دورية أكاديمية

The ribotoxic stress response drives UV-mediated cell death.

التفاصيل البيبلوغرافية
العنوان: The ribotoxic stress response drives UV-mediated cell death.
المؤلفون: Sinha NK; Department of Molecular Biology and Genetics, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Howard Hughes Medical Institute, Chevy Chase, MD 20815, USA., McKenney C; Department of Molecular Biology and Genetics, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Department of Oncology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Biochemistry, Cellular and Molecular Biology Graduate Program, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA., Yeow ZY; Department of Molecular Biology and Genetics, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA., Li JJ; Department of Molecular Biology and Genetics, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA., Nam KH; Cell Biology Program, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA., Yaron-Barir TM; Meyer Cancer Center, Weill Cornell Medicine, New York, NY 10021, USA; Englander Institute for Precision Medicine, Institute for Computational Biomedicine, Weill Cornell Medicine, New York, NY 10021, USA; Columbia University Vagelos College of Physicians and Surgeons, New York, NY 10032, USA., Johnson JL; Meyer Cancer Center, Weill Cornell Medicine, New York, NY 10021, USA; Department of Cell Biology, Harvard Medical School, Boston, MA 02115, USA; Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02215, USA., Huntsman EM; Meyer Cancer Center, Weill Cornell Medicine, New York, NY 10021, USA., Cantley LC; Meyer Cancer Center, Weill Cornell Medicine, New York, NY 10021, USA; Department of Cell Biology, Harvard Medical School, Boston, MA 02115, USA; Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02215, USA., Ordureau A; Cell Biology Program, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA. Electronic address: ordureaa@mskcc.org., Regot S; Department of Molecular Biology and Genetics, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Department of Oncology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA. Electronic address: sregot@jhmi.edu., Green R; Department of Molecular Biology and Genetics, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Howard Hughes Medical Institute, Chevy Chase, MD 20815, USA. Electronic address: ragreen@jhmi.edu.
المصدر: Cell [Cell] 2024 Jul 11; Vol. 187 (14), pp. 3652-3670.e40. Date of Electronic Publication: 2024 Jun 05.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Cell Press Country of Publication: United States NLM ID: 0413066 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1097-4172 (Electronic) Linking ISSN: 00928674 NLM ISO Abbreviation: Cell Subsets: MEDLINE
أسماء مطبوعة: Publication: Cambridge, Ma : Cell Press
Original Publication: Cambridge, MIT Press.
مواضيع طبية MeSH: Ultraviolet Rays*/adverse effects , Apoptosis*/radiation effects , DNA Damage*, Phosphorylation/radiation effects ; Humans ; Signal Transduction/radiation effects ; Protein Serine-Threonine Kinases/metabolism ; Stress, Physiological/radiation effects ; Ribosomes/metabolism ; Cell Death/radiation effects
مستخلص: While ultraviolet (UV) radiation damages DNA, eliciting the DNA damage response (DDR), it also damages RNA, triggering transcriptome-wide ribosomal collisions and eliciting a ribotoxic stress response (RSR). However, the relative contributions, timing, and regulation of these pathways in determining cell fate is unclear. Here we use time-resolved phosphoproteomic, chemical-genetic, single-cell imaging, and biochemical approaches to create a chronological atlas of signaling events activated in cells responding to UV damage. We discover that UV-induced apoptosis is mediated by the RSR kinase ZAK and not through the DDR. We identify two negative-feedback modules that regulate ZAK-mediated apoptosis: (1) GCN2 activation limits ribosomal collisions and attenuates ZAK-mediated RSR and (2) ZAK activity leads to phosphodegron autophosphorylation and its subsequent degradation. These events tune ZAK's activity to collision levels to establish regimes of homeostasis, tolerance, and death, revealing its key role as the cellular sentinel for nucleic acid damage.
