Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Oncology Letters
      • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Biomedical Reports
      • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • Information for Authors
    • Information for Reviewers
    • Information for Librarians
    • Information for Advertisers
    • Conferences
  • Language Editing
Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • For Authors
    • For Reviewers
    • For Librarians
    • For Advertisers
    • Conferences
  • Language Editing
Login Register Submit
  • This site uses cookies
  • You can change your cookie settings at any time by following the instructions in our Cookie Policy. To find out more, you may read our Privacy Policy.

    I agree
Search articles by DOI, keyword, author or affiliation
Search
Advanced Search
presentation
Oncology Letters
Join Editorial Board Propose a Special Issue
Print ISSN: 1792-1074 Online ISSN: 1792-1082
Journal Cover
September-2021 Volume 22 Issue 3

Full Size Image

Sign up for eToc alerts
Recommend to Library

Journals

International Journal of Molecular Medicine

International Journal of Molecular Medicine

International Journal of Molecular Medicine is an international journal devoted to molecular mechanisms of human disease.

International Journal of Oncology

International Journal of Oncology

International Journal of Oncology is an international journal devoted to oncology research and cancer treatment.

Molecular Medicine Reports

Molecular Medicine Reports

Covers molecular medicine topics such as pharmacology, pathology, genetics, neuroscience, infectious diseases, molecular cardiology, and molecular surgery.

Oncology Reports

Oncology Reports

Oncology Reports is an international journal devoted to fundamental and applied research in Oncology.

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine is an international journal devoted to laboratory and clinical medicine.

Oncology Letters

Oncology Letters

Oncology Letters is an international journal devoted to Experimental and Clinical Oncology.

Biomedical Reports

Biomedical Reports

Explores a wide range of biological and medical fields, including pharmacology, genetics, microbiology, neuroscience, and molecular cardiology.

Molecular and Clinical Oncology

Molecular and Clinical Oncology

International journal addressing all aspects of oncology research, from tumorigenesis and oncogenes to chemotherapy and metastasis.

World Academy of Sciences Journal

World Academy of Sciences Journal

Multidisciplinary open-access journal spanning biochemistry, genetics, neuroscience, environmental health, and synthetic biology.

International Journal of Functional Nutrition

International Journal of Functional Nutrition

Open-access journal combining biochemistry, pharmacology, immunology, and genetics to advance health through functional nutrition.

International Journal of Epigenetics

International Journal of Epigenetics

Publishes open-access research on using epigenetics to advance understanding and treatment of human disease.

Medicine International

Medicine International

An International Open Access Journal Devoted to General Medicine.

Journal Cover
September-2021 Volume 22 Issue 3

Full Size Image

Sign up for eToc alerts
Recommend to Library

  • Article
  • Citations
    • Cite This Article
    • Download Citation
    • Create Citation Alert
    • Remove Citation Alert
    • Cited By
  • Similar Articles
    • Related Articles (in Spandidos Publications)
    • Similar Articles (Google Scholar)
    • Similar Articles (PubMed)
  • Download PDF
  • Download XML
  • View XML

  • Supplementary Files
    • Supplementary_Data.pdf
Article Open Access

Induction of synergistic non‑apoptotic cell death by simultaneously targeting proteasomes with bortezomib and histone deacetylase 6 with ricolinostat in head and neck tumor cells

  • Authors:
    • Kazuhiro Hattori
    • Naoharu Takano
    • Hiromi Kazama
    • Shota Moriya
    • Keitaro Miyake
    • Masaki Hiramoto
    • Kiyoaki Tsukahara
    • Keisuke Miyazawa
  • View Affiliations / Copyright

    Affiliations: Department of Otolaryngology, Head and Neck Surgery, Tokyo Medical University, Tokyo 160‑8402, Japan, Department of Biochemistry, Tokyo Medical University, Tokyo 160‑8402, Japan
    Copyright: © Hattori et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
  • Article Number: 680
    |
    Published online on: July 22, 2021
       https://doi.org/10.3892/ol.2021.12941
  • Expand metrics +
Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )
Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )
Cited By (CrossRef): 0 citations Loading Articles...

