Two fighters against oxidative stress in peripheral organs in Parkinson's Disease: Brain-derived neurotrophic factor and hydrogen sulfide
Abstract
Aim: Parkinson's disease, which is a neurodegenerative disorder, has adverse consequences on peripheral organs as well as the brain. This study aims to investigate the effects of brain-derived neurotrophic factor and hydrogen sulfide on liver, kidney, stomach and intestine in Parkinson's disease model created in mice. Materials and Methods: To assess the achievement of the Parkinson's disease model and the effects of brain-derived neurotrophic factor and hydrogen sulfide on this model, animals in all groups were subjected to motor behavior tests. Oxidative stress in peripheral organs was determined biochemically by measuring total oxidant and total antioxidant levels. It was also evaluated histologically in terms of tissue damage and cellular degeneration. Results: According to the motor behaviour tests it was revealed that hydrogen sulfide increased motor performance and coordination against Parkinson's disease and decreased bradykinesia. Experimental Parkinson's Disease and inhibition of the brain-derived neurotrophic factor caused cellular changes in the liver, kidney, and intestine indicating oxidative stress-induced degeneration. It was revealed that hydrogen sulfide protects the histological structure especially in the liver and intestinal tissue and supports the process by increasing the antioxidant capacity in the liver and decreasing the oxidant capacity in the intestine. Conclusion: Brain-derived neurotrophic factor and hydrogen sulfide have different but generaly protective effects on oxidative stress in peripheral organs due to Parkinson's disease.
Keywords
Brain derived neurotrophic factor hydrogen sulfide oxidative stress Parkinson's disease peripheral organs
Ethical Statement
The authors declare no conflict of interest.
Thanks
The authors would like to thank Prof. Dr. Yigit UYANIKGIL, faculty member of Ege University Faculty of Medicine, Department of Histology and Embryology, for all his scientific support.
References
- 1. Moore DJ, West AB, Dawson VL, Dawson TM. Molecular pathophysiology of Parkinson's disease. Annual Review of Neuroscience 2005; 28:57-87.
- Giovannini D, Andreola F, Spitalieri P, Krasnowska EK, Colini Baldeschi A, Rossi S, et al. Natriuretic peptides are neuroprotective on in vitro models of PD and promote dopaminergic differentiation of hiPSCs derived neurons via the Wnt/β-catenin signaling. Cell Death Discovery 2021; 7(1):330.
- Beitz JM. Parkinson's disease: a review. Frontiers in Bioscience (Scholar Edition) 2014; 6(1):65-74.
- Narmashiri A, Abbaszadeh M, Ghazizadeh A. The effects of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) on the cognitive and motor functions in rodents: A systematic review and meta-analysis. Neuroscience and Biobehavioral Reviews 2022; 140:104792.
- Arora PK, Riachi NJ, Harik SI, Sayre LM. Chemical oxidation of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) and its in vivo metabolism in rat brain and liver. Biochemical and Biophysical Research Communications 1988; 152(3):1339-47.
- Lai F, Jiang R, Xie W, Liu X, Tang Y, Xiao H, et al. Intestinal Pathology and Gut Microbiota Alterations in a Methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) Mouse Model of Parkinson's Disease. Neurochemical Research 2018; 43(10):1986-99.
- Menozzi E, Macnaughtan J, Schapira AHV. The gut-brain axis and Parkinson disease: clinical and pathogenetic relevance. Annals of Medicine 2021; 53(1):611-25.
- Palasz E, Wysocka A, Gasiorowska A, Chalimoniuk M, Niewiadomski W, Niewiadomska G. BDNF as a Promising Therapeutic Agent in Parkinson's Disease. International Journal of Molecular Sciences 2020; 21(3):1170.
- Iu ECY, Chan CB. Is Brain-Derived Neurotrophic Factor a Metabolic Hormone in Peripheral Tissues? Biology (Basel) 2022; 11(7):1063.
- Afsar B, Afsar RE. Brain-derived neurotrophic factor (BDNF): a multifaceted marker in chronic kidney disease. Clinical and Experimental Nephrology 2022; 26(12):1149-59.
- Okugawa Y, Tanaka K, Inoue Y, Kawamura M, Kawamoto A, Hiro J, et al. Brain-derived neurotrophic factor/tropomyosin-related kinase B pathway in gastric cancer. British Journal of Cancer 2013; 108(1):121-30.
- Biddinger JE, Fox EA. Reduced intestinal brain-derived neurotrophic factor increases vagal sensory innervation of the intestine and enhances satiation. Journal of Neuroscience 2014; 34(31):10379-93.
- Esfandi F, Bouraghi H, Glassy MC, Taheri M, Kahaei MS, Kholghi Oskooei V, et al. Brain-derived neurotrophic factor downregulation in gastric cancer. Journal of Cellular Biochemistry 2019;120(10):17831-7.
