TFEB regulates lysosomal proteostasis

Human Molecular Genetics

Volumn 22, Issue 10, 2013, Pages 1994-2009

  Song, Wensi ^a   Wang, Fan ^a   Savini, Marzia ^a   Ake, Ashley ^a   di ronza, Alberto ^c   Sardiello, Marco ^c   Segatori, Laura ^a,b  

^a Rice University   (United States)

^b Department of Biochemistry and Cell Biology ^*  (United States)

^c TEXAS CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; BETA N ACETYLHEXOSAMINIDASE; CALNEXIN; CALRETICULIN; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; GLUCOSE REGULATED PROTEIN 78; GLUCOSYLCERAMIDASE; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; LYSOSOME ENZYME; SCATTER FACTOR; SOMATOMEDIN B RECEPTOR; SORTILIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR EB; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL VIABILITY; CELLULAR DISTRIBUTION; ENZYME ACTIVITY; ENZYME DEGRADATION; FIBROBLAST; GAUCHER DISEASE; GENE EXPRESSION; GLYCOSYLATION; LYSOSOME; MISSENSE MUTATION; NUCLEAR LOCALIZATION SIGNAL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN HOMEOSTASIS; SECRETORY PATHWAY; TAY SACHS DISEASE; UNFOLDED PROTEIN RESPONSE; UPREGULATION;

EID: 84877011421     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt052     Document Type: Article

References (74)

