Oxidized docosahexaenoic acid species and lipid peroxidation products increase amyloidogenic amyloid precursor protein processing

Neurodegenerative Diseases

Volumn 16, Issue 1-2, 2016, Pages 44-54

  Grimm, Marcus O W ^a   Haupenthal, Viola J ^a   Mett, Janine ^a   Stahlmann, Christoph P ^a   Blumel, Tamara ^a   Mylonas, Nadine T ^a   Endres, Kristina ^b   Grimm, Heike S ^a   Hartmann, Tobias ^a  

^a SAARLAND UNIVERSITY   (Germany)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

Amyloid precursor protein processing; Lipid peroxidation; Oxidized docosahexaenoic acid; Amyloid

Indexed keywords

4 HYDROXYNONENAL; AMYLOID PRECURSOR PROTEIN; BETA SECRETASE; DOCOSAHEXAENOIC ACID; GAMMA SECRETASE; OMEGA 3 FATTY ACID; OMEGA 6 FATTY ACID; REACTIVE OXYGEN METABOLITE; AMYLOID BETA PROTEIN; SECRETASE;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL CELL CULTURE; ANTIOXIDANT ACTIVITY; AUTOPSY; BLOOD LEVEL; CONFERENCE PAPER; HUMAN; HUMAN CELL; HUMAN TISSUE; LIPID PEROXIDATION; MOUSE; NEUROBLASTOMA CELL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PROCESSING; ANALOGS AND DERIVATIVES; ANIMAL; BRAIN; C57BL MOUSE; CELL CULTURE; CELL MEMBRANE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; MALE; MASS SPECTROMETRY; METABOLISM; NERVE CELL; OXIDATION REDUCTION REACTION; REAL TIME POLYMERASE CHAIN REACTION; TISSUE BANK; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; BRAIN; CELL MEMBRANE; CELLS, CULTURED; DOCOSAHEXAENOIC ACIDS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMANS; LIPID PEROXIDATION; MALE; MASS SPECTROMETRY; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURONS; OXIDATION-REDUCTION; REAL-TIME POLYMERASE CHAIN REACTION; TISSUE BANKS;

EID: 84958044754     PISSN: 16602854     EISSN: 16602862     Source Type: Journal    
DOI: 10.1159/000440839     Document Type: Conference Paper

References (41)

