Sex hormonal regulation and hormesis in aging and longevity: role of vitagenes

Journal of Cell Communication and Signaling

Volumn 8, Issue 4, 2014, Pages 369-384

  Calabrese, V ^a,c   Scapagnini, G ^b,c   Davinelli, S ^b   Koverech, G ^a   Koverech, A ^a   De Pasquale, C ^a   Salinaro, A Trovato ^a   Scuto, M ^a   Calabrese, E J ^d   Genazzani, A R ^e  

^a UNIVERSITY OF CATANIA   (Italy)

^b UNIVERSITY OF MOLISE   (Italy)

^c SannioTech Consortium Research Center   (Italy)

^d UNIVERSITY OF MASSACHUSETTS   (United States)

^e UNIVERSITY HOSPITAL OF PISA   (Italy)

Author keywords

Aging; Heme oxygenase; Hormesis; Hormones; Vitagenes

Indexed keywords

ANDROGEN; ANDROSTANOLONE; ANDROSTENEDIONE; CELASTROL; CONJUGATED ESTROGEN; CURCUMIN; DIALLYL TRISULFIDE; DIOSGENIN; EQUILENIN; ESTRADIOL; ESTRIOL; ESTRONE; FERULIC ACID; FUMARIC ACID DIMETHYL ESTER; HEAT SHOCK PROTEIN; HEME OXYGENASE 1; KELCH LIKE ECH ASSOCIATED PROTEIN 1; PHYTOESTROGEN; PRASTERONE; PRASTERONE SULFATE; PROGESTERONE; SEX HORMONE; SEX HORMONE BINDING GLOBULIN; STIGMASTEROL; SULFORAPHANE; TERT BUTYLHYDROQUINONE; TESTOSTERONE; TRANSCRIPTION FACTOR NRF2;

AGING; ANDROGEN THERAPY; ARTICLE; CELL DEATH; CELL DEGENERATION; CELLULAR STRESS RESPONSE; HORMESIS; HORMONAL REGULATION; HORMONE SUBSTITUTION; HUMAN; HYPOGONADISM; LONGEVITY; NONHUMAN; OVARY FOLLICLE DEVELOPMENT; PRIORITY JOURNAL;

EID: 84922074125     PISSN: 18739601     EISSN: 1873961X     Source Type: Journal    
DOI: 10.1007/s12079-014-0253-7     Document Type: Article

References (100)

