Heterozygous inactivation of tsc2 enhances tumorigenesis in p53 mutant zebrafish

DMM Disease Models and Mechanisms

Volumn 6, Issue 4, 2013, Pages 925-993

  Kim, Seok Hyung ^a   Kowalski, Marie L ^a   Carson, Robert P ^a   Bridges, L Richard ^a   Ess, Kevin C ^a  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; PROTEIN KINASE B;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER INCIDENCE; CARCINOGENESIS; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; GENE INTERACTION; HYPOXIA INDUCIBLE FACTOR 1ALPHA GENE; HYPOXIA INDUCIBLE FACTOR 2ALPHA GENE; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1 GENE; NONHUMAN; P53 GENE; PRIORITY JOURNAL; TUBEROUS SCLEROSIS COMPLEX 2 GENE; TUMOR GENE; TUMOR VOLUME; VASCULOTROPIN C GENE; ZEBRA FISH;

ABDOMINAL NEOPLASMS; ALLELES; ANIMALS; BLOOD VESSELS; CELL TRANSFORMATION, NEOPLASTIC; GENE SILENCING; HETEROZYGOTE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MULTIPROTEIN COMPLEXES; MUTATION; NEOVASCULARIZATION, PATHOLOGIC; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; SIROLIMUS; TOR SERINE-THREONINE KINASES; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; ZEBRAFISH; ZEBRAFISH PROTEINS;

ANIMALIA; DANIO RERIO;

EID: 84880006426     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.011494     Document Type: Article

References (51)

