Marine alkaloid Monanchocidin a overcomes drug resistance by induction of autophagy and lysosomal membrane permeabilization

Oncotarget

Volumn 6, Issue 19, 2015, Pages 17328-17341

  Dyshlovoy, Sergey A ^a,b,c   Hauschild, Jessica ^a   Amann, Kerstin ^d   Tabakmakher, Ksenia M ^b   Venz, Simone ^e   Walther, Reinhard ^e   Guzii, Alla G ^b   Makarieva, Tatiana N ^b   Shubina, Larisa K ^b   Fedorov, Sergey N ^b   Stonik, Valentin A ^b   Bokemeyer, Carsten ^a   Balabanov, Stefan ^a,f   Honecker, Friedemann ^a,g   Amsberg, Gunhild V ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b PACIFIC INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^c FAR EASTERN FEDERAL UNIVERSITY   (Russian Federation)

^d UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^e UNIVERSITY OF GREIFSWALD   (Germany)

^f UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^g Tumor Center ZeTuP   (Switzerland)

Author keywords

Autophagy; Cisplatin resistance; Germ cell tumor cells; Lysosomal membrane permeabilization; Monanchocidin A

Indexed keywords

3 METHYLADENINE; ALPHA TUBULIN; ANISOMYCIN; ANTINEOPLASTIC ALKALOID; BETA ACTIN; CASPASE 3; CATHEPSIN B; CELL PROTEIN; CISPLATIN; DOCETAXEL; LC3B II PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; MONANCHOCIDIN A; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; GUANIDINE; MONANCHOCIDIN;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGY; CANCER CELL LINE; CELL CYCLE PROGRESSION; CELL PERMEABILIZATION; CELL STRUCTURE; CONTROLLED STUDY; DNA FRAGMENTATION; DOSE RESPONSE; DRUG CYTOTOXICITY; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENTIATION; DRUG RESISTANCE; DRUG SENSITIVITY; DRUG STRUCTURE; EMBRYO; ENZYME ACTIVATION; G1 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; IC50; LYSOSOME MEMBRANE; MALE; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; S PHASE CELL CYCLE CHECKPOINT; UPREGULATION; ANALOGS AND DERIVATIVES; CELL CYCLE; CELL MEMBRANE PERMEABILITY; DRUG EFFECTS; FLOW CYTOMETRY; INTRACELLULAR MEMBRANE; LYSOSOME; MASS SPECTROMETRY; PATHOLOGY; TRANSMISSION ELECTRON MICROSCOPY; TUMOR CELL LINE; UROGENITAL TRACT TUMOR; WESTERN BLOTTING;

ANTINEOPLASTIC AGENTS; APOPTOSIS; AUTOPHAGY; BLOTTING, WESTERN; CELL CYCLE; CELL LINE, TUMOR; CELL MEMBRANE PERMEABILITY; DRUG RESISTANCE, NEOPLASM; FLOW CYTOMETRY; GUANIDINE; HUMANS; INTRACELLULAR MEMBRANES; LYSOSOMES; MASS SPECTROMETRY; MICROSCOPY, ELECTRON, TRANSMISSION; UROGENITAL NEOPLASMS;

EID: 84938284083     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.4175     Document Type: Article

References (47)

