Regulation of neuroendocrine plasticity by the RNA-binding protein ZFP36L1.


Journal

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

Informations de publication

Date de publication:
25 08 2022
Historique:
received: 21 09 2021
accepted: 08 07 2022
entrez: 25 8 2022
pubmed: 26 8 2022
medline: 30 8 2022
Statut: epublish

Résumé

Some small cell lung cancers (SCLCs) are highly sensitive to inhibitors of the histone demethylase LSD1. LSD1 inhibitors are thought to induce their anti-proliferative effects by blocking neuroendocrine differentiation, but the mechanisms by which LSD1 controls the SCLC neuroendocrine phenotype are not well understood. To identify genes required for LSD1 inhibitor sensitivity in SCLC, we performed a positive selection genome-wide CRISPR/Cas9 loss of function screen and found that ZFP36L1, an mRNA-binding protein that destabilizes mRNAs, is required for LSD1 inhibitor sensitivity. LSD1 binds and represses ZFP36L1 and upon LSD1 inhibition, ZFP36L1 expression is restored, which is sufficient to block the SCLC neuroendocrine differentiation phenotype and induce a non-neuroendocrine "inflammatory" phenotype. Mechanistically, ZFP36L1 binds and destabilizes SOX2 and INSM1 mRNAs, two transcription factors that are required for SCLC neuroendocrine differentiation. This work identifies ZFP36L1 as an LSD1 target gene that controls the SCLC neuroendocrine phenotype and demonstrates that modulating mRNA stability of lineage transcription factors controls neuroendocrine to non-neuroendocrine plasticity.

Identifiants

pubmed: 36008402
doi: 10.1038/s41467-022-31998-7
pii: 10.1038/s41467-022-31998-7
pmc: PMC9411550
doi:

Substances chimiques

Butyrate Response Factor 1 0
RNA-Binding Proteins 0
Repressor Proteins 0
Transcription Factors 0
ZFP36L1 protein, human 0
INSM1 protein, human 147955-03-1
Histone Demethylases EC 1.14.11.-

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

4998

Subventions

Organisme : NCI NIH HHS
ID : K08 CA222657
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA008748
Pays : United States
Organisme : NCI NIH HHS
ID : R35 CA263816
Pays : United States
Organisme : NCI NIH HHS
ID : R37 CA269990
Pays : United States

Informations de copyright

© 2022. The Author(s).

Références

Cancer Discov. 2021 Aug;11(8):1952-1969
pubmed: 33707236
Genes Dev. 2019 Dec 1;33(23-24):1718-1738
pubmed: 31727771
J Med Chem. 2020 Dec 10;63(23):14522-14529
pubmed: 33034194
Nature. 2017 May 18;545(7654):360-364
pubmed: 28489825
Sci Transl Med. 2011 Mar 23;3(75):75ra26
pubmed: 21430269
Lancet Oncol. 2015 Apr;16(4):e165-72
pubmed: 25846096
Cancer Res. 2016 Apr 1;76(7):1975-88
pubmed: 26837761
Nature. 2019 May;569(7757):503-508
pubmed: 31068700
Cell. 2018 Jul 26;174(3):549-563.e19
pubmed: 29937226
Cancer Discov. 2012 Sep;2(9):798-811
pubmed: 22961666
Bioinformatics. 2014 Apr 1;30(7):923-30
pubmed: 24227677
Cancer Cell. 2021 Mar 8;39(3):346-360.e7
pubmed: 33482121
Sci Adv. 2021 Feb 5;7(6):
pubmed: 33547076
J Natl Compr Canc Netw. 2013 Jan 1;11(1):78-98
pubmed: 23307984
Nat Commun. 2019 Dec 9;10(1):5622
pubmed: 31819055
Cancer Cell. 2014 Dec 8;26(6):909-922
pubmed: 25490451
Cell Rep. 2016 Aug 2;16(5):1259-1272
pubmed: 27452466
Nat Genet. 2012 Oct;44(10):1111-6
pubmed: 22941189
Cell. 2004 Dec 29;119(7):941-53
pubmed: 15620353
Cell. 2007 Mar 23;128(6):1063-76
pubmed: 17320161
Science. 1995 Mar 3;267(5202):1360-3
pubmed: 7871435
Commun Biol. 2021 Mar 9;4(1):314
pubmed: 33750914
Nat Immunol. 2010 Aug;11(8):717-24
pubmed: 20622884
Cell. 2021 Jun 24;184(13):3573-3587.e29
pubmed: 34062119
Proc Natl Acad Sci U S A. 2012 Nov 6;109(45):18499-504
pubmed: 23093672
Nat Methods. 2017 Nov;14(11):1083-1086
pubmed: 28991892
Cancer Res. 2008 Mar 15;68(6):1647-55
pubmed: 18339843
Cancer Cell. 2018 Mar 12;33(3):495-511.e12
pubmed: 29502954
Biochem Biophys Res Commun. 2019 Jul 12;515(1):214-221
pubmed: 31146914
Cancer Res. 2022 Jan 15;82(2):248-263
pubmed: 34810201
Nat Rev Cancer. 2019 May;19(5):289-297
pubmed: 30926931
Nat Commun. 2018 Dec 21;9(1):5416
pubmed: 30575746
Nat Rev Dis Primers. 2021 Jan 14;7(1):3
pubmed: 33446664
J Thorac Oncol. 2020 Dec;15(12):1823-1835
pubmed: 33011388
Sci Signal. 2019 Feb 05;12(567):
pubmed: 30723171
Genes Dev. 2021 Jun;35(11-12):847-869
pubmed: 34016693
Nat Genet. 2012 Oct;44(10):1104-10
pubmed: 22941188
Cancer Cell. 2015 Jul 13;28(1):57-69
pubmed: 26175415
Science. 2017 Jan 6;355(6320):84-88
pubmed: 28059768
Cell Rep. 2020 Dec 1;33(9):108460
pubmed: 33264623
Cancer Cell. 2017 Feb 13;31(2):286-299
pubmed: 28196596
Nature. 2012 Feb 01;482(7384):221-5
pubmed: 22297846
Cancer Res. 2020 Jan 15;80(2):219-233
pubmed: 31551365
Cell. 2007 Mar 9;128(5):889-900
pubmed: 17320163
J Clin Oncol. 2017 Sep 10;35(26):3065-3074
pubmed: 28498782
Am J Surg Pathol. 2017 Nov;41(11):1561-1569
pubmed: 28719469
Nucleic Acids Res. 2019 Jan 8;47(D1):D729-D735
pubmed: 30462313
Nature. 2015 Aug 6;524(7563):47-53
pubmed: 26168399
Oncogene. 2015 Nov 26;34(48):5869-78
pubmed: 25746006
Cancer Cell. 2020 Jul 13;38(1):60-78.e12
pubmed: 32473656
Sci Signal. 2013 Apr 02;6(269):pl1
pubmed: 23550210
Cancer Cell. 2019 Jul 8;36(1):17-34.e7
pubmed: 31287989
Mol Cancer Res. 2017 Aug;15(8):1012-1016
pubmed: 28442585
Oncogene. 2004 Nov 11;23(53):8673-80
pubmed: 15467755
J Clin Oncol. 2020 Dec 20;38(36):4260-4273
pubmed: 33052756
Proc Natl Acad Sci U S A. 2014 Oct 14;111(41):14788-93
pubmed: 25267614
Science. 2016 Apr 22;352(6284):453-9
pubmed: 27102483
Nucleic Acids Res. 2017 Jan 4;45(D1):D658-D662
pubmed: 27789702

