Salinomycin induces activation of autophagy, mitophagy and affects mitochondrial polarity: Differences between primary and cancer cells

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 9, 2013, Pages 2057-2069

  Jangamreddy, Jaganmohan Reddy ^a   Ghavami, Saeid ^b   Grabarek, Jerzy ^c   Kratz, Gunnar ^a,d   Wiechec, Emilia ^a   Fredriksson, Bengt Arne ^a   Pariti, Rama Krishna Rao ^a   Cieślar Pobuda, Artur ^a,e   Panigrahi, Soumya ^f   Łos, Marek J ^a,c  

^a LINKÖPING UNIVERSITY   (Sweden)

^b UNIVERSITY OF MANITOBA   (Canada)

^c POMERANIAN MEDICAL UNIVERSITY   (Poland)

^d Department of Plastic Surgery ^*  (Sweden)

^e SILESIAN UNIVERSITY OF TECHNOLOGY   (Poland)

^f LERNER RESEARCH INSTITUTE   (United States)

Author keywords

Cancer stem cells; Mitofusin; Mitophagy; MTOR; PGC1 ; Salinomycin

Indexed keywords

ADENOSINE TRIPHOSPHATE; CASPASE 3; SALINOMYCIN; CHLOROQUINE; ANTIINFECTIVE AGENT; CYTOTOXIN; PYRAN DERIVATIVE;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGY; BREAST CANCER; CANCER CELL; CANCER CELL CULTURE; CELL PROTECTION; CELL SUBPOPULATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; HUMAN; HUMAN CELL; HYPERPOLARIZATION; MALE; MEMBRANE DEPOLARIZATION; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MITOPHAGY; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; SKIN CELL; FIBROBLAST; ANIMAL; BREAST TUMOR; DERMIS; DRUG EFFECT; GENETICS; METABOLISM; MOUSE; MOUSE MUTANT; PATHOLOGY; PROSTATE TUMOR; TUMOR CELL LINE; WNT SIGNALING PATHWAY;

ADENOSINE TRIPHOSPHATE; ANIMALS; ANTI-BACTERIAL AGENTS; AUTOPHAGY; BREAST NEOPLASMS; CELL LINE, TUMOR; CYTOTOXINS; DERMIS; FEMALE; FIBROBLASTS; HUMANS; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, KNOCKOUT; MITOCHONDRIA; MITOCHONDRIAL DEGRADATION; PROSTATIC NEOPLASMS; PYRANS; WNT SIGNALING PATHWAY;

EID: 84882686716     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2013.04.011     Document Type: Article

References (50)

