Loss of PAFAH1B2 reduces amyloid-β generation by promoting the degradation of amyloid precursor protein C-terminal fragments

Journal of Neuroscience

Volumn 32, Issue 50, 2012, Pages 18204-18214

  Page, Richard M ^a   Münch, Anna ^a   Horn, Thomas ^d   Kuhn, Peer Hendrik ^a,b   Colombo, Alessio ^a,b   Reiner, Orly ^c   Boutros, Michael ^d   Steiner, Harald ^a,b   Lichtenthaler, Stefan F ^a,b,e,f   Haass, Christian ^a,b,f  

^a UNIVERSITY OF MUNICH   (Germany)

^b GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^c WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^d GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^e TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^f Germany 3 Munich Cluster for Systems Neurology   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

1 ALKYL 2 ACETYLGLYCEROPHOSPHOCHOLINE ESTERASE; 1 ALKYL 2 ACETYLGLYCEROPHOSPHOCHOLINE ESTERASE 1B2; AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DROSOPHILA; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RNA INTERFERENCE;

1-ALKYL-2-ACETYLGLYCEROPHOSPHOCHOLINE ESTERASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; DROSOPHILA; GENE KNOCKDOWN TECHNIQUES; HEK293 CELLS; HUMANS; MICE; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; PEPTIDE FRAGMENTS; RNA INTERFERENCE; TRANSFECTION;

EID: 84870998907     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2681-12.2012     Document Type: Article

References (49)

