Mammalian target of rapamycin (mTOR) activation in focal cortical dysplasia and related focal cortical malformations

Experimental Neurology

Volumn 244, Issue , 2013, Pages 22-26

  Wong, Michael ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Epilepsy; Malformation of cortical development; Seizure; Tuberous sclerosis complex

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR;

BRAIN DEVELOPMENT; BRAIN MALFORMATION; CLINICAL FEATURE; CORTICAL DYSPLASIA; DISEASE CLASSIFICATION; DISEASE MODEL; EPILEPSY; EPILEPTOGENESIS; FOCAL CORTICAL MALFORMATION; HUMAN; INTRACTABLE EPILEPSY; NONHUMAN; PATHOGENESIS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; SEIZURE; TUBEROUS SCLEROSIS;

ANIMALS; HUMANS; MALFORMATIONS OF CORTICAL DEVELOPMENT; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TUBEROUS SCLEROSIS;

EID: 84877589482     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2011.10.002     Document Type: Review

References (53)

1. Aronica E., Boer K., Baybis M., Yu J., Crino P. Co-expression of cyclin D1 and phosphorylated ribosomal S6 proteins in hemimegalencephaly. Acta Neuropathol. 2007, 114:287-293.
2. Barkovich A.J., Kuzniecky R.I., Jackson G.D., Guerrini R., Dobyns W.B. A developmental and genetic classification for malformations of cortical development. Neurology 2005, 65:1873-1887.
3. Bast T., Ramantani G., Seitz A., Rating D. Focal cortical dysplasia: prevalence, clinical presentation and epilepsy in children and adults. Acta Neurol. Scand. 2006, 113:72-81.
4. Baybis M., Yu J., Lee A., Golden J.A., Weiner H., McKhann G., Aronica E., Crino P.B. mTOR cascade activation distinguishes tubers from focal cortical dysplasia. Ann. Neurol. 2004, 56:478-487.
5. Becker A.J., Urbach H., Scheffler B.J., Baden T., Normann S., Lahl R., Pennek H.W., Tuxhorn I., Elger C.E., Schramm J., Wiestler O.D., Blumcke I. Focal cortical dysplasia of Taylor's balloon cell type: mutational analysis of the TSC1 gene indicates a pathogenic relationship to Tuberous Sclerosis. Ann. Neurol. 2002, 52:29-37.
6. Bissler J.J., McCormack F.X., Young L.R., Elwing J.M., Chuck G., Leonard J.M., Schmithorst V.J., Laor T., Brody A.S., Bean J., Salibury S., Franz D.N. Sirolimus for angiomyolipoma in tuberous sclerosis complex or lymphangioleiomyomatosis. N. Engl. J. Med. 2008, 358:140-151.
7. Blumcke I., Vinters H.V., Armstrong D., Aronica E., Thom M., Spreafico R. Malformations of cortical development and epilepsies: neuropathological findings on focal cortical dysplasia. Epileptic Disord. 2009, 11:181-193.
8. Blumcke I., Thom M., Aronica E., et al. The clinicopathologic spectrum of focal cortical dysplasias: a consensus classification proposed by an ad hoc Task Force of the ILAE Diagnostic Methods Commission. Epilepsia 2011, 52:158-174.
9. Boer K., Lucassen P.J., Spliet W.G., Vreugdenhil E., van Rijen P.C., Troost D., Jansen F.E., Aronica E. Doublecortin-like (DCL) expression in focal cortical dysplasia and cortical tubers. Epilepsia 2009, 50:2629-2637.
10. Cepeda C., Andre V.M., Yamazaki I., Hauptman J.S., Chen J.Y., Vinters H.V., Mathern G.W., Levine M.S. Comparative study of cellular and synaptic abnormalities in brain tissue samples from pediatric tuberous sclerosis complex and cortical dysplasia type II. Epilepsia 2010, 51(Suppl. 3):166-170.
11. Chern J.J., Patel A.J., Jea A., Curry D.J., Comair Y.G. Surgical outcome for focal cortical dysplasia: an analysis of recent surgical series. J. Neurosurg. Pediatr. 2010, 6:452-458.
12. Chu-Shore C.J., Major P., Camposano S., Muzykewicz D., Thiele E.A. The natural history of epilepsy in tuberous sclerosis complex. Epilepsia 2010, 51:1236-1241.
13. Cohen-Gadol A.A., Ozduman K., Bronen R.A., Kim J.H., Spencer D.D. Long-term outcome after epilepsy surgery for focal cortical dysplasia. J. Neurosurg. 2004, 101:55-65.
14. Crino P.B. Focal brain malformations: a spectrum of disorders along the mTOR cascade. Novartis Found. Symp. 2007, 288:260-272.
15. Crino P.B., Nathanson K.L., Henske E.P. The tuberous sclerosis complex. N. Engl. J. Med. 2006, 355:1345-1356.
