ABC-transporters as stem-cell markers in brain dysplasia/tumor epilepsies

Frontiers in Bioscience - Landmark

Volumn 19, Issue 8, 2014, Pages 1425-1435

  Czornyj, Lilliana ^a   Lazarowski, Alberto ^b,c  

^a Hospital de Pediatria SAMIC Prof Dr Juan P Garrahan   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c Fundacion Investigar   (Argentina)

Author keywords

ABC transporters; Brain tumors; Epileptogenesis; MCD; Review; Stem cell markers

Indexed keywords

ABC TRANSPORTER; ANTICONVULSIVE AGENT; BIOLOGICAL MARKER;

BRAIN; BRAIN TUMOR; COMPLICATION; CORTICAL DYSPLASIA; DRUG RESISTANCE; EPILEPSY; HUMAN; METABOLISM; PATHOLOGY; STEM CELL;

ANTICONVULSANTS; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL MARKERS; BRAIN; BRAIN NEOPLASMS; DRUG RESISTANCE; EPILEPSY; HUMANS; MALFORMATIONS OF CORTICAL DEVELOPMENT; STEM CELLS;

EID: 84904571846     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/4293     Document Type: Article

References (90)

1. National Institutes of Health. Consensus conference: Surgery for epilepsy. JAMA; 264:729-33 (1990)
2. Theodore, W. H., S. S. Spencer, S. Wiebe, J. T. Langfitt, A. Ali, P. O. Shafer, A. T. Berg and B. G. Vickrey. Epilepsy in North America: a report prepared under the auspices of the global campaign against epilepsy, the International Bureau for Epilepsy, the International League Against Epilepsy, and the World Health Organization. Epilepsia 47:1700-1722 (2006) (Pubitemid 44556405)
3. Berg, A. T. Identification of pharmacoresistant epilepsy. Neurol Clin 27:1003-13 (2009)
4. Kwan, P. and J. W. Sander. The natural history of epilepsy: an epidemiological view. J Neurol Neurosurg Psychiatry 75:1376-1381 (2004) (Pubitemid 39279801)
5. Kwan P, Brodie MJ. Early identification of refractory epilepsy. New Engl J Med 342:314-319 (2000) (Pubitemid 30075244)
6. Lazarowski, A. and L. Czornyj. Potential role of multidrug resistant proteins in refractory epilepsy and antiepileptic drugs interactions. Drug Metab Drug Interact 26:21-26 (2011)
7. Gallyasa, F., V. Kiglicsb, P. Baracskayb, G. Juhászb and A. Czurkób. The mode of death of epilepsy-induced "dark" neurons is neither necrosis nor apoptosis: An electronmicroscopic study. Brain Res 1239:207-215 (2008)
8. del Zoppo, G. J. Focus on research stroke and neurovascular protection. N Engl J Med 6:553-555 (2006) (Pubitemid 43209102)
9. Merelli, A., L. Czornyj and A. Lazarowski. Erythropoietin: a neuroprotective agent in cerebral hypoxia, neurodegeneration, and epilepsy. Curr Pharm Des 19:6791-801 (2013)
10. Blanc, F., L. Martinian, I. Liagkouras, C. Catarino, S. M. Sisodiya and M. Thom. Investigation of widespread neocortical pathology associated with hippocampal sclerosis in epilepsy: a postmortem study. Epilepsia 52(1):10-21 (2011)
11. Di Maio, R. Neuronal mechanisms of epileptogenesis. Front Cell Neurosci.; 8:29 (2014)
12. Pitkänen, A. and K. Lukasiuk. Mechanisms of epileptogenesis and potential treatment targets. Lancet Neurol 10:173-86 (2011)
13. Lazarowski, A. and L. Czornyj. "Genetics of Epilepsy and Refractory Epilepsy". Colloquium Series on: The Genetic Basis of Human Disease. Editor: Michael Dean, Ph. D. Copyright ©; by Morgan & Claypool Life Sciences (2013)