1. Futerman, A.H. and van Meer, G. (2004) The cell biology of lysosomal storage disorders. Nat. Rev. Mol. Cell Biol., 5, 554-565.
2. Schueler, U.H., Kolter, T., Kaneski, C.R., Zirzow, G.C., Sandhoff, K. and Brady, R.O. (2004) Correlation between enzyme activity and substrate storage in a cell culture model system for Gaucher disease. J. Inherit Metab. Dis., 27, 649-658.
3. Hruska, K.S., LaMarca, M.E., Scott, C.R. and Sidransky, E. (2008) Gaucher disease: mutation and polymorphism spectrum in the glucocerebrosidase gene (GBA). Hum. Mutat., 29, 567-583.
4. Grace, M.E., Newman, K.M., Scheinker, V., Berg-Fussman, A. and Grabowski, G.A. (1994) Analysis of human acid beta-glucosidase by site-directed mutagenesis and heterologous expression. J. Biol. Chem., 269, 2283-2291.
5. Schmitz, M., Alfalah, M., Aerts, J.M., Naim, H.Y. and Zimmer, K.P. (2005) Impaired trafficking of mutants of lysosomal glucocerebrosidase in Gaucher's disease. Int. J. Biochem. Cell Biol., 37, 2310-2320.
6. Lu, J., Chiang, J., Iyer, R.R., Thompson, E., Kaneski, C.R., Xu, D.S., Yang, C., Chen, M., Hodes, R.J., Lonser, R.R. et al. (2010) Decreased glucocerebrosidase activity in Gaucher disease parallels quantitative enzyme loss due to abnormal interaction with TCP1 and c-Cbl. Proc. Natl Acad. Sci. USA, 107, 21665-21670.
7. Sawkar, A.R., Cheng, W.C., Beutler, E., Wong, C.H., Balch, W.E. and Kelly, J.W. (2002) Chemical chaperones increase the cellular activity of N370S beta -glucosidase: a therapeutic strategy for Gaucher disease. Proc. Natl Acad. Sci. USA, 99, 15428-15433.
8. Yu, Z., Sawkar, A.R., Whalen, L.J., Wong, C.H. and Kelly, J.W. (2007) Isofagomine- and 2,5-anhydro-2,5-imino-D-glucitol-based glucocerebrosidase pharmacological chaperones for Gaucher disease intervention. J. Med. Chem., 50, 94-100.
9. Ron, I. and Horowitz, M. (2005) ER retention and degradation as the molecular basis underlying Gaucher disease heterogeneity. Hum. Mol. Genet., 14, 2387-2398.
10. Powers, E.T., Morimoto, R.I., Dillin, A., Kelly, J.W. and Balch, W.E. (2009) Biological and chemical approaches to diseases of proteostasis deficiency. Annu. Rev. Biochem., 78, 959-991.
11. Mu, T.W., Fowler, D.M. and Kelly, J.W. (2008) Partial restoration of mutant enzyme homeostasis in three distinct lysosomal storage disease cell lines by altering calcium homeostasis. PLoS Biol., 6, e26.
12. Mu, T.W., Ong, D.S., Wang, Y.J., Balch, W.E., Yates, J.R. 3rd, Segatori, L. and Kelly, J.W. (2008) Chemical and biological approaches synergize to ameliorate protein-folding diseases. Cell, 134, 769-781.
13. Ong, D.S., Mu, T.W., Palmer, A.E. and Kelly, J.W. (2010) Endoplasmic reticulum Ca2+ increases enhance mutant glucocerebrosidase proteostasis. Nat. Chem. Biol., 6, 424-432.
14. 2+ homeostasis modulation enhances the amenability of L444P glucosylcerebrosidase to proteostasis regulation in patient-derived fibroblasts. ACS Chem. Biol., 6, 158-168.
15. Wang, F., Chou, A. and Segatori, L. (2011) Lacidipine remodels protein folding and Ca2+ homeostasis in Gaucher's disease fibroblasts: a mechanism to rescue mutant glucocerebrosidase. Chem. Biol., 18, 766-776.
16. Wang, F., Song, W., Brancati, G. and Segatori, L. (2011) Inhibition of endoplasmic reticulum-associated degradation rescues native folding in loss of function protein misfolding diseases. J. Biol. Chem., 286, 43454-43464.
17. Koprivica, V., Stone, D.L., Park, J.K., Callahan, M., Frisch, A., Cohen, I.J., Tayebi, N. and Sidransky, E. (2000) Analysis and classification of 304 mutant alleles in patients with type 1 and type 3 Gaucher disease. Am. J. Hum. Genet., 66, 1777-1786.
