Influence of ADAM10 on prion protein processing and scrapie infectiosity in vivo

Neurobiology of Disease

Volumn 36, Issue 2, 2009, Pages 233-241

  Endres, Kristina ^a   Mitteregger, Gerda ^b   Kojro, Elzbieta ^a   Kretzschmar, Hans ^b   Fahrenholz, Falk ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

alpha Secretase; Gliosis; Neurotoxicity; Prion disease; Shedding

Indexed keywords

ALPHA SECRETASE; PRION PROTEIN; PROTEIN ADAM10; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; IN VIVO STUDY; INCUBATION TIME; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN PROCESSING; SCRAPIE; VIRUS VIRULENCE;

ADAM PROTEINS; AMINO ACID SEQUENCE; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; BRAIN; CATTLE; HUMANS; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; PRIONS; PROTEIN PROCESSING, POST-TRANSLATIONAL; SCRAPIE;

EID: 70349783752     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2009.07.015     Document Type: Article

References (58)

1. Aguzzi A., Baumann F., and Bremer J. The prion's elusive reason for being. Annu. Rev. Neurosci. 31 (2008) 439-477
2. Alfa C.M., Sunyach C., Slack B.E., Fisher A., Vincent B., and Checler F. M1 and M3 muscarinic receptors control physiological processing of cellular prion by modulating ADAM17 phosphorylation and activity. J. Neurosci. 27 (2007) 4083-4092
3. Armstrong R.A., Lantos P.L., and Cairns N.J. The spatial patterns of prion protein deposits in Creutzfeldt-Jakob disease: comparison with beta-amyloid deposits in Alzheimer's disease. Neurosci. Lett. 298 (2001) 53-56
4. Baek S.H., Ohgi K.A., Rose D.W., Koo E.H., Glass C.K., and Rosenfeld M.G. Exchange of N-CoR corepressor and Tip60 coactivator complexes links gene expression by NF-kappaB and beta-amyloid precursor protein. Cell 110 (2002) 55-67
5. Belyaev N.D., Nalivaeva N.N., Makova N.Z., and Turner A.J. Neprilysin gene expression requires binding of the amyloid precursor protein intracellular domain to its promoter: implications for Alzheimer disease. EMBO Rep. 10 (2009) 94-100
6. Bertram L., and Tanzi R.E. Thirty years of Alzheimer's disease genetics: the implications of systematic meta-analyses. Nat. Rev. Neurosci. 9 (2008) 768-778
7. Borchelt D.R., Rogers M., Stahl N., Telling G., and Prusiner S.B. Release of the cellular prion protein from cultured cells after loss of its glycoinositol phospholipid anchor. Glycobiology 3 (1993) 319-329
8. Bueler H., Aguzzi A., Sailer A., Greiner R.A., Autenried P., Aguet M., and Weissmann C. Mice devoid of PrP are resistant to scrapie. Cell 73 (1993) 1339-1347
9. Cabral A.L., Lee K.S., and Martins V.R. Regulation of the cellular prion protein gene expression depends on chromatin conformation. J. Biol. Chem. 277 (2002) 5675-5682
10. Cao X., and Sudhof T.C. Dissection of amyloid-beta precursor protein-dependent transcriptional transactivation. J. Biol. Chem. 279 (2004) 24601-24611
11. Checler F., and Vincent B. Alzheimer's and prion diseases: distinct pathologies, common proteolytic denominators. Trends Neurosci. 25 (2002) 616-620
12. Chen A.C., and Selkoe D.J. 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 (2007) 541-554 Neuron 53, 479-483
13. Chen S.G., Teplow D.B., Parchi P., Teller J.K., Gambetti P., and Utilio-Gambetti L. Truncated forms of the human prion protein in normal brain and in prion diseases. J. Biol. Chem. 270 (1995) 19173-19180
14. Chesebro B., Trifilo M., Race R., Meade-White K., Teng C., LaCasse R., Raymond L., Favara C., Baron G., Priola S., Caughey B., Masliah E., and Oldstone M. Anchorless prion protein results in infectious amyloid disease without clinical scrapie. Science 308 (2005) 1435-1439
