Neuroinflammation-induced neurodegeneration and associated microglia activation in Parkinson’s disease: a novel neurotherapeutic avenue

Authors

  • Panlekha Rungruang Molecular Medicine Program, Multidisciplinary Unit, Faculty of Science, Mahidol University, Bangkok, Thailand.
  • Veerawat Sansri Department of Basic Medical Science, Faculty of Medicine Vajira Hospital, Navamindradhiraj University, Bangkok, Thailand.
  • Morakot Sroyraya Department of Anatomy, Faculty of Science, Mahidol University, Bangkok, Thailand.

DOI:

https://doi.org/10.31117/neuroscirn.v7i1.271

Keywords:

Neuroinflammation, Neurodegenerative diseases, Microglia, Parkinson's disease

Abstract

Parkinson’s disease (PD) is classified as one type of neurodegenerative disorder. Movement disorder, which includes resting tremors and slowness of movement, is a common clinical symptom in PD patients. Neuroinflammation is one of the most important processes involved in the pathogenesis of PD. An inflammatory response in the brain can induce neuronal cell death. Microglia, a type of immune cell, plays a crucial role in neuroinflammation. In this review, we discussed the information on microglia-activated neuroinflammation, its relationship with PD, and therapeutic approaches for neuroinflammation in PD. Under normal conditions, microglia in their inactive state (M0) act as surveillance agents in the brain to investigate potential invasions. They regulate neuron production, remodel synapses, and secrete growth factors to protect the neurons. Under pathological conditions, the M0 transforms into active phenotypes, dividing into pro-inflammatory (M1) and anti-inflammatory (M2) microglia. The M1 and M2 microglia exhibit opposite functions, where M1 microglia promote pro-inflammatory responses, and M2 microglia promote anti-inflammatory responses. This dichotomy of functions is essential for maintaining a healthy level of inflammation in the brain. Presently, multiple therapeutic strategies are available for PD, encompassing anti-inflammatory drugs, neuroprotective compounds, antioxidants, nanoparticles targeting neuroinflammation, stem cell interventions, lifestyle adjustments, and microglia-focused treatments. These treatments improve patients' movement, allowing them to have lifestyles like others, consequently benefiting their mental and emotional well-being. Preventing microglia from polarising into the M1 phenotype and promoting their polarisation into the M2 phenotype could be a challenging and promising approach for treating PD.

References

Abdollahzadeh, M., Panahpour, H., Ghaheri, S., & Saadati, H. (2022). Calcitriol supplementation attenuates cisplatin-induced behavioral and cognitive impairments through up-regulation of BDNF in male rats. Brain Research Bulletin, 181, 21–29. https://doi.org/10.1016/J.BRAINRESBULL.2022.01.006

Amarante-Mendes, G. P., Adjemian, S., Branco, L. M., Zanetti, L. C., Weinlich, R., & Bortoluci, K. R. (2018). Pattern recognition receptors and the host cell death molecular machinery. Frontiers in Immunology, 9, 02379. https://doi.org/10.3389/FIMMU.2018.02379

Anwar, M. A., Panneerselvam, S., Shah, M., & Choi, S. (2015). Insights into the species-specific TLR4 signaling mechanism in response to Rhodobacter sphaeroides lipid A detection. Scientific Reports, 5(1), 1–11. https://doi.org/10.1038/srep07657

Arjomandnejad, M., Kopec, A. L., & Keeler, A. M. (2022). CAR-T Regulatory (CAR-Treg) cells: engineering and applications. Biomedicines, 10(2), 287. https://doi.org/10.3390/BIOMEDICINES10020287

Bachiller, S., Jiménez-Ferrer, I., Paulus, A., Yang, Y., Swanberg, M., Deierborg, T., & Boza-Serrano, A. (2018). Microglia in neurological diseases: a road map to brain-disease dependent-inflammatory response. Frontiers in Cellular Neuroscience, 12, 00488. https://doi.org/10.3389/FNCEL.2018.00488

Bahar-Shany, K., Ravid, A., & Koren, R. (2009). Upregulation of MMP-9 production by TNFα in keratinocytes and its attenuation by vitamin D. Journal of Cellular Physiology, 222(3), 729–737. https://doi.org/10.1002/JCP.22004

Bandopadhyay, R. (2016). sequential extraction of soluble and insoluble alpha-synuclein from Parkinsonian brains. Journal of Visualized Experiments : JoVE, 2016(107), 53415. https://doi.org/10.3791/53415

Behl, T., Arora, A., Singla, R. K., Sehgal, A., Makeen, H. A., Albratty, M., Meraya, A. M., Najmi, A., & Bungau, S. G. (2022). Understanding the role of “sunshine vitamin D” in Parkinson’s disease: A review. Frontiers in Pharmacology, 13, 993033. https://doi.org/10.3389/FPHAR.2022.993033

Bjarnason, I. T., Charlett, A., Dobbs, R. J., Dobbs, S. M., Ibrahim, M. A. A., Kerwin, R. W., Mahler, R. F., Oxlade, N. L., Peterson, D. W., Plant, J. M., Price, A. B., & Weller, C. (2005). Role of chronic infection and inflammation in the gastrointestinal tract in the etiology and pathogenesis of idiopathic parkinsonism. Helicobacter, 10(4), 276–287. https://doi.org/10.1111/J.1523-5378.2005.00330.X

Bloem, B. R., Okun, M. S., & Klein, C. (2021). Parkinson’s disease. The Lancet, 397(10291), 2284–2303. https://doi.org/10.1016/S0140-6736(21)00218-X

Brakedal, B., Tzoulis, C., Tysnes, O. B., & Haugarvoll, K. (2021). NSAID use is not associated with Parkinson’s disease incidence: A Norwegian Prescription Database study. PLoS ONE, 16(9), e0256602. https://doi.org/10.1371/JOURNAL.PONE.0256602

Brandes, M. S., & Gray, N. E. (2020). NRF2 as a therapeutic target in neurodegenerative diseases. ASN Neuro, 12, 1759091419899782. https://doi.org/10.1177/1759091419899782

