MTOR-dependent abnormalities in autophagy characterize human malformations of cortical development: Evidence from focal cortical dysplasia and tuberous sclerosis

Acta Neuropathologica

Volumn 126, Issue 2, 2013, Pages 207-218

  Yasin, Shireena A ^a,b   Ali, Abu M ^a   Tata, Mathew ^a   Picker, Simon R ^a,b,c   Anderson, Glenn W ^b   Latimer Bowman, Elizabeth ^b   Nicholson, Sarah L ^b   Harkness, William ^a,b   Cross, J Helen ^a,b   Paine, Simon M L ^a,b   Jacques, Thomas S ^a,b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b GREAT ORMOND STREET HOSPITAL   (United Kingdom)

^c NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

Autophagy; Balloon cells; Epilepsy; Focal cortical dysplasia; Tuberous sclerosis

Indexed keywords

LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN P62;

ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CELL DIFFERENTIATION; CELL NUCLEUS; CELL VACUOLE; CONTROLLED STUDY; CORTICAL DYSPLASIA; CYTOPLASM; DOR GENE; ENZYME ACTIVITY; GENE; GLIA; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; LYSOSOME; NERVE CELL; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; TUBEROUS SCLEROSIS;

ACID PHOSPHATASE; AUTOPHAGY; BRAIN; BRAIN DISEASES; CELLS, CULTURED; CHILD; CYTOPLASM; HUMANS; IMMUNOHISTOCHEMISTRY; LYSOSOME-ASSOCIATED MEMBRANE GLYCOPROTEINS; LYSOSOMES; MALFORMATIONS OF CORTICAL DEVELOPMENT; RNA-BINDING PROTEINS; TISSUE BANKS; TOR SERINE-THREONINE KINASES; TUBEROUS SCLEROSIS;

EID: 84881109740     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-013-1135-4     Document Type: Article

References (41)

