USP13 drives lung squamous cell carcinoma by switching lung club cell lineage plasticity.

GEMM Lineage plasticity Lung squamous cell carcinoma USP13 c-Myc

Journal

Molecular cancer
ISSN: 1476-4598
Titre abrégé: Mol Cancer
Pays: England
ID NLM: 101147698

Informations de publication

Date de publication:
13 Dec 2023
Historique:
received: 18 08 2023
accepted: 27 10 2023
medline: 14 12 2023
pubmed: 14 12 2023
entrez: 14 12 2023
Statut: epublish

Résumé

Lung squamous cell carcinoma (LUSC) is associated with high mortality and limited targeted therapies. USP13 is one of the most amplified genes in LUSC, yet its role in lung cancer is largely unknown. Here, we established a novel mouse model of LUSC by overexpressing USP13 on Kras

Identifiants

pubmed: 38093367
doi: 10.1186/s12943-023-01892-x
pii: 10.1186/s12943-023-01892-x
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

204

Subventions

Organisme : NCI NIH HHS
ID : R01 CA262418
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA262418
Pays : United States

Informations de copyright

© 2023. The Author(s).

Références

Siegel RL, Miller KD, Fuchs HE, Jemal A. Cancer statistics, 2022. CA Cancer J Clin. 2022;72(1):7–33.
doi: 10.3322/caac.21708 pubmed: 35020204
Thai AA, Solomon BJ, Sequist LV, Gainor JF, Heist RS. Lung cancer. Lancet. 2021;398(10299):535–54.
pubmed: 34273294 doi: 10.1016/S0140-6736(21)00312-3
Lau SCM, Pan Y, Velcheti V, Wong KK. Squamous cell lung cancer: Current landscape and future therapeutic options. Cancer Cell. 2022;40(11):1279–93.
pubmed: 36270277 doi: 10.1016/j.ccell.2022.09.018
Pan Y, Han H, Labbe KE, Zhang H, Wong KK. Recent advances in preclinical models for lung squamous cell carcinoma. Oncogene. 2021;40(16):2817–29.
pubmed: 33707749 doi: 10.1038/s41388-021-01723-7
Le Magnen C, Shen MM, Abate-Shen C. Lineage Plasticity in Cancer Progression and Treatment. Annu Rev Cancer Biol. 2018;2:271–89.
pubmed: 29756093 doi: 10.1146/annurev-cancerbio-030617-050224
Quintanal-Villalonga A, Chan JM, Yu HA, Pe’er D, Sawyers CL, Sen T, Rudin CM. Lineage plasticity in cancer: a shared pathway of therapeutic resistance. Nat Rev Clin Oncol. 2020;17(6):360–71.
pubmed: 32152485 pmcid: 7397755 doi: 10.1038/s41571-020-0340-z
Ferone G, Lee MC, Sage J, Berns A. Cells of origin of lung cancers: lessons from mouse studies. Genes Dev. 2020;34(15–16):1017–32.
pubmed: 32747478 pmcid: 7397855 doi: 10.1101/gad.338228.120
Hoadley KA, Yau C, Hinoue T, Wolf DM, Lazar AJ, Drill E, Shen R, Taylor AM, Cherniack AD, Thorsson V, et al. Cell-of-Origin Patterns Dominate the Molecular Classification of 10,000 Tumors from 33 Types of Cancer. Cell. 2018;173(2):291-304 e296.
pubmed: 29625048 pmcid: 5957518 doi: 10.1016/j.cell.2018.03.022
Nagaraj AS, Lahtela J, Hemmes A, Pellinen T, Blom S, Devlin JR, Salmenkivi K, Kallioniemi O, Mayranpaa MI, Narhi K, et al. Cell of Origin Links Histotype Spectrum to Immune Microenvironment Diversity in Non-small-Cell Lung Cancer Driven by Mutant Kras and Loss of Lkb1. Cell Rep. 2017;18(3):673–84.
pubmed: 28099846 doi: 10.1016/j.celrep.2016.12.059
Visvader JE. Cells of origin in cancer. Nature. 2011;469(7330):314–22.
pubmed: 21248838 doi: 10.1038/nature09781
Desai TJ, Brownfield DG, Krasnow MA. Alveolar progenitor and stem cells in lung development, renewal and cancer. Nature. 2014;507(7491):190–4.
pubmed: 24499815 pmcid: 4013278 doi: 10.1038/nature12930
Rock JR, Hogan BL. Epithelial progenitor cells in lung development, maintenance, repair, and disease. Annu Rev Cell Dev Biol. 2011;27:493–512.
