TRIM25 predominately associates with anti-viral stress granules.

Humans Poly-ADP-Ribose Binding Proteins / metabolism Tripartite Motif Proteins / metabolism RNA Recognition Motif Proteins / metabolism Ubiquitin-Protein Ligases / metabolism Stress Granules / metabolism RNA Helicases / metabolism Ubiquitination DNA Helicases / metabolism Signal Transduction DEAD Box Protein 58 / metabolism Transcription Factors / metabolism Immunity, Innate RNA, Double-Stranded / metabolism HEK293 Cells HeLa Cells Cytoplasmic Granules / metabolism RNA Virus Infections / virology Receptors, Immunologic / metabolism

Journal

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

Informations de publication

Date de publication:
15 May 2024
Historique:
received: 02 07 2023
accepted: 07 05 2024
medline: 16 5 2024
pubmed: 16 5 2024
entrez: 15 5 2024
Statut: epublish

Résumé

Stress granules (SGs) are induced by various environmental stressors, resulting in their compositional and functional heterogeneity. SGs play a crucial role in the antiviral process, owing to their potent translational repressive effects and ability to trigger signal transduction; however, it is poorly understood how these antiviral SGs differ from SGs induced by other environmental stressors. Here we identify that TRIM25, a known driver of the ubiquitination-dependent antiviral innate immune response, is a potent and critical marker of the antiviral SGs. TRIM25 undergoes liquid-liquid phase separation (LLPS) and co-condenses with the SG core protein G3BP1 in a dsRNA-dependent manner. The co-condensation of TRIM25 and G3BP1 results in a significant enhancement of TRIM25's ubiquitination activity towards multiple antiviral proteins, which are mainly located in SGs. This co-condensation is critical in activating the RIG-I signaling pathway, thus restraining RNA virus infection. Our studies provide a conceptual framework for better understanding the heterogeneity of stress granule components and their response to distinct environmental stressors.

Identifiants

DOI: 10.1038/s41467-024-48596-4 PMID: 38750080
pubmed: 38750080
doi: 10.1038/s41467-024-48596-4
pii: 10.1038/s41467-024-48596-4
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

4127

Informations de copyright

© 2024. The Author(s).

