Evolutionary changes to transthyretin: Structure-function relationships

FEBS Journal

Volumn 276, Issue 19, 2009, Pages 5330-5341

  Prapunpoj, P ^a   Leelawatwattana, L ^a  

^a PRINCE OF SONGKLA UNIVERSITY   (Thailand)

Author keywords

Binding affinity; Evolution; Function; Plasma protein; Protease; Retinol binding protein; Splicing; Structure; Thyroid hormone; Transthyretin

Indexed keywords

PREALBUMIN; PROTEINASE; RETINOL; RETINOL BINDING PROTEIN;

AMINO TERMINAL SEQUENCE; AMYLOIDOSIS; APOPTOSIS; HUMAN; MOLECULAR EVOLUTION; MOLECULAR MECHANICS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN BLOOD LEVEL; PROTEIN CEREBROSPINAL FLUID LEVEL; PROTEIN FUNCTION; SHORT SURVEY; VERTEBRATE; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; BASE SEQUENCE; DNA; EVOLUTION, MOLECULAR; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; PREALBUMIN; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; SEQUENCE HOMOLOGY, AMINO ACID; SEQUENCE HOMOLOGY, NUCLEIC ACID; THYROID HORMONES; VITAMIN A;

MUS; VERTEBRATA;

EID: 70349260510     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07243.x     Document Type: Short Survey

References (97)

