Postnatal neurogenesis generates heterotopias, olfactory micronodules and cortical infiltration following single-cell TSC1 deletion

Human Molecular Genetics

Volumn 21, Issue 4, 2012, Pages 799-810

  Feliciano, David M ^a   Quon, Jennifer L ^a   Su, Tiffany ^a   Taylor, M Morgan ^a   Bordey, Angélique ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN; PEPTIDES AND PROTEINS; TUBERIN; TUBEROUS SCLEROSIS COMPLEX 1 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN DAMAGE; BRAIN MALFORMATION; CELL ENLARGEMENT; CELL INFILTRATION; CELL SIZE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ELECTROPORATION; FOREBRAIN; GENE DELETION; GENOTYPE; GLIA CELL; HETEROTOPIA; MOUSE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; NUCLEUS ACCUMBENS; NULL ALLELE; OLFACTORY BULB; OLFACTORY CORTEX; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; SUBVENTRICULAR ZONE; TUBEROUS SCLEROSIS;

ANIMALS; ANIMALS, NEWBORN; CELL MOVEMENT; CEREBRAL CORTEX; DENDRITES; ELECTROPORATION; FEMALE; GENE DELETION; MALE; MICE; MICE, TRANSGENIC; NEUROGENESIS; NEUROGLIA; NEURONS; OLFACTORY BULB; PERIVENTRICULAR NODULAR HETEROTOPIA; SINGLE-CELL ANALYSIS; TOR SERINE-THREONINE KINASES; TUBEROUS SCLEROSIS; TUMOR SUPPRESSOR PROTEINS;

MUS MUSCULUS;

EID: 84856347592     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddr511     Document Type: Article

References (56)

