Dopamine-Angiotensin interactions in the basal ganglia and their relevance for Parkinson's disease

Movement Disorders

Volumn 28, Issue 10, 2013, Pages 1337-1342

  Labandeira Garcia, Jose L ^a,b   Rodriguez Pallares, Jannette ^a,b   Dominguez Meijide, Antonio ^a,b   Valenzuela, Rita ^a,b   Villar Cheda, Begoña ^a,b   Rodríguez Perez, Ana I ^a,b  

^a UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

Author keywords

Aging; Angiotensin; Degenerative disease; Dopamine; Neurodegeneration; Neuroinflammation; Oxidative stress; Parkinson's; Renin angiotensin system

Indexed keywords

ANGIOTENSIN; DOPAMINE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

BASAL GANGLION; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; DOPAMINERGIC SYSTEM; HORMONE RECEPTOR INTERACTION; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PRIORITY JOURNAL; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REVIEW; SUBSTANTIA NIGRA;

AGING; ANGIOTENSIN; DEGENERATIVE DISEASE; DOPAMINE; NEURODEGENERATION; NEUROINFLAMMATION; OXIDATIVE STRESS; PARKINSON'S; RENIN-ANGIOTENSIN SYSTEM;

ANGIOTENSINS; BASAL GANGLIA; BRAIN; DATA INTERPRETATION, STATISTICAL; DOPAMINE; HUMANS; NEOSTRIATUM; PARACRINE COMMUNICATION; PARKINSON DISEASE; RENIN-ANGIOTENSIN SYSTEM; SUBSTANTIA NIGRA;

EID: 84884705811     PISSN: 08853185     EISSN: 15318257     Source Type: Journal    
DOI: 10.1002/mds.25614     Document Type: Review

References (94)

