The role of the renin-angiotensin system in the pathogenesis of Parkinson’s disease
Keywords:
renin-angiotensin system, dopamine, oxidative stress, Parkinson's disease.
Abstract
Background. A large amount of literature on Parkinson’s disease is currently available. However, the role of the renin-angiotensin system in the pathogenesis of this disease is not sufficiently covered. Aim. To highlight new therapeutic possibilities based on pathophysiological mechanisms of Parkinson’s disease. Methods. The literature retrieved from the PubMed, Medline, and eLibrary databases focusing on the role of the renin-angiotensin system in the pathogenesis of Parkinson’s disease was analyzed. Results. Parkinson’s disease (PD) is a chronic neurodegenerative disease associated with persistent neurological disorders. Studies have demonstrated that a local renin-angiotensin system (RAS) exists in many tissues and organs along with the systemic RAS. The authors showed that dopamine and angiotensin II interact reciprocally in the substantia nigra (SN) and striatum. In animal models, a decrease in the dopamine level was accompanied by RAS overactivation. Furthermore, microglial tissue induced production of reactive oxygen species, which was associated with neuroinflammation. The angiotensin receptor blocker treatment used in animal models and clinical trials significantly reduced the progression of SN neurodegeneration. Conclusions. The authors reviewed the data of literature demonstrating that the progression of Parkinson’s disease is associated with overactivation of the cerebral RAS. Apparently, it is possible to influence therapeutically this new pathogenetic component of Parkinson’s disease. Further study is required for understanding the mechanisms of this process.
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References
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24. Gorjajnov S.A., Prockij S.V., Ohotin V.E., Pavlova G.V., Revishhin A.V., Potapov A.A. Role of astroglia of brain in norm and pathology. Annaly v nevrologii. 2013; 7 (1): 45–51.
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29. Zeng C., Liu Y., Wang Z, et al. Activation of D3 dopamine receptor decreases angiotensin II type 1 receptor expression in rat renal proximal tubule cells. Circ Res. 2006; 99: 494–500.
30. Villar-Cheda B., Rodrıguez-Pallares J., Munoz A., et al. Nigral and ~ striatal regulation of angiotensin receptor expression by dopamine and angiotensin in rodents: implications for progression of Parkinson’s disease. Eur J Neurosci. 2010; 32: 1695–1706.
31. Rodriguez-Pallares J., Rey P., Parga J.A., Munoz A., Guerra MJ, ~ Labandeira-Garcia J.L. Brain angiotensin enhances dopaminergic cell death via microglial activation and NADPH-derived ROS. Neurobiol Dis. 2008; 31: 58–73.
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2. Arnold A.C., Okamoto L.E., Gamboa A/, et al. Mineralocorticoid Receptor Activation Contributes to the Supine Hypertension of Autonomic Failure. Hypertension. 2016; 67: 424–9.
3. Labandeira-García J.L., Garrido-Gil P., Rodriguez-Pallares J., Valenzuela R., Borrajo A., Rodríguez-Perez A.I. Brain renin-angiotensin system and dopaminergic cell vulnerability. Front Neuroanat. 2014; 8;8:67.
4. Perez-Lloret S., Sampaio C., Rascol O. Disease-modifying strategies in Parkinson's Disease. In: Jankovik J., Tolosa E., editors. Parkinson's Disease and Movement Disorders. Philadelphia, PA: Wolters Kluwer; 2015.
5. Kalia L.V., Lang A.E. Parkinson disease in 2015: Evolving basic, pathological andclinical concepts in PD. Nat Rev Neurol. 2016; 12: 65-6.
6. Levin O.S., Fedorova N.V. Parkinson’s disease. M.: 2006. 265 p.
7. Bykov Ju.N., Bender T.V. Medication methods of treatment in patients with parkinson’s disease (review of literature). Bjulleten' Vostochno-Sibirskogo nauchnogo centra Sibirskogo otdelenija Rossijskoj akademii medicinskih nauk. 2016; 1 (3): 65–71.
8. Kaljagin A.N. Using of inhibitors of angiotensin-reverting enzyme and antagonists of AT1-receptors of angiotensin. // Sibirskij medicinskij zhurnal (Irkutsk). 2007; 73 (6): 98-103.
9. Honig, L.S., Boyd, C.D., Treatment of Alzheimer’s disease: current management and experimental therapeutics. Curr. Transl. Geniatr. Exp. Gerontol. Rep. 2013; 2: 174–181.
