ATM and LKB1 dependent activation of AMPK sensitizes cancer cells to etoposide-induced apoptosis

Cancer Letters

Volumn 328, Issue 1, 2013, Pages 114-119

  Luo, Lingyu ^a   Huang, Wei ^c   Tao, Rong ^b,e   Hu, Ningyan ^a   Xiao, Zhi Xiong ^d   Luo, Zhijun ^a,b  

^a NANCHANG UNIVERSITY   (China)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c GUANGZHOU MEDICAL UNIVERSITY   (China)

^d SICHUAN UNIVERSITY   (China)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Apoptosis; Etoposide

Indexed keywords

ATM PROTEIN; ETOPOSIDE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PROTEIN KINASE LKB1; SMALL INTERFERING RNA;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG POTENCY; DRUG RESPONSE; DRUG SENSITIZATION; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE SILENCING; HUMAN; HUMAN CELL; INCUBATION TIME; LUNG ADENOCARCINOMA; MALE; PRIORITY JOURNAL; PROSTATE CANCER; RNA INTERFERENCE;

AMP-ACTIVATED PROTEIN KINASES; ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; CELL CYCLE PROTEINS; CELL LINE, TUMOR; DNA-BINDING PROTEINS; ENZYME ACTIVATION; ETOPOSIDE; HUMANS; MALE; PROSTATIC NEOPLASMS; PROTEIN-SERINE-THREONINE KINASES; TUMOR SUPPRESSOR PROTEINS;

EID: 84868450290     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2012.08.034     Document Type: Article

References (44)

