Rapamycin suppresses seizures and neuronal hypertrophy in a mouse model of cortical dysplasia

DMM Disease Models and Mechanisms

Volumn 2, Issue 7-8, 2009, Pages 389-398

  Ljungberg, M Cecilia ^a   Sunnen, C Nicole ^a   Lugo, Joaquin N ^a   Anderson, Anne E ^a   D'Arcangelo, Gabriella ^b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; RAPAMYCIN; IMMUNOSUPPRESSIVE AGENT; PROTEIN KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; CONTROLLED STUDY; CORTICAL DYSPLASIA; DISEASE SEVERITY; ELECTROENCEPHALOGRAM; ENZYME ACTIVITY; GENE DELETION; GENE DISRUPTION; GENOTYPE; HYPERTROPHY; LOXP SITE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEIZURE; SIGNAL TRANSDUCTION; ANIMAL; DISEASE MODEL; ELECTROENCEPHALOGRAPHY; METABOLISM; METHODOLOGY; MOUSE MUTANT; MUTATION; NERVE CELL; PATHOLOGY; PHENOTYPE;

ANIMALIA; MAMMALIA; MUS;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; DISEASE MODELS, ANIMAL; ELECTROENCEPHALOGRAPHY; GENE DELETION; HYPERTROPHY; IMMUNOSUPPRESSIVE AGENTS; MALFORMATIONS OF CORTICAL DEVELOPMENT; MICE; MICE, KNOCKOUT; MUTATION; NEURONS; PHENOTYPE; PROTEIN KINASES; SEIZURES; SIROLIMUS;

EID: 68349100270     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.002386     Document Type: Article

References (37)

