831
Views
0
CrossRef citations to date
0
Altmetric
Research Paper

Inhibition of autophagy and induction of glioblastoma cell death by NEO214, a perillyl alcohol-rolipram conjugate

, ORCID Icon, , , ORCID Icon, ORCID Icon, ORCID Icon, , ORCID Icon, , & ORCID Icon show all
Pages 3169-3188 | Received 06 Feb 2022, Accepted 26 Jul 2023, Published online: 06 Aug 2023

References

  • Klionsky DJ, Abdel-Aziz AK, Abdelfatah S, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (4th edition)(1). Autophagy. 2021 Jan;17(1):1–382. doi: 10.1080/15548627.2020.1797280
  • Louis DN, Perry A, Wesseling P, et al. The 2021 WHO classification of tumors of the central nervous system: a summary. Neuro Oncol. 2021 Aug 2;23(8):1231–1251. doi: 10.1093/neuonc/noab106
  • Chin C, Lunking ES, de la Fuente M, et al. Immunotherapy and epigenetic pathway modulation in glioblastoma multiforme. Front Oncol. 2018;8:521. doi: 10.3389/fonc.2018.00521
  • Stupp R, Mason WP, van den Bent MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005 Mar 10;352(10):987–996. doi: 10.1056/NEJMoa043330
  • Weller M, Cloughesy T, Perry JR, et al. Standards of care for treatment of recurrent glioblastoma–are we there yet? Neuro Oncol. 2013 Jan;15(1):4–27. doi: 10.1093/neuonc/nos273
  • Golden EB, Cho HY, Hofman FM, et al. Quinoline-based antimalarial drugs: a novel class of autophagy inhibitors. Neurosurg Focus. 2015 Mar;38(3):E12. doi: 10.3171/2014.12.FOCUS14748
  • Golden EB, Cho HY, Jahanian A, et al. Chloroquine enhances temozolomide cytotoxicity in malignant gliomas by blocking autophagy. Neurosurg Focus. 2014 Dec;37(6):E12. doi: 10.3171/2014.9.FOCUS14504
  • Liu G, Pei F, Yang F, et al. Role of autophagy and apoptosis in non-small-cell lung cancer. Int J Mol Sci. 2017 Feb 10;18(2):367. doi: 10.3390/ijms18020367
  • Mizushima N, Levine B, Cuervo AM, et al. Autophagy fights disease through cellular self-digestion. Nature. 2008 Feb 28;451(7182):1069–1075. doi: 10.1038/nature06639
  • Hurley JH, Schulman BA Atomistic autophagy: the structures of cellular self-digestion. Cell. 2014 Apr 10;157(2):300–311. doi: 10.1016/j.cell.2014.01.070
  • Nixon RA. The role of autophagy in neurodegenerative disease. Nature Med. 2013 Aug;19(8):983–997. doi: 10.1038/nm.3232
  • Nezis IP, Simonsen A, Sagona AP, et al. Ref(2)p, the drosophila melanogaster homologue of mammalian p62, is required for the formation of protein aggregates in adult brain. J Cell Bio. 2008 Mar 24;180(6):1065–1071. doi: 10.1083/jcb.200711108
  • Zatloukal K, Stumptner C, Fuchsbichler A, et al. P62 is a common component of cytoplasmic inclusions in protein aggregation diseases. Am J Pathol. 2002 Jan;160(1):255–263. doi: 10.1016/S0002-9440(10)64369-6
  • Klionsky DJ, Abdelmohsen K, Abe A, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy. 2016;12(1):1–222. doi: 10.1080/15548627.2015.1100356
  • Apel A, Herr I, Schwarz H, et al. Blocked autophagy sensitizes resistant carcinoma cells to radiation therapy. Cancer Res. 2008 Mar 1;68(5):1485–1494. doi: 10.1158/0008-5472.CAN-07-0562
