3,373
Views
27
CrossRef citations to date
0
Altmetric
Research Paper - Basic Science

HDAC6 differentially regulates autophagy in stem-like versus differentiated cancer cells

ORCID Icon, , , , , , , , , , & show all
Pages 686-706 | Received 08 Feb 2017, Accepted 31 Oct 2018, Published online: 04 Dec 2018

References

  • Polyak K, Hahn WC. Roots and stems: stem cells in cancer. Nat Med. 2006 Mar;12(3):296–300. PubMed PMID: 16520777.
  • Dean M. Cancer stem cells: implications for cancer causation and therapy resistance. Discov Med. 2005 Jun;5(27):278–282. PubMed PMID: 20704888.
  • Clevers H. The cancer stem cell: premises, promises and challenges. Nat Med. 2011 Mar;17(3):313–319. PubMed PMID: 21386835.
  • Huang J, Klionsky DJ. Autophagy and human disease. Cell Cycle. 2007 Aug 1;6(15):1837–1849. PubMed PMID: 17671424.
  • Levy JMM, Towers CG, Thorburn A. Targeting autophagy in cancer. Nat Rev Cancer. 2017 Sep;17(9):528–542. PubMed PMID: 28751651.
  • Kimmelman AC, White E. Autophagy and tumor metabolism. Cell Metab. 2017 May 02;25(5):1037–1043. PubMed PMID: 28467923; PubMed Central PMCID: PMCPMC5604466.
  • Mathew R, Karantza-Wadsworth V, White E. Role of autophagy in cancer. Nat Rev Cancer. 2007 Dec;7(12):961–967. PubMed PMID: 17972889; PubMed Central PMCID: PMCPMC2866167.
  • Janku F, McConkey DJ, Hong DS, et al. Autophagy as a target for anticancer therapy. Nat Rev Clin Oncol. 2011 May 17;8(9):528–539. PubMed PMID: 21587219.
  • Levine B, Packer M, Codogno P. Development of autophagy inducers in clinical medicine. J Clin Invest. 2015 Jan;125(1):14–24. PubMed PMID: 25654546; PubMed Central PMCID: PMCPMC4382267.
  • Manic G, Obrist F, Kroemer G, et al. Chloroquine and hydroxychloroquine for cancer therapy. Mol Cell Oncol. 2014;1(1):e29911. PubMed PMID: 27308318; PubMed Central PMCID: PMCPMC4905171.
  • Sharif T, Martell E, Dai C, et al. Autophagic homeostasis is required for the pluripotency of cancer stem cells. Autophagy. 2017; 13(2):264–284. PubMed PMID: 27929731; PubMed Central PMCID: PMC5324853.
  • Pandey UB, Nie Z, Batlevi Y, et al. HDAC6 rescues neurodegeneration and provides an essential link between autophagy and the UPS. Nature. 2007 Jun 14;447(7146):859–863. PubMed PMID: 17568747.
  • Zhang Z, Yamashita H, Toyama T, et al. HDAC6 expression is correlated with better survival in breast cancer. Clin Cancer Res. 2004 Oct 15;10(20):6962–6968. PubMed PMID: 15501975.
  • Lee YS, Lim KH, Guo X, et al. The cytoplasmic deacetylase HDAC6 is required for efficient oncogenic tumorigenesis. Cancer Res. 2008 Sep 15;68(18):7561–7569. PubMed PMID: 18794144; PubMed Central PMCID: PMCPMC2978070.
  • Sakuma T, Uzawa K, Onda T, et al. Aberrant expression of histone deacetylase 6 in oral squamous cell carcinoma. Int J Oncol. 2006 Jul;29(1):117–124. PubMed PMID: 16773191.
  • Shan B, Yao TP, Nguyen HT, et al. Requirement of HDAC6 for transforming growth factor-beta1-induced epithelial-mesenchymal transition. J Biol Chem. 2008 Jul 25;283(30):21065–21073. PubMed PMID: 18499657; PubMed Central PMCID: PMCPMC2475688.
