Colorectal and Prostate Cancer Risk in Diabetes: Metformin, an Actor Behind the Scene
Open accessAbstract
Both diabetes and cancer are prevalent diseases whose incidence rates are increasing worldwide, especially in countries that are undergoing rapid industrialization changes. Apparently, lifestyle risk factors including diet, physical inactivity and obesity play pivotal, yet preventable, roles in the etiology of both diseases. Epidemiological studies provide strong evidence that subjects with diabetes are at significantly higher risk of developing many forms of cancer and especially solid tumors. In addition to pancreatic and breast cancer, the incidence of colorectal cancer and prostate cancer is increased in type 2 diabetes. While diabetes (type 2) and cancer share many risk factors, the biological links between the two diseases are poorly characterized. In this review, we highlight the mechanistic pathways that link diabetes to colorectal and prostate cancer and the use of Metformin, a diabetes drug, to prevent and/or treat colorectal and prostate cancer. We review the role of AMPK activation in autophagy, oxidative stress, inflammation, apoptosis, and cell cycle progression.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The link between metformin and activation of AMPK has been emphasized as the basis for the anti-proliferative effects of metformin.
“Similarly, the link between metformin and the activation of AMPK has been emphasized as the basis for the anti-proliferative effects of metformin (43).”
From A Critical Review of the Evidence That Metformin Is a Putative Anti-Aging Drug That Enhances Healthspan and Extends Lifespan (2021) · cites this paper as [43]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
1 retracted
Metformin monotherapy for type 2 diabetes mellitus
Sáenz, A., Fernandez-Esteban, I., Mataix, A. L., Segura, M. A., Figuls, M. R. I., & Moher, D. (2005) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd002966.pub3 · Cited by 304 · see citing works
RetractedRepertoires of Autophagy in the Pathogenesis of Ocular Diseases
Li, Y., Jiang, Q. L., Cao, G.-F., Yao, J., & Yan, B. (2015) · Cellular Physiology and Biochemistry · doi:10.1159/000373980 · Cited by 16,351 · see citing works
AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1
Kim, J., Kundu, M., Viollet, B., & Guan, K.-L. (2011) · Nature Cell Biology · doi:10.1038/ncb2152 · Cited by 7,227 · see citing works
Role of AMP-Activated Protein Kinase in Mechanism of Metformin Action
Zhou, G., Myers, R., Li, Y., Chen, Y., Shen, X., Fenyk-Melody, J., Wu, M., Ventre, J., Doebber, T., Fujii, N., et al. (2001) · Journal of Clinical Investigation · doi:10.1172/jci13505 · Cited by 5,652 · see citing works
Tumor suppressor p53 is a direct transcriptional activator of the human bax gene
Toshiyuki, M., & Reed, J. C. (1995) · Cell · doi:10.1016/0092-8674(95)90412-3 · Cited by 4,063 · see citing works
AMPK Phosphorylation of Raptor Mediates a Metabolic Checkpoint
Gwinn, D. M., Shackelford, D. B., Egan, D. F., Mihaylova, M. M., Mery, A., Vasquez, D. S., Turk, B. E., & Shaw, R. J. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.03.003 · Cited by 3,849 · see citing works