10. Farag E., Sessler D.I., Ebrahim Z., Kurz A., Morgan J., Ahuja S., Maheshwari K., John Doyle D. The renin angiotensin system and the brain: New developments. J Clin Neurosci. 2017; 46: 1-8.
11. O'Connor A.T., Clark M.A. Astrocytes and the Renin Angiotensin System: Relevance in Disease Pathogenesis. Neurochem Res. 2018; 43(7): 1297-1307.
12. Marc Y., Llorens-Cortes C. The role of the brain renin-angiotensin system in hypertension: implications for new treatment. Prog Neurobiol. 2011; 95 (2): 89-103.
13. Bodiga V.L.; Bodiga S. Renin angiotensin system in cognitive function and dementia. Asian J. Neurosci. 2013; 102602.
14. Gironacci M.M, Vicario A., Cerezo G., Silva M.G. The depressor axis of the renin-angiotensin system and brain disorders: a translational approach. Clinical Science. 2018; 132: 1021–1038.
15. Karamyan V.T., Arsenault J., Escher E., et al. Preliminary biochemical characterization of the novel, non-AT1, non-AT2 angiotensin binding site from the rat brain. Endocrine. 2010; 37: 442-8.
16. Tetzner A., Gebolys K., Meinert C., Klein S., Uhlich, A., Trebicka J., Villacanas O., Walther T. G-protein-coupled receptor MrgD is a receptor for angiotensin-(1–7) involving adenylyl cyclase, cAMP, and phosphokinase A. Hypertension 2016; 68, 185–194.
17. Costa-Besada M.A., Valenzuela R., Garrido-Gil P., Villar-Cheda B., Parga J.A., Lanciego J.L.; Labandeira-Garcia J.L. Paracrine and intracrine angiotensin 1–7/Mas receptor axis in the substantia nigra of rodents, monkeys, and humans. Mol Neurobiol. 2018; 55 (7): 5847-5867.
18. Royea J., Zhang L., Tong X.K. Hamel E. Angiotensin IV receptors mediate the cognitive and cerebrovascular benefits of losartan in a mouse model of Alzheimer’s disease. J. Neurosci. 2017; 37: 5562–5573.
19. Zawada W.M., Mrak R.E., Biedermann J., Palmer Q.D., Gentleman S.M., Aboud O., Griffin W.S. Loss of angiotensin II receptor expression in dopamine neurons in Parkinson’s disease correlates with pathological progression and is accompanied by increases in Nox4- and 8-OH guanosine-related nucleic acid oxidation and caspase-3 activation. Acta Neuropathol. Commun. 2015; 3: 9.
20. Valenzuela R., Costa-Besada M.A.; Iglesias-Gonzalez J., Perez-Costas, E., Villar-Cheda B., Garrido-Gil P.; Melendez-Ferro M., Soto-Otero R., Lanciego J.L., Henrion, D., et al. Mitochondrial angiotensin receptors in dopaminergic neurons. Role in cell protection and aging-related vulnerability to neurodegeneration. Cell Death Dis. 2016; 7: e2427.
21. Villar-Cheda B., Costa-Besada M.A., Valenzuela R., Perez-Costas E., Melendez-Ferro M., Labandeira-Garcia J.L. The intracellular angiotensin system buffers deleterious effects of the extracellular paracrine system. Cell Death Dis. 2017; 8: e3044.
22. Mertens B., Vanderheyden P., Michotte Y., Sarre S. The role of the central renin-angiotensin system in Parkinson's disease. J Renin Angiotensin Aldosterone Syst. 2010; 11 (1): 49-56.
23. John W. Wright., Leen H. Kawas and Joseph W. Harding. A role for the brain RAS in Alzheimer ’s and Parkinson’s diseases. Front Endocrinol (Lausanne). 2013; 25. 4: 158.
24. Gorjajnov S.A., Prockij S.V., Ohotin V.E., Pavlova G.V., Revishhin A.V., Potapov A.A. Role of astroglia of brain in norm and pathology. Annaly v nevrologii. 2013; 7 (1): 45–51.
25. Arroja M.M., Reid E., McCabe C. Therapeutic potential of the renin angiotensin system in ischaemic stroke. Exp. Transl. Stroke Med. 2016; 8: 8.
26. Labandeira-Garcia J.L., Rodríguez-Perez A.I., Garrido-Gil P., Rodriguez-Pallares J., Lanciego J.L., Guerra M.J. Brain Renin-Angiotensin System and Microglial Polarization: Implications for Aging and Neurodegeneration. Front Aging Neurosci. 2017; 3; 9: 129.
