J. D. What are super-enhancers? Nat. Genet. 47, 8–12 (2015).
pubmed: 25547603 doi: 10.1038/ng.3167
Ohira, M. et al. Gene identification in 1.6-Mb region of the Down syndrome region on chromosome 21. Genome Res. 7, 47–58 (1997).
pubmed: 9037601 doi: 10.1101/gr.7.1.47
Okamoto, K. et al. Inhibition of glucose-stimulated insulin secretion by KCNJ15, a newly identified susceptibility gene for type 2 diabetes. Diabetes 61, 1734–1741 (2012).
pubmed: 22566534 pmcid: 3379671 doi: 10.2337/db11-1201
Pearson, W. L., Dourado, M., Schreiber, M., Salkoff, L. & Nichols, C. G. Expression of a functional Kir4 family inward rectifier K+ channel from a gene cloned from mouse liver. J. Physiol. 514, 639–653 (1999).
pubmed: 9882736 pmcid: 2269105 doi: 10.1111/j.1469-7793.1999.639ad.x
Shuck, M. E. et al. Cloning and characterization of two K+ inward rectifier (Kir) 1.1 potassium channel homologs from human kidney (Kir1.2 and Kir1.3). J. Biol. Chem. 272, 586–593 (1997).
pubmed: 8995301 doi: 10.1074/jbc.272.1.586
Satproedprai, N. et al. Diagnostic value of blood gene expression signatures in active tuberculosis in Thais: a pilot study. Genes Immun. 16, 253–260 (2015).
pubmed: 25764116 doi: 10.1038/gene.2015.4
Lam, A. et al. Role of apoptosis and autophagy in tuberculosis. Am. J. Physiol. Lung Cell. Mol. Physiol. 313, L218–L229 (2017).
pubmed: 28495854 pmcid: 5582934 doi: 10.1152/ajplung.00162.2017
Shakeri, R., Kheirollahi, A. & Davoodi, J. Apaf-1: regulation and function in cell death. Biochimie 135, 111–125 (2017).
pubmed: 28192157 doi: 10.1016/j.biochi.2017.02.001
Suzuki-Karasaki, M., Ochiai, T. & Suzuki-Karasaki, Y. Crosstalk between mitochondrial ROS and depolarization in the potentiation of TRAIL-induced apoptosis in human tumor cells. Int. J. Oncol. 44, 616–628 (2014).
pubmed: 24337174 doi: 10.3892/ijo.2013.2215
West, A. P. et al. TLR signalling augments macrophage bactericidal activity through mitochondrial ROS. Nature 472, 476–480 (2011).
pubmed: 21525932 pmcid: 3460538 doi: 10.1038/nature09973
Singhal, A. et al. Metformin as adjunct antituberculosis therapy. Sci. Transl. Med. 6, 263ra159 (2014).
pubmed: 25411472 doi: 10.1126/scitranslmed.3009885
del Rosario, R. C.-H. et al. Sensitive detection of chromatin-altering polymorphisms reveals autoimmune disease mechanisms. Nat. Methods 12, 458–464 (2015).
pubmed: 25799442 doi: 10.1038/nmeth.3326
Grubert, F. et al. Genetic control of chromatin states in humans involves local and distal chromosomal interactions. Cell 162, 1051–1065 (2015).
pubmed: 26300125 pmcid: 4556133 doi: 10.1016/j.cell.2015.07.048
Kasowski, M. et al. Extensive variation in chromatin states across humans. Science 342, 750–752 (2013).
pubmed: 24136358 pmcid: 4075767 doi: 10.1126/science.1242510
Kilpinen, H. et al. Coordinated effects of sequence variation on DNA binding, chromatin structure, and transcription. Science 342, 744–747 (2013).
pubmed: 24136355 pmcid: 5502466 doi: 10.1126/science.1242463
McVicker, G. et al. Identification of genetic variants that affect histone modifications in human cells. Science 342, 747–749 (2013).
pubmed: 24136359 pmcid: 3947669 doi: 10.1126/science.1242429
Naranbhai, V. et al. Genomic modulators of gene expression in human neutrophils. Nat. Commun. 6, 7545 (2015).
