Sulforaphane as a Potential protective phytochemical against neurodegenerative diseases

Oxidative Medicine and Cellular Longevity

Volumn , Issue , 2013, Pages

  Tarozzi, Andrea ^a   Angeloni, Cristina ^a   Malaguti, Marco ^a   Morroni, Fabiana ^a   Hrelia, Silvana ^a   Hrelia, Patrizia ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ALZHEIMER'S DISEASE; BENEFICIAL EFFECTS; BRASSICA VEGETABLES; INTERVENTION STRATEGY; MISFOLDED PROTEINS; NEUROLOGICAL DISORDERS; NEUROPROTECTIVE EFFECTS; PARKINSON'S DISEASE;

CELL CULTURE; HEALTH CARE; MEDICINE;

NEURODEGENERATIVE DISEASES;

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; ACETYLCYSTEINE; ALPHA SYNUCLEIN; AQUAPORIN 4; CARBONYL DERIVATIVE; CYSTEINYLGLYCINE; DOPAMINE; GLUCOSINOLATE; GLUTAMIC ACID; GLUTATHIONE; GLUTATHIONE TRANSFERASE; HEAT SHOCK PROTEIN 27; HYDROGEN PEROXIDE; ISOTHIOCYANIC ACID; KELCH LIKE ECH ASSOCIATED PROTEIN 1; PEROXIREDOXIN; PROTEIN; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; SULFORAPHANE; TETRAHYDROBIOPTERIN; TRANSCRIPTION FACTOR NRF2; GLUCORAPHANIN; IMIDOESTER; ISOTHIOCYANIC ACID DERIVATIVE; NEUROPROTECTIVE AGENT; SULFORAFAN; THIOCYANIC ACID DERIVATIVE;

ALZHEIMER DISEASE; ANTIOXIDANT RESPONSIVE ELEMENT; APOPTOSIS; BLOOD CEREBROSPINAL FLUID BARRIER; BRAIN EDEMA; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; BRASSICA; BROCCOLI; CELL DEATH; COGNITION; CYTOTOXICITY; DEGENERATIVE DISEASE; DOPAMINERGIC NERVE CELL; DRUG ABSORPTION; DRUG BIOAVAILABILITY; DRUG TRANSFORMATION; ENZYME ACTIVITY; EXCITOTOXICITY; GENE EXPRESSION; HUMAN; HYDROLYSIS; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; INTRACELLULAR SIGNALING; LEWY BODY; LIPOPHILICITY; MEMBRANE PERMEABILITY; MOLECULAR SIZE; NERVE CELL; NERVE DEGENERATION; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PHYTOCHEMISTRY; PREFRONTAL CORTEX; PROTEIN FOLDING; REVIEW; SIGNAL TRANSDUCTION; SUBSTANTIA NIGRA PARS COMPACTA; TRAUMATIC BRAIN INJURY; VEGETABLE; WORKING MEMORY; ANIMAL; DRUG EFFECT; DRUG EFFECTS; NEURODEGENERATIVE DISEASES;

ANIMALS; GLUCOSINOLATES; HUMANS; IMIDOESTERS; ISOTHIOCYANATES; NEURODEGENERATIVE DISEASES; NEUROPROTECTIVE AGENTS; OXIDATIVE STRESS; THIOCYANATES;

EID: 84881494802     PISSN: 19420900     EISSN: 19420994     Source Type: Journal    
DOI: 10.1155/2013/415078     Document Type: Review

References (124)

1. Ritchie K., Lovestone S., The dementias. The Lancet 2002 360 9347 1759 1766 2-s2.0-0037202852 10.1016/S0140-6736(02)11667-9 (Pubitemid 35447916)
2. Akhlaq A., Farooqui A., Neurochemical Aspects of Neurotraumatic and Neurodegenerative Diseases 2010 Springer
3. Mandel S., Grünblatt E., Riederer P., Gerlach M., Levites Y., Youdim M. B. H., Neuroprotective strategies in Parkinson's disease: an update on progress. CNS Drugs 2003 17 10 729 762 2-s2.0-0041731997 10.2165/00023210- 200317100-00004 (Pubitemid 37000010)
4. Dauer W., Przedborski S., Parkinson's disease: mechanisms and models. Neuron 2003 39 6 889 909 2-s2.0-0141741347 10.1016/S0896-6273(03)00568-3 (Pubitemid 37130207)
5. Lee P. C., Bordelon Y., Bronstein J., Ritz B., Traumatic brain injury, paraquat exposure, and their relationship to Parkinson disease. Neurology 2012 79 20 2061 2066 10.1212/WNL.0b013e3182749f28
6. Campdelacreu J., Parkinson disease and Alzheimer disease: environmental risk factors. Neurologia. In press
7. Pluta R., From brain ischemia-reperfusion injury to possible sporadic Alzheimer's disease. Current Neurovascular Research 2004 1 5 441 453 2-s2.0-27744583160
8. Middleton E. Jr., Effect of plant flavonoids on immune and inflammatory cell function. Advances in Experimental Medicine and Biology 1998 439 175 182 2-s2.0-0031708667 (Pubitemid 28429016)
9. Hollman P. C. H., Katan M. B., Health effects and bioavailability of dietary flavonols. Free Radical Research 1999 31, supplement S75 S80 2-s2.0-0033387699
10. Eastwood M. A., Interaction of dietary antioxidants in vivo: how fruit and vegetables prevent disease? Quarterly Journal of Medicine 1999 92 9 527 530 2-s2.0-0032824007 10.1093/qjmed/92.9.527 (Pubitemid 29430051)
11. Matusheski N. V., Juvik J. A., Jeffery E. H., Heating decreases epithiospecifier protein activity and increases sulforaphane formation in broccoli. Phytochemistry 2004 65 9 1273 1281 2-s2.0-2942614968 10.1016/j.phytochem.2004.04.013 (Pubitemid 38746674)
