Metformin blocks progression of obesity-activated thyroid cancer in a mouse model

Oncotarget

Volumn 7, Issue 23, 2016, Pages 34832-34844

  Park, Jeongwon ^a   Kim, Won Gu ^a,b   Zhao, Li ^a   Enomoto, Keisuke ^a   Willingham, Mark ^a   Cheng, Sheue Yann ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b University of Ulsan College of Medicine   (South Korea)

Author keywords

Metformin; Mouse models; Obesity; Thyroid carcinogenesis

Indexed keywords

FIBRONECTIN; INTEGRIN; METFORMIN; MITOGEN ACTIVATED PROTEIN KINASE; STAT3 PROTEIN; VIMENTIN; ANTINEOPLASTIC AGENT; STAT3 PROTEIN, MOUSE;

ANAPLASTIC CARCINOMA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER GROWTH; CANCER INHIBITION; CANCER RISK; CANCER SURVIVAL; CELL DEDIFFERENTIATION; CONTROLLED STUDY; DISEASE ASSOCIATION; DRUG MECHANISM; MOUSE; NONHUMAN; OBESITY; SIGNAL TRANSDUCTION; SURVIVAL TIME; THYROID CANCER; TUMOR INVASION; ADENOCARCINOMA; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL PROLIFERATION; DISEASE MODEL; DRUG EFFECTS; LIPID DIET; PATHOLOGY; THYROID GLAND; THYROID TUMOR; TRANSGENIC MOUSE;

ADENOCARCINOMA, FOLLICULAR; ANAPLASIA; ANIMALS; ANTINEOPLASTIC AGENTS; CELL PROLIFERATION; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FIBRONECTINS; METFORMIN; MICE; MICE, TRANSGENIC; NEOPLASM INVASIVENESS; OBESITY; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; THYROID GLAND; THYROID NEOPLASMS; VIMENTIN;

EID: 84973642050     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.8989     Document Type: Article

References (55)