pubmed: 26151758 doi: 10.1038/ncomms8545
Fairfax, B. P. et al. Innate immune activity conditions the effect of regulatory variants upon monocyte gene expression. Science 343, 1246949 (2014).
pubmed: 24604202 pmcid: 4064786 doi: 10.1126/science.1246949
MacArthur, J. et al. The new NHGRI-EBI catalog of published genome-wide association studies (GWAS catalog). Nucleic Acids Res. 45, D896–D901 (2017).
pubmed: 27899670 doi: 10.1093/nar/gkw1133
Zanetti, D. & Weale, M. E. Transethnic differences in GWAS signals: a simulation study. Ann. Hum. Genet. 82, 280–286 (2018).
pubmed: 29733446 doi: 10.1111/ahg.12251
Luo, Y. et al. Early progression to active tuberculosis is a highly heritable trait driven by 3q23 in Peruvians. Nat. Commun. 10, 3765 (2019).
pubmed: 31434886 pmcid: 6704092 doi: 10.1038/s41467-019-11664-1
Finucane, H. K. et al. Partitioning heritability by functional annotation using genome-wide association summary statistics. Nat. Genet. 47, 1228–1235 (2015).
pubmed: 26414678 pmcid: 4626285 doi: 10.1038/ng.3404
Bortner, C. D. & Cidlowski, J. A. Ion channels and apoptosis in cancer. Phil. Trans. R. Soc. B. 369, 20130104 (2014).
pubmed: 24493752 pmcid: 3917358 doi: 10.1098/rstb.2013.0104
Cang, C., Aranda, K., Seo, Y., Gasnier, B. & Ren, D. TMEM175 is an organelle K(+) channel regulating lysosomal function. Cell 162, 1101–1112 (2015).
pubmed: 26317472 doi: 10.1016/j.cell.2015.08.002
Jamaati, H. et al. Nitric oxide in the pathogenesis and treatment of tuberculosis. Front. Microbiol. 8, 2008 (2017).
pubmed: 29085351 pmcid: 5649180 doi: 10.3389/fmicb.2017.02008
Gutierrez, M. G. et al. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119, 753–766 (2004).
pubmed: 15607973 doi: 10.1016/j.cell.2004.11.038
MacGilvary, N. J., Kevorkian, Y. L. & Tan, S. Potassium response and homeostasis in Mycobacterium tuberculosis modulates environmental adaptation and is important for host colonization. PLoS Pathog. 15, e1007591 (2019).
pubmed: 30716121 pmcid: 6375644 doi: 10.1371/journal.ppat.1007591
Wallis, R. S. & Hafner, R. Advancing host-directed therapy for tuberculosis. Nat. Rev. Immunol. 15, 255–263 (2015).
pubmed: 25765201 doi: 10.1038/nri3813
Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760 (2009).
pubmed: 19451168 pmcid: 2705234 doi: 10.1093/bioinformatics/btp324
Bujold, D. et al. The International Human Epigenome Consortium data portal. Cell Syst. 3, 496–499.e2 (2016).
pubmed: 27863956 doi: 10.1016/j.cels.2016.10.019
Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).
pubmed: 20110278 pmcid: 2832824 doi: 10.1093/bioinformatics/btq033
Matys, V. et al. TRANSFAC and its module TRANSCompel: transcriptional gene regulation in eukaryotes. Nucleic Acids Res. 34, D108–D110 (2006).
pubmed: 16381825 doi: 10.1093/nar/gkj143
Sveinbjornsson, G. et al. HLA class II sequence variants influence tuberculosis risk in populations of European ancestry. Nat. Genet. 48, 318–322 (2016).
pubmed: 26829749 pmcid: 5081101 doi: 10.1038/ng.3498
Sobota, R. S. et al. A locus at 5q33.3 confers resistance to tuberculosis in highly susceptible individuals. Am. J. Hum. Genet. 98, 514–524 (2016).
pubmed: 26942285 pmcid: 4800052 doi: 10.1016/j.ajhg.2016.01.015