Competing Interests: Declaration of interests R.G. is a member of the scientific advisory board (SAB) of Alltrna, Initial Therapeutics, and Arrakis Pharmaceuticals, consults for Vertex Pharmaceuticals, Brystol-Myers Squibb (Celgene), Monta Rosa Therapeutics, and Flagship Pioneering, and served on the SAB at Moderna. A.O. received consulting fees from Nine Square Therapeutics Co. L.C.C. is founder and member of the board of directors of Agios Pharmaceuticals; is founder and receives support from Petra Pharmaceuticals; is listed as inventor on a patent (WO2019232403A1, Weill Cornell Medicine); is co-founder and shareholder in Faeth Therapeutics; has equity in and consults for Cell Signaling Technologies, Volastra, Larkspur, and 1 Base Pharmaceuticals; and consults for Loxo-Lilly. T.M.Y.-B. is a co-founder of DeStroke. J.L.J received consulting fees from Scorpion Therapeutics and Volastra Therapeutics. R.G., S.R., N.K.S., and C.M. are listed as inventors on U.S. Provisional Patent Application No. 63/652,824, filed May 29, 2024.
(Copyright © 2024 The Authors. Published by Elsevier Inc. All rights reserved.)
References: Science. 2018 Aug 24;361(6404):806-810. (PMID: 30139873)
Elife. 2020 Sep 17;9:. (PMID: 32940599)
Genes Dev. 2000 Jun 15;14(12):1448-59. (PMID: 10859164)
Cell. 2009 Feb 20;136(4):731-45. (PMID: 19239892)
Elife. 2020 Apr 07;9:. (PMID: 32255427)
Mol Cell Biol. 1997 Jun;17(6):3373-81. (PMID: 9154836)
Nature. 2012 May 02;485(7396):109-13. (PMID: 22552098)
Nat Methods. 2007 Mar;4(3):207-14. (PMID: 17327847)
J Cell Biol. 1988 Mar;106(3):761-71. (PMID: 2450098)
Mol Cell Biol. 1998 Apr;18(4):1844-54. (PMID: 9528756)
Mol Cell. 2021 May 6;81(9):1879-1889.e6. (PMID: 33743194)
Curr Biol. 2002 Aug 6;12(15):1279-86. (PMID: 12176355)
Nature. 2015 Apr 30;520(7549):640-5. (PMID: 25901680)
Nat Commun. 2019 Dec 9;10(1):5611. (PMID: 31819057)
Cell Rep. 2021 Feb 23;34(8):108771. (PMID: 33626354)
Cancer Biol Ther. 2012 Sep;13(11):1072-81. (PMID: 22825331)
Proc Natl Acad Sci U S A. 2020 Jun 9;117(23):12806-12816. (PMID: 32444488)
Nat Commun. 2015 Sep 24;6:8350. (PMID: 26399197)
J Proteome Res. 2021 Jan 1;20(1):591-598. (PMID: 33190505)
Physiology (Bethesda). 2006 Oct;21:362-9. (PMID: 16990457)
Blood. 2023 Aug 17;142(7):629-642. (PMID: 37172201)
Anal Chem. 2019 Mar 19;91(6):4010-4016. (PMID: 30672687)
Mol Cell Proteomics. 2015 Sep;14(9):2394-404. (PMID: 25987413)
Mol Cell. 2017 Feb 16;65(4):743-750.e4. (PMID: 28065601)
Genes Dev. 2015 Nov 15;29(22):2331-6. (PMID: 26543160)
Elife. 2015 Feb 10;4:e05178. (PMID: 25668746)
J Biol Chem. 2005 May 13;280(19):19298-305. (PMID: 15737997)
J Clin Invest. 2022 Aug 15;132(16):. (PMID: 35763353)
J Proteome Res. 2020 Jan 3;19(1):554-560. (PMID: 31799850)
Mol Cell. 2022 Apr 21;82(8):1557-1572.e7. (PMID: 35180429)
