Reverse chemomodulatory effects of the SIRT1 activators resveratrol and SRT1720 in Ewing’s sarcoma cells: resveratrol suppresses and SRT1720 enhances etoposide- and vincristine-induced anticancer activity

详细信息    查看全文

• 作者：Jürgen Sonnemann ; Melanie Kahl…
• 关键词：Cancer therapy ; Ewing’s sarcoma ; SIRT1 ; STACs ; Resveratrol ; SRT1720
• 刊名：Journal of Cancer Research and Clinical Oncology
• 出版年：2016
• 出版时间：January 2016
• 年：2016
• 卷：142
• 期：1
• 页码：17-26
• 全文大小：546 KB
• 参考文献：Ahmad KA, Clement MV, Hanif IM, Pervaiz S (2004) Resveratrol inhibits drug-induced apoptosis in human leukemia cells by creating an intracellular milieu nonpermissive for death execution. Cancer Res 64:1452–1459PubMed CrossRef
  Amiri F, Zarnani AH, Zand H, Koohdani F, Jeddi-Tehrani M, Vafa M (2013) Synergistic anti-proliferative effect of resveratrol and etoposide on human hepatocellular and colon cancer cell lines. Eur J Pharmacol 718:34–40PubMed CrossRef
  Balamuth NJ, Womer RB (2010) Ewing’s sarcoma. Lancet Oncol 11:184–192PubMed CrossRef
  Baur JA, Ungvari Z, Minor RK, Le Couteur DG, de Cabo R (2012) Are sirtuins viable targets for improving healthspan and lifespan? Nat Rev Drug Discov 11:443–461PubMed PubMedCentral CrossRef
  Bhardwaj A, Sethi G, Vadhan-Raj S, Bueso-Ramos C, Takada Y, Gaur U, Nair AS, Shishodia S, Aggarwal BB (2007) Resveratrol inhibits proliferation, induces apoptosis, and overcomes chemoresistance through down-regulation of STAT3 and nuclear factor-kappaB-regulated antiapoptotic and cell survival gene products in human multiple myeloma cells. Blood 109:2293–2302PubMed CrossRef
  Brunet A, Sweeney LB, Sturgill JF, Chua KF, Greer PL, Lin Y, Tran H, Ross SE, Mostoslavsky R, Cohen HY, Hu LS, Cheng HL, Jedrychowski MP, Gygi SP, Sinclair DA, Alt FW, Greenberg ME (2004) Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303:2011–2015PubMed CrossRef
  Castillo-Pichardo L, Cubano LA, Dharmawardhane S (2013) Dietary grape polyphenol resveratrol increases mammary tumor growth and metastasis in immunocompromised mice. BMC Complement Altern Med 13:6PubMed PubMedCentral CrossRef
  Chan JY, Phoo MS, Clement MV, Pervaiz S, Lee SC (2008) Resveratrol displays converse dose-related effects on 5-fluorouracil-evoked colon cancer cell apoptosis: the roles of caspase-6 and p53. Cancer Biol Ther 7:1305–1312PubMed CrossRef
  Chauhan D, Bandi M, Singh AV, Ray A, Raje N, Richardson P, Anderson KC (2011) Preclinical evaluation of a novel SIRT1 modulator SRT1720 in multiple myeloma cells. Br J Haematol 155:588–598PubMed PubMedCentral CrossRef
  Chou TC (2006) Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev 58:621–681PubMed CrossRef
  Dasgupta B, Milbrandt J (2007) Resveratrol stimulates AMP kinase activity in neurons. Proc Natl Acad Sci USA 104:7217–7222PubMed PubMedCentral CrossRef
  Dorrie J, Gerauer H, Wachter Y, Zunino SJ (2001) Resveratrol induces extensive apoptosis by depolarizing mitochondrial membranes and activating caspase-9 in acute lymphoblastic leukemia cells. Cancer Res 61:4731–4739PubMed