1. Kabat EA, Moore DH Landow H (1942) An electrophoretic study of the protein components in cerebrospinal fluid and their relationship to the serum proteins. J Clin Invest 21, 571 577.
2. Siebert FB Nielson JW (1942) Electrophoresis study of the blood protein response in tuberculosis. J Biol Chem 143, 29 38.
3. Miller JB (1963) Pre-albumin variations in primates. Nature 200, 810.
4. Larsson M, Pettersson T Carlström A (1985) Thyroid hormone binding in serum of 15 vertebrate species: isolation of thyroxine-binding globulin and prealbumin analogs. Gen Comp Endocrinol 58, 360 375.
5. Duan W, Richardson SJ, Köhrle J, Chang L, Southwell BR, Harms PJ, Brack CM, Pettersson TM Schreiber G (1995a) Binding of thyroxine to pig transthyretin, its cDNA structure, and other properties. Eur J Biochem 230, 977 986.
6. Blake CCF, Geisow MJ, Oatley SJ, Rérat B Rérat C (1978) Structure of prealbumin: secondary, tertiary and quaternary interactions determined by Fourier refinement at 1.8 Å. J Mol Biol 121, 339 356.
7. Pettersson T, Carlström A Jörnvall H (1987) Different types of microheterogeneity of human thyroxine-binding prealbumin. Biochem 26, 4572 4583.
8. Sekijima Y, Tokuda T, Kametani F, Tanaka K, Maruyama K Ikeda S (2001) Serum transthyretin monomer in patients with familial amyloid polyneuropathy. Amyloid 8, 257 262.
9. Branch WT, Robbins J Edelhoch H (1972) Thyroxine binding prealbumin. Conformation in urea and guanidine. Arch Biochem Biophys 152, 144 151.
10. Taylor BA, Bailey DW, Cherry M, Riblet R Weigert M (1975) Genes for immunoglobulin heavy chain and serum prealbumin protein are linked in mouse. Nature 256, 644 646.
11. Bhat MK, Ashizawa K Cheng SY (1977) Heterogeneity of chicken prealbumin and specificity in binding to chicken retinol-binding protein and L-thyroxine. Indian J Biochem Biophys 14, 125 128.
12. Harms PJ, Tu GF, Richardson SJ, Aldred AR, Jaworowski A Schreiber G (1991) Transthyretin (prealbumin) gene expression in choroid plexus is strongly conserved during evolution of vertebrates. Comp Biochem Physiol B 99, 239 249.
13. Kopelman M, Cogan U, Mokady S Shinitzky M (1976) The interaction between retinol-binding proteins and prealbumins studied by fluorescence polarization. Biochim Biophys Acta 439, 449 460.
14. Terazaki H, Ando Y, Suhr O, Ohlsson PI, Obayashi K, Yamashita T, Yoshimatsu S, Suga M, Uchino M Ando M (1998) Post-translational modification of transthyretin in plasma. Biochem Biophys Res Commun 249, 26 30.
15. Aldred AR, Prapunpoj P Schreiber G (1997) Evolution of shorter and more hydrophilic transthyretin N-termini by stepwise conversion of exon 2 into intron 1 sequences (shifting the 39 splice site of intron 1). Eur J Biochem 246, 401 409.
16. Prapunpoj P, Richardson SJ Schreiber G (2002) Crocodile transthyretin: structure, function, and evolution. Am J Physiol Regul Integr Comp Physiol 283, R885 R896.
17. Prapunpoj P, Leelawatwatana L, Schreiber G Richardson SJ (2006) Change in structure of the N-terminal region of transthyretin produces change in affinity of transthyretin to T4 and T3. FEBS J 273, 4013 4023.
18. Liz MA, Faro CJ, Saraiva MJ Sousa MM (2004) Transthyretin, a new cryptic protease. J Biol Chem 279, 21431 21438.
19. Blake CCF, Swan ID, Rérat C, Berthou J, Laurent A Rérat B (1971) An X-ray study of the subunit structure of prealbumin. J Mol Biol 61, 217 224.
20. Ghosh M, Meerts IATM, Cook A, Bergman A, Brouwer A Johnson LN (2000) Structure of human transthyretin complexed with bromophenols: a new mode of binding. Acta Crystallogr 56, 1085 1095.
21. Blake CCF, Geisow MJ, Swan ID, Rérat C Rérat B (1974) Structure of human plasma prealbumin at 2.5 Å resolution. A preliminary report on the polypeptide chain conformation, quaternary structure and thyroxine binding. J Mol Biol 88, 1 12.
