The BH3 mimetic S1 induces autophagy through ER stress and disruption of Bcl-2/Beclin 1 interaction in human glioma U251 cells

Cancer Letters

Volumn 323, Issue 2, 2012, Pages 180-187

  Zhong, Jia teng ^a   Xu, Ye ^a,b   Yi, Hao wei ^a   Su, Jing ^a   Yu, Hui mei ^a   Xiang, Xi yan ^a   Li, Xiao ning ^a   Zhang, Zhi chao ^c   Sun, Lian kun ^a  

^a Basic Medical College   (China)

^b JILIN MEDICAL COLLEGE   (China)

^c DALIAN UNIVERSITY OF TECHNOLOGY   (China)

Author keywords

Autophagy; Bcl 2; BH3 mimetic; ER stress

Indexed keywords

3 METHYLADENINE; BECLIN 1; CHLOROQUINE; GIMERACIL PLUS OTERACIL POTASSIUM PLUS TEGAFUR; PROTEIN BCL 2;

APOPTOSIS; ARTICLE; AUTOPHAGY; CANCER CELL CULTURE; CANCER INHIBITION; CELL STRAIN U251; CELL VIABILITY; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DRUG MECHANISM; ENDOPLASMIC RETICULUM STRESS; GLIOMA CELL; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MITOCHONDRION; NICK END LABELING; PRIORITY JOURNAL; PROTEIN INTERACTION; WESTERN BLOTTING;

APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; BRAIN NEOPLASMS; CELL LINE, TUMOR; ENDOPLASMIC RETICULUM; GLIOMA; HUMANS; IN SITU NICK-END LABELING; MEMBRANE PROTEINS; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; MOLECULAR MIMICRY; PEPTIDE FRAGMENTS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2;

EID: 84863101358     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2012.04.009     Document Type: Article

References (40)

