P53-R273H mutation enhances colorectal cancer stemness through regulating specific lncRNAs

Yuechao Zhao1, Yiran Li1, Jie Sheng1, Fan Wu1, Kai Li1, R. Stephanie Huang1, Xiaojuan Wang1, Tao Jiao1, Xin Guan1, Yan Lu1, Xiaohong Chen2, Zhiwen Luo2, Yanchi Zhou2, Hanjie Hu2, Wenjie Liu2, Boyu Du3, Shiying Miao1, Jianqiang Cai2, Linfang Wang1, Haitao Zhao2, Jianming Ying4, Xinyu Bi2, Wei Song1
1Department of Biochemistry and Molecular Biology, State Key Laboratory of Medical Molecular Biology, Institute of Basic Medical Sciences Chinese Academy of Medical Sciences, School of Basic Medicine Peking Union Medical College, Beijing, 100005, China
2Department of Hepatobiliary Surgery, State Key Laboratory of Molecular Oncology, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, 100021, China
3Department of Medical Biology, School of Basic Medical Sciences, Hubei University of Medicine, Shiyan 442000, China
4Department of Pathology, State Key Laboratory of Molecular Oncology, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, 100021, China

Tóm tắt

Từ khóa


Tài liệu tham khảo

Valastyan S, Weinberg RA. Tumor metastasis: molecular insights and evolving paradigms. Cell. 2011;147(2):275–92.

Karsa LV, Lignini TA, Patnick J, Lambert R, Sauvaget C. The dimensions of the CRC problem. Best Pract Res Clin Gastroenterol. 2010;24(4):381–96.

Batlle E, Clevers H. Cancer stem cells revisited. Nat Med. 2017;23(10):1124–34.

Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH, Jones DL, Visvader J, Weissman IL, Wahl GM. Cancer stem cells-perspectives on current status and future directions: AACR work shop on cancer stem cells. Cancer Res Cancer Res. 2006;66(19):9339–44.

Kastenhuber ER, Lowe SW. Putting p53 in context. Cell. 2017;170(6):1062–78.

Petitjean A, Mathe E, Kato S, Ishioka C, Tavtigian SV, Hainaut P, Olivier M. Impact of mutant p53 functional properties on TP53 mutation patterns and tumor phenotype: lessons from recent developments in the IARC TP53 database. Hum Mutat. 2007;28(6):622–9.

Hosain SB, Khiste SK, Uddin MB, Vorubindi V, Ingram C, Zhang S, Hill RA, Gu X, Liu YY. Inhibition of glucosylceramide synthase eliminates the oncogenic function of p53 R273H mutant in the epithelial-mesenchymal transition and induced pluripotency of colon cancer cells. Oncotarget. 2016;7(37):60575–92.

Yan H, Bu P. Non-coding RNAs in cancer stem cells. Cancer Lett. 2018;421:121–6.

Kogo R, Shimamura T, Mimori K, Kawahara K, Imoto S, Sudo T, Tanaka F, Shibata K, Suzuki A, Komune S, Miyano S, Mori M. Long noncoding RNA HOTAIR regulates polycomb-dependent chromatin modification and is associated with poor prognosis in colorectal cancers. Cancer Res. 2011;71(20):6320–6.

Ge X, Chen Y, Liao X, Liu D, Li F, Ruan H, Jia W. Overexpression of long noncoding RNA PCAT-1 is anovel biomarker of poor prognosis in patients with colorectal cancer. Med Oncol. 2013;30(2):588.

Kopp F, Mendell JT. Functional classification and experimental dissection of long noncoding RNAs. Cell. 2018;172(3):393–407.

Hu WL, Jin L, Xu A, Wang YF, Thorne RF, Zhang XD, Wu M. GUARDIN is a p53-responsive long non-coding RNA that is essential for genomic stability. Nat Cell Biol. 2018;20(4):492–502.

S’anchez Y, Segura V, Marı’n-Be’jar O, Athie A, Marchese FP, Gonza’lez J, Bujanda L, Guo S, Matheu A, Huarte M. Genome-wide analysis of the human p53 transcriptional network unveils a lncRNA tumour suppressor signature. Nat Commun. 2014;5:5812.

Weisz L, Oren M, Rotter V. Transcription regulation by mutant p53. Oncogene. 2007;26(15):2202–11.

Quante T, Otto B, Brázdová M, Kejnovská I, Deppert W, Tolstonog GV. Mutant p53 is a transcriptional co-factor that binds to G-rich regulatory regions of active genes and generates transcriptional plasticity. Cell Cycle. 2012;11(17):3290–303.