This article is mentioned in:



Abstract

Following surgery and chemoradiation, ~50% of patients with locally advanced head and neck tumors experience relapse within the first two years, with a poor prognosis. Therefore, a novel therapeutic approach is required. The aim of the present study was to investigate the effect of combination treatment with the proteasome inhibitor bortezomib (BTZ), and ricolinostat (RCS), a specific inhibitor of histone deacetylase 6 (HDAC6), on CAL27 and Detroit562 head and neck cancer cells. BTZ and RCS exhibited cytotoxicity in a dose‑ and time‑dependent manner. Simultaneous treatment with BTZ and RCS resulted in the synergistic enhancement of non‑apoptotic cell death and autophagy. The receptor‑interacting serine/threonine‑protein kinase 1 (RIPK1) inhibitor, necrostatin, but not the autophagy inhibitor, 3‑methyladenine, attenuated the cytotoxicity of combined BTZ and RCS treatment. Thus, necroptosis [type‑III programmed cell death (PCD)], but not autophagic cell death (type‑II PCD), appeared to contribute to the pronounced cytotoxicity. However, no phosphorylation of RIPK1 or mixed lineage kinase domain‑like protein was detectable in response to BTZ or RCS. Furthermore, RCS induced α‑tubulin acetylation and inhibited BTZ‑induced aggresome formation along with endoplasmic reticulum stress loading. Combined treatment with BTZ and RCS enhanced the production of reactive oxygen species (ROS). The ROS scavenger, N‑acetyl cysteine, abrogated the increase in cytotoxicity. These results suggest the potential therapeutic value of the dual targeting of the proteasome and HDCA6 for head and neck cancers through the induction of necroptosis‑like cell death along with ROS generation.
View Figures

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Figure 6

Figure 7

View References

1 

Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA and Jemal A: Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 68:394–424. 2018. View Article : Google Scholar : PubMed/NCBI

2 

Brockstein BE: Management of recurrent head and neck cancer: Recent progress and future directions. Drugs. 71:1551–1559. 2011. View Article : Google Scholar : PubMed/NCBI

3 

de Ruijter AJM, van Gennip AH, Caron HN, Kemp S and van Kuilenburg ABP: Histone deacetylases (HDACs): Characterization of the classical HDAC family. Biochem J. 370:737–749. 2003. View Article : Google Scholar : PubMed/NCBI

4 

Boyault C, Sadoul K, Pabion M and Khochbin S: HDAC6, at the crossroads between cytoskeleton and cell signaling by acetylation and ubiquitination. Oncogene. 26:5468–5476. 2007. View Article : Google Scholar : PubMed/NCBI

5 

Gao YS, Hubbert CC, Lu J, Lee YS, Lee JY and Yao TP: Histone deacetylase 6 regulates growth factor-induced actin remodeling and endocytosis. Mol Cell Biol. 27:8637–8647. 2007. View Article : Google Scholar : PubMed/NCBI

6 

Kawaguchi Y, Kovacs JJ, McLaurin A, Vance JM, Ito A and Yao TP: The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress. Cell. 115:727–738. 2003. View Article : Google Scholar : PubMed/NCBI

7 

Scroggins BT, Robzyk K, Wang D, Marcu MG, Tsutsumi S, Beebe K, Cotter RJ, Felts S, Toft D, Karnitz L, et al: An acetylation site in the middle domain of Hsp90 regulates chaperone function. Mol Cell. 25:151–159. 2007. View Article : Google Scholar : PubMed/NCBI

8 

Li T, Zhang C, Hassan S, Liu X, Song F, Chen K, Zhang W and Yang J: Histone deacetylase 6 in cancer. J Hematol Oncol. 11:1112018. View Article : Google Scholar : PubMed/NCBI

9 

Wang XX, Wan RZ and Liu ZP: Recent advances in the discovery of potent and selective HDAC6 inhibitors. Eur J Med Chem. 143:1406–1418. 2018. View Article : Google Scholar : PubMed/NCBI

10 

Tabas I and Ron D: Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat Cell Biol. 13:184–190. 2011. View Article : Google Scholar : PubMed/NCBI

11 

Komatsu S, Moriya S, Che XF, Yokoyama T, Kohno N and Miyazawa K: Combined treatment with SAHA, bortezomib, and clarithromycin for concomitant targeting of aggresome formation and intracellular proteolytic pathways enhances ER stress-mediated cell death in breast cancer cells. Biochem Biophys Res Commun. 437:41–47. 2013. View Article : Google Scholar : PubMed/NCBI

12 

Porter NJ, Mahendran A, Breslow R and Christianson DW: Unusual zinc-binding mode of HDAC6-selective hydroxamate inhibitors. Proc Natl Acad Sci USA. 114:13459–13464. 2017. View Article : Google Scholar : PubMed/NCBI

