Suberoylanilide hydroxamic acid (SAHA) causes tumor growth slowdown and triggers autophagy in glioblastoma stem cells

References

• Furnari FB, Fenton T, Bachoo RM, Mukasa A, Stommel JM, Stegh A, Hahn WC, Ligon KL, Louis DN, Brennan C, et al. Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev 2007; 21:2683 - 710; http://dx.doi.org/10.1101/gad.1596707; PMID: 17974913
   PubMed Web of Science ®Google Scholar
• Ricci-Vitiani L, Pallini R, Biffoni M, Todaro M, Invernici G, Cenci T, Maira G, Parati EA, Stassi G, Larocca LM, et al. Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells. Nature 2010; 468:824 - 8; http://dx.doi.org/10.1038/nature09557; PMID: 21102434
   PubMed Web of Science ®Google Scholar
• Wang R, Chadalavada K, Wilshire J, Kowalik U, Hovinga KE, Geber A, Fligelman B, Leversha M, Brennan C, Tabar V. Glioblastoma stem-like cells give rise to tumour endothelium. Nature 2010; 468:829 - 33; http://dx.doi.org/10.1038/nature09624; PMID: 21102433
   PubMed Web of Science ®Google Scholar
• Chiao MT, Yang YC, Cheng WY, Shen CC, Ko JL. CD133+ glioblastoma stem-like cells induce vascular mimicry in vivo. Curr Neurovasc Res 2011; 8:210 - 9; http://dx.doi.org/10.2174/156720211796558023; PMID: 21675958
   PubMed Web of Science ®Google Scholar
• Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006; 444:756 - 60; http://dx.doi.org/10.1038/nature05236; PMID: 17051156
   PubMed Web of Science ®Google Scholar
• Johannessen TC, Bjerkvig R, Tysnes BB. DNA repair and cancer stem-like cells--potential partners in glioma drug resistance?. Cancer Treat Rev 2008; 34:558 - 67; http://dx.doi.org/10.1016/j.ctrv.2008.03.125; PMID: 18501520
   PubMed Web of Science ®Google Scholar
• Coates JM, Galante JM, Bold RJ. Cancer therapy beyond apoptosis: autophagy and anoikis as mechanisms of cell death. J Surg Res 2010; 164:301 - 8; http://dx.doi.org/10.1016/j.jss.2009.07.011; PMID: 20031162
   PubMed Web of Science ®Google Scholar
• Lefranc F, Brotchi J, Kiss R. Possible future issues in the treatment of glioblastomas: special emphasis on cell migration and the resistance of migrating glioblastoma cells to apoptosis. J Clin Oncol 2005; 23:2411 - 22; http://dx.doi.org/10.1200/JCO.2005.03.089; PMID: 15800333
   PubMed Web of Science ®Google Scholar
• Lum JJ, Bauer DE, Kong M, Harris MH, Li C, Lindsten T, Thompson CB. Growth factor regulation of autophagy and cell survival in the absence of apoptosis. Cell 2005; 120:237 - 48; http://dx.doi.org/10.1016/j.cell.2004.11.046; PMID: 15680329
   PubMed Web of Science ®Google Scholar
• He C, Klionsky DJ. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 2009; 43:67 - 93; http://dx.doi.org/10.1146/annurev-genet-102808-114910; PMID: 19653858
   PubMed Web of Science ®Google Scholar
• Maiuri MC, Tasdemir E, Criollo A, Morselli E, Vicencio JM, Carnuccio R, Kroemer G. Control of autophagy by oncogenes and tumor suppressor genes. Cell Death Differ 2009; 16:87 - 93; http://dx.doi.org/10.1038/cdd.2008.131; PMID: 18806760
   PubMed Web of Science ®Google Scholar