Buendia, I., Michalska, P., Navarro, E., Gameiro, I., Egea, J., & León, R. (2016). Nrf2-ARE pathway: An emerging target against oxidative stress and neuroinflammation in neurodegenerative diseases. Pharmacology and Therapeutics, 157, 84–104. https://doi.org/10.1016/j.pharmthera.2015.11.003

Cai, Y., Zhang, M. M., Wang, M., Jiang, Z. H., & Tan, Z. G. (2022). Bone marrow-derived mesenchymal stem cell-derived exosomes containing gli1 alleviate microglial activation and neuronal apoptosis in vitro and in a mouse Parkinson disease model by direct inhibition of Sp1 signaling. Journal of Neuropathology & Experimental Neurology, 81(7), 522–534. https://doi.org/10.1093/JNEN/NLAC037

Calvello, R., Cianciulli, A., Nicolardi, G., De Nuccio, F., Giannotti, L., Salvatore, R., Porro, C., Trotta, T., Panaro, M. A., & Lofrumento, D. D. (2016). Vitamin D treatment attenuates neuroinflammation and dopaminergic neurodegeneration in an animal model of Parkinson’s disease, shifting M1 to M2 microglia responses. Journal of Neuroimmune Pharmacology, 12(2), 327–339. https://doi.org/10.1007/S11481-016-9720-7

Caprnda, M., Kubatka, P., Gazdikova, K., Gasparova, I., Valentova, V., Stollarova, N., La Rocca, G., Kobyliak, N., Dragasek, J., Mozos, I., Prosecky, R., Siniscalco, D., Büsselberg, D., Rodrigo, L., & Kruzliak, P. (2017). Immunomodulatory effects of stem cells: Therapeutic option for neurodegenerative disorders. Biomedicine and Pharmacotherapy, 91, 60–69. https://doi.org/10.1016/J.BIOPHA.2017.04.034

Castelli, M. S., McGonigle, P., & Hornby, P. J. (2019). The pharmacology and therapeutic applications of monoclonal antibodies. Pharmacology Research & Perspectives, 7(6), e00535. https://doi.org/10.1002/PRP2.535

Chen, H. X., Liang, F. C., Gu, P., Xu, B. L., Xu, H. J., Wang, W. T., Hou, J. Y., Xie, D. X., Chai, X. Q., & An, S. J. (2020). Exosomes derived from mesenchymal stem cells repair a Parkinson’s disease model by inducing autophagy. Cell Death & Disease 2020 11:4, 11(4), 1–17. https://doi.org/10.1038/s41419-020-2473-5

Chen, H., Zhang, S. M., Hernán, M. A., Schwarzschild, M. A., Willett, W. C., Colditz, G. A., Speizer, F. E., & Ascherio, A. (2003). Non-steroidal anti-inflammatory drugs and the risk of Parkinson disease. Archives of Neurology, 60(8), 1059–1064. https://doi.org/10.1001/ARCHNEUR.60.8.1059

Chen, W. W., Zhang, X., & Huang, W. J. (2016). Role of neuroinflammation in neurodegenerative diseases. Molecular Medicine Reports, 13(4), 3391–3396. https://doi.org/10.3892/mmr.2016.4948

Cookson, M. R. (2009). α-Synuclein and neuronal cell death. Molecular Neurodegeneration, 4(1), 9. https://doi.org/10.1186/1750-1326-4-9

Couper, K. N., Blount, D. G., & Riley, E. M. (2008). IL-10: The master regulator of immunity to infection. Journal of Immunology, 180(9), 5771–5777. https://doi.org/10.4049/JIMMUNOL.180.9.5771

Croisier, E., Moran, L. B., Dexter, D. T., Pearce, R. K. B., & Graeber, M. B. (2005). Microglial inflammation in the Parkinsonian substantia nigra: Relationship to alpha-synuclein deposition. Journal of Neuroinflammation, 2(1), 1–8. https://doi.org/10.1186/1742-2094-2-14

Cui, B., Guo, X., You, Y., & Fu, R. (2019). Farrerol attenuates MPP + -induced inflammatory response by TLR4 signaling in a microglia cell line. Phytotherapy Research, 33(4), 1134–1141. https://doi.org/10.1002/PTR.6307

Cui, X., & Eyles, D. W. (2022). Vitamin D and the central nervous system: causative and preventative mechanisms in brain disorders. Nutrients, 14(20), 4353. https://doi.org/10.3390/NU14204353

De Nuccio, F., Cianciulli, A., Porro, C., Kashyrina, M., Ruggiero, M., Calvello, R., Miraglia, A., Nicolardi, G., Lofrumento, D. D., & Panaro, M. A. (2021). Inflammatory response modulation by vitamin C in an MPTP mouse model of Parkinson’s disease. Biology, 10(11), 1155. https://doi.org/10.3390/BIOLOGY10111155

Di Filippo, M., Chiasserini, D., Tozzi, A., Picconi, B., & Calabresi, P. (2010). Mitochondria and the link between neuroinflammation and neurodegeneration. Journal of Alzheimer’s Disease : JAD, 20(s2), S369-S379. https://doi.org/10.3233/JAD-2010-100543

Dixit, A., Srivastava, G., Verma, D., Mishra, M., Singh, P. K., Prakash, O., & Singh, M. P. (2013). Minocycline, levodopa and MnTMPyP induced changes in the mitochondrial proteome profile of MPTP and maneb and paraquat mice models of Parkinson’s disease. Biochimica et Biophysica Acta, 1832(8), 1227–1240. https://doi.org/10.1016/J.BBADIS.2013.03.019

Driver, J. A., Logroscino, G., Lu, L., Gaziano, J. M., & Kurth, T. (2011). Use of non-steroidal anti-inflammatory drugs and risk of Parkinson’s disease: nested case-control study. BMJ, 342, d198. https://doi.org/10.1136/BMJ.D198

Dzamko, N., Geczy, C. L., & Halliday, G. M. (2015). Inflammation is genetically implicated in Parkinson’s disease. Neuroscience, 302, 89–102. https://doi.org/10.1016/J.NEUROSCIENCE.2014.10.028

