Involvement of peroxisome proliferator-activated receptor β/δ (PPAR β/δ) in BDNF signaling during aging and in Alzheimer disease: Possible role of 4-hydroxynonenal (4-HNE)

Cell Cycle

Volumn 13, Issue 8, 2014, Pages 1335-1344

  Benedetti, Elisabetta ^a   D'Angelo, Barbara ^a   Cristiano, Loredana ^a   Di Giacomo, Erica ^a   Fanelli, Francesca ^b   Moreno, Sandra ^b   Cecconi, Francesco ^c   Fidoamore, Alessia ^a   Antonosante, Andrea ^a   Falcone, Roberta ^a   Ippoliti, Rodolfo ^a   Giordano, Antonio ^d,e   Cimini, Annamaria ^a,e  

^a UNIVERSITY OF L'AQUILA   (Italy)

^b ROMA TRE UNIVERSITY   (Italy)

^c UNIVERSITY OF ROME TOR VERGATA   (Italy)

^d UNIVERSITY OF SIENA   (Italy)

^e TEMPLE UNIVERSITY   (United States)

Author keywords

Aging; BDNF; JNK; Neurodegenerative disease; Oxidative stress; p75; Transcription factors; TrkB

Indexed keywords

4 HYDROXYNONENAL; BRAIN DERIVED NEUROTROPHIC FACTOR; GLUTATHIONE TRANSFERASE P1; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; 4-HYDROXY-2-NONENAL; ALDEHYDE; MEMBRANE PROTEIN; NTRK2 PROTEIN, MOUSE; PROTEIN TYROSINE KINASE;

AGE; AGING; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; DISEASE SEVERITY; FEMALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SURVIVAL; AGONISTS; ANIMAL; C57BL MOUSE; MALE; METABOLISM; PATHOLOGY;

AGING; ALDEHYDES; ALZHEIMER DISEASE; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; FEMALE; GLUTATHIONE S-TRANSFERASE PI; MALE; MEMBRANE GLYCOPROTEINS; MICE, INBRED C57BL; PPAR DELTA; PPAR-BETA; PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION;

EID: 84899088674     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.28295     Document Type: Article

References (47)