• Degenhardt K, Mathew R, Beaudoin B, Bray K, Anderson D, Chen G, Mukherjee C, Shi Y, Gélinas C, Fan Y, et al. Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 2006; 10:51 - 64; http://dx.doi.org/10.1016/j.ccr.2006.06.001; PMID: 16843265
   PubMed Web of Science ®Google Scholar
• Gozuacik D, Kimchi A. Autophagy and cell death. Curr Top Dev Biol 2007; 78:217 - 45; http://dx.doi.org/10.1016/S0070-2153(06)78006-1; PMID: 17338918
   PubMed Web of Science ®Google Scholar
• Hashimoto D, Ohmuraya M, Hirota M, Yamamoto A, Suyama K, Ida S, Okumura Y, Takahashi E, Kido H, Araki K, et al. Involvement of autophagy in trypsinogen activation within the pancreatic acinar cells. J Cell Biol 2008; 181:1065 - 72; http://dx.doi.org/10.1083/jcb.200712156; PMID: 18591426
   PubMed Web of Science ®Google Scholar
• Wang L, Zou X, Berger AD, Twiss C, Peng Y, Li Y, Chiu J, Guo H, Satagopan J, Wilton A, et al. Increased expression of histone deacetylaces (HDACs) and inhibition of prostate cancer growth and invasion by HDAC inhibitor SAHA. Am J Transl Res 2009; 1:62 - 71; PMID: 19966939
   PubMed Web of Science ®Google Scholar
• Duvic M, Talpur R, Ni X, Zhang C, Hazarika P, Kelly C, Chiao JH, Reilly JF, Ricker JL, Richon VM, et al. Phase 2 trial of oral vorinostat (suberoylanilide hydroxamic acid, SAHA) for refractory cutaneous T-cell lymphoma (CTCL). Blood 2007; 109:31 - 9; http://dx.doi.org/10.1182/blood-2006-06-025999; PMID: 16960145
   PubMed Web of Science ®Google Scholar
• Nawrocki ST, Carew JS, Pino MS, Highshaw RA, Andtbacka RH, Dunner K Jr., Pal A, Bornmann WG, Chiao PJ, Huang P, et al. Aggresome disruption: a novel strategy to enhance bortezomib-induced apoptosis in pancreatic cancer cells. Cancer Res 2006; 66:3773 - 81; http://dx.doi.org/10.1158/0008-5472.CAN-05-2961; PMID: 16585204
   PubMed Web of Science ®Google Scholar
• Sangeetha SR, Singh N, Vender JR, Dhandapani KM. Suberoylanilide hydroxamic acid (SAHA) induces growth arrest and apoptosis in pituitary adenoma cells. Endocrine 2009; 35:389 - 96; http://dx.doi.org/10.1007/s12020-009-9159-1; PMID: 19291426
   PubMed Web of Science ®Google Scholar
• Inoue S, Walewska R, Dyer MJ, Cohen GM. Downregulation of Mcl-1 potentiates HDACi-mediated apoptosis in leukemic cells. Leukemia 2008; 22:819 - 25; http://dx.doi.org/10.1038/leu.2008.1; PMID: 18239621
   PubMed Web of Science ®Google Scholar
• Brahmachari S, Fung YK, Pahan K. Induction of glial fibrillary acidic protein expression in astrocytes by nitric oxide. J Neurosci 2006; 26:4930 - 9; http://dx.doi.org/10.1523/JNEUROSCI.5480-05.2006; PMID: 16672668
   PubMed Web of Science ®Google Scholar
• Liu YL, Yang PM, Shun CT, Wu MS, Weng JR, Chen CC. Autophagy potentiates the anti-cancer effects of the histone deacetylase inhibitors in hepatocellular carcinoma. Autophagy 2010; 6:1057 - 65; http://dx.doi.org/10.4161/auto.6.8.13365; PMID: 20962572
   PubMed Web of Science ®Google Scholar
