Velcrin-induced selective cleavage of tRNA
Journal
Nature chemical biology
ISSN: 1552-4469
Titre abrégé: Nat Chem Biol
Pays: United States
ID NLM: 101231976
Informations de publication
Date de publication:
03 2023
03 2023
Historique:
received:
26
01
2022
accepted:
08
09
2022
pubmed:
28
10
2022
medline:
3
3
2023
entrez:
27
10
2022
Statut:
ppublish
Résumé
Velcrin compounds kill cancer cells expressing high levels of phosphodiesterase 3A (PDE3A) and Schlafen family member 12 (SLFN12) by inducing complex formation between these two proteins, but the mechanism of cancer cell killing by the PDE3A-SLFN12 complex is not fully understood. Here, we report that the physiological substrate of SLFN12 RNase is tRNA
Identifiants
pubmed: 36302897
doi: 10.1038/s41589-022-01170-9
pii: 10.1038/s41589-022-01170-9
doi:
Substances chimiques
RNA, Transfer, Leu
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
301-310Subventions
Organisme : NCI NIH HHS
ID : R35 CA197568
Pays : United States
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Nature America, Inc.
Références
de Waal, L. et al. Identification of cancer-cytotoxic modulators of PDE3A by predictive chemogenomics. Nat. Chem. Biol. 12, 102–108 (2016).
pubmed: 26656089
doi: 10.1038/nchembio.1984
Garvie, C. W. et al. Structure of PDE3A–SLFN12 complex reveals requirements for activation of SLFN12 RNase. Nat. Commun. 12, 4375 (2021).
pubmed: 34272366
pmcid: 8285493
doi: 10.1038/s41467-021-24495-w
Wu, X. et al. Mechanistic insights into cancer cell killing through interaction of phosphodiesterase 3A and Schlafen family member 12. J. Biol. Chem. 295, 3431–3446 (2020).
pubmed: 32005668
pmcid: 7076209
doi: 10.1074/jbc.RA119.011191
Ai, Y. et al. An alkaloid initiates phosphodiesterase 3A-Schlafen 12 dependent apoptosis without affecting the phosphodiesterase activity. Nat. Commun. 11, 3236 (2020).
pubmed: 32591543
pmcid: 7319972
doi: 10.1038/s41467-020-17052-4
An, R. et al. PDE3A inhibitor anagrelide activates death signaling pathway genes and synergizes with cell death-inducing cytokines to selectively inhibit cancer cell growth. Am. J. Cancer Res. 9, 1905–1921 (2019).
pubmed: 31598394
pmcid: 6780660
Lewis, T. A. et al. Optimization of PDE3A modulators for SLFN12-dependent cancer cell killing. ACS Med. Chem. Lett. 10, 1537–1542 (2019).
pubmed: 31749907
pmcid: 6862344
doi: 10.1021/acsmedchemlett.9b00360
Nazir, M. et al. Targeting tumor cells based on phosphodiesterase 3A expression. Exp. Cell. Res. 361, 308–315 (2017).
pubmed: 29107068
doi: 10.1016/j.yexcr.2017.10.032
Corsello, S. M. et al. Discovering the anti-cancer potential of non-oncology drugs by systematic viability profiling. Nat. Cancer 1, 235–248 (2020).
pubmed: 32613204
pmcid: 7328899
doi: 10.1038/s43018-019-0018-6
Li, D. et al. Estrogen-related hormones induce apoptosis by stabilizing Schlafen-12 protein turnover. Mol. Cell 75, 1103–1116 (2019).
pubmed: 31420216
doi: 10.1016/j.molcel.2019.06.040
Chen, J. et al. Structure of PDE3A–SLFN12 complex and structure-based design for a potent apoptosis inducer of tumor cells. Nat. Commun. 12, 6204 (2021).
pubmed: 34707099
pmcid: 8551160
doi: 10.1038/s41467-021-26546-8
de la Casa-Esperon, E. From mammals to viruses: the Schlafen genes in developmental, proliferative and immune processes. Biomol. Concepts 2, 159–169 (2011).
pubmed: 25962026
doi: 10.1515/bmc.2011.018
Puck, A. et al. Expression and regulation of Schlafen (SLFN) family members in primary human monocytes, monocyte-derived dendritic cells and T cells. Results Immunol. 5, 23–32 (2015).
