Oxidative stress defines the neuroprotective or neurotoxic properties of androgens in immortalized female rat dopaminergic neuronal cells

Endocrinology

Volumn 154, Issue 11, 2013, Pages 4281-4292

  Holmes, Shaletha ^a   Abbassi, Babak ^a   Su, Chang ^a   Singh, Meharvan ^a   Cunningham, Rebecca L ^a  

^a UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; ANDROGEN RECEPTOR; ANDROSTANOLONE; HYDROGEN PEROXIDE; TESTOSTERONE;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL DEATH; CELL FUNCTION; CELL IMMORTALIZATION; CELL VIABILITY; DOPAMINERGIC NERVE CELL; FEMALE; MITOCHONDRION; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT;

ANDROGENS; ANIMALS; CALCIUM; CELL LINE; CELL SURVIVAL; DIHYDROTESTOSTERONE; DOPAMINERGIC NEURONS; FEMALE; MITOCHONDRIA; NEUROPROTECTIVE AGENTS; OXIDATIVE STRESS; RATS; TESTOSTERONE;

EID: 84886522237     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2013-1242     Document Type: Article

References (97)

1. Braak H, Ghebremedhin E, Rub U, Bratzke H, Del Tredici K. Stages in the development of Parkinson's disease-related pathology. Cell Tissue Res. 2004;318(1): 121-134.
2. Dauer W, Przedborski S. Parkinson's disease: mechanisms and models. Neuron. 2003;39(6): 889-909.
3. Forno LS. Neuropathology of Parkinson's disease. J Neuropathol Exp Neurol. 1996;55(3): 259-272.
4. Dawson TM, Dawson VL. Molecular pathways of neurodegeneration in Parkinson's disease. Science. 2003;302(5646): 819-822.
5. Dietz V, Quintern J, Berger W. Electrophysiological studies of gait in spasticity and rigidity. Evidence that altered mechanical properties of muscle contribute to hypertonia. Brain. 1981;104(3): 431-449.
6. Shastry BS. Neurodegenerative disorders of protein aggregation. Neurochem Int. 2003;43(1): 1-7.
7. Hornykiewicz O. Dopamine (3-hydroxytyramine) and brain function. Pharmacol Rev. 1966;18(2): 925-964.
8. Riederer P, Wuketich S. Time course of nigrostriatal degeneration in Parkinson's disease. A detailed study of influential factors in human brain amine analysis. J Neural Transm. 1976;38(3-4): 277-301.
9. Lotharius J, Barg S, Wiekop P, Lundberg C, Raymon HK, Brundin P. Effect of mutant α-synuclein on dopamine homeostasis in a new human mesencephalic cell line. J Biol Chem. 2002;277(41): 38884-38894.
10. Jenner P. Oxidative stress in Parkinson's disease. Ann Neurol. 2003; 53(suppl 3):S26 -S36; discussion S36-S28.
11. Gille G, Hung ST, Reichmann H, Rausch WD. Oxidative stress to dopaminergic neurons as models of Parkinson's disease. Ann NY Acad Sci. 2004;1018: 533-540.
12. Kanthasamy AG, Kitazawa M, Kaul S, et al. Proteolytic activation of proapoptotic kinase PKCδ is regulated by overexpression of Bcl-2: implications for oxidative stress and environmental factors in Parkinson's disease. Ann NY Acad Sci. 2003;1010: 683-686.
13. Mayeux R, Marder K, Cote LJ, et al. The frequency of idiopathic Parkinson's disease by age, ethnic group, and sex in northern Manhattan, 1988-1993. Am J Epidemiol. 1995;142(8): 820-827.
14. Hofman A, Collette HJ, Bartelds AI. Incidence and risk factors of Parkinson's disease in The Netherlands. Neuroepidemiology. 1989; 8(6): 296-299.
15. Van Den Eeden S, Tanner C, Bernstein A, et al. Incidence of Parkinson's disease: variation by age, gender, and race/ethnicity. Am J Epidemiol. 2003;157(11): 1015-1022.
16. Hanrott K, Gudmunsen L, O'Neill MJ, Wonnacott S. 6-Hydroxydopamine- induced apoptosis is mediated via extracellular auto-oxidation and caspase 3-dependent activation of protein kinase Cδ. J Biol Chem. 2006;281(9): 5373-5382.