1. Hardie D.G. AMP-activated protein kinase as a drug target. Ann. Rev. Pharmacol. Toxicol. 2007, 47:185-210.
2. Luo Z., Saha A.K., Xiang X., Ruderman N.B. AMPK, the metabolic syndrome and cancer. Trends Pharmacol. Sci. 2005, 26:69-76.
3. Oakhill J.S., Steel R., Chen Z.P., Scott J.W., Ling N., Tam S., Kemp B.E. AMPK is a direct adenylate charge-regulated protein kinase. Science 2011, 332:1433-1435.
4. Luo Z., Zang M., Guo W. AMPK as a metabolic tumor suppressor: control of metabolism and cell growth. Future Oncol. 2010, 6:457-470.
5. Alessi D.R., Sakamoto K., Bayascas J.R. LKB1-dependent signaling pathways. Ann. Rev. Biochem. 2006, 75:137-163.
6. Sanchez-Cespedes M., Parrella P., Esteller M., Nomoto S., Trink B., Engles J.M., Westra W.H., Herman J.G., Sidransky D. Inactivation of LKB1/STK11 is a common event in adenocarcinomas of the lung. Cancer Res. 2002, 62:3659-3662.
7. Ji H., Ramsey M.R., Hayes D.N., Fan C., McNamara K., Kozlowski P., Torrice C., Wu M.C., Shimamura T., Perera S.A., Liang M.C., Cai D., Naumov G.N., Bao L., Contreras C.M., Li D., Chen L., Krishnamurthy J., Koivunen J., Chirieac L.R., Padera R.F., Bronson R.T., Lindeman N.I., Christiani D.C., Lin X., Shapiro G.I., Janne P.A., Johnson B.E., Meyerson M., Kwiatkowski D.J., Castrillon D.H., Bardeesy N., Sharpless N.E., Wong K.K. LKB1 modulates lung cancer differentiation and metastasis. Nature 2007, 448:807-810.
8. Wingo S.N., Gallardo T.D., Akbay E.A., Liang M.C., Contreras C.M., Boren T., Shimamura T., Miller D.S., Sharpless N.E., Bardeesy N., Kwiatkowski D.J., Schorge J.O., Wong K.K., Castrillon D.H. Somatic LKB1 mutations promote cervical cancer progression. PLoS One 2009, 4:e5137.
9. Ikediobi O.N., Davies H., Bignell G., Edkins S., Stevens C., O'Meara S., Santarius T., Avis T., Barthorpe S., Brackenbury L., Buck G., Butler A., Clements J., Cole J., Dicks E., Forbes S., Gray K., Halliday K., Harrison R., Hills K., Hinton J., Hunter C., Jenkinson A., Jones D., Kosmidou V., Lugg R., Menzies A., Mironenko T., Parker A., Perry J., Raine K., Richardson D., Shepherd R., Small A., Smith R., Solomon H., Stephens P., Teague J., Tofts C., Varian J., Webb T., West S., Widaa S., Yates A., Reinhold W., Weinstein J.N., Stratton M.R., Futreal P.A., Wooster R. Mutation analysis of 24 known cancer genes in the NCI-60 cell line set. Mol. Cancer Ther. 2006, 5:2606-2612.
10. Rattan R., Giri S., Singh A.K., Singh I. 5-Aminoimidazole-4-carboxamide-1-beta-D-ribofuranoside inhibits cancer cell proliferation in vitro and in vivo via AMP-activated protein kinase. J. Biol. Chem. 2005, 280:39582-39593.
11. Huang X., Wullschleger S., Shpiro N., McGuire V.A., Sakamoto K., Woods Y.L., McBurnie W., Fleming S., Alessi D.R. Important role of the LKB1-AMPK pathway in suppressing tumorigenesis in PTEN-deficient mice. Biochem. J. 2008, 412:211-221.
12. Evans J.M., Donnelly L.A., Emslie-Smith A.M., Alessi D.R., Morris A.D. Metformin and reduced risk of cancer in diabetic patients. BMJ 2005, 330:1304-1305.
13. Libby G., Donnelly L.A., Donnan P.T., Alessi D.R., Morris A.D., Evans J.M. New users of metformin are at low risk of incident cancer: a cohort study among people with type 2 diabetes. Diabetes Care 2009, 32:1620-1625.
14. Hadad S.M., Baker L., Quinlan P.R., Robertson K.E., Bray S.E., Thomson G., Kellock D., Jordan L.B., Purdie C.A., Hardie D.G., Fleming S., Thompson A.M. Histological evaluation of AMPK signalling in primary breast cancer. BMC Cancer 2009, 9:307.