1. Lev-Ran A, Porta M. Salt and hypertension: a phylogenetic perspective. Diabetes Metab Res Rev. 2005;21:118-31.
2. Ganong WF. Origin of the angiotensin II secreted by cells. Proc Soc Exp Biol Med. 1994;205:213-219.
3. Re RN. Tissue renin angiotensin systems. Med Clin North Am. 2004;88:19-38.
4. Baker KM, Chernin MI, Schreiber T, et al. Evidence of a novel intracrine mechanism in angiotensin II-induced cardiac hypertrophy. Regul Pept. 2004;120:5-13.
5. Kumar R, Singh VP, Baker KM. The intracellular renin-angiotensin system: a new paradigm. Trends Endocrinol Metab. 2007;18:208-214.
6. Kumar R, Singh VP, Baker KM. The intracellular renin-angiotensin system in the heart. Curr Hypertens Rep. 2009;11:104-10.
7. Unger T, Chung O, Csikos T, et al. Angiotensin receptors. J Hypertens. 1996;14(Suppl. 5):S95-S103.
8. Oro C, Qian H, Thomas WG. Type 1 angiotensin receptor pharmacology: signaling beyond G proteins. Pharmacol Ther. 2007;113:210-226.
9. Jones ES, Vinh A, McCarthy CA, Gaspari TA, Widdop RE. AT2 receptors: functional relevance in cardiovascular disease. Pharmacol Ther. 2008;120:292-316.
10. Chabrashvili T, Kitiyakara C, Blau J, et al. Effect of Ang II type 1 and 2 receptors on oxidative stress, renal NAD(P)H oxidase, and SOD expression. Am J Physiol Regu Integr Comp Physiol. 2003;285:R117-R124.
11. Jones ES, Vinh A, McCarthy CA, Gaspari TA, Widdop RE. AT2 receptors: functional relevance in cardiovascular disease. Pharmacol Ther. 2008;120:292-316.
12. Wright JW, Harding JW. The brain renin-angiotensin system: a diversity of functions and implications for CNS diseases. Pflugers Arch. 2013;465:133-51.
13. Cuadra AE, Shan Z, Sumners C, Raizada MK. A current view of brain renin-angiotensin system: is the (pro)renin receptor the missing link? Pharmacol Ther. 2010;125:27-38.
14. von Bohlen und Halbach O, Albrecht D. The CNS renin-angiotensin system. Cell Tissue Res. 2006;326:599-616.
15. Phillips MI, de Oliveira EM. Brain renin angiotensin in disease. J Mol Med. 2008;86:715-722.
16. Harding JW, Sullivan MJ, Hanesworth JM, Cushing LL, Wright JW. Inability of [125I.Sar1, Ile8-angiotensin II to move between the blood and cerebrospinal fluid compartments. J Neurochem. 1988;50:554-557.
17. Stornetta RL, Hawelu-Johnson CL, Guyenet PG, Lynch KR. Astrocytes synthesize angiotensinogen in brain. Science. 1988;242:1444-1446.
18. Milsted A, Barna BP, Ransohoff RM, Brosnihan KB, Ferrario CM. Astrocyte cultures derived from human brain tissue express angiotensinogen mRNA. Proc Natl Acad Sci U S A. 1990;87:5720-5723.
19. Kumar A, Rassoli A, Raizada MK. Angiotensinogen gene expression in neuronal and glial cells in primary cultures of rat brain. J Neurosci Res. 1988;19:287-290.
20. Thomas WG, Greenland KJ, Shinkel TA, Sernia C. Angiotensinogen is secreted by pure rat neuronal cell cultures. Brain Res. 1992;588:191-200.
21. Hoogwerf BJ. Renin-angiotensin system blockade and cardiovascular and renal protection. Am J Cardiol. 2010;105(1 Suppl):30A-35A.
22. Zalba G, San Jose G, Moreno MU, et al. Oxidative stress in arterial hypertension. Role of NADPH oxidase. Hypertension. 2001;38:1395-1399.
23. Babior BM. NADPH oxidase: an update. Blood. 1999;93:1464-1476.
24. Babior BM. NADPH oxidase. Curr Opin Immunol. 2004;16:42-47.
25. Cai H. NAD(P)H oxidase-dependent self-propagation of hydrogen peroxide and vascular disease. Circ Res. 2005;96:818-22.
26. Griendling KK, Sorescu D, Ushio-Fukai M. NADPH oxidase. Role in cardiovascular biology and disease. Circ Res. 2000;86:494-501.
27. Münzel T, Keany JF. Are ACE inhibitors a "magic bullet" against oxidative stress? Circulation. 2001;104:1571-1577.
28. Platten M, Youssef S, Hur EM, et al. Blocking angiotensin-converting enzyme induces potent regulatory T cells and modulates TH1- and TH17-mediated autoimmunity. Proc Natl Acad Sci U S A. 2009;106:14948-14953.
