Glucose starvation-mediated inhibition of salinomycin induced autophagy amplifies cancer cell specific cell death

Oncotarget

Volumn 6, Issue 12, 2015, Pages 10134-10145

  Jangamreddy, Jaganmohan R ^a   Jain, Mayur V ^a   Hallbeck, Anna Lotta ^a   Roberg, Karin ^a   Lotfi, Kourosh ^a,b   Łos, Marek J ^a,c  

^a LINKÖPING UNIVERSITY   (Sweden)

^b Department of Clinical Immunology and Transfusion Medicine   (Sweden)

^c POMERANIAN MEDICAL UNIVERSITY   (Poland)

Author keywords

2DG; 2FDG; Glucose starvation; Hypoxia; Normoxia

Indexed keywords

CASPASE; DEOXYGLUCOSE; FLUORODEOXYGLUCOSE; OXAMIC ACID; SALINOMYCIN; GLUCOSE; PYRAN DERIVATIVE;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGY; CANCER CELL; CELL DEATH; CONTROLLED STUDY; CYTOTOXICITY; DRUG MECHANISM; DRUG POTENTIATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IN VITRO STUDY; STARVATION; ANTAGONISTS AND INHIBITORS; CANCER STEM CELL; CELL HYPOXIA; DRUG EFFECTS; DRUG SCREENING; METABOLISM; NEOPLASMS; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

AUTOPHAGY; CELL DEATH; CELL HYPOXIA; CELL LINE, TUMOR; DRUG SCREENING ASSAYS, ANTITUMOR; GLUCOSE; HUMANS; NEOPLASMS; NEOPLASTIC STEM CELLS; PYRANS;

EID: 84929589903     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3548     Document Type: Article

References (42)