Etminan, M., Carleton, B. C., & Samii, A. (2008). Non-steroidal anti-inflammatory drug use and the risk of Parkinson disease: A retrospective cohort study. Journal of Clinical Neuroscience, 15(5), 576–577. https://doi.org/10.1016/J.JOCN.2007.02.095

Fang, C., Lv, L., Mao, S., Dong, H., & Liu, B. (2020). Cognition deficits in Parkinson’s disease: mechanisms and treatment. Parkinson’s Disease, 2020, 1–11. https://doi.org/10.1155/2020/2076942

Fatoba, O., Itokazu, T., & Yamashita, T. (2020). Microglia as therapeutic target in central nervous system disorders. Journal of Pharmacological Sciences, 144(3), 102–118. https://doi.org/10.1016/j.jphs.2020.07.004

Fontana, L., Ghezzi, L., Cross, A. H., & Piccio, L. (2021). Effects of dietary restriction on neuroinflammation in neurodegenerative diseases. Journal of Experimental Medicine, 218(2), e20190086. https://doi.org/10.1084/jem.20190086

Frenneaux, M., & Williams, L. (2007). Ventricular-Arterial and Ventricular-Ventricular interactions and their relevance to diastolic filling. Progress in Cardiovascular Diseases, 49(4), 252–262. https://doi.org/10.1016/j.pcad.2006.08.004

Fu, Y., Zhen, J., & Lu, Z. (2017). Synergetic neuroprotective effect of docosahexaenoic acid and aspirin in SH-Y5Y by inhibiting miR-21 and activating RXRα and PPARα. DNA and Cell Biology, 36(6), 482–489. https://doi.org/10.1089/DNA.2017.3643

Gagne, J. J., & Power, M. C. (2010). Anti-inflammatory drugs and risk of Parkinson disease: a meta-analysis. Neurology, 74(12), 995–1002. https://doi.org/10.1212/WNL.0B013E3181D5A4A3

Gao, X., Chen, H., Schwarzschild, M. A., & Ascherio, A. (2011). Use of ibuprofen and risk of Parkinson disease. Neurology, 76(10), 863–869. https://doi.org/10.1212/WNL.0B013E31820F2D79

Guo, S., Wang, H., & Yin, Y. (2022). Microglia polarization from M1 to M2 in neurodegenerative diseases. Frontiers in Aging Neuroscience, 14, 815347. https://doi.org/10.3389/FNAGI.2022.815347

Hansson, O., Janelidze, S., Hall, S., Magdalinou, N., Lees, A. J., Andreasson, U., Norgren, N., Linder, J., Forsgren, L., Constantinescu, R., Zetterberg, H., & Blennow, K. (2017). Blood-based NfL: A biomarker for differential diagnosis of parkinsonian disorder. Neurology, 88(10), 930–937. https://doi.org/10.1212/WNL.0000000000003680

Hare, D. J., Adlard, P. A., Doble, P. A., & Finkelstein, D. I. (2013). Metallobiology of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine neurotoxicity. Metallomics, 5(2), 91–109. https://doi.org/10.1039/C2MT20164J

Hattingen, E., Magerkurth, J., Pilatus, U., Mozer, A., Seifried, C., Steinmetz, H., Zanella, F., & Hilker, R. (2009). Phosphorus and proton magnetic resonance spectroscopy demonstrates mitochondrial dysfunction in early and advanced Parkinson’s disease. Brain, 132(12), 3285–3297. https://doi.org/10.1093/BRAIN/AWP293

Herrera, A. J., Castaño, A., Venero, J. L., Cano, J., & Machado, A. (2000). The single intranigral injection of LPS as a new model for studying the selective effects of inflammatory reactions on dopaminergic system. Neurobiology of Disease, 7(4), 429–447. https://doi.org/10.1006/NBDI.2000.0289

Hirsch, E. C., Vyas, S., & Hunot, S. (2012). Neuroinflammation in Parkinson’s disease. Parkinsonism & Related Disorders, 18(s1), S210–S212. https://doi.org/10.1016/S1353-8020(11)70065-7

Hou, Y., Wang, K., Wan, W., Cheng, Y., Pu, X., & Ye, X. (2018). Resveratrol provides neuroprotection by regulating the JAK2/STAT3/PI3K/AKT/mTOR pathway after stroke in rats. Genes & Diseases, 5(3), 245–255. https://doi.org/10.1016/J.GENDIS.2018.06.001

Hu, J., Wu, J., Wan, F., Kou, L., Yin, S., Sun, Y., Li, Y., Zhou, Q., & Wang, T. (2021). Calcitriol alleviates MPP+- and MPTP-Induced parthanatos through the VDR/PARP1 pathway in the model of Parkinson’s disease. Frontiers in Aging Neuroscience, 13, 657095. https://doi.org/10.3389/FNAGI.2021.657095

Hughes, C. D., Choi, M. L., Ryten, M., Hopkins, L., Drews, A., Botía, J. A., Iljina, M., Rodrigues, M., Gagliano, S. A., Gandhi, S., Bryant, C., & Klenerman, D. (2019). Picomolar concentrations of oligomeric alpha-synuclein sensitizes TLR4 to play an initiating role in Parkinson’s disease pathogenesis. Acta Neuropathologica, 137(1), 103–120. https://doi.org/10.1007/S00401-018-1907-Y

Hung, M. J., Cherng, W. J., Hung, M. Y., Wu, H. T., & Pang, J. H. S. (2010). Interleukin-6 inhibits endothelial nitric oxide synthase activation and increases endothelial nitric oxide synthase binding to stabilized caveolin-1 in human vascular endothelial cells. Journal of Hypertension, 28(5), 940–951. https://doi.org/10.1097/HJH.0B013E32833992EF

Jelinek, M., Jurajda, M., & Duris, K. (2021). oxidative stress in the brain: basic concepts and treatment strategies in stroke. Antioxidants, 10(12), 1886. https://doi.org/10.3390/ANTIOX10121886

Jiang, X., Ganesan, P., Rengarajan, T., Choi, D. K., & Arulselvan, P. (2018). Cellular phenotypes as inflammatory mediators in Parkinson’s disease: Interventional targets and role of natural products. Biomedicine and Pharmacotherapy, 106, 1052–1062. https://doi.org/10.1016/j.biopha.2018.06.162

