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Oxidative Medicine and Cellular Longevity
Volume 2015 (2015), Article ID 183928, 10 pages
http://dx.doi.org/10.1155/2015/183928
Review Article

Type 2 Diabetes and Breast Cancer: The Interplay between Impaired Glucose Metabolism and Oxidant Stress

1San Raffaele Rome University, IRCCS San Raffaele Pisana, Research Center, Via di Val Cannuta 247, 00166 Rome, Italy
2Department of Systems Medicine, Medical Oncology, Tor Vergata Clinical Center, University of Rome Tor Vergata, Viale Oxford 81, 00133 Rome, Italy
3Department of Surgery, Division of Surgical Oncology, Tor Vergata Clinical Center, University of Rome Tor Vergata, Viale Oxford 81, 00133 Rome, Italy

Received 8 January 2015; Accepted 28 May 2015

Academic Editor: Amina El Jamali

Copyright © 2015 Patrizia Ferroni et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. International Diabetes Federation, IDF Diabetes Atlas, 6th edition, 2014, http://www.idf.org/diabetesatlas/.
  2. E. Giovannucci, D. M. Harlan, M. C. Archer et al., “Diabetes and cancer: a consensus report,” Diabetes Care, vol. 33, no. 7, pp. 1674–1685, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. C. X. Xu, H. H. Zhu, and Y. M. Zhu, “Diabetes and cancer: associations, mechanisms, and implications for medical practice,” World Journal of Diabetes, vol. 5, no. 3, pp. 372–380, 2014. View at Publisher · View at Google Scholar
  4. S. C. Larsson, C. S. Mantzoros, and A. Wolk, “Diabetes mellitus and risk of breast cancer: a meta-analysis,” International Journal of Cancer, vol. 121, no. 4, pp. 856–862, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. A. A. Onitilo, J. M. Engel, I. Glurich, R. V. Stankowski, G. M. Williams, and S. A. Doi, “Diabetes and cancer I: risk, survival, and implications for screening,” Cancer Causes and Control, vol. 23, no. 6, pp. 967–981, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. Y. Handelsman, D. Leroith, Z. T. Bloomgarden et al., “Diabetes and cancer—an AACE/ACE consensus statement,” Endocrine Practice, vol. 19, no. 4, pp. 675–693, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. E. Gouveri, N. Papanas, and E. Maltezos, “The female breast and diabetes,” The Breast, vol. 20, no. 3, pp. 205–211, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. L. Vona-Davis and D. P. Rose, “Type 2 diabetes and obesity metabolic interactions: common factors for breast cancer risk and novel approaches to prevention and therapy,” Current Diabetes Reviews, vol. 8, no. 2, pp. 116–130, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. M. G. Schrauder, P. A. Fasching, L. Häberle et al., “Diabetes and prognosis in a breast cancer cohort,” Journal of Cancer Research and Clinical Oncology, vol. 137, no. 6, pp. 975–983, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. P. J. Goodwin, M. Ennis, K. I. Pritchard et al., “Insulin- and obesity-related variables in early-stage breast cancer: correlations and time course of prognostic associations,” Journal of Clinical Oncology, vol. 30, no. 2, pp. 164–171, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. K. M. J. de Bruijn, L. R. Arends, B. E. Hansen, S. Leeflang, R. Ruiter, and C. H. J. van Eijck, “Systematic review and meta-analysis of the association between diabetes mellitus and incidence and mortality in breast and colorectal cancer,” British Journal of Surgery, vol. 100, no. 11, pp. 1421–1429, 2013. View at Publisher · View at Google Scholar · View at Scopus
  12. M. Sant, C. Allemani, M. Santaquilani, A. Knijn, F. Marchesi, and R. Capocaccia, “Survival of cancer patients diagnosed in 1995–1999. Results and commentary,” European Journal of Cancer, vol. 45, no. 6, pp. 931–991, 2009. View at Google Scholar · View at Scopus