Références

Anderson, P. & Kedersha, N. RNA granules: post-transcriptional and epigenetic modulators of gene expression. Nat. Rev. Mol. Cell Biol. 10, 430–436 (2009).
pubmed: 19461665 doi: 10.1038/nrm2694
Guillen-Boixet, J. et al. RNA-induced conformational switching and clustering of G3BP drive stress granule assembly by condensation. Cell 181, 346–361.e17 (2020).
pubmed: 32302572 pmcid: 7181197 doi: 10.1016/j.cell.2020.03.049
Yang, P. et al. G3BP1 is a tunable switch that triggers phase separation to assemble stress granules. Cell 181, 325–345.e8 (2020).
pubmed: 32302571 pmcid: 7448383 doi: 10.1016/j.cell.2020.03.046
Eiermann, N., Haneke, K., Sun, Z., Stoecklin, G. & Ruggieri, A. Dance with the devil: stress granules and signaling in antiviral responses. Viruses 12, 984 (2020).
pubmed: 32899736 pmcid: 7552005 doi: 10.3390/v12090984
McCormick, C. & Khaperskyy, D. A. Translation inhibition and stress granules in the antiviral immune response. Nat. Rev. Immunol. 17, 647–660 (2017).
pubmed: 28669985 doi: 10.1038/nri.2017.63
Poblete-Duran, N., Prades-Perez, Y., Vera-Otarola, J., Soto-Rifo, R. & Valiente-Echeverria, F. Who regulates whom? An overview of RNA granules and viral infections. Viruses 8, 180 (2016).
pubmed: 27367717 pmcid: 4974515 doi: 10.3390/v8070180
Guan, Y. et al. Multiple functions of stress granules in viral infection at a glance. Front. Microbiol. 14, 1138864 (2023).
pubmed: 36937261 pmcid: 10014870 doi: 10.3389/fmicb.2023.1138864
Manjunath, L. et al. APOBEC3B drives PKR-mediated translation shutdown and protects stress granules in response to viral infection. Nat. Commun. 14, 820 (2023).
pubmed: 36781883 pmcid: 9925369 doi: 10.1038/s41467-023-36445-9
Wolozin, B. & Ivanov, P. Stress granules and neurodegeneration. Nat. Rev. Neurosci. 20, 649–666 (2019).
pubmed: 31582840 pmcid: 6986315 doi: 10.1038/s41583-019-0222-5
Marmor-Kollet, H. et al. Spatiotemporal proteomic analysis of stress granule disassembly using APEX reveals regulation by SUMOylation and links to ALS pathogenesis. Mol. Cell 80, 876–891.e6 (2020).
pubmed: 33217318 pmcid: 7816607 doi: 10.1016/j.molcel.2020.10.032
Markmiller, S. et al. Context-dependent and disease-specific diversity in protein interactions within stress granules. Cell 172, 590–604.e13 (2018).
pubmed: 29373831 pmcid: 5969999 doi: 10.1016/j.cell.2017.12.032
Asadi, M. R. et al. Stress granules involved in formation, progression and metastasis of cancer: a scoping review. Front. Cell Dev. Biol. 9, 745394 (2021).
pubmed: 34604242 pmcid: 8485071 doi: 10.3389/fcell.2021.745394
Lee, J. I. & Namkoong, S. Stress granules dynamics: benefits in cancer. BMB Rep. 55, 577–586 (2022).
pubmed: 36330685 pmcid: 9813431 doi: 10.5483/BMBRep.2022.55.12.141
Advani, V. M. & Ivanov, P. Stress granule subtypes: an emerging link to neurodegeneration. Cell Mol. Life Sci. 77, 4827–4845 (2020).
pubmed: 32500266 pmcid: 7668291 doi: 10.1007/s00018-020-03565-0
Aulas, A. et al. Stress-specific differences in assembly and composition of stress granules and related foci. J. Cell Sci. 130, 927–937 (2017).
pubmed: 28096475 pmcid: 5358336
Reineke, L. C. & Neilson, J. R. Differences between acute and chronic stress granules, and how these differences may impact function in human disease. Biochem. Pharmacol. 162, 123–131 (2019).
pubmed: 30326201 doi: 10.1016/j.bcp.2018.10.009
