Evaluation of the potential of a new ribavirin analog impairing the dissemination of ovarian cancer cells
Autoři:
Anaïs Wambecke aff001; Carine Laurent-Issartel aff001; Johanne Leroy-Dudal aff001; Florence Giffard aff002; Fanny Cosson aff003; Nadège Lubin-Germain aff003; Jacques Uziel aff003; Sabrina Kellouche aff001; Franck Carreiras aff001
Působiště autorů:
Equipe de Recherche sur les Relations Matrice Extracellulaire-Cellules, ERRMECe (EA1391), Institut des Matériaux, I-MAT (FD4122), University of Cergy-Pontoise, MIR, rue Descartes, France
aff001; Normandie University, UNICAEN, INSERM U1086 ANTICIPE (Interdisciplinary Research Unit for Cancers Prevention and Treatment, BioTICLA Axis (Biology and Innovative Therapeutics for Ovarian Cancers), Esplanade de la Paix, Caen, France
aff002; Laboratoire de Chimie Biologique, University of Cergy-Pontoise, mail Gay-Lussac, Cergy-pontoise, France
aff003
Vyšlo v časopise:
PLoS ONE 14(12)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0225860
Souhrn
Epithelial ovarian cancers are insidious pathologies that give a poor prognosis due to their late discovery and the increasing emergence of chemoresistance. Development of small pharmacological anticancer molecules remains a major challenge. Ribavirin, usually used in the treatment of hepatitis C virus infections and more recently few cancers, has been a suggestion. However, Ribavirin has many side-effects, suggesting that the synthesis of analogs might be more appropriate.
We have investigated the effect of a Ribavirin analog, SRO-91, on cancer cell behavioral characteristics considered as some of the hallmarks of cancer. Two human ovarian adenocarcinoma cell lines (SKOV3 and IGROV1) and normal cells (mesothelial and fibroblasts) have been used to compare the effects of SRO-91 with those of Ribavirin on cell behavior underlying tumor cell dissemination. SRO-91, like Ribavirin, inhibits proliferation, migration, clonogenicity and spheroids formation of cancer cells. Unlike Ribavirin, SRO-91 is preferentially toxic to cancer compared with normal cells. An in vitro physiologically relevant model showed that SRO-91, like Ribavirin or cisplatin, inhibits cancer cell implantation onto peritoneal mesothelium. In conclusion, SRO-91 analog effects on tumor dissemination and its safety regarding non-cancerous (normal) cells are encouraging findings a promising drug for the treatment of ovarian cancer.
Klíčová slova:
Cell cycle and cell division – Cancer treatment – Apoptosis – Cell staining – DAPI staining – Ovarian cancer – Actins – Cancer cell migration
Zdroje
1. Kipps E, Tan DSP, Kaye SB. Meeting the challenge of ascites in ovarian cancer: new avenues for therapy and research. Nat Rev Cancer. 2013;13(4):273–82. doi: 10.1038/nrc3432 23426401
2. Banerjee S, Kaye SB. New strategies in the treatment of ovarian cancer: current clinical perspectives and future potential. Clin Cancer Res Off J Am Assoc Cancer Res. 2013 Mar 1;19(5):961–8.
