Caveolin-3 upregulation activates β-secretase-mediated cleavage of the amyloid precursor protein in Alzheimer's disease

Journal of Neuroscience

Volumn 19, Issue 15, 1999, Pages 6538-6548

  Nishiyama, Kazutoshi ^a   Trapp, Bruce D ^a   Ikezu, Tsuneya ^a   Ransohoff, Richard M ^a   Tomita, Taisuke ^b   Iwatsubo, Takeshi ^b   Kanazawa, Ichiro ^c   Hsiao, Karen K ^d   Lisanti, Michael P ^e   Okamoto, Takashi ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF TOKYO   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d UNIVERSITY OF MINNESOTA   (United States)

^e ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Alzheimer's disease; Amyloid precursor protein; Astrocyte; Caveolin; Presenilin; Secretase

Indexed keywords

AMYLOID PRECURSOR PROTEIN; BETA SECRETASE; CAVEOLIN; ENZYME; PRESENILIN 1; UNCLASSIFIED DRUG;

AGED; ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; ASTROCYTE; BRAIN TISSUE; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENILE PLAQUE; TRANSGENIC MOUSE;

EID: 0033178782     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-15-06538.1999     Document Type: Article

References (50)

1. Barger SW, Harmon AD (1997) Microglial activation by Alzheimer amyloid precursor protein and modulation by apolipoprotein E. Nature 388:878-881.
2. Bouillot C, Prochiantz A, Rougon G, Allinquant B (1996) Axonal amyloid precursor protein expressed by neurons in vitro is present in a membrane fraction with caveolae-like properties. J Biol Chem 271:7640-7644.
3. Buxbaum JD, Gandy SE, Cicchetti P, Ehrlich ME, Czernk AJ, Fracasso RP, Ramabhadran TV, Unterbeck AJ, Greengard P (1990) Processing of Alzheimer beta/A4 amyloid precursor protein: modulation by agents that regulate protein phosphorylation. Proc Natl Acad Sci USA 87:6003-6006.
4. Cameron PL, Ruffin JW, Bollag R, Rasmussen H, Cameron RS (1997) Identification of caveolin and caveolin-related proteins in the brain. J Neurosci 17:9520-9535.
5. Couet J, Li S, Okamoto T, Ikezu T, Lisanti MP (1997) Identification of peptide and protein ligands for the caveolin-scaffolding domain. Implications for the interaction of caveolin with caveolae-associated proteins. J Biol Chem 272:6525-6533.
6. De Strooper B, Saftig P, Craessaerts K, Vanderstichele H, Guhde G, Annaert W, Von Figura K, Van Leuven F (1998) Deficiency of presenilin-1 inhibits the normal cleavage of amyloid precursor protein. Nature 391:387-390.
7. Dickson DW, Lee SC, Mattiace LA, Yen SH, Brosnan C (1993) Microglia and cytokines in neurological disease, with special reference to AIDS and Alzheimer's disease. Glia 7:75-83.
8. Forman MS, Cook DG, Leight S, Doms RW, Lee VMY (1997) Differential effects of the Swedish mutant amyloid precursor protein on beta-amyloid accumulation and secretion in neurons and nonneuronal cells. J Biol Chem 272:32247-32253.
9. Frautschy SA, Yang F, Irrizarry M, Hyman B, Saido TC, Hsiao K, Cole GM (1998) Microglial response to amyloid plaques in APPsw transgenic mice. Am J Pathol 152:307-317.
10. Galbiati F, Volonte D, Gil O, Zanazzi G, Salzer JL, Sargiacomo M, Scherer PE, Engelman JA, Schlegel A, Parenti M, Okamoto T, Lisanti MP (1998) Expression of caveolins 1 and 2 in differentiating PC12 cells and dorsal root ganglion cells. Proc Natl Acad Sci USA 95:10257-10262.
11. Gegelashvili G, Schousboe A, Linnemann D (1994) Expression of amyloid precursor protein (APP) in rat brain and cultured neural cells. Int J Dev Neurosci 12:703-708.
12. Haass C, Koo EH, Mellon A, Hung AY, Selkoe DJ (1992) Targeting of cell-surface beta-amyloid precursor protein to lysosomes: alternative processing into amyloid-bearing fragments. Nature 357:500-503.
13. Hayashi Y, Kashiwagi K, Yoshikawa K (1992) Protease inhibitors generate cytotoxic fragments from Alzheimer amyloid protein precursor in cDNA-transfected glioma cells. Biochem Biophys Res Commun 187:1249-1255.