Auteurs

Ricardo C H Del Rosario (RCH)

Genome Institute of Singapore, Agency for Science, Technology and Research (A*STAR), Singapore, Singapore.
Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard, Cambridge, MA, USA.
Department of Genetics, Harvard Medical School, Boston, MA, USA.
ORCID: 0000-0002-7038-9598

Jeremie Poschmann (J)

Genome Institute of Singapore, Agency for Science, Technology and Research (A*STAR), Singapore, Singapore.
Inserm, Université de Nantes, Centre de Recherche en Transplantation et Immunologie, ITUN, Nantes, France.
ORCID: 0000-0002-9613-5297

Carey Lim (C)

Singapore Immunology Network, A*STAR, Singapore, Singapore.
A*STAR Infectious Diseases Labs, A*STAR, Singapore, Singapore.

Catherine Y Cheng (CY)

Singapore Immunology Network, A*STAR, Singapore, Singapore.

Pavanish Kumar (P)

Singapore Immunology Network, A*STAR, Singapore, Singapore.
ORCID: 0000-0003-1832-4436

Catherine Riou (C)

Wellcome Centre for Infectious Diseases Research in Africa, University of Cape Town, Cape Town, South Africa.
Institute of Infectious Disease and Molecular Medicine, University of Cape Town, Cape Town, South Africa.
Division of Medical Virology, Department of Pathology, University of Cape Town, Cape Town, South Africa.
ORCID: 0000-0001-9679-0745

Seow Theng Ong (ST)

Lee Kong Chian School of Medicine, Nanyang Technological University, Singapore, Singapore.
ORCID: 0000-0001-6089-4745

Sherif Gerges (S)

Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard, Cambridge, MA, USA.
Department of Genetics, Harvard Medical School, Boston, MA, USA.
Analytic and Translational Genetics Unit, Department of Medicine, Massachusetts General Hospital, Boston, MA, USA.

Hajira Shreen Hajan (HS)

Genome Institute of Singapore, Agency for Science, Technology and Research (A*STAR), Singapore, Singapore.

Dilip Kumar (D)

Inserm, Université de Nantes, Centre de Recherche en Transplantation et Immunologie, ITUN, Nantes, France.
ORCID: 0000-0002-1848-3034

Mardiana Marzuki (M)

Singapore Immunology Network, A*STAR, Singapore, Singapore.
A*STAR Infectious Diseases Labs, A*STAR, Singapore, Singapore.

Xiaohua Lu (X)

Singapore Immunology Network, A*STAR, Singapore, Singapore.

Andrea Lee (A)

Singapore Immunology Network, A*STAR, Singapore, Singapore.
A*STAR Infectious Diseases Labs, A*STAR, Singapore, Singapore.

Giovani Claresta Wijaya (GC)

Genome Institute of Singapore, Agency for Science, Technology and Research (A*STAR), Singapore, Singapore.

Nirmala Arul Rayan (NA)

Genome Institute of Singapore, Agency for Science, Technology and Research (A*STAR), Singapore, Singapore.

Zhong Zhuang (Z)

Lee Kong Chian School of Medicine, Nanyang Technological University, Singapore, Singapore.

Elsa Du Bruyn (E)

Wellcome Centre for Infectious Diseases Research in Africa, University of Cape Town, Cape Town, South Africa.
Institute of Infectious Disease and Molecular Medicine, University of Cape Town, Cape Town, South Africa.

Cynthia Bin Eng Chee (CBE)

Tuberculosis Control Unit, Tan Tock Seng Hospital, Singapore, Singapore.

Bernett Lee (B)

Singapore Immunology Network, A*STAR, Singapore, Singapore.

Josephine Lum (J)

Singapore Immunology Network, A*STAR, Singapore, Singapore.
ORCID: 0000-0003-1108-5989

Francesca Zolezzi (F)

Singapore Immunology Network, A*STAR, Singapore, Singapore.

Michael Poidinger (M)

Singapore Immunology Network, A*STAR, Singapore, Singapore.
ORCID: 0000-0002-1047-2277

Olaf Rotzschke (O)

Singapore Immunology Network, A*STAR, Singapore, Singapore.
ORCID: 0000-0001-8336-5248

Chiea Chuen Khor (CC)

Genome Institute of Singapore, Agency for Science, Technology and Research (A*STAR), Singapore, Singapore.
ORCID: 0000-0002-1128-4729

Robert J Wilkinson (RJ)

Wellcome Centre for Infectious Diseases Research in Africa, University of Cape Town, Cape Town, South Africa.
Institute of Infectious Disease and Molecular Medicine, University of Cape Town, Cape Town, South Africa.
Department of Infectious Disease, Imperial College, London, UK.
The Francis Crick Institute, London, UK.

Yee T Wang (YT)

Tuberculosis Control Unit, Tan Tock Seng Hospital, Singapore, Singapore.

