Involvement of metformin and AMPK in the radioresponse and prognosis of luminal versus basal-like breast cancer treated with radiotherapy

Oncotarget

Volumn 5, Issue 24, 2014, Pages 12936-12949

  Zhang, Yimin ^a   Storr, Sarah J ^a   Johnson, Kerstie ^b   Green, Andrew R ^a   Rakha, Emad A ^a   Ellis, Ian O ^a   Morgan, David A L ^b   Martin, Stewart G ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b NOTTINGHAM CITY HOSPITAL   (United Kingdom)

Author keywords

AMPK; Breast cancer; Luminal phenotype; Metformin; Radiosensitivity

Indexed keywords

ADENOSINE MONOPHOSPHATE ACTIVATED KINASE ALPHA; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; METFORMIN; REACTIVE OXYGEN METABOLITE; THIOREDOXIN; UNCLASSIFIED DRUG;

ADULT; AGED; APOPTOSIS; ARTICLE; BASAL LIKE BREAST CANCER; BREAST CANCER; CANCER CELL; CANCER PROGNOSIS; CANCER RADIOTHERAPY; CANCER SPECIFIC SURVIVAL; CELL CYCLE PROGRESSION; CLONOGENIC ASSAY; CONTROLLED STUDY; ENZYME LOCALIZATION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; LOCAL RECURRENCE FREE SURVIVAL; LUMINAL BREAST CANCER; MAJOR CLINICAL STUDY; OXIDATION REDUCTION STATE; PROTEIN EXPRESSION; RADIATION RESPONSE; RADIOSENSITIVITY; RECURRENCE FREE SURVIVAL; WESTERN BLOTTING; BIOSYNTHESIS; BREAST NEOPLASMS; CARCINOMA, BASAL CELL; CHEMORADIOTHERAPY; COHORT ANALYSIS; ENZYMOLOGY; FEMALE; MCF 7 CELL LINE; METABOLISM; PROGNOSIS; SURVIVAL; TUMOR CELL LINE;

AMP-ACTIVATED PROTEIN KINASES; BREAST NEOPLASMS; CARCINOMA, BASAL CELL; CELL LINE, TUMOR; CHEMORADIOTHERAPY; COHORT STUDIES; FEMALE; HUMANS; MCF-7 CELLS; METFORMIN; PROGNOSIS; SURVIVAL ANALYSIS;

EID: 84921328301     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2683     Document Type: Article

References (56)

