Sulforaphane enhances proteasomal and autophagic activities in mice and is a potential therapeutic reagent for Huntington's disease

Journal of Neurochemistry

Volumn 129, Issue 3, 2014, Pages 539-547

  Liu, Yanying ^a   Hettinger, Casey L ^a   Zhang, Dong ^a   Rezvani, Khosrow ^a   Wang, Xuejun ^a   Wang, Hongmin ^a  

^a UNIVERSITY OF SOUTH DAKOTA   (United States)

Author keywords

autophagy; mutant huntingtin; neurodegeneration; protein degradation; sulforaphane; ubiquitin proteasome system

Indexed keywords

AUTOPHAGY; MUTANT HUNTINGTIN; NEURODEGENERATION; PROTEIN DEGRADATION; SULFORAPHANE; UBIQUITIN PROTEASOME SYSTEM;

ANIMALS; AUTOPHAGY; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; HEK293 CELLS; HELA CELLS; HUMANS; HUNTINGTON DISEASE; ISOTHIOCYANATES; MALE; MICE; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; PROTEASOME ENDOPEPTIDASE COMPLEX; TRANSFECTION;

EID: 84899421127     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12647     Document Type: Article

References (41)

1. Bates G., Harper P., and, Jones L., (2002) Huntington's Disease, 3rd edn. pp. 159-197. Oxford University Press, Oxford.
2. Bence N. F., Sampat R. M., and, Kopito R. R., (2001) Impairment of the ubiquitin-proteasome system by protein aggregation. Science 292, 1552-1555.
3. Caricchio R., Kovalenko D., Kaufmann W. K., and, Cohen P. L., (1999) Apoptosis provoked by the oxidative stress inducer menadione (Vitamin K(3) is mediated by the Fas/Fas ligand system. Clin. Immunol. 93, 65-74.
4. Chang D. T., Rintoul G. L., Pandipati S., and, Reynolds I. J., (2006) Mutant huntingtin aggregates impair mitochondrial movement and trafficking in cortical neurons. Neurobiol. Dis. 22, 388-400.
5. Chapple S. J., Siow R. C., and, Mann G. E., (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.
6. Clarke J. D., Hsu A., Williams D. E., Dashwood R. H., Stevens J. F., Yamamoto M., and, Ho E., (2011) Metabolism and tissue distribution of sulforaphane in Nrf2 knockout and wild-type mice. Pharm. Res. 28, 3171-3179.
7. Dong G., Ferguson J. M., Duling A. J., et al,. (2011) Modeling pathogenesis of Huntington's disease with inducible neuroprogenitor cells. Cell. Mol. Neurobiol. 31, 737-747.
8. Dong G., Callegari E., Gloeckner C. J., Ueffing M., and, Wang H., (2012a) Mass spectrometric identification of novel posttranslational modification sites in Huntingtin. Proteomics 12, 2060-2064.
9. Dong G., Callegari E. A., Gloeckner C. J., Ueffing M., and, Wang H., (2012b) Prothymosin-alpha interacts with mutant huntingtin and suppresses its cytotoxicity in cell culture. J. Biol. Chem. 287, 1279-1289.
10. Dong G., Gross K., Qiao F., et al,. (2012c) Calretinin interacts with huntingtin and reduces mutant huntingtin-caused cytotoxicity. J. Neurochem. 123, 437-446.
11. Fahey J. W., and, Talalay P., (1999) Antioxidant functions of sulforaphane: a potent inducer of Phase II detoxication enzymes. Food and Chem. Toxicol. 37, 973-979.
12. Gamet-Payrastre L., Li P. F., Lumeau S., Cassar G., Dupont M. A., Chevolleau S., Gasc N., Tulliez J., and, Terce F., (2000) Sulforaphane, a naturally occurring isothiocyanate, induces cell cycle arrest and apoptosis in HT29 human colon cancer cells. Cancer Res. 60, 1426-1433.
13. Gan N., Wu Y. C., Brunet M., Garrido C., Chung F. L., Dai C., and, Mi L., (2010) Sulforaphane activates heat shock response and enhances proteasome activity through up-regulation of Hsp27. J. Biol. Chem. 285, 35528-35536.
14. Goswami A., Dikshit P., Mishra A., Mulherkar S., Nukina N., and, Jana N. R., (2006) Oxidative stress promotes mutant huntingtin aggregation and mutant huntingtin-dependent cell death by mimicking proteasomal malfunction. Biochem. Biophys. Res. Commun. 342, 184-190.
15. Hanlon N., Coldham N., Gielbert A., Kuhnert N., Sauer M. J., King L. J., and, Ioannides C., (2008) Absolute bioavailability and dose-dependent pharmacokinetic behaviour of dietary doses of the chemopreventive isothiocyanate sulforaphane in rat. Br. J. Nutr. 99, 559-564.
16. Herman-Antosiewicz A., Johnson D. E., and, Singh S. V., (2006) Sulforaphane causes autophagy to inhibit release of cytochrome C and apoptosis in human prostate cancer cells. Cancer Res. 66, 5828-5835.
17. Jin Y. N., Yu Y. V., Gundemir S., Jo C., Cui M., Tieu K., and, Johnson G. V., (2013) Impaired mitochondrial dynamics and Nrf2 signaling contribute to compromised responses to oxidative stress in striatal cells expressing full-length mutant huntingtin. PLoS ONE 8, e57932.