pubmed: 21639799 doi: 10.1146/annurev-cellbio-100109-104040
Tata PR, Rajagopal J. Plasticity in the lung: making and breaking cell identity. Development. 2017;144(5):755–66.
pubmed: 28246210 pmcid: 5374348 doi: 10.1242/dev.143784
Chen Z, Fillmore CM, Hammerman PS, Kim CF, Wong KK. Non-small-cell lung cancers: a heterogeneous set of diseases. Nat Rev Cancer. 2014;14(8):535–46.
pubmed: 25056707 pmcid: 5712844 doi: 10.1038/nrc3775
Garraway LA, Lander ES. Lessons from the cancer genome. Cell. 2013;153(1):17–37.
pubmed: 23540688 doi: 10.1016/j.cell.2013.03.002
Morrisey EE, Hogan BL. Preparing for the first breath: genetic and cellular mechanisms in lung development. Dev Cell. 2010;18(1):8–23.
pubmed: 20152174 pmcid: 3736813 doi: 10.1016/j.devcel.2009.12.010
Bass AJ, Watanabe H, Mermel CH, Yu S, Perner S, Verhaak RG, Kim SY, Wardwell L, Tamayo P, Gat-Viks I, et al. SOX2 is an amplified lineage-survival oncogene in lung and esophageal squamous cell carcinomas. Nat Genet. 2009;41(11):1238–42.
pubmed: 19801978 pmcid: 2783775 doi: 10.1038/ng.465
Weir BA, Woo MS, Getz G, Perner S, Ding L, Beroukhim R, Lin WM, Province MA, Kraja A, Johnson LA, et al. Characterizing the cancer genome in lung adenocarcinoma. Nature. 2007;450(7171):893–8.
pmcid: 2538683 doi: 10.1038/nature06358
Teixeira VH, Pipinikas CP, Pennycuick A, Lee-Six H, Chandrasekharan D, Beane J, Morris TJ, Karpathakis A, Feber A, Breeze CE, et al. Deciphering the genomic, epigenomic, and transcriptomic landscapes of pre-invasive lung cancer lesions. Nat Med. 2019;25(3):517–25.
pubmed: 30664780 pmcid: 7614970 doi: 10.1038/s41591-018-0323-0
Fields AP, Justilien V, Murray NR. The chromosome 3q26 OncCassette: A multigenic driver of human cancer. Adv Biol Regul. 2016;60:47–63.
pubmed: 26754874 doi: 10.1016/j.jbior.2015.10.009
Foster JG, Wong SC, Sharp TV. The hypoxic tumor microenvironment: driving the tumorigenesis of non-small-cell lung cancer. Future Oncol. 2014;10(16):2659–74.
pubmed: 25531051 doi: 10.2217/fon.14.201
Ooi AT, Gower AC, Zhang KX, Vick JL, Hong L, Nagao B, Wallace WD, Elashoff DA, Walser TC, Dubinett SM, et al. Molecular profiling of premalignant lesions in lung squamous cell carcinomas identifies mechanisms involved in stepwise carcinogenesis. Cancer Prev Res (Phila). 2014;7(5):487–95.
pubmed: 24618292 doi: 10.1158/1940-6207.CAPR-13-0372
Acker F, Stratmann J, Aspacher L, Nguyen NTT, Wagner S, Serve H, Wild PJ, Sebastian M. KRAS Mutations in Squamous Cell Carcinomas of the Lung. Front Oncol. 2021;11:788084.
pubmed: 34976827 pmcid: 8714661 doi: 10.3389/fonc.2021.788084
Herbst RS, Morgensztern D, Boshoff C. The biology and management of non-small cell lung cancer. Nature. 2018;553(7689):446–54.
pubmed: 29364287 doi: 10.1038/nature25183
Kerr KM, Dafni U, Schulze K, Thunnissen E, Bubendorf L, Hager H, Finn S, Biernat W, Vliegen L, Losa JH, et al. Prevalence and clinical association of gene mutations through multiplex mutation testing in patients with NSCLC: results from the ETOP Lungscape Project. Ann Oncol. 2018;29(1):200–8.
pubmed: 29186353 doi: 10.1093/annonc/mdx629
Ruiz EJ, Diefenbacher ME, Nelson JK, Sancho R, Pucci F, Chakraborty A, Moreno P, Annibaldi A, Liccardi G, Encheva V, et al. LUBAC determines chemotherapy resistance in squamous cell lung cancer. J Exp Med. 2019;216(2):450–65.
pubmed: 30642944 pmcid: 6363428 doi: 10.1084/jem.20180742
Komander D, Clague MJ, Urbe S. Breaking the chains: structure and function of the deubiquitinases. Nat Rev Mol Cell Biol. 2009;10(8):550–63.
