Plumbagin, a novel Nrf2/ARE activator, protects against cerebral ischemia

Journal of Neurochemistry

Volumn 112, Issue 5, 2010, Pages 1316-1326

  Son, Tae Gen ^a   Camandola, Simonetta ^a   Arumugam, Thiruma V ^b   Cutler, Roy G ^a   Telljohann, Richard S ^a   Mughal, Mohamed R ^a   Moore, Tyson A ^b   Luo, Weiming ^a   Yu, Qian Sheng ^a   Johnson, Delinda A ^c   Johnson, Jeffrey A ^c   Greig, Nigel H ^a   Mattson, Mark P ^a,d  

^a NATIONAL INSTITUTE ON AGING   (United States)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Neuroprotection; Nrf2 ARE; Phytochemicals; Stroke

Indexed keywords

HEME OXYGENASE 1; PESTICIDE; PLUMBAGIN; REACTIVE OXYGEN METABOLITE; RNA; TRANSCRIPTION FACTOR NRF2;

ANIMAL TISSUE; ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; BRAIN CELL; BRAIN DAMAGE; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; C57BL 6 MOUSE; CELL NUCLEUS INCLUSION BODY; CELL PROTECTION; CELL SURVIVAL; CELLULAR DISTRIBUTION; DRUG SCREENING; ENZYME ACTIVATION; EXPOSURE; GENE CONTROL; GENE EXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; METABOLIC STRESS; MOUSE; NERVE CELL NECROSIS; NERVOUS SYSTEM INJURY; NEUROBLASTOMA CELL; NEUROPROTECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; REPERFUSION INJURY; RNA EXTRACTION; RNA INTERFERENCE; SPRAGUE DAWLEY RAT; TRANSCRIPTION INITIATION; WESTERN BLOTTING;

ANIMALS; ANOXIA; CELL LINE, TUMOR; CELL SURVIVAL; CELLS, CULTURED; CEREBRAL CORTEX; CEREBRAL INFARCTION; DISEASE MODELS, ANIMAL; EMBRYO, MAMMALIAN; GENE EXPRESSION REGULATION; GLUCOSE; HEME OXYGENASE-1; HUMANS; INFARCTION, MIDDLE CEREBRAL ARTERY; MICE; MICE, INBRED C57BL; NAPHTHOQUINONES; NEUROBLASTOMA; NEUROLOGIC EXAMINATION; NEURONS; NEUROPROTECTIVE AGENTS; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; TRANSCRIPTION FACTOR AP-1; TRANSFECTION;

HEXAPODA; MUS; RODENTIA;

EID: 75949124394     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2009.06552.x     Document Type: Article

References (51)