- Yarmohammadi F, Hayes AW, Karimi G. The cardioprotective effects of hydrogen sulfide by targeting endoplasmic reticulum stress and the Nrf2 signaling pathway: A review. BioFactors 2021; 47(5):701-12.
- Sarukhani M, Haghdoost-Yazdi H, Sarbazi Golezari A, Babayan-Tazehkand A, Dargahi T, Rastgoo N. Evaluation of the antiparkinsonism and neuroprotective effects of hydrogen sulfide in acute 6 hydroxydopamine-induced animal model of Parkinson's disease: behavioral, histological and biochemical studies. Neurological Research 2018; 40(7):523-31.
- Abdel-Zaher AO, Abd-Ellatief RB, Aboulhagag NA, Farghaly HSM, Al-Wasei FMM. The potential relationship between gasotransmitters and oxidative stress, inflammation and apoptosis in lead-induced hepatotoxicity in rats. Tissue and Cell 2021; 71:101511.
- Scammahorn JJ, Nguyen ITN, Bos EM, Van Goor H, Joles JA. Fighting Oxidative Stress with Sulfur: Hydrogen Sulfide in the Renal and Cardiovascular Systems. Antioxidants (Basel) 2021; 10(3):373.
- Gao S, Li W, Zou W, Zhang P, Tian Y, Xiao F, et al. H2S protects PC12 cells against toxicity of corticosterone by modulation of BDNF-TrkB pathway. Acta Biochimica et Biophysica Sinica 2015; 47(11):915-24.
- Paul BD, Snyder SH. Gasotransmitter hydrogen sulfide signaling in neuronal health and disease. Biochemical Pharmacology 2018; 149:101-9.
- Hacioglu G, Cirrik S, Tezcan Yavuz B, Tomruk C, Keskin A, Uzunoglu E, et al. The BDNF-TrkB signaling pathway is partially involved in the neuroprotective effects of hydrogen sulfide in Parkinson's disease. European Journal of Pharmacology 2023; 944:175595.
- Liu Y, Liao S, Quan H, Lin Y, Li J, Yang Q. Involvement of microRNA-135a-5p in the Protective Effects of Hydrogen Sulfide Against Parkinson's Disease. Cellular Physiology and Biochemistry 2016; 40(1-2):18-26.
- Schober A. Classic toxin-induced animal models of Parkinson's disease: 6-OHDA and MPTP. Cell and Tissue Research 2004; 318(1):215-24.
- Choi JY, Yun J, Hwang CJ, Lee HP, Kim HD, Chun H, et al. (E)-2-methoxy-4-(3-(4-methoxyphenyl) prop-1-en 1-yl) Phenol Ameliorates MPTP-Induced Dopaminergic Neurodegeneration by Inhibiting the STAT3 Pathway. International Journal of Molecular Sciences 2019; 20(11): 2632.
- Hou X, Yuan Y, Sheng Y, Yuan B, Wang Y, Zheng J, et al. GYY4137, an H2S Slow-Releasing Donor, Prevents Nitrative Stress and α-Synuclein Nitration in an MPTP Mouse Model of Parkinson's Disease. Frontiers in Pharmacology 2017; 8:741.
- Aziz NM, Elbassuoni EA, Kamel MY, Ahmed SM. Hydrogen sulfide renal protective effects: possible link between hydrogen sulfide and endogenous carbon monoxide in a rat model of renal injury. Cell Stress Chaperones 2020; 25(2):211-21.
- Sun HJ, Wu ZY, Nie XW, Wang XY, Bian JS. Implications of hydrogen sulfide in liver pathophysiology: Mechanistic insights and therapeutic potential. Journal of Advanced Research 2020; 27:127-35.
- Askari H, Seifi B, Kadkhodaee M, Sanadgol N, Elshiekh M, Ranjbaran M, et al. Protective effects of hydrogen sulfide on chronic kidney disease by reducing oxidative stress, inflammation and apoptosis. EXCLI Journal 2018; 17:14-23. Blachier F, Davila AM, Mimoun S, Benetti PH, Atanasiu C, Andriamihaja M, et al. Luminal sulfide and large intestine mucosa: friend or foe? Amino Acids 2010; 39(2):335-47.
