Metformin decreases growth of pancreatic cancer cells by decreasing reactive oxygen species: Role of NOX4

Biochemical and Biophysical Research Communications

Volumn 465, Issue 1, 2015, Pages 41-46

  Cheng, Guanjun ^a   Lanza Jacoby, Susan ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Cell survival; Metformin; NOX4; Oxidative stress; Pancreatic cancer

Indexed keywords

GLUCOSE; MANGANESE SUPEROXIDE DISMUTASE; METFORMIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; ANTIDIABETIC AGENT; CYBB PROTEIN, HUMAN; MEMBRANE PROTEIN; NOX4 PROTEIN, HUMAN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE DISMUTASE;

APOPTOSIS; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CANCER GROWTH; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DRUG EFFECT; GLUCOSE BLOOD LEVEL; HUMAN; HUMAN CELL; OXIDATIVE STRESS; PANCREAS CANCER; PANCREATIC CANCER CELL LINE; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANTAGONISTS AND INHIBITORS; CELL PROLIFERATION; DRUG EFFECTS; EPITHELIUM CELL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PANCREAS; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

AGOUTI PACA;

APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; EPITHELIAL CELLS; GENE EXPRESSION REGULATION, NEOPLASTIC; GLUCOSE; HUMANS; HYPOGLYCEMIC AGENTS; MEMBRANE GLYCOPROTEINS; METFORMIN; NADPH OXIDASE; PANCREAS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; SUPEROXIDE DISMUTASE;

EID: 84940453827     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2015.07.118     Document Type: Article

References (43)