1. Alam J., Stewart D., Touchard C., Boinapally S., Choi A. M. Cook J. L. (1999) Nrf2, a cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J. Biol. Chem. 274, 26071 26078.
2. Arumugam T. V., Tang S. C., Lathia J. D. et al. (2007) Intravenous immunoglobulin (IVIG) protects the brain against experimental stroke by preventing complement-mediated neuronal cell death. Proc. Natl Acad. Sci. USA 104, 14101 14109.
3. Calabrese E. J., Bachmann K. A., Bailer A. J. et al. (2007) Biological stress response terminology: integrating the concepts of adaptive response and preconditioning stress within a hormetic dose-response framework. Toxicol. Appl. Pharmacol. 222, 122 128.
4. Calixto J. B., Kassuya C. A., André E. Ferreira J. (2005) Contribution of natural products to the discovery of the transient receptor potential (TRP) channels family and their functions. Pharmacol. Ther. 106, 179 208.
5. Camandola S., Cutler R. G., Gary D. S., Milhavet O. Mattson M. P. (2005) Suppression of calcium release from IP3-sensitive stores mediates the anti-apoptostic function of NF-κB. J. Biol. Chem. 280, 22287 22296.
6. de Castro E., Hegi de Castro S. Johnson T. E. (2004) Isolation of long-lived mutants in Caenorhabditis elegans using selection for resistance to juglone. Free Radic. Biol. Med. 37, 139 145.
7. Chen K., Gunter K. Maines M. D. (2000) Neurons overexpressing heme oxygenase-1 resist oxidative stress-mediated cell death. J. Neurochem. 75, 304 313.
8. Cutler R. G., Pedersen W. A., Camandola S., Rothstein J. D. Mattson M. P. (2002) Evidence that accumulation of ceramides and cholesterol esters mediates oxidative stress-induced death of motor neurons in amyotrophic lateral sclerosis. Ann. Neurol. 52, 448 457.
9. Danilov C. A., Chandrasekaran K., Racz J., Soane L., Zielke C. Fiskum G. (2009) Sulforaphane protects astrocytes against oxidative stress and delayed death caused by oxygen and glucose deprivation. Glia 57, 645 656.
10. De Smet P. A. (1997) The role of plant-derived drugs and herbal medicines in healthcare. Drugs 54, 801 840.
11. Dinkova-Kostova A. T. Talalay P. (2008) Direct and indirect antioxidant properties of inducers of cytoprotective proteins. Mol. Nutr. Food Res. 52, S128 S138.
12. Gines S., Ivanova E., Seong I. S., Saura C. A. MacDonald M. E. (2003) Enhanced Akt signaling is an early pro-survival response that reflects N-methyl-D-aspartate receptor activation in Huntington's disease knock-in striatal cells. J. Biol. Chem. 278, 50514 50522.
13. Giordano G., White C. C., Mohar I., Kavanagh T. J. Costa L. G. (2007) Glutathione levels modulate domoic acid induced apoptosis in mouse cerebellar granule cells. Toxicol. Sci. 100, 433 444.
14. Hanneken A., Lin F. F., Johnson J. Maher P. (2006) Flavonoids protect human retinal pigment epithelial cells from oxidative-stress-induced death. Invest. Ophthalmol. Vis. Sci. 47, 3164 3177.
15. Inbaraj J. J. Chignell C. F. (2004) Cytotoxic action of juglone and plumbagin: a mechanistic study using HaCaT keratinocytes. Chem. Res. Toxicol. 17, 55 62.
16. Isman M. B. (2006) Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annu. Rev. Entomol. 51, 45 66.
17. Itoh K., Tong K. I. Yamamoto M. (2004) Molecular mechanism activating Nrf2-Keap1 pathway in regulation of adaptive response to electrophiles. Free Radic. Biol. Med. 36, 1208 1213.
18. Johnson D. A., Andrews G. K., Xu W. Johnson J. A. (2002) Activation of the antioxidant response element in primary cortical neuronal cultures derived from transgenic reporter mice. J. Neurochem. 81, 1233 1241.
19. Joo J. H. Jetten A. M. (2008) NF-kappaB-dependent transcriptional activation in lung carcinoma cells by farnesol involves p65/RelA(Ser276) phosphorylation via the MEK-MSK1 signaling pathway. J. Biol. Chem. 283, 16391 16399.
20. Juge N., Mithen R. F. Traka M. (2007) Molecular basis for chemoprevention by sulforaphane: a comprehensive review. Cell. Mol. Life Sci. 64, 1105 1127.
21. Kostrzewa R. M. Segura-Aguilar J. (2007) Botulinum neurotoxin: evolution from poison, to research tool onto medicinal therapeutic and future pharmaceutical panacea. Neurotox. Res. 12, 275 290.
22. Koul O. (2005) Insect Antifeedants, pp. 1 1005. CRC Press LLC, Boca Raton.
23. Koul O. Dhaliwal G. S. (2001) Phytochemical Biopesticides, 223 pp. Harwood Academic Publishers, Amsterdam, Netherlands.
24. Kraft A. D., Johnson D. A. Johnson J. A. (2004) 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. J. Neurosci. 24, 1101 1112.
25. Kraft A. D., Lee J. M., Johnson D. A., Kan Y. W. Johnson J. A. (2006) Neuronal sensitivity to kainic acid is dependent on the Nrf2-mediated actions of the antioxidant response element. J. Neurochem. 98, 1852 1865.
26. Lee J. M., Hanson J. M., Chu W. A. Johnson J. A. (2001) Phosphatidylinositol 3-kinase, not extracellular signal- regulated kinase, regulates activation of the antioxidant-responsive element in IMR-32 human neuroblastoma cells. J. Biol. Chem. 276, 20011 20016.