14. Magri, L., M. Cambiaghi, M. Cominelli, C. Alfaro-Cervello, M. Cursi, M. Pala, A. Bulfone, J. M. García-Verdugo, L. Leocani, F. Minicucci, P. L. Poliani and R. Galli. Sustained activation of mTOR pathway in embryonic neural stem cells leads to development of tuberous sclerosis complex-associated lesions. Cell Stem Cell 9:447-462 (2011)
15. Cepeda, C., V. M. André, J. S. Hauptman, I. Yamazaki, M. N. Huynh, J. W. Chang, J. Y. Chen, R. S. Fisher, H. V. Vinters, M. S. Levine and G. W. Mathern. Enhanced GABAergic network and receptor function in pediatric cortical dysplasia Type IIB compared with Tuberous Sclerosis Complex. Neurobiol Dis 45:310-321 (2012)
16. van Breemen, M., E. B. Wilms and C. J. Vecht. Epilepsy in patients with brain tumours: epidemiology, mechanisms, and management. Lancet Neurol 6:421-30 (2007) (Pubitemid 46551867)
17. Ferrier, C. H., E. Aronica, F. S. Leijten, W. G. Spliet, A. C. van Huffelen, P. C. van Rijen, and C. D. Binnie. Electrocorticographic discharge patterns in glioneuronal tumors and focal cortical dysplasia. Epilepsia 47:1477-86 (2006) (Pubitemid 44393860)
18. Blümcke, I. Neuropathology of focal epilepsies: A critical review. Epilepsy Behav 15:34-39 (2009)
19. Wadkins, R. M. and P. D. Roepe. Biophysical aspect of P-glycoprotein mediated multidrug resistance. Int Rev Cytol 171:121-65 (1997)
20. Auzmendi, J. A., S. Orozco-Suárez, I. Bañuelos-Cabrera, M. E. González-Trujano, E. C. González, L. Rocha and A. Lazarowski. P-glycoprotein contributes to cell membrane depolarization of hippocampus and neocortex in a model of repetitive seizures induced by pentylenetetrazole in rats. Current Pharm Desing 19, 38:6732-6738 (2013)
21. Brodtkorb, E., G. Nilsen, O. Smevik and PA Rinck. Epilepsy and anomalies of neuronal migration: MRI and clinical aspects. Acta Neurol Scand 86:24-32 (1992)
22. Huang, J. and B. D. Manning. The TSC1-TSC2 complex: a molecular switchboard controlling cell growth. Biochem J 412:179-90 (2008) (Pubitemid 351758225)
23. Chan, J. A., H. Zhang, P. S. Roberts, S. Jozwiak, G. Wieslawa, J. Lewin-Kowalik, K. Kotulska, and D. J. Kwiatkowski. Pathogenesis of tuberous sclerosis subependymal giant cell astrocytomas: biallelic inactivation of TSC1 or TSC2 leads to mTOR activation. J Neuropathol Exp Neurol 63:1236-42 (2004) (Pubitemid 39603395)
24. Avellino, A. M., M. S. Berger, R. C. Rostomily, C. M. Shaw and G. A. Ojemann. Surgical management and seizure outcome in patients with tuberous sclerosis. J Neurosurg 87:391-6 (1997) (Pubitemid 27362571)
25. Crino, P. B., H. Miyata and H. V. Vinters. Neurodevelopmental disorders as a cause of seizures: Neuropathologic, genetic, and mechanistic considerations. Brain Pathol 12:212-33 (2002) (Pubitemid 34259924)
26. Louis, D. N., H. Ohgaki, O. D. Wiestler, W. K. Cavenee, P. C. Burger, A. Jouvet, B. W. Scheithauer, P. Kleihues. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 114:97-109 (2007) Review. (Pubitemid 47103521)
27. Kim, S. K., K. C. Wang, B. K. Cho, H. W. Jung, Y. J. Lee, Y. S. Chung, J. Y. Lee, S. H. Park, Y. M. Kim, G. Choe and J. G. Chi. Biological behavior and tumorigenesis of subependymal giant cell astrocytomas. J Neurooncol 52:217-225 (2001) (Pubitemid 33638520)
28. Frèrebeau, P., J. Benezech, F. Segnarbieux, H. Harbi, A. Desy and C. Marty-Double. Intraventricular tumors in tuberous sclerosis. Childs Nerv Syst 1:45-8 (1985) (Pubitemid 15020990)
29. Shepherd, C. W., B. Scheithauer, and M. R. Gomez. Brain tumors in tuberous sclerosis: a clinicopathologic study of the Mayo clinic experience. Ann N Y Acad Sci 615:378-9 (1991)
