Soy isoflavones genistein and daidzein exert anti-apoptotic actions via a selective ER-mediated mechanism in neurons following HIV-1 Tat1-86 exposure

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Adams, Sheila M ^a   Aksenova, Marina V ^a   Aksenov, Michael Y ^a   Mactutus, Charles F ^a   Booze, Rosemarie M ^a  

^a UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; DAIDZEIN; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; GENISTEIN; ISOFLAVONE DERIVATIVE; PROTEIN BAX; TRANSACTIVATOR PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ANTIAPOPTOTIC ACTION; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; ENZYME ACTIVITY; ENZYME INHIBITION; FETUS; HUMAN IMMUNODEFICIENCY VIRUS 1; NERVE CELL; NONHUMAN; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; DOWN-REGULATION; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; GENISTEIN; HIV-1; ISOFLAVONES; NEURONS; PEPTIDE FRAGMENTS; PHYTOESTROGENS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ESTROGEN; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84861316682     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037540     Document Type: Article

References (70)

1. Antinori A, Arendt G, Becker JT, Brew BJ, Byrd DA, et al. (2007) Updated research nosology for HIV-associated neurocognitive disorders. Neurology 69 (18): 1789-1799.
2. Lindl KA, Marks DR, Kolson DL, Jordan-Sciutto KL, (2010) HIV-associated neurocognitive disorder: pathogenesis and therapeutic opportunities. J Neuroimmune Pharmacol 5 (3): 294-309.
3. Liner J, Hall CD, Robertson KR, (2008) Effects of antiretroviral therapy on cognitive impairment. Curr HIV/AIDS Rep 5: 64-71.
4. Boissé L, Gill MJ, Power C, (2008) HIV infection of the central nervous system: clinical features and neuropathogenesis. Neurol Clin 26: 799-819.
5. Gartner S, (2000) HIV infection and dementia. Science 287: 602-604.
6. Kaul M, Zheng J, Okamoto S, Gendelman HE, Lipton SA, (2005) HIV-1 infection and AIDS: consequences for the central nervous system. Cell Death Differ 12 (Suppl 1).
7. Kaul M, Lipton SA, (2006) Mechanisms of neuroimmunity and neurodegeneration associated with HIV-1 infection and AIDS. J Neuroimmune Pharmacol. 1: 138-151.
8. Rumbaugh JA, Steiner J, Sacktor N, Nath A, (2008) Developing neuroprotective strategies for treatment of HIV-associated neurocognitive dysfunction. Futur HIV Ther 2: 271-280.
9. Li W, Li G, Steiner J, Nath A, (2009) Role of Tat protein in HIV neuropathogenesis. Neurotox Res. 16 (3): 205-220.
10. Mediouni S, Darque A, Baillat G, Ravaux I, Dhiver C, et al. (2012) Antiretroviral therapy does not block the secretion of the human immodeficiency virus tat protein. Infect Disord Drug Targets 12: 81-86.
11. Campbell GR, Watkins JD, Loret EP, Spector SA, (2011) Differential induction of rat neuronal excitotoxic cell death by human immunodeficiency virus type 1 clade B and C tat proteins. AIDS Res Hum Retroviruses 27 (6): 647-654.
12. King JE, Eugenin EA, Buckner CM, Berman JW, (2006) HIV tat and neurotoxicity. Microbes Infect 8: 1347-1357.
13. King JE, Eugenin EA, Hazleton JE, Morgello S, Berman JW, (2010) Mechanisms of HIV-tat-induced phosphorylation of N-methyl-D-aspartate receptor subunit 2A in human primary neurons: implications for neuroAIDS pathogenesis. Am J Pathol 176 (6): 2819-2830.
14. Kim HJ, Martemyanov KA, Thayer SA, (2008) Human immunodeficiency virus protein Tat induces synapse loss via a reversible process that is distinct from cell death. J Neurosci 28: 12604-12613.
15. Aksenov MY, Aksenova MV, Mactutus CF, Booze RM, (2009) Attenuated neurotoxicity of the transactivation-defective HIV-1 Tat protein in hippocampal cell cultures. Exp Neurol 219: 586-590.
