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Glutamat Eksitotoksisitesi Oluşturulan Primer Kortikal Nöron Kültürlerinde Parietinin Nöroprotektif Etkisinin İncelenmesi

Yıl 2018, Cilt: 13 Sayı: 2, 165 - 173, 25.10.2018
https://doi.org/10.17094/ataunivbd.363858

Öz

Glutamat merkezi sinir sisteminin en önemli nörotransmitter maddesidir. Aşırı glutamat salınımı, glutamat reseptörlerinin

uzun süreli aktivasyonuna neden olarak eksitotoksisteye yol açar. Parietin, Rheum ribes L.’den izole edilen çeşitli farmakolojik

özelliklere sahip bir antrakinondur. Bu çalışmada glutamat eksitotoksisitesine maruz bırakılan primer kortikal nöron

kültürlerinde parietinin nöroprotektif etkisinin araştırılması amaçlanmıştır. Primer kortikal nöronlar, yeni doğan Sprague

Dawley cinsi sıçanlardan elde edildi. Glutamat eksitotoksisitesini stimüle etmek için, kültür medyumuna 10-5 M

konsantrasyonda glutamat uygulandı. Daha sonra hücrelere 2.5-500 μM konsantrasyonda parietin uygulanarak 24 saat

inkübasyona bırakıldı. Hücre canlılık oranı MTT yöntemi ile belirlendi. Aynı zamanda hücrelerde oluşan reaktif oksijen türleri

total antioksidan seviyesi (TAS)- total oksidan seviyesi (TOS) yöntemi ile değerlendirildi. MTT analiz sonuçlarına göre 10 μM

parietinin glutamat eksitotoksisitesine karşı nöronlarda anlamlı düzeyde koruyucu etkiye sahip olduğu tespit edildi. TAS-TOS

analiz sonuçlarına göre 10 μM parietinin hücrelerde antioksidan seviyesini anlamlı ölçüde artırırken, parietinin yüksek

konsantrasyonlarının hücrelerdeki oksidan seviyesini anlamlı ölçüde arttırdığı gözlendi. Bu çalışma sonucuna göre parietinin

primer kortikal nöron hücrelerinde glutamat eksitotoksisitesine karşı koruyucu etkiye sahip olduğu ve glutamat

eksitotoksisitesine karşı teropatik bir ajan olarak kullanılabileceği düşünülmektedir.

