ε-secretase: Reduction of amyloid precursor protein ε-site cleavage in Alzheimer's disease

Current Alzheimer Research

Volumn 5, Issue 2, 2008, Pages 165-171

  Kametani, Fuyuki ^a  

^a TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

Author keywords

secretase; secretase; A ; AICD; Alzheimer's disease; APP; Presenilin

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-40]; AMYLOID PRECURSOR PROTEIN; PRESENILIN 1; PRESENILIN 2; SECRETASE;

ALZHEIMER DISEASE; BINDING AFFINITY; BINDING SITE; CLINICAL FEATURE; CORRELATION ANALYSIS; GENE MUTATION; HUMAN; NONHUMAN; PATHOGENESIS; PATHOPHYSIOLOGY; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; DRUG EFFECT; ENZYMOLOGY; EXTRACELLULAR SPACE; METABOLISM;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; BINDING SITES; EXTRACELLULAR SPACE; HUMANS;

EID: 42149123761     PISSN: 15672050     EISSN: None     Source Type: Journal    
DOI: 10.2174/156720508783954776     Document Type: Review

References (90)

1. Selkoe DJ. Alzheimer's disease: genes, proteins, and therapy. Physiol Rev 81: 741-766 (2001).
2. Suh YH and Checler F. Amyloid precursor protein, presenilins, and alpha-synuclein: molecular pathogenesis and pharmacological applications in Alzheimer's disease. Pharmacol Rev 54: 469-525 (2002).
3. Buxbaum JD, Liu KN, Luo Y, Slack JL, Stocking KL, Peschon JJ, Johnson RS, et al. Evidence that tumor necrosis factor alpha converting enzyme is involved in regulated alpha-secretase cleavage of the Alzheimer amyloid protein precursor. J Biol Chem 273: 27765-27767 (1998).
4. Vassar R, Bennett BD, Babu-Khan S, Kahn S, Mendiaz EA, Denis P, et al. Beta-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science 286: 735-741 (1999).
5. Lammich S, Kojro E, Postina R, Gilbert S, Pfeiffer R, Jasionowski M, et al. Constitutive and regulated alpha-secretase cleavage of Alzheimer's amyloid precursor protein by a disintegrin metalloprotease. Proc Natl Acad Sci USA 96: 3922-3927 (1999).
6. De Strooper B, Saftig P, Craessaerts K, Vanderstichele H, Guhde G, Annaert W, et al. Deficiency of presenilin-1 inhibits the normal cleavage of amyloid precursor protein. Nature 391: 387-390 (1998).
7. Capell A, Grunberg J, Pesold B, Diehlmann A, Citron M, Nixon R, et al. The proteolytic fragments of the Alzheimer's disease-associated presenilin-1 form heterodimers and occur as a 100-150-kDa molecular mass complex. J Biol Chem 273: 3205-3211 (1998).
8. Yu G, Nishimura M, Arawaka S, Levitan D, Zhang L, Tandon A, et al. Nicastrin modulates presenilin-mediated notch/glp-1 signal transduction and betaAPP processing. Nature 407: 48-54 (2000).
9. Goutte C, Tsunozaki M, Hale VA and Priess JR. APH-1 is a multipass membrane protein essential for the Notch signaling pathway in Caenorhabditis elegans embryos. Proc Natl Acad Sci USA 99: 775-779 (2002).
10. Francis R, McGrath G, Zhang J, Ruddy DA, Sym M, Apfeld J, et al. aph-1 and pen-2 are required for Notch pathway signaling, gamma-secretase cleavage of betaAPP, and presenilin protein accumulation. Dev Cell 3: 85-97 (2002).
11. Takasugi N, Tomita T, Hayashi I, Tsuruoka M, Niimura M, Takahashi Y, et al. The role of presenilin cofactors in the gamma-secretase complex. Nature 422: 438-441 (2003).
12. Hardy J and Selkoe DJ. The amyloid hypothesis of alzheimer's disease: progress and problems on the road to therapeutics. Science 297: 353-356 (2002).