12. Cooper D. A., Webb D. R., Peters J. C., Evaluation of the potential for olestra to affect the availability of dietary phytochemicals. Journal of Nutrition 1997 124 8 1699S 1709S 2-s2.0-0031459258 (Pubitemid 27329540)
13. Winiwarter S., Bonham N. M., Ax F., Hallberg A., Lennernäs H., Karlén A., Correlation of human jejunal permeability (in vivo) of drugs with experimentally and theoretically derived parameters. A multivariate data analysis approach. Journal of Medicinal Chemistry 1998 41 25 4939 4949 2-s2.0-0032480901 10.1021/jm9810102 (Pubitemid 28555452)
14. Zhang Y., Callaway E. C., High cellular accumulation of sulphoraphane, a dietary anticarcinogen, is followed by rapid transporter-mediated export as a glutathione conjugate. Biochemical Journal 2002 364, part 1 301 307 2-s2.0-0037093463 (Pubitemid 34538974)
15. Kassahun K., Davis M., Hu P., Martin B., Baillie T., Biotransformation of the naturally occurring isothiocyanate sulforaphane in the rat: identification of phase I metabolites and glutathione conjugates. Chemical Research in Toxicology 1997 10 11 1228 1233 2-s2.0-0030781225 10.1021/tx970080t (Pubitemid 27524827)
16. Gasper A. V., Al-Janobi A., Smith J. A., Bacon J. R., Fortun P., Atherton C., Taylor M. A., Hawkey C. J., Barrett D. A., Mithen R. F., Glutathione S-transferase M1 polymorphism and metabolism of sulforaphane from standard and high-glucosinolate broccoli. American Journal of Clinical Nutrition 2005 82 6 1283 1291 2-s2.0-33644688761 (Pubitemid 43779728)
17. Shapiro T. A., Fahey J. W., Wade K. L., Stephenson K. K., Talalay P., Chemoprotective glucosinolates and isothiocyanates of broccoli sprouts: metabolism and excretion in humans. Cancer Epidemiology Biomarkers and Prevention 2001 10 5 501 508 2-s2.0-0034928041 (Pubitemid 32701637)
18. Egner P. A., Chen J. G., Wang J. B., Wu Y., Sun Y., Lu J. H., Zhu J., Zhang Y. H., Chen Y. S., Friesen M. D., Jacobson L. P., Muñoz A., Ng D., Qian G. S., Zhu Y. R., Chen T. Y., Botting N. P., Zhang Q., Fahey J. W., Talalay P., Groopman J. D., Kensler T. W., Bioavailability of sulforaphane from two broccoli sprout beverages: results of a short-term, cross-over clinical trial in Qidong, China. Cancer Prevention Research 2011 4 3 384 395 2-s2.0-79955834680 10.1158/1940-6207.CAPR-10-0296
19. Clarke J. D., Hsu A., Williams D. E., Dashwood R. H., Stevens J. F., Yamamoto M., Ho E., Metabolism and tissue distribution of sulforaphane in Nrf2 knockout and wild-type mice. Pharmaceutical Research 2011 28 12 3171 3179 2-s2.0-83555173511 10.1007/s11095-011-0500-z
20. Dinkova-Kostova A. T., Kostov R. V., Glucosinolates and isothiocyanates in health and disease. Trends in Molecular Medicine 2012 18 6 337 347 2-s2.0-84860641070 10.1016/j.molmed.2012.04.003
21. Veeranki O. L., Bhattacharya A., Marshall J. R., Zhang Y., Organ-specific exposure and response to sulforaphane, a key chemopreventive ingredient in broccoli: implications for cancer prevention. British Journal of Nutrition 2013 109 1 25 32 10.1017/S0007114512000657
22. Myzak M. C., Karplus P. A., Chung F.-L., Dashwood R. H., A novel mechanism of chemoprotection by sulforaphane: inhibition of histone deacetylase. Cancer Research 2004 64 16 5767 5774 2-s2.0-4143130097 10.1158/0008-5472.CAN- 04-1326 (Pubitemid 39095576)
23. Hwang E. S., Jeffery E. H., Induction of quinone reductase by sulforaphane and sulforaphane N-acetylcysteine conjugate in murine hepatoma cells. Journal of Medicinal Food 2005 8 2 198 203 2-s2.0-22444438840 10.1089/jmf.2005.8.198 (Pubitemid 41008983)
24. Tang L., Li G., Song L., Zhang Y., The principal urinary metabolites of dietary isothiocyanates, N-acetylcysteine conjugates, elicit the same anti-proliferative response as their parent compounds in human bladder cancer cells. Anti-Cancer Drugs 2006 17 3 297 305 2-s2.0-33646087882 10.1097/00001813-200603000-00008
25. Clarke J. D., Hsu A., Riedl K., Bella D., Schwartz S. J., Stevens J. F., Ho E., Bioavailability and inter-conversion of sulforaphane and erucin in human subjects consuming broccoli sprouts or broccoli supplement in a cross-over study design. Pharmacological Research 2011 64 5 456 463 2-s2.0-80054979844 10.1016/j.phrs.2011.07.005
26. Saha S., Hollands W., Teucher B., Isothiocyanate concentrations and interconversion of sulforaphane to erucin in human subjects after consumption of commercial frozen broccoli compared to fresh broccoli. Molecular Nutrition & Food Research 2012 56 12 1906 1916 10.1002/mnfr.201200225