• Li J, Liu R, Lei Y, Wang K, Lau QC, Xie N, Zhou S, Nie C, Chen L, Wei Y, et al. Proteomic analysis revealed association of aberrant ROS signaling with suberoylanilide hydroxamic acid-induced autophagy in Jurkat T-leukemia cells. Autophagy 2010; 6:711 - 24; http://dx.doi.org/10.4161/auto.6.6.12397; PMID: 20543569
   PubMed Web of Science ®Google Scholar
• Bjørkøy G, Lamark T, Brech A, Outzen H, Perander M, Overvatn A, Stenmark H, Johansen T. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol 2005; 171:603 - 14; http://dx.doi.org/10.1083/jcb.200507002; PMID: 16286508
   PubMed Web of Science ®Google Scholar
• Gammoh N, Marks PA, Jiang X. Curbing autophagy and histone deacetylases to kill cancer cells. Autophagy 2012; 8:1521 - 2; http://dx.doi.org/10.4161/auto.21151; PMID: 22894919
   PubMed Web of Science ®Google Scholar
• Gammoh N, Lam D, Puente C, Ganley I, Marks PA, Jiang X. Role of autophagy in histone deacetylase inhibitor-induced apoptotic and nonapoptotic cell death. Proc Natl Acad Sci U S A 2012; 109:6561 - 5; http://dx.doi.org/10.1073/pnas.1204429109; PMID: 22493260
   PubMed Web of Science ®Google Scholar
• Shintani T, Klionsky DJ. Autophagy in health and disease: a double-edged sword. Science 2004; 306:990 - 5; http://dx.doi.org/10.1126/science.1099993; PMID: 15528435
   PubMed Web of Science ®Google Scholar
• Cao Q, Yu C, Xue R, Hsueh W, Pan P, Chen Z, Wang S, McNutt M, Gu J. Autophagy induced by suberoylanilide hydroxamic acid in Hela S3 cells involves inhibition of protein kinase B and up-regulation of Beclin 1. Int J Biochem Cell Biol 2008; 40:272 - 83; http://dx.doi.org/10.1016/j.biocel.2007.07.020; PMID: 17881280
   PubMed Web of Science ®Google Scholar
• Petiot A, Ogier-Denis E, Blommaart EF, Meijer AJ, Codogno P. Distinct classes of phosphatidylinositol 3′-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J Biol Chem 2000; 275:992 - 8; http://dx.doi.org/10.1074/jbc.275.2.992; PMID: 10625637
   PubMed Web of Science ®Google Scholar
• Wu YT, Tan HL, Shui G, Bauvy C, Huang Q, Wenk MR, Ong CN, Codogno P, Shen HM. Dual role of 3-methyladenine in modulation of autophagy via different temporal patterns of inhibition on class I and III phosphoinositide 3-kinase. J Biol Chem 2010; 285:10850 - 61; http://dx.doi.org/10.1074/jbc.M109.080796; PMID: 20123989
   PubMed Web of Science ®Google Scholar
• Giansanti V, Torriglia A, Scovassi AI. Conversation between apoptosis and autophagy: “Is it your turn or mine?”. Apoptosis 2011; 16:321 - 33; http://dx.doi.org/10.1007/s10495-011-0589-x; PMID: 21404107
   PubMed Web of Science ®Google Scholar
• Basu S, Ganguly A, Chakraborty P, Sen R, Banerjee K, Chatterjee M, Efferth T, Choudhuri SK. Targeting the mitochondrial pathway to induce apoptosis/necrosis through ROS by a newly developed Schiff’s base to overcome MDR in cancer. Biochimie 2012; 94:166 - 83; http://dx.doi.org/10.1016/j.biochi.2011.10.004; PMID: 22037022
   PubMed Web of Science ®Google Scholar