Zhang M, Miao F, Huang R, et al. RHBDD1 promotes colorectal cancer metastasis through the Wnt signaling pathway and its downstream target ZEB1. J Exp Clin Cancer Res. 2018;37(1):22.

Han XY, Wei B, Fang JF, et al. Epithelial-mesenchymal transition associates with maintenance of stemness in spheroid-derived stem-like colon cancer cells. PLoS One. 2013;8(9):e73341.

McDermott M, Eustace AJ, Busschots S, et al. In vitro development of chemotherapy and targeted therapy drug-resistant Cancer cell lines: a practical guide with case studies. Front Oncol. 2014;4:40.

Jensen NF, Stenvang J, Beck MK, et al. Establishment and characterization of models of chemotherapy resistance in colorectal cancer: towards a predictive signature of chemoresistance. Mol Oncol. 2015;9(6):1169–85.

Xie M, Zhang L, He CS. Activation of Notch-1 enhances epithelial-mesenchymal transition in gefitinib-acquired resistant lung cancer cells. J Cell Biochem. 2012;113(5):1501–13.

Lister R, et al. Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell. 2008;133:523–36.

Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-seq. Nat Methods. 2008;5:621–8.

Cloonan N, et al. Stem cell transcriptome profiling via massive-scale mRNA sequencing. Nat Methods. 2008;5:613–9.

Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009;10:R25.

Zhang Y, et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 2008;9:R137.

Heinz S, et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell. 2010;38:576–89.

Zhang X, Guo C, Chen Y, Shulha HP, Schnetz MP, LaFramboise T, Bartels CF, Markowitz S, Weng Z, Scacheri PC, Wang Z. Epitope tagging of endogenous proteins for genome-wide ChIP-chip studies. Nat Methods. 2008;5(2):163–5.

Huang EH, Hynes MJ, Zhang T, Ginestier C, Dontu G, Appelman H, et al. Aldehyde dehydrogenase 1 is a marker for normal and malignant human colonic stem cells (SC) and tracks SC overpopulation during colon tumorigenesis. Cancer Res. 2009;69:3382e3389.

Chen J, Xia Q, Jiang B, Chang W, Yuan W, Ma Z, et al. Prognostic value of cancer stem cell marker ALDH1 expression in colorectal cancer: a systematic review and meta-analysis. PLoS One. 2015;10:1e15.

Prieto-Vila M, Takahashi RU, Usuba W, Kohama I, Ochiya T. Drug resistance driven by Cancer stem cells and their niche. Int J Mol Sci. 2017;1:18(12).

Spano JP, Milano G, Rixe C, Fagard R. JAK/STAT signalling pathway in colorectal cancer: a new biological target with therapeutic implications. Eur J Cancer. 2006;42(16):2668–70.

Lee SY, Jeong EK, Ju MK, Jeon HM, Kim MY, Kim CH, Park HG, Han SI, Kang HS. Induction of metastasis, cancer stem cell phenotype, and oncogenic metabolism in cancer cells by ionizing radiation. Mol Cancer. 2017;16(1):10.

Redelman-Sidi G, Binyamin A, Gaeta I, Palm W, Thompson CB, Romesser PB, Lowe SW, Bagul M, Doench JG, Root DE, Glickman MS. The canonical Wnt pathway drives macropinocytosis in Cancer. Cancer Res. 2018;78(16):4658–70.

Patel AP, Tirosh I, Trombetta JJ, Shalek AK, Gillespie SM, Wakimoto H, Cahill DP, Nahed BV, Curry WT, Martuza RL, Louis DN, Rozenblatt-Rosen O, Suvà ML, Regev A, Bernstein BE. Single-cell RNA-seq highlights intratumoral heterogeneity in primary glioblastoma. Science. 2014;344(6190):1396–401.

Wu SM, Liu H, Huang PJ, Chang IY, Lee CC, Yang CY, Tsai WS, Tan BC. circlncRNAnet: an integrated web-based resource for mapping functional networks of long or circular forms of noncoding RNAs. Gigascience. 2018;7(1):1–10.

Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature. 2001;414:105–11.

Huarte M. The emerging role of lncRNAs in cancer. Nat Med. 2015;21(11):1253–61.

Senapati P, Dey S, Sudarshan D, Das S, Kumar M, Kaypee S, Mohiyuddin A, Kodaganur GS, Kundu TK. Oncogene c-fos and mutant R175H p53 regulate expression of Nucleophosmin implicating cancer manifestation. FEBS J. 2018;285(18):3503–24.