  • Chen N, Karantza-Wadsworth V. Role and regulation of autophagy in cancer. Biochim Biophys Acta, Mol Cell Res. 2009 Sep;1793(9):1516–1523. doi: 10.1016/j.bbamcr.2008.12.013
  • Liu D, Yang Y, Liu Q, et al. Inhibition of autophagy by 3-MA potentiates cisplatin-induced apoptosis in esophageal squamous cell carcinoma cells. Med Oncol. 2011 Mar;28(1):105–111. doi: 10.1007/s12032-009-9397-3
  • Selvakumaran M, Amaravadi RK, Vasilevskaya IA, et al. Autophagy inhibition sensitizes colon cancer cells to antiangiogenic and cytotoxic therapy. Clin Cancer Res. 2013 Jun 1;19(11):2995–3007. doi: 10.1158/1078-0432.CCR-12-1542
  • Zheng L, Li H, Mo Y, et al. Autophagy inhibition sensitizes LY3023414-induced anti-glioma cell activity in vitro and in vivo. Oncotarget. 2017 Nov 17;8(58):98964–98973. doi: 10.18632/oncotarget.22147
  • Degtyarev M, De Mazière A, Orr C, et al. Akt inhibition promotes autophagy and sensitizes PTEN-null tumors to lysosomotropic agents. J Cell Bio. 2008 Oct 6;183(1):101–116. doi: 10.1083/jcb.200801099
  • Fan QW, Cheng C, Hackett C, et al. Akt and autophagy cooperate to promote survival of drug-resistant glioma. Sci Signaling. 2010 Nov 9;3(147):ra81. doi: 10.1126/scisignal.2001017
  • Weckman A, Rotondo F, Di Ieva A, et al. Autophagy in endocrine tumors. Endocr Relat Cancer. 2015 Aug;22(4):R205–18. doi: 10.1530/ERC-15-0042
  • Chude CI, Amaravadi RK Targeting autophagy in cancer: update on clinical trials and novel inhibitors. Int J Mol Sci. 2017 Jun 16;18(6):1279. doi: 10.3390/ijms18061279
  • Tanida I. Autophagosome formation and molecular mechanism of autophagy. Antioxid Redox Signaling. 2011 Jun;14(11):2201–2214. doi: 10.1089/ars.2010.3482
  • Rosenfeld MR, Ye X, Supko JG, et al. A phase I/II trial of hydroxychloroquine in conjunction with radiation therapy and concurrent and adjuvant temozolomide in patients with newly diagnosed glioblastoma multiforme. Autophagy. 2014 Aug;10(8):1359–1368. doi: 10.4161/auto.28984
  • Chen TC, Fonseca CO, Schönthal AH. Preclinical development and clinical use of perillyl alcohol for chemoprevention and cancer therapy. Am J Cancer Res. 2015;5(5):1580–1593.
  • Chen TC, Wadsten P, Su S, et al. The type IV phosphodiesterase inhibitor rolipram induces expression of the cell cycle inhibitors p21(Cip1) and p27(Kip1), resulting in growth inhibition, increased differentiation, and subsequent apoptosis of malignant A-172 glioma cells. Cancer Biol Ther. 2002 May-Jun;1(3):268–276. doi: 10.4161/cbt.80
  • Cho HY, Wang W, Jhaveri N, et al. Perillyl alcohol for the treatment of temozolomide-resistant gliomas. Mol Cancer Ther. 2012 Nov;11(11):2462–2472. doi: 10.1158/1535-7163.MCT-12-0321
  • Goldhoff P, Warrington NM, Limbrick DD Jr., et al. Targeted inhibition of cyclic AMP phosphodiesterase-4 promotes brain tumor regression. Clin Cancer Res. 2008 Dec 1;14(23):7717–7725. doi: 10.1158/1078-0432.CCR-08-0827
  • Pullamsetti SS, Banat GA, Schmall A, et al. Phosphodiesterase-4 promotes proliferation and angiogenesis of lung cancer by crosstalk with HIF. Oncogene. 2013 Feb 28;32(9):1121–1134. doi: 10.1038/onc.2012.136