16. Aksenova MV, Aksenov MY, Adams SM, Mactutus CF, Booze RM, (2009) Neuronal survival and resistance to HIV-1 Tat toxicity in the primary culture of rat fetal neurons. Exp Neurol 5: 253-263.
17. Self RL, Mulholland PJ, Nath A, Harris BR, Prendergast MA, (2004) The human immunodeficiency virus type-1 transcription factor Tat produces elevations in intracellular Ca2+ that require function of an N-methyl-D-aspartate receptor polyamine-sensitive site. Brain Res 995: 39-45.
18. Aksenov MY, Hasselrot U, Wu G, Nath A, Anderson C, Mactutus CF, Booze RM, (2003) Temporal relationships between HIV-1 Tat-induced neuronal degeneration, OX-42 immunoreactivity, reactive astrocytosis, and protein oxidation in the rat striatum. Brain Res 987: 1-9.
19. Zhu J, Mactutus CF, Wallace DR, Booze RM, (2009) HIV-1 Tat protein induced rapid and reversible decrease in (3H)dopamine uptake: dissociation of (3H) dopamine uptake and (3H)2beta-carbomethoxy-3-beta-(4-fluorophenyl)tropane (WIN 35,428) binding in rat striatal synaptosomes. J Pharmacol Exp Ther 329: 1071-1083.
20. Ferris MJ, Frederick-Duus D, Fadel J, Mactutus CF, Booze RM, (2010) Hyperdopaminergic tone in HIV-1 protein treated rats and cocaine sensitization. J Neurochem 115: 885-896.
21. Fitting S, Booze RM, Hasselrot U, Mactutus CF, (2006) Intrahippocampal injections of Tat: effects on prepulse inhibition of the auditory startle response in adult male rats. Pharmacol Biochem Behav 84: 189-196.
22. Fitting S, Booze RM, Mactutus CF, (2008) Neonatal intrahippocampal injection of the HIV-1 proteins gp120 and Tat: differential effects on behavior and the relationship to stereological hippocampal measures. Brain Res. 1232: 139-154.
23. Nath A, (2002) Human immunodeficiency virus (HIV) proteins in neuropathogenesis of HIV dementia. J Infect Dis 186 (Suppl 2): S193-S198.
24. Hudson L, Liu J, Nath A, Jones M, Raghavan R, et al. (2000) Detection of the human immunodeficiency virus regulatory protein tat in CNS tissues. J Neurovirol 6: 145-155.
25. Hult B, Chana G, Masliah E, Everall I, (2008) Neurobiology of HIV. Int Rev Psychiatry 20 (1): 3-13.
26. Jorgensen M, Vendelbo B, Skakkebaek NE, Leffers H, (2000) Assaying estrogenicity by quantitating the expression levels of endogenous estrogen-regulated genes. Environ Health Perspect 108 (5): 403-412.
27. Gruber CJ, Tschugguel W, Schneeberger C, Huber JC, (2002) Production and actions of estrogens. N Engl J Med 346: 340-352.
28. Kostelac D, Rechkemmer G, Briviba K, (2003) Phytoestrogens modulate binding response of estrogen receptors α and β to the estrogen response element. J Agric Food Chem 51 (26): 7632-7635.
29. Casanova M, You L, Gaido KW, Archibeque-Engle S, Janszen DB, Heck HA, (1999) Developmental effects of dietary phytoestrogens in Sprague-Dawley rats and interactions of genistein and daidzein with rat estrogen receptors alpha and beta in vitro. Toxicol Sci 51: 236-244.
30. Pan Y, Anthony M, Watson S, Clarkson TB, (2000) Soy phytoestrogens improve spatial arm maze performance in ovariectomized retired breeder rats and do not attenuate benefits of 17 β-estradiol treatment. Menopause 7: 230-23545.
31. File SE, Jarret N, Fluck E, Duffy R, Casey K, Wiseman H, (2001) Eating soya improves human memory. Psychopharm (Berl) 157: 430-436.
32. Luine V, Attalla S, Mohan G, Costa A, Frankfurt M, (2006) Dietary phytoestrogens enhance spatial memory and spine density in the hippocampus and prefrontal cortex of ovariectomized rats. Brain Res 1126 (1): 183-187.