1. Bailey CJ, Turner RC. Metformin. N Engl J Med. 1996; 334(9):574-579.
2. Shaw RJ, Lamia KA, Vasquez D, Koo SH, Bardeesy N, Depinho RA, Montminy M, Cantley LC. The kinase LKB1 mediates glucose homeostasis in liver and therapeutic effects of metformin. Science. 2005; 310(5754):1642-1646.
3. Owen MR, Doran E, Halestrap AP. Evidence that metformin exerts its anti-diabetic effects through inhibition of complex of the mitochondrial respiratory chain. Biochem J. 2000; Pt 3:607-614.
4. Hardie DG. (2011). AMP-activated protein kinase: a cellular energy sensor with a key role in metabolic disorders and in cancer. Biochem Soc Trans. (England, pp. 1-13.
5. Thompson AM. Molecular pathways: preclinical models and clinical trials with metformin in breast cancer. Clin Cancer Res. 2014; 20(10):2508-2515.
6. Libby G, Donnelly LA, Donnan PT, Alessi DR, Morris AD, Evans JM. New users of metformin are at low risk of incident cancer: a cohort study among people with type 2 diabetes. Diabetes Care. 2009; 32(9):1620-1625.
7. Bo S, Ciccone G, Rosato R, Villois P, Appendino G, Ghigo E, Grassi G. Cancer mortality reduction and metformin: a retrospective cohort study in type 2 diabetic patients. Diabetes Obes Metab. 2012; 14(1):23-29.
8. Lee MS, Hsu CC, Wahlqvist ML, Tsai HN, Chang YH, Huang YC. Type 2 diabetes increases and metformin reduces total, colorectal, liver and pancreatic cancer incidences in Taiwanese: a representative population prospective cohort study of 800,000 individuals. BMC Cancer. 2011; 11:20.
9. Skinner HD, Crane CH, Garrett CR, Eng C, Chang GJ, Skibber JM, Rodriguez-Bigas MA, Kelly P, Sandulache VC, Delclos ME, Krishnan S, Das P. Metformin use and improved response to therapy in rectal cancer. Cancer Med. 2013; 2(1):99-107.
10. Margel D, Urbach DR, Lipscombe LL, Bell CM, Kulkarni G, Austin PC, Fleshner N. Metformin use and all-cause and prostate cancer-specific mortality among men with diabetes. J Clin Oncol. 2013; 31(25):3069-3075.
11. Sadeghi N, Abbruzzese JL, Yeung SC, Hassan M, Li D. Metformin use is associated with better survival of diabetic patients with pancreatic cancer. Clin Cancer Res. 2012; 18(10):2905-2912.
12. Jiralerspong S, Palla SL, Giordano SH, Meric-Bernstam F, Liedtke C, Barnett CM, Hsu L, Hung MC, Hortobagyi GN, Gonzalez-Angulo AM. Metformin and pathologic complete responses to neoadjuvant chemotherapy in diabetic patients with breast cancer. J Clin Oncol. 2009; 27(20):3297-3302.
13. Rieken M, Kluth LA, Xylinas E, Fajkovic H, Becker A, Karakiewicz PI, Herman M, Lotan Y, Seitz C, Schramek P, Remzi M, Loidl W, Pummer K, et al. Association of diabetes mellitus and metformin use with biochemical recurrence in patients treated with radical prostatectomy for prostate cancer. World J Urol. 2013.
14. Kaushik D, Karnes RJ, Eisenberg MS, Rangel LJ, Carlson RE, Bergstralh EJ. Effect of metformin on prostate cancer outcomes after radical prostatectomy. Urol Oncol. 2013.
15. Zhang P, Li H, Tan X, Chen L, Wang S. Association of metformin use with cancer incidence and mortality: a metaanalysis. Cancer Epidemiol. 2013; 37(3):207-218.
16. Allott EH, Abern MR, Gerber L, Keto CJ, Aronson WJ, Terris MK, Kane CJ, Amling CL, Cooperberg MR, Moorman PG, Freedland SJ. Metformin does not affect risk of biochemical recurrence following radical prostatectomy: results from the SEARCH database. Prostate Cancer Prostatic Dis. 2013.
17. Carling D. The AMP-activated protein kinase cascade--a unifying system for energy control. Trends Biochem Sci. 2004; 29(1):18-24.
18. Steinberg GR, Kemp BE. AMPK in Health and Disease. Physiol Rev. 2009; 89(3):1025-1078.
19. Shackelford DB, Shaw RJ. The LKB1-AMPK pathway: metabolism and growth control in tumour suppression. Nat Rev Cancer. 2009; 9(8):563-575.
20. Zhou K, Bellenguez C, Spencer CC, Bennett AJ, Coleman RL, Tavendale R, Hawley SA, Donnelly LA, Schofield C, Groves CJ, Burch L, Carr F, Strange A, et al. Common variants near ATM are associated with glycemic response to metformin in type 2 diabetes. Nat Genet. 2011; 43(2):117- 120.