30. Riva, M. Brain tumoral epilepsy: a review. Neurol Sci 26(suppl 1):S40-S42 (2005) (Pubitemid 40637367)
31. Calatozzolo, C., M. Gelati, E. Ciusani, F. L. Sciacca, B. Pollo, L. Cajola, C. Marras, A. Silvani, L. Vitellaro-Zuccarello, D. Croci, A. Boiardi and A. Salmaggi. Expression of drug resistance proteins Pgp, MRP1, MRP3, MRP5 and GST-pi in human glioma. J Neurooncol 74:113-21 (2005) (Pubitemid 41478906)
32. Aronica, E., J. A. Gorter, G. H. Jansen, C. W. van Veelen, P. C. van Rijen, S. Leenstra, M. Ramkema, G. L. Scheffer, R. J. Scheper and D. Troost. Expression and cellular distribution of multidrug transporter proteins in two major causes of medically intractable epilepsy: focal cortical dysplasia and glioneuronal tumors. Neuroscience 118:417-29 (2003) (Pubitemid 36423257)
33. Tishler, D., K. Weinberg, D. Hinton, N. Barbaro, A. Geralyn and R. Corey. MDR1 gene expression in brain of patient with medically intractable epilepsy. Epilepsia 36:1-6 (1995)
34. Sisodiya, S. M., J. Heffernan and M. V. Squier. Overexpression of P-glycoprotein in malformations of cortical development. Neuroreport 10(16):3437-41 (1999)
35. Lazarowski, A., G. Sevlever, A. L. Taratuto and M. Massaro, A. Rabinowicz. Tuberous sclerosis associated with MDR1 gene expression and drug-resistant epilepsy. Pediatr Neurol 21(4):731-4 (1999) (Pubitemid 29505340)
36. Lazarowski, A., F. Lubieniecki, S. Camarero, H. Pomata, M. Bartuluchi, G. Sevlever and A. L. Taratuto, Multidrug resistance proteins in tuberous sclerosis and refractory epilepsy. Pediatr Neurol 30:102-106 (2004) (Pubitemid 38249343)
37. Lazarowski, A., F. Lubieniecki, S. Camarero, V. Cuccia and A. L. Taratuto. Stem-cell marker CD34, multidrug resistance proteins P-gp and BCRP in SEGA. Receptor Clin Invest 1, Ahead of prin (2014)
38. Fassunke, J., M. Majores, C. Ullmann, Ch. E. Elger, J. Schramm, O. D. Wiestler and A. J. Becker. In situ-RT and immunolaser microdissection for mRNA analysis of individual cells isolated from epilepsy-associated glioneuronal tumors. Lab Invest 84, 1520-1525 (2004) (Pubitemid 39482169)
39. Goodell, M. A., K. Brose, G. Paradis, A. S. Conner and R. C. Mulligan. Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med 183:1797-1806 (1996) (Pubitemid 26134320)
40. Bunting, K. D. ABC Transporters as Phenotypic Markers and Functional Regulators of Stem Cells. Stem Cells 20:11-20 (2002) (Pubitemid 34118906)
41. Reali, C., F. Scintu, R. Pillai, S. Cabras, F. Argiolu, M. S. Ristaldi, M. A. Sanna, M. Badiali and V. Sogos. Differentiation of human adult CD34+ stem cells into cells with a neural phenotype: role of astrocytes. Exp Neurol 197(2):399-406 (2006) (Pubitemid 43077148)
42. Fauser, S., A. Becker, A. Schulze-Bonhage, M. Hildebrandt, I. Tuxhorn, H. W. Pannek, R. Lahl, J. Schramm and I. Blumcke. CD34-immunoreactive balloon cells in cortical malformations. Acta Neuropathol 108:272-8 (2004) (Pubitemid 39317694)
43. De Rosa, M. J., D. L. Secor, M. Barsom, R. S. Fisher and H. V. Vinters. Neuropathologic findings in surgically treated hemimegalencephaly: immunohistochemical, morphometric, and ultrastructural study. Acta Neuropathol 84:250-60 (1992)
44. Farrell, M. A., M. J. DeRosa, J. G. Curran, D. L. Secor, M. E. Cornford, Y. G. Comair, W. J. Peacock, W. D. Shields and H. V. Vinters. Neuropathologic findings in cortical resections (including Hemispherectomies) performed for the treatment of intractable childhood epilepsy. Acta Neuropathol 83:246-259 (1992)
