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Effects of BDNF deficiency and endoplasmic reticulum stress on the GABAergic system

Yıl 2021, Cilt 14, Sayı 4, 792 - 802, 01.10.2021
https://doi.org/10.31362/patd.834832

Öz

Purpose: Protective pathways against endoplasmic reticulum stress in neurons are activated via brain-derived neurotrophic factor. However, it is not known how the inhibitory intermediate neuron types expressing the different Ca2+-binding proteins of GABAergic system will be affected with changes in Ca2+ homeostasis, in conditions of chronic reduction of brain-derived neurotrophic factor and endoplasmic reticulum stress. The study was planned to reveal the interaction of these factors. Materials and methods: 6-8 months old (30-40 g), wild-type (WT) and brain-derived neurotrophic factor heterozygous (BDNF(+/-)) male mice were used and 4 groups were formed. Groups 3 and 4 were treated with a single dose of tunicamycin to induce endoplasmic reticulum stress. On the 3rd day of tunicamycin injection, animals were sacrificed and blood and brain tissues were taken. In serum samples BDNF, in tissue homogenates GRP78, CHOP, Caspase-12, parvalbumin, calretinin, calbindin, GAD65 and GAD67 levels were investigated by ELISA method. One-way ANOVA and Tukey post-hoc tests were used for statistical evaluation. Results: Serum BDNF levels were significantly lower in BDNF(+/-) and tunicamycin-treated BDNF(+/-) groups. Caspase-12 and CHOP levels significantly increased with tunicamycin injection. Calbindin level decreased significantly with endoplasmic reticulum stress. GAD65 and GAD67 levels were similar in WT and BDNF(+/-) groups. However, GAD65 level was significantly decreased during endoplasmic reticulum stress in WT and BDNF(+/-) groups. Conclusion: Endoplasmic reticulum stress caused a significant decrease in glutamic acid decarboxylase GAD65 isoform and caldindin levels. This result indicates that the sensitivity of varied intermediate neurons in GABAergic system to endoplasmic reticulum stress may be different.