21. Zakikhani M, Dowling R, Fantus IG, Sonenberg N, Pollak M. Metformin is an AMP kinase-dependent growth inhibitor for breast cancer cells. Cancer Research. 2006; 66(21):10269-10273.
22. Liu BL, Fan ZY, Edgerton SM, Deng XS, Alimova IN, Lind SE, Thor AD. Metformin induces unique biological and molecular responses in triple negative breast cancer cells. Cell Cycle. 2009; 8(13):2031-2040.
23. Rattan R, Graham RP, Maguire JL, Giri S, Shridhar V. Metformin Suppresses Ovarian Cancer Growth and Metastasis with Enhancement of Cisplatin Cytotoxicity In Vivo. Neoplasia. 2011; 13(5):483-U130.
24. Alimova IN, Liu B, Fan Z, Edgerton SM, Dillon T, Lind SE, Thor AD. Metformin inhibits breast cancer cell growth, colony formation and induces cell cycle arrest in vitro. Cell Cycle. 2009; 8(6):909-915.
25. Martinez Marignac VL, Smith S, Toban N, Bazile M, Aloyz R. Resistance to Dasatinib in primary chronic lymphocytic leukemia lymphocytes involves AMPK-mediated energetic re-programming. Oncotarget. 2013; 4(12):2550-2566.
26. Moiseeva O, Deschenes-Simard X, St-Germain E, Igelmann S, Huot G, Cadar AE, Bourdeau V, Pollak MN, Ferbeyre G. Metformin inhibits the senescence-associated secretory phenotype by interfering with IKK/NF-kappaB activation. Aging Cell. 2013; 12(3):489-498.
27. Song CW, Lee H, Dings RPM, Williams B, Powers J, Dos Santos T, Choi BH, Park HJ. Metformin kills and radiosensitizes cancer cells and preferentially kills cancer stem cells. Scientific Reports. 2012; 2.
28. Sanli T, Rashid A, Liu C, Harding S, Bristow RG, Cutz JC, 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(1):221-229.
29. Storozhuk Y, Hopmans SN, Sanli T, Barron C, Tsiani E, Cutz JC, Pond G, Wright J, Singh G, Tsakiridis T. Metformin inhibits growth and enhances radiation response of non-small cell lung cancer (NSCLC) through ATM and AMPK. Br J Cancer. 2013; 108(10):2021-2032.
30. Zannella VE, Cojocari D, Hilgendorf S, Vellanki RN, Chung S, Wouters BG, Koritzinsky M. AMPK regulates metabolism and survival in response to ionizing radiation. Radiother Oncol. 2011; 99(3):293-299.
31. Hou XG, Song J, Li XN, Zhang L, Wang XL, Chen L, Shen YH. Metformin reduces intracellular reactive oxygen species levels by upregulating expression of the antioxidant thioredoxin via the AMPK-FOXO3 pathway. Biochemical and Biophysical Research Communications. 2010; 396(2):199-205.
32. Chai TF, Hong SY, He H, Zheng L, Hagen T, Luo Y, Yu FX. A potential mechanism of metformin-mediated regulation of glucose homeostasis: inhibition of Thioredoxin-interacting protein (Txnip) gene expression. Cell Signal. 2012; 24(8):1700-1705.
33. Zhang Y, Martin SG. Redox proteins and radiotherapy. Clin Oncol (R Coll Radiol). 2014; 26(5):289-300.
34. Powis G, Mustacich D, Coon A. The role of the redox protein thioredoxin in cell growth and cancer. Free Radical Biology and Medicine. 2000; 29(3-4):312-322.
35. Powis G, Montfort WR. Properties and biological activities of thioredoxins. Annual Review of Pharmacology and Toxicology. 2001; 41:261-295.
36. Nishiyama A, Matsui M, Iwata S, Hirota K, Masutani H, Nakamura H, Takagi Y, Sono H, Gon Y, Yodoi J. Identification of thioredoxin-binding protein-2/vitamin D-3 up-regulated protein 1 as a negative regulator of thioredoxin function and expression. Journal of Biological Chemistry. 1999; 274(31):21645-21650.
37. Yin M, Zhou J, Gorak EJ, Quddus F. Metformin Is Associated With Survival Benefit in Cancer Patients With Concurrent Type 2 Diabetes: A Systematic Review and Meta-Analysis. Oncologist. 2013.
38. Xiao Y, Zhang S, Hou G, Zhang X, Hao X, Zhang J. Clinical pathological characteristics and prognostic analysis of diabetic women with luminal subtype breast cancer. Tumour Biol. 2013.
39. He X, Esteva FJ, Ensor J, Hortobagyi GN, Lee MH, Yeung SC. Metformin and thiazolidinediones are associated with improved breast cancer-specific survival of diabetic women with HER2+ breast cancer. Ann Oncol. 2012; 23(7):1771- 1780.
