Assessing Caffeine's Neuroprotective Effects on Rotenone-Induced Parkinson's Disease: Unravelling the Neurological Dynamics of Striatal Impact

Authors

  • Timileyin A. Adeyeye Department of Anatomy, Olabisi Onabanjo University, Ogun State, Nigeria
  • Bamidele R. Babatunde Department of Anatomy, Olabisi Onabanjo University, Ogun State, Nigeria
  • Oluwadamilola F. Shallie
  •  Babatunde O. Osidele Department of Anatomy, Olabisi Onabanjo University, Ogun State, Nigeria
  • Philemon D. Shallie Department of Anatomy, Olabisi Onabanjo University, Ogun State, Nigeria https://orcid.org/0000-0001-9910-3584 (unauthenticated)

DOI:

https://doi.org/10.47081/njn2024.15.1/002

Keywords:

Caffeine, Parkinson’s disease, Rotenone, Striatum

Abstract

The alarming prevalence of Parkinson's disease (PD) has prompted a search for standard therapeutic interventions capable of altering or halting its progression. Identifying a neuroprotective or disease-modifying therapy for PD is akin to pursuing the Holy Grail. Numerous studies have affirmed the therapeutic benefits of adenosine A2A receptor blockade in alleviating both motor and non-motor symptoms in PD. Furthermore, A2A receptors are selectively localized in the basal ganglia. This study aimed to evaluate the impact of caffeine on the striatum of rats with PD induced by rotenone. Fifty adult male Wistar rats, weighing between 150 and 200g, were utilised in this study. The rats were randomly assigned to five groups, each consisting of ten rats: Group A (vehicle group, alcohol, 3mL/kg), group B (rotenone-only treated with 3mg/kg, ip.), group C (caffeine 30mg/kg + rotenone 3mg/kg, ip.), group D (rotenone 3mg/kg + caffeine 30mg/kg, ip.), and group E (caffeine-only treated with 30mg/kg, ip.). The findings revealed a significant (p<0.05) reduction in body weight and relative brain weight in response to caffeine treatments. Rotenone administration induced histological changes akin to those observed in PD, encompassing neuronal structural derangement, degenerated striatal bundled fibre, and loss of myelinated neurons and Nissl substance. This study adds to the growing body of research supporting the therapeutic potential of caffeine in PD. The results highlight caffeine's neuroprotective properties and its ability to mitigate striatal lesions. The pursuit of effective interventions for PD remains crucial, and caffeine emerges as a promising therapeutic agent in this regard.

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References

Adeyeye, T.A., Babatunde, B.R., Ehireme, S.E. and Shallie, P.D. (2023) Caffeine alleviates anxiety-like behavior and brainstem lesions in a rotenone induced rat model of Parkinson’s disease. J Chem Neuroanat. 132:102315. https://doi.org/10.1016/j.jchemneu.2023.102315.

Baydyuk, M. and Xu, B. (2014) BDNF signaling and survival of striatal neurons. Front Cell Neurosci. 8:254. https://doi.org/10.3389/fncel.2014.00254.

Breuss, M.W., Hansen, A.H, Landler, L. and Keays, D.A. (2017) Brain-specific knockin of the pathogenic Tubb5 E401K allele causes defects in motor coordination and prepulse inhibition. Behav Brain Res. 14(323):47-55. https://doi.org/10.1016/j.bbr.2017.01.029

Calon, F., Dridi, M., Hornykiewicz, O., BeÂdard, P.J., Rajput, A.H. and Paolo, T.D. (2004) Increased adenosine A2A receptors in the brain of Parkinson's disease patients with dyskinesias. Brain. 127:1075-1084. https://doi.org/10.1093/ brain/awh128.

Chase, T.N., Bibbiani, F., Bara-Jimenez, W., Dimitrova, T. and Oh-Lee, J.D. (2003) Translating A2A antagonist KW6002 from animal models to parkinsonian patients. Neurology. 61:S107–S111.

Corneli, M.C. (2019) The impact of caffeine and coffee on human health. Nutrients. 11:416. https://doi.org/10.3390/ nu11020416.

Deacon, R.M. (2013) Measuring motor coordination in mice. J Vis Exp. 2975):e2609. https://doi.org/10.3791/ 2609.

Fathalla, A.M., Soliman, A.M. and Moustafa, A.A. (2017) Selective A2A receptors blockade reduces degeneration of substantia nigra dopamine neurons in a rotenone induced rat model of Parkinson’s disease: A histological study. Neurosci Lett. 643:89–96. https://doi.org/10.1016/j.neulet. 2017.02.036

Geoff, C., Fidler, F. and Vaux, D.L. (2007) Error bars in experimental biology. J Cell Biol. 177(1):7-11.

