Interleukin-6 prevents NMDA-induced neuronal Ca2+ overload via suppression of IP3 receptors

Brain Injury

Volumn 27, Issue 9, 2013, Pages 1047-1055

  Liu, Zhan ^a,b   Fang, Xiao Xia ^b   Chen, Yu Ping ^b   Qiu, Yi Hua ^b   Peng, Yu Ping ^b  

^a SOOCHOW UNIVERSITY   (China)

^b NANTONG MEDICAL COLLEGE   (China)

Author keywords

Cerebellar granule neurons; Inositol 1,4,5 trisphosphate receptor; Interleukin 6; Intracellular Ca2+ overload; N methyl D aspartate; Ryanodine receptor

Indexed keywords

CALCIUM CHANNEL; DIZOCILPINE; INOSITOL 1,4,5 TRISPHOSPHATE; INTERLEUKIN 6; IP3 RECEPTOR PROTEIN; N METHYL DEXTRO ASPARTIC ACID; RECEPTOR PROTEIN; RYANODINE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CALCIUM CELL LEVEL; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EXPOSURE; FLUORESCENCE; NERVE CELL STIMULATION; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; RAT;

ANIMALS; ANIMALS, NEWBORN; CALCIUM; CELLS, CULTURED; CEREBELLUM; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; INTERLEUKIN-6; N-METHYLASPARTATE; NEURONS; NEUROPROTECTIVE AGENTS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 84880228891     PISSN: 02699052     EISSN: 1362301X     Source Type: Journal    
DOI: 10.3109/02699052.2013.794970     Document Type: Article

References (45)