Jurga, A. M., Paleczna, M., & Kuter, K. Z. (2020). Overview of general and discriminating markers of differential microglia phenotypes. Frontiers in Cellular Neuroscience, 14, 00198. https://doi.org/10.3389/fncel.2020.00198

Kahle, P. J., Neumann, M., Ozmen, L., Müller, V., Odoy, S., Okamoto, N., Jacobsen, H., Iwatsubo, T., Trojanowski, J. Q., Takahashi, H., Wakabayashi, K., Bogdanovic, N., Riederer, P., Kretzschmar, H. A., & Haass, C. (2001). Selective Insolubility of α-Synuclein in Human Lewy Body Diseases Is Recapitulated in a Transgenic Mouse Model. The American Journal of Pathology, 159(6), 2215–2225. https://doi.org/10.1016/S0002-9440(10)63072-6

Kempuraj, D., Thangavel, R., Natteru, P. A., Selvakumar, G. P., Saeed, D., Zahoor, H., Zaheer, S., Iyer, S. S., & Zaheer, A. (2016). Neuroinflammation Induces neurodegeneration. Journal of Neurology, Neurosurgery and Spine, 1(1), 1003. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5260818/

Kim, H., Shin, J. Y., Lee, Y. S., Yun, S. P., Maeng, H. J., & Lee, Y. (2020). Brain endothelial P-Glycoprotein level is reduced in Parkinson’s disease via a vitamin D Receptor-Dependent pathway. International Journal of Molecular Sciences, 21(22), 1–15. https://doi.org/10.3390/IJMS21228538

Kim, S., Cho, S. H., Kim, K. Y., Shin, K. Y., Kim, H. S., Park, C. H., Chang, K. A., Lee, S. H., Cho, D., & Suh, Y. H. (2009). α-Synuclein induces migration of BV-2 microglial cells by up-regulation of CD44 and MT1-MMP. Journal of Neurochemistry, 109(5), 1483–1496. https://doi.org/10.1111/J.1471-4159.2009.06075.X

Kobylecki, C. (2020). Update on the diagnosis and management of Parkinson’s disease. Clinical Medicine, 20(4), 393–398. https://doi.org/10.7861/CLINMED.2020-0220

Kojima, R., Bojar, D., Rizzi, G., Hamri, G. C. El, El-Baba, M. D., Saxena, P., Ausländer, S., Tan, K. R., & Fussenegger, M. (2018). Designer exosomes produced by implanted cells intracerebrally deliver therapeutic cargo for Parkinson’s disease treatment. Nature Communications, 9(1), 1–10. https://doi.org/10.1038/s41467-018-03733-8

Kouli, A., Torsney, K. M., & Kuan, W. L. (2018). Parkinson’s disease: etiology, neuropathology, and pathogenesis. Parkinson’s Disease: Pathogenesis and Clinical Aspects, 3–26. https://doi.org/10.15586/codonpublications.parkinsonsdisease.2018.ch1

Kummer, K. K., Zeidler, M., Kalpachidou, T., & Kress, M. (2021). Role of IL-6 in the regulation of neuronal development, survival and function. Cytokine, 144, 155582. https://doi.org/10.1016/J.CYTO.2021.155582

L’Episcopo, F., Tirolo, C., Caniglia, S., Testa, N., Serra, P. A., Impagnatiello, F., Morale, M. C., & Marchetti, B. (2010). Combining nitric oxide release with anti-inflammatory activity preserves nigrostriatal dopaminergic innervation and prevents motor impairment in a 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of Parkinson’s disease. Journal of Neuroinflammation, 7, 83. https://doi.org/10.1186/1742-2094-7-83

Lee, E. J., Woo, M. S., Moon, P. G., Baek, M. C., Choi, I. Y., Kim, W. K., Junn, E., & Kim, H. S. (2010). α-Synuclein activates microglia by inducing the expressions of matrix metalloproteinases and the subsequent activation of Protease-Activated receptor-1. Journal of Immunology, 185(1), 615–623. https://doi.org/10.4049/JIMMUNOL.0903480

Lee, S. T., Chu, K., Park, H. K., Jung, K. H., Kim, M., Lee, S. K., & Roh, J. K. (2008). New concept of neural stem cell transplantation: anti-inflammatory role. International Journal of Stem Cells, 1(1), 36–42. https://doi.org/10.15283/IJSC.2008.1.1.36

Leites, E. P., & Morais, V. A. (2021). The PINK1-mediated crosstalk between neural cells and the underlying link to Parkinson’s disease. Cells, 10(6), 1395. https://doi.org/10.3390/CELLS10061395

Leonoudakis, D., Rane, A., Angeli, S., Lithgow, G. J., Andersen, J. K., & Chinta, S. J. (2017). Anti-inflammatory and neuroprotective role of natural product securinine in activated glial cells: implications for Parkinson’s disease. Mediators of Inflammation, 2017, 1–11. https://doi.org/10.1155/2017/8302636

Li, J., Long, X., Hu, J., Bi, J., Zhou, T., Guo, X., Han, C., Huang, J., Wang, T., Xiong, N., & Lin, Z. (2019). Multiple pathways for natural product treatment of Parkinson’s disease: A mini review. Phytomedicine, 60, 152954. https://doi.org/10.1016/j.phymed.2019.152954

Li, Y. H., Yu, J. W., Xi, J. Y., Yu, W. B., Liu, J. C., Wang, Q., Song, L. J., Feng, L., Yan, Y. P., Zhang, G. X., Xiao, B. G., & Ma, C. (2017). fasudil enhances therapeutic efficacy of neural stem cells in the mouse model of MPTP-induced Parkinson’s disease. Molecular Neurobiology, 54(7), 5400–5413. https://doi.org/10.1007/S12035-016-0027-8

Liu, C. Y., Wang, X., Liu, C., & Zhang, H. (2019). Pharmacological targeting of microglial activation: new therapeutic approach. Frontiers in Cellular Neuroscience, 13, 00514. https://doi.org/10.3389/FNCEL.2019.00514

Liu, T., Zhang, L., Joo, D., & Sun, S. C. (2017). NF-κB signaling in inflammation. Signal Transduction and Targeted Therapy, 2(1), 1–9. https://doi.org/10.1038/sigtrans.2017.23

