Testosterone depletion increases the susceptibility of brain tissue to oxidative damage in a restraint stress mouse model

Journal of Neurochemistry

Volumn 136, Issue 1, 2016, Pages 106-117

  Son, Seung Wan ^a   Lee, Jin Seok ^b   Kim, Hyeong Geug ^b   Kim, Dong Woon ^c   Ahn, Yo Chan ^b   Son, Chang Gue ^a,b  

^a Korea University   (South Korea)

^b Daejeon University   (South Korea)

^c Chungnam National University   (South Korea)

Author keywords

corticosterone; neurodegeneration; orchiectomy; oxidative stress; psychological stress; testosterone

Indexed keywords

4 HYDROXYNONENAL; ADRENALIN; CORTICOSTERONE; TESTOSTERONE; REACTIVE OXYGEN METABOLITE;

ADRENALIN BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; HIPPOCAMPUS; IMMOBILIZATION STRESS; LIPID PEROXIDATION; MALE; MOUSE; NERVE CELL DEGENERATION; NONHUMAN; ORCHIECTOMY; OXIDATIVE STRESS; PEROXIDATION; PRIORITY JOURNAL; PROTEIN PEROXIDATION; STAINING; TESTOSTERONE BLOOD LEVEL; ADVERSE EFFECTS; ANIMAL; BAGG ALBINO MOUSE; BRAIN; DEFICIENCY; DISEASE MODEL; EXERCISE; MENTAL STRESS; METABOLISM; PATHOLOGY; PHYSIOLOGY;

ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; LIPID PEROXIDATION; MALE; MICE; MICE, INBRED BALB C; ORCHIECTOMY; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; RESTRAINT, PHYSICAL; STRESS, PSYCHOLOGICAL; TESTOSTERONE;

EID: 84951189430     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.13371     Document Type: Article

References (76)

