1,139
Views
11
CrossRef citations to date
0
Altmetric
Research Paper

Inhibition of nucleophosmin 1 suppresses colorectal cancer tumor growth of patient -derived xenografts via activation of p53 and inhibition of AKT

, ORCID Icon, , , , , & show all
Pages 112-123 | Received 26 Jul 2019, Accepted 22 Sep 2020, Published online: 15 Jan 2021

References

  • Borer RA, Lehner CF, Eppenberger HM, Nigg EA. Major nucleolar proteins shuttle between nucleus and cytoplasm. Cell. 1989;56:379–390. doi:10.1016/0092-8674(89)90241-9.
  • Grisendi S, Mecucci C, Falini B, Pandolfi PP. Nucleophosmin and cancer. Nat Rev Cancer. 2006;6:493–505. doi:10.1038/nrc1885.
  • Yun JP, Miao J, Chen GG, Tian QH, Zhang CQ, Xiang J, Fu J, Lai PBS. Increased expression of nucleophosmin/B23 in hepatocellular carcinoma and correlation with clinicopathological parameters. Br J Cancer. 2007;96:477–484. doi:10.1038/sj.bjc.6603574.
  • Pianta A, Puppin C, Franzoni A, Fabbro D, Di Loreto C, Bulotta S, Deganuto M, Paron I, Tell G, Puxeddu E, et al. Nucleophosmin is overexpressed in thyroid tumors. Biochem Biophys Res Commun. 2010;397:499–504. doi:10.1016/j.bbrc.2010.05.142.
  • Nozawa Y, Van Belzen N, Van der Made AC, Dinjens WN, Bosman FT. Expression of nucleophosmin/B23 in normal and neoplastic colorectal mucosa. J Pathol. 1996;178:48–52.
  • Tsui KH, Juang HH, Lee TH, Chang PL, Chen CL, Yung BY. Association of nucleophosmin/B23 with bladder cancer recurrence based on immunohistochemical assessment in clinical samples. Acta Pharmacol Sin. 2008;29:364–370. doi:10.1111/j.1745-7254.2008.00747.x.
  • Subong EN, Shue MJ, Epstein JI, Briggman JV, Chan PK, Partin AW. Monoclonal antibody to prostate cancer nuclear matrix protein (PRO:4-216) recognizes nucleophosmin/B23. Prostate. 1999;39:298–304.
  • Wong JC, Hasan MR, Rahman M, Yu AC, Chan SK, Schaeffer DF, Kennecke HF, Lim HJ, Owen D, Tai IT, et al. Nucleophosmin 1, upregulated in adenomas and cancers of the colon, inhibits p53-mediated cellular senescence. Int J Cancer. 2013;133:1567–1577. doi:10.1002/ijc.28180.
  • Liu Y, Zhang F, Zhang XF, Qi LS, Yang L, Guo H, Zhang N. Expression of nucleophosmin/NPM1 correlates with migration and invasiveness of colon cancer cells. J Biomed Sci. 2012;19:53. doi:10.1186/1423-0127-19-53.
  • Zlobec I, Steele R, Terracciano L, Jass JR, Lugli A. Selecting immunohistochemical cut-off scores for novel biomarkers of progression and survival in colorectal cancer. J Clin Pathol. 2007;60:1112–1116. doi:10.1136/jcp.2006.044537.
  • Zhu ZH, Sun BY, Ma Y, Shao JY, Long H, Zhang X, Fu J-H, Zhang L-J, Su X-D, Wu Q-L, et al. Three immunomarker support vector machines-based prognostic classifiers for stage IB non-small-cell lung cancer. J Clin Oncol. 2009;27:1091–1099. doi:10.1200/JCO.2008.16.6991.
  • Wagner HE, Thomas P, Wolf BC, Zamcheck N, Jessup JM, Steele GD Jr. Characterization of the tumorigenic and metastatic potential of a poorly differentiated human colon cancer cell line. Invasion Metastasis. 1990;10:253–266.
  • Qi W, Shakalya K, Stejskal A, Goldman A, Beeck S, Cooke L, Mahadevan D. NSC348884, a nucleophosmin inhibitor disrupts oligomer formation and induces apoptosis in human cancer cells. Oncogene. 2008;27:4210–4220. doi:10.1038/onc.2008.54.