1. Rubinsztein D.C., Gestwicki J.E., Murphy L.O., Klionsky D.J. Potential therapeutic applications of autophagy. Nat. Rev. Drug Discov. 2007, 6(4):304-312.
2. Salazar M., Carracedo A., Salanueva I.J., Hernández-Tiedra S., Lorente M., Egia A., Vázquez P., Blázquez C., Torres S., García S., Nowak J., Fimia G.M., Piacentini M., Cecconi F., Pandolfi P.P., González-Feria L., Iovanna J.L., Guzmán M., Boya P., Velasco G. Cannabinoid action induces autophagy-mediated cell death through stimulation of ER stress in human glioma cells. J. Clin. Invest. 2009, 119(5):1359-1372.
3. Klionsky D.J., Abeliovich H., Agostinis P., Agrawal D.K., Aliev G., Askew D.S., Baba M., Baehrecke E.H., Bahr B.A., Ballabio A., Bamber B.A., Bassham D.C., Bergamini E., Bi X., Biard-Piechaczyk M., Blum J.S., Bredesen D.E., Brodsky J.L., Brumell J.H., Brunk U.T., Bursch W., Camougrand N., Cebollero E., Cecconi F., Chen Y., Chin L.S., Choi A., Chu C.T., Chung J., Clarke P.G., Clark R.S., Clarke S.G., Clavé C., Cleveland J.L., Codogno P., Colombo M.I., Coto-Montes A., Cregg J.M., Cuervo A.M., Debnath J., Demarchi F., Dennis P.B., Dennis P.A., Deretic V., Devenish R.J., Di Sano F., Dice J.F., Difiglia M., Dinesh-Kumar S., Distelhorst C.W., Djavaheri-Mergny M., Dorsey F.C., Dröge W., Dron M., Dunn W.A., Duszenko M., Eissa N.T., Elazar Z., Esclatine A., Eskelinen E.L., Fésüs L., Finley K.D., Fuentes J.M., Fueyo J., Fujisaki K., Galliot B., Gao F.B., Gewirtz D.A., Gibson S.B., Gohla A., Goldberg A.L., Gonzalez R., González-Estévez C., Gorski S., Gottlieb R.A., Häussinger D., He Y.W., Heidenreich K., Hill J.A., Høyer-Hansen M., Hu X., Huang W.P., Iwasaki A., Jäättelä M., Jackson W.T., Jiang X., Jin S., Johansen T., Jung J.U., Kadowaki M., Kang C., Kelekar A., Kessel D.H., Kiel J.A., Kim H.P., Kimchi A., Kinsella T.J., Kiselyov K., Kitamoto K., Knecht E., Komatsu M., Kominami E., Kondo S., Kovács A.L., Kroemer G., Kuan C.Y., Kumar R., Kundu M., Landry J., Laporte M., Le W., Lei H.Y., Lenardo M.J., Levine B., Lieberman A., Lim K.L., Lin F.C., Liou W., Liu L.F., Lopez-Berestein G., López-Otín C., Lu B., Macleod K.F., Malorni W., Martinet W., Matsuoka K., Mautner J., Meijer A.J., Meléndez A., Michels P., Miotto G., Mistiaen W.P., Mizushima N., Mograbi B., Monastyrska I., Moore M.N., Moreira P.I., Moriyasu Y., Motyl T., Münz C., Murphy L.O., Naqvi N.I., Neufeld T.P., Nishino I., Nixon R.A., Noda T., Nürnberg B., Ogawa M., Oleinick N.L., Olsen L.J., Ozpolat B., Paglin S., Palmer G.E., Papassideri I., Parkes M., Perlmutter D.H., Perry G., Piacentini M., Pinkas-Kramarski R., Prescott M., Proikas-Cezanne T., Raben N., Rami A., Reggiori F., Rohrer B., Rubinsztein D.C., Ryan K.M., Sadoshima J., Sakagami H., Sakai Y., Sandri M., Sasakawa C., Sass M., Schneider C., Seglen P.O., Seleverstov O., Settleman J., Shacka J.J., Shapiro I.M., Sibirny A., Silva-Zacarin E.C., Simon H.U., Simone C., Simonsen A., Smith M.A., Spanel-Borowski K., Srinivas V., Steeves M., Stenmark H., Stromhaug P.E., Subauste C.S., Sugimoto S., Sulzer D., Suzuki T., Swanson M.S., Tabas I., Takeshita F., Talbot N.J., Tallóczy Z., Tanaka K., Tanaka K., Tanida I., Taylor G.S., Taylor J.P., Terman A., Tettamanti G., Thompson C.B., Thumm M., Tolkovsky A.M., Tooze S.A., Truant R., Tumanovska L.V., Uchiyama Y., Ueno T., Uzcátegui N.L., van der Klei I., Vaquero E.C., Vellai T., Vogel M.W., Wang H.G., Webster P., Wiley J.W., Xi Z., Xiao G., Yahalom J., Yang J.M., Yap G., Yin X.M., Yoshimori T., Yu L., Yue Z., Yuzaki M., Zabirnyk O., Zheng X., Zhu X., Deter R.L. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008, 4(2):151-175.
4. Levy J.M., Thorburn A. Targeting autophagy during cancer therapy to improve clinical outcomes. Pharmacol. Ther. 2011, 131(1):130-141.