22. Blake CC Oatley SJ (1977) Protein-DNA and protein-hormone interactions in prealbumin: a model of the thyroid hormone nuclear receptor? Nature 268, 115 120.
23. Hamilton JA, Steinrauf LK, Braden BC, Liepnieks JJ, Benson MD, Holmgren G, Sandgren O Steen L (1993) The X-ray crystal structure refinements of normal human transthyretin and the amyloidogenic Val30→ Met variant to 1.7 Å resolution. J Biol Chem 268, 2416 2424.
24. Wojtczak A, Cody V, Luft JR Paugborn W (1996) Structure of human transthyretin complexed with thyroxine at 2.0 Å resolution and 3′, 5′-dinitro-N-acetyl-L-thyronine at 2.2 Å resolution. Acta Crystallogr 52, 758 765.
25. Pages RA, Robbins J Edelhoch H (1973) Binding of thyroxine and thyroxine analogs to human serum prealbumin. Biochemistry 12, 2773 2779.
26. Nilsson SF, Rask L Peterson PA (1975) Studies on thyroid hormone-binding proteins. J Biol Chem 250, 8554 8563.
27. Neumann P, Cody V Wojtczak A (2001) Structural basis of negative cooperativity in transthyretin. Acta Biochim Pol 48, 867 875.
28. Hamilton JA Benson MD (2001) Transthyretin: a review from a structural perpective. Cell Mol Life Sci 58, 1491 1521.
29. Wojtczak A (1997) Crystal structure of rat transthyretin at 2.5 Å resolution: first report on a unique tetrameric structure. Acta Biochim Pol 44, 505 518.
30. Reixach N, Foss TR, Santelli E, Pascual J, Kelly JW Buxbaum JN (2008) Human-murine transthyretin heterotetramers are kinetically stable and non-amyloidogenic: a lesson in the generation of transgenic models of diseases involving oligomeric proteins. J Biol Chem 283, 2098 2107.
31. Sunde M, Richardson SJ, Chang L, Pettersson TM, Schreiber G Blake CCF (1996) The crystal structure of transthyretin from chicken. Eur J Biochem 236, 491 499.
32. Eneqvist T, Lundberg E, Nilsson L, Abagyan R Sauer-Eriksson AE (2004) The transthyretin-related protein faminly. Eur J Biochem 270, 518 532.
33. Folli C, Pasquato N, Ramazzina I, Battistutta R, Zanotti G Berni R (2003) Distinctive binding and structural properties of piscine transthyretin. FEBS Lett 555, 279 284.
34. Achen MG, Duan W, Pettersson TM, Harms PJ, Richardson SJ, Lawrence MC, Wettenhall REH, Aldred AR Schreiber G (1993) Transthyretin gene expression in choroid plexus first evolved in reptiles. Am J Physiol Regul Integr Comp Physiol 265, R982 R989.
35. Yamauchi K, Takeuchi H, Overall M, Dziadek M, Munro SLA Schreiber G (1998) Structural characteristics of bullfrog (Rana catesbeiana) transthyretin and its cDNA: comparison of its pattern of expression during metamorphosis with that of lipocalin. Eur J Biochem 256, 287 296.
36. Blake CCF (1981) Prealbumin and the thyroid hormone nuclear receptor. Proc R Soc Lond B Biol Sci 211, 413 431.
37. Chang L, Munro SLA, Richardson SJ Schreiber G (1999) Evolution of thyroid hormone binding by transthyretins in birds and mammals. Eur J Biochem 259, 534 542.
38. Prapunpoj P, Richardson SJ, Fumagalli L Schreiber G (2000a) The evolution of the thyroid hormone distributor protein transthyretin in the order Insectivora, class Mammalia. Mol Biol Evol 17, 199 1209.
39. Prapunpoj P, Yamauchi K, Nishiyama N, Richardson SJ Schreiber G (2000b) Evolution of structure, ontogeny of gene expression, and function of Xenopus laevis transthyretin. Am J Physiol Regul Integr Comp Physiol 279, R2026 R2041.
40. Manzon RG, Neuls TM Manzon LA (2007) Molecular cloning, tissue distribution, and developmental expression of lamprey transthyretins. Gen Comp Endocrinol 151, 55 65.
41. Robbins J, Cheng SY, Gershengorn MC, Glinoer D, Cahnmann HJ Edelnoch H (1978) Thyroxine transport proteins of plasma. Molecular properties and biosynthesis. Recent Prog Horm Res 34, 477 519.