Horiuchi, M., Smith, L., Maezawa, I. and Jin, L.W. (2017) CX3CR1 ablation ameliorates motor and respiratory dysfunctions and improves survival of a Rett syndrome mouse model. Brain Behav Immun. 60:106-116. https://doi:10. 1016/j.bbi.2016.02.014.

Huang, W.S., Lin, S.Z., Lin, J.C., Wey, S.P., Ting, G. and Liu, R.S. (2001) Evaluation of early-stage Parkinson’s disease with 99mTc-TRODAT-1 imaging. J Nuclear Med. 42(9):1303-1308.

Ikram, M., Park, T.J., Ali T. and Kim, M.O. (2020) Antioxidant and neuroprotective effects of caffeine against Alzheimer’s and Parkinson’s disease: Insight into the role of Nrf-2 and A2AR Signaling. Antioxidant. 9:902. https://doi.org/10.3390/antiox9090902.

Kachroo, A. and Schwarzschild, M.A. (2012) Adenosine A2A receptor gene disruption protects in an alpha synuclein model of Parkinson’s disease. Ann Neurol. 2012:71, 278–282. https://doi.org/10.1002/ana.22630.

Kanda, T. and Jenner, P. (2020) Can adenosine A2A receptor antagonists modify motor behavior and dyskinesia in experimental models of Parkinson's disease? Parkinsonism Relat Disord. 80:S21-S27.

Kernie, S.G. and Parent, J.M. (2010) Forebrain neurogenesis after focal ischemic and traumatic brain injury. Neurobiol Dis. 37(2):267-274. https://doi.org/10.1016/j.nbd.200 9.11.002.

Khadrawy, Y.A., Salem, A.M., El-Shamy, K.A., Ahmed, E.K., Fadl, N.N. and Hosny, E.N. (2017) Neuroprotective and therapeutic effect of caffeine on the rat model of Parkinson's disease induced by rotenone. J Dietary Supplements. https://doi.org/10.1080/19390211.2016.1275916.

Landais, E., Moskal, A., Mullee, A., Nicolas, G., Gunter, M.J., Huybrechts, I., et al. (2018). Coffee and tea consumption and the contribution of their added ingredients to total energy and nutrient intakes in 10 European countries: Benchmark data from the late 1990s. Nutrients. 10:725. https://doi.org/10.3390/nu10060725.

LeWitt, P.A. and Chaudhuri, K.R. (2020) Unmet needs in Parkinson disease: Motor and Non-motor Parkinsonism Relat Disord. 80(S1):S7S12. https://doi.org/10.1016/j.park reldis.2020.09.024.

LeWitt, P.A. and Jenner, P. (2020) Introduction. Parkinsonism Relat Disord. 80(S1):S1-S2. https://doi.org/10.1016/j. parkreldis.2020.10.001

Luan, Y., Ren, X., Zheng, W., Zeng, Z., Guo, Y., Hou, Z., et al. (2018) Chronic caffeine treatment protects against alpha-synucleinopathy by reestablishing autophagy activity in the mouse striatum. Front Neurosci. 12:301. nhttps://doi.org/10.3389/fnins.2018.00301.

Mitroi, D.N., Tian, M., Kawaguchi, R., Lowry, W.E. and Carmichaelet, S.T. (2022) Single-nucleus transcriptome analysis reveals disease- and regeneration-associated endothelial cells in white matter vascular dementia. J Cell Mol Med. 26:3183-3195. https://doi.org/10.1111/jcmm.17 315.

Mishina, M., Ishiwata, K., Kimura, Y., Naganawa, M., Oda, K., Kobayashi, S., et al. (2007) Evaluation of distribution of adenosine A2A receptors in normal human brain measured with [11C]TMSX PET. Synapse. 61:778-784. https://doi.org/10.1002/syn.20423.

Mori, A., Chen, J.-F., Uchida, S., Durlach, C., King, S.M. and Jenner, P. (2022) The pharmacological potential of adenosine A2A receptor antagonists for treating Parkinson’s disease. Molecules. 27:2366.

NIH (1978) Guide for the care and use of animal laboratory. 7:18. DOI:10.17226/12910.

Nissl, C.T. (2014) Histology: Lecture 29: Introduction to special stains techniques: Nerve Tissue Staining. 1-29. Available: www.histology.com (Accessed 2nd March, 2014).