pubmed: 26623250
pmcid: 4625362
doi: 10.1016/j.rinim.2015.10.001
Li, M. et al. DNA damage-induced cell death relies on SLFN11-dependent cleavage of distinct type II tRNAs. Nat. Struct. Mol. Biol. 25, 1047–1058 (2018).
pubmed: 30374083
pmcid: 6579113
doi: 10.1038/s41594-018-0142-5
Pisareva, V. P., Muslimov, I. A., Tcherepanov, A. & Pisarev, A. V. Characterization of novel ribosome-associated endoribonuclease SLFN14 from rabbit reticulocytes. Biochemistry 54, 3286–3301 (2015).
pubmed: 25996083
doi: 10.1021/acs.biochem.5b00302
Yang, J. Y. et al. Structure of Schlafen13 reveals a new class of tRNA/rRNA-targeting RNase engaged in translational control. Nat. Commun. 9, 1165 (2018).
pubmed: 29563550
pmcid: 5862951
doi: 10.1038/s41467-018-03544-x
Metzner, F. J., Huber, E., Hopfner, K. P. & Lammens, K. Structural and biochemical characterization of human Schlafen 5. Nucleic Acids Res. 50, 1147–1161 (2022).
pubmed: 35037067
pmcid: 8789055
doi: 10.1093/nar/gkab1278
Wilson, D. N. & Doudna Cate, J. H. The structure and function of the eukaryotic ribosome. Cold Spring Harb. Perspect. 4, a011536 (2012).
Gogakos, T. et al. Characterizing expression and processing of precursor and mature human tRNAs by hydro-tRNAseq and PAR-CLIP. Cell Rep. 20, 1463–1475 (2017).
pubmed: 28793268
pmcid: 5564215
doi: 10.1016/j.celrep.2017.07.029
Pan, T. Modifications and functional genomics of human transfer RNA. Cell Res. 28, 395–404 (2018).
pubmed: 29463900
pmcid: 5939049
doi: 10.1038/s41422-018-0013-y
van Zundert, G. C. P. et al. The HADDOCK2.2 web server: user-friendly integrative modeling of biomolecular complexes. J. Mol. Biol. 428, 720–725 (2016).
pubmed: 26410586
doi: 10.1016/j.jmb.2015.09.014
Hein, C. D., Liu, X. M. & Wang, D. Click chemistry, a powerful tool for pharmaceutical sciences. Pharm. Res. 25, 2216–2230 (2008).
pubmed: 18509602
pmcid: 2562613
doi: 10.1007/s11095-008-9616-1
Iordanov, M. S. et al. Ribotoxic stress response: activation of the stress-activated protein kinase JNK1 by inhibitors of the peptidyl transferase reaction and by sequence-specific RNA damage to the α-sarcin/ricin loop in the 28S rRNA. Mol. Cell. Biol. 17, 3373–3381 (1997).
pubmed: 9154836
pmcid: 232190
doi: 10.1128/MCB.17.6.3373
Wu, C. C., Peterson, A., Zinshteyn, B., Regot, S. & Green, R. Ribosome collisions trigger general stress responses to regulate cell fate. Cell 182, 404–416 (2020).
pubmed: 32610081
pmcid: 7384957
doi: 10.1016/j.cell.2020.06.006
Ivanov, P., Emara, M. M., Villen, J., Gygi, S. P. & Anderson, P. Angiogenin-induced tRNA fragments inhibit translation initiation. Mol. Cell 43, 613–623 (2011).
pubmed: 21855800
pmcid: 3160621
doi: 10.1016/j.molcel.2011.06.022
Barretina, J. et al. The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature 483, 603–607 (2012).
pubmed: 22460905
pmcid: 3320027
doi: 10.1038/nature11003
Zoppoli, G. et al. Putative DNA/RNA helicase Schlafen-11 (SLFN11) sensitizes cancer cells to DNA-damaging agents. Proc. Natl Acad. Sci. USA 109, 15030–15035 (2012).
pubmed: 22927417
pmcid: 3443151
doi: 10.1073/pnas.1205943109
Murai, J. et al. SLFN11 blocks stressed replication forks independently of ATR. Mol. Cell 69, 371–384 (2018).
pubmed: 29395061
pmcid: 5802881
doi: 10.1016/j.molcel.2018.01.012
Malone, D., Lardelli, R. M., Li, M. & David, M. Dephosphorylation activates the interferon-stimulated Schlafen family member 11 in the DNA damage response. J. Biol. Chem. 294, 14674–14685 (2019).