1. P.B. Gupta, T.T. Onder, G. Jiang, K. Tao, C. Kuperwasser, R.A. Weinberg, E.S. Lander, Identification of selective inhibitors of cancer stem cells by high-throughput screening, Cell 138 (2009) 645-659.
2. P.S. Oak, F. Kopp, C. Thakur, J.W. Ellwart, U.R. Rapp, A. Ullrich, E. Wagner, P. Knyazev, A. Roidl, Combinatorial treatment of mammospheres with trastuzumab and salinomycin efficiently targets HER2-positive cancer cells and cancer stem cells, Int. J. Cancer 131 (2012) 2808-2819.
3. Y.Wang, Effects of salinomycin on cancer stemcell in human lung adenocarcinoma A549 cells, Med. Chem. 7 (2011) 106-111.
4. Q.M. Zhi, X.H. Chen, J. Ji, J.N. Zhang, J.F. Li, Q. Cai, B.Y. Liu, Q.L. Gu, Z.G. Zhu, Y.Y. Yu, Salinomycin can effectively kill ALDH(high) stem-like cells on gastric cancer, Biomed. Pharmacother. 65 (2011) 509-515.
5. D. Lu, M.Y. Choi, J. Yu, J.E. Castro, T.J. Kipps, D.A. Carson, Salinomycin inhibits Wnt signaling and selectively induces apoptosis in chronic lymphocytic leukemia cells, Proc. Natl. Acad. Sci. U. S. A. 108 (2011) 13253-13257.
6. A. Huczynski, Salinomycin: a new cancer drug candidate, Chem. Biol. Drug Des. 79 (2012) 235-238.
7. S.M. Alavian, S.R. Ande, K.M. Coombs, B. Yeganeh, P. Davoodpour, M. Hashemi, M. Los, S. Ghavami, Virus-triggered autophagy in viral hepatitis - possible novel strategies for drug development, J. Viral Hepat. 18 (2011) 821-830.
8. W. Chaabane, S.D. User, M. El-Gazzah, R. Jaksik, E. Sajjadi, J. Rzeszowska-Wolny, M.J. Los, Autophagy, apoptosis, mitoptosis and necrosis: interdependence between those pathways and effects on cancer, Arch. Immunol. Ther. Exp. 61 (2013) 43-58.
9. B. Yeganeh, S. Mukherjee, L.M. Moir, K. Kumawat, H.H. Kashani, R.A. Bagchi, H.A. Baarsma, R. Gosens, S. Ghavami, Novel non-canonical TGF-beta signaling networks: emerging roles in airway smooth muscle phenotype and function, Pulm. Pharmacol. Ther. 26 (2012) 50-63.
10. B. Levine, Cell biology: autophagy and cancer, Nature 446 (2007) 745-747.
11. S. Ghavami, B. Yeganeh, G.L. Stelmack, H.H. Kashani, P. Sharma, R. Cunnington, S. Rattan, K. Bathe, T. Klonisch, I.M. Dixon, D.H. Freed, A.J. Halayko, Apoptosis, autophagy and ER stress in mevalonate cascade inhibition-induced cell death of human atrial fibroblasts, Cell Death Dis. 3 (2012) e330.
12. S. Ghavami, R.H. Cunnington, B. Yeganeh, J.J. Davies, S.G. Rattan, K. Bathe, M. Kavosh, M.J. Los, D.H. Freed, T. Klonisch, G.N. Pierce, A.J. Halayko, I.M. Dixon, Autophagy regulates trans fatty acid-mediated apoptosis in primary cardiac myofibroblasts, Biochim. Biophys. Acta 1823 (2012) 2274-2286.
13. Y. Nishida, S. Arakawa, K. Fujitani, H. Yamaguchi, T. Mizuta, T. Kanaseki, M. Komatsu, K. Otsu, Y. Tsujimoto, S. Shimizu, Discovery of Atg5/Atg7-independent alternative macroautophagy, Nature 461 (2009) 654-658.
14. H. Cheong, T. Lindsten, J. Wu, C. Lu, C.B. Thompson, Ammonia-induced autophagy is independent of ULK1/ULK2 kinases, Proc. Natl. Acad. Sci. U. S. A. 108 (2011) 11121-11126.
15. M.V. Jain, A.M. Paczulla, T. Klonisch, F.N. Dimgba, S.B. Rao, K. Roberg, F. Schweizer, C. Lengerke, P. Davoodpour, V.R. Palicharla, S. Maddika, M. Los, Interconnections between apoptotic, autophagic and necrotic pathways: implications for cancer therapy development, J. Cell. Mol. Med. 17 (2013) 12-29.
16. R.J. Youle, A.M. van der Bliek, Mitochondrial fission, fusion, and stress, Science 337 (2012) 1062-1065.
17. G. Benard, M. Karbowski, Mitochondrial fusion and division: regulation and role in cell viability, Semin. Cell Dev. Biol. 20 (2009) 365-374.
