Walnut diet reduces accumulation of polyubiquitinated proteins and inflammation in the brain of aged rats

Journal of Nutritional Biochemistry

Volumn 24, Issue 5, 2013, Pages 912-919

  Poulose, Shibu M ^a   Bielinski, Donna F ^a   Shukitt Hale, Barbara ^a  

^a TUFTS UNIVERSITY   (United States)

Author keywords

Autophagy; Inflammation; Phosphorylation; PUFA; Ubiquitin; Walnut

Indexed keywords

BECLIN 1; I KAPPA B;

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; BRAIN; CONTROLLED STUDY; CORPUS STRIATUM; DIET; HIPPOCAMPUS; INFLAMMATION; NONHUMAN; PROTEIN AGGREGATION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; RAT; UBIQUITINATION; UPREGULATION; WALNUT;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; BRAIN; COGNITION; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DIET; FATTY ACIDS, UNSATURATED; HIPPOCAMPUS; INFLAMMATION; JUGLANS; MALE; MEMORY; NF-KAPPA B; NUTS; OXIDATIVE STRESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; RATS; RATS, INBRED F344; TOR SERINE-THREONINE KINASES; UBIQUITIN-ACTIVATING ENZYMES; UBIQUITINATED PROTEINS; UP-REGULATION;

ANIMALIA; JUGLANS; RATTUS;

EID: 84876795525     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2012.06.009     Document Type: Article

References (49)