1. Gadient RA, Otten UH. Interleukin-6 (IL-6)-A molecule with both beneficial and destructive potentials. Progress in Neurobiology 1997;52:379-390
2. Gruol DL, Nelson TE. Physiological and pathological roles of interleukin-6 in the central nervous system. Molecular Neurobiology 1997;15:307-339
3. Benveniste EN. Cytokine actions in the central nervous system. Cytokine & Growth Factor Reviews 1998;9:259-275
4. Van Wagoner NJ, Benveniste EN. Interleukin-6 expression and regulation in astrocytes. Journal of Neuroimmunology 1999;100: 124-139
5. Ali C, Nicole O, Docagne F, Lesne S, MacKenzie ET, Nouvelot A, Buisson A, Vivien D. Ischemia-induced interleukin-6 as a potential endogenous neuroprotective cytokine against NMDA receptormediated excitotoxicity in the brain. Journal of Cerebral Blood Flow & Metabolism 2000;20:956-966
6. Baker DG, Ekhator NN, Kasckow JW, Hill KK, Zoumakis E, Dashevsky BA, Chrousos GP, Geracioti Jr TD. Plasma and cerebrospinal fluid interleukin-6 concentrations in posttraumatic stress disorder. Neuroimmunomodulation 2001;9:209-217
7. Mutlu LK, Woiciechowsky C, Bechmann I. Inflammatory response after neurosurgery. Best Practice & Research Clinical Anaesthesiology 2004;18:407-424
8. Nakamachi T, Tsuchida M, Kagami N, Yofu S, Wada Y, Hori M, Tsuchikawa D, Yoshikawa A, Imai N, Nakamura K, Arata S, Shioda S. IL-6 and PACAP receptor expression and localization after global brain ischemia in mice. Journal of Molecular Neuroscience 2012;48:518-525. Available online at: Http://www.springerlink-com/10.1007/s12031-012-9819-0, accessed 6 June 2012
9. Penkowa M, Giralt M, Carrasco J, Hadberg H, Hidalgo J. Impaired inflammatory response and increased oxidative stress and neurodegeneration after brain injury in interleukin-6-deficient mice. Glia 2000;32:271-285
10. Herrmann O, Tarabin V, Suzuki S, Attigah N, Coserea I, Schneider A, Vogel J, Prinz S, Schwab S, Monyer H, et al. Regulation of body temperature and neuroprotection by endogenous interleukin-6 in cerebral ischemia. Journal of Cerebral Blood Flow & Metabolism 2003;23:406-415
11. Spittau B, Zhou X, Ming M, Krieglstein K. IL6 protects MN9D cells and midbrain dopaminergic neurons from MPP-induced neurodegeneration. Neuromolecular Medicine 2012;14:317-327. Available online at: Http://www.springerlink.com/10. 1007/s12017-012-8189-7, accessed 8 July 2012
12. Bensadoun JC, de Almeida LP, Dreano M, Aebischer P, Deglon N. Neuroprotective effect of interleukin-6 and IL6/IL6R chimera in the quinolinic acid rat model of Huntington's syndrome. European Journal of Neuroscience 2001; 14:1753-1761
13. Inomata Y, Hirata A, Yonemura N, Koga T, Kido N, Tanihara H. Neuroprotective effects of interleukin-6 on NMDA-induced rat retinal damage. Biochemical & Biophysical Research Communications 2003;302:226-232
14. Peng YP, Qiu YH, Lu JH, Wang JJ. Interleukin-6 protects cultured cerebellar granule neurons against glutamate-induced neurotoxicity. Neuroscience Letters 2005; 374:192-196
15. Wang XQ, Peng YP, Lu JH, Cao BB, Qiu YH. Neuroprotection of interleukin-6 against NMDA attack and its signal transduction by JAK and MAPK. Neuroscience Letters 2009;450:122-126
16. Liu Z, Qiu YH, Li B, Ma SH, Peng YP. Neuroprotection of interleukin-6 against NMDA-induced apoptosis and its signaltransduction mechanisms. Neurotoxicity Research 2011;19: 484-495
17. Suzuki S, Tanaka K, Suzuki N. Ambivalent aspects of interleukin-6 in cerebral ischemia: Inflammatory versus neurotrophic aspects. Journal of Cerebral Blood Flow & Metabolism 2009;29:464-479
18. Spooren A, Kolmus K, Laureys G, Clinckers R, De Keyser J, Haegeman G, Gerlo S. Interleukin-6, a mental cytokine. Brain Research Reviews 2011;67:157-183
19. Arundine M, Tymianski M. Molecular mechanisms of calciumdependent neurodegeneration in excitotoxicity. Cell Calcium 2003; 34:325-337
20. Qiu Z, Gruol DL. Interleukin-6, beta-Amyloid peptide and NMDA interactions in rat cortical neurons. Journal of Neuroimmunology 2003;139:51-57
21. Cucchiaroni ML, Viscomi MT, Bernardi G, Molinari M, Guatteo E, Mercuri NB. 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. Journal of Neuroscience 2010;30:5176-5188
22. Wang XC, Qiu YH, Peng YP. Interleukin-6 protects cerebellar granule neurons from NMDA-induced neurotoxicity. Sheng Li Xue Bao 2007;59:150-156
23. Qiu Z, Parsons KL, Gruol DL. Interleukin-6 selectively enhances the intracellular calcium response to NMDA in developing CNS neurons. Journal of Neuroscience 1995;15:6688-6699
