Cooperative stabilization of transthyretin by clusterin and diflunisal

Biochemistry

Volumn 54, Issue 2, 2015, Pages 268-278

  Greene, Michael J ^a   Klimtchuk, Elena S ^a   Seldin, David C ^a   Berk, John L ^a   Connors, Lawreen H ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYLIC ACIDS; CIRCULAR DICHROISM SPECTROSCOPY; DICHROISM; DISEASES; HISTOLOGY; OLIGOMERS; PROTEINS; SURFACE PLASMON RESONANCE; TISSUE;

AMYLOID FIBRIL FORMATION; DIRECT INTERACTIONS; HIGH MOLECULAR WEIGHT; HYDROPHOBIC REGIONS; MISFOLDED PROTEINS; SMALL-MOLECULE DRUGS; SYSTEMIC AMYLOIDOSIS; TETRAMERIC STRUCTURES;

GLYCOPROTEINS;

AMYLOID; CLUSTERIN; CONGO RED; DIFLUNISAL; MONOMER; OLIGOMER; PREALBUMIN; NONSTEROID ANTIINFLAMMATORY AGENT; RECOMBINANT PROTEIN;

ANIMAL CELL; ARTICLE; CIRCULAR DICHROISM; CONTROLLED STUDY; HUMAN; IN VITRO STUDY; MOUSE; NONHUMAN; NORMAL HUMAN; OLIGOMERIZATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN QUATERNARY STRUCTURE; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; PROTEIN UNFOLDING; SURFACE PLASMON RESONANCE; ANTAGONISTS AND INHIBITORS; CHEMISTRY; DRUG EFFECTS; GENETICS; MALE; METABOLISM; MUTATION;

AMYLOID; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; CLUSTERIN; DIFLUNISAL; HUMANS; MALE; MUTATION; PREALBUMIN; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; PROTEIN UNFOLDING; RECOMBINANT PROTEINS;

EID: 84922424211     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi5011249     Document Type: Article

References (62)