18. Grabowski, G.A. (1997) Gaucher disease: gene frequencies and genotype/ phenotype correlations. Genet. Test, 1, 5-12.
19. Lu, J., Yang, C., Chen, M., Ye, D.Y., Lonser, R.R., Brady, R.O. and Zhuang, Z. (2011) Histone deacetylase inhibitors prevent the degradation and restore the activity of glucocerebrosidase in Gaucher disease. Proc. Natl Acad. Sci. USA, 108, 21200-21205.
20. Sardiello, M., Palmieri, M., di Ronza, A., Medina, D.L., Valenza, M., Gennarino, V.A., Di Malta, C., Donaudy, F., Embrione, V., Polishchuk, R.S. et al. (2009) A gene network regulating lysosomal biogenesis and function. Science, 325, 473-477.
21. Steingrimsson, E., Copeland, N.G. and Jenkins, N.A. (2004) Melanocytes and the microphthalmia transcription factor network. Annu. Rev. Genet., 38, 365-411.
22. Palmieri, M., Impey, S., Kang, H., di Ronza, A., Pelz, C., Sardiello, M. and Ballabio, A. (2011) Characterization of the CLEAR network reveals an integrated control of cellular clearance pathways. Hum. Mol. Genet., 20, 3852-3866.
23. Medina, D.L., Fraldi, A., Bouche, V., Annunziata, F., Mansueto, G., Spampanato, C., Puri, C., Pignata, A., Martina, J.A., Sardiello, M. et al. (2011) Transcriptional activation of lysosomal exocytosis promotes cellular clearance. Dev. Cell, 21, 421-430.
24. Settembre, C., Di Malta, C., Polito, V.A., Garcia Arencibia, M., Vetrini, F., Erdin, S., Erdin, S.U., Huynh, T., Medina, D., Colella, P. et al. (2011) TFEB links autophagy to lysosomal biogenesis. Science, 332, 1429-1433.
25. Reczek, D., Schwake, M., Schroder, J., Hughes, H., Blanz, J., Jin, X.Y., Brondyk, W., Van Patten, S., Edmunds, T. and Saftig, P. (2007) LIMP-2 is a receptor for lysosomal mannose-6-phosphate-independent targeting of beta-glucocerebrosidase. Cell, 131, 770-783.
26. Welch, W.J. and Brown, C.R. (1996) Influence of molecular and chemical chaperones on protein folding. Cell Stress Chaperones, 1, 109-115.
27. Kim, S.H., Yan, Y.B. and Zhou, H.M. (2006) Role of osmolytes as chemical chaperones during the refolding of aminoacylase. Biochem. Cell Biol., 84, 30-38.
28. Brown, C.R., Hong-Brown, L.Q., Biwersi, J., Verkman, A.S. and Welch, W.J. (1996) Chemical chaperones correct the mutant phenotype of the delta F508 cystic fibrosis transmembrane conductance regulator protein. Cell Stress Chaperones, 1, 117-125.
29. Ferrao-Gonzales, A.D., Palmieri, L., Valory, M., Silva, J.L., Lashuel, H., Kelly, J.W. and Foguel, D. (2003) Hydration and packing are crucial to amyloidogenesis as revealed by pressure studies on transthyretin variants that either protect or worsen amyloid disease. J. Mol. Biol., 328, 963-974.
30. Maley, F., Trimble, R.B., Tarentino, A.L. and Plummer, T.H. Jr (1989) Characterization of glycoproteins and their associated oligosaccharides through the use of endoglycosidases. Anal. Biochem., 180, 195-204.
31. Michelakakis, H., Dimitriou, E., Van Weely, S., Boot, R.G., Mavridou, I., Verhoek, M. and Aerts, J.M. (1995) Characterization of glucocerebrosidase in Greek Gaucher disease patients: mutation analysis and biochemical studies. J. Inherit Metab. Dis., 18, 609-615.
32. Karageorgos, L.E., Isaac, E.L., Brooks, D.A., Ravenscroft, E.M., Davey, R., Hopwood, J.J. and Meikle, P.J. (1997) Lysosomal biogenesis in lysosomal storage disorders. Exp. Cell Res., 234, 85-97.
33. Gennarino, V.A., D'Angelo, G., Dharmalingam, G., Fernandez, S., Russolillo, G., Sanges, R., Mutarelli, M., Belcastro, V., Ballabio, A., Verde, P. et al. (2012) Identification of microRNA-regulated gene networks by expression analysis of target genes. Genome Res., 22, 1163-1172.
34. Lopes, C.T., Franz, M., Kazi, F., Donaldson, S.L., Morris, Q. and Bader, G.D. (2010) Cytoscape Web: an interactive web-based network browser. Bioinformatics, 26, 2347-2348.