1. Selkoe DJ. Alzheimer's disease. Cold Spring Harb Perspect Biol 2011; 3:3; PMID:21576255; http://dx.doi.org/10.1101/cshperspect.a004457
2. Selkoe DJ. Biochemistry and molecular biology of amyloid beta-protein and the mechanism of Alzheimer's disease. Handb Clin Neurol 2008; 89:245-60; PMID:18631749; http://dx.doi.org/10.1016/S0072-9752(07)01223-7
3. LaFerla FM, Oddo S. Alzheimer's disease: Abeta, tau and synaptic dysfunction. Trends Mol Med 2005; 11:170-6; PMID:15823755; http://dx.doi.org/10. 1016/j.molmed.2005.02.009
4. Walsh DM, Selkoe DJ. A beta oligomers - a decade of discovery. J Neurochem 2007; 101:1172-84; PMID:17286590; http://dx.doi.org/10.1111/j.1471- 4159.2006.04426.x
5. Sayre LM, Perry G, Smith MA. Oxidative stress and neurotoxicity. Chem Res Toxicol 2008; 21:172-88; PMID:18052107; http://dx.doi.org/10.1021/tx700210j
6. Comporti M. Lipid peroxidation and biogenic aldehydes: from the identification of 4-hydroxynonenal to further achievements in biopathology. Free Radic Res 1998; 28:623-35; PMID:9736314; http://dx.doi.org/10.3109/ 10715769809065818
7. Catalá A. Lipid peroxidation of membrane phospholipids generates hydroxy-alkenals and oxidized phospholipids active in physiological and/or pathological conditions. Chem Phys Lipids 2009; 157:1-11; PMID:18977338; http://dx.doi.org/10.1016/j.chemphyslip.2008.09.004
8. Uchida K, Kanematsu M, Sakai K, Matsuda T, Hattori N, Mizuno Y, Suzuki D, Miyata T, Noguchi N, Niki E, et al. Protein-bound acrolein: potential markers for oxidative stress. Proc Natl Acad Sci U S A 1998; 95:4882-7; PMID:9560197; http://dx.doi.org/10.1073/pnas.95.9.4882
9. Friguet B, Szweda LI. Inhibition of the multicatalytic proteinase (proteasome) by 4-hydroxy-2-nonenal cross-linked protein. FEBS Lett 1997; 405:21-5; PMID:9094417; http://dx.doi.org/10.1016/S0014-5793(97)00148-8
10. Ferrington DA, Kapphahn RJ. Catalytic site-specific inhibition of the 20S proteasome by 4-hydroxynonenal. FEBS Lett 2004; 578:217-23; PMID:15589823; http://dx.doi.org/10.1016/j.febslet.2004.11.003
11. Kruman I, Bruce-Keller AJ, Bredesen D, Waeg G, Mattson MP. Evidence that 4-hydroxynonenal mediates oxidative stress-induced neuronal apoptosis. J Neurosci 1997; 17:5089-100; PMID:9185546
12. Ji C, Amarnath V, Pietenpol JA, Marnett LJ. 4-hydroxynonenal induces apoptosis via caspase-3 activation and cytochrome c release. Chem Res Toxicol 2001; 14:1090-6; PMID:11511183; http://dx.doi.org/10.1021/tx000186f
13. Awasthi YC, Yang Y, Tiwari NK, Patrick B, Sharma A, Li J, Awasthi S. Regulation of 4-hydroxynonenal-mediated signaling by glutathione S-transferases. Free Radic Biol Med 2004; 37:607-19; PMID:15288119; http://dx.doi.org/10.1016/ j.freeradbiomed.2004.05.033
14. Coleman JD, Prabhu KS, Thompson JT, Reddy PS, Peters JM, Peterson BR, Reddy CC, Vanden Heuvel JP. The oxidative stress mediator 4-hydroxynonenal is an intracellular agonist of the nuclear receptor peroxisome proliferator-activated receptor-beta/ delta (PPARbeta/delta). Free Radic Biol Med 2007; 42:1155-64; PMID:17382197; http://dx.doi.org/10.1016/j.freeradbiomed.2007.01.003
15. Heneka MT, Landreth GE. PPARs in the brain. Biochim Biophys Acta 2007; 1771:1031-45; PMID:17569578; http://dx.doi.org/10.1016/j.bbalip.2007.04.016
16. Bright JJ, Kanakasabai S, Chearwae W, Chakraborty S. PPAR Regulation of Inflammatory Signaling in CNS Diseases. PPAR Res 2008; 2008:658520; PMID:18670616; http://dx.doi.org/10.1155/2008/658520
17. Cimini A, Moreno S, D'Amelio M, Cristiano L, D'Angelo B, Falone S, Benedetti E, Carrara P, Fanelli F, Cecconi F, et al. Early biochemical and morphological modifications in the brain of a transgenic mouse model of Alzheimer's disease: a role for peroxisomes. J Alzheimers Dis 2009; 18:935-52; PMID:19749434
