Apigenin in combination with Akt inhibition significantly enhances thyrotropin-stimulated radioiodide accumulation in thyroid cells

Thyroid

Volumn 24, Issue 5, 2014, Pages 878-887

  Lakshmanan, Aparna ^a   Doseff, Andrea I ^a   Ringel, Matthew D ^a   Saji, Motoyasu ^a   Rousset, Bernard ^b   Zhang, Xiaoli ^a   Jhiang, Sissy M ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b CENTRE DE RECHERCHE EN CANCÉROLOGIE DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; 8 [4 (1 AMINOCYCLOBUTYL)PHENYL] 9 PHENYL 1,2,4 TRIAZOLO[3,4 F][1,6]NAPHTHYRIDIN 3(2H) ONE; APIGENIN; B RAF KINASE; DIMETHYL SULFOXIDE; DORAMAPIMOD; DOXYCYCLINE; INSULIN; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN KINASE B; RADIOACTIVE IODINE; TANESPIMYCIN; THYROTROPIN; AGENTS AFFECTING WATER, MOLECULE OR ION TRANSPORT; ANTINEOPLASTIC AGENT; PROTEIN KINASE INHIBITOR; RADIOPHARMACEUTICAL AGENT; TUMOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOTINYLATION; CELL LYSATE; CELL SURFACE; CONTROLLED STUDY; DRUG ACCUMULATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STEADY STATE; THYROID CANCER; THYROID CELL; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL LINE; DIET SUPPLEMENTATION; DIET THERAPY; DRUG EFFECTS; GENETICS; HUMAN; KINETICS; METABOLISM; PATHOLOGY; RNA INTERFERENCE; THYROID GLAND; THYROID NEOPLASMS; TRANSPORT AT THE CELLULAR LEVEL; TUMOR CELL CULTURE; UPREGULATION;

ANIMALS; ANTINEOPLASTIC AGENTS; APIGENIN; BIOLOGICAL TRANSPORT; CELL LINE; DIETARY SUPPLEMENTS; HUMANS; IODINE RADIOISOTOPES; KINETICS; MEMBRANE TRANSPORT MODULATORS; MICE; NEOPLASM PROTEINS; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; RADIOPHARMACEUTICALS; RATS; RNA INTERFERENCE; THYROID GLAND; THYROID NEOPLASMS; THYROTROPIN; TUMOR CELLS, CULTURED; UP-REGULATION;

EID: 84901280921     PISSN: 10507256     EISSN: 15579077     Source Type: Journal    
DOI: 10.1089/thy.2013.0614     Document Type: Article

References (45)

