Cytosolic proteins lose solubility as amyloid deposits in a transgenic mouse model of alzheimer-type amyloidosis

Human Molecular Genetics

Volumn 22, Issue 14, 2013, Pages 2765-2774

  Xu, Guilian ^a,b   Stevens, Stanley M ^b,c   Moore, Brenda D ^a   McClung, Scott ^b   Borchelt, David R ^a,b  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID; CHAPERONE; CYTOSOL RECEPTOR; GLYCOLYTIC ENZYME; POLYUBIQUITIN;

ALZHEIMER DISEASE; AMYLOIDOSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEOMICS; SEDIMENTATION;

EID: 84880252026     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt121     Document Type: Article

References (50)

1. Braak, H. and Braak, E. (1991) Neuropathological staging of Alzheimer-related changes. Acta Neuropathol., 82, 239-259.
2. Hardy, J., and Selkoe, D.J. (2002) The amyloid hypothesis of Alzheimer's disease: progress, and problems on the road to therapeutics. Science, 297, 353-356.
3. Games, D., Adams, D., Alessandrini, R., Barbour, R., Berthelette, P., Blackwell, C., Carr, T., Clemens, J., Donaldson, T., Gillespie, F. et al. (1995) Alzheimer-type neuropathology in transgenic mice overexpressing V717F b-amyloid precursor protein. Nature, 373, 523-527.
4. Borchelt, D.R., Ratovitski, T., Van Lare, J., Lee, M.K., Gonzales, V.B., Jenkins, N.A., Copeland, N.G., Price, D.L., and Sisodia, S.S. (1997) Accelerated amyloid deposition in the brains of transgenic mice co-expressing mutant presenilin 1, and amyloid precursor proteins. Neuron, 19, 939-945.
5. Jankowsky, J.L., Slunt, H.H., Ratovitski, T., Jenkins, N.A., Copeland, N.G., and Borchelt, D.R. (2001) Co-expression of multiple transgenes in mouse CNS: a comparison of strategies. Biomol. Eng., 17, 157-165.
6. Jankowsky, J.L., Fadale, D.J., Anderson, J., Xu, G.M., Gonzales, V., Jenkins, N.A., Copeland, N.G., Lee, M.K., Younkin, L.H., Wagner, S.L. et al. (2004) Mutant presenilins specifically elevate the levels of the 42 residue beta-amyloid peptide in vivo: evidence for augmentation of a 42-specific gamma secretase. Hum. Mol. Genet., 13, 159-170.
7. Hardy, J.A., and Higgins, G.A. (1992) Alzheimer's disease: the amyloid cascade hypothesis. Science, 256, 184-185.
8. Marsh, S.E., and Blurton-Jones, M. (2012) Examining the mechanisms that link beta-amyloid, and alpha-synuclein pathologies. Alzheimers Res. Ther., 4, 11.
9. Amador-Ortiz, C., Lin, W.L., Ahmed, Z., Personett, D., Davies, P., Duara, R., Graff-Radford, N.R., Hutton, M.L., and Dickson, D.W. (2007) TDP-43 immunoreactivity in hippocampal sclerosis, and Alzheimer's disease. Ann. Neurol., 61, 435-445.
10. Balch, W.E., Morimoto, R.I., Dillin, A., and Kelly, J.W. (2008) Adapting proteostasis for disease intervention. Science, 319, 916-919.
11. Skovronsky, D.M., Lee, V.M., and Trojanowski, J.Q. (2006) Neurodegenerative diseases: new concepts of pathogenesis, and their therapeutic implications. Annu. Rev. Pathol., 1, 151-170.
12. Gidalevitz, T., Ben Zvi, A., Ho, K.H., Brignull, H.R., and Morimoto, R.I. (2006) Progressive disruption of cellular protein folding in models of polyglutamine diseases. Science, 311, 1471-1474.
13. Gidalevitz, T., Krupinski, T., Garcia, S., and Morimoto, R.I. (2009) Destabilizing protein polymorphisms in the genetic background direct phenotypic expression of mutant SOD1 toxicity. PLoS Genet., 5, e1000399.
14. Morimoto, R.I. (2006) Stress, aging,, and neurodegenerative disease. N. Engl. J. Med., 355, 2254-2255.
15. Xu, G., Stevens, S.M. Jr, Kobiessy, F., Brown, H., McClung, S., Gold, M.S., and Borchelt, D.R. (2012) Identification of proteins sensitive to thermal stress in human neuroblastoma, and glioma cell lines. PLoS ONE, 7, e49021.
16. McKinley, M.P., Meyer, R.K., Kenaga, L., Rahbar, F., Cotter, R., Serban, A., and Prusiner, S.B. (1991) Scrapie prion rod formation in vitro requires both detergent extraction, and limited proteolysis. J. Virol., 65, 1340-1351.