13. Hardy JA and Higgins GA. Alzheimer's disease: the amyloid cascade hypothesis. Science 256: 184-185 (1992).
14. Moehlmann T, Winkler E, Xia X, Edbauer D, Murrell J, Capell A, et al. Presenilin-1 mutations of leucine 166 equally affect the generation of the Notch and APP intracellular domains independent of their effect on Abeta 42 production. Proc Natl Acad Sci USA 99: 8025-8030 (2002).
15. Chen F, Gu Y, Hasegawa H, Ruan X, Arawaka S, Fraser P, et al. Presenilin 1 mutations activate gamma 42-secretase but reciprocally inhibit epsilon-secretase cleavage of amyloid precursor protein (APP) and S3-cleavage of notch. J Biol Chem 277: 36521-36526 (2002).
16. Walker ES, Martinez M, Brunkan AL and Goate A. Presenilin 2 familial Alzheimer's disease mutations result in partial loss of function and dramatic changes in Abeta 42/40 ratios. J Neurochem 92: 294-301 (2005).
17. Bentahir M, Nyabi O, Verhamme J, Tolia A, Horre K, Wiltfang J, et al. Presenilin clinical mutations can affect gamma-secretase activity by different mechanisms. J Neurochem 96: 732-742 (2006).
18. Wiley JC, Hudson M, Kanning KC, Schecterson LC and Bothwell M. Familial Alzheimer's disease mutations inhibit gamma-secretase-mediated liberation of beta-amyloid precursor protein carboxy-terminal fragment. J Neurochem 94: 1189-1201 (2005).
19. Tesco G, Ginestroni A, Hiltunen M, Kim M, Dolios G, Hyman BT, et al. APP substitutions V715F and L720P alter PS1 conformation and differentially affect Abeta and AICD generation. J Neurochem 95: 446-456 (2005).
20. Shen J and Kelleher RJ, III. The presenilin hypothesis of Alzheimer's disease: Evidence for a loss-of-function pathogenic mechanism. Proc Natl Acad Sci USA 104: 403-409 (2007).
21. Citron M, Oltersdorf T, Haass C, McConlogue L, Hung AY, Seubert P, et al. Mutation of the beta-amyloid precursor protein in familial Alzheimer's disease increases beta-protein production. Nature 360: 672-674 (1992).
22. Piccini A, Zanusso G, Borghi R, Noviello C, Monaco S, Russo R, et al. Association of a presenilin 1 s170f mutation with a novel alzheimer disease molecular phenotype. Arch Neurol 64: 738-745 (2007).
23. German DC and Eisch AJ. Mouse models of Alzheimer's disease: insight into treatment. Rev Neurosci 15: 353-369 (2004).
24. http://www.molgen.ua.ac.be/ADMutations/
25. Deng Y, Tarassishin L, Kallhoff V, Peethumnongsin E, Wu L, Li Y-M, et al. Deletion of presenilin 1 hydrophilic loop sequence leads to impaired gamma-secretase activity and exacerbated amyloid pathology. J Neurosci 26: 3845-3854 (2006).
26. Wang R, Wang B, He W and Zheng H. Wild-type presenilin 1 protects against Alzheimer's disease mutation-induced amyloid pathology. J Biol Chem 281: 15330-15336 (2006).
27. Siman R, Reaume AG, Savage MJ, Trusko S, Lin Y-G, Scott RW, et al. Presenilin-1 P264L Knock-in mutation: differential effects on abeta production, amyloid deposition, and neuronal vulnerability. J Neurosci 20: 8717-8726 (2000).
28. Brunkan AL, Martinez M, Wang J, Walker ES, Beher D, Shearman MS, et al. Two domains within the first putative transmembrane domain of presenilin 1 differentially influence presenilinase and gamma-secretase activity. J Neurochem 94: 1315-1328 (2005).
29. Schroeter EH, Ilagan MXG, Brunkan AL, Hecimovic S, Li Y-M, Xu M, et al. A presenilin dimer at the core of the gamma-secretase enzyme: Insights from parallel analysis of Notch 1 and APP proteolysis. Proc Natl Acad Sci 100: 13075-13080 (2003).
