Subscribe to RSS
DOI: 10.1055/s-0029-1215572
© Georg Thieme Verlag KG Stuttgart · New York
Modeling Thyroid Cancer in the Mouse
Publication History
received 02.02.2009
accepted 03.03.2009
Publication Date:
08 April 2009 (online)

Abstract
Thyroid carcinomas, the most common endocrine tumors in humans, have an increasing incidence in the U.S. and worldwide. There are four major types of thyroid cancers: papillary, follicular, anaplastic, and medullary carcinomas. In recent years, significant progress has been made in the identification of genetic alterations in thyroid carcinomas, particularly, papillary and medullary thyroid cancers. Mouse models of thyroid cancer are valuable tools in elucidating molecular genetic changes underlying thyroid carcinogenesis and in identifying potential molecular targets for therapeutic intervention. Representative mouse models of papillary, follicular, and medullary carcinomas are reviewed here with particular emphasis on those for follicular thyroid carcinomas. Challenges for further development in the modeling of thyroid cancer will also be discussed.
Key words
thyroid cancer - thyroid hormone - mouse models
References
- 1
Nikiforova MN, Nikiforov YE.
Molecular genetics of thyroid cancer: implications for diagnosis, treatment and prognosis.
Expert Rev Mol Diagn.
2008;
8
83-95
MissingFormLabel
- 2
Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T, Thun MJ.
Cancer statistics, 2008.
CA Cancer J Clin.
2008;
58
71-96
MissingFormLabel
- 3
Lodish MB, Stratakis CA.
RET oncogene in MEN2, MEN2B, MTC and other forms of thyroid cancer.
Expert Rev Anticancer Ther.
2008;
8
625-632
MissingFormLabel
- 4
Mauchamp J, Mirrione A, Alquier C, Andre F.
Follicle-like structure and polarized monolayer: role of the extracellular matrix
on thyroid cell organization in primary culture.
Biol Cell.
1998;
90
369-380
MissingFormLabel
- 5
De Felice M, Di Lauro R.
Thyroid development and its disorders: genetics and molecular mechanisms.
Endocr Rev.
2004;
25
722-746
MissingFormLabel
- 6
Lazzaro D, Price M, de Felice M, Di Lauro R.
The transcription factor TTF-1 is expressed at the onset of thyroid and lung morphogenesis
and in restricted regions of the foetal brain.
Development.
1991;
113
1093-1104
MissingFormLabel
- 7
Postiglione MP, Parlato R, Rodriguez-Mallon A, Rosica A, Mithbaokar P, Maresca M, Marians RC, Davies TF, Zannini MS, De Felice M, Di Lauro R.
Role of the thyroid-stimulating hormone receptor signaling in development and differentiation
of the thyroid gland.
Proc Natl Acad Sci USA.
2002;
99
15462-15467
MissingFormLabel
- 8
Meunier D, Aubin J, Jeannotte L.
Perturbed thyroid morphology and transient hypothyroidism symptoms in Hoxa5 mutant
mice.
Dev Dyn.
2003;
227
367-378
MissingFormLabel
- 9
Castellone MD, Santoro M.
Dysregulated RET signaling in thyroid cancer.
Endocrinol Metab Clin North Am.
2008;
37
363-374
, viii
MissingFormLabel
- 10
Nikiforov YE.
RET/PTC rearrangement in thyroid tumors.
Endocr Pathol.
2002;
13
3-16
MissingFormLabel
- 11
Nikiforova MN, Stringer JR, Blough R, Medvedovic M, Fagin JA, Nikiforov YE.
Proximity of chromosomal loci that participate in radiation-induced rearrangements
in human cells.
Science.
2000;
290
138-141
MissingFormLabel
- 12
Grieco M, Santoro M, Berlingieri MT, Melillo RM, Donghi R, Bongarzone I, Pierotti MA, Della Porta G, Fusco A, Vecchio G.
PTC is a novel rearranged form of the ret proto-oncogene and is frequently detected
in vivo in human thyroid papillary carcinomas.
Cell.
1990;
60
557-563
MissingFormLabel
- 13
Bongarzone I, Butti MG, Coronelli S, Borrello MG, Santoro M, Mondellini P, Pilotti S, Fusco A, Della Porta G, Pierotti MA.