• Carew JS, Nawrocki ST, Kahue CN, Zhang H, Yang C, Chung L, Houghton JA, Huang P, Giles FJ, Cleveland JL. Targeting autophagy augments the anticancer activity of the histone deacetylase inhibitor SAHA to overcome Bcr-Abl-mediated drug resistance. Blood 2007; 110:313 - 22; http://dx.doi.org/10.1182/blood-2006-10-050260; PMID: 17363733
   PubMed Web of Science ®Google Scholar
• Fariss MW, Chan CB, Patel M, Van Houten B, Orrenius S. Role of mitochondria in toxic oxidative stress. Mol Interv 2005; 5:94 - 111; http://dx.doi.org/10.1124/mi.5.2.7; PMID: 15821158
   PubMed Web of Science ®Google Scholar
• Azad MB, Chen Y, Gibson SB. Regulation of autophagy by reactive oxygen species (ROS): implications for cancer progression and treatment. Antioxid Redox Signal 2009; 11:777 - 90; http://dx.doi.org/10.1089/ars.2008.2270; PMID: 18828708
   PubMed Web of Science ®Google Scholar
• Dictus C, Tronnier V, Unterberg A, Herold-Mende C. Comparative analysis of in vitro conditions for rat adult neural progenitor cells. J Neurosci Methods 2007; 161:250 - 8; http://dx.doi.org/10.1016/j.jneumeth.2006.11.012; PMID: 17207861
   PubMed Web of Science ®Google Scholar
• Ziegler DS, Kung AL, Kieran MW. Anti-apoptosis mechanisms in malignant gliomas. J Clin Oncol 2008; 26:493 - 500; http://dx.doi.org/10.1200/JCO.2007.13.9717; PMID: 18202424
   PubMed Web of Science ®Google Scholar
• Bertrand J, Begaud-Grimaud G, Bessette B, Verdier M, Battu S, Jauberteau MO. Cancer stem cells from human glioma cell line are resistant to Fas-induced apoptosis. Int J Oncol 2009; 34:717 - 27; PMID: 19212677
   PubMed Web of Science ®Google Scholar
• Zhuang W, Li B, Long L, Chen L, Huang Q, Liang Z. Induction of autophagy promotes differentiation of glioma-initiating cells and their radiosensitivity. Int J Cancer 2011; 129:2720 - 31; http://dx.doi.org/10.1002/ijc.25975; PMID: 21384342
   PubMed Web of Science ®Google Scholar
• Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, Askew DS, Baba M, Baehrecke EH, Bahr BA, Ballabio A, et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008; 4:151 - 75; PMID: 18188003
   PubMed Web of Science ®Google Scholar
• Faraco G, Pancani T, Formentini L, Mascagni P, Fossati G, Leoni F, Moroni F, Chiarugi A. Pharmacological inhibition of histone deacetylases by suberoylanilide hydroxamic acid specifically alters gene expression and reduces ischemic injury in the mouse brain. Mol Pharmacol 2006; 70:1876 - 84; http://dx.doi.org/10.1124/mol.106.027912; PMID: 16946032
   PubMed Web of Science ®Google Scholar
• Di Bernardo G, Squillaro T, Dell’Aversana C, Miceli M, Cipollaro M, Cascino A, Altucci L, Galderisi U. Histone deacetylase inhibitors promote apoptosis and senescence in human mesenchymal stem cells. Stem Cells Dev 2009; 18:573 - 81; http://dx.doi.org/10.1089/scd.2008.0172; PMID: 18694296
   PubMed Web of Science ®Google Scholar
• Gillenwater AM, Zhong M, Lotan R. Histone deacetylase inhibitor suberoylanilide hydroxamic acid induces apoptosis through both mitochondrial and Fas (Cd95) signaling in head and neck squamous carcinoma cells. Mol Cancer Ther 2007; 6:2967 - 75; http://dx.doi.org/10.1158/1535-7163.MCT-04-0344; PMID: 18025281
