The organellar peptidasome, PreP: A journey from Arabidopsis to Alzheimer's disease

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1797, Issue 6-7, 2010, Pages 1076-1080

  Glaser, Elzbieta ^a   Alikhani, Nyosha ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

Alzheimer's disease; Amyloid peptide; Mitochondria; Peptide degradation; Presequence protease; Targeting peptide

Indexed keywords

AMYLOID BETA PROTEIN; PRESEQUENCE PROTEASE; PROTEINASE; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ARABIDOPSIS; BRAIN MITOCHONDRION; CATALYSIS; CHLOROPLAST; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME LOCALIZATION; ENZYME MECHANISM; ENZYME SPECIFICITY; ENZYME STRUCTURE; GENE DELETION; HUMAN; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REVIEW;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BRAIN; HUMANS; MICE; MICE, TRANSGENIC; MITOCHONDRIA; MODELS, BIOLOGICAL; MODELS, MOLECULAR; ORGANELLES; PEPTIDE HYDROLASES; SACCHAROMYCES CEREVISIAE; SUBSTRATE SPECIFICITY;

ARABIDOPSIS; ARABIDOPSIS THALIANA; MUS MUSCULUS;

EID: 77953772172     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2009.12.016     Document Type: Review

References (47)

1. Chan C.B., Harper M.E. Uncoupling proteins: role in insulin resistance and insulin insufficiency. Curr. Diabetes Rev. 2006, 2:271-283.
2. Kwong J.Q., Beal M.F., Manfredi G. The role of mitochondria in inherited neurodegenerative diseases. J. Neurochem. 2006, 97:1659-1675.
3. Lin M.T., Beal M.F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 2006, 443:787-795.
4. Andreyev A.Y., Kushnareva Y.E., Starkov A.A. Mitochondrial metabolism of reactive oxygen species. Biochemistry (Mosc) 2005, 70:200-214.
5. Kaser M., Langer T. Protein degradation in mitochondria. Semin. Cell Dev. Biol. 2000, 11:181-190.
6. Baker T.A., Sauer R.T. ATP-dependent proteases of bacteria: recognition logic and operating principles. Trends Biochem. Sci. 2006, 31:647-653.
7. Moberg P., Stahl A., Bhushan S., Wright S.J., Eriksson A., Bruce B.D., Glaser E. Characterization of a novel zinc metalloprotease involved in degrading targeting peptides in mitochondria and chloroplasts. Plant J. 2003, 36:616-628.
8. Stahl A., Moberg P., Ytterberg J., Panfilov O., Brockenhuus Von Lowenhielm H., Nilsson F., Glaser E. Isolation and identification of a novel mitochondrial metalloprotease (PreP) that degrades targeting presequences in plants. J. Biol. Chem. 2002, 277:41931-41939.
9. Stahl A., Pavlov P.F., Szigyarto C., Glaser E. Rapid degradation of the presequence of the f1beta precursor of the ATP synthase inside mitochondria. Biochem. J. 2000, 349(Pt 3):703-707.
10. McDermott J.R., Gibson A.M. Degradation of Alzheimer's beta-amyloid protein by human and rat brain peptidases: involvement of insulin-degrading enzyme. Neurochem. Res. 1997, 22:49-56.
11. Morelli L., Llovera R.E., Mathov I., Lue L.F., Frangione B., Ghiso J., Castano E.M. Insulin-degrading enzyme in brain microvessels: proteolysis of amyloid beta vasculotropic variants and reduced activity in cerebral amyloid angiopathy. J. Biol. Chem. 2004, 279:56004-56013.
12. Gouras G.K., Almeida C.G., Takahashi R.H. Intraneuronal Abeta accumulation and origin of plaques in Alzheimer's disease. Neurobiol. Aging 2005, 26:1235-1244.
13. Wirths O., Multhaup G., Bayer T.A. A modified beta-amyloid hypothesis: intraneuronal accumulation of the beta-amyloid peptide-the first step of a fatal cascade. J. Neurochem. 2004, 91:513-520.
14. Manczak M., Anekonda T.S., Henson E., Park B.S., Quinn J., Reddy P.H. Mitochondria are a direct site of A beta accumulation in Alzheimer's disease neurons: implications for free radical generation and oxidative damage in disease progression. Hum. Mol. Genet. 2006, 15:1437-1449.
