Seizure evoked regulation of LIM-HD genes and co-factors in the postnatal and adult hippocampus

F1000Research

Volumn 2, Issue , 2013, Pages

  Vaidya, Vidita A ^a   Lakhina, Vanisha ^a,b   Subramanian, Lakshmi ^a,c   Huilgol, Dhananjay ^a,d   Shetty, Ashwin S ^a   Tole, Shubha ^a  

^a TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

^b PRINCETON UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d Simons Center for Quantitative Biology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIM HOMEODOMAIN PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; BRAIN REGION; CONTROLLED STUDY; DENTATE GYRUS; DISEASE ACTIVITY; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCATION; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; LIM HD GENE; MALE; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; NERVE CELL PLASTICITY; NONHUMAN; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; REGULATOR GENE; SEIZURE;

EID: 84914816089     PISSN: 20461402     EISSN: 1759796X     Source Type: Journal    
DOI: 10.12688/f1000research.2-205.v1     Document Type: Article

References (64)

1. Guillemot F: Cell fate specification in the mammalian telencephalon. Prog Neurobiol. 2007;83(1):37-52. 17517461 10.1016/j.pneurobio.2007.02.009
2. Polleux F Ince-Dunn G Ghosh A: Transcriptional regulation of vertebrate axon guidance and synapse formation. Nat Rev Neurosci. 2007;8(5):331-40. 17453014 10.1038/nrn2118
3. Nóbrega-Pereira S Marín O: Transcriptional control of neuronal migration in the developing mouse brain. Cereb Cortex. 2009;19(Suppl 1):i107-13. 19357392 10.1093/cercor/bhp044
4. Lonze BE Ginty DD: Function and regulation of CREB family transcription factors in the nervous system. Neuron. 2002;35(4):605-23. 12194863 10.1016/S0896-6273(02)00828-0
5. Parrish JZ Emoto K Kim MD: Mechanisms that regulate establishment, maintenance, and remodeling of dendritic fields. Annu Rev Neurosci. 2007;30:399-423. 17378766 10.1146/annurev.neuro.29.051605.112907
6. West AE Greenberg ME: Neuronal activity-regulated gene transcription in synapse development and cognitive function. Cold Spring Harb Perspect Biol. 2011;3(6):a005744. 21555405 10.1101/cshperspect.a005744 3098681
7. Lundgren SE Callahan CA Thor S: Control of neuronal pathway selection by the Drosophila LIM homeodomain gene apterous. Development. 1995;121(6):1769-73. 7600992
8. Porter FD Drago J Xu Y: Lhx2, a LIM homeobox gene, is required for eye forebrain, and definitive erythrocyte development. Development. 1997;124(15):2935-4. 9247336
9. Thor S Andersson SG Tomlinson A: A LIM-homeodomain combinatorial code for motor-neuron pathway selection. Nature. 1999;397(6714):76-80. 9892357 10.1038/16275
10. Ando H Kobayashi M Tsubokawa T: Lhx2 mediates the activity of Six3 in zebrafish forebrain growth. Dev Biol. 2005;287(2):456-468. 16226737 10.1016/j.ydbio.2005.09.023
11. Mangale VS Hirokawa KE Satyaki PR: Lhx2 selector activity specifies cortical identity and suppresses hippocampal organizer fate. Science. 2008;319(5861):304-309. 18202285 10.1126/science.1151695 2494603
12. Milan M Cohen SM: Regulation of LIM homeodomain activity in vivo: a tetramer of dLDB and apterous confers activity and capacity for regulation by dLMO. Mol Cell. 1999;4(2):267-273. 10488342 10.1016/S1097-2765(00)80374-3
13. Thaler JP Lee SK Jurata LW: LIM factor Lhx3 contributes to the specification of motor neuron and interneuron identity through cell-type-specific protein-protein interactions. Cell. 2002;110(2):237-249. 12150931 10.1016/S0092-8674(02)00823-1