1. Osborne, J.P., Fryer, A. and Webb, D. (1991) Epidemiology of tuberous sclerosis. Ann. N. Y. Acad. Sci., 615, 125-127.
2. European Chromosome 16 Tuberous Sclerosis Consortium. (1993) Identification and characterization of the tuberous sclerosis gene on chromosome 16. Cell, 75, 1305-1315.
3. Curatolo, P., Seri, S., Verdecchia, M. and Bombardieri, R. (2001) Infantile spasms in tuberous sclerosis complex. Brain Dev., 23, 502-507.
4. Holmes, G.L. and Stafstrom, C.E. (2007) Tuberous sclerosis complex and epilepsy: recent developments and future challenges. Epilepsia, 48, 617-630.
5. Webb, D.W., Fryer, A.E. and Osborne, J.P. (1996) Morbidity associated with tuberous sclerosis: a population study. Dev. Med. Child Neurol., 38, 146-155.
6. Weiner, D.M., Ewalt, D.H., Roach, E.S. and Hensle, T.W. (1998) The tuberous sclerosis complex: a comprehensive review. J. Am. Coll. Surg., 187, 548-561.
7. Crino, P.B. (2004) Molecular pathogenesis of tuber formation in tuberous sclerosis complex. J. Child Neurol., 19, 716-725.
8. Crino, P.B., Aronica, E., Baltuch, G. and Nathanson, K.L. (2010) Biallelic TSC gene inactivation in tuberous sclerosis complex. Neurology, 74, 1716-1723.
9. Feliciano, D.M., Su, T., Lopez, J., Platel, J.C. and Bordey, A. (2011) Single-cell Tsc1 knockout during corticogenesis generates tuber-like lesions and reduces seizure threshold in mice. J. Clin. Invest., 121, 1596-1607.
10. Thiele, E.A. (2004) Managing epilepsy in tuberous sclerosis complex. J. Child Neurol., 19, 680-686.
11. Uhlmann, E.J., Wong, M., Baldwin, R.L., Bajenaru, M.L., Onda, H., Kwiatkowski, D.J., Yamada, K. and Gutmann, D.H. (2002) Astrocyte-specific TSC1 conditional knockout mice exhibit abnormal neuronal organization and seizures. Ann. Neurol., 52, 285-296.
12. Meikle, L., Talos, D.M., Onda, H., Pollizzi, K., Rotenberg, A., Sahin, M., Jensen, F.E. and Kwiatkowski, D.J. (2007) A mouse model of tuberous sclerosis: neuronal loss of Tsc1 causes dysplastic and ectopic neurons, reduced myelination, seizure activity, and limited survival. J. Neurosci., 27, 5546-5558.
13. Way, S.W., McKenna, J. III, Mietzsch, U., Reith, R.M., Wu, H.C. and Gambello, M.J. (2009) Loss of Tsc2 in radial glia models the brain pathology of tuberous sclerosis complex in the mouse. Hum. Mol. Genet., 7, 1252-1265.
14. Zeng, L.H., Rensing, N.R., Zhang, B., Gutmann, D.H., Gambello, M.J. and Wong, M. (2010) Tsc2 gene inactivation causes a more severe epilepsy phenotype than Tsc1 inactivation in a mouse model of tuberous sclerosis complex. Hum. Mol. Genet., 3, 445-454.
15. Choi, Y.J., Di Nardo, A., Kramvis, I., Meikle, L., Kwiatkowski, D.J., Sahin, M. and He, X. (2008) Tuberous sclerosis complex proteins control axon formation. Genes Dev., 22, 2485-2495.
16. Mizuguchi, M. and Takashima, S. (2001) Neuropathology of tuberous sclerosis. Brain Dev., 23, 508-515.
17. Wei, J., Li, P., Chiriboga, L., Mizuguchi, M., Yee, H., Miller, D.C. and Greco, M.A. (2002) Tuberous sclerosis in a 19-week fetus: immunohistochemical and molecular study of hamartin and tuberin. Pediatr. Dev. Pathol., 5, 448-464.
18. Eriksson, P.S., Perfilieva, E., Bjork-Eriksson, T., Alborn, A.M., Nordborg, C., Peterson, D.A. and Gage, F.H. (1998) Neurogenesis in the adult human hippocampus. Nat. Med., 4, 1313-1317.
19. Curtis, M.A., Kam, M., Nannmark, U., Anderson, M.F., Axell, M.Z., Wikkelso, C., Holtas, S., Roon-Mom, W.M., Bjork-Eriksson, T., Nordborg, C. et al. (2007) Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science, 315, 1243-1249.
20. Wang, C., Liu, F., Liu, Y.Y., Zhao, C.H., You, Y., Wang, L., Zhang, J., Wei, B., Ma, T., Zhang, Q. et al. (2011) Identification and characterization of neuroblasts in the subventricular zone and rostral migratory stream of the adult human brain. Cell Res., 11, 1534-1150.