1. Abraham NG, Levere RD, Freedman ML (1985) Effect of age on rat liver heme and drug metabolism. Exp Gerontol 20:277–284
2. Akerfelt M, Vihervaara A, Laiho A, Conter A, Christians ES, Sistonen L, Henriksson E (2012) Heat shock transcription factor 1 localizes to sex chromatin during meiotic repression. J Biol Chem 285:34469–34476
3. Alam J, Cook JL (2007) How many transcription factors does it take to turn on the heme oxygenase-1 gene? Am J Respir Cell Mol Biol 36:166–174
4. Anand P, Nair HB, Sung B, Kunnumakkara AB, Yadav VR, Tekmal RR, Aggarwal BB (2010) Design of curcumin-loaded PLGA nanoparticles formulation with enhanced cellular uptake, and increased bioactivity in vitro and superior bioavailability in vivo. Biochem Pharmacol 79:330–338
5. Bao Q, Pan J, Qi H, Wang L, Qian H, Jiang F, Shao Z, Xu F, Tao Z, Ma Q, Nelson P, Hu X (2014) Aging and age-related diseases - from endocrine therapy to target therapy. Mol Cell Endocrinol 394:115–118
6. Basaria S (2013) Reproductive aging in Men. Endocrinol Metab Clin N Am 42:255–270
7. Basaria S, Wahlstrom JT, Dobs AS (2001) Anabolic-androgenic steroid therapy in the treatment of chronic diseases. J Clin Endocrinol Metab 86:5108–5117
8. Bellia F, Vecchio G, Cuzzocrea S, Calabrese V, Rizzarelli E (2011) Neuroprotection in oxidative driven diseases by carnosine. Mol Asp Med 32:258–266
9. Bensasson RV, Zoete V, Dinkova-Kostova AT, Talalay P (2008) Two-step mechanism of induction of the gene expression of a prototypic cancer-protective enzyme by diphenols. Chem Res Toxicol 21:805–812
10. Bhavnani BR, Stanczyk FZ (2012) Misconception and concerns about bioidentical hormones used for custom-compounded hormone therapy. J Clin Endocrinol Metab 97:756–759
11. Bloomer SA, Zhang HJ, Brown KE, Kregel KC (2009) Differential regulation of hepatic heme oxygenase-1 protein with aging and heat stress. J Gerontol A Biol Sci Med Sci 64419–25
12. Brandes LJ (2005) Hormetic effects of hormones, antihormones, and antidepressants on cancer cell growth in culture: in vivo correlates. Crit Rev Toxicol 35:587–592
13. Brown-Sequard CE (1889) Note on the effects produced on man by subcutaneous injections of a liquid obtained from the testicles of animals. Lancet 2:105–107
14. Butenandt A, Guenther H, Turba F (1960) On the primary metabolic action of testosterone. Hoppe Seylers Z Physiol Chem 322:28–37
15. Calabrese EJ (2013) Biphasic dose responses in biology, toxicology and medicine: accounting for their generalizability and quantitative features. Environ Pollut 182:452–460. doi:10.1016/j.envpol.2013.07.046
16. Calabrese V, Butterfield DA, Scapagnini G, Stella AM, Maines MD (2006) Redox regulation of heat shock protein expression by signaling involving nitric oxide and carbon monoxide: relevance to brain aging, neurodegenerative disorders, and longevity. Antioxid Redox Signal 8:444–477
17. Calabrese V, Guagliano E, Sapienza M, Panebianco M, Calafato S, Puleo E, Pennisi G, Mancuso C, Butterfield AD, Giuffrida Stella AM (2007) Redox regulation of cellular stress response in aging and neurodegenerative disorders: role of vitagenes. Neurochem Res 32:757–773
18. Calabrese V, Cornelius C, Mancuso C, Pennisi G, Calafato S, Bellia F, Bates TE, Giuffrida Stella AM, Schapira T, Dinkova Kostova AT, Rizzarelli E (2008) Cellular stress response: a novel target for chemoprevention and nutritional neuroprotection in aging, neurodegenerative disorders and longevity. Neurochem Res 33:2444–2471