Watterson, K. R., Bestow, D., Gallagher, J. R., Hamilton, D. L., Ashford, F. B., Meakin, P. J., & Ashford, M. L. J. (2012) · Neurosignals · doi:10.1159/000334144 · Cited by 3,395 · see citing works
Phosphorylation of ULK1 (hATG1) by AMP-Activated Protein Kinase Connects Energy Sensing to Mitophagy
Egan, D. F., Shackelford, D. B., Mihaylova, M. M., Gelino, S., Kohnz, R. A., Mair, W., Vasquez, D. S., Joshi, A., Gwinn, D. M., Taylor, R., et al. (2011) · Science · doi:10.1126/science.1196371 · Cited by 2,600 · see citing works
Metformin and reduced risk of cancer in diabetic patients
Evans, J. M. M., Donnelly, L. A., Emslie-Smith, A. M., Alessi, D. R., & Morris, A. D. (2005) · BMJ · doi:10.1136/bmj.38415.708634.f7 · Cited by 2,388 · see citing works
OWEN, M. R., DORAN, E., & HALESTRAP, A. P. (2000) · Biochemical Journal · doi:10.1042/bj3480607 · Cited by 2,157 · see citing works
Bailey, C. J., & Turner, R. C. (1996) · New England Journal of Medicine · doi:10.1056/nejm199602293340906 · Cited by 1,726 · see citing works
Cellular and molecular mechanisms of metformin: an overview
Viollet, B., Guigas, B., Garcia, N. S., Leclerc, J., Foretz, M., & Andreelli, F. (2012) · Clinical Science · doi:10.1042/cs20110386 · Cited by 1,720 · see citing works
Protein Sensors for Membrane Sterols
Goldstein, J. L., DeBose‐Boyd, R. A., & Brown, M. S. (2006) · Cell · doi:10.1016/j.cell.2005.12.022 · Cited by 1,677 · see citing works
Structural mechanism for statin inhibition of HMG-CoA reductase
Istvan, E. S., & Deisenhofer, J. (2001) · Science · doi:10.1126/science.1059344 · Cited by 1,644 · see citing works
Kinaan, M., Ding, H., & Triggle, C. R. (2015) · Medical Principles and Practice · doi:10.1159/000381643 · Cited by 1,515 · see citing works
El-Mir, M.-Y., Nogueira, V., Fontaine, E., Avéret, N., Rigoulet, M., & Leverve, X. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.1.223 · Cited by 1,399 · see citing works
Clinical pharmacokinetics of metformin
Graham, G. G., Punt, J., Arora, M., Day, R. O., Doogue, M. P., Duong, J. K., Furlong, T. J., Greenfield, J. R., Greenup, L. C., Kirkpatrick, C. M., et al. (2011) · Clinical Pharmacokinetics · doi:10.2165/11534750-000000000-00000 · Cited by 1,318 · see citing works
Metabolic Syndrome and Risk of Cancer
Esposito, K., Chiodini, P., Colao, A. A. L., Lenzi, A., & Giugliano, D. (2012) · Diabetes Care · doi:10.2337/dc12-0336 · Cited by 1,212 · see citing works
AMPK regulates NADPH homeostasis to promote tumour cell survival during energy stress
Jeon, S.-M., Chandel, N. S., & Hay, N. (2012) · Nature · doi:10.1038/nature11066 · Cited by 1,132 · see citing works
Oral Antihyperglycemic Therapy for Type 2 Diabetes
Inzucchi, S. E. (2002) · JAMA · doi:10.1001/jama.287.3.360 · Cited by 1,057 · see citing works
Diabetes Mellitus and Risk of Colorectal Cancer: A Meta-Analysis
Larsson, S. C., Orsini, N., & Wolk, A. (2005) · JNCI: Journal of the National Cancer Institute · doi:10.1093/jnci/dji375 · Cited by 1,038 · see citing works
New Users of Metformin Are at Low Risk of Incident Cancer
Libby, G., Donnelly, L. A., Donnan, P. T., Alessi, D. R., Morris, A. D., & Evans, J. M. M. (2009) · Diabetes Care · doi:10.2337/dc08-2175 · Cited by 996 · see citing works
Effect of genetic variation in the organic cation transporter 1 (OCT1) on metformin action