21. Zhao, C., Deng, W. and Gage, F.H. (2008) Mechanisms and functional implications of adult neurogenesis. Cell, 132, 645-660.
22. Bordey, A. (2009) Neonatal progenitor contribution to epilepsy-associated cortical malformations. In Schwartzkroin, P.A. (ed.), Encyclopedia of Basic Epilepsy Research. Elsevier, Boston.
23. Pathania, M., Yan, L.D. and Bordey, A. (2010) A symphony of signals conduct early and late stages of adult neurogenesis. Neuropharmacology, 6, 1060-1070.
24. Sanai, N., Tramontin, A.D., Quinones-Hinojosa, A., Barbaro, N.M., Gupta, N., Kunwar, S., Lawton, M.T., McDermott, M.W., Parsa, A.T., Manuel-Garcia, V.J. et al. (2004) Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature, 427, 740-744.
25. van den Berge, S.A., Middeldorp, J., Zhang, C.E., Curtis, M.A., Leonard, B.W., Mastroeni, D., Voorn, P., van de Berg, W.D., Huitinga, I. and Hol, E.M. (2010) Longterm quiescent cells in the aged human subventricular neurogenic system specifically express GFAP-delta. Aging Cell, 9, 313-326.
26. Quinones-Hinojosa, A. and Chaichana, K. (2007) The human subventricular zone: a source of new cells and a potential source of brain tumors. Exp. Neurol., 205, 313-324.
27. Levison, S.W. and Goldman, J.E. (1993) Both oligodendrocytes and astrocytes develop from progenitors in the subventricular zone of postnatal rat forebrain. Neuron, 10, 201-212.
28. van Strien, M.E., van den Berge, S.A. and Hol, E.M. (2011) Migrating neuroblasts in the adult human brain: a stream reduced to a trickle. Cell Res., 11, 1523-1525.
29. Shapiro, L.A., Ng, K.L., Kinyamu, R., Whitaker-Azmitia, P., Geisert, E.E., Blurton-Jones, M., Zhou, Q.Y. and Ribak, C.E. (2007) Origin, migration and fate of newly generated neurons in the adult rodent piriform cortex. Brain Struct. Funct., 212, 133-148.
30. De Marchis, S., Fasolo, A. and Puche, A.C. (2004) Subventricular zone-derived neuronal progenitors migrate into the subcortical forebrain of postnatal mice. J. Comp. Neurol., 476, 290-300.
31. Inta, D., Alfonso, J., von Engelhardt, J., Kreuzberg, M.M., Meyer, A.H., van Hooft, J.A. and Monyer, H. (2008) Neurogenesis and widespread forebrain migration of distinct GABAergic neurons from the postnatal subventricular zone. PNAS, 52: 20994-20999.
32. Ridler, K., Suckling, J., Higgins, N., Bolton, P. and Bullmore, E. (2004) Standardized whole brain mapping of tubers and subependymal nodules in tuberous sclerosis complex. J. Child Neurol., 19, 658-665.
33. de Leon, G.A., Zaeri, N. and Foley, C.M. (1988) Olfactory hamartomas in tuberous sclerosis. J. Neurol. Sci., 87, 187-194.
34. Braffman, B.H., Bilaniuk, L.T., Naidich, T.P., Altman, N.R., Post, M.J., Quencer, R.M., Zimmerman, R.A. and Brody, B.A. (1992) MR imaging of tuberous sclerosis: pathogenesis of this phakomatosis, use of gadopentetate dimeglumine, and literature review. Radiology, 183, 227-238.
35. Cusmai, R., Chiron, C., Curatolo, P., Dulac, O. and Tran-Dinh, S. (1990) Topographic comparative study of magnetic resonance imaging and electroencephalography in 34 children with tuberous sclerosis. Epilepsia, 31, 747-755.
36. Gallagher, A., Chu-Shore, C.J., Montenegro, M.A., Major, P., Costello, D.J., Lyczkowski, D.A., Muzykewicz, D., Doherty, C. and Thiele, E.A. (2009) Associations between electroencephalographic and magnetic resonance imaging findings in tuberous sclerosis complex. Epilepsy Res., 87, 197-202.
37. Inoue, Y., Nemoto, Y., Murata, R., Tashiro, T., Shakudo, M., Kohno, K., Matsuoka, O. and Mochizuki, K. (1998) CT and MR imaging of cerebral tuberous sclerosis. Brain Dev., 20, 209-221.
38. Raznahan, A., Higgins, N.P., Griffiths, P.D., Humphrey, A., Yates, J.R. and Bolton, P.F. (2007) Biological markers of intellectual disability in tuberous sclerosis. Psychol. Med., 37, 1293-1304.