pubmed: 19626045 doi: 10.1038/nrm2731
Li X, Yang G, Zhang W, Qin B, Ye Z, Shi H, Zhao X, Chen Y, Song B, Mei Z, et al. USP13: Multiple Functions and Target Inhibition. Front Cell Dev Biol. 2022;10:875124.
pubmed: 35445009 pmcid: 9014248 doi: 10.3389/fcell.2022.875124
Han C, Yang L, Choi HH, Baddour J, Achreja A, Liu Y, Li Y, Li J, Wan G, Huang C, et al. Amplification of USP13 drives ovarian cancer metabolism. Nat Commun. 2016;7:13525.
pubmed: 27892457 pmcid: 5133706 doi: 10.1038/ncomms13525
Kwon J, Choi H, Ware AD, Morillo BC, Wang H, Bouker KB, Lu X, Waldman T, Han C. USP13 promotes development and metastasis of high-grade serous ovarian carcinoma in a novel mouse model. Oncogene. 2022;41(13):1974–85.
pubmed: 35173307 pmcid: 8956511 doi: 10.1038/s41388-022-02224-x
Fang X, Zhou W, Wu Q, Huang Z, Shi Y, Yang K, Chen C, Xie Q, Mack SC, Wang X, et al. Deubiquitinase USP13 maintains glioblastoma stem cells by antagonizing FBXL14-mediated Myc ubiquitination. J Exp Med. 2017;214(1):245–67.
pubmed: 27923907 pmcid: 5206492 doi: 10.1084/jem.20151673
Zhang S, Zhang M, Jing Y, Yin X, Ma P, Zhang Z, Wang X, Di W, Zhuang G. Deubiquitinase USP13 dictates MCL1 stability and sensitivity to BH3 mimetic inhibitors. Nat Commun. 2018;9(1):215.
pubmed: 29335437 pmcid: 5768685 doi: 10.1038/s41467-017-02693-9
Zhao X, Fiske B, Kawakami A, Li J, Fisher DE. Regulation of MITF stability by the USP13 deubiquitinase. Nat Commun. 2011;2:414.
pubmed: 21811243 doi: 10.1038/ncomms1421
Man X, Piao C, Lin X, Kong C, Cui X, Jiang Y. USP13 functions as a tumor suppressor by blocking the NF-kB-mediated PTEN downregulation in human bladder cancer. J Exp Clin Cancer Res. 2019;38(1):259.
pubmed: 31200745 pmcid: 6570860 doi: 10.1186/s13046-019-1262-4
Qu Z, Zhang R, Su M, Liu W. USP13 serves as a tumor suppressor via the PTEN/AKT pathway in oral squamous cell carcinoma. Cancer Manag Res. 2019;11:9175–83.
pubmed: 31802942 pmcid: 6829296 doi: 10.2147/CMAR.S186829
Xiang S, Fang J, Wang S, Deng B, Zhu L. MicroRNA-135b regulates the stability of PTEN and promotes glycolysis by targeting USP13 in human colorectal cancers. Oncol Rep. 2015;33(3):1342–8.
pubmed: 25571954 doi: 10.3892/or.2014.3694
Zhang J, Zhang P, Wei Y, Piao HL, Wang W, Maddika S, Wang M, Chen D, Sun Y, Hung MC, et al. Deubiquitylation and stabilization of PTEN by USP13. Nat Cell Biol. 2013;15(12):1486–94.
pubmed: 24270891 pmcid: 3951854 doi: 10.1038/ncb2874
Kasinski AL, Slack FJ. Generation of Mouse Lung Epithelial Cells. Bio Protoc. 2013;3(15):e837.
pubmed: 27239482 doi: 10.21769/BioProtoc.837
Prieto-Garcia C, Hartmann O, Reissland M, Braun F, Fischer T, Walz S, Schulein-Volk C, Eilers U, Ade CP, Calzado MA, et al. Maintaining protein stability of ∆Np63 via USP28 is required by squamous cancer cells. EMBO Mol Med. 2020;12(4):e11101.
pubmed: 32128997 pmcid: 7136964 doi: 10.15252/emmm.201911101
DuPage M, Dooley AL, Jacks T. Conditional mouse lung cancer models using adenoviral or lentiviral delivery of Cre recombinase. Nat Protoc. 2009;4(7):1064–72.
pubmed: 19561589 pmcid: 2757265 doi: 10.1038/nprot.2009.95
Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15(12):550.
pubmed: 25516281 pmcid: 4302049 doi: 10.1186/s13059-014-0550-8
Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A. 2005;102(43):15545–50.
pubmed: 16199517 pmcid: 1239896 doi: 10.1073/pnas.0506580102
Liberzon A, Subramanian A, Pinchback R, Thorvaldsdottir H, Tamayo P, Mesirov JP. Molecular signatures database (MSigDB) 3.0. Bioinformatics. 2011;27(12):1739–40.