27. Jakubíková J., Sedlák J., Mithen R., Bao Y., Role of PI3K/Akt and MEK/ERK signaling pathways in sulforaphane- and erucin-induced phase II enzymes and MRP2 transcription, G2/M arrest and cell death in Caco-2 cells. Biochemical Pharmacology 2005 69 11 1543 1552 2-s2.0-19344367171 10.1016/j.bcp.2005.03.015 (Pubitemid 40719490)
28. Hanlon N., Coldham N., Sauer M. J., Ioannides C., Modulation of rat pulmonary carcinogen-metabolising enzyme systems by the isothiocyanates erucin and sulforaphane. Chemico-Biological Interactions 2009 177 2 115 120 2-s2.0-57649184041 10.1016/j.cbi.2008.08.015
29. Melchini A., Costa C., Traka M., Miceli N., Mithen R., de Pasquale R., Trovato A., Erucin, a new promising cancer chemopreventive agent from rocket salads, shows anti-proliferative activity on human lung carcinoma A549 cells. Food and Chemical Toxicology 2009 47 7 1430 1436 2-s2.0-67349224103 10.1016/j.fct.2009.03.024
30. Jazwa A., Rojo A. I., Innamorato N. G., Hesse M., Fernández-Ruiz J., Cuadrado A., Pharmacological targeting of the transcription factor NRf2 at the basal ganglia provides disease modifying therapy for experimental parkinsonism. Antioxidants and Redox Signaling 2011 14 12 2347 2360 2-s2.0-79957515007 10.1089/ars.2010.3731
31. Melo A., Monteiro L., Lima R. M. F., de Oliveira D. M., de Cerqueira M. D., El-Bachá R. S., Oxidative stress in neurodegenerative diseases: mechanisms and therapeutic perspectives. Oxidative Medicine and Cellular Longevity 2011 2011 14 2-s2.0-84855584833 10.1155/2011/467180 467180
32. Halliwell B., Reactive oxygen species and the central nervous system. Journal of Neurochemistry 1992 59 5 1609 1623 2-s2.0-0026754574 10.1111/j.1471-4159.1992.tb10990.x
33. Hamilton M. L., van Remmen H., Drake J. A., Yang H., Guo Z. M., Kewitt K., Walter C. A., Richardson A., Does oxidative damage to DNA increase with age? Proceedings of the National Academy of Sciences of the United States of America 2001 98 18 10469 10474 2-s2.0-0035964315 10.1073/pnas.171202698 (Pubitemid 32803043)
34. Aruoma O. I., Neuroprotection by dietary antioxidants: new age of research. Nahrung 2002 46 6 381 382 2-s2.0-0036982645
35. Nguyen T., Huang H. C., Pickett C. B., Transcriptional regulation of the antioxidant response element. Activation by Nrf2 and repression by MafK. The Journal of Biological Chemistry 2000 275 20 15466 15473 2-s2.0-0034685897 10.1074/jbc.M000361200 (Pubitemid 30337278)
36. Itoh K., Chiba T., Takahashi S., Ishii T., Igarashi K., Katoh Y., Oyake T., Hayashi N., Satoh K., Hatayama I., Yamamoto M., Nabeshima Y.-I., An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochemical and Biophysical Research Communications 1997 236 2 313 322 2-s2.0-0031577292 10.1006/bbrc.1997.6943 (Pubitemid 27373291)
37. Jin W., Wang H., Yan W., Xu L., Wang X., Zhao X., Yang X., Chen G., Ji Y., Disruption of Nrf2 enhances upregulation of nuclear factor- B activity, proinflammatory cytokines, and intercellular adhesion molecule-1 in the brain after traumatic brain injury. Mediators of Inflammation 2008 2008 7 2-s2.0-59549099432 10.1155/2008/725174 725174
38. Murphy T. H., de Long M. J., Coyle J. T., Enhanced NAD(P)H: quinone reductase activity prevents glutamate toxicity produced by oxidative stress. Journal of Neurochemistry 1991 56 3 990 995 2-s2.0-0026062165 (Pubitemid 21922713)
39. Duffy S., So A., Murphy T. H., Activation of endogenous antioxidant defenses in neuronal cells prevents free radical-mediated damage. Journal of Neurochemistry 1998 71 1 69 77 2-s2.0-0031866279 (Pubitemid 28292536)
40. Li J., Lee J. M., Johnson J. A., Microarray analysis reveals an antioxidant responsive element-driven gene set involved in conferring protection from an oxidative stress-induced apoptosis in IMR-32 cells. The Journal of Biological Chemistry 2002 277 1 388 394 2-s2.0-0037016759 10.1074/jbc.M109380200 (Pubitemid 34952070)
41. Juge N., Mithen R. F., Traka M., Molecular basis for chemoprevention by sulforaphane: a comprehensive review. Cellular and Molecular Life Sciences 2007 64 9 1105 1127 2-s2.0-34247606510 10.1007/s00018-007-6484-5 (Pubitemid 46684547)
