Identification of ML-9 as a lysosomotropic agent targeting autophagy and cell death

Cell Death and Disease

Volumn 5, Issue 4, 2014, Pages

  Kondratskyi, A ^a   Yassine, M ^a   Slomianny, C ^a   Kondratska, K ^a   Gordienko, D ^a,b   Dewailly, E ^a   Lehen'kyi, V ^a   Skryma, R ^a   Prevarskaya, N ^a  

^a Université des Sciences et Technologies de Lille   (France)

^b BOGOMOLETZ INSTITUTE OF PHYSIOLOGY   (Ukraine)

Author keywords

Autophagy; Calcium; Cell death; Lysosomotropic agents; ML 9

Indexed keywords

1 (5 CHLORO 1 NAPHTHALENESULFONYL)HEXAHYDRO 1H 1,4 DIAZEPINE; BAFILOMYCIN A1; DOCETAXEL; IONOMYCIN; MYOSIN LIGHT CHAIN KINASE; MYOSIN LIGHT CHAIN KINASE INHIBITOR; PROTEIN KINASE B; STROMAL INTERACTION MOLECULE 1; THAPSIGARGIN; WORTMANNIN; AZEPINE DERIVATIVE; CALCIUM; MTOR PROTEIN, HUMAN; PHOSPHATIDYLINOSITOL 3 KINASE; TARGET OF RAPAMYCIN KINASE;

ADJUVANT THERAPY; ANTINEOPLASTIC ACTIVITY; APOPTOSIS ASSAY; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CANCER CELL LINE; CANCER CHEMOTHERAPY; CELL DEATH; CELL VIABILITY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTRON MICROSCOPY; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; LYSOSOME; MALE; MONOTHERAPY; PRIORITY JOURNAL; PROSTATE CANCER; WESTERN BLOTTING; BIOLOGICAL MODEL; DOWN REGULATION; DRUG EFFECTS; HOMEOSTASIS; METABOLISM; PATHOLOGY; PH; PHAGOSOME; PROSTATE TUMOR; TUMOR CELL LINE; ULTRASTRUCTURE;

AUTOPHAGY; AZEPINES; CALCIUM; CELL LINE, TUMOR; CLASS III PHOSPHATIDYLINOSITOL 3-KINASES; DOWN-REGULATION; HOMEOSTASIS; HUMANS; HYDROGEN-ION CONCENTRATION; LYSOSOMES; MALE; MODELS, BIOLOGICAL; PHAGOSOMES; PROSTATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS C-AKT; TOR SERINE-THREONINE KINASES;

EID: 84901048224     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2014.156     Document Type: Article

References (52)