  Fang Y, Nicholl MB (2011) Sirtuin 1 in malignant transformation: friend or foe? Cancer Lett 306:10–14PubMed CrossRef
  Ferraz da Costa DC, Casanova FA, Quarti J, Malheiros MS, Sanches D, Dos Santos PS, Fialho E, Silva JL (2012) Transient transfection of a wild-type p53 gene triggers resveratrol-induced apoptosis in cancer cells. PLoS One 7:e48746PubMed PubMedCentral CrossRef
  Fukui M, Yamabe N, Zhu BT (2010) Resveratrol attenuates the anticancer efficacy of paclitaxel in human breast cancer cells in vitro and in vivo. Eur J Cancer 46:1882–1891PubMed PubMedCentral CrossRef
  Fulda S, Debatin KM (2004) Sensitization for anticancer drug-induced apoptosis by the chemopreventive agent resveratrol. Oncogene 23:6702–6711PubMed CrossRef
  Fulda S, Debatin KM (2005) Resveratrol-mediated sensitisation to TRAIL-induced apoptosis depends on death receptor and mitochondrial signalling. Eur J Cancer 41:786–798PubMed CrossRef
  Gatta G, Botta L, Rossi S, Aareleid T, Bielska-Lasota M, Clavel J, Dimitrova N, Jakab Z, Kaatsch P, Lacour B, Mallone S, Marcos-Gragera R, Minicozzi P, Sanchez-Perez MJ, Sant M, Santaquilani M, Stiller C, Tavilla A, Trama A, Visser O, Peris-Bonet R (2014) Childhood cancer survival in Europe 1999–2007: results of EUROCARE-5-a population-based study. Lancet Oncol 15:35–47PubMed CrossRef
  Guarente L, Franklin H (2011) Epstein lecture: sirtuins, aging, and medicine. N Engl J Med 364:2235–2244PubMed CrossRef
  Gupta SC, Kannappan R, Reuter S, Kim JH, Aggarwal BB (2011) Chemosensitization of tumors by resveratrol. Ann NY Acad Sci 1215:150–160PubMed PubMedCentral CrossRef
  Harikumar KB, Kunnumakkara AB, Sethi G, Diagaradjane P, Anand P, Pandey MK, Gelovani J, Krishnan S, Guha S, Aggarwal BB (2010) Resveratrol, a multitargeted agent, can enhance antitumor activity of gemcitabine in vitro and in orthotopic mouse model of human pancreatic cancer. Int J Cancer 127:257–268PubMed PubMedCentral
  Huang C, Ma WY, Goranson A, Dong Z (1999) Resveratrol suppresses cell transformation and induces apoptosis through a p53-dependent pathway. Carcinogenesis 20:237–242PubMed CrossRef
  Hubbard BP, Sinclair DA (2014) Small molecule SIRT1 activators for the treatment of aging and age-related diseases. Trends Pharmacol Sci 35:146–154PubMed PubMedCentral CrossRef
  Hubbard BP, Gomes AP, Dai H, Li J, Case AW, Considine T, Riera TV, Lee JE, SY E, Lamming DW, Pentelute BL, Schuman ER, Stevens LA, Ling AJ, Armour SM, Michan S, Zhao H, Jiang Y, Sweitzer SM, Blum CA, Disch JS, Ng PY, Howitz KT, Rolo AP, Hamuro Y, Moss J, Perni RB, Ellis JL, Vlasuk GP, Sinclair DA (2013) Evidence for a common mechanism of SIRT1 regulation by allosteric activators. Science 339:1216–1219PubMed PubMedCentral CrossRef
  Jang M, Cai L, Udeani GO, Slowing KV, Thomas CF, Beecher CW, Fong HH, Farnsworth NR, Kinghorn AD, Mehta RG, Moon RC, Pezzuto JM (1997) Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science 275:218–220PubMed CrossRef
  Jazirehi AR, Bonavida B (2004) Resveratrol modifies the expression of apoptotic regulatory proteins and sensitizes non-Hodgkin’s lymphoma and multiple myeloma cell lines to paclitaxel-induced apoptosis. Mol Cancer Ther 3:71–84PubMed CrossRef