1. Pacini F, Ladenson PW, Schlumberger M, Driedger A, Luster M, Kloos RT, Sherman S, Haugen B, Corone C, Molinaro E, Elisei R, Ceccarelli C, Pinchera A, Wahl RL, Leboulleux S, Ricard M, Yoo J, Busaidy NL, Delpassand E, Hanscheid H, Felbinger R, Lassmann M, Reiners C 2006 Radioiodine ablation of thyroid remnants after preparation with recombinant human thyrotropin in differentiated thyroid carcinoma: Results of an international, randomized, controlled study. J Clin Endocrinol Metab 91:926-932. (Pubitemid 43357760)
2. Molinaro E, Giani C, Agate L, Biagini A, Pieruzzi L, Bianchi F, Brozzi F, Ceccarelli C, Viola D, Piaggi P, Vitti P, Pacini F, Elisei R 2013 Patients with differentiated thyroid cancer who underwent radioiodine thyroid remnant ablation with low-Activity 131I after either recombinant human TSH or thyroid hormone therapy withdrawal showed the same outcome after a 10-year follow-up. J Clin Endocrinol Metab 98:2693-2700.
3. Vadysirisack DD, Venkateswaran A, Zhang Z, Jhiang SM 2007 MEK signaling modulates sodium iodide symporter at multiple levels and in a paradoxical manner. Endocr Relat Cancer 14:421-432. (Pubitemid 47242640)
4. Marsee DK, Venkateswaran A, Tao H, Vadysirisack D, Zhang Z, Vandre DD, Jhiang SM 2004 Inhibition of heat shock protein 90, a novel RET/PTC1-Associated protein, increases radioiodide accumulation in thyroid cells. J Biol Chem 279:43990-43997. (Pubitemid 39390707)
5. Liu YY, Zhang X, Ringel MD, Jhiang SM 2012 Modulation of sodium iodide symporter expression and function by LY294002, Akti-1/2 and Rapamycin in thyroid cells. Endocr Relat Cancer 19:291-304.
6. Liu D, Hu S, Hou P, Jiang D, Condouris S, Xing M 2007 Suppression of BRAF/MEK/MAP kinase pathway restores expression of iodide-metabolizing genes in thyroid cells expressing the V600E BRAF mutant. Clin Cancer Res 13:1341-1349. (Pubitemid 46424076)
7. 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, Fagin JA 2011 Small-molecule MAPK inhibitors restore radioiodine incorporation in mouse thyroid cancers with conditional BRAF activation. J Clin Invest 121:4700-4711.
8. Liu YY, Brandt MP, Shen DH, Kloos RT, Zhang X, Jhiang SM 2011 Single photon emission computed tomography imaging for temporal dynamics of thyroidal and salivary radionuclide accumulation in 17-Allyamino-17-demothoxygeldanamycin- Treated thyroid cancer mouse model. Endocr Relat Cancer 18:27-37.
9. Ho AL, Grewal RK, Leboeuf R, Sherman EJ, Pfister DG, Deandreis D, Pentlow KS, Zanzonico PB, Haque S, Gavane S, Ghossein RA, Ricarte-Filho JC, Dominguez JM, Shen R, Tuttle RM, Larson SM, Fagin JA 2013 Selumetinibenhanced radioiodine uptake in advanced thyroid cancer. N Engl J Med 368:623-632.
10. Mitsutake N, Knauf JA, Mitsutake S, Mesa C Jr, Zhang L, Fagin JA 2005 Conditional BRAFV600E expression induces DNA synthesis, apoptosis, dedifferentiation, and chromosomal instability in thyroid PCCL3 cells. Cancer Res 65:2465-2473.
11. Kaneshige M, Kaneshige K, Zhu X, Dace A, Garrett L, Carter TA, Kazlauskaite R, Pankratz DG, Wynshaw-Boris A, Refetoff S, Weintraub B, Willingham MC, Barlow C, Cheng S 2000 Mice with a targeted mutation in the thyroid hormone beta receptor gene exhibit impaired growth and resistance to thyroid hormone. Proc Natl Acad Sci USA 97:13209-13214.
12. Gordi T, Khamis H 2004 Simple solution to a common statistical problem: Interpreting multiple tests. Clin Ther 26:780-786. (Pubitemid 38736968)
13. Holm S 1979 A simple sequentially rejective multiple test procedure. Scand J Stat 6:65-70.
14. Costamagna E, Garcia B, Santisteban P 2004 The functional interaction between the paired domain transcription factor Pax8 and Smad3 is involved in transforming growth factor-beta repression of the sodium/iodide symporter gene. J Biol Chem 279:3439-3446. (Pubitemid 38140582)