Shu, Y., Sheardown, S. A., Brown, C., Owen, R., Zhang, S., Castro, R. A., Ianculescu, A. G., Lin, Y., Lo, J. C.-M., Burchard, E. G., et al. (2007) · Journal of Clinical Investigation · doi:10.1172/jci30558 · Cited by 963 · see citing works
Bowker, S. L., Majumdar, S. R., Veugelers, P., & Johnson, J. A. (2006) · Diabetes Care · doi:10.2337/diacare.29.02.06.dc05-1558 · Cited by 933 · see citing works
Buzzai, M., Jones, R. G., Amaravadi, R. K., Lum, J. J., DeBerardinis, R. J., Zhao, F., Viollet, B., & Thompson, C. B. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-4447 · Cited by 923 · see citing works
Metformin and Cancer Risk in Diabetic Patients: A Systematic Review and Meta-analysis
DeCensi, A., Puntoni, M., Goodwin, P., Cazzaniga, M., Gennari, A., Bonanni, B., & Gandini, S. (2010) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-10-0157 · Cited by 918 · see citing works
Metformin, independent of AMPK, inhibits mTORC1 in a rag GTPase-dependent manner
Kalender, A., Selvaraj, A., Kim, S. Y., Gulati, P., Brûlé, S., Viollet, B., Kemp, B. E., Bardeesy, N., Dennis, P., Schlager, J. J., et al. (2010) · Cell Metabolism · doi:10.1016/j.cmet.2010.03.014 · Cited by 889 · see citing works
Liang, J., Shao, S. H., Xu, Z.-X., Hennessy, B. T., Ding, Z., Larrea, M. D., Kondo, S., Dumont, D. J., Gutterman, J. U., Walker, C. L., et al. (2007) · Nature Cell Biology · doi:10.1038/ncb1537 · Cited by 868 · see citing works
Sahra, I. B., Laurent, K., Loubat, A., Giorgetti-Peraldi, S., Colosetti, P., Auberger, P., Tanti, J. F., Le Marchand-Brustel, Y., & Bost, F. (2008) · Oncogene · doi:10.1038/sj.onc.1211024 · Cited by 861 · see citing works
Greer, E. L., Oskoui, P. R., Banko, M. R., Maniar, J. M., Gygi, M. P., Gygi, S. P., & Brunet, A. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m705325200 · Cited by 820 · see citing works
Endo, A., Kuroda, M., & Tanzawa, K. (1976) · FEBS Letters · doi:10.1016/0014-5793(76)80996-9 · Cited by 800 · see citing works
LKB1 and AMP-activated protein kinase control of mTOR signalling and growth
Shaw, R. J. (2009) · Acta Physiologica · doi:10.1111/j.1748-1716.2009.01972.x · Cited by 644 · see citing works
Metformin: An Old But Still the Best Treatment for Type 2 Diabetes
Rojas, L. B. A., & Gomes, M. B. (2013) · Diabetology & Metabolic Syndrome · doi:10.1186/1758-5996-5-6 · Cited by 567 · see citing works
Cancer risk in diabetic patients treated with metformin: a systematic review and meta-analysis
Noto, H., Goto, A., Tsujimoto, T., & Noda, M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033411 · Cited by 566 · see citing works
Regulation of fatty acid synthesis and oxidation by the AMP-activated protein kinase
Hardie, D. G., & Pan, D. A. (2002) · Biochemical Society Transactions · doi:10.1042/bst0301064 · Cited by 561 · see citing works
Sahra, I. B., Laurent, K., Giuliano, S., Larbret, F., Ponzio, G., Gounon, P., MARCHAND‐BRUSTEL, Y. L., Giorgetti‐Peraldi, S., Cormont, M., Bertolotto, C., et al. (2010) · Cancer Research · doi:10.1158/0008-5472.can-09-2782 · Cited by 536 · see citing works
Metformin Associated With Lower Cancer Mortality in Type 2 Diabetes
Landman, G. W. D., Kleefstra, N., van Hateren, K. J. J., Groenier, K. H., Gans, R. O. B., & Bilo, H. J. G. (2010) · Diabetes Care · doi:10.2337/dc09-1380 · Cited by 502 · see citing works