1. Sipos JA and Mazzaferri EL. Thyroid cancer epidemiology and prognostic variables. Clinical oncology. 2010; 22:395-404.
2. Jemal A, Bray F, Center MM, Ferlay J, Ward E and Forman D. Global cancer statistics. CA. 2011; 61:69-90.
3. Aschebrook-Kilfoy B, Sabra MM, Brenner A, Moore SC, Ron E, Schatzkin A, Hollenbeck A and Ward MH. Diabetes and thyroid cancer risk in the National Institutes of Health-AARP Diet and Health Study. Thyroid. 2011; 21:957-963.
4. Kitahara CM, Platz EA, Freeman LE, Hsing AW, Linet MS, Park Y, Schairer C, Schatzkin A, Shikany JM and Berrington de Gonzalez A. Obesity and thyroid cancer risk among U.S. men and women: a pooled analysis of five prospective studies. Cancer epidemiology, biomarkers & prevention. 2011; 20:464-472.
5. Pappa T and Alevizaki M. Obesity and thyroid cancer: a clinical update. Thyroid. 2014; 24:190-199.
6. Zhao ZG, Guo XG, Ba CX, Wang W, Yang YY, Wang J and Cao HY. Overweight, obesity and thyroid cancer risk: a meta-analysis of cohort studies. The Journal of international medical research. 2012; 40:2041-2050.
7. Kim HJ, Kim NK, Choi JH, Sohn SY, Kim SW, Jin SM, Jang HW, Suh S, Min YK, Chung JH and Kim SW. Associations between body mass index and clinicopathological characteristics of papillary thyroid cancer. Clinical endocrinology. 2013; 78:134-140.
8. Guigon CJ, Zhao L, Willingham MC and Cheng SY. PTEN deficiency accelerates tumour progression in a mouse model of thyroid cancer. Oncogene. 2009; 28:509-517.
9. Kim WG, Park JW, Willingham MC and Cheng SY. Dietinduced obesity increases tumor growth and promotes anaplastic change in thyroid cancer in a mouse model. Endocrinology. 2013; 154:2936-2947.
10. Park JW, Han CR, Zhao L, Willingham MC and Cheng SY. Inhibition of STAT3 activity delays obesity-induced thyroid carcinogenesis in a mouse model. Endocrine-related cancer. 2016; 23:53-63.
11. Pierotti MA, Berrino F, Gariboldi M, Melani C, Mogavero A, Negri T, Pasanisi P and Pilotti S. Targeting metabolism for cancer treatment and prevention: metformin, an old drug with multi-faceted effects. Oncogene. 2013; 32:1475-1487.
12. Crandall JP, Knowler WC, Kahn SE, Marrero D, Florez JC, Bray GA, Haffner SM, Hoskin M, Nathan DM and Diabetes Prevention Program Research G. The prevention of type 2 diabetes. Nature clinical practice Endocrinology & metabolism. 2008; 4:382-393.
13. Giovannucci E, Harlan DM, Archer MC, Bergenstal RM, Gapstur SM, Habel LA, Pollak M, Regensteiner JG and Yee D. Diabetes and cancer: a consensus report. Diabetes care. 2010; 33:1674-1685.
14. Anisimov VN. Metformin and rapamycin are master-keys for understanding the relationship between cell senescent, aging and cancer. Aging (Albany, NY). 2013; 5:337-338. doi: 10.18632/aging.100561.
15. Moiseeva O, Deschenes-Simard X, Pollak M and Ferbeyre G. Metformin, aging and cancer. Aging (Albany, NY) . 2013; 5:330-331. doi: 10.18632/aging.100556.
16. Berstein LM. Metformin in obesity, cancer and aging: addressing controversies. Aging (Albany, NY). 2012; 4:320-329. doi: 10.18632/aging.100455.
17. Leontieva OV, Paszkiewicz GM and Blagosklonny MV. Comparison of rapamycin schedules in mice on high-fat diet. Cell Cycle. 2014; 13:3350-3356.
18. Leontieva OV, Paszkiewicz GM and Blagosklonny MV. Weekly administration of rapamycin improves survival and biomarkers in obese male mice on high-fat diet. Aging cell. 2014; 13:616-622.
19. Blagosklonny MV. Common drugs and treatments for cancer and age-related diseases: revitalizing answers to NCI's provocative questions. Oncotarget. 2012; 3:1711-1724. doi: 10.18632/aging.890.
20. Bo S, Benso A, Durazzo M and Ghigo E. Does use of metformin protect against cancer in Type 2 diabetes mellitus? Journal of endocrinological investigation. 2012; 35:231-235.
21. Franciosi M, Lucisano G, Lapice E, Strippoli GF, Pellegrini F and Nicolucci A. Metformin therapy and risk of cancer in patients with type 2 diabetes: systematic review. PloS one. 2013; 8:e71583.
22. Becker C, Jick SS, Meier CR and Bodmer M. No evidence for a decreased risk of thyroid cancer in association with use of metformin or other antidiabetic drugs: a case-control study. BMC cancer. 2015; 15:719.
