Mechanisms of epigenomic and functional convergence between glucocorticoid- and IL4-driven macrophage programming.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
18 Oct 2024
Historique:
received: 10 01 2024
accepted: 24 09 2024
medline: 19 10 2024
pubmed: 19 10 2024
entrez: 18 10 2024
Statut: epublish

Résumé

Macrophages adopt distinct phenotypes in response to environmental cues, with type-2 cytokine interleukin-4 promoting a tissue-repair homeostatic state (M2

Identifiants

pubmed: 39424780
doi: 10.1038/s41467-024-52942-x
pii: 10.1038/s41467-024-52942-x
doi:

Substances chimiques

Kruppel-Like Factor 4 0
Klf4 protein, mouse 0
Glucocorticoids 0
Kruppel-Like Transcription Factors 0
Receptors, Glucocorticoid 0
Interleukin-4 207137-56-2
Grip1 protein, mouse 0
Nerve Tissue Proteins 0
Il4 protein, mouse 0
Adaptor Proteins, Signal Transducing 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

9000

Subventions

Organisme : U.S. Department of Health & Human Services | National Institutes of Health (NIH)
ID : NIH R01DK099087
Organisme : U.S. Department of Health & Human Services | National Institutes of Health (NIH)
ID : NIH R01AI148129
Organisme : U.S. Department of Health & Human Services | National Institutes of Health (NIH)
ID : F31 HL152706-01A1
Organisme : U.S. Department of Health & Human Services | National Institutes of Health (NIH)
ID : NIH R01AI148416

Informations de copyright

© 2024. The Author(s).