  13. P. Minicozzi, F. Berrino, F. Sebastiani et al., “High fasting blood glucose and obesity significantly and independently increase risk of breast cancer death in hormone receptor-positive disease,” European Journal of Cancer, vol. 49, no. 18, pp. 3881–3888, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. L. A. Carey, C. M. Perou, C. A. Livasy et al., “Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study,” The Journal of the American Medical Association, vol. 295, no. 21, pp. 2492–2502, 2006. View at Publisher · View at Google Scholar · View at Scopus
  15. A. A. Memon, L. Bennet, B. Zöller et al., “Circulating human epidermal growth factor receptor 2 (HER2) is associated with hyperglycaemia and insulin resistance2 (HER2),” Journal of Diabetes, vol. 7, no. 3, pp. 369–377, 2015. View at Publisher · View at Google Scholar
  16. J. M. Fernndez-Real, J. A. Menendez, G. Frühbeck, J. M. Moreno-Navarrete, A. Vazquez-Martín, and W. Ricart, “Serum HER-2 concentration is associated with insulin resistance and decreases after weight loss,” Nutrition and Metabolism, vol. 7, article 14, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. N. Vazzana, S. Riondino, V. Toto et al., “Obesity-driven inflammation and colorectal cancer,” Current Medicinal Chemistry, vol. 19, no. 34, pp. 5837–5853, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. A. Marble, “Diabetes and cancer,” The New England Journal of Medicine, vol. 211, no. 8, pp. 339–349, 1934. View at Publisher · View at Google Scholar
  19. M. Pollak, “The insulin and insulin-like growth factor receptor family in neoplasia: an update,” Nature Reviews Cancer, vol. 12, no. 3, pp. 159–169, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. E. Orgel and S. D. Mittelman, “The links between insulin resistance, diabetes, and cancer,” Current Diabetes Reports, vol. 13, no. 2, pp. 213–222, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. H. Noto, A. Goto, T. Tsujimoto, K. Osame, and M. Noda, “Latest insights into the risk of cancer in diabetes,” Journal of Diabetes Investigation, vol. 4, no. 3, pp. 225–232, 2013. View at Publisher · View at Google Scholar · View at Scopus
  22. R. C. Baxter, “IGF binding proteins in cancer: mechanistic and clinical insights,” Nature Reviews Cancer, vol. 14, no. 5, pp. 329–341, 2014. View at Publisher · View at Google Scholar · View at Scopus
  23. P. Vigneri, F. Frasca, L. Sciacca, G. Pandini, and R. Vigneri, “Diabetes and cancer,” Endocrine-Related Cancer, vol. 16, no. 4, pp. 1103–1123, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. L. C. Richardson and L. A. Pollack, “Therapy insight: influence of type 2 diabetes on the development, treatment and outcomes of cancer,” Nature Clinical Practice Oncology, vol. 2, no. 1, pp. 48–53, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. P. Muti, T. Quattrin, B. J. B. Grant et al., “Fasting glucose is a risk factor for breast cancer: a prospective study,” Cancer Epidemiology Biomarkers and Prevention, vol. 11, no. 11, pp. 1361–1368, 2002. View at Google Scholar · View at Scopus
  26. D. A. Lawlor, G. D. Smith, and S. Ebrahim, “Hyperinsulinaemia and increased risk of breast cancer: findings from the British women's heart and health study,” Cancer Causes and Control, vol. 15, no. 3, pp. 267–275, 2004. View at Publisher · View at Google Scholar · View at Scopus
  27. M. J. Gunter, D. R. Hoover, H. Yu et al., “Insulin, insulin-like growth factor-I, and risk of breast cancer in postmenopausal women,” Journal of the National Cancer Institute, vol. 101, no. 1, pp. 48–60, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. G. Chodick and I. Zucker, “Diabetes, gestational diabetes and the risk of cancer in women: epidemiologic evidence and possible biologic mechanisms,” Women's Health, vol. 7, no. 2, pp. 227–237, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. V. Formica, M. Tesauro, C. Cardillo, and M. Roselli, “Insulinemia and the risk of breast cancer and its relapse,” Diabetes, Obesity and Metabolism, vol. 14, no. 12, pp. 1073–1080, 2012. View at Publisher · View at Google Scholar · View at Scopus