Zeng, W. J. et al. Initiation of stress granule assembly by rapid clustering of IGF2BP proteins upon osmotic shock. Biochim. Biophys. Acta Mol. Cell Res. 1867, 118795 (2020).
pubmed: 32668274 doi: 10.1016/j.bbamcr.2020.118795
Liu, Y. et al. Hypoxia-induced FUS-circTBC1D14 stress granules promote autophagy in TNBC. Adv. Sci. 10, e2204988 (2023).
doi: 10.1002/advs.202204988
Cabral, A. J., Costello, D. C. & Farny, N. G. The enigma of ultraviolet radiation stress granules: research challenges and new perspectives. Front. Mol. Biosci. 9, 1066650 (2022).
pubmed: 36533077 pmcid: 9751325 doi: 10.3389/fmolb.2022.1066650
Rozman, B., Fisher, T. & Stern-Ginossar, N. Translation—a tug of war during viral infection. Mol. Cell 83, 481–495 (2023).
pubmed: 36334591 doi: 10.1016/j.molcel.2022.10.012
Kim, S. S., Sze, L., Liu, C. & Lam, K. P. The stress granule protein G3BP1 binds viral dsRNA and RIG-I to enhance interferon-beta response. J. Biol. Chem. 294, 6430–6438 (2019).
pubmed: 30804210 pmcid: 6484135 doi: 10.1074/jbc.RA118.005868
Liu, Z. S. et al. G3BP1 promotes DNA binding and activation of cGAS. Nat. Immunol. 20, 18–28 (2019).
pubmed: 30510222 doi: 10.1038/s41590-018-0262-4
Zhao, M. et al. The stress granule protein G3BP1 promotes pre-condensation of cGAS to allow rapid responses to DNA. EMBO Rep. 23, e53166 (2022).
pubmed: 34779554 doi: 10.15252/embr.202153166
Yoo, J. S. et al. DHX36 enhances RIG-I signaling by facilitating PKR-mediated antiviral stress granule formation. PLoS Pathog. 10, e1004012 (2014).
pubmed: 24651521 pmcid: 3961341 doi: 10.1371/journal.ppat.1004012
Huang, W. et al. Molecular determinants for regulation of G3BP1/2 phase separation by the SARS-CoV-2 nucleocapsid protein. Cell Discov. 7, 69 (2021).
pubmed: 34400613 pmcid: 8368218 doi: 10.1038/s41421-021-00306-w
Luo, L. et al. SARS-CoV-2 nucleocapsid protein phase separates with G3BPs to disassemble stress granules and facilitate viral production. Sci. Bull. 66, 1194–1204 (2021).
doi: 10.1016/j.scib.2021.01.013
Zheng, Z. Q., Wang, S. Y., Xu, Z. S., Fu, Y. Z. & Wang, Y. Y. SARS-CoV-2 nucleocapsid protein impairs stress granule formation to promote viral replication. Cell Discov. 7, 38 (2021).
pubmed: 34035218 pmcid: 8147577 doi: 10.1038/s41421-021-00275-0
Bao, M., Hofsink, N. & Plosch, T. LPS versus Poly I:C model: comparison of long-term effects of bacterial and viral maternal immune activation on the offspring. Am. J. Physiol. Regul. Integr. Comp. Physiol. 322, R99–R111 (2022).
pubmed: 34874190 doi: 10.1152/ajpregu.00087.2021
Roux, K. J., Kim, D. I., Raida, M. & Burke, B. A promiscuous biotin ligase fusion protein identifies proximal and interacting proteins in mammalian cells. J. Cell Biol. 196, 801–810 (2012).
pubmed: 22412018 pmcid: 3308701 doi: 10.1083/jcb.201112098
Burke, J. M., Lester, E. T., Tauber, D. & Parker, R. RNase L promotes the formation of unique ribonucleoprotein granules distinct from stress granules. J. Biol. Chem. 295, 1426–1438 (2020).
pubmed: 31896577 pmcid: 7008361 doi: 10.1074/jbc.RA119.011638
Burke, J. M., Moon, S. L., Matheny, T. & Parker, R. RNase L reprograms translation by widespread mRNA turnover escaped by antiviral mRNAs. Mol. Cell 75, 1203–1217.e5 (2019).
pubmed: 31494035 pmcid: 6754297 doi: 10.1016/j.molcel.2019.07.029
Sanchez, J. G. et al. TRIM25 binds RNA to modulate cellular anti-viral defense. J. Mol. Biol. 430, 5280–5293 (2018).