Kaynakça

  • DeFelipe J. Chandelier cells and epilepsy. Brain 1999;122:1807-1822. https://doi.org/10.1093/brain/122.10.1807
  • Martin DL, Rimvall K. Regulation of gamma-aminobutyric acid synthesis in the brain. J Neurochem 1993;60:395-407. https://doi.org/10.1111/j.1471-4159.1993.tb03165.x
  • Esclapez M, Tillakaratne NJ, Kaufman DL, Tobin AJ, Houser CR. Comparative localization of two forms of glutamic acid decarboxylase and their mRNAs in rat brain supports the concept of functional differences between the forms. J Neurosci 1994;14:1834-1855. https://doi.org/10.1523/JNEUROSCI.14-03-01834.1994
  • Kawaguchi Y, Kubota Y. Neurochemical features and synaptic connections of large physiologically-identified GABAergic cells in the rat frontal cortex. Neuroscience 1998;85:677-701. https://doi.org/10.1016/S0306-4522(97)00685-4
  • Markram H, Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C. Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 2004;5:793-807. https://doi.org/10.1038/nrn1519
  • Blatow M, Rozov A, Katona I, et al. A novel network of multipolar bursting interneurons generates theta frequency oscillations in neocortex. Neuron 2003;38:805-817. https://doi.org/10.1016/s0896-6273(03)00300-3
  • Lewin GR, Barde YA. 1996. Physiology of neurotrophins. Annu Rev Neurosci 1996;19:289-317. https://doi.org/10.1146/annurev.ne.19.030196.001445
  • Nieto Gonzalez JL, Jensen K. BDNF depresses excitability of parvalbumin -positive interneurons through an M-like current in rat dentate gyrus. PLoS One 2013;8:e67318. https://doi.org/10.1371/journal.pone.0067318
  • Benes FM, Berretta S. GABAergic interneurons: implications for understanding schizophrenia and bipolar disorder. Neuropsychopharmacol 2001;25:1-27. https://doi.org/10.1016/S0893-133X(01)00225-1
  • Bravo R, Parra V, Gatica D, et al. Endoplasmic reticulum and the unfolded protein response: dynamics and metabolic integration. Int Rev Cell Mol Biol 2013;301:215-290. https://doi.org/10.1016/B978-0-12-407704-1.00005-1
  • Wärri A, Cook KL, Hu R, et al. Autophagy and unfolded protein response (UPR) regulate mammary gland involution by restraining apoptosis-driven irreversible changes. Cell Death Discov 2018;15;4:40. https://doi.org/10.1038/s41420-018-0105-y
  • Zhang K, Kaufman RJ. The unfolded protein response: a stress signaling pathway critical for health and disease. Neurology 2006;24:102-109. https://doi.org/10.1212/01.wnl.0000192306.98198.ec
  • Groenendyk J, Peng Z, Dudek E, et al. Interplay between the oxidoreductase PDIA6 and microRNA-322 controls the response to disrupted endoplasmic reticulum calcium homeostasis. Sci Signal 2014;7:54. https://doi.org/10.1126/scisignal.2004983
  • Yang Y, Ma F, Liu Z, et al. The ER-localized Ca2+-binding protein calreticulin couples ER stress to autophagy by associating with microtubule-associated protein 1A/1B light chain 3. J Biol Chem 2019;294:772-782. https://doi.org/10.1074/jbc.RA118.005166
  • Xiao F, Zhang P, Chen AH, et al. Hydrogen sulfide inhibits MPP+-induced aldehyde stress and endoplasmic reticulum stress in PC12 cells: involving upregulation of BDNF. Exp Cell Res 2016;348:106-114. https://doi.org/10.1016/j.yexcr.2016.09.006
  • Shimoke K, Utsumi T, Kishi S, et al. Prevention of endoplasmic reticulum stress-induced cell death by brain-derived neurotrophic factor in cultured cerebral cortical neurons. Brain Res 2004;1028:105-111. https://doi.org/10.1016/j.brainres.2004.09.005
  • Chen G, Fan Z, Wang X, et al. Brain-derived neurotrophic factor suppresses tunicamycin-induced upregulation of CHOP in neurons. J Neurosci Res 2007;85:1674-1684. https://doi.org/10.1002/jnr.21292
  • Korte M, Carroll P, Wolf E, Brem G, Thoenen H, Bonhoeffer T. Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc Natl Acad Sci USA 1995;92:8856-8860. https://doi.org/10.1073/pnas.92.19.8856
  • Abidin I, Yildirim M, Aydin-Abidin S, et al. Penicillin-induced epileptiform activity and EEG spectrum analysis of BDNF heterozygous mice: an in vivo electrophysiological study. Brain Res Bull 2011;86:159-164. https://doi.org/10.1016/j.brainresbull.2011.06.015
  • De Miguel C, Hamrick WC, Hobbs JL, Pollock DM, Carmines PK, Pollock JS. Endothelin receptor-specific control of endoplasmic reticulum stress and apoptosis in the kidney. Sci Rep 2017;7:43152. https://doi.org/10.1038/srep43152
  • Hodeify R, Megyesi J, Tarcsafalvi A, Mustafa HI, Lar Seng NS, Price PM. Gender differences control the susceptibility to ER stress-induced acute kidney injury. Am J Physiol Renal Physiol 2013;304:875-882. https://doi.org/10.1152/ajprenal.00590.2012
