Dynamic changes in RNA m


Journal

Cellular and molecular life sciences : CMLS
ISSN: 1420-9071
Titre abrégé: Cell Mol Life Sci
Pays: Switzerland
ID NLM: 9705402

Informations de publication

Date de publication:
23 May 2024
Historique:
received: 06 02 2024
accepted: 01 05 2024
revised: 27 04 2024
medline: 23 5 2024
pubmed: 23 5 2024
entrez: 23 5 2024
Statut: epublish

Résumé

RNA modifications are essential for the establishment of cellular identity. Although increasing evidence indicates that RNA modifications regulate the innate immune response, their role in monocyte-to-macrophage differentiation and polarisation is unclear. While m

Identifiants

pubmed: 38780787
doi: 10.1007/s00018-024-05261-9
pii: 10.1007/s00018-024-05261-9
doi:

Substances chimiques

RNA, Messenger 0
RNA 63231-63-0
Adenosine K72T3FS567

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

229

Subventions

Organisme : National Health and Medical Research Council
ID : 1126306
Organisme : National Health and Medical Research Council
ID : 1128175
Organisme : National Health and Medical Research Council
ID : 1128175
Organisme : National Health and Medical Research Council
ID : 1177305
Organisme : National Health and Medical Research Council
ID : 1191613
Organisme : Cancer Institute NSW
ID : 2018/CDF002
Organisme : Cancer Institute NSW
ID : 2105/ECF113

Informations de copyright

© 2024. The Author(s).