45. Blümcke, I., H. V. Vinters, D. Armstrong, E. Aronica, M. Thom and R Spreafico. Malformations of cortical development and epilepsies: neuropathological findings with emphasis on focal cortical dysplasia. Epileptic Disord 11:181-93 (2009)
46. Orlova, K. A., V. Tsai, M. Baybis, G. G. Heuer, S. Sisodiya, M. Thom, K. Strauss, E. Aronica, Ph. B. Storm and P. B. Crino. Early Progenitor Cell Marker Expression Distinguishes Type II from Type I Focal Cortical Dysplasias. J Neuropathol Exp Neurol 69:850-863 (2010)
47. Crino, P. B., J. Q. Trojanowski, M. A. Dichter and J. Eberwine. Embryonic neuronal markers in tuberous sclerosis: single-cell molecular pathology. Proc Natl Acad Sci USA. 93(24):14152-7 (1996) (Pubitemid 26424261)
48. French, J. A. Refractory epilepsy: clinical overview. Epilepsia 48(Suppl. 1):3-7 (2007) (Pubitemid 46280512)
49. Sisodiya, S. M., W. R. Lin, B. N. Harding, M. V. Squier, M. Thom. Drug Resistance in Epilepsy: Expression of Drug-resistance Proteins in Common Causes of Refractory Epilepsy. Brain 125(Pt 1):22-31 (2002) (Pubitemid 34084034)
50. van Breemen, M. S., E. B. Wilms, C. J. Vecht. Epilepsy in patients with brain tumours: epidemiology, mechanisms, and management. Lancet Neurol 6:421-30 (2007) (Pubitemid 46551867)
51. Aronica, E., S. M. Sisodiya and J. A. Gorter. Cerebral expression of drug transporters in epilepsy. Adv Drug Deliv Rev 64:919-29 (2012)
52. Hadjivassiliou, G., L. Martinian, W. Squier, I. Blumcke, E. Aronica, S. M. Sisodiya and M. Thom. The application of cortical layer markers in the evaluation of cortical dysplasias in epilepsy. Acta Neuropathol 120:517-528 (2010)
53. Rajneesh, K. F. and D. K. Binder. Tumor-associated epilepsy. Neurosurg Focus 27(2):E4 (2009)
54. Clarke, M. F. and M. Fuller. Stem cells and cancer: two faces of eve. Cell 124:1111-1115 (2006)
55. Dean, M., T. Fojo and S. Bates. Tumor stem cells and drug resistance. Nat Rev Cancer 5:275-284 (2005) (Pubitemid 40488633)
56. Huntly, B. J. and D. G. Gilliland. Leukemia stem cells and the evolution of Cancer Stem Cells. Nat Rev Cancer 5:311-321 (2005) (Pubitemid 40488636)
57. Lin, T., O. Islam and K. Heese. ABC transporters, neural stem cells and neurogenesis - a different perspective. Cell Res 16:857-871 (2006) (Pubitemid 44764195)
58. Schumacher, T., M. Krohn, J. Hofrichter, C. Lange, J. Stenzel, J. Steffen, T. Dunkelmann, K. Paarmann, C. Fröhlich, A. Uecker, A. S. Plath, A. Sommer, T. Brüning, H. J. Heinze, and J. Pahnke. ABC transporters B1, C1 and G2 differentially regulate neuroregeneration in mice. PLoS One. 7(4):e35613 (2012)
59. Gritti, A., A. L. Vescovi and R. Galli. Adult neural stem cells: plasticity and developmental potential. J Physiol 96, 81-90 (2002) (Pubitemid 34087035)
60. Engel, J. Jr, S. Wiebe, J. French, M. Sperling, P. Williamson, D. Spencer, R. Gumnit, C. Zahn, E. Westbrook, B. Enos, Quality Standards Subcommittee of the American Academy of Neurology; American Epilepsy Society and American Association of Neurological Surgeons. Practice parameter: temporal lobe and localized neocortical resections for epilepsy: report of the Quality Standards Subcommittee of the American Academy of Neurology, in association with the American Epilepsy Society and the American Association of Neurological Surgeons. Neurology 60:538-547 (2003) (Pubitemid 36246066)