1. Picken, M. M. (2010) Amyloidosis: Where Are We Now and Where Are We Heading? Arch. Pathol. Lab. Med. 134, 545-551
2. Westermark, P., Benson, M. D., Buxbaum, J. N., Cohen, A. S., Frangione, B., Ikeda, S.-I., Masters, C. L., Merlini, G., Saraiva, M. J., and Sipe, J. D. (2007) A primer of amyloid nomenclature Amyloid 14, 179-183
3. Ruberg, F. L. and Berk, J. L. (2012) Transthyretin (TTR) Cardiac Amyloidosis Circulation 126, 1286-1300
4. Connors, L. H., Doros, G., Sam, F., Badiee, A., Seldin, D. C., and Skinner, M. (2011) Clinical features and survival in senile systemic amyloidosis: Comparison to familial transthyretin cardiomyopathy Amyloid 18, 157-159
5. Chiti, F. and Dobson, C. M. (2006) Protein Misfolding, Functional Amyloid, and Human Disease Annu. Rev. Biochem. 75, 333-366
6. Invernizzi, G., Papaleo, E., Sabate, R., and Ventura, S. (2012) Protein aggregation: Mechanisms and functional consequences Int. J. Biochem. Cell Biol. 44, 1541-1554
7. Rodrigues, J. R., Simões, C. J. V., Silva, C. G., and Brito, R. M. M. (2010) Potentially amyloidogenic conformational intermediates populate the unfolding landscape of transthyretin: Insights from molecular dynamics simulations Protein Sci. 19, 202-219
8. Morello, J. P., Petäjä-Repo, U. E., Bichet, D. G., and Bouvier, M. (2000) Pharmacological chaperones: A new twist on receptor folding Trends Pharmacol. Sci. 21, 466-469
9. Conn, P., Leaños-Miranda, A., and Janovick, J. (2002) Protein Origami: Therapeutic Rescue of Misfolded Gene Products Mol. Interventions 2, 308-316
10. Cohen, F. E. and Kelly, J. W. (2003) Therapeutic approaches to protein-misfolding diseases Nature 426, 905-909
11. Miroy, G., Lai, Z., Lashuel, H., Peterson, S., Strang, C., and Kelly, J. (1996) Inhibiting transthyretin amyloid fibril formation via protein stabilization Proc. Natl. Acad. Sci. U.S.A. 93, 15051-15056
12. Baures, P. W., Oza, V. B., Peterson, S. A., and Kelly, J. W. (1999) Synthesis and evaluation of inhibitors of transthyretin amyloid formation based on the non-steroidal anti-inflammatory drug, flufenamic acid Bioorg. Med. Chem. 7, 1339-1347
13. Hammarström, P., Wiseman, R. L., Powers, E. T., and Kelly, J. W. (2003) Prevention of Transthyretin Amyloid Disease by Changing Protein Misfolding Energetics Science 299, 713-716
14. Buxbaum, J. and Reixach, N. (2009) Transthyretin: The servant of many masters Cell. Mol. Life Sci. 66, 3095-3101
15. Ferreira, N., Saraiva, M. J., and Almeida, M. R. (2011) Natural polyphenols inhibit different steps of the process of transthyretin (TTR) amyloid fibril formation FEBS Lett. 585, 2424-2430
16. Ferreira, N., Saraiva, M. J., and Almeida, M. R. (2012) Natural polyphenols as modulators of TTR amyloidogenesis: In vitro and in vivo evidences towards therapy Amyloid 19, 39-42
17. Sant'Anna, R. O., Braga, C. A., Polikarpov, I., Ventura, S., Lima, L. M., and Foguel, D. (2013) Inhibition of Human Transthyretin Aggregation by Non-Steroidal Anti-Inflammatory Compounds: A Structural and Thermodynamic Analysis Int. J. Mol. Sci. 14, 5284-5311
18. Klabunde, T., Petrassi, H. M., Oza, V. B., Raman, P., Kelly, J. W., and Sacchettini, J. C. (2000) Rational design of potent human transthyretin amyloid disease inhibitors Nat. Struct. Mol. Biol. 7, 312-321
19. Adamski-Werner, S. L., Palaninathan, S. K., Sacchettini, J. C., and Kelly, J. W. (2004) Diflunisal Analogues Stabilize the Native State of Transthyretin. Potent Inhibition of Amyloidogenesis J. Med. Chem. 47, 355-374
20. Miller, S. R., Sekijima, Y., and Kelly, J. W. (2004) Native state stabilization by NSAIDs inhibits transthyretin amyloidogenesis from the most common familial disease variants Lab. Invest. 84, 545-552
21. Tojo, K., Sekijima, Y., Kelly, J. W., and Ikeda, S.-I. (2006) Diflunisal stabilizes familial amyloid polyneuropathy-associated transthyretin variant tetramers in serum against dissociation required for amyloidogenesis Neurosci. Res. 56, 441-449
22. Kingsbury, J. S., Laue, T. M., Klimtchuk, E. S., Théberge, R., Costello, C. E., and Connors, L. H. (2008) The Modulation of Transthyretin Tetramer Stability by Cysteine 10 Adducts and the Drug Diflunisal: Direct Analysis by Fluorescence-Detected Analytical Ultracentrifugation J. Biol. Chem. 283, 11887-11896
23. Berk, J. L., Suhr, O. B., Sekijima, Y., Yamashita, T., Heneghan, M., Zeldenrust, S. R., Ando, Y., Ikeda, S.-I., Gorevic, P., Merlini, G., Kelly, J. W., Skinner, M., Bisbee, A. B., Dyck, P. J., and Obici, L. (2012) The Diflunisal Trial: Study accrual and drug tolerance Amyloid 19, 37-38