Kaynakça

  • 1. Albright TD., Jessell TM., Kandel ER., Posner MI., 2000. Neural science: a century of progress and the mysteries that remain. Cell, 100, 1-55. 2. Elmann A., Telerman A., Ofir R., Kashman Y., 2017. Glutamate Toxicity to Differentiated Neuroblastoma N2a Cells Is Prevented by the Sesquiterpene Lactone Achillolide A and the Flavonoid 3, 5, 4′-Trihydroxy-6, 7, 3′-Trimethoxyflavone from Achillea fragrantissima. Journal of Molecular Neuroscience, 62, 99-105. 3. Wen SY., Li AM., Mi KQ., Wang RZ., Li H., Liu HX., Xing Y., 2017. In vitro neuroprotective effects of ciliary neurotrophic factor on dorsal root ganglion neurons with glutamate-induced neurotoxicity. Neural Regeneration Research, 12, 1716-1721. 4. Hacimuftuoglu A., Tatar A., Cetin D., Taspinar N., Saruhan F., Okkay U., Turkez H., Unal D., Stephens RL., Suleyman H., 2016. Astrocyte/neuron ratio and its importance on glutamate toxicity: an in vitro voltammetric study. Cytotechnology, 68, 1425-1433 5. Kanamori K., 2016. In vivo N-15 MRS study of glutamate metabolism in the rat brain. Analytical biochemistry, 529, 179-192 6. Zhao J., Verwer R., van Wamelen D., Qi XR., Gao SF., Lucassen P., Swaab D., 2016. Prefrontal changes in the glutamate-glutamine cycle and neuronal/glial glutamate transporters in depression with and without suicide. Journal of psychiatric research, 82, 8-15. 7. Kostic M., Zivkovic N., Cvetanovic A., Stojanovic I., Colic M., 2017. IL-17 signalling in astrocytes promotes glutamate excitotoxicity: Indications for the link between inflammatory and neurodegenerative events in multiple sclerosis. Multiple sclerosis and related disorders, 11, 12-17. 8. Song JH., Kang K., Choi Y., 2017. Protective effect of casuarinin against glutamate-induced apoptosis in HT22 cells through inhibition of oxidative stress-mediated MAPK phosphorylation. Bioorganic & Medicinal Chemistry Letters, 27, 5109-5113. 9. ZhaoH., Ji ZH., Liu C., Yu XY., 2015. Neuroprotective mechanisms of 9-hydroxy epinootkatol against glutamate-induced neuronal apoptosis in primary neuron culture. Journal of Molecular Neuroscience, 56, 808-814. 10. Jia N., Sun Q., Su Q., Chen G., 2016. SIRT1-mediated deacetylation of PGC1α attributes to the protection of curcumin against glutamate excitotoxicity in cortical neurons. Biochemical and biophysical research communications, 478, 1376-1381. 11. Floyd RA., Hensley K., 2002. Oxidative stress in brain aging: implications for therapeutics of neurodegenerative diseases. Neurobiology of aging, 23, 795-807. 12. Kim HT., Prochiantz A., Kim JW., 2016. Donating Otx2 to support neighboring neuron survival. BMB reports, 49, 69-70. 13. Mehta A., Prabhakar M., Kumar P., Deshmukh R., Sharma P., 2013. Excitotoxicity: bridge to various triggers in neurodegenerative disorders. European journal of pharmacology, 698, 6-18. 14. Verrier J., Kochanek P., Jackson T., 2013. Anthraquinone-2-sulfonic acid (AQ2S) is a novel neurotherapeutic agent. Cell death & Disease, 4, 451-459. 15. Wei G., Wu Y., Gao Q., Zhou C., Wang K., Shen C., Wang G., Wang K., Sun X., Li X., 2017 Effect of Emodin on Preventing Postoperative Intra-Abdominal Adhesion Formation. Oxidative medicine and cellular longevity, 2017. 16. Turkmen O., Crka M., Suat E., 2005. Initial evaluation of a new edible wild rhubarb species (Rheum ribes L.) with a modified weighted scaling index method. Pakistan Journal of Biological Sciences, 8, 763-765. 17. Hong JY., Chung HJ., Bae SY., Trung TN., Bae K., Lee SK., 2014. Induction of cell cycle arrest and apoptosis by physcion, an anthraquinone isolated from rhubarb (rhizomes of Rheum tanguticum), in MDA-MB-231 human breast cancer cells. Journal of cancer prevention, 19, 273. 18. Pang, MJ., Yang Z., Zhang Xl., Liu ZF., Fan J., Zhang HY., 2016. Physcion, a naturally occurring anthraquinone derivative, induces apoptosis and autophagy in human nasopharyngeal carcinoma. Acta Pharmacologica Sinica, 37, 1623–1640. 