Glyoxalase i inhibition induces apoptosis in irradiated MCF-7 cells via a novel mechanism involving Hsp27, p53 and NF-κB

British Journal of Cancer

Volumn 111, Issue 2, 2014, Pages 395-406

  Antognelli, C ^a   Palumbo, I ^a   Aristei, C ^a   Talesa, V N ^a  

^a UNIVERSITY OF PERUGIA   (Italy)

Author keywords

apoptosis; argpyrimidine; Erk1 2; ER ; glyoxalase I; Hsp27; ionising radiation; MCF 7 cells; NF kB; p53; reactive oxygen species

Indexed keywords

ESTROGEN RECEPTOR ALPHA; HEAT SHOCK PROTEIN 27; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LACTOYLGLUTATHIONE LYASE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN P53; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA;

APOPTOSIS; ARTICLE; CELL VIABILITY; CYTOTOXICITY; DNA FRAGMENTATION ASSAY; DOWN REGULATION; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; IONIZING RADIATION; MCF 7 CELL LINE; MITOCHONDRION; NICK END LABELING; OXIDATIVE STRESS; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SPECTROPHOTOMETRY; WESTERN BLOTTING;

APOPTOSIS; BREAST NEOPLASMS; CELL CULTURE TECHNIQUES; HSP27 HEAT-SHOCK PROTEINS; HUMANS; LACTOYLGLUTATHIONE LYASE; MCF-7 CELLS; NF-KAPPA B; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; RNA, SMALL INTERFERING; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84904561581     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2014.280     Document Type: Article

References (66)