15. Cisse M.A., Sunyach C., Lefranc-Jullien S., Postina R., Vincent B., and Checler F. The disintegrin ADAM9 indirectly contributes to the physiological processing of cellular prion by modulating ADAM10 activity. J. Biol. Chem. 280 (2005) 40624-40631
16. Clement A.B., Hanstein R., Schroder A., Nagel H., Endres K., Fahrenholz F., and Behl C. Effects of neuron-specific ADAM10 modulation in an in vivo model of acute excitotoxic stress. Neuroscience 152 (2008) 459-468
17. Eggert S., Paliga K., Soba P., Evin G., Masters C.L., Weidemann A., and Beyreuther K. The proteolytic processing of the amyloid precursor protein gene family members APLP-1 and APLP-2 involves alpha-, beta-, gamma-, and epsilon-like cleavages: modulation of APLP-1 processing by n-glycosylation. J. Biol. Chem. 279 (2004) 18146-18156
18. Endres K., Postina R., Schroeder A., Mueller U., and Fahrenholz F. Shedding of the amyloid precursor protein-like protein APLP2 by disintegrin-metalloproteinases. FEBS J. 272 (2005) 5808-5820
19. Freese C., Garratt A.N., Fahrenholz F., and Endres K. The effects of alpha-secretase ADAM10 on the proteolysis of neuregulin-1. FEBS J. 276 (2009) 1568-1580
20. Gavin R., Urena J., Rangel A., Pastrana M.A., Requena J.R., Soriano E., Aguzzi A., and Del Rio J.A. Fibrillar prion peptide PrP(106-126) treatment induces Dab1 phosphorylation and impairs APP processing and Abeta production in cortical neurons. Neurobiol. Dis. 30 (2008) 243-254
21. Gralle M., Botelho M.G., and Wouters F.S. Neuroprotective secreted amyloid precursor protein acts by disrupting amyloid precursor protein dimers. J. Biol. Chem. (2009)
22. 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 (2001) 35235-35238
23. Harris D.A., Huber M.T., van D.P., Shyng S.L., Chait B.T., and Wang R. Processing of a cellular prion protein: identification of N- and C-terminal cleavage sites. Biochemistry 32 (1993) 1009-1016
24. Hooper N.M. Roles of proteolysis and lipid rafts in the processing of the amyloid precursor protein and prion protein. Biochem. Soc. Trans. 33 (2005) 335-338
25. Jimenez-Huete A., Lievens P.M., Vidal R., Piccardo P., Ghetti B., Tagliavini F., Frangione B., and Prelli F. Endogenous proteolytic cleavage of normal and disease-associated isoforms of the human prion protein in neural and non-neural tissues. Am. J. Pathol. 153 (1998) 1561-1572
26. Kempster S., Bate C., and Williams A. Simvastatin treatment prolongs the survival of scrapie-infected mice. Neuroreport 18 (2007) 479-482
27. Laffont-Proust I., Faucheux B.A., Hassig R., Sazdovitch V., Simon S., Grassi J., Hauw J.J., Moya K.L., and Haik S. The N-terminal cleavage of cellular prion protein in the human brain. FEBS Lett. 579 (2005) 6333-6337
28. Laffont-Proust I., Hassig R., Haik S., Simon S., Grassi J., Fonta C., Faucheux B.A., and Moya K.L. Truncated PrP(c) in mammalian brain: interspecies variation and location in membrane rafts. Biol. Chem. 387 (2006) 297-300
29. Lammich S., Kojro E., Postina R., Gilbert S., Pfeiffer R., Jasionowski M., Haass C., and Fahrenholz F. Constitutive and regulated alpha-secretase cleavage of Alzheimer's amyloid precursor protein by a disintegrin metalloprotease. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 3922-3927
30. Lauren J., Gimbel D.A., Nygaard H.B., Gilbert J.W., and Strittmatter S.M. Cellular prion protein mediates impairment of synaptic plasticity by amyloid-beta oligomers. Nature 457 (2009) 1128-1132