Auteurs

Hsiao-Yun Chen (HY)

Department of Medical Oncology, Dana-Farber Cancer Institute and Brigham and Women's Hospital, Harvard Medical School, Boston, MA, 02215, USA.

Yavuz T Durmaz (YT)

Department of Medical Oncology, Dana-Farber Cancer Institute and Brigham and Women's Hospital, Harvard Medical School, Boston, MA, 02215, USA.

Yixiang Li (Y)

Department of Medical Oncology, Dana-Farber Cancer Institute and Brigham and Women's Hospital, Harvard Medical School, Boston, MA, 02215, USA.

Amin H Sabet (AH)

Department of Medical Oncology, Dana-Farber Cancer Institute and Brigham and Women's Hospital, Harvard Medical School, Boston, MA, 02215, USA.

Amir Vajdi (A)

Department of Informatics and Analytics, Dana-Farber Cancer Institute, Boston, MA, 02215, USA.

Thomas Denize (T)

Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, 02115, USA.

Emily Walton (E)

Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, 02115, USA.

Yasmin Nabil Laimon (YN)

Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, 02115, USA.

John G Doench (JG)

Broad Institute of MIT and Harvard, Cambridge, MA, 02142, USA.

Navin R Mahadevan (NR)

Department of Medical Oncology, Dana-Farber Cancer Institute and Brigham and Women's Hospital, Harvard Medical School, Boston, MA, 02215, USA.
Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, 02115, USA.

Julie-Aurore Losman (JA)

Department of Medical Oncology, Dana-Farber Cancer Institute and Brigham and Women's Hospital, Harvard Medical School, Boston, MA, 02215, USA.
Division of Hematology, Department of Medicine, Brigham and Women's Hospital, Boston, MA, 02115, USA.

David A Barbie (DA)

Department of Medical Oncology, Dana-Farber Cancer Institute and Brigham and Women's Hospital, Harvard Medical School, Boston, MA, 02215, USA.

Michael Y Tolstorukov (MY)

Department of Informatics and Analytics, Dana-Farber Cancer Institute, Boston, MA, 02215, USA.

Charles M Rudin (CM)

Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Triparna Sen (T)

Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY, USA.

Sabina Signoretti (S)

Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, 02115, USA.

Matthew G Oser (MG)

Department of Medical Oncology, Dana-Farber Cancer Institute and Brigham and Women's Hospital, Harvard Medical School, Boston, MA, 02215, USA. Matthew_Oser@dfci.harvard.edu.
Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, 02115, USA. Matthew_Oser@dfci.harvard.edu.

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