14. Milan M Diaz-Benjumea FJ Cohen SM: Beadex encodes an LMO protein that regulates Apterous LIM-homeodomain activity in Drosophila wing development: a model for LMO oncogene function. Genes Dev. 1998;12(18):2912-2920. 9744867 10.1101/gad.12.18.2912 317163
15. Weihe U Milan M Cohen SM: Regulation of Apterous activity in Drosophila wing development. Development. 2001;128(22):4615-4622. 11714686
16. Bulchand S Subramanian L Tole S: Dynamic spatiotemporal expression of LIM genes and cofactors in the embryonic and postnatal cerebral cortex. Dev Dyn. 2003;226(3):460-469. 12619132 10.1002/dvdy.10235
17. Bulchand S Grove EA Porter FD: LIM-homeodomain gene Lhx2 regulates the formation of the cortical hem. Mech Dev. 2001;100(2):165-175. 11165475 10.1016/S0925-4773(00)00515-3
18. Subramanian L Sarkar A Shetty AS: Transcription factor Lhx2 is necessary and sufficient to suppress astrogliogenesis and promote neurogenesis in the developing hippocampus. Proc Natl Acad Sci U S A. 2011;108(27):E265-74. 21690374 10.1073/pnas.1101109108 3131330
19. Zhao Y Sheng HZ Amini R: Control of hippocampal morphogenesis and neuronal differentiation by the LIM homeobox gene Lhx5. Science. 1999;284(5417):1155-8. 10325223 10.1126/science.284.5417.1155
20. Yan CH Levesque M Claxton S: Lmx1a and lmx1b function cooperatively to regulate proliferation, specification, and differentiation of midbrain dopaminergic progenitors. J Neurosci. 2011;31(35):12413-25. 21880902 10.1523/JNEUROSCI.1077-11.2011
21. Lakhina V Falnikar A Bhatnagar L: Early thalamocortical tract guidance and topographic sorting of thalamic projections requires LIM-homeodomain gene Lhx2. Dev Biol. 2007;306(2):703-13. 17493606 10.1016/j.ydbio.2007.04.007
22. Marcos-Mondéjar P Peregrín S Li JY: The lhx2 transcription factor controls thalamocortical axonal guidance by specific regulation of robo1 and robo2 receptors. J Neurosci. 2012;32(13):4372-85. 22457488 10.1523/JNEUROSCI.5851-11.2012
23. Hobert O Tessmar K Ruvkun G: The Caenorhabditis elegans lim-6 LIM homeobox gene regulates neurite outgrowth and function of particular GABAergic neurons. Development. 1999;126(7):1547-1562. 10068647
24. Manetopoulos C Hansson A Karlsson J: The LIM-only protein LMO4 modulates the transcriptional activity of HEN1. Biochem Biophys Res Commun. 2003;307(4):891-9. 12878195 10.1016/S0006-291X(03)01298-1
25. Elliott RC Khademi S Pleasure SJ: Differential regulation of basic helix-loop-helix mRNAs in the dentate gyrus following status epilepticus. Neuroscience. 2001;106(1):79-88. 11564418 10.1016/S0306-4522(01)00198-1
26. Elliott RC Miles MF Lowenstein DH: Overlapping microarray profiles of dentate gyrus gene expression during development- and epilepsy-associated neurogenesis and axon outgrowth. J Neurosci. 2003;23(6):2218-27. 12657681
27. Takasu MA Dalva MB Zigmond RE: Modulation of NMDA receptor-dependent calcium influx and gene expression through EphB receptors. Science. 2002;295(5554):491-5. 11799243 10.1126/science.1065983
28. Parent JM Lowenstein DH: Seizure-induced neurogenesis: are more new neurons good for an adult brain? Prog Brain Res. 2002;135:121-131. 12143334 10.1016/S0079-6123(02)35012-X
29. Nadler JV: The recurrent mossy fiber pathway of the epileptic brain. Neurochem Res. 2003;28(11):1649-58. 14584819 10.1023/A:1026004904199