pubmed: 21546393 pmcid: 3106198 doi: 10.1093/bioinformatics/btr260
Kramer A, Green J, Pollard J Jr, Tugendreich S. Causal analysis approaches in Ingenuity Pathway Analysis. Bioinformatics. 2014;30(4):523–30.
pubmed: 24336805 doi: 10.1093/bioinformatics/btt703
Jackson EL, Olive KP, Tuveson DA, Bronson R, Crowley D, Brown M, Jacks T. The differential effects of mutant p53 alleles on advanced murine lung cancer. Cancer Res. 2005;65(22):10280–8.
pubmed: 16288016 doi: 10.1158/0008-5472.CAN-05-2193
Jackson EL, Willis N, Mercer K, Bronson RT, Crowley D, Montoya R, Jacks T, Tuveson DA. Analysis of lung tumor initiation and progression using conditional expression of oncogenic K-ras. Genes Dev. 2001;15(24):3243–8.
pubmed: 11751630 pmcid: 312845 doi: 10.1101/gad.943001
Farrell AS, Joly MM, Allen-Petersen BL, Worth PJ, Lanciault C, Sauer D, Link J, Pelz C, Heiser LM, Morton JP, et al. MYC regulates ductal-neuroendocrine lineage plasticity in pancreatic ductal adenocarcinoma associated with poor outcome and chemoresistance. Nat Commun. 2017;8(1):1728.
pubmed: 29170413 pmcid: 5701042 doi: 10.1038/s41467-017-01967-6
Mollaoglu G, Jones A, Wait SJ, Mukhopadhyay A, Jeong S, Arya R, Camolotto SA, Mosbruger TL, Stubben CJ, Conley CJ, et al. The Lineage-Defining Transcription Factors SOX2 and NKX2-1 Determine Lung Cancer Cell Fate and Shape the Tumor Immune Microenvironment. Immunity. 2018;49(4):764-779 e769.
pubmed: 30332632 pmcid: 6197489 doi: 10.1016/j.immuni.2018.09.020
Camolotto SA, Pattabiraman S, Mosbruger TL, Jones A, Belova VK, Orstad G, Streiff M, Salmond L, Stubben C, Kaestner KH, et al. FoxA1 and FoxA2 drive gastric differentiation and suppress squamous identity in NKX2-1-negative lung cancer. Elife. 2018;7:e38579.
pubmed: 30475207 pmcid: 6303105 doi: 10.7554/eLife.38579
Wilkerson MD, Yin X, Hoadley KA, Liu Y, Hayward MC, Cabanski CR, Muldrew K, Miller CR, Randell SH, Socinski MA, et al. Lung squamous cell carcinoma mRNA expression subtypes are reproducible, clinically important, and correspond to normal cell types. Clin Cancer Res. 2010;16(19):4864–75.
pubmed: 20643781 pmcid: 2953768 doi: 10.1158/1078-0432.CCR-10-0199
Huang J, Gu ZL, Chen W, Xu YY, Chen M. Knockdown of ubiquitin-specific peptidase 13 inhibits cell growth of hepatocellular carcinoma by reducing c-Myc expression. Kaohsiung J Med Sci. 2020;36(8):615–21.
pubmed: 32255563 doi: 10.1002/kjm2.12209
Liu J, Xia H, Kim M, Xu L, Li Y, Zhang L, Cai Y, Norberg HV, Zhang T, Furuya T, et al. Beclin1 controls the levels of p53 by regulating the deubiquitination activity of USP10 and USP13. Cell. 2011;147(1):223–34.
pubmed: 21962518 pmcid: 3441147 doi: 10.1016/j.cell.2011.08.037
He X, Kim JS, Diaz-Martinez LA, Han C, Lane WS, Budnik B, Waldman T. USP13 interacts with cohesin and regulates its ubiquitination in human cells. J Biol Chem. 2021;296:100194.
pubmed: 33334891 doi: 10.1074/jbc.RA120.015762
Seguin L, Durandy M, Feral CC. Lung Adenocarcinoma Tumor Origin: A Guide for Personalized Medicine. Cancers (Basel). 2022;14(7):1759.
pubmed: 35406531 doi: 10.3390/cancers14071759
Sutherland KD, Song JY, Kwon MC, Proost N, Zevenhoven J, Berns A. Multiple cells-of-origin of mutant K-Ras-induced mouse lung adenocarcinoma. Proc Natl Acad Sci U S A. 2014;111(13):4952–7.
pubmed: 24586047 pmcid: 3977239 doi: 10.1073/pnas.1319963111
Xu X, Rock JR, Lu Y, Futtner C, Schwab B, Guinney J, Hogan BL, Onaitis MW. Evidence for type II cells as cells of origin of K-Ras-induced distal lung adenocarcinoma. Proc Natl Acad Sci U S A. 2012;109(13):4910–5.