42. Dinkova-Kostova A. T., Talalay P., Direct and indirect antioxidant properties of inducers of cytoprotective proteins. Molecular Nutrition and Food Research 2008 52 supplement 1 S128 S138 2-s2.0-52449089630 10.1002/mnfr. 200700195
43. Angeloni C., Leoncini E., Malaguti M., Angelini S., Hrelia P., Hrelia S., Modulation of phase II enzymes by sulforaphane: implications for its cardioprotective potential. Journal of Agricultural and Food Chemistry 2009 57 12 5615 5622 2-s2.0-67649197558 10.1021/jf900549c
44. Dinkova-Kostova A. T., Holtzclaw W. D., Cole R. N., Itoh K., Wakabayashi N., Katoh Y., Yamamoto M., Talalay P., Direct evidence that sulfhydryl groups of Keap1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidants. Proceedings of the National Academy of Sciences of the United States of America 2002 99 18 11908 11913 2-s2.0-0037015035 10.1073/pnas.172398899 (Pubitemid 34994497)
45. Negi G., Kumar A., Sharma S. S., Nrf2 and NF- B modulation by sulforaphane counteracts multiple manifestations of diabetic neuropathy in rats and high glucose-induced changes. Current Neurovascular Research 2011 8 4 294 304 2-s2.0-82155197554 10.2174/156720211798120972
46. Mas S., Gassó P., Trias G., Bernardo M., Lafuente A., Sulforaphane protects SK-N-SH cells against antipsychotic-induced oxidative stress. Fundamental & Clinical Pharmacology 2012 26 6 712 721 2-s2.0-80053449289 10.1111/j.1472-8206.2011.00988.x
47. Mizuno K., Kume T., Muto C., Takada-Takatori Y., Izumi Y., Sugimoto H., Akaike A., Glutathione biosynthesis via activation of the nuclear factor E2-related factor 2 (Nrf2)-antioxidant-response element (ARE) pathway is essential for neuroprotective effects of sulforaphane and 6-(methylsulfinyl) hexyl isothiocyanate. Journal of Pharmacological Sciences 2011 115 3 320 328 2-s2.0-79952792525 10.1254/jphs.10257FP
48. Sánchez-Font M. F., Sebastià J., Sanfeliu C., Cristòfol R., Marfany G., Gonzàlez-Duarte R., Peroxiredoxin 2 (PRDX2), an antioxidant enzyme, is under-expressed in Down syndrome fetal brains. Cellular and Molecular Life Sciences 2003 60 7 1513 1523 2-s2.0-0041867880 10.1007/s00018-003-3048-1 (Pubitemid 36900532)
49. Talalay P., de Long M. J., Prochaska H. J., Identification of a common chemical signal regulating the induction of enzymes that protect against chemical carcinogenesis. Proceedings of the National Academy of Sciences of the United States of America 1988 85 21 8261 8265 2-s2.0-0344915418
50. Itoh K., Wakabayashi N., Katoh Y., Ishii T., Igarashi K., Engel J. D., Yamamoto M., Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes and Development 1999 13 1 76 86 2-s2.0-0032953192 (Pubitemid 29045117)
51. Baird L., Dinkova-Kostova A. T., The cytoprotective role of the Keap1-Nrf2 pathway. Archives of Toxicology 2011 85 4 241 272 2-s2.0-79954416526 10.1007/s00204-011-0674-5
52. Marini M. G., Chan K., Casula L., Kan Y. W., Cao A., Moi P., hMAF, a small human transcription factor that heterodimerizes specifically with Nrf1 and Nrf2. The Journal of Biological Chemistry 1997 272 26 16490 16497 2-s2.0-0030974478 10.1074/jbc.272.26.16490 (Pubitemid 27276476)
53. Yao J., Taylor M., Davey F., Ren Y., Aiton J., Coote P., Fang F., Chen J. X., Yan S. D., Gunn-Moore F. J., Interaction of amyloid binding alcohol dehydrogenase/A β mediates up-regulation of peroxiredoxin II in the brains of Alzheimer's disease patients and a transgenic Alzheimer's disease mouse model. Molecular and Cellular Neuroscience 2007 35 2 377 382 2-s2.0-34249720583 10.1016/j.mcn.2007.03.013 (Pubitemid 46843572)
54. Hattori F., Murayama N., Noshita T., Oikawa S., Mitochondrial peroxiredoxin-3 protects hippocampal neurons from excitotoxic injury in vivo. Journal of Neurochemistry 2003 86 4 860 868 2-s2.0-0042731713 10.1046/j.1471-4159.2003.01918.x (Pubitemid 36988798)
55. Boulos S., Meloni B. P., Arthur P. G., Bojarski C., Knuckey N. W., Peroxiredoxin 2 overexpression protects cortical neuronal cultures from ischemic and oxidative injury but not glutamate excitotoxicity, whereas Cu/Zn superoxide dismutase 1 overexpression protects only against oxidative injury. Journal of Neuroscience Research 2007 85 14 3089 3097 2-s2.0-35848954507 10.1002/jnr.21429 (Pubitemid 350057364)
56. Soriano F. X., Léveillé F., Papadia S., Higgins L. G., Varley J., Baxter P., Hayes J. D., Hardingham G. E., Induction of sulfiredoxin expression and reduction of peroxiredoxin hyperoxidation by the neuroprotective Nrf2 activator 3H-1,2-dithiole-3-thione. Journal of Neurochemistry 2008 107 2 533 543 2-s2.0-53149110452 10.1111/j.1471-4159.2008.05648.x