30. Duering M, Grimm MOW, Grimm HS, Schroder J and Hartmann T. Mean age of onset in familial Alzheimer's disease is determined by amyloid beta 42. Neurobiol Aging 26: 785-788 (2005).
31. Kumar-Singh S, Theuns J, Van Broeck B, Pirici D, Vennekens K, Corsmit E, et al. Mean age-of-onset of familial alzheimer disease caused by presenilin mutations correlates with both increased Abeta42 and decreased Abeta40. Hum Mutat 27: 686-695 (2006).
32. De Jonghe C, Esselens C, Kumar-Singh S, Craessaerts K, Serneels S, Checler F, et al. Pathogenic APP mutations near the gamma-secretase cleavage site differentially affect Abeta secretion and APP C-terminal fragment stability. Hum Mol Genet 10: 1665-1671 (2001).
33. Shioi J, Georgakopoulos A, Mehta P, Kouchi Z, Litterst CM, Baki L, et al. FAD mutants unable to increase neurotoxic Abeta 42 suggest that mutation effects on neurodegeneration may be independent of effects on Abeta. J Neurochem 101: 674-681 (2007).
34. Dickson DW, Crystal HA, Mattiace LA, Masur DM, Blau AD, Davies P, et al. Identification of normal and pathological aging in prospectively studied nondemented elderly humans. Neurobiol Aging 13: 179-189 (1992).
35. Irizarry MC, Soriano F, McNamara M, Page KJ, Schenk D, Games D, et al. Abeta deposition is associated with neuropil changes, but not with overt neuronal loss in the human amyloid precursor protein v717f (PDAPP) transgenic mouse. J Neurosci 17: 7053-7059 (1997).
36. Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, Liosatos M, et al. Diffusible, nonfibrillar ligands derived from Abeta 1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci 95: 6448-6453 (1998).
37. Walsh DM, Hartley DM, Kusumoto Y, Fezoui Y, Condron MM, Lomakin A, et al. Amyloid beta -protein fibrillogenesis. structure and biological activity of protrofibrillar intermediates. J Biol Chem 274: 25945-25952 (1999).
38. Gong Y, Chang L, Viola KL, Lacor PN, Lambert MP, Finch CE, et al. Alzheimer's disease-affected brain: Presence of oligomeric Abeta ligands (ADDLs) suggests a molecular basis for reversible memory loss. Proc Natl Acad Sci USA 100: 10417-10422 (2003).
39. Klyubin I, Walsh DM, Lemere CA, Cullen WK, Shankar GM, Betts V, et al. Amyloid beta protein immunotherapy neutralizes Abeta oligomers that disrupt synaptic plasticity in vivo. Nat Med 11: 556-561 (2005).
40. Lesne S, Koh MT, Kotilinek L, Kayed R, Glabe CG, Yang A, et al. A specific amyloid-beta protein assembly in the brain impairs memory. Nature 440: 352-357 (2006).
41. Dewachter I, Reverse D, Caluwaerts N, Ris L, Kuiperi C, Van den Haute C, et al. Neuronal deficiency of presenilin 1 inhibits amyloid plaque formation and corrects hippocampal long-term potentiation but not a cognitive defect of amyloid precursor protein [V717I] transgenic mice. J Neurosci 22: 3445-3453 (2002).
42. Saura CA, Chen G, Malkani S, Choi S-Y, Takahashi RH, Zhang D, et al. Conditional inactivation of presenilin 1 prevents amyloid accumulation and temporarily rescues contextual and spatial working memory impairments in amyloid precursor protein transgenic mice. J Neurosci 25: 6755-6764 (2005).
43. Galvan V, Gorostiza OF, Banwait S, Ataie M, Logvinova AV, Sitaraman S, et al. Reversal of Alzheimer's-like pathology and behavior in human APP transgenic mice by mutation of Asp664. Proc Natl Acad Sci USA 103: 7130-7135 (2006).