33. Lund TD, West TW, Tian LY, Bu LH, Simmons DL, et al. (2001) Visual spatial memory is enhanced in female rats (but inhibited in males) by dietary soy phytoestrogens. BMC Neurosci 2: 20.
34. Casini ML, Marelli G, Papaleo E, Ferrari A, D'Ambrosio F, Unfer V, (2006) Psychological assessment of the effects of treatment with phytoestrogens on postmenopausal women: a randomized, double-blind, crossover, placebo controlled study. Fertil Steril 85 (4): 972-978.
35. Neese SL, Wang VC, Doerge DR, Woodling KA, Andrade JE, et al. (2010) Impact of dietary genistein and aging on executive function in rats. Neurotoxicol Teratol 32 (2): 200-211.
36. Zhao L, Chen Q, Diaz Brinton R, (2002) Neuroprotective and neurotrophic efficacy of phytoestrogens in cultured hippocampal neurons. Exp Biol Med (Maywood) 227 (7): 509-519.
37. Zeng H, Chen Q, Zhao B, (2004) Genistein ameliorates beta-amyloid peptide (25-35)-induced hippocampal neuronal apoptosis. Free Radic Biol Med 36 (2): 180-188.
38. Aksenova MV, Silvers JM, Aksenov MY, Nath A, Ray PD, (2006) HIV-1 Tat neurotoxicity in primary cultures of rat midbrain fetal neurons: changes in dopamine transporter binding and immunoreactivity. Neurosci Lett 395 (3): 259-259.
39. Silvers JM, Aksenova MV, Aksenov MY, Mactutus CF, Booze RM, (2007) Neurotoxicity of HIV-1 Tat protein: involvement of D1 dopamine receptor. Neurotoxicology 28 (6): 1184-1190.
40. Luine VN, Richards ST, Wu VY, Beck KD, (1998) Estradiol enhances learning and memory in a spatial memory task and effects levels of monoaminergic neurotransmitters. Horm Behav 34: 149-162.
41. Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg C, et al. (2002) Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women's Health Initiative randomized controlled trial. JAMA 288 (3): 321-333.
42. Reeves GK, Beral V, Green J, Gathani T, Bull D; Million Women Study Collaborators, (2006) Hormonal therapy for menopause and breast-cancer risk by histological type: a cohort study and meta-analysis. Lancet Oncol 7 (11): 910-918.
43. Setchell KD, Cassidy A, (1999) Dietary isoflavones: biological effects and relevance to human health. J Nutr 129: 758S-767S.
44. Messina M, Nagata C, Wu AH, (2006) Estimated Asian soy protein and isoflavone intakes. Nutr Cancer 55: 1-12.
45. Patisaul HB, Jefferson W, (2010) The pros and cons of phytoestrogens. Front Neuroendocrin 31: 400-419.
46. Mortensen A, Kulling SE, Schwartz H, Rowland I, Ruefer CE, et al. (2009) Analytical and compositional aspects of isoflavones in food and their biological effects. Mol Nutr Food Res 53: S266-S309.
47. Lee YB, Lee HJ, Sohn HS, (2005) Soy isoflavones and cognitive function. J Nutr Biochem 16 (11): 641-64973.
48. Hamilton-Reeves JM, Vazquez G, Duval SJ, Phipps WR, Kurzer MS, (2010) Clinical studies show no effects of soy protein or isoflavones on reproductive hormones in men: results of a meta-analysis. Fertil Steril 94: 997-1007.
49. Busby MG, Jeffcoat AR, Bloedon LT, Koch MA, Black T, et al. (2002) Clinical characteristics and pharmacokinetics of purified soy isoflavones: single dose administration to healthy men. Am J Clin Nutr 75: 126-136.
50. Adams SM, Aksenova MV, Aksenov MY, Mactutus CF, Booze RM, (2010) ERβ mediates 17 β-estradiol attenuation of HIV-1 Tat-induced apoptotic signaling. Synapse 64 (11): 829-838.
51. Clifford DB, (2008) HIV-associated neurocognitive disease continues in the antiretroviral era. Top HIV Med 16 (2): 94-98.