3. Auersperg N, Wong AS, Choi KC, Kang SK, Leung PC. Ovarian surface epithelium: biology, endocrinology, and pathology. Endocr Rev. 2001 Apr;22(2):255–88. doi: 10.1210/edrv.22.2.0422 11294827
4. Ozols RF, Bookman MA, Connolly DC, Daly MB, Godwin AK, Schilder RJ, et al. Focus on epithelial ovarian cancer. Cancer Cell. 2004 Jan;5(1):19–24. doi: 10.1016/s1535-6108(04)00002-9 14749123
5. Borden KLB, Culjkovic-Kraljacic B. Ribavirin as an anti-cancer therapy: acute myeloid leukemia and beyond? Leuk Lymphoma. 2010 Oct;51(10):1805–15. doi: 10.3109/10428194.2010.496506 20629523
6. Kai J, Wang Y, Xiong F, Wang S. Genetic and pharmacological inhibition of eIF4E effectively targets esophageal cancer cells and augments 5-FU’s efficacy. J Thorac Dis. 2018 Jul;10(7):3983–91. doi: 10.21037/jtd.2018.06.43 30174840
7. Kökény S, Papp J, Weber G, Vaszkó T, Carmona-Saez P, Oláh E. Ribavirin acts via multiple pathways in inhibition of leukemic cell proliferation. Anticancer Res. 2009 Jun;29(6):1971–80. 19528454
8. Topisirovic I, Ruiz-Gutierrez M, Borden KLB. Phosphorylation of the eukaryotic translation initiation factor eIF4E contributes to its transformation and mRNA transport activities. Cancer Res. 2004 Dec 1;64(23):8639–42. doi: 10.1158/0008-5472.CAN-04-2677 15574771
9. Pettersson F, Yau C, Dobocan MC, Culjkovic-Kraljacic B, Retrouvey H, Retrouvay H, et al. Ribavirin treatment effects on breast cancers overexpressing eIF4E, a biomarker with prognostic specificity for luminal B-type breast cancer. Clin Cancer Res Off J Am Assoc Cancer Res. 2011 May 1;17(9):2874–84.
10. Li W, Shen F, Weber G. Ribavirin and quercetin synergistically downregulate signal transduction and are cytotoxic in human ovarian carcinoma cells. Oncol Res. 1999;11(5):243–7. 10608619
11. Assouline S, Culjkovic-Kraljacic B, Bergeron J, Caplan S, Cocolakis E, Lambert C, et al. A phase I trial of ribavirin and low-dose cytarabine for the treatment of relapsed and refractory acute myeloid leukemia with elevated eIF4E. Haematologica. 2015 Jan;100(1):e7–9.
12. Youcef RA, Dos Santos M, Roussel S, Baltaze J-P, Lubin-Germain N, Uziel J. Huisgen cycloaddition reaction of C-alkynyl ribosides under micellar catalysis: synthesis of ribavirin analogues. J Org Chem. 2009 Jun 5;74(11):4318–23. doi: 10.1021/jo900594x 19438214
13. Solarte C, Santos MD, Gonzalez S, Miranda LSM, Guillot R, Ferry A, et al. Synthesis of C-Ribosyl-1,2,3-triazolyl Carboxamides. Synthesis. 2017 May;49(9):1993–2002.
14. Cosson F, Faroux A, Baltaze J-P, Farjon J, Guillot R, Uziel J, et al. Synthesis of ribavirin 2’-Me-C-nucleoside analogues. Beilstein J Org Chem. 2017;13:755–61. doi: 10.3762/bjoc.13.74 28503210
15. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011 Mar 4;144(5):646–74. doi: 10.1016/j.cell.2011.02.013 21376230
16. Shaw TJ, Senterman MK, Dawson K, Crane CA, Vanderhyden BC. Characterization of intraperitoneal, orthotopic, and metastatic xenograft models of human ovarian cancer. Mol Ther J Am Soc Gene Ther. 2004 Dec;10(6):1032–42.
17. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012 Jun 28;9(7):676–82. doi: 10.1038/nmeth.2019 22743772
18. Carduner L, Leroy-Dudal J, Picot CR, Gallet O, Carreiras F, Kellouche S. Ascites-induced shift along epithelial-mesenchymal spectrum in ovarian cancer cells: enhancement of their invasive behavior partly dependant on αv integrins. Clin Exp Metastasis. 2014 Aug;31(6):675–88. doi: 10.1007/s10585-014-9658-1 24946950
19. Kellouche S, Fernandes J, Leroy-Dudal J, Gallet O, Dutoit S, Poulain L, et al. Initial formation of IGROV1 ovarian cancer multicellular aggregates involves vitronectin. Tumor Biol. 2010 Apr;31(2):129–39.
