Knockdown of STIM1 Improves Neuronal Survival After Traumatic Neuronal Injury Through Regulating mGluR1-Dependent Ca2+ Signaling in Mouse Cortical Neurons

Cellular and Molecular Neurobiology

Volumn 35, Issue 2, 2015, Pages 283-292

  Hou, Peng Fei ^a,b   Liu, Zhan Hui ^b   Li, Nan ^a,c   Cheng, Wen Jia ^b   Guo, Shi Wen ^a  

^a THE FIRST AFFILIATED HOSPITAL OF XI AN JIAOTONG UNIVERSITY   (China)

^b Ninth Hospital of xi'An   (China)

^c Department of Neurosurgery Xi an Chidren s Hospital   (China)

Author keywords

Endoplasmic reticulum; mGluR1; STIM1; Traumatic brain injury

Indexed keywords

INOSITOL TRISPHOSPHATE; LACTATE DEHYDROGENASE; METABOTROPIC RECEPTOR 1; RYANODINE RECEPTOR; STROMAL INTERACTION MOLECULE 1; CALCIUM CHANNEL; METABOTROPIC GLUTAMATE RECEPTOR TYPE 1; METABOTROPIC RECEPTOR; STIM1 PROTEIN, MOUSE;

ANIMAL CELL; APOPTOSIS; ARTICLE; BRAIN CELL; CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; ENDOPLASMIC RETICULUM; MOUSE; NERVE INJURY; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; TRAUMATIC NEURONAL INJURY; ANIMAL; BRAIN CORTEX; C57BL MOUSE; GENE SILENCING; INTRACELLULAR SPACE; METABOLISM; NERVE CELL; PATHOLOGY;

MAMMALIA;

ANIMALS; APOPTOSIS; CALCIUM CHANNELS; CALCIUM SIGNALING; CELL SURVIVAL; CEREBRAL CORTEX; ENDOPLASMIC RETICULUM; GENE KNOCKDOWN TECHNIQUES; INTRACELLULAR SPACE; MICE, INBRED C57BL; NEURONS; RECEPTORS, METABOTROPIC GLUTAMATE;

EID: 84923551039     PISSN: 02724340     EISSN: 15736830     Source Type: Journal    
DOI: 10.1007/s10571-014-0123-0     Document Type: Article

References (44)