Obeso, J.A., Marin, C., Rodriguez-Oroz, C., Blesa, J., Benitez-Temino, B., Mena- Segovia, J. et al. (2008) The basal ganglia in Parkinson’s disease: Current concepts and unexplained observations. Ann Neurol. 64:S30-S46. https://doi.org/10.1002/ana.21481.

Obeso, J.A., Rodriguez-Oroz, M.C., Rodriguez, M., Lanciego, J.L., Artieda, J., Gonzalo, N. et al. (2000) Pathophysiology of the basal ganglia in Parkinson’s disease. Trends Neurosci. 23:S8–S19.

Ortiz-Hidalgo, C. and Pina-Oviedo, S. (2019) Hematoxylin: Mesoamerica's gift to histopathology. Palo de Campeche (logwood tree), pirates' most desired treasure, and irreplaceable tissue stain. Int J Surg Pathol. 27(1):4-14. https://doi.org/10.1177/1066896918787652.

Reyes, C.M. and Cornelis, M.C. (2018) Caffeine in the diet: Country-level consumption and guidelines. Nutrients. 10:1772. https://doi.org/10.3390/nu10111772.

Rosin, D.L., Hettinger, B.D., Lee, A. and Linden, J. (2003) Anatomy of adenosine A2A receptors in brain: morphological substrates for integration of striatal function. Neurology. https://doi.org/10.1212/01.wnl.0000095205.33940.99.

Schröter, N. and Jost, W.H. (2022) Role of adenosine A2A receptor antagonists in the treatment of Parkinson’s disease Vol. 26 current topics in Pharmacology.

Souza, M.F.D., Bispo, J.M.M., Leal, P.C., Gois, A.M.D. and Santos, J.R.D. (2017) Commentary: Adenosine A(2A) receptor blockade prevents rotenone induced motor impairment in a rat model of Parkinsonism. Front Behav Neurosci. 11:93. https://doi.org/10.3389/fnbeh.2017.00093.

Sturman, O., Germain, P.L. and Bohacek, J. (2018) Exploratory rearing: a context and stress-sensitive behavior recorded in the open-field test. Stress. 21(5):443–452. https://doi.org/10.1080/10253890.2018.1438405.

Svenningsson, P., Hall, H., Sedvall, G. and Fredholm, B.B. (1997) Distribution of adenosine receptors in the postmortem human brain: an extended autoradiographic study. Synapse. 27:322-335. https://doi.org/10.1002/(SICI)1098

Tatem, K.S., Quinn, J.L., Phadke, A., Yu, Q., Gordish-Dressman, H. and Nagaraju, K. (2014) Behavioral and locomotor measurements using an open field activity monitoring system for skeletal muscle diseases. J Vis Exp (91):e51785. doi:10.3791/51785.

Uchida, S., Tashiro, T., Kawai-Uchida, M., Mori, A., Jenner, P. and Kanda, T. (2014) Adenosine A2A receptor antagonist istradefylline enhances the motor response of L-DOPA without worsening dyskinesia in MPTP-treated common marmosets. J. Pharmacol Sci. 124:480-485.

Uchida, S., Soshiroda, K., Okita, E., Kawai-Uchida, M., Mori, A., Jenner, P., et al. (2015) The adenosine A2A receptor antagonist, istradefylline enhances the antiParkinsonian activity of low doses of dopamine agonists in MPTP treated common marmosets. Eur J Pharmacol. 747: 160-165. https://doi.org/10.1016/j.ejphar.2015.09.028.

Vuorimaa, A., Rissanen, E. and Airas, L. (2017) In vivo PET imaging of adenosine 2A receptors in neuroinflammatory and neurodegenerative disease. Contrast Media Mol Imaging. 2017:6975841. http://dx.doi.org/10.1155/2017/69 75841.

Waggan, I., Rissanen, E., Tuisku, J., Matilainen, M., Helin, S., Parkkola, R. et al. (2021) Effect of dopaminergic medication on adenosine 2A receptor availability in patients with Parkinson’s disease. Parkinsonism Relat Disord. 86:40-44. https://doi.org/10.1016/j.parkreldis.2021.03.030.

Zimmermann, M. (1983) Ethical guidelines for investigations of experimental pain in conscious animals. Pain. 16:109-110.

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Published

2024-03-25

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How to Cite

Assessing Caffeine’s Neuroprotective Effects on Rotenone-Induced Parkinson’s Disease: Unravelling the Neurological Dynamics of Striatal Impact. (2024). Nigerian Journal of Neuroscience, 15(1), 14-21. https://doi.org/10.47081/njn2024.15.1/002

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