Parkinson hastalığında periferik organlardaki oksidatif strese karşı iki savaşçı: Beyin kaynaklı nörotrofik faktör ve hidrojen sülfit
Abstract
Amaç: Nörodejeneratif bir hastalık olan Parkinson hastalığının beyinde olduğu gibi periferik organlarda da olumsuz sonuçları vardır. Bu çalışmada farelerde oluşturulan Parkinson hastalığı modelinde beyin kaynaklı nörotrofik faktör ve hidrojen sülfitin karaciğer, böbrek, mide ve bağırsak üzerindeki etkilerinin araştırılması amaçlanmaktadır. Gereç ve Yöntem: Parkinson hastalığı modelinin başarısını ve beyin kaynaklı nörotrofik faktör ile hidrojen sülfitin bu model üzerindeki etkilerini değerlendirmek için tüm gruplardaki hayvanlar motor davranış testlerine tabi tutuldu. Periferik organlardaki oksidatif stres, biyokimyasal olarak toplam oksidan ve toplam antioksidan seviyeleri ölçülerek belirlendi. Ayrıca histolojik olarak doku hasarı ve hücresel dejenerasyon bakımından değerlendirildi. Bulgular: Motor davranış testlerine göre hidrojen sülfitin Parkinson hastalığına karşı motor performansı ve koordinasyonu arttırdığı, bradikineziyi azalttığı ortaya çıktı. Deneysel Parkinson hastalığı ve beyin kaynaklı nörotrofik faktörün inhibisyonu, karaciğer, böbrek ve bağırsakta oksidatif stresin neden olduğu dejenerasyona işaret eden hücresel değişikliklere neden oldu. Hidrojen sülfitin özellikle karaciğer ve bağırsak dokusunda histolojik yapıyı koruduğu ve karaciğerde antioksidan kapasiteyi artırarak, bağırsakta ise oksidan kapasiteyi azaltarak süreci desteklediği ortaya çıktı. Sonuç: Beyin kaynaklı nörotrofik faktör ve hidrojen sülfitin, Parkinson hastalığına bağlı olarak periferik organlarda meydana gelen oksidatif stres üzerinde, farklı ancak genel olarak koruyucu etkileri vardır.
Keywords
Beyin kaynaklı nörotrofik faktör hidrojen sülfit oksidatif stres Parkinson hastalığı periferik organlar
References
- 1. Moore DJ, West AB, Dawson VL, Dawson TM. Molecular pathophysiology of Parkinson's disease. Annual Review of Neuroscience 2005; 28:57-87.
- Giovannini D, Andreola F, Spitalieri P, Krasnowska EK, Colini Baldeschi A, Rossi S, et al. Natriuretic peptides are neuroprotective on in vitro models of PD and promote dopaminergic differentiation of hiPSCs derived neurons via the Wnt/β-catenin signaling. Cell Death Discovery 2021; 7(1):330.
- Beitz JM. Parkinson's disease: a review. Frontiers in Bioscience (Scholar Edition) 2014; 6(1):65-74.
- Narmashiri A, Abbaszadeh M, Ghazizadeh A. The effects of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) on the cognitive and motor functions in rodents: A systematic review and meta-analysis. Neuroscience and Biobehavioral Reviews 2022; 140:104792.
- Arora PK, Riachi NJ, Harik SI, Sayre LM. Chemical oxidation of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) and its in vivo metabolism in rat brain and liver. Biochemical and Biophysical Research Communications 1988; 152(3):1339-47.
- Lai F, Jiang R, Xie W, Liu X, Tang Y, Xiao H, et al. Intestinal Pathology and Gut Microbiota Alterations in a Methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) Mouse Model of Parkinson's Disease. Neurochemical Research 2018; 43(10):1986-99.
- Menozzi E, Macnaughtan J, Schapira AHV. The gut-brain axis and Parkinson disease: clinical and pathogenetic relevance. Annals of Medicine 2021; 53(1):611-25.
- Palasz E, Wysocka A, Gasiorowska A, Chalimoniuk M, Niewiadomski W, Niewiadomska G. BDNF as a Promising Therapeutic Agent in Parkinson's Disease. International Journal of Molecular Sciences 2020; 21(3):1170.
- Iu ECY, Chan CB. Is Brain-Derived Neurotrophic Factor a Metabolic Hormone in Peripheral Tissues? Biology (Basel) 2022; 11(7):1063.
- Afsar B, Afsar RE. Brain-derived neurotrophic factor (BDNF): a multifaceted marker in chronic kidney disease. Clinical and Experimental Nephrology 2022; 26(12):1149-59.
- Okugawa Y, Tanaka K, Inoue Y, Kawamura M, Kawamoto A, Hiro J, et al. Brain-derived neurotrophic factor/tropomyosin-related kinase B pathway in gastric cancer. British Journal of Cancer 2013; 108(1):121-30.
- Biddinger JE, Fox EA. Reduced intestinal brain-derived neurotrophic factor increases vagal sensory innervation of the intestine and enhances satiation. Journal of Neuroscience 2014; 34(31):10379-93.