24. Berk, J. L., Suhr, O. B., Obici, L., Sekijima, Y., Zeldenrust, S. R., Yamashita, T., Heneghan, M. A., Gorevic, P. D., Litchy, W. J., Wiesman, J. F., Nordh, E., Corato, M., Lozza, A., Cortese, A., Robinson-Papp, J., Colton, T., Rybin, D. V., Bisbee, A. B., Ando, Y., Ikeda, S.-I., Seldin, D. C., Merlini, G., Skinner, M., Kelly, J. W., and Dyck, P. J. (2013) Repurposing Diflunisal for Familial Amyloid Polyneuropathy: A Randomized Clinical Trial JAMA, J. Am. Med. Assoc. 24, 2658-2667
25. Johnson, S. M., Connelly, S., Fearns, C., Powers, E. T., and Kelly, J. W. (2012) The Transthyretin Amyloidoses: From Delineating the Molecular Mechanism of Aggregation Linked to Pathology to a Regulatory-Agency-Approved Drug J. Mol. Biol. 421, 185-203
26. Lashuel, H. A., Lai, Z., and Kelly, J. W. (1998) Characterization of the transthyretin acid denaturation pathways by analytical ultracentrifugation: Implications for wild-type, V30M, and L55P amyloid fibril formation Biochemistry 37, 17851-17864
27. Quintas, A., Saraiva, M. J. M., and Brito, R. M. M. (1999) The Tetrameric Protein Transthyretin Dissociates to a Non-native Monomer in Solution: A Novel Model for Amyloidogenesis J. Biol. Chem. 274, 32943-32949
28. Quintas, A., Vaz, D. C., Cardoso, I., Saraiva, M. J. M., and Brito, R. M. M. (2001) Tetramer Dissociation and Monomer Partial Unfolding Precedes Protofibril Formation in Amyloidogenic Transthyretin Variants J. Biol. Chem. 276, 27207-27213
29. Jiang, X., Buxbaum, J. N., and Kelly, J. W. (2001) The V122I cardiomyopathy variant of transthyretin increases the velocity of rate-limiting tetramer dissociation, resulting in accelerated amyloidosis Proc. Natl. Acad. Sci. U.S.A. 98, 14943-14948
30. Jiang, X., Smith, C. S., Petrassi, H. M., Hammarström, P., White, J. T., Sacchettini, J. C., and Kelly, J. W. (2001) An Engineered Transthyretin Monomer that Is Nonamyloidogenic, Unless It Is Partially Denatured Biochemistry 40, 11442-11452
31. Sebastião, M. P., Lamzin, V., Saraiva, M. J., and Damas, A. M. (2001) Transthyretin stability as a key factor in amyloidogenesis: X-ray analysis at atomic resolution J. Mol. Biol. 306, 733-744
32. Shinohara, Y., Mizuguchi, M., Matsubara, K., Takeuchi, M., Matsuura, A., Aoki, T., Igarashi, K., Nagadome, H., Terada, Y., and Kawano, K. (2003) Biophysical Analyses of the Transthyretin Variants, Tyr114His and Tyr116Ser, Associated with Familial Amyloidotic Polyneuropathy Biochemistry 42, 15053-15060
33. Hurshman Babbes, A. R., Powers, E. T., and Kelly, J. W. (2008) Quantification of the Thermodynamically Linked Quaternary and Tertiary Structural Stabilities of Transthyretin and Its Disease-Associated Variants: The Relationship between Stability and Amyloidosis Biochemistry 47, 6969-6984
34. Hurshman, A. R., White, J. T., Powers, E. T., and Kelly, J. W. (2004) Transthyretin Aggregation under Partially Denaturing Conditions Is a Downhill Polymerization Biochemistry 43, 7365-7381
35. Alexandrescu, A. T. (2005) Amyloid accomplices and enforcers Protein Sci. 14, 1-12
36. Bourgault, S., Solomon, J. P., Reixach, N., and Kelly, J. W. (2011) Sulfated Glycosaminoglycans Accelerate Transthyretin Amyloidogenesis by Quaternary Structural Conversion Biochemistry 50, 1001-1015
37. Mold, M., Shrive, A. K., and Exley, C. (2012) Serum Amyloid P Component Accelerates the Formation and Enhances the Stability of Amyloid Fibrils in a Physiologically Significant Under-Saturated Solution of Amyloid-β42 J. Alzheimer's Dis. 29, 875-881
38. Wilson, M. R., Yerbury, J. J., and Poon, S. (2008) Potential roles of abundant extracellular chaperones in the control of amyloid formation and toxicity Mol. BioSyst. 4, 42-52
39. Humphreys, D. T., Carver, J. A., Easterbrook-Smith, S. B., and Wilson, M. R. (1999) Clusterin Has Chaperone-like Activity Similar to That of Small Heat Shock Proteins J. Biol. Chem. 274, 6875-6881
40. Wilson, M. R. and Easterbrook-Smith, S. B. (2000) Clusterin is a secreted mammalian chaperone Trends Biochem. Sci. 25, 95-98
41. Poon, S., Easterbrook-Smith, S. B., Rybchyn, M. S., Carver, J. A., and Wilson, M. R. (2000) Clusterin Is an ATP Independent Chaperone with Very Broad Substrate Specificity that Stabilizes Stressed Proteins in a Folding-Competent State Biochemistry 39, 15953-15960