pubmed: 30342007 pmcid: 6289755 doi: 10.1016/j.jmb.2018.10.003
Haubrich, K. et al. Mechanistic insights into RNA binding and RNA-regulated RIG-I ubiquitination by TRIM25. bioRxiv https://doi.org/10.1101/2020.05.04.070177 (2021).
Álvarez, L. et al. The molecular dissection of TRIM25‘s RNA-binding mechanism provides key insights into its antiviral activity. Res. Sq. https://doi.org/10.21203/rs.3.rs-3692619/v1 (2023).
Panas, M. D. et al. Viral and cellular proteins containing FGDF motifs bind G3BP to block stress granule formation. PLoS Pathog. 11, e1004659 (2015).
pubmed: 25658430 pmcid: 4450067 doi: 10.1371/journal.ppat.1004659
Yang, E. et al. Elucidation of TRIM25 ubiquitination targets involved in diverse cellular and antiviral processes. PLoS Pathog. 18, e1010743 (2022).
pubmed: 36067236 pmcid: 9481182 doi: 10.1371/journal.ppat.1010743
Schulte, T. et al. Combined structural, biochemical and cellular evidence demonstrates that both FGDF motifs in alphavirus nsP3 are required for efficient replication. Open Biol. 6, 160078 (2016).
pubmed: 27383630 pmcid: 4967826 doi: 10.1098/rsob.160078
Kruse, T. et al. Large scale discovery of coronavirus-host factor protein interaction motifs reveals SARS-CoV-2 specific mechanisms and vulnerabilities. Nat. Commun. 12, 6761 (2021).
pubmed: 34799561 pmcid: 8605023 doi: 10.1038/s41467-021-26498-z
Choudhury, N. R. et al. RNA-binding activity of TRIM25 is mediated by its PRY/SPRY domain and is required for ubiquitination. BMC Biol. 15, 105 (2017).
pubmed: 29117863 pmcid: 5678581 doi: 10.1186/s12915-017-0444-9
Koliopoulos, M. G. et al. Molecular mechanism of influenza A NS1-mediated TRIM25 recognition and inhibition. Nat. Commun. 9, 1820 (2018).
pubmed: 29739942 pmcid: 5940772 doi: 10.1038/s41467-018-04214-8
Lian, H. et al. The zinc-finger protein ZCCHC3 binds RNA and facilitates viral RNA sensing and activation of the RIG-I-like receptors. Immunity 49, 438–448.e5 (2018).
pubmed: 30193849 doi: 10.1016/j.immuni.2018.08.014
Lian, H. et al. ZCCHC3 is a co-sensor of cGAS for dsDNA recognition in innate immune response. Nat. Commun. 9, 3349 (2018).
pubmed: 30135424 pmcid: 6105683 doi: 10.1038/s41467-018-05559-w
Li, B. et al. circNDUFB2 inhibits non-small cell lung cancer progression via destabilizing IGF2BPs and activating anti-tumor immunity. Nat. Commun. 12, 295 (2021).
pubmed: 33436560 pmcid: 7804955 doi: 10.1038/s41467-020-20527-z
Galao, R. P. et al. TRIM25 and ZAP target the Ebola virus ribonucleoprotein complex to mediate interferon-induced restriction. PLoS Pathog. 18, e1010530 (2022).
pubmed: 35533151 pmcid: 9119685 doi: 10.1371/journal.ppat.1010530
Yang, E., Nguyen, L. P., Wisherop, C. A., Kan, R. L. & Li, M. M. H. The role of ZAP and TRIM25 RNA binding in restricting viral translation. Front. Cell Infect. Microbiol. 12, 886929 (2022).
pubmed: 35800389 pmcid: 9253567 doi: 10.3389/fcimb.2022.886929
Law, L. M. J. et al. ZAP’s stress granule localization is correlated with its antiviral activity and induced by virus replication. PLoS Pathog. 15, e1007798 (2019).
pubmed: 31116799 pmcid: 6548403 doi: 10.1371/journal.ppat.1007798
Li, M. M. et al. TRIM25 enhances the antiviral action of zinc-finger antiviral protein (ZAP). PLoS Pathog. 13, e1006145 (2017).
pubmed: 28060952 pmcid: 5245905 doi: 10.1371/journal.ppat.1006145