18. T. Koshiba, S.A. Detmer, J.T. Kaiser, H. Chen, J.M. McCaffery, D.C. Chan, Structural basis of mitochondrial tethering by mitofusin complexes, Science 305 (2004) 858-862.
19. S. Frank, B. Gaume, E.S. Bergmann-Leitner, W.W. Leitner, E.G. Robert, F. Catez, C.L. Smith, R.J. Youle, The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis, Dev. Cell 1 (2001) 515-525.
20. N. Taguchi, N. Ishihara, A. Jofuku, T. Oka, K. Mihara, Mitotic phosphorylation of dynamin-related GTPase Drp1 participates in mitochondrial fission, J. Biol. Chem. 282 (2007) 11521-11529.
21. H. Chen, S.A. Detmer, A.J. Ewald, E.E. Griffin, S.E. Fraser, D.C. Chan, Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development, J. Cell Biol. 160 (2003) 189-200.
22. J. Rehman, H.J. Zhang, P.T. Toth, Y. Zhang, G. Marsboom, Z. Hong, R. Salgia, A.N. Husain, C. Wietholt, S.L. Archer, Inhibition of mitochondrial fission prevents cell cycle progression in lung cancer, FASEB J. 26 (2012) 2175-2186.
23. M. Los, S. Wesselborg, K. Schulze-Osthoff, The role of caspases in development, immunity, and apoptotic signal transduction: lessons from knockout mice, Immunity 10 (1999) 629-639.
24. D.D. Newmeyer, S. Ferguson-Miller, Mitochondria: releasing power for life and unleashing the machineries of death, Cell 112 (2003) 481-490.
25. J.L. Scarlett, P.W. Sheard, G. Hughes, E.C. Ledgerwood, H.H. Ku, M.P. Murphy, Changes in mitochondrial membrane potential during staurosporine-induced apoptosis in Jurkat cells, FEBS Lett. 475 (2000) 267-272.
26. N.J. Waterhouse, J.C. Goldstein, O. von Ahsen, M. Schuler, D.D. Newmeyer, D.R. Green, Cytochrome c maintains mitochondrial transmembrane potential and ATP generation after outer mitochondrial membrane permeabilization during the apoptotic process, J. Cell Biol. 153 (2001) 319-328.
27. M. Poppe, C. Reimertz, H. Dussmann, A.J. Krohn, C.M. Luetjens, D. Bockelmann, A.L. Nieminen, D. Kogel, J.H. Prehn, Dissipation of potassium and proton gradients inhibits mitochondrial hyperpolarization and cytochrome c release during neural apoptosis, J. Neurosci. 21 (2001) 4551-4563.
28. R.M. Kluck, M.D. Esposti, G. Perkins, C. Renken, T. Kuwana, E. Bossy-Wetzel, M. Goldberg, T. Allen, M.J. Barber, D.R. Green, D.D. Newmeyer, The pro-apoptotic proteins, Bid and Bax, cause a limited permeabilization of the mitochondrial outer membrane that is enhanced by cytosol, J. Cell Biol. 147 (1999) 809-822.
29. S. Ghavami, M.M. Mutawe, P. Sharma, B. Yeganeh, K.D. McNeill, T. Klonisch, H. Unruh, H.H. Kashani, D. Schaafsma, M. Los, A.J. Halayko, Mevalonate cascade regulation of airway mesenchymal cell autophagy and apoptosis: a dual role for p53, PLoS One 6 (2011) e16523.
30. A. Kuma,M. Hatano,M.Matsui, A. Yamamoto, H. Nakaya, T. Yoshimori, Y. Ohsumi, T. Tokuhisa, N.Mizushima, The role of autophagy during the early neonatal starvation period, Nature 432 (2004) 1032-1036.
31. J. Rakar, S. Lonnqvist, P. Sommar, J. Junker, G. Kratz, Interpreted gene expression of human dermal fibroblasts after adipo-, chondro- and osteogenic phenotype shifts, Differentiation 84 (2012) 305-313.
32. S. Liu, D.B. Stolz, P.L. Sappington, C.A. Macias, M.E. Killeen, J.J. Tenhunen, R.L. Delude, M.P. Fink, HMGB1 is secreted by immunostimulated enterocytes and contributes to cytomix-induced hyperpermeability of Caco-2 monolayers, American journal of physiology, Cell Physiol. 290 (2006) C990-C999.
33. M. Mancini, M. Sedghinasab, K. Knowlton, A. Tam, D. Hockenbery, B.O. Anderson, Flow cytometric measurement of mitochondrial mass and function: a novel method for assessing chemoresistance, Ann. Surg. Oncol. 5 (1998) 287-295.
