Caffeine induces apoptosis by enhancement of autophagy via PI3K/Akt/mTOR/p70S6K inhibition

Autophagy

Volumn 7, Issue 2, 2011, Pages 176-187

  Saiki, Shinji ^a   Sasazawa, Yukiko ^b   Imamichi, Yoko ^a   Kawajiri, Sumihiro ^a   Fujimaki, Takahiro ^b   Tanida, Isei ^c   Kobayashi, Hiroki ^b   Sato, Fumiaki ^a   Sato, Shigeto ^a   Ishikawa, Kei Ichi ^a   Imoto, Masaya ^b   Hattori, Nobutaka ^a  

^a JUNTENDO UNIVERSITY   (Japan)

^b KEIO UNIVERSITY   (Japan)

^c NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

Apoptosis; Autophagy; Caffeine; ERK1 2; PI3K Akt mTOR p70S6K

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 3 METHYLADENINE; ALOXISTATIN; CAFFEINE; INSULIN; MAMMALIAN TARGET OF RAPAMYCIN; MICROTUBULE ASSOCIATED PROTEIN 1; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN P53; PROTEIN P70; RIBOSOME PROTEIN; STAUROSPORINE;

APOPTOSIS; ARTICLE; AUTOPHAGY; CELL CYCLE REGULATION; CELL DEATH; CONTROLLED STUDY; DOSE RESPONSE; ELECTRON MICROSCOPY; ENZYME INHIBITION; FIBROBLAST; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; PHAGOSOME; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; WESTERN BLOTTING;

EID: 79551508637     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.7.2.14074     Document Type: Article

References (43)