1. Courtney KD, Corcoran RB, Engelman JA. The PI3K pathway as drug target in human cancer. J Clin Oncol 2010; 28: 1075-1083.
2. McCubrey JA, Steelman LS, Kempf CR, Chappell WH, Abrams SL, Stivala F et al. Therapeutic resistance resulting from mutations in Raf/MEK/ERK and PI3K/PTEN/Akt/ mTOR signaling pathways. J Cell Physiol 2011; 226: 2762-2781.
3. Cheng CK, Fan QW, Weiss WA. PI3K signaling in glioma-animal models and therapeutic challenges. Brain Pathol 2009; 19: 112-120.
4. Fan QW, Knight ZA, Goldenberg DD, Yu W, Mostov KE, Stokoe D et al. A dual PI3 kinase/ mTOR inhibitor reveals emergent efficacy in glioma. Cancer Cell 2006; 9: 341-349.
5. Klionsky DJ. The molecular machinery of autophagy: unanswered questions. J Cell Sci 2005; 118(Pt 1): 7-18.
6. Ravikumar B, Sarkar S, Davies JE, FutterM, Garcia-ArencibiaM, Green-Thompson ZW et al. Regulation of mammalian autophagy in physiology and pathophysiology. Physiol Rev 2010; 90: 1383-1435.
7. Shen S, Kepp O, Kroemer G. The end of autophagic cell death? Autophagy 2012; 8: 1-3.
8. Choi AM, Ryter SW, Levine B. Autophagy in human health and disease. N Engl J Med 2013; 368: 651-662.
9. Yang S, Wang X, Contino G, Liesa M, Sahin E, Ying H et al. Pancreatic cancers require autophagy for tumor growth. Genes Dev 2011; 25: 717-729.
10. Yang ZJ, Chee CE, Huang S, Sinicrope FA. The role of autophagy in cancer: therapeutic implications. Mol Cancer Ther 2011; 10: 1533-1541.
11. Guo XL, Li D, Hu F, Song JR, Zhang SS, Deng WJ et al. Targeting autophagy potentiates chemotherapy-induced apoptosis and proliferation inhibition in hepatocarcinoma cells. Cancer Lett 2012; 320: 171-179.
12. Selvakumaran M, Amaravadi RK, Vasilevskaya IA, O'Dwyer PJ. Autophagy inhibition sensitizes colon cancer cells to antiangiogenic and cytotoxic therapy. Clin Cancer Res 2013; 19: 2995-3007.
13. White E. Deconvoluting the context-dependent role for autophagy in cancer. Nat Rev Cancer 2012; 12: 401-410.
14. Degtyarev M, De Maziere A, Orr C, Lin J, Lee BB, Tien JY et al. Akt inhibition promotes autophagy and sensitizes PTEN-null tumors to lysosomotropic agents. J Cell Biol 2008; 183: 101-116.
15. Lamoureux F, Thomas C, Crafter C, Kumano M, Zhang F, Davies BR et al. Blocked autophagy using lysosomotropic agents sensitizes resistant prostate tumor cells to the novel Akt inhibitor AZD5363. Clin Cancer Res 2013; 19: 833-844.
16. Lamoureux F, Zoubeidi A. Dual inhibition of autophagy and the AKT pathway in prostate cancer. Autophagy 2013; 9: 1119-1120.
17. Garcia BG, Wei Y, Moron JA, Lin RZ, Javitch JA, Galli A. Akt is essential for insulin modulation of amphetamine-induced human dopamine transporter cell-surface redistribution. Mol Pharmacol 2005; 68: 102-109.
18. Smith U, Carvalho E, Mosialou E, Beguinot F, Formisano P, Rondinone C. PKB inhibition prevents the stimulatory effect of insulin on glucose transport and protein translocation but not the antilipolytic effect in rat adipocytes. Biochem Biophys Res Commun 2000; 268: 315-320.
19. Saitoh M, Ishikawa T, Matsushima S, Naka M, Hidaka H. Selective inhibition of catalytic activity of smooth muscle myosin light chain kinase. J Biol Chem 1987; 262: 7796-7801.
20. Smyth JT, Dehaven WI, Bird GS, Putney JW Jr. Ca2+-store-dependent and -independent reversal of Stim1 localization and function. J Cell Sci 2008; 121(Pt 6): 762-772.
21. Connell LE, Helfman DM. Myosin light chain kinase plays a role in the regulation of epithelial cell survival. J Cell Sci 2006; 119(Pt 11): 2269-2281.
22. Gu LZ, Hu WY, Antic N, Mehta R, Turner JR, de Lanerolle P. Inhibiting myosin light chain kinase retards the growth of mammary and prostate cancer cells. Eur J Cancer 2006; 42: 948-957.
23. Kaneko K, Satoh K, Masamune A, Satoh A, Shimosegawa T. Myosin light chain kinase inhibitors can block invasion and adhesion of human pancreatic cancer cell lines. Pancreas 2002; 24: 34-41.
24. Zhang L, Yu J, Pan H, Hu P, Hao Y, Cai W et al. Small molecule regulators of autophagy identified by an image-based high-throughput screen. Proc Natl Acad Sci USA 2007; 104: 19023-19028.
25. Bitting RL, Armstrong AJ. Targeting the PI3K/Akt/mTOR pathway in castration-resistant prostate cancer. Endocr Relat Cancer 2013; 20: R83-R99.
26. Majumder PK, Sellers WR. Akt-regulated pathways in prostate cancer. Oncogene 2005; 24: 7465-7474.
27. Morgan TM, Koreckij TD, Corey E. Targeted therapy for advanced prostate cancer: inhibition of the PI3K/Akt/mTOR pathway. Curr Cancer Drug Targets 2009; 9: 237-249.