  • Ernst E. Functional foods, neutraceuticals, designer foods: innocent fad or counterproductive marketing ploy? Eur J Clin Pharmacol. 2001 Aug;57(5):353–355. doi: 10.1007/s002280100327
  • Stark MJ, Burke YD, McKinzie JH, et al. Chemotherapy of pancreatic cancer with the monoterpene perillyl alcohol. Cancer Lett. 1995 Sep 4;96(1):15–21. doi: 10.1016/0304-3835(95)03912-G
  • Schönthal AH, Peereboom DM, Wagle N, et al. Phase I trial of intranasal NEO100, highly purified perillyl alcohol, in adult patients with recurrent glioblastoma. Neurooncol Adv. 2021 Jan-Dec;3(1):vdab005. doi: 10.1093/noajnl/vdab005
  • Chen TC, Chan N, Labib S, et al. Induction of pro-apoptotic endoplasmic reticulum stress in multiple myeloma cells by NEO214, perillyl alcohol conjugated to rolipram. Int J Mol Sci. 2018 Jan 17;19(1):277. doi: 10.3390/ijms19010277
  • Cho HY, Thein TZ, Wang W, et al. The rolipram-perillyl alcohol conjugate (NEO214) is a mediator of cell death through the death receptor pathway. Mol Cancer Ther. 2019 Mar;18(3):517–530. doi: 10.1158/1535-7163.MCT-18-0465
  • Jäger R, Bertrand MJ, Gorman AM, et al. The unfolded protein response at the crossroads of cellular life and death during endoplasmic reticulum stress. Biol Cell. 2012 May;104(5):259–270. doi: 10.1111/boc.201100055
  • Kabeya Y, Mizushima N, Ueno T, et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. Embo J. 2000 Nov 1;19(21):5720–5728. doi: 10.1093/emboj/19.21.5720
  • Mizushima N, Yamamoto A, Matsui M, et al. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. ?Mol Biol Cell. 2004 Mar;15(3):1101–1111. doi: 10.1091/mbc.e03-09-0704
  • Mizushima N, Yoshimori T, Levine B Methods in mammalian autophagy research. Cell. 2010 Feb 5;140(3):313–326. doi: 10.1016/j.cell.2010.01.028
  • Bjørkøy G, Lamark T, Brech A, et al. P62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Bio. 2005 Nov 21;171(4):603–614. doi: 10.1083/jcb.200507002
  • Kim HW, Ha SH, Lee MN, et al. Cyclic AMP controls mTOR through regulation of the dynamic interaction between Rheb and phosphodiesterase 4D. Mol Cell Biol. 2010 Nov;30(22):5406–5420. doi: 10.1128/MCB.00217-10
  • McGrath ME. The lysosomal cysteine proteases. Annu Rev Biophys Biomol Struct. 1999;28(1):181–204. doi: 10.1146/annurev.biophys.28.1.181
  • You JO, Auguste DT. The effect of swelling and cationic character on gene transfection by Ph-sensitive nanocarriers. Biomaterials. 2010 Sep;31(26):6859–6866. doi: 10.1016/j.biomaterials.2010.04.048
  • Gallagher LE, Williamson LE, Chan EY Advances in autophagy regulatory mechanisms. Cells. 2016 May 13;5(2):24. doi: 10.3390/cells5020024
  • Sardiello M. Transcription factor EB: from master coordinator of lysosomal pathways to candidate therapeutic target in degenerative storage diseases. Ann N Y Acad Sci. 2016 May;1371(1):3–14. doi: 10.1111/nyas.13131
  • Settembre C, Di Malta C, Polito VA, et al. TFEB links autophagy to lysosomal biogenesis. Science. 2011 Jun 17;332(6036):1429–1433. doi: 10.1126/science.1204592
  • Sardiello M, Palmieri M, di Ronza A, et al. A gene network regulating lysosomal biogenesis and function. Science. 2009 Jul 24;325(5939):473–477. doi: 10.1126/science.1174447