13 

Mishima Y, Santo L, Eda H, Cirstea D, Nemani N, Yee AJ, O'Donnell E, Selig MK, Quayle SN, Arastu-Kapur S, et al: Ricolinostat (ACY-1215) induced inhibition of aggresome formation accelerates carfilzomib-induced multiple myeloma cell death. Br J Haematol. 169:423–434. 2015. View Article : Google Scholar : PubMed/NCBI

14 

Komatsu S, Miyazawa K, Moriya S, Takase A, Naito M, Inazu M, Kohno N, Itoh M and Tomoda A: Clarithromycin enhances bortezomib-induced cytotoxicity via endoplasmic reticulum stress-mediated CHOP (GADD153) induction and autophagy in breast cancer cells. Int J Oncol. 40:1029–1039. 2012. View Article : Google Scholar : PubMed/NCBI

15 

Moriya S, Che XF, Komatsu S, Abe A, Kawaguchi T, Gotoh A, Inazu M, Tomoda A and Miyazawa K: Macrolide antibiotics block autophagy flux and sensitize to bortezomib via endoplasmic reticulum stress-mediated CHOP induction in myeloma cells. Int J Oncol. 42:1541–1550. 2013. View Article : Google Scholar : PubMed/NCBI

16 

Kazama H, Hiramoto M, Miyahara K, Takano N and Miyazawa K: Designing an effective drug combination for ER stress loading in cancer therapy using a real-time monitoring system. Biochem Biophys Res Commun. 501:286–292. 2018. View Article : Google Scholar : PubMed/NCBI

17 

Takeda A, Takano N, Kokuba H, Hino H, Moriya S, Abe A, Hiramoto M, Tsukahara K and Miyazawa K: Macrolide antibiotics enhance the antitumor effect of lansoprazole resulting in lysosomal membrane permeabilization-associated cell death. Int J Oncol. 57:1280–1292. 2020. View Article : Google Scholar : PubMed/NCBI

18 

Tanaka H, Hino H, Moriya S, Kazama H, Miyazaki M, Takano N, Hiramoto M, Tsukahara K and Miyazawa K: Comparison of autophagy inducibility in various tyrosine kinase inhibitors and their enhanced cytotoxicity via inhibition of autophagy in cancer cells in combined treatment with azithromycin. Biochem Biophys Rep. 22:1007502020.PubMed/NCBI

19 

Iwawaki T, Akai R, Kohno K and Miura M: A transgenic mouse model for monitoring endoplasmic reticulum stress. Nat Med. 10:98–102. 2003. View Article : Google Scholar : PubMed/NCBI

20 

Di Veroli GY, Fornari C, Wang D, Mollard S, Bramhall JL, Richards FM and Jodrell DI: Combenefit: An interactive platform for the analysis and visualization of drug combinations. Bioinformatics. 32:2866–2868. 2016. View Article : Google Scholar : PubMed/NCBI

21 

Amengual JE, Johannet P, Lombardo M, Zullo K, Hoehn D, Bhagat G, Scotto L, Jirau-Serrano X, Radeski D, Heinen J, et al: Dual targeting of protein degradation pathways with the selective HDAC6 inhibitor ACY-1215 and bortezomib is synergistic in lymphoma. Clin Cancer Res. 21:4663–4675. 2015. View Article : Google Scholar : PubMed/NCBI

22 

Yin C and Li P: Growth suppression of glioma cells using HDAC6 inhibitor, tubacin. Open Med. 13:221–226. 2018. View Article : Google Scholar : PubMed/NCBI

23 

Lohitesh K, Saini H, Srivastava A, Mukherjee S, Roy A and Chowdhury R: Autophagy inhibition potentiates SAHA-mediated apoptosis in glioblastoma cells by accumulation of damaged mitochondria. Oncol Rep. 39:2787–2796. 2018.PubMed/NCBI

24 

Kaizuka T, Morishita H, Hama Y, Tsukamoto S, Matsui T, Toyota Y, Kodama A, Ishihara T, Mizushima T and Mizushima N: An autophagic flux probe that releases an internal control. Mol Cell. 64:835–849. 2016. View Article : Google Scholar : PubMed/NCBI

25 

Papadopoulos C, Kravic B and Meyer H: Repair or lysophagy: Dealing with damaged lysosomes. J Mol Biol. 64:835–849. 2020.