23. Bosco JL, Antonsen S, Sorensen HT, Pedersen L and Lash TL. Metformin and incident breast cancer among diabetic women: a population-based case-control study in Denmark. Cancer epidemiology, biomarkers & prevention. 2011; 20:101-111.
24. Donadon V, Balbi M, Mas MD, Casarin P and Zanette G. Metformin and reduced risk of hepatocellular carcinoma in diabetic patients with chronic liver disease. Liver international. 2010; 30:750-758.
25. Klubo-Gwiezdzinska J, Costello J, Jr., Patel A, Bauer A, Jensen K, Mete M, Burman KD, Wartofsky L and Vasko V. Treatment with metformin is associated with higher remission rate in diabetic patients with thyroid cancer. The Journal of clinical endocrinology and metabolism. 2013; 98:3269-3279.
26. Chen G, Xu S, Renko K and Derwahl M. Metformin inhibits growth of thyroid carcinoma cells, suppresses selfrenewal of derived cancer stem cells, and potentiates the effect of chemotherapeutic agents. The Journal of clinical endocrinology and metabolism. 2012; 97:E510-520.
27. Klubo-Gwiezdzinska J, Jensen K, Costello J, Patel A, Hoperia V, Bauer A, Burman KD, Wartofsky L and Vasko V. Metformin inhibits growth and decreases resistance to anoikis in medullary thyroid cancer cells. Endocrine-related cancer. 2012; 19:447-456.
28. Li Z, Shen J, Wu WK, Yu X, Liang J, Qiu G and Liu J. Leptin induces cyclin D1 expression and proliferation of human nucleus pulposus cells via JAK/STAT, PI3K/Akt and MEK/ERK pathways. PloS one. 2012; 7:e53176.
29. Wu Y, Diab I, Zhang X, Izmailova ES and Zehner ZE. Stat3 enhances vimentin gene expression by binding to the antisilencer element and interacting with the repressor protein, ZBP-89. Oncogene. 2004; 23:168-178.
30. Xiong H, Hong J, Du W, Lin YW, Ren LL, Wang YC, Su WY, Wang JL, Cui Y, Wang ZH and Fang JY. Roles of STAT3 and ZEB1 proteins in E-cadherin down-regulation and human colorectal cancer epithelial-mesenchymal transition. The Journal of biological chemistry. 2012; 287:5819-5832.
31. Virtakoivu R, Mai A, Mattila E, De Franceschi N, Imanishi SY, Corthals G, Kaukonen R, Saari M, Cheng F, Torvaldson E, Kosma VM, Mannermaa A, Muharram G, Gilles C, Eriksson J, Soini Y, et al. Vimentin-ERK Signaling Uncouples Slug Gene Regulatory Function. Cancer research. 2015; 75:2349-2362.
32. Perlson E, Michaelevski I, Kowalsman N, Ben-Yaakov K, Shaked M, Seger R, Eisenstein M and Fainzilber M. Vimentin binding to phosphorylated Erk sterically hinders enzymatic dephosphorylation of the kinase. Journal of molecular biology. 2006; 364:938-944.
33. Pankov R and Yamada KM. Fibronectin at a glance. Journal of cell science. 2002; 115:3861-3863.
34. Guan X. Cancer metastases: challenges and opportunities. Acta pharmaceutica Sinica B. 2015; 5:402-418.
35. Karnevi E, Andersson R and Rosendahl AH. Tumoureducated macrophages display a mixed polarisation and enhance pancreatic cancer cell invasion. Immunology and cell biology. 2014; 92:543-552.
36. Jang EK, Kim WG, Kwon H, Choi YM, Jeon MJ, Kim TY, Shong YK, Kim WB and Kim EY. Metformin Is Associated with a Favorable Outcome in Diabetic Patients with Cervical Lymph Node Metastasis of Differentiated Thyroid Cancer. European thyroid journal. 2015; 4:181-188.
37. Duquette M, Sadow PM, Lawler J and Nucera C. Thrombospondin-1 Silencing Down-Regulates Integrin Expression Levels in Human Anaplastic Thyroid Cancer Cells with BRAF(V600E): New Insights in the Host Tissue Adaptation and Homeostasis of Tumor Microenvironment. Frontiers in endocrinology. 2013; 4:189.
38. Kim SK, Kim DK, Oh IH, Song JY, Kwon KH, Choe BK and Kim YH. A missense polymorphism (rs11895564, Ala380Thr) of integrin alpha 6 is associated with the development and progression of papillary thyroid carcinoma in Korean population. Journal of the Korean Surgical Society. 2011; 81:308-315.
39. Zaafar DK, Zaitone SA and Moustafa YM. Role of metformin in suppressing 1,2-dimethylhydrazine-induced colon cancer in diabetic and non-diabetic mice: effect on tumor angiogenesis and cell proliferation. PloS one. 2014; 9:e100562.
