Inhibition of autophagic flux by salinomycin results in anti-cancer effect in hepatocellular carcinoma cells

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Klose, Johannes ^a,b   Stankov, Metodi V ^b   Kleine, Moritz ^b   Ramackers, Wolf ^b   Panayotova Dimitrova, Diana ^c   Jäger, Mark D ^b   Klempnauer, Jürgen ^b   Winkler, Michael ^b   Bektas, Hüseyin ^b   Behrens, Georg M N ^b,d   Vondran, Florian W R ^b,d  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d Center for Experimental and Clinical Infection Research   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

REACTIVE OXYGEN METABOLITE; SALINOMYCIN; ANTINEOPLASTIC AGENT; ATG7 PROTEIN, HUMAN; COCCIDIOSTATIC AGENT; GREEN FLUORESCENT PROTEIN; LIGHT CHAIN 3, HUMAN; MICROTUBULE ASSOCIATED PROTEIN; PYRAN DERIVATIVE; UBIQUITIN PROTEIN LIGASE;

ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL VIABILITY; CONTROLLED STUDY; DRUG SELECTIVITY; FLOW CYTOMETRY; HEPATOCELLULAR CARCINOMA CELL LINE; HEPG2 CELL LINE; HUMAN; HUMAN CELL; LIVER CELL; MITOCHONDRION; WESTERN BLOTTING; CELL CULTURE; CELL PROLIFERATION; CELL SURVIVAL; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; GENETICS; LIVER CELL CARCINOMA; LIVER TUMOR; METABOLISM; PATHOLOGY; RNA INTERFERENCE; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; AUTOPHAGY; BLOTTING, WESTERN; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; COCCIDIOSTATS; DOSE-RESPONSE RELATIONSHIP, DRUG; FLOW CYTOMETRY; GREEN FLUORESCENT PROTEINS; HEP G2 CELLS; HEPATOCYTES; HUMANS; LIVER NEOPLASMS; MICROTUBULE-ASSOCIATED PROTEINS; PYRANS; REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; UBIQUITIN-ACTIVATING ENZYMES;

EID: 84901290161     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0095970     Document Type: Article

References (41)