Hanel W, Marchenko N, Xu S, Yu SX, Weng W, Moll U. Two hot spot mutant p53 mouse models display differential gain of function in tumorigenesis. Cell Death Differ. 2013;20(7):898–909.

Wong RP, Tsang WP, Chau PY, Co NN, Tsang TY, Kwok TT. p53-R273H gains new function in induction of drug resistance through down-regulation of procaspase-3. Mol Cancer Ther. 2007;6(3):1054–61.

Cooks T, Pateras IS, Tarcic O, Solomon H, Schetter AJ, Wilder S, Lozano G, Pikarsky E, Forshew T, Rozenfeld N, Harpaz N, Itzkowitz S, Harris CC, Rotter V, Gorgoulis VG, Oren M. Mutant p53 prolongs NF-κB activation and promotes chronic inflammation and inflammation-associated colorectal cancer. Cancer Cell. 2013;23(5):634–46.

Pruszko M, Milano E, Forcato M, Donzelli S, Ganci F, Di Agostino S, De Panfilis S, Fazi F, Bates DO, Bicciato S, Zylicz M, Zylicz A, Blandino G, Fontemaggi G. The mutant p53-ID4 complex controls VEGFA isoforms by recruiting lncRNA MALAT1. EMBO Rep. 2017;18(8):1331–51.

Oren M, Rotter V. Mutant p53 gain-of-function in cancer. Cold Spring Harb Perspect Biol. 2010;2(2):a001107.

Kim MP, Lozano G. Mutant p53 partners in crime. Cell Death Differ. 2018;25(1):161–8.

Shetzer Y, Molchadsky A, Rotter V. Oncogenic mutant p53 gain of FunctionNourishes the vicious cycle of TumorDevelopment and Cancer stem-cell formation. Cold Spring Harb Perspect Med. 2016;3:6(10).

Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, et al. The epithelial-mesenchymaltransition generates cells with properties of stem cells. Cell1. 2008;33:704–15.

Chang L, Graham PH, Hao J, et al. Acquisition of epithelialmesenchymal transition and cancer stem cell phenotypes is associated with activation of the PI3K/Akt/mTOR pathway in prostate cancer radioresistance. Cell Death Dis. 2013;4:e875.

Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in developmentand disease. Cell. 2009;139:871–90.

Yang AD, Fan F, Camp ER, van Buren G, Liu W, Somcio R, et al. Chronic oxaliplatin resistance inducesepithelial-to-mesenchymal transition in colorectal cancercell lines. Clin Cancer Res. 2006;12:4147–53.

Brabletz T. EMT and MET in metastasis: where are the cancer stem cells? Cancer Cell. 2012;22(6):699–701.

Cieply B, Farris J, Denvir J, et al. Epithelial-mesenchymal transition and tumor suppression are controlled by a reciprocal feedback loop between ZEB1 and Grainyhead-like-2. Cancer Res. 2013;73(20):6299–309.

Choi HJ, Park JH, Park M, et al. UTX inhibits EMT-induced breast CSC properties by epigenetic repression of EMT genes in cooperation with LSD1 and HDAC1. EMBO Rep. 2015;16(10):1288–98.

Lehmann W, Mossmann D, Kleemann J, et al. ZEB1 turns into a transcriptional activator by interacting with YAP1 in aggressive cancer types. Nat Commun. 2016;7:10498.

Zhang Y, Xu L, Li A, et al. The roles of ZEB1 in tumorigenic progression and epigenetic modifications. Biomed Pharmacother. 2019;110:400–8.

Moyret-Lalle C, Ruiz E, Puisieux A. Epithelial-mesenchymal transition transcription factors and miRNAs: “plastic surgeons” of breast cancer. World J Clin Oncol. 2014;5(3):311–22.

Ma Z, Peng P, Zhou J, Hui B, Ji H, Wang J, Wang K. Long non-coding RNA SH3PXD2A-AS1 promotes cell progression partly through epigenetic silencing P57 and KLF2 in colorectal Cancer. Cell Physiol Biochem. 2018;46(6):2197–214.

Parrales A, Iwakuma T. Targeting Oncogenic Mutant p53 for Cancer Therapy. Front Oncol. 2015;5:288.

Ren J, Ding L, Zhang D, Shi G, Xu Q, Shen S, Wang Y, Wang T, Hou Y. Carcinoma-associated fibroblasts promote the stemness and chemoresistance of colorectal cancer by transferring exosomal lncRNA H19. Theranostics. 2018;8(14):3932–48.

Malhotra A, Jain M, Prakash H, Vasquez KM, Jain A. The regulatory roles of long non-coding RNAs in the development of chemoresistance in breast cancer. Oncotarget. 2017;8(66):110671–84.