Upregulation and Diverse Roles of TRPC3 and TRPC6 in Synaptic Reorganization of the Mossy Fiber Pathway in Temporal Lobe Epilepsy

Molecular Neurobiology

Volumn 52, Issue 1, 2015, Pages 562-572

  Zeng, Chang ^a,b   Zhou, Pinting ^b   Jiang, Ting ^a   Yuan, Chunyun ^c   Ma, Yan ^d   Feng, Li ^b   Liu, Renkai ^e   Tang, Weiting ^b   Long, Xiaoyan ^b   Xiao, Bo ^b   Tian, Fafa ^b  

^a CENTRAL SOUTH UNIVERSITY   (China)

^b CENTRAL SOUTH UNIVERSITY   (China)

^c Hunan Aerospace Administration Bureau   (China)

^d Department of Dentistry The First People s Hospital of Yueyang   (China)

^e GUANGDONG MEDICAL UNIVERSITY   (China)

Author keywords

Pilocarpine; Synaptic reorganization; Temporal lobe epilepsy; TRPC3 channel; TRPC6 channel

Indexed keywords

TRANSIENT RECEPTOR POTENTIAL CHANNEL 3; TRANSIENT RECEPTOR POTENTIAL CHANNEL 6; PILOCARPINE; TRANSIENT RECEPTOR POTENTIAL CHANNEL C; TRPC6 PROTEIN, HUMAN; TRPC6 PROTEIN, MOUSE;

ADOLESCENT; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; EPILEPTOGENESIS; HIPPOCAMPAL CA3 REGION; HIPPOCAMPAL MOSSY FIBER; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SYNAPTIC REORGANIZATION; SYNAPTIC TRANSMISSION; TEMPORAL CORTEX; TEMPORAL LOBE EPILEPSY; UPREGULATION; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CASE CONTROL STUDY; CHEMICALLY INDUCED; DENDRITE; EPILEPTIC STATE; METABOLISM; MIDDLE AGED; PATHOLOGY; SYNAPSE; TEMPORAL LOBE; YOUNG ADULT;

ADOLESCENT; ADULT; ANIMALS; CA3 REGION, HIPPOCAMPAL; CASE-CONTROL STUDIES; CHILD; DENDRITES; EPILEPSY, TEMPORAL LOBE; HUMANS; MALE; MICE, INBRED C57BL; MIDDLE AGED; MOSSY FIBERS, HIPPOCAMPAL; PILOCARPINE; STATUS EPILEPTICUS; SYNAPSES; TEMPORAL LOBE; TRPC CATION CHANNELS; UP-REGULATION; YOUNG ADULT;

EID: 84937926095     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-014-8871-x     Document Type: Article

References (41)