Lương, K., & Nguyễn, L. (2012). Role of Vitamin D in Parkinson’s disease. ISRN Neurology, 2012, 1–11. https://doi.org/10.5402/2012/134289

Lv, Q. K., Tao, K. X., Wang, X. B., Yao, X. Y., Pang, M. Z., Liu, J. Y., Wang, F., & Liu, C. F. (2023). Role of α-synuclein in microglia: autophagy and phagocytosis balance neuroinflammation in Parkinson’s disease. Inflammation Research, 72(3), 443–462. https://doi.org/10.1007/S00011-022-01676-X

Madore, C., Yin, Z., Leibowitz, J., & Butovsky, O. (2020). Microglia, lifestyle stress, and neurodegeneration. Immunity, 52(2), 222–240. https://doi.org/10.1016/J.IMMUNI.2019.12.003

Marques, O., & Outeiro, T. F. (2012). Alpha-synuclein: from secretion to dysfunction and death. Cell Death & Disease, 3, e350. https://doi.org/10.1038/cddis.2012.94

McGeer, P. L., Itagaki, S., Boyes, B. E., & McGeer, E. G. (1988). Reactive microglia are positive for HLA‐DR in the substantia nigra of Parkinson’s and Alzheimer’s disease brains. Neurology, 38(8), 1285. https://doi.org/10.1212/WNL.38.8.1285

Moehle, M. S., & West, A. B. (2015). M1 and M2 immune activation in Parkinson’s disease: foe and ally? Neuroscience, 302, 59–73. https://doi.org/10.1016/J.NEUROSCIENCE.2014.11.018

Moehle, M. S., Webber, P. J., Tse, T., Sukar, N., Standaert, D. G., Desilva, T. M., Cowell, R. M., & West, A. B. (2012). LRRK2 inhibition attenuates microglial inflammatory responses. The Journal of Neuroscience, 32(5), 1602–1611. https://doi.org/10.1523/JNEUROSCI.5601-11.2012

Moghaddam, H. F., Hemmati, A., Nazari, Z., Mehrab, H., Abid, K. M., & Ardestani, M. S. (2007). Effects of aspirin and celecoxib on rigidity in a rat model of Parkinson’s disease. Pakistan Journal of Biological Sciences, 10(21), 3853–3858. https://doi.org/10.3923/PJBS.2007.3853.3858

Nakagawa, Y., & Chiba, K. (2014). Role of microglial M1/M2 polarization in relapse and remission of psychiatric disorders and diseases. Pharmaceuticals, 7(12), 1028–1048. https://doi.org/10.3390/ph7121028

Navarro, A., & Boveris, A. (2009). Brain mitochondrial dysfunction and oxidative damage in Parkinson’s disease. Journal of Bioenergetics and Biomembranes, 41(6), 517–521. https://doi.org/10.1007/S10863-009-9250-6

Noelker, C., Morel, L., Lescot, T., Osterloh, A., Alvarez-Fischer, D., Breloer, M., Henze, C., Depboylu, C., Skrzydelski, D., Michel, P. P., Dodel, R. C., Lu, L., Hirsch, E. C., Hunot, S., & Hartmann, A. (2013). Toll like receptor 4 mediates cell death in a mouse MPTP model of Parkinson disease. Scientific Reports, 3, 1393. https://doi.org/10.1038/SREP01393

Nzogang, P. M., & Donkeng, M. B. (2020). Neuroprotection: the way of anti-inflammatory agents. Neuroprotection - New Approaches and Prospects, 90509. https://doi.org/10.5772/intechopen.90509

Ohtsuka, C., Sasaki, M., Konno, K., Koide, M., Kato, K., Takahashi, J., Takahashi, S., Kudo, K., Yamashita, F., & Terayama, Y. (2013). Changes in substantia nigra and locus coeruleus in patients with early-stage Parkinson’s disease using neuromelanin-sensitive MR imaging. Neuroscience Letters, 541, 93–98. https://doi.org/10.1016/J.NEULET.2013.02.012

Olanow, C. W. (2007). The pathogenesis of cell death in Parkinson’s disease–2007. Movement Disorders, 22(s17), S335–S342. https://doi.org/10.1002/MDS.21675

Omura, T., Sasaoka, M., Hashimoto, G., Imai, S., Yamamoto, J., Sato, Y., Nakagawa, S., Yonezawa, A., Nakagawa, T., Yano, I., Tasaki, Y., & Matsubara, K. (2018). Oxicam-derived non-steroidal anti-inflammatory drugs suppress 1-methyl-4-phenyl pyridinium-induced cell death via repression of endoplasmic reticulum stress response and mitochondrial dysfunction in SH-SY5Y cells. Biochemical and Biophysical Research Communications, 503(4), 2963–2969. https://doi.org/10.1016/J.BBRC.2018.08.078

Orihuela, R., McPherson, C. A., & Harry, G. J. (2015). Microglial M1/M2 polarization and metabolic states. British Journal of Pharmacology, 173(4), 649–665. https://doi.org/10.1111/bph.13139

Park, J. H., Park, Y. S., Lee, J. B., Park, K. H., Paik, M. kyoung, Jeong, M., & Koh, H. C. (2015). Meloxicam inhibits fipronil-induced apoptosis via modulation of the oxidative stress and inflammatory response in SH-SY5Y cells. Journal of Applied Toxicology, 36(1), 10–23. https://doi.org/10.1002/JAT.3136

Poly, T. N., Islam, M. M., Yang, H. C., & Li, Y. C. J. (2019). Non-steroidal anti-inflammatory drugs and risk of Parkinson’s disease in the elderly population: a meta-analysis. European Journal of Clinical Pharmacology, 75(1), 99–108. https://doi.org/10.1007/S00228-018-2561-Y