29. Stegbauer J, Lee DH, Seubert S, et al. Role of the renin-angiotensin system in autoimmune inflammation of the central nervous system. Proc Natl Acad Sci U S A. 2009;106:14942-14947.
30. Kehoe PG, Wilcock GK. Is inhibition of the renin-angiotensin system a new treatment option for Alzheimer's disease? Lancet Neurol. 2007;6:373-378.
31. Mogi M, Horiuchi M. Effects of angiotensin II receptor blockers on dementia. Hypertens Res. 2009;32:738-40.
32. Lou M, Blume A, Zhao Y, et al. Sustained blockade of brain AT1 receptors before and after focal cerebral ischemia alleviates neurologic deficits and reduces neuronal injury, apoptosis, and inflammatory responses in the rat. J Cereb Blood Flow Metab. 2004;24:536-547.
33. Iwanami J, Mogi M, Tsukuda K, et al. Low dose of telmisartan prevents ischemic brain damage with peroxisome proliferator-activated receptor-gamma activation in diabetic mice. J Hypertens. 2010;28:1730-1737.
34. Allen AM, MacGregor DP, Chai SY, et al. Angiotensin II receptor binding associated with nigrostriatal dopaminergic neurons in human basal ganglia. Ann Neurol. 1992;32:339-344.
35. Simonnet G, Giorguieff-Chesselet MF, Carayon A, et al. Angiotensin II and the nigrostriatal system. J Physiol. 1981;77:71-79.
36. Quinlan JT, Phillips MI. Immunoreactivity for angiotensin II-like peptide in the human brain. Brain Res. 1981;205:212-218.
37. Brownfield MS, Reid IA, Ganten D, Ganong WF. Differential distribution of immunoreactive angiotensin and angiotensin-converting enzyme in rat brain. Neuroscience. 1982;7:1759-1769.
38. Chai SY, Mendelsohn FAO, Paxinos G. Angiotensin converting enzyme in rat brain visualized by quantitative in vitro autoradiography. Neuroscience. 1987;20:615-627.
39. Valenzuela R, Barroso-Chinea P, Muñoz A, et al. Location of prorenin receptors in primate substantia nigra: effects on dopaminergic cell death. J Neuropathol Exp Neurol. 2010;69:1130-1142.
40. Rodriguez-Pallares J, Rey P, Parga JA, Muñoz A, Guerra MJ, Labandeira-Garcia JL. Brain angiotensin enhances dopaminergic cell death via microglial activation and NADPH-derived ROS. Neurobiol Dis. 2008;31:58-73.
41. Joglar B, Rodriguez-Pallares J, Rodríguez-Perez AI, Rey P, Guerra MJ, Labandeira-Garcia JL. 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. Garrido-Gil P, Valenzuela R, Villar-Cheda B, Lanciego JL, 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.
43. Rodriguez-Pallares J, Quiroz CR, Parga JA, Guerra MJ, Labandeira-Garcia JL. Angiotensin II increases differentiation of dopaminergic neurons from mesencephalic precursors via angiotensin type 2 receptors. Eur J Neurosci. 2004;20:1489-1498.
44. Rodriguez-Pallares J, Parga JA, Muñoz A, Rey P, Guerra MJ, Labandeira-Garcia JL. Mechanism of 6-hydroxydopamine neurotoxicity: the role of NADPH oxidase and microglial activation in 6-hydroxydopamine-induced degeneration of dopaminergic neurons. J Neurochem. 2007;103:145-156.
45. Khan F, Spicarová Z, Zelenin S, Holtbäck U, Scott L, Aperia A. Negative reciprocity between angiotensin II type 1 and dopamine D1 receptors in rat renal proximal tubule cells. Am J Physiol Renal Physiol. 2008;295:F1110-F1116.
46. Gildea JJ. Dopamine and angiotensin as renal counterregulatory systems controlling sodium balance. Curr Opin Nephrol Hypertens. 2009;18:28-32.
47. 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.
48. Padia SH, Kemp BA, Howell NL, Keller SR, Gildea JJ, Carey RM. Mechanisms of dopamine D(1) and angiotensin type 2 receptor interaction in natriuresis. Hypertension. 2012;59:437-445.
49. Villar-Cheda B, Rodríguez-Pallares J, Muñoz 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.
50. Miyazaki I, Asanuma M, Diaz-Corrales FJ, Miyoshi K, Ogawa N. Direct evidence for expression of dopamine receptors in astrocytes from basal ganglia. Brain Res. 2004;1029:120-123.