16. Ehninger D., Han S., Shiyansky C., Zhou Y., Li W., Kwaitkowski D.J., Ramesh V., Silva A.J. Reversal of learning deficits in a Tsc2+/- mouse model of tuberous sclerosis. Nat. Med. 2008, 14:843-848.
17. Fauser S., Becker A., Schulze-Bonhage A., Hildebrandt M., Tuxhorn I., Pannek H.W., Lahl R., Schramm J., Blumcke I. CD34-immunoreactive balloon cells in cortical malformations. Acta Neuropathol. 2004, 108:272-278.
18. Grajkowski W., Kotulska K., Matyja E., Larysz-Brysz M., Mandera M., Roszkowski M., Domanska-Pakilela D., Lewik-Kowalik J., Jozwiak S. Expression of tuberin and hamartin in tuberous sclerosis complex-associated and sporadic cortical dysplasia of Taylor's balloon cell type. Folia Neuropathol. 2008, 46:43-48.
19. Gumbinger C., Rohsbach C.B., Schulze-Bonhage A., Korinthenberg R., Zentner J., Haffner M., Fauser S. Focal cortical dysplasia: a genotype-phenotype analysis of polymorphisms and mutations in the TSC genes. Epilepsia 2009, 50:1396-1408.
20. Kossoff E.H., Thiele E.A., Pfeifer H.H., McGrogan J.R., Freeman J.M. Tuberous sclerosis complex and the ketogenic diet. Epilepsia 2005, 46:1684-1686.
21. Krueger D.A., Care M.M., Holland K., Agricola K., Tydor C., Mangeshkar P., Wilson K.A., Byars A., Sahmoud T., Franz D.N. Everolimus for subependymal giant-cell astrocytomas in tuberous sclerosis. N. Engl. J. Med. 2010, 363:1801-1811.
22. Kuzniecky R.I. Malformations of cortical development and epilepsy, part 1: diagnosis and classification scheme. Rev. Neurol. Dis. 2006, 3:151-162.
23. Kwon C.H., Zhu X., Zhang J., Baker S.J. mTOR is required for hypertrophy of Pten-deficient neuronal soma in vivo. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:12923-12928.
24. Lamparello P., Baybis M., Pollard J., Hol E.M., Eisenstat D.D., Aronica E., Crino P.B. Developmental lineage of cell types in cortical dysplasia with balloon cells. Brain 2007, 130:2267-2276.
25. Lee A., Maldanado M., Baybis M., Walsh C.A., Scheithauer B., Yeung R., Parent J., Weiner H.L., Crino P.B. Markers of cellular proliferation are expressed in cortical tubers. Ann. Neurol. 2003, 53:668-673.
26. Ljungberg M.C., Bhattacharjee M.B., Lu Y., Armstrong D.L., Yoshor D., Swann J.W., Sheldon M., D'Arcangelo G. Activation of mammalian target of rapamycin in cytomegalic neurons of human cortical dysplasia. Ann. Neurol. 2006, 60:420-429.
27. Ljungberg M.C., Sunnen C.N., Lugo J.N., Anderson A.E., D'Arcangelo G. Rapamycin suppresses seizures and neuronal hypertrophy in a mouse model of cortical dysplasia. Dis. Model. Mech. 2009, 2:389-398.
28. Lugnier C., Majores M., Fassunke J., Pernhorst K., Niehusmann P., Simon M., Nellist M., Schoch S., Becker A. Hamartin variants that are frequent in focal dysplasias and cortical tubers have reduced tuberin binding and aberrant subcellular distribution in vitro. J. Neuropathol. Exp. Neurol. 2009, 68:1136-1146.
29. Madhavan D., Schaffer S., Yankovsky A., Arzimanoglou A., Renaldo F., Zaorff C.M., LaJoie J., Weiner H.L., Andermann E., Franz D.N., Leonard J., Connolly M., Cascino G.D., Devinsky O. Surgical outcome in tuberous sclerosis complex: a multicenter survey. Epilepsia 2007, 48:1625-1628.
30. Major P., Rakowski S., Simon M.V., Cheng M.L., Eskandar E., Baron J., Leeman B.A., Frosch M.P., Thiele E.A. Are cortical tubers epileptogenic? Evidence from electrocorticography. Epilepsia 2009, 50:147-154.
31. Meikle L., Pollizzi K., Egnor A., Kramvis I., Lane H., Sahin M., Kwiatkowski D.J. Response of a neuronal model of tuberous sclerosis to mammalian target of rapamycin (mTOR) inhibitors: effects on mTORC1 and Akt signaling lead to improved survival and function. J. Neurosci. 2008, 28:5422-5432.
32. Miyata H., Chiang A.C.Y., Vinters H.V. Insulin signaling pathways in cortical dysplasia and TSC-tubers: tissue microarray analysis. Ann. Neurol. 2004, 56:510-519.
33. Mizuguchi M., Yamanouchi Hl, Becker L.E., Itoh M., Takshima S. Doublecortin immunoreactivity in giant cells of tuberous sclerosis and focal cortical dysplasia. Acta Neuropathol. 2002, 104:418-424.
34. Muncy J., Butler I.J., Koenig M.K. Rapamycin reduces seizure frequency in tuberous sclerosis complex. J. Child Neurol. 2009, 24:477.