19. Calabrese V, Cornelius C, Dinkova-Kostova AT, Calabrese EJ, Mattson MP (2010) Cellular stress responses, the hormesis paradigm and vitagenes: novel targets for therapeutic intervention in neurodegenerative disorders. Antioxid Redox Signal 13:1763–1811
20. Calabrese V, Cornelius C, Cuzzocrea S, Iavicoli I, Rizzarelli E, Calabrese EJ (2011) Hormesis, cellular stress response and vitagenes as critical determinants in aging and longevity. Mol Asp Med 32:279–304
21. Calabrese EJ, Iavicoli I, Calabrese V (2012) Hormesis: why it is important to biogerontologists. Biogerontology 13:215–235
22. Calabrese E, Iavicoli I, Calabrese V (2013) Hormesis: its impact on medicine and health. Hum Exp Toxicol 32:120–152
23. Chapple SJ, Siow RC, Mann GE (2012) Crosstalk between Nrf2 and the proteasome: therapeutic potential of Nrf2 inducers in vascular disease and aging. Int J Biochem Cell Biol 44:1315–1320
24. Chen YC, Kuo TC, Lin-Shiau SY, Lin JK (1996) Induction of HSP70 gene expression by modulation of Ca(+2) ion and cellular p53 protein by curcumin in colorectal carcinoma cells. Mol Carcinog 17:224–234
25. Chou YH, Ho FM, Liu DZ, Lin SY, Tsai LH, Chen CH, Ho YS, Hung LF, Liang YC (2005) The possible role of heat shock factor-1 in the negative regulation of heme oxygenase-1. Int J Biochem Cell Biol 37:604–615
26. Clark JH (2006) A critique of Women’s health initiative studies. Nucl Recept Signal 4:1–10
27. Cleren C, Calingasan NY, Chen J, Beal MF (2005) Celastrol protects against MPTP- and 3-nitropropionic acid-induced neurotoxicity. J Neurochem 94:995–1004
28. Cornelius C, Perrotta R, Graziano A, Calabrese EJ, Calabrese V (2013) Stress responses, vitagenes and hormesis as critical determinants in aging and longevity: mitochondria as a “chi”. Immun Ageing 10:15
29. Cornelius C, Koverech G, Crupi R, Di Paola R, Koverech A, Lodato F, Scuto M, Salinaro AT, Cuzzocrea S, Calabrese EJ, Calabrese V (2014) Osteoporosis and Alzheimer pathology: role of cellular stress response and hormetic redox signaling in aging and bone remodeling. Front Pharmacol 5:120
30. Corson TW, Crews CM (2007) Molecular understanding and modern application of traditional medicines: triumphs and trials. Cell 130:769–774
31. Currò M, Trovato-Salinaro A, Gugliandolo A, Koverech G, Lodato F, Caccamo D, Calabrese V, Ientile R (2014) Resveratrol protects against homocysteine-induced cell damage via cell stress response in neuroblastoma cells. J Neurosci Res. doi:10.1002/jnr.23453 [Epub ahead of print]
32. Davinelli S, Scapagnini G, Denaro F, Calabrese V, Benedetti F, Krishnan S, Curreli S, Bryant J, Zella D (2014) Altered expression pattern of Nrf2/HO-1 axis during accelerated-senescence in HIV-1 transgenic rat. Biogerontology. doi:10.1007/s10522-014-9511-6, Epub 2014 Jul 16
33. De Long MJ, Prochaska HJ, Talalay P (1985) Tissue-specific induction patterns of cancer-protective enzymes in mice by tert-butyl-4-hydroxyanisole and related substituted phenols. Cancer Res 45:546–551
34. Der Sarkissian S, Cailhier JF, Borie M, Stevens LM, Gaboury L, Mansour S, Hamet P, Noiseux N (2014) Celastrol protects ischemic myocardium through heat shock response with upregulation of heme oxygenase-1. Br J Pharmacol. Epub ahead of print
35. Di Domenico F, Perluigi M, Butterfield DA, Cornelius C, Calabrese V (2010) Oxidative damage in Rat brain during aging: interplay between energy and metabolic Key target proteins. Neurochem Res 35:2184–2192