19. Li W., Li F., Zhu Y., Song D., 2017. Physcion 8-O-β-glucopyranosideregulates cell cycle, apoptosis, and invasion in glioblastoma cells through modulating Skp2. Biomedicine & Pharmacotherapy, 95, 1129-1138. 20. Wang Q., Jiang Y., Guo R., Lv R., Liu T., Wei H., Ming H., Tian X., 2017. Physcion 8-O-β-glucopyranoside suppresses tumor growth of Hepatocellular carcinoma by downregulating PIM1. Biomedicine & Pharmacotherapy, 92, 451-458. 21. Michaels R., Rothman SM., 1990. Glutamate neurotoxicity in vitro: antagonist pharmacology and intracellular calcium concentrations. Journal of Neuroscience, 10, 283-292. 22. Sasaki-Hamada S., Suzuki A., Sanai E., Matsumoto K., Oka JI., 2017. Neuroprotection by chotosan, a Kampo formula, against glutamate excitotoxicity involves the inhibition of GluN2B-, but not GluN2A-containing NMDA receptor-mediated responses in primary cultured cortical neurons. Journal of Pharmacological Sciences. 23. Coyle JT., Puttfarcken P., 1993. Oxidative stress, glutamate, and neurodegenerative disorders. Science-New York Then Washington, 262, 689-699. 24. Depp C., Bas-Orth C., Schroeder L., Hellwig A., Bading H., 2017. Synaptic activity protects neurons against calcium-mediated oxidation and contraction of mitochondria during excitotoxicity. Antioxidants & Redox Signaling, 28,530-537 25. Lipton SA., Rosenberg PA., 1994. Excitatory amino acids as a final common pathway for neurologic disorders. New England Journal of Medicine, 330, 613-622. 26. Kortagere S., Mortensen OV., Xia J., Lester W., Fang Y., Srikanth YV., Salvino JM., Fontana ACK., 2017. Identification of novel allosteric modulators of glutamate transporter EAAT2. ACS Chemical Neuroscience. 27. Gao F., Liu W., Guo Q., Bai Y., Yang H., Chen H., 2017. Physcion blocks cell cycle and induces apoptosis in human B cell precursor acute lymphoblastic leukemia cells by downregulating HOXA5. Biomedicine & Pharmacotherapy, 94, 850-857. 28. Sylvester PW., 2011. Optimization of the tetrazolium dye (MTT) colorimetric assay for cellular growth and viability. Drug Design and Discovery: Methods and Protocols, 32, 157-168. 29. Wang Q., Wang Y., Xing Y., Yan Y., Guo P., Zhuang J., Qin F., Zhang J., 2016. Physcion 8-O-β-glucopyranoside induces apoptosis, suppresses invasion and inhibits epithelial to mesenchymal transition of hepatocellular carcinoma HepG2 cells. Biomedicine & Pharmacotherapy, 83, 372-380. 30. Büyükokuroğlu ME., Gepdiremen A., Hacimüftüoğlu A., Oktay M., 2003. The effects of aqueous extract of Lavandula angustifolia flowers in glutamate-induced neurotoxicity of cerebellar granular cell culture of rat pups. Journal of Ethnopharmacology, 84, 91-94. 31. Ghezzi F., Monni L., Corsini S., Rauti R., Nistri A., 2017. Propofol Protects Rat Hypoglossal Motoneurons in an In Vitro Model of Excitotoxicity by Boosting GABAergic Inhibition and Reducing Oxidative Stress. Neuroscience, 367, 15-33. 32. Hara Y., McKeehan N., Dacks P., Fillit H., 2017. Evaluation of the Neuroprotective Potential of N-Acetylcysteine for Prevention and Treatment of Cognitive Aging and Dementia. Evaluation, 4. 33. Brkanac SR., Geric M., Gajski G., Vujcic V., Garaj-Vrhovac V., Kremer D., Domijan AM., 2015. Toxicity and antioxidant capacity of Frangula alnus Mill. bark and its active component emodin. Regulatory Toxicology and Pharmacology, 73, 923-929. 34. Sun YN., Li W., Lee SH., Jang HD., Ma JY., Kim YH., 2017. Antioxidant and anti-osteoporotic effects of anthraquinones and related constituents from the aqueous dissolved Aloe exudates. Natural Product Research, 23,1-4. 35. Gu JW., Hasuo H., Takeya M., Akasu T., 2005. Effects of emodin on synaptic transmission in rat hippocampal CA1 pyramidal neurons in vitro. Neuropharmacology, 49, 103-111.