35. Subramanian, A., Tamayo, P., Mootha, V.K., Mukherjee, S., Ebert, B.L., Gillette, M.A., Paulovich, A., Pomeroy, S.L., Golub, T.R., Lander, E.S. et al. (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA, 102, 15545-15550.
36. Lubke, T., Lobel, P. and Sleat, D.E. (2009) Proteomics of the lysosome. Biochim. Biophys. Acta, 1793, 625-635.
37. Sawkar, A.R., Schmitz, M., Zimmer, K.P., Reczek, D., Edmunds, T., Balch, W.E. and Kelly, J.W. (2006) Chemical chaperones and permissive temperatures alter localization of Gaucher disease associated glucocerebrosidase variants. ACS Chem. Biol., 1, 235-251.
38. Tropak, M.B., Reid, S.P., Guiral, M., Withers, S.G. and Mahuran, D. (2004) Pharmacological enhancement of beta-hexosaminidase activity in fibroblasts from adult Tay-Sachs and Sandhoff Patients. J. Biol. Chem., 279, 13478-13487.
39. Meikle, P.J., Hopwood, J.J., Clague, A.E. and Carey, W.F. (1999) Prevalence of lysosomal storage disorders. JAMA, 281, 249-254.
40. Dionisi-Vici, C., Rizzo, C., Burlina, A.B., Caruso, U., Sabetta, G., Uziel, G. and Abeni, D. (2002) Inborn errors of metabolism in the Italian pediatric population: a national retrospective survey. J. Pediatr., 140, 321-327.
41. Roversi, F.M., Galdieri, L.C., Grego, B.H., Souza, F.G., Micheletti, C., Martins, A.M. and D'Almeida, V. (2006) Blood oxidative stress markers in Gaucher disease patients. Clin. Chim. Acta, 364, 316-320.
42. Fu, R., Yanjanin, N.M., Bianconi, S., Pavan, W.J. and Porter, F.D. (2010) Oxidative stress in Niemann-Pick disease, type C. Mol. Genet. Metab., 101, 214-218.
43. Lieberman, A.P., Puertollano, R., Raben, N., Slaugenhaupt, S., Walkley, S.U. and Ballabio, A. (2012) Autophagy in lysosomal storage disorders. Autophagy, 8, 719-730.
44. Ginzburg, L. and Futerman, A.H. (2005) Defective calcium homeostasis in the cerebellum in a mouse model of Niemann-Pick A disease. J. Neurochem., 95, 1619-1628.
45. 2+ homeostasis in lysosomal storage diseases. Cell Calcium, 44, 103-111.
46. Wei, H., Kim, S.J., Zhang, Z., Tsai, P.C., Wisniewski, K.E. and Mukherjee, A.B. (2008) ER and oxidative stresses are common mediators of apoptosis in both neurodegenerative and non-neurodegenerative lysosomal storage disorders and are alleviated by chemical chaperones. Hum. Mol. Genet., 17, 469-477.
47. Abrahamov, A., Elstein, D., Gross-Tsur, V., Farber, B., Glaser, Y., Hadas-Halpern, I., Ronen, S., Tafakjdi, M., Horowitz, M. and Zimran, A. (1995) Gaucher's disease variant characterised by progressive calcification of heart valves and unique genotype. Lancet, 346, 1000-1003.
48. Zhao, H. and Grabowski, G.A. (2002) Gaucher disease: Perspectives on a prototype lysosomal disease. Cell Mol. Life Sci., 59, 694-707.
49. Grabowski, G.A. and Hopkin, R.J. (2003) Enzyme therapy for lysosomal storage disease: principles, practice, and prospects. Annu. Rev. Genomics Hum. Genet., 4, 403-436.
50. Rohrbach, M. and Clarke, J.T. (2007) Treatment of lysosomal storage disorders: progress with enzymereplacement therapy.Drugs, 67, 2697-2716.
51. Desnick, R.J. and Schuchman, E.H. (2012) Enzyme replacement therapy for lysosomal diseases: lessons from 20 years of experience and remaining challenges. Annu. Rev. Genomics Hum. Genet., 13, 307-335.
52. Beutler, E. (2004) Enzyme replacement in Gaucher disease. PLoS Med., 1, e21.
53. Altarescu, G., Hill, S., Wiggs, E., Jeffries, N., Kreps, C., Parker, C.C., Brady, R.O., Barton, N.W. and Schiffmann, R. (2001) The efficacy of enzyme replacement therapy in patients with chronic neuronopathic Gaucher's disease. J. Pediatr., 138, 539-547.