   PubMed Web of Science ®Google Scholar
• Mielcarek M, Benn CL, Franklin SA, Smith DL, Woodman B, Marks PA, Bates GP. SAHA decreases HDAC 2 and 4 levels in vivo and improves molecular phenotypes in the R6/2 mouse model of Huntington’s disease. PLoS One 2011; 6:e27746; http://dx.doi.org/10.1371/journal.pone.0027746; PMID: 22140466
   PubMedGoogle Scholar
• Benn CL, Butler R, Mariner L, Nixon J, Moffitt H, Mielcarek M, Woodman B, Bates GP. Genetic knock-down of HDAC7 does not ameliorate disease pathogenesis in the R6/2 mouse model of Huntington’s disease. PLoS One 2009; 4:e5747; http://dx.doi.org/10.1371/journal.pone.0005747; PMID: 19484127
   PubMedGoogle Scholar
• Tormo D, Checińska A, Alonso-Curbelo D, Pérez-Guijarro E, Cañón E, Riveiro-Falkenbach E, Calvo TG, Larribere L, Megías D, Mulero F, et al. Targeted activation of innate immunity for therapeutic induction of autophagy and apoptosis in melanoma cells. Cancer Cell 2009; 16:103 - 14; http://dx.doi.org/10.1016/j.ccr.2009.07.004; PMID: 19647221
   PubMed Web of Science ®Google Scholar
• Shao Y, Gao Z, Marks PA, Jiang X. Apoptotic and autophagic cell death induced by histone deacetylase inhibitors. Proc Natl Acad Sci U S A 2004; 101:18030 - 5; http://dx.doi.org/10.1073/pnas.0408345102; PMID: 15596714
   PubMed Web of Science ®Google Scholar
• Boya P, González-Polo RA, Casares N, Perfettini JL, Dessen P, Larochette N, Métivier D, Meley D, Souquere S, Yoshimori T, et al. Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol 2005; 25:1025 - 40; http://dx.doi.org/10.1128/MCB.25.3.1025-1040.2005; PMID: 15657430
   PubMed Web of Science ®Google Scholar
• Ciechomska IA, Goemans GC, Skepper JN, Tolkovsky AM. Bcl-2 complexed with Beclin-1 maintains full anti-apoptotic function. Oncogene 2009; 28:2128 - 41; http://dx.doi.org/10.1038/onc.2009.60; PMID: 19347031
   PubMed Web of Science ®Google Scholar
• Geng Y, Kohli L, Klocke BJ, Roth KA. Chloroquine-induced autophagic vacuole accumulation and cell death in glioma cells is p53 independent. Neuro Oncol 2010; 12:473 - 81; PMID: 20406898
   PubMed Web of Science ®Google Scholar
• Kim EL, Wüstenberg R, Rübsam A, Schmitz-Salue C, Warnecke G, Bücker EM, Pettkus N, Speidel D, Rohde V, Schulz-Schaeffer W, et al. Chloroquine activates the p53 pathway and induces apoptosis in human glioma cells. Neuro Oncol 2010; 12:389 - 400; http://dx.doi.org/10.1093/neuonc/nop046; PMID: 20308316
   PubMed Web of Science ®Google Scholar
• Mathew R, Karp CM, Beaudoin B, Vuong N, Chen G, Chen HY, Bray K, Reddy A, Bhanot G, Gelinas C, et al. Autophagy suppresses tumorigenesis through elimination of p62. Cell 2009; 137:1062 - 75; http://dx.doi.org/10.1016/j.cell.2009.03.048; PMID: 19524509
   PubMed Web of Science ®Google Scholar
• Mathew R, Karantza-Wadsworth V, White E. Role of autophagy in cancer. Nat Rev Cancer 2007; 7:961 - 7; http://dx.doi.org/10.1038/nrc2254; PMID: 17972889
   PubMed Web of Science ®Google Scholar