  • Kern DH, Morgan CR, Hildebrand-Zanki SU. In vitro pharmacodynamics of 1-beta-D-arabinofuranosylcytosine: synergy of antitumor activity with cis-diamminedichloroplatinum(II). Cancer Res. 1988;48:117–121.
  • Romanelli S, Perego P, Pratesi G, Carenini N, Tortoreto M, Zunino F. In vitro and in vivo interaction between cisplatin and topotecan in ovarian carcinoma systems. Cancer Chemother Pharmacol. 1998;41:385–390. doi:10.1007/s002800050755.
  • Rahman M, Selvarajan K, Hasan MR, Chan AP, Jin C, Kim J, Chan SK, Le ND, Kim Y-B, Tai IT, et al. Inhibition of COX-2 in colon cancer modulates tumor growth and MDR-1 expression to enhance tumor regression in therapy-refractory cancers in vivo. Neoplasia. 2012;14:624–633. doi:10.1593/neo.12486.
  • Chou TC. Drug combination studies and their synergy quantification using the Chou-Talalay method. Cancer Res. 2010;70:440–446. doi:10.1158/0008-5472.CAN-09-1947.
  • Parsana P, Riester M, Waldron L. CuratedCRCData: clinically annotated data for the colorectal Cancer transcriptome. Bioconductor. 2013. http://www.bioconductor.org/packages/curatedCRCData/.
  • Hingorani K, Szebeni A, Olson MO. Mapping the functional domains of nucleolar protein B23. J Biol Chem. 2000;275:24451–24457.
  • Lee HH, Kim HS, Kang JY, Lee BI, Ha JY, Yoon HJ, Lim SO, Jung G, Suh SW. Crystal structure of human nucleophosmin-core reveals plasticity of the pentamer-pentamer interface. Proteins. 2007;69:672–678. doi:10.1002/prot.21504.
  • Mitrea DM, Grace CR, Buljan M, Yun MK, Pytel NJ, Satumba J, Nourse A, Park C-G, Madan Babu M, White SW, et al. Structural polymorphism in the N-terminal oligomerization domain of NPM1. Proc Natl Acad Sci U S A. 2014;111:4466–4471. doi:10.1073/pnas.1321007111.
  • Yan N, Shi Y. Mechanisms of apoptosis through structural biology. Annu Rev Cell Dev Biol. 2005;21:35–56.
  • Tibbetts RS, Brumbaugh KM, Williams JM, Sarkaria JN, Cliby WA, Shieh SY, Taya Y, Prives C, Abraham RT. A role for ATR in the DNA damage-induced phosphorylation of p53. Genes Dev. 1999;13:152–157. doi:10.1101/gad.13.2.152.
  • Wu GS, Ding Z. Caspase 9 is required for p53-dependent apoptosis and chemosensitivity in a human ovarian cancer cell line. Oncogene. 2002;21:1–8. doi:10.1038/sj.onc.1205020.
  • Agarwal E, Brattain MG, Chowdhury S. Cell survival and metastasis regulation by Akt signaling in colorectal cancer. Cell Signal. 2013;25:1711–1719. doi:10.1016/j.cellsig.2013.03.025.
  • Green DR, Kroemer G. Cytoplasmic functions of the tumour suppressor p53. Nature. 2009;458:1127–1130.
  • Danielsen SA, Eide PW, Nesbakken A, Guren T, Leithe E, Lothe RA. Portrait of the PI3K/AKT pathway in colorectal cancer. Biochim Biophys Acta. 2015;1855:104–121.
  • Papadatos-Pastos D, Rabbie R, Ross P, Sarker D. The role of the PI3K pathway in colorectal cancer. Crit Rev Oncol Hematol. 2015;94:18–30. doi:10.1016/j.critrevonc.2014.12.006.
  • Luo H, Yang Y, Duan J, Wu P, Jiang Q, Xu C. PTEN-regulated AKT/FoxO3a/Bim signaling contributes to reactive oxygen species-mediated apoptosis in selenite-treated colorectal cancer cells. Cell Death Dis. 2013;4:e481. doi:10.1038/cddis.2013.3.
  • Franke TF. PI3K/Akt: getting it right matters. Oncogene. 2008;27:6473–6488.