Références

Louloupi A, Ntini E, Conrad T, Ørom UAV (2018) Transient N-6-methyladenosine transcriptome sequencing reveals a regulatory role of m6A in splicing efficiency. Cell Rep 23(12):3429–3437
pubmed: 29924987 doi: 10.1016/j.celrep.2018.05.077
Roundtree IA, Luo G-Z, Zhang Z, Wang X, Zhou T, Cui Y, Sha J, Huang X, Guerrero L, Xie P, He E, Shen B, He C (2017) YTHDC1 mediates nuclear export of N6-methyladenosine methylated mRNAs. Elife 6:e31311
pubmed: 28984244 pmcid: 5648532 doi: 10.7554/eLife.31311
Shi H, Wang X, Lu Z, Zhao BS, Ma H, Hsu PJ, Liu C, He C (2017) YTHDF3 facilitates translation and decay of N6-methyladenosine-modified RNA. Cell Res 27(3):315–328
pubmed: 28106072 pmcid: 5339834 doi: 10.1038/cr.2017.15
Wang X, Zhao Boxuan S, Roundtree Ian A, Lu Z, Han D, Ma H, Weng X, Chen K, Shi H, He C (2015) N6-methyladenosine modulates messenger RNA translation efficiency. Cell 161(6):1388–1399
pubmed: 26046440 pmcid: 4825696 doi: 10.1016/j.cell.2015.05.014
Frye M, Harada BT, Behm M, He C (2018) RNA modifications modulate gene expression during development. Science 361(6409):1346–1349
pubmed: 30262497 pmcid: 6436390 doi: 10.1126/science.aau1646
Jonkhout N, Tran J, Smith MA, Schonrock N, Mattick JS, Novoa EM (2017) The RNA modification landscape in human disease. RNA 23(12):1754–1769
pubmed: 28855326 pmcid: 5688997 doi: 10.1261/rna.063503.117
Meyer Kate D, Saletore Y, Zumbo P, Elemento O, Mason Christopher E, Jaffrey Samie R (2012) Comprehensive analysis of mRNA methylation reveals enrichment in 3′ UTRs and near stop codons. Cell 149(7):1635–1646
pubmed: 22608085 pmcid: 3383396 doi: 10.1016/j.cell.2012.05.003
Liu J, Yue Y, Han D, Wang X, Fu Y, Zhang L, Jia G, Yu M, Lu Z, Deng X, Dai Q, Chen W, He C (2014) A METTL3–METTL14 complex mediates mammalian nuclear RNA N6-adenosine methylation. Nat Chem Biol 10(2):93–95
pubmed: 24316715 doi: 10.1038/nchembio.1432
Ping X-L, Sun B-F, Wang L, Xiao W, Yang X, Wang W-J, Adhikari S, Shi Y, Lv Y, Chen Y-S, Zhao X, Li A, Yang Y, Dahal U, Lou X-M, Liu X, Huang J, Yuan W-P, Zhu X-F, Cheng T, Zhao Y-L, Wang X, Danielsen JMR, Liu F, Yang Y-G (2014) Mammalian WTAP is a regulatory subunit of the RNA N6-methyladenosine methyltransferase. Cell Res 24(2):177–189
pubmed: 24407421 pmcid: 3915904 doi: 10.1038/cr.2014.3
Schwartz S, Mumbach Maxwell R, Jovanovic M, Wang T, Maciag K, Bushkin GG, Mertins P, Ter-Ovanesyan D, Habib N, Cacchiarelli D, Sanjana Neville E, Freinkman E, Pacold Michael E, Satija R, Mikkelsen Tarjei S, Hacohen N, Zhang F, Carr Steven A, Lander Eric S, Regev A (2014) Perturbation of m6A writers reveals two distinct classes of mRNA methylation at internal and 5′ sites. Cell Rep 8(1):284–296
pubmed: 24981863 pmcid: 4142486 doi: 10.1016/j.celrep.2014.05.048
Wen J, Lv R, Ma H, Shen H, He C, Wang J, Jiao F, Liu H, Yang P, Tan L, Lan F, Shi YG, He C, Shi Y, Diao J (2018) Zc3h13 regulates nuclear RNA m6A methylation and mouse embryonic stem cell self-renewal. Mol Cell 69(6):1028-1038.e1026
pubmed: 29547716 pmcid: 5858226 doi: 10.1016/j.molcel.2018.02.015
Yue Y, Liu J, Cui X, Cao J, Luo G, Zhang Z, Cheng T, Gao M, Shu X, Ma H, Wang F, Wang X, Shen B, Wang Y, Feng X, He C, Liu J (2018) VIRMA mediates preferential m6A mRNA methylation in 3′UTR and near stop codon and associates with alternative polyadenylation. Cell Discov 4(1):10
pubmed: 29507755 pmcid: 5826926 doi: 10.1038/s41421-018-0019-0
Gerken T, Girard CA, Tung Y-CL, Webby CJ, Saudek V, Hewitson KS, Yeo GSH, McDonough MA, Cunliffe S, McNeill LA, Galvanovskis J, Rorsman P, Robins P, Prieur X, Coll AP, Ma M, Jovanovic Z, Farooqi IS, Sedgwick B, Barroso I, Lindahl T, Ponting CP, Ashcroft FM, O’Rahilly S, Schofield CJ (2007) The obesity-associated FTO gene encodes a 2-oxoglutarate-dependent nucleic acid demethylase. Science 318(5855):1469–1472
pubmed: 17991826 pmcid: 2668859 doi: 10.1126/science.1151710
Zheng G, Dahl John A, Niu Y, Fedorcsak P, Huang C-M, Li Charles J, Vågbø Cathrine B, Shi Y, Wang W-L, Song S-H, Lu Z, Bosmans Ralph PG, Dai Q, Hao Y-J, Yang X, Zhao W-M, Tong W-M, Wang X-J, Bogdan F, Furu K, Fu Y, Jia G, Zhao X, Liu J, Krokan Hans E, Klungland A, Yang Y-G, He C (2013) ALKBH5 Is a mammalian RNA demethylase that impacts RNA metabolism and mouse fertility. Mol Cell 49(1):18–29
pubmed: 23177736 doi: 10.1016/j.molcel.2012.10.015
Zaccara S, Ries RJ, Jaffrey SR (2019) Reading, writing and erasing mRNA methylation. Nat Rev Mol Cell Biol 20(10):608–624
pubmed: 31520073 doi: 10.1038/s41580-019-0168-5
Wang Y, Li Y, Toth JI, Petroski MD, Zhang Z, Zhao JC (2014) N6-methyladenosine modification destabilizes developmental regulators in embryonic stem cells. Nat Cell Biol 16(2):191–198
pubmed: 24394384 pmcid: 4640932 doi: 10.1038/ncb2902
Cheng Y, Luo H, Izzo F, Pickering BF, Nguyen D, Myers R, Schurer A, Gourkanti S, Brüning JC, Vu LP, Jaffrey SR, Landau DA, Kharas MG (2019) m6A RNA methylation maintains hematopoietic stem cell identity and symmetric commitment. Cell Rep 28(7):1703-1716.e1706
pubmed: 31412241 pmcid: 6818972 doi: 10.1016/j.celrep.2019.07.032
Rubio RM, Depledge DP, Bianco C, Thompson L, Mohr I (2018) RNA m6 A modification enzymes shape innate responses to DNA by regulating interferon β. Genes Dev 32(23–24):1472–1484
pubmed: 30463905 pmcid: 6295168 doi: 10.1101/gad.319475.118
Shulman Z, Stern-Ginossar N (2020) The RNA modification N6-methyladenosine as a novel regulator of the immune system. Nat Immunol 21(5):501–512
pubmed: 32284591 doi: 10.1038/s41590-020-0650-4
Winkler R, Gillis E, Lasman L, Safra M, Geula S, Soyris C, Nachshon A, Tai-Schmiedel J, Friedman N, Le-Trilling VTK, Trilling M, Mandelboim M, Hanna JH, Schwartz S, Stern-Ginossar N (2019) m6A modification controls the innate immune response to infection by targeting type I interferons. Nat Immunol 20(2):173–182