15. Nicolussi A, D'Inzeo S, Santulli M, Colletta G, Coppa A 2003 TGF-beta control of rat thyroid follicular cells differentiation. Mol Cell Endocrinol 207:1-11. (Pubitemid 37102948)
16. Riesco-Eizaguirre G, Rodriguez I, De la Vieja A, Costamagna E, Carrasco N, Nistal M, Santisteban P 2009 The BRAFV600E oncogene induces transforming growth factor beta secretion leading to sodium iodide symporter repression and increased malignancy in thyroid cancer. Cancer Res 69:8317-8325.
17. Vasko V, Espinosa AV, Scouten W, He H, Auer H, Liyanarachchi S, Larin A, Savchenko V, Francis GL, de la Chapelle A, Saji M, Ringel MD 2007 Gene expression and functional evidence of epithelial-To-mesenchymal transition in papillary thyroid carcinoma invasion. Proc Natl Acad Sci USA 104:2803-2808. (Pubitemid 46327960)
18. Knauf JA, Sartor MA, Medvedovic M, Lundsmith E, Ryder M, Salzano M, Nikiforov YE, Giordano TJ, Ghossein RA, Fagin JA Progression of BRAF-induced thyroid cancer is associated with epithelial-mesenchymal transition requiring concomitant MAP kinase and TGFbeta signaling. Oncogene 30:3153-3162.
19. Chen W, Wu S, Zhang G, Wang W, Shi Y 2013 Effect of AKT inhibition on epithelial-mesenchymal transition and ZEB1-potentiated radiotherapy in nasopharyngeal carcinoma. Oncol Lett 6:1234-1240.
20. Chen WC, Lai YA, Lin YC, Ma JW, Huang LF, Yang NS, Ho CT, Kuo SC, Way TD 2013 Curcumin suppresses doxorubicin-induced epithelial-mesenchymal transition via the inhibition of TGF-beta and PI3K/AKT signaling pathways in triple-negative breast cancer cells. J Agric Food Chem 61:11817-11824.
21. Chen WF, Gao WD, Li QL, Zhou PH, Xu MD, Yao LQ 2013 SLIT2 inhibits cell migration in colorectal cancer through the AKT-GSK3beta signaling pathway. Int J Colorectal Dis 28:933-940.
22. Hong KO, Kim JH, Hong JS, Yoon HJ, Lee JI, Hong SP, Hong SD 2009 Inhibition of Akt activity induces the mesenchymal-To-epithelial reverting transition with restoring Ecadherin expression in KB and KOSCC-25B oral squamous cell carcinoma cells. J Exp Clin Cancer Res 28:28.
23. Qian X, Anzovino A, Kim S, Suyama K, Yao J, Hulit J, Agiostratidou G, Chandiramani N, McDaid HM, Nagi C, Cohen HW, Phillips GR, Norton L, Hazan RB 2013 Ncadherin/ FGFR promotes metastasis through epithelial-Tomesenchymal transition and stem/progenitor cell-like properties. Oncogene 2013 Aug 26 [Epub ahead of print]; DOI: 10.1038/onc.2013.310.
24. Kaur P, Shukla S, Gupta S 2008 Plant flavonoid apigenin inactivates Akt to trigger apoptosis in human prostate cancer: An in vitro and in vivo study. Carcinogenesis 29: 2210-2217.
25. Van Dross RT, Hong X, Pelling JC 2005 Inhibition of TPAinduced cyclooxygenase-2 (COX-2) expression by apigenin through downregulation of Akt signal transduction in human keratinocytes. Mol Carcinog 44:83-91. (Pubitemid 41397173)
26. Yuan WX, XiuJuan Zhao, XiaoHua Zhang, Ling Zhang, Kun Wu 2007 Inhibition of PKB/Akt activity involved in apigenin-induced apoptosis in human gastric carcinoma cells. Chinese Sci Bull 52:2226-2232.
27. Way TD, Kao MC, Lin JK 2004 Apigenin induces apoptosis through proteasomal degradation of HER2/neu in HER2/ neu-overexpressing breast cancer cells via the phosphatidylinositol 3-kinase/Akt-dependent pathway. J Biol Chem 279:4479-4489.
28. Fang J, Xia C, Cao Z, Zheng JZ, Reed E, Jiang BH 2005 Apigenin inhibits VEGF and HIF-1 expression via PI3K/ AKT/p70S6K1 and HDM2/p53 pathways. FASEB J 19: 342-353. (Pubitemid 40316522)
29. Yap TA, Yan L, Patnaik A, Fearen I, Olmos D, Papadopoulos K, Baird RD, Delgado L, Taylor A, Lupinacci L, Riisnaes R, Pope LL, Heaton SP, Thomas G, Garrett MD, Sullivan DM, de Bono JS, Tolcher AW 2011 First-in-man clinical trial of the oral pan-AKT inhibitor MK-2206 in patients with advanced solid tumors. J Clin Oncol 29:4688-4695.