15. Jiralerspong S., Palla S.L., Giordano S.H., Meric-Bernstam F., Liedtke C., Barnett C.M., Hsu L., Hung M.C., Hortobagyi G.N., Gonzalez-Angulo A.M. Metformin and pathologic complete responses to neoadjuvant chemotherapy in diabetic patients with breast cancer. J. Clin. Oncol. 2009, 27:3297-3302.
16. Jones R.G., Plas D.R., Kubek S., Buzzai M., Mu J., Xu Y., Birnbaum M.J., Thompson C.B. AMP-activated protein kinase induces a p53-dependent metabolic checkpoint. Mol. Cell. 2005, 18:283-293.
17. Inoki K., Zhu T., Guan K.L. TSC2 mediates cellular energy response to control cell growth and survival. Cell 2003, 115:577-590.
18. Gwinn D.M., Shackelford D.B., Egan D.F., Mihaylova M.M., Mery A., Vasquez D.S., Turk B.E., Shaw R.J. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol. Cell. 2008, 30:214-226.
19. Liang J., Shao S.H., Xu Z.X., Hennessy B., Ding Z., Larrea M., Kondo S., Dumont D.J., Gutterman J.U., Walker C.L., Slingerland J.M., Mills G.B. The energy sensing LKB1-AMPK pathway regulates p27(kip1) phosphorylation mediating the decision to enter autophagy or apoptosis. Nat. Cell. Biol. 2007, 9:218-224.
20. Greer E.L., Oskoui P.R., Banko M.R., Maniar J.M., Gygi M.P., Gygi S.P., Brunet A. The energy sensor AMP-activated protein kinase directly regulates the mammalian FOXO3 transcription factor. J. Biol. Chem. 2007, 282:30107-30119.
21. Lavin M.F., Kozlov S. ATM activation and DNA damage response. Cell Cycle 2007, 6:931-942.
22. Shiloh Y., Kastan M.B. ATM: genome stability, neuronal development, and cancer cross paths. Adv. Cancer Res. 2001, 83:209-254.
23. Schneider J.G., Finck B.N., Ren J., Standley K.N., Takagi M., Maclean K.H., Bernal-Mizrachi C., Muslin A.J., Kastan M.B., Semenkovich C.F. ATM-dependent suppression of stress signaling reduces vascular disease in metabolic syndrome. Cell Metab. 2006, 4:377-389.
24. Suzuki A., Kusakai G., Kishimoto A., Shimojo Y., Ogura T., Lavin M.F., Esumi H. IGF-1 phosphorylates AMPK-alpha subunit in ATM-dependent and LKB1-independent manner. Biochem. Biophys. Res. Commun. 2004, 324:986-992.
25. Sun Y., Connors K.E., Yang D.Q. AICAR induces phosphorylation of AMPK in an ATM-dependent, LKB1-independent manner. Mol. Cell. Biochem. 2007, 306:239-245.
26. Fu X., Wan S., Lyu Y.L., Liu L.F., Qi H. Etoposide induces ATM-dependent mitochondrial biogenesis through AMPK activation. PLoS One 2008, 3:e2009.
27. Sanli T., Rashid A., Liu C., Harding S., Bristow R.G., Cutz J.C., Singh G., Wright J., Tsakiridis T. Ionizing radiation activates AMP-activated kinase (AMPK): a target for radiosensitization of human cancer cells. Int. J. Radiat. Oncol. Biol. Phys. 2010, 78:221-229.
28. Alexander A., Cai S.L., Kim J., Nanez A., Sahin M., MacLean K.H., Inoki K., Guan K.L., Shen J., Person M.D., Kusewitt D., Mills G.B., Kastan M.B., Walker C.L. ATM signals to TSC2 in the cytoplasm to regulate mTORC1 in response to ROS. Proc. Natl. Acad. Sci. USA 2010, 107:4153-4158.
29. Zajkowicz A., Rusin M. The activation of the p53 pathway by the AMP mimetic AICAR is reduced by inhibitors of the ATM or mTOR kinases. Mech. Age. Dev. 2011, 132:543-551.
30. Menendez J.A., Cufi S., Oliveras-Ferraros C., Martin-Castillo B., Joven J., Vellon L., Vazquez-Martin A. Metformin and the ATM DNA Damage Response (DDR): Accelerating the Onset of Stress-Induced Senescence to Boost Protection Against Cancer. Aging (Albany NY) 2011, 3:1063-1077.
