Long-term genetic fate mapping of adult generated neurons in a mouse temporal lobe epilepsy model

Neurobiology of Disease

Volumn 48, Issue 3, 2012, Pages 454-463

  Jafari, Mehrnoosh ^a   Soerensen, Jonna ^a   Bogdanović, Renée Marie ^a   Dimou, Leda ^a,b   Götz, Magdalena ^a,b   Potschka, Heidrun ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

Adult neurogenesis; CreERT2; EGFP; GLAST; Neuron integration

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; GENETIC FATE MAPPING; GENETIC PROCEDURES; GRAND MAL SEIZURE; GRANULE CELL; KINDLING; MOUSE; NERVE CELL; NERVE CELL NETWORK; NONHUMAN; PRIORITY JOURNAL; TEMPORAL LOBE EPILEPSY;

ADULT STEM CELLS; ANIMALS; DENTATE GYRUS; DISEASE MODELS, ANIMAL; EPILEPSY, TEMPORAL LOBE; KINDLING, NEUROLOGIC; MICE; NEURAL STEM CELLS; NEUROGENESIS; NEURONS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84865061142     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2012.06.014     Document Type: Article

References (54)

1. Arisi G.M., Ruch M., Foresti M.L., Mukherjee S., Ribak C.E., Shapiro L.A. Astrocyte alterations in the hippocampus following pilocarpine-induced seizures in aged rats. Aging Dis. 2011, 2:294-300.
2. Cha B.H., Akman C., Silveira D.C., Liu X., Holmes G.L. Spontaneous recurrent seizure following status epilepticus enhances dentate gyrus neurogenesis. Brain Dev. 2004, 26:394-397.
3. Coras R., Siebzehnrubl F.A., Pauli E., Huttner H.B., Njunting M., Kobow K., et al. Low proliferation and differentiation capacities of adult hippocampal stem cells correlate with memory dysfunction in humans. Brain 2010, 133:3359-3372.
4. Couillard-Despres S., Winner B., Schaubeck S., Aigner R., Vroemen M., Weidner N., et al. Doublecortin expression levels in adult brain reflect neurogenesis. Eur. J. Neurosci. 2005, 21:1-14.
5. Danzer S.C. Depression, stress, epilepsy and adult neurogenesis. Exp. Neurol. 2012, 233:22-32.
6. Feil R., Wagner J., Metzger D., Chambon P. Regulation of Cre recombinase activity by mutated estrogen receptor ligand-binding domains. Biochem. Biophys. Res. Commun. 1997, 237:752-757.
7. Feng R., Rampon C., Tang Y.P., Shrom D., Jin J., Kyin M., et al. Deficient neurogenesis in forebrain-specific presenilin-1 knockout mice is associated with reduced clearance of hippocampal memory traces. Neuron 2001, 32:911-926.
8. Fournier N.M., Andersen D.R., Botterill J.J., Sterner E.Y., Lussier A.L., Caruncho H.J., et al. The effect of amygdala kindling on hippocampal neurogenesis coincides with decreased reelin and DISC1 expression in the adult dentate gyrus. Hippocampus 2010, 20:659-671.
9. Goddard G.V., McIntyre D.C., Leech C.K. A permanent change in brain function resulting from daily electrical stimulation. Exp. Neurol. 1969, 25:295-330.
10. Hattiangady B., Shetty A.K. Implications of decreased hippocampal neurogenesis in chronic temporal lobe epilepsy. Epilepsia 2008, 49(Suppl. 5):26-41.
11. Hattiangady B., Shetty A.K. Decreased neuronal differentiation of newly generated cells underlies reduced hippocampal neurogenesis in chronic temporal lobe epilepsy. Hippocampus 2010, 20:97-112.
12. Hattiangady B., Rao M.S., Shetty A.K. Chronic temporal lobe epilepsy is associated with severely declined dentate neurogenesis in the adult hippocampus. Neurobiol. Dis. 2004, 17:473-490.
13. Hawrylak N., Chang F.L., Greenough W.T. Astrocytic and synaptic response to kindling in hippocampal subfield CA1. II. Synaptogenesis and astrocytic process increases to in vivo kindling. Brain Res. 1993, 603:309-316.