Références

Germic, N., Frangez, Z., Yousefi, S. & Simon, H.-U. Regulation of the innate immune system by autophagy: monocytes, macrophages, dendritic cells and antigen presentation. Cell Death Differ. 26, 715–727 (2019).
pubmed: 30737475 pmcid: 6460400 doi: 10.1038/s41418-019-0297-6
Davies, L. C., Jenkins, S. J., Allen, J. E. & Taylor, P. R. Tissue-resident macrophages. Nat. Immunol. 14, 986–995 (2013).
pubmed: 24048120 pmcid: 4045180 doi: 10.1038/ni.2705
Perdiguero, E. G. & Geissmann, F. The development and maintenance of resident macrophages. Nat. Immunol. 17, 2–8 (2016).
pubmed: 26681456 pmcid: 4950995 doi: 10.1038/ni.3341
Locati, M., Curtale, G. & Mantovani, A. Diversity, mechanisms and significance of macrophage plasticity. Annu. Rev. Pathol. 15, 123 (2020).
pubmed: 31530089 doi: 10.1146/annurev-pathmechdis-012418-012718
Wynn, T. A. & Vannella, K. M. Macrophages in tissue repair, regeneration, and fibrosis. Immunity 44, 450–462 (2016).
pmcid: 4794754 doi: 10.1016/j.immuni.2016.02.015
Glass, C. K. & Natoli, G. Molecular control of activation and priming in macrophages. Nat. Immunol. 17, 26–33 (2015).
pmcid: 4795476 doi: 10.1038/ni.3306
Murray, P. J. Macrophage polarization. Annu. Rev. Physiol. 79, 541–566 (2017).
pubmed: 27813830 doi: 10.1146/annurev-physiol-022516-034339
Shapouri-Moghaddam, A. et al. Macrophage plasticity, polarization, and function in health and disease. J. Cell Physiol. 233, 6425–6440 (2018).
pubmed: 29319160 doi: 10.1002/jcp.26429
Xue, J. et al. Transcriptome-based network analysis reveals a spectrum model of human macrophage activation. Immunity 40, 274–288 (2014).
pmcid: 3991396 doi: 10.1016/j.immuni.2014.01.006
Hoeksema, M. A. et al. Mechanisms underlying divergent responses of genetically distinct macrophages to IL−4. Sci. Adv. 7, eabf9808 (2021).
pubmed: 34134993 pmcid: 8208725 doi: 10.1126/sciadv.abf9808
Daniel, B. et al. The nuclear receptor PPARγ controls progressive macrophage polarization as a ligand-insensitive epigenomic ratchet of transcriptional memory. Immunity 49, 615–626.e616 (2018).
pubmed: 30332629 pmcid: 6197058 doi: 10.1016/j.immuni.2018.09.005
Junttila, I. S. Tuning the cytokine responses: an update on interleukin (IL)-4 and IL-13 receptor complexes. Front. Immunol. 9, 888 (2018).
pubmed: 29930549 pmcid: 6001902 doi: 10.3389/fimmu.2018.00888
Czimmerer, Z. et al. The transcription factor STAT6 mediates direct repression of inflammatory enhancers and limits activation of alternatively polarized macrophages. Immunity 48, 75–90.e76 (2018).
pubmed: 29343442 pmcid: 5772169 doi: 10.1016/j.immuni.2017.12.010
Daniel, B. et al. The transcription factor EGR2 is the molecular linchpin connecting STAT6 activation to the late, stable epigenomic program of alternative macrophage polarization. Genes Dev. 34, 1474–1492 (2020).
pubmed: 33060136 pmcid: 7608752 doi: 10.1101/gad.343038.120
Liao, X. et al. Kruppel-like factor 4 regulates macrophage polarization. J. Clin. Invest. 121, 2736–2749 (2011).
pmcid: 3223832 doi: 10.1172/JCI45444
Coutinho, A. E. & Chapman, K. E. The anti-inflammatory and immunosuppressive effects of glucocorticoids, recent developments and mechanistic insights. Mol. Cell Endocrinol. 335, 2–13 (2011).
pubmed: 20398732 pmcid: 3047790 doi: 10.1016/j.mce.2010.04.005
Vandewalle, J., Luypaert, A., De Bosscher, K. & Libert, C. Therapeutic mechanisms of glucocorticoids. Trends Endocrinol. Metab. 29, 42–54 (2018).
pubmed: 29162310 doi: 10.1016/j.tem.2017.10.010
Barnes, P. J. Glucocorticosteroids. Handb. Exp. Pharm. 237, 93–115 (2017).
doi: 10.1007/164_2016_62
Mantovani, A. et al. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 25, 677–686 (2004).
doi: 10.1016/j.it.2004.09.015
Chinenov, Y. et al. Role of transcriptional coregulator GRIP1 in the anti-inflammatory actions of glucocorticoids. Proc. Natl. Acad. Sci. USA 109, 11776–11781 (2012).
pubmed: 22753499 pmcid: 3406827 doi: 10.1073/pnas.1206059109
Sacta, M. A. et al. Gene-specific mechanisms direct glucocorticoid-receptor-driven repression of inflammatory response genes in macrophages. Elife 7, e34864 (2018).
pubmed: 29424686 pmcid: 5821458 doi: 10.7554/eLife.34864
