PRMT5-mediated RNF4 methylation promotes therapeutic resistance of APL cells to As

Animals Antineoplastic Agents / pharmacology Arsenic Trioxide / pharmacology Cell Line, Tumor / drug effects Drug Resistance, Neoplasm / genetics Humans Isoquinolines / pharmacology Leukemia, Promyelocytic, Acute / drug therapy Methylation Mice Nuclear Proteins / genetics Oncogene Proteins, Fusion / genetics Protein-Arginine N-Methyltransferases / antagonists & inhibitors Pyrimidines / pharmacology Transcription Factors / genetics Ubiquitination
Acute promyelocytic leukemia Methylation PML-RARα PRMT5 RNF4 Ubiquitination

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:
27 May 2022
Historique:
received: 25 01 2022
accepted: 08 05 2022
revised: 23 04 2022
entrez: 27 5 2022
pubmed: 28 5 2022
medline: 1 6 2022
Statut: epublish

Résumé

Acute promyelocytic leukemia (APL) is a hematological malignancy driven by the oncoprotein PML-RARα, which can be treated with arsenic trioxide (As

Identifiants

DOI: 10.1007/s00018-022-04358-3 PMID: 35622143
pubmed: 35622143
doi: 10.1007/s00018-022-04358-3
pii: 10.1007/s00018-022-04358-3
doi:

Substances chimiques

Antineoplastic Agents 0
GSK3235025 0
Isoquinolines 0
Nuclear Proteins 0
Oncogene Proteins, Fusion 0
Pyrimidines 0
RNF4 protein, human 0
Transcription Factors 0
promyelocytic leukemia-retinoic acid receptor alpha fusion oncoprotein 0
PRMT5 protein, human EC 2.1.1.319
Protein-Arginine N-Methyltransferases EC 2.1.1.319
Arsenic Trioxide S7V92P67HO

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

319

Subventions

Organisme : National Natural Science Foundation of China
ID : 82130081
Organisme : National Natural Science Foundation of China
ID : 81730080
Organisme : Natural Science Foundation of Beijing Municipality
ID : 5212008