20. Carduner L, Picot CR, Leroy-Dudal J, Blay L, Kellouche S, Carreiras F. Cell cycle arrest or survival signaling through αv integrins, activation of PKC and ERK1/2 lead to anoikis resistance of ovarian cancer spheroids. Exp Cell Res. 2014 Jan 15;320(2):329–42. doi: 10.1016/j.yexcr.2013.11.011 24291221
21. Heyman L, Kellouche S, Fernandes J, Dutoit S, Poulain L, Carreiras F. Vitronectin and its receptors partly mediate adhesion of ovarian cancer cells to peritoneal mesothelium in vitro. Tumour Biol. 2008;29(4):231–44. doi: 10.1159/000152941 18781095
22. Villedieu M, Briand M, Duval M, Héron JF, Gauduchon P, Poulain L. Anticancer and chemosensitizing effects of 2,3-DCPE in ovarian carcinoma cell lines: link with ERK activation and modulation of p21WAF1/CIP1, Bcl-2 and Bcl-xL expression. Gynecol Oncol. 2007 May;105(2):373–84. doi: 10.1016/j.ygyno.2006.12.019 17276501
23. Xi C, Wang L, Yu J, Ye H, Cao L, Gong Z. Inhibition of eukaryotic translation initiation factor 4E is effective against chemo-resistance in colon and cervical cancer. Biochem Biophys Res Commun. 2018 18;503(4):2286–92. doi: 10.1016/j.bbrc.2018.06.150 29959920
24. Kentsis A, Topisirovic I, Culjkovic B, Shao L, Borden KLB. Ribavirin suppresses eIF4E-mediated oncogenic transformation by physical mimicry of the 7-methyl guanosine mRNA cap. Proc Natl Acad Sci U S A. 2004 Dec 28;101(52):18105–10. doi: 10.1073/pnas.0406927102 15601771
25. Tan K, Culjkovic B, Amri A, Borden KLB. Ribavirin targets eIF4E dependent Akt survival signaling. Biochem Biophys Res Commun. 2008 Oct 24;375(3):341–5. doi: 10.1016/j.bbrc.2008.07.163 18706892
26. Assouline S, Culjkovic B, Cocolakis E, Rousseau C, Beslu N, Amri A, et al. Molecular targeting of the oncogene eIF4E in acute myeloid leukemia (AML): a proof-of-principle clinical trial with ribavirin. Blood. 2009 Jul 9;114(2):257–60. doi: 10.1182/blood-2009-02-205153 19433856
27. Tóvári J, Bocsi J, Ladányi A, Lapis K, Timár J. The antitumor effect of Tiazofurin (TR) consists of anti-proliferative and anti-invasive elements. Anticancer Res. 1996 Dec;16(6A):3307–12. 9042305
28. Zaoui K, Honoré S, Isnardon D, Braguer D, Badache A. Memo-RhoA-mDia1 signaling controls microtubules, the actin network, and adhesion site formation in migrating cells. J Cell Biol. 2008 Nov 3;183(3):401–8. doi: 10.1083/jcb.200805107 18955552
29. Carreiras F, Rigot V, Cruet S, André F, Gauduchon P, Marvaldi J. Migration properties of the human ovarian adenocarcinoma cell line IGROV1: Importance of ?v?3 integrins and vitronectin. Int J Cancer. 1999 Jan 18;80(2):285–94. doi: 10.1002/(sici)1097-0215(19990118)80:2<285::aid-ijc19>3.0.co;2-l 9935212
30. Leroy-Dudal J, Demeilliers C, Gallet O, Pauthe E, Dutoit S, Agniel R, et al. Transmigration of human ovarian adenocarcinoma cells through endothelial extracellular matrix involves alphav integrins and the participation of MMP2. Int J Cancer. 2005 Apr 20;114(4):531–43. doi: 10.1002/ijc.20778 15609323
31. Heyman L, Leroy-Dudal J, Fernandes J, Seyer D, Dutoit S, Carreiras F. Mesothelial vitronectin stimulates migration of ovarian cancer cells. Cell Biol Int. 2010 Apr 1;34(5):493–502. doi: 10.1042/CBI20090331 20121701
32. Pettersson F, Del Rincon SV, Emond A, Huor B, Ngan E, Ng J, et al. Genetic and pharmacologic inhibition of eIF4E reduces breast cancer cell migration, invasion, and metastasis. Cancer Res. 2015 Mar 15;75(6):1102–12. doi: 10.1158/0008-5472.CAN-14-1996 25608710
33. Michaelis M, Michaelis R, Suhan T, Schmidt H, Mohamed A, Doerr HW, et al. Ribavirin inhibits angiogenesis by tetrahydrobiopterin depletion. FASEB J Off Publ Fed Am Soc Exp Biol. 2007 Jan;21(1):81–7.