Frequent activation of ret protooncogene by fusion with a new activating gene in papillary
thyroid carcinomas.
Cancer Res.
1994;
54
2979-2985
MissingFormLabel
- 14
Boice Jr JD.
Radiation-induced thyroid cancer – what’s new?.
J Natl Cancer Inst.
2005;
97
703-705
MissingFormLabel
- 15
Cardis E, Kesminiene A, Ivanov V, Malakhova I, Shibata Y, Khrouch V, Drozdovitch V, Maceika E, Zvonova I, Vlassov O, Bouville A, Goulko G, Hoshi M, Abrosimov A, Anoshko J, Astakhova L, Chekin S, Demidchik E, Galanti R, Ito M, Korobova E, Lushnikov E, Maksioutov M, Masyakin V, Nerovnia A, Parshin V, Parshkov E, Piliptsevich N, Pinchera A, Polyakov S, Shabeka N, Suonio E, Tenet V, Tsyb A, Yamashita S, Williams D.
Risk of thyroid cancer after exposure to 131I in childhood.
J Natl Cancer Inst.
2005;
97
724-732
MissingFormLabel
- 16
Klugbauer S, Lengfelder E, Demidchik EP, Rabes HM.
High prevalence of RET rearrangement in thyroid tumors of children from Belarus after
the Chernobyl reactor accident.
Oncogene.
1995;
11
2459-2467
MissingFormLabel
- 17
Tallini G.
Molecular pathobiology of thyroid neoplasms.
Endocr Pathol.
2002;
13
271-288
MissingFormLabel
- 18
Bongarzone I, Fugazzola L, Vigneri P, Mariani L, Mondellini P, Pacini F, Basolo F, Pinchera A, Pilotti S, Pierotti MA.
Age-related activation of the tyrosine kinase receptor protooncogenes RET and NTRK1
in papillary thyroid carcinoma.
J Clin Endocrinol Metab.
1996;
81
2006-2009
MissingFormLabel
- 19
Kimura ET, Nikiforova MN, Zhu Z, Knauf JA, Nikiforov YE, Fagin JA.
High prevalence of BRAF mutations in thyroid cancer: genetic evidence for constitutive
activation of the RET/PTC-RAS-BRAF signaling pathway in papillary thyroid carcinoma.
Cancer Res.
2003;
63
1454-1457
MissingFormLabel
- 20
Namba H, Rubin SA, Fagin JA.
Point mutations of ras oncogenes are an early event in thyroid tumorigenesis.
Mol Endocrinol.
1990;
4
1474-1479
MissingFormLabel
- 21
Benvenga S.
Update on thyroid cancer.
Horm Metab Res.
2008;
40
323-328
MissingFormLabel
- 22
Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S, Teague J, Woffendin H, Garnett MJ, Bottomley W, Davis N, Dicks E, Ewing R, Floyd Y, Gray K, Hall S, Hawes R, Hughes J, Kosmidou V, Menzies A, Mould C, Parker A, Stevens C, Watt S, Hooper S, Wilson R, Jayatilake H, Gusterson BA, Cooper C, Shipley J, Hargrave D, Pritchard-Jones K, Maitland N, Chenevix-Trench G, Riggins GJ, Bigner DD, Palmieri G, Cossu A, Flanagan A, Nicholson A, Ho JW, Leung SY, Yuen ST, Weber BL, Seigler HF, Darrow TL, Paterson H, Marais R, Marshall CJ, Wooster R, Stratton MR, Futreal PA.
Mutations of the BRAF gene in human cancer.
Nature.
2002;
417
949-954
MissingFormLabel
- 23
Ciampi R, Nikiforov YE.
RET/PTC rearrangements and BRAF mutations in thyroid tumorigenesis.
Endocrinology.
2007;
148
936-941
MissingFormLabel
- 24
Saxena N, Lahiri SS, Hambarde S, Tripathi RP.
RAS: target for cancer therapy.
Cancer Invest.
2008;
26
948-955
MissingFormLabel
- 25
Riesco-Eizaguirre G, Santisteban P.
New insights in thyroid follicular cell biology and its impact in thyroid cancer therapy.
Endocr Relat Cancer.
