Emerging Potential Agents against Malignant Pleural Mesothelioma: A Review of in vitro Studies

  • İlknur Porsuk Doru
  • Atiye Seda Yar Sağlam
  • Hacer İlke Önen
Keywords: Malignant pleural mesothelioma, apoptosis, inhibitors, preclinical, in vitro

Abstract

Malignant pleural mesothelioma is a highly aggressive and therapy-resistant tumor with poor prognosis. Approximately 80% of MPM cases worldwide are associated with exposure to asbestos. Incidence of MPM has increased in the world. Most patients survive around 12 months in spite of given treatments. Since about 80% of MPM cases have been diagnosed in stage III/IV, they are no longer suitable for surgical intervention. Moreover, the conventional therapy strategies have failed to extend survival of MPM patients. Although the combination therapy, consisting of cisplatin and pemetrexed, has shown promising prognostic results and became the standard first-line treatment for mesothelioma, it has not yielded satisfactory outcomes regarding overall survival of patients. For these reasons, more effective therapy strategies are still needed. In this review, in vitro research studies that are related to inhibitors administrated on MPM cells are summarized. Results of in vitro studies are important for identification of potential therapeutic agents.

References

Robinson BW, Musk AW, Lake RA. Malignant mesothelioma. Lancet. 2005; 366: 397-408.

Peto J, Decarli A, La Vecchia C, Levi F, Negri E. The European mesothelioma epidemic. Br J Cancer. 1999;79:666-72.

Powers A, Carbone M. The role of environmental carcinogens, viruses and genetic predisposition in the pathogenesis of mesothelioma. Cancer Biol Ther. 2002; 1: 348-53.

Attanoos RL, Churg A, Galateau-Salle F, Gibbs AR, Roggli VL. Malign mesothelioma and its non-asbestos causes. Arch Pathol Lab Med. 2018; 142: 753-760.

Virta RL. Worldwide asbestos supply and consumption trends from 1900 through 2003: US Geological Survey; 2006. 80 p. Circular No: 1298. Available from: URL: https://pubs.usgs.gov/circ/2006/1298/c1298.pdf.

Patel SC, Dowell JE. Modern management of malignant pleural mesothelioma. Lung Cancer (Auckl). 2016 May 3; 7: 63-72.

Delgermaa V, Takahashi K, Park EK, Le GV, Hara T, Sorahan T. Global mesothelioma deaths reported to the World Health Organization between 1994 and 2008. Bull World Health Organ. 2011; 89): 716-24.

Attanoos RL, Gibbs AR. Pathology of malignant mesothelioma. Histopathology. 1997; 30: 403-18.

Favoni RE, Florio T. Combined chemotherapy with cytotoxic and targeted compounds for the management of human malignant pleural mesothelioma. Trends Pharmacol Sci. 2011; 32: 463-79.

Scherpereel A, Astoul P, Baas P, Berghmans T, Clayson H, de Vuyst P, et al. Guidelines of the European Respiratory Society and the European Society of Thoracic Surgeons for the management of malignant pleural mesothelioma. Eur Respir J. 2010; 35: 479-95.

Rini BI. Temsirolimus, an inhibitor of mammalian target of rapamycin. Clin Cancer Res. 2008; 14: 1286-90.

Mikami I, Zhang F, Hirata T, Okamoto J, Koizumi K, Shimizu K, et al. Inhibition of activated phosphatidylinositol 3-kinase/AKT pathway in malignant pleural mesothelioma leads to G1 cell cycle arrest. Oncol Rep. 2010 ; 24: 1677-81.

Hoda MA, Mohamed A, Ghanim B, Filipits M, Hegedus B, Tamura M, et al. Temsirolimus inhibits malignant pleural mesothelioma growth in vitro and in vivo: synergism with chemotherapy. J Thorac Oncol. 2011; 6: 852-63.

Miyoshi S, Hamada H, Hamaguchi N, Kato A, Katayama H, Irifune K, et al. Antitumor activity of MEK and PI3K inhibitors against malignant pleural mesothelioma cells in vitro and in vivo. Int J Oncol. 2012; 41: 449-56.

Pinton G, Manente AG, Murer B, De Marino E, Mutti L, Moro L. PARP1 inhibition affects pleural mesothelioma cell viability and uncouples AKT/mTOR axis via SIRT1. J Cell Mol Med. 2013; 17: 233-41.