54. Shapiro, E.G., Lockman, L.A., Balthazor, M. and Krivit, W. (1995) Neuropsychological outcomes of several storage diseases with and without bone marrow transplantation. J. Inherit Metab. Dis., 18, 413-429.
55. Krivit, W., Aubourg, P., Shapiro, E. and Peters, C. (1999) Bone marrow transplantation for globoid cell leukodystrophy, adrenoleukodystrophy, metachromatic leukodystrophy, and Hurler syndrome. Curr. Opin. Hematol., 6, 377-382.
56. Krivit, W., Peters, C. and Shapiro, E.G. (1999) Bone marrow transplantation as effective treatment of central nervous system disease in globoid cell leukodystrophy, metachromatic leukodystrophy, adrenoleukodystrophy, mannosidosis, fucosidosis, aspartylglucosaminuria, Hurler, Maroteaux-Lamy, and Sly syndromes, and Gaucher disease type III. Curr. Opin. Neurol., 12, 167-176.
57. Krivit, W. (2002) Stem cell bone marrow transplantation in patients with metabolic storage diseases. Adv. Pediatr., 49, 359-378.
58. Seregin, S.S. and Amalfitano, A. (2011) Gene therapy for lysosomal storage diseases: progress, challenges and future prospects. Curr. Pharm. Des., 17, 2558-2574.
59. Sands, M.S. and Davidson, B.L. (2006) Gene therapy for lysosomal storage diseases. Mol. Ther., 13, 839-849.
60. Tsuji, S., Choudary, P.V., Martin, B.M., Stubblefield, B.K., Mayor, J.A., Barranger, J.A. and Ginns, E.I. (1987) A mutation in the human glucocerebrosidase gene in neuronopathic Gaucher's disease. N. Engl. J. Med., 316, 570-575.
61. Tsuji, S., Martin, B.M., Barranger, J.A., Stubblefield, B.K., LaMarca, M.E. and Ginns, E.I. (1988) Genetic heterogeneity in type 1 Gaucher disease: multiple genotypes in Ashkenazic and non-Ashkenazic individuals. Proc. Natl Acad. Sci. USA, 85, 2349-2352.
62. Neufeld, E.F. (1991) Lysosomal storage diseases. Annu. Rev. Biochem., 60, 257-280.
63. Gieselmann, V. (1995) Lysosomal storage diseases. Biochim. Biophys. Acta, 1270, 103-136.
64. Balch, W.E., Roth, D.M. and Hutt, D.M. (2011) Emergent properties of proteostasis inmanaging cystic fibrosis. Cold Spring Harb. Perspect. Biol., 3, pii: a004499.
65. Balch, W.E., Morimoto, R.I., Dillin, A. and Kelly, J.W. (2008) Adapting proteostasis for disease intervention. Science, 319, 916-919.
66. Sardiello, M. and Ballabio, A. (2009) Lysosomal enhancement: a CLEAR answer to cellular degradative needs. Cell Cycle, 8, 4021-4022.
67. Ma, X., Godar, R., Liu, H. and Diwan, A. (2012) Enhancing lysosome biogenesis attenuates BNIP3-induced cardiomyocyte death. Autophagy, 8, 297-309.
68. Tsunemi, T., Ashe, T., Morrison, B., Soriano, K., Au, J., Roque, R., Lazarowski, E., Damian, V., Masliah, E. and La Spada, A. (2012) PGC-1a rescues Huntington's disease proteotoxicity by preventing oxidative stress and promoting TFEB function. Sci. Transl. Med., 4, 142ra97.
69. Parr, C., Carzaniga, R., Gentleman, S.M., Van Leuven, F., Walter, J. and Sastre, M. (2012) Glycogen synthase kinase 3 inhibition promotes lysosomal biogenesis and autophagic degradation of the amyloid-beta precursor protein. Mol. Cell Biol., 32, 4410-4418.
70. Cho, S. and Hwang, E.S. (2012) Status of mTOR activity may phenotypically differentiate senescence and quiescence. Mol. Cells, 33, 597-604.
71. Nigg, E.A. (1997) Nucleocytoplasmic transport: signals, mechanisms and regulation. Nature, 386, 779-787.
72. Christophe, D., Christophe-Hobertus, C. and Pichon, B. (2000) Nuclear targeting of proteins: how many different signals? Cell Signal., 12, 337-341.
73. Huang, D.W., Sherman, B.T. and Lempicki, R.A. (2008) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc., 4, 44-57.
74. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A. and Speleman, F. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol., 3, RESEARCH0034.