17. Beal MF. Mitochondrial dysfunction in neurodegenerative diseases. Biochim Biophys Acta. 1998;1366(1-2): 211-223.
18. de Lau LM, Giesbergen PC, de Rijk MC, Hofman A, Koudstaal PJ, Breteler MM. Incidence of parkinsonism and Parkinson disease in a general population: the Rotterdam Study. Neurology. 2004;63(7): 1240-1244.
19. de Rijk MC, Tzourio C, Breteler MM, et al. Prevalence of parkinsonism and Parkinson's disease in Europe: the EUROPARKINSON Collaborative Study. European Community Concerted Action on the Epidemiology of Parkinson's disease. J Neurol Neurosurg Psychiatry. 1997;62(1): 10-15.
20. Benitez-Rivero S, Marin-Oyaga VA, Garcia-Solis D, et al. Clinical features and 123I-FP-CIT SPECT imaging in vascular parkinsonism and Parkinson's disease. J Neurol Neurosurg Psychiatry. 2013; 84(2): 122-129.
21. Thanvi B, Lo N, Robinson T. Vascular parkinsonism-an important cause of parkinsonism in older people. Age Ageing. 2005;34(2): 114-119.
22. Doyle KP, Simon RP, Stenzel-Poore MP. Mechanisms of ischemic brain damage. Neuropharmacology. 2008;55(3): 310-318.
23. Mehta SL, Manhas N, Raghubir R. Molecular targets in cerebral ischemia for developing novel therapeutics. Brain Res Rev. 2007; 54(1): 34-66.
24. Hollander M, Koudstaal PJ, Bots ML, Grobbee DE, Hofman A, Breteler MM. Incidence, risk, and case fatality of first ever stroke in the elderly population. The Rotterdam Study. J Neurol Neurosurg Psychiatry. 2003;74(3): 317-321.
25. Gavrilova N, Lindau ST. Salivary sex hormone measurement in a national, population-based study of older adults. J Gerontol B Psychol Sci Soc Sci. 2009:gbn028.
26. Ahlbom E, Grandison L, Bonfoco E, Zhivotovsky B, Ceccatelli S. Androgen treatment of neonatal rats decreases susceptibility of cerebellar granule neurons to oxidative stress in vitro. Eur J Neurosci. 1999;11(4): 1285-1291.
27. Ahlbom E, Prins GS, Ceccatelli S. Testosterone protects cerebellar granule cells from oxidative stress-induced cell death through a receptor mediated mechanism. Brain Res. 2001;892(2): 255-262.
28. Cunningham RL, Giuffrida A, Roberts JL. Androgens induce dopaminergic neurotoxicity via caspase-3-dependent activation of protein kinase Cδ. Endocrinology. 2009;150(12): 5539-5548.
29. Cunningham RL, Macheda T, Watts LT, et al. Androgens exacerbate motor asymmetry in male rats with unilateral 6-hydroxydopamine lesion. Horm Behav. 2011;60(5): 617-624.
30. Orth M, Schapira AH. Mitochondria and degenerative disorders. Am J Med Genet. 2001;106(1): 27-36.
31. Ichas F, Jouaville LS, Sidash SS, Mazat JP, Holmuhamedov EL. Mitochondrial calcium spiking: a transduction mechanism based on calcium-induced permeability transition involved in cell calcium signalling. FEBS Lett. 1994;348(2): 211-215.
32. Jouaville LS, Ichas F, Holmuhamedov EL, Camacho P, Lechleiter JD. Synchronization of calcium waves by mitochondrial substrates in Xenopus laevis oocytes. Nature. 1995;377(6548): 438-441.
33. Ichas F, Jouaville LS, Mazat JP. Mitochondria are excitable organelles capable of generating and conveying electrical and calcium signals. Cell. 1997;89(7): 1145-1153.
34. Guzman JN, Sanchez-Padilla J, Wokosin D, et al. Oxidant stress evoked by pacemaking in dopaminergic neurons is attenuated by DJ-1. Nature. 2010;468(7324): 696-700.
35. Chan CS, Guzman JN, Ilijic E, et al. 'Rejuvenation' protects neurons in mouse models of Parkinson's disease. Nature. 2007;447(7148): 1081-1086.
36. Danzer KM, Haasen D, Karow AR, et al. Different species of α-synuclein oligomers induce calcium influx and seeding. J Neurosci. 2007;27(34): 9220-9232.
37. Gandhi S, Wood-Kaczmar A, Yao Z, et al. PINK1-associated Parkinson's disease is caused by neuronal vulnerability to calcium-induced cell death. Mol Cell. 2009;33(5): 627-638.