1. Abraham I. M., Harkany T., Horvath K. M., and, Luiten P. G., (2001) Action of glucocorticoids on survival of nerve cells: promoting neurodegeneration or neuroprotection? J. Neuroendocrinol. 13, 749-760.
2. Adams C., and, Kumar R., (2013) The effect of estrogen in a man with Parkinson's disease and a review of its therapeutic potential. Int. J. Neurosci. 123, 741-742.
3. Al-Damegh M. A., (2014) Stress-induced changes in testosterone secretion in male rats: role of oxidative stress and modulation by antioxidants. Open. J. Anim. Sci. 4, 70-78.
4. Alkadhi K. A., Alzoubi K. H., Srivareerat M., and, Tran T. T., (2011) Chronic psychosocial stress exacerbates impairment of synaptic plasticity in beta-amyloid rat model of Alzheimer's disease: prevention by nicotine. Curr. Alzheimer Res. 8, 718-731.
5. Baldereschi M., Di Carlo A., Lepore V., Bracco L., Maggi S., Grigoletto F., Scarlato G., and, Amaducci L., (1998) Estrogen-replacement therapy and Alzheimer's disease in the Italian Longitudinal Study on Aging. Neurology 50, 996-1002.
6. Beer T. M., Bland L. B., Bussiere J. R., Neiss M. B., Wersinger E. M., Garzotto M., Ryan C. W., and, Janowsky J. S., (2006) Testosterone loss and estradiol administration modify memory in men. J. Urol. 175, 130-135.
7. Behl C., (2002) Sex hormones, neuroprotection and cognition. Prog. Brain Res. 138, 135-142.
8. Benzie I. F., (2000) Evolution of antioxidant defence mechanisms. Eur. J. Nutr. 39, 53-61.
9. Bimonte-Nelson H. A., Singleton R. S., Nelson M. E., Eckman C. B., Barber J., Scott T. Y., and, Granholm A. C., (2003) Testosterone, but not nonaromatizable dihydrotestosterone, improves working memory and alters nerve growth factor levels in aged male rats. Exp. Neurol. 181, 301-312.
10. Bradley M. A., Markesbery W. R., and, Lovell M. A., (2010) Increased levels of 4-hydroxynonenal and acrolein in the brain in preclinical Alzheimer disease. Free Radic. Biol. Med. 48, 1570-1576.
11. Bruno M., Moore T., Nesnow S., and, Ge Y., (2009) Protein carbonyl formation in response to propiconazole-induced oxidative stress. J. Proteome Res. 8, 2070-2078.
12. Buynitsky T., and, Mostofsky D. I., (2009) Restraint stress in biobehavioral research: recent developments. Neurosci. Biobehav. Rev. 33, 1089-1098.
13. Carroll J. C., and, Rosario E. R., (2012) The potential use of hormone-based therapeutics for the treatment of Alzheimer's disease. Curr. Alzheimer Res. 9, 18-34.
14. Carroll J. C., Rosario E. R., Chang L., Stanczyk F. Z., Oddo S., LaFerla F. M., and, Pike C. J., (2007) Progesterone and estrogen regulate Alzheimer-like neuropathology in female 3xTg-AD mice. J. Neurosci. 27, 13357-13365.
15. Chen G., Jing C. H., Liu P. P., Ruan D., and, Wang L., (2013) Induction of autophagic cell death in the rat brain caused by iron. Am. J. Med. Sci. 345, 369-374.
16. Chisu V., Manca P., Lepore G., Gadau S., Zedda M., and, Farina V., (2006) Testosterone induces neuroprotection from oxidative stress. Effects on catalase activity and 3-nitro-L-tyrosine incorporation into alpha-tubulin in a mouse neuroblastoma cell line. Arch. Ital. Biol. 144, 63-73.
17. Colaianna M., Schiavone S., Zotti M., et al,. (2013) Neuroendocrine profile in a rat model of psychosocial stress: relation to oxidative stress. Antioxid. Redox Signal. 18, 1385-1399.
18. Czeh B., Welt T., Fischer A. K., Erhardt A., Schmitt W., Muller M. B., Toschi N., Fuchs E., and, Keck M. E., (2002) Chronic psychosocial stress and concomitant repetitive transcranial magnetic stimulation: effects on stress hormone levels and adult hippocampal neurogenesis. Biol. Psychiatry 52, 1057-1065.
19. Deviche P., Gao S., Davies S., Sharp P. J., and, Dawson A., (2012) Rapid stress-induced inhibition of plasma testosterone in free-ranging male rufous-winged sparrows, Peucaea carpalis: characterization, time course, and recovery. Gen. Comp. Endocrinol. 177, 1-8.