Polymeropoulos, M. H., Lavedan, C., Leroy, E., Ide, S. E., Dehejia, A., Dutra, A., Pike, B., Root, H., Rubenstein, J., Boyer, R., Stenroos, E. S., Chandrasekharappa, S., Athanassiadou, A., Papapetropoulos, T., Johnson, W. G., Lazzarini, A. M., Duvoisin, R. C., Di Iorio, G., Golbe, L. I., & Nussbaum, R. L. (1997). Mutation in the α-synuclein gene identified in families with Parkinson’s disease. Science, 276(5321), 2045–2047. https://doi.org/10.1126/SCIENCE.276.5321.2045

Prencipe, G., Minnone, G., Strippoli, R., De Pasquale, L., Petrini, S., Caiello, I., Manni, L., De Benedetti, F., & Bracci-Laudiero, L. (2014). Nerve growth factor downregulates inflammatory response in human monocytes through TrkA. The Journal of Immunology, 192(7), 3345–3354. https://doi.org/10.4049/JIMMUNOL.1300825

Rangasamy, S. B., Dasarathi, S., Pahan, P., Jana, M., & Pahan, K. (2019). Low-dose aspirin upregulates tyrosine hydroxylase and increases dopamine production in dopaminergic neurons: Implications for Parkinson’s disease. Journal of Neuroimmune Pharmacology, 14(2), 173–187. https://doi.org/10.1007/S11481-018-9808-3

Rees, K., Stowe, R., Patel, S., Ives, N., Breen, K., Clarke, C. E., & Ben-Shlomo, Y. (2011). Non-steroidal anti-inflammatory drugs as disease-modifying agents for Parkinson’s disease: evidence from observational studies. Cochrane Database of Systematic Reviews, CD008454. https://doi.org/10.1002/14651858.CD008454.PUB2

Ren, L., Yi, J., Yang, J., Li, P., Cheng, X., & Mao, P. (2018). Non-steroidal anti-inflammatory drugs use and risk of Parkinson disease: A dose–response meta-analysis. Medicine, 97(37), e12172. https://doi.org/10.1097/MD.0000000000012172

Ricciardolo, F. L. M., Zaagsma, J., & Meurs, H. (2005). The therapeutic potential of drugs targeting the arginase pathway in asthma. Expert Opinion on Investigational Drugs, 14(10), 1221–1231. https://doi.org/10.1517/13543784.14.10.1221

Rojanathammanee, L., Murphy, E. J., & Combs, C. K. (2011). Expression of mutant alpha-synuclein modulates microglial phenotype in vitro. Journal of Neuroinflammation, 8(1), 1–12. https://doi.org/10.1186/1742-2094-8-44

Romeika, J., Wurzelmann, M., & Sun, D. (2017). TrkB receptor agonist 7,8-dihydroxyflavone and its therapeutic potential for traumatic brain injury. New Therapeutics for Traumatic Brain Injury: Prevention of Secondary Brain Damage and Enhancement of Repair and Regeneration, 225–234. https://doi.org/10.1016/B978-0-12-802686-1.00014-6

Ros-Bernal, F., Hunot, S., Herrero, M. T., Parnadeau, S., Corvol, J. C., Lu, L., Alvarez-Fischer, D., Sauvage, M. A. C. De, Saurini, F., Coussieu, C., Kinugawa, K., Prigent, A., Höglinger, G., Hamon, M., Tronche, F., Hirsch, E. C., & Vyas, S. (2011). Microglial glucocorticoid receptors play a pivotal role in regulating dopaminergic neurodegeneration in parkinsonism. Proceedings of the National Academy of Sciences of the United States of America, 108(16), 6632–6637. https://doi.org/10.1073/PNAS.1017820108

Sadeghian, M., Mullali, G., Pocock, J. M., Piers, T., Roach, A., & Smith, K. J. (2015). Neuroprotection by safinamide in the 6-hydroxydopamine model of Parkinson’s disease. Neuropathology and Applied Neurobiology, 42(5), 423–435. https://doi.org/10.1111/NAN.12263

Saha, S., Buttari, B., Panieri, E., Profumo, E., & Saso, L. (2020). An overview of Nrf2 signaling pathway and its role in inflammation. Molecules, 25(22), 5474. https://doi.org/10.3390/molecules25225474

Saitgareeva, A. R., Bulygin, K. V., Gareev, I. F., Beylerli, O. A., & Akhmadeeva, L. R. (2020). The role of microglia in the development of neurodegeneration. Neurological Sciences, 41(12), 3609–3615. https://doi.org/10.1007/S10072-020-04468-5

Samarpita, S., Kim, J. Y., Rasool, M. K., & Kim, K. S. (2020). Investigation of toll-like receptor (TLR) 4 inhibitor TAK-242 as a new potential anti-rheumatoid arthritis drug. Arthritis Research and Therapy, 22(1), 1–10. https://doi.org/10.1186/S13075-020-2097-2

Samii, A., Etminan, M., Wiens, M. O., & Jafari, S. (2009). NSAID use and the risk of parkinsons disease: Systematic review and meta-analysis of observational studies. Drugs and Aging, 26(9), 769–779. https://doi.org/10.2165/11316780-000000000-00000

Sarbishegi, M., Alhagh, E., & Gorgich, C. (2019). the effects of celecoxib on rotenone-induced rat model of Parkinson’s disease: suppression of neuroinflammation and oxidative stress-mediated apoptosis. Gene, Cell and Tissue, 6(2), 92178. https://doi.org/10.5812/GCT.92178

Schirinzi, T., Martella, G., Imbriani, P., Di Lazzaro, G., Franco, D., Colona, V. L., Alwardat, M., Salimei, P. S., Mercuri, N. B., Pierantozzi, M., & Pisani, A. (2019). Dietary Vitamin E as a protective factor for Parkinson’s disease: clinical and experimental evidence. Frontiers in Neurology, 10, 148. https://doi.org/10.3389/FNEUR.2019.00148

Schönecker, S., Brendel, M., Palleis, C., Beyer, L., Höglinger, G. U., Schuh, E., Rauchmann, B. S., Sauerbeck, J., Rohrer, G., Sonnenfeld, S., Furukawa, K., Ishiki, A., Okamura, N., Bartenstein, P., Dieterich, M., Bötzel, K., Danek, A., Rominger, A., & Levin, J. (2019). PET imaging of astrogliosis and tau facilitates diagnosis of Parkinsonian syndromes. Frontiers in Aging Neuroscience, 11, 249. https://doi.org/10.3389/FNAGI.2019.00249