39. Bender, B.L. and Yunis, E.J. (1982) The pathology of tuberous sclerosis. Pathol. Annu., 17(Pt 1), 339-382.
40. Ess, K.C., Kamp, C.A., Tu, B.P. and Gutmann, D.H. (2005) Developmental origin of subependymal giant cell astrocytoma in tuberous sclerosis complex. Neurology, 64, 1446-1449.
41. Zhou, J., Shrikhande, G., Xu, J., McKay, R.M., Burns, D.K., Johnson, J.E. and Parada, L.F. (2011) Tsc1 mutant neural stem/progenitor cells exhibit migration deficits and give rise to subependymal lesions in the lateral ventricle. Genes Dev., 25, 1595-1600.
42. Lagace, D.C., Whitman, M.C., Noonan, M.A., Ables, J.L., DeCarolis, N.A., Arguello, A.A., Donovan, M.H., Fischer, S.J., Farnbauch, L.A., Beech, R.D. et al. (2007) Dynamic contribution of nestin-expressing stem cells to adult neurogenesis. J Neurosci., 27, 12623-12629.
43. Shuang, M., Liu, J., Jia, M.X., Yang, J.Z., Wu, S.P., Gong, X.H., Ling, Y.S., Ruan, Y., Yang, X.L. and Zhang, D. (2004) Family-based association study between autism and glutamate receptor 6 gene in Chinese Han trios. Am. J Med. Genet. B Neuropsychiatr. Genet., 131B, 48-50.
44. Misson, J.P., Edwards, M.A., Yamamoto, M. and Caviness, V.S. Jr. (1988) Identification of radial glial cells within the developing murine central nervous system: studies based upon a new immunohistochemical marker. Brain Res. Dev. Brain Res., 44, 95-108.
45. Lacar, B., Young, S.Z., Platel, J.C. and Bordey, A. (2010) Imaging and recording subventricular zone progenitor cells in live tissue of postnatal mice. Front Neurosci., 4, 43.
46. Petreanu, L. and Alvarez-Buylla, A. (2002) Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J. Neurosci., 22, 6106-6113.
47. Platel, J.C., Dave, K.A., Gordon, V., Lacar, B., Rubio, M.E. and Bordey, A. (2010) NMDA receptors activated by subventricular zone astrocytic glutamate are critical for neuroblast survival prior to entering a synaptic network. Neuron, 65, 859-872.
48. Platel, J., Heintz, T., Young, S., Gordon, V. and Bordey, A. (2008) Tonic activation of GLUK5 kainate receptors decreases neuroblast migration in a whole mount preparation of the subventricular zone. J. Physiol. (Lond.), 586, 3783-3793.
49. Bolteus, A.J. and Bordey, A. (2004) GABA release and uptake regulate neuronal precursor migration in the postnatal subventricular zone. J. Neurosci., 24, 7623-7631.
50. Goorden, S.M., van Woerden, G.M., van der, W.L., Cheadle, J.P. and Elgersma, Y. (2007) Cognitive deficits in Tsc1+/- mice in the absence of cerebral lesions and seizures. Ann. Neurol., 62, 648-655.
51. Chan, J.A., Zhang, H., Roberts, P.S., Jozwiak, S., Wieslawa, G., Lewin-Kowalik, J., Kotulska, K. and Kwiatkowski, D.J. (2004) Pathogenesis of tuberous sclerosis subependymal giant cell astrocytomas: biallelic inactivation of TSC1 or TSC2 leads to mTOR activation. J. Neuropathol. Exp. Neurol., 63, 1236-1242.
52. 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.
53. Kwiatkowski, D.J., Zhang, H., Bandura, J.L., Heiberger, K.M., Glogauer, M., el Hashemite, N. and Onda, H. (2002) A mouse model of TSC1 reveals sex-dependent lethality from liver hemangiomas, and up-regulation of p70S6 kinase activity in Tsc1 null cells. Hum. Mol. Genet., 11, 525-534.
54. Meikle, L., McMullen, J.R., Sherwood, M.C., Lader, A.S., Walker, V., Chan, J.A. and Kwiatkowski, D.J. (2005) A mouse model of cardiac rhabdomyoma generated by loss of Tsc1 in ventricular myocytes. Hum. Mol. Genet., 14, 429-435.
55. Platel, J.C., Gordon, V., Heintz, T. and Bordey, A. (2009) GFAP-GFP neural progenitors are antigenically homogeneous and anchored in their enclosed mosaic niche. Glia, 57, 66-78.
56. Thevenaz, P., Ruttimann, U.E. and Unser, M. (1998) A pyramid approach to subpixel registration based on intensity. IEEE Trans. Image Process, 7, 27-41.