Thyroid hormone suppresses cell proliferation through endoglin-mediated promotion of p21 stability

Oncogene

Volumn 32, Issue 33, 2013, Pages 3904-3914

  Lin, Y H ^a   Huang, Y H ^b   Wu, M H ^a   Wu, S M ^a   Chi, H C ^a   Liao, C J ^a   Chen, C Y ^a   Tseng, Y H ^a   Tsai, C Y ^a   Tsai, M M ^c   Lin, K H ^a  

^a CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^b CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

^c CHANG GUNG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Taiwan)

Author keywords

cell proliferation; endoglin; hepatocellular carcinoma; thyroid hormome

Indexed keywords

ENDOGLIN; LIOTHYRONINE; MESSENGER RNA; PROPIDIUM IODIDE; PROTEIN P21;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL CULTURE; CANCER GRADING; CANCER PATIENT; CELL ASSAY; CELL CYCLE PROGRESSION; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DISEASE ASSOCIATION; DOWN REGULATION; GEL MOBILITY SHIFT ASSAY; HISTOPATHOLOGY; IMMUNOBLOTTING; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL CARCINOMA; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN STABILITY; QUANTITATIVE ANALYSIS; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; THYROIDECTOMY; UBIQUITINATION; UPREGULATION;

ANTIGENS, CD; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; CYCLIN-DEPENDENT KINASE INHIBITOR P21; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; LIVER NEOPLASMS; PROTEIN STABILITY; RECEPTORS, CELL SURFACE; RECEPTORS, THYROID HORMONE; RESPONSE ELEMENTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRIIODOTHYRONINE;

EID: 84882453656     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.5     Document Type: Article

References (44)

