Thioredoxin interacting protein (TXNIP) is a novel tumor suppressor in thyroid cancer

Molecular Cancer

Volumn 13, Issue 1, 2014, Pages

  Morrison, Jennifer A ^a   Pike, Laura A ^a   Sams, Sharon B ^b   Sharma, Vibha ^a   Zhou, Qiong ^c   Severson, Jill J ^a   Tan, Aik Choon ^b   Wood, William M ^a   Haugen, Bryan R ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF COLORADO CANCER CENTER   (United States)

^c UNIVERSITY OF COLORADO   (United States)

Author keywords

Orthotopic model; PPAR ; Thioredoxin interacting protein; Thyroid cancer; Tumor suppressor; TXNIP

Indexed keywords

PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; REACTIVE OXYGEN METABOLITE; THIOREDOXIN INTERACTING PROTEIN;

ANAPLASTIC THYROID CANCER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CELL INVASION; CELL PROLIFERATION; CONTROLLED STUDY; DIFFERENTIATED THYROID CANCER; DOWN REGULATION; GENE EXPRESSION; GENETIC TRANSDUCTION; GLUCOSE TRANSPORT; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; POORLY DIFFERENTIATED THYROID CANCER; PROMOTER REGION; PROTEIN DEPLETION; THYROID CANCER CELL LINE; TUMOR SUPPRESSOR GENE; UPREGULATION;

ANIMALS; BLOTTING, WESTERN; CARRIER PROTEINS; CELL LINE, TUMOR; GENES, TUMOR SUPPRESSOR; HETEROGRAFTS; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; THYROID NEOPLASMS; TRANSDUCTION, GENETIC;

EID: 84899506046     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-13-62     Document Type: Article

References (52)

1. Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA Cancer J Clin 2014, 64:9-29. 10.3322/caac.21208, 24399786.
2. Grant CS, Thompson G. Anaplastic thyroid carcinoma: hope on the horizon?. Surgery 2011, 150:1220-1221. 10.1016/j.surg.2011.10.006, 22136843.
3. Smallridge RC, Copland JA. Anaplastic thyroid carcinoma: pathogenesis and emerging therapies. Clin Oncol (R Coll Radiol) 2010, 22:486-497. 10.1016/j.clon.2010.03.013, 3905320, 20418080.
4. Wood WM, Sharma V, Bauerle KT, Pike LA, Zhou Q, Fretwell DL, Schweppe RE, Haugen BR. PPARgamma Promotes Growth and Invasion of Thyroid Cancer Cells. PPAR Res 2011, 2011:171765. 3236353, 22194735.
5. Parikh H, Carlsson E, Chutkow WA, Johansson LE, Storgaard H, Poulsen P, Saxena R, Ladd C, Schulze PC, Mazzini MJ, Jensen CB, Krook A, Bjornholm M, Tonqvist H, Zierath JR, Ridderstrale M, Altshuler D, Lee RT, Vaag A, Groop LC, Mootha VK. TXNIP regulates peripheral glucose metabolism in humans. PLoS Med 2007, 4:e158. 10.1371/journal.pmed.0040158, 1858708, 17472435.
6. Jin HO, Seo SK, Kim YS, Woo SH, Lee KH, Yi JY, Lee SJ, Choe TB, Lee JH, An S, Hong SI, Park IC. TXNIP potentiates Redd1-induced mTOR suppression through stabilization of Redd1. Oncogene 2011, 30:3792-3801. 10.1038/onc.2011.102, 21460850.
7. Patwari P, Chutkow WA, Cummings K, Verstraeten VL, Lammerding J, Schreiter ER, Lee RT. Thioredoxin-independent regulation of metabolism by the alpha-arrestin proteins. J Biol Chem 2009, 284:24996-25003. 10.1074/jbc.M109.018093, 2757204, 19605364.
8. Han SH, Jeon JH, Ju HR, Jung U, Kim KY, Yoo HS, Lee YH, Song KS, Hwang HM, Na YS, Yang Y, Lee KN, Choi I. VDUP1 upregulated by TGF-beta1 and 1,25-dihydorxyvitamin D3 inhibits tumor cell growth by blocking cell-cycle progression. Oncogene 2003, 22:4035-4046. 10.1038/sj.onc.1206610, 12821938.
9. Jeon JH, Lee KN, Hwang CY, Kwon KS, You KH, Choi I. Tumor suppressor VDUP1 increases p27(kip1) stability by inhibiting JAB1. Cancer Res 2005, 65:4485-4489. 10.1158/0008-5472.CAN-04-2271, 15930262.
10. Elgort MG, O'Shea JM, Jiang Y, Ayer DE. Transcriptional and Translational Downregulation of Thioredoxin Interacting Protein Is Required for Metabolic Reprogramming during G(1). Genes Cancer 2010, 1:893-907. 10.1177/1947601910389604, 3092257, 21779470.
11. Chutkow WA, Patwari P, Yoshioka J, Lee RT. Thioredoxin-interacting protein (Txnip) is a critical regulator of hepatic glucose production. J Biol Chem 2008, 283:2397-2406. 10.1074/jbc.M708169200, 17998203.
12. Patwari P, Higgins LJ, Chutkow WA, Yoshioka J, Lee RT. The interaction of thioredoxin with Txnip. Evidence for formation of a mixed disulfide by disulfide exchange. J Biol Chem 2006, 281:21884-21891. 10.1074/jbc.M600427200, 1609191, 16766796.
13. Junn E, Han SH, Im JY, Yang Y, Cho EW, Um HD, Kim DK, Lee KW, Han PL, Rhee SG, Choi I. Vitamin D3 up-regulated protein 1 mediates oxidative stress via suppressing the thioredoxin function. J Immunol 2000, 164:6287-6295.
14. Nishiyama A, Matsui M, Iwata S, Hirota K, Masutani H, Nakamura H, Takagi Y, Sono H, Gon Y, Yodoi J. Identification of thioredoxin-binding protein-2/vitamin D(3) up-regulated protein 1 as a negative regulator of thioredoxin function and expression. J Biol Chem 1999, 274:21645-21650. 10.1074/jbc.274.31.21645, 10419473.