1. Altomare, D. A., Wang, H. Q., Skele, K. L., De Rienzo, A., Klein-Szanto, A. J., Godwin, A. K. and Testa, J. R. (2004). AKT and mTOR phosphorylation is frequently detected in ovarian cancer and can be targeted to disrupt ovarian tumor cell growth. Oncogene 23, 5853-5857. (Pubitemid 39093031)
2. Berghmans, S., Murphey, R. D., Wienholds, E., Neuberg, D., Kutok, J. L., Fletcher, C. D., Morris, J. P., Liu, T. X., Schulte-Merker, S., Kanki, J. P. et al. (2005). tp53 mutant zebrafish develop malignant peripheral nerve sheath tumors. Proc. Natl. Acad. Sci. USA 102, 407-412. (Pubitemid 40116780)
3. Bonneau, D. and Longy, M. (2000). Mutations of the human PTEN gene. Hum. Mutat. 16, 109-122. (Pubitemid 30604900)
4. Choo, A. Y., Kim, S. G., Vander Heiden, M. G., Mahoney, S. J., Vu, H., Yoon, S. O., Cantley, L. C. and Blenis, J. (2010). Glucose addiction of TSC null cells is caused by failed mTORC1-dependent balancing of metabolic demand with supply. Mol. Cell 38, 487-499.
5. Crino, P. B., Nathanson, K. L. and Henske, E. P. (2006). The tuberous sclerosis complex. N. Engl. J. Med. 355, 1345-1356.
6. Davies, D. M., Johnson, S. R., Tattersfield, A. E., Kingswood, J. C., Cox, J. A., McCartney, D. L., Doyle, T., Elmslie, F., Saggar, A., de Vries, P. J. et al. (2008). Sirolimus therapy in tuberous sclerosis or sporadic lymphangioleiomyomatosis. N. Engl. J. Med. 358, 200-203.
7. Edlund, K., Larsson, O., Ameur, A., Bunikis, I., Gyllensten, U., Leroy, B., Sundström, M., Micke, P., Botling, J. and Soussi, T. (2012). Data-driven unbiased curation of the TP53 tumor suppressor gene mutation database and validation by ultradeep sequencing of human tumors. Proc. Natl. Acad. Sci. USA 109, 9551-9556.
8. Feitsma, H. and Cuppen, E. (2008). Zebrafish as a cancer model. Mol. Cancer Res. 6, 685-694.
9. Feng, Z., Zhang, H., Levine, A. J. and Jin, S. (2005). The coordinate regulation of the p53 and mTOR pathways in cells. Proc. Natl. Acad. Sci. USA 102, 8204-8209. (Pubitemid 40800067)
10. Feng, Z., Hu, W., de Stanchina, E., Teresky, A. K., Jin, S., Lowe, S. and Levine, A. J. (2007). The regulation of AMPK beta1, TSC2, and PTEN expression by p53: stress, cell and tissue specificity, and the role of these gene products in modulating the IGF-1-AKT-mTOR pathways. Cancer Res. 67, 3043-3053. (Pubitemid 46724841)
11. Finlay, C. A., Hinds, P. W. and Levine, A. J. (1989). The p53 proto-oncogene can act as a suppressor of transformation. Cell 57, 1083-1093. (Pubitemid 19169804)
12. Franz, D. N., Leonard, J., Tudor, C., Chuck, G., Care, M., Sethuraman, G., Dinopoulos, A., Thomas, G. and Crone, K. R. (2006). Rapamycin causes regression of astrocytomas in tuberous sclerosis complex. Ann. Neurol. 59, 490-498. (Pubitemid 43358069)
13. Gad, S., Lefèvre, S. H., Khoo, S. K., Giraud, S., Vieillefond, A., Vasiliu, V., Ferlicot, S., Molinié, V., Denoux, Y., Thiounn, N. et al. (2007). Mutations in BHD and TP53 genes, but not in HNF1beta gene, in a large series of sporadic chromophobe renal cell carcinoma. Br. J. Cancer 96, 336-340. (Pubitemid 46160640)
14. Goessling, W., North, T. E. and Zon, L. I. (2007). New waves of discovery: modeling cancer in zebrafish. J. Clin. Oncol. 25, 2473-2479. (Pubitemid 46999219)
15. Habib, S. L., Yadav, A., Mahimainathan, L. and Valente, A. J. (2011). Regulation of PI 3-K, PTEN, p53, and mTOR in malignant and benign tumors deficient in tuberin. Genes Cancer 2, 1051-1060.
16. Harrington, L. S., Findlay, G. M., Gray, A., Tolkacheva, T., Wigfield, S., Rebholz, H., Barnett, J., Leslie, N. R., Cheng, S., Shepherd, P. R. et al. (2004). The TSC1-2 tumor suppressor controls insulin-PI3K signaling via regulation of IRS proteins. J. Cell Biol. 166, 213-223. (Pubitemid 38988774)
17. Hu, X., Pandolfi, P. P., Li, Y., Koutcher, J. A., Rosenblum, M. and Holland, E. C. (2005). mTOR promotes survival and astrocytic characteristics induced by Pten/AKT signaling in glioblastoma. Neoplasia 7, 356-368. (Pubitemid 40664225)
18. Inoki, K., Li, Y., Zhu, T., Wu, J. and Guan, K. L. (2002). TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat. Cell Biol. 4, 648-657. (Pubitemid 34993700)
19. Inoki, K., Li, Y., Xu, T. and Guan, K. L. (2003). Rheb GTPase is a direct target of TSC2 GAP activity and regulates mTOR signaling. Genes Dev. 17, 1829-1834. (Pubitemid 36944560)
20. Inoki, K., Corradetti, M. N. and Guan, K. L. (2005). Dysregulation of the TSC-mTOR pathway in human disease. Nat. Genet. 37, 19-24. (Pubitemid 40070934)
21. Jacinto, E., Loewith, R., Schmidt, A., Lin, S., Rüegg, M. A., Hall, A. and Hall, M. N. (2004). Mammalian TOR complex 2 controls the actin cytoskeleton and is rapamycin insensitive. Nat. Cell Biol. 6, 1122-1128. (Pubitemid 39468014)
22. Kim, D. D., Kleinman, D. M., Kanetaka, T., Gerritsen, M. E., Nivaggioli, T., Weber, D. and Durán, W. N. (2010). Rapamycin inhibits VEGF-induced microvascular hyperpermeability in vivo. Microcirculation 17, 128-136.
23. Kim, S. H., Speirs, C. K., Solnica-Krezel, L. and Ess, K. C. (2011). Zebrafish model of tuberous sclerosis complex reveals cell-autonomous and non-cell-autonomous functions of mutant tuberin. Dis. Model. Mech. 4, 255-267.
24. Lai, K. P., Leong, W. F., Chau, J. F., Jia, D., Zeng, L., Liu, H., He, L., Hao, A., Zhang, H., Meek, D. et al. (2010). S6K1 is a multifaceted regulator of Mdm2 that connects nutrient status and DNA damage response. EMBO J. 29, 2994-3006.