pubmed: 30559377 doi: 10.1038/s41590-018-0275-z
Delatte B, Wang F, Ngoc LV, Collignon E, Bonvin E, Deplus R, Calonne E, Hassabi B, Putmans P, Awe S, Wetzel C, Kreher J, Soin R, Creppe C, Limbach PA, Gueydan C, Kruys V, Brehm A, Minakhina S, Defrance M, Steward R, Fuks F (2016) Transcriptome-wide distribution and function of RNA hydroxymethylcytosine. Science 351(6270):282–285
pubmed: 26816380 doi: 10.1126/science.aac5253
Huber SM, van Delft P, Mendil L, Bachman M, Smollett K, Werner F, Miska EA, Balasubramanian S (2015) Formation and abundance of 5-hydroxymethylcytosine in RNA. ChemBioChem 16(5):752–755
pubmed: 25676849 pmcid: 4471624 doi: 10.1002/cbic.201500013
Lan J, Rajan N, Bizet M, Penning A, Singh NK, Guallar D, Calonne E, Li Greci A, Bonvin E, Deplus R, Hsu PJ, Nachtergaele S, Ma C, Song R, Fuentes-Iglesias A, Hassabi B, Putmans P, Mies F, Menschaert G, Wong JJL, Wang J, Fidalgo M, Yuan B, Fuks F (2020) Functional role of Tet-mediated RNA hydroxymethylcytosine in mouse ES cells and during differentiation. Nat Commun 11(1):4956
pubmed: 33009383 pmcid: 7532169 doi: 10.1038/s41467-020-18729-6
Shen Q, Zhang Q, Shi Y, Shi Q, Jiang Y, Gu Y, Li Z, Li X, Zhao K, Wang C, Li N, Cao X (2018) Tet2 promotes pathogen infection-induced myelopoiesis through mRNA oxidation. Nature 554(7690):123–127
pubmed: 29364877 doi: 10.1038/nature25434
Guallar D, Bi X, Pardavila JA, Huang X, Saenz C, Shi X, Zhou H, Faiola F, Ding J, Haruehanroengra P, Yang F, Li D, Sanchez-Priego C, Saunders A, Pan F, Valdes VJ, Kelley K, Blanco MG, Chen L, Wang H, Sheng J, Xu M, Fidalgo M, Shen X, Wang J (2018) RNA-dependent chromatin targeting of TET2 for endogenous retrovirus control in pluripotent stem cells. Nat Genet 50(3):443–451
pubmed: 29483655 pmcid: 5862756 doi: 10.1038/s41588-018-0060-9
Jiang X, Liu B, Nie Z, Duan L, Xiong Q, Jin Z, Yang C, Chen Y (2021) The role of m6A modification in the biological functions and diseases. Signal Transduct Target Ther 6(1):74
pubmed: 33611339 pmcid: 7897327 doi: 10.1038/s41392-020-00450-x
Je L, Li K, Cai J, Zhang M, Zhang X, Xiong X, Meng H, Xu X, Huang Z, Peng J, Fan J, Yi C (2020) Landscape and regulation of m6A and m6Am methylome across human and mouse tissues. Mol Cell 77(2):426-440.e426
doi: 10.1016/j.molcel.2019.09.032
Zaccara S, Jaffrey SR (2020) A unified model for the function of YTHDF proteins in regulating m6A-modified mRNA. Cell 181(7):1582-1595.e1518
pubmed: 32492408 pmcid: 7508256 doi: 10.1016/j.cell.2020.05.012
Ginhoux F, Jung S (2014) Monocytes and macrophages: developmental pathways and tissue homeostasis. Nat Rev Immunol 14(6):392–404
pubmed: 24854589 doi: 10.1038/nri3671
Pollard JW (2009) Trophic macrophages in development and disease. Nat Rev Immunol 9(4):259–270
pubmed: 19282852 pmcid: 3648866 doi: 10.1038/nri2528
Park MD, Silvin A, Ginhoux F, Merad M (2022) Macrophages in health and disease. Cell 185(23):4259–4279
pubmed: 36368305 pmcid: 9908006 doi: 10.1016/j.cell.2022.10.007
Yin H, Zhang X, Yang P, Zhang X, Peng Y, Li D, Yu Y, Wu Y, Wang Y, Zhang J, Ding X, Wang X, Yang A, Zhang R (2021) RNA m6A methylation orchestrates cancer growth and metastasis via macrophage reprogramming. Nat Commun 12(1):1394
pubmed: 33654093 pmcid: 7925544 doi: 10.1038/s41467-021-21514-8
Tong J, Wang X, Liu Y, Ren X, Wang A, Chen Z, Yao J, Mao K, Liu T, Meng F-L, Pan W, Zou Q, Liu J, Zhou Y, Xia Q, Flavell RA, Zhu S, Li H-B (2021) Pooled CRISPR screening identifies m6A as a positive regulator of macrophage activation. Sci Adv 7(18):eabd4742
pubmed: 33910903 pmcid: 8081357 doi: 10.1126/sciadv.abd4742
Lee J-H, Wang R, Xiong F, Krakowiak J, Liao Z, Nguyen PT, Moroz-Omori EV, Shao J, Zhu X, Bolt MJ, Wu H, Singh PK, Bi M, Shi CJ, Jamal N, Li G, Mistry R, Jung SY, Tsai K-L, Ferreon JC, Stossi F, Caflisch A, Liu Z, Mancini MA, Li W (2021) Enhancer RNA m6A methylation facilitates transcriptional condensate formation and gene activation. Mol Cell 81(16):3368-3385.e3369
pubmed: 34375583 pmcid: 8383322 doi: 10.1016/j.molcel.2021.07.024
Chelmicki T, Roger E, Teissandier A, Dura M, Bonneville L, Rucli S, Dossin F, Fouassier C, Lameiras S, Bourc’his D, (2021) m6A RNA methylation regulates the fate of endogenous retroviruses. Nature 591(7849):312–316
pubmed: 33442060 doi: 10.1038/s41586-020-03135-1
Xu W, Li J, He C, Wen J, Ma H, Rong B, Diao J, Wang L, Wang J, Wu F, Tan L, Shi YG, Shi Y, Shen H (2021) METTL3 regulates heterochromatin in mouse embryonic stem cells. Nature 591(7849):317–321
pubmed: 33505026 doi: 10.1038/s41586-021-03210-1
McClatchy J, Strogantsev R, Wolfe E, Lin HY, Mohammadhosseini M, Davis BA, Eden C, Goldman D, Fleming WH, Conley P, Wu G, Cimmino L, Mohammed H, Agarwal A (2023) Clonal hematopoiesis related TET2 loss-of-function impedes IL1β-mediated epigenetic reprogramming in hematopoietic stem and progenitor cells. Nat Commun 14(1):8102
pubmed: 38062031 pmcid: 10703894 doi: 10.1038/s41467-023-43697-y
Marshall LL, Killinger BA, Ensink E, Li P, Li KX, Cui W, Lubben N, Weiland M, Wang X, Gordevicius J, Coetzee GA, Ma J, Jovinge S, Labrie V (2020) Epigenomic analysis of Parkinson’s disease neurons identifies Tet2 loss as neuroprotective. Nat Neurosci 23(10):1203–1214
pubmed: 32807949 doi: 10.1038/s41593-020-0690-y
Chou W-C, Chou S-C, Liu C-Y, Chen C-Y, Hou H-A, Kuo Y-Y, Lee M-C, Ko B-S, Tang J-L, Yao M, Tsay W, Wu S-J, Huang S-Y, Hsu S-C, Chen Y-C, Chang Y-C, Kuo Y-Y, Kuo K-T, Lee F-Y, Liu M-C, Liu C-W, Tseng M-H, Huang C-F, Tien H-F (2011) TET2 mutation is an unfavorable prognostic factor in acute myeloid leukemia patients with intermediate-risk cytogenetics. Blood 118(14):3803–3810