2007;
14
957-977
MissingFormLabel
- 26
Quayle FJ, Moley JF.
Medullary thyroid carcinoma: including MEN 2A and MEN 2B syndromes.
J Surg Oncol.
2005;
89
122-129
MissingFormLabel
- 27
Gimm O, Dralle H.
C-cell cancer – prevention and treatment.
Langenbecks Arch Surg.
1999;
384
16-23
MissingFormLabel
- 28
Michiels FM, Chappuis S, Caillou B, Pasini A, Talbot M, Monier R, Lenoir GM, Feunteun J, Billaud M.
Development of medullary thyroid carcinoma in transgenic mice expressing the RET protooncogene
altered by a multiple endocrine neoplasia type 2A mutation.
Proc Natl Acad Sci USA.
1997;
94
3330-3335
MissingFormLabel
- 29
Esapa CT, Johnson SJ, Kendall-Taylor P, Lennard TW, Harris PE.
Prevalence of Ras mutations in thyroid neoplasia.
Clin Endocrinol (Oxf).
1999;
50
529-535
MissingFormLabel
- 30
Motoi N, Sakamoto A, Yamochi T, Horiuchi H, Motoi T, Machinami R.
Role of ras mutation in the progression of thyroid carcinoma of follicular epithelial
origin.
Pathol Res Pract.
2000;
196
1-7
MissingFormLabel
- 31
Suarez HG, du Villard JA, Severino M, Caillou B, Schlumberger M, Tubiana M, Parmentier C, Monier R.
Presence of mutations in all three ras genes in human thyroid tumors.
Oncogene.
1990;
5
565-570
MissingFormLabel
- 32
Basolo F, Pisaturo F, Pollina LE, Fontanini G, Elisei R, Molinaro E, Iacconi P, Miccoli P, Pacini F.
N-ras mutation in poorly differentiated thyroid carcinomas: correlation with bone
metastases and inverse correlation to thyroglobulin expression.
Thyroid.
2000;
10
19-23
MissingFormLabel
- 33
Saavedra HI, Knauf JA, Shirokawa JM, Wang J, Ouyang B, Elisei R, Stambrook PJ, Fagin JA.
The RAS oncogene induces genomic instability in thyroid PCCL3 cells via the MAPK pathway.
Oncogene.
2000;
19
3948-3954
MissingFormLabel
- 34
Dwight T, Thoppe SR, Foukakis T, Lui WO, Wallin G, Hoog A, Frisk T, Larsson C, Zedenius J.
Involvement of the PAX8/peroxisome proliferator-activated receptor gamma rearrangement
in follicular thyroid tumors.
J Clin Endocrinol Metab.
2003;
88
4440-4445
MissingFormLabel
- 35
French CA, Alexander EK, Cibas ES, Nose V, Laguette J, Faquin W, Garber J, Moore Jr F, Fletcher JA, Larsen PR, Kroll TG.
Genetic and biological subgroups of low-stage follicular thyroid cancer.
Am J Pathol.
2003;
162
1053-1060
MissingFormLabel
- 36
Nikiforova MN, Lynch RA, Biddinger PW, Alexander EK, Dorn 2nd GW, Tallini G, Kroll TG, Nikiforov YE.
RAS point mutations and PAX8-PPAR gamma rearrangement in thyroid tumors: evidence
for distinct molecular pathways in thyroid follicular carcinoma.
J Clin Endocrinol Metab.
2003;
88
2318-2326
MissingFormLabel
- 37
Kroll TG, Sarraf P, Pecciarini L, Chen CJ, Mueller E, Spiegelman BM, Fletcher JA.
PAX8-PPARgamma1 fusion oncogene in human thyroid carcinoma [corrected].
Science.
2000;
289
1357-1360
MissingFormLabel
- 38
Placzkowski KA, Reddi HV, Grebe SK, Eberhardt NL, McIver B.
The role of the PAX8/PPARgamma fusion oncogene in thyroid cancer.
PPAR Res.
2008;
, Oct 29 [Epub ahead of print]
MissingFormLabel
- 39
Gandolfi PP, Frisina A, Raffa M, Renda F, Rocchetti O, Ruggeri C, Tombolini A.