15. Falkevall A., Alikhani N., Bhushan S., Pavlov P.F., Busch K., Johnson K.A., Eneqvist T., Tjernberg L., Ankarcrona M., Glaser E. Degradation of the amyloid beta-protein by the novel mitochondrial peptidasome, PreP. J. Biol. Chem. 2006, 281:29096-29104.
16. Gabaldon T., Huynen M.A. Shaping the mitochondrial proteome. Biochim. Biophys. Acta 2004, 1659:212-220.
17. Glaser E., Dessi P. Integration of the mitochondrial-processing peptidase into the cytochrome bc1 complex in plants. J. Bioenerg. Biomembr. 1999, 31:259-274.
18. Roise D., Horvath S.J., Tomich J.M., Richards J.H., Schatz G. A chemically synthesized pre-sequence of an imported mitochondrial protein can form an amphiphilic helix and perturb natural and artificial phospholipid bilayers. EMBO J. 1986, 5:1327-1334.
19. Backman H.G., Pessoa J., Eneqvist T., Glaser E. Binding of divalent cations is essential for the activity of the organellar peptidasome in Arabidopsis thaliana, AtPreP. FEBS Lett. 2009, 583:2727-2733.
20. Stahl A., Nilsson S., Lundberg P., Bhushan S., Biverstahl H., Moberg P., Morisset M., Vener A., Maler L., Langel U., Glaser E. Two novel targeting peptide degrading proteases, PrePs, in mitochondria and chloroplasts, so similar and still different. J. Mol. Biol. 2005, 349:847-860.
21. Bhushan S., Lefebvre B., Stahl A., Wright S.J., Bruce B.D., Boutry M., Glaser E. Dual targeting and function of a protease in mitochondria and chloroplasts. EMBO Rep. 2003, 4:1073-1078.
22. Bhushan S., Stahl A., Nilsson S., Lefebvre B., Seki M., Roth C., McWilliam D., Wright S.J., Liberles D.A., Shinozaki K., Bruce B.D., Boutry M., Glaser E. Catalysis, subcellular localization, expression and evolution of the targeting peptides degrading protease, AtPreP2. Plant Cell Physiol. 2005, 46:985-996.
23. Nilsson Cederholm S., Backman H.G., Pesaresi P., Leister D., Glaser E. Deletion of an organellar peptidasome PreP affects early development in Arabidopsis thaliana. Plant Mol. Biol. 2009, 71:497-508.
24. Johnson K.A., Bhushan S., Stahl A., Hallberg B.M., Frohn A., Glaser E., Eneqvist T. The closed structure of presequence protease PreP forms a unique 10,000Angstroms3 chamber for proteolysis. EMBO J. 2006, 25:1977-1986.
25. Isaya G., Kalousek F., Fenton W.A., Rosenberg L.E. Cleavage of precursors by the mitochondrial processing peptidase requires a compatible mature protein or an intermediate octapeptide. J. Cell Biol. 1991, 113:65-76.
26. Kambacheld M., Augustin S., Tatsuta T., Muller S., Langer T. Role of the novel metallopeptidase Mop112 and saccharolysin for the complete degradation of proteins residing in different subcompartments of mitochondria. J. Biol. Chem. 2005, 280:20132-20139.
27. Vogtle F.N., Wortelkamp S., Zahedi R.P., Becker D., Leidhold C., Gevaert K., Kellermann J., Voos W., Sickmann A., Pfanner N., Meisinger C. Global analysis of the mitochondrial N-proteome identifies a processing peptidase critical for protein stability. Cell 2009, 139:428-439.
28. Selkoe D.J. Translating cell biology into therapeutic advances in Alzheimer's disease. Nature 1999, 399:A23-A31.
29. Kimberly W.T., LaVoie M.J., Ostaszewski B.L., Ye W., Wolfe M.S., Selkoe D.J. Gamma-secretase is a membrane protein complex comprised of presenilin, nicastrin, Aph-1, and Pen-2. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:6382-6387.
30. Vassar R., Bennett B.D., Babu-Khan S., Kahn S., Mendiaz E.A., Denis P., Teplow D.B., Ross S., Amarante P., Loeloff R., Luo Y., Fisher S., Fuller J., Edenson S., Lile J., Jarosinski M.A., Biere A.L., Curran E., Burgess T., Louis J.C., Collins F., Treanor J., Rogers G., Citron M. Beta-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science 1999, 286:735-741.
31. Glenner G.G., Wong C.W. Alzheimer's disease and Down's syndrome: sharing of a unique cerebrovascular amyloid fibril protein. Biochem. Biophys. Res. Commun. 1984, 122:1131-1135.