36. Di Paola R, Impellizzeri D, Trovato Salinaro A, Mazzon E, Bellia F, Cavallaro M, Cornelius C, Vecchio G, Calabrese V, Rizzarelli E, Cuzzocrea S (2011) Administration of carnosine in the treatment of acute spinal cord injury. Biochem Pharmacol 82:1478–1489
37. Dinkova-Kostova AT (2008) The isothiocyanate sulforaphane induces the phase 2 response by signaling of the Keap1-Nrf2-ARE pathway: Implications for dietary protection against cancer. In: Dietary Modulation of Cell Signaling Pathways, edited by YJ Surh, Z. Dong, E. Cadenas and L. Packer, pp. 205–229
38. Dinkova-Kostova AT, Talalay P (2000) Persuasive evidence that quinone reductase type 1 (DT diaphorase) protects cells against the toxicity of electrophiles and reactive forms of oxygen. Free Radic Biol Med 29:231–240
39. Dinkova-Kostova AT, Massiah MA, Bozak RE, Hicks RJ, Talalay P (2001) Potency of Michael reaction acceptors as inducers of enzymes that protect against carcinogenesis depends on their reactivity with sulfhydryl groups. Proc Natl Acad Sci U S A 98:3404–3409
40. Dinkova-Kostova AT, Fahey JW, Talalay P (2004) Chemical structures of inducers of nicotinamide quinone oxidoreductase 1 (NQO1). Methods Enzymol 382:423–448
41. Dwyer BE, Nishimura RN, Lu SY (1995) Differential expression of heme oxygenase-1 in cultured cortical neurons and astrocytes determined by the aid of a new heme oxygenase antibody. Response to oxidative stress. Brain Res Mol Brain Res 30:37–47
42. Ewing JF, Maines MD (2006) Regulation and expression of heme oxygenase enzymes in aged-rat brain: age related depression in HO-1 and HO-2 expression and altered stressresponse. J Neural Transm 113:439–454
43. FDA Consumer Health Information. Bio-identicals: sorting myths from facts. http://www.fda.gov/ForConsumers/ConsumerUpdates/ucm049311.htm
44. Fujimoto M, Hayashida N, Katoh T, Oshima K, Shinkawa T, Prakasam R, Tan K, Inouye S, Takii R, Nakai A (2010) A novel mouse HSF3 has the potential to activate nonclassical heat-shock genes during heat shock. Mol Biol Cell 21:106–116
45. Handelsman DJ (2004) Trends and regional differences in testosterone prescribing in Australia, 1991–2001. Med J Aust 181:419–422
46. Hunt PR, Son TG, Wilson MA, Yu QS, Wood WH, Zhang Y, Becker KG, Greig NH, Mattson MP, Camandola S, Wolkow CA (2011) Extension of lifespan in C. elegans by naphthoquinones that act through stress hormesis mechanisms. PLoS One e21922. doi: 10.1371/journal.pone.0021922
47. Inagaki T, Gautreaux C, Luine V (2010) Acute estrogen treatment facilitates recognition memory consolidation and alters monoamine levels in memory-related brain areas. Horm Behav 58:415–426
48. Innamorato NG, Rojo AI, García-Yagüe AJ, Yamamoto M, de Ceballos ML, Cuadrado A (2008) The transcription factor Nrf2 is a therapeutic target against brain inflammation. J Immunol 181:680–689
49. Itoh K, Chiba T, Takahashi S, Ishii T, Igarashi K, Katoh Y, Oyake T, Hayashi N, Satoh K, Hatayama I, Yamamoto M, Nabeshima Y (1996) An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun 236:313–322
50. Kang MJ, Kim HJ, Kim HK, Lee JY, Kim DH, Jung KJ, Kim KW, Baik HS, Yoo MA, Yu BP, Chung HY (2005) The effect of age and calorie restriction on HIF-1-responsive genes in aged liver. Biogerontology 6:27–37