14. Imayoshi I., Sakamoto M., Ohtsuka T., Takao K., Miyakawa T., Yamaguchi M., et al. Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat. Neurosci. 2008, 11:1153-1161.
15. Jakubs K., Nanobashvili A., Bonde S., Ekdahl C.T., Kokaia Z., Kokaia M., et al. Environment matters: synaptic properties of neurons born in the epileptic adult brain develop to reduce excitability. Neuron 2006, 52:1047-1059.
16. Jessberger S., Nakashima K., Clemenson G.D., Mejia E., Mathews E., Ure K., et al. Epigenetic modulation of seizure-induced neurogenesis and cognitive decline. J. Neurosci. 2007, 27:5967-5975.
17. Kawamoto S., Niwa H., Tashiro F., Sano S., Kondoh G., Takeda J., et al. A novel reporter mouse strain that expresses enhanced green fluorescent protein upon Cre-mediated recombination. FEBS Lett. 2000, 470:263-268.
18. Kempermann G., Wiskott L., Gage F.H. Functional significance of adult neurogenesis. Curr. Opin. Neurobiol. 2004, 14:186-191.
19. Khurgel M., Ivy G.O. Astrocytes in kindling: relevance to epileptogenesis. Epilepsy Res. 1996, 26:163-175.
20. Kokaia M. Seizure-induced neurogenesis in the adult brain. Eur. J. Neurosci. 2011, 33:1133-1138.
21. Lagace D.C., Whitman M.C., Noonan M.A., Ables J.L., DeCarolis N.A., Arguello A.A., et al. Dynamic contribution of nestin-expressing stem cells to adult neurogenesis. J. Neurosci. 2007, 27:12623-12629.
22. Longo B., Romariz S., Blanco M.M., Vasconcelos J.F., Bahia L., Soares M.B., et al. Distribution and proliferation of bone marrow cells in the brain after pilocarpine-induced status epilepticus in mice. Epilepsia 2010, 51:1628-1632.
23. Loscher W., Brandt C. Prevention or modification of epileptogenesis after brain insults: experimental approaches and translational research. Pharmacol. Rev. 2010, 62:668-700.
24. Mandyam C.D., Harburg G.C., Eisch A.J. Determination of key aspects of precursor cell proliferation, cell cycle length and kinetics in the adult mouse subgranular zone. Neuroscience 2007, 146:108-122.
25. McIntyre D.C., Poulter M.O., Gilby K. Kindling: some old and some new. Epilepsy Res. 2002, 50:79-92.
26. Meltzer L.A., Yabaluri R., Deisseroth K. A role for circuit homeostasis in adult neurogenesis. Trends Neurosci. 2005, 28:653-660.
27. Mori T., Tanaka K., Buffo A., Wurst W., Kuhn R., Gotz M. Inducible gene deletion in astroglia and radial glia-a valuable tool for functional and lineage analysis. GLIA 2006, 54:21-34.
28. Murphy B.L., Pun R.Y., Yin H., Faulkner C.R., Loepke A.W., Danzer S.C. Heterogeneous integration of adult-generated granule cells into the epileptic brain. J. Neurosci. 2011, 31:105-117.
29. Nakamura T., Colbert M.C., Robbins J. Neural crest cells retain multipotential characteristics in the developing valves and label the cardiac conduction system. Circ. Res. 2006, 98:1547-1554.
30. Ninkovic J., Mori T., Gotz M. Distinct modes of neuron addition in adult mouse neurogenesis. J. Neurosci. 2007, 27:10906-10911.
31. Parent J.M., Murphy G.G. Mechanisms and functional significance of aberrant seizure-induced hippocampal neurogenesis. Epilepsia 2008, 49(Suppl. 5):19-25.
32. Parent J.M., Janumpalli S., McNamara J.O., Lowenstein D.H. Increased dentate granule cell neurogenesis following amygdala kindling in the adult rat. Neurosci. Lett. 1998, 247:9-12.
33. Parent J.M., Tada E., Fike J.R., Lowenstein D.H. Inhibition of dentate granule cell neurogenesis with brain irradiation does not prevent seizure-induced mossy fiber synaptic reorganization in the rat. J. Neurosci. 1999, 19:4508-4519.
34. Parent J.M., Valentin V.V., Lowenstein D.H. Prolonged seizures increase proliferating neuroblasts in the adult rat subventricular zone-olfactory bulb pathway. J. Neurosci. 2002, 22:3174-3188.