Investigation of Protective Effect of Parietin Against Glutamate Excitotoxicity in Primary Cortical Neuron Culture

Yıl 2018, Cilt: 13 Sayı: 2, 165 - 173, 25.10.2018
https://doi.org/10.17094/ataunivbd.363858

Öz

Glutamate is the most important neurotransmitter in the central nervous system. Excitotoxicity is induced by

excessive release of glutamate followed by overstimulation of glutamate receptor. Parietin is an anthraquinone from Rheum

ribes L. and has been reported to have a variety of pharmacological properties. The present study investigated the

neuroprotective effects of parietin in primary cortical neuron cultures against glutamate excitotoxicity. Primary rat cortical

neuronal cultures were obtained from new born Sprague Dawley rats. Cultures were subject to 10-5 M glutamate to stimulate

glutamate excitotoxicity. After that, cells were treated with 2.5-500 μM concentrations of parietin during 24 h in dose

dependent manner. Cell viability was determined using MTT assay. Reactive oxygen species generation was assessed using

the total antioxidant status (TAS)-total antioxidant status (TOS) assays. The results of MTT analysis showed that 10 μM parietin

effectively protected neuron from glutamate toxicity. According to the results of TAS-TOS analysis, it showed that 10 μM

parietin significantly increased the antioxidant level in the cells, whereas high concentrations of parietin significantly

increased the oxidant level in the cells. The results of this study suggest that parietin had neuroprotective effect against

glutamate excitotoxicity in primary rat cortical neuron cultures and it may be conceive that parietin can be used as a

therapeutic agent for glutamate excitotoxicity.