32. Masters C.L., Simms G., Weinman N.A., Multhaup G., McDonald B.L., Beyreuther K. Amyloid plaque core protein in Alzheimer disease and Down syndrome. Proc. Natl. Acad. Sci. U. S. A. 1985, 82:4245-4249.
33. Soderberg L., Bogdanovic N., Axelsson B., Winblad B., Naslund J., Tjernberg L.O. Analysis of single Alzheimer solid plaque cores by laser capture microscopy and nanoelectrospray/tandem mass spectrometry. Biochemistry 2006, 45:9849-9856.
34. Caspersen C., Wang N., Yao J., Sosunov A., Chen X., Lustbader J.W., Xu H.W., Stern D., McKhann G., Yan S.D. Mitochondrial Abeta: a potential focal point for neuronal metabolic dysfunction in Alzheimer's disease. FASEB J. 2005, 19:2040-2041.
35. Lustbader J.W., Cirilli M., Lin C., Xu H.W., Takuma K., Wang N., Caspersen C., Chen X., Pollak S., Chaney M., Trinchese F., Liu S., Gunn-Moore F., Lue L.F., Walker D.G., Kuppusamy P., Zewier Z.L., Arancio O., Stern D., Yan S.S., Wu H. ABAD directly links Abeta to mitochondrial toxicity in Alzheimer's disease. Science 2004, 304:448-452.
36. Cardoso S.M., Proenca M.T., Santos S., Santana I., Oliveira C.R. Cytochrome c oxidase is decreased in Alzheimer's disease platelets. Neurobiol. Aging 2004, 25:105-110.
37. Kish S.J., Mastrogiacomo F., Guttman M., Furukawa Y., Taanman J.W., Dozic S., Pandolfo M., Lamarche J., DiStefano L., Chang L.J. Decreased brain protein levels of cytochrome oxidase subunits in Alzheimer's disease and in hereditary spinocerebellar ataxia disorders: a nonspecific change?. J. Neurochem. 1999, 72:700-707.
38. Du H., Guo L., Fang F., Chen D., Sosunov A.A., McKhann G.M., Yan Y., Wang C., Zhang H., Molkentin J.D., Gunn-Moore F.J., Vonsattel J.P., Arancio O., Chen J.X., Yan S.D. Cyclophilin D deficiency attenuates mitochondrial and neuronal perturbation and ameliorates learning and memory in Alzheimer's disease. Nat. Med. 2008, 14:1097-1105.
39. H. Du, L. Guo, W. Zhang, M. Rydzewska, S. Yan, Cyclophilin D deficiency improves mitochondrial function and learning/memory in aging Alzheimer disease mouse model, Neurobiol. Aging (in press).
40. Anandatheerthavarada H.K., Biswas G., Robin M.A., Avadhani N.G. Mitochondrial targeting and a novel transmembrane arrest of Alzheimer's amyloid precursor protein impairs mitochondrial function in neuronal cells. J. Cell Biol. 2003, 161:41-54.
41. Anandatheerthavarada H.K., Devi L. Amyloid precursor protein and mitochondrial dysfunction in Alzheimer's disease. Neuroscientist 2007, 13:626-638.
42. Devi L., Prabhu B.M., Galati D.F., Avadhani N.G., Anandatheerthavarada H.K. Accumulation of amyloid precursor protein in the mitochondrial import channels of human Alzheimer's disease brain is associated with mitochondrial dysfunction. J. Neurosci. 2006, 26:9057-9068.
43. Hansson Petersen C.A., Alikhani N., Behbahani H., Wiehager B., Pavlov P.F., Alafuzoff I., Leinonen V., Ito A., Winblad B., Glaser E., Ankarcrona M. The amyloid beta-peptide is imported into mitochondria via the TOM import machinery and localized to mitochondrial cristae. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:13145-13150.
44. Mzhavia N., Berman Y.L., Qian Y., Yan L., Devi L.A. Cloning, expression, and characterization of human metalloprotease 1: a novel member of the pitrilysin family of metalloendoproteases. DNA Cell Biol. 1999, 18:369-380.
45. Taylor S.W., Fahy E., Zhang B., Glenn G.M., Warnock D.E., Wiley S., Murphy A.N., Gaucher S.P., Capaldi R.A., Gibson B.W., Ghosh S.S. Characterization of the human heart mitochondrial proteome. Nat. Biotechnol. 2003, 21:281-286.
46. Shen Y., Joachimiak A., Rosner M.R., Tang W.J. Structures of human insulin-degrading enzyme reveal a new substrate recognition mechanism. Nature 2006, 443:870-874.
47. Taylor A.B., Smith B.S., Kitada S., Kojima K., Miyaura H., Otwinowski Z., Ito A., Deisenhofer J. Crystal structures of mitochondrial processing peptidase reveal the mode for specific cleavage of import signal sequences. Structure 2001, 9:615-625.