  • Briceño E, Calderon A, Sotelo J. Institutional experience with chloroquine as an adjuvant to the therapy for glioblastoma multiforme. Surg Neurol. 2007 Apr;67(4):388–391. doi: 10.1016/j.surneu.2006.08.080
  • Mariño G, Niso-Santano M, Baehrecke EH, et al. Self-consumption: the interplay of autophagy and apoptosis. Nat Rev Mol Cell Biol. 2014 Feb;15(2):81–94. doi: 10.1038/nrm3735
  • Amaravadi R, Kimmelman AC, White E Recent insights into the function of autophagy in cancer. Genes Dev. 2016 Sep 1;30(17):1913–1930. doi: 10.1101/gad.287524.116
  • O’Reilly KE, Rojo F, She QB, et al. mTOR inhibition induces upstream receptor tyrosine kinase signaling and activates Akt. Cancer Res. 2006 Feb 1;66(3):1500–1508. doi: 10.1158/0008-5472.CAN-05-2925
  • Mahalingam D, Mita M, Sarantopoulos J, et al. Combined autophagy and HDAC inhibition: a phase I safety, tolerability, pharmacokinetic, and pharmacodynamic analysis of hydroxychloroquine in combination with the HDAC inhibitor vorinostat in patients with advanced solid tumors. Autophagy. 2014 Aug;10(8):1403–1414. doi: 10.4161/auto.29231
  • Kong C, Li Y, Liu Z, et al. Targeting the oncogene KRAS mutant pancreatic cancer by synergistic blocking of lysosomal acidification and rapid drug release. ACS Nano. 2019 Apr 23;13(4):4049–4063. doi: 10.1021/acsnano.8b08246
  • Mathew R, Karantza-Wadsworth V, White E. Role of autophagy in cancer. Nat Rev Cancer. 2007 Dec;7(12):961–967. doi: 10.1038/nrc2254
  • Jiang GM, Tan Y, Wang H, et al. The relationship between autophagy and the immune system and its applications for tumor immunotherapy. Mol Cancer. 2019 Jan 24;18(1):17. doi: 10.1186/s12943-019-0944-z
  • Stupp R, Hegi ME, van den Bent MJ, et al. Changing paradigms–an update on the multidisciplinary management of malignant glioma. Oncology. 2006 Feb;11(2):165–180. doi: 10.1634/theoncologist.11-2-165
  • Dehdashti AR, Hegi ME, Regli L, et al. New trends in the medical management of glioblastoma multiforme: the role of temozolomide chemotherapy. Neurosurg Focus. 2006 Apr 15;20(4):E6. doi: 10.3171/foc.2006.20.4.3
  • Franceschi E, Tosoni A, Bartolini S, et al. Treatment options for recurrent glioblastoma: pitfalls and future trends. Expert Rev Anticancer Ther. 2009 May;9(5):613–619. doi: 10.1586/era.09.23
  • Jhaveri N, Cho H, Torres S, et al. Noscapine inhibits tumor growth in TMZ-resistant gliomas. Cancer Lett. 2011 Dec 22;312(2):245–252. doi: 10.1016/j.canlet.2011.08.015
  • Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) Method. Methods (San Diego Calif). 2001 Dec;25(4):402–408. doi: 10.1006/meth.2001.1262
  • Heinonen JK, Lahti RJ A new and convenient colorimetric determination of inorganic orthophosphate and its application to the assay of inorganic pyrophosphatase. Anal Biochem. 1981 May 15;113(2):313–317. doi: 10.1016/0003-2697(81)90082-8
  • Cho HY, Wang W, Jhaveri N, et al. NEO212, temozolomide conjugated to perillyl alcohol, is a novel drug for effective treatment of a broad range of temozolomide-resistant gliomas. Mol Cancer Ther. 2014 Aug;13(8):2004–2017. doi: 10.1158/1535-7163.MCT-13-0964

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.