52. Moore DJ, Masliah E, Rippeh JD, Gonzalez R, Carey CL, et al. (2006) Cortical and subcortical neurodegeneration is associated with HIV neurocognitive impairment. AIDS 20: 879-887.
53. Shughrue PJ, Lane MV, Merchenthaler I, (1997) Comparative distribution of estrogen receptor-alpha and-beta mRNA in the rat central nervous system. J Comp Neurol 388 (4): 507-525.
54. Shughrue PJ, Merchenthaler I, (2001) Distribution of estrogen receptor beta immunoreactivity in the rat central nervous system. J Comp Neurol 436: 64-81.
55. Zhao L, Mao Z, Brinton RD, (2009) A select combination of clinically relevant phytoestrogens enhances estrogen receptor beta-binding selectivity and neuroprotective activities in vitro and in vivo. Endocrin. 150 (2): 770-783.
56. Bonavia R, Bajetto A, Barbero S, Albini A, Noonan DM, (2001) HIV-1 tat causes apoptotic death and calcium homeostasis alterations in rat neurons. Biochem. Biophys. Res. Commun 288 (2): 301-308.
57. Hall JM, Couse JF, Korach KS, (2001) The multifaceted mechanisms of estradiol and estrogen receptor signaling. J Biol Chem 279 (40): 36869-36872.
58. Zhao L, Wu TW, Brinton RD, (2004) Estrogen receptor subtypes alpha and beta contribute to neuroprotection and increased Bcl-2 expression in primary hippocampal neurons. Brain Res 1010 (1-2): 22-34.
59. Bryant DN, Dorsa DM, (2010) Roles of estrogen receptors alpha and beta in sexually dimorphic neuroprotection against glutamate toxicity. Neurosci. 170 (4): 1261-1269.
60. Elzer JG, Muhammad S, Wintermantel TM, Regnier-Vigouroux A, Ludwig J, et al. (2010) Neuronal estrogen receptor-alpha mediates neuroprotection by 17 beta-estradiol. J Cereb Blood Flow Metab 30 (5): 935-942.
61. Cohen GM, (1997) Caspases: the executioners of apoptosis. Biochem J 326: 1-16.
62. Porter AG, Janicke RU, (1999) Emerging roles of caspase-3 in apoptosis. Cell Death Differ 6 (2): 99-104.
63. Stennicke HR, Salvesen GS, (2000) Caspases - controlling intracellular signals by protease zymogen activation. Biochim. Biophys. Acta. 1477: 299-306.
64. Yang S, Liu R, Perez EJ, Wen Y, Stevens SM, et al. (2004) Mitochondrial localization of estrogen receptor β. Proc Natl Acad Sci USA 101: 4130-4135.
65. Tee MK, Rogatsky I, Tzagarakis-Foster C, Cvoro A, An J, et al. (2004) Estradiol and selective estrogen receptor modulators differentially regulate target genes with estrogen receptors alpha and beta. Mol Biol Cell 15 (3): 1262-1272.
66. Paruthiyil S, Cvoro A, Zhao X, Wu Z, Sui Y, et al. (2009) Drug and cell type-specific regulation of genes with different classes of estrogen receptor β-selective agonists. PLoS One 4 (7): e6271.
67. Sheldahl LC, Shapiro RA, Bryant DN, Koerner IP, Dorsa DM, (2008) Estrogen induces rapid translocation of estrogen receptor beta, but no estrogen receptor alpha, to the neuronal plasma membrane. Neurosci 153 (3): 751-761.
68. Herrick SP, Waters EM, Drake CT, McEwen BS, Milner TA, (2006) Extranuclear estrogen receptor beta immunoreactivity is on doublecortin-containing cells in the adult and neonatal rat dentate gyrus. Brain Res 1121 (1): 46-58.
69. Bryant DN, Sheldahl LC, Marriot LK, Shapiro RA, Dorsa DM, (2006) Multiple pathways transmit neuroprotective effects of gonadal steroids. Endocrine 29 (2): 199-207.
70. Björnström L, Sjöberg M, (2005) Mechanisms of estrogen receptor signaling: convergence of genomic and nongenomic actions on target genes.