1. Aebi HE (1974) Catalase. In Methods in Enzymatic Analysis, Bergmeyer HU (ed) pp 673-684. Academic Press: New York
2. Alikhani Z, Alikhani M, Boyd CM, Nagao K, Trackman PC, Graves DT (2005) Advanced glycation end products enhance expression of pro-apoptotic genes and stimulate fibroblast apoptosis through cytoplasmic and mitochondrial pathways. J Biol Chem 280: 12087-12095.
3. Amir S, Ma AH, Shi XB, Xue L, Kung HJ, Devere White RW (2013) Oncomir miR-125b suppresses p14(ARF) to modulate p53-dependent and p53-independent apoptosis in prostate cancer. PLoS One 8: e61064.
4. Antognelli C, Mezzasoma L, Fettucciari K, Talesa VN (2013) A novel mechanism of methylglyoxal cytotoxicity in prostate cancer cells. Int J Biochem Cell Biol 45: 836-844.
5. Antognelli C, Mezzasoma L, Fettucciari K, Mearini E, Talesa VN (2013) Role of glyoxalase I in the proliferation and apoptosis control of human LNCaP and PC3 prostate cancer cells. Prostate 73: 121-132.
6. Baeuerle PA, Baltimore D (1988) I kappa B: a specific inhibitor of the NF-kappa B transcription factor. Science 242: 540-546.
7. Baldwin AS (2001) Control of oncogenesis and cancer therapy resistance by the transcription factor NF-kappaB. J Clin Invest 107: 241-246.
8. Bolisetty S, Jaimes EA (2013) Mitochondria and reactive oxygen species: physiology and pathophysiology. Int J Mol Sci 14: 6306-6344.
9. Bondong S, Kiefel H, Hielscher T, Zeimet AG, Zeillinger R, Pils D, Schuster E, Castillo-Tong DC, Cadron I, Vergote I, Braicu I, Sehouli J, Mahner S, Fogel M, Altevogt P (2012) Prognostic significance of L1CAM in ovarian cancer and its role in constitutive NF-kB activation. Ann Oncol 23: 1795-17802.
10. Calvo FA, Gonzalez-Domingo M, Usychin S (2013) Intraoperative irradiation. In Encyclopedia of Radiation Oncology, Brady LW, Yaeger TE (eds) pp 388-399.
11. Springer: Heidelberg. Chance B, Sies H, Boveris A (1979) Hydroperoxide metabolism in mammalian organs. Physiol Rev 59: 527-605.
12. Charalambous C, Pitta CA, Constantinou AI (2013) Equol enhances tamoxifen's anti-tumor activity by induction of caspase-mediated apoptosis in MCF-7 breast cancer cells. BMC Cancer 13: 238.
13. Chen H, Yang K, Choi S, Fischer JH, Jeong H (2009) Up-regulation of UDP-glucuronosyltransferase (UGT) 1A4 by 17beta-estradiol: a potential mechanism of increased lamotrigine elimination in pregnancy. Drug Metab Dispos 37: 1841-1847.
14. Chen T, Chen M, Chen J (2013) Ionizing radiation potentiates dihydroartemisinin-induced apoptosis of A549 cells via a caspase-8-dependent pathway. PLoS One 8: e59827.
15. Esterbauer H, Schaur RJ, Zollner H (1991) Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med 11: 81-128.
16. Fettucciari K, Fetriconi I, Mannucci R, Nicoletti I, Bartoli A, Coaccioli S, Marconi P (2006) Group B Streptococcus induces macrophage apoptosis by calpain activation. J Immunol 176: 7542-7556.
17. Fleming TH, Theilen TM, Masania J, Wunderle M, Karimi J, Vittas S, Bernauer R, Bierhaus A, Rabbani N, Thornalley PJ, Kroll J, Tyedmers J, Nawrotzki R, Herzig S, Brownlee M, Nawroth PP (2013) Aging-dependent reduction in glyoxalase 1 delays wound healing. Gerontology 59: 427-437.
18. Forman HJ, Torres M (2001) Redox signaling in macrophages. Mol Aspects Med 22: 189-216.
19. Gasparian AV, Yao YJ, Kowalczyk D, Lyakh LA, Karseladze A, Slaga TJ, Budunova IV (2002) The role of IKK in constitutive activation of NF-kappaB transcription factor in prostate carcinoma cells. J Cell Sci 115: 141-151.
20. Golden EB, Pellicciotta I, Demaria S, Barcellos-Hoff MH, Formenti SC (2012) The convergence of radiation and immunogenic cell death signaling pathways. Front Oncol 2: 88.
21. Honda S, Farboud B, Hjelmeland L, Handa J (2001) Induction of an aging mRNA retinal pigment epithelial cell phenotype by matrix-containing advanced glycation end products in vitro. Investig Ophthalmol Vis Sci 42: 2419-2425.
22. Hwang JR, Jo K, Lee Y, Sung BJ, Park YW, Lee JH (2012) Upregulation of CD9 in ovarian cancer is related to the induction of TNF-a gene expression and constitutive NF-kB activation. Carcinogenesis 33: 77-83.
23. Kanagasabai R, Karthikeyan K, Vedam K, Qien W, Zhu Q, Ilangovan G (2010) Hsp27 protects adenocarcinoma cells from UV-induced apoptosis by Akt and p21-dependent pathways of survival. Mol Cancer Res 8: 1399-1412.