1. Arai H, Koizumi H, Aoki J, Inoue K (2002) Platelet-activating factor acetylhydrolase (PAF-AH). J Biochem 131:635-640. CrossRef Medline
2. Bechler ME, Doody AM, Ha KD, Judson BL, Chen I, Brown WJ (2011) The phospholipase A enzyme complex PAFAH Ib mediates endosomal membrane tubule formation and trafficking. Mol Biol Cell 22:2348-2359. CrossRef Medline
3. Blank ML, Lee T, Fitzgerald V, Snyder F (1981) A specific acetylhydrolase for 1-alkyl-2-acetyl-sn-glycero-3-phosphocholine (a hypotensive and platelet-activating lipid). J Biol Chem 256:175-178. Medline
4. Boutros M, Ahringer J (2008) The art and design of genetic screens: RNA interference. Nat Rev Genet 9:554-566. CrossRef Medline
5. Boutros M, Kiger AA, Armknecht S, Kerr K, Hild M, Koch B, Haas SA, Paro R, Perrimon N; Heidelberg Fly Array Consortium (2004) Genome-wide RNAi analysis of growth and viability in Drosophila cells. Science 303:832-835. CrossRef Medline
6. Boutros M, Brás LP, Huber W (2006) Analysis of cell-based RNAi screens. Genome Biol 7:R66. CrossRef Medline
7. Carmine-Simmen K, Proctor T, Tschäpe J, Poeck B, Triphan T, Strauss R, Kretzschmar D (2009) Neurotoxic effects induced by the Drosophila amyloid-beta peptide suggest a conserved toxic function. Neurobiol Dis 33:274-281. CrossRef Medline
8. Chen WJ, Goldstein JL, Brown MS (1990) NPXY, a sequence often found in cytoplasmic tails, is required for coated pit-mediated internalization of the low density lipoprotein receptor. J Biol Chem 265:3116-3123. Medline
9. Citron M (2010) Alzheimer's disease: strategies for disease modification. Nat Rev Drug Discov 9:387-398. CrossRef Medline
10. Citron M, Oltersdorf T, Haass C, McConlogue L, Hung AY, Seubert P, Vigo-Pelfrey C, Lieberburg I, Selkoe DJ (1992) Mutation of the beta-amyloid precursor protein in familial Alzheimer's disease increases beta-protein production. Nature 360:672-674. CrossRef Medline
11. Colombo A, Wang H, Kuhn PH, Page R, Kremmer E, Dempsey PJ, Crawford HC, Lichtenthaler SF (2012) Constitutive alpha-and beta-secretase cleavages of the amyloid precursor protein are partially coupled in neurons, but not in frequently used cell lines. Neurobiol Dis 49C:137-147. CrossRef Medline
12. Edbauer D, Winkler E, Haass C, Steiner H (2002) Presenilin and nicastrin regulate each other and determine amyloid beta-peptide production via complex formation. Proc Natl Acad Sci U S A 99:8666-8671. CrossRef Medline
13. Edbauer D, Winkler E, Regula JT, Pesold B, Steiner H, Haass C (2003) Reconstitution of gamma-secretase activity. Nat Cell Biol 5:486-488. CrossRef Medline
14. Fossgreen A, Brückner B, Czech C, Masters CL, Beyreuther K, Paro R (1998) Transgenic Drosophila expressing human amyloid precursor protein show gamma-secretase activity and a blistered-wing phenotype. Proc Natl Acad Sci U S A 95:13703-13708. CrossRef Medline
15. Greeve I, Kretzschmar D, Tschäpe JA, Beyn A, Brellinger C, Schweizer M, Nitsch RM, Reifegerste R (2004) Age-dependent neurodegeneration and Alzheimer-amyloid plaque formation in transgenic Drosophila. J Neurosci 24:3899-3906. CrossRef Medline
16. Haass C (2004) Take five: BACE and the gamma-secretase quartet conduct Alzheimer's amyloid beta-peptide generation. EMBO J 23:483-488. CrossRef Medline
17. Haass C, Selkoe DJ (2007) Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide. Nat Rev Mol Cell Biol 8:101-112. CrossRef Medline
18. Haass C, Koo EH, Mellon A, Hung AY, Selkoe DJ (1992) Targeting of cellsurface beta-amyloid precursor protein to lysosomes: alternative processing into amyloid-bearing fragments. Nature 357:500-503. CrossRef Medline
19. Haass C, Hung AY, Schlossmacher MG, Teplow DB, Selkoe DJ (1993) beta-Amyloid peptide and a 3-kDa fragment are derived by distinct cellular mechanisms. J Biol Chem 268:3021-3024. Medline
20. Haass C, Lemere CA, Capell A, Citron M, Seubert P, Schenk D, Lannfelt L, Selkoe DJ (1995) The Swedish mutation causes early-onset Alzheimer's disease by beta-secretase cleavage within the secretory pathway. Nat Med 1:1291-1296. CrossRef Medline
21. Hattori M, Arai H, Inoue K (1993) Purification and characterization of bovine brain platelet-activating factor acetylhydrolase. J Biol Chem 268: 18748-18753. Medline
22. He G, Luo W, Li P, Remmers C, Netzer WJ, Hendrick J, Bettayeb K, Flajolet M, Gorelick F, Wennogle LP, Greengard P (2010) Gamma-secretase activating protein is a therapeutic target for Alzheimer's disease. Nature 467:95-98. CrossRef Medline
23. Horn T, Sandmann T, Boutros M (2010) Design and evaluation of genomewide libraries for RNA interference screens. Genome Biol 11:R61. CrossRef Medline
24. Kawasumi M, Matsuda S, Matsuoka M, Nishimoto I (2004) Cytoplasmic tail adaptors of Alzheimer's amyloid-beta protein precursor. Mol Neurobiol 30:185-200. CrossRef Medline
25. Koizumi H, Yamaguchi N, Hattori M, Ishikawa TO, Aoki J, Taketo MM, Inoue K, Arai H (2003) Targeted disruption of intracellular type I platelet activating factor-acetylhydrolase catalytic subunits causes severe impairment in spermatogenesis. J Biol Chem 278:12489-12494. CrossRef Medline
26. Kuhn PH, Wang H, Dislich B, Colombo A, Zeitschel U, Ellwart JW, Kremmer E, Rossner S, Lichtenthaler SF (2010) ADAM10 is the physiologically relevant, constitutive alpha-secretase of the amyloid precursor protein in primary neurons. EMBO J 29:3020-3032. CrossRef Medline
27. Lichtenthaler SF (2011) Alpha-secretase in Alzheimer's disease: molecular identity, regulation and therapeutic potential. J Neurochem 116:10-21. CrossRef Medline