1. Koppenol WH, Bounds PL and Dang CV. Otto Warburg's contributions to current concepts of cancer metabolism. Nature reviews Cancer. 2011; 11(5):325-337.
2. Cieslar-Pobuda A, Back M, Magnusson K, Jain MV, Rafat M, Ghavami S, Nilsson KP and Los MJ. Cell type related differences in staining with pentameric thiophene derivatives. Cytometry Part A : the journal of the International Society for Analytical Cytology. 2014; 85(7):628-635.
3. Farahani E, Patra HK, Jangamreddy JR, Rashedi I, Kawalec M, Rao Pariti RK, Batakis P and Wiechec E. Cell adhesion molecules and their relation to (cancer) cell stemness. Carcinogenesis. 2014; 35(4):747-759.
4. Wasik AM, Grabarek J, Pantovic A, Cieslar-Pobuda A, Asgari HR, Bundgaard-Nielsen C, Rafat M, Dixon IM, Ghavami S and Los MJ. Reprogramming and carcinogenesis--parallels and distinctions. International review of cell and molecular biology. 2014; 308:167-203.
5. Gupta PB, Onder TT, Jiang G, Tao K, Kuperwasser C, Weinberg RA and Lander ES. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell. 2009; 138(4):645-659.
6. Antoszczak M and Huczynski A. Anticancer Activity of Polyether Ionophore - Salinomycin. Anti-cancer agents in medicinal chemistry. 2015.
7. Calzolari A, Saulle E, De Angelis ML, Pasquini L, Boe A, Pelacchi F, Ricci-Vitiani L, Baiocchi M and Testa U. Salinomycin potentiates the cytotoxic effects of TRAIL on glioblastoma cell lines. PloS one. 2014; 9(4):e94438.
8. He L, Wang F, Dai WQ, Wu D, Lin CL, Wu SM, Cheng P, Zhang Y, Shen M, Wang CF, Lu J, Zhou YQ, Xu XF, Xu L and Guo CY. Mechanism of action of salinomycin on growth and migration in pancreatic cancer cell lines. Pancreatology : official journal of the International Association of Pancreatology. 2013; 13(1):72-78.
9. Jangamreddy JR, Ghavami S, Grabarek J, Kratz G, Wiechec E, Fredriksson BA, Rao Pariti RK, Cieslar-Pobuda A, Panigrahi S and Los MJ. Salinomycin induces activation of autophagy, mitophagy and affects mitochondrial polarity:differences between primary and cancer cells. Biochimica et biophysica acta. 2013; 1833(9):2057-2069.
10. Larzabal L, El-Nikhely N, Redrado M, Seeger W, Savai R and Calvo A. Differential effects of drugs targeting cancer stem cell (CSC) and non-CSC populations on lung primary tumors and metastasis. PloS one. 2013; 8(11):e79798.
11. Parajuli B, Shin SJ, Kwon SH, Cha SD, Chung R, Park WJ, Lee HG and Cho CH. Salinomycin induces apoptosis via death receptor-5 up-regulation in cisplatin-resistant ovarian cancer cells. Anticancer research. 2013; 33(4):1457-1462.
12. Chaabane W, User SD, El-Gazzah M, Jaksik R, Sajjadi E, Rzeszowska-Wolny J and Los MJ. Autophagy, apoptosis, mitoptosis and necrosis: interdependence between those pathways and effects on cancer. Archivum immunologiae et therapiae experimentalis. 2013; 61(1):43-58.
13. Ghavami S, Shojaei S, Yeganeh B, Ande SR, Jangamreddy JR, Mehrpour M, Christoffersson J, Chaabane W, Moghadam AR, Kashani HH, Hashemi M, Owji AA and Los MJ. Autophagy and apoptosis dysfunction in neurodegenerative disorders. Progress in neurobiology. 2014; 112:24-49.
14. Jangamreddy JR and Los MJ. Mitoptosis, a novel mitochondrial death mechanism leading predominantly to activation of autophagy. Hepatitis monthly. 2012; 12(8):e6159.
15. Story P and Doube A. A case of human poisoning by salinomycin, an agricultural antibiotic. The New Zealand medical journal. 2004; 117(1190):U799.
16. Boehmerle W and Endres M. Salinomycin induces calpain and cytochrome c-mediated neuronal cell death. Cell death & disease. 2011; 2:e168.
17. Boehmerle W, Muenzfeld H, Springer A, Huehnchen P and Endres M. Specific targeting of neurotoxic side effects and pharmacological profile of the novel cancer stem cell drug salinomycin in mice. Journal of molecular medicine. 2014; 92(8):889-900.
18. Oak PS, Kopp F, Thakur C, Ellwart JW, Rapp UR, Ullrich A, Wagner E, Knyazev P and Roidl A. Combinatorial treatment of mammospheres with trastuzumab and salinomycin efficiently targets HER2-positive cancer cells and cancer stem cells. International journal of cancer Journal international du cancer. 2012; 131(12):2808-2819.
19. Zhang Y, Zhang H, Wang X, Wang J, Zhang X and Zhang Q. The eradication of breast cancer and cancer stem cells using octreotide modified paclitaxel active targeting micelles and salinomycin passive targeting micelles. Biomaterials. 2012; 33(2):679-691.
20. Klose J, Stankov MV, Kleine M, Ramackers W, Panayotova-Dimitrova D, Jager MD, Klempnauer J, Winkler M, Bektas H, Behrens GM and Vondran FW. Inhibition of autophagic flux by salinomycin results in anticancer effect in hepatocellular carcinoma cells. PloS one. 2014; 9(5):e95970.
21. Booth L, Roberts JL, Conley A, Cruickshanks N, Ridder T, Grant S, Poklepovic A and Dent P. HDAC inhibitors enhance the lethality of low dose salinomycin in parental and stem-like GBM cells. Cancer biology & therapy. 2014; 15(3):305-316.
22. Parajuli B, Lee HG, Kwon SH, Cha SD, Shin SJ, Lee GH, Bae I and Cho CH. Salinomycin inhibits Akt/NF-kappaB and induces apoptosis in cisplatin resistant ovarian cancer cells. Cancer epidemiology. 2013; 37(4):512-517.