24. Qiu Z, Sweeney DD, Netzeband JG, Gruol DL. Chronic interleukin-6 alters NMDA receptor-mediated membrane responses and enhances neurotoxicity in developing CNS neurons. Journal of Neuroscience 1998;18:10445-10456
25. Verkhratsky A, Petersen OH. The endoplasmic reticulum as an integrating signaling organelle: From neuronal signaling to neuronal death. European Journal of Pharmacology 2002;447:141-154
26. Sun XM, Lu JH, Qiu YH, Liu Z, Wang XQ, Peng YP. Interleukin-6 reduces NMDA-induced Ca2 overload via prevention of Ca2 release from intracellular store. International Journal of Neuroscience 2011;121:423-429
27. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using Real-Time quantitative PCR and the 2-DDCt method. Methods 2001;25:402-408
28. Hagar RE, Burgstahler AD, Nathanson MH, Ehrlich BE. Type III InsP3 receptor channel stays open in the presence of increased calcium. Nature 1998;396:81-84
29. Yang J, Mcbride S, Mark DO, Vardi N, Palczewski K, Haeseleer F, Foskett JK. Identification of a family of calcium sensors as protein ligands of inositol trisphosphate receptor (Ca2) release channels. Proceedings of the National Academy of Sciences USA 2002;99: 7711-7716
30. Bootman MD, Berridge MJ, Roderick HL. Activating calcium release through inositol 1,4,5-Trisphosphate receptors without inositol 1,4,5-Trisphosphate. Proceedings of the National Academy of Sciences USA 2002;99:7320-7322
31. Kasri NN, Holmes AM, Bultynck G, Parys JB, Bootman MD, Rietdorf K, Missiaen L, McDonald F, De Smedt H, Conway SJ, et al. Regulation of InsP3 receptor activicity by neuronal Ca2-binding proteins. EMBO Journal 2004;23: 312-321
32. Popescu AT, Saghyan AA, Nagy FZ, Paré D. Facilitation of corticostriatal plasticity by the amygdala requires Ca2-induced Ca2 release in the ventral striatum. Journal of Neurophysiology 2010;104:1673-1680
33. Gruol DL, Netzeband JG, Nelson TE. Somatic Ca2 signaling in cerebellar Purkinje neurons. Journal of Neuroscience Research 2010;88:275-289
34. Nakata H, Nakamura S. Brain-derived neurotrophic factor regulates AMPA receptor trafficking to post-synaptic densities via IP3R and TRPC calcium signaling. FEBS Letters 2007;581: 2047-2054
35. Turovskaya MV, Turovsky EA, Zinchenko VP, Levin SG, Godukhin OV. Interleukin-10 modulates [Ca2]i response induced by repeated NMDA receptor activation with brief hypoxia through inhibition of InsP(3)-sensitive internal stores in hippocampal neurons. Neuroscience Letters 2012;516: 151-155
36. Moriyoshi K, Masu M, Ishii T, Shigemono R, Mizuno N, Nakanishi S. Molecular cloning and characterization of the rat NMDA receptor. Nature 1991;354:31-37
37. Resink A, Villa M, Boer GJ, Möhler H, Balázs R. Agonistinduced down regulation of NMDA receptors in cerebellar granule cell cultures. European Journal of Neuroscience 1995;7: 1700-1706
38. Resink A, Villa M, Benke D, Hidaka H, Möhler H, Balázs R. Characterization of agonist-induced down regulation of NMDA receptors in cerebellar granule cell cultures. Journal of Neurochemistry 1996;66:369-377
39. Brandoli C, Sanna A, De Bernardi MA, Follesa P, Brooker G, Mocchetti I. Brain-derived neurotrophic factor and basic fibroblast growth factor downregulate NMDA receptor function in cerebellar granule cells. Journal of Neuroscience 1998;18: 7953-7961
40. Kutsuwada T, Kashiwabuchi N, Mori H, Sakimura K, Kushiya E, Araki K, Meguro H, Masaki H, Kumanishi T, Arakawa M, et al. Molecular diversity of the NMDA receptor channel. Nature 1992; 358:36-42
41. Monyer H, Sprengel R, Schoepfer R, Herb A, Higuci M, Lomeli H, Burnashev N, Sakmann B, Seeburg PH. Heteromeric NMDA receptors: Molecular and functional distinction of subtypes. Science 1992;256: 1217-1221
42. Hollmann M, Heinemann H. Cloned glutamate receptors. Annual Review of Neuroscience 1994;17:31-108
43. Genazzani AA, Carafoli E, Guerini D. Calcineurin controls inositol 1,4,5-Trisphosphate type 1 receptor expression in neurons. Proceedings of the National Academy of Science USA 1999;96: 5797-5801
44. Gruol DL, Puro A, Hao C, Blakely P, Janneke E, Vo K. Neuroadaptive changes in cerebellar neurons induced by chronic exposure to IL-6. Journal of Neuroimmunology 2011;239: 28-36
45. Mhyre TR, Maine DN, Holliday J. Calciuminduced calcium release from intracellular stores is developmentally regulated in primary cultures of cerebellar granule neurons. Journal of Neurobiology 2000;42: 134-147