A meta-analysis of diabetes mellitus and the risk of prostate cancer
Kasper, J. S., & Giovannucci, E. (2006) · Cancer Epidemiology, Biomarkers & Prevention · doi:10.1158/1055-9965.epi-06-0410 · Cited by 491 · see citing works
Lee, M.-S., Hsu, C.-C., Wahlqvist, M. L., Tsai, H.-N., Chang, Y., & Huang, Y.-C. (2011) · BMC Cancer · doi:10.1186/1471-2407-11-20 · Cited by 460 · see citing works
Anisimov, V. N., Berstein, L. M., Egormin, P. A., Piskunova, T. S., Popovich, I. G., Zabezhinski, M. A., Kovalenko, I. G., Poroshina, T. E., Semenchenko, A. V., Provinciali, M., et al. (2005) · Experimental Gerontology · doi:10.1016/j.exger.2005.07.007 · Cited by 402 · see citing works
Important role of the LKB1-AMPK pathway in suppressing tumorigenesis in PTEN-deficient mice
Huang, X., Wullschleger, S., Shpiro, N., McGuire, V. A., Sakamoto, K., Woods, Y. L., Mcburnie, W., Fleming, S., & Alessi, D. R. (2008) · Biochemical Journal · doi:10.1042/bj20080557 · Cited by 396 · see citing works
The blooming of the French lilac
Witters, L. A. (2001) · Journal of Clinical Investigation · doi:10.1172/jci14178 · Cited by 370 · see citing works
Clarke, P. R., & Hardie, D. G. (1990) · The EMBO Journal · doi:10.1002/j.1460-2075.1990.tb07420.x · Cited by 322 · see citing works
Metformin Suppresses Colorectal Aberrant Crypt Foci in a Short-term Clinical Trial
Hosono, K., Endo, H., Takahashi, H., Sugiyama, M., Sakai, E., Uchiyama, T., Suzuki, K., Iida, H., Sakamoto, Y., Yoneda, K., et al. (2010) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-10-0186 · Cited by 311 · see citing works
Batandier, C., Guigas, B., Détaille, D., El-Mir, M. Y. A., Fontaine, E. M., Rigoulet, M., & Leverve, X. M. (2006) · Journal of Bioenergetics and Biomembranes · doi:10.1007/s10863-006-9003-8 · Cited by 306 · see citing works
Aiding and abetting roles of NOX oxidases in cellular transformation
Block, K. L., & Gorin, Y. C. (2012) · Nature reviews. Cancer · doi:10.1038/nrc3339 · Cited by 301 · see citing works
LKB1 and AMPK and the cancer-metabolism link - ten years after
Hardie, D. G., & Alessi, D. R. (2013) · BMC Biology · doi:10.1186/1741-7007-11-36 · Cited by 298 · see citing works
Zakikhani, M., Dowling, R. J. O., Sonenberg, N., & Pollak, M. (2008) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-08-0081 · Cited by 294 · see citing works
Reduced Risk of Colorectal Cancer With Metformin Therapy in Patients With Type 2 Diabetes
Zhang, Z.-J., Zheng, Z., Kan, H., Song, Y., Cui, W., Zhao, G., & Kip, K. E. (2011) · Diabetes Care · doi:10.2337/dc11-0512 · Cited by 291 · see citing works
Brusselmans, K., De Schrijver, E., Verhoeven, G., & Swinnen, J. V. (2005) · Cancer Research · doi:10.1158/0008-5472.can-05-0571 · Cited by 277 · see citing works
Wright, J. L., & Stanford, J. L. (2009) · Cancer Causes & Control · doi:10.1007/s10552-009-9407-y · Cited by 276 · see citing works
Cancer Risk Associated with Use of Metformin and Sulfonylurea in Type 2 Diabetes: A Meta-Analysis
Soranna, D., Scotti, L., Zambon, A., Bosetti, C., Grassi, G. M., Catapano, A. L., Vecchia, C. L., Mancia, G., & Corrao, G. (2012) · The Oncologist · doi:10.1634/theoncologist.2011-0462 · Cited by 273 · see citing works
AMPK: A Contextual Oncogene or Tumor Suppressor?