  • Wang KH, Kao AP, Chang CC, et al. Increasing CD44+/CD24(-) tumor stem cells, and upregulation of COX-2 and HDAC6, as major functions of HER2 in breast tumorigenesis. Mol Cancer. 2010 Nov 02;9:288. PubMed PMID: 21044318; PubMed Central PMCID: PMCPMC2989327.
  • Mak AB, Nixon AM, Kittanakom S, et al. Regulation of CD133 by HDAC6 promotes beta-catenin signaling to suppress cancer cell differentiation. Cell Rep. 2012 Oct 25;2(4):951–963. PubMed PMID: 23084749; PubMed Central PMCID: PMCPMC3590846.
  • Bradbury CA, Khanim FL, Hayden R, et al. Histone deacetylases in acute myeloid leukaemia show a distinctive pattern of expression that changes selectively in response to deacetylase inhibitors. Leukemia. 2005 Oct;19(10):1751–1759. PubMed PMID: 16121216.
  • Jung KH, Noh JH, Kim JK, et al. Histone deacetylase 6 functions as a tumor suppressor by activating c-Jun NH2-terminal kinase-mediated beclin 1-dependent autophagic cell death in liver cancer. Hepatology. 2012 Aug;56(2):644–657. PubMed PMID: 22392728.
  • Lee JY, Koga H, Kawaguchi Y, et al. HDAC6 controls autophagosome maturation essential for ubiquitin-selective quality-control autophagy. Embo J. 2010 Mar 03;29(5):969–980. PubMed PMID: 20075865; PubMed Central PMCID: PMCPMC2837169.
  • Zhu T, Zhao D, Song Z, et al. HDAC6 alleviates prion peptide-mediated neuronal death via modulating PI3K-Akt-mTOR pathway. Neurobiol Aging. 2016 Jan;37:91–102. PubMed PMID: 26507311.
  • West AC, Johnstone RW. New and emerging HDAC inhibitors for cancer treatment. J Clin Invest. 2014 Jan;124(1):30–39. PubMed PMID: 24382387; PubMed Central PMCID: PMCPMC3871231.
  • Marchion D, Munster P. Development of histone deacetylase inhibitors for cancer treatment. Expert Rev Anticancer Ther. 2007 Apr;7(4):583–598. PubMed PMID: 17428177.
  • Valente S, Mai A. Small-molecule inhibitors of histone deacetylase for the treatment of cancer and non-cancer diseases: a patent review (2011–2013). Expert Opin Ther Pat. 2014 Apr;24(4):401–415. PubMed PMID: 24397271.
  • Ceccacci E, Minucci S. Inhibition of histone deacetylases in cancer therapy: lessons from leukaemia. Br J Cancer. 2016 Mar 15;114(6):605–611. PubMed PMID: 26908329; PubMed Central PMCID: PMCPMC4800301.
  • Santo L, Hideshima T, Kung AL, et al. Preclinical activity, pharmacodynamic, and pharmacokinetic properties of a selective HDAC6 inhibitor, ACY-1215, in combination with bortezomib in multiple myeloma. Blood. 2012 Mar 15;119(11):2579–2589. PubMed PMID: 22262760; PubMed Central PMCID: PMCPMC3337713.
  • Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006 Aug 25;126(4):663–676. PubMed PMID: 16904174.
  • Lin Y, Yang Y, Li W, et al. Reciprocal regulation of Akt and Oct4 promotes the self-renewal and survival of embryonal carcinoma cells. Mol Cell. 2012 Nov 30;48(4):627–640. PubMed PMID: 23041284; PubMed Central PMCID: PMCPMC3601782.
  • Kim BS, Lee CH, Chang GE, et al. A potent and selective small molecule inhibitor of sirtuin 1 promotes differentiation of pluripotent P19 cells into functional neurons. Sci Rep. 2016 Sep 29;6:34324. PubMed PMID: 27680533; PubMed Central PMCID: PMCPMC5041152.