1. Masters CL, Simms G, Weinman NA, Multhaup G, McDonald BL, Beyreuther K: Amyloid plaque core protein in Alzheimer disease and Down syndrome. Pro Natl Acad Sci USA 1985; 82: 4245-4249.
2. Grundke-Iqbal I, Iqbal K, Tung YC, Quinlan M, Wisniewski HM, Binder LI: Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology. Proc Natl Acad Sci USA 1986; 83: 4913-4917.
3. Zhang YW, Thompson R, Zhang H, Xu H: APP processing in Alzheimer's disease. Mol Brain 2011; 4: 3.
4. Kimberly WT, LaVoie MJ, Ostaszewski BL, Ye W, Wolfe MS, Selkoe DJ: Gamma-secretase is a membrane protein complex comprised of presenilin, nicastrin, APH-1, and presenilin enhancer 2. Proc Natl Acad Sci USA 2003; 100: 6382-6387.
5. Ehehalt R, Keller P, Haass C, Thiele C, Simons K: Amyloidogenic processing of the Alzheimer beta-amyloid precursor protein depends on lipid rafts. J Cell Biol 2003; 160: 113-123.
6. Grimm MO, Zinser EG, Grosgen S, Hundsdorfer B, Rothhaar TL, Burg VK, Kaestner L, Bayer TA, Lipp P, Muller U, Grimm HS, Hartmann T: Amyloid precursor protein (APP) mediated regulation of ganglioside homeostasis linking Alzheimer's disease pathology with ganglioside metabolism. PLoS One 2012; 7:e34095.
7. Zha Q, Ruan Y, Hartmann T, Beyreuther K, Zhang D: GM1 ganglioside regulates the proteolysis of amyloid precursor protein. Mol Psychiatry 2004; 9: 946-952.
8. Grimm MO, Grimm HS, Patzold AJ, Zinser EG, Halonen R, Duering M, Tschape JA, De Strooper B, Muller U, Shen J, Hartmann T: Regulation of cholesterol and sphingomyelin metabolism by amyloid-beta and presenilin. Nat Cell Biol 2005; 7: 1118-1123.
9. Grimm MO, Rothhaar TL, Grosgen S, Burg VK, Hundsdorfer B, Haupenthal VJ, Friess P, Kins S, Grimm HS, Hartmann T: Trans fatty acids enhance amyloidogenic processing of the Alzheimer amyloid precursor protein (APP). J Nutr Biochem 2012; 23: 1214-1223.
10. Burg VK, Grimm HS, Rothhaar TL, Grosgen S, Hundsdorfer B, Haupenthal VJ, Zimmer VC, Mett J, Weingartner O, Laufs U, Broersen LM, Tanila H, Vanmierlo T, Lutjohann D, Hartmann T, Grimm MO: Plant sterols the better cholesterol in Alzheimer's disease? A mechanistical study. J Neurosci 2013; 33: 16072-16087.
11. Grimm MO, Grimm HS, Tomic I, Beyreuther K, Hartmann T, Bergmann C: Independent inhibition of Alzheimer disease beta- and gamma-secretase cleavage by lowered cholesterol levels. J Biol Chem 2008; 283: 11302-11311.
12. Grimm MO, Kuchenbecker J, Grosgen S, Burg VK, Hundsdorfer B, Rothhaar TL, Friess P, de Wilde MC, Broersen LM, Penke B, Peter M, Vigh L, Grimm HS, Hartmann T: Docosahexaenoic acid reduces amyloid beta production via multiple pleiotropic mechanisms. J Biol Chem 2011; 286: 14028-14039.
13. Lim GP, Calon F, Morihara T, Yang F, Teter B, Ubeda O, Salem N Jr, Frautschy SA, Cole GM: A diet enriched with the omega-3 fatty acid docosahexaenoic acid reduces amyloid burden in an aged Alzheimer mouse model. J Neurosci 2005; 25: 3032-3040.
14. Oksman M, Iivonen H, Hogyes E, Amtul Z, Penke B, Leenders I, Broersen L, Lutjohann D, Hartmann T, Tanila H: Impact of different saturated fatty acid, polyunsaturated fatty acid and cholesterol containing diets on beta-amyloid accumulation in APP/PS1 transgenic mice. Neurobiol Dis 2006; 23: 563-572.
15. Perez SE, Berg BM, Moore KA, He B, Counts SE, Fritz JJ, Hu YS, Lazarov O, Lah JJ, Mufson EJ: DHA diet reduces AD pathology in young APPSWE/PS1 delta E9 transgenic mice: possible gender effects. J Neurosci Res 2010; 88: 1026-1040.
16. Soderberg M, Edlund C, Kristensson K, Dallner G: Fatty acid composition of brain phospholipids in aging and in Alzheimer's disease. Lipids 1991; 26: 421-425.
17. Tully AM, Roche HM, Doyle R, Fallon C, Bruce I, Lawlor B, Coakley D, Gibney MJ: Low serum cholesteryl ester-docosahexaenoic acid levels in Alzheimer's disease: a case-control study. Br J Nutr 2003; 89: 483-489.
18. Bazinet RP, Laye S: Polyunsaturated fatty acids and their metabolites in brain function and disease. Nat Rev Neurosci 2014; 15: 771-785.
19. Cai Z, Zhao B, Ratka A: Oxidative stress and beta-amyloid protein in Alzheimer's disease. Neuromol Med 2011; 13: 223-250.
20. Lukiw WJ, Cui JG, Marcheselli VL, Bodker M, Botkjaer A, Gotlinger K, Serhan CN, Bazan NG: A role for docosahexaenoic acid-derived neuroprotectin D1 in neural cell survival and Alzheimer disease. J Clin Invest 2005; 115: 2774-2783.
21. Roberts LJ 2nd, Montine TJ, Markesbery WR, Tapper AR, Hardy P, Chemtob S, Dettbarn WD, Morrow JD: Formation of isoprostanelike compounds (neuroprostanes) in vivo from docosahexaenoic acid. J Biol Chem 1998; 273: 13605-13612.
22. Subbarao KV, Richardson JS, Ang LC: Autopsy samples of Alzheimer's cortex show increased peroxidation in vitro. J Neurochem 1990; 55: 342-345.