18. Schintu N, Frau L, Ibba M, Caboni P, Garau A, Carboni E, Carta AR. PPAR-gamma-mediated neuroprotection in a chronic mouse model of Parkinson's disease. Eur J Neurosci 2009; 29:954-63; PMID:19245367; http://dx.doi.org/10. 1111/j.1460-9568.2009.06657.x
19. Heneka MT, Reyes-Irisarri E, Hüll M, Kummer MP. Impact and Therapeutic Potential of PPARs in Alzheimer's Disease. Curr Neuropharmacol 2011; 9:643-50; PMID:22654722; http://dx.doi.org/10.2174/157015911798376325
20. Bhateja DK, Dhull DK, Gill A, Sidhu A, Sharma S, Reddy BV, Padi SS. Peroxisome proliferator-activated receptor-á activation attenuates 3-nitropropionic acid induced behavioral and biochemical alterations in rats: possible neuroprotective mechanisms. Eur J Pharmacol 2012; 674:33-43; PMID:22056833; http://dx.doi.org/10.1016/j.ejphar.2011.10.029
21. Sodhi RK, Singh N, Jaggi AS. Neuroprotective mechanisms of peroxisome proliferator-activated receptor agonists in Alzheimer's disease. Naunyn Schmiedebergs Arch Pharmacol 2011; 384:115-24; PMID:21607645; http://dx.doi.org/10.1007/s00210-011-0654-6
22. Fanelli F, Sepe S, D'Amelio M, Bernardi C, Cristiano L, Cimini A, Cecconi F, Ceru' MP, Moreno S. Agedependent roles of peroxisomes in the hippocampus of a transgenic mouse model of Alzheimer's disease. Mol Neurodegener 2013; 8:8; PMID:23374228; http://dx.doi.org/10.1186/1750-1326-8-8
23. Braissant O, Wahli W. Differential expression of peroxisome proliferator-activated receptor- α, - β, and - γ during rat embryonic development. Endocrinology 1998; 139:2748-54; PMID:9607781
24. Krémarik-Bouillaud P, Schohn H, Dauça M. Regional distribution of PPARbeta in the cerebellum of the rat. J Chem Neuroanat 2000; 19:225-32; PMID:11036239; http://dx.doi.org/10.1016/S0891-0618(00)00065-X
25. Moreno S, Farioli-Vecchioli S, Cerù MP. Immunolocalization of peroxisome proliferator-activated receptors and retinoid X receptors in the adult rat CNS. Neuroscience 2004; 123:131-45; PMID:14667448; http://dx.doi.org/10.1016/j.neuroscience.2003.08.064
26. Di Loreto S, D'Angelo B, D'Amico MA, Benedetti E, Cristiano L, Cinque B, Cifone MG, Cerù MP, Festuccia C, Cimini A. PPARbeta agonists trigger neuronal differentiation in the human neuroblastoma cell line SH-SY5Y. J Cell Physiol 2007; 211:837-47; PMID:17390299; http://dx.doi.org/10.1002/jcp.20996
27. D'Angelo B, Benedetti E, Di Loreto S, Cristiano L, Laurenti G, Cerù MP, Cimini A. Signal transduction pathways involved in PPAR β / δ -induced neuronal differentiation. J Cell Physiol 2011; 226:2170-80; PMID:21520069; http://dx.doi.org/10.1002/jcp.22552
28. Tapia-Arancibia L, Aliaga E, Silhol M, Arancibia S. New insights into brain BDNF function in normal aging and Alzheimer disease. Brain Res Rev 2008; 59:201-20; PMID:18708092; http://dx.doi.org/10.1016/j.brainresrev.2008.07.007
29. Hsiao K, Chapman P, Nilsen S, Eckman C, Harigaya Y, Younkin S, Yang F, Cole G. Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 1996; 274:99-102; PMID:8810256; http://dx.doi.org/10. 1126/science.274.5284.99
30. Jacobsen JS, Wu CC, Redwine JM, Comery TA, Arias R, Bowlby M, Martone R, Morrison JH, Pangalos MN, Reinhart PH, et al. Early-onset behavioral and synaptic deficits in a mouse model of Alzheimer's disease. Proc Natl Acad Sci U S A 2006; 103:5161-6; PMID:16549764; http://dx.doi.org/10.1073/pnas.0600948103
31. D'Amelio M, Cavallucci V, Middei S, Marchetti C, Pacioni S, Ferri A, Diamantini A, De Zio D, Carrara P, Battistini L, et al. Caspase-3 triggers early synaptic dysfunction in a mouse model of Alzheimer's disease. Nat Neurosci 2011; 14:69-76; PMID:21151119; http://dx.doi.org/10.1038/nn.2709
32. Aksenov MY, Tucker HM, Nair P, Aksenova MV, Butterfield DA, Estus S, Markesbery WR. The expression of key oxidative stress-handling genes in different brain regions in Alzheimer's disease. J Mol Neurosci 1998; 11:151-64; PMID:10096042; http://dx.doi.org/10.1385/JMN:11:2:151