1. Joseph J.A., Shukitt-Hale B., Willis L.M. Grape juice, berries, and walnuts affect brain aging and behavior. J Nutr 2009, 139:1813S-1817S.
2. Casadesus G., Shukitt-Hale B., Stellwagen H.M., Zhu X., Lee H.G., Smith M.A., et al. Modulation of hippocampal plasticity and cognitive behavior by short-term blueberry supplementation in aged rats. Nutr Neurosci 2004, 7:309-316.
3. Joseph J.A., Shukitt-Hale B., Casadesus G. Reversing the deleterious effects of aging on neuronal communication and behavior: beneficial properties of fruit polyphenolic compounds. Am J Clin Nutr 2005, 81:313S-316S.
4. Joseph J.A., Shukitt-Hale B., Denisova N.A., Bielinski D., Martin A., McEwen J.J., et al. Reversals of age-related declines in neuronal signal transduction, cognitive, and motor behavioral deficits with blueberry, spinach, or strawberry dietary supplementation. J Neurosci 1999, 19:8114-8121.
5. Willis L.M., Shukitt-Hale B., Cheng V., Joseph J.A. Dose-dependent effects of walnuts on motor and cognitive function in aged rats. Br J Nutr 2009, 101:1140-1144.
6. Willis L.M., Bielinski D.F., Fisher D.R., Matthan N.R., Joseph J.A. Walnut extract inhibits LPS-induced activation of BV-2 microglia via internalization of TLR4: possible involvement of phospholipase D2. Inflammation 2010, 33:325-333.
7. Oliveira I., Sousa A., Ferreira I.C., Bento A., Estevinho L., Pereira J.A. Total phenols, antioxidant potential and antimicrobial activity of walnut (Juglans regia L.) green husks. Food Chem Toxicol 2008, 46:2326-2331.
8. Pereira J.A., Oliveira I., Sousa A., Valentao P., Andrade P.B., Ferreira I.C., et al. Walnut (Juglans regia L.) leaves: phenolic compounds, antibacterial activity and antioxidant potential of different cultivars. Food Chem Toxicol 2007, 45:2287-2295.
9. Willis L.M., Shukitt-Hale B., Joseph J.A. Dietary polyunsaturated fatty acids improve cholinergic transmission in the aged brain. Genes Nutr 2009, 4:309-314.
10. Willis L.M., Shukitt-Hale B., Joseph J.A. Modulation of cognition and behavior in aged animals: role for antioxidant- and essential fatty acid-rich plant foods. Am J Clin Nutr 2009, 89:1602S-1606S.
11. Pribis P., Bailey R.N., Russell A.A., Kilsby M.A., Hernandez M., Craig W.J., et al. Effects of walnut consumption on cognitive performance in young adults. Br J Nutr 2012, 107:1393-1401.
12. Banel D.K., Hu F.B. Effects of walnut consumption on blood lipids and other cardiovascular risk factors: a meta-analysis and systematic review. Am J Clin Nutr 2009, 90:56-63.
13. Ma Y., Njike V.Y., Millet J., Dutta S., Doughty K., Treu J.A., et al. Effects of walnut consumption on endothelial function in type 2 diabetic subjects: a randomized controlled crossover trial. Diabetes Care 2010, 33:227-232.
14. McKay D.L., Chen C.Y., Yeum K.J., Matthan N.R., Lichtenstein A.H., Blumberg J.B. Chronic and acute effects of walnuts on antioxidant capacity and nutritional status in humans: a randomized, cross-over pilot study. Nutr J 2010, 9:21.
15. Tapsell L.C., Gillen L.J., Patch C.S., Batterham M., Owen A., Bare M., et al. Including walnuts in a low-fat/modified-fat diet improves HDL cholesterol-to-total cholesterol ratios in patients with type 2 diabetes. Diabetes Care 2004, 27:2777-2783.
16. Sabate J., Oda K., Ros E. Nut consumption and blood lipid levels: a pooled analysis of 25 intervention trials. Arch Intern Med 2010, 170:821-827.
17. Mizushima N., Levine B., Cuervo A.M., Klionsky D.J. Autophagy fights disease through cellular self-digestion. Nature 2008, 451:1069-1075.
18. Nixon R.A. Autophagy, amyloidogenesis and Alzheimer disease. J Cell Sci 2007, 120:4081-4091.
19. Sun Q., Fan W., Zhong Q. Regulation of Beclin 1 in autophagy. Autophagy 2009, 5:713-716.
20. Pickford F., Masliah E., Britschgi M., Lucin K., Narasimhan R., Jaeger P.A., et al. The autophagy-related protein beclin 1 shows reduced expression in early Alzheimer disease and regulates amyloid beta accumulation in mice. J Clin Invest 2008, 118:2190-2199.
21. Ohsumi Y., Mizushima N. Two ubiquitin-like conjugation systems essential for autophagy. Semin Cell Dev Biol 2004, 15:231-236.
22. Komatsu M., Wang Q.J., Holstein G.R., Friedrich V.L., Iwata J., Kominami E., et al. Essential role for autophagy protein Atg7 in the maintenance of axonal homeostasis and the prevention of axonal degeneration. Proc Natl Acad Sci U S A 2007, 104:14489-14494.
23. Bjorkoy G., Lamark T., Brech A., Outzen H., Perander M., Overvatn A., et al. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol 2005, 171:603-614.
24. Deretic V. Autophagosome and phagosome. Methods Mol Biol 2008, 445:1-10.
25. Munoz L., Ralay Ranaivo H., Roy S.M., Hu W., Craft J.M., McNamara L.K., et al. A novel p38 alpha MAPK inhibitor suppresses brain proinflammatory cytokine up-regulation and attenuates synaptic dysfunction and behavioral deficits in an Alzheimer's disease mouse model. J Neuroinflammation 2007, 4:21.