Rogatsky, I., Zarember, K. A. & Yamamoto, K. R. Factor recruitment and TIF2/GRIP1 corepressor activity at a collagenase-3 response element that mediates regulation by phorbol esters and hormones. EMBO J. 20, 6071–6083 (2001).
pubmed: 11689447 pmcid: 125702 doi: 10.1093/emboj/20.21.6071
Chinenov, Y., Sacta, M. A., Cruz, A. R. & Rogatsky, I. GRIP1-associated SET-domain methyltransferase in glucocorticoid receptor target gene expression. Proc. Natl. Acad. Sci. USA 105, 20185–20190 (2008).
pubmed: 19074285 pmcid: 2629346 doi: 10.1073/pnas.0810863105
Hong, H., Kohli, K., Garabedian, M. J. & Stallcup, M. R. GRIP1, a transcriptional coactivator for the AF-2 transactivation domain of steroid, thyroid, retinoid, and vitamin D receptors. Mol. Cell. Biol. 17, 2735–2744 (1997).
pubmed: 9111344 pmcid: 232124 doi: 10.1128/MCB.17.5.2735
Voegel, J. J. et al. The coactivator TIF2 contains three nuclear receptor-binding motifs and mediates transactivation through CBP binding-dependent and -independent pathways. EMBO J. 17, 507–519 (1998).
pubmed: 9430642 pmcid: 1170401 doi: 10.1093/emboj/17.2.507
Vago, J. P. et al. Glucocorticoid-induced leucine zipper modulates macrophage polarization and apoptotic cell clearance. Pharm. Res. 158, 104842 (2020).
doi: 10.1016/j.phrs.2020.104842
van de Garde, M. D. et al. Chronic exposure to glucocorticoids shapes gene expression and modulates innate and adaptive activation pathways in macrophages with distinct changes in leukocyte attraction. J. Immunol. 192, 1196–1208 (2014).
pubmed: 24395918 doi: 10.4049/jimmunol.1302138
Garabuczi, E., Sarang, Z. & Szondy, Z. Glucocorticoids enhance prolonged clearance of apoptotic cells by upregulating liver X receptor, peroxisome proliferator-activated receptor-delta and UCP2. Biochim. Biophys. Acta 1853, 573–582 (2015).
pubmed: 25523142 doi: 10.1016/j.bbamcr.2014.12.014
Shepherd, V. L., Konish, M. G. & Stahl, P. Dexamethasone increases expression of mannose receptors and decreases extracellular lysosomal enzyme accumulation in macrophages. J. Biol. Chem. 260, 160–164 (1985).
pubmed: 3965445 doi: 10.1016/S0021-9258(18)89708-3
Chinenov, Y., Coppo, M., Gupte, R., Sacta, M. A. & Rogatsky, I. Glucocorticoid receptor coordinates transcription factor-dominated regulatory network in macrophages. BMC Genomics 15, 656 (2014).
pubmed: 25099603 pmcid: 4133603 doi: 10.1186/1471-2164-15-656
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).
pmcid: 2898526 doi: 10.1016/j.molcel.2010.05.004
Bannister, A. J. & Kouzarides, T. Regulation of chromatin by histone modifications. Cell Res. 21, 381–395 (2011).
pubmed: 21321607 pmcid: 3193420 doi: 10.1038/cr.2011.22
Creyghton, M. P. et al. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc. Natl. Acad. Sci. USA 107, 21931–21936 (2010).
pubmed: 21106759 pmcid: 3003124 doi: 10.1073/pnas.1016071107
Johnson, A. B. & O’Malley, B. W. Steroid receptor coactivators 1, 2, and 3: critical regulators of nuclear receptor activity and steroid receptor modulator (SRM)-based cancer therapy. Mol. Cell Endocrinol. 348, 430–439 (2012).
pubmed: 21664237 doi: 10.1016/j.mce.2011.04.021
Rogatsky, I., Luecke, H. F., Leitman, D. C. & Yamamoto, K. R. Alternate surfaces of transcriptional coregulator GRIP1 function in different glucocorticoid receptor activation and repression contexts. Proc. Natl. Acad. Sci. USA 99, 16701–16706 (2002).
pubmed: 12481024 pmcid: 139207 doi: 10.1073/pnas.262671599
Rollins, D. A. et al. Glucocorticoid-induced phosphorylation by CDK9 modulates the coactivator functions of transcriptional cofactor GRIP1 in macrophages. Nat. Commun. 8, 1739 (2017).
pubmed: 29170386 pmcid: 5700924 doi: 10.1038/s41467-017-01569-2
Coppo, M., Chinenov, Y., Sacta, M. A. & Rogatsky, I. The transcriptional coregulator GRIP1 controls macrophage polarization and metabolic homeostasis. Nat. Commun. 7, 12254 (2016).
pubmed: 27464507 pmcid: 4974480 doi: 10.1038/ncomms12254
Bosurgi, L. et al. Macrophage function in tissue repair and remodeling requires IL-4 or IL-13 with apoptotic cells. Science 356, 1072–1076 (2017).
pubmed: 28495875 pmcid: 5556699 doi: 10.1126/science.aai8132