28. Pourmand G, Ziaee AA, Abedi AR, Mehrsai A, Alavi HA, Ahmadi A et al. Role of PTEN gene in progression of prostate cancer. Urol J 2007; 4: 95-100.
29. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012; 8: 445-544.
30. Ouyang DY, Xu LH, He XH, Zhang YT, Zeng LH, Cai JY et al. Autophagy is differentially induced in prostate cancer LNCaP, DU145 and PC-3 cells via distinct splicing profiles of ATG5. Autophagy 2013; 9: 20-32.
31. Bjorkoy G, Lamark T, Brech A, Outzen H, Perander M, Overvatn A et al. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtininduced cell death. J Cell Biol 2005; 171: 603-614.
32. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H et al. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 2007; 282: 24131-24145.
33. Norwood N, Moore TM, Dean DA, Bhattacharjee R, Li M, Stevens T. Store-operated calcium entry and increased endothelial cell permeability. Am J Physiol Lung Cell Mol Physiol 2000; 279: L815-L824.
34. Tran QK, Watanabe H, Le HY, Pan L, Seto M, Takeuchi K et al. Myosin light chain kinase regulates capacitative ca(2+) entry in human monocytes/ macrophages. Arterioscler Thromb Vasc Biol 2001; 21: 509-515.
35. Watanabe H, Takahashi R, Zhang XX, Kakizawa H, Hayashi H, Ohno R. Inhibition of agonist-induced Ca2+ entry in endothelial cells by myosin light-chain kinase inhibitor. Biochem Biophys Res Commun 1996; 225: 777-784.
36. Kaufman RJ. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev 1999; 13: 1211-1233.
37. Ma Y, Hendershot LM. The unfolding tale of the unfolded protein response. Cell 2001; 107: 827-830.
38. Ogata M, Hino S, Saito A, Morikawa K, Kondo S, Kanemoto S et al. Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Biol 2006; 26: 9220-9231.
39. Yorimitsu T, Nair U, Yang Z, Klionsky DJ. Endoplasmic reticulum stress triggers autophagy. J Biol Chem 2006; 281: 30299-30304.
40. Hoyer-Hansen M, Bastholm L, Szyniarowski P, Campanella M, Szabadkai G, Farkas T et al. Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-beta, and Bcl-2. Mol Cell 2007; 25: 193-205.
41. Leitman EM, Tewari A, Horn M, Urbanski M, Damanakis E, Einheber S et al. MLCK regulates Schwann cell cytoskeletal organization, differentiation and myelination. J Cell Sci 2011; 124(Pt 22): 3784-3796.
42. Qin L, Wang Z, Tao L, Wang Y. ER stress negatively regulates AKT/TSC/mTOR pathway to enhance autophagy. Autophagy 2010; 6: 239-247.
43. Decuypere JP, Welkenhuyzen K, Luyten T, Ponsaerts R, Dewaele M, Molgo J et al. Ins(1,4,5)P3 receptor-mediated Ca2+ signaling and autophagy induction are interrelated. Autophagy 2011; 7: 1472-1489.
44. Parys JB, Decuypere JP, Bultynck G. Role of the inositol 1,4,5-trisphosphate receptor/ Ca2+-release channel in autophagy. Cell Commun Signal 2012; 10: 17.
45. Wang SH, Shih YL, Ko WC, Wei YH, Shih CM. Cadmium-induced autophagy and apoptosis are mediated by a calcium signaling pathway. Cell Mol Life Sci 2008; 65: 3640-3652.
46. Avivar-Valderas A, Salas E, Bobrovnikova-Marjon E, Diehl JA, Nagi C, Debnath J et al. PERK integrates autophagy and oxidative stress responses to promote survival during extracellular matrix detachment. Mol Cell Biol 2011; 31: 3616-3629.
47. Verfaillie T, Salazar M, Velasco G, Agostinis P, Linking ER. Stress to autophagy: potential implications for cancer therapy. Int J Cell Biol 2010; 2010: 930509.
48. Ito H, Daido S, Kanzawa T, Kondo S, Kondo Y. Radiation-induced autophagy is associated with LC3 and its inhibition sensitizes malignant glioma cells. Int J Oncol 2005; 26: 1401-1410.
49. Kondo Y, Kanzawa T, Sawaya R, Kondo S. The role of autophagy in cancer development and response to therapy. Nat Rev Cancer 2005; 5: 726-734.
50. Schayowitz A, Sabnis G, Goloubeva O, Njar VC, Brodie AM. Prolonging hormone sensitivity in prostate cancer xenografts through dual inhibition of AR and mTOR. Br J Cancer 2010; 103: 1001-1007.
51. Festuccia C, Gravina GL, Angelucci A, Millimaggi D, Muzi P, Vicentini C et al. Additive antitumor effects of the epidermal growth factor receptor tyrosine kinase inhibitor, gefitinib (Iressa), and the nonsteroidal antiandrogen, bicalutamide (Casodex), in prostate cancer cells in vitro. Int J Cancer 2005; 115: 630-640.
52. Schayowitz A, Sabnis G, Njar VC, Brodie AM. Synergistic effect of a novel antiandrogen, VN/124-1, and signal transduction inhibitors in prostate cancer progression to hormone independence in vitro. Mol Cancer Ther 2008; 7: 121-132.