57. Han J. M., Lee Y. J., Lee S. Y., Protective effect of sulforaphane against dopaminergic cell death. Journal of Pharmacology and Experimental Therapeutics 2007 321 1 249 256 2-s2.0-33947379500 10.1124/jpet.106.110866 (Pubitemid 46456990)
58. Kraft A. D., Johnson D. A., Johnson J. A., Nuclear factor E2-related factor 2-dependent antioxidant response element activation by tert-butylhydroquinone and sulforaphane occurring preferentially in astrocytes conditions neurons against oxidative insult. Journal of Neuroscience 2004 24 5 1101 1112 2-s2.0-0842304134 10.1523/JNEUROSCI.3817-03.2004 (Pubitemid 38177017)
59. Innamorato N. G., Rojo A. I., García-Yagüe Á. J., Yamamoto M., de Ceballos M. L., Cuadrado A., The transcription factor Nrf2 is a therapeutic target against brain inflammation. The Journal of Immunology 2008 181 1 680 689 2-s2.0-47949083810
60. Navarro A., Boveris A., Brain mitochondrial dysfunction and oxidative damage in Parkinson's disease. Journal of Bioenergetics and Biomembranes 2009 41 6 517 521 2-s2.0-76949089544 10.1007/s10863-009-9250-6
61. Starkov A. A., Chinopoulos C., Fiskum G., Mitochondrial calcium and oxidative stress as mediators of ischemic brain injury. Cell Calcium 2004 36 3-4 257 264 2-s2.0-3342910554 10.1016/j.ceca.2004.02.012 (Pubitemid 38992351)
62. Niizuma K., Fujimura M., Takahashi T., Takahashi A., Watanabe M., Tominaga T., Exclusively extradural arteriovenous malformation with neurogenic claudication: case illustration. Journal of Neurosurgery 2004 100 4 397 2-s2.0-1642317839 (Pubitemid 38381250)
63. Greco T., Fiskum G., Brain mitochondria from rats treated with sulforaphane are resistant to redox-regulated permeability transition. Journal of Bioenergetics and Biomembranes 2010 42 6 491 497 2-s2.0-78751644875 10.1007/s10863-010-9312-9
64. Pun P. B. L., Lu J., Moochhala S., Involvement of ROS in BBB dysfunction. Free Radical Research 2009 43 4 348 364 2-s2.0-67650153191 10.1080/ 10715760902751902
65. Zhao J., Moore A. N., Redell J. B., Dash P. K., Enhancing expression of Nrf2-driven genes protects the blood-brain barrier after brain injury. Journal of Neuroscience 2007 27 38 10240 10248 2-s2.0-34548850603 10.1523/JNEUROSCI. 1683-07.2007 (Pubitemid 47450456)
66. Chen G., Fang Q., Zhang J., Zhou D., Wang Z., Role of the Nrf2-ARE pathway in early brain injury after experimental subarachnoid hemorrhage. Journal of Neuroscience Research 2011 89 4 515 523 2-s2.0-79751525643 10.1002/jnr.22577
67. Ott B. R., Cohen R. A., Gongvatana A., Okonkwo O. C., Johanson C. E., Stopa E. G., Donahue J. E., Silverberg G. D., Brain ventricular volume and cerebrospinal fluid biomarkers of Alzheimer's disease. Journal of Alzheimer's Disease 2010 20 2 647 657 2-s2.0-77954491973 10.3233/JAD-2010-1406
68. Xiang J., Alesi G. N., Zhou N., Keep R. F., Protective effects of isothiocyanates on blood-CSF barrier disruption induced by oxidative stress. American Journal of Physiology 2012 303 1 R1 R7 10.1152/ajpregu.00518.2011
69. Zhao J., Kobori N., Aronowski J., Dash P. K., Sulforaphane reduces infarct volume following focal cerebral ischemia in rodents. Neuroscience Letters 2006 393 2-3 108 112 2-s2.0-29244479186 10.1016/j.neulet.2005.09.065 (Pubitemid 41821089)
70. Ping Z., Liu W., Kang Z., Cai J., Wang Q., Cheng N., Wang S., Wang S., Zhang J. H., Sun X., Sulforaphane protects brains against hypoxic-ischemic injury through induction of Nrf2-dependent phase 2 enzyme. Brain Research 2010 1343 178 185 2-s2.0-77953620909 10.1016/j.brainres.2010.04.036
71. Soane L., Li Dai W., Fiskum G., Bambrick L. L., Sulforaphane protects immature hippocampal neurons against death caused by exposure to hemin or to oxygen and glucose deprivation. Journal of Neuroscience Research 2010 88 6 1355 1363 2-s2.0-77951526269 10.1002/jnr.22307
72. Danilov C. A., Chandrasekaran K., Racz J., Soane L., Zielke C., Fiskum G., Sulforaphane protects astrocytes against oxidative stress and delayed death caused by oxygen and glucose deprivation. Glia 2009 57 6 645 656 2-s2.0-65549118899 10.1002/glia.20793
73. Porritt M. J., Andersson H. C., Hou L., Photothrombosis-induced infarction of the mouse cerebral cortex is not affected by the Nrf2-activator sulforaphane. PLoS ONE 2012 7 7 e41090 10.1371/journal.pone.0041090