38. Crocker SJ, Smith PD, Jackson-Lewis V, et al. Inhibition of calpains prevents neuronal and behavioral deficits in an MPTP mouse model of Parkinson's disease. J Neurosci. 2003;23(10): 4081-4091.
39. Besancon E, Guo S, Lok J, Tymianski M, Lo EH. Beyond NMDA and AMPA glutamate receptors: emerging mechanisms for ionic imbalance and cell death in stroke. Trends Pharmacol Sci. 2008; 29(5): 268-275.
40. Kobayashi T, Mori Y. Ca2+ channel antagonists and neuroprotection from cerebral ischemia. Eur J Pharmacol. 1998;363(1): 1-15.
41. Adams FS, La Rosa FG, Kumar S, et al. Characterization and transplantation of two neuronal cell lines with dopaminergic properties. Neurochem Res. 1996;21(5): 619-627.
42. Miyajima A, Sunouchi M, Mitsunaga K, Yamakoshi Y, Nakazawa K, Usami M. Sexing of postimplantation rat embryos in stored twodimensional electrophoresis (2-DE) samples by polymerase chain reaction (PCR) of an Sry sequence. J Toxicol Sci. 2009;34(6): 681-685.
43. Fall CP, Bennett JP Jr. Visualization of cyclosporin A and Ca2+- sensitive cyclical mitochondrial depolarizations in cell culture. Biochim Biophys Acta. 1999;1410(1): 77-84.
44. Ward MW, Huber HJ, Weisova P, Dussmann H, Nicholls DG, Prehn JH. Mitochondrial and plasma membrane potential of cultured cerebellar neurons during glutamate-induced necrosis, apoptosis, and tolerance. J Neurosci. 2007;27(31): 8238-8249.
45. Liang H, Van Remmen H, Frohlich V, Lechleiter J, Richardson A, Ran Q. Gpx4 protects mitochondrial ATP generation against oxidative damage. Biochem Biophys Res Commun. 2007;356(4): 893-898.
46. World Health Organization, Nieschlag E, Wang C, et al. Guidelines for the Use of Androgens. Heidelberg: Springer; 1992.
47. Smith KW, Feldman HA, McKinlay JB. Construction and field validation of a self-administered screener for testosterone deficiency (hypogonadism) in ageing men. Clin Endocrinol (Oxf). 2000;53(6): 703-711.
48. Zitzmann M, Brune M, Nieschlag E. Vascular reactivity in hypogonadal men is reduced by androgen substitution. J Clin Endocrinol Metab. 2002;87(11): 5030-5037.
49. Gunter TE, Pfeiffer DR. Mechanisms by which mitochondria transport calcium. Am J Physiol. 1990;258(5 Pt 1):C755-C786.
50. Boitier E, Rea R, Duchen MR. Mitochondria exert a negative feedback on the propagation of intracellular Ca2+ waves in rat cortical astrocytes. J Cell Biol. 1999;145(4): 795-808.
51. Loew LM, Tuft RA, Carrington W, Fay FS. Imaging in five dimensions: time-dependent membrane potentials in individual mitochondria. Biophys J. 1993;65(6): 2396-2407.
52. Nicholls DG, Budd SL. Mitochondria and neuronal survival. Physiol Rev. 2000;80(1): 315-360.
53. Grynkiewicz G, Poenie M, Tsien RY. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem. 1985;260(6): 3440-3450.
54. Carvour M, Song C, Kaul S, Anantharam V, Kanthasamy A. Chronic low-dose oxidative stress induces caspase-3-dependent PKCδ proteolytic activation and apoptosis in a cell culture model of dopaminergic neurodegeneration. Ann NY Acad Sci. 2008;1139: 197-205.
55. Moldeus P, Cotgreave IA, Berggren M. Lung protection by a thiolcontaining antioxidant: N-acetylcysteine. Respiration. 1986; 50(suppl 1): 31-42.
56. Aruoma OI, Halliwell B, Hoey BM, Butler J. The antioxidant action of N-acetylcysteine: its reaction with hydrogen peroxide, hydroxyl radical, superoxide, and hypochlorous acid. Free Radic Biol Med. 1989;6(6): 593-597.
57. Estrada M, Uhlen P, Ehrlich BE. Ca2+ oscillations induced by testosterone enhance neurite outgrowth. J Cell Sci. 2006;119(Pt 4): 733-743.
58. Abramov AY, Duchen MR. Measurements of threshold of mitochondrial permeability transition pore opening in intact and permeabilized cells by flash photolysis of caged calcium. Methods Mol Biol. 2011;793: 299-309.