The incidence of thyroid carcinoma in multinodular goiter: retrospective analysis.
Acta Biomed.
2004;
75
114-117
MissingFormLabel
- 40
Lawal O, Agbakwuru A, Olayinka OS, Adelusola K.
Thyroid malignancy in endemic nodular goitres: prevalence, pattern and treatment.
Eur J Surg Oncol.
2001;
27
157-161
MissingFormLabel
- 41
Rivas M, Santisteban P.
TSH-activated signaling pathways in thyroid tumorigenesis.
Mol Cell Endocrinol.
2003;
213
31-45
MissingFormLabel
- 42
Ward JM, Ohshima M.
The role of iodine in carcinogenesis.
Adv Exp Med Biol.
1986;
206
529-542
MissingFormLabel
- 43
Mack WJ, Preston-Martin S, Bernstein L, Qian D, Xiang M.
Reproductive and hormonal risk factors for thyroid cancer in Los Angeles County females.
Cancer Epidemiol Biomarkers Prev.
1999;
8
991-997
MissingFormLabel
- 44
Rios A, Rodriguez JM, Canteras M, Galindo PJ, Balsalobre MD, Parrilla P.
Risk factors for malignancy in multinodular goitres.
Eur J Surg Oncol.
2004;
30
58-62
MissingFormLabel
- 45
Truong T, Orsi L, Dubourdieu D, Rougier Y, Hemon D, Guenel P.
Role of goiter and of menstrual and reproductive factors in thyroid cancer: a population-based
case-control study in New Caledonia (South Pacific), a very high incidence area.
Am J Epidemiol.
2005;
161
1056-1065
MissingFormLabel
- 46
Capen CC.
Overview of structural and functional lesions in endocrine organs of animals.
Toxicol Pathol.
2001;
29
8-33
MissingFormLabel
- 47
Capen CC.
Mechanistic data and risk assessment of selected toxic end points of the thyroid gland.
Toxicol Pathol.
1997;
25
39-48
MissingFormLabel
- 48
Ledent C, Denef JF, Cottecchia S, Lefkowitz R, Dumont J, Vassart G, Parmentier M.
Costimulation of adenylyl cyclase and phospholipase C by a mutant alpha 1B-adrenergic
receptor transgene promotes malignant transformation of thyroid follicular cells.
Endocrinology.
1997;
138
369-378
MissingFormLabel
- 49
Ledent C, Marcotte A, Dumont JE, Vassart G, Parmentier M.
Differentiated carcinomas develop as a consequence of the thyroid specific expression
of a thyroglobulin-human papillomavirus type 16 E7 transgene.
Oncogene.
1995;
10
1789-1797
MissingFormLabel
- 50
Ledent C, Dumont JE, Vassart G, Parmentier M.
Thyroid expression of an A2 adenosine receptor transgene induces thyroid hyperplasia
and hyperthyroidism.
EMBO J.
1992;
11
537-542
MissingFormLabel
- 51
Mazzaferri EL.
Management of a solitary thyroid nodule.
N Engl J Med.
1993;
328
553-559
MissingFormLabel
- 52
Michiels FM, Caillou B, Talbot M, Dessarps-Freichey F, Maunoury MT, Schlumberger M, Mercken L, Monier R, Feunteun J.
Oncogenic potential of guanine nucleotide stimulatory factor alpha subunit in thyroid
glands of transgenic mice.
Proc Natl Acad Sci USA.
1994;
91
10488-10492
MissingFormLabel
- 53
Zeiger MA, Saji M, Gusev Y, Westra WH, Takiyama Y, Dooley WC, Kohn LD, Levine MA.
Thyroid-specific expression of cholera toxin A1 subunit causes thyroid hyperplasia
and hyperthyroidism in transgenic mice.
Endocrinology.
1997;
138
3133-3140
MissingFormLabel
- 54
Chevillard S, Ugolin N, Vielh P, Ory K, Levalois C, Elliott D, Clayman GL, El-Naggar AK.
Gene expression profiling of differentiated thyroid neoplasms: diagnostic and clinical
implications.
Clin Cancer Res.
2004;
10
6586-6597
MissingFormLabel
- 55
Ying H, Suzuki H, Furumoto H, Walker R, Meltzer P, Willingham MC, Cheng SY.