51. Kappos L, Gold R, Miller DH, Macmanus DG, Havrdova E, Limmroth V, Polman CH, Schmierer K, Yousry TA, Yang M, Eraksoy M, Meluzinova E, Rektor I, Dawson KT, Sandrock AW, O’Neill GN (2008) BG-12 Phase IIb Study Investigators. Efficacy and safety of oral fumarate in patients with relapsing-remitting multiple sclerosis: a multicentre, randomised, double-blind, placebo-controlled phase IIb study. Lancet 372:1463–1472
52. Kitamuro T, Takahashi K, Ogawa K, Udono-Fujimori R, Takeda K, Furuyama K, Nakayama M, Sun J, Fujita H, Hida W, Hattori T, Shirato K, Igarashi K, Shibahara S (2003) Bach1 functions as a hypoxia-inducible repressor for the heme oxygenase-1 gene in human cells. J Biol Chem 278:9125–9133
53. Kuroda K, Akao M (1980) Reduction by fumaric acid of side effects of mitomycin C. Biochem Pharmacol 29:2839–2844
54. Kuroda K, Takagi K (1968) Physiologically active substance in Capsella bursa-pastoris. Nature 220:707–708
55. Lavrovsky Y, Song CS, Chatterjee B, Roy AK (2000) Agedependent increase of heme oxygenase-1 gene expression in the liver mediated by NFkappaB. Mech Ageing Dev 114:49–60
56. Lee JM, Li J, Johnson DA, Stein TD, Kraft AD, Calkins MJ, Jakel RJ, Johnson JA (2005) Nrf2, a multi-organ protector? FASEB J 19:1061–1066
57. Lipton SA (2007) Pathologically activated therapeutics for neuroprotection. Nat Rev Neurosci 8:803–808
58. Mancuso C, Santangelo R, Calabrese V (2013) The heme oxygenase/biliverdin reductase system: a potential drug target in Alzheimer’s disease. J Biol Regul Homeost Agents 27:75–87
59. Matsuoka Y, Okazaki M, Kitamura Y (1999) Induction of inducible heme oxygenase (HO-1) in the central nervous system: is HO-1 helpful or harmful? Neurotox Res 1:113–117
60. McMahon M, Thomas N, Itoh K, Yamamoto M, Hayes JD (2006) Dimerization of substrate adaptors can facilitate Cullin-mediated ubiquitylation of proteins by a “tethering” mechanism: a two-site interaction model for the Nrf2-Keap1 complex. J Biol Chem 281:24756–24768
61. Morse D, Choi AM (2002) Heme oxygenase-1: the “emerging molecule” has arrived. Am J Respir Cell Mol Biol 27:8–16
62. Motohashi H, Yamamoto M (2004) Nrf2-Keap1 defines a physiologically important stress response mechanism. Trends Mol Med 10:549–557
63. Motterlini R, Foresti R, Bassi R, Green CJ (2000) Curcumin, an antioxidant and anti-inflammatory agent, induces heme oxygenase-1 and protects endothelial cells against oxidative stress. Free Radic Biol Med 28:1303–1312
64. Patriarca S, Furfaro AL, Cosso L, Pesce Maineri E, Balbis E, Domenicotti C, Nitti M, Cottalasso D, Marinari UM, Pronzato MA, Traverso N (2007) Heme oxygenase 1 expression in rat liver during ageing and ethanol intoxication. Biogerontology 8:365–372
65. Pennisi G, Cornelius C, Cavallaro MM, Trovato Salinaro A, Cambria MT, Pennisi M, Bella R, Milone P, Ventimiglia B, Migliore MR, Di Renzo L, De Lorenzo A, Calabrese V (2011) Redox regulation of cellular stress response in multiple sclerosis. Biochem Pharmacol 82:1490–1499
66. Perluigi M, Joshi G, Sultana R, Calabrese V, De Marco C, Coccia R, Cini C, Butterfield DA (2006) In vivo protective effects of ferulic acid ethyl ester against amyloid-beta peptide 1-42-induced oxidative stress. J Neurosci Res 84:418–426
67. Perluigi M, Di Domenico F, Giorgi A, Schininà ME, Coccia R, Cini C, Bellia F, Cambria MT, Cornelius C, Butterfield DA, Calabrese V (2010) Redox proteomics in aging rat brain: involvement of mitochondrial reduced glutathione status and mitochondrial protein oxidation in the aging process. J Neurosci Res 88:3498–3507