31. Zhou K., Bellenguez C., Spencer C.C., Bennett A.J., Coleman R.L., Tavendale R., Hawley S.A., Donnelly L.A., Schofield C., Groves C.J., Burch L., Carr F., Strange A., Freeman C., Blackwell J.M., Bramon E., Brown M.A., Casas J.P., Corvin A., Craddock N., Deloukas P., Dronov S., Duncanson A., Edkins S., Gray E., Hunt S., Jankowski J., Langford C., Markus H.S., Mathew C.G., Plomin R., Rautanen A., Sawcer S.J., Samani N.J., Trembath R., Viswanathan A.C., Wood N.W., Harries L.W., Hattersley A.T., Doney A.S., Colhoun H., Morris A.D., Sutherland C., Hardie D.G., Peltonen L., McCarthy M.I., Holman R.R., Palmer C.N., Donnelly P., Pearson E.R. Common variants near ATM are associated with glycemic response to metformin in type 2 diabetes. Nat. Genet. 2011, 43:117-120.
32. Rashid A., Liu C., Sanli T., Tsiani E., Singh G., Bristow R.G., Dayes I., Lukka H., Wright J., Tsakiridis T. Resveratrol enhances prostate cancer cell response to ionizing radiation. Modulation of the AMPK, Akt and mTOR pathways. Radiat. Oncol. 2011, 6:144.
33. Ji C., Yang B., Yang Y.L., He S.H., Miao D.S., He L., Bi Z.G. Exogenous cell-permeable C6 ceramide sensitizes multiple cancer cell lines to Doxorubicin-induced apoptosis by promoting AMPK activation and mTORC1 inhibition. Oncogene 2010, 29:6557-6568.
34. Chen M.B., Shen W.X., Yang Y., Wu X.Y., Gu J.H., Lu P.H. Activation of AMP-activated protein kinase is involved in vincristine-induced cell apoptosis in B16 melanoma cell. J. Cell. Physiol. 2011, 226:1915-1925.
35. Chen M.B., Wu X.Y., Gu J.H., Guo Q.T., Shen W.X., Lu P.H. Activation of AMP-activated protein kinase contributes to doxorubicin-induced cell death and apoptosis in cultured myocardial H9c2 cells. Cell Biochem. Biophys. 2011, 60:311-322.
36. Hwang J.T., Park O.J., Lee Y.K., Sung M.J., Hur H.J., Kim M.S., Ha J.H., Kwon D.Y. Anti-tumor effect of luteolin is accompanied by AMP-activated protein kinase and nuclear factor-kappaB modulation in HepG2 hepatocarcinoma cells. Int. J. Mol. Med. 2011, 28:25-31.
37. Rocha G.Z., Dias M.M., Ropelle E.R., Osorio-Costa F., Rossato F.A., Vercesi A.E., Saad M.J., Carvalheira J.B. Metformin amplifies chemotherapy-induced AMPK activation and antitumoral growth. Clin. Cancer Res. 2011, 17:3993-4005.
38. Xie B.S., Zhao H.C., Yao S.K., Zhuo D.X., Jin B., Lv D.C., Wu C.L., Ma D.L., Gao C., Shu X.M., Ai Z.L. Autophagy inhibition enhances etoposide-induced cell death in human hepatoma G2 cells. Int. J. Mol. Med. 2011, 27:599-606.
39. Janjetovic K., Vucicevic L., Misirkic M., Vilimanovich U., Tovilovic G., Zogovic N., Nikolic Z., Jovanovic S., Bumbasirevic V., Trajkovic V., Harhaji-Trajkovic L. Metformin reduces cisplatin-mediated apoptotic death of cancer cells through AMPK-independent activation of Akt. Eur. J. Pharmacol. 2011, 651:41-50.
40. Harhaji-Trajkovic L., Vilimanovich U., Kravic-Stevovic T., Bumbasirevic V., Trajkovic V. AMPK-mediated autophagy inhibits apoptosis in cisplatin-treated tumour cells. J. Cell. Mol. Med. 2009, 13:3644-3654.
41. Zhou J., Huang W., Tao R., Ibaragi S., Lan F., Ido Y., Wu X., Alekseyev Y.O., Lenburg M.E., Hu G.F., Luo Z. Inactivation of AMPK alters gene expression and promotes growth of prostate cancer cells. Oncogene 2009, 28:1993-2002.
42. Xiang X., Saha A.K., Wen R., Ruderman N.B., Luo Z. AMP-activated protein kinase activators can inhibit the growth of prostate cancer cells by multiple mechanisms. Biochem. Biophys. Res. Commun. 2004, 321:161-167.
43. Pelicano H., Martin D.S., Xu R.H., Huang P. Glycolysis inhibition for anticancer treatment. Oncogene 2006, 25:4633-4646.
44. Belda-Iniesta C., Pernia O., Simo R. Metformin: a new option in cancer treatment. Clin. Transl. Oncol. 2011, 13:363-367.