31. Lichtenthaler S.F., and Haass C. Amyloid at the cutting edge: activation of alpha-secretase prevents amyloidogenesis in an Alzheimer disease mouse model. J. Clin. Invest. 113 (2004) 1384-1387
32. McMahon H.E., Mange A., Nishida N., Creminon C., Casanova D., and Lehmann S. Cleavage of the amino terminus of the prion protein by reactive oxygen species. J. Biol. Chem. 276 (2001) 2286-2291
33. Mead S., Poulter M., Uphill J., Beck J., Whitfield J., Webb T.E., Campbell T., Adamson G., Deriziotis P., Tabrizi S.J., Hummerich H., Verzilli C., Alpers M.P., Whittaker J.C., and Collinge J. Genetic risk factors for variant Creutzfeldt-Jakob disease: a genome-wide association study. Lancet Neurol. 8 (2009) 57-66
34. Mok S.W., Thelen K.M., Riemer C., Bamme T., Gultner S., Lutjohann D., and Baier M. Simvastatin prolongs survival times in prion infections of the central nervous system. Biochem. Biophys. Res. Commun. 348 (2006) 697-702
35. Mok S.W., Riemer C., Madela K., Hsu D.K., Liu F.T., Gultner S., Heise I., and Baier M. Role of galectin-3 in prion infections of the CNS. Biochem. Biophys. Res. Commun. 359 (2007) 672-678
36. Pardossi-Piquard R., Petit A., Kawarai T., Sunyach C., ves da C.C., Vincent B., Ring S., D'Adamio L., Shen J., Muller U., St George H.P., and Checler F. Presenilin-dependent transcriptional control of the Abeta-degrading enzyme neprilysin by intracellular domains of betaAPP and APLP. Neuron 46 (2005) 541-554
37. Parizek P., Roeckl C., Weber J., Flechsig E., Aguzzi A., and Raeber A.J. Similar turnover and shedding of the cellular prion protein in primary lymphoid and neuronal cells. J. Biol. Chem. 276 (2001) 44627-44632
38. Parkin E., and Harris B. A disintegrin and metalloproteinase (ADAM)-mediated ectodomain shedding of ADAM10. J. Neurochem. 108 (2009) 1464-1479
39. Parkin E.T., Watt N.T., Turner A.J., and Hooper N.M. Dual mechanisms for shedding of the cellular prion protein. J. Biol. Chem. 279 (2004) 11170-11178
40. Parkin E.T., Watt N.T., Hussain I., Eckman E.A., Eckman C.B., Manson J.C., Baybutt H.N., Turner A.J., and Hooper N.M. Cellular prion protein regulates beta-secretase cleavage of the Alzheimer's amyloid precursor protein. Proc. Natl. Acad. Sci. U. S. A 104 (2007) 11062-11067
41. Pfeifer A., Eigenbrod S., Al-Khadra S., Hofmann A., Mitteregger G., Moser M., Bertsch U., and Kretzschmar H. Lentivector-mediated RNAi efficiently suppresses prion protein and prolongs survival of scrapie-infected mice. J. Clin. Invest 116 (2006) 3204-3210
42. Plamont M.A., Chasseigneaux S., Asnerie-Laupretre N., Beaudry P., Peoc'h K., and Laplanche J.L. Variation at the ADAM10 gene locus is not associated with Creutzfeldt-Jakob disease. Neurosci. Lett. 344 (2003) 132-134
43. Postina R., Schroeder A., Dewachter I., Bohl J., Schmitt U., Kojro E., Prinzen C., Endres K., Hiemke C., Blessing M., Flamez P., Dequenne A., Godaux E., van L.F., and Fahrenholz F. A disintegrin-metalloproteinase prevents amyloid plaque formation and hippocampal defects in an Alzheimer disease mouse model. J. Clin. Invest. 113 (2004) 1456-1464
44. Price D.L., Borchelt D.R., and Sisodia S.S. Alzheimer disease and the prion disorders amyloid beta-protein and prion protein amyloidoses. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 6381-6384
45. Ring S., Weyer S.W., Kilian S.B., Waldron E., Pietrzik C.U., Filippov M.A., Herms J., Buchholz C., Eckman C.B., Korte M., Wolfer D.P., and Muller U.C. 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 (2007) 7817-7826