1. Spencer DD, Spencer SS, Mattson RH, Williamson PD, Novelly RA (1984) Access to the posterior medial temporal lobe structures in the surgical treatment of temporal lobe epilepsy. Neurosurgery 15(5):667–671
2. Bae EK, Jung KH, Chu K, Lee ST, Kim JH, Park KI, Kim M, Chung CK, Lee SK, Roh JK (2010) Neuropathologic and clinical features of human medial temporal lobe epilepsy. J Clin Neurol 6(2):73–80
3. Ikegaya Y, Nishiyama N, Matsuki N (2000) L-type Ca(2+) channel blocker inhibits mossy fiber sprouting and cognitive deficits following pilocarpine seizures in immature mice. Neuroscience 98(4):647–659
4. Becker AJ, Pitsch J, Sochivko D, Opitz T, Staniek M, Chen CC, Campbell KP, Schoch S, Yaari Y, Beck H (2008) Transcriptional upregulation of Cav3.2 mediates epileptogenesis in the pilocarpine model of epilepsy. J Neurosci 28(49):13341–13353
5. Clapham DE (2003) TRP channels as cellular sensors. Nature 426(6966):517–524
6. Vazquez G, Wedel BJ, Aziz O, Trebak M, Putney JW (2004) The mammalian TRPC cation channels. Biochim Biophys Acta-Mol Cell Res 1742(1–3):21–36
7. Wes PD, Chevesich J, Jeromin A, Rosenberg C, Stetten G, Montell C (1995) TRPC1, a human homolog of a Drosophila store-operated channel. Proc Natl Acad Sci U S A 92(21):9652–9656
8. Zhu X, Chu PB, Peyton M, Birnbaumer L (1995) Molecular cloning of a widely expressed human homologue for the Drosophila trp gene. FEBS Lett 373(3):193–198
9. Harteneck C, Plant TD, Schultz G (2000) From worm to man: three subfamilies of TRP channels. Trends Neurosci 23(4):159–166
10. Montell C, Birnbaumer L, Flockerzi V (2002) The TRP channels, a remarkably functional family. Cell 108(5):595–598
11. Kunert-Keil C, Bisping F, Kruger J, Brinkmeier H (2006) Tissue-specific expression of TRP channel genes in the mouse and its variation in three different mouse strains. BMC Genomics 7:159
12. Riccio A, Medhurst AD, Mattei C, Kelsell RE, Calver AR, Randall AD, Benham CD, Pangalos MN (2002) mRNA distribution analysis of human TRPC family in CNS and peripheral tissues. Mol Brain Res 109(1–2):95–104
13. Li Y, Jia YC, Cui K, Li N, Zheng ZY, Wang YZ, Yuan XB (2005) Essential role of TRPC channels in the guidance of nerve growth cones by brain-derived neurotrophic factor. Nature 434(7035):894–898
14. Greka A, Navarro B, Oancea E, Duggan A, Clapham DE (2003) TRPC5 is a regulator of hippocampal neurite length and growth cone morphology. Nat Neurosci 6(8):837–845
15. Jia YC, Zhou J, Tai YL, Wang YZ (2007) TRPC channels promote cerebellar granule neuron survival. Nat Neurosci 10(5):559–567
16. Zhou J, Du WL, Zhou KC, Tai YL, Yao HL, Jia YC, Ding YQ, Wang YZ (2008) Critical role of TRPC6 channels in the formation of excitatory synapses. Nat Neurosci 11(7):741–743
17. Xie A, Aihara Y, Bouryi VA, Nikitina E, Jahromi BS, Zhang ZD, Takahashi M, Macdonald RL (2007) Novel mechanism of endothelin-1-induced vasospasm after subarachnoid hemorrhage. J Cereb Blood Flow Metab 27(10):1692–1701
18. Yamamoto S, Wajima T, Hara Y, Nishida M, Mori Y (2007) Transient receptor potential channels in Alzheimer’s disease. Biochim Biophys Acta-Mol Basis Dis 1772(8):958–967
19. Becker EBE, Olivera PL, Glitsch MD, Banks GT, Achilli F, Hardy A, Nolan PM, Fisher EMC, Davies KE (2009) A point mutation in TRPC3 causes abnormal Purkinje cell development and cerebellar ataxia in moonwalker mice. Proc Natl Acad Sci U S A 106(16):6706–6711
20. Wang M, Bianchi R, Chuang SC, Zhao WF, Wong RKS (2007) Group I metabotropic glutamate receptor-dependent TRPC channel trafficking in hippocampal neurons. J Neurochem 101(2):411–421
21. Kim DS, Ryu HJ, Kim JE, Kang TC (2013) The reverse roles of transient receptor potential canonical channel-3 and -6 in neuronal death following pilocarpine-induced status epilepticus. Cell Mol Neurobiol 33(1):99–109