Informations de copyright

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

Références

de The H, Chen Z (2010) Acute promyelocytic leukaemia: novel insights into the mechanisms of cure. Nat Rev Cancer 10(11):775–783
pubmed: 20966922 doi: 10.1038/nrc2943
Burnett AK, Russell NH, Hills RK, Bowen D, Kell J, Knapper S et al (2015) Arsenic trioxide and all-trans retinoic acid treatment for acute promyelocytic leukaemia in all risk groups (AML17): results of a randomised, controlled, phase 3 trial. Lancet Oncol 16(13):1295–1305
pubmed: 26384238 doi: 10.1016/S1470-2045(15)00193-X
Strocchio L, Gurnari C, Santoro N, Putti MC, Micalizzi C, Zecca M et al (2019) Arsenic trioxide and all-trans retinoic acid treatment for childhood acute promyelocytic leukaemia. Br J Haematol 185(2):360–363
pubmed: 30028005 doi: 10.1111/bjh.15507
Lallemand-Breitenbach V, de The H (2010) PML nuclear bodies. Cold Spring Harb Perspect Biol 2(5):a000661
pubmed: 20452955 pmcid: 2857171 doi: 10.1101/cshperspect.a000661
Kwok C, Zeisig BB, Dong S, So CW (2006) Forced homo-oligomerization of RARalpha leads to transformation of primary hematopoietic cells. Cancer Cell 9(2):95–108
pubmed: 16473277 doi: 10.1016/j.ccr.2006.01.005
Martens JH, Brinkman AB, Simmer F, Francoijs KJ, Nebbioso A, Ferrara F et al (2010) PML-RARalpha/RXR alters the epigenetic landscape in acute promyelocytic leukemia. Cancer Cell 17(2):173–185
pubmed: 20159609 doi: 10.1016/j.ccr.2009.12.042
Kayser S, Schlenk RF, Platzbecker U (2018) Management of patients with acute promyelocytic leukemia. Leukemia 32(6):1277–1294
pubmed: 29743722 doi: 10.1038/s41375-018-0139-4
Coombs CC, Tavakkoli M, Tallman MS (2015) Acute promyelocytic leukemia: where did we start, where are we now, and the future. Blood Cancer J 5:e304
pubmed: 25885425 pmcid: 4450325 doi: 10.1038/bcj.2015.25
Lo-Coco F, Avvisati G, Vignetti M, Thiede C, Orlando SM, Iacobelli S et al (2013) Retinoic acid and arsenic trioxide for acute promyelocytic leukemia. N Engl J Med 369(2):111–121
pubmed: 23841729 doi: 10.1056/NEJMoa1300874
Lallemand-Breitenbach V, Zhu J, Chen Z, de The H (2012) Curing APL through PML/RARA degradation by As2O3. Trends Mol Med 18(1):36–42
pubmed: 22056243 doi: 10.1016/j.molmed.2011.10.001
Dos Santos GA, Kats L, Pandolfi PP (2013) Synergy against PML-RARa: targeting transcription, proteolysis, differentiation, and self-renewal in acute promyelocytic leukemia. J Exp Med 210(13):2793–2802
pubmed: 24344243 pmcid: 3865469 doi: 10.1084/jem.20131121
Tatham MH, Geoffroy MC, Shen L, Plechanovova A, Hattersley N, Jaffray EG et al (2008) RNF4 is a poly-SUMO-specific E3 ubiquitin ligase required for arsenic-induced PML degradation. Nat Cell Biol 10(5):538–546
pubmed: 18408734 doi: 10.1038/ncb1716
Lallemand-Breitenbach V, Jeanne M, Benhenda S, Nasr R, Lei M, Peres L et al (2008) Arsenic degrades PML or PML-RARalpha through a SUMO-triggered RNF4/ubiquitin-mediated pathway. Nat Cell Biol 10(5):547–555
pubmed: 18408733 doi: 10.1038/ncb1717
Lu Y, Yan JS, Xia L, Qin K, Yin QQ, Xu HT et al (2019) 2-Bromopalmitate targets retinoic acid receptor alpha and overcomes all-trans retinoic acid resistance of acute promyelocytic leukemia. Haematologica 104(1):102–112
pubmed: 30076181 pmcid: 6312026 doi: 10.3324/haematol.2018.191916