  30. K. S. Peairs, B. B. Barone, C. F. Snyder et al., “Diabetes mellitus and breast cancer outcomes: a systematic review and meta-analysis,” Journal of Clinical Oncology, vol. 29, no. 1, pp. 40–46, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. E. Weiderpass, G. Gridley, I. Persson, O. Nyrén, A. Ekbom, and H.-O. Adami, “Risk of endometrial and breast cancer in patients with diabetes mellitus,” International Journal of Cancer, vol. 71, no. 3, pp. 360–363, 1997. View at Publisher · View at Google Scholar · View at Scopus
  32. G. C. Kabat, M. Kim, B. J. Caan et al., “Repeated measures of serum glucose and insulin in relation to postmenopausal breast cancer,” International Journal of Cancer, vol. 125, no. 11, pp. 2704–2710, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. W.-W. Chen, Y.-Y. Shao, W.-Y. Shau et al., “The impact of diabetes mellitus on prognosis of early breast cancer in Asia,” The Oncologist, vol. 17, no. 4, pp. 485–491, 2012. View at Publisher · View at Google Scholar · View at Scopus
  34. D. P. Rose and L. Vona-Davis, “The cellular and molecular mechanisms by which insulin influences breast cancer risk and progression,” Endocrine-Related Cancer, vol. 19, no. 6, pp. R225–R241, 2012. View at Publisher · View at Google Scholar · View at Scopus
  35. Z. Suba, “Interplay between insulin resistance and estrogen deficiency as co-activators in carcinogenesis,” Pathology and Oncology Research, vol. 18, no. 2, pp. 123–133, 2012. View at Publisher · View at Google Scholar · View at Scopus
  36. B. Arcidiacono, S. Iiritano, A. Nocera et al., “Insulin resistance and cancer risk: an overview of the pathogenetic mechanisms,” Experimental Diabetes Research, vol. 2012, Article ID 789174, 12 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  37. M. Weichhaus, J. Broom, K. Wahle, and G. Bermano, “A novel role for insulin resistance in the connection between obesity and postmenopausal breast cancer,” International Journal of Oncology, vol. 41, no. 2, pp. 745–752, 2012. View at Publisher · View at Google Scholar · View at Scopus
  38. E. J. Gallagher and D. LeRoith, “Diabetes, antihyperglycemic medications and cancer risk: smoke or fire?” Current Opinion in Endocrinology, Diabetes and Obesity, vol. 20, no. 5, pp. 485–494, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. M. P. Cleary and M. E. Grossmann, “Minireview: obesity and breast cancer: the estrogen connection,” Endocrinology, vol. 150, no. 6, pp. 2537–2542, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. W. R. Miller, “Aromatase and the breast: regulation and clinical aspects,” Maturitas, vol. 54, no. 4, pp. 335–341, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. Y. Hawsawi, R. El-Gendy, C. Twelves, V. Speirs, and J. Beattie, “Insulin-like growth factor—oestradiol crosstalk and mammary gland tumourigenesis,” Biochimica et Biophysica Acta, vol. 1836, no. 2, pp. 345–353, 2013. View at Publisher · View at Google Scholar · View at Scopus
  42. C.-W. Lin, L.-Y. Yang, S.-C. Shen, and Y.-C. Chen, “IGF-I plus E2 induces proliferation via activation of ROS-dependent ERKs and JNKs in human breast carcinoma cells,” Journal of Cellular Physiology, vol. 212, no. 3, pp. 666–674, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. A. V. Lee, P. Zhang, M. Ivanova et al., “Developmental and hormonal signals dramatically alter the localization and abundance of insulin receptor substrate proteins in the mammary gland,” Endocrinology, vol. 144, no. 6, pp. 2683–2694, 2003. View at Publisher · View at Google Scholar · View at Scopus
  44. D. Sachdev and D. Yee, “The IGF system and breast cancer,” Endocrine-Related Cancer, vol. 8, no. 3, pp. 197–209, 2001. View at Publisher · View at Google Scholar · View at Scopus
  45. J. Á. Fresno Vara, E. Casado, J. de Castro, P. Cejas, C. Belda-Iniesta, and M. González-Barón, “P13K/Akt signalling pathway and cancer,” Cancer Treatment Reviews, vol. 30, no. 2, pp. 193–204, 2004. View at Publisher · View at Google Scholar · View at Scopus