Proteomics. 2011 May;11(10):2019-26. (PMID: 21500348)
J Virol. 1998 Nov;72(11):8463-71. (PMID: 9765382)
Genes Dev. 2000 Feb 15;14(4):397-402. (PMID: 10691732)
Elife. 2013 Nov 05;2:e00969. (PMID: 24192036)
J Proteomics. 2016 Oct 4;148:85-93. (PMID: 27432472)
Nat Rev Mol Cell Biol. 2019 Apr;20(4):199-210. (PMID: 30824861)
Science. 2003 Jun 6;300(5625):1542-8. (PMID: 12791985)
J Biol Chem. 1998 Jun 19;273(25):15794-803. (PMID: 9624179)
Elife. 2020 Aug 03;9:. (PMID: 32744497)
FEBS J. 2015 Sep;282(17):3275-85. (PMID: 25996081)
Nat Rev Mol Cell Biol. 2017 Oct;18(10):622-636. (PMID: 28811666)
Proc Natl Acad Sci U S A. 2006 Jun 27;103(26):9891-6. (PMID: 16788066)
Anal Chem. 2014 Jul 15;86(14):7150-8. (PMID: 24927332)
Nucleic Acids Res. 2020 Feb 20;48(3):1084-1096. (PMID: 31950154)
J Biol Chem. 2019 Oct 11;294(41):15158-15171. (PMID: 31439666)
Nature. 2009 Apr 9;458(7239):732-6. (PMID: 19360080)
Nat Rev Immunol. 2013 Sep;13(9):679-92. (PMID: 23954936)
J Cell Sci. 1992 Sep;103 ( Pt 1):97-103. (PMID: 1358902)
Genes Dev. 2005 May 1;19(9):1040-52. (PMID: 15833913)
PLoS One. 2009 Aug 06;4(8):e6529. (PMID: 19657394)
J Cell Biol. 2010 Jan 25;188(2):191-8. (PMID: 20100909)
Nat Rev Mol Cell Biol. 2021 May;22(5):346-366. (PMID: 33504982)
EMBO J. 2000 Dec 1;19(23):6517-26. (PMID: 11101524)
Mol Cell Biol. 2003 Jan;23(1):370-81. (PMID: 12482988)
Nature. 2003 Feb 27;421(6926):961-6. (PMID: 12607005)
Nature. 2020 Jul;583(7815):303-309. (PMID: 32612236)
Nat Rev Mol Cell Biol. 2018 Nov;19(11):731-745. (PMID: 30305710)
Blood. 2021 Feb 4;137(5):661-677. (PMID: 33197925)
Mol Cell. 2018 Nov 1;72(3):469-481.e7. (PMID: 30293783)
Cell Mol Life Sci. 2016 Jun;73(11-12):2405-10. (PMID: 27048813)
Nature. 2000 Nov 23;408(6811):433-9. (PMID: 11100718)
Mol Cell. 2017 Oct 19;68(2):361-373.e5. (PMID: 28943311)
EMBO J. 1988 Nov;7(11):3559-69. (PMID: 2850168)
J Am Soc Mass Spectrom. 2016 Oct;27(10):1620-5. (PMID: 27400695)
Nat Protoc. 2018 Jan;13(1):155-169. (PMID: 29266096)
EMBO J. 2019 Mar 1;38(5):. (PMID: 30609991)
Dev Cell. 2021 Jun 21;56(12):1712-1726.e6. (PMID: 34081908)
Cell Cycle. 2009 Apr 1;8(7):1044-52. (PMID: 19270522)
Proc Natl Acad Sci U S A. 1985 May;82(10):3262-6. (PMID: 2860667)
Annu Rev Biochem. 2021 Jun 20;90:403-429. (PMID: 33823649)
Mol Cell. 2021 Feb 4;81(3):614-628.e4. (PMID: 33338396)
J Proteome Res. 2019 Mar 1;18(3):1299-1306. (PMID: 30658528)
Sci Signal. 2019 Apr 30;12(579):. (PMID: 31040261)
Mol Cell. 2020 Nov 5;80(3):410-422.e6. (PMID: 33108758)
Cell Microbiol. 2008 Jul;10(7):1468-77. (PMID: 18331592)
Cell. 2010 Dec 23;143(7):1174-89. (PMID: 21183079)
Cell Metab. 2023 Dec 5;35(12):2216-2230.e8. (PMID: 37979583)
Science. 2024 May 3;384(6695):eadi2421. (PMID: 38696576)
Nat Protoc. 2016 Dec;11(12):2301-2319. (PMID: 27809316)