Gaut D, Sasine J, Schiller G (2018) Secondary clonal hematologic neoplasia following successful therapy for acute promyelocytic leukemia (APL): a report of two cases and review of the literature. Leuk Res Rep 9:65–71
pubmed: 29892552 pmcid: 5993360
Lehmann-Che J, Bally C, de The H (2014) Resistance to therapy in acute promyelocytic leukemia. N Engl J Med 371(12):1170–1172
pubmed: 25229938 doi: 10.1056/NEJMc1409040
Zhang X, Pan J (2017) Resistance to arsenic trioxide and retinoic acid therapy in acute promyelocytic leukemia. Ann Hematol 96(4):707–708
pubmed: 28154895 doi: 10.1007/s00277-017-2923-z
Zhu HH, Qin YZ, Huang XJ (2014) Resistance to arsenic therapy in acute promyelocytic leukemia. N Engl J Med 370(19):1864–1866
pubmed: 24806185 doi: 10.1056/NEJMc1316382
Smith E, Zhou W, Shindiapina P, Sif S, Li C, Baiocchi RA (2018) Recent advances in targeting protein arginine methyltransferase enzymes in cancer therapy. Expert Opin Ther Targets 22(6):527–545
pubmed: 29781349 pmcid: 6311705 doi: 10.1080/14728222.2018.1474203
Jarrold J, Davies CC (2019) PRMTs and arginine methylation: cancer’s best-kept secret? Trends Mol Med 25(11):993–1009
pubmed: 31230909 doi: 10.1016/j.molmed.2019.05.007
Pal S, Sif S (2007) Interplay between chromatin remodelers and protein arginine methyltransferases. J Cell Physiol 213(2):306–315
pubmed: 17708529 doi: 10.1002/jcp.21180
Blanc RS, Richard S (2017) Arginine methylation: the coming of age. Mol Cell 65(1):8–24
pubmed: 28061334 doi: 10.1016/j.molcel.2016.11.003
Yan F, Alinari L, Lustberg ME, Martin LK, Cordero-Nieves HM, Banasavadi-Siddegowda Y et al (2014) Genetic validation of the protein arginine methyltransferase PRMT5 as a candidate therapeutic target in glioblastoma. Cancer Res 74(6):1752–1765
pubmed: 24453002 pmcid: 3959215 doi: 10.1158/0008-5472.CAN-13-0884
Hu D, Gur M, Zhou Z, Gamper A, Hung MC, Fujita N et al (2015) Interplay between arginine methylation and ubiquitylation regulates KLF4-mediated genome stability and carcinogenesis. Nat Commun 6:8419
pubmed: 26420673 doi: 10.1038/ncomms9419
Kanda M, Shimizu D, Fujii T, Tanaka H, Shibata M, Iwata N et al (2016) Protein arginine methyltransferase 5 is associated with malignant phenotype and peritoneal metastasis in gastric cancer. Int J Oncol 49(3):1195–1202
pubmed: 27315569 doi: 10.3892/ijo.2016.3584
Jin Y, Zhou J, Xu F, Jin B, Cui L, Wang Y et al (2016) Targeting methyltransferase PRMT5 eliminates leukemia stem cells in chronic myelogenous leukemia. J Clin Investig 126(10):3961–3980
pubmed: 27643437 pmcid: 5096815 doi: 10.1172/JCI85239
Li K, Wang F, Cao WB, Lv XX, Hua F, Cui B et al (2017) TRIB3 Promotes APL progression through stabilization of the oncoprotein PML-RARalpha and inhibition of p53-mediated senescence. Cancer Cell 31(5):697-710 e7
pubmed: 28486108 doi: 10.1016/j.ccell.2017.04.006
Li T, Guan J, Huang Z, Hu X, Zheng X (2014) RNF168-mediated H2A neddylation antagonizes ubiquitylation of H2A and regulates DNA damage repair. J Cell Sci 127(Pt 10):2238–2248
pubmed: 24634510
Zhu D, Xu R, Huang X, Tang Z, Tian Y, Zhang J et al (2021) Deubiquitinating enzyme OTUB1 promotes cancer cell immunosuppression via preventing ER-associated degradation of immune checkpoint protein PD-L1. Cell Death Differ 28(6):1773–1789
pubmed: 33328570 doi: 10.1038/s41418-020-00700-z