24. Kanagasabai R, Krishnamurthy K, Druhan LJ, Ilangovan G (2011) Forced expression of heat shock protein 27 (Hsp27) reverses P-Glycoprotein (ABCB1)-mediated drug efflux and MDR1gene expression in adriamycinresistant human breast cancer cells. J Biol Chem 286: 33289-33300.
25. Kaufmann SH, Hengartner MO (2001) Programmed cell death: alive and well in the new millennium. Trends Cell Biol 11: 526-534.
26. Kazmierczuk A, Kilianska ZM (2010) Role of heat shock proteins in cell apoptosis. Postepy Hig Med Dosw 64: 273-283.
27. Kim A, Lee JE, Jang WS, Lee SJ, Park S, Kang HJ, Lee SS (2012) A combination of methotrexate and irradiation promotes cell death in NK/T-cell lymphoma cells via down-regulation of NF-kB signaling. Leuk Res 36: 350-357.
28. Kim KM, Kim YS, Jung DH, Lee J, Kim JS (2012a) Increased glyoxalase I levels inhibit accumulation of oxidative stress and an advanced glycation end product in mouse mesangial cells cultured in high glucose. Exp Cell Res 318: 152-159.
29. Kim J, Kim OS, Kim CS, Sohn E, Jo K, Kim JS (2012b) Accumulation of argpyrimidine, a methylglyoxal-derived advanced glycation end product, increases apoptosis of lens epithelial cells both in vitro and in vivo. Exp Mol Med 44: 167-175.
30. Kwon JE, Kim BY, Kwak SY, Bae IH, Han YH (2013) Ionizing radiationinducible microRNA miR-193a-3p induces apoptosis by directly targeting Mcl-1. Apoptosis 18: 896-909.
31. Lindholm PF, Bub J, Kaul S, Shidham VB, Kajdacsy-Balla A (2000) The role of constitutive NF-kappaB activity in PC-3 human prostate cancer cell invasive behavior. Clin Exp Metastasis 18: 471-479.
32. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real time quantitative PCR and the 2-DDCT method. Methods 25: 402-408.
33. Ludwig L, Kessler H, Wagner M, Hoang-Vu C, Dralle H, Adler G, Böhm BO, Schmid RM (2001) Nuclear factor-kappaB is constitutively active in C-cell carcinoma and required for RET-induced transformation. Cancer Res 61: 4526-4535.
34. Mannervik B, Aronsson AC, Marmstal E, Tibellin G (1981) Glyoxalase I (rat liver). In Methods in Enzymatic Analysis, Jakoby WB (ed) pp 297-301. Academic Press: New York.
35. McCord JM, Fridovich I (1969) Superoxide dismutase. an enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244: 6049-6055.
36. Miyake N, Chikumi H, Takata M, Nakamoto M, Igishi T, Shimizu E (2012) Rapamycin induces p53-independent apoptosis through the mitochondrial pathway in non-small cell lung cancer cells. Oncol Rep 28: 848-854.
37. Morales A, Miranda M, Sánchez-Reyes A, Biete A, Fernández-Checa JC (1998) Oxidative damage of mitochondrial and nuclear DNA induced by ionizing radiation in human hepatoblastoma cells. Int J Radiat Oncol Biol Phys 42: 191-203.
38. Na HK, Kim EH, Choi MA, Park JM, Kim DH, Surh YJ (2012) Diallyl trisulfide induces apoptosis in human breast cancer cells through ROS-mediated activation of JNK and AP-1. Biochem Pharmacol 84: 1241-1250.
39. O'Callaghan-Sunol C, Gabai VL, Sherman MY (2007) Hsp27 modulates p53 signaling and suppresses cellular senescence. Cancer Res 67: 11779-11788.
40. Osborne CK, Wakeling A, Nicholson RI (2004) Fulvestrant: an oestrogen receptor antagonist with a novel mechanism of action. Br J Cancer 90: S2-S6.
41. Paglia DE, Valentine WN (1967) Studies on the qualitative and quantitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70: 158-169.
42. Park MT, Song MJ, Lee H, Oh ET, Choi BH, Jeong SY, Choi EK, Park HJ (2011) b-lapachone significantly increases the effect of ionizing radiation to cause mitochondrial apoptosis via JNK activation in cancer cells. PLoS One 6: e25976.
43. Rabbani N, Thornalley PJ (2012) Methylglyoxal, glyoxalase 1 and the dicarbonyl proteome. Amino Acids 42: 1133-1142.
44. Ranuncolo SM, Pittaluga S, Evbuomwan MO, Jaffe ES, Lewis BA (2012) Hodgkin lymphoma requires stabilized NIK and constitutive RelB expression for survival. Blood 120: 3756-3763.
45. Rulli A, Antognelli C, Prezzi E, Baldracchini F, Piva F, Giovannini E, Talesa V (2006) A possible regulatory role of 17b-estradiol and tamoxifen on glyoxalase I and glyoxalase II genes expression in MCF7 and BT20 human breast cancer cells. Breast Cancer Res Treat 96: 187-196.
46. Sakamoto H, Mashima T, Yamamoto K, Tsuruo T (2002) Modulation of heat-shock protein 27 (Hsp27) anti-apoptotic activity by methylglyoxal modification. J Biol Chem 277: 45770-45775.