  Lain S, Hollick JJ, Campbell J, Staples OD, Higgins M, Aoubala M, McCarthy A, Appleyard V, Murray KE, Baker L, Thompson A, Mathers J, Holland SJ, Stark MJ, Pass G, Woods J, Lane DP, Westwood NJ (2008) Discovery, in vivo activity, and mechanism of action of a small-molecule p53 activator. Cancer Cell 13:454–463PubMed PubMedCentral CrossRef
  Lessnick SL, Ladanyi M (2012) Molecular pathogenesis of Ewing sarcoma: new therapeutic and transcriptional targets. Annu Rev Pathol 7:145–159PubMed PubMedCentral CrossRef
  Lim JH, Lee YM, Chun YS, Chen J, Kim JE, Park JW (2010) Sirtuin 1 modulates cellular responses to hypoxia by deacetylating hypoxia-inducible factor 1alpha. Mol Cell 38:864–878PubMed CrossRef
  Liontas A, Yeger H (2004) Curcumin and resveratrol induce apoptosis and nuclear translocation and activation of p53 in human neuroblastoma. Anticancer Res 24:987–998PubMed
  Liu M, Wilk SA, Wang A, Zhou L, Wang RH, Ogawa W, Deng C, Dong LQ, Liu F (2010) Resveratrol inhibits mTOR signaling by promoting the interaction between mTOR and DEPTOR. J Biol Chem 285:36387–36394PubMed PubMedCentral CrossRef
  Luo J, Nikolaev AY, Imai S, Chen D, Su F, Shiloh A, Guarente L, Gu W (2001) Negative control of p53 by Sir2alpha promotes cell survival under stress. Cell 107:137–148PubMed CrossRef
  Mahida JP, Antczak C, Decarlo D, Champ KG, Francis JH, Marr B, Polans AS, Albert DM, Abramson DH, Djaballah H (2013) A synergetic screening approach with companion effector for combination therapy: application to retinoblastoma. PLoS One 8:e59156PubMed PubMedCentral CrossRef
  Marshall GM, Liu PY, Gherardi S, Scarlett CJ, Bedalov A, Xu N, Iraci N, Valli E, Ling D, Thomas W, van Bekkum M, Sekyere E, Jankowski K, Trahair T, Mackenzie KL, Haber M, Norris MD, Biankin AV, Perini G, Liu T (2011) SIRT1 promotes N-Myc oncogenesis through a positive feedback loop involving the effects of MKP3 and ERK on N-Myc protein stability. PLoS Genet 7:e1002135PubMed PubMedCentral CrossRef
  Milne JC, Lambert PD, Schenk S, Carney DP, Smith JJ, Gagne DJ, Jin L, Boss O, Perni RB, Vu CB, Bemis JE, Xie R, Disch JS, Ng PY, Nunes JJ, Lynch AV, Yang H, Galonek H, Israelian K, Choy W, Iffland A, Lavu S, Medvedik O, Sinclair DA, Olefsky JM, Jirousek MR, Elliott PJ, Westphal CH (2007) Small molecule activators of SIRT1 as therapeutics for the treatment of type 2 diabetes. Nature 450:712–716PubMed PubMedCentral CrossRef
  Nicolini G, Rigolio R, Miloso M, Bertelli AA, Tredici G (2001) Anti-apoptotic effect of trans-resveratrol on paclitaxel-induced apoptosis in the human neuroblastoma SH-SY5Y cell line. Neurosci Lett 302:41–44PubMed CrossRef
  Niu XF, Liu BQ, Du ZX, Gao YY, Li C, Li N, Guan Y, Wang HQ (2011) Resveratrol protects leukemic cells against cytotoxicity induced by proteasome inhibitors via induction of FOXO1 and p27Kip1. BMC Cancer 11:99PubMed PubMedCentral CrossRef