74. Srivastava S., Alfieri A., Siow R. C., Mann G. E., Fraser P. A., Temporal and spatial distribution of Nrf2 in rat brain following stroke: quantitation of nuclear to cytoplasmic Nrf2 content using a novel immunohistochemical technique. The Journal of Physiology 2013 10.1113/jphysiol.2013.257964
75. Maas A. I., Stocchetti N., Bullock R., Moderate and severe traumatic brain injury in adults. The Lancet Neurology 2008 7 8 728 741 2-s2.0-46849094295 10.1016/S1474-4422(08)70164-9 (Pubitemid 351957931)
76. Woodcock T., Morganti-Kossmann M. C., The role of markers of inflammation in traumatic brain injury. Frontiers in Neurology 2013 4 18 10.3389/fneur.2013.00018
77. Masel B. E., DeWitt D. S., Traumatic brain injury: a disease process, not an event. Journal of Neurotrauma 2010 27 8 1529 1540 2-s2.0-77955912778 10.1089/neu.2010.1358
78. Gaetz M., The neurophysiology of brain injury. Clinical Neurophysiology 2004 115 1 4 18 2-s2.0-0347990376 10.1016/S1388-2457(03)00258-X (Pubitemid 38045590)
79. Bramlett H. M., Dietrich W. D., Progressive damage after brain and spinal cord injury: pathomechanisms and treatment strategies. Progress in Brain Research 2007 161 125 141 2-s2.0-34347356395 10.1016/S0079-6123(06)61009-1 (Pubitemid 47017402)
80. Zhao J., Moore A. N., Clifton G. L., Dash P. K., Sulforaphane enhances aquaporin-4 expression and decreases cerebral edema following traumatic brain injury. Journal of Neuroscience Research 2005 82 4 499 506 2-s2.0-27644587832 10.1002/jnr.20649 (Pubitemid 41579349)
81. Manley G. T., Binder D. K., Papadopoulos M. C., Verkman A. S., New insights into water transport and edema in the central nervous system from phenotype analysis of aquaporin-4 null mice. Neuroscience 2004 129 4 983 991 2-s2.0-9344226163 10.1016/j.neuroscience.2004.06.088 (Pubitemid 39556249)
82. Hong Y., Yan W., Chen S., The role of Nrf2 signaling in the regulation of antioxidants and detoxifying enzymes after traumatic brain injury in rats and mice. Acta Pharmacologica Sinica 2010 31 11 1421 1430 2-s2.0-78149399227 10.1038/aps.2010.101
83. Dash P. K., Zhao J., Orsi S. A., Zhang M., Moore A. N., Sulforaphane improves cognitive function administered following traumatic brain injury. Neuroscience Letters 2009 460 2 103 107 2-s2.0-66949123850 10.1016/j.neulet. 2009.04.028
84. Benedict A. L., Mountney A., Hurtado A., Neuroprotective effects of sulforaphane after contusive spinal cord injury. Journal of Neurotrauma 2012 29 16 2576 2586 10.1089/neu.2012.2474
85. Tannenberg R. K., Scott H. L., Tannenberg A. E. G., Dodd P. R., Selective loss of synaptic proteins in Alzheimer's disease: evidence for an increased severity with APOE ε 4. Neurochemistry International 2006 49 7 631 639 2-s2.0-33750016561 10.1016/j.neuint.2006.05.004 (Pubitemid 44572565)
86. Querfurth H. W., LaFerla F. M., Alzheimer's disease. The New England Journal of Medicine 2010 362 4 329 344 2-s2.0-75449102536 10.1056/NEJMra0909142
87. Loewen C. A., Feany M. B., The unfolded protein response protects from tau neurotoxicity in vivo. PLoS ONE 2010 5 9 2-s2.0-77958529500 10.1371/journal.pone.0013084 e13084
88. Tarozzi A., Morroni F., Merlicco A., Bolondi C., Teti G., Falconi M., Cantelli-Forti G., Hrelia P., Neuroprotective effects of cyanidin 3-O-glucopyranoside on amyloid beta (25-35) oligomer-induced toxicity. Neuroscience Letters 2010 473 2 72 76 2-s2.0-77949914396 10.1016/j.neulet.2010. 02.006
89. Liu Y., Dargusch R., Banh C., Miller C. A., Schubert D., Detecting bioactive amyloid β peptide species in Alzheimer's disease. Journal of Neurochemistry 2004 91 3 648 656 2-s2.0-7244225197 10.1111/j.1471-4159.2004. 02751.x (Pubitemid 39431159)
90. Hoozemans J. J. M., Veerhuis R., van Haastert E. S., Rozemuller J. M., Baas F., Eikelenboom P., Scheper W., The unfolded protein response is activated in Alzheimer's disease. Acta Neuropathologica 2005 110 2 165 172 2-s2.0-24344489466 10.1007/s00401-005-1038-0 (Pubitemid 41245205)
91. Lopez Salon M., Morelli L., Castano E. M., Soto E. F., Pasquini J. M., Defective ubiquitination of cerebral proteins in Alzheimer's disease. Journal of Neuroscience Research 2000 62 2 302 310