- Esfandi F, Bouraghi H, Glassy MC, Taheri M, Kahaei MS, Kholghi Oskooei V, et al. Brain-derived neurotrophic factor downregulation in gastric cancer. Journal of Cellular Biochemistry 2019;120(10):17831-7.
- Yarmohammadi F, Hayes AW, Karimi G. The cardioprotective effects of hydrogen sulfide by targeting endoplasmic reticulum stress and the Nrf2 signaling pathway: A review. BioFactors 2021; 47(5):701-12.
- Sarukhani M, Haghdoost-Yazdi H, Sarbazi Golezari A, Babayan-Tazehkand A, Dargahi T, Rastgoo N. Evaluation of the antiparkinsonism and neuroprotective effects of hydrogen sulfide in acute 6 hydroxydopamine-induced animal model of Parkinson's disease: behavioral, histological and biochemical studies. Neurological Research 2018; 40(7):523-31.
- Abdel-Zaher AO, Abd-Ellatief RB, Aboulhagag NA, Farghaly HSM, Al-Wasei FMM. The potential relationship between gasotransmitters and oxidative stress, inflammation and apoptosis in lead-induced hepatotoxicity in rats. Tissue and Cell 2021; 71:101511.
- Scammahorn JJ, Nguyen ITN, Bos EM, Van Goor H, Joles JA. Fighting Oxidative Stress with Sulfur: Hydrogen Sulfide in the Renal and Cardiovascular Systems. Antioxidants (Basel) 2021; 10(3):373.
- Gao S, Li W, Zou W, Zhang P, Tian Y, Xiao F, et al. H2S protects PC12 cells against toxicity of corticosterone by modulation of BDNF-TrkB pathway. Acta Biochimica et Biophysica Sinica 2015; 47(11):915-24.
- Paul BD, Snyder SH. Gasotransmitter hydrogen sulfide signaling in neuronal health and disease. Biochemical Pharmacology 2018; 149:101-9.
- Hacioglu G, Cirrik S, Tezcan Yavuz B, Tomruk C, Keskin A, Uzunoglu E, et al. The BDNF-TrkB signaling pathway is partially involved in the neuroprotective effects of hydrogen sulfide in Parkinson's disease. European Journal of Pharmacology 2023; 944:175595.
- Liu Y, Liao S, Quan H, Lin Y, Li J, Yang Q. Involvement of microRNA-135a-5p in the Protective Effects of Hydrogen Sulfide Against Parkinson's Disease. Cellular Physiology and Biochemistry 2016; 40(1-2):18-26.
- Schober A. Classic toxin-induced animal models of Parkinson's disease: 6-OHDA and MPTP. Cell and Tissue Research 2004; 318(1):215-24.
- Choi JY, Yun J, Hwang CJ, Lee HP, Kim HD, Chun H, et al. (E)-2-methoxy-4-(3-(4-methoxyphenyl) prop-1-en 1-yl) Phenol Ameliorates MPTP-Induced Dopaminergic Neurodegeneration by Inhibiting the STAT3 Pathway. International Journal of Molecular Sciences 2019; 20(11): 2632.
- Hou X, Yuan Y, Sheng Y, Yuan B, Wang Y, Zheng J, et al. GYY4137, an H2S Slow-Releasing Donor, Prevents Nitrative Stress and α-Synuclein Nitration in an MPTP Mouse Model of Parkinson's Disease. Frontiers in Pharmacology 2017; 8:741.
- Aziz NM, Elbassuoni EA, Kamel MY, Ahmed SM. Hydrogen sulfide renal protective effects: possible link between hydrogen sulfide and endogenous carbon monoxide in a rat model of renal injury. Cell Stress Chaperones 2020; 25(2):211-21.
- Sun HJ, Wu ZY, Nie XW, Wang XY, Bian JS. Implications of hydrogen sulfide in liver pathophysiology: Mechanistic insights and therapeutic potential. Journal of Advanced Research 2020; 27:127-35.
- Askari H, Seifi B, Kadkhodaee M, Sanadgol N, Elshiekh M, Ranjbaran M, et al. Protective effects of hydrogen sulfide on chronic kidney disease by reducing oxidative stress, inflammation and apoptosis. EXCLI Journal 2018; 17:14-23. Blachier F, Davila AM, Mimoun S, Benetti PH, Atanasiu C, Andriamihaja M, et al. Luminal sulfide and large intestine mucosa: friend or foe? Amino Acids 2010; 39(2):335-47.
Details
| Primary Language | English |
|---|---|
| Subjects | Central Nervous System, Histology and Embryology |
| Journal Section | Research Articles |
| Authors | |
| Publication Date | June 10, 2024 |
| Submission Date | September 5, 2023 |
| Published in Issue | Year 2024 |