59. Figueroa-Valverde L, Luna H, Castillo-Henkel C, Munoz-Garcia O, Morato-Cartagena T, Ceballos-Reyes G. Synthesis and evaluation of the cardiovascular effects of two, membrane impermeant, macromolecular complexes of dextran-testosterone. Steroids. 2002; 67(7): 611-619.
60. Kampa M, Nifli AP, Charalampopoulos I, et al. Opposing effects of estradiol- and testosterone-membrane binding sites on T47D breast cancer cell apoptosis. Exp Cell Res. 2005;307(1): 41-51.
61. Kampa M, Papakonstanti EA, Hatzoglou A, Stathopoulos EN, Stournaras C, Castanas E. The human prostate cancer cell line LNCaP bears functional membrane testosterone receptors that increase PSA secretion and modify actin cytoskeleton. FASEB J. 2002; 16(11): 1429-1431.
62. Gatson JW, Singh M. Activation of a membrane-associated androgen receptor promotes cell death in primary cortical astrocytes. Endocrinology. 2007;148(5): 2458-2464.
63. Gatson JW, Kaur P, Singh M. Dihydrotestosterone differentially modulates the mitogen-activated protein kinase and the phosphoinositide 3-kinase/Akt pathways through the nuclear and novel membrane androgen receptor in C6 cells. Endocrinology. 2006; 147(4): 2028-2034.
64. Garcia MV, Cabezas JA, Perez-Gonzalez MN. Effects of oestradiol, testosterone and medroxyprogesterone on subcellular fraction marker enzyme activities from rat liver and brain. Comp Biochem Physiol B. 1985;80(2): 347-354.
65. Borodinsky LN, Root CM, Cronin JA, Sann SB, Gu X, Spitzer NC. Activity-dependent homeostatic specification of transmitter expression in embryonic neurons. Nature. 2004;429(6991): 523-530.
66. Ciccolini F, Collins TJ, Sudhoelter J, Lipp P, Berridge MJ, Bootman MD. Local and global spontaneous calcium events regulate neurite outgrowth and onset of GABAergic phenotype during neural precursor differentiation. J Neurosci. 2003;23(1): 103-111.
67. Root CM, Velazquez-Ulloa NA, Monsalve GC, Minakova E, Spitzer NC. Embryonically expressed GABA and glutamate drive electrical activity regulating neurotransmitter specification. J Neurosci. 2008;28(18): 4777-4784.
68. Steinsapir J, Socci R, Reinach P. Effects of androgen on intracellular calcium of LNCaP cells. Biochem Biophys Res Commun. 1991; 179(1):90-96.
69. Koenig H, Fan CC, Goldstone AD, Lu CY, Trout JJ. Polyamines mediate androgenic stimulation of calcium fluxes and membrane transport in rat heart myocytes. Circ Res. 1989;64(3): 415-426.
70. Benten WP, Guo Z, Krucken J, Wunderlich F. Rapid effects of androgens in macrophages. Steroids. 2004;69(8-9): 585-590.
71. Yano S, Tokumitsu H, Soderling TR. Calcium promotes cell survival through CaM-K kinase activation of the protein-kinase-B pathway. Nature. 1998;396(6711): 584-587.
72. Hu SC, Chrivia J, Ghosh A. Regulation of CBP-mediated transcription by neuronal calcium signaling. Neuron. 1999;22(4): 799-808.
73. Pike CJ, Carroll JC, Rosario ER, Barron AM. Protective actions of sex steroid hormones in Alzheimer's disease. Front Neuroendocrinol. 2009;30(2): 239-258.
74. Pike CJ, Rosario ER, Nguyen TV. Androgens, aging, and Alzheimer's disease. Endocrine. 2006;29(2): 233-241.
75. Jeppesen LL, Jorgensen HS, Nakayama H, RaaschouHO,Olsen TS, Winther K. Decreased serum testosterone in men with acute ischemic stroke. Arterioscler Thromb Vasc Biol. 1996;16(6): 749-754.
76. Harman SM, Tsitouras PD. Reproductive hormones in aging men. I. Measurement of sex steroids, basal luteinizing hormone, and Leydig cell response to human chorionic gonadotropin. J Clin Endocrinol Metab. 1980;51(1): 35-40.
77. Okun MS, DeLong MR, Hanfelt J, Gearing M, Levey A. Plasma testosterone levels in Alzheimer and Parkinson diseases. Neurology. 2004;62(3): 411-413.