pubmed: 22411819 pmcid: 3323959 doi: 10.1073/pnas.1112499109
Rosigkeit S, Kruchem M, Thies D, Kreft A, Eichler E, Boegel S, Jansky S, Siegl D, Kaps L, Pickert G, et al. Definitive evidence for Club cells as progenitors for mutant Kras/Trp53-deficient lung cancer. Int J Cancer. 2021;149(9):1670–82.
pubmed: 34331774 doi: 10.1002/ijc.33756
Quintanal-Villalonga A, Taniguchi H, Zhan YA, Hasan MM, Chavan SS, Meng F, Uddin F, Allaj V, Manoj P, Shah NS, et al. Comprehensive molecular characterization of lung tumors implicates AKT and MYC signaling in adenocarcinoma to squamous cell transdifferentiation. J Hematol Oncol. 2021;14(1):170.
pubmed: 34656143 pmcid: 8520275 doi: 10.1186/s13045-021-01186-z
Kishimoto Y, Murakami Y, Shiraishi M, Hayashi K, Sekiya T. Aberrations of the p53 tumor suppressor gene in human non-small cell carcinomas of the lung. Cancer Res. 1992;52(17):4799–804.
pubmed: 1324794
Tammemagi MC, McLaughlin JR, Bull SB. Meta-analyses of p53 tumor suppressor gene alterations and clinicopathological features in resected lung cancers. Cancer Epidemiol Biomarkers Prev. 1999;8(7):625–34.
pubmed: 10428201
Ku SY, Rosario S, Wang Y, Mu P, Seshadri M, Goodrich ZW, Goodrich MM, Labbe DP, Gomez EC, Wang J, et al. Rb1 and Trp53 cooperate to suppress prostate cancer lineage plasticity, metastasis, and antiandrogen resistance. Science. 2017;355(6320):78–83.
pubmed: 28059767 pmcid: 5367887 doi: 10.1126/science.aah4199
Meuwissen R, Linn SC, Linnoila RI, Zevenhoven J, Mooi WJ, Berns A. Induction of small cell lung cancer by somatic inactivation of both Trp53 and Rb1 in a conditional mouse model. Cancer Cell. 2003;4(3):181–9.
pubmed: 14522252 doi: 10.1016/S1535-6108(03)00220-4
Mu P, Zhang Z, Benelli M, Karthaus WR, Hoover E, Chen CC, Wongvipat J, Ku SY, Gao D, Cao Z, et al. SOX2 promotes lineage plasticity and antiandrogen resistance in TP53- and RB1-deficient prostate cancer. Science. 2017;355(6320):84–8.
pubmed: 28059768 pmcid: 5247742 doi: 10.1126/science.aah4307
Niederst MJ, Sequist LV, Poirier JT, Mermel CH, Lockerman EL, Garcia AR, Katayama R, Costa C, Ross KN, Moran T, et al. RB loss in resistant EGFR mutant lung adenocarcinomas that transform to small-cell lung cancer. Nat Commun. 2015;6:6377.
pubmed: 25758528 doi: 10.1038/ncomms7377
Offin M, Chan JM, Tenet M, Rizvi HA, Shen R, Riely GJ, Rekhtman N, Daneshbod Y, Quintanal-Villalonga A, Penson A, et al. Concurrent RB1 and TP53 Alterations Define a Subset of EGFR-Mutant Lung Cancers at risk for Histologic Transformation and Inferior Clinical Outcomes. J Thorac Oncol. 2019;14(10):1784–93.
pubmed: 31228622 pmcid: 6764905 doi: 10.1016/j.jtho.2019.06.002
McConnell AM, Yao C, Yeckes AR, Wang Y, Selvaggio AS, Tang J, Kirsch DG, Stripp BR. p53 Regulates Progenitor Cell Quiescence and Differentiation in the Airway. Cell Rep. 2016;17(9):2173–82.
pubmed: 27880895 doi: 10.1016/j.celrep.2016.11.007
Zhou Q, Lin M, Feng X, Ma F, Zhu Y, Liu X, Qu C, Sui H, Sun B, Zhu A, et al. Targeting CLK3 inhibits the progression of cholangiocarcinoma by reprogramming nucleotide metabolism. J Exp Med. 2020;217(8):e20191779.
pubmed: 32453420 pmcid: 7398168 doi: 10.1084/jem.20191779
Davis RJ, Welcker M, Clurman BE. Tumor suppression by the Fbw7 ubiquitin ligase: mechanisms and opportunities. Cancer Cell. 2014;26(4):455–64.
pubmed: 25314076 pmcid: 4227608 doi: 10.1016/j.ccell.2014.09.013