pubmed: 21828143 doi: 10.1182/blood-2011-02-339747
Daigneault M, Preston JA, Marriott HM, Whyte MKB, Dockrell DH (2010) The identification of markers of macrophage differentiation in PMA-stimulated THP-1 cells and monocyte-derived macrophages. PLoS ONE 5(1):e8668
pubmed: 20084270 pmcid: 2800192 doi: 10.1371/journal.pone.0008668
Genin M, Clement F, Fattaccioli A, Raes M, Michiels C (2015) M1 and M2 macrophages derived from THP-1 cells differentially modulate the response of cancer cells to etoposide. BMC Cancer 15(1):577
pubmed: 26253167 pmcid: 4545815 doi: 10.1186/s12885-015-1546-9
Green ID, Pinello N, Song R, Lee Q, Halstead James M, Kwok C-T, Wong ACH, Nair SS, Clark Susan J, Roediger B, Schmitz U, Larance M, Hayashi R, Rasko John EJ, Wong JJL (2020) Macrophage development and activation involve coordinated intron retention in key inflammatory regulators. Nucleic Acids Res 48(12):6513–6529
pubmed: 32449925 pmcid: 7337907 doi: 10.1093/nar/gkaa435
Madhvi A, Mishra H, Leisching GR, Mahlobo PZ, Baker B (2019) Comparison of human monocyte derived macrophages and THP1-like macrophages as in vitro models for M. tuberculosis infection. Compar Immunol Microbiol Infect Diseases 67:101355
doi: 10.1016/j.cimid.2019.101355
Lee Q, Song R, Phan DAV, Pinello N, Tieng J, Su A, Halstead JM, Wong ACH, van Geldermalsen M, Lee BSL, Rong B, Cook KM, Larance M, Liu R, Lan F, Tiffen JC, Wong JJL (2023) Overexpression of VIRMA confers vulnerability to breast cancers via the m6A-dependent regulation of unfolded protein response. Cell Mol Life Sci 80(6):157
pubmed: 37208522 pmcid: 10198946 doi: 10.1007/s00018-023-04799-4
Yoshikawa H, Larance M, Harney DJ, Sundaramoorthy R, Ly T, Owen-Hughes T, Lamond AI (2018) Efficient analysis of mammalian polysomes in cells and tissues using Ribo Mega-SEC. Elife 7:e36530
pubmed: 30095066 pmcid: 6086667 doi: 10.7554/eLife.36530
Zeng Y, Wang S, Gao S, Soares F, Ahmed M, Guo H, Wang M, Hua JT, Guan J, Moran MF, Tsao MS, He HH (2018) Refined RIP-seq protocol for epitranscriptome analysis with low input materials. PLoS Biol 16(9):e2006092
pubmed: 30212448 pmcid: 6136692 doi: 10.1371/journal.pbio.2006092
Ratnadiwakara M, Änkö M-L (2018) mRNA stability assay using transcription inhibition by actinomycin D in mouse pluripotent stem cells. Bio-Protoc 8(21):e3072
pubmed: 34532533 pmcid: 8342049
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30(15):2114–2120
pubmed: 24695404 pmcid: 4103590 doi: 10.1093/bioinformatics/btu170
Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR (2013) STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29(1):15–21
pubmed: 23104886 doi: 10.1093/bioinformatics/bts635
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Subgroup GPDP (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25(16):2078–2079
pubmed: 19505943 pmcid: 2723002 doi: 10.1093/bioinformatics/btp352
Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, Liu XS (2008) Model-based Analysis of ChIP-Seq (MACS). Genome Biol 9(9):R137
pubmed: 18798982 pmcid: 2592715 doi: 10.1186/gb-2008-9-9-r137
Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, Cheng JX, Murre C, Singh H, Glass CK (2010) Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell 38(4):576–589
pubmed: 20513432 pmcid: 2898526 doi: 10.1016/j.molcel.2010.05.004
Quinlan AR, Hall IM (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26(6):841–842
pubmed: 20110278 pmcid: 2832824 doi: 10.1093/bioinformatics/btq033
Crooks GE, Hon G, Chandonia J-M, Brenner SE (2004) WebLogo: A sequence logo generator. Genome Res 14(6):1188–1190
pubmed: 15173120 pmcid: 419797 doi: 10.1101/gr.849004
Cui X, Wei Z, Zhang L, Liu H, Sun L, Zhang S-W, Huang Y, Meng J (2016) Guitar: An R/Bioconductor package for gene annotation guided transcriptomic analysis of RNA-related genomic features. Biomed Res Int 2016:8367534
pubmed: 27239475 pmcid: 4864564 doi: 10.1155/2016/8367534
Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15(12):550
pubmed: 25516281 pmcid: 4302049 doi: 10.1186/s13059-014-0550-8
Yu G, Wang L-G, Han Y, He Q-Y (2012) clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS 16(5):284–287
pubmed: 22455463 pmcid: 3339379 doi: 10.1089/omi.2011.0118
Liao Y, Smyth GK, Shi W (2014) featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30(7):923–930
pubmed: 24227677 doi: 10.1093/bioinformatics/btt656
Pinello N, Song R, Lee Q, Calonne E, Larance M, Fuks F, Wong JJL (2024) A multiomics dataset for the study of RNA modifications in human macrophage differentiation and polarisation. Scientific Data 11(1):252
pubmed: 38418823 pmcid: 10902381 doi: 10.1038/s41597-024-03076-8
Seim GL, Britt EC, John SV, Yeo FJ, Johnson AR, Eisenstein RS, Pagliarini DJ, Fan J (2019) Two-stage metabolic remodelling in macrophages in response to lipopolysaccharide and interferon-γ stimulation. Nat Metab 1(7):731–742
pubmed: 32259027 pmcid: 7108803 doi: 10.1038/s42255-019-0083-2
Forrester MA, Wassall HJ, Hall LS, Cao H, Wilson HM, Barker RN, Vickers MA (2018) Similarities and differences in surface receptor expression by THP-1 monocytes and differentiated macrophages polarized using seven different conditioning regimens. Cell Immunol 332:58–76
pubmed: 30077333 pmcid: 7611637 doi: 10.1016/j.cellimm.2018.07.008
Kimura Y, Inoue A, Hangai S, Saijo S, Negishi H, Nishio J, Yamasaki S, Iwakura Y, Yanai H, Taniguchi T (2016) The innate immune receptor Dectin-2 mediates the phagocytosis of cancer cells by Kupffer cells for the suppression of liver metastasis. Proc Natl Acad Sci 113(49):14097–14102
pubmed: 27872290 pmcid: 5150405 doi: 10.1073/pnas.1617903113