28. Lichtenthaler SF, Multhaup G, Masters CL, Beyreuther K (1999) A novel substrate for analyzing Alzheimer's disease gamma-secretase. FEBS Lett 453:288-292. CrossRef Medline
29. Livnat I, Finkelshtein D, Ghosh I, Arai H, Reiner O (2010) PAF-AH catalytic subunits modulate the Wnt pathway in developing GABAergic neurons. Front Cell Neurosci 4. pii:19. Medline
30. Lorenzen A, Samosh J, Vandewark K, Anborgh PH, Seah C, Magalhaes AC, Cregan SP, Ferguson SS, Pasternak SH (2010) Rapid and direct transport of cell surface APP to the lysosome defines a novel selective pathway. Mol Brain 3:11. CrossRef Medline
31. Majercak J, Ray WJ, Espeseth A, Simon A, Shi XP, Wolffe C, Getty K, Marine S, Stec E, Ferrer M, Strulovici B, Bartz S, Gates A, Xu M, Huang Q, Ma L, Shughrue P, Burchard J, Colussi D, Pietrak B, et al. (2006) LRRTM3 promotes processing of amyloid-precursor protein by BACE1 and is a positional candidate gene for late-onset Alzheimer's disease. Proc Natl Acad Sci U S A 103:17967-17972. CrossRef Medline
32. Okochi M, Steiner H, Fukumori A, Tanii H, Tomita T, Tanaka T, Iwatsubo T, Kudo T, Takeda M, Haass C (2002) Presenilins mediate a dual intramembranous gamma-secretase cleavage of Notch-1. EMBO J 21: 5408-5416. CrossRef Medline
33. Page RM, Baumann K, Tomioka M, Pérez-Revuelta BI, Fukumori A, Jacobsen H, Flohr A, Luebbers T, Ozmen L, Steiner H, Haass C (2008) Generation of Abeta38 and Abeta42 is independently and differentially affected by familial Alzheimer disease-associated presenilin mutations and gammasecretase modulation. J Biol Chem 283:677-683. CrossRef Medline
34. Page RM, Gutsmiedl A, Fukumori A, Winkler E, Haass C, Steiner H (2010) Beta-amyloid precursor protein mutants respond to gamma-secretase modulators. J Biol Chem 285:17798-17810. CrossRef Medline
35. Ring S, Weyer SW, Kilian SB, Waldron E, Pietrzik CU, Filippov MA, Herms J, Buchholz C, Eckman CB, Korte M, Wolfer DP, Müller UC (2007) The secreted beta-amyloid precursor protein ectodomain APPs alpha is sufficient to rescue the anatomical, behavioral, and electrophysiological abnormalities of APP-deficient mice. J Neurosci 27:7817-7826. CrossRef Medline
36. Rooke J, Pan D, Xu T, Rubin GM (1996) KUZ, a conserved metalloproteasedisintegrin protein with two roles in Drosophila neurogenesis. Science 273:1227-1231. CrossRef Medline
37. Rubin GM, Yandell MD, Wortman JR, Gabor Miklos GL, Nelson CR, Hariharan IK, Fortini ME, Li PW, Apweiler R, Fleischmann W, Cherry JM, Henikoff S, Skupski MP, Misra S, Ashburner M, Birney E, Boguski MS, Brody T, Brokstein P, Celniker SE, et al. (2000) Comparative genomics of the eukaryotes. Science 287:2204-2215. CrossRef Medline
38. Schroeter EH, Kisslinger JA, Kopan R (1998) Notch-1 signalling requires ligand-induced proteolytic release of intracellular domain. Nature 393: 382-386. CrossRef Medline
39. Selkoe DJ, Yamazaki T, Citron M, Podlisny MB, Koo EH, Teplow DB, Haass C (1996) The role of APP processing and trafficking pathways in the formation of amyloid beta-protein. Ann N Y Acad Sci 777:57-64. CrossRef Medline
40. Sheffield PJ, Garrard S, Caspi M, Aoki J, Arai H, Derewenda U, Inoue K, Suter B, Reiner O, Derewenda ZS (2000) Homologs of the alpha-and betasubunits of mammalian brain platelet-activating factor acetylhydrolase Ib in the Drosophila melanogaster genome. Proteins 39:1-8. CrossRef Medline
41. Shinohara M, Sato N, Kurinami H, Takeuchi D, Takeda S, Shimamura M, Yamashita T, Uchiyama Y, Rakugi H, Morishita R (2010) Reduction of brain beta-amyloid (Abeta) by fluvastatin, a hydroxymethylglutaryl-CoA reductase inhibitor, through increase in degradation of amyloid precursor protein C-terminal fragments (APP-CTFs) and Abeta clearance. J Biol Chem 285:22091-22102. CrossRef Medline
42. Six E, Ndiaye D, Laabi Y, Brou C, Gupta-Rossi N, Israel A, Logeat F (2003) The Notch ligand Delta1 is sequentially cleaved by an ADAM protease and gamma-secretase. Proc Natl Acad Sci U S A 100:7638-7643. CrossRef Medline
43. Steiner H, Kostka M, Romig H, Basset G, Pesold B, Hardy J, Capell A, Meyn L, Grim ML, Baumeister R, Fechteler K, Haass C (2000) Glycine 384 is required for presenilin-1 function and is conserved in bacterial polytopic aspartyl proteases. Nat Cell Biol 2:848-851. CrossRef Medline
44. Steiner H, Fluhrer R, Haass C (2008) Intramembrane proteolysis by gamma-secretase. J Biol Chem 283:29627-29631. CrossRef Medline
45. Tarricone C, Perrina F, Monzani S, Massimiliano L, Kim MH, Derewenda ZS, Knapp S, Tsai LH, Musacchio A (2004) Coupling PAF signaling to dynein regulation: structure of LIS1 in complex with PAF-acetylhydrolase. Neuron 44:809-821. CrossRef Medline
46. Thathiah A, Spittaels K, Hoffmann M, Staes M, Cohen A, Horré K, Vanbrabant M, Coun F, Baekelandt V, Delacourte A, Fischer DF, Pollet D, De Strooper B, Merchiers P (2009) The orphan G protein-coupled receptor 3 modulates amyloid-beta peptide generation in neurons. Science 323: 946-951. CrossRef Medline
47. Thinakaran G, Koo EH (2008) Amyloid precursor protein trafficking, processing, and function. J Biol Chem 283:29615-29619. CrossRef Medline
48. Yan W, Assadi AH, Wynshaw-Boris A, Eichele G, Matzuk MM, Clark GD (2003) Previously uncharacterized roles of platelet-activating factor acetylhydrolase 1b complex in mouse spermatogenesis. Proc Natl Acad Sci U S A 100:7189-7194. CrossRef Medline
49. Zhang G, Assadi AH, McNeil RS, Beffert U, Wynshaw-Boris A, Herz J, Clark GD, D'Arcangelo G (2007) The Pafah1b complex interacts with the reelin receptor VLDLR. PLoS One 2:e252. CrossRef Medline