92. Kwak M. K., Cho J. M., Huang B., Shin S., Kensler T. W., Role of increased expression of the proteasome in the protective effects of sulforaphane against hydrogen peroxide-mediated cytotoxicity in murine neuroblastoma cells. Free Radical Biology and Medicine 2007 43 5 809 817 2-s2.0-34547092719 10.1016/j.freeradbiomed.2007.05.029 (Pubitemid 47103310)
93. Park H. M., Kim J. A., Kwak M. K., Protection against amyloid beta cytotoxicity by sulforaphane: role of the proteasome. Archives of Pharmacal Research 2009 32 1 109 115 2-s2.0-59449100511 10.1007/s12272-009-1124-2
94. Gan N., Wu Y. C., Brunet M., Garrido C., Chung F.-L., Dai C., Mi L., Sulforaphane activates heat shock response and enhances proteasome activity through up-regulation of Hsp27. The Journal of Biological Chemistry 2010 285 46 35528 35536 2-s2.0-78149260516 10.1074/jbc.M110.152686
95. Kim H. V., Kim H. Y., Ehrlich H. Y., Choi S. Y., Kim D. J., Kim Y., Amelioration of Alzheimer's disease by neuroprotective effect of sulforaphane in animal model. Amyloid 2013 20 1 7 12
96. Dawson T. M., Dawson V. L., Molecular pathways of neurodegeneration in Parkinson's disease. Science 2003 302 5646 819 822 2-s2.0-0242363670 10.1126/science.1087753 (Pubitemid 37339614)
97. Calne S., Schoenberg B., Martin W., Uitti R. J., Spencer P., Calne D. B., Familial Parkinson's disease: possible role of environmental factors. Canadian Journal of Neurological Sciences 1987 14 3 303 305 2-s2.0-0023203395 (Pubitemid 17147210)
98. Schoenberg B. S., Environmental risk factors for Parkinson's disease: the epidemiologic evidence. Canadian Journal of Neurological Sciences 1987 14 3 407 413 2-s2.0-0023272803 (Pubitemid 17147623)
99. Kitada T., Asakawa S., Hattori N., Matsumine H., Yamamura Y., Minoshima S., Yokochi M., Mizuno Y., Shimizu N., Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 1998 392 6676 605 608 2-s2.0-0032499264 10.1038/33416 (Pubitemid 28207717)
100. Spillantini M. G., Schmidt M. L., Lee V. M., Trojanowski J. Q., Jakes R., Goedert M., -synuclein in Lewy bodies. Nature 1997 388 6645 839 840 2-s2.0-0030882856 10.1038/42166 (Pubitemid 27377048)
101. Polymeropoulos M. H., Lavedan C., Leroy E., Ide S. E., Dehejia A., Dutra A., Pike B., Root H., Rubenstein J., Boyer R., Stenroos E. S., Chandrasekharappa S., Athanassiadou A., Papapetropoulos T., Johnson W. G., Lazzarini A. M., Duvoisin R. C., Di Iorio G., Golbe L. I., Nussbaum R. L., Mutation in the -synuclein gene identified in families with Parkinson's disease. Science 1997 276 5321 2045 2047 2-s2.0-0030744876 10.1126/science.276.5321.2045 (Pubitemid 27443610)
102. Krüger R., Kuhn W., Müller T., Woitalla D., Graeber M., Kösel S., Przuntek H., Epplen J. T., Schöls L., Riess O., Ala30Pro mutation in the gene encoding -synuclein in Parkinson's disease. Nature Genetics 1998 18 2 106 108 2-s2.0-0031990490
103. Zarranz J. J., Alegre J., Gómez-Esteban J. C., Lezcano E., Ros R., Ampuero I., Vidal L., Hoenicka J., Rodriguez O., Atarés B., Llorens V., Gomez Tortosa E., Del Ser T., Muñoz D. G., de Yebenes J. G., The new mutation, E46K, of -synuclein causes Parkinson and Lewy body dementia. Annals of Neurology 2004 55 2 164 173 2-s2.0-10744230149 10.1002/ana.10795 (Pubitemid 38166992)
104. Cuervo A. M., Stafanis L., Fredenburg R., Lansbury P. T., Sulzer D., Impaired degradation of mutant -synuclein by chaperone-mediated autophagy. Science 2004 305 5688 1292 1295 2-s2.0-4344659685 10.1126/science.1101738 (Pubitemid 39129234)
105. Jenner P., Oxidative stress in Parkinson's disease. Annals of Neurology 2003 53 supplement 3 S26 S38 10.1002/ana.10483 (Pubitemid 36368560)
106. Lee S. Y., Moon Y., Hee Choi D., Jin Choi H., Hwang O., Particular vulnerability of rat mesencephalic dopaminergic neurons to tetrahydrobiopterin: relevance to Parkinson's disease. Neurobiology of Disease 2007 25 1 112 120 2-s2.0-33751090747 10.1016/j.nbd.2006.08.024 (Pubitemid 44765221)
107. Dunnett S. B., Björklund A., Prospects for new restorative and neuroprotective treatments in Parkinson's disease. Nature 1999 399 6738, supplement A32 A39 2-s2.0-0040368216
108. Conway K. A., Rochet J.-C., Bieganski R. M., Lansbury P. T. Jr., Kinetic stabilization of the -synuclein protofibril by a dopamine- -synuclein adduct. Science 2001 294 5545 1346 1349 2-s2.0-0035834360 10.1126/science.1063522 (Pubitemid 33063102)