Liang, J., & Mills, G. B. (2013) · Cancer Research · doi:10.1158/0008-5472.can-12-3876 · Cited by 254 · see citing works
Zhou, M., Li, X., & Wang, J. (2007) · Drug Metabolism and Disposition · doi:10.1124/dmd.107.015495 · Cited by 251 · see citing works
Xiang, X., Saha, A. K., Wen, R., Ruderman, N. B., & Luo, Z. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.06.133 · Cited by 250 · see citing works
Zhuang, Y., & Miskimins, W. K. (2008) · Journal of Molecular Signaling · doi:10.1186/1750-2187-3-18 · Cited by 247 · see citing works
Metformin Activates AMP Kinase through Inhibition of AMP Deaminase
Ouyang, J., Parakhia, R. A., & Ochs, R. S. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.121806 · Cited by 246 · see citing works
Igata, M., Motoshima, H., Tsuruzoe, K., Kojima, K., Matsumura, T., Kondo, T., Taguchi, T., Nakamaru, K., Yano, M., Kukidome, D., et al. (2005) · Circulation Research · doi:10.1161/01.res.0000185823.73556.06 · Cited by 244 · see citing works
Li, X., Song, J., Zhang, L., LeMaire, S. A., Hou, X., Zhang, C., Coselli, J. S., Chen, L., Wang, X. L., Zhang, Y., et al. (2009) · Diabetes · doi:10.2337/db08-1512 · Cited by 237 · see citing works
Chen, L., Xu, B., Liu, L., Luo, Y., Yin, J., Zhou, H., Chen, W., Shen, T., Han, X., & Huang, S. (2010) · Laboratory Investigation · doi:10.1038/labinvest.2010.36 · Cited by 236 · see citing works
Algire, C., Amrein, L., Zakikhani, M., Panasci, L., & Pollak, M. (2010) · Endocrine Related Cancer · doi:10.1677/erc-09-0252 · Cited by 234 · see citing works
Lower Risk of Cancer in Patients on Metformin in Comparison With Those on Sulfonylurea Derivatives
Ruiter, R., Visser, L. E., van Herk‐Sukel, M. P. P., Coebergh, J. W. W., Haak, H. R., Geelhoed-Duijvestijn, P. H. L. M., Straus, S. M. J. M., Herings, R. M. C., & Stricker, B. H. C. (2011) · Diabetes Care · doi:10.2337/dc11-0857 · Cited by 232 · see citing works
The effects of metformin on the survival of colorectal cancer patients with diabetes mellitus
Lee, J. H., Kim, T. I., Jeon, S. M., Hong, S. P., Cheon, J. H., & Kim, W. H. (2011) · International Journal of Cancer · doi:10.1002/ijc.26421 · Cited by 203 · see citing works
Deng, L., Gui, Z., Zhao, L., Wang, J., & Shen, L. (2012) · Digestive Diseases and Sciences · doi:10.1007/s10620-012-2055-1 · Cited by 202 · see citing works
Hou, X., Song, J., Li, X., Zhang, L., Wang, X., Chen, L., & Shen, Y. H. (2010) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2010.04.017 · Cited by 202 · see citing works
STOCKER, S. L., Morrissey, K. M., Yee, S. W., Castro, R. A., Xu, L., Dahlin, A., Ramirez, A. H., Roden, D. M., Wilke, R. A., McCarty, C. A., et al. (2012) · Clinical Pharmacology & Therapeutics · doi:10.1038/clpt.2012.210 · Cited by 193 · see citing works
Diabetes mellitus and risk of prostate cancer in the health professionals follow‐up study
Kasper, J. S., Liu, Y., & Giovannucci, E. L. (2008) · International Journal of Cancer · doi:10.1002/ijc.24044 · Cited by 181 · see citing works
Reactive species: A cell damaging rout assisting to chemical carcinogens
Goetz, M. E., & Luch, A. (2008) · Cancer Letters · doi:10.1016/j.canlet.2008.02.035 · Cited by 179 · see citing works
Hosono, K., Endo, H., Takahashi, H., Sugiyama, M., Uchiyama, T., Suzuki, K., Nozaki, Y., Yoneda, K., Fujita, K., Yoneda, M., et al. (2010) · Molecular Carcinogenesis · doi:10.1002/mc.20637 · Cited by 177 · see citing works
Bowker, S. L., Majumdar, S. R., Veugelers, P. J., & Johnson, J. A. (2006) · Diabetes Care · doi:10.2337/dc06-0997 · Cited by 175 · see citing works
Metformin restores endothelial function in aorta of diabetic rats
