Structural Insight into pH-Induced Conformational Changes within the Native Human Transthyretin Tetramer

Journal of Molecular Biology

Volumn 382, Issue 5, 2008, Pages 1157-1167

  Palaninathan, Satheesh K ^a   Mohamedmohaideen, Nilofar N ^a   Snee, William C ^a   Kelly, Jeffery W ^b   Sacchettini, James C ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

amyloid fibrils; amyloidosis; crystal structure; low pH; transthyretin

Indexed keywords

AMYLOID; ASPARTIC ACID; GLUTAMIC ACID; HELIX LOOP HELIX PROTEIN; HISTIDINE; LYSINE; MONOMER; PREALBUMIN; PROTEIN SUBUNIT; TETRAMER;

ACIDIFICATION; ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; HUMAN; PH; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STRUCTURE; WILD TYPE;

EID: 51349136571     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.07.029     Document Type: Article

References (58)

1. Monaco H.L., Rizzi M., and Coda A. Structure of a complex of two plasma proteins: transthyretin and retinol-binding protein. Science 268 (1995) 1039-1041
2. Naylor H.M., and Newcomer M.E. The structure of human retinol-binding protein (RBP) with its carrier protein transthyretin reveals an interaction with the carboxy terminus of RBP. Biochemistry 38 (1999) 2647-2653
3. Johnson S.M., Wiseman R.L., Sekijima Y., Green N.S., Adamski-Werner S.L., and Kelly J.W. Native state kinetic stabilization as a strategy to ameliorate protein misfolding diseases: a focus on the transthyretin amyloidoses. Acc. Chem. Res. 38 (2005) 911-921
4. Hamilton J.A., and Benson M.D. Transthyretin: a review from a structural perspective. Cell. Mol. Life Sci. 58 (2001) 1491-1521
5. McCutchen S.L., Colon W., and Kelly J.W. Transthyretin mutation Leu-55-Pro significantly alters tetramer stability and increases amyloidogenicity. Biochemistry 32 (1993) 12119-12127
6. Colon W., and Kelly J.W. Partial denaturation of transthyretin is sufficient for amyloid fibril formation in vitro. Biochemistry 31 (1992) 8654-8660
7. Hurshman A.R., White J.T., Powers E.T., and Kelly J.W. Transthyretin aggregation under partially denaturing conditions is a downhill polymerization. Biochemistry 43 (2004) 7365-7381
8. Jiang X., Smith C.S., Petrassi H.M., Hammarstrom P., White J.T., Sacchettini J.C., and Kelly J.W. An engineered transthyretin monomer that is nonamyloidogenic, unless it is partially denatured. Biochemistry 40 (2001) 11442-11452
9. Kelly J.W., Colon W., Lai Z., Lashuel H.A., McCulloch J., McCutchen S.L., et al. Transthyretin quaternary and tertiary structural changes facilitate misassembly into amyloid. Adv. Protein Chem. 50 (1997) 161-181
10. Lashuel H.A., Wurth C., Woo L., and Kelly J.W. The most pathogenic transthyretin variant, L55P, forms amyloid fibrils under acidic conditions and protofilaments under physiological conditions. Biochemistry 38 (1999) 13560-13573
11. Liu K., Cho H.S., Lashuel H.A., Kelly J.W., and Wemmer D.E. A glimpse of a possible amyloidogenic intermediate of transthyretin. Nat. Struct. Biol. 7 (2000) 754-757
12. McCutchen S.L., Lai Z., Miroy G.J., Kelly J.W., and Colon W. Comparison of lethal and nonlethal transthyretin variants and their relationship to amyloid disease. Biochemistry 34 (1995) 13527-13536
13. Westermark P., Sletten K., Johansson B., and Cornwell III G.G. Fibril in senile systemic amyloidosis is derived from normal transthyretin. Proc. Natl Acad. Sci. USA 87 (1990) 2843-2845
14. Saraiva M.J., Costa P.P., and Goodman D.S. Biochemical marker in familial amyloidotic polyneuropathy, Portuguese type. Family studies on the transthyretin (prealbumin)-methionine-30 variant. J. Clin. Invest. 76 (1985) 2171-2177
15. Jacobson D.R., Pastore R.D., Yaghoubian R., Kane I., Gallo G., Buck F.S., and Buxbaum J.N. Variant-sequence transthyretin (isoleucine 122) in late-onset cardiac amyloidosis in black Americans. N. Engl. J. Med. 336 (1997) 466-773
16. Benson M.D. Leptomeningeal amyloid and variant transthyretins. Am. J. Pathol. 148 (1996) 351-354
17. Ikeda S. Clinical picture and outcome of transthyretin-related familial amyloid polyneuropathy (FAP) in Japanese patients. Clin. Chem. Lab. Med. 40 (2002) 1257-1261