109. Trinh K., Moore K., Wes P. D., Muchowski P. J., Dey J., Andrews L., Pallanck L. J., Induction of the phase II detoxification pathway suppresses neuron loss in Drosophila models of Parkinson's disease. Journal of Neuroscience 2008 28 2 465 472 2-s2.0-38349014710 10.1523/JNEUROSCI.4778-07.2008
110. Yoon N. S., Cho Y., Lee S. Y., Choi H. J., Hwang O., Inactivation of aconitase by tetrahydrobiopterin in DArgic cells: relevance to PD. Experimental Neurobiology 2010 19 1 23 29 10.5607/en.2010.19.1.23
111. Spencer J. P. E., Whiteman M., Jenner P., Halliwell B., 5-s-cysteinyl-conjugates of catecholamines induce cell damage, extensive DNA base modification and increases in caspase-3 activity in neurons. Journal of Neurochemistry 2002 81 1 122 129 2-s2.0-0036074531 10.1046/j.1471-4159.2002. 00808.x (Pubitemid 34808859)
112. Vauzour D., Ravaioli G., Vafeiadou K., Rodriguez-Mateos A., Angeloni C., Spencer J. P. E., Peroxynitrite induced formation of the neurotoxins 5-S-cysteinyl-dopamine and DHBT-1: implications for Parkinson's disease and protection by polyphenols. Archives of Biochemistry and Biophysics 2008 476 2 145 151 2-s2.0-48049106637 10.1016/j.abb.2008.03.011
113. Vauzour D., Vafeiadou K., Spencer J. P. E., Inhibition of the formation of the neurotoxin 5-S-cysteinyl-dopamine by polyphenols. Biochemical and Biophysical Research Communications 2007 362 2 340 346 2-s2.0-34548250927 10.1016/j.bbrc.2007.07.153 (Pubitemid 47332414)
114. Spencer J. P. E., Jenner P., Daniel S. E., Lees A. J., Marsden D. C., Halliwell B., Conjugates of catecholamines with cysteine and GSH in Parkinson's disease: possible mechanisms of formation involving reactive oxygen species. Journal of Neurochemistry 1998 71 5 2112 2122 2-s2.0-0031722906 (Pubitemid 28491568)
115. Vauzour D., Buonfiglio M., Corona G., Chirafisi J., Vafeiadou K., Angeloni C., Hrelia S., Hrelia P., Spencer J. P. E., Sulforaphane protects cortical neurons against 5-S-cysteinyl-dopamine-induced toxicity through the activation of ERK1/2, NrF-2 and the upregulation of detoxification enzymes. Molecular Nutrition and Food Research 2010 54 4 532 542 2-s2.0-77951076084 10.1002/mnfr.200900197
116. Tarozzi A., Morroni F., Merlicco A., Hrelia S., Angeloni C., Cantelli-Forti G., Hrelia P., Sulforaphane as an inducer of glutathione prevents oxidative stress-induced cell death in a dopaminergic-like neuroblastoma cell line. Journal of Neurochemistry 2009 111 5 1161 1171 2-s2.0-70350761712 10.1111/j.1471-4159.2009.06394.x
117. Tarozzi A., Morroni F., Bolondi C., Neuroprotective effects of erucin against 6-hydroxydopamine-induced oxidative damage in a dopaminergic-like neuroblastoma cell line. International Journal of Molecular Sciences 2012 13 9 10899 10910 10.3390/ijms130910899
118. Deng C., Tao R., Yu S. Z., Jin H., Sulforaphane protects against 6-hydroxydopamine-induced cytotoxicity by increasing expression of heme oxygenase-1 in a PI3K/Akt-dependent manner. Molecular Medicine Reports 2012 5 3 847 851 2-s2.0-84856257180 10.3892/mmr.2011.731
119. Siebert A., Desai V., Chandrasekaran K., Fiskum G., Jafri M. S., Nrf2 activators provide neuroprotection against 6-hydroxydopamine toxicity in rat organotypic nigrostriatal cocultures. Journal of Neuroscience Research 2009 87 7 1659 1669 2-s2.0-65849512212 10.1002/jnr.21975
120. Morroni F., Tarozzi A., Sita G., Neuroprotective effect of sulforaphane in 6-hydroxydopamine-lesioned mouse model of Parkinson's disease. Neurotoxicology 2013 36 63 71 10.1016/j.neuro.2013.03.004
121. Ma Q., He X., Molecular basis of electrophilic and oxidative defense: promises and perils of Nrf2. Pharmacological Reviews 2012 64 4 1055 1081 10.1124/pr.110.004333
122. Calkins M. J., Johnson D. A., Townsend J. A., Vargas M. R., Dowell J. A., Williamson T. P., Kraft A. D., Lee J.-M., Li J., Johnson J. A., The Nrf2/ARE pathway as a potential therapeutic target in neurodegenerative disease. Antioxidants and Redox Signaling 2009 11 3 497 508 2-s2.0-58849110632 10.1089/ars.2008.2242
123. Shapiro T. A., Fahey J. W., Dinkova-Kostova A. T., Holtzclaw W. D., Stephenson K. K., Wade K. L., Ye L., Talalay P., Safety, tolerance, and metabolism of broccoli sprout glucosinolates and isothiocyanates: a clinical phase I study. Nutrition and Cancer 2006 55 1 53 62 2-s2.0-33749165612 10.1207/s15327914nc5501-7 (Pubitemid 44477045)
124. Surh Y. J., Cancer chemoprevention with dietary phytochemicals. Nature Reviews Cancer 2003 3 10 768 780 2-s2.0-0142166328