61. Lhatoo, S. D., J. K. Solomon, A. W. McEvoy, N. D. Kitchen, S. D. Shorvon and J. W. Sander. A prospective study of the requirement for and the provision of epilepsy surgery in the United Kingdom. Epilepsia 44:673-676 (2003) (Pubitemid 36554635)
62. McIntosh, A. M., R. M. Kalnins, L. A. Mitchell, G. C. Fabinyi, R. S. Briellmann and S. F. Berkovic. Temporal lobectomy: long-term seizure outcome, late recurrence and risks for seizure recurrence. Brain 127:2018-30 (2004) (Pubitemid 39150260)
63. de Tisi, J., G. S. Bell, J. L. Peacock, A. W. McEvoy, W. F. J. Harkness, J. W. Sander and J. S. Duncan. The longterm outcome of adult epilepsy surgery, patterns of seizure remission, and relapse: a cohort study. Lancet 378:1388-95 (2011)
64. Janszky, J., H. W. Pannek, I. Janszky, R. Schulz, F. Behne, M. Hoppe and A. Ebner. Failed surgery for temporal lobe epilepsy: predictors of long-term seizure-free course. Epilepsy Res 64:35-44 (2005) (Pubitemid 40726164)
65. Jehi, L., R. Sarkis, W. Bingaman, P. Kotagal and I. Najm. When is a postoperative seizure equivalent to "epilepsy recurrence" after epilepsy surgery? Epilepsia 51:994-1003 (2010)
66. Wiebe, S. Epilepsy: Outcome patterns in epilepsy surgery-the long-term view. Nat Rev Neurol 8:123-124 (2012)
67. Hirsch, L. J. Long-Term Outcome after epilepsy surgery: relapsing, remitting disorder? Epilepsy Curr 12, 4:140-142 (2012)
68. Marín, O. Interneuron dysfunction in psychiatric disorders. Nat Rev Neurosci 18, 13:107-20 (2012)
69. Espuny-Camacho, I., K. A. Michelsen, D. Gall, D. Linaro, A. Hasche, J. Bonnefont, C. Bali, D. Orduz, A. Bilheu, A. Herpoel, N. Lambert, N. Gaspard, S. Péron, S. N. Schiffmann, M. Giugliano, A. Gaillard and P Vanderhaeghen. Pyramidal neurons derived from human pluripotent stem cells integrate efficiently into mouse brain circuits in vivo. Neuron 77:440-56 (2013)
70. Maroof, A. M., S. Keros, J. A. Tyson, S. W. Ying, Y. M. Ganat, F. T. Merkle, B. Liu, A. Goulburn, E. G. Stanley, A. G. Elefanty, H. R. Widmer, K. Eggan, P. A. Goldstein, S. A. Anderson and L. Studer. Directed differentiation and functional maturation of cortical interneurons from human embryonic stem cells. Cell Stem Cell 12:559-72 (2013)
71. Nicholas, C. R., J. Chen, Y. Tang, D. G. Southwell, N. Chalmers, D. Vogt, C. M. Arnold, Y. J. Chen, E. G. Stanley, A. G. Elefanty, Y. Sasai, A. Alvarez-Buylla, J. L. Rubenstein and A. R. Kriegstein. Functional maturation of hPSC-derived forebrain interneurons requires an extended timeline and mimics human neural development. Cell Stem Cell 12:573-86 (2013)
72. Richardson, R. M., N. M. Barbaro, A. Alvarez-Buylla and SC Baraban. Developing cell transplantation for temporal lobe epilepsy. Neurosurg Focus 24: E17 (2008)
73. Naegele, J. R., X. Maisano, J. Yang, S. Royston and E. Ribeiro. Recent advancements in stem cell and gene therapies for neurological disorders and intractable epilepsy. Neuropharmacology 58:855-864 (2010)
74. Inoue, H., N. Nagata, H. Kurokawa and S. Yamanaka. iPS cells: a game changer for future medicine. EMBO J. 33(5):409-17 (2014)
75. Jiao, J., Y. Yang, Y. Shi, J. Chen, R. Gao, Y. Fan, H. Yao, W. Liao, X-F. Sun and S. Gao. Modeling Dravet syndrome using induced pluripotent stem cells (iPSCs) and directly converted neurons. Hum Mol Genet. 22(21):4241-52 (2013)