Park EK, Jung HS, Yang HI, Yoo MC, Kim C, Kim KS (2007) Optimized THP-1 differentiation is required for the detection of responses to weak stimuli. Inflamm Res 56(1):45–50
pubmed: 17334670 doi: 10.1007/s00011-007-6115-5
Reales-Calderón JA, Aguilera-Montilla N, Corbí ÁL, Molero G, Gil C (2014) Proteomic characterization of human proinflammatory M1 and anti-inflammatory M2 macrophages and their response to Candida albicans. Proteomics 14(12):1503–1518
pubmed: 24687989 doi: 10.1002/pmic.201300508
Tedesco S, De Majo F, Kim J, Trenti A, Trevisi L, Fadini GP, Bolego C, Zandstra PW, Cignarella A, Vitiello L (2018) Convenience versus biological significance: are PMA-differentiated THP-1 cells a reliable substitute for blood-derived macrophages when studying in vitro polarization? Front Pharmacol 9:71
pubmed: 29520230 pmcid: 5826964 doi: 10.3389/fphar.2018.00071
Dominissini D, Moshitch-Moshkovitz S, Schwartz S, Salmon-Divon M, Ungar L, Osenberg S, Cesarkas K, Jacob-Hirsch J, Amariglio N, Kupiec M, Sorek R, Rechavi G (2012) Topology of the human and mouse m6A RNA methylomes revealed by m6A-seq. Nature 485(7397):201–206
pubmed: 22575960 doi: 10.1038/nature11112
Huang H, Weng H, Zhou K, Wu T, Zhao BS, Sun M, Chen Z, Deng X, Xiao G, Auer F, Klemm L, Wu H, Zuo Z, Qin X, Dong Y, Zhou Y, Qin H, Tao S, Du J, Liu J, Lu Z, Yin H, Mesquita A, Yuan CL, Hu Y-C, Sun W, Su R, Dong L, Shen C, Li C, Qing Y, Jiang X, Wu X, Sun M, Guan J-L, Qu L, Wei M, Müschen M, Huang G, He C, Yang J, Chen J (2019) Histone H3 trimethylation at lysine 36 guides m6A RNA modification co-transcriptionally. Nature 567(7748):414–419
pubmed: 30867593 pmcid: 6438714 doi: 10.1038/s41586-019-1016-7
Li Y, Xia L, Tan K, Ye X, Zuo Z, Li M, Xiao R, Wang Z, Liu X, Deng M, Cui J, Yang M, Luo Q, Liu S, Cao X, Zhu H, Liu T, Hu J, Shi J, Xiao S, Xia L (2020) N6-Methyladenosine co-transcriptionally directs the demethylation of histone H3K9me2. Nat Genet 52(9):870–877
pubmed: 32778823 doi: 10.1038/s41588-020-0677-3
Meyer Kate D, Patil Deepak P, Zhou J, Zinoviev A, Skabkin Maxim A, Elemento O, Pestova Tatyana V, Qian S-B, Jaffrey Samie R (2015) 5′UTR m6A promotes cap-independent translation. Cell 163(4):999–1010
pubmed: 26593424 pmcid: 4695625 doi: 10.1016/j.cell.2015.10.012
Zhou J, Wan J, Gao X, Zhang X, Jaffrey SR, Qian S-B (2015) Dynamic m6A mRNA methylation directs translational control of heat shock response. Nature 526(7574):591–594
pubmed: 26458103 pmcid: 4851248 doi: 10.1038/nature15377
Liu L, Lu Y, Martinez J, Bi Y, Lian G, Wang T, Milasta S, Wang J, Yang M, Liu G, Green DR, Wang R (2016) Proinflammatory signal suppresses proliferation and shifts macrophage metabolism from Myc-dependent to HIF1α-dependent. Proc Natl Acad Sci 113(6):1564–1569
pubmed: 26811453 pmcid: 4760828 doi: 10.1073/pnas.1518000113
Liu T, Zhang L, Joo D, Sun S-C (2017) NF-κB signaling in inflammation. Signal Transduct Target Ther 2(1):17023
pubmed: 29158945 pmcid: 5661633 doi: 10.1038/sigtrans.2017.23
Salim T, Sershen CL, May EE (2016) Investigating the role of TNF-α and IFN-γ activation on the dynamics of iNOS gene expression in LPS stimulated macrophages. PLoS ONE 11(6):e0153289
pubmed: 27276061 pmcid: 4898755 doi: 10.1371/journal.pone.0153289
Takeuchi O, Akira S (2010) Pattern recognition receptors and inflammation. Cell 140(6):805–820
pubmed: 20303872 doi: 10.1016/j.cell.2010.01.022
Kimura T, Nada S, Takegahara N, Okuno T, Nojima S, Kang S, Ito D, Morimoto K, Hosokawa T, Hayama Y, Mitsui Y, Sakurai N, Sarashina-Kida H, Nishide M, Maeda Y, Takamatsu H, Okuzaki D, Yamada M, Okada M, Kumanogoh A (2016) Polarization of M2 macrophages requires Lamtor1 that integrates cytokine and amino-acid signals. Nat Commun 7(1):13130
pubmed: 27731330 pmcid: 5064021 doi: 10.1038/ncomms13130
Martinez P, Denys A, Delos M, Sikora A-S, Carpentier M, Julien S, Pestel J, Allain F (2015) Macrophage polarization alters the expression and sulfation pattern of glycosaminoglycans. Glycobiology 25(5):502–513
pubmed: 25504800 doi: 10.1093/glycob/cwu137
Rao Z, Pace S, Jordan PM, Bilancia R, Troisi F, Börner F, Andreas N, Kamradt T, Menche D, Rossi A, Serhan CN, Gerstmeier J, Werz O (2019) Vacuolar (H+)-ATPase critically regulates apecialized proresolving mediator pathways in human M2-like monocyte-derived macrophages and has a crucial role in resolution of inflammation. J Immunol 203(4):1031–1043
pubmed: 31300512 doi: 10.4049/jimmunol.1900236
Wu M-Y, Lu J-H (2020) Autophagy and macrophage functions: Inflammatory response and phagocytosis. Cells 9(1):70
doi: 10.3390/cells9010070
Pixley FJ, Stanley ER (2004) CSF-1 regulation of the wandering macrophage: complexity in action. Trends Cell Biol 14(11):628–638
pubmed: 15519852 doi: 10.1016/j.tcb.2004.09.016
Gudgeon J, Marín-Rubio JL, Trost M (2022) The role of macrophage scavenger receptor 1 (MSR1) in inflammatory disorders and cancer. Front Immunol 13:1012002
pubmed: 36325338 pmcid: 9618966 doi: 10.3389/fimmu.2022.1012002
Silverstein RL, Febbraio M (2009) CD36 a scavenger receptor involved in immunity, metabolism, angiogenesis, and behavior. Sci Signal 2(72):re3
pubmed: 19471024 pmcid: 2811062 doi: 10.1126/scisignal.272re3
Beutler B (2000) Tlr4: central component of the sole mammalian LPS sensor. Curr Opin Immunol 12(1):20–26
pubmed: 10679411 doi: 10.1016/S0952-7915(99)00046-1
Wiesolek HL, Bui TM, Lee JJ, Dalal P, Finkielsztein A, Batra A, Thorp EB, Sumagin R (2020) Intercellular adhesion molecule 1 functions as an efferocytosis receptor in inflammatory macrophages. Am J Pathol 190(4):874–885
pubmed: 32035057 pmcid: 7180595 doi: 10.1016/j.ajpath.2019.12.006