35. Orlova K.A., Parker W.E., Heuer G.G., Tsai V., Yoon J., Baybis M., Fenning R.S., Strauss K., Crino P.B. STRADa deficiency results in aberrant mTORC1 signaling during corticogenesis. J. Clin. Invest. 2010, 120:1591-1602.
36. Palmini A., Najm I., Avanzini G., Babb T., Guerrini R., Foldvary-Schaefer N., Jackson G., Luders H.O., Prayson R., Spreafico R., Vinters H.V. Terminology and classification of cortical dysplasias. Neurology 2004, 62(Suppl. 3):S2-S8.
37. Samadani U., Judkins A., Akpalu A., Aronica E., Crino P.B. Differential gene expression in neurons and astrocytes in ganglioglioma. Epilepsia 2007, 48:646-653.
38. Sarbassov D.D., Ali S.M., Sabatini D.M. Growing roles for the mTOR pathway. Curr. Opin. Cell Biol. 2005, 17:596-603.
39. Schick V., Majores M., Engels G., Hartmann W., Elger C.E., Schramm J., Schoch S., Becker A.J. Differential Pi3K-pathway activation in cortical tubers and focal cortical dysplasias with balloon cells. Brain Pathol. 2007, 17:165-173.
40. Schonberger A., Niehusmann P., Urbach H., Majores M., Grote A., Holthausen H., Blumcke I., Deckert M., Becker A.J. Increased frequency of distinct TSC2 alleleic variants in focal cortical dysplasias with balloon cells and mineralization. Neuropathology 2009, 29:559-565.
41. Sisodiya S.M. Malformations of cortical development: burdens and insights from important causes of human epilepsy. Lancet Neurol. 2004, 3:29-38.
42. Sparagana S.P., Delgado M.R., Batchelor L.L., Roach E.S. Seizure remission and antiepileptic drug discontinuation in children with tuberous sclerosis complex. Arch. Neurol. 2003, 60:1286-1289.
43. Tassi L., Colombo N., Garbelli R., Francione S., Lo Russo G., Mai R., Cardinale F., Cossu M., Ferrario A., Galli C., Bramerio M., Citterio A., Spreafico R. Focal cortical dysplasia: neuropathological subtypes, EEG, neuroimaging and surgical outcome. Brain 2002, 125:1719-1732.
44. Uhlmann E.J., Wong M., Baldwin R.L., Bajenaru M.L., Onda H., Kwiatkowski D.J., Yamada K.A., Gutmann D.H. Astrocyte-specific TSC1 conditional knockout mice exhibit abnormal neuronal organization and seizures. Ann. Neurol. 2002, 52:285-296.
45. Way S.W., McKenna J., Mietzsch U., Reith R.M., Wu H.C., Gambello M.J. Loss of Tsc2 in radial glia models the brain pathology of tuberous sclerosis complex in the mouse. Hum. Mol. Genet. 2009, 18:1252-1265.
46. Weiner H.L., Carlson C., Ridgway E.B., Zaroff C.M., Miles D., LaJoie J., Devinsky O. Epilepsy surgery in young children with tuberous sclerosis: results of a novel approach. Pediatrics 2006, 117:1494-1502.
47. Wong M. Mechanisms of epileptogenesis in tuberous sclerosis complex and related malformations of cortical development involving abnormal glioneuronal proliferation. Epilepsia 2008, 49:8-21.
48. Wong M. Mammalian target of rapamycin (mTOR) inhibition as potential antiepileptogenic therapy: From tuberous sclerosis to common acquired epilepsies. Epilepsia 2010, 51:27-36.
49. Wong M., Ess K.E., Uhlmann E.J., Jansen L.A., Li W., Crino P.B., Mennerick S., Yamada K.A., Gutmann D.H. Impaired astrocyte glutamate transport in a mouse epilepsy model of tuberous sclerosis complex. Ann. Neurol. 2003, 54:251-256.
50. Yasin S.A., Latak K., Becherini F., Ganapathi A., Miller K., Campos O., Picker S.R., Bier N., Smith M., Thom M., Anderson G., Cross J.H., Harkness W., Harding B., Jacques T.S. Balloon cells in human cortical dysplasia and tuberous sclerosis: isolation of a pathological progenitor-like cell. Acta Neuropathol. 2010, 120:85-96.
51. Zeng L.H., Xu L., Gutmann D.H., Wong M. Rapamycin prevents epilepsy in a mouse model of tuberous sclerosis complex. Ann. Neurol. 2008, 63:444-453.
52. Zeng L.H., Rensing N.R., Zhang B., Gutmann D.H., Gambello M.J., Wong M. Tsc2 gene inactivation causes a more severe epilepsy phenotype than Tsc1 inactivation in a mouse model of tuberous sclerosis complex. Hum. Mol. Genet. 2011, 20:445-454.
53. Zhou J., Blundell J., Ogawa S., Kwon C.H., Zhang W., Sinton C., Powell C.M., Parada L.F. Pharmacological inhibition of mTORC1 suppresses anatomical, cellular, and behavioral abnormalities in neural-specific Pten knock-out mice. J. Neurosci. 2009, 29:1773-1783.