17. Pike, C.J., Walencewicz, A.J., Glabe, C.G., and Cotman, C.W. (1991) In vitro aging of b-amyloid protein causes peptide aggregation, and neurotoxicity. Brain Res., 563, 311-314.
18. Johnston, J.A., Ward, C.L., and Kopito, R.R. (1998) Aggresomes: a cellular response to misfolded proteins. J. Cell Biol., 143, 1883-1898.
19. Giasson, B.I., Uryu, K., Trojanowski, J.Q., and Lee, V.M. (1999) Mutant, and wild type human alpha-synucleins assemble into elongated filaments with distinct morphologies in vitro. J. Biol. Chem., 274, 7619-7622.
20. Ishihara, T., Hong, M., Zhang, B., Nakagawa, Y., Lee, M.K., Trojanowski, J.Q., and Lee, V.M. (1999) Age-dependent emergence, and progression of a tauopathy in transgenic mice overexpressing the shortest human tau isoform. Neuron, 24, 751-762.
21. Scherzinger, E., Sittler, A., Schweiger, K., Heiser, V., Lurz, R., Hasenbank, R., Lehrach, H., and Wanker, E.E. (1999) Self-assembly of polyglutamine-containing huntingtin fragments into amyloid-like fibrils: implications for Huntington's disease pathology. Proc. Natl Acad. Sci. USA, 96, 4604-4609.
22. Wang, J., Slunt, H., Gonzales, V., Fromholt, D., Coonfield, M., Copeland, N.G., Jenkins, N.A., and Borchelt, D.R. (2003) Copper-binding-site-null SOD1 causes ALS in transgenic mice: aggregates of non-native SOD1 delineate a common feature. Hum. Mol. Genet., 12, 2753-2764.
23. Karch, C.M., and Borchelt, D.R. (2008) A limited role for disulfide cross-linking in the aggregation of mutant SOD1 linked to familial amyotrophic lateral sclerosis. J. Biol. Chem., 283, 13528-13537.
24. Munch, C., and Bertolotti, A. (2010) Exposure of hydrophobic surfaces initiates aggregation of diverse ALS-causing superoxide dismutase-1 mutants. J. Mol. Biol., 399, 512-525.
25. Bolognesi, B., Kumita, J.R., Barros, T.P., Esbjorner, E.K., Luheshi, L.M., Crowther, D.C., Wilson, M.R., Dobson, C.M., Favrin, G., and Yerbury, J.J. (2010) ANS binding reveals common features of cytotoxic amyloid species. ACS Chem. Biol., 5, 735-740.
26. Lesuisse, C., Xu, G., Anderson, J., Wong, M., Jankowsky, J., Holtz, G., Gonzalez, V., Wong, P.C.Y., Price, D.L., Tang, F. et al. (2001) Hyper-expression of human apolipoprotein E4 in astroglia, and neurons does not enhance amyloid deposition in transgenic mice. Hum. Mol. Gen., 10, 2525-2537.
27. Calero, M., Rostagno, A., Matsubara, E., Zlokovic, B., Frangione, B., and Ghiso, J. (2000) Apolipoprotein J (clusterin), and Alzheimer's disease. Microsc. Res. Tech., 50, 305-315.
28. Martin-Rehrmann, M.D., Hoe, H.S., Capuani, E.M., and Rebeck, G.W. (2005) Association of apolipoprotein J-positive beta-amyloid plaques with dystrophic neurites in Alzheimer's disease brain. Neurotox. Res., 7, 231-242.
29. Peng, J., Schwartz, D., Elias, J.E., Thoreen, C.C., Cheng, D., Marsischky, G., Roelofs, J., Finley, D., and Gygi, S.P. (2003) A proteomics approach to understanding protein ubiquitination. Nat. Biotechnol., 21, 921-926.
30. Bennett, E.J., Shaler, T.A., Woodman, B., Ryu, K.Y., Zaitseva, T.S., Becker, C.H., Bates, G.P., Schulman, H., and Kopito, R.R. (2007) Global changes to the ubiquitin system in Huntington's disease. Nature, 448, 704-708.
31. Woltjer, R.L., Cimino, P.J., Boutte, A.M., Schantz, A.M., Montine, K.S., Larson, E.B., Bird, T., Quinn, J.F., Zhang, J., and Montine, T.J. (2005) Proteomic determination of widespread detergent-insolubility including Abeta but not tau early in the pathogenesis of Alzheimer's disease. FASEB J., 19, 1923-1925.
32. Gozal, Y.M., Duong, D.M., Gearing, M., Cheng, D., Hanfelt, J.J., Funderburk, C., Peng, J., Lah, J.J., and Levey, A.I. (2009) Proteomics analysis reveals novel components in the detergent-insoluble subproteome in Alzheimer's disease. J. Proteome. Res., 8, 5069-5079.
33. Bence, N.F., Sampat, R.M., and Kopito, R.R. (2001) Impairment of the ubiquitin-proteasome system by protein aggregation. Science, 292, 1552-1555.
