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Science 289 (5483): 1357-1360

Copyright © 2000 by the American Association for the Advancement of Science

PAX8-PPARgamma 1 Fusion Oncogene in Human Thyroid Carcinoma

Todd G. Kroll,1* Pasha Sarraf,2 Lorenza Pecciarini,1 Chang-Jie Chen,1 Elisabetta Mueller,2 Bruce M. Spiegelman,2 Jonathan A. Fletcher123*

Chromosomal translocations that encode fusion oncoproteins have been observed consistently in leukemias/lymphomas and sarcomas but not in carcinomas, the most common human cancers. Here, we report that t(2;3)(q13;p25), a translocation identified in a subset of human thyroid follicular carcinomas, results in fusion of the DNA binding domains of the thyroid transcription factor PAX8 to domains A to F of the peroxisome proliferator-activated receptor (PPAR) gamma 1. PAX8-PPARgamma 1 mRNA and protein were detected in 5 of 8 thyroid follicular carcinomas but not in 20 follicular adenomas, 10 papillary carcinomas, or 10 multinodular hyperplasias. PAX8-PPARgamma 1 inhibited thiazolidinedione-induced transactivation by PPARgamma 1 in a dominant negative manner. The experiments demonstrate an oncogenic role for PPARgamma and suggest that PAX8-PPARgamma 1 may be useful in the diagnosis and treatment of thyroid carcinoma.

1 Department of Pathology, Brigham and Women's Hospital, 75 Francis Street, Boston, MA 02115, USA, and Harvard Medical School, Boston, MA 02115, USA.
2 Dana-Farber Cancer Institute and Department of Cell Biology, Harvard Medical School, Boston, MA 02115, USA.
3 Departments of Pathology and Pediatric Oncology, Children's Hospital, Boston, MA 02115, USA.
*   To whom correspondence should be addressed. E-mail: tkroll{at}rics.bwh.harvard.edu; jfletcher{at}rics.bwh.harvard.edu

