235
Views
8
CrossRef citations to date
0
Altmetric
Original Articles

Romidepsin (FK228) fails in counteracting the transformed phenotype of rhabdomyosarcoma cells but efficiently radiosensitizes, in vitro and in vivo, the alveolar phenotype subtype

, , , , , , , , , , , ORCID Icon, , , , , , , , , & show all
Pages 943-957 | Received 26 Jan 2021, Accepted 05 May 2021, Published online: 04 Jun 2021

References

  • Akervall J, Brun E, Dictor M, Wennerberg J. 2001. Cyclin D1 overexpression versus response to induction chemotherapy in squamous cell carcinoma of the head and neck–preliminary report. Acta Oncol. 40:505–511.
  • Bharathy N, Berlow NE, Wang E, Abraham J, Settelmeyer TP, Hooper JE, Svalina MN, Bajwa Z, Goros MW, Hernandez BS, et al. 2019. Preclinical rationale for entinostat in embryonal rhabdomyosarcoma. Skelet Muscle. 9:12.
  • Bradley A, Kayton ML, Chi YY, Hawkins DS, Tian J, Breneman J, Woldenc SL, Walterhouse D, Rodeberg DA, Donaldson SS. 2019. Treatment approach and outcomes in infants with localized rhabdomyosarcoma: a report from the soft tissue sarcoma committee of the children’s oncology group. Int J Radiat Oncol Biol Phys. 103:19–27.
  • Buglio D, Khaskhely NM, Voo KS, Martinez-Valdez H, Liu YJ, Younes A. 2011. HDAC11 plays an essential role in regulating OX40 ligand expression in Hodgkin lymphoma. Blood. 117(10):2910–2917.
  • Camero S, Camicia L, Marampon F, Ceccarelli S, Shukla R, Mannarino O, Pizer B, Schiavetti A, Pizzuti A, Tombolini V, et al. 2020. BET inhibition therapy counteracts cancer cell survival, clonogenic potential and radioresistance mechanisms in rhabdomyosarcoma cells. Cancer Lett. 479:71–88.
  • Ciccarelli C, Vulcano F, Milazzo L, Gravina GL, Marampon F, Macioce G, Giampaolo A, Tombolini V, Di Paolo V, Hassan HJ, et al. 2016. Key role of MEK/ERK pathway in sustaining tumorigenicity and in vitro radioresistance of embryonal rhabdomyosarcoma stem-like cell population. Mol Cancer. 15:16.
  • Dutta C, Day T, Kopp N, van Bodegom D, Davids MS, Ryan J, Bird L, Kommajosyula N, Weigert O, Yoda A, et al. 2012. BCL2 suppresses PARP1 function and nonapoptotic cell death. Cancer Res. 72:4193–4203.
  • Eberharter A, Becker PB. 2002. Histone acetylation: a switch between repressive and permissive chromatin. Second in review series on chromatin dynamics. EMBO Rep. 3:224–229.
  • El-Naggar AM, Somasekharan SP, Wang Y, Cheng H, Negri GL, Pan M, Wang XQ, Delaidelli A, Rafn B, Cran J, et al. 2019. Class I HDAC inhibitors enhance YB-1 acetylation and oxidative stress to block sarcoma metastasis. EMBO Rep. 20:e48375.
  • Furumai R, Matsuyama A, Kobashi N, Lee KH, Nishiyama M, Nakajima H, Tanaka A, Komatsu Y, Nishino N, Yoshida M, et al. 2002. FK228 (depsipeptide) as a natural prodrug that inhibits class I histone deacetylases. Cancer Res. 62:4916–4921.
  • Gravina GL, Festuccia C, Popov VM, Di Rocco A, Colapietro A, Sanità P, Monache SD, Musio D, De Felice F, Di Cesare E, et al. 2016. c-Myc sustains transformed phenotype and promotes radioresistance of embryonal rhabdomyosarcoma cell lines. Radiat Res. 185:411–422.
  • Gravina GL, Mancini A, Ranieri G, Di Pasquale B, Marampon F, Di Clemente L, Ricevuto E, Festuccia C. 2013. Phenotypic characterization of human prostatic stromal cells in primary cultures derived from human tissue samples. Int J Oncol. 42(6):2116–2122.
  • Gravina GL, Mancini A, Sanita P, Vitale F, Marampon F, Ventura L, Landesman Y, McCauley D, Kauffman M, Shacham S, et al. 2015. KPT-330, a potent and selective exportin-1 (XPO-1) inhibitor, shows antitumor effects modulating the expression of cyclin D1 and survivin in prostate cancer models. BMC Cancer. 15:941.