  • Sharif T, Auger C, Bronner C, et al. Selective proapoptotic activity of polyphenols from red wine on teratocarcinoma cell, a model of cancer stem-like cell. Invest New Drugs. 2011 Apr;29(2):239–247. PubMed PMID: 19943082.
  • Silvan U, Diez-Torre A, Arluzea J, et al. Hypoxia and pluripotency in embryonic and embryonal carcinoma stem cell biology. Differentiation. 2009 Sep-Oct;78(2–3):159–168. PubMed PMID: 19604622.
  • Tripathi R, Samadder T, Gupta S, et al. Anticancer activity of a combination of cisplatin and fisetin in embryonal carcinoma cells and xenograft tumors. Mol Cancer Ther. 2011 Feb;10(2):255–268. PubMed PMID: 21216935.
  • Mani SA, Guo W, Liao MJ, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell. 2008 May 16;133(4):704–715. PubMed PMID: 18485877; PubMed Central PMCID: PMCPMC2728032.
  • Gupta PB, Onder TT, Jiang G, et al. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell. 2009 Aug 21;138(4):645–659. PubMed PMID: 19682730; PubMed Central PMCID: PMCPMC4892125.
  • Andrews PW. Retinoic acid induces neuronal differentiation of a cloned human embryonal carcinoma cell line in vitro. Dev Biol. 1984 Jun;103(2):285–293. PubMed PMID: 6144603.
  • Weekes MP, Tomasec P, Huttlin EL, et al. Quantitative temporal viromics: an approach to investigate host-pathogen interaction. Cell. 2014 Jun 5;157(6):1460–1472. PubMed PMID: 24906157; PubMed Central PMCID: PMCPMC4048463.
  • Park SW, Lim HY, Do HJ, et al. Regulation of human growth and differentiation factor 3 gene expression by NANOG in human embryonic carcinoma NCCIT cells. FEBS Lett. 2012 Sep 21;586(19):3529–3535. PubMed PMID: 22963770.
  • Caricasole AA, van Schaik RH, Zeinstra LM, et al. Human growth-differentiation factor 3 (hGDF3): developmental regulation in human teratocarcinoma cell lines and expression in primary testicular germ cell tumours. Oncogene. 1998 Jan 08;16(1):95–103. PubMed PMID: 9467948.
  • Vaz AP, Ponnusamy MP, Rachagani S, et al. Novel role of pancreatic differentiation 2 in facilitating self-renewal and drug resistance of pancreatic cancer stem cells. Br J Cancer. 2014 Jul 29;111(3):486–496. PubMed PMID: 25003666; PubMed Central PMCID: PMCPMC4119968.
  • Escobar B, de Carcer G, Fernandez-Miranda G, et al. Brick1 is an essential regulator of actin cytoskeleton required for embryonic development and cell transformation. Cancer Res. 2010 Nov 15;70(22):9349–9359. PubMed PMID: 20861187.
  • Tominaga M, Tomooka Y. Novel genes cloned from a neuronal cell line newly established from a cerebellum of an adult p53(-/-) mouse. Biochem Biophys Res Commun. 2002 Sep 27;297(3):473–479. PubMed PMID: 12270117.
  • Ruggero D, Pandolfi PP. Does the ribosome translate cancer? Nat Rev Cancer. 2003 Mar;3(3):179–192. PubMed PMID: 12612653.
  • Duncan EM, Muratore-Schroeder TL, Cook RG, et al. Cathepsin L proteolytically processes histone H3 during mouse embryonic stem cell differentiation. Cell. 2008 Oct 17;135(2):284–294. PubMed PMID: 18957203; PubMed Central PMCID: PMCPMC2579750.
  • Vossaert L, Meert P, Scheerlinck E, et al. Identification of histone H3 clipping activity in human embryonic stem cells. Stem Cell Res. 2014 Jul;13(1):123–134. PubMed PMID: 24874291.