26 

Kondo Y, Kanzawa T, Sawaya R and Kondo S: The role of autophagy in cancer development and response to therapy. Nat Rev Cancer. 5:726–734. 2005. View Article : Google Scholar : PubMed/NCBI

27 

Bialik S, Dasari SK and Kimchi A: Autophagy-dependent cell death-where, how and why a cell eats itself to death. J Cell Sci. 131:jcs2151522018. View Article : Google Scholar : PubMed/NCBI

28 

Galluzzi L, Vitale I, Aaronson SA, Abrams JM, Adam D, Agostinis P, Alnemri ES, Altucci L, Amelio I, Andrews DW, et al: Molecular mechanisms of cell death: Recommendations of the Nomenclature Committee on Cell Death 2018. Cell Death Differ. 25:486–541. 2018. View Article : Google Scholar : PubMed/NCBI

29 

Galluzzi L, Kepp O and Kroemer G: MLKL regulates necrotic plasma membrane permeabilization. Cell Res. 24:139–140. 2014. View Article : Google Scholar : PubMed/NCBI

30 

Huang D, Zheng X, Wang ZA, Chen X, He WT, Zhang Y, Xu JG, Zhao H, Shi W, Wang X, et al: The MLKL channel in necroptosis is an octamer formed by tetramers in a dyadic process. Mol Cell Biol. 37:e00497–16. 2017. View Article : Google Scholar

31 

Yan J: Interplay between HDAC6 and its interacting partners: Essential roles in the aggresome-autophagy pathway and neurodegenerative diseases. DNA Cell Biol. 33:567–580. 2014. View Article : Google Scholar : PubMed/NCBI

32 

Morrow CS, Porter TJ, Xu N, Arndt ZP, Ako-Asare K, Heo HJ, Thompson EAN and Moore DL: Vimentin coordinates protein turnover at the aggresome during neural stem cell quiescence exit. Cell Stem Cell. 26:558–568.e559. 2020. View Article : Google Scholar : PubMed/NCBI

33 

Johnston JA, Ward CL and Kopito RR: Aggresomes: A cellular response to misfolded proteins. J Cell Biol. 143:1883–1898. 1998. View Article : Google Scholar : PubMed/NCBI

34 

Miyahara K, Kazama H, Kokuba H, Komatsu S, Hirota A, Takemura J, Hirasawa K, Moriya S, Abe A, Hiramoto M, et al: Targeting bortezomib-induced aggresome formation using vinorelbine enhances the cytotoxic effect along with ER stress loading in breast cancer cell lines. Int J Oncol. 49:1848–1858. 2016. View Article : Google Scholar : PubMed/NCBI

35 

Marciniak SJ, Yun CY, Oyadomari S, Novoa I, Zhang Y, Jungreis R, Nagata K, Harding HP and Ron D: CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev. 18:3066–77. 2004. View Article : Google Scholar : PubMed/NCBI

36 

Goodall ML, Fitzwalter BE, Zahedi S, Wu M, Rodriguez D, Mulcahy-Levy JM, Green DR, Morgan M, Cramer SD and Thorburn A: The autophagy machinery controls cell death switching between apoptosis and necroptosis. Dev Cell. 37:337–349. 2016. View Article : Google Scholar : PubMed/NCBI

37 

Saito Y, Moriya S, Kazama H, Hirasawa K, Miyahara K, Kokuba H, Hino H, Kikuchi H, Takano N, Hiramoto M, et al: Amino acid starvation culture condition sensitizes EGFR-expressing cancer cell lines to gefitinib-mediated cytotoxicity by inducing atypical necroptosis. Int J Oncol. 52:1165–1177. 2018.PubMed/NCBI

38 

Moriya S, Komatsu S, Yamasaki K, Kawai Y, Kokuba H, Hirota A, Che XF, Inazu M, Gotoh A, Hiramoto M and Miyazawa K: Targeting the integrated networks of aggresome formation, proteasome, and autophagy potentiates ER stress-mediated cell death in multiple myeloma cells. Int J Oncol. 46:474–486. 2015. View Article : Google Scholar : PubMed/NCBI

39 

Tu BP and Weissman JS: Oxidative protein folding in eukaryotes: Mechanisms and consequences. J Cell Biol. 164:341–346. 2004. View Article : Google Scholar : PubMed/NCBI

40 

Chakravarthi S, Jessop CE and Bulleid NJ: The role of glutathione in disulfide bond formation and endoplasmic-reticulum-generated oxidative stress. EMBO Rep. 7:271–275. 2006. View Article : Google Scholar : PubMed/NCBI