Alterations in genomic profiles during tumor progression in a mouse model of follicular
thyroid carcinoma.
Carcinogenesis.
2003;
24
1467-1479
MissingFormLabel
- 56
Kato Y, Ying H, Zhao L, Furuya F, Araki O, Willingham MC, Cheng SY.
PPARgamma insufficiency promotes follicular thyroid carcinogenesis via activation
of the nuclear factor-kappaB signaling pathway.
Oncogene.
2006;
25
2736-2747
MissingFormLabel
- 57
Hosal SA, Apel RL, Freeman JL, Azadian A, Rosen IB, LiVolsi VA, Asa SL.
Immunohistochemical Localization of p53 in Human Thyroid Neoplasms: Correlation with
Biological Behavior.
Endocr Pathol.
1997;
8
21-28
MissingFormLabel
- 58
Nikiforov YE.
Genetic alterations involved in the transition from well-differentiated to poorly
differentiated and anaplastic thyroid carcinomas.
Endocr Pathol.
2004;
15
319-327
MissingFormLabel
- 59
Quiros RM, Ding HG, Gattuso P, Prinz RA, Xu X.
Evidence that one subset of anaplastic thyroid carcinomas are derived from papillary
carcinomas due to BRAF and p53 mutations.
Cancer.
2005;
103
2261-2268
MissingFormLabel
- 60
Garcia-Rostan G, Tallini G, Herrero A, D’Aquila TG, Carcangiu ML, Rimm DL.
Frequent mutation and nuclear localization of beta-catenin in anaplastic thyroid carcinoma.
Cancer Res.
1999;
59
1811-1815
MissingFormLabel
- 61
Jhiang SM, Sagartz JE, Tong Q, Parker-Thornburg J, Capen CC, Cho JY, Xing S, Ledent C.
Targeted expression of the ret/PTC1 oncogene induces papillary thyroid carcinomas.
Endocrinology.
1996;
137
375-378
MissingFormLabel
- 62
Cho JY, Sagartz JE, Capen CC, Mazzaferri EL, Jhiang SM.
Early cellular abnormalities induced by RET/PTC1 oncogene in thyroid-targeted transgenic
mice.
Oncogene.
1999;
18
3659-3665
MissingFormLabel
- 63
Santoro M, Chiappetta G, Cerrato A, Salvatore D, Zhang L, Manzo G, Picone A, Portella G, Santelli G, Vecchio G, Fusco A.
Development of thyroid papillary carcinomas secondary to tissue-specific expression
of the RET/PTC1 oncogene in transgenic mice.
Oncogene.
1996;
12
1821-1826
MissingFormLabel
- 64
Sagartz JE, Jhiang SM, Tong Q, Capen CC.
Thyroid-stimulating hormone promotes growth of thyroid carcinomas in transgenic mice
with targeted expression of the ret/PTC1 oncogene.
Lab Invest.
1997;
76
307-318
MissingFormLabel
- 65
La Perle KM, Jhiang SM, Capen CC.
Loss of p53 promotes anaplasia and local invasion in ret/PTC1-induced thyroid carcinomas.
Am J Pathol.
2000;
157
671-677
MissingFormLabel
- 66
Powell Jr DJ, Russell J, Nibu K, Li G, Rhee E, Liao M, Goldstein M, Keane WM, Santoro M, Fusco A, Rothstein JL.
The RET/PTC3 oncogene: metastatic solid-type papillary carcinomas in murine thyroids.
Cancer Res.
1998;
58
5523-5528
MissingFormLabel
- 67
Burniat A, Jin L, Detours V, Driessens N, Goffard JC, Santoro M, Rothstein J, Dumont JE, Miot F, Corvilain B.
Gene expression in RET/PTC3 and E7 transgenic mouse thyroids: RET/PTC3 but not E7
tumors are partial and transient models of human papillary thyroid cancers.
Endocrinology.
2008;
149
5107-5117
MissingFormLabel
- 68
Jin L, Burniat A, Dumont JE, Miot F, Corvilain B, Franc B.
Human thyroid tumours, the puzzling lessons from E7 and RET/PTC3 transgenic mice.
Br J Cancer.