  • Jiao G, Hao L, Wang M, et al. Upregulation of endoplasmic reticulum stress is associated with diaphragm contractile dysfunction in a rat model of sepsis. Mol Med Rep 2017;15:366-374. https://doi.org/10.3892/mmr.2016.6014
  • Huang Y, Leng TD, Inoue K, et al. TRPM7 channels play a role in high glucose-induced endoplasmic reticulum stress and neuronal cell apoptosis. J Biol Chem 2018;293:14393-14406. https://doi.org/10.1074/jbc.RA117.001032
  • Abidin I, Köhler T, Weiler E, Zoidl G, Eysel UT, Lessmann V, et al. Reduced presynaptic efficiency of excitatory synaptic transmission impairs LTP in the visual cortex of BDNF-heterozygous mice. Eur J Neurosci 2006;24:3519-3531. https://doi.org/10.1111/j.1460-9568.2006.05242.x
  • Lyons WE, Mamounas LA, Ricaurte GA, et al. Brain-derived neurotrophic factor-deficient mice develop aggressiveness and hyperphagia in conjunction with brain serotonergic abnormalities. Proc Natl Acad Sci USA 1999;9:15239-15244. https://doi.org/10.1073/pnas.96.26.15239
  • Duan W, Guo Z, Jiang H, Ware M, Mattson MP. Reversal of behavioral and metabolic abnormalities, and insulin resistance syndrome, by dietary restriction in mice deficient in brain-derived neurotrophic factor. Endocrinology 2003;144:2446-2453. https://doi.org/10.1210/en.2002-0113
  • Steele KE, Seth P, Lebaron KM, et al. Tunicamycin enhances neuroinvasion and encephalitis in mice infected with Venezuelan equine encephalitis virus. Vet Pathol 2006;43:904-913. https://doi.org/10.1354/vp.43-6-904
  • Xu C, Bailly-Maitre B, Reed JC. Endoplasmic reticulum stress: cell life and death decisions. J Clin Invest 2005;115:2656-2664. https://doi.org/10.1172/JCI26373
  • Cao SS, Kaufman RJ. Unfolded protein response. Curr Biol 2012;22:622-626. https://doi.org/10.1016/j.cub.2012.07.004
  • Breckenridge DG, Germain M, Mathai JP, Nguyen M, Shore GC. Regulation of apoptosis by endoplasmic reticulum pathways. Oncogene 2003;22:8608-8618. https://doi.org/10.1038/sj.onc.1207108
  • Oyadomari S, Mori M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 2004;11:381-389. https://doi.org/10.1038/sj.cdd.4401373
  • Wei HJ, Xu JH, Li MH,et al. Hydrogen sulfide inhibits homocysteine-induced endoplasmic reticulum stress and neuronal apoptosis in rat hippocampus via upregulation of the BDNF-TrkB pathway. Acta Pharmacol Sin 2014;35:707-715. https://doi.org/10.1038/aps.2013.197
  • Fish KN, Rocco BR, Lewis DA. Laminar distribution of subsets of GABAergic axon terminals in human prefrontal cortex. Front Neuroanat 2018;16;12:9. https://doi.org/10.3389/fnana.2018.00009
  • Grosse G, Djalali S, Deng DR, Höltje M, Hinz B, Schwartzkopff K, et al. Area-specific effects of brain-derived neurotrophic factor (BDNF) genetic ablation on various neuronal subtypes of the mouse brain. Dev Brain Res 2005;156:111-126. https://doi.org/10.1016/j.devbrainres.2004.12.012
  • Turovsky EA, Zinchenko VP, Gaidin SG, Turovskaya MV. Calcium-binding proteins protect GABAergic neurons of the hippocampus from hypoxia and ischemia in vitro. Biochem Moscow Suppl 2018;12:74-84. https://doi.org/10.1134/S1990747818010105
  • Elliott JL, Snider WD. Parvalbumin is a marker of ALS-resistant motor neurons. Neuroreport 1995;6:449-452. https://doi.org/:10.1097/00001756-199502000-00011
  • D’Orlando C, Fellay B, Schwaller B, Salicio V, Bloc A, Gotzos V, et al. Calretinin and calbindin D-28k delay the onset of cell death after excitotoxic stimulation in transfected P19 cells. Brain Res 2001;909:145-158. https://doi.org/10.1016/S0006-8993(01)02671-3
  • Lewis DA, Hashimoto T, Volk DW. Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 2005;6:312-324. https://doi.org/10.1038/nrn1648
  • Cramer NP, Best TK, Stoffel M, Siarey RJ, Galdzicki Z. GABAB-GIRK2- mediated signaling in Down syndrome. Adv Pharmacol 2010;58:397-426. https://doi.org/10.1016/S1054-3589(10)58015-3
  • Rossignol E. Genetics and function of neocortical GABAergic interneurons in neurodevelopmental disorders. Neural Plast 2011;2011:649325. https://doi.org/10.1155/2011/649325
  • Lee B, Zhang Y, Kim Y, Kim S, Lee Y, Han K. Age-dependent decrease of GAD65/67 mRNAs but normal densities of GABAergic interneurons in the brain regions of Shank3-overexpressing manic mouse model. Neurosci Lett 2017;649:48-54. https://doi.org/10.1016/j.neulet.2017.04.016
  • Gogolla N, Leblanc JJ, Quast KB, Südhof TC, Fagiolini M, Hensch TK. Common circuit defect of excitatory-inhibitory balance in mouse models of autism. J Neurodev Disord 2009;1:172-181. https://doi.org/10.1007/s11689-009-9023-x