Yamaji M, Ota A, Wahiduzzaman M, Karnan S, Hyodo T, Konishi H, et al. Novel ATP‐competitive Akt inhibitor afuresertib suppresses the proliferation of malignant pleural mesothelioma cells. Cancer Med. 2017 ; 6: 2646-59.

Beevers CS, Li F, Liu L, et al. Curcumin inhibits the mammalian target of rapamycin-mediated signaling pathways in cancer cells. Int J Canc 2006; 119: 757–764.

Wang Y, Rishi AK, Wu W, Polin L, Sharma S, Levi E, et al. Curcumin suppresses growth of mesothelioma cells in vitro and in vivo, in part, by stimulating apoptosis. Mol Cell Biochem. 2011; 357: 83-94.

Yamauchi Y, Izumi Y, Asakura K, Hayashi Y, Nomori H. Curcumin induces autophagy in ACC‐MESO‐1 Cells. Phytother Res. 2012; 26: 1779-83.

Onen HI, Yilmaz A, Alp E, Celik A, Demiroz SM, Konac E, et al. EF24 and RAD001 potentiates the anticancer effect of platinum-based agents in human malignant pleural mesothelioma (MSTO-211H) cells and protects nonmalignant mesothelial (MET-5A) cells. Hum Exp Toxicol. 2015; 34: 117-26.

Zhang C, Hao Y, Wu L, Dong X, Jiang N, Cong B, et al. Curcumin induces apoptosis and inhibits angiogenesis in murine malignant mesothelioma. Int J Oncol. 2018; 5: 2531-41.

Cho H, Matsumoto S, Fujita Y, Kuroda A, Menju T, Sonobe M, et al. Trametinib plus 4-methylumbelliferone exhibits antitumor effects by ERK blockade and CD44 downregulation and affects PD-1 and PD-L1 in malignant pleural mesothelioma. J Thorac Oncol. 2017; 12: 477-490.

Hwang JH, Takagi M, Murakami H, Sekido Y, Shin-ya K. Induction of tubulin polymerization and apoptosis in malignant mesothelioma cells by a new compound JBIR-23. Cancer Lett. 2011; 300: 189-96.

Kaku Y, Tsuchiya A, Kanno T, Nakano T, Nishizaki T. Dipalmitoleoyl-phosphatidylethanolamine induces apoptosis of NCI-H28 malignant mesothelioma cells. Anticancer Res. 2014; 34: 1759-64.

Tsuchiya A, Kaku Y, Nakano T, Nishizaki T. Diarachidonoylphosphoethanolamine induces apoptosis of malignant pleural mesothelioma cells through a Trx/ASK1/p38 MAPK pathway. J Pharmacol Sci. 2015; 129: 160-8.

Polkinghorn WR, Tarbell NJ. Medulloblastoma: tumorigenesis, current clinical paradigm, and efforts to improve risk stratification. Nat Clin Pract Oncol. 2007; 4: 295-304.

Shi Y, Moura U, Opitz I, Soltermann A, Rehrauer H, Thies S, et al. Role of hedgehog signaling in malignant pleural mesothelioma. Clin Cancer Res. 2012; 18: 4646-56.

You M, Varona-Santos J, Singh S, Robbins DJ, Savaraj N, Nguyen DM. Targeting of the Hedgehog signal transduction pathway suppresses survival of malignant pleural mesothelioma cells in vitro. J Thorac Cardiovasc Surg. 2014; 147: 508-16.

Birchmeier C, Gherardi E. Developmental roles of HGF/SF and its receptor, the c-Met tyrosine kinase. Trends Cell Biol. 1998; 8: 404-10.

Birchmeier C, Birchmeier W, Gherardi E, Woude GF. Met, metastasis, motility and more. Nat Rev Mol Cell Biol. 2003; 4: 915-25.

Suzuki Y, Sakai K, Ueki J, Xu Q, Nakamura T, Shimada H, et al. Inhibition of Met/HGF receptor and angiogenesis by NK4 leads to suppression of tumor growth and migration in malignant pleural mesothelioma. Int J Cancer. 2010; 127: 1948-57.

Leon LG, Gemelli M, Sciarrillo R, Avan A, Funel N, Giovannetti E. Synergistic activity of the c-Met and tubulin inhibitor tivantinib (ARQ197) with pemetrexed in mesothelioma cells. Curr Drug Targets. 2014; 15: 1331-40.