Yip, J. L. K., Balasuriya, G. K., Spencer, S. J. & Hill-Yardin, E. L. The role of intestinal macrophages in gastrointestinal homeostasis: Heterogeneity and Implications in Disease. Cell Mol. Gastroenterol. Hepatol. 12, 1701–1718 (2021).
pubmed: 34506953 pmcid: 8551786 doi: 10.1016/j.jcmgh.2021.08.021
McColl, A. et al. Glucocorticoids induce protein S-dependent phagocytosis of apoptotic neutrophils by human macrophages. J. Immunol. 183, 2167–2175 (2009).
pubmed: 19597001 doi: 10.4049/jimmunol.0803503
Balce, D. R. et al. Alternative activation of macrophages by IL-4 enhances the proteolytic capacity of their phagosomes through synergistic mechanisms. Blood 118, 4199–4208 (2011).
pubmed: 21846901 doi: 10.1182/blood-2011-01-328906
Galuppo, P. et al. The glucocorticoid receptor in monocyte-derived macrophages is critical for cardiac infarct repair and remodeling. FASEB J. 31, 5122–5132 (2017).
pubmed: 28768721 pmcid: 5636710 doi: 10.1096/fj.201700317R
Jayme, T. S. et al. Human interleukin-4-treated regulatory macrophages promote epithelial wound healing and reduce colitis in a mouse model. Sci. Adv. 6, eaba4376 (2020).
pubmed: 32548267 pmcid: 7274799 doi: 10.1126/sciadv.aba4376
Martinez, F. O., Gordon, S., Locati, M. & Mantovani, A. Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J. Immunol. 177, 7303–7311 (2006).
pubmed: 17082649 doi: 10.4049/jimmunol.177.10.7303
Murray, P. J. et al. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 41, 14–20 (2014).
pubmed: 25035950 pmcid: 4123412 doi: 10.1016/j.immuni.2014.06.008
Adelman, K. et al. Immediate mediators of the inflammatory response are poised for gene activation through RNA polymerase II stalling. Proc. Natl. Acad. Sci. USA 106, 18207–18212 (2009).
pubmed: 19820169 pmcid: 2775335 doi: 10.1073/pnas.0910177106
Yu, L. et al. Negative elongation factor complex enables macrophage inflammatory responses by controlling anti-inflammatory gene expression. Nat. Commun. 11, 2286 (2020).
pubmed: 32385332 pmcid: 7210294 doi: 10.1038/s41467-020-16209-5
Reichardt, S. D. et al. The role of glucocorticoids in inflammatory diseases. Cells 10, 2921 (2021).
pubmed: 34831143 pmcid: 8616489 doi: 10.3390/cells10112921
Escoter-Torres, L. et al. Fighting the fire: Mechanisms of inflammatory gene regulation by the glucocorticoid receptor. Front. Immunol. 10, 1859 (2019).
pubmed: 31440248 pmcid: 6693390 doi: 10.3389/fimmu.2019.01859
Ruffell, D. et al. A CREB-C/EBPbeta cascade induces M2 macrophage-specific gene expression and promotes muscle injury repair. Proc. Natl. Acad. Sci. USA 106, 17475–17480 (2009).
pubmed: 19805133 pmcid: 2762675 doi: 10.1073/pnas.0908641106
Puig-Kroger, A. et al. Folate receptor beta is expressed by tumor-associated macrophages and constitutes a marker for M2 anti-inflammatory/regulatory macrophages. Cancer Res. 69, 9395–9403 (2009).
pubmed: 19951991 doi: 10.1158/0008-5472.CAN-09-2050
Lopez-Lopez, S. et al. NOTCH4 potentiates the IL-13 induced genetic program in M2 alternative macrophages through the AP1 and IRF4-JMJD3 axis. Int. Immunol. 35, 497–509 (2023).
pubmed: 37478314 doi: 10.1093/intimm/dxad028
Li, Z. H. et al. Mesenchymal stem cells promote polarization of M2 macrophages in mice with acute-on-chronic liver failure via Mertk/JAK1/STAT6 signaling. Stem Cells 41, 1171–1184 (2023).
pubmed: 37659098 doi: 10.1093/stmcls/sxad069
Grontved, L. et al. C/EBP maintains chromatin accessibility in liver and facilitates glucocorticoid receptor recruitment to steroid response elements. EMBO J. 32, 1568–1583 (2013).
pubmed: 23665916 pmcid: 3671252 doi: 10.1038/emboj.2013.106
Rath, M., Muller, I., Kropf, P., Closs, E. I. & Munder, M. Metabolism via Arginase or Nitric Oxide synthase: Two competing arginine pathways in macrophages. Front. Immunol. 5, 532 (2014).
pubmed: 25386178 pmcid: 4209874 doi: 10.3389/fimmu.2014.00532
Sevilla, L. M. et al. Glucocorticoid receptor and Klf4 co-regulate anti-inflammatory genes in keratinocytes. Mol. Cell Endocrinol. 412, 281–289 (2015).
pubmed: 26001834 doi: 10.1016/j.mce.2015.05.015
Lee, Y. H., Koh, S. S., Zhang, X., Cheng, X. & Stallcup, M. R. Synergy among nuclear receptor coactivators: selective requirement for protein methyltransferase and acetyltransferase activities. Mol. Cell Biol. 22, 3621–3632 (2002).