23. Musiek ES, Cha JK, Yin H, Zackert WE, Terry ES, Porter NA, Montine TJ, Morrow JD: Quantification of F-ring isoprostane-like compounds (F4-neuroprostanes) derived from docosahexaenoic acid in vivo in humans by a stable isotope dilution mass spectrometric assay. J Chromatogr B Anal Technol Biomed Life Sci 2004; 799: 95-102.
24. Ida N, Hartmann T, Pantel J, Schroder J, Zerfass R, Forstl H, Sandbrink R, Masters CL, Beyreuther K: Analysis of heterogeneous A4 peptides in human cerebrospinal fluid and blood by a newly developed sensitive Western blot assay. J Biol Chem 1996; 271: 22908-22914.
25. Grimm MO, Stahlmann CP, Mett J, Haupenthal VJ, Zimmer VC, Lehmann J, Hundsdorfer B, Endres K, Grimm HS, Hartmann T: Vitamin E: curse or benefit in Alzheimer's disease? A systematic investigation of the impact of α-, γ- and δ-tocopherol on A. generation and degradation in neuroblastoma cells. J Nutr Health Aging 2015; 19: 646-656.
26. Rothhaar TL, Grosgen S, Haupenthal VJ, Burg VK, Hundsdorfer B, Mett J, Riemenschneider M, Grimm HS, Hartmann T, Grimm MO: Plasmalogens inhibit APP processing by directly affecting gamma-secretase activity in Alzheimer's disease. Sci World J 2012; 2012: 141240.
27. Oakley H, Cole SL, Logan S, Maus E, Shao P, Craft J, Guillozet-Bongaarts A, Ohno M, Disterhoft J, Van Eldik L, Berry R, Vassar R: Intraneuronal beta-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer's disease mutations: potential factors in amyloid plaque formation. J Neurosci 2006; 26: 10129-10140.
28. Sahlin C, Pettersson FE, Nilsson LN, Lannfelt L, Johansson AS: Docosahexaenoic acid stimulates non-amyloidogenic APP processing resulting in reduced Abeta levels in cellular models of Alzheimer's disease. Eur J Neurosci 2007; 26: 882-889.
29. Marcheselli VL, Hong S, Lukiw WJ, Tian XH, Gronert K, Musto A, Hardy M, Gimenez JM, Chiang N, Serhan CN, Bazan NG: Novel docosanoids inhibit brain ischemia-reperfusion- mediated leukocyte infiltration and proinflammatory gene expression. J Biol Chem 2003; 278: 43807-43817.
30. Groeger AL, Cipollina C, Cole MP, Woodcock SR, Bonacci G, Rudolph TK, Rudolph V, Freeman BA, Schopfer FJ: Cyclooxygenase-2 generates anti-inflammatory mediators from omega-3 fatty acids. Nat Chem Biol 2010; 6: 433-441.
31. Serhan CN, Hong S, Gronert K, Colgan SP, Devchand PR, Mirick G, Moussignac RL: Resolvins: a family of bioactive products of omega- 3 fatty acid transformation circuits initiated by aspirin treatment that counter proinflammation signals. J Exp Med 2002; 196: 1025-1037.
32. Freund-Levi Y, Eriksdotter-Jonhagen M, Cederholm T, Basun H, Faxen-Irving G, Garlind A, Vedin I, Vessby B, Wahlund LO, Palmblad J: Omega-3 fatty acid treatment in 174 patients with mild to moderate Alzheimer disease: Omegad study: a randomized double-blind trial. Arch Neurol 2006; 63: 1402-1408.
33. Chiu CC, Su KP, Cheng TC, Liu HC, Chang CJ, Dewey ME, Stewart R, Huang SY: The effects of omega-3 fatty acids monotherapy in Alzheimer's disease and mild cognitive impairment: a preliminary randomized doubleblind placebo-controlled study. Prog Neuropsychopharmacol Biol Psychiatry 2008; 32: 1538-1544.
34. Quinn JF, Raman R, Thomas RG, Yurko- Mauro K, Nelson EB, Van Dyck C, Galvin JE, Emond J, Jack CR Jr, Weiner M, Shinto L, Aisen PS: Docosahexaenoic acid supplementation and cognitive decline in Alzheimer disease: a randomized trial. JAMA 2010; 304: 1903-1911.
35. Lee LK, Shahar S, Chin AV, Yusoff NA: Docosahexaenoic acid-concentrated fish oil supplementation in subjects with mild cognitive impairment (MCI): a 12-month randomised, double-blind, placebo-controlled trial. Psychopharmacology 2013; 225: 605-612.
36. Kalmijn S, Launer LJ, Ott A, Witteman JC, Hofman A, Breteler MM: Dietary fat intake and the risk of incident dementia in the Rotterdam Study. Ann Neurol 1997; 42: 776-782.
37. Barberger-Gateau P, Letenneur L, Deschamps V, Peres K, Dartigues JF, Renaud S: Fish, meat, and risk of dementia: cohort study. BMJ 2002; 325: 932-933.
38. Morris MC, Evans DA, Bienias JL, Tangney CC, Bennett DA, Wilson RS, Aggarwal N, Schneider J: Consumption of fish and n-3 fatty acids and risk of incident Alzheimer disease. Arch Neurol 2003; 60: 940-946.
39. Schaefer EJ, Bongard V, Beiser AS, Lamon- Fava S, Robins SJ, Au R, Tucker KL, Kyle DJ, Wilson PW, Wolf PA: Plasma phosphatidylcholine docosahexaenoic acid content and risk of dementia and Alzheimer disease: the Framingham Heart Study. Arch Neurol 2006; 63: 1545-1550.
40. Van de Rest O, van der Zwaluw N, Beekman AT, de Groot LC, Geleijnse JM: The reliability of three depression rating scales in a general population of Dutch older persons. Int J Geriatr Psychiatry 2010; 25: 998-1005.
41. Stough C, Downey L, Silber B, Lloyd J, Kure C, Wesnes K, Camfield D: The effects of 90- day supplementation with the omega-3 essential fatty acid docosahexaenoic acid (DHA) on cognitive function and visual acuity in a healthy aging population. Neurobiol Aging 2012; 33: 824. e821-e823.