de The H, Pandolfi PP, Chen Z (2017) Acute promyelocytic leukemia: a paradigm for oncoprotein-targeted cure. Cancer Cell 32(5):552–560
pubmed: 29136503 doi: 10.1016/j.ccell.2017.10.002
Cicconi L, Fenaux P, Kantarjian H, Tallman M, Sanz MA, Lo-Coco F (2018) Molecular remission as a therapeutic objective in acute promyelocytic leukemia. Leukemia 32(8):1671–1678
pubmed: 30026570 doi: 10.1038/s41375-018-0219-5
Yang Y, Bedford MT (2013) Protein arginine methyltransferases and cancer. Nat Rev Cancer 13(1):37–50
pubmed: 23235912 doi: 10.1038/nrc3409
Nasr R, Lallemand-Breitenbach V, Zhu J, Guillemin MC, de The H (2009) Therapy-induced PML/RARA proteolysis and acute promyelocytic leukemia cure. Clin Cancer Res 15(20):6321–6326
pubmed: 19808868 doi: 10.1158/1078-0432.CCR-09-0209
Karkhanis V, Hu YJ, Baiocchi RA, Imbalzano AN, Sif S (2011) Versatility of PRMT5-induced methylation in growth control and development. Trends Biochem Sci 36(12):633–641
pubmed: 21975038 pmcid: 3225484 doi: 10.1016/j.tibs.2011.09.001
Maimaitiyiming Y, Wang QQ, Yang C, Ogra Y, Lou YJ, Smith CA et al (2021) Hyperthermia selectively destabilizes oncogenic fusion proteins. Blood Cancer Discov 2(4):388–401
pubmed: 34661159 pmcid: 8513904 doi: 10.1158/2643-3230.BCD-20-0188
Zhao S, Shi P, Zhong Q, Shao S, Huang Y, Sun Y et al (2019) Identification of a point mutation PML(S214L)-RARalpha that alters PML body organization, dynamics and SUMOylation. Biochem Biophys Res Commun 511(3):518–523
pubmed: 30824184 doi: 10.1016/j.bbrc.2019.02.101
Bai DM, Zheng XF (2017) PML-RARA mutations confer varying arsenic trioxide resistance. Protein Cell 8(4):296–301
pubmed: 28028657 doi: 10.1007/s13238-016-0356-4
Jo S, Lee YL, Kim S, Lee H, Chung H (2016) PCGF2 negatively regulates arsenic trioxide-induced PML-RARA protein degradation via UBE2I inhibition in NB4 cells. Biochim Biophys Acta 1863(7 Pt A):1499–1509
pubmed: 27030546 doi: 10.1016/j.bbamcr.2016.03.019
Li ASM, Li F, Eram MS, Bolotokova A, Dela Sena CC, Vedadi M (2020) Chemical probes for protein arginine methyltransferases. Methods 175:30–43
pubmed: 31809836 doi: 10.1016/j.ymeth.2019.11.017
Mei M, Zhang R, Zhou ZW, Ying Z, Wang J, Zhang H et al (2019) PRMT5-mediated H4R3sme2 confers cell differentiation in pediatric B-cell precursor acute lymphoblastic leukemia. Clin Cancer Res 25(8):2633–2643
pubmed: 30635341 doi: 10.1158/1078-0432.CCR-18-2342
Tarighat SS, Santhanam R, Frankhouser D, Radomska HS, Lai H, Anghelina M et al (2016) The dual epigenetic role of PRMT5 in acute myeloid leukemia: gene activation and repression via histone arginine methylation. Leukemia 30(4):789–799
pubmed: 26536822 doi: 10.1038/leu.2015.308
Radzisheuskaya A, Shliaha PV, Grinev V, Lorenzini E, Kovalchuk S, Shlyueva D et al (2019) PRMT5 methylome profiling uncovers a direct link to splicing regulation in acute myeloid leukemia. Nat Struct Mol Biol 26(11):999–1012
pubmed: 31611688 pmcid: 6858565 doi: 10.1038/s41594-019-0313-z
Zhu F, Rui L (2019) PRMT5 in gene regulation and hematologic malignancies. Genes Dis 6(3):247–257
pubmed: 32042864 pmcid: 6997592 doi: 10.1016/j.gendis.2019.06.002
Chan-Penebre E, Kuplast KG, Majer CR, Boriack-Sjodin PA, Wigle TJ, Johnston LD et al (2015) A selective inhibitor of PRMT5 with in vivo and in vitro potency in MCL models. Nat Chem Biol 11(6):432–437
pubmed: 25915199 doi: 10.1038/nchembio.1810