Sena, C. M., Matafome, P. N., Louro, T. M., Nunes, E., Fernandes, R., & Seiça, R. M. F. (2011) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2011.01230.x · Cited by 168 · see citing works
Metformin and Weight Loss in Obese Women with Polycystic Ovary Syndrome: Comparison of Doses
Harborne, L., Sattar, N. A., Norman, J. E., & Fleming, R. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-2283 · Cited by 166 · see citing works
Association of Diabetes With Prostate Cancer Risk in the Multiethnic Cohort
Waters, K. M., Henderson, B. E., Stram, D. O., Wan, P., Kolonel, L. N., & Haiman, C. A. (2009) · American Journal of Epidemiology · doi:10.1093/aje/kwp003 · Cited by 161 · see citing works
Kita, Y., Takamura, T., Misu, H., Ota, T., Kurita, S., Takeshita, Y., Uno, M., Nagata, N., Kato, K., Ando, H., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0043056 · Cited by 153 · see citing works
Caballero, A. E., Delgado, A., Aguilar-Salinas, C. A., Herrera, A. N., Castillo, J. L., Cabrera, T., Gomez-Perez, F. J., & Rull, J. A. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-0019 · Cited by 151 · see citing works
Garrett, C. R., Hassabo, H. M., Bhadkamkar, N. A., Wen, S., Baladandayuthapani, V., Kee, B. K., Eng, C., & Hassan, M. (2012) · British Journal of Cancer · doi:10.1038/bjc.2012.71 · Cited by 151 · see citing works
Metformin inhibits inflammatory response via AMPK-PTEN pathway in vascular smooth muscle cells
Kim, S. A., & Choi, H. C. (2012) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2012.07.165 · Cited by 149 · see citing works
Metformin induces suppression of NAD(P)H oxidase activity in podocytes
Piwkowska, A., Rogacka, D., Jankowski, M., Dominiczak, M. H., Stępiński, J., & Angielski, S. (2010) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2010.01.119 · Cited by 147 · see citing works
Structural mechanism for statin inhibition of 3-hydroxy-3-methylglutaryl coenzyme A reductase
Istvan, E. S. (2002) · American Heart Journal · doi:10.1067/mhj.2002.130300 · Cited by 142 · see citing works
Polymorphism in Human Organic Cation Transporters and Metformin Action
Takane, H., Shikata, E., Otsubo, K., Higuchi, S., & Ieiri, I. (2008) · Pharmacogenomics · doi:10.2217/14622416.9.4.415 · Cited by 140 · see citing works
Crea, F., Nobili, S., Paolicchi, E., Perrone, G., Napoli, C., Landini, I., Danesi, R., & Mini, E. (2011) · Drug Resistance Updates · doi:10.1016/j.drup.2011.08.001 · Cited by 137 · see citing works
zu Schwabedissen, H. E. M., Verstuyft, C., Kroemer, H. K., et al. (2010) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00431.2009 · Cited by 133 · see citing works
Metformin and the Incidence of Prostate Cancer in Patients with Type 2 Diabetes
Azoulay, L., Dell’Aniello, S., Gagnon, B., Pollak, M., & Suissa, S. (2011) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-10-0940 · Cited by 133 · see citing works
Abnormal DNA methylation, epigenetics, and prostate cancer
William, G. N. (2007) · Frontiers in bioscience · doi:10.2741/2385 · Cited by 128 · see citing works
Regulation of NAD(P)H oxidases by AMPK in cardiovascular systems
Song, P., & Zou, M. (2012) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2012.01.025 · Cited by 119 · see citing works
Metformin and Cancer Occurrence in Insulin-Treated Type 2 Diabetic Patients
Monami, M., Colombi, C., Balzi, D., Dicembrini, I., Giannini, S., Melani, C., Vitale, V., Romano, D., Barchielli, A., Marchionni, N., et al. (2010) · Diabetes Care · doi:10.2337/dc10-1287 · Cited by 109 · see citing works
Chen, L., Takizawa, M., Chen, E., et al. (2010) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.110.170159 · Cited by 95 · see citing works
Diet, Lifestyle, and Colorectal Cancer: Is Hyperinsulinemia the Missing Link?