78. Morales A, Johnston B, Heaton JP, Lundie M. Testosterone supplementation for hypogonadal impotence: assessment of biochemical measures and therapeutic outcomes. J Urol. 1997;157(3): 849-854.
79. Mitchell E, Thomas D, Burnet R. Testosterone improves motor function in Parkinson's disease. J Clin Neurosci. 2006;13(1): 133-136.
80. Committee on Assessing the Need for Clinical Trials of Testosterone Replacement Therapy. Testosterone and Aging: Clinical Research Directions. Washington, D.C.: The National Academies Press; 2004.
81. Borras C, Sastre J, Garcia-Sala D, Lloret A, Pallardo FV, Vina J. Mitochondria from females exhibit higher antioxidant gene expression and lower oxidative damage than males. Free Radic Biol Med. 2003;34(5): 546-552.
82. Guevara R, Santandreu FM, Valle A, Gianotti M, Oliver J, Roca P. Sex-dependent differences in aged rat brain mitochondrial function and oxidative stress. Free Radic Biol Med. 2009;46(2): 169-175.
83. Loft S, Vistisen K, Ewertz M, Tjonneland A, Overvad K, Poulsen HE. OxidativeDNAdamage estimated by 8-hydroxydeoxyguanosine excretion in humans: influence of smoking, gender and body mass index. Carcinogenesis. 1992;13(12): 2241-2247.
84. Toescu EC, Myronova N, Verkhratsky A. Age-related structural and functional changes of brain mitochondria. Cell Calcium. 2000; 28(5-6): 329-338.
85. Fiskum G. Mitochondrial participation in ischemic and traumatic neural cell death. J Neurotrauma. 2000;17(10): 843-855.
86. Beal MF. Excitotoxicity and nitric oxide in Parkinson's disease pathogenesis. Ann Neurol. 1998;44(3 suppl 1):S110-S114.
87. Jambrina E, Alonso R, Alcalde M, et al. Calcium influx through receptor-operated channel induces mitochondria-triggered paraptotic cell death. J Biol Chem. 2003;278(16): 14134-14145.
88. Reynolds IJ. Mitochondrial membrane potential and the permeability transition in excitotoxicity. Ann NY Acad Sci. 1999;893: 33-41.
89. Bae JH, Park JW, Kwon TK. Ruthenium red, inhibitor of mitochondrial Ca2+ uniporter, inhibits curcumin-induced apoptosis via the prevention of intracellular Ca2+ depletion and cytochrome c release. Biochem Biophys Res Commun. 2003;303(4): 1073-1079.
90. Lee WT, Yin HS, Shen YZ. The mechanisms of neuronal death produced by mitochondrial toxin 3-nitropropionic acid: the roles of N-methyl-D-aspartate glutamate receptors and mitochondrial calcium overload. Neuroscience. 2002;112(3): 707-716.
91. Papakonstanti EA, Kampa M, Castanas E, Stournaras C. A rapid, nongenomic, signaling pathway regulates the actin reorganization induced by activation of membrane testosterone receptors. Mol Endocrinol. 2003;17(5): 870-881.
92. Uchida M, Palmateer JM, Herson PS, DeVries AC, Cheng J, Hurn PD. Dose-dependent effects of androgens on outcome after focal cerebral ischemia in adult male mice. J Cereb Blood Flow Metab. 2009;29(8): 1454-1462.
93. Tunez I, Feijoo M, Collado JA, et al. Effect of testosterone on oxidative stress and cell damage induced by 3-nitropropionic acid in striatum of ovariectomized rats. Life Sci. 2007;80(13): 1221-1227.
94. Ramsden M, Nyborg AC, Murphy MP, et al. Androgens modulate β-amyloid levels in male rat brain. J Neurochem. 2003;87(4): 1052-1055.
95. Rosario ER, Carroll JC, Oddo S, LaFerla FM, Pike CJ. Androgens regulate the development of neuropathology in a triple transgenic mouse model of Alzheimer's disease. J Neurosci. 2006;26(51): 13384-13389.
96. Yang SH, Perez E, Cutright J, et al. Testosterone increases neurotoxicity of glutamate in vitro and ischemia-reperfusion injury in an animal model. J Appl Physiol. 2002;92(1): 195-201.
97. Hawk T, Zhang YQ, Rajakumar G, Day AL, Simpkins JW. Testosterone increases and estradiol decreases middle cerebral artery occlusion lesion size in male rats. Brain Res. 1998;796(1-2): 296-298.