44. Malm TM, Iivonen H, Goldsteins G, Keksa-Goldsteine V, Ahtoniemi T, Kanninen K, et al. Pyrrolidine dithiocarbamate activates akt and improves spatial learning in app/ps1 mice without affecting beta-amyloid burden. J Neurosci 27: 3712-3721 (2007).
45. Wu P, Shen Q, Dong S, Xu Z, Tsien JZ and Hu Y. Calorie restriction ameliorates neurodegenerative phenotypes in forebrain-specific presenilin-1 and presenilin-2 double knockout mice. Neurobiol Aging (2007) [Epub ahead of print]
46. Klunk WE, Price JC, Mathis CA, Tsopelas ND, Lopresti BJ, Ziolko SK, et al. Amyloid Deposition Begins in the Striatum of Presenilin-1 Mutation Carriers from Two Unrelated Pedigrees. J Neurosci 27: 6174-6184 (2007).
47. Vetrivel K, Zhang Y.-W, Xu H and Thinakaran G. Pathological and physiological functions of presenilins. Mol Neurodegen 1: 4 (2006).
48. Gu Y, Misonou H, Sato T, Dohmae N, Takio K and Ihara Y. Distinct intramembrane cleavage of the beta-amyloid precursor protein family resembling gamma-secretase-like cleavage of Notch. J Biol Chem 276: 35235-35238 (2001).
49. Sastre M, Steiner H, Fuchs K, Capell A, Multhaup G, Condron MM, et al. Presenilin-dependent gamma-secretase processing of beta-amyloid precursor protein at a site corresponding to the S3 cleavage of Notch. EMBO Rep 2: 835-841 (2001).
50. Weidemann A, Eggert S, Reinhard FB, Vogel M, Paliga K, Baier G, et al. A novel epsilon-cleavage within the transmembrane domain of the Alzheimer amyloid precursor protein demonstrates homology with Notch processing. Biochemistry 41: 2825-2835 (2002).
51. Yu C, Kim SH, Ikeuchi T, Xu H, Gasparini L, Wang R, et al. Characterization of a presenilin-mediated amyloid precursor protein carboxyl-terminal fragment gamma. Evidence for distinct mechanisms involved in gamma -secretase processing of the APP and Notch1 transmembrane domains. J Biol Chem 276: 43756-43760 (2001).
52. Zhao G, Cui M-Z, Mao G, Dong Y, Tan J, Sun L, et al. Gamma-cleavage is dependent on zeta-cleavage during the proteolytic processing of amyloid precursor protein within its transmembrane domain. J Biol Chem 280: 37689-37697 (2005).
53. Kume H and Kametani F. Abeta 11-40/42 production without gamma-secretase epsilon-site cleavage. Biochem Biophys Res Commun 349: 1356-1360 (2006).
54. Kume H, Sekijima Y, Maruyama K and Kametani F. Gamma-secretase can cleave amyloid precursor protein fragments independent of alpha- and beta-secretase pre-cutting. Int J Mol Med 12: 57-60 (2003).
55. Kume H, Maruyama K and Kametani F. Intracellular domain generation of amyloid precursor protein by epsilon-cleavage depends on C-terminal fragment by alpha-secretase cleavage. Int J Mol Med 13: 121-125 (2004).
56. Lefranc-Jullien S, Sunyach C and Checler F. APPepsilon, the epsilon-secretase-derived N-terminal product of the beta-amyloid precursor protein, behaves as a type I protein and undergoes alpha-, beta-, and gamma-secretase cleavages. J Neurochem 97: 807-817 (2006).
57. Kametani F. Secretion of long Abeta-related peptides processed at epsilon-cleavage site is dependent on the alpha-secretase precutting. FEBS Lett 570: 73-76 (2004).
58. Ryan KA and Pimplikar SW. Activation of GSK-3 and phosphorylation of CRMP2 in transgenic mice expressing APP intracellular domain. J Cell Biol 171: 327-335 (2005).