pubmed: 31395656
pmcid: 6779438
doi: 10.1074/jbc.RA118.006588
Yan, B. et al. Multiple PDE3A modulators act as molecular glues promoting PDE3A–SLFN12 interaction and induce SLFN12 dephosphorylation and cell death. Cell Chem. Biol. 29, 958–969 (2022).
pubmed: 35104454
doi: 10.1016/j.chembiol.2022.01.006
Katsoulidis, E. et al. Role of interferon α (IFN α)-inducible Schlafen-5 in regulation of anchorage-independent growth and invasion of malignant melanoma cells. J. Biol. Chem. 285, 40333–40341 (2010).
pubmed: 20956525
pmcid: 3001013
doi: 10.1074/jbc.M110.151076
Kane, M. et al. Identification of interferon-stimulated genes with antiretroviral activity. Cell Host Microbe 20, 392–405 (2016).
pubmed: 27631702
pmcid: 5026698
doi: 10.1016/j.chom.2016.08.005
Kim, E. T. et al. Comparative proteomics identifies Schlafen 5 (SLFN5) as a herpes simplex virus restriction factor that suppresses viral transcription. Nat. Microbiol. 6, 234–245 (2021).
pubmed: 33432153
pmcid: 7856100
doi: 10.1038/s41564-020-00826-3
Li, M. et al. Codon-usage-based inhibition of HIV protein synthesis by human Schlafen 11. Nature 491, 125–128 (2012).
pubmed: 23000900
pmcid: 3705913
doi: 10.1038/nature11433
Seong, R. K. et al. Schlafen 14 (SLFN14) is a novel antiviral factor involved in the control of viral replication. Immunobiology 222, 979–988 (2017).
pubmed: 28734654
pmcid: 5990420
doi: 10.1016/j.imbio.2017.07.002
Chan, P. P. & Lowe, T. M. GtRNAdb 2.0: an expanded database of transfer RNA genes identified in complete and draft genomes. Nucleic Acids Res. 44, D184–D189 (2016).
pubmed: 26673694
doi: 10.1093/nar/gkv1309
Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760 (2009).
pubmed: 19451168
pmcid: 2705234
doi: 10.1093/bioinformatics/btp324
Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012).
pubmed: 22930834
pmcid: 5554542
doi: 10.1038/nmeth.2089
Liu, Q., Shvarts, T., Sliz, P. & Gregory, R. I. RiboToolkit: an integrated platform for analysis and annotation of ribosome profiling data to decode mRNA translation at codon resolution. Nucleic Acids Res. 48, W218–W229 (2020).
pubmed: 32427338
pmcid: 7319539
doi: 10.1093/nar/gkaa395
Kumari, R., Michel, A. M. & Baranov, P. V. PausePred and Rfeet: webtools for inferring ribosome pauses and visualizing footprint density from ribosome profiling data. RNA 24, 1297–1304 (2018).
pubmed: 30049792
pmcid: 6140459
doi: 10.1261/rna.065235.117
Zuker, M. & Stiegler, P. Optimal computer folding of large RNA sequences using thermodynamics and auxiliary information. Nucleic Acids Res. 9, 133–148 (1981).
pubmed: 6163133
pmcid: 326673
doi: 10.1093/nar/9.1.133
Bailey, T. L., Johnson, J., Grant, C. E. & Noble, W. S. The MEME suite. Nucleic Acids Res. 43, W39–W49 (2015).
pubmed: 25953851
pmcid: 4489269
doi: 10.1093/nar/gkv416
Kwon, N. H. et al. Transfer-RNA-mediated enhancement of ribosomal proteins S6 kinases signaling for cell proliferation. RNA Biol. 15, 635–648 (2018).
pubmed: 28816616
pmcid: 6103689
doi: 10.1080/15476286.2017.1356563
Sanjana, N. E., Shalem, O. & Zhang, F. Improved vectors and genome-wide libraries for CRISPR screening. Nat. Methods 11, 783–784 (2014).
pubmed: 25075903
pmcid: 4486245
doi: 10.1038/nmeth.3047
Tamaki, S., Tomita, M., Suzuki, H. & Kanai, A. Systematic analysis of the binding surfaces between tRNAs and their respective aminoacyl tRNA synthetase based on structural and evolutionary data. Front. Genet. 8, 227 (2017).
pubmed: 29358943
doi: 10.3389/fgene.2017.00227