1. Huang YH, Tsai MM, Lin KH. Thyroid hormone dependent regulation of target genes and their physiological significance. Chang Gung Med J 2008; 31: 325-334.
2. Yen PM. Physiological and molecular basis of thyroid hormone action. Physiol Rev 2001; 81: 1097-1142.
3. Cheng SY. Multiple mechanisms for regulation of the transcriptional activity of thyroid hormone receptors. Rev Endocr Metab Disord 2000; 1: 9-18.
4. Harvey CB, Williams GR. Mechanism of thyroid hormone action. Thyroid 2002; 12: 441-446.
5. Chamba A, Neuberger J, Strain A, Hopkins J, Sheppard MC, Franklyn JA. Expression and function of thyroid hormone receptor variants in normal and chronically diseased human liver. J Clin Endocrinol Metab 1996; 81: 360-367.
6. Ando S, Sarlis NJ, Krishnan J, Feng X, Refetoff S, Zhang MQ et al. Aberrant alternative splicing of thyroid hormone receptor in a TSH-secreting pituitary tumor is a mechanism for hormone resistance. Mol Endocrinol 2001; 15: 1529-1538.
7. Lin KH, Wu YH, Chen SL. Impaired interaction of mutant thyroid hormone receptors associated with human hepatocellular carcinoma with transcriptional coregulators. Endocrinology 2001; 142: 653-662.
8. Puzianowska-Kuznicka M, Krystyniak A, Madej A, Cheng SY, Nauman J. Functionally impaired TR mutants are present in thyroid papillary cancer. J Clin Endocrinol Metab 2002; 87: 1120-1128.
9. Hassan MM, Kaseb A, Li D, Patt YZ, Vauthey JN, Thomas MB et al. Association between hypothyroidism and hepatocellular carcinoma: a case-control study in the United States. Hepatology 2009; 49: 1563-1570.
10. Barbara NP, Wrana JL, Letarte M. Endoglin is an accessory protein that interacts with the signaling receptor complex of multiple members of the transforming growth factor-beta superfamily. J Biol Chem 1999; 274: 584-594.
11. Lastres P, Letamendia A, Zhang H, Rius C, Almendro N, Raab U et al. Endoglin modulates cellular responses to TGF-beta 1. J Cell Biol 1996; 133: 1109-1121.
12. Fonsatti E, Altomonte M, Nicotra MR, Natali PG, Maio M. Endoglin (CD105): a powerful therapeutic target on tumor-associated angiogenetic blood vessels. Oncogene 2003; 22: 6557-6563.
13. Liu Y, Jovanovic B, Pins M, Lee C, Bergan RC. Over expression of endoglin in human prostate cancer suppresses cell detachment, migration and invasion. Oncogene 2002; 21: 8272-8281.
14. Henry LA, Johnson DA, Sarrio D, Lee S, Quinlan PR, Crook T et al. Endoglin expression in breast tumor cells suppresses invasion and metastasis and correlates with improved clinical outcome. Oncogene 2011; 30: 1046-1058.
15. Perez-Gomez E, Villa-Morales M, Santos J, Fernandez-Piqueras J, Gamallo C, Dotor J et al. A role for endoglin as a suppressor of malignancy during mouse skin carcinogenesis. Cancer Res 2007; 67: 10268-10277.
16. Laptenko O, Beckerman R, Freulich E, Prives C. p53 binding to nucleosomes within the p21 promoter in vivo leads to nucleosome loss and transcriptional activation. Proc Natl Acad Sci USA 2011; 108: 10385-10390.
17. Aliouat-Denis CM, Dendouga N, Van den Wyngaert I, Goehlmann H, Steller U, van de Weyer I et al. p53-independent regulation of p21Waf1/Cip1 expression and senescence by Chk2. Mol Cancer Res 2005; 3: 627-634.
18. Bloom J, Amador V, Bartolini F, DeMartino G, Pagano M. Proteasome-mediated degradation of p21 via N-terminal ubiquitinylation. Cell 2003; 115: 71-82.
19. Lee H, Zeng SX, Lu H. UV Induces p21 rapid turnover independently of ubiquitin and Skp2. J Biol Chem 2006; 281: 26876-26883.
20. Cayrol C, Knibiehler M, Ducommun B. p21 binding to PCNA causes G1 and G2 cell cycle arrest in p53-deficient cells. Oncogene 1998; 16: 311-320.
21. Kagawa S, Fujiwara T, Kadowaki Y, Fukazawa T, Sok-Joo R, Roth JA et al. Overexpression of the p21 sdi1 gene induces senescence-like state in human cancer cells: implication for senescence-directed molecular therapy for cancer. Cell Death Differ 1999; 6: 765-772.
22. Gougos A, Letarte M. Primary structure of endoglin, an RGD-containing glycoprotein of human endothelial cells. J Biol Chem 1990; 265: 8361-8364.