1. Bode AM, Dong Z. The enigmatic effects of caffeine in cell cycle and cancer. Cancer Lett 2007; 247:26-39.
2. Jang MH, Shin MC, Kang IS, Baik HH, Cho YH, Chu JP, et al. Caffeine induces apoptosis in human neuroblastoma cell line SK-N-MC. J Korean Med Sci 2002; 17:674-8.
3. Gururajanna B, Al-Katib AA, Li YW, Aranha O, Vaitkevicius VK, Sarkar FH. Molecular effects of taxol and caffeine on pancreatic cancer cells. Int J Mol Med 1999; 4:501-7.
4. Qi W, Qiao D, Martinez JD. Caffeine induces TP53-independent G(1)-phase arrest and apoptosis in human lung tumor cells in a dose-dependent manner. Radiat Res 2002; 157:166-74.
5. Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature 2008; 451:1069-75.
6. Rubinsztein DC. The roles of intracellular protein-degradation pathways in neurodegeneration. Nature 2006; 443:780-6.
7. Eisenberg-Lerner A, Bialik S, Simon HU, Kimchi A. Life and death partners: apoptosis, autophagy and the cross-talk between them. Cell Death Differ 2009; 16:966-75.
8. Espert L, Denizot M, Grimaldi M, Robert-Hebmann V, Gay B, Varbanov M, et al. Autophagy is involved in T cell death after binding of HIV-1 envelope proteins to CXCR4. J Clin Invest 2006; 116:2161-72.
9. Foukas LC, Daniele N, Ktori C, Anderson KE, Jensen J, Shepherd PR. Direct effects of caffeine and theophylline on p110delta and other phosphoinositide 3-kinases. Differential effects on lipid kinase and protein kinase activities. J Biol Chem 2002; 277:37124-30.
10. Kudchodkar SB, Yu Y, Maguire TG, Alwine JC. Human cytomegalovirus infection alters the substrate specificities and rapamycin sensitivities of raptor- and rictor-containing complexes. Proc Natl Acad Sci USA 2006; 103:14182-7.
11. Winter G, Hazan R, Bakalinsky AT, Abeliovich H. Caffeine induces macroautophagy and confers a cytocidal effect on food spoilage yeast in combination with benzoic acid. Autophagy 2008; 4:28-36.
12. Rubinsztein DC, Cuervo AM, Ravikumar B, Sarkar S, Korolchuk V, Kaushik S, Klionsky DJ. In search of an "autophagomometer". Autophagy 2009; 5:585-9.
13. Tanida I, Ueno T, Kominami E. LC3 and Autophagy. Methods Mol Biol 2008; 445:77-88.
14. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000; 19:5720-8.
15. Yamamoto A, Tagawa Y, Yoshimori T, Moriyama Y, Masaki R, Tashiro Y. Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell Struct Funct 1998; 23:33-42.
16. Mizushima N, Yoshimori T, Levine B. Methods in mammalian autophagy research. Cell 140:313-26.
17. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000; 100:57-70.
18. Ikenoue T, Hong S, Inoki K. Monitoring mammalian target of rapamycin (mTOR) activity. Methods Enzymol 2009; 452:165-80.
19. Sinn B, Tallen G, Schroeder G, Grassl B, Schulze J, Budach V, Tinhofer I. Caffeine confers radiosensitization of PTEN-deficient malignant glioma cells by enhancing ionizing radiation-induced G1 arrest and negatively regulating Akt phosphorylation. Mol Cancer Ther 9:480-8.
20. Sarkaria JN, Busby EC, Tibbetts RS, Roos P, Taya Y, Karnitz LM, Abraham RT. Inhibition of ATM and ATR kinase activities by the radiosensitizing agent, caffeine. Cancer Res 1999; 59:4375-82.
21. Inoki K, Li Y, Xu T, Guan KL. Rheb GTPase is a direct target of TSC2 GAP activity and regulates mTOR signaling. Genes Dev 2003; 17:1829-34. (Pubitemid 36944560)
22. Inoki K, Li Y, Zhu T, Wu J, Guan KL. TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat Cell Biol 2002; 4:648-57.
23. Garami A, Zwartkruis FJ, Nobukuni T, Joaquin M, Roccio M, Stocker H, et al. Insulin activation of Rheb, a mediator of mTOR/S6K/4E-BP signaling, is inhibited by TSC1 and 2. Mol Cell 2003; 11:1457-66.
24. Muise-Helmericks RC, Grimes HL, Bellacosa A, Malstrom SE, Tsichlis PN, Rosen N. Cyclin D expression is controlled post-transcriptionally via a phosphatidylinositol- 3-kinase/Akt-dependent pathway. J Biol Chem 1998; 273:29864-72.
25. 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; 183:101-16.
26. Wan X, Harkavy B, Shen N, Grohar P, Helman LJ. Rapamycin induces feedback activation of Akt signaling through an IGF-1R-dependent mechanism. Oncogene 2007; 26:1932-40.
27. Sun SY, Rosenberg LM, Wang X, Zhou Z, Yue P, Fu H, Khuri FR. Activation of Akt and eIF4E survival pathways by rapamycin-mediated mammalian target of rapamycin inhibition. Cancer Res 2005; 65:7052-8.
28. O'Reilly KE, Rojo F, She QB, Solit D, Mills GB, Smith D, et al. mTOR inhibition induces upstream receptor tyrosine kinase signaling and activates Akt. Cancer Res 2006; 66:1500-8.
29. Cirstea D, Hideshima T, Rodig S, Santo L, Pozzi S, Vallet S, et al. Dual inhibition of akt/mammalian target of rapamycin pathway by nanoparticle albumin-bound-rapamycin and perifosine induces antitumor activity in multiple myeloma. Mol Cancer Ther 2010; 9:963-75.
30. Aoki H, Takada Y, Kondo S, Sawaya R, Aggarwal BB, Kondo Y. Evidence that curcumin suppresses the growth of malignant gliomas in vitro and in vivo through induction of autophagy: role of Akt and extracellular signal-regulated kinase signaling pathways. Mol Pharmacol 2007; 72:29-39.
31. Ellington AA, Berhow MA, Singletary KW. Inhibition of Akt signaling and enhanced ERK1/2 activity are involved in induction of macroautophagy by triterpenoid B-group soyasaponins in colon cancer cells. Carcinogenesis 2006; 27:298-306.
32. Rubinsztein DC, Gestwicki JE, Murphy LO, Klionsky DJ. Potential therapeutic applications of autophagy. Nat Rev Drug Discov 2007; 6:304-12.
33. Ravikumar B, Vacher C, Berger Z, Davies JE, Luo S, Oroz LG, et al. Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat Genet 2004; 36:585-95.
34. Kotake Y, Ohta S. MPP+ analogs acting on mitochondria and inducing neuro-degeneration. Curr Med Chem 2003; 10:2507-16. (Pubitemid 37456021)
35. Hagan MP, Hopcia KL, Sylvester FC, Held KD. Caffeine-induced apoptosis reveals a persistent lesion after treatment with bromodeoxyuridine and ultraviolet-B light. Radiat Res 1997; 147:674-9.
36. Efferth T, Fabry U, Glatte P, Osieka R. Expression of apoptosis-related oncoproteins and modulation of apoptosis by caffeine in human leukemic cells. J Cancer Res Clin Oncol 1995; 121:648-56.
37. 2/M. Cytometry 1997; 27:365-73.
38. Lau CC, Pardee AB. Mechanism by which caffeine potentiates lethality of nitrogen mustard. Proc Natl Acad Sci USA 1982; 79:2942-6.
39. Takagi M, Shigeta T, Asada M, Iwata S, Nakazawa S, Kanke Y, et al. DNA damage-associated cell cycle and cell death control is differentially modulated by caffeine in clones with p53 mutations. Leukemia 1999; 13:70-7.
40. Ormerod MG, Collins MK, Rodriguez-Tarduchy G, Robertson D. Apoptosis in interleukin-3-dependent haemopoietic cells. Quantification by two flow cytometric methods. J Immunol Methods 1992; 153:57-65.
41. Kawatani M, Uchi M, Simizu S, Osada H, Imoto M. Transmembrane domain of Bcl-2 is required for inhibition of ceramide synthesis, but not cytochrome c release in the pathway of inostamycin-induced apoptosis. Exp Cell Res 2003; 286:57-66.
42. Kawajiri S, Saiki S, Sato S, Sato F, Hatano T, Eguchi H, Hattori N. PINK1 is recruited to mitochondria with parkin and associates with LC3 in mitophagy. FEBS Lett 2010; 584:1073-9.
43. Sarkar S, Davies JE, Huang Z, Tunnacliffe A, Rubinsztein DC. Trehalose, a novel mTOR-independent autophagy enhancer, accelerates the clearance of mutant huntingtin and alpha-synuclein. J Biol Chem 2007; 282:5641-52.