26. Choi Y., Lee M.K., Lim S.Y., Sung S.H., Kim Y.C. Inhibition of inducible NO synthase, cyclooxygenase-2 and interleukin-1beta by torilin is mediated by mitogen-activated protein kinases in microglial BV2 cells. Br J Pharmacol 2009, 156:933-940.
27. Harari O.A., Liao J.K. NF-kappaB and innate immunity in ischemic stroke. Ann N Y Acad Sci 2010, 1207:32-40.
28. Qin Z.H., Tao L.Y., Chen X. Dual roles of NF-kappaB in cell survival and implications of NF-kappaB inhibitors in neuroprotective therapy. Acta Pharmacol Sin 2007, 28:1859-1872.
29. Benito E., Barco A. CREB's control of intrinsic and synaptic plasticity: implications for CREB-dependent memory models. Trends Neurosci 2010, 33:230-240.
30. Sakamoto K., Karelina K., Obrietan K. CREB: a multifaceted regulator of neuronal plasticity and protection. J Neurochem 2011, 116:1-9.
31. Vellai T., Takacs-Vellai K., Sass M., Klionsky D.J. The regulation of aging: does autophagy underlie longevity?. Trends Cell Biol 2009, 19:487-494.
32. Spilman P., Podlutskaya N., Hart M.J., Debnath J., Gorostiza O., Bredesen D., et al. Correction: inhibition of mTOR by rapamycin abolishes cognitive deficits and reduces amyloid-beta levels in a mouse model of Alzheimer's disease. PLoS One 2011, 6.
33. Webb J.L., Ravikumar B., Atkins J., Skepper J.N., Rubinsztein D.C. Alpha-Synuclein is degraded by both autophagy and the proteasome. J Biol Chem 2003, 278:25009-25013.
34. Ravikumar B., Vacher C., Berger Z., Davies J.E., Luo S., Oroz L.G., et al. Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat Genet 2004, 36:585-595.
35. Crews L., Spencer B., Desplats P., Patrick C., Paulino A., Rockenstein E., et al. Selective molecular alterations in the autophagy pathway in patients with Lewy body disease and in models of alpha-synucleinopathy. PLoS One 2010, 5:e9313.
36. Kuusisto E., Suuronen T., Salminen A. Ubiquitin-binding protein p62 expression is induced during apoptosis and proteasomal inhibition in neuronal cells. Biochem Biophys Res Commun 2001, 280:223-228.
37. Spencer B., Potkar R., Trejo M., Rockenstein E., Patrick C., Gindi R., et al. Beclin 1 gene transfer activates autophagy and ameliorates the neurodegenerative pathology in alpha-synuclein models of Parkinson's and Lewy body diseases. J Neurosci 2009, 29:13578-13588.
38. Guo W., Qian L., Zhang J., Zhang W., Morrison A., Hayes P., et al. Sirt1 overexpression in neurons promotes neurite outgrowth and cell survival through inhibition of the mTOR signaling. J Neurosci Res 2011, 89:1723-1736.
39. Poulose S.M., Bielinski D.F., Carrihill-Knoll K., Rabin B.M., Shukitt-Hale B. Exposure to (16)O-Particle Radiation Causes Aging-Like Decrements in Rats through Increased Oxidative Stress, Inflammation and Loss of Autophagy. Radiat Res 2011, 176:761-769.
40. Viiri J., Hyttinen J.M., Ryhanen T., Rilla K., Paimela T., Kuusisto E., et al. p62/sequestosome 1 as a regulator of proteasome inhibitor-induced autophagy in human retinal pigment epithelial cells. Mol Vis 2010, 16:1399-1414.
41. Kuusisto E., Salminen A., Alafuzoff I. Early accumulation of p62 in neurofibrillary tangles in Alzheimer's disease: possible role in tangle formation. Neuropathol Appl Neurobiol 2002, 28:228-237.
42. Massey A.C., Follenzi A., Kiffin R., Zhang C., Cuervo A.M. Early cellular changes after blockage of chaperone-mediated autophagy. Autophagy 2008, 4:442-456.
43. Djavaheri-Mergny M., Amelotti M., Mathieu J., Besancon F., Bauvy C., Souquere S., et al. NF-kappaB activation represses tumor necrosis factor-alpha-induced autophagy. J Biol Chem 2006, 281:30373-30382.
44. Scherz-Shouval R., Shvets E., Fass E., Shorer H., Gil L., Elazar Z. Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J 2007, 26:1749-1760.
45. Farooqui A.A., Horrocks L.A., Farooqui T. Modulation of inflammation in brain: a matter of fat. J Neurochem 2007, 101:577-599.
46. Samuels I.S., Seibenhener M.L., Neidigh K.B., Wooten M.W. Nerve growth factor stimulates the interaction of ZIP/p62 with atypical protein kinase C and targets endosomal localization: evidence for regulation of nerve growth factor-induced differentiation. J Cell Biochem 2001, 82:452-466.
47. Sanz L., Diaz-Meco M.T., Nakano H., Moscat J. The atypical PKC-interacting protein p62 channels NF-kappaB activation by the IL-1-TRAF6 pathway. EMBO J 2000, 19:1576-1586.
48. Pugazhenthi S., Wang M., Pham S., Sze C.I., Eckman C.B. Downregulation of CREB expression in Alzheimer's brain and in Abeta-treated rat hippocampal neurons. Mol Neurodegener 2011, 6:60.
49. Rubinsztein D.C., Gestwicki J.E., Murphy L.O., Klionsky D.J. Potential therapeutic applications of autophagy. Nat Rev Drug Discov 2007, 6:304-312.