30. Saito J, Kohn AD, Roth RA, Noguchi Y, Tatsumo I, Hirai A, Suzuki K, Kohn LD, Saji M, Ringel MD 2001 Regulation of FRTL-5 thyroid cell growth by phosphatidylinositol (OH) 3 kinase-dependent Akt-mediated signaling. Thyroid 11:339-351. (Pubitemid 32422626)
31. Kim SH, Kang JG, Kim CS, Ihm SH, Choi MG, Yoo HJ, Lee SJ 2013 Apigenin induces c-Myc-mediated apoptosis in FRO anaplastic thyroid carcinoma cells. Mol Cell Endocrinol 369:130-139.
32. Gonzalez-Mejia ME, Voss OH, Murnan EJ, Doseff AI 2010 Apigenin-induced apoptosis of leukemia cells is mediated by a bimodal and differentially regulated residue-specific phosphorylation of heat-shock protein-27. Cell Death Dis 1:e64.
33. Vargo MA, Voss OH, Poustka F, Cardounel AJ, Grotewold E, Doseff AI 2006 Apigenin-induced-Apoptosis is mediated by the activation of PKCdelta and caspases in leukemia cells. Biochem Pharmacol 72:681-692. (Pubitemid 44233544)
34. Kim SJ, Lee KE, Myong JP, Park JH, Jeon YK, Min HS, Park SY, Jung KC, Koo do H, Youn YK 2012 BRAF V600E mutation is associated with tumor aggressiveness in papillary thyroid cancer. World J Surg 36:310-317.
35. Mian C, Barollo S, Pennelli G, Pavan N, Rugge M, Pelizzo MR, Mazzarotto R, Casara D, Nacamulli D, Mantero F, Opocher G, Busnardo B, Girelli ME 2008 Molecular characteristics in papillary thyroid cancers (PTCs) with no 131I uptake. Clin Endocrinol (Oxf) 68:108-116. (Pubitemid 350243490)
36. Suzuki H, Willingham MC, Cheng SY 2002 Mice with a mutation in the thyroid hormone receptor beta gene spontaneously develop thyroid carcinoma: A mouse model of thyroid carcinogenesis. Thyroid 12:963-969. (Pubitemid 35404130)
37. Ying H, Suzuki H, Zhao L, Willingham MC, Meltzer P, Cheng SY 2003 Mutant thyroid hormone receptor beta represses the expression and transcriptional activity of peroxisome proliferator-Activated receptor gamma during thyroid carcinogenesis. Cancer Res 63:5274-5280. (Pubitemid 37139841)
38. Bourque S, Lemoine R, Sequeira-Legrand A, Fayolle L, Delrot S, Pugin A 2002 The elicitor cryptogein blocks glucose transport in tobacco cells. Plant Physiol 130:2177-2187. (Pubitemid 36035213)
39. Rigor RR, Damoc C, Phinney BS, Cala PM 2011 Phosphorylation and activation of the plasma membrane Na + / H+ exchanger (NHE1) during osmotic cell shrinkage. PLoS One 6:e29210.
40. Riedel C, Levy O, Carrasco N 2001 Post-Transcriptional regulation of the sodium/iodide symporter by thyrotropin. J Biol Chem 276:21458-21463.
41. Vadysirisack DD, Chen ES, Zhang Z, Tsai MD, Chang GD, Jhiang SM 2007 Identification of in vivo phosphorylation sites and their functional significance in the sodium iodide symporter. J Biol Chem 282:36820-36828.
42. Pomerance M, Abdullah HB, Kamerji S, Correze C, Blondeau JP 2000 Thyroid-stimulating hormone and cyclic AMP activate p38 mitogen-Activated protein kinase cascade. Involvement of protein kinase A, rac1, and reactive oxygen species. J Biol Chem 275:40539-40546. (Pubitemid 32064691)
43. Kogai T, Ohashi E, Jacobs MS, Sajid-Crockett S, Fisher ML, Kanamoto Y, Brent GA 2008 Retinoic acid stimulation of the sodium/iodide symporter in MCF-7 breast cancer cells is mediated by the insulin growth factor-I/ phosphatidylinositol 3-kinase and p38 mitogen-Activated protein kinase signaling pathways. J Clin Endocrinol Metab 93:1884-1892. (Pubitemid 351656534)
44. Matowe WC, Gupta S, Ginsberg J 1996 Regulation of protein kinase C isoforms in FRTL-5 thyroid cells by TSH and phorbol ester. Thyroid 6:53-58.
45. Kim SH, Kang JG, Kim CS, Ihm SH, Choi MG, Yoo HJ, Lee SJ 2013 Akt inhibition enhances the cytotoxic effect of apigenin in combination with PLX4032 in anaplastic thyroid carcinoma cells harboring BRAFV600E. J Endocrinol Invest 36:1099-1104.