34. J.R. Jangamreddy, M.J. Los, Mitoptosis, a novel mitochondrial death mechanism leading predominantly to activation of autophagy, Hepat. Mon. 12 (2012) e6159.
35. D.W. Hailey, A.S. Rambold, P. Satpute-Krishnan, K.Mitra, R. Sougrat, P.K. Kim, J. Lippincott-Schwartz, Mitochondria supply membranes for autophagosome biogenesis during starvation, Cell 141 (2010) 656-667.
36. P. Icard, H. Lincet, A global view of the biochemical pathways involved in the regulation of themetabolism of cancer cells, Biochim. Biophys. Acta 1826 (2012) 423-433.
37. E. Wirawan, T. Vanden Berghe, S. Lippens, P. Agostinis, P. Vandenabeele, Autophagy: for better or for worse, Cell Res. 22 (2012) 43-61.
38. L.C. Gomes, L. Scorrano, Mitochondrial morphology in mitophagy and macroautophagy, Biochim. Biophys. Acta 1833 (2013) 205-212.
39. M. Mitani, T. Yamanishi, Y.Miyazaki, N. Otake, Salinomycin effects on mitochondrial ion translocation and respiration,Antimicrob. Agents Chemother. 9 (1976) 655-660.
40. J.M. Rodriguez-Vargas, M.J. Ruiz-Magana, C. Ruiz-Ruiz, J. Majuelos-Melguizo, A. Peralta-Leal, M.I. Rodriguez, J.A. Munoz-Gamez, M.R. de Almodovar, E. Siles, A.L. Rivas,M. Jaattela, F.J. Oliver, ROS-induced DNA damage and PARP-1 are required for optimal induction of starvation-induced autophagy, Cell Res. 22 (2012) 1181-1198.
41. S.W. Tait, D.R. Green, Mitochondria and cell signalling, J. Cell Sci. 125 (2012) 807-815.
42. E. Bossy-Wetzel, D.D. Newmeyer, D.R. Green, Mitochondrial cytochrome c release in apoptosis occurs upstream of DEVD-specific caspase activation and independently of mitochondrial transmembrane depolarization, EMBO J. 17 (1998) 37-49.
43. P.F. Li, R. Dietz, R. von Harsdorf, p53 regulates mitochondrial membrane potential through reactive oxygen species and induces cytochrome c-independent apoptosis blocked by Bcl-2, EMBO J. 18 (1999) 6027-6036.
44. E.D. Michelakis, G. Sutendra, P. Dromparis, L. Webster, A. Haromy, E. Niven, C. Maguire, T.L. Gammer, J.R. Mackey, D. Fulton, B. Abdulkarim, M.S. McMurtry, K.C. Petruk, Metabolic modulation of glioblastoma with dichloroacetate, Sci. Transl. Med. 2 (2010) 31ra34.
45. S. Bonnet, S.L. Archer, J. Allalunis-Turner, A. Haromy, C. Beaulieu, R. Thompson, C.T. Lee, G.D. Lopaschuk, L. Puttagunta, S. Bonnet, G. Harry, K. Hashimoto, C.J. Porter, M.A. Andrade, B. Thebaud, E.D. Michelakis, A mitochondria-K+ channel axis is suppressed in cancer and its normalization promotes apoptosis and inhibits cancer growth, Cancer Cell 11 (2007) 37-51.
46. D. Brusa, E.Migliore, S. Garetto,M. Simone, L.Matera, Immunogenicity of 56 degrees C and UVC-treated prostate cancer is associated with release of HSP70 and HMGB1 from necrotic cells, Prostate 69 (2009) 1343-1352.
47. D.G. Craig, P. Lee, E.A. Pryde, G.S. Masterton, P.C. Hayes, K.J. Simpson, Circulating apoptotic and necrotic cell death markers in patients with acute liver injury, Liver Int. 31 (2011) 1127-1136.
48. V.M. Betin, J.D. Lane, Caspase cleavage of Atg4D stimulates GABARAP-L1 processing and triggers mitochondrial targeting and apoptosis, J. Cell Sci. 122 (2009) 2554-2566.
49. M. Djavaheri-Mergny,M.C.Maiuri, G. Kroemer, Cross talk between apoptosis and autophagy by caspase-mediated cleavage of Beclin 1, Oncogene 29 (2010) 1717-1719.
50. P. Vandenabeele, W. Declercq, F. Van Herreweghe, T. Vanden Berghe, The role of the kinases RIP1 and RIP3 in TNF-induced necrosis, Sci. Signal. 3 (2010) re4.