  • Greider C, Chattopadhyay A, Parkhurst C, Yang E. 2002. BCL-x(L) and BCL2 delay Myc-induced cell cycle entry through elevation of p27 and inhibition of G1 cyclin-dependent kinases. Oncogene. 21:7765–7775.
  • Grobner SN, Worst BC, Weischenfeldt J, Buchhalter I, Kleinheinz K, Rudneva VA, et al. 2018. The landscape of genomic alterations across childhood cancers. Nature. 555:321–327.
  • Groselj B, Sharma NL, Hamdy FC, Kerr M, Kiltie AE. 2013. Histone deacetylase inhibitors as radiosensitisers: effects on DNA damage signalling and repair. Br J Cancer. 108:748–754.
  • Gross A, Katz SG. 2017. Non-apoptotic functions of BCL-2 family proteins. Cell Death Differ. 24:1348–1358.
  • Gryder BE, Wu L, Woldemichael GM, Pomella S, Quinn TR, Park PMC, Cleveland A, Stanton BZ, Song Y, Rota R, et al. 2019. Chemical genomics reveals histone deacetylases are required for core regulatory transcription. Nat Commun. 10:3004.
  • Guha M. 2015. HDAC inhibitors still need a home run, despite recent approval. Nat Rev Drug Discov. 14:225–226.
  • Hedrick E, Crose L, Linardic CM, Safe S. 2015. Histone deacetylase inhibitors inhibit rhabdomyosarcoma by reactive oxygen species-dependent targeting of specificity protein transcription factors. Mol Cancer Ther. 14:2143–2153.
  • Hinson AR, Jones R, Crose LE, Belyea BC, Barr FG, Linardic CM. 2013. Human rhabdomyosarcoma cell lines for rhabdomyosarcoma research: utility and pitfalls. Front Oncol. 3:183.
  • Hochhauser D, Schnieders B, Ercikan-Abali E, Gorlick R, Muise-Helmericks R, Li WW, Fan J, Banerjee D, Bertino JR. 1996. Effect of cyclin D1 overexpression on drug sensitivity in a human fibrosarcoma cell line. J Natl Cancer Inst. 88(18):1269–1275.
  • Hontecillas-Prieto L, Flores-Campos R, Silver A, de Álava E, Hajji N, García-Domínguez DJ. 2020. Synergistic enhancement of cancer therapy using HDAC inhibitors: opportunity for clinical trials. Front Genet. 11:578011.
  • Hydbring P, Malumbres M, Sicinski P. 2016. Non-canonical functions of cell cycle cyclins and cyclin-dependent kinases. Nat Rev Mol Cell Biol. 17(5):280–292.
  • Illert AL, Kawaguchi H, Antinozzi C, Bassermann F, Quintanilla-Martinez L, von Klitzing C, Hiwatari M, Peschel C, de Rooij DG, Morris SW, et al. 2012. Targeted inactivation of nuclear interaction partner of ALK disrupts meiotic prophase. Development. 139(14):2523–2534.
  • Jeyakumar M, Liu XF, Erdjument-Bromage H, Tempst P, Bagchi MK. 2007. Phosphorylation of thyroid hormone receptor-associated nuclear receptor corepressor holocomplex by the DNA-dependent protein kinase enhances its histone deacetylase activity. J Biol Chem. 282(13):9312–9322.
  • Kaushal A, Citrin D. 2008. The role of radiation therapy in the management of sarcomas. Surg Clin North Am. 88:629–viii.
  • Kummar S, Gutierrez M, Doroshow JH, Murgo AJ. 2006. Drug development in oncology: classical cytotoxics and molecularly targeted agents. Br J Clin Pharmacol. 62:15–26.
  • Kurmasheva RT, Bandyopadhyay A, Favours E, Del Pozo V, Ghilu S, Phelps DA, Erickson SW, Peer CJ, Figg WD, Smith MA, et al. 2019. Evaluation of entinostat alone and in combination with standard-of-care cytotoxic agents against rhabdomyosarcoma xenograft models. Pediatr Blood Cancer. 66:e27820.
  • Le TV, Seo Y, Ryu CJ, Lee HR, Park HJ. 2010. Increased expression of p27 is associated with the cisplatin resistance in gastric cancer cell line YCC-3. Arch Pharm Res. 33:1127–1132.
  • Lee JH, Choy ML, Marks PA. 2012. Mechanisms of resistance to histone deacetylase inhibitors. Adv Cancer Res. 116:39–86.