Kanteti R, Riehm JJ, Dhanasingh I, Lennon FE, Mirzapoiazova T, Mambetsariev B, et al. PI3 kinase pathway and MET inhibition is efficacious in malignant pleural mesothelioma. Sci Rep. 2016; 6: 32992-3004.

Whitson BA, Kratzke RA. Molecular pathways in malignant pleural mesothelioma. Cancer Lett. 2006; 239: 183-9.

Whitson BA, Jacobson BA, Frizelle S, Patel MR, Yee D, Maddaus MA, et al. Effects of insulin-like growth factor-1 receptor inhibition in mesothelioma. Ann Thorac Surg. 2006; 82: 996-1001.

Kai K, D’Costa S, Sills RC, Kim Y. Inhibition of the insulin-like growth factor 1 receptor pathway enhances the antitumor effect of cisplatin in human malignant mesothelioma cell lines. Cancer Lett. 2009; 278: 49-55.

Tsao AS, He D, Saigal B, Liu S, Lee JJ, Bakkannagari S, et al. Inhibition of c-Src expression and activation in malignant pleural mesothelioma tissues leads to apoptosis, cell cycle arrest, and decreased migration and invasion. Mol Cancer Ther. 2007; 6: 1962-72.

Monica V, Iacono ML, Bracco E, Busso S, Di Blasio L, Primo L, et al. Dasatinib modulates sensitivity to pemetrexed in malignant pleural mesothelioma cell lines. Oncotarget. 2016; 7: 76577-89.

Bertino P, Porta C, Barbone D, Germano S, Busacca S, Pinato S, et al. Preliminary data suggestive of a novel translational approach to mesothelioma treatment: imatinib mesylate with gemcitabine or pemetrexed. Thorax. 2007; 62: 690-5.

Katz SI, Zhou L, Chao G, Smith CD, Ferrara T, Wang W, et al. Sorafenib inhibits ERK1/2 and MCL-1L phosphorylation levels resulting in caspase-independent cell death in malignant pleural mesothelioma. Cancer Biol Ther. 2009; 8: 2406-16.

Favoni RE, Pattarozzi A, Casto M, Barbieri F, Gatti M, Paleari L, et al. Gefitinib targets EGFR dimerization and ERK1/2 phosphorylation to inhibit pleural mesothelioma cell proliferation. Curr Cancer Drug Targets. 2010; 10: 176-91.

Pignochino Y, Dell’Aglio C, Inghilleri S, Zorzetto M, Basiricò M, Capozzi F, et al. The combination of sorafenib and everolimus shows antitumor activity in preclinical models of malignant pleural mesothelioma. BMC Cancer. 2015; 15: 374-86.

Pattarozzi A, Carra E, Favoni RE, Würth R, Marubbi D, Filiberti RA, et al. The inhibition of FGF receptor 1 activity mediates sorafenib antiproliferative effects in human malignant pleural mesothelioma tumor-initiating cells. Stem Cell Res Ther. 2017; 8: 119-35.

Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, Walther TC, et al. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science. 2009; 325: 834-40.

Shahbazian MD, Grunstein M. Functions of site-specific histone acetylation and deacetylation. Annu Rev Biochem. 2007; 76: 75-100.

Hurwitz JL, Stasik I, Kerr EM, Holohan C, Redmond KM, McLaughlin KM, et al. Vorinostat/SAHA-induced apoptosis in malignant mesothelioma is FLIP/caspase 8-dependent and HR23B-independent. Eur J Cancer. 2012; 48: 1096-107.

Nguyen DM, Schrump WD, Chen GA, Tsai W, Nguyen P, Trepel JB, et al. Abrogation of p21 expression by flavopiridol enhances depsipeptide-mediated apoptosis in malignant pleural mesothelioma cells. Clin Cancer Res. 2004; 10: 1813-25.

Yamauchi Y, Izumi Y, Asakura K, Fukutomi T, Serizawa A, Kawai K, et al. Lovastatin and valproic acid additively attenuate cell invasion in ACC-MESO-1 cells. Biochem Biophys Res Commun. 2011; 410: 328-32.

Crawford N, Stasik I, Holohan C, Majkut J, McGrath M, Johnston PG, et al. SAHA overcomes FLIP-mediated inhibition of SMAC mimetic-induced apoptosis in mesothelioma. Cell Death Dis. 2013 ; 4: e733.