Schwerk, J. et al. RNA-binding protein isoforms ZAP-S and ZAP-L have distinct antiviral and immune resolution functions. Nat. Immunol. 20, 1610–1620 (2019).
pubmed: 31740798 pmcid: 7240801 doi: 10.1038/s41590-019-0527-6
Sanchez-Aparicio, M. T., Ayllon, J., Leo-Macias, A., Wolff, T. & Garcia-Sastre, A. Subcellular localizations of RIG-I, TRIM25, and MAVS complexes. J. Virol. 91, e01155-16 (2017).
pubmed: 27807226 pmcid: 5215348 doi: 10.1128/JVI.01155-16
Loo, Y. M. & Gale, M. Jr. Immune signaling by RIG-I-like receptors. Immunity 34, 680–692 (2011).
pubmed: 21616437 pmcid: 3177755 doi: 10.1016/j.immuni.2011.05.003
Hou, F. et al. MAVS forms functional prion-like aggregates to activate and propagate antiviral innate immune response. Cell 146, 448–461 (2011).
pubmed: 21782231 pmcid: 3179916 doi: 10.1016/j.cell.2011.06.041
Gack, M. U. et al. TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 446, 916–920 (2007).
pubmed: 17392790 doi: 10.1038/nature05732
Cadena, C. et al. Ubiquitin-dependent and -independent roles of E3 ligase RIPLET in innate immunity. Cell 177, 1187–1200.e16 (2019).
pubmed: 31006531 pmcid: 6525047 doi: 10.1016/j.cell.2019.03.017
Heikel, G., Choudhury, N. R. & Michlewski, G. The role of Trim25 in development, disease and RNA metabolism. Biochem. Soc. Trans. 44, 1045–1050 (2016).
pubmed: 27528750 doi: 10.1042/BST20160077
Kato, K. et al. Structural analysis of RIG-I-like receptors reveals ancient rules of engagement between diverse RNA helicases and TRIM ubiquitin ligases. Mol. Cell 81, 599–613.e8 (2021).
pubmed: 33373584 doi: 10.1016/j.molcel.2020.11.047
Sanchez, J. G. et al. Mechanism of TRIM25 catalytic activation in the antiviral RIG-I pathway. Cell Rep. 16, 1315–1325 (2016).
pubmed: 27425606 pmcid: 5076470 doi: 10.1016/j.celrep.2016.06.070
Lin, H. et al. The long noncoding RNA Lnczc3h7a promotes a TRIM25-mediated RIG-I antiviral innate immune response. Nat. Immunol. 20, 812–823 (2019).
pubmed: 31036902 doi: 10.1038/s41590-019-0379-0
Zeng, W. et al. Reconstitution of the RIG-I pathway reveals a signaling role of unanchored polyubiquitin chains in innate immunity. Cell 141, 315–330 (2010).
pubmed: 20403326 pmcid: 2919214 doi: 10.1016/j.cell.2010.03.029
Gack, M. U. et al. Roles of RIG-I N-terminal tandem CARD and splice variant in TRIM25-mediated antiviral signal transduction. Proc. Natl Acad. Sci. USA 105, 16743–16748 (2008).
pubmed: 18948594 pmcid: 2575490 doi: 10.1073/pnas.0804947105
Song, D. et al. Yin and yang regulation of stress granules by Caprin-1. Proc. Natl Acad. Sci. USA 119, e2207975119 (2022).
pubmed: 36279435 pmcid: 9636964 doi: 10.1073/pnas.2207975119
Yang, Y. et al. TRIM25-mediated ubiquitination of G3BP1 regulates the proliferation and migration of human neuroblastoma cells. Biochim. Biophys. Acta Gene Regul. Mech. 1866, 194954 (2023).
Goncalves-Carneiro, D., Takata, M. A., Ong, H., Shilton, A. & Bieniasz, P. D. Origin and evolution of the zinc finger antiviral protein. PLoS Pathog. 17, e1009545 (2021).
pubmed: 33901262 pmcid: 8102003 doi: 10.1371/journal.ppat.1009545
Portz, B., Lee, B. L. & Shorter, J. FUS and TDP-43 phases in health and disease. Trends Biochem. Sci. 46, 550–563 (2021).
pubmed: 33446423 pmcid: 8195841 doi: 10.1016/j.tibs.2020.12.005