5. Zhang H., Kong X., Kang J., Su J., Li Y., Zhong J., Sun L. Oxidative stress induces parallel autophagy and mitochondria dysfunction in human glioma U251 cells. Toxicol. Sci. 2009, 110(2):376-388.
6. Adams J.M., Cory S. The Bcl-2 apoptotic switch in cancer development and therapy. Oncogene 2007, 26(9):1324-1337.
7. Dai Y., Grant S. Targeting multiple arms of the apoptotic regulatory machinery. Cancer Res. 2007, 67(7):2908-2911.
8. Nguyen M., Marcellus R.C., Roulston A., Watson M., Serfass L., Murthy Madiraju S.R., Goulet D., Viallet J., Bélec L., Billot X., Acoca S., Purisima E., Wiegmans A., Cluse L., Johnstone R.W., Beauparlant P., Shore G.C. Small molecule obatoclax (GX15-070) antagonizes MCL-1 and overcomes MCL-1-mediated resistance to apoptosis. Proc. Natl. Acad. Sci. USA 2007, 104(49):19512-19517. (Epub. 2007 November 26).
9. Pan J., Cheng C., Verstovsek S., Chen Q., Jin Y., Cao Q. The BH3-mimetic GX15-070 induces autophagy, potentiates the cytotoxicity of carboplatin and 5-fluorouracil in esophageal carcinoma cells. Cancer Lett. 2010, 293(2):167-174.
10. Maiuri M.C., Criollo A., Tasdemir E., Vicencio J.M., Tajeddine N., Hickman J.A., Geneste O., Kroemer G. BH3-only proteins and BH3 mimetics induce autophagy by competitively disrupting the interaction between Beclin 1 and Bcl-2/Bcl-X(L). Autophagy 2007, 3(4):374-376.
11. Wang J. Beclin 1 bridges autophagy, apoptosis and differentiation. Autophagy 2008, 4(7):947-948.
12. Malik S.A., Shen S., Mariño G., BenYounès A., Maiuri M.C., Kroemer G. BH3 mimetics reveal the network properties of autophagy-regulatory signaling cascades. Autophagy 2011, 7(8):914-916. (Epub. 2011 August 1).
13. Lépine S., Allegood J.C., Park M., Dent P., Milstien S., Spiegel S. Sphingosine-1-phosphate phosphohydrolase-1 regulates ER stress-induced autophagy. Cell Death Differ. 2011, 18(2):350-361. (Epub. 2010 August 27).
14. Younce C.W., Kolattukudy P.E. MCP-1 causes cardiomyoblast death via autophagy resulting from ER stress caused by oxidative stress generated by inducing a novel zinc-finger protein, MCPIP. Biochemistry 2010, 426(1):43-53.
15. Schönthal A.H. Endoplasmic reticulum stress and autophagy as targets for cancer therapy. Cancer Lett. 2009, 275(2):163-169. (Epub. 2008 August 9).
16. 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.
17. Morin M.J., Porter C.W., McKernan P., Bernacki R.J. The biochemical and ultrastructural effects of tunicamycin and d-glucosamine in L1210 leukemic cells. J. Cell. Physiol. 1983, 114(2):162-172.
18. Werstuck G.H., Khan M.I., Femia G., Kim A.J., Tedesco V., Trigatti B., Shi Y. Glucosamine-induced endoplasmic reticulum dysfunction is associated with accelerated atherosclerosis in a hyperglycemic mouse model. Diabetes 2006, 55(1):93-101.
19. Ogata M., Hino S., Saito A., Morikawa K., Kondo S., Kanemoto S., Murakami T., Taniguchi M., Tanii I., Yoshinaga K., Shiosaka S., Hammarback J.A., Urano F., Imaizumi K. Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol. Cell. Biol. 2006, 26(24):9220-9231.
20. Ding W.X., Ni H.M., Gao W., Hou Y.F., Melan M.A., Chen X., Stolz D.B., Shao Z.M., Yin X.M. Differential effects of endoplasmic reticulum stress-induced autophagy on cell survival. J. Biol. Chem. 2007, 282(7):4702-4710.
21. Szegezdi E., Logue S.E., Gorman A.M., Samali A. Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep. 2006, 7(9):880-885.
22. Zhang Z., Song T., Zhang T., Gao J., Wu G., An L., Du G. A novel BH3 mimetic S1 potently induces Bax/Bak-dependent apoptosis by targeting both Bcl-2 and Mcl-1. Int. J. Cancer 2011, 128(7):1724-1735.
23. Lee A.S. The glucose-regulated proteins: stress induction and clinical applications. Trends Biochem. Sci. 2001, 26(8):504-510.