Welcker M, Clurman BE. FBW7 ubiquitin ligase: a tumour suppressor at the crossroads of cell division, growth and differentiation. Nat Rev Cancer. 2008;8(2):83–93.
pubmed: 18094723 doi: 10.1038/nrc2290
Ferone G, Song JY, Sutherland KD, Bhaskaran R, Monkhorst K, Lambooij JP, Proost N, Gargiulo G, Berns A. SOX2 Is the Determining Oncogenic Switch in Promoting Lung Squamous Cell Carcinoma from Different Cells of Origin. Cancer Cell. 2016;30(4):519–32.
pubmed: 27728803 pmcid: 5065004 doi: 10.1016/j.ccell.2016.09.001
Fukazawa T, Guo M, Ishida N, Yamatsuji T, Takaoka M, Yokota E, Haisa M, Miyake N, Ikeda T, Okui T, et al. SOX2 suppresses CDKN1A to sustain growth of lung squamous cell carcinoma. Sci Rep. 2016;6:20113.
pubmed: 26846300 pmcid: 4742851 doi: 10.1038/srep20113
Jeong Y, Hoang NT, Lovejoy A, Stehr H, Newman AM, Gentles AJ, Kong W, Truong D, Martin S, Chaudhuri A, et al. Role of KEAP1/NRF2 and TP53 Mutations in Lung Squamous Cell Carcinoma Development and Radiation Resistance. Cancer Discov. 2017;7(1):86–101.
pubmed: 27663899 doi: 10.1158/2159-8290.CD-16-0127
Mukhopadhyay A, Berrett KC, Kc U, Clair PM, Pop SM, Carr SR, Witt BL, Oliver TG. Sox2 cooperates with Lkb1 loss in a mouse model of squamous cell lung cancer. Cell Rep. 2014;8(1):40–9.
pubmed: 24953650 pmcid: 4410849 doi: 10.1016/j.celrep.2014.05.036
Tata PR, Chow RD, Saladi SV, Tata A, Konkimalla A, Bara A, Montoro D, Hariri LP, Shih AR, Mino-Kenudson M, et al. Developmental History Provides a Roadmap for the Emergence of Tumor Plasticity. Dev Cell. 2018;44(6):679-693 e675.
pubmed: 29587142 pmcid: 5875457 doi: 10.1016/j.devcel.2018.02.024
Watanabe H, Ma Q, Peng S, Adelmant G, Swain D, Song W, Fox C, Francis JM, Pedamallu CS, DeLuca DS, et al. SOX2 and p63 colocalize at genetic loci in squamous cell carcinomas. J Clin Invest. 2014;124(4):1636–45.
pubmed: 24590290 pmcid: 3973117 doi: 10.1172/JCI71545
Xu X, Huang L, Futtner C, Schwab B, Rampersad RR, Lu Y, Sporn TA, Hogan BL, Onaitis MW. The cell of origin and subtype of K-Ras-induced lung tumors are modified by Notch and Sox2. Genes Dev. 2014;28(17):1929–39.
pubmed: 25184679 pmcid: 4197950 doi: 10.1101/gad.243717.114
Maeda Y, Tsuchiya T, Hao H, Tompkins DH, Xu Y, Mucenski ML, Du L, Keiser AR, Fukazawa T, Naomoto Y, et al. Kras(G12D) and Nkx2-1 haploinsufficiency induce mucinous adenocarcinoma of the lung. J Clin Invest. 2012;122(12):4388–400.
pubmed: 23143308 pmcid: 3533546 doi: 10.1172/JCI64048
Snyder EL, Watanabe H, Magendantz M, Hoersch S, Chen TA, Wang DG, Crowley D, Whittaker CA, Meyerson M, Kimura S, et al. Nkx2-1 represses a latent gastric differentiation program in lung adenocarcinoma. Mol Cell. 2013;50(2):185–99.
pubmed: 23523371 pmcid: 3721642 doi: 10.1016/j.molcel.2013.02.018
Orstad G, Fort G, Parnell TJ, Jones A, Stubben C, Lohman B, Gillis KL, Orellana W, Tariq R, Klingbeil O, et al. FoxA1 and FoxA2 control growth and cellular identity in NKX2-1-positive lung adenocarcinoma. Dev Cell. 2022;57(15):1866-1882 e1810.
pubmed: 35835117 pmcid: 9378547 doi: 10.1016/j.devcel.2022.06.017
Hou S, Han X, Ji H. Squamous Transition of Lung Adenocarcinoma and Drug Resistance. Trends Cancer. 2016;2(9):463–6.
pubmed: 28741476 doi: 10.1016/j.trecan.2016.08.002
Kuiper JL, Ronden MI, Becker A, Heideman DA, van Hengel P, Ylstra B, Thunnissen E, Smit EF. Transformation to a squamous cell carcinoma phenotype of an EGFR-mutated NSCLC patient after treatment with an EGFR-tyrosine kinase inhibitor. J Clin Pathol. 2015;68(4):320–1.
pubmed: 25661795 doi: 10.1136/jclinpath-2015-202866
