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PMID: 18775310 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Chemical and biological approaches synergize to ameliorate protein-folding diseases.

Cell ·Vol. 134 ·No. 5 ·2008-09-05 ·Pages 769-81

Mu TW, Ong DS, Wang YJ, Balch WE, Yates JR, Segatori L, Kelly JW

Abstract

Loss-of-function diseases are often caused by a mutation in a protein traversing the secretory pathway that compromises the normal balance between protein folding, trafficking, and degradation. We demonstrate that the innate cellular protein homeostasis, or proteostasis, capacity can be enhanced to fold mutated enzymes that would otherwise misfold and be degraded, using small molecule proteostasis regulators. Two proteostasis regulators are reported that alter the composition of the proteostasis network in the endoplasmic reticulum through the unfolded protein response, increasing the mutant folded protein concentration that can engage the trafficking machinery, restoring function to two nonhomologous mutant enzymes associated with distinct lysosomal storage diseases. Coapplication of a pharmacologic chaperone and a proteostasis regulator exhibits synergy because of the former's ability to further increase the concentration of trafficking-competent mutant folded enzymes. It may be possible to ameliorate loss-of-function diseases by using proteostasis regulators alone or in combination with a pharmacologic chaperone.

MeSH Terms
Cell Line Fibroblasts/metabolism Gaucher Disease/drug therapy,metabolism Humans Leupeptins/pharmacology Lysosomal Storage Diseases/drug therapy,metabolism Molecular Chaperones/pharmacology Pentacyclic Triterpenes Protein Folding Proteins/metabolism Tay-Sachs Disease/drug therapy,metabolism Triterpenes/pharmacology
Chemicals
Leupeptins Molecular Chaperones Pentacyclic Triterpenes Proteins Triterpenes celastrol benzyloxycarbonylleucyl-leucyl-leucine aldehyde
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Mu Ting-Wei
Department of Chemistry and The Skaggs Institute for Chemical Biology, The Scripps Research Institute, La Jolla, CA 92037, USA.
Ong Derrick Sek Tong
Wang Ya-Juan
Balch William E
Yates John R
Segatori Laura
Kelly Jeffery W
References (53)
53 references, click to expand
  1. Correcting temperature-sensitive protein folding defects.
    J Clin Invest. 1997 Mar 15;99(6):1432-44 PMID: 9077553
  2. When an inhibitor promotes activity.
    Chem Biol. 2007 Mar;14(3):241-2 PMID: 17379138
  3. Orchestrating the unfolded protein response in health and disease.
    J Clin Invest. 2002 Nov;110(10):1389-98 PMID: 12438434
  4. Proteasome inhibition leads to a heat-shock response, induction of endoplasmic reticulum chaperones, and thermotolerance.
    J Biol Chem. 1997 Apr 4;272(14):9086-92 PMID: 9083035
  5. Role of ubiquitin-proteasome degradation pathway in biogenesis efficiency of {beta}-cell ATP-sensitive potassium channels.
    Am J Physiol Cell Physiol. 2005 Nov;289(5):C1351-9 PMID: 15987767
  6. Chaperone-assisted folding of newly synthesized proteins in the cytosol.
    Crit Rev Biochem Mol Biol. 2004 Sep-Dec;39(5-6):261-77 PMID: 15763705
  7. Endoplasmic reticulum stress increases the expression of methylenetetrahydrofolate reductase through the IRE1 transducer.
    J Biol Chem. 2008 Feb 8;283(6):3151-3160 PMID: 18065414
  8. Heat shock response relieves ER stress.
    EMBO J. 2008 Apr 9;27(7):1049-59 PMID: 18323774
  9. Heat shock response modulators as therapeutic tools for diseases of protein conformation.
    J Biol Chem. 2005 Sep 30;280(39):33097-100 PMID: 16076838