  • Samuels Y, Wang Z, Bardelli A, Silliman N, Ptak J, Szabo S, Yan H, Gazdar A, Powell SM, Riggins GJ, et al. High frequency of mutations of the PIK3CA gene in human cancers. Science. 2004;304:554. doi:10.1126/science.1096502.
  • Medico E, Russo M, Picco G, Cancelliere C, Valtorta E, Corti G, Buscarino M, Isella C, Lamba S, Martinoglio B, et al. The molecular landscape of colorectal cancer cell lines unveils clinically actionable kinase targets. Nat Commun. 2015;6:7002. doi:10.1038/ncomms8002.
  • Alessi DR, James SR, Downes CP, Holmes AB, Gaffney PR, Reese CB, Cohen P. Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase Balpha. Curr Biol. 1997;7:261–269. doi:10.1016/S0960-9822(06)00122-9.
  • Sarbassov DD, Guertin DA, Ali SM, Sabatini DM. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science. 2005;307:1098–1101. doi:10.1126/science.1106148.
  • Ahn JY, Liu X, Cheng D, Peng J, Chan PK, Wade PA, Ye K. Nucleophosmin/B23, a nuclear PI(3,4,5)P(3) receptor, mediates the antiapoptotic actions of NGF by inhibiting CAD. Mol Cell. 2005;18:435–445. doi:10.1016/j.molcel.2005.04.010.
  • Lee SB, Xuan Nguyen TL, Choi JW, Lee KH, Cho SW, Liu Z, Ye K, Bae SS, Ahn J-Y. Nuclear Akt interacts with B23/NPM and protects it from proteolytic cleavage, enhancing cell survival. Proc Natl Acad Sci U S A. 2008;105:16584–16589. doi:10.1073/pnas.0807668105.
  • Kim CK, Nguyen TL, Lee SB, Park SB, Lee KH, Cho SW, Ahn JY. Akt2 and nucleophosmin/B23 function as an oncogenic unit in human lung cancer cells. Exp Cell Res. 2011;317:966–975. doi:10.1016/j.yexcr.2010.12.013.
  • Lo SJ, Fan LC, Tsai YF, Lin KY, Huang HL, Wang TH, Liu H, Chen T-C, Huang S-F, Chang C-J, et al. A novel interaction of nucleophosmin with BCL2-associated X protein regulating death evasion and drug sensitivity in human hepatoma cells. Hepatology. 2013;57:1893–1905. doi:10.1002/hep.26209.
  • Chan HJ, Weng JJ, Yung BYM. Nucleophosmin/B23-binding peptide inhibits tumor growth and up-regulates transcriptional activity of p53. Biochem Biophys Res Commun. 2005;333:396–403. doi:10.1016/j.bbrc.2005.04.176.
  • Jian Y, Gao Z, Sun J, Shen Q, Feng F, Jing Y, Yang C. RNA aptamers interfering with nucleophosmin oligomerization induce apoptosis of cancer cells. Oncogene. 2009;28:4201–4211. doi:10.1038/onc.2009.275.
  • Sarduy M, García I, Coca M, Perera A, Torres L, Valenzuela C, Baladrón I, Solares M, Reyes V, Hernández I, et al. Optimizing CIGB-300 intralesional delivery in locally advanced cervical cancer. Br J Cancer. 2015;112:1636–1643. doi:10.1038/bjc.2015.137.
  • Destouches D, Page N, Hamma-Kourbali Y, Machi V, Chaloin O, Frechault S, Birmpas C, Katsoris P, Beyrath J, Albanese P, et al. A simple approach to cancer therapy afforded by multivalent pseudopeptides that target cell-surface nucleoproteins. Cancer Res. 2011;71:3296–3305. doi:10.1158/0008-5472.CAN-10-3459.
  • De Cola A, Franceschini M, Di Matteo A, Colotti G, Celani R, Clemente E, Ippoliti R, Cimini AM, Dhez AC, Vallée B, et al. N6L pseudopeptide interferes with nucleophosmin protein-protein interactions and sensitizes leukemic cells to chemotherapy. Cancer Lett. 2018;412:272–282. doi:10.1016/j.canlet.2017.10.038.

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.