18. Kabeya Y., Mizushima N., Ueno T., Yamamoto A., Kirisako T., Noda T., Kominami E., Ohsumi Y., and, Yoshimori T., (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19, 5720-5728.
19. Kensler T. W., Wakabayashi N., and, Biswal S., (2007) Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu. Rev. Pharmacol. Toxicol. 47, 89-116.
20. Keum Y. S., Khor T. O., Lin W., Shen G., Kwon K. H., Barve A., Li W., and, Kong A. N., (2009) Pharmacokinetics and pharmacodynamics of broccoli sprouts on the suppression of prostate cancer in transgenic adenocarcinoma of mouse prostate (TRAMP) mice: implication of induction of Nrf2, HO-1 and apoptosis and the suppression of Akt-dependent kinase pathway. Pharm. Res. 26, 2324-2331.
21. Kim H. V., Kim H. Y., Ehrlich H. Y., Choi S. Y., Kim D. J., and, Kim Y., (2013) Amelioration of Alzheimer's disease by neuroprotective effect of sulforaphane in animal model. Amyloid, 20, 7-12.
22. Kisselev A. F., and, Goldberg A. L., (2005) Monitoring activity and inhibition of 26S proteasomes with fluorogenic peptide substrates. Methods Enzymol. 398, 364-378.
23. Kumarapeli A. R., Horak K. M., Glasford J. W., Li J., Chen Q., Liu J., Zheng H., and, Wang X., (2005) A novel transgenic mouse model reveals deregulation of the ubiquitin-proteasome system in the heart by doxorubicin. FASEB J. 19, 2051-2053.
24. Kwak M. K., Cho J. M., Huang B., Shin S., and, Kensler T. W., (2007) Role of increased expression of the proteasome in the protective effects of sulforaphane against hydrogen peroxide-mediated cytotoxicity in murine neuroblastoma cells. Free Radical Biol. Med. 43, 809-817.
25. Li X. J., and, Li S., (2011) Proteasomal dysfunction in aging and Huntington disease. Neurobiol. Dis. 43, 4-8.
26. Li X., Li H., and, Li X. J., (2008) Intracellular degradation of misfolded proteins in polyglutamine neurodegenerative diseases. Brain Res. Rev. 59, 245-252.
27. Li J., Powell S. R., and, Wang X., (2011) Enhancement of proteasome function by PA28α overexpression protects against oxidative stress. FASEB J. 25, 883-893.
28. Liang Q., Ouyang X., Schneider L., and, Zhang J., (2011) Reduction of mutant huntingtin accumulation and toxicity by lysosomal cathepsins D and B in neurons. Mol Neurodegener. 6, 37.
29. Liu J., Zheng H., Tang M., Ryu Y. C., and, Wang X., (2008) A therapeutic dose of doxorubicin activates ubiquitin-proteasome system-mediated proteolysis by acting on both the ubiquitination apparatus and proteasome. Am. J. Physiol. Heart Circ. Physiol. 295, H2541-H2550.
30. Mizushima N., and, Yoshimori T., (2007) How to interpret LC3 immunoblotting. Autophagy 3, 542-545.
31. Morroni F., Tarozzi A., Sita G., Bolondi C., Zolezzi Moraga J. M., Cantelli-Forti G., and, Hrelia P., (2013) Neuroprotective effect of sulforaphane in 6-hydroxydopamine-lesioned mouse model of Parkinson's disease. Neurotoxicology 36C, 63-71.
32. Ogata M., Hino S., Saito A., et al,. (2006) Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol. Cell. Biol. 26, 9220-9231.
33. Ravikumar B., Vacher C., Berger Z., et al,. (2004) Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat. Genet. 36, 585-595.
34. Rubinsztein D. C., (2006) The roles of intracellular protein-degradation pathways in neurodegeneration. Nature 443, 780-786.
35. Seo H., Sonntag K. C., and, Isacson O., (2004) Generalized brain and skin proteasome inhibition in Huntington's disease. Ann Neurol. 56, 319-328.
36. Seo H., Sonntag K. C., Kim W., Cattaneo E., and, Isacson O., (2007) Proteasome activator enhances survival of huntington's disease neuronal model cells. PLoS ONE 2, e238.
37. Vyas A. R., Hahm E. R., Arlotti J. A., Watkins S., Stolz D. B., Desai D., Amin S., and, Singh S. V., (2013) Chemoprevention of prostate cancer by d, l-sulforaphane is augmented by pharmacological inhibition of autophagy. Cancer Res. 73, 5985-5995.
38. Wang H., Lim P. J., Yin C., Rieckher M., Vogel B. E., and, Monteiro M. J., (2006) Suppression of polyglutamine-induced toxicity in cell and animal models of Huntington's disease by ubiquilin. Hum. Mol. Genet. 15, 1025-1041.
39. Wojcik C., and, DeMartino G. N., (2003) Intracellular localization of proteasomes. Int. J. Biochem. Cell Biol. 35, 579-589.
40. Zhang Y., Talalay P., Cho C. G., and, Posner G. H., (1992) A major inducer of anticarcinogenic protective enzymes from broccoli: isolation and elucidation of structure. Proc. Natl Acad. Sci. USA 89, 2399-2403.
41. Zoghbi H. Y., and, Orr H. T., (2000) Glutamine repeats and neurodegeneration. Annu. Rev. Neurosci. 23, 217-247.