• O’Donovan TR, O’Sullivan GC, McKenna SL. Induction of autophagy by drug-resistant esophageal cancer cells promotes their survival and recovery following treatment with chemotherapeutics. Autophagy 2011; 7:509 - 24; http://dx.doi.org/10.4161/auto.7.5.15066; PMID: 21325880
   PubMed Web of Science ®Google Scholar
• Guo XL, Li D, Hu F, Song JR, Zhang SS, Deng WJ, Sun K, Zhao QD, Xie XQ, Song YJ, et al. Targeting autophagy potentiates chemotherapy-induced apoptosis and proliferation inhibition in hepatocarcinoma cells. Cancer Lett 2012; 320:171 - 9; http://dx.doi.org/10.1016/j.canlet.2012.03.002; PMID: 22406827
   PubMed Web of Science ®Google Scholar
• Chen N, Debnath J. Autophagy and tumorigenesis. FEBS Lett 2010; 584:1427 - 35; http://dx.doi.org/10.1016/j.febslet.2009.12.034; PMID: 20035753
   PubMed Web of Science ®Google Scholar
• Goss P, Allan AL, Rodenhiser DI, Foster PJ, Chambers AF. New clinical and experimental approaches for studying tumor dormancy: does tumor dormancy offer a therapeutic target?. APMIS 2008; 116:552 - 68; PMID: 18834402
   PubMed Web of Science ®Google Scholar
• Fan QW, Weiss WA. Autophagy and Akt promote survival in glioma. Autophagy 2011; 7:536 - 8; http://dx.doi.org/10.4161/auto.7.5.14779; PMID: 21266843
   PubMed Web of Science ®Google Scholar
• Sundberg AL, Steffen AC. Enhancing the effect of radionuclide tumor targeting, using lysosomotropic weak bases. Int J Radiat Oncol Biol Phys 2007; 67:279 - 87; http://dx.doi.org/10.1016/j.ijrobp.2006.07.1369; PMID: 17189076
   PubMed Web of Science ®Google Scholar
• Young AR, Narita M, Ferreira M, Kirschner K, Sadaie M, Darot JF, Tavaré S, Arakawa S, Shimizu S, Watt FM, et al. Autophagy mediates the mitotic senescence transition. Genes Dev 2009; 23:798 - 803; http://dx.doi.org/10.1101/gad.519709; PMID: 19279323
   PubMed Web of Science ®Google Scholar
• Frew AJ, Johnstone RW, Bolden JE. Enhancing the apoptotic and therapeutic effects of HDAC inhibitors. Cancer Lett 2009; 280:125 - 33; http://dx.doi.org/10.1016/j.canlet.2009.02.042; PMID: 19359091
   PubMed Web of Science ®Google Scholar
• Boocock DJ, Faust GE, Patel KR, Schinas AM, Brown VA, Ducharme MP, Booth TD, Crowell JA, Perloff M, Gescher AJ, et al. Phase I dose escalation pharmacokinetic study in healthy volunteers of resveratrol, a potential cancer chemopreventive agent. Cancer Epidemiol Biomarkers Prev 2007; 16:1246 - 52; http://dx.doi.org/10.1158/1055-9965.EPI-07-0022; PMID: 17548692
   PubMed Web of Science ®Google Scholar
• Pasquier E, Kavallaris M, André N. Metronomic chemotherapy: new rationale for new directions. Nat Rev Clin Oncol 2010; 7:455 - 65; http://dx.doi.org/10.1038/nrclinonc.2010.82; PMID: 20531380
   PubMed Web of Science ®Google Scholar
• Hsin IL, Sheu GT, Chen HH, Chiu LY, Wang HD, Chan HW, Hsu CP, Ko JL. N-acetyl cysteine mitigates curcumin-mediated telomerase inhibition through rescuing of Sp1 reduction in A549 cells. Mutat Res 2010; 688:72 - 7; http://dx.doi.org/10.1016/j.mrfmmm.2010.03.011; PMID: 20363232
   PubMed Web of Science ®Google Scholar