15. Dunn LL, Buckle AM, Cooke JP, Ng MK. The emerging role of the thioredoxin system in angiogenesis. Arterioscler Thromb Vasc Biol 2010, 30:2089-2098. 10.1161/ATVBAHA.110.209643, 3142174, 20798378.
16. Liu Y, Min W. Thioredoxin promotes ASK1 ubiquitination and degradation to inhibit ASK1-mediated apoptosis in a redox activity-independent manner. Circ Res 2002, 90:1259-1266. 10.1161/01.RES.0000022160.64355.62, 12089063.
17. Saitoh M, Nishitoh H, Fujii M, Takeda K, Tobiume K, Sawada Y, Kawabata M, Miyazono K, Ichijo H. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J 1998, 17:2596-2606. 10.1093/emboj/17.9.2596, 1170601, 9564042.
18. Welsh SJ, Bellamy WT, Briehl MM, Powis G. The redox protein thioredoxin-1 (Trx-1) increases hypoxia-inducible factor 1alpha protein expression: Trx-1 overexpression results in increased vascular endothelial growth factor production and enhanced tumor angiogenesis. Cancer Res 2002, 62:5089-5095.
19. Farina AR, Tacconelli A, Cappabianca L, Masciulli MP, Holmgren A, Beckett GJ, Gulino A, Mackay AR. Thioredoxin alters the matrix metalloproteinase/tissue inhibitors of metalloproteinase balance and stimulates human SK-N-SH neuroblastoma cell invasion. Eur J Biochem 2001, 268:405-413. 10.1046/j.1432-1033.2001.01892.x, 11168376.
20. Oh JH, Chung AS, Steinbrenner H, Sies H, Brenneisen P. Thioredoxin secreted upon ultraviolet A irradiation modulates activities of matrix metalloproteinase-2 and tissue inhibitor of metalloproteinase-2 in human dermal fibroblasts. Arch Biochem Biophys 2004, 423:218-226. 10.1016/j.abb.2003.12.026, 14871484.
21. Zhou J, Yu Q, Chng WJ. TXNIP (VDUP-1, TBP-2): a major redox regulator commonly suppressed in cancer by epigenetic mechanisms. Int J Biochem Cell Biol 2011, 43:1668-1673. 10.1016/j.biocel.2011.09.005, 21964212.
22. Kwon HJ, Won YS, Nam KT, Yoon YD, Jee H, Yoon WK, Nam KH, Kang JS, Han SU, Choi IP, Kim DY, Kim HC. Vitamin D(3) upregulated protein 1 deficiency promotes N-methyl-N-nitrosourea and Helicobacter pylori-induced gastric carcinogenesis in mice. Gut 2012, 61:53-63. 10.1136/gutjnl-2011-300361, 21917648.
23. Shin D, Jeon JH, Jeong M, Suh HW, Kim S, Kim HC, Moon OS, Kim YS, Chung JW, Yoon SR, Kim WH, Choi I. VDUP1 mediates nuclear export of HIF1alpha via CRM1-dependent pathway. Biochim Biophys Acta 2008, 1783:838-848. 10.1016/j.bbamcr.2007.10.012, 18062927.
24. Nishizawa K, Nishiyama H, Matsui Y, Kobayashi T, Saito R, Kotani H, Masutani H, Oishi S, Toda Y, Fujii N, Yodoi J, Ogawa O. Thioredoxin-interacting protein suppresses bladder carcinogenesis. Carcinogenesis 2011, 32:1459-1466. 10.1093/carcin/bgr137, 21771725.
25. Sheth SS, Bodnar JS, Ghazalpour A, Thipphavong CK, Tsutsumi S, Tward AD, Demant P, Kodama T, Aburatani H, Lusis AJ. Hepatocellular carcinoma in Txnip-deficient mice. Oncogene 2006, 25:3528-3536. 10.1038/sj.onc.1209394, 16607285.
26. Shin KH, Kim RH, Kang MK, Park NH. hnRNP G elicits tumor-suppressive activity in part by upregulating the expression of Txnip. Biochem Biophys Res Commun 2008, 372:880-885. 10.1016/j.bbrc.2008.05.175, 2519094, 18541147.
27. Goldberg SF, Miele ME, Hatta N, Takata M, Paquette-Straub C, Freedman LP, Welch DR. Melanoma metastasis suppression by chromosome 6: evidence for a pathway regulated by CRSP3 and TXNIP. Cancer Res 2003, 63:432-440.