46. Scheinfeld M.H., Ghersi E., Laky K., Fowlkes B.J., and D'Adamio L. Processing of beta-amyloid precursor-like protein-1 and -2 by gamma-secretase regulates transcription. J. Biol. Chem. 277 (2002) 44195-44201
47. Schwarze-Eicker K., Keyvani K., Gortz N., Westaway D., Sachser N., and Paulus W. Prion protein (PrPc) promotes beta-amyloid plaque formation. Neurobiol. Aging 26 (2005) 1177-1182
48. Sethi S., Lipford G., Wagner H., and Kretzschmar H. Postexposure prophylaxis against prion disease with a stimulator of innate immunity. Lancet 360 (2002) 229-230
49. Tamguney G., Giles K., Glidden D.V., Lessard P., Wille H., Tremblay P., Groth D.F., Yehiely F., Korth C., Moore R.C., Tatzelt J., Rubinstein E., Boucheix C., Yang X., Stanley P., Lisanti M.P., Dwek R.A., Rudd P.M., Moskovitz J., Epstein C.J., Cruz T.D., Kuziel W.A., Maeda N., Sap J., Ashe K.H., Carlson G.A., Tesseur I., Wyss-Coray T., Mucke L., Weisgraber K.H., Mahley R.W., Cohen F.E., and Prusiner S.B. Genes contributing to prion pathogenesis. J. Gen. Virol. 89 (2008) 1777-1788
50. Tousseyn T.A., Thathiah A., Jorissen E., Raemaekers T., Konietzko U., Reiss K., Maes E., Snellinx A., Serneels L., Nyabi O., Annaert W., Saftig P., Hartmann D., and De S.B. ADAM10, the rate-limiting protease of regulated intramembrane proteolysis of notch and other proteins, is processed itself by ADAMS 9, -15, and gamma-secretase. J. Biol. Chem. (2009)
51. Trifilo M.J., Sanchez-Alavez M., Solforosi L., Bernard-Trifilo J., Kunz S., McGavern D., and Oldstone M.B. Scrapie-induced defects in learning and memory of transgenic mice expressing anchorless prion protein are associated with alterations in the gamma aminobutyric acid-ergic pathway. J. Virol. 82 (2008) 9890-9899
52. Vazquez M.C., Vargas L.M., Inestrosa N.C., and Alvarez A.R. c-Abl modulates AICD dependent cellular responses: transcriptional induction and apoptosis. J. Cell Physiol. (2009)
53. Vella L.J., Sharples R.A., Nisbet R.M., Cappai R., and Hill A.F. The role of exosomes in the processing of proteins associated with neurodegenerative diseases. Eur. Biophys. J. 37 (2008) 323-332
54. Vincent B., Paitel E., Saftig P., Frobert Y., Hartmann D., De S.B., Grassi J., Lopez-Perez E., and Checler F. The disintegrins ADAM10 and TACE contribute to the constitutive and phorbol ester-regulated normal cleavage of the cellular prion protein. J. Biol. Chem. 276 (2001) 37743-37746
55. Waldron E., Isbert S., Kern A., Jaeger S., Martin A.M., Hebert S.S., Behl C., Weggen S., De S.B., and Pietrzik C.U. Increased AICD generation does not result in increased nuclear translocation or activation of target gene transcription. Exp. Cell Res. 314 (2008) 2419-2433
56. Walsh D.M., Fadeeva J.V., LaVoie M.J., Paliga K., Eggert S., Kimberly W.T., Wasco W., and Selkoe D.J. gamma-Secretase cleavage and binding to FE65 regulate the nuclear translocation of the intracellular C-terminal domain (ICD) of the APP family of proteins. Biochemistry 42 (2003) 6664-6673
57. Yadavalli R., Guttmann R.P., Seward T., Centers A.P., Williamson R.A., and Telling G.C. Calpain-dependent endoproteolytic cleavage of PrPSc modulates scrapie prion propagation. J. Biol. Chem. 279 (2004) 21948-21956
58. Ye X., Meeker H.C., Kozlowski P., and Carp R.I. The occurrence of vacuolation, and periodic acid-Schiff (PAS)-positive granules and plaques in the brains of C57BL/6J, AKR, senescence-prone (SAMP8) and senescence-resistant (SAMR1) mice infected with various scrapie strains. Brain Res. 995 (2004) 158-166