1. Daugschies A, Gasslein U, Rommel M (1998) Comparative efficacy of anticoccidials under the conditions of commercial broiler production and in battery trials. Vet Parasitol 76: 163-171. (Pubitemid 28218714)
2. Callaway TR, Edrington TS, Rychlik JL, Genovese KJ, Poole TL, et al (2003) Ionophores: their use as ruminant growth promotants and impact on food safety. Curr Issues Intest Microbiol 4: 43-51. (Pubitemid 37121567)
3. Lindemann MD, Kornegay ET, Stahly TS, Cromwell GL, Easter RA, et al. (1985) The efficacy of salinomycin as a growth promotant for swine from 9 to 97 kg. J Anim Sci 61: 782-788.
4. Naujokat C, Fuchs D, Opelz G (2010) Salinomycin in cancer: A new mission for an old agent. Mol Med Report 3: 555-559.
5. Gupta PB, Onder TT, Jiang G, Tao K, Kuperwasser C, et al. (2009) Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 138: 645-659.
6. Kim JH, Chae M, Kim WK, Kim YJ, Kang HS, et al. (2011) Salinomycin sensitizes cancer cells to the effects of doxorubicin and etoposide treatment by increasing DNA damage and reducing p21 protein. Br J Pharmacol 162: 773-784.
7. Dong TT, Zhou HM, Wang LL, Feng B, Lv B, et al. (2011) Salinomycin selectively targets 'CD133+' cell subpopulations and decreases malignant traits in colorectal cancer lines. Ann Surg Oncol18: 1797-1804.
8. Fuchs D, Daniel V, Sadeghi M, Opelz G, Naujokat C (2010) Salinomycin overcomes ABC transporter-mediated multidrug and apoptosis resistance in human leukemia stem cell-like KG-1a cells. Biochem Biophys Res Commun 394: 1098-1104.
9. Fuchs D, Heinold A, Opelz G, Daniel V, Naujokat C (2009) Salinomycin induces apoptosis and overcomes apoptosis resistance in human cancer cells. Biochem Biophys Res Commun 390: 743-749.
10. Wang F, He L, Dai WQ, Xu YP, Wu D, et al. (2012) Salinomycin inhibits proliferation and induces apoptosis of human hepatocellular carcinoma cells in vitro and in vivo. PLoS One 7: e50638.
11. Lieke T, Ramackers W, Bergmann S, Klempnauer J, Winkler M, et al. (2012) Impact of Salinomycin on human cholangiocarcinoma: induction of apoptosis and impairment of tumor cell proliferation in vitro. BMC Cancer 12:466.
12. Lu D, Choi MY, Yu J, Castro JE, Kipps TJ, et al. (2011) Salinomycin inhibits Wnt signaling and selectively induces apoptosis in chronic lymphocytic leukemia cells. Proc Natl Acad Sci U S A 108: 13253-13257.
13. Huczynski A (2012) Salinomycin: a new cancer drug candidate. Chem Biol Drug Des 79: 235-238.
14. Yue W, Hamai A, Tonelli G, Bauvy C, Nicolas V, et al. (2013) Inhibition of the autophagic flux by salinomycin in breast cancer stem-like/progenitor cells interferes with their maintenance. Autophagy 9: 714-729.
15. Jangamreddy JR, Ghavami S, Grabarek J, Kratz G, Wiechec E, et al. (2013) Salinomycin induces activation of autophagy, mitophagy and affects mitochondrial polarity: differences between primary and cancer cells. Biochim Biophys Acta 1833: 2057-2069.
16. Li T, Su L, Zhong N, Hao X, Zhong D, et al. (2013) Salinomycin induces cell death with autophagy through activation of endoplasmic reticulum stress in human cancer cells. Autophagy 9:Epub ahead of print.
17. Verdoodt B, Vogt M, Schmitz I, Liffers ST, Tannapfel A, et al. (2012) Salinomycin induces autophagy in colon and breast cancer cells with concomitant generation of reactive oxygen species PLoS One 7: e44132.
18. Vondran FW, Katenz E, Schwartlander R, Morgul MH, Raschzok N, et al. (2008) Isolation of primary human hepatocytes after partial hepatectomy: criteria for identification of the most promising liver specimen. Artif Organs 32: 205-213. (Pubitemid 351326754)
19. Nakabayashi H, Taketa K, Miyano K, Yamane T, Sato J (1982) Growth of human hepatoma cell lines with differentiated functions in chemically defined medium. Cancer Res 42: 3858-63 (Pubitemid 12054507)
20. Stankov MV, Panayotova-Dimitrova D, Leverkus M, Vondran FW, Bauerfeind R, et al. (2012) Autophagy inhibition due to thymidine analogues as novel mechanism leading to hepatocyte dysfunction and lipid accumulation. Aids 26: 1995-2006.
21. Fung C, Lock R, Gao S, Salas E, Debnath J (2008) Induction of autophagy during extracellular matrix detachment promotes cell survival. Mol Biol Cell 1: 797-806. (Pubitemid 351481798)
22. Stankov MV, Panayotova-Dimitrova D, Leverkus M, Schmidt RE, Behrens GM (2013) Thymidine analogues suppress autophagy and adipogenesis in cultured adipocytes. Antimicrob Agents Chemother 57: 543-551.
23. Mizushima N, Yoshimori T, Levine B (2010) Methods in mammalian autophagy research. Cell; 140: 313-326.
24. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, et al. (2008) Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 4: 151-175.
25. Stankov MV, El Khatib M, Thakur BK, Heitmann K, Panayotova-Dimitrova D, et al. (2013) Histone deacetylase inhibitors induce apoptosis in myeloid leukemia by suppressing autophagy. Leukemia; in press.
26. Stankov MV, Lucke T, Das AM, Schmidt RE, Behrens GM (2010) Mitochondrial DNA depletion and respiratory chain activity in primary human subcutaneous adipocytes treated with nucleoside analogue reverse transcriptase inhibitors. Antimicrob Agents Chemother 54: 280-287.
27. Kleine M, Schrem H, Borlak J, Klempnauer J (2008) Clinical versatility of porcine hepatocytes in the light of interspecies differences in cytochrome P450 regulation and expression. Xenotransplantation 15: 208-217.
28. Chan LL, Shen D, Wilkinson AR, Patton W, Lai N, et al (2012) A novel image-based cytometry method for autophagy detection in living cells. Autophagy 8:1371-1382.
29. Nakahira K, Haspel JA, Rathinam VA, Lee SJ, Dolinay T, et al (2011) Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat Immunol 12: 222-230.
30. Zhang Y, Qi H, Taylor R, Xu W, Liu LF, et al. (2007) The role of autophagy in mitochondria maintenance: characterization of mitochondrial functions in autophagy-deficient S. cerevisiae strains. Autophagy 3: 337-346. (Pubitemid 46986338)
31. Kanki T, Klionsky DJ (2010) The molecular mechanism of mitochondria autophagy in yeast Mol Microbiol 75: 795-800.
32. Wallace DC (2005) A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu Rev Genet 39: 359-407.
33. Mathew R, Karantza-Wadsworth V, White E (2007) Role of autophagy in cancer. Nat Rev Cancer 7: 961-967. (Pubitemid 350165856)
34. Altekruse SF, McGlynn KA, Reichman ME (2009) Hepatocellular carcinoma incidence, mortality, and survival trends in the United States from 1975 to 2005. J Clin Oncol 27: 1485-1491.
35. Maluccio M, Covey A (2012) Recent progress in understanding, diagnosing, and treating hepatocellular carcinoma CA Cancer J Clin62: 394-399.
36. Colell A, Ricci JE, Tait S, Milasta S, Maurer U, et al (2007) GAPDH and autophagy preserve survival after apoptotic cytochrome c release in the absence of caspase activation. Cell 129: 983-997. (Pubitemid 46813151)
37. Kim I, Rodriguez-Enriquez S, Lemasters JJ (2007) Selective degradation of mitochondria by mitophagy. Arch Biochem Biophys 46: 245-253. (Pubitemid 46876640)
38. Kosal ME, Anderson DE (2004) An unaddressed issue of agricultural terrorism: a case study on feed security. J Anim Sci 82: 3394-3400. (Pubitemid 39431731)
39. Plumlee KH, Johnson B, Galey FD (1995) Acute salinomycin toxicosis of pigs J Vet Diagn Invest 7:419-420.
40. Story P, Doube A (2004) A case of human poisoning by salinomycin, an agricultural antibiotic. N Z Med J 117: U799.
41. Ketola K, Hilvo M, Hyotylainen T, Vuoristo A, Ruskeepaa AL, et al. (2012) Salinomycin inhibits prostate cancer growth and migration via induction of oxidative stress. Br J Cancer 106: 99-106.