27. Garrido-Gil P., Valenzuela, R., Villar-Cheda B., Lanciego J.L., Labandeira-Garcia J.L. Expression of angiotensinogen and receptors for angiotensin and prorenin in the monkey and human substantia nigra: An intracellular renin-angiotensin system in the nigra. Brain Struct. Funct. 2013; 218: 373–388.
28. Gildea J.J. Dopamine and angiotensin as renal counterregulatory systems controlling sodium balance. Curr Opin Nephrol Hypertens. 2009; 18: 28–32.
29. Zeng C., Liu Y., Wang Z, et al. Activation of D3 dopamine receptor decreases angiotensin II type 1 receptor expression in rat renal proximal tubule cells. Circ Res. 2006; 99: 494–500.
30. Villar-Cheda B., Rodrıguez-Pallares J., Munoz A., et al. Nigral and ~ striatal regulation of angiotensin receptor expression by dopamine and angiotensin in rodents: implications for progression of Parkinson’s disease. Eur J Neurosci. 2010; 32: 1695–1706.
31. Rodriguez-Pallares J., Rey P., Parga J.A., Munoz A., Guerra MJ, ~ Labandeira-Garcia J.L. Brain angiotensin enhances dopaminergic cell death via microglial activation and NADPH-derived ROS. Neurobiol Dis. 2008; 31: 58–73.
32. Joglar B., Rodriguez-Pallares J., Rodrıguez-Perez A.I., Rey P., Guerra M.J., Labandeira-Garcia J.L. The inflammatory response in the MPTP model of Parkinson’s disease is mediated by brain angiotensin: relevance to progression of the disease. J Neurochem. 2009; 109: 656–669. 42.
33. Garrido-Gil P., Valenzuela R., Villar-Cheda B., Lanciego J.L., Labandeira-Garcia JL. Expression of angiotensinogen and receptors for angiotensin and prorenin in the monkey and human substantia nigra: an intracellular renin-angiotensin system in the nigra. Brain Struct Funct. 2013; 218: 373–388.
34. Rodriguez-Pallares J., Quiroz C.R., Parga J.A., Guerra M.J., Labandeira-Garcia J.L. Angiotensin II increases differentiation of dopaminergic neurons from mesencephalic precursors via angiotensin type 2 receptors. Eur J Neurosci. 2004; 20: 1489–1498.
35. Miyazaki I., Asanuma M., Diaz-Corrales F.J., Miyoshi K., Ogawa N. Direct evidence for expression of dopamine receptors in astrocytes from basal ganglia. Brain Res. 2004; 1029: 120–123.
36. Farber K., Pannasch U., Kettenmann H. Dopamine and noradrenaline control distinct functions in rodent microglial cells. Mol Cell Neurosci. 2005; 29: 128–138.
37. Joglar B., Rodriguez-Pallares J., Rodrıguez-Perez A.I, Rey P., Guerra M.J., Labandeira-Garcia J.L. The inflammatory response in the MPTP model of Parkinson’s disease is mediated by brain angiotensin: relevance to progression of the disease. J Neurochem. 2009; 109: 656–669.
38. Gao H.M., Liu B., Zhang W., Hong J.S. Critical role of microglial NADPH oxidase-derived free radicals in the in vitro MPTP model of Parkinson’s disease. FASEB J. 2003; 17: 1954–1956. 61.
39. Wu D., Teisman P., Tieu K., et al. NADPH oxidase mediates oxidative stress in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of Parkinson’s disease. Proc Natl Acad Sci USA. 2003; 100: 6145–6150.
40. Doughan A.K., Harrison D.G., Dikalov S.I. Molecular mechanisms of angiotensin II-mediated mitochondrial dysfunction: linking mitochondrial oxidative damage and vascular endothelial dysfunction. Circ Res. 2008; 102: 488–496. 63.
41. Bocharov E.V., Kucherjanu V.G., Ol'ga A.B. Functional edges of DOPA-system and cancer (Part 1) // Patologicheskaja fiziologija i jeksperimental'naja terapija. 2017. T. 61. № 3. S. 116-126.
42. Wosniak J. Jr., Santos C.X., Kowaltowski A.J., Laurindo F.R. Crosstalk between mitochondria and NADPH oxidase: effects of mild mitochondrial dysfunction on angiotensin II-mediated increase in Nox isoform expression and activity in vascular smooth muscle cells. Antioxid Redox Signal. 2009; 11: 1265–1278.
43. Zawada W.M., Banninger G.P., Thornton J., et al. Generation of reactive oxygen species in 1-methyl-4-phenylpyridinium (MPP1) treated dopaminergic neurons occurs as an NADPH oxidasedependent two-wave cascade. J Neuroinflammation. 2011; 8: 129. 65.