BDNF eksikliği ve endoplazmik retikulum stresinin GABAerjik sistem üzerindeki etkileri

Yıl 2021, Cilt 14, Sayı 4, 792 - 802, 01.10.2021
https://doi.org/10.31362/patd.834832

Öz

Amaç: Nöronlarda endoplazmik retikulum stresine karşı koruyucu yollar, beyin kaynaklı nörotrofik faktör aracılığıyla etkinleştirilir. Bununla birlikte, GABAerjik sistemin farklı Ca2+-bağlayıcı proteinlerini eksprese eden inhibitör ara nöron tiplerinin, beyin kaynaklı nörotrofik faktörün kronik azalması ve endoplazmik retikulum stres koşullarında Ca2+ homeostazındaki değişikliklerden nasıl etkileneceği bilinmemektedir. Çalışma, bu faktörlerin etkileşimini ortaya çıkarmak için planlandı. Gereç ve yöntem: 6-8 aylık (30-40 gr), yabanıl tip (WT) ve beyin kaynaklı nörotrofik faktör heterozigot (BDNF(+/-)) erkek fareler kullanılmış ve 4 grup oluşturulmuştur. Grup 3 ve 4, endoplazmik retikulum stresini indüklemek için tek doz tunikamisin ile muamele edildi. Tunikamisin enjeksiyonunun 3. gününde hayvanlar feda edilerek kan ve beyin dokuları alındı. Serum örneklerinde BDNF, doku homojenatlarında GRP78, CHOP, Kaspaz-12, parvalbumin, kalretinin, kalbindin, GAD65 ve GAD67 düzeyleri ELISA yöntemi ile analiz edildi. İstatistiksel değerlendirme için tek yönlü ANOVA ve Tukey post-hoc testleri kullanıldı. Bulgular: Serum BDNF seviyeleri, BDNF(+/-) ve tunikamisin ile tedavi edilen BDNF(+/-) gruplarında anlamlı olarak daha düşüktü. Tunikamisin enjeksiyonu ile Kaspaz-12 ve CHOP seviyeleri önemli ölçüde artmıştır. Kalbindin düzeyi endoplazmik retikulum stresi ile önemli ölçüde azaldı. GAD65 ve GAD67 seviyeleri WT ve BDNF(+/-) gruplarında yakındı. Ancak WT ve BDNF(+/-) gruplarında endoplazmik retikulum stresi sırasında GAD65 düzeyi anlamlı olarak azaldı. Sonuç: Endoplazmik retikulum stresi glutamik asit dekarboksilazın GAD65 izoformunda ve kalbindin düzeylerinde anlamlı bir düşüşe sebep olmuştur. Bu sonuç, GABAerjik sistemdeki çeşitli ara nöronların endoplazmik retikulum stresine duyarlılıklarının farklı olabileceğini göstermektedir.