40. Bonanni B, Puntoni M, Cazzaniga M, Pruneri G, Serrano D, Guerrieri-Gonzaga A, Gennari A, Trabacca MS, Galimberti V, Veronesi P, Johansson H, Aristarco V, Bassi F, et al. Dual effect of metformin on breast cancer proliferation in a randomized presurgical trial. J Clin Oncol. 2012; 30(21):2593-2600.
41. Zhang T, Zhang L, Fan J, Wu K, Guan Z, Wang X, Li L, Hsieh JT, He D, Guo P. Metformin Sensitizes Prostate Cancer Cells to Radiation Through EGFR/p-DNA-PKCS In Vitro and In Vivo. Radiat Res. 2014; 181(6):641-649.
42. Hadad SM, Baker L, Quinlan PR, Robertson KE, Bray SE, Thomson G, Kellock D, Jordan LB, Purdie CA, Hardie DG, Fleming S, Thompson AM. Histological evaluation of AMPK signalling in primary breast cancer. BMC Cancer. 2009; 9:307.
43. Woods A, Vertommen D, Neumann D, Turk R, Bayliss J, Schlattner U, Wallimann T, Carling D, Rider MH. Identification of phosphorylation sites in AMP-activated protein kinase (AMPK) for upstream AMPK kinases and study of their roles by site-directed mutagenesis. J Biol Chem. 2003; 278(31):28434-28442.
44. Vidal AP, Andrade BM, Vaisman F, Cazarin J, Pinto LF, Breitenbach MM, Corbo R, Caroli-Bottino A, Soares F, Vaisman M, Carvalho DP. AMP-activated protein kinase signaling is upregulated in papillary thyroid cancer. Eur J Endocrinol. 2013; 169(4):521-528.
45. Fox MM, Phoenix KN, Kopsiaftis SG, Claffey KP. AMPActivated Protein Kinase alpha 2 Isoform Suppression in Primary Breast Cancer Alters AMPK Growth Control and Apoptotic Signaling. Genes Cancer. 2013; 4(1-2):3-14.
46. Bayraktar S, Hernadez-Aya LF, Lei X, Meric-Bernstam F, Litton JK, Hsu L, Hortobagyi GN, Gonzalez-Angulo AM. Effect of metformin on survival outcomes in diabetic patients with triple receptor-negative breast cancer. Cancer. 2012; 118(5):1202-1211.
47. Hall EJ, Giaccia AJ. (2012). Radiobiology for the radiologist. (Philadelphia: Wolters Kluwer Health/ Lippincott Williams & Wilkins).
48. Algire C, Moiseeva O, Deschenes-Simard X, Amrein L, Petruccelli L, Birman E, Viollet B, Ferbeyre G, Pollak MN. Metformin reduces endogenous reactive oxygen species and associated DNA damage. Cancer Prev Res (Phila). 2012; 5(4):536-543.
49. Sanli T, Storozhuk Y, Linher-Melville K, Bristow RG, Laderout K, Viollet B, Wright J, Singh G, Tsakiridis T. Ionizing radiation regulates the expression of AMPactivated protein kinase (AMPK) in epithelial cancer cells: modulation of cellular signals regulating cell cycle and survival. Radiother Oncol. 2012; 102(3):459-465.
50. Woolston CM, Storr SJ, Ellis IO, Morgan DAL, Martin SG. Expression of thioredoxin system and related peroxiredoxin proteins is associated with clinical outcome in radiotherapy treated early stage breast cancer. Radiotherapy and Oncology. 2011; 100(2):308-313.
51. Shaked M, Ketzinel-Gilad M, Cerasi E, Kaiser N, Leibowitz G. AMP-activated protein kinase (AMPK) mediates nutrient regulation of thioredoxin-interacting protein (TXNIP) in pancreatic beta-cells. PLoS One. 2011; 6(12):e28804.
52. McShane LM, Altman DG, Sauerbrei W, Taube SE, Gion M, Clark GM. REporting recommendations for tumor MARKer prognostic studies (REMARK). Nat Clin Pract Urol. 2005; 2(8):416-422.
53. Abdel-Fatah TM, Powe DG, Agboola J, Adamowicz-Brice M, Blamey RW, Lopez-Garcia MA, Green AR, Reis- Filho JS, Ellis IO. The biological, clinical and prognostic implications of p53 transcriptional pathways in breast cancers. J Pathol. 2010; 220(4):419-434.
54. Rakha EA, El-Rehim DA, Paish C, Green AR, Lee AH, Robertson JF, Blamey RW, Macmillan D, Ellis IO. Basal phenotype identifies a poor prognostic subgroup of breast cancer of clinical importance. Eur J Cancer. 2006; 42(18):3149-3156.
55. Rakha EA, El-Sayed ME, Green AR, Paish EC, Lee AH, Ellis IO. Breast carcinoma with basal differentiation: a proposal for pathology definition based on basal cytokeratin expression. Histopathology. 2007; 50(4):434-438.
56. Sorlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, Hastie T, Eisen MB, van de Rijn M, Jeffrey SS, Thorsen T, Quist H, Matese JC, et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proceedings of the National Academy of Sciences of the United States of America. 2001; 98(19):10869-10874.