Shen, J., Xu, S., Zhou, H., Liu, H., Jiang, W., Hao, J., & Hu, Z. (2017a). IL-1β induces apoptosis and autophagy via mitochondria pathway in human degenerative nucleus pulposus cells. Scientific Reports, 7(1), 1–12. https://doi.org/10.1038/srep41067

Shen, Y., Guo, X., Han, C., Wan, F., Ma, K., Guo, S., Wang, L., Xia, Y., Liu, L., Lin, Z., Huang, J., Xiong, N., & Wang, T. (2017b). The implication of neuronimmunoendocrine (NIE) modulatory network in the pathophysiologic process of Parkinson’s disease. Cellular and Molecular Life Sciences, 74(20), 3741–3768. https://doi.org/10.1007/S00018-017-2549-2

Simpson, D. S. A., & Oliver, P. L. (2020). ROS generation in microglia: understanding oxidative stress and inflammation in neurodegenerative disease. Antioxidants, 9(8), 1–27. https://doi.org/10.3390/ANTIOX9080743

Sims, S. K., Wilken-Resman, B., Smith, C. J., Mitchell, A., McGonegal, L., & Sims-Robinson, C. (2022). Brain-derived neurotrophic factor and nerve growth factor therapeutics for brain injury: the current translational challenges in preclinical and clinical research. Neural Plasticity, 2022, 1–15. https://doi.org/10.1155/2022/3889300

Sobhon, P., Savedvanich, G., & Weerakiet, S. (2023a). Oxidative stress, inflammation, dysfunctional redox homeostasis and autophagy cause age-associated diseases. Exploration of Medicine, 4(1), 45–70. https://doi.org/10.37349/EMED.2023.00124

Sobhon, P., Savedvanich, G., & Weerakiet, S. (2023b). Oxidative stress and inflammation: the root causes of aging. Exploration of Medicine, 127–156. https://doi.org/10.37349/emed.2023.00129

Song, N. , Chen, L., & Xie, J. (2021). Alpha-synuclein handling by microglia: activating, combating, and worsening. Neuroscience Bulletin, 37(5), 751–753. https://doi.org/10.1007/S12264-021-00651-6

Song, N., Scholtemeijer, M., & Shah, K. (2020). mesenchymal stem cell immunomodulation: mechanisms and therapeutic potential. Trends in Pharmacological Sciences, 41(9), 653–664. https://doi.org/10.1016/J.TIPS.2020.06.009

Sui, Y., Stanić, D., Tomas, D., Jarrott, B., & Horne, M. K. (2009). Meloxicam reduces lipopolysaccharide-induced degeneration of dopaminergic neurons in the rat substantia nigra pars compacta. Neuroscience Letters, 460(2), 121–125. https://doi.org/10.1016/J.NEULET.2009.05.033

Sun, E., Motolani, A., Campos, L., & Lu, T. (2022). The pivotal role of NF-kB in the pathogenesis and therapeutics of Alzheimer’s disease. International Journal of Molecular Sciences, 23(16), 8972. https://doi.org/10.3390/IJMS23168972

Sun, F., & Liu, F. (2020). Platycodin D inhibits MPP+-induced inflammatory response in BV-2 cells through the TLR4/MyD88/NF-κB signaling pathway. Journal of Receptors and Signal Transduction, 40(5), 479–485. https://doi.org/10.1080/10799893.2020.1767135

Sun, S., Zhang, Q., Li, M., Gao, P., Huang, K., Beejadhursing, R., Jiang, W., Lei, T., Zhu, M., & Shu, K. (2020). gdnf promotes survival and therapeutic efficacy of humanadipose-derived mesenchymal stem cells in a mouse model of Parkinson’s disease. Cell Transplantation, 29, 096368972090851. https://doi.org/10.1177/0963689720908512

Świa̧tkiewicz, M., Zaremba, M., Joniec, I., Czonkowski, A., & Kurkowska-Jastrzêbska, I. (2013). Potential neuroprotective effect of ibuprofen, insights from the mice model of Parkinson’s disease. Pharmacological Reports, 65(5), 1227–1236. https://doi.org/10.1016/S1734-1140(13)71480-4

Tai, W., Ye, X., Bao, X., Zhao, B., Wang, X., & Zhang, D. (2013). Inhibition of Src tyrosine kinase activity by squamosamide derivative FLZ attenuates neuroinflammation in both in vivo and in vitro Parkinson’s disease models. Neuropharmacology, 75, 201–212. https://doi.org/10.1016/j.neuropharm.2013.07.020

Thelin, E. P., Tajsic, T., Zeiler, F. A., Menon, D. K., Hutchinson, P. J. A., Carpenter, K. L. H., Morganti-Kossmann, M. C., & Helmy, A. (2017). Monitoring the neuroinflammatory response following acute brain injury. Frontiers in Neurology, 8, 351. https://doi.org/10.3389/FNEUR.2017.00351

Timmerman, R., Burm, S. M., & Bajramovic, J. J. (2018). An overview of in vitro methods to study microglia. Frontiers in Cellular Neuroscience, 12, 242. https://doi.org/10.3389/FNCEL.2018.00242

Tolosa, E., Garrido, A., Scholz, S. W., & Poewe, W. (2021). Challenges in the diagnosis of Parkinson’s disease. The Lancet Neurology, 20(5), 385–397. https://doi.org/10.1016/S1474-4422(21)00030-2

Troncoso-Escudero, P., Parra, A., Nassif, M., & Vidal, R. L. (2018). Outside in: Unraveling the role of neuroinflammation in the progression of Parkinson’s disease. Frontiers in Neurology, 9(OCT), 860. https://doi.org/10.3389/FNEUR.2018.00860

Trudler, D., Weinreb, O., Mandel, S. A., Youdim, M. B. H., & Frenkel, D. (2014). DJ-1 deficiency triggers microglia sensitivity to dopamine toward a pro-inflammatory phenotype that is attenuated by rasagiline. Journal of Neurochemistry, 129(3), 434–447. https://doi.org/10.1111/JNC.12633