Meli VS, Atcha H, Veerasubramanian PK, Nagalla RR, Luu TU, Chen EY, Guerrero-Juarez CF, Yamaga K, Pandori W, Hsieh JY, Downing TL, Fruman DA, Lodoen MB, Plikus MV, Wang W, Liu WF (2020) YAP-mediated mechanotransduction tunes the macrophage inflammatory response. Sci Adv 6(49):eabb8471
pubmed: 33277245 pmcid: 7717914 doi: 10.1126/sciadv.abb8471
Fabriek BO, van Bruggen R, Deng DM, Ligtenberg AJM, Nazmi K, Schornagel K, Vloet RPM, Dijkstra CD, van den Berg TK (2009) The macrophage scavenger receptor CD163 functions as an innate immune sensor for bacteria. Blood 113(4):887–892
pubmed: 18849484 doi: 10.1182/blood-2008-07-167064
Relloso M, Puig-Kröger A, Pello OMi, Rodríguez-Fernández JL, de la Rosa G, Longo N, Navarro Jn, Muñoz-Fernández MA, Sánchez-Mateos P, Corbí AL, (2002) DC-SIGN (CD209) expression Is IL-4 dependent and is negatively regulated by IFN, TGF-β, and anti-Inflammatory agents. J Immunol 168(6):2634–2643
pubmed: 11884427 doi: 10.4049/jimmunol.168.6.2634
Schnoor M, Cullen P, Lorkowski J, Stolle K, Robenek H, Troyer D, Lorkowski RS (2008) Production of Type VI collagen by human macrophages: A new dimension in macrophage Functional heterogeneity. J Immunol 180(8):5707–5719
pubmed: 18390756 doi: 10.4049/jimmunol.180.8.5707
Zhang D-E, Hetherington CJ, Chen H-M, Tenen DG (1994) The macrophage transcription factor PU.1 directs tissue-specific expression of the macrophage colony-stimulating factor receptor. Mol Cell Biol 14(1):373–381
pubmed: 8264604 pmcid: 358386
Audesse AJ, Dhakal S, Hassell L-A, Gardell Z, Nemtsova Y, Webb AE (2019) FOXO3 directly regulates an autophagy network to functionally regulate proteostasis in adult neural stem cells. PLoS Genet 15(4):e1008097
pubmed: 30973875 pmcid: 6478346 doi: 10.1371/journal.pgen.1008097
de Bruin RG, Shiue L, Prins J, de Boer HC, Singh A, Fagg WS, van Gils JM, Duijs JMGJ, Katzman S, Kraaijeveld AO, Böhringer S, Leung WY, Kielbasa SM, Donahue JP, van der Zande PHJ, Sijbom R, van Alem CMA, Bot I, van Kooten C, Jukema JW, Van Esch H, Rabelink TJ, Kazan H, Biessen EAL, Ares M Jr, van Zonneveld AJ, van der Veer EP (2016) Quaking promotes monocyte differentiation into pro-atherogenic macrophages by controlling pre-mRNA splicing and gene expression. Nat Commun 7(1):10846
pubmed: 27029405 pmcid: 4821877 doi: 10.1038/ncomms10846
Richter E, Ventz K, Harms M, Mostertz J, Hochgräfe F (2016) Induction of macrophage function in human THP-1 cells is associated with rewiring of MAPK signaling and activation of MAP3K7 (TAK1) protein kinase. Front Cell Develop Biol 4:21
doi: 10.3389/fcell.2016.00021
Zhang Y, Choksi S, Chen K, Pobezinskaya Y, Linnoila I, Liu Z-G (2013) ROS play a critical role in the differentiation of alternatively activated macrophages and the occurrence of tumor-associated macrophages. Cell Res 23(7):898–914
pubmed: 23752925 pmcid: 3698641 doi: 10.1038/cr.2013.75
Marriott HM, Bingle CD, Read RC, Braley KE, Kroemer G, Hellewell PG, Craig RW, Whyte MKB, Dockrell DH (2005) Dynamic changes in Mcl-1 expression regulate macrophage viability or commitment to apoptosis during bacterial clearance. J Clin Investig 115(2):359–368
pubmed: 15650769 pmcid: 544034 doi: 10.1172/JCI200521766
Grainger DJ, Reckless J, McKilligin E (2004) Apolipoprotein E modulates clearance of apoptotic bodies in vitro and in vivo, resulting in a systemic proinflammatory state in apolipoprotein E-deficient mice. J Immunol 173(10):6366–6375
pubmed: 15528376 doi: 10.4049/jimmunol.173.10.6366
Gratchev A, Guillot P, Hakiy N, Politz O, Orfanos CE, Schledzewski K, Goerdt S (2001) Alternatively activated macrophages differentially express fibronectin and its splice variants and the extracellular matrix protein βIG-H3. Scand J Immunol 53(4):386–392
pubmed: 11285119 doi: 10.1046/j.1365-3083.2001.00885.x
Mor-Vaknin N, Punturieri A, Sitwala K, Markovitz DM (2003) Vimentin is secreted by activated macrophages. Nat Cell Biol 5(1):59–63
pubmed: 12483219 doi: 10.1038/ncb898
Li A, Chen Y-S, Ping X-L, Yang X, Xiao W, Yang Y, Sun H-Y, Zhu Q, Baidya P, Wang X, Bhattarai DP, Zhao Y-L, Sun B-F, Yang Y-G (2017) Cytoplasmic m6A reader YTHDF3 promotes mRNA translation. Cell Res 27(3):444–447
pubmed: 28106076 pmcid: 5339832 doi: 10.1038/cr.2017.10
Wilinski D, Dus M (2023) N6-adenosine methylation controls the translation of insulin mRNA. Nat Struct Mol Biol 30(9):1260–1264
pubmed: 37488356 doi: 10.1038/s41594-023-01048-x
Chen L-L, Morcelle C, Cheng Z-L, Chen X, Xu Y, Gao Y, Song J, Li Z, Smith MD, Shi M, Zhu Y, Zhou N, Cheng M, He C, Liu KY, Lu G, Zhang L, Zhang C, Zhang J, Sun Y, Qi T, Lyu Y, Ren Z-Z, Tan X-M, Yin J, Lan F, Liu Y, Yang H, Qian M, Duan C, Chang X, Zhou Y, Shen L, Baldwin AS, Guan K-L, Xiong Y, Ye D (2022) Itaconate inhibits TET DNA dioxygenases to dampen inflammatory responses. Nat Cell Biol 24(3):353–363
pubmed: 35256775 pmcid: 9305987 doi: 10.1038/s41556-022-00853-8
Alver BH, Kim KH, Lu P, Wang X, Manchester HE, Wang W, Haswell JR, Park PJ, Roberts CWM (2017) The SWI/SNF chromatin remodelling complex is required for maintenance of lineage specific enhancers. Nat Commun 8(1):14648
pubmed: 28262751 pmcid: 5343482 doi: 10.1038/ncomms14648
Han L, Madan V, Mayakonda A, Dakle P, Teoh WW, Shyamsunder P, Nordin HBM, Cao Z, Sundaresan J, Lei I, Wang Z, Koeffler HP (2018) ARID1A is critical for maintaining normal hematopoiesis in mice. Blood 132:3833
doi: 10.1182/blood-2018-99-117993
Hu Y, Wang X, Song J, Wu J, Xu J, Chai Y, Ding Y, Wang B, Wang C, Zhao Y, Shen Z, Xu X, Cao X (2021) Chromatin remodeler ARID1A binds IRF3 to selectively induce antiviral interferon production in macrophages. Cell Death Dis 12(8):743
pubmed: 34315861 pmcid: 8316351 doi: 10.1038/s41419-021-04032-9