Auteurs

Xinping Huang (X)

State Key Laboratory of Protein and Plant Gene Research, School of Life Sciences, Peking University, Beijing, 100871, China.
Department of Biochemistry and Molecular Biology, School of Life Sciences, Peking University, Beijing, China.

Yongfeng Yang (Y)

State Key Laboratory of Protein and Plant Gene Research, School of Life Sciences, Peking University, Beijing, 100871, China.
Department of Biochemistry and Molecular Biology, School of Life Sciences, Peking University, Beijing, China.

Dan Zhu (D)

State Key Laboratory of Protein and Plant Gene Research, School of Life Sciences, Peking University, Beijing, 100871, China.
Department of Biochemistry and Molecular Biology, School of Life Sciences, Peking University, Beijing, China.

Yan Zhao (Y)

State Key Laboratory of Protein and Plant Gene Research, School of Life Sciences, Peking University, Beijing, 100871, China.
Department of Biochemistry and Molecular Biology, School of Life Sciences, Peking University, Beijing, China.

Min Wei (M)

State Key Laboratory of Protein and Plant Gene Research, School of Life Sciences, Peking University, Beijing, 100871, China.
Department of Biochemistry and Molecular Biology, School of Life Sciences, Peking University, Beijing, China.

Ke Li (K)

NHC Key Laboratory of Biotechnology of Antibiotics, Institute of Medicinal Biotechnology, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, China.

Hong-Hu Zhu (HH)

Department of Hematology and Institute of Hematology, Zhejiang Province Key Laboratory of Hematology Oncology Diagnosis and Treatment, The First Affiliated Hospital, Zhejiang University, Hangzhou, China.

Xiaofeng Zheng (X)

State Key Laboratory of Protein and Plant Gene Research, School of Life Sciences, Peking University, Beijing, 100871, China. xiaofengz@pku.edu.cn.
Department of Biochemistry and Molecular Biology, School of Life Sciences, Peking University, Beijing, China. xiaofengz@pku.edu.cn.
ORCID: 0000-0001-6790-0669

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Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › PRMT5-mediated RNF4 methylation promotes...
questionsmedicales.fr › Actions chimiques et utilisations › Actions pharmacologiques › Utilisations thérapeutiques › Antinéoplasiques › PRMT5-mediated RNF4 methylation promotes...
questionsmedicales.fr › Produits chimiques inorganiques › Composés de l'oxygène › Oxydes › Trioxyde d'arsenic › PRMT5-mediated RNF4 methylation promotes...
questionsmedicales.fr › Cellules › Cellules cultivées › Cellules cancéreuses en culture › Lignée cellulaire tumorale › PRMT5-mediated RNF4 methylation promotes...
questionsmedicales.fr › Phénomènes physiologiques › Phénomènes pharmacologiques et toxicologiques › Phénomènes pharmacologiques › Résistance aux substances › Résistance aux médicaments antinéoplasiques › PRMT5-mediated RNF4 methylation promotes...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › PRMT5-mediated RNF4 methylation promotes...
questionsmedicales.fr › Composés hétérocycliques › Composés hétérocycliques à cycles fusionnés › Composés hétérobicycliques › Isoquinoléines › PRMT5-mediated RNF4 methylation promotes...
questionsmedicales.fr › Tumeurs › Tumeurs par type histologique › Leucémies › Leucémie myéloïde › Leucémie aigüe myéloïde › Leucémie aiguë promyélocytaire › PRMT5-mediated RNF4 methylation promotes...
questionsmedicales.fr › Métabolisme › Alkylation › Méthylation › PRMT5-mediated RNF4 methylation promotes...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › PRMT5-mediated RNF4 methylation promotes...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines nucléaires › PRMT5-mediated RNF4 methylation promotes...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines tumorales › Protéines oncogènes › Protéines de fusion oncogènes › PRMT5-mediated RNF4 methylation promotes...
questionsmedicales.fr › Enzymes et coenzymes › Enzymes › Transferases › One-carbon group transferases › Methyltransferases › Protein Methyltransferases › Protein-arginine N-methyltransferases › PRMT5-mediated RNF4 methylation promotes...
questionsmedicales.fr › Composés hétérocycliques › Composés hétéromonocycliques › Pyrimidines › PRMT5-mediated RNF4 methylation promotes...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Facteurs de transcription › PRMT5-mediated RNF4 methylation promotes...
questionsmedicales.fr › Phénomènes génétiques › Régulation de l'expression des gènes › Modification traductionnelle des protéines › Maturation post-traductionnelle des protéines › Ubiquitination › PRMT5-mediated RNF4 methylation promotes...