  • Klionsky DJ, Abdelmohsen K, Abe A, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy. 2016 Jan 2;12(1):1–222. PubMed PMID: 26799652; Eng.
  • Hay N, Sonenberg N. Upstream and downstream of mTOR. Genes Dev. 2004 Aug 15;18(16):1926–1945. PubMed PMID: 15314020.
  • Nave BT, Ouwens M, Withers DJ, et al. Mammalian target of rapamycin is a direct target for protein kinase B: identification of a convergence point for opposing effects of insulin and amino-acid deficiency on protein translation. Biochem J. 1999 Dec 01;344 Pt 2:427–431. PubMed PMID: 10567225; PubMed Central PMCID: PMCPMC1220660.
  • Inoki K, Li Y, Xu T, et al. Rheb GTPase is a direct target of TSC2 GAP activity and regulates mTOR signaling. Genes Dev. 2003 Aug 01;17(15):1829–1834. PubMed PMID: 12869586; PubMed Central PMCID: PMCPMC196227.
  • Inoki K, Li Y, Zhu T, et al. TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat Cell Biol. 2002 Sep;4(9):648–657. PubMed PMID: 12172553.
  • Goncharova EA, Goncharov DA, Eszterhas A, et al. Tuberin regulates p70 S6 kinase activation and ribosomal protein S6 phosphorylation. A role for the TSC2 tumor suppressor gene in pulmonary lymphangioleiomyomatosis (LAM). J Biol Chem. 2002 Aug 23;277(34):30958–30967. PubMed PMID: 12045200.
  • Ng S, Wu YT, Chen B, et al. Impaired autophagy due to constitutive mTOR activation sensitizes TSC2-null cells to cell death under stress. Autophagy. 2011 Oct;7(10):1173–1186. PubMed PMID: 21808151.
  • Fingar DC, Salama S, Tsou C, et al. Mammalian cell size is controlled by mTOR and its downstream targets S6K1 and 4EBP1/eIF4E. Genes Dev. 2002 Jun 15;16(12):1472–1487. PubMed PMID: 12080086; PubMed Central PMCID: PMCPMC186342.
  • Debacq-Chainiaux F, Erusalimsky JD, Campisi J, et al. Protocols to detect senescence-associated beta-galactosidase (SA-betagal) activity, a biomarker of senescent cells in culture and in vivo. Nat Protoc. 2009;4(12):1798–1806. PubMed PMID: 20010931.
  • Aldana-Masangkay GI, Sakamoto KM. The role of HDAC6 in cancer. J Biomed Biotechnol. 2011;2011:875824. PubMed PMID: 21076528; PubMed Central PMCID: PMCPMC2975074.
  • Bazzaro M, Lin Z, Santillan A, et al. Ubiquitin proteasome system stress underlies synergistic killing of ovarian cancer cells by bortezomib and a novel HDAC6 inhibitor. Clin Cancer Res. 2008 Nov 15;14(22):7340–7347. PubMed PMID: 19010849; PubMed Central PMCID: PMCPMC2744414.
  • O’Brien CA, Pollett A, Gallinger S, et al. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature. 2007 Jan 4;445(7123):106–110. PubMed PMID: 17122772.
  • Ricci-Vitiani L, Lombardi DG, Pilozzi E, et al. Identification and expansion of human colon-cancer-initiating cells. Nature. 2007 Jan 4;445(7123):111–115. PubMed PMID: 17122771.
  • Lapidot T, Sirard C, Vormoor J, et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature. 1994 Feb 17;367(6464):645–648. PubMed PMID: 7509044; eng.
  • Blum B, Benvenisty N. The tumorigenicity of human embryonic stem cells. Adv Cancer Res. 2008;100:133–158. PubMed PMID: 18620095.
  • Nichols J, Zevnik B, Anastassiadis K, et al. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell. 1998 Oct 30;95(3):379–391. PubMed PMID: 9814708.