pubmed: 11997499 pmcid: 133819 doi: 10.1128/MCB.22.11.3621-3632.2002
Xu, J. & Li, Q. Review of the in vivo functions of the p160 steroid receptor coactivator family. Mol. Endocrinol. 17, 1681–1692 (2003).
pubmed: 12805412 doi: 10.1210/me.2003-0116
Comoglio, F. et al. Dissection of acute stimulus-inducible nucleosome remodeling in mammalian cells. Genes Dev. 33, 1159–1174 (2019).
pubmed: 31371436 pmcid: 6719622 doi: 10.1101/gad.326348.119
Piccolo, V. et al. Opposing macrophage polarization programs show extensive epigenomic and transcriptional cross-talk. Nat. Immunol. 18, 530–540 (2017).
pubmed: 28288101 pmcid: 5524187 doi: 10.1038/ni.3710
Munoz-Rojas, A. R., Kelsey, I., Pappalardo, J. L., Chen, M. & Miller-Jensen, K. Co-stimulation with opposing macrophage polarization cues leads to orthogonal secretion programs in individual cells. Nat. Commun. 12, 301 (2021).
pubmed: 33436596 pmcid: 7804107 doi: 10.1038/s41467-020-20540-2
Czimmerer, Z. et al. The epigenetic state of IL-4-polarized macrophages enables inflammatory cistromic expansion and extended synergistic response to TLR ligands. Immunity 55, 2006–2026 e2006 (2022).
pubmed: 36323312 pmcid: 9649892 doi: 10.1016/j.immuni.2022.10.004
Caratti, G. et al. Glucocorticoid activation of anti-inflammatory macrophages protects against insulin resistance. Nat. Commun. 14, 2271 (2023).
pubmed: 37080971 pmcid: 10119112 doi: 10.1038/s41467-023-37831-z
Buenrostro, J. D., Wu, B., Chang, H. Y. & Greenleaf, W. J. ATAC-seq: A method for assaying chromatin accessibility genome-wide. Curr. Protoc. Mol. Biol. 109, 21–29 (2015).
pmcid: 4374986
Corces, M. R. et al. An improved ATAC-seq protocol reduces background and enables interrogation of frozen tissues. Nat. Methods 14, 959–962 (2017).
pmcid: 5623106 doi: 10.1038/nmeth.4396
Zhou, Y. et al. Intestinal toxicity to CTLA-4 blockade driven by IL-6 and myeloid infiltration. J. Exp. Med. 220, e20221333 (2023).
pubmed: 36367776 doi: 10.1084/jem.20221333
Chen, S., Zhou, Y., Chen, Y. & Gu, J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34, i884–i890 (2018).
pubmed: 30423086 pmcid: 6129281 doi: 10.1093/bioinformatics/bty560
Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).
pubmed: 23104886 doi: 10.1093/bioinformatics/bts635
Liao, Y., Smyth, G. K. & Shi, W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923–930 (2014).
pubmed: 24227677 doi: 10.1093/bioinformatics/btt656
Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140 (2010).
pubmed: 19910308 doi: 10.1093/bioinformatics/btp616
Yaari, G., Bolen, C. R., Thakar, J. & Kleinstein, S. H. Quantitative set analysis for gene expression: a method to quantify gene set differential expression including gene-gene correlations. Nucleic Acids Res. 41, e170 (2013).
pubmed: 23921631 pmcid: 3794608 doi: 10.1093/nar/gkt660
Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).
pmcid: 3322381 doi: 10.1038/nmeth.1923
Li, H. et al. The sequence alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
pubmed: 19505943 pmcid: 2723002 doi: 10.1093/bioinformatics/btp352
Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).
pmcid: 2592715 doi: 10.1186/gb-2008-9-9-r137
Kawaji, H., Kasukawa, T., Forrest, A., Carninci, P. & Hayashizaki, Y. The FANTOM5 collection, a data series underpinning mammalian transcriptome atlases in diverse cell types. Sci. Data 4, 170113 (2017).
pubmed: 28850107 pmcid: 5574373 doi: 10.1038/sdata.2017.113
Castro-Mondragon, J. A. et al. JASPAR 2022: the 9th release of the open-access database of transcription factor binding profiles. Nucleic Acids Res. 50, D165–D173 (2022).
pubmed: 34850907 doi: 10.1093/nar/gkab1113
Mammana, A. & Helmuth, J. bamsignals: Extract read count signals from bam files. (2023).
Nordin, A., Zambanini, G., Pagella, P. & Cantu, C. The CUT&RUN suspect list of problematic regions of the genome. Genome Biol. 24, 185 (2023).
pubmed: 37563719 pmcid: 10416431 doi: 10.1186/s13059-023-03027-3
Ogata, J. D. et al. excluderanges: exclusion sets for T2T-CHM13, GRCm39, and other genome assemblies. Bioinformatics 39, btad198 (2023).
pubmed: 37067481 pmcid: 10126321 doi: 10.1093/bioinformatics/btad198