  46. P. F. Christopoulos, P. Msaouel, and M. Koutsilieris, “The role of the insulin-like growth factor-1 system in breast cancer,” Molecular Cancer, vol. 14, no. 1, article 43, 2015. View at Publisher · View at Google Scholar
  47. Z. Y. Jiang, Z. He, B. L. King et al., “Characterization of multiple signaling pathways of insulin in the regulation of vascular endothelial growth factor expression in vascular cells and angiogenesis,” The Journal of Biological Chemistry, vol. 278, no. 34, pp. 31964–31971, 2003. View at Publisher · View at Google Scholar · View at Scopus
  48. J. Riedemann and V. M. Macaulay, “IGF1R signalling and its inhibition,” Endocrine-Related Cancer, vol. 13, supplement 1, pp. S33–S43, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. I. F. Godsland, “Insulin resistance and hyperinsulinaemia in the development and progression of cancer,” Clinical Science, vol. 118, no. 5, pp. 315–332, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. J. E. Goldberg and K. L. Schwertfeger, “Proinflammatory cytokines in breast cancer: mechanisms of action and potential targets for therapeutics,” Current Drug Targets, vol. 11, no. 9, pp. 1133–1146, 2010. View at Publisher · View at Google Scholar · View at Scopus
  51. M. Murata, M. Mizutani, S. Oikawa, Y. Hiraku, and S. Kawanishi, “Oxidative DNA damage by hyperglycemia-related aldehydes and its marked enhancement by hydrogen peroxide,” FEBS Letters, vol. 554, no. 1-2, pp. 138–142, 2003. View at Publisher · View at Google Scholar · View at Scopus
  52. P. Ferroni, S. Basili, A. Falco, and G. Davì, “Platelet activation in type 2 diabetes mellitus,” Journal of Thrombosis and Haemostasis, vol. 2, no. 8, pp. 1282–1291, 2004. View at Publisher · View at Google Scholar · View at Scopus
  53. R. Wisastra and F. Dekker, “Inflammation, cancer and oxidative lipoxygenase activity are intimately linked,” Cancers, vol. 6, no. 3, pp. 1500–1521, 2014. View at Publisher · View at Google Scholar
  54. P. Ferroni, N. Vazzana, S. Riondino, C. Cuccurullo, F. Guadagni, and G. Davì, “Platelet function in health and disease: from molecular mechanisms, redox considerations to novel therapeutic opportunities,” Antioxidants & Redox Signaling, vol. 17, no. 10, pp. 1447–1485, 2012. View at Publisher · View at Google Scholar · View at Scopus
  55. A. Likidlilid, N. Patchanans, T. Peerapatdit, and C. Sriratanasathavorn, “Lipid peroxidation and antioxidant enzyme activities in erythrocytes of type 2 diabetic patients,” Journal of the Medical Association of Thailand, vol. 93, no. 6, pp. 682–693, 2010. View at Google Scholar · View at Scopus
  56. M. Matsuda and I. Shimomura, “Increased oxidative stress in obesity: implications for metabolic syndrome, diabetes, hypertension, dyslipidemia, atherosclerosis, and cancer,” Obesity Research & Clinical Practice, vol. 7, no. 5, pp. e330–e341, 2013. View at Publisher · View at Google Scholar · View at Scopus
  57. M. Parri and P. Chiarugi, “Redox molecular machines involved in tumor progression,” Antioxidants & Redox Signaling, vol. 19, no. 15, pp. 1828–1845, 2013. View at Publisher · View at Google Scholar · View at Scopus
  58. U. Martinez-Outschoorn, F. Sotgia, and M. P. Lisanti, “Tumor microenvironment and metabolic synergy in breast cancers: critical importance of mitochondrial fuels and function,” Seminars in Oncology, vol. 41, no. 2, pp. 195–216, 2014. View at Publisher · View at Google Scholar · View at Scopus
  59. Q. Wu and X. Ni, “ROS-mediated DNA methylation pattern alterations in carcinogenesis,” Current Drug Targets, vol. 16, no. 1, pp. 13–19, 2015. View at Publisher · View at Google Scholar
  60. A. M. Korwar, H. S. Bhonsle, A. D. Chougale et al., “Analysis of AGE modified proteins and RAGE expression in HER2/neu negative invasive ductal carcinoma,” Biochemical and Biophysical Research Communications, vol. 419, no. 3, pp. 490–494, 2012. View at Publisher · View at Google Scholar · View at Scopus