14. Howland DS, Trusko SP, Savage MJ, Reaume AG, Lang DM, Hirsch JD, Maeda N, Siman R, Greenberg BD, Scott RW, Flood DG (1998) Modulation of secreted beta-amyloid precursor protein and amyloid beta-peptide in brain by cholesterol. J Biol Chem 273:16576-16582.
15. Hsiao K, Chapman P, Nilsen S, Eckman C, Harigaya Y, Younkin S, Yang F, Cole G (1996) Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 274:99-102.
16. Ikezu T, Trapp BD, Song KS, Schlegel A, Lisanti MP, Okamoto T (1998a) Caveolae, plasma membrane microdomains for alpha-secretase-mediated processing of the amyloid protein precursor. J Biol Chem 273:10485-10495.
17. Ikezu T, Ueda H, Trapp BD, Nishiyama K, Sha JF, Volonte D, Galbiati F, Byrd AL, Bassell G, Serizawa H, Lane WS, Lisanti MP, Okamoto T (1998b) Affinity-purification and characterization of caveolins from the brain. Brain Res 804:177-192.
18. Iwatsubo T, Odaka A, Suzuki N, Mizusawa H, Nukina N, Ihara Y (1994) Visualization of A beta 42(43) and A beta 40 in senile plaques with end-specific A beta monoclonals: evidence that an initially deposited species is A beta 42(43). Neuron 13:45-53.
19. Kim KS, Wen GY, Bancher CM, Chen J, Sapeenza VJ, Hong H, Wisniewski HM (1990) Detection of quantitation of amyloid b-peptide with 2 monoclonal antibodies. Neurosci Res Commun 7:118-122.
20. Kitaguchi N, Tokushima Y, Oishi K, Takahashi Y, Shiojiri S, Nakamura S, Tanaka S, Kodaira R, Ito H (1990) Determination of amyloid beta protein precursors harboring active form of proteinase inhibitor domains in cerebrospinal fluid of Alzheimer's disease patients by trypsin-antibody sandwich ELISA. Biochem Biophys Res Commun 166:1453-1459.
21. Kurzchalia T, Dupree P, Parton RG, Kellner R, Virta H, Lehnert M, Simons K (1992) VIP 21, a 21-kD membrane protein, is an integral component of trans-Golgi-network-derived transport vesicles. J Cell Biol 118:1003-1014.
22. Lee S-J, Liyanage U, Bickel PE, Xia W, Lansbury PT, Kosik KS (1998) A detergent-insoluble membrane compartment contains Abeta in vivo. Nat Med 4:730-734.
23. McGeer PL, McGeer EG (1996) Anti-inflammatory drugs in the fight against Alzheimer's disease. Ann NY Acad Sci 777:213-220.
24. Mochizuki A, Peterson JW, Mufson EJ, Trapp BD (1996) Amyloid load and neuronal elements in Alzheimer's disease and non-demented individuals with high amyloid plaque density. Exp Neurol 142:89-102.
25. Moir RD, Lynch T, Bush AI, Whyte S, Henry A, Portbury S, Multhaup G, Small DH, Tanzi RE, Beyreuther K, Masters CL (1998) Relative increase in Alzheimer's disease of soluble forms of cerebral Abeta amyloid protein precursor containing the Kunitz protease inhibitory domain. J Biol Chem 273:5013-5019.
26. Okamoto T, Takeda S, Murayama Y, Ogata E, Nishimoto I (1995) Ligand-dependent G protein-coupling of amyloid transmembrane precursor. J Biol Chem 270:4205-4208.
27. Okamoto T, Schlegel A, Scherer PE, Lisanti MP (1998) Caveolins, a family of scaffolding proteins for organizing "preassembled signaling complexes" at the plasma membrane. J Biol Chem 273:5419-5422.
28. Palmert MR, Usiak M, Mayeux R. Raskind M, Tourtellotte WW, Younkin SG (1990) Soluble derivatives of the beta amyloid protein precursor in cerebrospinal fluid: alterations in normal aging and in Alzheimer's disease. Neurology 40:1028-1034.
29. Pioro EP, Mitsumoto H (1995) Animal models of ALS. Clin Neurosci 3:375-385.
30. Ransohoff RM, Devajyothi C, Estes ML, Babcock G, Rudick RA, Frohman EM, Barna BP (1991) Interferon-beta specifically inhibits interferon-gamma-induced class II major histocompatibility complex gene transcription in a human astrocytoma cell line. J Neuroimmunol 33:103-112.
31. Scherer PE, Tang Z-L, Chun MC, Sargiacomo M, Lodish HF, Lisanti MP (1995) Caveolin isoforms differ in their N-terminal protein sequence and subcellular distribution: identification and epitope mapping of an isoform-specific monoclonal antibody probe. J Biol Chem 270:16395-16401.