George K Chandy (GK)

Lee Kong Chian School of Medicine, Nanyang Technological University, Singapore, Singapore.

Gennaro De Libero (G)

Singapore Immunology Network, A*STAR, Singapore, Singapore.
Department of Biomedicine, University of Basel, Basel, Switzerland.

Amit Singhal (A)

Singapore Immunology Network, A*STAR, Singapore, Singapore. amit_singhal@idlabs.a-star.edu.sg.
A*STAR Infectious Diseases Labs, A*STAR, Singapore, Singapore. amit_singhal@idlabs.a-star.edu.sg.
Lee Kong Chian School of Medicine, Nanyang Technological University, Singapore, Singapore. amit_singhal@idlabs.a-star.edu.sg.

Shyam Prabhakar (S)

Genome Institute of Singapore, Agency for Science, Technology and Research (A*STAR), Singapore, Singapore. prabhakars@gis.a-star.edu.sg.
ORCID: 0000-0002-6409-0661

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female

Evaluation of Low-Value Services Across Major Medicare Advantage Insurers and Traditional Medicare.

Ciara Duggan, Adam L Beckman, Ishani Ganguli et al.
1.00
Humans United States Aged Cross-Sectional Studies Medicare Part C

Effectiveness of Virtual Yoga for Chronic Low Back Pain: A Randomized Clinical Trial.

Hallie Tankha, Devyn Gaskins, Amanda Shallcross et al.
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH

questionsmedicales.fr › Métabolisme › Acylation › Acétylation › Histone acetylome-wide associations in immune...
questionsmedicales.fr › Personnes › Tranches d'âge › Adulte › Histone acetylome-wide associations in immune...
questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Structures de chromosome › Chromatine › Histone acetylome-wide associations in immune...
questionsmedicales.fr › Environnement et santé publique › Santé publique › Méthodes épidémiologiques › Caractéristiques des études épidémiologiques › Études épidémiologiques › Études de cohortes › Histone acetylome-wide associations in immune...
questionsmedicales.fr › Techniques d'investigation › Techniques génétiques › Études d'associations génétiques › Histone acetylome-wide associations in immune...
questionsmedicales.fr › Systèmes sanguin et immunitaire › Système immunitaire › Leucocytes › Granulocytes › Histone acetylome-wide associations in immune...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Nucléoprotéines › Histone › Histone acetylome-wide associations in immune...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Histone acetylome-wide associations in immune...
questionsmedicales.fr › Environnement et santé publique › Santé publique › Méthodes épidémiologiques › Caractéristiques des études épidémiologiques › Études épidémiologiques › Études de cohortes › Études longitudinales › Histone acetylome-wide associations in immune...
questionsmedicales.fr › Systèmes sanguin et immunitaire › Système immunitaire › Phagocytes › Monocytes › Histone acetylome-wide associations in immune...
questionsmedicales.fr › Bactéries › Bactéries à Gram positif › Bâtonnets à Gram positif › Bâtonnets asporogènes à Gram positif › Bâtonnets asporogènes réguliers à Gram positif › Mycobacteriaceae › Mycobacterium › Mycobacterium tuberculosis › Histone acetylome-wide associations in immune...
questionsmedicales.fr › Disciplines des sciences naturelles › Science › Recherche › Étude de validation de principe › Histone acetylome-wide associations in immune...
questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Génome › Composants de génome › Locus génétiques › Locus de caractère quantitatif › Histone acetylome-wide associations in immune...
questionsmedicales.fr › Régions géographiques › Asie › Asie du Sud-Est › Singapour › Histone acetylome-wide associations in immune...
questionsmedicales.fr › Régions géographiques › Afrique › Afrique subsaharienne › Afrique australe › République d'Afrique du Sud › Histone acetylome-wide associations in immune...
questionsmedicales.fr › Cellules › Cellules cultivées › Cellules cancéreuses en culture › Lignée cellulaire tumorale › Cellules THP-1 › Histone acetylome-wide associations in immune...
questionsmedicales.fr › Infection › Infections bactériennes et mycoses › Infections bactériennes › Infections bactériennes à Gram positif › Infections à Actinomycetales › Infections à Mycobacterium › Tuberculose › Histone acetylome-wide associations in immune...
questionsmedicales.fr › Personnes › Tranches d'âge › Adulte › Jeune adulte › Histone acetylome-wide associations in immune...