23. Bellon T, Corbi A, Lastres P, Cales C, Cebrian M, Vera S et al. Identification and expression of two forms of the human transforming growth factor-betabinding protein endoglin with distinct cytoplasmic regions. Eur J Immunol 1993; 23: 2340-2345.
24. Chen RN, Huang YH, Yeh CT, Liao CH, Lin KH. Thyroid hormone receptors suppress pituitary tumor transforming gene 1 activity in hepatoma. Cancer Res 2008; 68: 1697-1706.
25. Gougos A, Letarte M. Biochemical characterization of the 44G4 antigen from the HOON pre-B leukemic cell line. J Immunol 1988; 141: 1934-1940.
26. Lee JY, Yu SJ, Park YG, Kim J, Sohn J. Glycogen synthase kinase 3beta phosphorylates p21WAF1/CIP1 for proteasomal degradation after UV irradiation. Mol Cell Biol 2007; 27: 3187-3198.
27. Yoo YD, Choi JY, Lee SJ, Kim JS, Min BR, Lee YI et al. TGF-beta-induced cell-cycle arrest through the p21(WAF1/CIP1)-G1 cyclin/Cdks-p130 pathway in gastric-carcinoma cells. Int J Cancer 1999; 83: 512-517.
28. Li Y, Dowbenko D, Lasky LA. AKT/PKB phosphorylation of p21Cip/WAF1 enhances protein stability of p21Cip/WAF1 and promotes cell survival. J Biol Chem 2002; 277: 11352-11361.
29. Oxmann D, Held-Feindt J, Stark AM, Hattermann K, Yoneda T, Mentlein R. Endoglin expression in metastatic breast cancer cells enhances their invasive phenotype. Oncogene 2008; 27: 3567-3575.
30. Craft CS, Romero D, Vary CP, Bergan RC. Endoglin inhibits prostate cancer motility via activation of the ALK2-Smad1 pathway. Oncogene 2007; 26: 7240-7250.
31. Yu D, Zhuang L, Sun X, Chen J, Yao Y, Meng K et al. Particular distribution and expression pattern of endoglin (CD105) in the liver of patients with hepatocellular carcinoma. BMC Cancer 2007; 7: 122.
32. Benetti A, Berenzi A, Gambarotti M, Garrafa E, Gelati M, Dessy E et al. Transforming growth factor-beta1 and CD105 promote the migration of hepatocellular carcinoma-derived endothelium. Cancer Res 2008; 68: 8626-8634.
33. Yen CC, Huang YH, Liao CY, Liao CJ, Cheng WL, Chen WJ et al. Mediation of the inhibitory effect of thyroid hormone on proliferation of hepatoma cells by transforming growth factor-beta. J Mol Endocrinol 2006; 36: 9-21.
34. Bressac B, Galvin KM, Liang TJ, Isselbacher KJ, Wands JR, Ozturk M. Abnormal structure and expression of p53 gene in human hepatocellular carcinoma. Proc Natl Acad Sci USA 1990; 87: 1973-1977.
35. Kress E, Skah S, Sirakov M, Nadjar J, Gadot N, Scoazec JY et al. Cooperation between the thyroid hormone receptor TRalpha1 and the WNT pathway in the induction of intestinal tumorigenesis. Gastroenterology 2010; 138: 1863-1874.
36. Suzuki H, Willingham MC, 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.
37. Martinez-Iglesias O, Garcia-Silva S, Tenbaum SP, Regadera J, Larcher F, Paramio JM et al. Thyroid hormone receptor beta1 acts as a potent suppressor of tumor invasiveness and metastasis. Cancer Res 2009; 69: 501-509.
38. Liao CH, Yeh CT, Huang YH, Wu SM, Chi HC, Tsai MM et al. Dickkopf 4 positively regulated by the thyroid hormone receptor suppresses cell invasion in human hepatoma cells. Hepatology 2012; 55: 910-920.
39. Wu SM, Huang YH, Yeh CT, Tsai MM, Liao CH, Cheng WL et al. Cathepsin H regulated by the thyroid hormone receptors associate with tumor invasion in human hepatoma cells. Oncogene 2011; 30: 2057-2069.
40. Liao CJ, Wu TI, Huang YH, Chang TC, Wang CS, Tsai MM et al. Glucose-regulated protein 58 modulates cell invasiveness and serves as a prognostic marker for cervical cancer. Cancer Sci 2011; 102: 2255-2263.
41. Liao CH, Yeh SC, Huang YH, Chen RN, Tsai MM, Chen WJ et al. Positive regulation of spondin 2 by thyroid hormone is associated with cell migration and invasion. Endocr Relat Cancer 2010; 17: 99-111.
42. Lin KH, Shieh HY, Hsu HC. Negative regulation of the antimetastatic gene Nm23-H1 by thyroid hormone receptors. Endocrinology 2000; 141: 2540-2547.
43. Chen RN, Huang YH, Lin YC, Yeh CT, Liang Y, Chen SL et al. Thyroid hormone promotes cell invasion through activation of furin expression in human hepatoma cell lines. Endocrinology 2008; 149: 3817-3831.
44. He TC, Zhou S, da Costa LT, Yu J, Kinzler KW, Vogelstein B. A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci USA 1998; 95: 2509-2514.