51. Färber K, Pannasch U, Kettenmann H. Dopamine and noradrenaline control distinct functions in rodent microglial cells. Mol Cell Neurosci. 2005;29:128-138.
52. Zeng C, Luo Y, Asico LD, et al. Perturbation of D1 dopamine and AT1 receptor interaction in spontaneously hypertensive rats. Hypertension. 2003;42:787-792.
53. Bek MJ, Wang X, Asico LD, et al. Angiotensin-II type 1 receptor-mediated hypertension in D4 dopamine receptor-deficient mice. Hypertension. 2006;47:288-295.
54. Yang S, Yao B, Zhou Y, Yin H, Zhang MZ, Harris RC. Intrarenal dopamine modulates progressive angiotensin II-mediated renal injury. Am J Physiol Renal Physiol. 2012;302:F742-749.
55. Ruiz-Ortega M, Lorenzo O, Ruperez M, Suzuki Y, Egido J. Proinflammatory actions of angiotensin II. Curr Opin Nephrol Hypertens. 2001;10:321-329.
56. Suzuki Y, Ruiz-Ortega M, Lorenzo O, Ruperez M, Esteban V, Egido J. Inflammation and angiotensin II. Int J Biochem Cell Biol. 2003;35:881-900.
57. Okamura A, Rakugi H, Ohishi M, et al. Upregulation of renin-angiotensin system during differentiation of monocytes to macrophages. J Hypertens. 1999;17:537-545.
58. Yanagitani Y, Rakugi H, Okamura A, et al. Angiotensin II type 1 receptor-mediated peroxide production in human macrophages. Hypertension. 1999;33:335-339.
59. 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.
60. Gao HM, Liu B, Zhang W, Hong JS. 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. 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 U S A. 2003;100:6145-6150.
62. Doughan AK, Harrison DG, Dikalov SI. Molecular mechanisms of angiotensin II-mediated mitochondrial dysfunction: linking mitochondrial oxidative damage and vascular endothelial dysfunction. Circ Res. 2008;102:488-496.
63. Wosniak J Jr, Santos CX, Kowaltowski AJ, Laurindo FR. Cross-talk 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.
64. Zawada WM, Banninger GP, Thornton J, et al. Generation of reactive oxygen species in 1-methyl-4-phenylpyridinium (MPP+) treated dopaminergic neurons occurs as an NADPH oxidase-dependent two-wave cascade. J Neuroinflammation. 2011;8:129.
65. Rodriguez-Pallares J, Parga JA, Joglar B, Guerra MJ, Labandeira-Garcia JL. The mitochondrial ATP-sensitive potassium channel blocker 5-hydroxydecanoate inhibits toxicity of 6-hydroxydopamine on dopaminergic neurons. Neurotox Res. 2009;15:82-95.
66. Rodriguez-Pallares J, Parga JA, Joglar B, Guerra MJ, Labandeira-Garcia 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.
67. 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.
68. Muñoz A, Rey P, Guerra MJ, Mendez-Alvarez E, Soto-Otero R, Labandeira-Garcia JL. Reduction of dopaminergic degeneration and oxidative stress by inhibition of angiotensin converting enzyme in a MPTP model of parkinsonism. Neuropharmacology. 2006;51:112-120.
69. Rey P, Lopez-Real A, Sanchez-Iglesias S, Muñoz A, Soto-Otero R, Labandeira-Garcia JL. Angiotensin type-1-receptor antagonists reduce 6-hydroxydopamine toxicity for dopaminergic neurons. Neurobiol Aging. 2007;28:555-567.
70. Garrido-Gil P, Joglar B, Rodriguez-Perez AI, Guerra MJ, Labandeira-Garcia JL. Involvement of PPAR-γin 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.
71. Villar-Cheda B, Dominguez-Meijide A, Joglar B, Rodriguez-Perez AI, Guerra MJ, Labandeira-Garcia JL. 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.
72. Lucius R, Gallinat S, Rosenstiel P, Herdegen T, Sievers J, Unger T. The angiotensin II type 2 receptor promotes axonal regeneration in the optic nerve of adult rats. J Exp Med. 1998;188:661-670.
73. Namsolleck P, Boato F, Schwengel K, et al. AT2-receptor stimulation enhances axonal plasticity after spinal cord injury by upregulating BDNF expression. Neurobiol Dis. 2013;51:177-191.
74. Wang Y, Chan GL, Holden JE, et al. Age-dependent decline of dopamine D1 receptors in human brain: a PET study. Synapse. 1998;30:56-61.