  61. Y. A. Cho, M.-K. Sung, J.-Y. Yeon, J. Ro, and J. Kim, “Prognostic role of interleukin-6, interleukin-8, and leptin levels according to breast cancer subtype,” Cancer Research and Treatment, vol. 45, no. 3, pp. 210–219, 2013. View at Publisher · View at Google Scholar · View at Scopus
  62. C. A. Gilbert and J. M. Slingerland, “Cytokines, obesity, and cancer: new insights on mechanisms linking obesity to cancer risk and progression,” Annual Review of Medicine, vol. 64, pp. 45–57, 2013. View at Publisher · View at Google Scholar · View at Scopus
  63. M. M. Mohamed, E. A. El-Ghonaimy, M. A. Nouh, R. J. Schneider, B. F. Sloane, and M. El-Shinawi, “Cytokines secreted by macrophages isolated from tumor microenvironment of inflammatory breast cancer patients possess chemotactic properties,” International Journal of Biochemistry and Cell Biology, vol. 46, no. 1, pp. 138–147, 2014. View at Publisher · View at Google Scholar · View at Scopus
  64. P. Rodrigues, G. de Marco, J. Furriol et al., “Oxidative stress in susceptibility to breast cancer: study in Spanish population,” BMC Cancer, vol. 14, no. 1, article 861, 2014. View at Publisher · View at Google Scholar
  65. G. Libby, L. A. Donnelly, P. T. Donnan, D. R. Alessi, A. D. Morris, and J. M. M. Evans, “New users of metformin are at low risk of incident cancer: a cohort study among people with type 2 diabetes,” Diabetes Care, vol. 32, no. 9, pp. 1620–1625, 2009. View at Publisher · View at Google Scholar · View at Scopus
  66. C. J. Currie, C. D. Poole, and E. A. M. Gale, “The influence of glucose-lowering therapies on cancer risk in type 2 diabetes,” Diabetologia, vol. 52, no. 9, pp. 1766–1777, 2009. View at Publisher · View at Google Scholar · View at Scopus
  67. M. Bodmer, C. Meier, S. Krähenbühl, S. S. Jick, and C. R. Meier, “Long-term metformin use is associated with decreased risk of breast cancer,” Diabetes Care, vol. 33, no. 6, pp. 1304–1308, 2010. View at Publisher · View at Google Scholar · View at Scopus
  68. J. L. F. Bosco, S. Antonsen, H. T. Sørensen, L. Pedersen, and T. L. Lash, “Metformin and incident breast cancer among diabetic women: a population-based case-control study in Denmark,” Cancer Epidemiology Biomarkers and Prevention, vol. 20, no. 1, pp. 101–111, 2011. View at Publisher · View at Google Scholar · View at Scopus
  69. R. Ruiter, L. E. Visser, M. P. P. van Herk-Sukel et al., “Lower risk of cancer in patients on metformin in comparison with those on sulfonylurea derivatives: Results from a large population-based follow-up study,” Diabetes Care, vol. 35, no. 1, pp. 119–124, 2012. View at Publisher · View at Google Scholar · View at Scopus
  70. R. T. Chlebowski, A. McTiernan, J. Wactawski-Wende et al., “Diabetes, metformin, and breast cancer in postmenopausal women,” Journal of Clinical Oncology, vol. 30, no. 23, pp. 2844–2852, 2012. View at Publisher · View at Google Scholar · View at Scopus
  71. T. P. van Staa, D. Patel, A. M. Gallagher, and M. L. de Bruin, “Glucose-lowering agents and the patterns of risk for cancer: a study with the General Practice Research Database and secondary care data,” Diabetologia, vol. 55, no. 3, pp. 654–665, 2012. View at Publisher · View at Google Scholar · View at Scopus
  72. E. García-Esquinas, E. Guinó, G. Castaño-Vinyals et al., “Association of diabetes and diabetes treatment with incidence of breast cancer,” Acta Diabetologica, 2015. View at Publisher · View at Google Scholar
  73. A. DeCensi, M. Puntoni, P. Goodwin et al., “Metformin and cancer risk in diabetic patients: a systematic review and meta-analysis,” Cancer Prevention Research, vol. 3, no. 11, pp. 1451–1461, 2010. View at Publisher · View at Google Scholar · View at Scopus
  74. H. M. Colhoun and SDRN Epidemiology Group, “Use of insulin glargine and cancer incidence in Scotland: a study from the Scottish Diabetes Research Network Epidemiology Group,” Diabetologia, vol. 52, no. 9, pp. 1755–1765, 2009. View at Publisher · View at Google Scholar · View at Scopus