1. Baek S-H, Kim E-K, Goudreau JL, Lookingland KJ, Kim SW, Yu S-W (2009) Insulin withdrawal-induced cell death in adult hippocampal neural stem cells as a model of autophagic cell death. Autophagy 5(2):277-279
2. Baumgartner BG, Orpinell M, Duran J et al (2007) Identification of a novel modulator of thyroid hormone receptor-mediated action. PLoS ONE 2(11):e1183
3. Baybis M, Yu J, Lee A, Golden JA, Weiner H, Mckhann G, Aronica E, Crino PB (2004) mTOR cascade activation distinguishes tubers from focal cortical dysplasia. Ann Neurol 56(4):478-487
4. Becker AJ, Urbach H, Scheffler B et al (2002) Focal cortical dysplasia of Taylor's balloon cell type: mutational analysis of the TSC1 gene indicates a pathogenic relationship to tuberous sclerosis. Ann Neurol 52(1):29-37
5. Berg AT, Mathern GW, Bronen RA, Fulbright RK, DiMario F, Testa FM, Levy SR (2009) Frequency, prognosis and surgical treatment of structural abnormalities seen with magnetic resonance imaging in childhood epilepsy. Brain 132(Pt 10):2785-2797
6. Bjorkoy G (2005) p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol 171(4):603-614
7. Blümcke I, Thom M, Aronica E et al (2011) The clinicopathologic spectrum of focal cortical dysplasias: a consensus classification proposed by an ad hoc Task Force of the ILAE Diagnostic Methods Commission. Epilepsia 52(1):158-174
8. Chen J, Tsai V, Parker WE, Aronica E, Baybis M, Crino PB (2012) Detection of human papillomavirus in human focal cortical dysplasia type IIB. Ann Neurol 72(6):881-892
9. Choo AY, Yoon S-O, Kim SG, Roux PP, Blenis J (2008) Rapamycin differentially inhibits S6Ks and 4E-BP1 to mediate cell-type-specific repression of mRNA translation. Proc Natl Acad Sci USA 105(45):17414-17419
10. Crino PB, Trojanowski JQ, Eberwine J (1997) Internexin, MAP1B, and nestin in cortical dysplasia as markers of developmental maturity. Acta Neuropathol 93(6):619-627
11. Crino PB (2011) mTOR: a pathogenic signaling pathway in developmental brain malformations. Trends Mol Med 17(12):734-742
12. Crino PB (2013) Evolving neurobiology of tuberous sclerosis complex. Acta Neuropathol 125(3):317-332
13. Glick D, Barth S, Macleod KF (2010) Autophagy: cellular and molecular mechanisms. J Pathol 221(1):3-12
14. Grajkowska W, Kotulska K, Matyja E, Larysz-Brysz M, Mandera M, Roszkowski M, Domańska-Pakieła D, Lewik-Kowalik J, Jozwiak S (2008) Expression of tuberin and hamartin in tuberous sclerosis complex-associated and sporadic cortical dysplasia of Taylor's balloon cell type. Folia Neuropathol 46(1):43-48
15. Hall MN (2008) mTOR-what does it do? TPS 40(10 Suppl):S5-S8
16. Hosokawa N, Hara T, Kaizuka T et al (2009) Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy. Mol Biol Cell 20(7):1981-1991
17. Ichimura Y, Komatsu M (2010) Selective degradation of p62 by autophagy. Semin Immunopathol 32(4):431-436
18. Joint Epilepsy Council (2011) Epilepsy prevalence, incidence and other statistics. Available via http://www.jointepilepsycouncil.org.uk/resources/ publications.html
19. Jozwiak J, Jozwiak S, Wlodarski P (2008) Possible mechanisms of disease development in tuberous sclerosis. Lancet Oncol 9(1):73-79
20. Jung CH, Jun CB, Ro S-H, Kim Y-M, Otto NM, Cao J, Kundu M, Kim D-H (2009) ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol Biol Cell 20(7):1992-2003
21. Kim J, Kundu M, Viollet B, Guan K-L (2011) AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol 13(2):132-141
22. Kurtz Z, Tookey P, Ross E (1998) Epilepsy in young people: 23 year follow up of the British national child development study. BMJ 316(7128):339-342
23. Lamparello P, Baybis M, Pollard J, Hol EM, Eisenstat DD, Aronica E, Crino PB (2007) Developmental lineage of cell types in cortical dysplasia with balloon cells. Brain 130(Pt 9):2267-2276
24. Ljungberg MC, Bhattacharjee MB, Lu Y, Armstrong DL, Yoshor D, Swann JW, Sheldon M, D'arcangelo G (2006) Activation of mammalian target of rapamycin in cytomegalic neurons of human cortical dysplasia. Ann Neurol 60(4):420-429
25. Lugnier C, Majores M, Fassunke J, Pernhorst K, Niehusmann P, Simon M, Nellist M, Schoch S, Becker A (2009) 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 68(10):1136-1146
26. Ma J-F, Huang Y, Chen S-D, Halliday G (2010) Immunohistochemical evidence for macroautophagy in neurones and endothelial cells in Alzheimer's disease. Neuropathol Appl Neurobiol 36(4):312-319
27. Mauvezin C, Orpinell M, Francis VA, Mansilla F, Duran J, Ribas V, Palacín M, Boya P, Teleman AA, Zorzano A (2010) The nuclear cofactor DOR regulates autophagy in mammalian and Drosophila cells. EMBO Rep 11(1):37-44
28. Mauvezin C, Sancho A, Ivanova S, Palacín M, Zorzano A (2012) DOR undergoes nucleo-cytoplasmic shuttling, which involves passage through the nucleolus. FEBS Lett 586(19):3179-3186
29. McMahon J, Huang X, Yang J, Komatsu M, Yue Z, Qian J, Zhu X, Huang Y (2012) Impaired autophagy in neurons after disinhibition of mammalian target of rapamycin and its contribution to epileptogenesis. J Neurosci 32(45):15704-15714
30. Miyahara H, Natsumeda M, Shiga A et al (2013) Suppressed expression of autophagosomal protein LC3 in cortical tubers of tuberous sclerosis complex. Brain Pathol 23(3):254-262
31. Miyata H, Chiang ACY, Vinters HV (2004) Insulin signaling pathways in cortical dysplasia and TSC-tubers: tissue microarray analysis. Ann Neurol 56(4):510-519
32. Mizuguchi M, Ikeda K, Takashima S (2000) Simultaneous loss of hamartin and tuberin from the cerebrum, kidney and heart with tuberous sclerosis. Acta Neuropathol 99(5):503-510
33. Mizuguchi M, Kato M, Yamanouchi H, Ikeda K, Takashima S (1996) Loss of tuberin from cerebral tissues with tuberous sclerosis and astrocytoma. Ann Neurol 40(6):941-944
34. Schick V, Majores M, Engels G, Hartmann W, Elger CE, Schramm J, Schoch S, Becker AJ (2007) Differential Pi3K-pathway activation in cortical tubers and focal cortical dysplasias with balloon cells. Brain Pathol 17(2):165-173
35. Schick V, Majores M, Koch A, Elger CE, Schramm J, Urbach H, Becker AJ (2007) Alterations of phosphatidylinositol 3-kinase pathway components in epilepsy-associated glioneuronal lesions. Epilepsia 48(Suppl 5):65-73
36. Sebire N, Malone M, Ashworth M, Jacques TS (2010) Diagnostic Pediatric Surgical Pathology. Elsevier, London
37. Urbach H, Scheffler B, Heinrichsmeier T, von Oertzen J, Kral T, Wellmer J, Schramm J, Wiestler OD, Blümcke I (2002) Focal cortical dysplasia of Taylor's balloon cell type: a clinicopathological entity with characteristic neuroimaging and histopathological features, and favorable postsurgical outcome. Epilepsia 43(1):33-40
38. Vázquez P, Arroba AI, Cecconi F, de la Rosa EJ, Boya P, de Pablo F (2012) Atg5 and Ambra1 differentially modulate neurogenesis in neural stem cells. Autophagy 8((2):187-199
39. Yasin SA, Latak K, Becherini F et al (2010) Balloon cells in human cortical dysplasia and tuberous sclerosis: isolation of a pathological progenitor-like cell. Acta Neuropathol 120(1):85-96
40. Ying Z, Gonzalez-Martinez J, Tilelli C, Bingaman W, Najm I (2005) Expression of neural stem cell surface marker CD133 in balloon cells of human focal cortical dysplasia. Epilepsia 46(11):1716-1723
41. Yu L, Mcphee CK, Zheng L et al (2010) Termination of autophagy and reformation of lysosomes regulated by mTOR. Nature 465(7300):942-946