75. Ishibashi K, Ishii K, Oda K, Kawasaki K, Mizusawa H, Ishiwata K. Regional analysis of age-related decline in dopamine transporters and dopamine D2-like receptors in human striatum. Synapse. 2009;63:282-290.
76. Rieckmann A, Karlsson S, Karlsson P, et al. Dopamine D1 receptor associations within and between dopaminergic pathways in younger and elderly adults: links to cognitive performance. Cereb Cortex. 2011;21:2023-2032.
77. Collier TJ, Lipton J, Daley BF, et al. Aging-related changes in the nigrostriatal dopamine system and the response to MPTP in nonhuman primates: diminished compensatory mechanisms as a prelude to parkinsonism. Neurobiol Dis. 2007;26:56-65.
78. Kubis N, Faucheux BA, Ransmayr G, et al. Preservation of midbrain catecholaminergic neurons in very old human subjects. Brain. 2000;123:366-373.
79. Villar-Cheda B, Sousa-Ribeiro D, Rodriguez-Pallares J, Rodriguez-Perez AI, Guerra MJ, Labandeira-Garcia JL. Aging and sedentarism decrease vascularization and VEGF levels in the rat substantia nigra. Implications for Parkinson's disease. J Cereb Blood Flow Metab. 2009;29:230-234.
80. Villar-Cheda B, Valenzuela R, Rodriguez-Perez AI, Guerra MJ, Labandeira-Garcia JL. Aging-related changes in the nigral angiotensin system enhances proinflammatory and pro-oxidative markers and 6-OHDA-induced dopaminergic degeneration. Neurobiol Aging. 2012;33:204.e1-e11.
81. Rodriguez-Perez AI, Valenzuela R, Villar-Cheda B, Guerra MJ, Lanciego JL, Labandeira-Garcia JL. Estrogen and angiotensin interaction in the substantia nigra. Relevance to postmenopausal Parkinson's disease. Exp Neurol. 2010;224:517-526.
82. Rodriguez-Perez AI, Valenzuela R, Villar-Cheda B, Guerra MJ, Labandeira-Garcia JL. Different dopaminergic neuroprotection of hormonal replacement therapy in young and aged menopausal rats. Role of the brain angiotensin system. Brain. 2012;135:124-138.
83. Rodriguez-Perez AI, Dominguez-Meijide A, Lanciego JL, Guerra MJ, Labandeira-Garcia JL. Dopaminergic degeneration is enhanced by chronic brain hypoperfusion and inhibited by angiotensin receptor blockage. Age (Dordr). 2012 [Epub ahead of print].
84. Rodriguez-Perez AI, Valenzuela R, Joglar B, Garrido-Gil P, Guerra MJ, Labandeira-Garcia JL. Renin angiotensin system and gender differences in dopaminergic degeneration. Mol Neurodegener. 2011;6:58.
85. Grammatopoulos TN, Jones SM, Ahmadi FA, et al. Angiotensin type 1 receptor antagonist losartan, reduces MPTP-induced degeneration of dopaminergic neurons in substantia nigra. Mol Neurodegener. 2007;2:1.
86. Konings CH, Kuiper MA, Bergmans PL, Grijpma AM, van Kamp GJ, Wolters EC. Increased angiotensin-converting enzyme activity in cerebrospinal fluid of treated patients with Parkinson's disease. Clin Chim Acta 1994;23:101-106.
87. Lin JJ, Yueh KC, Chang DC, Lin SZ. Association between genetic polymorphism of angiotensin-converting enzyme gene and Parkinson disease. J Neurol Sci. 2002;199:25-29.
88. Reardon KA, Mendelsohn FA, Chai SY, Horne MK. The angiotensin converting enzyme (ACE) inhibitor, perindopril, modifies the clinical features of Parkinson's disease. Aust N Z Med. 2000;30:48-53.
89. Chang YP, Shih PY. A case of Parkinson's disease worsened by captopril: an unexpected adverse effect. Mov Disord. 2009;24:790.
90. Sandyk R. Parkinsonism induced by captopril. Clin Neuropharmacol. 1985;8:197-198.
91. Sarma GR, Kamath V, Mathew T, Roy AK. A case of parkinsonism worsened by losartan: a probable new adverse effect. Mov Disord. 2008;23:1055.
92. Becker C, Jick SS, Meier CR. Use of antihypertensives and the risk of Parkinson disease. Neurology. 2008;70:1438-1444.
93. Pasternak B, Svanström H, Nielsen NM, Fugger L, Melbye M, Hviid A. Use of calcium channel blockers and Parkinson's disease. Am J Epidemiol. 2012;175:627-635.
94. Ascherio A, Tanner CM. Use of antihypertensives and the risk of Parkinson's disease. Neurology. 2009;72:578-579.