1. A.A. Arsian, K.J. Helzisouer, and C. Kooperberg Anthropometric measures, body mass index, and pancreatic cancer. A pooled analysis from the Pancreatic Cancer Cohort Consortium Arch. Intern. Med. 170 2010 791 802
2. J.M. Genkinger, D. Spiegelman, and K.E. Anderson A pooled analysis of 14 cohort studies of anthropometric factors and pancreatic cancer risk Int. J. Cancer 129 2011 1708 1717
3. L. Jiao, A. Berrington de Gonzalez, and P. Hartge Body mass index, effect modifiers, and risk of pancreatic cancer: a pooled study of seven prospective cohorts Cancer Causes Control 21 2010 1305 1314
4. A. Berrington de Gonzalez, S. Sweetland, and E. Spencer A meta-analysis of obesity and risk of pancreatic cancer Br. J. Cancer 89 2001 519 523
5. S.C. Larsson, N. Orsini, and A. Wolk Body mass index and pancreatic cancer risk: a meta-analysis of prospective studies Int. J. Cancer 120 2007 1993 1998
6. A.G. Renehan, M. Tyson, M. Egger, R.F. Heller, and M. Zwahlen Body-mass index and incidence of cancer: a systematic review and meta-analysis of prospective observational studies Lancet 371 2008 569 578
7. D.F. Birt, J.C. Pelling, L.T. White, K. Dimitroff, and T. Barnett Influence of diet and calorie restriction on the initiation and promotion of skin carcinogenesis in the SENCAR mouse model Cancer Res. 51 1991 1851 1854
8. A. Koizumi, M. Tsukada, S. Hirano, S. Kamiyama, H. Masuda, and K.T. Suzuki Energy restriction that inhibits cellular proliferation by torpor can decrease susceptibility to spontaneous and asbestos-induced lung tumors in A/J mice Lab. Invest. 68 6 1993 728 739
9. S. Lanza-Jacoby, G. Yan, G. Radice, C. LePhong, J. Baliff, and R. Hess Calorie restriction delays the progression of PanIn lesions to pancreatic cancer in LSL-KrasG12D,Pdx-1Cre mouse model of pancreatic cancer Exp. Biol. Med. 238 2013 787 797
10. S. Bolen, L. Feldman, and J. Vassy Systematic review: comparative effectiveness and safety of oral medications for type 2 diabetes mellitus Ann. Intern. Med. 147 2007 386 399
11. N. Sadeghi, J.L. Abbruxxese, S.C. Yeung, M. Hassan, and D. Li Metformin use is associated with better survival of diabetic patients with pancreatic cancer Clin. Cancer Res. 18 2012 2905 2912
12. J.M. Evans, L.A. Donnelly, A.M. Emslie-Smith, D.R. Alessi, and A.D. Morris Metformin and reduced risk of cancer in diabetic patients BMJ 2005 1304 1305
13. S.L. Bowker, S.R. Majumdar, P. Veugelers, and J.A. Johnson Increased cancer-related mortality for patients with type 2 diabetes who use sulfonylureas or insulin Diabetes Care 29 2006 254 258
14. M.Y. El Mir, V. Nogueira, E. Fontaine, N. Averet, M. Rigoulet, and X. Leverve Dimethylbiguanide inhibits cell respiration via an indirect effect targeted on the respiratory chain complex I J. Biol. Chem. 275 2000 223 228
15. E.C. Vaquero, M. Edderkaoui, S.J. Pandol, I. Gukovsky, and A.S. Gukovskaya Reactive oxygen species produced by NADPH oxidase inhibits apoptosis in pancreatic cancer cells J. Biol. Chem. 279 2004 34643 34654
16. F. Weinberg, R. Hamanaka, W.W. Wheaton, S. Weinberg, J. Joseph, M. Lopez, and et al. Mitochrondrial metabolism and ROS generation are essential for Kras-mediated tumorigenicity PNAS 107 2010 8788 8789
17. J. Du, S. Nelson, A.L. Simons, K.E. Olney, J.C. Moser, H.E. Schrock, B.A. Wagner, G.R. Buettner, B.J. Smith, M.L. Teoh, M.S. Tsao, and J.J. Cullen Regulation of pancreatic cancer growth by superoxide Mol. Carcinog. 52 2013 555 567
18. D. Bonnefont-Rousselot, B. Raji, S. Walrand, M. Gardes-Albert, D. Jore, A. Legrand, J. Peynet, and M.P. Vasson An intracellular modulation of free radical production could contribute to the beneficial effects of metformin towards oxidative stress Metabolism 52 2003 586 589
19. L. Li, N. Mamputi, N. Wiernsperger, and G. Renier Signaling pathways involved in human vascular smooth muscle cell proliferation and matrix metalloproteinase-2 expression induced by leptin: inhibitory effect of metformin Diabetes 54 2005 2227 2234
20. X. Hou, J. Song, X.-N. Li, L. Zhanh, X. Wang, L. Chen, and Y.H. Shen Metformin reduces intracellar reactive oxygen species levels by upregulating expression of the antioxidant thioredoxin via AMPK-FOXO3 pathway Bioch. Biophy. Res. Commun. 396 2010 199 205
21. j Sinnett-Smith, K. Kisfalvi, R. Kui, and E. Rozengurt Metformin inhibition of mTORC1 activation, DNA synthesis and proliferation in pancreatic cancer cells: dependence on glucose concentration and role of AMPK Biochem. Biophys. Res. Commun. 430 2013 352 357
22. E. Karnevi, K. Said, R. Andersson, and A.H. Rosendahl Metformin-mediated growth inhibition involves suppression of the IGF-1 receptor signaling pathway in human pancreatic cancer cells BMC Cancer 13 2013 235 245