23. Zhang GN, Liang Y, Zhou LJ, Chen SP, Chen G, Zhang TP, Kang T and Zhao YP. Combination of salinomycin and gemcitabine eliminates pancreatic cancer cells. Cancer letters. 2011; 313(2):137-144.
24. La Fleur L, Johansson AC and Roberg K. A CD44high/ EGFRlow subpopulation within head and neck cancer cell lines shows an epithelial-mesenchymal transition phenotype and resistance to treatment. PloS one. 2012; 7(9):e44071.
25. Keats JJ, Chesi M, Egan JB, Garbitt VM, Palmer SE, Braggio E, Van Wier S, Blackburn PR, Baker AS, Dispenzieri A, Kumar S, Rajkumar SV, Carpten JD, Barrett M, Fonseca R, Stewart AK, et al. Clonal competition with alternating dominance in multiple myeloma. Blood. 2012; 120(5):1067-1076.
26. Notta F, Mullighan CG, Wang JC, Poeppl A, Doulatov S, Phillips LA, Ma J, Minden MD, Downing JR and Dick JE. Evolution of human BCR-ABL1 lymphoblastic leukaemiainitiating cells. Nature. 2011; 469(7330):362-367.
27. Raffaghello L, Lee C, Safdie FM, Wei M, Madia F, Bianchi G and Longo VD. Starvation-dependent differential stress resistance protects normal but not cancer cells against highdose chemotherapy. Proceedings of the National Academy of Sciences of the United States of America. 2008; 105(24):8215-8220.
28. Lee C, Safdie FM, Raffaghello L, Wei M, Madia F, Parrella E, Hwang D, Cohen P, Bianchi G and Longo VD. Reduced levels of IGF-I mediate differential protection of normal and cancer cells in response to fasting and improve chemotherapeutic index. Cancer research. 2010; 70(4):1564-1572.
29. Michelakis ED, Sutendra G, Dromparis P, Webster L, Haromy A, Niven E, Maguire C, Gammer TL, Mackey JR, Fulton D, Abdulkarim B, McMurtry MS and Petruk KC. Metabolic modulation of glioblastoma with dichloroacetate. Science translational medicine. 2010; 2(31):31ra34.
30. Sutendra G, Dromparis P, Kinnaird A, Stenson TH, Haromy A, Parker JM, McMurtry MS and Michelakis ED. Mitochondrial activation by inhibition of PDKII suppresses HIF1a signaling and angiogenesis in cancer. Oncogene. 2013; 32(13):1638-1650.
31. Mitani M, Yamanishi T, Miyazaki Y and Otake N. Salinomycin effects on mitochondrial ion translocation and respiration. Antimicrobial agents and chemotherapy. 1976; 9(4):655-660.
32. Bissinger R, Malik A, Jilani K and Lang F. Triggering of Erythrocyte Cell Membrane Scrambling by Salinomycin. Basic & clinical pharmacology & toxicology. 2014; 115(5):396-402.
33. Zhu LQ, Zhen YF, Zhang Y, Guo ZX, Dai J and Wang XD. Salinomycin activates AMP-activated protein kinasedependent autophagy in cultured osteoblastoma cells: a negative regulator against cell apoptosis. PloS one. 2013; 8(12):e84175.
34. Cheong JH, Park ES, Liang J, Dennison JB, Tsavachidou D, Nguyen-Charles C, Wa Cheng K, Hall H, Zhang D, Lu Y, Ravoori M, Kundra V, Ajani J, Lee JS, Ki Hong W and Mills GB. Dual inhibition of tumor energy pathway by 2-deoxyglucose and metformin is effective against a broad spectrum of preclinical cancer models. Molecular cancer therapeutics. 2011; 10(12):2350-2362.
35. Verdoodt B, Vogt M, Schmitz I, Liffers ST, Tannapfel A and Mirmohammadsadegh A. Salinomycin induces autophagy in colon and breast cancer cells with concomitant generation of reactive oxygen species. PloS one. 2012; 7(9):e44132.
36. Chaabane W, Cieslar-Pobuda A, El-Gazzah M, Jain MV, Rzeszowska-Wolny J, Rafat M, Stetefeld J, Ghavami S and Los MJ. Human-gyrovirus-Apoptin triggers mitochondrial death pathway--Nur77 is required for apoptosis triggering. Neoplasia (New York, NY). 2014; 16(9):679-693.
37. Jangamreddy JR, Panigrahi S, Lotfi K, Yadav M, Maddika S, Tripathi AK, Sanyal S and Los MJ. Mapping of apoptininteraction with BCR-ABL1, and development of apoptinbased targeted therapy. Oncotarget. 2014; 5(16):7198-7211.
38. Rollano Penaloza OM, Lewandowska M, Stetefeld J, Ossysek K, Madej M, Bereta J, Sobczak M, Shojaei S, Ghavami S and Los MJ. Apoptins: selective anticancer agents. Trends in molecular medicine. 2014; 20(9):519-528.
39. Roberg K, Ceder R, Farnebo L, Norberg-Spaak L and Grafstrom RC. Multiple genotypic aberrances associate to terminal differentiation-deficiency of an oral squamous cell carcinoma in serum-free culture. Differentiation; research in biological diversity. 2008; 76(8):868-880.
40. Lotfi K, Mansson E, Spasokoukotskaja T, Pettersson B, Liliemark J, Peterson C, Eriksson S and Albertioni F. Biochemical pharmacology and resistance to 2-chloro-2'- arabino-fluoro-2'-deoxyadenosine, a novel analogue of cladribine in human leukemic cells. Clinical cancer research : an official journal of the American Association for Cancer Research. 1999; 5(9):2438-2444.
41. Bedner E, Smolewski P, Amstad P and Darzynkiewicz Z. Activation of caspases measured in situ by binding of fluorochrome-labeled inhibitors of caspases (FLICA):correlation with DNA fragmentation. Experimental cell research. 2000; 259(1):308-313.
42. Jangamreddy JR, Panigrahi S and Los MJ. Monitoring of autophagy is complicated-salinomycin as an example. Biochimica et biophysica acta. 2015; 1853(3):604-610.