  10. Dissociation from BiP and retrotranslocation of unassembled immunoglobulin light chains are tightly coupled to proteasome activity.
    Mol Biol Cell. 2000 Jan;11(1):217-26 PMID: 10637303
  11. A selective inhibitor of eIF2alpha dephosphorylation protects cells from ER stress.
    Science. 2005 Feb 11;307(5711):935-9 PMID: 15705855
  12. ER retention and degradation as the molecular basis underlying Gaucher disease heterogeneity.
    Hum Mol Genet. 2005 Aug 15;14(16):2387-98 PMID: 16000318
  13. Upregulation of heat shock protein expression by proteasome inhibition: an antiapoptotic mechanism in the lens.
    Invest Ophthalmol Vis Sci. 2005 Jun;46(6):2082-91 PMID: 15914627
  14. Accelerated transport and maturation of lysosomal alpha-galactosidase A in Fabry lymphoblasts by an enzyme inhibitor.
    Nat Med. 1999 Jan;5(1):112-5 PMID: 9883849
  15. Multiple proteolytic systems, including the proteasome, contribute to CFTR processing.
    Cell. 1995 Oct 6;83(1):129-35 PMID: 7553864
  16. The protective and destructive roles played by molecular chaperones during ERAD (endoplasmic-reticulum-associated degradation).
    Biochem J. 2007 Jun 15;404(3):353-63 PMID: 17521290
  17. Impaired trafficking of mutants of lysosomal glucocerebrosidase in Gaucher's disease.
    Int J Biochem Cell Biol. 2005 Nov;37(11):2310-20 PMID: 15982918
  18. Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer.
    Cell. 2007 Dec 14;131(6):1190-203 PMID: 18083107
  19. Chemical chaperones and permissive temperatures alter localization of Gaucher disease associated glucocerebrosidase variants.
    ACS Chem Biol. 2006 May 23;1(4):235-51 PMID: 17163678
  20. Partial enzyme deficiencies: residual activities and the development of neurological disorders.
    Dev Neurosci. 1983-1984;6(1):58-71 PMID: 6421563
  21. The cell biology of lysosomal storage disorders.
    Nat Rev Mol Cell Biol. 2004 Jul;5(7):554-65 PMID: 15232573
  22. Systems analyses reveal two chaperone networks with distinct functions in eukaryotic cells.
    Cell. 2006 Jan 13;124(1):75-88 PMID: 16413483
  23. Isofagomine- and 2,5-anhydro-2,5-imino-D-glucitol-based glucocerebrosidase pharmacological chaperones for Gaucher disease intervention.
    J Med Chem. 2007 Jan 11;50(1):94-100 PMID: 17201413
  24. Celastrol, a triterpene extracted from the Chinese "Thunder of God Vine," is a potent proteasome inhibitor and suppresses human prostate cancer growth in nude mice.
    Cancer Res. 2006 May 1;66(9):4758-65 PMID: 16651429
  25. Enzyme replacement for lysosomal diseases.
    Annu Rev Med. 2006;57:283-96 PMID: 16409150
  26. The mammalian unfolded protein response.
    Annu Rev Biochem. 2005;74:739-89 PMID: 15952902
  27. Adapting proteostasis for disease intervention.
    Science. 2008 Feb 15;319(5865):916-9 PMID: 18276881
  28. A new frontier in pharmacology: the endoplasmic reticulum as a regulated export pathway in health and disease.
    Expert Opin Ther Targets. 2001 Apr;5(2):165-76 PMID: 15992174
  29. Hsp90 cochaperone Aha1 downregulation rescues misfolding of CFTR in cystic fibrosis.
    Cell. 2006 Nov 17;127(4):803-15 PMID: 17110338
  30. Chemical chaperones increase the cellular activity of N370S beta -glucosidase: a therapeutic strategy for Gaucher disease.
    Proc Natl Acad Sci U S A. 2002 Nov 26;99(24):15428-33 PMID: 12434014
  31. BDNF induces widespread changes in synaptic protein content and up-regulates components of the translation machinery: an analysis using high-throughput proteomics.
    J Proteome Res. 2007 Mar;6(3):1059-71 PMID: 17330943
  32. Pharmacological enhancement of beta-hexosaminidase activity in fibroblasts from adult Tay-Sachs and Sandhoff Patients.