Li, Z., Liu, X. & Liu, M. Stress granule homeostasis, aberrant phase transition, and amyotrophic lateral sclerosis. ACS Chem. Neurosci. 13, 2356–2370 (2022).
pubmed: 35905138 doi: 10.1021/acschemneuro.2c00262
Wang, L., Yang, W., Li, B., Yuan, S. & Wang, F. Response to stress in biological disorders: implications of stress granule assembly and function. Cell Prolif. 54, e13086 (2021).
pubmed: 34170048 pmcid: 8349659 doi: 10.1111/cpr.13086
Cui, Q. et al. Diverse CMT2 neuropathies are linked to aberrant G3BP interactions in stress granules. Cell 186, 803–820.e5 (2023).
pubmed: 36738734 doi: 10.1016/j.cell.2022.12.046
Paget, M. et al. Stress granules are shock absorbers that prevent excessive innate immune responses to dsRNA. Mol. Cell 83, 1180–1196.e8 (2023).
pubmed: 37028415 pmcid: 10170497 doi: 10.1016/j.molcel.2023.03.010
Sears, R. M., May, D. G. & Roux, K. J. BioID as a tool for protein-proximity labeling in living cells. Methods Mol. Biol. 2012, 299–313 (2019).
pubmed: 31161514 pmcid: 6583792 doi: 10.1007/978-1-4939-9546-2_15
Lyu, H. et al. Proximity labeling reveals OTUD3 as a DNA-binding deubiquitinase of cGAS. Cell Rep. 42, 112309 (2023).
pubmed: 36966392 doi: 10.1016/j.celrep.2023.112309
Mao, L. et al. Phosphorylation of SNX27 by MAPK11/14 links cellular stress-signaling pathways with endocytic recycling. J. Cell Biol. 220, e202010048 (2021).
pubmed: 33605979 pmcid: 7901142 doi: 10.1083/jcb.202010048
Han, Z. et al. Model-based analysis uncovers mutations altering autophagy selectivity in human cancer. Nat. Commun. 12, 3258 (2021).
pubmed: 34059679 pmcid: 8166871 doi: 10.1038/s41467-021-23539-5
Gao, B. et al. Inhibition of anti-viral stress granule formation by coronavirus endoribonuclease nsp15 ensures efficient virus replication. PLoS Pathog. 17, e1008690 (2021).
pubmed: 33635931 pmcid: 7946191 doi: 10.1371/journal.ppat.1008690
Wang, S. et al. TRIM25 inhibits infectious bursal disease virus replication by targeting VP3 for ubiquitination and degradation. PLoS Pathog. 17, e1009900 (2021).
pubmed: 34516573 pmcid: 8459960 doi: 10.1371/journal.ppat.1009900
Shen, C. et al. Phase separation drives RNA virus-induced activation of the NLRP6 inflammasome. Cell 184, 5759–5774.e20 (2021).
pubmed: 34678144 pmcid: 8643277 doi: 10.1016/j.cell.2021.09.032
Liu, Z. et al. SCGN deficiency is a risk factor for autism spectrum disorder. Signal Transduct. Target. Ther. 8, 3 (2023).
pubmed: 36588101 pmcid: 9806109 doi: 10.1038/s41392-022-01225-2
Zhao, M. et al. A Golgi-resident GPR108 cooperates with E3 ubiquitin ligase Smurf1 to suppress antiviral innate immunity. Cell Rep. 42, 112655 (2023).
pubmed: 37330913 doi: 10.1016/j.celrep.2023.112655
Qin, Z. et al. Deactylation by SIRT1 enables liquid-liquid phase separation of IRF3/IRF7 in innate antiviral immunity. Nat. Immunol. 23, 1193–1207 (2022).
pubmed: 35879450 doi: 10.1038/s41590-022-01269-0
Gao, Y., Li, X., Li, P. & Lin, Y. A brief guideline for studies of phase-separated biomolecular condensates. Nat. Chem. Biol. 18, 1307–1318 (2022).
pubmed: 36400991 doi: 10.1038/s41589-022-01204-2
Yong, X. et al. SNX27-FERM-SNX1 complex structure rationalizes divergent trafficking pathways by SNX17 and SNX27. Proc. Natl Acad. Sci. USA 118, e2105510118 (2021).
pubmed: 34462354 pmcid: 8433557 doi: 10.1073/pnas.2105510118
Tu, Y. et al. TBC1D23 mediates Golgi-specific LKB1 signaling. Nat. Commun. 15, 1785 (2024).