Tsai, S. J., Kuo, W. W., Liu, W. H., & Yin, M. C. (2010). Antioxidative and anti-inflammatory protection from carnosine in the striatum of MPTP-treated mice. Journal of Agricultural and Food Chemistry, 58(21), 11510–11516. https://doi.org/10.1021/JF103258P

Wang, X., Zhang, Y., Zhu, C., Li, G., Kang, J., Chen, F., & Yang, L. (2019). The diagnostic value of SNpc using NM-MRI in Parkinson’s disease: meta-analysis. Neurological Sciences, 40(12), 2479–2489. https://doi.org/10.1007/S10072-019-04014-Y

Wang, Z., Cui, Y., Wen, L., Yu, H., Feng, J., Yuan, W., & He, X. (2022). Dietary restriction against Parkinson’s disease: what we know so far. Nutrients, 14(19), 4108. https://doi.org/10.3390/NU14194108

Wang, Z., Dong, H., Wang, J., Huang, Y., Zhang, X., Tang, Y., Li, Q., Liu, Z., Ma, Y., Tong, J., Huang, L., Fei, J., Yu, M., Wang, J., & Huang, F. (2020). Pro-survival and anti-inflammatory roles of NF-κB c-Rel in the Parkinson’s disease models. Redox Biology, 30, 101427. https://doi.org/10.1016/J.REDOX.2020.101427

Won, S., Ko, J. H., Jeon, H., Park, S. S., & Kim, S. N. (2021). Co-administration of gagam-sipjeondaebo-tang and ibuprofen alleviates the inflammatory response in MPTP-induced Parkinson’s disease mouse model and RAW264.7 Macrophages. Pathogens, 10(3), 1–15. https://doi.org/10.3390/PATHOGENS10030268

Xiao, L., Wei, F., Zhou, Y., Anderson, G. J., Frazer, D. M., Lim, Y. C., Liu, T., & Xiao, Y. (2020). Dihydrolipoic acid-gold nanoclusters regulate microglial polarization and have the potential to alter neurogenesis. Nano Letters, 20(1), 478–495. https://doi.org/10.1021/ACS.NANOLETT.9B04216

Xu, D., Lian, D., Wu, J., Liu, Y., Zhu, M., Sun, J., He, D., & Li, L. (2017). Brain-derived neurotrophic factor reduces inflammation and hippocampal apoptosis in experimental Streptococcus pneumoniae meningitis. Journal of Neuroinflammation, 14(1), 1–13. https://doi.org/10.1186/S12974-017-0930-6

Yacoubian, T. A., & Standaert, D. G. (2009). Targets for neuroprotection in Parkinson’s disease. Biochimica et Biophysica Acta, 1792(7), 676–687. https://doi.org/10.1016/J.BBADIS.2008.09.009

Yamazaki, T., Muramoto, M., Oe, T., Morikawa, N., Okitsu, O., Nagashima, T., Nishimura, S., Katayama, Y., & Kita, Y. (2006). Diclofenac, a non-steroidal anti-inflammatory drug, suppresses apoptosis induced by endoplasmic reticulum stresses by inhibiting caspase signaling. Neuropharmacology, 50(5), 558–567. https://doi.org/10.1016/J.NEUROPHARM.2005.10.016

Zaragozá, R. (2020). Transport of amino acids across the blood-brain barrier. Frontiers in Physiology, 11, 973. https://doi.org/10.3389/fphys.2020.00973

Zhang, H., Bai, L., He, J., Zhong, L., Duan, X., Ouyang, L., Zhu, Y., Wang, T., Zhang, Y., & Shi, J. (2017). Recent advances in discovery and development of natural products as source for anti-Parkinson’s disease lead compounds. European Journal of Medicinal Chemistry, 141, 257–272. https://doi.org/10.1016/j.ejmech.2017.09.068

Zhang, L. F., Yu, X. L., Ji, M., Liu, S. Y., Wu, X. L., Wang, Y. J., & Liu, R. T. (2018). Resveratrol alleviates motor and cognitive deficits and neuropathology in the A53T α-synuclein mouse model of Parkinson’s disease. Food & Function, 9(12), 6414–6426. https://doi.org/10.1039/C8FO00964C

Zhang, W., Tian, T., Gong, S. X., Huang, W. Q., Zhou, Q. Y., Wang, A. P., & Tian, Y. (2021a). Microglia-associated neuroinflammation is a potential therapeutic target for ischemic stroke. Neural Regeneration Research, 16(1), 6–11. https://doi.org/10.4103/1673-5374.286954

Zhang, Z. D., Yang, Y. J., Qin, Z., Liu, X. W., Li, S. H., Bai, L. X., & Li, J. Y. (2021b). Protective activity of aspirin eugenol ester on paraquat-induced cell damage in SH-SY5Y cells. Oxidative Medicine and Cellular Longevity, 2021, 1–17. https://doi.org/10.1155/2021/6697872

Zheng, T., & Zhang, Z. (2021). Activated microglia facilitate the transmission of α-synuclein in Parkinson’s disease. Neurochemistry International, 148, 105094. https://doi.org/10.1016/J.NEUINT.2021.105094

Zhou, P., Weng, R., Chen, Z., Wang, R., Zou, J., Liu, X., Liao, J., Wang, Y., Xia, Y., & Wang, Q. (2016). TLR4 signaling in MPP+-induced activation of BV-2 cells. Neural Plasticity, 2016, 1–9. https://doi.org/10.1155/2016/5076740

Zhu, F. D., Hu, Y. J., Yu, L., Zhou, X. G., Wu, J. M., Tang, Y., Qin, D. L., Fan, Q. Z., & Wu, A. G. (2021). Nanoparticles: a hope for the treatment of inflammation in CNS. Frontiers in Pharmacology, 12, 683935. https://doi.org/10.3389/FPHAR.2021.683935

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2024-03-17

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Rungruang, P., Sansri, V. and Sroyraya, M. (2024) “Neuroinflammation-induced neurodegeneration and associated microglia activation in Parkinson’s disease: a novel neurotherapeutic avenue”, Neuroscience Research Notes, 7(1), pp. 271.1–271.21. doi: 10.31117/neuroscirn.v7i1.271.