Kaynakça

  • DeFelipe J. Chandelier cells and epilepsy. Brain 1999;122:1807-1822. https://doi.org/10.1093/brain/122.10.1807
  • Martin DL, Rimvall K. Regulation of gamma-aminobutyric acid synthesis in the brain. J Neurochem 1993;60:395-407. https://doi.org/10.1111/j.1471-4159.1993.tb03165.x
  • Esclapez M, Tillakaratne NJ, Kaufman DL, Tobin AJ, Houser CR. Comparative localization of two forms of glutamic acid decarboxylase and their mRNAs in rat brain supports the concept of functional differences between the forms. J Neurosci 1994;14:1834-1855. https://doi.org/10.1523/JNEUROSCI.14-03-01834.1994
  • Kawaguchi Y, Kubota Y. Neurochemical features and synaptic connections of large physiologically-identified GABAergic cells in the rat frontal cortex. Neuroscience 1998;85:677-701. https://doi.org/10.1016/S0306-4522(97)00685-4
  • Markram H, Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C. Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 2004;5:793-807. https://doi.org/10.1038/nrn1519
  • Blatow M, Rozov A, Katona I, et al. A novel network of multipolar bursting interneurons generates theta frequency oscillations in neocortex. Neuron 2003;38:805-817. https://doi.org/10.1016/s0896-6273(03)00300-3
  • Lewin GR, Barde YA. 1996. Physiology of neurotrophins. Annu Rev Neurosci 1996;19:289-317. https://doi.org/10.1146/annurev.ne.19.030196.001445
  • Nieto Gonzalez JL, Jensen K. BDNF depresses excitability of parvalbumin -positive interneurons through an M-like current in rat dentate gyrus. PLoS One 2013;8:e67318. https://doi.org/10.1371/journal.pone.0067318
  • Benes FM, Berretta S. GABAergic interneurons: implications for understanding schizophrenia and bipolar disorder. Neuropsychopharmacol 2001;25:1-27. https://doi.org/10.1016/S0893-133X(01)00225-1
  • Bravo R, Parra V, Gatica D, et al. Endoplasmic reticulum and the unfolded protein response: dynamics and metabolic integration. Int Rev Cell Mol Biol 2013;301:215-290. https://doi.org/10.1016/B978-0-12-407704-1.00005-1
  • Wärri A, Cook KL, Hu R, et al. Autophagy and unfolded protein response (UPR) regulate mammary gland involution by restraining apoptosis-driven irreversible changes. Cell Death Discov 2018;15;4:40. https://doi.org/10.1038/s41420-018-0105-y
  • Zhang K, Kaufman RJ. The unfolded protein response: a stress signaling pathway critical for health and disease. Neurology 2006;24:102-109. https://doi.org/10.1212/01.wnl.0000192306.98198.ec
  • Groenendyk J, Peng Z, Dudek E, et al. Interplay between the oxidoreductase PDIA6 and microRNA-322 controls the response to disrupted endoplasmic reticulum calcium homeostasis. Sci Signal 2014;7:54. https://doi.org/10.1126/scisignal.2004983
  • Yang Y, Ma F, Liu Z, et al. The ER-localized Ca2+-binding protein calreticulin couples ER stress to autophagy by associating with microtubule-associated protein 1A/1B light chain 3. J Biol Chem 2019;294:772-782. https://doi.org/10.1074/jbc.RA118.005166
  • Xiao F, Zhang P, Chen AH, et al. Hydrogen sulfide inhibits MPP+-induced aldehyde stress and endoplasmic reticulum stress in PC12 cells: involving upregulation of BDNF. Exp Cell Res 2016;348:106-114. https://doi.org/10.1016/j.yexcr.2016.09.006
  • Shimoke K, Utsumi T, Kishi S, et al. Prevention of endoplasmic reticulum stress-induced cell death by brain-derived neurotrophic factor in cultured cerebral cortical neurons. Brain Res 2004;1028:105-111. https://doi.org/10.1016/j.brainres.2004.09.005
  • Chen G, Fan Z, Wang X, et al. Brain-derived neurotrophic factor suppresses tunicamycin-induced upregulation of CHOP in neurons. J Neurosci Res 2007;85:1674-1684. https://doi.org/10.1002/jnr.21292
  • Korte M, Carroll P, Wolf E, Brem G, Thoenen H, Bonhoeffer T. Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc Natl Acad Sci USA 1995;92:8856-8860. https://doi.org/10.1073/pnas.92.19.8856
  • Abidin I, Yildirim M, Aydin-Abidin S, et al. Penicillin-induced epileptiform activity and EEG spectrum analysis of BDNF heterozygous mice: an in vivo electrophysiological study. Brain Res Bull 2011;86:159-164. https://doi.org/10.1016/j.brainresbull.2011.06.015
  • De Miguel C, Hamrick WC, Hobbs JL, Pollock DM, Carmines PK, Pollock JS. Endothelin receptor-specific control of endoplasmic reticulum stress and apoptosis in the kidney. Sci Rep 2017;7:43152. https://doi.org/10.1038/srep43152
  • Hodeify R, Megyesi J, Tarcsafalvi A, Mustafa HI, Lar Seng NS, Price PM. Gender differences control the susceptibility to ER stress-induced acute kidney injury. Am J Physiol Renal Physiol 2013;304:875-882. https://doi.org/10.1152/ajprenal.00590.2012