2008;
99
1874-1883
MissingFormLabel
- 69
Knauf JA, Ma X, Smith EP, Zhang L, Mitsutake N, Liao XH, Refetoff S, Nikiforov YE, Fagin JA.
Targeted expression of BRAFV600E in thyroid cells of transgenic mice results in papillary
thyroid cancers that undergo dedifferentiation.
Cancer Res.
2005;
65
4238-4245
MissingFormLabel
- 70
Xing M.
BRAF mutation in thyroid cancer.
Endocr Relat Cancer.
2005;
12
245-262
MissingFormLabel
- 71
Russell JP, Powell DJ, Cunnane M, Greco A, Portella G, Santoro M, Fusco A, Rothstein JL.
The TRK-T1 fusion protein induces neoplastic transformation of thyroid epithelium.
Oncogene.
2000;
19
5729-5735
MissingFormLabel
- 72
Feunteun J, Michiels F, Rochefort P, Caillou B, Talbot M, Fournes B, Mercken L, Schlumberger M, Monier R.
Targeted oncogenesis in the thyroid of transgenic mice.
Horm Res.
1997;
47
137-139
MissingFormLabel
- 73
Rochefort P, Caillou B, Michiels FM, Ledent C, Talbot M, Schlumberger M, Lavelle F, Monier R, Feunteun J.
Thyroid pathologies in transgenic mice expressing a human activated Ras gene driven
by a thyroglobulin promoter.
Oncogene.
1996;
12
111-118
MissingFormLabel
- 74
Vitagliano D, Portella G, Troncone G, Francione A, Rossi C, Bruno A, Giorgini A, Coluzzi S, Nappi TC, Rothstein JL, Pasquinelli R, Chiappetta G, Terracciano D, Macchia V, Melillo RM, Fusco A, Santoro M.
Thyroid targeting of the N-ras(Gln61Lys) oncogene in transgenic mice results in follicular
tumors that progress to poorly differentiated carcinomas.
Oncogene.
2006;
25
5467-5474
MissingFormLabel
- 75
Coppee F, Gerard AC, Denef JF, Ledent C, Vassart G, Dumont JE, Parmentier M.
Early occurrence of metastatic differentiated thyroid carcinomas in transgenic mice
expressing the A2a adenosine receptor gene and the human papillomavirus type 16 E7
oncogene.
Oncogene.
1996;
13
1471-1482
MissingFormLabel
- 76
Santelli G, de Franciscis V, Portella G, Chiappetta G, D’Alessio A, Califano D, Rosati R, Mineo A, Monaco C, Manzo G, Pozzi L, Vecchio G.
Production of transgenic mice expressing the Ki-ras oncogene under the control of
a thyroglobulin promoter.
Cancer Res.
1993;
53
5523-5527
MissingFormLabel
- 77
Ribeiro-Neto F, Leon A, Urbani-Brocard J, Lou L, Nyska A, Altschuler DL.
cAMP-dependent oncogenic action of Rap1b in the thyroid gland.
J Biol Chem.
2004;
279
46868-46875
MissingFormLabel
- 78
Yen PM.
Molecular basis of resistance to thyroid hormone.
Trends Endocrinol Metab.
2003;
14
327-333
MissingFormLabel
- 79
Ono S, Schwartz ID, Mueller OT, Root AW, Usala SJ, Bercu BB.
Homozygosity for a dominant negative thyroid hormone receptor gene responsible for
generalized resistance to thyroid hormone.
J Clin Endocrinol Metab.
1991;
73
990-994
MissingFormLabel
- 80
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.
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.
2000;
97
13209-13214
MissingFormLabel
- 81
Parrilla R, Mixson AJ, McPherson JA, MacClaskey JH, Weintraub BD.
Characterization of seven novel mutations of the c-erbA beta gene in unrelated kindreds
with generalized thyroid hormone resistance. Evidence for two “hot spot” regions of
the ligand binding domain.
J Clin Invest.
1991;
88
2123-2130
MissingFormLabel
- 82
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
MissingFormLabel
- 83
Ying H, Suzuki H, Zhao L, Willingham MC, Meltzer P, Cheng SY.