Gultekin KE, Yurdakonar MK, Yaman E, Yuce US, Yilmaz A, Alp E, et al. Effects of cisplatin and panobinostat on human mesothelial (Met-5A) and malignant pleural mesothelioma (MSTO-211H) cells. Genet Mol Res. 2013; 12: 5405-13.

Gueugnon F, Cartron PF, Charrier C, Bertrand P, Fonteneau JF, Gregoire M, et al. New histone deacetylase inhibitors improve cisplatin antitumor properties against thoracic cancer cells. Oncotarget. 2014; 5: 4504-15.

Stimson L, Rowlands MG, Newbatt YM, Smith NF, Raynaud FI, Rogers P, et al. Isothiazolones as inhibitors of PCAF and p300 histone acetyltransferase ctivity. Mol Cancer Ther 2005; 4: 1521-32.

Onen HI, Yılmaz A, Alp E, Celik A, Demiroz SM, Tastepe AI, et al. Malign plevral mezotelyoma hücre hattında histon asetil transferaz inhibitörü olan anakardik asitin sisplatin cevabını arttırıcı etkisi. Turkiye Klinikleri J Med Sci. 2013; 33: 478-84

Ou WB, Hubert C, Fletcher JA, Corson JM, Bueno R, Flynn DL, et al. Targeted inhibition of multiple receptor tyrosine kinases in mesothelioma. Neoplasia. 2011; 13: 12-22.

Okamoto J, Mikami I, Tominaga Y, Kuchenbecker KM, Lin YC, Bravo DT, et al. Inhibition of Hsp90 leads to cell cycle arrest and apoptosis in human malignant pleural mesothelioma. J Thorac Oncol. 2008; 3: 1089-95.

Gasparini G, Longo R, Sarmiento R, Morabito A. Inhibitors of cyclo-oxygenase 2: a new class of anticancer agents?. Lancet Oncol. 2003; 4: 605-15.

Catalano A, Graciotti L, Rinaldi L, Raffaelli G, Rodilossi S, Betta P, et al. Preclinical evaluation of the nonsteroidal anti‐inflammatory agent celecoxib on malignant mesothelioma chemoprevention. Int J Cancer. 2004 ; 109: 322-8.

O’Kane SL, Eagle GL, Greenman J, Lind MJ, Cawkwell L. COX-2 specific inhibitors enhance the cytotoxic effects of pemetrexed in mesothelioma cell lines. Lung Cancer. 2010 ; 67: 160-5.

Stoppoloni D, Canino C, Cardillo I, Verdina A, Baldi A, Sacchi A, et al. Synergistic effect of gefitinib and rofecoxib in mesothelioma cells. Mol Cancer. 2010 ; 9: 27-36.

Adams J. The development of proteasome inhibitors as anticancer drugs. Cancer cell. 2004; 5: 417-21.

Yuan BZ, Chapman JA, Reynolds SH. Proteasome inhibitor MG132 induces apoptosis and inhibits invasion of human malignant pleural mesothelioma cells. Transl Oncol. 2008; 1: 129-40.

Yang H, Wang Y, Cheryan VT, Wu W, Cui CQ, Polin LA, et al. Withaferin A inhibits the proteasome activity in mesothelioma in vitro and in vivo. PLoS One. 2012; 7: e41214.

Cheriyan VT, Wang Y, Muthu M, Jamal S, Chen D, Yang H, et al. Disulfiram suppresses growth of the malignant pleural mesothelioma cells in part by inducing apoptosis. PLoS One. 2014; 9: e93711.

Cerruti F, Jocollè G, Salio C, Oliva L, Paglietti L, Alessandria B, et al. Proteasome stress sensitizes malignant pleural mesothelioma cells to bortezomib-induced apoptosis. Sci Rep. 2017; 7: 17626-37.

Gordon GJ, Mani M, Maulik G, Mukhopadhyay L, Yeap BY, Kindler HL, et al. Preclinical studies of the proteasome inhibitor bortezomib in malignant pleural mesothelioma. Cancer Chemother Pharmacol. 2008; 61: 549-58.

Wang Y, Rishi AK, Puliyappadamba VT, Sharma S, Yang H, Tarca A, et al. Targeted proteasome inhibition by Velcade induces apoptosis in human mesothelioma and breast cancer cell lines. Cancer Chemother Pharmacol. 2010; 66:455-66.