59. Li Y-M, Lai M-T, Xu M, Huang Q, DiMuzio-Mower J, Sardana MK, et al. Presenilin 1 is linked with gamma -secretase activity in the detergent solubilized state. Proc Natl Acad Sci USA 97: 6138-6143 (2000).
60. Esler WP, Kimberly WT, Ostaszewski BL, Diehl TS, Moore CL, Tsai J-Y, et al. Transition-state analogue inhibitors of [ggr]-secretase bind directly to presenilin-1. 2: 428-434 (2000).
61. Funamoto S, Morishima-Kawashima M, Tanimura Y, Hirotani N, Saido TC and Ihara Y. Truncated carboxyl-terminal fragments of beta-amyloid precursor protein are processed to amyloid beta-proteins 40 and 42. Biochemistry 43: 13532-13540 (2004).
62. Zhao G, Mao G, Tan J, Dong Y, Cui M-Z, Kim S-H, et al. Identification of a new presenilin-dependent zeta -cleavage site within the transmembrane domain of amyloid precursor protein. J Biol Chem 279: 50647-50650 (2004).
63. Petit A, Bihel F, da Costa CA, Pourquie O, Checler F and Kraus JL. New protease inhibitors prevent gamma-secretase-mediated production of Abeta40/42 without affecting Notch cleavage. Nat Cell Biol 3: 507-511 (2001).
64. Petit A, Pasini A, Alves Da Costa C, Ayral E, Hernandez JF, Dumanchin-Njock C, et al. JLK isocoumarin inhibitors: selective gamma-secretase inhibitors that do not interfere with notch pathway in vitro or in vivo. J Neurosci Res 74: 370-377 (2003).
65. Checler F, Alves da Costa C, Ayral E, Andrau D, Dumanchin C, Farzan M, et al. JLK inhibitors: isocoumarin compounds as putative probes to selectively target the gamma-secretase pathway. Curr Alzheimer Res 2: 327-334 (2005).
66. Netzer WJ, Dou F, Cai D, Veach D, Jean S, Li Y, et al. Gleevec inhibits beta-amyloid production but not Notch cleavage. Proc Natl Acad Sci USA 100: 12444-12449 (2003).
67. Anderson JJ, Holtz G, Baskin PP, Turner M, Rowe B, Wang B, et al. Reductions in beta-amyloid concentrations in vivo by the gamma-secretase inhibitors BMS-289948 and BMS-299897. Biochem Pharmacol 69: 689-698 (2005).
68. Chen F, Hasegawa H, Schmitt-Ulms G, Kawarai T, Bohm C, Katayama T, et al. TMP21 is a presenilin complex component that modulates gamma-secretase but not epsilon-secretase activity. Nature 440: 1208-1212 (2006).
69. Skovronsky DM, Moore DB, Milla ME, Doms RW and Lee VM. Protein kinase C-dependent alpha-secretase competes with beta-secretase for cleavage of amyloid-beta precursor protein in the trans-golgi network. J Biol Chem 275: 2568-2575 (2000).
70. Holsinger RM, McLean CA, Beyreuther K, Masters CL and Evin G. Increased expression of the amyloid precursor beta-secretase in Alzheimer's disease. Ann Neurol 51: 783-786 (2002).
71. Yang LB, Lindholm K, Yan R, Citron M, Xia W, Yang XL, et al. Elevated beta-secretase expression and enzymatic activity detected in sporadic Alzheimer disease. Nat Med 9: 3-4 (2003).
72. Cao X and Sudhof TC. A transcriptionally active complex of APP with Fe65 and histone acetyltransferase Tip60. Science 293: 115-120 (2001).
73. Baek SH, Ohgi KA, Rose DW, Koo EH, Glass CK and Rosenfeld MG. Exchange of N-CoR corepressor and Tip60 coactivator complexes links Gene expression by NF-kappaB and beta-amyloid precursor protein. Cell 110: 55-67 (2002).
74. Kim H-S, Kim E-M, Lee J-P, Park CH, Kim S, Seo J-H, et al. C-terminal fragments of amyloid precursor protein exert neurotoxicity by inducing glycogen synthase kinase-3 beta expression. FASEB J 17: 1951-1953 (2003).