20. Dinkel K., Ogle W. O., and, Sapolsky R. M., (2002) Glucocorticoids and central nervous system inflammation. J. Neurovirol. 8, 513-528.
21. Elliott E. M., and, Sapolsky R. M., (1993) Corticosterone impairs hippocampal neuronal calcium regulation-possible mediating mechanisms. Brain Res. 602, 84-90.
22. Enciu A. M., Gherghiceanu M., and, Popescu B. O., (2013) Triggers and effectors of oxidative stress at blood-brain barrier level: relevance for brain ageing and neurodegeneration. Oxid. Med. Cell. Longev. 2013, 297512.
23. Esch T., Stefano G. B., Fricchione G. L., and, Benson H., (2002) The role of stress in neurodegenerative diseases and mental disorders. Neuro Endocrinol. Lett. 23, 199-208.
24. Fanaei H., Karimian S. M., Sadeghipour H. R., Hassanzade G., Kasaeian A., Attari F., Khayat S., Ramezani V., and, Javadimehr M., (2014) Testosterone enhances functional recovery after stroke through promotion of antioxidant defenses, BDNF levels and neurogenesis in male rats. Brain Res. 1558, 74-83.
25. Floyd R. A., (1999) Antioxidants, oxidative stress, and degenerative neurological disorders. Proc. Soc. Exp. Biol. Med. 222, 236-245.
26. Francis K. T., (1981) The relationship between high and low trait psychological stress, serum testosterone, and serum cortisol. Experientia 37, 1296-1297.
27. Gao H. B., Shan L. X., Monder C., and, Hardy M. P., (1996) Suppression of endogenous corticosterone levels in vivo increases the steroidogenic capacity of purified rat Leydig cells in vitro. Endocrinology 137, 1714-1718.
28. Gatto N. M., Deapen D., Stoyanoff S., Pinder R., Narayan S., Bordelon Y., and, Ritz B., (2014) Lifetime exposure to estrogens and Parkinson's disease in California teachers. Parkinsonism Relat. Disord. 20, 1149-1156.
29. Gonzales R. J., Ansar S., Duckles S. P., and, Krause D. N., (2007) Androgenic/estrogenic balance in the male rat cerebral circulation: metabolic enzymes and sex steroid receptors. J. Cereb. Blood Flow Metab. 27, 1841-1852.
30. Gourley S. L., Swanson A. M., and, Koleske A. J., (2013) Corticosteroid-induced neural remodeling predicts behavioral vulnerability and resilience. J. Neurosci. 33, 3107-3112.
31. Green L. C., Wagner D. A., Glogowski J., Skipper P. L., Wishnok J. S., and, Tannenbaum S. R., (1982) Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal. Biochem. 126, 131-138.
32. Handa R. J., Kudwa A. E., Donner N. C., McGivern R. F., and, Brown R., (2013) Central 5-alpha reduction of testosterone is required for testosterone's inhibition of the hypothalamo-pituitary-adrenal axis response to restraint stress in adult male rats. Brain Res. 1529, 74-82.
33. Hayashi I., Morishita Y., Imai K., Nakamura M., Nakachi K., and, Hayashi T., (2007) High-throughput spectrophotometric assay of reactive oxygen species in serum. Mutat. Res. 631, 55-61.
34. Herbert V., Shaw S., Jayatilleke E., and, Stopler-Kasdan T., (1994) Most free-radical injury is iron-related: it is promoted by iron, hemin, holoferritin and vitamin C, and inhibited by desferoxamine and apoferritin. Stem Cells 12, 289-303.
35. Jellinger K. A., (2010) Basic mechanisms of neurodegeneration: a critical update. J. Cell Mol. Med. 14, 457-487.
36. Kurth F., Luders E., Sicotte N. L., Gaser C., Giesser B. S., Swerdloff R. S., Montag M. J., Voskuhl R. R., and, Mackenzie-Graham A., (2014) Neuroprotective effects of testosterone treatment in men with multiple sclerosis. Neuroimage Clin. 4, 454-460.
37. Lau A., and, Tymianski M., (2010) Glutamate receptors, neurotoxicity and neurodegeneration. Pflugers Arch. 460, 525-542.
38. Liu J., and, Mori A., (1999) Stress, aging, and brain oxidative damage. Neurochem. Res. 24, 1479-1497.
39. Liu Z., Gastard M., Verina T., Bora S., Mouton P. R., and, Koliatsos V. E., (2001) Estrogens modulate experimentally induced apoptosis of granule cells in the adult hippocampus. J. Comp. Neurol. 441, 1-8.