30. Overstreet-Wadiche LS Bromberg DA Bensen AL: Seizures accelerate functional integration of adult-generated granule cells. J Neurosci. 2006;26(15):4095-103. 16611826 10.1523/JNEUROSCI.5508-05.2006
31. Scharfman HE McCloskey DP: Postnatal neurogenesis as a therapeutic target in temporal lobe epilepsy. Epilepsy Res. 2009;85(2-3):150-61. 19369038 10.1016/j.eplepsyres.2009.03.006 2713813
32. Sperber EF Haas KZ Stanton PK: Resistance of the immature hippocampus to seizure-induced synaptic reorganization. Brain Res Dev Brain Res. 1991;60(1):88-93. 1717181 10.1016/0165-3806(91)90158-F
33. Lynch M Sayin U Bownds J: Long-term consequences of early postnatal seizures on hippocampal learning and plasticity. Eur J Neurosci. 2000;12(7):2252-64. 10947804 10.1046/j.1460-9568.2000.00117.x
34. Porter BE: Neurogenesis and epilepsy in the developing brain. Epilepsia. 2008;49(Suppl 5):50-4. 18522600 10.1111/j.1528-1167.2008.01637.x 2700768
35. Alberini CM: Transcription factors in long-term memory and synaptic plasticity. Physiol Rev. 2009;89(1):121-45. 19126756 10.1152/physrev.00017.2008
36. Hinks GL Shah B French SJ: Expression of LIM protein genes Lmo1, Lmo2, and Lmo3 in adult mouse hippocampus and other forebrain regions: differential regulation by seizure activity. J Neurosci. 1997;17(14):5549-59. 9204936
37. Altman J Das GD: Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol. 1965;124(3):319-35. 5861717 10.1002/cne.901240303
38. Guéneau G Privat A Drouet J: Subgranular zone of the dentate gyrus of young rabbits as a secondary matrix. A high-resolution autoradiographic study. Dev Neurosci. 1982;5(4):345-58. 7140583 10.1159/000112694
39. Eckenhoff MF Rakic P: Nature and fate of proliferative cells in the hippocampal dentate gyrus during the life span of the rhesus monkey. J Neurosci. 1988;8(8):2729-47. 3411351
40. Gray WP Sundstrom LE: Kainic acid increases the proliferation of granule cell progenitors in the dentate gyrus of the adult rat. Brain Res. 1998;790(1-2):52-9. 9593820 10.1016/S0006-8993(98)00030-4
41. Wenzel HJ Woolley CS Robbins CA: Kainic acid-induced mossy fiber sprouting and synapse formation in the dentate gyrus of rats. Hippocampus. 2000;10(3):244-60. 10902894 10.1002/1098-1063(2000)10:3&<244::AID-HIPO5&>3.0.CO;2-7
42. Lein ES Zhao X Gage FH: Defining a molecular atlas of the hippocampus using DNA microarrays and high-throughput in situ hybridization. J Neurosci. 2004;24(15):3879-89. 15084669 10.1523/JNEUROSCI.4710-03.2004
43. Dong H Csernansky CA Goico B: Hippocampal neurogenesis follows kainic acid-induced apoptosis in neonatal rats. J Neurosci. 2003;23(5):1742-9. 12629178
44. Okazaki MM Evenson DA Nadler JV: Hippocampal mossy fiber sprouting and synapse formation after status epilepticus in rats: visualization after retrograde transport of biocytin. J Comp Neurol. 1995;352(4):515-34. 7721998 10.1002/cne.903520404
45. Smith BN Dudek FE: Short- and long-term changes in CA1 network excitability after kainate treatment in rats. J Neurophysiol. 2001;85(1):1-9. 11152700
46. Parent JM Yu TW Leibowitz RT: Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci. 1997;17(10):3727-38. 9133393
47. Jiang M Lee CL Smith KL: Spine loss and other persistent alterations of hippocampal pyramidal cell dendrites in a model of early-onset epilepsy. J Neurosci. 1998;18(20):8356-68. 9763479
48. Ribak CE Navetta MS: An immature mossy fiber innervation of hilar neurons may explain their resistance to kainate-induced cell death in 15-day-old rats. Brain Res Dev Brain Res. 1994;79(1):47-62. 8070064 10.1016/0165-3806(94)90048-5
