3,123
Views
36
CrossRef citations to date
0
Altmetric
Research Paper

Mutant p53 drives cancer chemotherapy resistance due to loss of function on activating transcription of PUMA

, , , , , , , & show all
Pages 3442-3455 | Received 26 Jul 2019, Accepted 03 Oct 2019, Published online: 14 Nov 2019

References

  • Vega P, Valentín F, Cubiella J. Colorectal cancer diagnosis: Pitfalls and opportunities. World J Gastrointest Oncol. 2015;7:422–33.
  • Arnold M, Sierra MS, Laversanne M, et al. Global patterns and trends in colorectal cancer incidence and mortality. Gut. 2017;66:683–691.
  • Sullivan KD, Galbraith MD, Andrysik Z, et al. Mechanisms of transcriptional regulation by p53. Cell Death Differ. 2018;25:133–143.
  • Kastenhuber ER, Lowe SW. Putting p53 in context. Cell. 2017;170:1062–1078.
  • Krause K, Wasner M, Reinhard W, et al. The tumour suppressor protein p53 can repress transcription of cyclin B. Nucleic Acids Res. 2000;28:4410–4418.
  • Taylor WR, Schonthal AH, Galante J. Stark GR. p130/E2F4 binds to and represses the cdc2 promoter in response to p53. J Biol Chem. 2001;276:1998–2006.
  • Wang H, Yan C. A small-molecule p53 activator induces apoptosis through inhibiting MDMX expression in breast cancer cells. Neoplasia. 2011;13:611–619.
  • Nakano K, Vousden KH. PUMA, a novel proapoptotic gene, is induced by p53. Mol Cell. 2001;7:683.
  • Yu J, Zhang L, Hwang PM, et al. PUMA induces the rapid apoptosis of colorectal cancer cells. Mol Cell. 2001;7:673.
  • Shamas-Din A, Kale J, Leber B, et al. Mechanisms of action of Bcl-2 family proteins. Cold Spring Harb Perspect Biol. 2013;5:a008714.
  • Yu J, Wang Z, Kinzler KW, et al. PUMA mediates the apoptotic response to p53 in colorectal cancer cells. Proc Natl Acad Sci U S A. 2003;100:1931–1936.
  • Huanan Wang LZ. PUMA mediates the combinational therapy of 5-FU and NVP-BEZ235 in colon cancer. Oncotarget. 2015;6:14385–14398.
  • Yang S, Zhu Z, Zhang X, et al. Idelalisib induces PUMA-dependent apoptosis in colon cancer cells. Oncotarget. 2017;8:6102–6113.
  • Fruman DA, Cantley LC. Idelalisib – a PI3Kdelta inhibitor for B-cell cancers. N Engl J Med. 2014;370:1061–1062.
  • Zhang L, Huang X, Li W. Pazopanib, a novel multi-kinase inhibitor, shows potent antitumor activity in colon cancer through PUMA-mediated apoptosis. Oncotarget. 2017;8:3289–3303.
  • Paoluzzi L, Cacavio A, Ghesani M, et al. Response to anti-PD1 therapy with nivolumab in metastatic sarcomas. Clin Sarcoma Res. 2016;6:24.
  • Sun L, Huang Y, Liu Y, et al. Ipatasertib, a novel Akt inhibitor, induces transcription factor FoxO3a and NF-kappaB directly regulates PUMA-dependent apoptosis. Cell Death Dis. 2018;9:911.
  • Kim SB, Dent R, Im SA, et al. Ipatasertib plus paclitaxel versus placebo plus paclitaxel as first-line therapy for metastatic triple-negative breast cancer (LOTUS): a multicentre, randomised, double-blind, placebo-controlled, phase 2 trial. Lancet Oncol. 2017;18:1360–1372.
  • Jacks T, Remington L, Williams BO, et al. Tumor spectrum analysis in p53-mutant mice. Curr Biol Cb. 1994;4:1–7.
  • Rodrigues NR, Rowan A, Smith ME, et al. p53 mutations in colorectal cancer. Proc Natl Acad Sci U S A. 1990;87:7555–7559.
  • Muller PAJ, Vousden KH. p53 mutations in cancer. Nat Cell Biol. 2013;15:2.
  • Levine AJ, Wu MC, Chang A, et al. The spectrum of mutations at the p53 locus. Evidence for tissue-specific mutagenesis, selection of mutant alleles, and a “gain of function” phenotype. Ann N Y Acad Sci. 1995;768:111–128.