40. Madrigal J. L., Garcia-Bueno B., Caso J. R., Perez-Nievas B. G., and, Leza J. C., (2006) Stress-induced oxidative changes in brain. CNS Neurol. Disord. Drug Targets 5, 561-568.
41. McCracken E., Valeriani V., Simpson C., Jover T., McCulloch J., and, Dewar D., (2000) The lipid peroxidation by-product 4-hydroxynonenal is toxic to axons and oligodendrocytes. J. Cereb. Blood Flow Metab. 20, 1529-1536.
42. McEwen B. S., (2007) Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol. Rev. 87, 873-904.
43. Meraz-Rios M. A., Franco-Bocanegra D., Toral Rios D., and, Campos-Pena V., (2014) Early onset Alzheimer's disease and oxidative stress. Oxid. Med. Cell. Longev. 2014, 375968.
44. Michael R. P., Bonsall R. W., and, Rees H. D., (1986) The nuclear accumulation of [3H]testosterone and [3H]estradiol in the brain of the female primate: evidence for the aromatization hypothesis. Endocrinology 118, 1935-1944.
45. Mihara M., and, Uchiyama M., (1978) Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal. Biochem. 86, 271-278.
46. Morakinyo A. O., Adekunbi D. A., Dada K. A., and, Adegoke O. A., (2014) Testosterone promotes glucose intolerance, lipid disorder and oxidative stress in type 1 diabetic rats. J. Basic Clin. Physiol. Pharmacol. 25, 13-20.
47. Numakawa T., Matsumoto T., Numakawa Y., Richards M., Yamawaki S., and, Kunugi H., (2011) Protective Action of Neurotrophic Factors and Estrogen against Oxidative Stress-Mediated Neurodegeneration. J. Toxicol. 2011, 405194.
48. Patel R., McIntosh L., McLaughlin J., Brooke S., Nimon V., and, Sapolsky R., (2002) Disruptive effects of glucocorticoids on glutathione peroxidase biochemistry in hippocampal cultures. J. Neurochem. 82, 118-125.
49. Perluigi M., Coccia R., and, Butterfield D. A., (2012) 4-Hydroxy-2-nonenal, a reactive product of lipid peroxidation, and neurodegenerative diseases: a toxic combination illuminated by redox proteomics studies. Antioxid. Redox Signal. 17, 1590-1609.
50. Reed T. T., (2011) Lipid peroxidation and neurodegenerative disease. Free Radic. Biol. Med. 51, 1302-1319.
51. Regensburger M., Prots I., and, Winner B., (2014) Adult hippocampal neurogenesis in Parkinson's disease: impact on neuronal survival and plasticity. Neural. Plast. 2014, 454696.
52. Retana-Marquez S., Bonilla-Jaime H., Vazquez-Palacios G., Martinez-Garcia R., and, Velazquez-Moctezuma J., (2003) Changes in masculine sexual behavior, corticosterone and testosterone in response to acute and chronic stress in male rats. Horm. Behav. 44, 327-337.
53. Reynolds I. J., and, Hastings T. G., (1995) Glutamate induces the production of reactive oxygen species in cultured forebrain neurons following NMDA receptor activation. J. Neurosci. 15, 3318-3327.
54. Robert S. M., Ogunrinu-Babarinde T., Holt K. T., and, Sontheimer H., (2014) Role of glutamate transporters in redox homeostasis of the brain. Neurochem. Int. 73, 181-191.
55. Rubinow D. R., Roca C. A., Schmidt P. J., Danaceau M. A., Putnam K., Cizza G., Chrousos G., and, Nieman L., (2005) Testosterone suppression of CRH-stimulated cortisol in men. Neuropsychopharmacology 30, 1906-1912.
56. Sankar B. R., Maran R. R., Sudha S., Govindarajulu P., and, Balasubramanian K., (2000) Chronic corticosterone treatment impairs Leydig cell 11beta-hydroxysteroid dehydrogenase activity and LH-stimulated testosterone production. Horm. Metab. Res. 32, 142-146.
57. Sapolsky R. M., (1985) A mechanism for glucocorticoid toxicity in the hippocampus: increased neuronal vulnerability to metabolic insults. J. Neurosci. 5, 1228-1232.
58. Sato H., Takahashi T., Sumitani K., Takatsu H., and, Urano S., (2010) Glucocorticoid generates ROS to induce oxidative injury in the hippocampus, leading to impairment of cognitive function of rats. J. Clin. Biochem. Nutr. 47, 224-232.
59. Schoenfeld T. J., and, Gould E., (2012) Stress, stress hormones, and adult neurogenesis. Exp. Neurol. 233, 12-21.