  • Niwa H, Miyazaki J, Smith AG. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet. 2000 Apr;24(4):372–376. PubMed PMID: 10742100.
  • Hubbert C, Guardiola A, Shao R, et al. HDAC6 is a microtubule-associated deacetylase. Nature. 2002 May 23;417(6887):455–458. PubMed PMID: 12024216.
  • Zhang X, Yuan Z, Zhang Y, et al. HDAC6 modulates cell motility by altering the acetylation level of cortactin. Mol Cell. 2007 Jul 20;27(2):197–213. PubMed PMID: 17643370; PubMed Central PMCID: PMCPMC2684874.
  • Connelly JT, Gautrot JE, Trappmann B, et al. Actin and serum response factor transduce physical cues from the microenvironment to regulate epidermal stem cell fate decisions. Nat Cell Biol. 2010 Jul;12(7):711–718. PubMed PMID: 20581838.
  • Hideshima T, Bradner JE, Wong J, et al. Small-molecule inhibition of proteasome and aggresome function induces synergistic antitumor activity in multiple myeloma. Proc Natl Acad Sci U S A. 2005 Jun 14;102(24):8567–8572. PubMed PMID: 15937109; PubMed Central PMCID: PMCPMC1150844.
  • Qin HX, Cui HK, Pan Y, et al. HDAC6 siRNA inhibits proliferation and induces apoptosis of HeLa cells and its related molecular mechanism. Asian Pac J Cancer Prev. 2012;13(7):3367–3371. PubMed PMID: 22994762.
  • Tang DG. Understanding cancer stem cell heterogeneity and plasticity. Cell Res. 2012 Mar;22(3):457–472. PubMed PMID: 22357481; PubMed Central PMCID: PMCPMC3292302.
  • Gupta PB, Chaffer CL, Weinberg RA. Cancer stem cells: mirage or reality? Nat Med. 2009 Sep;15(9):1010–1012. PubMed PMID: 19734877.
  • Artero-Castro A, Perez-Alea M, Feliciano A, et al. Disruption of the ribosomal P complex leads to stress-induced autophagy. Autophagy. 2015;11(9):1499–1519. PubMed PMID: 26176264; PubMed Central PMCID: PMCPMC4590587.
  • Yeo SK, Wen J, Chen S, et al. Autophagy differentially regulates distinct breast cancer stem-like cells in murine models via EGFR/Stat3 and Tgfbeta/Smad signaling. Cancer Res. 2016 Jun 01;76(11):3397–3410. PubMed PMID: 27197172; PubMed Central PMCID: PMCPMC4990205.
  • Kondo Y, Kondo S. Autophagy and cancer therapy. Autophagy. 2006 Apr-Jun;2(2):85–90. PubMed PMID: 16874083.
  • White E, DiPaola RS. The double-edged sword of autophagy modulation in cancer. Clin Cancer Res. 2009 Sep 01;15(17):5308–5316. PubMed PMID: 19706824; PubMed Central PMCID: PMCPMC2737083.
  • Kingston RE, Chen CA, Rose JK. Calcium phosphate transfection. Curr Protoc Mol Biol. 2003 Aug. Chapter 9: Unit9 1. PubMed PMID: 18265332. DOI:10.1002/0471142727.mb0901s63
  • Murphy JP, Stepanova E, Everley RA, et al. Comprehensive temporal protein dynamics during the diauxic shift in saccharomyces cerevisiae. Mol Cell Proteomics. 2015 Sep;14(9):2454–2465. PubMed PMID: 26077900; PubMed Central PMCID: PMCPMC4563728.
  • Rappsilber J, Ishihama Y, Mann M. Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal Chem. 2003 Feb 1;75(3):663–670. PubMed PMID: 12585499.
  • Ting L, Rad R, Gygi SP, et al. MS3 eliminates ratio distortion in isobaric multiplexed quantitative proteomics. Nat Methods. 2011 Nov;8(11):937–940. PubMed PMID: 21963607; PubMed Central PMCID: PMCPMC3205343.

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.