18. Buxbaum J.N., and Tagoe C.E. The genetics of the amyloidoses. Annu. Rev. Med. 51 (2000) 543-569
19. Saraiva M.J. Transthyretin mutations in health and disease. Hum. Mutat. 5 (1995) 191-196
20. Sekijima Y., Wiseman R.L., Matteson J., Hammarstrom P., Miller S.R., Sawkar A.R., et al. The biological and chemical basis for tissue-selective amyloid disease. Cell 121 (2005) 73-85
21. Hammarstrom P., Sekijima Y., White J.T., Wiseman R.L., Lim A., Costello C.E., et al. D18G transthyretin is monomeric, aggregation prone, and not detectable in plasma and cerebrospinal fluid: a prescription for central nervous system amyloidosis?. Biochemistry 42 (2003) 6656-6663
22. Sekijima Y., Hammarstrom P., Matsumura M., Shimizu Y., Iwata M., Tokuda T., et al. Energetic characteristics of the new transthyretin variant A25T may explain its atypical central nervous system pathology. Lab. Invest. 83 (2003) 409-417
23. Wojtczak A., Cody V., Luft J.R., and Pangborn W. Structures of human transthyretin complexed with thyroxine at 2.0 A resolution and 3′,5′-dinitro-N-acetyl-l-thyronine at 2.2 A resolution. Acta Crystallogr. Sect. D 52 (1996) 758-765
24. Hornberg A., Eneqvist T., Olofsson A., Lundgren E., and Sauer-Eriksson A.E. A comparative analysis of 23 structures of the amyloidogenic protein transthyretin. J. Mol. Biol. 302 (2000) 649-669
25. Chung C.M., Connors L.H., Benson M.D., and Walsh M.T. Biophysical analysis of normal transthyretin: implications for fibril formation in senile systemic amyloidosis. Amyloid 8 (2001) 75-83
26. Ferrao-Gonzales A.D., Palmieri L., Valory M., Silva J.L., Lashuel H., Kelly J.W., and Foguel D. 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 (2003) 963-974
27. Ferrao-Gonzales A.D., Souto S.O., Silva J.L., and Foguel D. The preaggregated state of an amyloidogenic protein: hydrostatic pressure converts native transthyretin into the amyloidogenic state. Proc. Natl Acad. Sci. USA 97 (2000) 6445-6450
28. Lai Z., Colon W., and Kelly J.W. The acid-mediated denaturation pathway of transthyretin yields a conformational intermediate that can self-assemble into amyloid. Biochemistry 35 (1996) 6470-6482
29. Foss T.R., Wiseman R.L., and Kelly J.W. The pathway by which the tetrameric protein transthyretin dissociates. Biochemistry 44 (2005) 15525-15533
30. Lashuel H.A., Lai Z., and Kelly J.W. Characterization of the transthyretin acid denaturation pathways by analytical ultracentrifugation: implications for wild-type, V30M, and L55P amyloid fibril formation. Biochemistry 37 (1998) 17851-17864
31. Wiseman R.L., Johnson S.M., Kelker M.S., Foss T., Wilson I.A., and Kelly J.W. Kinetic stabilization of an oligomeric protein by a single ligand binding event. J. Am. Chem. Soc. 127 (2005) 5540-5551
32. Hammarstrom P., Wiseman R.L., Powers E.T., and Kelly J.W. Prevention of transthyretin amyloid disease by changing protein misfolding energetics. Science 299 (2003) 713-716
33. Wiseman R.L., Green N.S., and Kelly J.W. Kinetic stabilization of an oligomeric protein under physiological conditions demonstrated by a lack of subunit exchange: implications for transthyretin amyloidosis. Biochemistry 44 (2005) 9265-9274
34. McCammon M.G., Scott D.J., Keetch C.A., Greene L.H., Purkey H.E., Petrassi H.M., et al. Screening transthyretin amyloid fibril inhibitors: characterization of novel multiprotein, multiligand complexes by mass spectrometry. Structure 10 (2002) 851-863
35. Foss T.R., Kelker M.S., Wiseman R.L., Wilson I.A., and Kelly J.W. Kinetic stabilization of the native state by protein engineering: implications for inhibition of transthyretin amyloidogenesis. J. Mol. Biol. 347 (2005) 841-854
36. Hamilton J.A., Steinrauf L.K., Braden B.C., Liepnieks J., Benson M.D., Holmgren G., et al. The X-ray crystal structure refinements of normal human transthyretin and the amyloidogenic Val-30 → Met variant to 1.7-A resolution. J. Biol. Chem. 268 (1993) 2416-2424