Kim, Y. (2009) · Nutrition Reviews · doi:10.1111/j.1753-4887.1998.tb01765.x · Cited by 75 · see citing works
Influence of Obesity and Related Metabolic Alterations on Colorectal Cancer Risk
Aleksandrova, K., Nimptsch, K., & Pischon, T. (2012) · Current Nutrition Reports · doi:10.1007/s13668-012-0036-9 · Cited by 74 · see citing works
Metformin efficacy and safety for colorectal polyps: a double-blind randomized controlled trial
Higurashi, T., Takahashi, H., Endo, H., Hosono, K., Yamada, E., Ohkubo, H., Sakai, E., Uchiyama, T., Hata, Y., Fujisawa, N., et al. (2012) · BMC Cancer · doi:10.1186/1471-2407-12-118 · Cited by 55 · see citing works
Lee, J. H., Jeon, S. M., Hong, S. P., Cheon, J. H., Kim, T. I., & Kim, W. H. (2012) · Digestive and Liver Disease · doi:10.1016/j.dld.2012.06.007 · Cited by 54 · see citing works
Activation of AMP-Activated Protein Kinase Inhibits the Proliferation of Human Endothelial Cells
Peyton, K. J., Liu, X., Yu, Y., Yates, B., & Durante, W. (2012) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.112.194712 · Cited by 51 · see citing works
Self-citationNotarnicola, M., Messa, C., Pricci, M., et al. (2005) · PubMed · Cited by 49 · see citing works
Lee, E. K., Jeong, J. U., Chang, J. W., et al. (2012) · Nephron Experimental Nephrology · doi:10.1159/000342802 · Cited by 43 · see citing works
Soraya, H., Esfahanian, N., Shakiba, Y., Ghazi-Khansari, M., Nikbin, B., Hafezzadeh, H., Maleki‐Dizaji, N., & Garjani, A. (2012) · Europe PMC (PubMed Central) · Cited by 35 · see citing works
The Relationship between Metformin and Cancer in Patients with Type 2 Diabetes
Chung, H. H., Moon, J. S., Yoon, J. S., Lee, H. W., & Won, K. C. (2013) · Diabetes & Metabolism Journal · doi:10.4093/dmj.2013.37.2.125 · Cited by 22 · see citing works
Epigenetics and cancer, 2nd IARC meeting, Lyon, France, 6 and 7 December 2007
Lambert, M.-P., & Herceg, Z. (2008) · Molecular Oncology · doi:10.1016/j.molonc.2008.03.005 · Cited by 20 · see citing works
Herceg, Z., & 牛島, 俊. (2010) · Elsevier eBooks · Cited by 9 · see citing works
Ashokkumar, N., Pari, L., & Rao, C. A. (2006) · Archives of Physiology and Biochemistry · doi:10.1080/13813450600935339 · Cited by 8 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Mohammed, I., Hollenberg, M. D., Ding, H., & Triggle, C. R. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.718942 · Cited by 278 · see citing works
Liu, F., Yan, L., Wang, Z., Lu, Y., Chu, Y., Li, X., Liu, Y., Rui, D., Nie, S., & Xiang, H. (2017) · Oncotarget · doi:10.18632/oncotarget.13762 · Cited by 99 · see citing works
El Massry, M., Alaeddine, L. M., Ali, L., Saad, C., & Eid, A. A. (2021) · Current Medicinal Chemistry · doi:10.2174/0929867327666200908114902 · Cited by 27 · see citing works
Self-citation
- Authors
- Anwar, M. A., Kheir, W. A., Eid, S., Fares, J., Liu, X., Eid, A. H., & Eid, A. A.
- Affiliations
- Qatar University (QA)
- American University of Beirut (LB)
- Purdue University West Lafayette (US)
- Corresponding author
- Eid, Ali H.
- Venue
- Journal of Cancer
- Publisher
- Ivyspring International Publisher
- Published
- 2014
- Volume
- 5
- Issue
- 9
- Pages
- 736-744
- ISSN
- 1837-9664 (ISSN-L)
- PMC
- PMC4216797
- OpenAlex
- W2162068421
- Cited by
- 35
- References
- 99
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 1 · 2023: 3 · 2022: 2 · 2021: 5 · 2020: 2 · 2019: 1 · 2018: 2 · 2017: 3 · 2016: 5 · 2015: 7
- FWCI
- 0.47
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by-nc
- Locations
- Journal of Cancer (publishedVersion, cc-by-nc)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Qatar University QSpace (Qatar University) (submittedVersion)
- Funders
- Qatar Foundation
- Fonds National de la Recherche Luxembourg
- Qatar National Research Fund
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Lipids, and Metabolism
- Keywords
- type 2 diabetes, colorectal cancer, prostate cancer, metformin, AMPK activation, autophagy, oxidative stress, inflammation, apoptosis, cell cycle progression, cancer risk, cancer prevention
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