24. Kim R., Emi M., Tanabe K., Murakami S. Role of the unfolded protein response in cell death. Apoptosis 2006, 11(1):5-13.
25. Nakagawa T., Zhu H., Morishima N., Li E., Xu J., Yankner B.A., Yuan J. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 2000, 403(6765):98-103.
26. Paglin S., Lee N.Y., Nakar C., Fitzgerald M., Plotkin J., Deuel B., Hackett N., McMahill M., Sphicas E., Lampen N., Yahalom J. Rapamycinsensitive pathway regulates mitochondrial membrane potential, autophagy, and survival in irradiated MCF-7 cells. Cancer Res. 2005, 65(23):11061-11070.
27. Takeuchi H., Kondo Y., Fujiwara K., Kanzawa T., Aoki H., Mills G.B., Kondo S. Synergistic augmentation of rapamycin-induced autophagy in malignant glioma cells by phosphatidylinositol 3-kinase/protein kinase B inhibitors. Cancer Res. 2005, 65(8):3336-3346.
28. Cullen K.J., Yang Z., Schumaker L., Guo Z. Mitochondria as a critical target of the chemotherapeutic agent cisplatin in head and neckcancer. J. Bioenerg. Biomembr. 2007, 39(1):43-50.
29. Zeng H., Zhang S., Yang K.Y., Wang T., Hu J.L., Huang L.L., Wu G. Knockdown of second mitochondria-derived activator of caspase expression by RNAi enhances growth and cisplatin resistance of human lung cancer cells. Cancer Biother. Radiopharm. 2010, 25(6):705-712.
30. Podratz J.L., Knight A.M., Ta L.E., Staff N.P., Gass J.M., Genelin K., Schlattau A., Lathroum L., Windebank A.J. Cisplatin induced mitochondrial DNA damage in dorsal root ganglion neurons. Neurobiol. Dis. 2011, 41(3):661-668. (Epub. 2010 December 8).
31. Jiang M., Wang C.Y., Huang S., Yang T., Dong Z. Cisplatin-induced apoptosis in p53-deficient renal cells via the intrinsic mitochondrial pathway. Am. J. Physiol. Renal Physiol. 2009, 296(5):F983-F993. (Epub. 2009 March 11).
32. Wei Q., Dong G., Franklin J., Dong Z. The pathological role of Bax in cisplatin nephrotoxicity. Kidney Int. 2007, 72(1):53-62.
33. Berridge M.J. The endoplasmic reticulum: a multifunctional signaling organelle. Cell Calcium 2002, 32(5-6):235-249.
34. Yu H., Su J., Xu Y., Kang J., Li H., Zhang L., Yi H., Xiang X., Liu F., Sun L. P62/SQSTM1 involved in cisplatin resistance in human ovarian cancer cells by clearing ubiquitinated proteins. Eur. J. Cancer 2011, 47(10):1585-1594. (Epub. 2011 March 1).
35. Xu Y., Yu H., Qin H., Kang J., Yu C., Zhong J., Su J., Li H., Sun L. Inhibition of autophagy enhances cisplatin cytotoxicity through endoplasmic reticulum stress in human cervical cancer cells. Cancer Lett. 2012, 314(2):232-243. (Epub. 2011 October 2).
36. Germain M., Mathai J.P., Shore G.C. BH-3-only BIK functions at the endoplasmic reticulum to stimulate cytochrome c release from mitochondria. J. Biol. Chem. 2002, 277(20):18053-18060.
37. 2+ uptake by mitochondria without affecting ER calcium store content. Cell Calcium 2008, 44(3):324-338. (Epub. 2008 April 14).
38. Jones R.G., Bui T., White C., Madesh M., Krawczyk C.M., Lindsten T., Hawkins B.J., Kubek S., Frauwirth K.A., Wang Y.L., Conway S.J., Roderick H.L., Bootman M.D., Shen H., Foskett J.K., Thompson C.B. The proapoptotic factors Bax and Bak regulate T Cell proliferation through control of endoplasmic reticulum Ca(2+) homeostasis. Immunity 2007, 27(2):268-280. (Epub. 2007 August 9).
39. Morishima N., Nakanishi K., Tsuchiya K., Shibata T., Seiwa E. Translocation of Bim to the endoplasmic reticulum (ER) mediates ER stress signaling for activation of caspase-12 during ER stress-induced apoptosis. J. Biol. Chem. 2004, 279(48):50375-50381.
40. Zong W.X., Li C., Hatzivassiliou G., Lindsten T., Yu Q.C., Yuan J., Thompson C.B. Bax and Bak can localize to the endoplasmic reticulum to initiate apoptosis. J. Cell Biol. 2003, 162(1):59-69.