32. Scherer PE, Okamoto T, Chun M, Nishimoto I, Lodish HF, Lisanti MP (1996) Identification, sequence, and expression of caveolin-2 defines a caveolin gene family. Proc Natl Acad Sci USA 93:131-135.
33. Scherer PE, Lewis RY, Volonté D, Engelman JA, Galbiati F, Couet J, Kohtz DS, van Donselaar E, Peters P, Lisanti MP (1997) Cell-type and tissue-specific expression of caveolin-2. Caveolins 1 and 2 co-localize and form a stable hetero-oligomeric complex in vivo. J Biol Chem 272:29337-29346.
34. Selkoe DJ (1994a) Cell biology of the amyloid beta-protein precursor and the mechanism of Alzheimer's disease. Annu Rev Cell Biol 10:373-403.
35. Selkoe DJ (1994b) Normal and abnormal biology of the beta-amyloid precursor protein. Annu Rev Neurosci 17:489-517.
36. Shrikant P, Lee SJ, Kalvakolanu I, Ransohoff RM, Benveniste EN (1996) Stimulus-specific inhibition of intracellular adhesion molecule-1 gene expression by TGF-beta. J Immunol 157:892-900.
37. Simons K, Ikonen E (1997) Functional rafts in cell membranes. Nature 387:569-572.
38. Simons M, Keller P, De Strooper B, Beyreuther K, Dotti CG, Simons K (1998) Cholesterol depletion inhibits the generation of beta-amyloid in hippocampal neurons. Proc Natl Acad Sci USA 95:6460-6464.
39. Sisodia SS (1992) Beta-amyloid precursor protein cleavage by a membrane-bound protease. Proc Natl Acad Sci USA 89:6075-6079.
40. Sisodia SS, Koo EH, Beyreuther K, Unterbeck A, Price DL (1990) Evidence that beta-amyloid protein in Alzheimer's disease is not derived by normal processing. Science 248:492-495.
41. Smart EJ, Ying Y, Mineo C, Anderson RGW (1995) A detergent free method for purifying caveolae membrane from tissue cultured cells. Proc Natl Acad Sci USA 92:10104-10108.
42. Smine A, Xu X, Nishiyama K, Katada T, Gambetti P, Yadav SP, Wu X, Shi Y-C, Yasuhara S, Homburger V, Okamoto T (1998) Regulation of brain G-protein, Go, by Alzheimer disease gene presenilin-1. J Biol Chem 273:16281-16288.
43. Song KS, Li S, Okamoto T, Quilliam L, Sargiacomo M, Lisanti MP (1996a) Copurification and direct interaction of Ras with caveolin, an integral membrane protein of caveolae microdomains. Detergent free purification of caveolae membranes. J Biol Chem 271:9690-9697.
44. Song KS, Scherer PE, Tang Z-L, Okamoto T, Li S, Chafel M, Chu C, Kohtz DS, Lisanti MP (1996b) Expression of caveolin-3 in skeletal, cardiac, and smooth muscle cells. Caveolin-3 is a component of the sarcolemma and co-fractionates with dystrophin and dystrophin-associated glycoproteins. J Biol Chem 271:15160-15165.
45. Song KS, Tang Z, Li S, Lisanti MP (1997) Mutational analysis of the properties of caveolin-1. A novel role for the C-terminal domain in mediating homo-typic caveolin-caveolin interactions. J Biol Chem 272:4398-4403.
46. Tang Z, Scherer PE, Okamoto T, Song K, Chu C, Kohtz DS, Nishimoto I, Lodish HF, Lisanti MP (1996) Molecular cloning of caveolin-3, a novel member of the caveolin gene family expressed predominantly in muscle. J Biol Chem 271:2255-2261.
47. Tomita T, Maruyama K, Saido TC, Kume H, Shinozaki K, Tokuhiro S, Capell A, Walter J, Grunberg J, Haass C, Iwatsubo T, Obata K (1997) The presenilin 2 mutation (N141I) linked to familial Alzheimer disease (Volga German families) increases the secretion of amyloid beta protein ending at the 42nd (or 43rd) residue. Proc Natl Acad Sci USA 94:2025-2030.
48. Wu C, Butz S, Ying YS, Anderson RGW (1997) Tyrosine kinase receptors concentrated in caveolae-like domains from neuronal plasma membrane. J Biol Chem 272:3554-3559.
49. Yamada T, Sasaki H, Furuya H, Miyata T, Goto I, Sakaki Y (1987) Complementary DNA for the mouse homolog of the human amyloid β protein precursor. Biochem Biophys Res Commun 149:665-671.
50. Zhang J, Kang DE, Xia W, Okochi M, Mori H, Selkoe DJ, Koo EH (1998) Subcellular distribution and turnover of presenilins in transfected cells. J Biol Chem 273:12436-12442.