68. Prochaska HJ, Santamaria AB (1988) Direct measurement of NAD(P)H:quinone reductase from cells cultured in microtiter wells: a screening assay for anticarcinogenic enzyme inducers. Anal Biochem 169:328–336
69. Prochaska HJ, De Long MJ, Talalay P (1985) On the mechanisms of induction of cancer-protective enzymes: a unifying proposal. Proc Natl Acad Sci U S A 82:8232–8236
70. Ryter SW, Alam J, Choi AM (2006) Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 86:583–650
71. Satoh T, Lipton SA (2007) Redox regulation of neuronal survival mediated by electrophilic compounds. Trends Neurosci 30:37–45
72. Satoh T, Kosaka K, Itoh K, Kobayashi A, Yamamoto M, Shimojo Y, Kitajima C, Cui J, Kamins J, Okamoto S, Izumi M, Shirasawa T, Lipton SA (2008) Carnosic acid, a catechol-type electrophilic compound, protects neurons both in vitro and in vivo through activation of the Keap1/Nrf2 pathway via S-alkylation of targeted cysteines on Keap1. J Neurochem 104:1116–1131
73. Satoh T, Saitoh S, Hosaka M, Kosaka K (2009) Simple ortho- and para-hydroquinones as compounds neuroprotective against oxidative stress in a manner associated with specific transcriptional activation. Biochem Biophys Res Commun 379:537–541
74. Scapagnini G, Butterfield DA, Colombrita C, Sultana R, Pascale A, Calabrese V (2004) Ethyl Ferulate, a Lipophilic Polyphenol, Induces HO-1 and Protects Rat Neurons Against Oxidative Stress. Antioxid Redox Signal 6:811–818
75. Scapagnini G, Colombrita C, Amadio M, D’Agata V, Arcelli E, Sapienza M, Quattrone A, Calabrese V (2006) Curcumin activates defensive genes and protects neurons against oxidative stress. Antioxid Redox Signal 8:395–403
76. Scapagnini G, Caruso C, Calabrese V (2011) Therapeutic potential of dietary polyphenols against brain ageing and neurodegenerative disorders. Adv Exp Med Biol 698:27–35
77. Schilling S, Goelz S, Linker R, Luehder F, Gold R (2006) Fumaric acid esters are effective in chronic experimental autoimmune encephalomyelitis and suppress macrophage infiltration. Clin Exp Immunol 145:101–107
78. Schimrigk S, Brune N, Hellwig K, Lukas C, Bellenberg B, Rieks M, Hoffmann V, Pöhlau D, Przuntek H (2006) Oral fumaric acid esters for the treatment of active multiple sclerosis: an open-label, baseline-controlled pilot study. Eur J Neurol 13:604–610
79. Schipper HM (2000) Heme oxygenase-1: role in brain aging and neurodegeneration. Exp Gerontol 35:821–830
80. Sethi G, Ahn KS, Pandey MK, Aggarwal BB (2007) Celastrol, a novel triterpene, potentiates TNF-induced apoptosis and suppresses invasion of tumor cells by inhibiting NF-kappaB-regulated gene products and TAK1-mediated NF-kB activation. Blood 109:2727–2735
81. Siciliano R, Barone E, Calabrese V, Rispoli V, Butterfield DA, Mancuso C (2011) Experimental research on nitric oxide and the therapy of Alzheimer disease: a challenging bridge. CNS Neurol Disord Drug Targets 10:766–776
82. Siebert A, Desai V, Chandrasekaran K, Fiskum G, Jafri MS (2009) Nrf2 activators provide neuroprotection against 6-hydroxydopamine toxicity in rat organotypic nigrostriatal cocultures. J Neurosci Res 87:1659–1669
83. Sparnins VL, Barany G, Wattenberg LW (1988) Effects of organosulfur compounds from garlic and onions on benzo[a]pyrene-induced neoplasia and glutathione S-transferase activity in the mouse. Carcinogenesis 9:131–134