60. Seale J. V., Wood S. A., Atkinson H. C., Bate E., Lightman S. L., Ingram C. D., Jessop D. S., and, Harbuz M. S., (2004) Gonadectomy reverses the sexually diergic patterns of circadian and stress-induced hypothalamic-pituitary-adrenal axis activity in male and female rats. J. Neuroendocrinol. 16, 516-524.
61. Seidel E. M., Silani G., Metzler H., Thaler H., Lamm C., Gur R. C., Kryspin-Exner I., Habel U., and, Derntl B., (2013) The impact of social exclusion vs. inclusion on subjective and hormonal reactions in females and males. Psychoneuroendocrinology 38, 2925-2932.
62. Smith I. K., Vierheller T. L., and, Thorne C. A., (1988) Assay of glutathione reductase in crude tissue homogenates using 5,5′-dithiobis(2-nitrobenzoic acid). Anal. Biochem. 175, 408-413.
63. Spijker S., (2011) Dissection of rodent brain regions. Neuromethods 57, 13-26.
64. Takuma K., Mizoguchi H., Funatsu Y., et al,. (2012) Combination of chronic stress and ovariectomy causes conditioned fear memory deficits and hippocampal cholinergic neuronal loss in mice. Neuroscience 207, 261-273.
65. Tan R. S., and, Pu S. J., (2003) A pilot study on the effects of testosterone in hypogonadal aging male patients with Alzheimer's disease. Aging Male 6, 13-17.
66. Treccani G., Musazzi L., Perego C., et al,. (2014) Stress and corticosterone increase the readily releasable pool of glutamate vesicles in synaptic terminals of prefrontal and frontal cortex. Mol. Psychiatry 19, 433-443.
67. Tsang K. L., Ho S. L., and, Lo S. K., (2000) Estrogen improves motor disability in parkinsonian postmenopausal women with motor fluctuations. Neurology 54, 2292-2298.
68. Valen-Sendstad A., Engedal K., Stray-Pedersen B., Strobel C., Barnett L., Meyer N., and, Nurminemi M., (2010) Effects of hormone therapy on depressive symptoms and cognitive functions in women with Alzheimer disease: a 12 month randomized, double-blind, placebo-controlled study of low-dose estradiol and norethisterone. Am. J. Geriatr. Psychiatry 18, 11-20.
69. Vandresen-Filho S., Martins W. C., Bertoldo D. B., Mancini G., De Bem A. F., and, Tasca C. I., (2015) Cerebral cortex, hippocampus, striatum and cerebellum show differential susceptibility to quinolinic acid-induced oxidative stress. Neurol. Sci. 36, 1449-1456.
70. Vega-Rivera N. M., Fernandez-Guasti A., Ramirez-Rodriguez G., and, Estrada-Camarena E., (2013) Acute stress further decreases the effect of ovariectomy on immobility behavior and hippocampal cell survival in rats. Psychoneuroendocrinology 38, 1407-1417.
71. Viau V., and, Meaney M. J., (2004) Testosterone-dependent variations in plasma and intrapituitary corticosteroid binding globulin and stress hypothalamic-pituitary-adrenal activity in the male rat. J. Endocrinol. 181, 223-231.
72. Victor V. M., Rocha M., Banuls C., Rovira-Llopis S., Gomez M., and, Hernandez-Mijares A., (2014) Mitochondrial impairment and oxidative stress in leukocytes after testosterone administration to female-to-male transsexuals. J. Sex. Med. 11, 454-461.
73. Weissman B. A., Sottas C. M., Zhou P., Iadecola C., and, Hardy M. P., (2007) Testosterone production in mice lacking inducible nitric oxide synthase expression is sensitive to restraint stress. Am. J. Physiol. Endocrinol. Metab. 292, E615-E620.
74. Wheeler C. R., Salzman J. A., Elsayed N. M., Omaye S. T., and, Korte D. W., Jr, (1990) Automated assays for superoxide dismutase, catalase, glutathione peroxidase, and glutathione reductase activity. Anal. Biochem. 184, 193-199.
75. Winters S. J., and, Troen P., (1986) Testosterone and estradiol are co-secreted episodically by the human testis. J. Clin. Invest. 78, 870-873.
76. Yeung S. T., Myczek K., Kang A. P., Chabrier M. A., Baglietto-Vargas D., and, Laferla F. M., (2014) Impact of hippocampal neuronal ablation on neurogenesis and cognition in the aged brain. Neuroscience 259, 214-222.