34. Dammer, E.B., Na, C.H., Xu, P., Seyfried, N.T., Duong, D.M., Cheng, D., Gearing, M., Rees, H., Lah, J.J., Levey, A.I. et al. (2011) Polyubiquitin linkage profiles in three models of proteolytic stress suggest the etiology of Alzheimer disease. J. Biol. Chem., 286, 10457-10465.
35. Liao, L., Cheng, D., Wang, J., Duong, D.M., Losik, T.G., Gearing, M., Rees, H.D., Lah, J.J., Levey, A.I., and Peng, J. (2004) Proteomic characterization of postmortem amyloid plaques isolated by laser capture microdissection. J. Biol. Chem., 279, 37061-37068.
36. Wang, Q., Woltjer, R.L., Cimino, P.J., Pan, C., Montine, K.S., Zhang, J., and Montine, T.J. (2005) Proteomic analysis of neurofibrillary tangles in Alzheimer disease identifies GAPDH as a detergent-insoluble paired helical filament tau binding protein. FASEB J., 19, 869-871.
37. Xia, Q., Liao, L., Cheng, D., Duong, D.M., Gearing, M., Lah, J.J., Levey, A.I., and Peng, J. (2008) Proteomic identification of novel proteins associated with Lewy bodies. Front. Biosci., 13, 3850-3856.
38. Olzscha, H., Schermann, S.M., Woerner, A.C., Pinkert, S., Hecht, M.H., Tartaglia, G.G., Vendruscolo, M., Hayer-Hartl, M., Hartl, F.U., and Vabulas, R.M. (2011) Amyloid-like aggregates sequester numerous metastable proteins with essential cellular functions. Cell, 144, 67-78.
39. David, D.C., Ollikainen, N., Trinidad, J.C., Cary, M.P., Burlingame, A.L., and Kenyon, C. (2010) Widespread protein aggregation as an inherent part of aging in C. elegans. PLoS Biol., 8, e1000450.
40. Kikis, E.A., Gidalevitz, T., and Morimoto, R.I. (2010) Protein homeostasis in models of aging, and age-related conformational disease. Adv. Exp. Med. Biol., 694, 138-159.
41. Borchelt, D.R., Davis, J., Fischer, M., Lee, M.K., Slunt, H.H., Ratovitsky, T., Regard, J., Copeland, N.G., Jenkins, N.A., Sisodia, S.S., and Price, D.L. (1996) A vector for expressing foreign genes in the brains, and hearts of transgenic mice. Genet. Anal. Biomol. Eng., 13, 159-163.
42. Kersey, P.J., Duarte, J., Williams, A., Karavidopoulou, Y., Birney, E., and Apweiler, R. (2004) The International Protein Index: an integrated database for proteomics experiments. Proteomics, 4, 1985-1988.
43. Keller, A., Nesvizhskii, A.I., Kolker, E., and Aebersold, R. (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS, and database search. Anal. Chem., 74, 5383-5392.
44. Nesvizhskii, A.I., Keller, A., Kolker, E., and Aebersold, R. (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem., 75, 4646-4658.
45. Thomas, P.D., Kejariwal, A., Guo, N., Mi, H., Campbell, M.J., Muruganujan, A., and Lazareva-Ulitsky, B. (2006) Applications for protein sequence-function evolution data: mRNA/protein expression analysis, and coding SNP scoring tools. Nucleic Acids Res., 34, W645-W650.
46. Mi, H., Lazareva-Ulitsky, B., Loo, R., Kejariwal, A., Vandergriff, J., Rabkin, S., Guo, N., Muruganujan, A., Doremieux, O., Campbell, M.J. et al. (2005) The PANTHER database of protein families, subfamilies, functions, and pathways. Nucleic Acids Res., 33, D284-D288.
47. Prokai, L., Stevens, S.M. Jr, Rauniyar, N., and Nguyen, V. (2009) Rapid label-free identification of estrogen-induced differential protein expression in vivo from mouse brain, and uterine tissue. J. Proteome Res., 8, 3862-3871.
48. Old, W.M., Meyer-Arendt, K., Aveline-Wolf, L., Pierce, K.G., Mendoza, A., Sevinsky, J.R., Resing, K.A., and Ahn, N.G. (2005) Comparison of label-free methods for quantifying human proteins by shotgun proteomics. Mol. Cell. Proteomics, 4, 1487-1502.
49. Higgs, R.E., Knierman, M.D., Gelfanova, V., Butler, J.P., and Hale, J.E. (2005) Comprehensive label-free method for the relative quantification of proteins from biological samples. J. Proteome Res., 4, 1442-1450.
50. Sokal, R.R., and Rohlf, F.J. (1995) Biometry: The Principles, and Practice of Statistics in Biological Research, 3rd edn. W.H. Freeman, and Company, New York, NY.