  • Jiao G, Hao L, Wang M, et al. Upregulation of endoplasmic reticulum stress is associated with diaphragm contractile dysfunction in a rat model of sepsis. Mol Med Rep 2017;15:366-374. https://doi.org/10.3892/mmr.2016.6014
  • Huang Y, Leng TD, Inoue K, et al. TRPM7 channels play a role in high glucose-induced endoplasmic reticulum stress and neuronal cell apoptosis. J Biol Chem 2018;293:14393-14406. https://doi.org/10.1074/jbc.RA117.001032
  • Abidin I, Köhler T, Weiler E, Zoidl G, Eysel UT, Lessmann V, et al. Reduced presynaptic efficiency of excitatory synaptic transmission impairs LTP in the visual cortex of BDNF-heterozygous mice. Eur J Neurosci 2006;24:3519-3531. https://doi.org/10.1111/j.1460-9568.2006.05242.x
  • Lyons WE, Mamounas LA, Ricaurte GA, et al. Brain-derived neurotrophic factor-deficient mice develop aggressiveness and hyperphagia in conjunction with brain serotonergic abnormalities. Proc Natl Acad Sci USA 1999;9:15239-15244. https://doi.org/10.1073/pnas.96.26.15239
  • Duan W, Guo Z, Jiang H, Ware M, Mattson MP. Reversal of behavioral and metabolic abnormalities, and insulin resistance syndrome, by dietary restriction in mice deficient in brain-derived neurotrophic factor. Endocrinology 2003;144:2446-2453. https://doi.org/10.1210/en.2002-0113
  • Steele KE, Seth P, Lebaron KM, et al. Tunicamycin enhances neuroinvasion and encephalitis in mice infected with Venezuelan equine encephalitis virus. Vet Pathol 2006;43:904-913. https://doi.org/10.1354/vp.43-6-904
  • Xu C, Bailly-Maitre B, Reed JC. Endoplasmic reticulum stress: cell life and death decisions. J Clin Invest 2005;115:2656-2664. https://doi.org/10.1172/JCI26373
  • Cao SS, Kaufman RJ. Unfolded protein response. Curr Biol 2012;22:622-626. https://doi.org/10.1016/j.cub.2012.07.004
  • Breckenridge DG, Germain M, Mathai JP, Nguyen M, Shore GC. Regulation of apoptosis by endoplasmic reticulum pathways. Oncogene 2003;22:8608-8618. https://doi.org/10.1038/sj.onc.1207108
  • Oyadomari S, Mori M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 2004;11:381-389. https://doi.org/10.1038/sj.cdd.4401373
  • Wei HJ, Xu JH, Li MH,et al. Hydrogen sulfide inhibits homocysteine-induced endoplasmic reticulum stress and neuronal apoptosis in rat hippocampus via upregulation of the BDNF-TrkB pathway. Acta Pharmacol Sin 2014;35:707-715. https://doi.org/10.1038/aps.2013.197
  • Fish KN, Rocco BR, Lewis DA. Laminar distribution of subsets of GABAergic axon terminals in human prefrontal cortex. Front Neuroanat 2018;16;12:9. https://doi.org/10.3389/fnana.2018.00009
  • Grosse G, Djalali S, Deng DR, Höltje M, Hinz B, Schwartzkopff K, et al. Area-specific effects of brain-derived neurotrophic factor (BDNF) genetic ablation on various neuronal subtypes of the mouse brain. Dev Brain Res 2005;156:111-126. https://doi.org/10.1016/j.devbrainres.2004.12.012
  • Turovsky EA, Zinchenko VP, Gaidin SG, Turovskaya MV. Calcium-binding proteins protect GABAergic neurons of the hippocampus from hypoxia and ischemia in vitro. Biochem Moscow Suppl 2018;12:74-84. https://doi.org/10.1134/S1990747818010105
  • Elliott JL, Snider WD. Parvalbumin is a marker of ALS-resistant motor neurons. Neuroreport 1995;6:449-452. https://doi.org/:10.1097/00001756-199502000-00011
  • D’Orlando C, Fellay B, Schwaller B, Salicio V, Bloc A, Gotzos V, et al. Calretinin and calbindin D-28k delay the onset of cell death after excitotoxic stimulation in transfected P19 cells. Brain Res 2001;909:145-158. https://doi.org/10.1016/S0006-8993(01)02671-3
  • Lewis DA, Hashimoto T, Volk DW. Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 2005;6:312-324. https://doi.org/10.1038/nrn1648
  • Cramer NP, Best TK, Stoffel M, Siarey RJ, Galdzicki Z. GABAB-GIRK2- mediated signaling in Down syndrome. Adv Pharmacol 2010;58:397-426. https://doi.org/10.1016/S1054-3589(10)58015-3
  • Rossignol E. Genetics and function of neocortical GABAergic interneurons in neurodevelopmental disorders. Neural Plast 2011;2011:649325. https://doi.org/10.1155/2011/649325
  • Lee B, Zhang Y, Kim Y, Kim S, Lee Y, Han K. Age-dependent decrease of GAD65/67 mRNAs but normal densities of GABAergic interneurons in the brain regions of Shank3-overexpressing manic mouse model. Neurosci Lett 2017;649:48-54. https://doi.org/10.1016/j.neulet.2017.04.016
  • Gogolla N, Leblanc JJ, Quast KB, Südhof TC, Fagiolini M, Hensch TK. Common circuit defect of excitatory-inhibitory balance in mouse models of autism. J Neurodev Disord 2009;1:172-181. https://doi.org/10.1007/s11689-009-9023-x