1. Koster R, van Vugt MA, Timmer-Bosscha H, Gietema JA and de Jong S. Unravelling mechanisms of cisplatin sensitivity and resistance in testicular cancer. Expert Rev Mol Med. 2013; 15:e12.
2. Beyer J, Albers P, Altena R, Aparicio J, Bokemeyer C, Busch J, Cathomas R, Cavallin-Stahl E, Clarke NW, Classen J, Cohn-Cedermark G, Dahl AA, Daugaard G, De Giorgi U, De Santis M, De Wit M, et al. Maintaining success, reducing treatment burden, focusing on survivorship: highlights from the third European consensus conference on diagnosis and treatment of germ-cell cancer. Ann Oncol. 2013; 24:878-888.
3. Boublikova L, Buchler T, Stary J, Abrahamova J and Trka J. Molecular biology of testicular germ cell tumors: unique features awaiting clinical application. Crit Rev Oncol Hematol. 2014; 89:366-385.
4. Jacobsen C and Honecker F. Cisplatin resistance in germ cell tumours: models and mechanisms. Andrology. 2015; 3:111-121.
5. Yamanaka K, Rocchi P, Miyake H, Fazli L, So A, Zangemeister-Wittke U and Gleave ME. Induction of apoptosis and enhancement of chemosensitivity in human prostate cancer LNCaP cells using bispecific antisense oligonucleotide targeting Bcl-2 and Bcl-xL genes. BJU Int. 2006; 97:1300-1308.
6. Antonarakis ES, Lu C, Wang H, Luber B, Nakazawa M, Roeser JC, Chen Y, Mohammad TA, Fedor HL, Lotan TL, Zheng Q, De Marzo AM, Isaacs JT, Isaacs WB, Nadal R, Paller CJ, et al. AR-V7 and resistance to enzalutamide and abiraterone in prostate cancer. N Engl J Med. 2014; 371:1028-1038.
7. Antonarakis ES and Armstrong AJ. Evolving standards in the treatment of docetaxel-refractory castration-resistant prostate cancer. Prostate Cancer Prostatic Dis. 2011; 14:192-205.
8. Sun S, Sprenger CC, Vessella RL, Haugk K, Soriano K, Mostaghel EA, Page ST, Coleman IM, Nguyen HM, Sun H, Nelson PS and Plymate SR. Castration resistance in human prostate cancer is conferred by a frequently occurring androgen receptor splice variant. J Clin Invest. 2010; 120:2715-2730.
9. Bellmunt J, von der Maase H, Mead GM, Skoneczna I, De Santis M, Daugaard G, Boehle A, Chevreau C, Paz-Ares L, Laufman LR, Winquist E, Raghavan D, Marreaud S, Collette S, Sylvester R and de Wit R. Randomized phase III study comparing paclitaxel/cisplatin/gemcitabine and gemcitabine/cisplatin in patients with locally advanced or metastatic urothelial cancer without prior systemic therapy: EORTC Intergroup Study 30987. J Clin Oncol. 2012; 30:1107-1113.
10. Molinski TF, Dalisay DS, Lievens SL and Saludes JP. Drug development from marine natural products. Nat Rev Drug Discov. 2009; 8:69-85.
11. Newman DJ and Cragg GM. Marine-sourced anti-cancer and cancer pain control agents in clinical and late preclinical development. Mar Drugs. 2014; 12:255-278.
12. Stonik V. Marine natural products: A way to new drugs. Acta Naturae. 2009; 2:15-25.
13. Newman DJ and Cragg GM. Marine natural products and related compounds in clinical and advanced preclinical trials. J Nat Prod. 2004; 67:1216-1238.
14. Galmarini CM, D'Incalci M and Allavena P. Trabectedin and plitidepsin: drugs from the sea that strike the tumor microenvironment. Mar Drugs. 2014; 12:719-733.
15. Guzii AG, Makarieva TN, Denisenko VA, Dmitrenok PS, Kuzmich AS, Dyshlovoy SA, Krasokhin VB and Stonik VA. Monanchocidin: A new apoptosis-inducing polycyclic guanidine alkaloid from the marine sponge Monanchora pulchra. Org Lett. 2010; 12:4292-4295.
16. Oechsle K, Honecker F, Cheng T, Mayer F, Czaykowski P, Winquist E, Wood L, Fenner M, Glaesener S, Hartmann JT, Chi K, Bokemeyer C and Kollmannsberger C. Preclinical and clinical activity of sunitinib in patients with cisplatin-refractory or multiply relapsed germ cell tumors: a Canadian Urologic Oncology Group/German Testicular Cancer Study Group cooperative study. Ann Oncol. 2011; 22:2654-2660.
17. Port M, Glaesener S, Ruf C, Riecke A, Bokemeyer C, Meineke V, Honecker F and Abend M. Micro-RNA expression in cisplatin resistant germ cell tumor cell lines. Mol Cancer. 2011; 10.
18. Schweyer S, Soruri A, Meschter O, Heintze A, Zschunke F, Miosge N, Thelen P, Schlott T, Radzun HJ and Fayyazi A. Cisplatin-induced apoptosis in human malignant testicular germ cell lines depends on MEK/ERK activation. Br J Cancer. 2004; 91:589-598.
19. Chou T-C. Drug Combination Studies and Their Synergy Quantification Using the Chou-Talalay Method. Cancer Res. 2010; 70:440-446.
20. Chou TC and Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Advances in Enzyme Regulation. 1984; 22:27-55.
21. Lang T, Schaeffeler E, Bernreuther D, Bredschneider M, Wolf DH and Thumm M. Aut2p and Aut7p, two novel microtubule-associated proteins are essential for delivery of autophagic vesicles to the vacuole. EMBO J. 1998; 17:3597-3607.