41 

Görlach A, Bertram K, Hudecova S and Krizanova O: Calcium and ROS: A mutual interplay. Redox Biol. 6:260–271. 2015. View Article : Google Scholar

42 

Seervi M, Rani A, Sharma AK and Santhosh Kumar TR: ROS mediated ER stress induces Bax-Bak dependent and independent apoptosis in response to thioridazine. Biomed Pharmacother. 106:200–209. 2018. View Article : Google Scholar : PubMed/NCBI

43 

Lin Y, Jiang M, Chen W, Zhao T and Wei Y: Cancer and ER stress: Mutual crosstalk between autophagy, oxidative stress and inflammatory response. Biomed Pharmacother. 118:1092492019. View Article : Google Scholar : PubMed/NCBI

Related Articles

  • Abstract
  • View
  • Download
  • Twitter
Copy and paste a formatted citation
Spandidos Publications style
Hattori K, Takano N, Kazama H, Moriya S, Miyake K, Hiramoto M, Tsukahara K and Miyazawa K: Induction of synergistic non‑apoptotic cell death by simultaneously targeting proteasomes with bortezomib and histone deacetylase 6 with ricolinostat in head and neck tumor cells. Oncol Lett 22: 680, 2021.
APA
Hattori, K., Takano, N., Kazama, H., Moriya, S., Miyake, K., Hiramoto, M. ... Miyazawa, K. (2021). Induction of synergistic non‑apoptotic cell death by simultaneously targeting proteasomes with bortezomib and histone deacetylase 6 with ricolinostat in head and neck tumor cells. Oncology Letters, 22, 680. https://doi.org/10.3892/ol.2021.12941
MLA
Hattori, K., Takano, N., Kazama, H., Moriya, S., Miyake, K., Hiramoto, M., Tsukahara, K., Miyazawa, K."Induction of synergistic non‑apoptotic cell death by simultaneously targeting proteasomes with bortezomib and histone deacetylase 6 with ricolinostat in head and neck tumor cells". Oncology Letters 22.3 (2021): 680.
Chicago
Hattori, K., Takano, N., Kazama, H., Moriya, S., Miyake, K., Hiramoto, M., Tsukahara, K., Miyazawa, K."Induction of synergistic non‑apoptotic cell death by simultaneously targeting proteasomes with bortezomib and histone deacetylase 6 with ricolinostat in head and neck tumor cells". Oncology Letters 22, no. 3 (2021): 680. https://doi.org/10.3892/ol.2021.12941
Copy and paste a formatted citation
x
Spandidos Publications style
Hattori K, Takano N, Kazama H, Moriya S, Miyake K, Hiramoto M, Tsukahara K and Miyazawa K: Induction of synergistic non‑apoptotic cell death by simultaneously targeting proteasomes with bortezomib and histone deacetylase 6 with ricolinostat in head and neck tumor cells. Oncol Lett 22: 680, 2021.
APA
Hattori, K., Takano, N., Kazama, H., Moriya, S., Miyake, K., Hiramoto, M. ... Miyazawa, K. (2021). Induction of synergistic non‑apoptotic cell death by simultaneously targeting proteasomes with bortezomib and histone deacetylase 6 with ricolinostat in head and neck tumor cells. Oncology Letters, 22, 680. https://doi.org/10.3892/ol.2021.12941
MLA
Hattori, K., Takano, N., Kazama, H., Moriya, S., Miyake, K., Hiramoto, M., Tsukahara, K., Miyazawa, K."Induction of synergistic non‑apoptotic cell death by simultaneously targeting proteasomes with bortezomib and histone deacetylase 6 with ricolinostat in head and neck tumor cells". Oncology Letters 22.3 (2021): 680.
Chicago
Hattori, K., Takano, N., Kazama, H., Moriya, S., Miyake, K., Hiramoto, M., Tsukahara, K., Miyazawa, K."Induction of synergistic non‑apoptotic cell death by simultaneously targeting proteasomes with bortezomib and histone deacetylase 6 with ricolinostat in head and neck tumor cells". Oncology Letters 22, no. 3 (2021): 680. https://doi.org/10.3892/ol.2021.12941
Follow us
  • Twitter
  • LinkedIn
  • Facebook
About
  • Spandidos Publications
  • Careers
  • Cookie Policy
  • Privacy Policy
How can we help?
  • Help
  • Live Chat
  • Contact
  • Email to our Support Team