47. Santha S, Bommareddy A, Rule B, Guillermo R, Kaushik RS, Young A, Dwivedi C (2013) Antineoplastic effects of a-santalol on estrogen receptor-positive and estrogen receptor-negative breast cancer cells through cell cycle arrest at G2/M phase and induction of apoptosis. PLoS One 8: e56982.
48. Shibuya T, Watanabe Y, Nalley KA, Fusco A, Salafsky B (1989) The BCA protein determination system: an analysis of several buffers, incubation temperature and protein standards. Tokyo Ika Daigaku Zasshi 47: 677-682.
49. Shukla S, Gupta S (2004) Suppression of constitutive and tumor necrosis factor alpha-induced nuclear factor (NF)-kappaB activation and induction of apoptosis by apigenin in human prostate carcinoma PC-3 cells: Correlation with downregulation of NF-kappaB-responsive genes. Clin Cancer Res 10: 3169-3178.
50. Sinha K, Das J, Pal PB, Sil PC (2013) Oxidative stress: the mitochondriadependent and mitochondria-independent pathways of apoptosis. Arch Toxicol 87: 1157-1180.
51. Soga M, Matsuzawa A, Ichijo H (2012) Oxidative stress-induced diseases via the ASK1 Signaling pathway. Int J Cell Biol 2012: 439587.
52. Sovak MA, Bellas RE, Kim DW, Zanieski GJ, Rogers AE, Traish AM, Sonenshein GE (1997) Aberrant nuclear factor-kappaB/Rel expression and the pathogenesis of breast cancer. J Clin Invest. 100: 2952-2960.
53. Suh J, Payvandi F, Edelstein LC, Amenta PS, Zong WX, Gélinas C, Rabson AB (2002) Mechanisms of constitutive NF-kappaB activation in human prostate cancer cells. Prostate 52: 183-200.
54. Sun M, Zigman S (1978) An improved spectrophotometric assay for superoxide dismutase based on epinephrine autoxidation. Anal Biochem 90: 81-89.
55. Thornalley PJ, Yurek-George A, Argirov OK (2000) Kinetics and mechanism of the reaction of aminoguanidine with the alpha-oxoaldehydes glyoxal, methylglyoxal, and 3-deoxyglucosone under physiological conditions. Biochem Pharmacol 60: 55-65.
56. Urashima T, Nagasawa H, Wang K, Adelstein SJ, Little JB, Kassis AI (2006) Induction of apoptosis in human tumor cells after exposure to Auger electrons: comparison with gamma-ray exposure. Nucl Med Biol 33: 1055-1063.
57. Van Laethem A, Nys K, Van Kelst S, Claerhout S, Ichijo H, Vandenheede JR, Garmyn M, Agostinis P (2006) Apoptosis signal regulating kinase-1 connects reactive oxygen species to p38 MAPK-induced mitochondrial apoptosis in UVB-irradiated human keratinocytes. Free Radic Biol Med 41: 1361-1371.
58. Veronesi U, Orecchia R, Luini A, Galimberti V, Zurrida S, Intra M, Veronesi P, Arnone P, Leonardi MC, Ciocca M, Lazzari R, Caldarella P, Rotmensz N, Sangalli C, Sances D, Maisonneuve P (2010) Intraoperative radiotherapy during breast conserving surgery: a study on 1,822 cases treated with electrons. Breast Cancer Res Treat 124: 141-151.
59. Wang Z, Sun Y (2010) Targeting p53 for novel anticancer therapy. Transl Oncol 3: 1-12.
60. Weitsman GE, Weebadda W, Ung K, Murphy LC (2009) Reactive oxygen species induce phosphorylation of serine 118 and 167 on estrogen receptor alpha. Breast Cancer Res Treat 118: 269-279.
61. Yamagishi S, Inagaki Y, Amano S, Okamoto T, Takeuchi M, Makita Z (2002) Pigment epithelium-derived factor protects cultured retinal pericytes from advanced glycation end product-induced injury through its antioxidative properties. Biochem Biophys Res Commun 296: 877-882.
62. Yeh CH, Yang YY, Huang YF, Chow KC, Chen MF (2012) Induction of apoptosis in human Hep3B hepatoma cells by norcantharidin through a p53 independent pathway via TRAIL/DR5 signal transduction. Chin J Integr Med 18: 676-682.
63. Yi H, Liang B, Jia J, Liang N, Xu H, Ju G, Ma S, Liu X (2013) Differential roles of miR-199a-5p in radiation-induced autophagy in breast cancer cells. FEBS Lett 587: 436-443.
64. Zhang Y, Luo M, Zu Y, Fu Y, Gu C, Wang W, Yao L, Efferth T (2012) Dryofragin, a phloroglucinol derivative, induces apoptosis in human breast cancer MCF-7 cells through ROS-mediated mitochondrial pathway. Chem Biol Interact 199: 129-136.
65. Zhang S, He Y, Tong Q, Chen Q, Wu X, Huang W (2013) Deltonin induces apoptosis in MDA-MB-231 human breast cancer cells via reactive oxygen species-mediated mitochondrial dysfunction and ERK/AKT signaling pathways. Mol Med Rep 7: 1038-1044.
66. Zhu Q, Wang J, Zhang Y, Sun S (2012) Mechanisms of MPP-induced PC12 cell apoptosis via reactive oxygen species. J Huazhong Univ Sci Technolog Med Sci 32: 861-866.