22. Tanida I, Ueno T and Kominami E. LC3 and Autophagy. Methods Mol Biol. 2008; 445:77-88.
23. Erdal H, Berndtsson M, Castro J, Brunk U, Shoshan MC and Linder S. Induction of lysosomal membrane permeabilization by compounds that activate p53-independent apoptosis. Proc Natl Acad Sci U S A. 2005; 102:192-197.
24. Canonico PG and Bird JWC. The use of acridine orange as a lysosomal marker in rat skeletal muscle. The Journal of Cell Biology. 1969; 43:367-371.
25. Boya P and Kroemer G. Lysosomal membrane permeabilization in cell death. Oncogene. 2008; 27:6434-6451.
26. Geng Y, Kohli L, Klocke BJ and Roth KA. Chloroquine-induced autophagic vacuole accumulation and cell death in glioma cells is p53 independent. Neuro Oncol. 2010; 12(5):473-481.
27. Seglen PO and Bohley P. Autophagy and other vacuolar protein degradation mechanisms. Experientia. 1992; 48:158-172.
28. Yang ZJ, Chee CE, Huang S and Sinicrope FA. The Role of Autophagy in Cancer: Therapeutic Implications. Mol Cancer Ther. 2011; 10:1533-1541.
29. Mizushima N. Methods for monitoring autophagy. Int J Biochem Cell Biol. 2004; 36:2491-2502.
30. Mathew R, Karantza-Wadsworth V and White E. Role of autophagy in cancer. Nature reviews Cancer. 2007; 7:961-967.
31. Gewirtz DA. The four faces of autophagy: implications for cancer therapy. Cancer Res. 2014; 74:647-651.
32. Hippert MM, O'Toole PS and Thorburn A. Autophagy in cancer: good, bad, or both? Cancer Res. 2006; 66:9349-9351.
33. Kung H-J, Changou C, Nguyen HG, Yang JC, Evans CP, Bold RJ and Chuang F. (2013). Autophagy and Prostate Cancer Therapeutics. In: Tindal DJ, ed. Prostate cancer: Springer), pp. 497-518.
34. Seglen PO and Gordon PB. 3-Methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc Natl Acad Sci U S A. 1982; 79:1889-1892.
35. Johansson AC, Appelqvist H, Nilsson C, Kagedal K, Roberg K and Ollinger K. Regulation of apoptosis-associated lysosomal membrane permeabilization. Apoptosis. 2010; 15:527-540.
36. Leist M and Jaattela M. Triggering of apoptosis by cathepsins. Cell Death Differ. 2001; 8:324-326.
37. Kroemer G and Jaattela M. Lysosomes and autophagy in cell death control. Nat Rev Cancer. 2005; 5:886-897.
38. Schotte P, Declercq W, Van Huffel S, Vandenabeele P and Beyaert R. Non-specific effects of methyl ketone peptide inhibitors of caspases. Febs Lett. 1999; 442:117-121.
39. Farrow JM, Yang JC and Evans CP. Autophagy as a modulator and target in prostate cancer. Nat Rev Urol. 2014; 11:508-516.
40. Siddik ZH. Cisplatin: mode of cytotoxic action and molecular basis of resistance. Oncogene. 2003; 22:7265-7279.
41. Tamaki H, Harashima N, Hiraki M, Arichi N, Nishimura N, Shiina H, Naora K and Harada M. Bcl-2 family inhibition sensitizes human prostate cancer cells to docetaxel and promotes unexpected apoptosis under caspase-9 inhibition. Oncotarget. 2014; 5:11399-11412.
42. Liu C, Zhu Y, Lou W, Nadiminty N, Chen X, Zhou Q, Shi XB, deVere White RW and Gao AC. Functional p53 determines docetaxel sensitivity in prostate cancer cells. Prostate. 2013; 73:418-427.
43. Dyshlovoy SA, Venz S, Shubina LK, Fedorov SN, Walther R, Jacobsen C, Stonik VA, Bokemeyer C, Balabanov S and Honecker F. Activity of aaptamine and two derivatives, demethyloxyaaptamine and isoaaptamine, in cisplatin-resistant germ cell cancer. J Proteomics. 2014; 96:223-239.
44. Dyshlovoy SA, Fedorov SN, Kalinovsky AI, Shubina LK, Bokemeyer C, Stonik VA and Honecker F. Mycalamide A shows cytotoxic properties and prevents EGF-induced neoplastic transformation through inhibition of nuclear factors. Mar Drugs. 2012; 10:1212-1224.
45. Dyshlovoy SA, Naeth I, Venz S, Preukschas M, Sievert H, Jacobsen C, Shubina LK, Gesell Salazar M, Scharf C, Walther R, Krepstakies M, Priyadarshini P, Hauber J, Fedorov SN, Bokemeyer C, Stonik VA, et al. Proteomic profiling of germ cell cancer cells treated with aaptamine, a marine alkaloid with antiproliferative activity. J Proteome Res. 2012; 11:2316-2330.
46. Sievert H, Venz S, Platas-Barradas O, Dhople VM, Schaletzky M, Nagel CH, Braig M, Preukschas M, Pallmann N, Bokemeyer C, Brummendorf TH, Portner R, Walther R, Duncan KE, Hauber J and Balabanov S. Protein-protein-interaction network organization of the hypusine modification system. Mol Cell Proteomics. 2012; 11:1289-1305.
47. Pelageev DN, Dyshlovoy SA, Pokhilo ND, Denisenko VA, Borisova KL, Keller-von Amsberg G, Bokemeyer C, Fedorov SN, Honecker F and Anufriev VP. Quinone-carbohydrate nonglucoside conjugates as a new type of cytotoxic agents: synthesis and determination of in vitro activity. Eur J Med Chem. 2014; 77:139-144.