Ayrıntılar

Birincil Dil İngilizce
Konular Fizyoloji
Yayınlanma Tarihi Ekim 2021
Bölüm Araştırma Makalesi
Yazarlar

Gulay HACIOĞLU (Sorumlu Yazar)
Giresun Üniversitesi Tıp Fakültesi Fizyoloji AD.
0000-0002-8528-2371
Türkiye


Selma CIRRIK
ORDU ÜNİVERSİTESİ, TIP FAKÜLTESİ
0000-0001-8474-0185
Türkiye


Hakan YÜZÜAK
GİRESUN ÜNİVERSİTESİ, TIP FAKÜLTESİ
0000-0002-9783-0451
Türkiye


Selcen AYDIN Bu kişi benim
KARADENİZ TEKNİK ÜNİVERSİTESİ, TIP FAKÜLTESİ
0000-0002-5843-5539
Türkiye


İsmail ABİDİN
KARADENİZ TEKNİK ÜNİVERSİTESİ, TIP FAKÜLTESİ
0000-0003-2510-9718
Türkiye

Destekleyen Kurum Giresun Üniversitesi
Proje Numarası SAĞ-BAP-A-230218-85
Yayımlanma Tarihi 1 Ekim 2021
Yayınlandığı Sayı Yıl 2021, Cilt 14, Sayı 4