Mutant thyroid hormone receptor beta represses the expression and transcriptional
activity of peroxisome proliferator-activated receptor gamma during thyroid carcinogenesis.
Cancer Res.
2003;
63
5274-5280
MissingFormLabel
- 84
Kim CS, Vasko VV, Kato Y, Kruhlak M, Saji M, Cheng SY, Ringel MD.
AKT activation promotes metastasis in a mouse model of follicular thyroid carcinoma.
Endocrinology.
2005;
146
4456-4463
MissingFormLabel
- 85
Furuya F, Guigon CJ, Zhao L, Lu C, Hanover JA, Cheng SY.
Nuclear receptor corepressor is a novel regulator of phosphatidylinositol 3-kinase
signaling.
Mol Cell Biol.
2007;
27
6116-6126
MissingFormLabel
- 86
Furuya F, Hanover JA, Cheng SY.
Activation of phosphatidylinositol 3-kinase signaling by a mutant thyroid hormone
beta receptor.
Proc Natl Acad Sci USA.
2006;
103
1780-1785
MissingFormLabel
- 87
Furuya F, Lu C, Willingham MC, Cheng SY.
Inhibition of phosphatidylinositol 3-kinase delays tumor progression and blocks metastatic
spread in a mouse model of thyroid cancer.
Carcinogenesis.
2007;
28
2451-2458
MissingFormLabel
- 88
Ying H, Furuya F, Zhao L, Araki O, West BL, Hanover JA, Willingham MC, Cheng SY.
Aberrant accumulation of PTTG1 induced by a mutated thyroid hormone beta receptor
inhibits mitotic progression.
J Clin Invest.
2006;
116
2972-2984
MissingFormLabel
- 89
Zimonjic DB, Kato Y, Ying H, Popescu NC, Cheng SY.
Chromosomal aberrations in cell lines derived from thyroid tumors spontaneously developed
in TRbetaPV/PV mice.
Cancer Genet Cytogenet.
2005;
161
104-109
MissingFormLabel
- 90
Kim CS, Ying H, Willingham MC, Cheng SY.
The pituitary tumor-transforming gene promotes angiogenesis in a mouse model of follicular
thyroid cancer.
Carcinogenesis.
2007;
28
932-939
MissingFormLabel
- 91
Kim CS, Furuya F, Ying H, Kato Y, Hanover JA, Cheng SY.
Gelsolin: a novel thyroid hormone receptor-beta interacting protein that modulates
tumor progression in a mouse model of follicular thyroid cancer.
Endocrinology.
2007;
148
1306-1312
MissingFormLabel
- 92
Torres-Arzayus MI, Font de Mora J, Yuan J, Vazquez F, Bronson R, Rue M, Sellers WR, Brown M.
High tumor incidence and activation of the PI3K/AKT pathway in transgenic mice define
AIB1 as an oncogene.
Cancer Cell.
2004;
6
263-274
MissingFormLabel
- 93
Ying H, Willingham MC, Cheng SY.
The steroid receptor coactivator-3 is a tumor promoter in a mouse model of thyroid
cancer.
Oncogene.
2008;
27
823-830
MissingFormLabel
- 94
Furuya F, Ying H, Zhao L, Cheng SY.
Novel functions of thyroid hormone receptor mutants: beyond nucleus-initiated transcription.
Steroids.
2007;
72
171-179
MissingFormLabel
- 95
Guigon CJ, Zhao L, Lu C, Willingham MC, Cheng SY.
Regulation of beta-catenin by a novel nongenomic action of thyroid hormone beta receptor.
Mol Cell Biol.
2008;
28
4598-4608
MissingFormLabel
- 96
Kato Y, Ying H, Willingham MC, Cheng SY.
A tumor suppressor role for thyroid hormone beta receptor in a mouse model of thyroid
carcinogenesis.
Endocrinology.
2004;
145
4430-4438
MissingFormLabel
- 97
Ledent C, Dumont J, Vassart G, Parmentier M.
Thyroid adenocarcinomas secondary to tissue-specific expression of simian virus-40
large T-antigen in transgenic mice.
Endocrinology.
1991;
129
1391-1401
MissingFormLabel
- 98
Mulligan LM, Kwok JB, Healey CS, Elsdon MJ, Eng C, Gardner E, Love DR, Mole SE, Moore JK, Papi L, Ponder MA, Telenius H, Tunnacliffe A, Ponder BAJ.