Auteurs

Dinesh K Deochand (DK)

Hospital for Special Surgery Research Institute, David Z. Rosensweig Genomics Center, New York, NY, USA.
Department of Microbiology and Immunology, Weill Cornell Medicine, New York, NY, USA.

Marija Dacic (M)

Hospital for Special Surgery Research Institute, David Z. Rosensweig Genomics Center, New York, NY, USA.
Graduate Program in Physiology, Biophysics and Systems Biology, Weill Cornell Graduate School of Medical Sciences, New York, NY, USA.

Michael J Bale (MJ)

Department of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, NY, USA.
Graduate Program in Immunology and Microbial Pathogenesis, Weill Cornell Graduate School of Medical Sciences, New York, NY, USA.

Andrew W Daman (AW)

Department of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, NY, USA.
Graduate Program in Immunology and Microbial Pathogenesis, Weill Cornell Graduate School of Medical Sciences, New York, NY, USA.

Vidyanath Chaudhary (V)

Hospital for Special Surgery Research Institute, David Z. Rosensweig Genomics Center, New York, NY, USA.
Department of Microbiology and Immunology, Weill Cornell Medicine, New York, NY, USA.

Steven Z Josefowicz (SZ)

Department of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, NY, USA.
Graduate Program in Immunology and Microbial Pathogenesis, Weill Cornell Graduate School of Medical Sciences, New York, NY, USA.

David Oliver (D)

Hospital for Special Surgery Research Institute, David Z. Rosensweig Genomics Center, New York, NY, USA.

Yurii Chinenov (Y)

Hospital for Special Surgery Research Institute, David Z. Rosensweig Genomics Center, New York, NY, USA.

Inez Rogatsky (I)

Hospital for Special Surgery Research Institute, David Z. Rosensweig Genomics Center, New York, NY, USA. rogatskyi@hss.edu.
Department of Microbiology and Immunology, Weill Cornell Medicine, New York, NY, USA. rogatskyi@hss.edu.
Graduate Program in Immunology and Microbial Pathogenesis, Weill Cornell Graduate School of Medical Sciences, New York, NY, USA. rogatskyi@hss.edu.

Articles similaires

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
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male
Humans Meals Time Factors Female Adult

Classifications MeSH