Genes Dev. 2012 Dec 15;26(24):2684-9. (PMID: 23249732)
Mol Cell. 2017 Feb 16;65(4):751-760.e4. (PMID: 28132843)
Nat Rev Genet. 2018 Jun;19(6):385-397. (PMID: 29556092)
Cancer Biol Ther. 2010 Aug 1;10(3):258-66. (PMID: 20559024)
Cell. 2014 Jun 19;157(7):1724-34. (PMID: 24949979)
Nat Biotechnol. 2006 Oct;24(10):1285-92. (PMID: 16964243)
Science. 2019 Oct 4;366(6461):109-115. (PMID: 31604311)
Microbiol Mol Biol Rev. 2011 Mar;75(1):50-83. (PMID: 21372320)
Cell. 2020 Jul 23;182(2):404-416.e14. (PMID: 32610081)
J Proteome Res. 2020 May 1;19(5):2026-2034. (PMID: 32126768)
Proc Natl Acad Sci U S A. 2021 Apr 6;118(14):. (PMID: 33790014)
Cell. 2013 Oct 10;155(2):369-83. (PMID: 24075009)
Proteomics. 2013 Jan;13(1):22-4. (PMID: 23148064)
Cold Spring Harb Perspect Biol. 2013 Sep 01;5(9):. (PMID: 24003211)
Cell. 1997 Dec 26;91(7):961-71. (PMID: 9428519)
Nat Genet. 2003 Apr;33(4):497-501. (PMID: 12640452)
Mol Cell Proteomics. 2019 Aug 9;18(8 suppl 1):S193-S201. (PMID: 31088857)
J Cell Sci. 2019 Nov 1;132(21):. (PMID: 31676663)
Cell Death Differ. 2018 Jan;25(1):104-113. (PMID: 29149101)
Nature. 2023 Jan;613(7945):759-766. (PMID: 36631611)
Cell. 2000 Oct 13;103(2):239-52. (PMID: 11057897)
Mol Cell. 2020 May 21;78(4):700-713.e7. (PMID: 32289254)
Nat Methods. 2016 Sep;13(9):731-40. (PMID: 27348712)
Cell. 2020 Jul 23;182(2):481-496.e21. (PMID: 32649862)
Crit Rev Biochem Mol Biol. 2009 Jan-Feb;44(1):34-49. (PMID: 19089684)
Mol Cell. 2021 Apr 1;81(7):1372-1383. (PMID: 33713598)
Nat Protoc. 2019 Jan;14(1):68-85. (PMID: 30464214)
Nat Methods. 2012 Jul;9(7):671-5. (PMID: 22930834)
Proc Natl Acad Sci U S A. 2021 Jul 20;118(29):. (PMID: 34272277)
Int J Mol Sci. 2021 Sep 04;22(17):. (PMID: 34502507)
Elife. 2020 Jul 13;9:. (PMID: 32657267)
Oncogene. 2001 Sep 20;20(42):6026-38. (PMID: 11593410)
Nat Commun. 2021 Mar 23;12(1):1836. (PMID: 33758175)
Nat Methods. 2022 Nov;19(11):1371-1375. (PMID: 36280721)
Curr Biol. 2000 Apr 20;10(8):479-82. (PMID: 10801416)
ACS Chem Biol. 2016 Jun 17;11(6):1595-602. (PMID: 26999302)
Mol Cell. 1998 Aug;2(2):223-32. (PMID: 9734359)
معلومات مُعتمدة: R35 GM133499 United States GM NIGMS NIH HHS; P30 CA008748 United States CA NCI NIH HHS; UL1 TR003098 United States TR NCATS NIH HHS; K99 GM146031 United States GM NIGMS NIH HHS; R37 GM059425 United States GM NIGMS NIH HHS
فهرسة مساهمة: Keywords: DNA damage response; GCN2; UV radiation; ZAK; apoptosis; collisions; phosphoproteomics; ribosomes; ribotoxic stress; signaling
المشرفين على المادة: EC 2.7.11.1 (Protein Serine-Threonine Kinases)
تواريخ الأحداث: Date Created: 20240606 Date Completed: 20240712 Latest Revision: 20240716
رمز التحديث: 20240716
مُعرف محوري في PubMed: PMC11246228
DOI: 10.1016/j.cell.2024.05.018
PMID: 38843833
قاعدة البيانات: MEDLINE
الوصف
تدمد:1097-4172
DOI:10.1016/j.cell.2024.05.018