42. Richardson SJ, Aldred AR, Leng SL, Renfree MB, Hulbert AJ Schreiber G (2002) Developmental profile of thyroid hormone distributor proteins in a marsupial, the tammar wallaby Macropus eugenii. Gen Comp Endocrinol 125, 92 103.
43. Richardson SJ, Bradley AJ, Duan W, Wettenhall REH, Harms PJ, Babon JJ, Southwell BR, Nicol S, Donnellan SC Schreiber G (1994) Evolution of marsupial and other vertebrate thyroxine-binding plasma proteins. Am J Physiol Regul Integr Comp Physiol 266, R1359 R1360.
44. Richardson SJ, Hennebry SC, Smith BJ Wright HM (2005) Evolution of the thyroid hormone distributor protein transthyretin in microbes, C. elegans, and vertebrates. Ann N Y Acad Sci 1040, 448 451.
45. Santos CR Power DM (1999) Identification of transthyretin in fish (Sparus aurata): cDNA cloning and characterisation. Endocrinology 140, 2430 2433.
46. Funkenstein B, Perrot V Brown CL (1999) Cloning of putative piscine (Sparus aurata) transthyretin: developmental expression and tissue distribution. Mol Cell Endocrinol 157, 67 73.
47. Yamauchi K, Nakajima J, Hayashi H Hara A (1999) Purification and characterization of thyroid-hormone-binding protein from masu salmon serum: A homolog of higher-vertebrate transthyretin. Eur J Biochem 265, 944 949.
48. Dickson PW, Aldred AR, Marley PD, Bannister D Schreiber G (1986) Rat choroids plexus specializes in the synthesis and the secretion of transthyretin (prealbumin)-regulation of transthyretin synthesis in choroid plexus is independent from that in liver. J Biol Chem 261, 3475 3478.
49. Tsykin A Schreiber G (1993) Sheep thyroxine-binding globulin: cDNA sequence and expression. Mol Cell Endocrinol 98, 91 97.
50. Reiber H (2001) Dynamics of brain-derived proteins in cerebrospinal fluid. Clin Chim Acta 310, 173 186.
51. Stauder AJ, Dickson PW, Aldred AR, Schreiber G, Mendelsohn FAO Hudson P (1986) Synthesis of transthyretin (prealbumin) mRNA in choroids plexus epithelial cells, localized by in situ hybridization in the rat brain. J Histochem Cytochem 34, 949 952.
52. Schreiber G, Aldred AR, Jaworowski A, Nilsson C, Achen MG Segal MB (1990) Thyroxine transport from blood to brain via transthyretin synthesis in choroid plexus. Am J Physiol 258, R338 R345.
53. Southwell BR, Duan W, Alcorn D, Brack C, Richardson SJ, Köhrle J Schreiber G (1993) Thyroxine transport to the brain: role of protein synthesis by the choroids plexus. Endocrinology 133, 2116 2126.
54. Richardson SJ, Lemkine GF, Alfama G, Hassani Z Demeneix BA (2007) Cell division and apoptosis in the adult neural stem cell niche are differentially affected in transthyretin null mice. Neurosci Lett 421, 234 238.
55. Morgado I, Melo EP, Lundberg E, Estrela NL, Sauer-Eriksson AE Power DM (2008) Hormone affinity and fibril formation of piscine transthyretin: the role of the N-terminal. Mol Cell Endocrinol 295, 48 58.
56. Ronne H, Ocklind C, Wiman K, Rask L, Obrink B Peterson PA (1983) Ligand-dependent regulation of intracellular protein transport: effect of vitamin A on the secretion of the retinol-binding protein. J Cell Biol 96, 907 910.
57. van Jaarsveld PP, Edelhoch H, Goodman DS Robbins J (1973) The interaction of human plasma retinol-binding protein and prealbumin. J Biol Chem 248, 4698 4705.
58. Berni R, Stoppini M, Zapponi MC, Meloni ML, Monaco HL Zanotti G (1990) The bovine plasma retinol-binding protein. Amino acid sequence, interaction with transthyretin, crystallization and preliminay X-ray data. Eur J Biochem 192, 507 513.
59. Noy N, Slosberg E Scarlata S (1992) Interactions of retinol with binding proteins studies retinol-binding protein and with transthyretin. Biochemistry 31, 1118 1124.