  • Bieging KT, Mello SS, Attardi LD. Unravelling mechanisms of p53-mediated tumour suppression. Nat Rev Cancer. 2014;14:359.
  • Zhang Y, Coillie SV, Fang JY, et al. Gain of function of mutant p53: R282W on the peak? Oncogenesis. 2016;5:e196.
  • Yue X, Zhang C, Zhao Y, et al. Gain-of-function mutant p53 activates small GTPase Rac1 through SUMOylation to promote tumor progression. Genes Dev. 2017;31:1641–1654.
  • Schulz-Heddergott R, Stark N, Edmunds SJ, et al. Therapeutic ablation of gain-of-function mutant p53 in colorectal cancer inhibits stat3-mediated tumor growth and invasion. Cancer Cell. 2018;34:298–314 e7.
  • Walerych D, Lisek K, Sommaggio R, et al. Proteasome machinery is instrumental in a common gain-of-function program of the p53 missense mutants in cancer. Nat Cell Biol. 2016;18:897–909.
  • Weissmueller S, Manchado E, Saborowski M, et al. Mutant p53 drives pancreatic cancer metastasis through cell-autonomous PDGF receptor beta signaling. Cell. 2014;157:382–394.
  • Tan BS, Tiong KH, Choo HL, et al. Mutant p53-R273H mediates cancer cell survival and anoikis resistance through AKT-dependent suppression of BCL2-modifying factor (BMF). Cell Death Dis. 2015;6:e1826.
  • Wiegering A, Matthes N, Mühling B, et al. Reactivating p53 and inducing tumor apoptosis (RITA) enhances the response of RITA-sensitive colorectal cancer cells to chemotherapeutic agents 5-fluorouracil and oxaliplatin. Neoplasia. 2017;19:301–309.
  • Raguz S, Yague E. Resistance to chemotherapy: new treatments and novel insights into an old problem. Br J Cancer. 2008;99:387–391.
  • Fearon ER, Vogelstein B. A genetic model for colorectal tumorigenesis. Cell. 1990;61:759–767.
  • Yaeger R, Chatila WK, Lipsyc MD, et al. Clinical sequencing defines the genomic landscape of metastatic colorectal cancer. Cancer Cell. 2018;33:125–36 e3.
  • Audrey P, Ewy M, Shunsuke K, et al. Impact of mutant p53 functional properties on TP53 mutation patterns and tumor phenotype: lessons from recent developments in the IARC TP53 database. Hum Mutat. 2010;28:622–629.
  • Lv Y, Zhang Y, Rubinsky B. Molecular and histological study on the effects of electrolytic electroporation on the liver. Bioelectrochemistry. 2018;125:79–89.
  • Wang P, Yu J, Zhang L The nuclear function of p53 is required for PUMA-mediated apoptosis induced by DNA damage. Proc Natl Acad Sci USA. 2007;104(10):4054–4059. DOI:10.1073/pnas.0700020104. Epub 2007 Feb 28.
  • Gonzalez KD, Noltner KA, Buzin CH, et al. Beyond Li fraumeni syndrome: clinical characteristics of families with p53 germline mutations. J Clin Oncol. 2009;27:1250–1256.
  • Malkin D, Li FP, Strong LC, et al. Germ line p53 mutations in a familial syndrome of breast cancer, sarcomas, and other neoplasms. Science. 1990;250:1233–1238.
  • Vogelstein B, Lane D, Levine AJ. Surfing the p53 network. Nature. 2000;408:307–310.
  • Whibley C, Pharoah PD, Hollstein M. p53 polymorphisms: cancer implications. Nat Rev Cancer. 2009;9:95–107.
  • Punt CJA, Koopman M, Vermeulen L. From tumour heterogeneity to advances in precision treatment of colorectal cancer. Nat Rev Clin Oncol. 2016;14:235.
  • Sabapathy K, Lane DP. Therapeutic targeting of p53: all mutants are equal, but some mutants are more equal than others. Nat Rev Clin Oncol. 2018;15:13–30.
  • Alam SK, Yadav VK, Bajaj S, et al. DNA damage-induced ephrin-B2 reverse signaling promotes chemoresistance and drives EMT in colorectal carcinoma harboring mutant p53. Cell Death Differ. 2016;23:707–722.
  • He C, Li L, Guan X, et al. Mutant p53 gain of function and chemoresistance: the role of mutant p53 in response to clinical chemotherapy. Chemotherapy. 2017;62:43–53.