49. Cornejo BJ Mesches MH Coultrap S: A single episode of neonatal seizures permanently alters glutamatergic synapses. Ann Neurol. 2007;61(5):411-26. 17323345 10.1002/ana.21071
50. Cross DJ Cavazos JE: Synaptic reorganization in subiculum and CA3 after early-life status epilepticus in the kainic acid rat model. Epilepsy Res. 2007;73(2):156-65. 17070016 10.1016/j.eplepsyres.2006.09.004 1876715
51. Gray WP May K Sundstrom LE: Seizure induced dentate neurogenesis does not diminish with age in rats. Neurosci Lett. 2002;330(3):235-8. 12270636 10.1016/S0304-3940(02)00810-8
52. Bender RA Dubé C Gonzalez-Vega R: Mossy fiber plasticity and enhanced hippocampal excitability, without hippocampal cell loss or altered neurogenesis, in an animal model of prolonged febrile seizures. Hippocampus. 2003;13(3):399-412. 12722980 10.1002/hipo.10089 2927853
53. Liu H Kaur J Dashtipour K: Suppression of hippocampal neurogenesis is associated with developmental stage, number of perinatal seizure episodes, and glucocorticosteroid level. Exp Neurol. 2003;184(1):196-213. 14637092 10.1016/S0014-4886(03)00207-3
54. Watanabe Y Johnson RS Butler LS: Null mutation of c-fos impairs structural and functional plasticities in the kindling model of epilepsy. J Neurosci. 1996;16(12):3827-36. 8656277
55. Kashani AH Qiu Z Jurata L: Calcium activation of the LMO4 transcription complex and its role in the patterning of thalamocortical connections. J Neurosci. 2006;26(32):8398-408. 16899735 10.1523/JNEUROSCI.0618-06.2006
56. Pennypacker KR McMillian MK Douglass J: Ontogeny of kainate-induced gene expression in rat hippocampus. J Neurochem. 1994;62(2):438-44. 8294905 10.1046/j.1471-4159.1994.62020438.x
57. Tauck DL Nadler JV: Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J Neurosci. 1985;5(4):1016-22. 3981241
58. Represa A Jorquera I Le Gal La Salle G: Epilepsy induced collateral sprouting of hippocampal mossy fibers: does it induce the development of ectopic synapses with granule cell dendrites? Hippocampus. 1993;3(3):257-68. 8353609 10.1002/hipo.450030303
59. Lynch M Sutula T: Recurrent excitatory connectivity in the dentate gyrus of kindled and kainic acid-treated rats. J Neurophysiol. 2000;83(2):693-704. 10669485
60. Perez Y Morin F Beaulieu C: Axonal sprouting of CA1 pyramidal cells in hyperexcitable hippocampal slices of kainate-treated rats. Eur J Neurosci. 1996;8(4):736-748. 9081625 10.1111/j.1460-9568.1996.tb01259.x
61. Lee SK Pfaff SL: Synchronization of neurogenesis and motor neuron specification by direct coupling of bHLH and homeodomain transcription factors. Neuron. 2003;38(5):731-45. 12797958 10.1016/S0896-6273(03)00296-4
62. Xu B Li S Brown A: EphA/ephrin-A interactions regulate epileptogenesis and activity-dependent axonal sprouting in adult rats. Mol Cell Neurosci. 2003;24(4):984-99. 14697663 10.1016/j.mcn.2003.08.003
63. Chen HH Schock SC Xu J: Extracellular ATP-dependent upregulation of the transcription cofactor LMO4 promotes neuron survival from hypoxia. Exp Cell Res. 2007;313(14):3106-16. 17524392 10.1016/j.yexcr.2007.04.026
64. Nair A Vadodaria KC Banerjee SB: Stressor-specific regulation of distinct brain-derived neurotrophic factor transcripts and cyclic AMP response element-binding protein expression in the postnatal and adult rat hippocampus. Neuropsychopharmacology. 2007;32(7):1504-19. 17164818 10.1038/sj.npp.1301276