Kaynakça

  • 1. Albright TD., Jessell TM., Kandel ER., Posner MI., 2000. Neural science: a century of progress and the mysteries that remain. Cell, 100, 1-55. 2. Elmann A., Telerman A., Ofir R., Kashman Y., 2017. Glutamate Toxicity to Differentiated Neuroblastoma N2a Cells Is Prevented by the Sesquiterpene Lactone Achillolide A and the Flavonoid 3, 5, 4′-Trihydroxy-6, 7, 3′-Trimethoxyflavone from Achillea fragrantissima. Journal of Molecular Neuroscience, 62, 99-105. 3. Wen SY., Li AM., Mi KQ., Wang RZ., Li H., Liu HX., Xing Y., 2017. In vitro neuroprotective effects of ciliary neurotrophic factor on dorsal root ganglion neurons with glutamate-induced neurotoxicity. Neural Regeneration Research, 12, 1716-1721. 4. Hacimuftuoglu A., Tatar A., Cetin D., Taspinar N., Saruhan F., Okkay U., Turkez H., Unal D., Stephens RL., Suleyman H., 2016. Astrocyte/neuron ratio and its importance on glutamate toxicity: an in vitro voltammetric study. Cytotechnology, 68, 1425-1433 5. Kanamori K., 2016. In vivo N-15 MRS study of glutamate metabolism in the rat brain. Analytical biochemistry, 529, 179-192 6. Zhao J., Verwer R., van Wamelen D., Qi XR., Gao SF., Lucassen P., Swaab D., 2016. Prefrontal changes in the glutamate-glutamine cycle and neuronal/glial glutamate transporters in depression with and without suicide. Journal of psychiatric research, 82, 8-15. 7. Kostic M., Zivkovic N., Cvetanovic A., Stojanovic I., Colic M., 2017. IL-17 signalling in astrocytes promotes glutamate excitotoxicity: Indications for the link between inflammatory and neurodegenerative events in multiple sclerosis. Multiple sclerosis and related disorders, 11, 12-17. 8. Song JH., Kang K., Choi Y., 2017. Protective effect of casuarinin against glutamate-induced apoptosis in HT22 cells through inhibition of oxidative stress-mediated MAPK phosphorylation. Bioorganic & Medicinal Chemistry Letters, 27, 5109-5113. 9. ZhaoH., Ji ZH., Liu C., Yu XY., 2015. Neuroprotective mechanisms of 9-hydroxy epinootkatol against glutamate-induced neuronal apoptosis in primary neuron culture. Journal of Molecular Neuroscience, 56, 808-814. 10. Jia N., Sun Q., Su Q., Chen G., 2016. SIRT1-mediated deacetylation of PGC1α attributes to the protection of curcumin against glutamate excitotoxicity in cortical neurons. Biochemical and biophysical research communications, 478, 1376-1381. 11. Floyd RA., Hensley K., 2002. Oxidative stress in brain aging: implications for therapeutics of neurodegenerative diseases. Neurobiology of aging, 23, 795-807. 12. Kim HT., Prochiantz A., Kim JW., 2016. Donating Otx2 to support neighboring neuron survival. BMB reports, 49, 69-70. 13. Mehta A., Prabhakar M., Kumar P., Deshmukh R., Sharma P., 2013. Excitotoxicity: bridge to various triggers in neurodegenerative disorders. European journal of pharmacology, 698, 6-18. 14. Verrier J., Kochanek P., Jackson T., 2013. Anthraquinone-2-sulfonic acid (AQ2S) is a novel neurotherapeutic agent. Cell death & Disease, 4, 451-459. 15. Wei G., Wu Y., Gao Q., Zhou C., Wang K., Shen C., Wang G., Wang K., Sun X., Li X., 2017 Effect of Emodin on Preventing Postoperative Intra-Abdominal Adhesion Formation. Oxidative medicine and cellular longevity, 2017. 16. Turkmen O., Crka M., Suat E., 2005. Initial evaluation of a new edible wild rhubarb species (Rheum ribes L.) with a modified weighted scaling index method. Pakistan Journal of Biological Sciences, 8, 763-765. 17. Hong JY., Chung HJ., Bae SY., Trung TN., Bae K., Lee SK., 2014. Induction of cell cycle arrest and apoptosis by physcion, an anthraquinone isolated from rhubarb (rhizomes of Rheum tanguticum), in MDA-MB-231 human breast cancer cells. Journal of cancer prevention, 19, 273. 18. Pang, MJ., Yang Z., Zhang Xl., Liu ZF., Fan J., Zhang HY., 2016. Physcion, a naturally occurring anthraquinone derivative, induces apoptosis and autophagy in human nasopharyngeal carcinoma. Acta Pharmacologica Sinica, 37, 1623–1640. 