25. Lawson, N. D. and Weinstein, B. M. (2002). In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev. Biol. 248, 307-318. (Pubitemid 35002091)
26. Lee, C. H., Inoki, K., Karbowniczek, M., Petroulakis, E., Sonenberg, N., Henske, E. P. and Guan, K. L. (2007). Constitutive mTOR activation in TSC mutants sensitizes cells to energy starvation and genomic damage via p53. EMBO J. 26, 4812-4823. (Pubitemid 350191300)
27. Lendvay, T. S., Broecker, B. and Smith, E. A. (2002). Renal cell carcinoma in a 2-yearold child with tuberous sclerosis. J. Urol. 168, 1131-1132.
28. Levine, A. J. (1997). p53, the cellular gatekeeper for growth and division. Cell 88, 323-331.
29. Levine, A. J., Feng, Z., Mak, T. W., You, H. and Jin, S. (2006). Coordination and communication between the p53 and IGF-1-AKT-TOR signal transduction pathways. Genes Dev. 20, 267-275. (Pubitemid 43200281)
30. Maddocks, O. D. and Vousden, K. H. (2011). Metabolic regulation by p53. J. Mol. Med. (Berl.) 89, 237-245.
31. Mahimainathan, L., Ghosh-Choudhury, N., Venkatesan, B., Das, F., Mandal, C. C., Dey, N., Habib, S. L., Kasinath, B. S., Abboud, H. E. and Ghosh Choudhury, G. (2009). TSC2 deficiency increases PTEN via HIF1alpha. J. Biol. Chem. 284, 27790-27798.
32. Manning, B. D., Tee, A. R., Logsdon, M. N., Blenis, J. and Cantley, L. C. (2002). Identification of the tuberous sclerosis complex-2 tumor suppressor gene product tuberin as a target of the phosphoinositide 3-kinase/akt pathway. Mol. Cell 10, 151-162. (Pubitemid 34876569)
33. Manning, B. D., Logsdon, M. N., Lipovsky, A. I., Abbott, D., Kwiatkowski, D. J. and Cantley, L. C. (2005). Feedback inhibition of Akt signaling limits the growth of tumors lacking Tsc2. Genes Dev. 19, 1773-1778. (Pubitemid 41126916)
34. Mehenni, H., Lin-Marq, N., Buchet-Poyau, K., Reymond, A., Collart, M. A., Picard, D. and Antonarakis, S. E. (2005). LKB1 interacts with and phosphorylates PTEN: a functional link between two proteins involved in cancer predisposing syndromes. Hum. Mol. Genet. 14, 2209-2219. (Pubitemid 41418020)
35. Memmott, R. M. and Dennis, P. A. (2010). The role of the Akt/mTOR pathway in tobacco carcinogen-induced lung tumorigenesis. Clin. Cancer Res. 16, 4-10.
36. Menon, S. and Manning, B. D. (2008). Common corruption of the mTOR signaling network in human tumors. Oncogene 27 Suppl. 2, S43-S51.
37. Mione, M. C. and Trede, N. S. (2010). The zebrafish as a model for cancer. Dis. Model. Mech. 3, 517-523.
38. Noon, A. P., Vlatković, N., Polański, R., Maguire, M., Shawki, H., Parsons, K. and Boyd, M. T. (2010). p53 and MDM2 in renal cell carcinoma: biomarkers for disease progression and future therapeutic targets? Cancer 116, 780-790.
39. Parant, J. M., George, S. A., Holden, J. A. and Yost, H. J. (2010). Genetic modeling of Li-Fraumeni syndrome in zebrafish. Dis. Model. Mech. 3, 45-56.
40. Riley, T., Sontag, E., Chen, P. and Levine, A. (2008). Transcriptional control of human p53-regulated genes. Nat. Rev. Mol. Cell Biol. 9, 402-412. (Pubitemid 351574202)
41. Sarbassov, D. D., Guertin, D. A., Ali, S. M. and Sabatini, D. M. (2005). Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307, 1098-1101. (Pubitemid 40262113)
42. Shah, O. J., Wang, Z. and Hunter, T. (2004). Inappropriate activation of the TSC/Rheb/mTOR/S6K cassette induces IRS1/2 depletion, insulin resistance, and cell survival deficiencies. Curr. Biol. 14, 1650-1656. (Pubitemid 39239362)
43. Stambolic, V., MacPherson, D., Sas, D., Lin, Y., Snow, B., Jang, Y., Benchimol, S. and Mak, T. W. (2001). Regulation of PTEN transcription by p53. Mol. Cell 8, 317-325. (Pubitemid 32831549)
44. Tee, A. R., Fingar, D. C., Manning, B. D., Kwiatkowski, D. J., Cantley, L. C. and Blenis, J. (2002). Tuberous sclerosis complex-1 and -2 gene products function together to inhibit mammalian target of rapamycin (mTOR)-mediated downstream signaling. Proc. Natl. Acad. Sci. USA 99, 13571-13576. (Pubitemid 35215423)
45. Toschi, A., Lee, E., Gadir, N., Ohh, M. and Foster, D. A. (2008). Differential dependence of hypoxia-inducible factors 1 alpha and 2 alpha on mTORC1 and mTORC2. J. Biol. Chem. 283, 34495-34499.
46. Veprintsev, D. B. and Fersht, A. R. (2008). Algorithm for prediction of tumour suppressor p53 affinity for binding sites in DNA. Nucleic Acids Res. 36, 1589-1598. (Pubitemid 351426111)
47. Vogelstein, B., Lane, D. and Levine, A. J. (2000). Surfing the p53 network. Nature 408, 307-310.
48. Vousden, K. H. and Prives, C. (2009). Blinded by the light: the growing complexity of p53. Cell 137, 413-431.
49. Zhang, H., Cicchetti, G., Onda, H., Koon, H. B., Asrican, K., Bajraszewski, N., Vazquez, F., Carpenter, C. L. and Kwiatkowski, D. J. (2003). Loss of Tsc1/Tsc2 activates mTOR and disrupts PI3K-Akt signaling through downregulation of PDGFR. J. Clin. Invest. 112, 1223-1233. (Pubitemid 38056299)
50. Zhang, G., Hoersch, S., Amsterdam, A., Whittaker, C. A., Lees, J. A. and Hopkins, N. (2010). Highly aneuploid zebrafish malignant peripheral nerve sheath tumors have genetic alterations similar to human cancers. Proc. Natl. Acad. Sci. USA 107, 16940-16945.
51. Zon, L. I. and Peterson, R. T. (2005). In vivo drug discovery in the zebrafish. Nat. Rev. Drug Discov. 4, 35-44. (Pubitemid 40109588)