60. Kanai M, Raz A Goodman DS (1968) Retinol-binding protein: the transport protein for vitamin A in human plasma. J Clin Invest 47, 2025 2044.
61. Raz A Goodman DS (1969) The interaction of thyroxine with human plasma prealbumin and with the prealbumin-retinol-binding protein complex. J Biol Chem 244, 3230 3237.
62. Goodman DS (1974) Vitamin A transport and retinol-binding protein metabolism. Vitamin Horm 32, 167 180.
63. Yamamoto Y, Yoshizawa T, Kamio S, Aoki O, Kawamata Y, Masushige S Kato S (1997) Interactions of transthyretin (TTR) and retinol-binding protein (RBP) in the uptake of retinol by primary rat hepatocytes. Exp Cell Res 234, 373 378.
64. Monaco H, Rizzi M Coda A (1995) Structure of a complex of two plasma proteins: transthyretin and retinol-binding protein. Science 268, 1039 1041.
65. Naylor HM Newcomer ME (1999) The structure of human retinol-binding protein (RBP) with its carrier protein transthyretin reveals an interaction with the carboxy terminus of RBP. Biochemistry 38, 2647 2653.
66. Rostom AA, Sunde M, Richardson SJ, Schreiber G, Jarvis S, Bateman R, Dobson CM Robinson CV (1998) Dissection of multi-protein complexes using mass spectrometry-subunit interactions in transthyretin and retinol-binding protein complexes. Proteins 33 (Suppl 2 3 11.
67. Selkoe DJ Schenk D (2002) Alzheimer's disease: molecular understanding predicts amyloid-based therapeutics. Annu Rev Pharmacol Toxicol 43, 545 584.
68. Walsh DM Selkoe DJ (2007) Aβ oligomers-a decade of discovery. J Neurochem 101, 1172 1184.
69. Strittmatter WJ, Weisgraber KH, Huang DY, Dong LM, Salvesen GS, Pericak-Vance M, Schmechel D, Saunders AM, Goldgaber D Roses AD (1993a) Binding of human apolipoprotein E to synthetic amyloid beta peptide: isoform-specific effects and implications for late-onset Alzheimer disease. Proc Natl Acad Sci USA 90, 8089 8102.
70. Strittmatter WJ, Huang DY, Bhasin R, Roses AD Goldgaber D (1993b) Avid binding of Aβ amyloid peptide to its own precursor. Exp Neurol 122, 327 334.
71. Ghiso J, Matsubara E, Koudinov A, Choi-Miura NH, Tomita M, Wisniewski T Frangione B (1993) The cerebrospinal-fluid soluble form of Alzheimer's amyloid beta is complexed to SP-40,40 (apolipoprotein J), an inhibitor of the component membrane-attack complex. Biochem J 293, 27 30.
72. Schwarzman AL, Gregori L, Vitex MP, Lyubski S Strittmatter WJ (1994) Transthyretin sequesters amyloid beta protein and prevents amyloid formation. Proc Natl Acad Sci USA 91, 8368 8372.
73. Costa R, Gonçalves A, Saraiva MJ Cardoso I (2008) Transthyretin binding to A-Beta peptide-Impact on A-Beta fibrillogenesis and toxicity. FEBS Lett 582, 936 942.
74. Schwarzman AL Goldgaber D (1996) Interaction of transthyretin with amyloid beta-protein: binding and inhibition of amyloid formation. Ciba Found Symp 199, 146 160.
75. Schwarzman AL, Tsiper M, Wente H, Wang A, Vitek MP, Vasiliev V Goldgaber D (2004) Amyloidogenic and anti-amyloidogenic properties of recombinant transthyretin variants. Amyloid 11, 1 9.
76. Costa R, Ferreira-da-Silva F, Saraiva MJ Cardoso I (2008) Transthyretin protects against A-Beta peptide toxicity by proteolytic cleavage of the peptide: a mechanism sentitive to the Kunitz protease inhibitor. PLoS ONE 3, e2899.
77. Liz MA, Gomes CM, Saraiva MJ Sousa MM (2007) ApoA-I cleaved by transthyretin has reduced ability to promote cholesterol efflux and increased amyloidogenicity. J Lipid Res 48, 2385 2395.
78. Liz MA, Fleming CE, Nunes AF, Almeida MR, Mar FM, Choe Y, Craik CS, Powers JC, Bogyo M Sousa MM (2009) Substrate specificity of transthyretin: identification of natural substrates in the nervous system. Biochem J 419, 467 474.