Liu Z, Jiang Y, Li Y, Wang J, Fan L, Scott MJ, Xiao G, Li S, Billiar TR, Wilson MA, Fan J (2013) TLR4 signaling augments monocyte chemotaxis by regulating G protein–coupled receptor kinase 2 translocation. J Immunol 191(2):857–864
pubmed: 23772028 doi: 10.4049/jimmunol.1300790
Patial S, Saini Y, Parvataneni S, Appledorn DM, Dorn Ii GW, LaPres JJ, Amalfitano A, Senagore P, Parameswaran N (2011) Myeloid-specific GPCR kinase-2 negatively regulates NF-κB1p105-ERK pathway and limits endotoxemic shock in mice. J Cell Physiol 226(3):627–637
pubmed: 20717897 pmcid: 3013243 doi: 10.1002/jcp.22384
Lin S, Choe J, Du P, Triboulet R, Gregory Richard I (2016) The m6A methyltransferase METTL3 promotes translation in human cancer cells. Mol Cell 62(3):335–345
pubmed: 27117702 pmcid: 4860043 doi: 10.1016/j.molcel.2016.03.021
Zhao Y, Chen Y, Jin M, Wang J (2021) The crosstalk between m6A RNA methylation and other epigenetic regulators: a novel perspective in epigenetic remodeling. Theranostics 11(9):4549–4566
pubmed: 33754077 pmcid: 7977459 doi: 10.7150/thno.54967
Courtney David G, Chalem A, Bogerd Hal P, Law Brittany A, Kennedy Edward M, Holley Christopher L, Cullen Bryan R (2019) Extensive epitranscriptomic methylation of A and C residues on murine leukemia virus transcripts enhances viral gene expression. MBio. https://doi.org/10.1128/mbio.01209-01219
doi: 10.1128/mbio.01209-01219 pubmed: 31186331 pmcid: 6561033
Li Q, Li X, Tang H, Jiang B, Dou Y, Gorospe M, Wang W (2017) NSUN2-mediated m5C methylation and METTL3/METTL14-mediated m6A methylation cooperatively enhance p21 translation. J Cell Biochem 118(9):2587–2598
pubmed: 28247949 pmcid: 5509477 doi: 10.1002/jcb.25957
Fu L, Guerrero CR, Zhong N, Amato NJ, Liu Y, Liu S, Cai Q, Ji D, Jin S-G, Niedernhofer LJ, Pfeifer GP, Xu G-L, Wang Y (2014) Tet-mediated formation of 5-hydroxymethylcytosine in RNA. J Am Chem Soc 136(33):11582–11585
pubmed: 25073028 pmcid: 4140497 doi: 10.1021/ja505305z
Cull AH, Snetsinger B, Buckstein R, Wells RA, Rauh MJ (2017) Tet2 restrains inflammatory gene expression in macrophages. Exp Hematol 55:56-70.e13
pubmed: 28826859 doi: 10.1016/j.exphem.2017.08.001
Onodera A, González-Avalos E, Lio C-WJ, Georges RO, Bellacosa A, Nakayama T, Rao A (2021) Roles of TET and TDG in DNA demethylation in proliferating and non-proliferating immune cells. Genome Biol 22(1):186
pubmed: 34158086 pmcid: 8218415 doi: 10.1186/s13059-021-02384-1
Sun F, Abreu-Rodriguez I, Ye S, Gay S, Distler O, Neidhart M, Karouzakis E (2019) TET1 is an important transcriptional activator of TNFα expression in macrophages. PLoS ONE 14(6):e0218551
pubmed: 31216336 pmcid: 6583962 doi: 10.1371/journal.pone.0218551
Deng S, Zhang J, Su J, Zuo Z, Zeng L, Liu K, Zheng Y, Huang X, Bai R, Zhuang L, Ye Y, Li M, Pan L, Deng J, Wu G, Li R, Zhang S, Wu C, Lin D, Chen J, Zheng J (2022) RNA m6A regulates transcription via DNA demethylation and chromatin accessibility. Nat Genet 54(9):1427–1437
pubmed: 36071173 doi: 10.1038/s41588-022-01173-1
Shi H, Wei J, He C (2019) Where, when, and how: Context-dependent functions of RNA methylation writers, readers, and erasers. Mol Cell 74(4):640–650
pubmed: 31100245 pmcid: 6527355 doi: 10.1016/j.molcel.2019.04.025
Lin EY, Nguyen AV, Russell RG, Pollard JW (2001) Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy. J Exp Med 193(6):727–740
pubmed: 11257139 pmcid: 2193412 doi: 10.1084/jem.193.6.727
Wan S, Zhao E, Kryczek I, Vatan L, Sadovskaya A, Ludema G, Simeone DM, Zou W, Welling TH (2014) Tumor-associated macrophages produce interleukin 6 and signal via STAT3 to promote expansion of human hepatocellular carcinoma stem cells. Gastroenterology 147(6):1393–1404
pubmed: 25181692 doi: 10.1053/j.gastro.2014.08.039
Hughes R, Qian B-Z, Rowan C, Muthana M, Keklikoglou I, Olson OC, Tazzyman S, Danson S, Addison C, Clemons M, Gonzalez-Angulo AM, Joyce JA, De Palma M, Pollard JW, Lewis CE (2015) Perivascular M2 macrophages stimulate tumor relapse after chemotherapy. Can Res 75(17):3479–3491
doi: 10.1158/0008-5472.CAN-14-3587
Casanova-Acebes M, Dalla E, Leader AM, LeBerichel J, Nikolic J, Morales BM, Brown M, Chang C, Troncoso L, Chen ST, Sastre-Perona A, Park MD, Tabachnikova A, Dhainaut M, Hamon P, Maier B, Sawai CM, Agulló-Pascual E, Schober M, Brown BD, Reizis B, Marron T, Kenigsberg E, Moussion C, Benaroch P, Aguirre-Ghiso JA, Merad M (2021) Tissue-resident macrophages provide a pro-tumorigenic niche to early NSCLC cells. Nature 595(7868):578–584
pubmed: 34135508 pmcid: 8923521 doi: 10.1038/s41586-021-03651-8
Moore KJ, Sheedy FJ, Fisher EA (2013) Macrophages in atherosclerosis: a dynamic balance. Nat Rev Immunol 13(10):709–721
pubmed: 23995626 pmcid: 4357520 doi: 10.1038/nri3520
Jun H-S, Yoon C-S, Zbytnuik L, van Rooijen N, Yoon J-W (1999) The role of macrophages in T Cell–mediated autoimmune diabetes in nonobese diabetic mice. J Exp Med 189(2):347–358
pubmed: 9892617 pmcid: 2192977 doi: 10.1084/jem.189.2.347
Udalova IA, Mantovani A, Feldmann M (2016) Macrophage heterogeneity in the context of rheumatoid arthritis. Nat Rev Rheumatol 12(8):472–485
pubmed: 27383913 doi: 10.1038/nrrheum.2016.91
Zhang H, Cai D, Bai X (2020) Macrophages regulate the progression of osteoarthritis. Osteoarth Cartil 28(5):555–561
doi: 10.1016/j.joca.2020.01.007
Wilson C, Chen PJ, Miao Z, Liu DR (2020) Programmable m6A modification of cellular RNAs with a Cas13-directed methyltransferase. Nat Biotechnol 38(12):1431–1440
pubmed: 32601430 pmcid: 7718427 doi: 10.1038/s41587-020-0572-6
Shi H, Xu Y, Tian N, Yang M, Liang F-S (2022) Inducible and reversible RNA N6-methyladenosine editing. Nat Commun 13(1): 1958