1. Abramov AY, Duchen MR (2008) Mechanisms underlying the loss of mitochondrial membrane potential in glutamate excitotoxicity. Biochim Biophys Acta 1777(7–8):953–964. doi:10.1016/j.bbabio.2008.04.017
2. Algattas H, Huang JH (2014) Traumatic brain injury pathophysiology and treatments: early, intermediate, and late phases post-injury. Int J Mol Sci 15(1):309–341. doi:10.3390/ijms15010309
3. Arundine M, Tymianski M (2004) Molecular mechanisms of glutamate-dependent neurodegeneration in ischemia and traumatic brain injury. Cell Mol Life Sci 61(6):657–668. doi:10.1007/s00018-003-3319-x
4. Baba Y, Kurosaki T (2009) Physiological function and molecular basis of STIM1-mediated calcium entry in immune cells. Immunol Rev 231(1):174–188. doi:10.1111/j.1600-065X.2009.00813.x
5. Batchelor AM, Madge DJ, Garthwaite J (1994) Synaptic activation of metabotropic glutamate receptors in the parallel fibre-Purkinje cell pathway in rat cerebellar slices. Neuroscience 63(4):911–915
6. Belousov AB (2012) Novel model for the mechanisms of glutamate-dependent excitotoxicity: role of neuronal gap junctions. Brain Res 1487:123–130. doi:10.1016/j.brainres.2012.05.063
7. Chen T, Liu W, Chao X, Zhang L, Qu Y, Huo J, Fei Z (2011) Salvianolic acid B attenuates brain damage and inflammation after traumatic brain injury in mice. Brain Res Bull 84(2):163–168. doi:10.1016/j.brainresbull.2010.11.015
8. Chen T, Cao L, Dong W, Luo P, Liu W, Qu Y, Fei Z (2012a) Protective effects of mGluR5 positive modulators against traumatic neuronal injury through PKC-dependent activation of MEK/ERK pathway. Neurochem Res 37(5):983–990. doi:10.1007/s11064-011-0691-z
9. Chen T, Fei F, Jiang XF, Zhang L, Qu Y, Huo K, Fei Z (2012b) Down-regulation of Homer1b/c attenuates glutamate-mediated excitotoxicity through endoplasmic reticulum and mitochondria pathways in rat cortical neurons. Free Radic Biol Med 52(1):208–217. doi:10.1016/j.freeradbiomed.2011.10.451
10. Chen T, Zhang L, Qu Y, Huo K, Jiang X, Fei Z (2012c) The selective mGluR5 agonist CHPG protects against traumatic brain injury in vitro and in vivo via ERK and Akt pathway. Int J Mol Med 29(4):630–636. doi:10.3892/ijmm.2011.870
11. Chen T, Yang YF, Luo P, Liu W, Dai SH, Zheng XR, Fei Z, Jiang XF (2013a) Homer1 knockdown protects dopamine neurons through regulating calcium homeostasis in an in vitro model of Parkinson’s disease. Cell Signal 25(12):2863–2870. doi:10.1016/j.cellsig.2013.09.004
12. Chen T, Zhu J, Zhang C, Huo K, Fei Z, Jiang XF (2013b) Protective effects of SKF-96365, a non-specific inhibitor of SOCE, against MPP + -induced cytotoxicity in PC12 cells: potential role of Homer1. PLoS One 8(1):e55601. doi:10.1371/journal.pone.0055601
13. Cheng G, Kong RH, Zhang LM, Zhang JN (2012) Mitochondria in traumatic brain injury and mitochondrial-targeted multipotential therapeutic strategies. Br J Pharmacol 167(4):699–719. doi:10.1111/j.1476-5381.2012.02025.x
14. Cucchiaroni ML, Viscomi MT, Bernardi G, Molinari M, Guatteo E, Mercuri NB (2010) Metabotropic glutamate receptor 1 mediates the electrophysiological and toxic actions of the cycad derivative beta-N-Methylamino-l-alanine on substantia nigra pars compacta DAergic neurons. J Neurosci 30(15):5176–5188. doi:10.1523/JNEUROSCI.5351-09.2010
15. Dziadek MA, Johnstone LS (2007) Biochemical properties and cellular localisation of STIM proteins. Cell Calcium 42(2):123–132. doi:10.1016/j.ceca.2007.02.006
16. Faden AI, O’Leary DM, Fan L, Bao W, Mullins PG, Movsesyan VA (2001) Selective blockade of the mGluR1 receptor reduces traumatic neuronal injury in vitro and improvesoOutcome after brain trauma. Exp Neurol 167(2):435–444. doi:10.1006/exnr.2000.7577
17. Fahrner M, Muik M, Derler I, Schindl R, Fritsch R, Frischauf I, Romanin C (2009) Mechanistic view on domains mediating STIM1-Orai coupling. Immunol Rev 231(1):99–112. doi:10.1111/j.1600-065X.2009.00815.x
18. Fei Z, Zhang X, Jiang XF, Huang WD, Bai HM (2005) Altered expression patterns of metabotropic glutamate receptors in diffuse brain injury. Neurosci Lett 380(3):280–283. doi:10.1016/j.neulet.2005.01.063
19. Fei Z, Zhang X, Bai HM, Jiang XF, Wang XL (2006) Metabotropic glutamate receptor antagonists and agonists: potential neuroprotectors in diffuse brain injury. J Clin Neurosci 13(10):1023–1027. doi:10.1016/j.jocn.2005.11.042
20. Feyen BF, Sener S, Jorens PG, Menovsky T, Maas AI (2012) Neuromonitoring in traumatic brain injury. Minerva Anestesiol 78(8):949–958
21. Finch EA, Augustine GJ (1998) Local calcium signalling by inositol-1,4,5-trisphosphate in Purkinje cell dendrites. Nature 396(6713):753–756. doi:10.1038/25541