40. Wang J, Li G, Wang Y, Tang S, Sun X, Feng X, Li Y, Bao G, Li P, Mao X, Wang M and Liu P. Suppression of tumor angiogenesis by metformin treatment via a mechanism linked to targeting of HER2/HIF-1alpha/VEGF secretion axis. Oncotarget. 2015; 6:44579-44592. doi: 10.18632/oncotarget.6373.
41. Orecchioni S, Reggiani F, Talarico G, Mancuso P, Calleri A, Gregato G, Labanca V, Noonan DM, Dallaglio K, Albini A and Bertolini F. The biguanides metformin and phenformin inhibit angiogenesis, local and metastatic growth of breast cancer by targeting both neoplastic and microenvironment cells. International journal of cancer. 2015; 136:E534-544.
42. Gao S, Jiang J, Li P, Song H, Wang W, Li C and Kong D. Attenuating tumour angiogenesis: a preventive role of metformin against breast cancer. BioMed research international. 2015; 2015:592523.
43. Shaw RJ, Lamia KA, Vasquez D, Koo SH, Bardeesy N, Depinho RA, Montminy M and Cantley LC. The kinase LKB1 mediates glucose homeostasis in liver and therapeutic effects of metformin. Science. 2005; 310:1642-1646.
44. Zhou G, Myers R, Li Y, Chen Y, Shen X, Fenyk-Melody J, Wu M, Ventre J, Doebber T, Fujii N, Musi N, Hirshman MF, Goodyear LJ and Moller DE. Role of AMP-activated protein kinase in mechanism of metformin action. The Journal of clinical investigation. 2001; 108:1167-1174.
45. Dasgupta B and Chhipa RR. Evolving Lessons on the Complex Role of AMPK in Normal Physiology and Cancer. Trends in pharmacological sciences. 2015.
46. Yecies JL, Zhang HH, Menon S, Liu S, Yecies D, Lipovsky AI, Gorgun C, Kwiatkowski DJ, Hotamisligil GS, Lee CH and Manning BD. Akt stimulates hepatic SREBP1c and lipogenesis through parallel mTORC1-dependent and independent pathways. Cell metabolism. 2011; 14:21-32.
47. Buzzai M, Jones RG, Amaravadi RK, Lum JJ, DeBerardinis RJ, Zhao F, Viollet B and Thompson CB. Systemic treatment with the antidiabetic drug metformin selectively impairs p53-deficient tumor cell growth. Cancer research. 2007; 67:6745-6752.
48. Birsoy K, Possemato R, Lorbeer FK, Bayraktar EC, Thiru P, Yucel B, Wang T, Chen WW, Clish CB and Sabatini DM. Metabolic determinants of cancer cell sensitivity to glucose limitation and biguanides. Nature. 2014; 508:108-112.
49. Suzuki H, Willingham MC and Cheng SY. Mice with a mutation in the thyroid hormone receptor beta gene spontaneously develop thyroid carcinoma: a mouse model of thyroid carcinogenesis. Thyroid. 2002; 12:963-969.
50. Zhu X, Zhao L, Park JW, Willingham MC and Cheng SY. Synergistic signaling of KRAS and thyroid hormone receptor beta mutants promotes undifferentiated thyroid cancer through MYC up-regulation. Neoplasia. 2014; 16:757-769.
51. Sponziello M, Lavarone E, Pegolo E, Di Loreto C, Puppin C, Russo MA, Bruno R, Filetti S, Durante C, Russo D, Di Cristofano A and Damante G. Molecular differences between human thyroid follicular adenoma and carcinoma revealed by analysis of a murine model of thyroid cancer. Endocrinology. 2013; 154:3043-3053.
52. Antico-Arciuch VG, Dima M, Liao XH, Refetoff S and Di Cristofano A. Cross-talk between PI3K and estrogen in the mouse thyroid predisposes to the development of follicular carcinomas with a higher incidence in females. Oncogene. 2010; 29:5678-5686.
53. Chakravarty D, Santos E, Ryder M, Knauf JA, Liao XH, West BL, Bollag G, Kolesnick R, Thin TH, Rosen N, Zanzonico P, Larson SM, Refetoff S, Ghossein R and Fagin JA. Small-molecule MAPK inhibitors restore radioiodine incorporation in mouse thyroid cancers with conditional BRAF activation. The Journal of clinical investigation. 2011; 121:4700-4711.
54. Franco AT, Malaguarnera R, Refetoff S, Liao XH, Lundsmith E, Kimura S, Pritchard C, Marais R, Davies TF, Weinstein LS, Chen M, Rosen N, Ghossein R, Knauf JA and Fagin JA. Thyrotrophin receptor signaling dependence of Braf-induced thyroid tumor initiation in mice. Proceedings of the National Academy of Sciences of the United States of America. 2011; 108:1615-1620.
55. Anisimov VN, Egormin PA, Piskunova TS, Popovich IG, Tyndyk ML, Yurova MN, Zabezhinski MA, Anikin IV, Karkach AS and Romanyukha AA. Metformin extends life span of HER-2/neu transgenic mice and in combination with melatonin inhibits growth of transplantable tumors in vivo. Cell cycle. 2010; 9:188-197.