Yuan BZ, Chapman J, Ding M, Wang J, Jiang B, Rojanasakul Y, et al. TRAIL and proteasome inhibitors combination induces a robust apoptosis in human malignant pleural mesothelioma cells through Mcl-1 and Akt protein cleavages. BMC Cancer. 2013; 13: 140-9.

Yuan X, Li D, Zhao H, Jiang J, Wang P, Ma X, et al. Licochalcone A-induced human bladder cancer T24 cells apoptosis triggered by mitochondria dysfunction and endoplasmic reticulum stress. Biomed Res Int. 2013; 2013: 474272.

Chae JI, Cho JH, Lee K, Choi NJ, Seo KS, Kim SB, et al. Role of transcription factor Sp1 in the quercetin-mediated inhibitory effect on human malignant pleural mesothelioma. Int J Mol Med. 2012; 30: 835-41.

Lee KA, Lee SH, Lee YJ, Baeg SM, Shim JH. Hesperidin induces apoptosis by inhibiting Sp1 and its regulatory protein in MSTO-211H cells. Biomol Ther (Seoul). 2012; 20: 273-9.

Lee K, Lee YJ, Ban JO, Lee YJ, Lee SH, Cho MK, et al. The flavonoid resveratrol suppresses growth of human malignant pleural mesothelioma cells through direct inhibition of specificity protein 1. International journal of molecular medicine. Int J Mol Med. 2012; 30: 21-7.

Kim KH, Yoon G, Cho JJ, Cho JH, Cho YS, Chae JI, et al. Licochalcone A induces apoptosis in malignant pleural mesothelioma through downregulation of Sp1 and subsequent activation of mitochondria-related apoptotic pathway. Int J Oncol. 2015; 46: 1385-92.

Rao M, Atay SM, Shukla V, Hong Y, Upham T, Ripley RT, et al. Mithramycin depletes specificity protein 1 and activates p53 to mediate senescence and apoptosis of malignant pleural mesothelioma cells. Clin Cancer Res. 2016; 22: 1197-210.

Kim KH, Chae JI, Oh H, Cho JH, Lee RH, Yoon G, et al. Manumycin A induces apoptosis in malignant pleural mesothelioma through regulation of Sp1 and activation of the mitochondria-related apoptotic pathway. Oncol Rep. 2016; 36: 117-24.

Belyanskaya LL, Marti TM, Hopkins-Donaldson S, Kurtz S, Felley-Bosco E, Stahel RA. Human agonistic TRAIL receptor antibodies Mapatumumab and Lexatumumab induce apoptosis in malignant mesothelioma and act synergistically with cisplatin. Mol Cancer. 2007; 6: 66.

Urso L, Cavallari I, Silic-Benussi M, Biasini L, Zago G, Calabrese F, et al. Synergistic targeting of malignant pleural mesothelioma cells by MDM2 inhibitors and TRAIL agonists. Oncotarget. 2017; 8: 44232-41.

Hamaguchi N, Hamada H, Miyoshi S, Irifune K, Ito R, Miyazaki T, et al. In vitro and in vivo therapeutic efficacy of the PPAR‐γ agonist troglitazone in combination with cisplatin against malignant pleural mesothelioma cell growth. Cancer Sci. 2010; 101: 1955-64.

Zanellato I, Boidi CD, Lingua G, Betta PG, Orecchia S, Monti E, et al. In vitro anti-mesothelioma activity of cisplatin–gemcitabine combinations: evidence for sequence-dependent effects. Cancer Chemother Pharmacol. 2011; 67: 265-73.

De Luca A, Pellizzari Tregno F, Sau A, Pastore A, Palumbo C, Alama A, et al. Glutathione S‐transferase P 1‐1 as a target for mesothelioma treatment. Cancer Sci. 2013; 104: 223-30.

Hoda MA, Pirker C, Dong Y, Schelch K, Heffeter P, Kryeziu K, et al. Trabectedin is active against malignant pleural mesothelioma cell and xenograft models and synergizes with chemotherapy and Bcl-2 inhibition in vitro. Mol Cancer Ther. 2016; 15: 2357-69.

Pinton G, Manente AG, Daga A, Cilli M, Rinaldi M, Nilsson S, et al. Agonist activation of estrogen receptor beta (ERβ) sensitizes malignant pleural mesothelioma cells to cisplatin cytotoxicity. Mol Cancer. 2014; 13: 227-40.

Published
2019-03-25
Section
Literature Review With Cases