28. Kwon HJ, Won YS, Suh HW, Jeon JH, Shao Y, Yoon SR, Chung JW, Kim TD, Kim HM, Nam KH, Yoon WK, Kim DG, Kim JH, Kim YS, Kim DY, Kim HC, Choi I. Vitamin D3 upregulated protein 1 suppresses TNF-alpha-induced NF-kappaB activation in hepatocarcinogenesis. J Immunol 2010, 185:3980-3989. 10.4049/jimmunol.1000990, 20826751.
29. Qi W, Chen X, Holian J, Tan CY, Kelly DJ, Pollock CA. Transcription factors Kruppel-like factor 6 and peroxisome proliferator-activated receptor-{gamma} mediate high glucose-induced thioredoxin-interacting protein. Am J Pathol 2009, 175:1858-1867. 10.2353/ajpath.2009.090263, 2774051, 19808645.
30. Ogata FT, Batista WL, Sartori A, Gesteira TF, Masutani H, Arai RJ, Yodoi J, Stern A, Monteiro HP. Nitrosative/Oxidative Stress Conditions Regulate Thioredoxin-Interacting Protein (TXNIP) Expression and Thioredoxin-1 (TRX-1) Nuclear Localization. PLoS One 2013, 8:e84588. 10.1371/journal.pone.0084588, 3869934, 24376827.
31. Nagano M, Hatakeyama K, Kai M, Nakamura H, Yodoi J, Asada Y, Chijiiwa K. Nuclear expression of thioredoxin-1 in the invasion front is associated with outcome in patients with gallbladder carcinoma. HPB (Oxford) 2012, 14:573-582. 10.1111/j.1477-2574.2012.00482.x, 3461382, 22882193.
32. Shan W, Zhong W, Zhao R, Oberley TD. Thioredoxin 1 as a subcellular biomarker of redox imbalance in human prostate cancer progression. Free Radic Biol Med 2010, 49:2078-2087. 10.1016/j.freeradbiomed.2010.10.691, 3010556, 20955789.
33. Lincoln DT, Ali Emadi EM, Tonissen KF, Clarke FM. The thioredoxin-thioredoxin reductase system: over-expression in human cancer. Anticancer Res 2003, 23:2425-2433.
34. Cha MK, Suh KH, Kim IH. Overexpression of peroxiredoxin I and thioredoxin1 in human breast carcinoma. J Exp Clin Cancer Res 2009, 28:93. 10.1186/1756-9966-28-93, 2711968, 19566940.
35. Arner ES, Holmgren A. Physiological functions of thioredoxin and thioredoxin reductase. Eur J Biochem 2000, 267:6102-6109. 10.1046/j.1432-1327.2000.01701.x, 11012661.
36. Yoshihara E, Masaki S, Matsuo Y, Chen Z, Tian H, Yodoi J. Thioredoxin/Txnip: Redoxisome, as a Redox Switch for the Pathogenesis of Diseases. Front Immunol 2014, 4:514. 3885921, 24409188.
37. Hendrix MJ, Seftor EA, Seftor RE, Fidler IJ. A simple quantitative assay for studying the invasive potential of high and low human metastatic variants. Cancer Lett 1987, 38:137-147. 10.1016/0304-3835(87)90209-6, 3690504.
38. Chan CM, Jing X, Pike LA, Zhou Q, Lim DJ, Sams SB, Lund GS, Sharma V, Haugen BR, Schweppe RE. Targeted inhibition of Src kinase with dasatinib blocks thyroid cancer growth and metastasis. Clin Cancer Res 2012, 18:3580-3591. 10.1158/1078-0432.CCR-11-3359, 3931551, 22586301.
39. Kim S, Park YW, Schiff BA, Doan DD, Yazici Y, Jasser SA, Younes M, Mandal M, Bekele BN, Myers JN. An orthotopic model of anaplastic thyroid carcinoma in athymic nude mice. Clin Cancer Res 2005, 11:1713-1721. 10.1158/1078-0432.CCR-04-1908, 15755992.
40. Ahn SH, Henderson Y, Kang Y, Chattopadhyay C, Holton P, Wang M, Briggs K, Clayman GL. An orthotopic model of papillary thyroid carcinoma in athymic nude mice. Arch Otolaryngol Head Neck Surg 2008, 134:190-197. 10.1001/archoto.2007.36, 18283163.
41. Nucera C, Nehs MA, Mekel M, Zhang X, Hodin R, Lawler J, Nose V, Parangi S. A novel orthotopic mouse model of human anaplastic thyroid carcinoma. Thyroid 2009, 19:1077-1084. 10.1089/thy.2009.0055, 2833178, 19772429.