75. von Rotz RC, Kohli BM, Bosset J, Meier M, Suzuki T, Nitsch RM, et al. The APP intracellular domain forms nuclear multiprotein complexes and regulates the transcription of its own precursor. J Cell Sci 117: 4435-4448 (2004).
76. Pardossi-Piquard R, Petit A, Kawarai T, Sunyach C, Alves da Costa C, Vincent B, et al. Presenilin-dependent transcriptional control of the abeta-degrading enzyme neprilysin by intracellular domains of betaAPP and APLP. Neuron 46: 541-554 (2005).
77. Hebert SS, Serneels L, Tolia A, Craessaerts K, Derks C, Filippov MA, et al. Regulated intramembrane proteolysis of amyloid precursor protein and regulation of expression of putative target genes. EMBO Rep 7: 739-745 (2006).
78. Chen AC and Selkoe DJ. Response to: Pardossi-Piquard, et al., "Presenilin-Dependent Transcriptional Control of the Abeta-Degrading Enzyme Neprilysin by Intracellular Domains of betaAPP and APLP." Neuron 46, 541-554. Neuron 53: 479-483 (2007).
79. Pardossi-Piquard R, Dunys J, Kawarai T, Sunyach C, Alves da Costa C, Vincent B, et al. Response to Correspondence: Pardossi-Piquard, et al., "Presenilin-Dependent Transcriptional Control of the Abeta-Degrading Enzyme Neprilysin by Intracellular Domains of betaAPP and APLP." Neuron 46, 541-554. Neuron 53: 483-486 (2007).
80. Howell S, Nalbantoglu J and Crine P. Neutral endopeptidase can hydrolyze beta-amyloid(1-40) but shows no effect on beta-amyloid precursor protein metabolism. Peptides 16: 647-652 (1995).
81. Iwata N, Tsubuki S, Takaki Y, Watanabe K, Sekiguchi M, Hosoki E, et al. Identification of the major Abeta 1-42-degrading catabolic pathway in brain parenchyma: Suppression leads to biochemical and pathological deposition. 6: 143-150 (2000).
82. Farris W, Schutz SG, Cirrito JR, Shankar GM, Sun X, George A, et al. Loss of neprilysin function promotes amyloid plaque formation and causes cerebral amyloid angiopathy. Am J Pathol 171: 241-251 (2007).
83. Kopan R and Ilagan MXG. Gamma-secretase: proteasome of membrane? Nat Rev Mol Cell Biol 5: 499-504 (2004).
84. Yoshikawa K, Aizawa T and Hayashi Y. Degeneration in vitro of post-mitotic neurons overexpressing the Alzheimer amyloid protein precursor. Nature 359: 64-67 (1992).
85. Oster-Granite ML, McPhie DL, Greenan J and Neve RL. Age-dependent neuronal and synaptic degeneration in mice transgenic for the C Terminus of the amyloid precursor protein. J Neurosci 16: 6732-6741 (1996).
86. Gunawardena S and Goldstein LS. Disruption of axonal transport and neuronal viability by amyloid precursor protein mutations in Drosophila. Neuron 32: 389-401 (2001).
87. Salehi A, Delcroix J-D, Belichenko PV, Zhan K, Wu C, Valletta JS, et al. Increased App expression in a mouse model of down's syndrome disrupts NGF transport and causes cholinergic neuron degeneration. Neuron 51: 29-42 (2006).
88. Kimberly WT, Zheng JB, Guenette SY and Selkoe DJ. The intracellular domain of the beta-amyloid precursor protein is stabilized by Fe65 and translocates to the nucleus in a notch-like manner. J Biol Chem 276: 40288-40292 (2001).
89. Rovelet-Lecrux A, Hannequin D, Raux G, Meur NL, Laquerriere A, Vital A, et al. APP locus duplication causes autosomal dominant early-onset Alzheimer disease with cerebral amyloid angiopathy. Nat Genet 38: 24-26 (2006).
90. Theuns J, Marjaux E, Vandenbulcke M, Van Laere K, Kumar-Singh S, Bormans G, et al. Alzheimer dementia caused by a novel mutation located in the APP C-terminal intracytosolic fragment. Hum Mutat 27: 888-896 (2006).