79. Kato M, Kato K, Blaner WS, Chertow BS Goodman DS (1985) Plasma and cellular retinol-binding proteins and transthyretin (prealbumin) are all localized in the islets of Langerhans in the rat. Proc Natl Acad Sci USA 82, 2488 2492.
80. Jacobsson B (1989) In situ localization of transthyretin-mRNA in the adult human liver, choroid plexus and pancreatic islets and in endocrine tumors of the pancreas and gut. Histochem 91, 299 304.
81. Westermark GT Westermak P (2008) Transthyretin and amyloid in the islets of Langerhans in type-2 diabetes. Exp Diabetes Res 2008, 429274 429280.
82. Refai E, Dekki N, Yang SN, Imreh G, Cabrera O, Yu L, Yang G, Norgren S, Rössner SM, Inverardi L et al. (2005) Transthyretin constitutes a functional component in pancreatic β-cell stimulus-secretion coupling. Proc Natl Acad Sci USA 102, 17020 17025.
83. Mita S, Maeda S, Shimada K Araki S (1984) Cloning and sequence analysis of cDNA for human prealbumin. Biochem Biophys Res Commun 124, 558 564.
84. Tsuzuki T, Mita S, Maeda S, Araki S Shimada K (1985) Structure of the human prealbumin gene. J Biol Chem 260, 12224 12227.
85. Tu G-F, Cole T, Duan W Schreiber G (1989) The nucleotide sequence of transthyretin cDNA isolated from a sheep choroid plexus cDNA library. Nucleic Acids Res 17, 6384. (Pubitemid 19198608)
86. Schreiber G, Pettersson TM, Southwell BR, Aldred AR, Harms PJ, Richardson SJ, Wettenhall REH, Duan W Nicol SC (1993) Transthyretin expression evolved more recently in liver than in brain. Comp Biochem Physiol 105B, 317 325.
87. Sundelin J, Melhus H, Das S, Eriksson U, Link P, Trägargh L, Peterson PA Rask L (1985) The primary structure of rabbit and rat prealbumin and a comparison with the tertiary structure of human prealbumin. J Biol Chem 260, 6481 6487.
88. Dickson PW, Howlett GJ Schreiber G (1985) Rat transthyretin (prealbumin): molecular cloning, nucleotide sequence, and gene expression in liver and brain. J Biol Chem 260, 8214 8219.
89. Duan W, Cole T Schreiber G (1989) Cloning and nucleotide sequencing of transthyretin (prealbumin) cDNA from rat choroids plexus and liver. Nucleic Acids Res 17, 3979.
90. Fung WP, Thomas T, Dickson PW, Aldred AR, Milland J, Dziadek M, Power B, Hudson P Schreiber G (1988) Structure and expression of the rat transthyretin (prealbumin) gene. J Biol Chem 263, 480 488. (Pubitemid 18041101)
91. Wakasugi S, Maeda S, Shimada K, Nakashima H Migita S (1985) Structure comparisons between mouse and human prealbumin. J Biochem (Tokyo) 98, 1707 1714.
92. Wakasugi S, Maeda S Shimada K (1986) Structure and expression of the mouse prealbumin gene. J Biochem (Tokyo) 100, 49 58.
93. Brack CM, Duan W, Hulbert AJ Schreiber G (1995) Wallaby transthyretin. Comp Biochem Physiol 110B, 523 529.
94. Duan W, Richardson SJ, Babon JJ, Heyes RJ, Southwell BR, Harms PJ, Wettenhall REH, Dziegielewska KM, Selwood L, Bradley AJ et al. (1995b) Evolution transthyretin in marsupials. Eur J Biochem 227, 396 406.
95. Duan W, Achen MG, Richardson SJ, Lawrence MC, Wettenhall REH, Jaworowski A Schreiber G (1991) Isolation, characterization, cDNA cloning and gene expression of an avian transthyretin. Implications for the evolution of structure and function of transthyretin in vertebrates. Eur J Biochem 200, 679 687.
96. Yamauchi K, Kasahara T, Hayashi H Horiuchi R (1993) Purification and characterization of a 3,5,3′-L-triiodothyronine-specific binding protein from bullfrog tadpole plasma: a homolog of mammalian transthyretin. Endocrinology 132, 2254 2261.
97. Moore MJ, Query CC Sharp PA (1993) Splicing of precursors to mRNA by the spliceosome. In The RNA World (Gesteland RF Atkins JF eds pp. 303 357. Cold Spring Harbor Laboratory Press, Plainview, NY.