33. Xie C, Lovell MA, Xiong S, Kindy MS, Guo J, Xie J, Amaranth V, Montine TJ, Markesbery WR. Expression of glutathione-S-transferase isozyme in the SY5Y neuroblastoma cell line increases resistance to oxidative stress. Free Radic Biol Med 2001; 31:73-81; PMID:11425492; http://dx.doi.org/10.1016/S0891-5849(01) 00553-6
34. Nunomura A, Tamaoki T, Tanaka K, Motohashi N, Nakamura M, Hayashi T, Yamaguchi H, Shimohama S, Lee HG, Zhu X, et al. Intraneuronal amyloid beta accumulation and oxidative damage to nucleic acids in Alzheimer disease. Neurobiol Dis 2010; 37:731-7; PMID:20034567; http://dx.doi.org/10.1016/j.nbd. 2009.12.012
35. Swomley AM, Förster S, Keeney JT, Triplett J, Zhang Z, Sultana R, Butterfield DA. Abeta, oxidative stress in Alzheimer disease: Evidence based on proteomics studies. Biochim Biophys Acta 2013; PMID:24120836; http://dx.doi.org/10.1016/j.bbadis.2013.09.015
36. Hardas SS, Sultana R, Clark AM, Beckett TL, Szweda LI, Murphy MP, Butterfield DA. Oxidative modification of lipoic acid by HNE in Alzheimer disease brain. Redox Biol 2013; 1:80-5; PMID:24024140; http://dx.doi.org/10. 1016/j.redox.2013.01.002
37. Teng HK, Teng KK, Lee R, Wright S, Tevar S, Almeida RD, Kermani P, Torkin R, Chen ZY, Lee FS, et al. ProBDNF induces neuronal apoptosis via activation of a receptor complex of p75NTR and sortilin. J Neurosci 2005; 25:5455-63; PMID:15930396; http://dx.doi.org/10.1523/JNEUROSCI.5123-04.2005
38. Hellweg R, Lohmann P, Huber R, Kühl A, Riepe MW. Spatial navigation in complex and radial mazes in APP23 animals and neurotrophin signaling as a biological marker of early impairment. Learn Mem 2006; 13:63-71; PMID:16418433; http://dx.doi.org/10.1101/lm.2606
39. Schulte-Herbrüggen O, Eckart S, Deicke U, Kühl A, Otten U, Danker-Hopfe H, Abramowski D, Staufenbiel M, Hellweg R. Age-dependent time course of cerebral brain-derived neurotrophic factor, nerve growth factor, and neurotrophin-3 in APP23 transgenic mice. J Neurosci Res 2008; 86:2774-83; PMID:18438945; http://dx.doi.org/10.1002/jnr.21704
40. Burbach GJ, Hellweg R, Haas CA, Del Turco D, Deicke U, Abramowski D, Jucker M, Staufenbiel M, Deller T. Induction of brain-derived neurotrophic factor in plaque-associated glial cells of aged APP23 transgenic mice. J Neurosci 2004; 24:2421-30; PMID:15014117; http://dx.doi.org/10.1523/JNEUROSCI. 5599-03.2004
41. Provenzano MJ, Minner SA, Zander K, Clark JJ, Kane CJ, Green SH, Hansen MR. p75(NTR) expression and nuclear localization of p75(NTR) intracellular domain in spiral ganglion Schwann cells following deafness correlate with cell proliferation. Mol Cell Neurosci 2011; 47:306-15; PMID:21658451; http://dx.doi.org/10.1016/j.mcn.2011.05.010
42. Mattson MP. Calcium and neurodegeneration. Aging Cell 2007; 6:337-50; PMID:17328689; http://dx.doi.org/10.1111/j.1474-9726.2007.00275.x
43. Armogida M, Nisticò R, Mercuri NB. Therapeutic potential of targeting hydrogen peroxide metabolism in the treatment of brain ischaemia. Br J Pharmacol 2012; 166:1211-24; PMID:22352897; http://dx.doi.org/10.1111/j.1476- 5381.2012.01912.x
44. Ristow M, Schmeisser S. Extending life span by increasing oxidative stress. Free Radic Biol Med 2011; 51:327-36; PMID:21619928; http://dx.doi.org/ 10.1016/j.freeradbiomed.2011.05.010
45. Lesné S, Koh MT, Kotilinek L, Kayed R, Glabe CG, Yang A, Gallagher M, Ashe KH. A specific amyloid-beta protein assembly in the brain impairs memory. Nature 2006; 440:352-7; PMID:16541076; http://dx.doi.org/10.1038/ nature04533
46. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25:402-8; PMID:11846609; http://dx.doi.org/10.1006/meth.2001.1262
47. D'Angelo B, Benedetti E, Di Loreto S, Cristiano L, Laurenti G, Cerù MP, Cimini A. Signal transduction pathways involved in PPAR β/δ-induced neuronal differentiation. J Cell Physiol 2011; 226:2170-80; PMID:21520069; http://dx.doi.org/10.1002/jcp.22552