34. Stoeck M, Miescher S, MacDonald HR, Von Fliedner V. Transforming growth factors beta slow down cell-cycle progression in a murine interleukin-2 dependent T-cell line. J Cell Physiol. 1989 Oct;141(1):65–73. doi: 10.1002/jcp.1041410111 2789227
35. Chao HX, Poovey CE, Privette AA, Grant GD, Chao HY, Cook JG, et al. Orchestration of DNA Damage Checkpoint Dynamics across the Human Cell Cycle. Cell Syst. 2017 22;5(5):445–459.e5. doi: 10.1016/j.cels.2017.09.015 29102360
36. Fidorra J, Mielke T, Booz J, Feinendegen LE. Cellular and nuclear volume of human cells during the cell cycle. Radiat Environ Biophys. 1981;19(3):205–14. doi: 10.1007/bf01324188 7267987
37. Roca-Cusachs P, Alcaraz J, Sunyer R, Samitier J, Farré R, Navajas D. Micropatterning of single endothelial cell shape reveals a tight coupling between nuclear volume in G1 and proliferation. Biophys J. 2008 Jun;94(12):4984–95. doi: 10.1529/biophysj.107.116863 18326659
38. Kochhar DM, Penner JD, Knudsen TB. Embryotoxic, teratogenic, and metabolic effects of ribavirin in mice. Toxicol Appl Pharmacol. 1980 Jan;52(1):99–112. doi: 10.1016/0041-008x(80)90252-5 7361317
39. Thiery JP, Acloque H, Huang RYJ, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell. 2009 Nov 25;139(5):871–90. doi: 10.1016/j.cell.2009.11.007 19945376
40. Ahmed N, Abubaker K, Findlay J, Quinn M. Epithelial mesenchymal transition and cancer stem cell-like phenotypes facilitate chemoresistance in recurrent ovarian cancer. Curr Cancer Drug Targets. 2010 May;10(3):268–78. doi: 10.2174/156800910791190175 20370691
41. Vergara D, Merlot B, Lucot J-P, Collinet P, Vinatier D, Fournier I, et al. Epithelial-mesenchymal transition in ovarian cancer. Cancer Lett. 2010 May 1;291(1):59–66. doi: 10.1016/j.canlet.2009.09.017 19880243
Článok vyšiel v časopise
PLOS One
2019 Číslo 12
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Těžké menstruační krvácení může značit poruchu krevní srážlivosti. Jaký management vyšetření a léčby je v takovém případě vhodný?
- Ne každé mimoděložní těhotenství musí končit salpingektomií
- Masturbační chování žen v ČR − dotazníková studie
Najčítanejšie v tomto čísle
- Methylsulfonylmethane increases osteogenesis and regulates the mineralization of the matrix by transglutaminase 2 in SHED cells
- Oregano powder reduces Streptococcus and increases SCFA concentration in a mixed bacterial culture assay
- Parametric CAD modeling for open source scientific hardware: Comparing OpenSCAD and FreeCAD Python scripts
- The characteristic of patulous eustachian tube patients diagnosed by the JOS diagnostic criteria
Zvýšte si kvalifikáciu online z pohodlia domova
Všetky kurzy