    J Biol Chem. 2004 Apr 2;279(14):13478-87 PMID: 14724290
  33. Proteasome inhibition induces differential heat shock protein response but not unfolded protein response in HepG2 cells.
    J Cell Biochem. 2006 Nov 1;99(4):1085-95 PMID: 16767695
  34. Partial restoration of mutant enzyme homeostasis in three distinct lysosomal storage disease cell lines by altering calcium homeostasis.
    PLoS Biol. 2008 Feb;6(2):e26 PMID: 18254660
  35. An adaptable standard for protein export from the endoplasmic reticulum.
    Cell. 2007 Nov 16;131(4):809-21 PMID: 18022373
  36. Lysosomal storage diseases: natural history and ethical and economic aspects.
    Mol Genet Metab. 2006 Jul;88(3):208-15 PMID: 16515872
  37. Celastrols as inducers of the heat shock response and cytoprotection.
    J Biol Chem. 2004 Dec 31;279(53):56053-60 PMID: 15509580
  38. Pyrimethamine as a potential pharmacological chaperone for late-onset forms of GM2 gangliosidosis.
    J Biol Chem. 2007 Mar 23;282(12):9150-61 PMID: 17237499
  39. Correlation between enzyme activity and substrate storage in a cell culture model system for Gaucher disease.
    J Inherit Metab Dis. 2004;27(5):649-58 PMID: 15669681
  40. Therapeutic strategies to ameliorate lysosomal storage disorders--a focus on Gaucher disease.
    Cell Mol Life Sci. 2006 May;63(10):1179-92 PMID: 16568247
  41. A model for random sampling and estimation of relative protein abundance in shotgun proteomics.
    Anal Chem. 2004 Jul 15;76(14):4193-201 PMID: 15253663
  42. Glycosphingolipid lysosomal storage diseases: therapy and pathogenesis.
    Neuropathol Appl Neurobiol. 2002 Oct;28(5):343-57 PMID: 12366816
  43. Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators.
    Genes Dev. 1998 Dec 15;12(24):3788-96 PMID: 9869631
  44. Pathways of chaperone-mediated protein folding in the cytosol.
    Nat Rev Mol Cell Biol. 2004 Oct;5(10):781-91 PMID: 15459659
  45. Hematologically important mutations: Gaucher disease.
    Blood Cells Mol Dis. 2005 Nov-Dec;35(3):355-64 PMID: 16185900
  46. Gaucher disease-associated glucocerebrosidases show mutation-dependent chemical chaperoning profiles.
    Chem Biol. 2005 Nov;12(11):1235-44 PMID: 16298303
  47. Pharmacological chaperone corrects lysosomal storage in Fabry disease caused by trafficking-incompetent variants.
    Am J Physiol Cell Physiol. 2006 Apr;290(4):C1076-82 PMID: 16531566
  48. Therapeutic approaches to protein-misfolding diseases.
    Nature. 2003 Dec 18;426(6968):905-9 PMID: 14685252
  49. Enzyme replacement therapy in Gaucher's disease: preliminary clinical trial of a new enzyme preparation.
    Proc Natl Acad Sci U S A. 1977 Oct;74(10):4620-3 PMID: 200923
  50. Proteasomes and molecular chaperones: cellular machinery responsible for folding and destruction of unfolded proteins.
    Cell Cycle. 2003 Nov-Dec;2(6):585-90 PMID: 14512774
  51. Signal integration in the endoplasmic reticulum unfolded protein response.
    Nat Rev Mol Cell Biol. 2007 Jul;8(7):519-29 PMID: 17565364
  52. The heat-shock response.
    Annu Rev Biochem. 1986;55:1151-91 PMID: 2427013
  53. Pharmacologic rescue of conformationally-defective proteins: implications for the treatment of human disease.
    Traffic. 2004 Nov;5(11):821-37 PMID: 15479448
Article Info
Journal
Cell
Abbr.
Cell
ISSN
1097-4172
Published
2008-09-05
Pages
769-81
Language
English
Region
United States
NLM ID
0413066
PMCID
PMC2650088
Subset
IM
Grants
NIDDK NIH HHS · R01 DK075295 · United States
NIDDK NIH HHS · R01 DK075295-03 · United States
NIDDK NIH HHS · DK75295 · United States
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