19. Li W., Li F., Zhu Y., Song D., 2017. Physcion 8-O-β-glucopyranosideregulates cell cycle, apoptosis, and invasion in glioblastoma cells through modulating Skp2. Biomedicine & Pharmacotherapy, 95, 1129-1138. 20. Wang Q., Jiang Y., Guo R., Lv R., Liu T., Wei H., Ming H., Tian X., 2017. Physcion 8-O-β-glucopyranoside suppresses tumor growth of Hepatocellular carcinoma by downregulating PIM1. Biomedicine & Pharmacotherapy, 92, 451-458. 21. Michaels R., Rothman SM., 1990. Glutamate neurotoxicity in vitro: antagonist pharmacology and intracellular calcium concentrations. Journal of Neuroscience, 10, 283-292. 22. Sasaki-Hamada S., Suzuki A., Sanai E., Matsumoto K., Oka JI., 2017. Neuroprotection by chotosan, a Kampo formula, against glutamate excitotoxicity involves the inhibition of GluN2B-, but not GluN2A-containing NMDA receptor-mediated responses in primary cultured cortical neurons. Journal of Pharmacological Sciences. 23. Coyle JT., Puttfarcken P., 1993. Oxidative stress, glutamate, and neurodegenerative disorders. Science-New York Then Washington, 262, 689-699. 24. Depp C., Bas-Orth C., Schroeder L., Hellwig A., Bading H., 2017. Synaptic activity protects neurons against calcium-mediated oxidation and contraction of mitochondria during excitotoxicity. Antioxidants & Redox Signaling, 28,530-537 25. Lipton SA., Rosenberg PA., 1994. Excitatory amino acids as a final common pathway for neurologic disorders. New England Journal of Medicine, 330, 613-622. 26. Kortagere S., Mortensen OV., Xia J., Lester W., Fang Y., Srikanth YV., Salvino JM., Fontana ACK., 2017. Identification of novel allosteric modulators of glutamate transporter EAAT2. ACS Chemical Neuroscience. 27. Gao F., Liu W., Guo Q., Bai Y., Yang H., Chen H., 2017. Physcion blocks cell cycle and induces apoptosis in human B cell precursor acute lymphoblastic leukemia cells by downregulating HOXA5. Biomedicine & Pharmacotherapy, 94, 850-857. 28. Sylvester PW., 2011. Optimization of the tetrazolium dye (MTT) colorimetric assay for cellular growth and viability. Drug Design and Discovery: Methods and Protocols, 32, 157-168. 29. Wang Q., Wang Y., Xing Y., Yan Y., Guo P., Zhuang J., Qin F., Zhang J., 2016. Physcion 8-O-β-glucopyranoside induces apoptosis, suppresses invasion and inhibits epithelial to mesenchymal transition of hepatocellular carcinoma HepG2 cells. Biomedicine & Pharmacotherapy, 83, 372-380. 30. Büyükokuroğlu ME., Gepdiremen A., Hacimüftüoğlu A., Oktay M., 2003. The effects of aqueous extract of Lavandula angustifolia flowers in glutamate-induced neurotoxicity of cerebellar granular cell culture of rat pups. Journal of Ethnopharmacology, 84, 91-94. 31. Ghezzi F., Monni L., Corsini S., Rauti R., Nistri A., 2017. Propofol Protects Rat Hypoglossal Motoneurons in an In Vitro Model of Excitotoxicity by Boosting GABAergic Inhibition and Reducing Oxidative Stress. Neuroscience, 367, 15-33. 32. Hara Y., McKeehan N., Dacks P., Fillit H., 2017. Evaluation of the Neuroprotective Potential of N-Acetylcysteine for Prevention and Treatment of Cognitive Aging and Dementia. Evaluation, 4. 33. Brkanac SR., Geric M., Gajski G., Vujcic V., Garaj-Vrhovac V., Kremer D., Domijan AM., 2015. Toxicity and antioxidant capacity of Frangula alnus Mill. bark and its active component emodin. Regulatory Toxicology and Pharmacology, 73, 923-929. 34. Sun YN., Li W., Lee SH., Jang HD., Ma JY., Kim YH., 2017. Antioxidant and anti-osteoporotic effects of anthraquinones and related constituents from the aqueous dissolved Aloe exudates. Natural Product Research, 23,1-4. 35. Gu JW., Hasuo H., Takeya M., Akasu T., 2005. Effects of emodin on synaptic transmission in rat hippocampal CA1 pyramidal neurons in vitro. Neuropharmacology, 49, 103-111.
Toplam 1 adet kaynakça vardır.