22. Peng Z, Houser CR (2005) Temporal patterns of fos expression in the dentate gyrus after spontaneous seizures in a mouse model of temporal lobe epilepsy. J Neurosci: Off J Soc Neurosci 25(31):7210–7220
23. Muramatsu R, Ikegaya Y, Matsuki N, Koyama R (2008) Early-life status epilepticus induces ectopic granule cells in adult mice dentate gyrus. Exp Neurol 211(2):503–510
24. Holmes GL, Sarkisian M, Ben-Ari Y, Chevassus-Au-Louis N (1999) Mossy fiber sprouting after recurrent seizures during early development in rats. J Comp Neurol 404(4):537–553
25. Chung YH, Ahn HS, Kim D, Shin DH, Kim SS, Kim KY, Lee WB, Cha CI (2006) Immunohistochemical study on the distribution of TRPC channels in the rat hippocampus. Brain Res 1085:132–137
26. Tai YL, Feng SJ, Ge RL, Du WL, Zhang XX, He ZH, Wang YZ (2008) TRPC6 channels promote dendritic growth via the CaMKIV-CREB pathway. J Cell Sci 121(14):2301–2307
27. Cross DJ, Cavazos JE (2007) Synaptic reorganization in subiculum and CA3 after early-life status epilepticus in the kainic acid rat model. Epilepsy Res 73(2):156–165
28. Tian FF, Zeng C, Guo TH, Chen Y, Chen JM, Ma YF, Fang J, Cai XF, Li FR, Wang XH, Huang WJ, Fu JJ, Dang J (2009) Mossy fiber sprouting, hippocampal damage and spontaneous recurrent seizures in pentylenetetrazole kindling rat model. Acta Neurol Belg 109(4):298–304
29. Feng L, Long HY, Liu RK, Sun DN, Liu C, Long LL, Li Y, Chen S, Xiao B (2013) A quantum dot probe conjugated with abeta antibody for molecular imaging of Alzheimer’s disease in a mouse model. Cell Mol Neurobiol 33(6):759–765
30. Klyubin I, Walsh DM, Lemere CA, Cullen WK, Shankar GM, Betts V, Spooner ET, Jiang L, Anwyl R, Selkoe DJ, Rowan MJ (2005) Amyloid beta protein immunotherapy neutralizes Abeta oligomers that disrupt synaptic plasticity in vivo. Nat Med 11(5):556–561
31. Amaral MD, Pozzo-Miller L (2007) TRPC3 channels are necessary for brain-derived neurotrophic factor to activate a nonselective cationic current and to induce dendritic spine formation. J Neurosci 27(19):5179–5189
32. Minke B, Selinger Z (1996) Role of Drosophila TRP in inositide-mediated Ca2+ entry. Mol Neurobiol 12(2):163–180
33. Hering H, Sheng M (2001) Dendritic spines: structure, dynamics and regulation. Nat Rev Neurosci 2(12):880–888
34. Isokawa M (1998) Remodeling dendritic spines in the rat pilocarpine model of temporal lobe epilepsy. Neurosci Lett 258(2):73–76
35. Ferhat L, Esclapez M, Represa A, Fattoum A, Shirao T, Ben-Ari Y (2003) Increased levels of acidic calponin during dendritic spine plasticity after pilocarpine-induced seizures. Hippocampus 13(7):845–858
36. Wong M (2005) Modulation of dendritic spines in epilepsy: cellular mechanisms and functional implications. Epilepsy Behav 7(4):569–577
37. Kurz JE, Moore BJ, Henderson SC, Campbell JN, Churn SB (2008) A cellular mechanism for dendritic spine loss in the pilocarpine model of status epilepticus. Epilepsia 49(10):1696–1710
38. Bundman MC, Pico RM, Gall CM (1994) Ultrastructural plasticity of the dentate gyrus granule cells following recurrent limbic seizures: I. Increase in somatic spines. Hippocampus 4(5):601–610
39. Isokawa M (2000) Remodeling dendritic spines of dentate granule cells in temporal lobe epilepsy patients and the rat pilocarpine model. Epilepsia 41(Suppl 6):S14–S17
40. Sierra-Paredes G, Oreiro-Garcia T, Nunez-Rodriguez A, Vazquez-Lopez A, Sierra-Marcuno G (2006) Seizures induced by in vivo latrunculin a and jasplakinolide microperfusion in the rat hippocampus. J Mol Neurosci 28(2):151–160
41. Isokawa M (1997) Preservation of dendrites with the presence of reorganized mossy fiber collaterals in hippocampal dentate granule cells in patients with temporal lobe epilepsy. Brain Res 744(2):339–343