  Oberdoerffer P, Michan S, McVay M, Mostoslavsky R, Vann J, Park SK, Hartlerode A, Stegmuller J, Hafner A, Loerch P, Wright SM, Mills KD, Bonni A, Yankner BA, Scully R, Prolla TA, Alt FW, Sinclair DA (2008) SIRT1 redistribution on chromatin promotes genomic stability but alters gene expression during aging. Cell 135:907–918PubMed PubMedCentral CrossRef
  O’Connor PM, Jackman J, Bae I, Myers TG, Fan S, Mutoh M, Scudiero DA, Monks A, Sausville EA, Weinstein JN, Friend S, Fornace AJ Jr, Kohn KW (1997) Characterization of the p53 tumor suppressor pathway in cell lines of the National Cancer Institute anticancer drug screen and correlations with the growth-inhibitory potency of 123 anticancer agents. Cancer Res 57:4285–4300PubMed
  Park SJ, Ahmad F, Philp A, Baar K, Williams T, Luo H, Ke H, Rehmann H, Taussig R, Brown AL, Kim MK, Beaven MA, Burgin AB, Manganiello V, Chung JH (2012) Resveratrol ameliorates aging-related metabolic phenotypes by inhibiting cAMP phosphodiesterases. Cell 148:421–433PubMed PubMedCentral CrossRef
  Patties I, Kortmann RD, Glasow A (2013) Inhibitory effects of epigenetic modulators and differentiation inducers on human medulloblastoma cell lines. J Exp Clin Cancer Res 32:27PubMed PubMedCentral CrossRef
  Rigolio R, Miloso M, Nicolini G, Villa D, Scuteri A, Simone M, Tredici G (2005) Resveratrol interference with the cell cycle protects human neuroblastoma SH-SY5Y cell from paclitaxel-induced apoptosis. Neurochem Int 46:205–211PubMed CrossRef
  Roth M, Chen WY (2014) Sorting out functions of sirtuins in cancer. Oncogene 33:1609–1620PubMed PubMedCentral CrossRef
  Scuto A, Kirschbaum M, Buettner R, Kujawski M, Cermak JM, Atadja P, Jove R (2013) SIRT1 activation enhances HDAC inhibition-mediated upregulation of GADD45G by repressing the binding of NF-kappaB/STAT3 complex to its promoter in malignant lymphoid cells. Cell Death Dis 4:e635PubMed PubMedCentral CrossRef
  Shin DH, Choi YJ, Park JW (2014) SIRT1 and AMPK mediate hypoxia-induced resistance of non-small cell lung cancers to cisplatin and doxorubicin. Cancer Res 74:298–308PubMed CrossRef
  Sinclair DA, Guarente L (2014) Small-molecule allosteric activators of sirtuins. Annu Rev Pharmacol Toxicol 54:363–380PubMed PubMedCentral CrossRef
  Sonnemann J, Marx C, Becker S, Wittig S, Palani CD, Krämer OH, Beck JF (2014) p53-dependent and p53-independent anticancer effects of different histone deacetylase inhibitors. Br J Cancer 110:656–667PubMed PubMedCentral CrossRef
  Sonnemann J, Grauel D, Blümel L, Hentschel J, Marx C, Blumrich A, Focke K, Becker S, Wittig S, Schinkel S, Krämer OH, Beck JF (2015) RETRA exerts anticancer activity in Ewing’s sarcoma cells independent of their TP53 status. Eur J Cancer 51:841–851PubMed CrossRef
  Soto BL, Hank JA, Van De Voort TJ, Subramanian L, Polans AS, Rakhmilevich AL, Yang RK, Seo S, Kim K, Reisfeld RA, Gillies SD, Sondel PM (2011) The anti-tumor effect of resveratrol alone or in combination with immunotherapy in a neuroblastoma model. Cancer Immunol Immunother 60:731–738PubMed PubMedCentral CrossRef