  75. P. Zhang, H. Li, X. Tan, L. Chen, and S. Wang, “Association of metformin use with cancer incidence and mortality: a meta-analysis,” Cancer Epidemiology, vol. 37, no. 3, pp. 207–218, 2013. View at Publisher · View at Google Scholar · View at Scopus
  76. D. Soranna, L. Scotti, A. Zambon et al., “Cancer risk associated with use of metformin and sulfonylurea in type 2 diabetes: a meta-analysis,” The Oncologist, vol. 17, no. 6, pp. 813–822, 2012. View at Publisher · View at Google Scholar · View at Scopus
  77. M. Franciosi, G. Lucisano, E. Lapice, G. F. M. Strippoli, F. Pellegrini, and A. Nicolucci, “Metformin therapy and risk of cancer in patients with type 2 diabetes: systematic review,” PLoS ONE, vol. 8, no. 8, Article ID e71583, 2013. View at Publisher · View at Google Scholar · View at Scopus
  78. N. F. Col, L. Ochs, V. Springmann, A. K. Aragaki, and R. T. Chlebowski, “Metformin and breast cancer risk: a meta-analysis and critical literature review,” Breast Cancer Research and Treatment, vol. 135, no. 3, pp. 639–646, 2012. View at Publisher · View at Google Scholar · View at Scopus
  79. I. N. Colmers, S. L. Bowker, and J. A. Johnson, “Thiazolidinedione use and cancer incidence in type 2 diabetes: a systematic review and meta-analysis,” Diabetes and Metabolism, vol. 38, no. 6, pp. 475–484, 2012. View at Publisher · View at Google Scholar · View at Scopus
  80. H. C. Lin, Y. T. Hsu, B. H. Kachingwe, C. Y. Hsu, Y. S. Uang, and L. H. Wang, “Dose effect of thiazolidinedione on cancer risk in type 2 diabetes mellitus patients: a six-year population-based cohort study,” Journal of Clinical Pharmacy and Therapeutics, vol. 39, no. 4, pp. 354–360, 2014. View at Publisher · View at Google Scholar · View at Scopus
  81. G. E. C. Sun, B. J. Wells, K. Yip et al., “Gender-specific effects of oral hypoglycaemic agents on cancer risk in type 2 diabetes mellitus,” Diabetes, Obesity and Metabolism, vol. 16, no. 3, pp. 276–283, 2014. View at Publisher · View at Google Scholar · View at Scopus
  82. C. J. Currie, C. D. Poole, and E. A. Gale, “The influence of glucose-lowering therapies on cancer risk in type 2 diabetes,” Diabetes Care, vol. 35, no. 2, pp. 299–304, 2012. View at Publisher · View at Google Scholar
  83. S. Bayraktar, L. F. Hernadez-Aya, X. Lei et al., “Effect of metformin on survival outcomes in diabetic patients with triple receptor-negative breast cancer,” Cancer, vol. 118, no. 5, pp. 1202–1211, 2012. View at Publisher · View at Google Scholar · View at Scopus
  84. X. He, F. J. Esteva, J. Ensor, G. N. Hortobagyi, M.-H. Lee, and S.-C. J. Yeung, “Metformin and thiazolidinediones are associated with improved breast cancer-specific survival of diabetic women with HER2+ breast cancer,” Annals of Oncology, vol. 23, no. 7, pp. 1771–1780, 2012. View at Publisher · View at Google Scholar · View at Scopus
  85. P. J. H. L. Peeters, M. T. Bazelier, P. Vestergaard et al., “Use of metformin and survival of diabetic women with breast cancer,” Current Drug Safety, vol. 8, no. 5, pp. 357–363, 2013. View at Publisher · View at Google Scholar · View at Scopus
  86. I. C. Lega, P. C. Austin, A. Gruneir, P. J. Goodwin, P. A. Rochon, and L. L. Lipscombe, “Association between metformin therapy and mortality after breast cancer: a population-based study,” Diabetes Care, vol. 36, no. 10, pp. 3018–3026, 2013. View at Publisher · View at Google Scholar · View at Scopus
  87. G. Hou, S. Zhang, X. Zhang, P. Wang, X. Hao, and J. Zhang, “Clinical pathological characteristics and prognostic analysis of 1,013 breast cancer patients with diabetes,” Breast Cancer Research and Treatment, vol. 137, no. 3, pp. 807–816, 2013. View at Publisher · View at Google Scholar · View at Scopus
  88. B. A. Oppong, L. A. Pharmer, S. Oskar et al., “The effect of metformin on breast cancer outcomes in patients with type 2 diabetes,” Cancer Medicine, vol. 3, no. 4, pp. 1025–1034, 2014. View at Publisher · View at Google Scholar