Auteurs

Natalia Pinello (N)

Faculty of Medicine and Health, The University of Sydney, Camperdown, 2050, Australia.
Epigenetics and RNA Biology Program Centenary Institute, The University of Sydney, Camperdown, 2050, Australia.
Functional Genomics Laboratory, Institut Pasteur de Montevideo, 11400, Montevideo, Uruguay.

Renhua Song (R)

Faculty of Medicine and Health, The University of Sydney, Camperdown, 2050, Australia.
Epigenetics and RNA Biology Program Centenary Institute, The University of Sydney, Camperdown, 2050, Australia.

Quintin Lee (Q)

Faculty of Medicine and Health, The University of Sydney, Camperdown, 2050, Australia.
Epigenetics and RNA Biology Program Centenary Institute, The University of Sydney, Camperdown, 2050, Australia.

Emilie Calonne (E)

Laboratory of Cancer Epigenetics, Faculty of Medicine, ULB Cancer Research Center (U-CRC), Jules Bordet Institute, Université Libre de Bruxelles (ULB), Brussels, Belgium.

Kun-Long Duan (KL)

The Molecular and Cell Biology Lab, Key Laboratory of Medical Epigenetics and Metabolism, Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University, Shanghai, China.

Emilie Wong (E)

Faculty of Medicine and Health, The University of Sydney, Camperdown, 2050, Australia.
Epigenetics and RNA Biology Program Centenary Institute, The University of Sydney, Camperdown, 2050, Australia.

Jessica Tieng (J)

Faculty of Medicine and Health, The University of Sydney, Camperdown, 2050, Australia.
Epigenetics and RNA Biology Program Centenary Institute, The University of Sydney, Camperdown, 2050, Australia.

Majid Mehravar (M)

Faculty of Medicine and Health, The University of Sydney, Camperdown, 2050, Australia.
Epigenetics and RNA Biology Program Centenary Institute, The University of Sydney, Camperdown, 2050, Australia.

Bowen Rong (B)

Shanghai Key Laboratory of Medical Epigenetics, International Co-Laboratory of Medical Epigenetics and Metabolism, Ministry of Science and Technology, Institutes of Biomedical Sciences, and Key Laboratory of Carcinogenesis and Cancer Invasion, Ministry of Education, Liver Cancer Institute, Zhongshan Hospital, Fudan University, Shanghai, 200032, China.

Fei Lan (F)

Shanghai Key Laboratory of Medical Epigenetics, International Co-Laboratory of Medical Epigenetics and Metabolism, Ministry of Science and Technology, Institutes of Biomedical Sciences, and Key Laboratory of Carcinogenesis and Cancer Invasion, Ministry of Education, Liver Cancer Institute, Zhongshan Hospital, Fudan University, Shanghai, 200032, China.

Ben Roediger (B)

Faculty of Medicine and Health, The University of Sydney, Camperdown, 2050, Australia.
Skin Inflammation Group, Centenary Institute, The University of Sydney, Camperdown, 2050, Australia.
Autoimmunity, Transplantation and Inflammation (ATI) Disease Area, Novartis Institutes for BioMedical Research, Basel, Switzerland.

Cheng-Jie Ma (CJ)

School of Public Health, Wuhan University, Wuhan, 430071, China.

Bi-Feng Yuan (BF)

School of Public Health, Wuhan University, Wuhan, 430071, China.

John E J Rasko (JEJ)

Faculty of Medicine and Health, The University of Sydney, Camperdown, 2050, Australia.
Gene and Stem Cell Therapy Program, Centenary Institute, The University of Sydney, Camperdown, 2050, Australia.
Cell and Molecular Therapies, Royal Prince Alfred Hospital, Camperdown, 2050, NSW, Australia.

Mark Larance (M)

Faculty of Medicine and Health, The University of Sydney, Camperdown, 2050, Australia.
Charles Perkins Centre, School of Medical Sciences, University of Sydney, Sydney, 2006, Australia.

Dan Ye (D)

The Molecular and Cell Biology Lab, Key Laboratory of Medical Epigenetics and Metabolism, Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University, Shanghai, China.

François Fuks (F)

Laboratory of Cancer Epigenetics, Faculty of Medicine, ULB Cancer Research Center (U-CRC), Jules Bordet Institute, Université Libre de Bruxelles (ULB), Brussels, Belgium.

Justin J-L Wong (JJ)

Faculty of Medicine and Health, The University of Sydney, Camperdown, 2050, Australia. justin.wong@sydney.edu.au.
Epigenetics and RNA Biology Program Centenary Institute, The University of Sydney, Camperdown, 2050, Australia. justin.wong@sydney.edu.au.
Charles Perkins Centre, School of Medical Sciences, University of Sydney, Sydney, 2006, Australia. justin.wong@sydney.edu.au.

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

Classifications MeSH