23. J. Du, D.H. Daniels, C. Asbury, S. Venkataraman, J. Liu, D.H. Spitz, L.W. Oberley, and J.J. Cullen Mitochrondria production of reactive oxygen species mediate dicumarol-induced cytoxicity in cancer cells J. Biol. Chem. 281 2006 37416 37426
24. G. Yan, and S. Lanza-Jacoby Nexrutine inhibits survival and induces G1 cell cycle arrest, which is associated with apoptosis or autophagy depending on the breast cancer cell line Nutr. Cancer 66 2014 506 516
25. M.L. Teoh, W. Sun, B.J. Smith, L.W. Oberley, and J.J. Cullen Modulation of reative oxygen species in pancreatic cancer Clin. Cancer Res. 13 2007 7441 7450
26. J.J. Cullen, F.A. Mitros, and L.W. Oberley Expression of antioxidant enzymes in diseases of the human pancreas. Another link between chronic pancreatitis and pancreatic cancer Pancreas 26 2003 23 27
27. J.H. Lee, J.H. Kim, J.S. Kim, J.W. Chang, S.B. Kim, and S.K. Lee AMP-activated ptotein kinase inhibits TGF-b, angiotesion II, aldosterone, high glucose, and albumin-induced epithelial-mesenchymal transition Am. J. Physiol. Ren. Physiol. 304 2013 F666 F697
28. K. Block, and Y. Gorin Aiding and abetting roles of NOX oxidases in cellular transformation Nat. Rev. Cancer 12 2012 627 637
29. R. Higara, M. Kato, S. Miyagawa, and T. Kamata NOX4-derived ROS signaling contributes to TGF-B-induced epithelial mesenchymal transition in pancreatic cancer cells Anticancer Res. 33 2013 4431 4438
30. J.K. Lee, M. Edderkaoul, P. Hong, P. Truong, J.A. Berti, J. Pandol, and A.S. Gukovskaya NADH oxidase NOX4 mediates pancreatic cancer cell survival by activating JAK2 kinases. Involvement of LMW-PTP protein tyrosine phosphatase Pancreas 31 2005 451 452
31. K. Kisfalvi, G. Eibl, J. Sinnett-Smith, and E. Rozengurt Metformin disrupts crosstalk between G-protein-coupled receptor and insulin receptor signaling systems and inhibits pancreatic tumor growth Cancer Res. 15 2009 6539 6545
32. K. Kisfalvi, A. Moro, J. Sinnett-Smith, G. Eibl, and E. Rozengurt Metformin inhibits the growth of human pancreatic xenografts Pancreas 42 2013 781 785
33. A. Piwkowska, D. Rogacka, M. Jankowski, M.H. Dominiczak, J.K. Stepinski, and S. Angielski Metformin induces suppression of NAD(P)H oxidase activity in podocytes Biochem. Biophys. Res. Commun. 303 2010 268 273
34. J. Bai, N. Zhang, Y. Hua, B. Wang, L. Ling, A. Ferro, and B. Xu Metformin inhibits angiotensin II-induced differentiation of cardiac fibroblast into myofibroblasts Plos One 8 2013 e72120 10.1371/journal.pone.0072120
35. X. Hou, J. Song, X.-N. Li, L. Zhanh, X. Wang, L. Chen, and et al. Metformin reduces intracellar reactive oxygen species levels by upregulating expression of the antioxidant thioredoxin via AMPK-FOXO3 pathway Biochem. Biophys. Res. Commun. 396 2010 199 205
36. S.Q. Zhang, Y.T. Sun, T.H. Xu, X.F. Zhang, Y.Z. Liu, M.J. Ma, L.N. Wang, and L. Yao Protective effect of metformin on renal injury of C57BL/6J mouse treated with high fat diet Pharmazie 69 2014 904 908
37. C. Algire, O. Moiseeva, X. Deschenes-Simard, L. Amrein, L. Petruccelli, E. Birman, B. Viollet, G. Ferbeyre, and M. Pollak Metformin reduces endogenous reactive oxygen species and associated DNA damage Cancer Prev. Res. 5 2012 536 543
38. J.J. Cullen, C. Weydert, M.M. Hinkhouse, J. Ritchie, F.E. Domann, D. Spitz, and L.W. Oberley The role of manganese superoxide dismutase in growth of pancreatic adenocarcinoma Cancer Res. 63 2003 1297 1303
39. R.J. Teng, J. Du, A.J. Afolayan, A. Eis, Y. Shi, and G.G. Konduri AMPKinase activation improves angiogenesis in pulmonary artery endothelial cells with in utero pulmonary hypertension Am. J. Physiol. Lung. Cell. Mol. Physiol. 304 2013 L29 L42
40. D. Kukidome, T. Nishikawa, K. Sonoda, K. Imoto, K. Fujisawa, M. Yano, and et al. Activation of AMP-activated protein kinase reduces hyperglycemia-induced mitochondrial reactive oxygen species production and promotes mitochondrial biogenesis in human umbilical vein endothelial cells Diabetes 55 2006 120 127
41. S.K. Dhar, and S.K. St. Clair Manganese superoxide dismutase regulation and cancer Free Radic. Biol. Med. 52 2012 2209 2222
42. E.A.I. Queiroz, S. Puukila, R. Eichler, S.C. Sampaio, H.L. Forsyth, S.J. Lees, A.M. Barbosa, R.F. Dekker, Z.B. Fortes, and N. Khaper Metformin induced apoptosis and cell cycle arrest mediated by oxidative stress, AMPK, and FOXO3a in MCF-7 breast cancer cells PLoS One 9 5 2014 May 23 e98207 10.1371
43. S. Correia, C. Carvalho, M.S. Santos, T. Proenca, E. Nunes, A. Duarte, P. Monteiro, R. Seica, C.R. Oliveira, and P. Moreira Metformin protects the brain against oxidative imbalance promoted by Type 2 diabetes Med. Chem. 4 2009 358 364