Auteurs

Zehua Shang (Z)

Key Laboratory of Birth Defects and Related Diseases of Women and Children, Department of Pediatrics, West China Second University Hospital, State Key Laboratory of Biotherapy, Sichuan University, Chengdu, 610041, China.

Sitao Zhang (S)

Key Laboratory of Birth Defects and Related Diseases of Women and Children, Department of Pediatrics, West China Second University Hospital, State Key Laboratory of Biotherapy, Sichuan University, Chengdu, 610041, China.

Jinrui Wang (J)

Key Laboratory of Birth Defects and Related Diseases of Women and Children, Department of Pediatrics, West China Second University Hospital, State Key Laboratory of Biotherapy, Sichuan University, Chengdu, 610041, China.

Lili Zhou (L)

Institutes of Biology and Medical Science, Soochow University, Suzhou, 215000, China.

Xinyue Zhang (X)

Key Laboratory of Birth Defects and Related Diseases of Women and Children, Department of Pediatrics, West China Second University Hospital, State Key Laboratory of Biotherapy, Sichuan University, Chengdu, 610041, China.

Daniel D Billadeau (DD)

Division of Oncology Research and Schulze Center for Novel Therapeutics, Mayo Clinic, Rochester, MN, 55905, USA.

Peiguo Yang (P)

School of Life Sciences, Westlake University, Hangzhou, 310024, 310030, China.
ORCID: 0000-0002-2334-5664

Lingqiang Zhang (L)

State Key Laboratory of Proteomics, Beijing Proteome Research Center, National Center for Protein Sciences (Beijing), Beijing Institute of Lifeomics, 100850, Beijing, China.
ORCID: 0000-0002-9795-2141

Fangfang Zhou (F)

Institutes of Biology and Medical Science, Soochow University, Suzhou, 215000, China.
ORCID: 0000-0003-1870-7584

Peng Bai (P)

Department of Forensic Genetics, West China School of Basic Medical Sciences & Forensic Medicine, Sichuan University, Chengdu, 610041, China. baipeng@scu.edu.cn.

Da Jia (D)

Key Laboratory of Birth Defects and Related Diseases of Women and Children, Department of Pediatrics, West China Second University Hospital, State Key Laboratory of Biotherapy, Sichuan University, Chengdu, 610041, China. JiaDa@scu.edu.cn.
ORCID: 0000-0002-2205-1998

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Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › TRIM25 predominately associates with...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines nucléaires › Protéines liant le poly-adp-ribose › TRIM25 predominately associates with...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines à motif tripartite › TRIM25 predominately associates with...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Nucléoprotéines › Protéines de liaison à l'ARN › Protéines à motif de reconnaissance de l'ARN › TRIM25 predominately associates with...
questionsmedicales.fr › Enzymes et coenzymes › Enzymes › Ligases › Ubiquitin-protein ligase complexes › Ubiquitin-protein ligases › TRIM25 predominately associates with...
questionsmedicales.fr › Cellules › Structures cellulaires › Espace intracellulaire › Cytoplasme › Structures cytoplasmiques › Organites › Vésicules cytoplasmiques › Granulations cytoplasmiques › Granules ribonucléoprotéiques cytoplasmiques › Granules de stress › TRIM25 predominately associates with...
questionsmedicales.fr › Enzymes et coenzymes › Enzymes › Transferases › Phosphotransferases › Nucleotidyltransferases › RNA nucleotidyltransferases › RNA helicases › TRIM25 predominately associates with...
questionsmedicales.fr › Phénomènes génétiques › Régulation de l'expression des gènes › Modification traductionnelle des protéines › Maturation post-traductionnelle des protéines › Ubiquitination › TRIM25 predominately associates with...
questionsmedicales.fr › Enzymes et coenzymes › Enzymes › Isomerases › Helicase › TRIM25 predominately associates with...
questionsmedicales.fr › Phénomènes physiologiques cellulaires › Transduction du signal › TRIM25 predominately associates with...
questionsmedicales.fr › Enzymes et coenzymes › Enzymes › Transferases › Phosphotransferases › Nucleotidyltransferases › RNA nucleotidyltransferases › RNA helicases › DEAD-box RNA helicases › Protéine-58 à domaine DEAD › TRIM25 predominately associates with...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Facteurs de transcription › TRIM25 predominately associates with...
questionsmedicales.fr › Phénomènes du système immunitaire › Immunité › Immunité innée › TRIM25 predominately associates with...
questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Conformation d'acide nucléique › ARN double brin › TRIM25 predominately associates with...
questionsmedicales.fr › Cellules › Cellules épithéliales › Cellules HEK293 › TRIM25 predominately associates with...
questionsmedicales.fr › Cellules › Cellules épithéliales › Cellules HeLa › TRIM25 predominately associates with...
questionsmedicales.fr › Cellules › Structures cellulaires › Espace intracellulaire › Cytoplasme › Structures cytoplasmiques › Organites › Vésicules cytoplasmiques › Granulations cytoplasmiques › TRIM25 predominately associates with...
questionsmedicales.fr › Infection › Maladies virales › Infections à virus à ARN › TRIM25 predominately associates with...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines membranaires › Récepteurs de surface cellulaire › Récepteurs immunologiques › TRIM25 predominately associates with...