42. Woolston CM, Madhusudan S, Soomro IN, Lobo DN, Reece-Smith AM, Parsons SL, Martin SG. Thioredoxin interacting protein and its association with clinical outcome in gastro-oesophageal adenocarcinoma. Redox Biol 2013, 1:285-291. 10.1016/j.redox.2013.04.006, 3757700, 24024162.
43. Woolston CM, Zhang L, Storr SJ, Al-Attar A, Shehata M, Ellis IO, Chan SY, Martin SG. The prognostic and predictive power of redox protein expression for anthracycline-based chemotherapy response in locally advanced breast cancer. Mod Pathol 2012, 25:1106-1116. 10.1038/modpathol.2012.60, 3410251, 22481283.
44. Lim JY, Yoon SO, Hong SW, Kim JW, Choi SH, Cho JY. Thioredoxin and thioredoxin-interacting protein as prognostic markers for gastric cancer recurrence. World J Gastroenterol 2012, 18:5581-5588. 10.3748/wjg.v18.i39.5581, 3482645, 23112551.
45. Ikarashi M, Takahashi Y, Ishii Y, Nagata T, Asai S, Ishikawa K. Vitamin D3 up-regulated protein 1 (VDUP1) expression in gastrointestinal cancer and its relation to stage of disease. Anticancer Res 2002, 22:4045-4048.
46. Cadenas C, Franckenstein D, Schmidt M, Gehrmann M, Hermes M, Geppert B, Schormann W, Maccoux LJ, Schug M, Schumann A, Wilhelm C, Freis E, Ickstadt K, Rahnenfuhrer J, Baumbach JI, Sickmann A, Hengstler JG. Role of thioredoxin reductase 1 and thioredoxin interacting protein in prognosis of breast cancer. Breast Cancer Res 2010, 12:R44. 10.1186/bcr2599, 2917039, 20584310.
47. Tome ME, Johnson DB, Rimsza LM, Roberts RA, Grogan TM, Miller TP, Oberley LW, Briehl MM. A redox signature score identifies diffuse large B-cell lymphoma patients with a poor prognosis. Blood 2005, 106:3594-3601. 10.1182/blood-2005-02-0487, 1895056, 16081686.
48. Nishinaka Y, Nishiyama A, Masutani H, Oka S, Ahsan KM, Nakayama Y, Ishii Y, Nakamura H, Maeda M, Yodoi J. Loss of thioredoxin-binding protein-2/vitamin D3 up-regulated protein 1 in human T-cell leukemia virus type I-dependent T-cell transformation: implications for adult T-cell leukemia leukemogenesis. Cancer Res 2004, 64:1287-1292. 10.1158/0008-5472.CAN-03-0908, 14983878.
49. Wang W, Larson SM, Fazzari M, Tickoo SK, Kolbert K, Sgouros G, Yeung H, Macapinlac H, Rosai J, Robbins RJ. Prognostic value of [18F]fluorodeoxyglucose positron emission tomographic scanning in patients with thyroid cancer. J Clin Endocrinol Metab 2000, 85:1107-1113.
50. Deandreis D, Al Ghuzlan A, Leboulleux S, Lacroix L, Garsi JP, Talbot M, Lumbroso J, Baudin E, Caillou B, Bidart JM, Schlumberger M. Do histological, immunohistochemical, and metabolic (radioiodine and fluorodeoxyglucose uptakes) patterns of metastatic thyroid cancer correlate with patient outcome?. Endocr Relat Cancer 2011, 18:159-169. 10.1677/ERC-10-0233, 21118976.
51. Schweppe RE, Klopper JP, Korch C, Pugazhenthi U, Benezra M, Knauf JA, Fagin JA, Marlow LA, Copland JA, Smallridge RC, Haugen BR. Deoxyribonucleic acid profiling analysis of 40 human thyroid cancer cell lines reveals cross-contamination resulting in cell line redundancy and misidentification. J Clin Endocrinol Metab 2008, 93:4331-4341. 10.1210/jc.2008-1102, 2582569, 18713817.
52. Pear WS, Nolan GP, Scott ML, Baltimore D. Production of high-titer helper-free retroviruses by transient transfection. Proc Natl Acad Sci U S A 1993, 90:8392-8396. 10.1073/pnas.90.18.8392, 47362, 7690960.