27. Lee J. M., Shih A. Y., Murphy T. H. Johnson J. A. (2003) NF-E2-related factor-2 mediates neuroprotection against mitochondrial complex I inhibitors and increased concentrations of intracellular calcium in primary cortical neurons. J. Biol. Chem. 278, 37948 37956.
28. Leonard M. O. (2006) Reoxygenation-specific activation of the antioxidant transcription factor Nrf2 mediates cytoprotective gene expression in ischemia-reperfusion injury. FASEB J. 20, 2624 2626.
29. Lim G. P., Chu T., Yang F., Beech W., Frautschy S. A. Cole G. M. (2001) The curry spice curcumin reduces oxidative damage and amyloid pathology in an Alzheimer transgenic mouse. J. Neurosci. 21, 8370 8377.
30. Lim J. H., Kim K. M., Kim S. W., Hwang O. Choi H. J. (2008) Bromocriptine activates NQO1 via Nrf2-PI3K/Akt signaling: novel cytoprotective mechanism against oxidative damage. Pharmacol. Res. 57, 325 331.
31. Mattson M. P. (2008) Awareness of hormesis will enhance future research in basic and applied neuroscience. Crit. Rev. Toxicol. 38, 633 639.
32. Mattson M. P. Cheng A. (2006) Neurohormetic phytochemicals: low-dose toxins that induce adaptive neuronal stress responses. Trends Neurosci. 29, 632 639.
33. Na H. K., Kim E. H., Jung J. H., Lee H. H., Hyun J. W. Surh Y. J. (2008) (-)-Epigallocatechin gallate induces Nrf2-mediated antioxidant enzyme expression via activation of PI3K and ERK in human mammary epithelial cells. Arch. Biochem. Biophys. 476, 171 177.
34. Nakaso K., Yano H., Fukuhara Y., Takeshima T., Wada-Isoe K. Nakashima K. (2003) PI3K is a key molecule in the Nrf2-mediated regulation of antioxidative proteins by hemin in human neuroblastoma cells. FEBS Lett. 546, 181 184.
35. Nakazawa T., Shimura M., Tomita H., Akiyama H., Yoshioka Y., Kudou H. Tamai M. (2003) Intrinsic activation of PI3K/Akt signaling pathway and its neuroprotective effect against retinal injury. Curr. Eye Res. 26, 55 63.
36. Nelson R. L., Guo Z., Halagappa V. M. et al. (2007) Prophylactic treatment with paroxetine ameliorates behavioral deficits and retards the development of amyloid and tau pathologies in 3xTgAD mice. Exp. Neurol. 205, 166 176.
37. de Paiva S. R., Figueiredo M. R., Aragão T. V. Kaplan M. A. (2003) Antimicrobial activity in vitro of plumbagin isolated from Plumbago species. Mem. Inst. Oswaldo Cruz 98, 959 961.
38. Pathak N. Khandelwal S. (2007) Cytoprotective and immunomodulating properties of piperine on murine splenocytes: an in vitro study. Eur. J. Pharmacol. 576, 160 170.
39. Satoh T., Baba M., Nakatsuka D. et al. (2003) Role of heme oxygenase-1 protein in the neuroprotective effects of cyclopentenone prostaglandin derivatives under oxidative stress. Eur. J. Neurosci. 17, 2249 2255.
40. Satoh T., Okamoto S. I., Cui J., Watanabe Y., Furuta K., Suzuki M., Tohyama K. Lipton S. A. (2006) Activation of the Keap1/Nrf2 pathway for neuroprotection by electrophilic [correction of electrophillic] phase II inducers. Proc. Natl Acad. Sci. USA 103, 768 773.
41. Satoh T., Kosaka K., Itoh K. et al. (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.
42. Shafeek A., Jaya Prasanthi R. P., Reddy G. H., Chetty C. S. Reddy G. R. (2004) Exposure to azadirachtin produced an excitatory effect on spontaneous electrical activity as well as cercal sensory-mediated giant-fiber responses in the cockroach. Ecotoxicol. Environ. Saf. 59, 205 208.
43. Shih A. Y., Li P. Murphy T. H. (2005) A small-molecule-inducible Nrf2-mediated antioxidant response provides effective prophylaxis against cerebral ischemia in vivo. J. Neurosci. 25, 10321 10335.
44. Sugie S., Okamoto K., Rahman K. M., Tanaka T., Kawai K., Yamahara J. Mori H. (1998) Inhibitory effects of plumbagin and juglone on azoxymethane-induced intestinal carcinogenesis in rats. Cancer Lett. 127, 177 183.
45. Tang S. C., Arumugam T. V., Cutler R. G. et al. (2007) Neuroprotective actions of a histidine analogus in models of ischemic stroke. J. Neurochem. 101, 729 736.
46. Tanito M., Agbaga M. P. Anderson R. E. (2007) Upregulation of thioredoxin system via Nrf2-antioxidant responsive element pathway in adaptive retinal neuroprotection in vivo and in vitro. Free Radic. Biol. Med. 42, 1838 1850.
47. Tarnopolsky M. A. (1994) Caffeine and endurance performance. Sports Med. 18, 109 125.
48. Wilson R. I. Nicoll R. A. (2002) Endocannabinoid signaling in the brain. Science 296, 678 682.
49. Wright D. A., Dawson R., Cutler S. J., Cutler H. G. Orano-Dawson C. E. (2007) Screening of natural product biocides for control of non-indigenous species. Environ. Technol. 28, 309 319.
50. Wruck C. J., Götz M. E., Herdegen T., Varoga D., Brandenburg L. O. Pufe T. (2008) Kavalactones protect neural cells against amyloid beta peptide-induced neurotoxicity via extracellular signal-regulated kinase 1/2-dependent nuclear factor erythroid 2-related factor 2 activation. Mol. Pharmacol. 73, 1785 1795.
51. Zhao J., Kobori N., Aronowski J. Dash P. K. (2006) Sulforaphane reduces infarct volume following focal cerebral ischemia in rodents. Neurosci. Lett. 393, 108 112.