  • Aglietti RA, Dueber EC. Recent insights into the molecular mechanisms underlying pyroptosis and gasdermin family functions. Trends Immunol. 2017;38:261–271.
  • Fink SL, Cookson BT. Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect Immun. 2005;73:1907–1916.
  • Bergsbaken T, Fink SL, Cookson BT. Pyroptosis: host cell death and inflammation. Nat Rev Microbiol. 2009;7:99–109.
  • Li T, Kon N, Jiang L, et al. Tumor suppression in the absence of p53-mediated cell-cycle arrest, apoptosis, and senescence. Cell. 2012;149:1269–1283.
  • Engeland K. Cell cycle arrest through indirect transcriptional repression by p53: I have a DREAM. Cell Death Differ. 2018;25:114–132.
  • Bykov VJN, Eriksson SE, Bianchi J, et al. Targeting mutant p53 for efficient cancer therapy. Nat Rev Cancer. 2018;18:89–102.
  • Chen Y, Zhang X, Dantas Machado AC, et al. Structure of p53 binding to the BAX response element reveals DNA unwinding and compression to accommodate base-pair insertion. Nucleic Acids Res. 2013;41:8368–8376.
  • Farooqi AA, de la Roche M, Djamgoz MBA, et al. Overview of the oncogenic signaling pathways in colorectal cancer: mechanistic insights. Semin Cancer Biol. 2019;58:65–79.
  • Campomenosi P, Monti P, Aprile A, et al. p53 mutants can often transactivate promoters containing a p21 but not Bax or PIG3 responsive elements. Oncogene. 2001;20:3573–3579.
  • Chipuk JE, Kuwana T, Bouchier-Hayes L, et al. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science. 2004;303:1010–1014.
  • Liu YC, Margolskee E, Allan JN, et al. Chronic lymphocytic leukemia with TP53 gene alterations: a detailed clinicopathologic analysis. Mod Pathol. 2019. DOI:10.1038/s41379-019-0356-z
  • Tanaka N, Zhao M, Tang L, et al. Gain-of-function mutant p53 promotes the oncogenic potential of head and neck squamous cell carcinoma cells by targeting the transcription factors FOXO3a and FOXM1. Oncogene. 2018;37:1279–1292.
  • Blandino G, Di Agostino S. New therapeutic strategies to treat human cancers expressing mutant p53 proteins. J Exp Clin Cancer Res. 2018;37:30.
  • Touil Y, Igoudjil W, Corvaisier M, et al. Colon cancer cells escape 5FU chemotherapy-induced cell death by entering stemness and quiescence associated with the c-Yes/YAP axis. Clin Cancer Res off J Am Assoc Cancer Res. 2014;20:837–846.
  • Stambolsky P, Tabach Y, Fontemaggi G, et al. Modulation of the vitamin D3 response by cancer-associated mutant p53. Cancer Cell. 2010;17:273–285.
  • White KA, Ruiz DG, Szpiech ZA, et al. Cancer-associated arginine-to-histidine mutations confer a gain in pH sensing to mutant proteins. Sci Signal. 2017;10(495). pii: eaam9931. DOI:10.1126/scisignal.aam9931.
  • Nowak DG, Katsenelson KC, Watrud KE, et al. The PHLPP2 phosphatase is a druggable driver of prostate cancer progression. J Cell Biol. 2019;218:1943–1957.
  • Brognard J, Sierecki E, Gao T, et al. PHLPP and a second isoform, PHLPP2, differentially attenuate the amplitude of Akt signaling by regulating distinct Akt isoforms. Mol Cell. 2007;25:917–931.
  • Newton AC, Trotman LC. Turning off AKT: PHLPP as a drug target. Annu Rev Pharmacol Toxicol. 2014;54:537–558.
  • Chen J, Jiang CC, Jin L, et al. Regulation of PD-L1: a novel role of pro-survival signalling in cancer. Ann Oncol. 2016;27:409–416.
  • Casey SC, Tong L, Li Y, Do R, Walz S, Fitzgerald KN, Gouw AM, Baylot V, Gutgemann I, Eilers M, et al.MYC regulates the antitumor immune response through CD47 and PD-L1. Science. 2016;352:227–231.
  • Atsaves V, Tsesmetzis N, Chioureas D, et al. PD-L1 is commonly expressed and transcriptionally regulated by STAT3 and MYC in ALK-negative anaplastic large-cell lymphoma. Leukemia. 2017;31:1633–1637.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.