42. Poon, S., Treweek, T. M., Wilson, M. R., Easterbrook-Smith, S. B., and Carver, J. A. (2002) Clusterin is an extracellular chaperone that specifically interacts with slowly aggregating proteins on their off-folding pathway FEBS Lett. 513, 259-266
43. Poon, S., Rybchyn, M. S., Easterbrook-Smith, S. B., Carver, J. A., Pankhurst, G. J., and Wilson, M. R. (2002) Mildly Acidic pH Activates the Extracellular Molecular Chaperone Clusterin J. Biol. Chem. 277, 39532-39540
44. Yerbury, J. J., Poon, S., Meehan, S., Thompson, B., Kumita, J. R., Dobson, C. M., and Wilson, M. R. (2007) The extracellular chaperone clusterin influences amyloid formation and toxicity by interacting with prefibrillar structures FASEB J. 21, 2312-2322
45. Wyatt, A. R., Yerbury, J. J., and Wilson, M. R. (2009) Structural Characterization of Clusterin-Chaperone Client Protein Complexes J. Biol. Chem. 284, 21920-21927
46. Greene, M. J., Sam, F., Soo Hoo, P. T., Patel, R. S., Seldin, D. C., and Connors, L. H. (2011) Evidence for a Functional Role of the Molecular Chaperone Clusterin in Amyloidotic Cardiomyopathy Am. J. Pathol. 178, 61-68
47. Kingsbury, J. S., Klimtchuk, E. S., Théberge, R., Costello, C. E., and Connors, L. H. (2007) Expression, purification, and in vitro cysteine-10 modification of native sequence recombinant human transthyretin Protein Expression Purif. 53, 370-377
48. Wilson, M. and Easterbrook-Smith, S. (1992) Clusterin binds by a multivalent mechanism to the Fc and Fab regions of IgG Biochim. Biophys. Acta 1159, 319-326
49. Lai, Z., Colon, W., and Kelly, J. W. (1996) The Acid-Mediated Denaturation Pathway of Transthyretin Yields a Conformational Intermediate That Can Self-Assemble into Amyloid Biochemistry 35, 6470-6482
50. Lindgren, M., Sörgjerd, K., and Hammarström, P. (2005) Detection and Characterization of Aggregates, Prefibrillar Amyloidogenic Oligomers, and Protofibrils Using Fluorescence Spectroscopy Biophys. J. 88, 4200-4212
51. John, D. M. and Weeks, K. M. (2000) Van't Hoff enthalpies without baselines Protein Sci. 9, 1416-1419
52. Klunk, W. E., Pettegrew, J. W., and Abraham, D. J. (1989) Quantitative evaluation of congo red binding to amyloid-like proteins with a β-pleated sheet conformation J. Histochem. Cytochem. 37, 1273-1281
53. Klunk, W. E., Jacob, R. F., Mason, R. P., and Ronald, W. (1999) Quantifying amyloid by congo red spectral shift assay. In Methods in Enzymology, pp 285-305, Academic Press, San Diego.
54. Hochgrebe, T., Pankhurst, G. J., Wilce, J., and Easterbrook-Smith, S. B. (2000) pH-Dependent Changes in the in Vitro Ligand-Binding Properties and Structure of Human Clusterin Biochemistry 39, 1411-1419
55. Shnyrov, V. L., Villar, E., Zhadan, G. G., Sanchez-Ruiz, J. M., Quintas, A., Saraiva, M. J. M., and Brito, R. M. M. (2000) Comparative calorimetric study of non-amyloidogenic and amyloidogenic variants of the homotetrameric protein transthyretin Biophys. Chem. 88, 61-67
56. 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
57. Lindquist, S. L. and Kelly, J. W. (2012) Chemical and Biological Approaches for Adapting Proteostasis to Ameliorate Protein Misfolding and Aggregation Diseases-Progress and Prognosis Cold Spring Harbor Perspect. Biol. 3, 1-34
58. Wyatt, A. R., Yerbury, J. J., Dabbs, R. A., and Wilson, M. R. (2012) Roles of Extracellular Chaperones in Amyloidosis J. Mol. Biol. 421, 499-516
59. Wyatt, A. R. and Wilson, M. R. (2010) Identification of human plasma proteins as major clients for the extracellular chaperone clusterin J. Biol. Chem. 285, 3532-3539
60. Wyatt, A. R., Yerbury, J. J., Berghofer, P., Greguric, I., Katsifis, A., Dobson, C. M., and Wilson, M. R. (2011) Clusterin facilitates in vivo clearance of extracellular misfolded proteins Cell. Mol. Life Sci. 68, 3919-3931
61. Azevedo, E. P. C., Pereira, H. M., Garratt, R. C., Kelly, J. W., Foguel, D., and Palhano, F. L. (2011) Dissecting the Structure, Thermodynamic Stability, and Aggregation Properties of the A25T Transthyretin (A25T-TTR) Variant Involved in Leptomeningeal Amyloidosis: Identifying Protein Partners That Co-Aggregate during A25T-TTR Fibrillogenesis in Cerebrospinal Fluid Biochemistry 50, 11070-11083
62. Magalhães, J. and Saraiva, M. J. (2011) Clusterin Overexpression and Its Possible Protective Role in Transthyretin Deposition in Familial Amyloidotic Polyneuropathy J. Neuropathol. Exp. Neurol. 70, 1097-1106