37. Pasquato N., Berni R., Folli C., Alfieri B., Cendron L., and Zanotti G. Acidic pH-induced conformational changes in amyloidogenic mutant transthyretin. J. Mol. Biol. 366 (2007) 711-719
38. Peterson S.A., Klabunde T., Lashuel H.A., Purkey H., Sacchettini J.C., and Kelly J.W. Inhibiting transthyretin conformational changes that lead to amyloid fibril formation. Proc. Natl Acad. Sci. USA 95 (1998) 12956-12960
39. Reddy V., Swanson S.M., Segelke B., Kantardjieff K.A., Sacchettini J.C., and Rupp B. Effective electron-density map improvement and structure validation on a Linux multi-CPU web cluster: The TB Structural Genomics Consortium Bias Removal Web Service. Acta Crystallogr. Sect. D 59 (2003) 2200-2210
40. McRee D.E. XtalView/Xfit-a versatile program for manipulating atomic coordinates and electron density. J. Struct. Biol. 125 (1999) 156-165
41. Merritt E.A., and Murphy M.E. Raster3D version 2.0. A program for photorealistic molecular graphics. Acta Crystallogr. Sect. D 50 (1994) 869-873
42. Kabsch W. A solution for the best rotation to relate two sets of vectors. Acta Crystallogr. Sect. A 32 (1976) 922-923
43. Thurlkill R.L., Grimsley G.R., Scholtz J.M., and Pace C.N. pK values of the ionizable groups of proteins. Protein Sci. 15 (2006) 1214-1218
44. Neto-Silva R.M., Macedo-Ribeiro S., Pereira P.J., Coll M., Saraiva M.J., and Damas A.M. X-ray crystallographic studies of two transthyretin variants: further insights into amyloidogenesis. Acta Crystallogr. Sect. D 61 (2005) 333-339
45. Green N.S., Palaninathan S.K., Sacchettini J.C., and Kelly J.W. Synthesis and characterization of potent bivalent amyloidosis inhibitors that bind prior to transthyretin tetramerization. J. Am. Chem. Soc. 125 (2003) 13404-13414
46. Hamilton J.A., Steinrauf L.K., Braden B.C., Murrell J.R., and Benson M.D. Structural changes in transthyretin produced by the Ile84Ser mutation which result in decreased affinity for retinol-binding protein. Amyloid 3 (1996) 1-12
47. Hou X., Aguilar M.I., and Small D.H. Transthyretin and familial amyloidotic polyneuropathy. Recent progress in understanding the molecular mechanism of neurodegeneration. FEBS J. 274 (2007) 1637-1650
48. 1H-NMR structural studies of a cystine-linked peptide containing residues 71-93 of transthyretin and effects of a Ser84 substitution implicated in familial amyloidotic polyneuropathy. Eur. J. Biochem. 262 (1999) 586-594
49. Hammarstrom P., Jiang X., Hurshman A.R., Powers E.T., and Kelly J.W. Sequence-dependent denaturation energetics: a major determinant in amyloid disease diversity. Proc. Natl Acad. Sci. USA 99 (2002) 16427-16432
50. Yang M., Lei M., and Huo S. Why is Leu55 → Pro55 transthyretin variant the most amyloidogenic: insights from molecular dynamics simulations of transthyretin monomers. Protein Sci. 12 (2003) 1222-1231
51. Redondo C., Damas A.M., Olofsson A., Lundgren E., and Saraiva M.J. Search for intermediate structures in transthyretin fibrillogenesis: soluble tetrameric Tyr78Phe TTR expresses a specific epitope present only in amyloid fibrils. J. Mol. Biol. 304 (2000) 461-470
52. Magy N., Liepnieks J.J., Gil H., Kantelip B., Dupond J.L., Kluve-Beckerman B., and Benson M.D. A transthyretin mutation (Tyr78Phe) associated with peripheral neuropathy, carpal tunnel syndrome and skin amyloidosis. Amyloid 10 (2003) 29-33
53. Laskowski R.A., MacArthur M.W., Moss D.S., and Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26 (1993) 283-291
54. Otwinowski Z.M.W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
55. Kissinger C.R., Gehlhaar D.K., and Fogel D.B. Rapid automated molecular replacement by evolutionary search. Acta Crystallogr. Sect. D 55 (1999) 484-491
56. Storoni L.C., McCoy A.J., and Read R.J. Likelihood-enhanced fast rotation functions. Acta Crystallogr. Sect. D 60 (2004) 432-438
57. Collaborative Computational Project, Number 4*. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. Sect. D 50 (1994) 760-763
58. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., and Ferrin T.E. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25 (2004) 1605-1612