  89. Y. Xiao, S. Zhang, G. Hou, X. Zhang, X. Hao, and J. Zhang, “Clinical pathological characteristics and prognostic analysis of diabetic women with luminal subtype breast cancer,” Tumor Biology, vol. 35, no. 3, pp. 2035–2045, 2014. View at Publisher · View at Google Scholar · View at Scopus
  90. H. J. Kim, H. Kwon, J. W. Lee et al., “Metformin increases survival in hormone receptor-positive, Her2-positive breast cancer patients with diabetes,” Breast Cancer Research, vol. 17, no. 1, article 64, 2015. View at Publisher · View at Google Scholar
  91. P. A. Vissers, C. R. Cardwell, L. V. van de Poll-Franse, I. S. Young, F. Pouwer, and L. J. Murray, “The association between glucose-lowering drug use and mortality among breast cancer patients with type 2 diabetes,” Breast Cancer Research and Treatment, vol. 150, no. 2, pp. 427–437, 2015. View at Publisher · View at Google Scholar
  92. A. Gönenç, Y. Özkan, M. Torun, and B. Şmşek, “Plasma malondialdehyde (MDA) levels in breast and lung cancer patients,” Journal of Clinical Pharmacy and Therapeutics, vol. 26, no. 2, pp. 141–144, 2001. View at Publisher · View at Google Scholar · View at Scopus
  93. C. Panis, V. J. Victorino, A. C. S. A. Herrera et al., “Differential oxidative status and immune characterization of the early and advanced stages of human breast cancer,” Breast Cancer Research and Treatment, vol. 133, no. 3, pp. 881–888, 2012. View at Publisher · View at Google Scholar · View at Scopus
  94. A. C. Herrera, V. J. Victorino, F. C. Campos et al., “Impact of tumor removal on the systemic oxidative profile of patients with breast cancer discloses lipid peroxidation at diagnosis as a putative marker of disease recurrence,” Clinical Breast Cancer, vol. 14, no. 6, pp. 451–459, 2014. View at Publisher · View at Google Scholar
  95. M. Janghorbani, M. Dehghani, and M. Salehi-Marzijarani, “Systematic review and meta-analysis of insulin therapy and risk of cancer,” Hormones and Cancer, vol. 3, no. 4, pp. 137–146, 2012. View at Publisher · View at Google Scholar · View at Scopus
  96. A. Leone, E. Di Gennaro, F. Bruzzese, A. Avallone, and A. Budillon, “New perspective for an old antidiabetic drug: metformin as anticancer agent.,” Cancer treatment and research, vol. 159, pp. 355–376, 2014. View at Google Scholar · View at Scopus
  97. I. B. Sahra, K. Laurent, A. Loubat et al., “The antidiabetic drug metformin exerts an antitumoral effect in vitro and in vivo through a decrease of cyclin D1 level,” Oncogene, vol. 27, no. 25, pp. 3576–3586, 2008. View at Publisher · View at Google Scholar · View at Scopus
  98. E. A. I. F. Queiroz, S. Puukila, R. Eichler et al., “Metformin induces apoptosis and cell cycle arrest mediated by oxidative stress, AMPK and FOXO3a in MCF-7 breast cancer cells,” PLoS ONE, vol. 9, no. 5, Article ID e98207, 2014. View at Publisher · View at Google Scholar · View at Scopus
  99. L. M. Berstein, W. Yue, J.-P. Wang, and R. J. Santen, “Isolated and combined action of tamoxifen and metformin in wild-type, tamoxifen-resistant, and estrogen-deprived MCF-7 cells,” Breast Cancer Research & Treatment, vol. 128, no. 1, pp. 109–117, 2011. View at Publisher · View at Google Scholar · View at Scopus
  100. B. Kermode-Scott, “Meta-analysis confirms raised risk of bladder cancer from pioglitazone,” British Medical Journal, vol. 345, Article ID e4541, 2012. View at Publisher · View at Google Scholar · View at Scopus
  101. E. S. Epel and G. J. Lithgow, “Stress biology and aging mechanisms: toward understanding the deep connection between adaptation to stress and longevity,” Journals of Gerontology Series A: Biological Sciences and Medical Sciences, vol. 69, no. 1, pp. S10–S16, 2014. View at Publisher · View at Google Scholar · View at Scopus
  102. D. F. Dai, Y. A. Chiao, D. J. Marcinek, H. H. Szeto, and P. S. Rabinovitch, “Mitochondrial oxidative stress in aging and healthspan,” Longevity & Healthspan, vol. 3, no. 1, article 6, 2014. View at Publisher · View at Google Scholar