Park S, Shim JH, Lee B, Cho I, Park WY, Kim Y, Lee SH, Choi Y, Han J, Ahn JS, et al. Paired genomic analysis of squamous cell carcinoma transformed from EGFR-mutated lung adenocarcinoma. Lung Cancer. 2019;134:7–15.
pubmed: 31319998 doi: 10.1016/j.lungcan.2019.05.024
Schoenfeld AJ, Chan JM, Kubota D, Sato H, Rizvi H, Daneshbod Y, Chang JC, Paik PK, Offin M, Arcila ME, et al. Tumor Analyses Reveal Squamous Transformation and Off-Target Alterations As Early Resistance Mechanisms to First-line Osimertinib in EGFR-Mutant Lung Cancer. Clin Cancer Res. 2020;26(11):2654–63.
pubmed: 31911548 pmcid: 7448565 doi: 10.1158/1078-0432.CCR-19-3563
Toyokawa G, Bersani F, Bironzo P, Picca F, Tabbo F, Haratake N, Takenaka T, Seto T, Yoshizumi T, Novello S, et al. Tumor plasticity and therapeutic resistance in oncogene-addicted non-small cell lung cancer: from preclinical observations to clinical implications. Crit Rev Oncol Hematol. 2023;184:103966.
pubmed: 36925092 doi: 10.1016/j.critrevonc.2023.103966
Awad MM, Liu S, Rybkin II, Arbour KC, Dilly J, Zhu VW, Johnson ML, Heist RS, Patil T, Riely GJ, et al. Acquired Resistance to KRAS(G12C) Inhibition in Cancer. N Engl J Med. 2021;384(25):2382–93.
pubmed: 34161704 pmcid: 8864540 doi: 10.1056/NEJMoa2105281
Han X, Li F, Fang Z, Gao Y, Li F, Fang R, Yao S, Sun Y, Li L, Zhang W, et al. Transdifferentiation of lung adenocarcinoma in mice with Lkb1 deficiency to squamous cell carcinoma. Nat Commun. 2014;5:3261.
pubmed: 24531128 doi: 10.1038/ncomms4261
Ji H, Ramsey MR, Hayes DN, Fan C, McNamara K, Kozlowski P, Torrice C, Wu MC, Shimamura T, Perera SA, et al. LKB1 modulates lung cancer differentiation and metastasis. Nature. 2007;448(7155):807–10.
pubmed: 17676035 doi: 10.1038/nature06030
Xu C, Fillmore CM, Koyama S, Wu H, Zhao Y, Chen Z, Herter-Sprie GS, Akbay EA, Tchaicha JH, Altabef A, et al. Loss of Lkb1 and Pten leads to lung squamous cell carcinoma with elevated PD-L1 expression. Cancer Cell. 2014;25(5):590–604.
pubmed: 24794706 pmcid: 4112370 doi: 10.1016/j.ccr.2014.03.033
Becker W. Therapy of thyroid gland autonomy. Klin Wochenschr. 1990;68(12):640–6.
pubmed: 2198385 doi: 10.1007/BF01660967
Chang WH, Lai AG. Aberrations in Notch-Hedgehog signalling reveal cancer stem cells harbouring conserved oncogenic properties associated with hypoxia and immunoevasion. Br J Cancer. 2019;121(8):666–78.
pubmed: 31523055 pmcid: 6889439 doi: 10.1038/s41416-019-0572-9
Li X, Li C, Guo C, Zhao Q, Cao J, Huang HY, Yue M, Xue Y, Jin Y, Hu L, et al. PI3K/Akt/mTOR signaling orchestrates the phenotypic transition and chemo-resistance of small cell lung cancer. J Genet Genomics. 2021;48(7):640–51.
pubmed: 34167917 doi: 10.1016/j.jgg.2021.04.001
Chen Y, Toth R, Chocarro S, Weichenhan D, Hey J, Lutsik P, Sawall S, Stathopoulos GT, Plass C, Sotillo R. Club cells employ regeneration mechanisms during lung tumorigenesis. Nat Commun. 2022;13(1):4557.
pubmed: 35931677 pmcid: 9356049 doi: 10.1038/s41467-022-32052-2
Sun XX, Yu Q. Intra-tumor heterogeneity of cancer cells and its implications for cancer treatment. Acta Pharmacol Sin. 2015;36(10):1219–27.
pubmed: 26388155 pmcid: 4648179 doi: 10.1038/aps.2015.92
Ireland AS, Micinski AM, Kastner DW, Guo B, Wait SJ, Spainhower KB, Conley CC, Chen OS, Guthrie MR, Soltero D, et al. MYC Drives Temporal Evolution of Small Cell Lung Cancer Subtypes by Reprogramming Neuroendocrine Fate. Cancer Cell. 2020;38(1):60-78 e12.
pubmed: 32473656 pmcid: 7393942 doi: 10.1016/j.ccell.2020.05.001