22. Ghajar J (2000) Traumatic brain injury. Lancet 356(9233):923–929. doi:10.1016/S0140-6736(00)02689-1
23. Gong QZ, Delahunty TM, Hamm RJ, Lyeth BG (1995) Metabotropic glutamate antagonist, MCPG, treatment of traumatic brain injury in rats. Brain Res 700(1–2):299–302
24. Goudet C, Magnaghi V, Landry M, Nagy F, Gereau RWt, Pin JP (2009) Metabotropic receptors for glutamate and GABA in pain. Brain Res Rev 60(1):43–56. doi:10.1016/j.brainresrev.2008.12.007
25. Gruszczynska-Biegala J, Pomorski P, Wisniewska MB, Kuznicki J (2011) Differential roles for STIM1 and STIM2 in store-operated calcium entry in rat neurons. PLoS One 6(4):e19285. doi:10.1371/journal.pone.0019285
26. Harraz OF, Altier C (2014) STIM1-mediated bidirectional regulation of Ca(2 +) entry through voltage-gated calcium channels (VGCC) and calcium-release activated channels (CRAC). Front Cell Neurosci 8:43. doi:10.3389/fncel.2014.00043
27. Hartmann J, Karl RM, Alexander RP, Adelsberger H, Brill MS, Ruhlmann C, Ansel A, Sakimura K, Baba Y, Kurosaki T, Misgeld T, Konnerth A (2014) STIM1 controls neuronal Ca(2)(+) signaling, mGluR1-dependent synaptic transmission, and cerebellar motor behavior. Neuron 82(3):635–644. doi:10.1016/j.neuron.2014.03.027
28. Hayashi MK, Tang C, Verpelli C, Narayanan R, Stearns MH, Xu RM, Li H, Sala C, Hayashi Y (2009) The postsynaptic density proteins Homer and Shank form a polymeric network structure. Cell 137(1):159–171. doi:10.1016/j.cell.2009.01.050
29. Huang WD, Fei Z, Zhang X (2005) Traumatic injury induced homer-1a gene expression in cultured cortical neurons of rat. Neurosci Lett 389(1):46–50. doi:10.1016/j.neulet.2005.07.014
30. Klejman ME, Gruszczynska-Biegala J, Skibinska-Kijek A, Wisniewska MB, Misztal K, Blazejczyk M, Bojarski L, Kuznicki J (2009) Expression of STIM1 in brain and puncta-like co-localization of STIM1 and ORAI1 upon depletion of Ca(2 +) store in neurons. Neurochem Int 54(1):49–55. doi:10.1016/j.neuint.2008.10.005
31. Lau A, Tymianski M (2010) Glutamate receptors, neurotoxicity and neurodegeneration. Pflugers Arch 460(2):525–542. doi:10.1007/s00424-010-0809-1
32. Li Y, Song J, Liu X, Zhang M, An J, Sun P, Li D, Jin T, Wang J (2013) High expression of STIM1 in the early stages of diffuse axonal injury. Brain Res 1495:95–102. doi:10.1016/j.brainres.2012.12.005
33. Li B, Xiao L, Wang ZY, Zheng PS (2014) Knockdown of STIM1 inhibits 6-hydroxydopamine-induced oxidative stress through attenuating calcium-dependent ER stress and mitochondrial dysfunction in undifferentiated PC12 cells. Free Radical Res 48(7):758–768. doi:10.3109/10715762.2014.905687
34. Ng AN, Krogh M, Toresson H (2011) Dendritic EGFP-STIM1 activation after type I metabotropic glutamate and muscarinic acetylcholine receptor stimulation in hippocampal neuron. J Neurosci Res 89(8):1235–1244. doi:10.1002/jnr.22648
35. O’Shea RD (2002) Roles and regulation of glutamate transporters in the central nervous system. Clin Exp Pharmacol Physiol 29(11):1018–1023
36. Parekh AB, Putney JW Jr (2005) Store-operated calcium channels. Physiol Rev 85(2):757–810. doi:10.1152/physrev.00057.2003
37. Potier M, Gonzalez JC, Motiani RK, Abdullaev IF, Bisaillon JM, Singer HA, Trebak M (2009) Evidence for STIM1- and Orai1-dependent store-operated calcium influx through ICRAC in vascular smooth muscle cells: role in proliferation and migration. FASEB J 23(8):2425–2437. doi:10.1096/fj.09-131128
38. Raghupathi R (2004) Cell death mechanisms following traumatic brain injury. Brain Pathol 14(2):215–222
39. Schindl R, Muik M, Fahrner M, Derler I, Fritsch R, Bergsmann J, Romanin C (2009) Recent progress on STIM1 domains controlling Orai activation. Cell Calcium 46(4):227–232. doi:10.1016/j.ceca.2009.08.003
40. Smith JS, Fulop ZL, Levinsohn SA, Darrell RS, Stein DG (2000) Effects of the novel NMDA receptor antagonist gacyclidine on recovery from medial frontal cortex contusion injury in rats. Neural plasticity 7(1–2):73–91. doi:10.1155/NP.2000.73
41. Stoica BA, Faden AI (2010) Cell death mechanisms and modulation in traumatic brain injury. Neurotherapeutics 7(1):3–12. doi:10.1016/j.nurt.2009.10.023
42. Stone TW, Addae JI (2002) The pharmacological manipulation of glutamate receptors and neuroprotection. Eur J Pharmacol 447(2–3):285–296
43. Urra H, Dufey E, Lisbona F, Rojas-Rivera D, Hetz C (2013) When ER stress reaches a dead end. Biochimica Et Biophysica Acta 1833(12):3507–3517. doi:10.1016/j.bbamcr.2013.07.024
44. Worley PF, Zeng W, Huang GN, Yuan JP, Kim JY, Lee MG, Muallem S (2007) TRPC channels as STIM1-regulated store-operated channels. Cell Calcium 42(2):205–211. doi:10.1016/j.ceca.2007.03.004