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J. Clin. Endocrinol. Metab. 88, 5399-5404
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p73 Tumor-Suppressor Activity Is Impaired in Human Thyroid Cancer.
F. Frasca, V. Vella, A. Aloisi, A. Mandarino, E. Mazzon, R. Vigneri, and P. Vigneri (2003)
Cancer Res. 63, 5829-5837
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Involvement of the PAX8/Peroxisome Proliferator-Activated Receptor {gamma} Rearrangement in Follicular Thyroid Tumors.
T. Dwight, S. R. Thoppe, T. Foukakis, W. O. Lui, G. Wallin, A. Hoog, T. Frisk, C. Larsson, and J. Zedenius (2003)
J. Clin. Endocrinol. Metab. 88, 4440-4445
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Cyclin D1 Repression of Peroxisome Proliferator-Activated Receptor {gamma} Expression and Transactivation.
C. Wang, N. Pattabiraman, J. N. Zhou, M. Fu, T. Sakamaki, C. Albanese, Z. Li, K. Wu, J. Hulit, P. Neumeister, et al. (2003)
Mol. Cell. Biol. 23, 6159-6173
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Mutant Thyroid Hormone Receptor {beta} Represses the Expression and Transcriptional Activity of Peroxisome Proliferator-activated Receptor {gamma} during Thyroid Carcinogenesis.
H. Ying, H. Suzuki, L. Zhao, M. C. Willingham, P. Meltzer, and S.-Y. Cheng (2003)
Cancer Res. 63, 5274-5280
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Alterations in genomic profiles during tumor progression in a mouse model of follicular thyroid carcinoma.
H. Ying, H. Suzuki, H. Furumoto, R. Walker, P. Meltzer, M. C. Willingham, and S.-Y. Cheng (2003)
Carcinogenesis 24, 1467-1479
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Changes in the Expression of the Peroxisome Proliferator-Activated Receptor {gamma} Gene in the Colonic Polyps and Colonic Mucosa of Acromegalic Patients.
F. Bogazzi, F. Ultimieri, F. Raggi, D. Russo, P. Viacava, D. Cecchetti, A. Costa, S. Brogioni, C. Cosci, M. Gasperi, et al. (2003)
J. Clin. Endocrinol. Metab. 88, 3938-3942
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Caveolin-1 and Caveolin-2,Together with Three Bone Morphogenetic Protein-related Genes, May Encode Novel Tumor Suppressors Down-Regulated in Sporadic Follicular Thyroid Carcinogenesis.
M. A. Aldred, M. E. Ginn-Pease, C. D. Morrison, A. P. Popkie, O. Gimm, C. Hoang-Vu, U. Krause, H. Dralle, S. M. Jhiang, C. Plass, et al. (2003)
Cancer Res. 63, 2864-2871
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Activation of Signal Transducer and Activator of Transcription 3 by Oncogenic RET/PTC (Rearranged in Transformation/Papillary Thyroid Carcinoma) Tyrosine Kinase: Roles in Specific Gene Regulation and Cellular Transformation.
J. H. Hwang, D. W. Kim, J. M. Suh, H. Kim, J. H. Song, E. S. Hwang, K. C. Park, H. K. Chung, J. M. Kim, T.-H. Lee, et al. (2003)
Mol. Endocrinol. 17, 1155-1166
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RAS Point Mutations and PAX8-PPAR{gamma} Rearrangement in Thyroid Tumors: Evidence for Distinct Molecular Pathways in Thyroid Follicular Carcinoma.
M. N. Nikiforova, R. A. Lynch, P. W. Biddinger, E. K. Alexander, G. W. Dorn II, G. Tallini, T. G. Kroll, and Y. E. Nikiforov (2003)
J. Clin. Endocrinol. Metab. 88, 2318-2326
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Simian Virus 40-Like Sequences from Early and Late Regions in Human Thyroid Tumors of Different Histotypes.
A. Vivaldi, F. Pacini, F. Martini, L. Iaccheri, F. Pezzetti, R. Elisei, A. Pinchera, P. Faviana, F. Basolo, and M. Tognon (2003)
J. Clin. Endocrinol. Metab. 88, 892-899
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A Thyroid Tumor-Specific Antigen Formed by the Fusion of Two Self Proteins.
D. J. Powell Jr., L. C. Eisenlohr, and J. L. Rothstein (2003)
J. Immunol. 170, 861-869
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Detection of the PAX8-PPAR{gamma} Fusion Oncogene in Both Follicular Thyroid Carcinomas and Adenomas.
L. Cheung, M. Messina, A. Gill, A. Clarkson, D. Learoyd, L. Delbridge, J. Wentworth, J. Philips, R. Clifton-Bligh, and B. G. Robinson (2003)
J. Clin. Endocrinol. Metab. 88, 354-357
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Peroxisome Proliferator-activated Receptor {gamma} and Cancers.
H. P. Koeffler (2003)
Clin. Cancer Res. 9, 1-9
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Inhibitory Effects of Peroxisome Proliferator-Activated Receptor {gamma} on Thyroid Carcinoma Cell Growth.
M. L. Martelli, R. Iuliano, I. Le Pera, I. Sama', C. Monaco, S. Cammarota, T. Kroll, L. Chiariotti, M. Santoro, and A. Fusco (2002)
J. Clin. Endocrinol. Metab. 87, 4728-4735
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Galectin-3 Messenger Ribonucleic Acid and Protein Are Expressed in Benign Thyroid Tumors.
L. Martins, S. E. Matsuo, K. N. Ebina, M. A. V. Kulcsar, C. U. M. Friguglietti, and E. T. Kimura (2002)
J. Clin. Endocrinol. Metab. 87, 4806-4810
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Expression of PAX8-PPAR{gamma}1 Rearrangements in Both Follicular Thyroid Carcinomas and Adenomas.
A. R. Marques, C. Espadinha, A. L. Catarino, S. Moniz, T. Pereira, L. G. Sobrinho, and V. Leite (2002)
J. Clin. Endocrinol. Metab. 87, 3947-3952
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Controversy: PPARgamma as a target for treatment of colorectal cancer.
R. A. Gupta and R. N. Dubois (2002)
Am J Physiol Gastrointest Liver Physiol 283, G266-G269
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Perspective: Lessons Learned from Molecular Genetic Studies of Thyroid Cancer--Insights into Pathogenesis and Tumor-Specific Therapeutic Targets.
J. A. Fagin (2002)
Endocrinology 143, 2025-2028
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Nuclear Receptors: I. PPARgamma in the gastrointestinal tract: gain or pain?.
J. Auwerx (2002)
Am J Physiol Gastrointest Liver Physiol 282, G581-G585
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Expression and Localization of the Homeodomain-Containing Protein HEX in Human Thyroid Tumors.
A. V. D'Elia, G. Tell, D. Russo, F. Arturi, F. Puglisi, G. Manfioletti, V. Gattei, D. L. Mack, P. Cataldi, S. Filetti, et al. (2002)
J. Clin. Endocrinol. Metab. 87, 1376-1383
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Peroxisome Proliferator-activated Receptor Modulators As Potential Chemopreventive Agents.
L. Kopelovich, J. R. Fay, R. I. Glazer, and J. A. Crowell (2002)
Mol. Cancer Ther. 1, 357-363
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The RET/PTC Oncogene Is Frequently Activated in Oncocytic Thyroid Tumors (Hurthle Cell Adenomas and Carcinomas), but Not in Oncocytic Hyperplastic Lesions.
G. Chiappetta, P. Toti, F. Cetta, A. Giuliano, F. Pentimalli, I. Amendola, S. Lazzi, M. Monaco, L. Mazzuchelli, P. Tosi, et al. (2002)
J. Clin. Endocrinol. Metab. 87, 364-369
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Allelotyping of Follicular Thyroid Carcinoma: Frequent Allelic Losses in Chromosome Arms 7q, 11p, and 22q.
Y. Kitamura, K. Shimizu, K. Ito, S. Tanaka, and M. Emi (2001)
J. Clin. Endocrinol. Metab. 86, 4268-4272
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Anticancer Effects of Thiazolidinediones Are Independent of Peroxisome Proliferator-activated Receptor {gamma} and Mediated by Inhibition of Translation Initiation.
S. S. Palakurthi, H. Aktas, L. M. Grubissich, R. M. Mortensen, and J. A. Halperin (2001)
Cancer Res. 61, 6213-6218
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