Ayrıntılar

Birincil Dil Türkçe
Konular Sağlık Kurumları Yönetimi
Bölüm Araştırma Makaleleri
Yazarlar

Gülşah Gündoğdu

Ali Taghizadehghalehjoughi Bu kişi benim

Betül Çiçek Bu kişi benim

Onur Şenol

Kemal Alp Nalcı Bu kişi benim

Alper Kürşat Demirkaya

Ahmet Hacımüftüoğlu Bu kişi benim

Yayımlanma Tarihi 25 Ekim 2018
Yayımlandığı Sayı Yıl 2018 Cilt: 13 Sayı: 2

Kaynak Göster

APA Gündoğdu, G., Taghizadehghalehjoughi, A., Çiçek, B., Şenol, O., vd. (2018). Glutamat Eksitotoksisitesi Oluşturulan Primer Kortikal Nöron Kültürlerinde Parietinin Nöroprotektif Etkisinin İncelenmesi. Atatürk Üniversitesi Veteriner Bilimleri Dergisi, 13(2), 165-173. https://doi.org/10.17094/ataunivbd.363858
AMA Gündoğdu G, Taghizadehghalehjoughi A, Çiçek B, Şenol O, Nalcı KA, Demirkaya AK, Hacımüftüoğlu A. Glutamat Eksitotoksisitesi Oluşturulan Primer Kortikal Nöron Kültürlerinde Parietinin Nöroprotektif Etkisinin İncelenmesi. Atatürk Üniversitesi Veteriner Bilimleri Dergisi. Ekim 2018;13(2):165-173. doi:10.17094/ataunivbd.363858
Chicago Gündoğdu, Gülşah, Ali Taghizadehghalehjoughi, Betül Çiçek, Onur Şenol, Kemal Alp Nalcı, Alper Kürşat Demirkaya, ve Ahmet Hacımüftüoğlu. “Glutamat Eksitotoksisitesi Oluşturulan Primer Kortikal Nöron Kültürlerinde Parietinin Nöroprotektif Etkisinin İncelenmesi”. Atatürk Üniversitesi Veteriner Bilimleri Dergisi 13, sy. 2 (Ekim 2018): 165-73. https://doi.org/10.17094/ataunivbd.363858.
EndNote Gündoğdu G, Taghizadehghalehjoughi A, Çiçek B, Şenol O, Nalcı KA, Demirkaya AK, Hacımüftüoğlu A (01 Ekim 2018) Glutamat Eksitotoksisitesi Oluşturulan Primer Kortikal Nöron Kültürlerinde Parietinin Nöroprotektif Etkisinin İncelenmesi. Atatürk Üniversitesi Veteriner Bilimleri Dergisi 13 2 165–173.
IEEE G. Gündoğdu, “Glutamat Eksitotoksisitesi Oluşturulan Primer Kortikal Nöron Kültürlerinde Parietinin Nöroprotektif Etkisinin İncelenmesi”, Atatürk Üniversitesi Veteriner Bilimleri Dergisi, c. 13, sy. 2, ss. 165–173, 2018, doi: 10.17094/ataunivbd.363858.
ISNAD Gündoğdu, Gülşah vd. “Glutamat Eksitotoksisitesi Oluşturulan Primer Kortikal Nöron Kültürlerinde Parietinin Nöroprotektif Etkisinin İncelenmesi”. Atatürk Üniversitesi Veteriner Bilimleri Dergisi 13/2 (Ekim 2018), 165-173. https://doi.org/10.17094/ataunivbd.363858.
JAMA Gündoğdu G, Taghizadehghalehjoughi A, Çiçek B, Şenol O, Nalcı KA, Demirkaya AK, Hacımüftüoğlu A. Glutamat Eksitotoksisitesi Oluşturulan Primer Kortikal Nöron Kültürlerinde Parietinin Nöroprotektif Etkisinin İncelenmesi. Atatürk Üniversitesi Veteriner Bilimleri Dergisi. 2018;13:165–173.
MLA Gündoğdu, Gülşah vd. “Glutamat Eksitotoksisitesi Oluşturulan Primer Kortikal Nöron Kültürlerinde Parietinin Nöroprotektif Etkisinin İncelenmesi”. Atatürk Üniversitesi Veteriner Bilimleri Dergisi, c. 13, sy. 2, 2018, ss. 165-73, doi:10.17094/ataunivbd.363858.
Vancouver Gündoğdu G, Taghizadehghalehjoughi A, Çiçek B, Şenol O, Nalcı KA, Demirkaya AK, Hacımüftüoğlu A. Glutamat Eksitotoksisitesi Oluşturulan Primer Kortikal Nöron Kültürlerinde Parietinin Nöroprotektif Etkisinin İncelenmesi. Atatürk Üniversitesi Veteriner Bilimleri Dergisi. 2018;13(2):165-73.