76. Shetty, A. K. Progress in cell grafting therapy for temporal lobe epilepsy. Neurotherapeutics 8:721-735 (2011)
77. Gallego, J. M., F. J. Sancho, S. Vidueira, L. Ortiz, U. Comez-Pinedo and J. A. Barcia. Injection of embryonic median ganglionic eminence cells or fibroblasts within the amygdala in rats kindled from the piriform cortex. Seizure 19:461-466 (2010)
78. Calcagnotto, M. E., I. Zipancic, M. Piquer-Gil, L. E. Mello and M Alvarez-Dolado. Grafting of GABAergic precursors rescues deficits in hippocampal inhibition. Epilepsia 51(Suppl. 3), 66-70 (2010)
79. Corti, S., M. Nizzardo, M. Nardini, C. Donadoni, S. Salani, C. Simone, M. Falcone, G. Riboldi, A. Govoni, N. Bresolin and G. P. Comi. Systemic transplantation of c-kit+ cells exerts a therapeutic effect in a model of amyotrophic lateral sclerosis. Hum Mol Genet 19, 3782-3796 (2010)
80. Chailangkarn, T., A. Acab and AR. Muotri. Modeling neurodevelopmental disorders using human neurons. Curr Opin Neurobiol 22, 785-790 (2012)
81. Yan, Y., S. Shin, B. S. Jha, Q. Liu, J. Sheng, F. Li, M. Zhan, J. Davis, K. Bharti, X. Zeng, M. Rao, N. Malik and M. C. Vemuri. Efficient and rapid derivation of primitive neural stem cells and generation of brain subtype neurons from human pluripotent stem cells. Stem Cells Transl Med 2:862-870 (2013)
82. Miltiadous, P., A. Stamatakis, P. N. Koutsoudaki, D. G. Tiniakos and F. Stylianopoulou. IGF-I ameliorates hippocampal neurodegeneration and protects against cognitive deficits in an animal model of temporal lobe epilepsy. Exp Neurol 231, 223-235 (2011)
83. Russo, E., R. Citraro, A. Constanti and G. De Sarro. The mTOR signaling pathway in the brain: Focus on epilepsy and epileptogenesis. Mol Neurobiol 46, 662-681 (2012)
84. Canpolat, M., H. Per, H. Gumus, A. Yikilmaz, E. Unal, T. Patiroglu, L. Cinar, A. Kurtsoy and S. Kumandas. Rapamycin has a beneficial effect on controlling epilepsy in children with tuberous sclerosis complex: results of 7 children from a cohort of 86. Childs Nerv Syst 30:227-40 (2014)
85. Huang, X., H. Zhang, J. Yang, J. Wu, J. McMahon, Y. Lin, Z. Cao, M. Gruenthal and Y. Huang. Pharmacological Inhibition of the Mammalian Target of Rapamycin Pathway Suppresses Acquired Epilepsy. Neurobiol Dis 40:193-199 (2010)
86. Krueger, D. A., M. M. Care, K. Holland, K. Agricola, C. Tudor, P. Mangeshkar, K. A. Wilson, A. Byars, T. Sahmoud, D. N. Franz. Everolimus for Subependymal Giant-Cell Astrocytomas in Tuberous Sclerosis. N Engl J Med 363:1801-11 (2010)
87. Zeng, L. H., N. R. Rensing and M Wong. The mammalian target of rapamycin signaling pathway mediates epileptogenesis in a model of temporal lobe epilepsy. J Neurosci 29:6964-6972 (2009)
88. Boer, K., D. Troost; W. Timmermans, P. C. van Rijen, W. G. M. Spliet and E. Aronica. 4Pi3K-mTOR Signaling and AMOG Expression in Epilepsy-associated Glioneuronal Tumors. Brain Pathol 20:234-244 (2010)
89. Schick, V., M. Majores, A. Koch, C. E. Elger, J. Schramm, H. Urbach, A. J. Becker. Alterations of phosphatidylinositol 3-kinase pathway components in epilepsy-associated glioneuronal lesions. Epilepsia 48 Suppl 5:65-73 (2007) (Pubitemid 47512204)
90. Wang, S. F., Y. C. Chou, N. Mazumder, F. J. Kao, L. D. Nagy, F. P. Guengerich, C. Huang, H. C. Lee, P. S. Lai and Y. F. Ueng. 7-Ketocholesterol induces P-glycoprotein through PI3K/mTOR signaling in hepatoma cells. Biochem Pharmacol 86:548-60 (2013)