  van Ginkel PR, Sareen D, Subramanian L, Walker Q, Darjatmoko SR, Lindstrom MJ, Kulkarni A, Albert DM, Polans AS (2007) Resveratrol inhibits tumor growth of human neuroblastoma and mediates apoptosis by directly targeting mitochondria. Clin Cancer Res 13:5162–5169PubMed CrossRef
  Vaziri H, Dessain SK, Ng EE, Imai SI, Frye RA, Pandita TK, Guarente L, Weinberg RA (2001) hSIR2(SIRT1) functions as an NAD-dependent p53 deacetylase. Cell 107:149–159PubMed CrossRef
  Villalba JM, Alcain FJ (2012) Sirtuin activators and inhibitors. BioFactors 38:349–359PubMed PubMedCentral CrossRef
  Wang Q, Li H, Wang XW, Wu DC, Chen XY, Liu J (2003) Resveratrol promotes differentiation and induces Fas-independent apoptosis of human medulloblastoma cells. Neurosci Lett 351:83–86PubMed CrossRef
  Wang RH, Zheng Y, Kim HS, Xu X, Cao L, Luhasen T, Lee MH, Xiao C, Vassilopoulos A, Chen W, Gardner K, Man YG, Hung MC, Finkel T, Deng CX (2008) Interplay among BRCA1, SIRT1, and survivin during BRCA1-associated tumorigenesis. Mol Cell 32:11–20PubMed PubMedCentral CrossRef
  Wieder T, Prokop A, Bagci B, Essmann F, Bernicke D, Schulze-Osthoff K, Dorken B, Schmalz HG, Daniel PT, Henze G (2001) Piceatannol, a hydroxylated analog of the chemopreventive agent resveratrol, is a potent inducer of apoptosis in the lymphoma cell line BJAB and in primary, leukemic lymphoblasts. Leukemia 15:1735–1742PubMed CrossRef
  Yaseen A, Chen S, Hock S, Rosato R, Dent P, Dai Y, Grant S (2012) Resveratrol sensitizes acute myelogenous leukemia cells to histone deacetylase inhibitors through reactive oxygen species-mediated activation of the extrinsic apoptotic pathway. Mol Pharmacol 82:1030–1041PubMed PubMedCentral CrossRef
  Yeung F, Hoberg JE, Ramsey CS, Keller MD, Jones DR, Frye RA, Mayo MW (2004) Modulation of NF-kappaB-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J 23:2369–2380PubMed PubMedCentral CrossRef
  
• 作者单位：Jürgen Sonnemann (1) (3)
  Melanie Kahl (1)
  Priyanka M. Siranjeevi (1)
  Annelie Blumrich (1)
  Lisa Blümel (1)
  Sabine Becker (1)
  Susan Wittig (1)
  René Winkler (1)
  Oliver H. Krämer (2)
  James F. Beck (1)
  
  1. Children’s Clinic, Department of Pediatric Hematology and Oncology, Jena University Hospital, Jena, Germany
  3. Klinik für Kinder- und Jugendmedizin, Friedrich-Schiller-Universität Jena, Kochstr. 2, 07745, Jena, Germany
  2. Department of Toxicology, University Medical Center, Obere Zahlbacher Str. 67, 55131, Mainz, Germany
  
• 刊物类别：Medicine
• 刊物主题：Medicine & Public Health
  Oncology
  Cancer Research
  Internal Medicine
  Hematology
  
• 出版者：Springer Berlin / Heidelberg
• ISSN：1432-1335

文摘

Purpose SIRT1-activating compounds (STACs) may have potential in the management of cancer. However, the best-studied STAC, the naturally occurring compound resveratrol, is reported to have contradictory effects in combination chemotherapy regimens: It has been shown both to increase and to decrease the action of anticancer agents. To shed more light on this issue, we comparatively investigated the impact of resveratrol and the synthetic STAC SRT1720 on the responsiveness of Ewing’s sarcoma (ES) cells to the chemotherapeutic drugs etoposide and vincristine.