Germ-line mutations of the RET proto-oncogene in multiple endocrine neoplasia type
2A.
Nature.
1993;
363
458-460
MissingFormLabel
- 99
Harvey M, Vogel H, Lee EY, Bradley A, Donehower LA.
Mice deficient in both p53 and Rb develop tumors primarily of endocrine origin.
Cancer Res.
1995;
55
1146-1151
MissingFormLabel
- 100
Ziebold U, Lee EY, Bronson RT, Lees JA.
E2F3 loss has opposing effects on different pRB-deficient tumors, resulting in suppression
of pituitary tumors but metastasis of medullary thyroid carcinomas.
Mol Cell Biol.
2003;
23
6542-6552
MissingFormLabel
- 101
Coxon AB, Ward JM, Geradts J, Otterson GA, Zajac-Kaye M, Kaye FJ.
RET cooperates with RB/p53 inactivation in a somatic multi-step model for murine thyroid
cancer.
Oncogene.
1998;
17
1625-1628
MissingFormLabel
- 102
Nakagawa T, Mabry M, de Bustros A, Ihle JN, Nelkin BD, Baylin SB.
Introduction of v-Ha-ras oncogene induces differentiation of cultured human medullary
thyroid carcinoma cells.
Proc Natl Acad Sci USA.
1987;
84
5923-5927
MissingFormLabel
- 103
Johnston D, Hatzis D, Sunday ME.
Expression of v-Ha-ras driven by the calcitonin/calcitonin gene-related peptide promoter:
a novel transgenic murine model for medullary thyroid carcinoma.
Oncogene.
1998;
16
167-177
MissingFormLabel
- 104
Cranston AN, Ponder BA.
Modulation of medullary thyroid carcinoma penetrance suggests the presence of modifier
genes in a RET transgenic mouse model.
Cancer Res.
2003;
63
4777-4780
MissingFormLabel
- 105
Jackson EL, Willis N, Mercer K, Bronson RT, Crowley D, Montoya R, Jacks T, Tuveson DA.
Analysis of lung tumor initiation and progression using conditional expression of
oncogenic K-ras.
Genes Dev.
2001;
15
3243-3248
MissingFormLabel
- 106
Lakso M, Sauer B, Mosinger Jr B, Lee EJ, Manning RW, Yu SH, Mulder KL, Westphal H.
Targeted oncogene activation by site-specific recombination in transgenic mice.
Proc Natl Acad Sci USA.
1992;
89
6232-6236
MissingFormLabel
- 107
Johnson L, Mercer K, Greenbaum D, Bronson RT, Crowley D, Tuveson DA, Jacks T.
Somatic activation of the K-ras oncogene causes early onset lung cancer in mice.
Nature.
2001;
410
1111-1116
MissingFormLabel
- 108
Smith AJ, De Sousa MA, Kwabi-Addo B, Heppell-Parton A, Impey H, Rabbitts P.
A site-directed chromosomal translocation induced in embryonic stem cells by Cre-loxP
recombination.
Nat Genet.
1995;
9
376-385
MissingFormLabel
- 109
Buchholz F, Refaeli Y, Trumpp A, Bishop JM.
Inducible chromosomal translocation of AML1 and ETO genes through Cre/loxP-mediated
recombination in the mouse.
EMBO Rep.
2000;
1
133-139
MissingFormLabel
- 110
Collins EC, Pannell R, Simpson EM, Forster A, Rabbitts TH.
Inter-chromosomal recombination of Mll and Af9 genes mediated by cre-loxP in mouse
development.
EMBO Rep.
2000;
1
127-132
MissingFormLabel
- 111
Sheils O.
Molecular classification and biomarker discovery in papillary thyroid carcinoma.
Expert Rev Mol Diagn.
2005;
5
927-946
MissingFormLabel
Correspondence
S-y. Cheng
Laboratory of Molecular Biology
National Cancer Institute
37 Convent Dr, Room 5128
Bethesda
20892-4264 MD
USA
Phone: +1/301/496 42 80
Fax: +1/301/402 13 44
Email: chengs@mail.nih.gov