1. Backman, S. A., Stambolic, V., Suzuki, A., Haight, J., Elia, A., Pretorius, J., Tsao, M. S., Shannon, P., Bolon, B., Ivy, G. O. et al. (2001). Deletion of Pten in mouse brain causes seizures, ataxia and defects in soma size resembling Lhermitte-Duclos disease. Nat. Genet. 29, 396-403. (Pubitemid 34326689)
2. Backman, S., Stambolic, V. and Mak, T. (2002). PTEN function in mammalian cell size regulation. Curr. Opin. Neurobiol. 12, 516-522. (Pubitemid 35284086)
3. Baybis, M., Yu, J., Lee, A., Golden, J. A., Weiner, H., McKhann, G., 2nd, Aronica, E. and Crino, P. B. (2004). mTOR cascade activation distinguishes tubers from focal cortical dysplasia. Ann. Neurol. 56, 478-487.
4. Butler, M. G., Dasouki, M. J., Zhou, X. P., Talebizadeh, Z., Brown, M., Takahashi, T. N., Miles, J. H., Wang, C. H., Stratton, R., Pilarski, R. et al. (2005). Subset of individuals with autism spectrum disorders and extreme macrocephaly associated with germline PTEN tumour suppressor gene mutations. J. Med. Genet. 42, 318-321. (Pubitemid 40523954)
5. Cepeda, C., Andre, V. M., Levine, M. S., Salamon, N., Miyata, H., Vinters, H. V. and Mathern, G. W. (2006). Epileptogenesis in pediatric cortical dysplasia: the dysmature cerebral developmental hypothesis. Epilepsy Behav. 9, 219-235. (Pubitemid 44307962)
6. Chow, L. M. and Baker, S. J. (2006). PTEN function in normal and neoplastic growth. Cancer Lett. 241, 184-196. (Pubitemid 44163047)
7. Eng, C. (2003). PTEN: one gene, many syndromes. Hum. Mutat. 22, 183-198.
8. Eshleman, J. S., Carlson, B. L., Mladek, A. C., Kastner, B. D., Shide, K. L. and Sarkaria, J. N. (2002). Inhibition of the mammalian target of rapamycin sensitizes U87 xenografts to fractionated radiation therapy. Cancer Res. 62, 7291-7297.
9. European Chromosome 16 Tuberous Sclerosis Consortium (1993). Identification and characterization of the tuberous sclerosis gene on chromosome 16. Cell 75, 1305-1315. (Pubitemid 24021906)
10. 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)
11. Fraser, M. M., Zhu, X., Kwon, C. H., Uhlmann, E. J., Gutmann, D. H. and Baker, S. J. (2004). Pten loss causes hypertrophy and increased proliferation of astrocytes in vivo. Cancer Res. 64, 7773-7779. (Pubitemid 39446909)
12. Gabis, L., Pomeroy, J. and Andriola, M. R. (2005). Autism and epilepsy: cause, consequence, comorbidity, or coincidence? Epilepsy Behav. 7, 652-656. (Pubitemid 43013011)
13. Goffin, A., Hoefsloot, L. H., Bosgoed, E., Swillen, A. and Fryns, J. P. (2001). PTEN mutation in a family with Cowden syndrome and autism. Am. J. Med. Genet. 105, 521-524. (Pubitemid 32729819)
14. Harris, T. E. and Lawrence, J. C., Jr (2003). TOR signaling. Sci STKE 2003, re15.
15. Holmes, G. L. and Stafstrom, C. E. (2007). Tuberous sclerosis complex and epilepsy: recent developments and future challenges. Epilepsia 48, 617-630.
16. Hou, L. and Klann, E. (2004). Activation of the phosphoinositide 3-kinase-Aktmammalian target of rapamycin signaling pathway is required for metabotropic glutamate receptor-dependent long-term depression. J. Neurosci. 24, 6352-6361. (Pubitemid 38944226)
17. Jaworski, J., Spangler, S., Seeburg, D. P., Hoogenraad, C. C. and Sheng, M. (2005). Control of dendritic arborization by the phosphoinositide-3′- kinase-Akt-mammalian target of rapamycin pathway. J. Neurosci. 25, 11300-11312. (Pubitemid 43083704)
18. Kumar, V., Zhang, M. X., Swank, M. W., Kunz, J. and Wu, G. Y. (2005). Regulation of dendritic morphogenesis by Ras-PI3K-Akt-mTOR and Ras-MAPK signaling pathways. J. Neurosci. 25, 11288-11299. (Pubitemid 43083703)
19. Kwon, C. H., Zhu, X., Zhang, J., Knoop, L. L., Tharp, R., Smeyne, R. J., Eberhart, C. G., Burger, P. C. and Baker, S. J. (2001). Pten regulates neuronal soma size: a mouse model of Lhermitte-Duclos disease. Nat. Genet. 29, 404-411. (Pubitemid 34326690)
20. Kwon, C. H., Zhu, X., Zhang, J. and Baker, S. J. (2003). mTor is required for hypertrophy of Pten-deficient neuronal soma in vivo. Proc. Natl. Acad. Sci. USA 100, 12923-12928. (Pubitemid 37340001)
21. Kwon, C. H., Luikart, B. W., Powell, C. M., Zhou, J., Matheny, S. A., Zhang, W., Li, Y., Baker, S. J. and Parada, L. F. (2006). Pten regulates neuronal arborization and social interaction in mice. Neuron 50, 377-388.
22. Leevers, S. J., Vanhaesebroeck, B. and Waterfield, M. D. (1999). Signalling through phosphoinositide 3-kinases: the lipids take centre stage. Curr. Opin. Cell Biol. 11, 219-225. (Pubitemid 29164037)
23. Li, J., Yen, C., Liaw, D., Podsypanina, K., Bose, S., Wang, S. I., Puc, J., Miliaresis, C., Rodgers, L., McCombie, R. et al. (1997). PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. Science 275, 1943-1947. (Pubitemid 27148818)
24. Ljungberg, M. C., Bhattacharjee, M. B., Lu, Y., Armstrong, D. L., Yoshor, D., Swann, J. W., Sheldon, M. and D'Arcangelo, G. (2006). Activation of mammalian target of rapamycin in cytomegalic neurons of human cortical dysplasia. Ann. Neurol. 60, 420-429. (Pubitemid 44684978)
25. Maehama, T. and Dixon, J. E. (1998). The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. J. Biol. Chem. 273, 13375-13378. (Pubitemid 28268370)
26. Miyata, H., Chiang, A. C. and Vinters, H. V. (2004). Insulin signaling pathways in cortical dysplasia and TSC-tubers: tissue microarray analysis. Ann. Neurol. 56, 510-519. (Pubitemid 39319341)
27. Ogawa, S., Kwon, C. H., Zhou, J., Koovakkattu, D., Parada, L. F. and Sinton, C. M. (2007). A seizure-prone phenotype is associated with altered free-running rhythm in Pten mutant mice. Brain Res. 1168, 112-123. (Pubitemid 47320632)
28. Podsypanina, K., Ellenson, L. H., Nemes, A., Gu, J., Tamura, M., Yamada, K. M., Cordon-Cardo, C., Catoretti, G., Fisher, P. E. and Parsons, R. (1999). Mutation of Pten/Mmac1 in mice causes neoplasia in multiple organ systems. Proc. Natl. Acad. Sci. USA 96, 1563-1568.
29. Raab-Graham, K. F., Haddick, P. C., Jan, Y. N. and Jan, L. Y. (2006). Activity- and mTOR-dependent suppression of Kv1.1 channel mRNA translation in dendrites. Science 314, 144-148.
30. Ruegg, S., Baybis, M., Juul, H., Dichter, M. and Crino, P. B. (2007). Effects of rapamycin on gene expression, morphology, and electrophysiological properties of rat hippocampal neurons. Epilepsy Res. 77, 85-92. (Pubitemid 350137689)
31. 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.
32. Suzuki, A., de la Pompa, J. L., Stambolic, V., Elia, A. J., Sasaki, T., del Barco Barrantes, I., Ho, A., Wakeham, A., Itie, A., Khoo, W. et al. (1998). High cancer susceptibility and embryonic lethality associated with mutation of the PTEN tumor suppressor gene in mice. Curr. Biol. 8, 1169-1178. (Pubitemid 28494715)
33. Tavazoie, S. F., Alvarez, V. A., Ridenour, D. A., Kwiatkowski, D. J. and Sabatini, B. L. (2005). Regulation of neuronal morphology and function by the tumor suppressors Tsc1 and Tsc2. Nat. Neurosci. 8, 1727-1734.
34. van Slegtenhorst, M., de Hoogt, R., Hermans, C., Nellist, M., Janssen, B., Verhoef, S., Lindhout, D., van den Ouweland, A., Halley, D., Young, J. et al. (1997). Identification of the tuberous sclerosis gene TSC1 on chromosome 9q34. Science 277, 805-808. (Pubitemid 27366729)
35. Vinters, H. V., Park, S. H., Johnson, M. W., Mischel, P. S., Catania, M. and Kerfoot, C. (1999). Cortical dysplasia, genetic abnormalities and neurocutaneous syndromes. Dev. Neurosci. 21, 248-259.
36. Zeng, L. H., Xu, L., Gutman, D. H. and Wong, M. (2008). Rapamycin prevents epilepsy in a mouse model of Tuberous Sclerosis Complex. Ann. Neurol. 63, 444-453. (Pubitemid 351614710)
37. Zori, R. T., Marsh, D. J., Graham, G. E., Marliss, E. B. and Eng, C. (1998). Germline PTEN mutation in a family with Cowden syndrome and Bannayan-Riley-Ruvalcaba syndrome. Am. J. Med. Genet. 80, 399-402. (Pubitemid 28541607)