35. Pauli E., Hildebrandt M., Romstock J., Stefan H., Blumcke I. Deficient memory acquisition in temporal lobe epilepsy is predicted by hippocampal granule cell loss. Neurology 2006, 67:1383-1389.
36. Paxinos G., Franklin K.B.J. The mouse brain in sterotaxic coordinates 2004, Academic Press, Elsevier Science, San Diego USA. 2nd edition.
37. Pekcec A., Muhlenhoff M., Gerardy-Schahn R., Potschka H. Impact of the PSA-NCAM system on pathophysiology in a chronic rodent model of temporal lobe epilepsy. Neurobiol. Dis. 2007, 27:54-66.
38. Pekcec A., Fuest C., Muhlenhoff M., Gerardy-Schahn R., Potschka H. Targeting epileptogenesis-associated induction of neurogenesis by enzymatic depolysialylation of NCAM counteracts spatial learning dysfunction but fails to impact epilepsy development. J. Neurochem. 2008, 105:389-400.
39. Pekcec A., Lupke M., Baumann R., Seifert H., Potschka H. Modulation of neurogenesis by targeted hippocampal irradiation fails to affect kindling progression. Hippocampus 2011, 21:866-876.
40. Racine R.J. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr. Clin. Neurophysiol. 1972, 32:281-294.
41. Rogawski M.A. Astrocytes get in the act in epilepsy. Nat. Med. 2005, 11:919-920.
42. Scharfman H.E., McCloskey D.P. Postnatal neurogenesis as a therapeutic target in temporal lobe epilepsy. Epilepsy Res. 2009, 85:150-161.
43. Scharfman H.E., Goodman J.H., Sollas A.L. Granule-like neurons at the hilar/CA3 border after status epilepticus and their synchrony with area CA3 pyramidal cells: functional implications of seizure-induced neurogenesis. J. Neurosci. 2000, 20:6144-6158.
44. Scott B.W., Wang S., Burnham W.M., De Boni U., Wojtowicz J.M. Kindling-induced neurogenesis in the dentate gyrus of the rat. Neurosci. Lett. 1998, 248:73-76.
45. Seeger N., Zellinger C., Rode A., Roloff F., Bicker G., Russmann V., et al. The erythropoietin-derived peptide mimetic pHBSP affects cellular and cognitive consequences in a rat post-status epilepticus model. Epilepsia 2011, 52:2333-2343.
46. Seifert G., Carmignoto G., Steinhauser C. Astrocyte dysfunction in epilepsy. Brain Res. Rev. 2010, 63:212-221.
47. Shapiro L.A., Ribak C.E. Integration of newly born dentate granule cells into adult brains: hypotheses based on normal and epileptic rodents. Brain Res. Brain Res. Rev. 2005, 48:43-56.
48. Taupin P. BrdU immunohistochemistry for studying adult neurogenesis: paradigms, pitfalls, limitations, and validation. Brain Res. Rev. 2007, 53:198-214.
49. Taupin P. Protocols for studying adult neurogenesis: insights and recent developments. Regen. Med. 2007, 2:51-62.
50. Tian G.F., Azmi H., Takano T., Xu Q., Peng W., Lin J., et al. An astrocytic basis of epilepsy. Nat. Med. 2005, 11:973-981.
51. Vezzani A., Aronica E., Mazarati A., Pittman Q.J. Epilepsy and brain inflammation. Exp. Neurol. 2011, (Electronic publication ahead of print).
52. Wiskott L., Rasch M.J., Kempermann G. A functional hypothesis for adult hippocampal neurogenesis: avoidance of catastrophic interference in the dentate gyrus. Hippocampus 2006, 16:329-343.
53. Wood J.C., Jackson J.S., Jakubs K., Chapman K.Z., Ekdahl C.T., Kokaia Z., et al. Functional integration of new hippocampal neurons following insults to the adult brain is determined by characteristics of pathological environment. Exp. Neurol. 2011, 229:484-493.
54. Zhan R.Z., Timofeeva O., Nadler J.V. High ratio of synaptic excitation to synaptic inhibition in hilar ectopic granule cells of pilocarpine-treated rats. J. Neurophysiol. 2010, 104:3293-3304.