44. Rodriguez-Pallares J., Parga J.A., Joglar B., Guerra M.J., LabandeiraGarcia J.L. The mitochondrial ATP-sensitive potassium channel blocker 5-hydroxydecanoate inhibits toxicity of 6-hydroxydopamine on dopaminergic neurons. Neurotox Res. 2009; 15: 82–95.
45. Rodriguez-Pallares J., Parga J.A., Joglar B., Guerra M.J., LabandeiraGarcia JL. Mitochondrial ATP-sensitive potassium channels enhance angiotensin-induced oxidative damage and dopaminergic neuron degeneration. Relevance for aging-associated susceptibility to Parkinson’s disease. Age (Dordr). 2012; 34: 863–880.
46. Qin L., Liu Y., Wang T., et al. NADPH oxidase mediates lipopolysaccharide-induced neurotoxicity and proinflammatory gene expression in activated microglia. J Biol Chem. 2004; 279: 1415–1421.
47. Lopez-Real A., Rey P., Soto-Otero R., Mendez-Alvarez E., Labandeira-Garcia JL. Angiotensin-converting enzyme inhibitors reduce oxidative stress and protect dopaminergic neurons in a 6- hydroxydopamine rat model of parkinsonism. J Neurosci Res. 2005; 81: 865–873.
48. Munoz A., Rey P., Guerra M.J., Mendez-Alvarez E., Soto-Otero R., ~ Labandeira-Garcia J.L. Reduction of dopaminergic degeneration and oxidative stress by inhibition of angiotensin converting enzyme in a MPTP model of parkinsonism. Neuropharmacology. 2006; 51: 112–120.
49. Lu J., Wu L., Jiang T., et al. Angiotensin AT2 receptor stimulation inhibits activation of NADPH oxidase and ameliorates oxidative stress in rotenone model of Parkinson's disease in CATH.a cells. Neurotoxicol Teratol. 2015; 47: 16- 24.
50. Gironacci M.M., Cerniello F.M., Longo Carbajosa N.A., Goldstein J., Cerrato B.D. Protective axis of the renin–angiotensin system in the brain. Clinical Science. 2014. 127, 295–306.
51. Wu L., Tian Y.Y., Shi J.P., et al. Inhibition of endoplasmic reticulum stress is involved in the neuroprotective effects of candesartan cilexitil in the rotenone rat model of Parkinson's disease. Neurosci Lett. 2013; 548: 50-55.
52. Garrido-Gil P., Joglar B., Rodriguez-Perez A.I., Guerra M.J., Labandeira-Garcia JL. Involvement of PPAR-gin the neuroprotective and anti-inflammatory effects of angiotensin type 1 receptor inhibition: effects of the receptor antagonist telmisartan and receptor deletion in a mouse MPTP model of Parkinson’s disease. J Neuroinflammation. 2012; 9: 38.
53. Villar-Cheda B., Dominguez-Meijide A., Joglar B., Rodriguez-Perez A.I., Guerra M.J., Labandeira-Garcia J.L. Involvement of microglial RhoA/Rho-Kinase pathway activation in the dopaminergic neuron death. Role of angiotensin via angiotensin type 1 receptors. Neurobiol Dis. 2012; 47: 268–279.
54. Zawada W.M., Banninger G.P., Thornton J., et al. Generation of reactive oxygen species in 1-methyl-4-phenylpyridinium (MPP1) treated dopaminergic neurons occurs as an NADPH oxidasedependent two-wave cascade. J Neuroinflammation. 2011; 8: 129.
55. Grammatopoulos T.N., Jones S.M., Ahmadi F.A., et al. Angiotensin type 1 receptor antagonist losartan, reduces MPTP-induced degeneration of dopaminergic neurons in substantia nigra. Mol Neurodegener. 2007; 2: 1.
56. Juan M. Saavedra. Angiotensin II AT1 receptor blockers as treatments for inflammatory brain disorders. 2012. Clin Sci (Lond). 2012; 123 (10): 567-90.
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Published
2021-03-14
How to Cite
Bykov Y., Tetyushkin N., Chipizubov V., Kalyagin A., Lavrick S. The role of the renin-angiotensin system in the pathogenesis of Parkinson’s disease // Patologicheskaya Fiziologiya i Eksperimental’naya Terapiya (Pathological physiology and experimental therapy). 2021. VOL. 65. № 1. PP. 107–115.
Issue
Section
Reviews