Kaynak Göster

Bibtex @araştırma makalesi { patd834832, journal = {Pamukkale Tıp Dergisi}, issn = {}, eissn = {1308-0865}, address = {Pamukkale Üniversitesi Tıp Fakültesi Eğitim Blokları Kınıklı kampüsü 20070 Kınıklı, Denizli}, publisher = {Pamukkale Üniversitesi}, year = {2021}, volume = {14}, pages = {792 - 802}, doi = {10.31362/patd.834832}, title = {Effects of BDNF deficiency and endoplasmic reticulum stress on the GABAergic system}, key = {cite}, author = {Hacıoğlu, Gulay and Cırrık, Selma and Yüzüak, Hakan and Aydın, Selcen and Abidin, İsmail} }
APA Hacıoğlu, G. , Cırrık, S. , Yüzüak, H. , Aydın, S. & Abidin, İ. (2021). Effects of BDNF deficiency and endoplasmic reticulum stress on the GABAergic system . Pamukkale Tıp Dergisi , 14 (4) , 792-802 . DOI: 10.31362/patd.834832
MLA Hacıoğlu, G. , Cırrık, S. , Yüzüak, H. , Aydın, S. , Abidin, İ. "Effects of BDNF deficiency and endoplasmic reticulum stress on the GABAergic system" . Pamukkale Tıp Dergisi 14 (2021 ): 792-802 <https://dergipark.org.tr/tr/pub/patd/issue/63191/834832>
Chicago Hacıoğlu, G. , Cırrık, S. , Yüzüak, H. , Aydın, S. , Abidin, İ. "Effects of BDNF deficiency and endoplasmic reticulum stress on the GABAergic system". Pamukkale Tıp Dergisi 14 (2021 ): 792-802
RIS TY - JOUR T1 - Effects of BDNF deficiency and endoplasmic reticulum stress on the GABAergic system AU - Gulay Hacıoğlu , Selma Cırrık , Hakan Yüzüak , Selcen Aydın , İsmail Abidin Y1 - 2021 PY - 2021 N1 - doi: 10.31362/patd.834832 DO - 10.31362/patd.834832 T2 - Pamukkale Tıp Dergisi JF - Journal JO - JOR SP - 792 EP - 802 VL - 14 IS - 4 SN - -1308-0865 M3 - doi: 10.31362/patd.834832 UR - https://doi.org/10.31362/patd.834832 Y2 - 2021 ER -
EndNote %0 Pamukkale Tıp Dergisi Effects of BDNF deficiency and endoplasmic reticulum stress on the GABAergic system %A Gulay Hacıoğlu , Selma Cırrık , Hakan Yüzüak , Selcen Aydın , İsmail Abidin %T Effects of BDNF deficiency and endoplasmic reticulum stress on the GABAergic system %D 2021 %J Pamukkale Tıp Dergisi %P -1308-0865 %V 14 %N 4 %R doi: 10.31362/patd.834832 %U 10.31362/patd.834832
ISNAD Hacıoğlu, Gulay , Cırrık, Selma , Yüzüak, Hakan , Aydın, Selcen , Abidin, İsmail . "Effects of BDNF deficiency and endoplasmic reticulum stress on the GABAergic system". Pamukkale Tıp Dergisi 14 / 4 (Ekim 2021): 792-802 . https://doi.org/10.31362/patd.834832
AMA Hacıoğlu G. , Cırrık S. , Yüzüak H. , Aydın S. , Abidin İ. Effects of BDNF deficiency and endoplasmic reticulum stress on the GABAergic system. Pam Tıp Derg. 2021; 14(4): 792-802.
Vancouver Hacıoğlu G. , Cırrık S. , Yüzüak H. , Aydın S. , Abidin İ. Effects of BDNF deficiency and endoplasmic reticulum stress on the GABAergic system. Pamukkale Tıp Dergisi. 2021; 14(4): 792-802.
IEEE G. Hacıoğlu , S. Cırrık , H. Yüzüak , S. Aydın ve İ. Abidin , "Effects of BDNF deficiency and endoplasmic reticulum stress on the GABAergic system", Pamukkale Tıp Dergisi, c. 14, sayı. 4, ss. 792-802, Eki. 2021, doi:10.31362/patd.834832