  • Lee S, Rauch J, Kolch W. 2020. Targeting MAPK signaling in cancer: mechanisms of drug resistance and sensitivity. Int J Mol Sci. 21(3):1102.
  • Leslie PL, Chao YL, Tsai YH, Ghosh SK, Porrello A, Van Swearingen AED, Harrison EB, Cooley BC, Parker JS, Carey LA, Pecot CV. 2019. Histone deacetylase 11 inhibition promotes breast cancer metastasis from lymph nodes. Nat Commun. 10:4192.
  • Li Y, Seto E. 2016. HDACs and HDAC inhibitors in cancer development and therapy. Cold Spring Harb Perspect Med. 6(10):a026831.
  • Liu R, Chen Y, Liu G, Li C, Song Y, Cao Z, Li W, Hu J, Lu C, Liu Y. 2020. PI3K/AKT pathway as a key link modulates the multidrug resistance of cancers. Cell Death Dis. 11:797.
  • Lombard DB, Cierpicki T, Grembecka J. 2019. Combined MAPK pathway and HDAC inhibition breaks melanoma. Cancer Discov. 9(4):469–471.
  • Mah LJ, El-Osta A, Karagiannis TC. 2010. GammaH2AX: a sensitive molecular marker of DNA damage and repair. Leukemia. 24:679–686.
  • Marampon F, Codenotti S, Megiorni F, Del Fattore A, Camero S, Gravina GL, Festuccia C, Musio D, De Felice F, Nardone V, et al. 2019. NRF2 orchestrates the redox regulation induced by radiation therapy, sustaining embryonal and alveolar rhabdomyosarcoma cells radioresistance. J Cancer Res Clin Oncol. 145:881–893.
  • Marampon F, Di Nisio V, Pietrantoni I, Petragnano F, Fasciani I, Scicchitano BM, Ciccarelli C, Gravina GL, Festuccia C, Del Fattore A, et al. 2019. Pro-differentiating and radiosensitizing effects of inhibiting HDACs by PXD-101 (Belinostat) in in vitro and in vivo models of human rhabdomyosarcoma cell lines. Cancer Lett. 461:90–101.
  • Megiorni F, Gravina GL, Camero S, Ceccarelli s, Del Fattore A, Desiderio V, Papaccio F, McDowell HP, Shukla R, Pizzuti A, et al. 2017. Pharmacological targeting of the ephrin receptor kinase signalling by GLPG1790 in vitro and in vivo reverts oncophenotype, induces myogenic differentiation and radiosensitizes embryonal rhabdomyosarcoma cells. J Hematol Oncol. 10:161.
  • Menegon S, Columbano A, Giordano S. 2016. The dual roles of NRF2 in cancer. Trends Mol Med. 22:578–593.
  • Mirabella AC, Foster BM, Bartke T. 2016. Chromatin deregulation in disease. Chromosoma. 125:75–93.
  • Mirzayans R, Murray D. 2020. Intratumor heterogeneity and therapy resistance: contributions of dormancy, dpoptosis reversal (anastasis) and cell fusion to disease recurrence. Int J Mol Sci. 21(4):1308.
  • Oesterle EC, Chien WM, Campbell S, Nellimarla P, Fero ML. 2011. p27(Kip1) is required to maintain proliferative quiescence in the adult cochlea and pituitary. Cell Cycle. 10(8):1237–1248.
  • Pacheco M, Nielsen TO. 2012. Histone deacetylase 1 and 2 in mesenchymal tumors. Mod Pathol. 25(2):222–230.
  • Pal A, Chiu HY, Taneja R. 2019. Genetics, epigenetics and redox homeostasis in rhabdomyosarcoma: emerging targets and therapeutics. Redox Biol. 25:101124.
  • Petragnano F, Pietrantoni I, Camero S, Codenotti S, Milazzo L, Vulcano F, Macioce G, Giordani I, Tini P, Cheleschi S, et al. 2020. Clinically relevant radioresistant rhabdomyosarcoma cell lines: functional, molecular and immune-related characterization. J Biomed Sci. 27:90.
  • Petragnano F, Pietrantoni I, Di Nisio V, Fasciani I, Del Fattore A, Capalbo C, Cheleschi S, Tini P, Orelli S, Codenotti S, et al. 2020. Modulating the dose-rate differently affects the responsiveness of human epithelial prostate- and mesenchymal rhabdomyosarcoma-cancer cell line to radiation. Int J Radiat Biol. 96:823–835.