84. Spencer SR, Wilczak CA, Talalay P (1990) Induction of glutathione transferases and NAD(P)H:quinone reductase by fumaric acid derivatives in rodent cells and tissues. Cancer Res 50:7871–7875
85. Stoof TJ, Flier J, Sampat S, Nieboer C, Tensen CP, Boorsma DM (2001) The antipsoriatic drug dimethylfumarate strongly suppresses chemokine production in human keratinocytes and peripheral blood mononuclear cells. Br J Dermatol 144:1114–11120
86. Sun MM, Bu H, Li B, Yu JX, Guo YS, Li CY (2009) Neuroprotective potential of phase II enzyme inducer diallyl trisulfide. Neurol Res 31:23–27
87. Talalay P (2000) Chemoprotection against cancer by induction of phase 2 enzymes. Biofactors 12:5–11
88. Talalay P, Dinkova-Kostova AT, Holtzclaw WD (2003) Importance of phase 2 gene regulation in protection against electrophile and reactive oxygen toxicity and carcinogenesis. Adv Enzym Regul 43:121–134
89. Tenhunen R, Marver HS, Schmid R (1968) The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc Natl Acad Sci U S A 61:748–755
90. Trott A, West JD, Klaić L, Westerheide SD, Silverman RB, Morimoto RI, Morano KA (2008) Activation of heat shock and antioxidant responses by the natural product celastrol: transcriptional signatures of a thiol-targeted molecule. Mol Biol Cell19:1104–1112
91. Trovato Salinaro A, Cornelius C, Koverech G, Koverech A, Scuto M, Lodato F, Fronte V, Muccilli V, Reibaldi M, Longo A, Uva MG, Calabrese V (2014) Cellular stress response, redox status, and vitagenes in glaucoma: a systemic oxidant disorder linked to Alzheimer’s disease. Front Pharmacol 5:129
92. Viñas R, Jeng YJ, Watson CS (2012) Non-genomic effects of xenoestrogen mixtures. Int J Environ Res Public Health 9:2694–2714
93. Wang C, Nieschlag E, Swerdloff R, Behre HM, Hellstrom WJ, Gooren LJ, Kaufman JM, Legros JJ, Lunenfeld B, Morales A, Morley JE, Schulman C, Thompson IM, Weidner W, Wu FC (2008) Investigation, treatment and monitoring of late-onset hypogonadism in males: ISA, ISSAM, EAU, EAA and ASA recommendations. Eur J Endocrinol 159:507–514
94. Westerheide SD, Raynes R, Powell C, Xue B, Uversky VN (2012) HSF transcription factor family, heat shock response, and protein intrinsic disorder. Curr Protein Pept Sci 13:86–103
95. Yang F, Lim GP, Begum AN, Ubeda OJ, Simmons MR, Ambegaokar SS, Chen PP, Kayed R, Glabe CG, Frautschy SA, Cole GM (2005) Curcumin inhibits formation of amyloid beta oligomers and fibrils, binds plaques, and reduces amyloid in vivo. J Biol Chem 280:5892–5901
96. Zhang Y, Ahn YH, Benjamin IJ, Honda T, Hicks RJ, Calabrese V, Cole PA, Dinkova-Kostova AT (2011) HSF1-dependent upregulation of Hsp70 by sulfhydryl-reactive inducers of the KEAP1/NRF2/ARE pathway. Chem Biol 18:1355–1361
97. Zhao J, Moore AN, Clifton GL, Dash PK (2005) Sulforaphane enhances aquaporin-4 expression and decreases cerebral edema following traumatic brain injury. J Neurosci Res 82:499–506
98. Zhao J, Kobori N, Aronowski J, Dash PK (2006) Sulforaphane reduces infarct volume following focal cerebral ischemia in rodents. Neurosci Lett 393:108–112
99. Zhao J, Moore AN, Redell JB, Dash PK (2007a) Enhancing expression of Nrf2-driven genes protects the blood brain barrier after brain injury. J Neurosci 27:10240–10248
100. Zhao X, Sun G, Zhang J, Strong R, Dash PK, Kan YW, Grotta JC, Aronowski J (2007b) Transcription factor Nrf2 protects the brain from damage produced by intracerebral hemorrhage. Stroke 38:3280–3286