Auteurs

Juntae Kwon (J)

Department of Oncology, Georgetown University School of Medicine, Washington D.C, USA.

Jinmin Zhang (J)

Department of Biochemistry and Molecular & Cellular Biology, Georgetown University School of Medicine, Washington D.C, USA.

Boram Mok (B)

Department of Oncology, Georgetown University School of Medicine, Washington D.C, USA.

Samuel Allsup (S)

Department of Biochemistry and Molecular & Cellular Biology, Georgetown University School of Medicine, Washington D.C, USA.

Chul Kim (C)

Division of Hematology and Oncology, Georgetown University School of Medicine, Washington D.C, USA.
MedStar Georgetown University Hospital, Washington D.C, USA.
Lombardi Comprehensive Cancer Center, Washington D.C, USA.

Jeffrey Toretsky (J)

Department of Oncology, Georgetown University School of Medicine, Washington D.C, USA.
Lombardi Comprehensive Cancer Center, Washington D.C, USA.
Departments of Pediatrics, Washington D.C, USA.

Cecil Han (C)

Department of Oncology, Georgetown University School of Medicine, Washington D.C, USA. ch1182@georgetown.edu.
Lombardi Comprehensive Cancer Center, Washington D.C, USA. ch1182@georgetown.edu.

Classifications MeSH