  • Phelps MP, Bailey JN, Vleeshouwer-Neumann T, Chen EY. 2016. CRISPR screen identifies the NCOR/HDAC3 complex as a major suppressor of differentiation in rhabdomyosarcoma. Proc Natl Acad Sci USA. 113(52):15090–15095.
  • Rahmani M, Aust MM, Benson EC, Wallace L, Friedberg J, Grant S. 2014. PI3K/mTOR inhibition markedly potentiates HDAC inhibitor activity in NHL cells through BIM- and MCL-1-dependent mechanisms in vitro and in vivo. Clin Cancer Res. 15(18):4849–4860.
  • Ray Chaudhuri A, Nussenzweig A. 2017. The multifaceted roles of PARP1 in DNA repair and chromatin remodelling. Nat Rev Mol Cell Biol. 18:610–621.
  • Rixe O, Fojo T. 2007. Is cell death a critical end point for anticancer therapies or is cytostasis sufficient? Clin Cancer Res. 13:7280–7287.
  • Robert C, Rassool FV. 2012. HDAC inhibitors: roles of DNA damage and repair. Adv Cancer Res. 116:87–129.
  • Skapek SX, Ferrari A, Gupta AA, Lupo PJ, Butler E, Shipley J, Barr FG, Hawkins DS. 2019. Rhabdomyosarcoma. Nat Rev Dis Primers. 5(1):1.
  • Strzyz P. 2016. Cell signalling: signalling to cell cycle arrest. Nat Rev Mol Cell Biol. 17:536.
  • Tabackman AA, Frankson R, Marsan ES, Perry K, Cole KE. 2016. Structure of ‘linkerless’ hydroxamic acid inhibitor-HDAC8 complex confirms the formation of an isoform-specific subpocket. J Struct Biol. 195(3):373–378.
  • Taylor SC, Berkelman T, Yadav G, Hammond M. 2013. A defined methodology for reliable quantification of Western blot data. Mol Biotechnol. 55:217–226.
  • Toulany M. 2019. Targeting DNA double-strand break repair pathways to improve radiotherapy response. Genes. 10(1):25.
  • van Erp AEM, Versleijen-Jonkers YMH, van der Graaf WTA, Fleuren EDG. 2018. Targeted therapy-based combination treatment in rhabdomyosarcoma. Mol Cancer Ther. 17:1365–1380.
  • Vleeshouwer-Neumann T, Phelps M, Bammler TK, MacDonald JW, Jenkins I, Chen EY. 2015. Histone deacetylase inhibitors antagonize distinct pathways to suppress tumorigenesis of embryonal rhabdomyosarcoma. PLoS One. 10:e0144320.
  • Vulcano F, Milazzo L, Ciccarelli C, Eramo A, Sette G, Mauro A, Macioce G, Martinelli A, La Torre R, Casalbore P, et al. 2016. Wharton’s jelly mesenchymal stromal cells have contrasting effects on proliferation and phenotype of cancer stem cells from different subtypes of lung cancer. Exp Cell Res. 345:190–198.
  • Wang P, Wang Z, Liu J. 2020. Correction to: role of HDACs in normal and malignant hematopoiesis. Mol Cancer. 19:55.
  • Woods GM, Bondra K, Chronowski C, Leasure J, Singh M, Hensley L, Cripe TP, Chakravarti A, Houghton P. 2015. Radiation therapy may increase metastatic potential in alveolar rhabdomyosarcoma. Pediatr Blood Cancer. 62:1550–1554.
  • Xu WS, Parmigiani RB, Marks PA. 2007. Histone deacetylase inhibitors: molecular mechanisms of action. Oncogene. 26(37):5541–5552.
  • Zhang K, Yao Y, Tu Z, Liao C, Wang Z, Qiu Y, Chen D, Hamilton DJ, Li Z, Jiang S. 2020. Discovery of class I histone deacetylase inhibitors based on romidpesin with promising selectivity for cancer cells. Future Med. 12(4):311–323.
  • Zhang J, Zhong Q. 2014. Histone deacetylase inhibitors and cell death. Cell Mol Life Sci. 71:3885–3901.
  • Zhao RP, Yu XL, Zhang Z, Jia LJ, Feng Y, Yang ZZ, Chen XX, Wang J, Ma SL, Guo XM. 2016. The efficacy of postoperative radiotherapy in localized primary soft tissue sarcoma treated with conservative surgery. Radiat Oncol. 11:25.
  • Zhou S, Ye W, Shao Q, Zhang M, Liang J. 2013. Nrf2 is a potential therapeutic target in radioresistance in human cancer. Crit Rev Oncol Hematol. 88:706–715.

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.