Abstract
A considerable body of evidence has been accumulated showing the interrelationship between zinc and the plasma thyroid hormone (TH) distributor protein, transthyretin (TTR). TTR is a multi-functional protein, which emerged from 5-hydroxyisourate hydrolase (HIUHase) by neo-functionalization after gene duplication during early chordate evolution. HIUHase is also a zinc-binding protein. Most biochemical and molecular biological findings have been obtained from mammalian studies. However, in the past two decades, it has become clear that fish TTR displays zinc-dependent TH binding. After a brief introduction on plasma zinc, THs and their binding proteins, this review will focus on the role of zinc in TTR functions of various vertebrates. In particular primitive fish TTR has an extremely high zinc content, with an increased number of histidine residues which are involved in TH binding. However, zinc-dependent TH binding may have been gradually lost from TTRs during higher vertebrate evolution. Although human TTR has a low zinc content, zinc plays an essential role in TTR functions other than TH binding: the stability of TTR-holo retinol binding protein 4 (holoRBP4) complex, TTR amyloidogenesis, the sequestration of amyloid β (Aβ) fibrils and cryptic proteolytic activity. The interaction of TTR with metallothioneins may be a critical step in the exertion of some of these functions. Evolutionary and physiological insights on zinc-dependent functions of TTRs are also discussed.
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Abbreviations
- Aβ:
-
Amyloid β peptide(s)
- apoA-I:
-
Apolipoprotein AI
- EDTA:
-
Ethylenediaminetetraacetic acid
- HDL:
-
High density lipoprotein
- HIUHase:
-
5-Hydroxyisourate hydrolase
- MT:
-
Metallothionein
- RBP4:
-
Retinol binding protein 4
- T3:
-
3,3′,5-Triiodothyronine
- T4:
-
Thyroxine
- TBG:
-
Thyroxine-binding globulin
- TH:
-
Thyroid hormone
- THDP:
-
TH distributor protein
- TTR:
-
Transthyretin
- ZBS:
-
Zinc binding site
References
Adlard PA, West AK, Vickers JC (1998) Increased density of metallothionein I/II-immunopositive cortical glial cells in the early stages of Alzheimer’s disease. Neurobiol Dis 5:349–356. https://doi.org/10.1006/nbdi.1998.0203
Amici A, Levine RL, Tsai L, Stadtman ER (1989) Conversion of amino acid residues in proteins and amino acid homopolymers to carbonyl derivatives by metal-catalyzed oxidation reactions. J Biol Chem 264:3341–3346
Andersson K, Olofsson A, Nielsen EH, Svehag SE, Lundgren E (2002) Only amyloidogenic intermediates of transthyretin induce apoptosis. Biochem Biophys Res Commun 294:309–314. https://doi.org/10.1016/S0006-291X(02)00465-5
Andreini C, Banci L, Bertini I, Rosato A (2006) Counting the zinc-proteins encoded in the human genome. J Proteome Res 5:196–201. https://doi.org/10.1021/pr050361j
Atrian S, Capdevila M (2013) Metallothionein-protein interactions. Biomol Concepts 4:143–160. https://doi.org/10.1515/bmc-2012-0049
Baltaci AK, Mogulkoc R, Baltaci SB (2019) Review: the role of zinc in the endocrine system. Pak J Pharm Sci 32:231–239
Barron M, McAllister D, Smith SM, Lough J (1998) Expression of retinol binding protein and transthyretin during early embryogenesis. Dev Dyn 212:413–422. https://doi.org/10.1002/(SICI)1097-0177(199807)212:3%3c413::AID-AJA9%3e3.0.CO;2-K
Bentley PJ (1991) A high-affinity zinc-binding plasma protein in channel catfish (Ictalurus punctatus). Comp Biochem Physiol C 100:491–494. https://doi.org/10.1016/0742-8413(91)90028-r
Bettger WJ, Spry DJ, Cockell KA, Cho CY, Hilton JW (1987) The distribution of zinc and copper in plasma, erythrocytes and erythrocyte membranes of rainbow trout (Salmo gairdneri). Comp Biochem Physiol C 87:445–451. https://doi.org/10.1016/0742-8413(87)90036-3
Blake CCF, Geisow MJ, Swan IDA, Rerat C, Rerat 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. https://doi.org/10.1016/0022-2836(74)90291-5
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. https://doi.org/10.1016/0022-2836(78)90368-6
Bloxam DL, Tan JC, Parkinson CE (1984) Non-protein bound zinc concentration in human plasma and amniotic fluid measured by ultrafiltration. Clin Chim Acta 144:81–93. https://doi.org/10.1016/0009-8981(84)90041-X
Brandão-Neto J, Madureira G, Mendonça BB, Bloise W, Castro AV (1995) Endocrine interaction between zinc and prolactin. An interpretative review. Biol Trace Elem Res 49:139–149. https://doi.org/10.1007/BF02788963
Castro-Rodrigues AF, Gales L, Saraiva MJ, Damas AM (2011) Structural insights into a zinc-dependent pathway leading to Leu55Pro transthyretin amyloid fibrils. Acta Crystallogr D Biol Crystallogr 67(Pt 12):1035–1044. https://doi.org/10.1107/S090744491104491X
Cort T, Masuoka J, Lance VA, Saltman P (1995) Plasma zinc concentrations in snakes and other vertebrates correlate with specific zinc-binding plasma proteins. J Zool Lond 236:513–520. https://doi.org/10.1111/j.1469-7998.1995.tb02728.x
Costa R, Ferreira-da-Silva F, Saraiva MJ, Cardoso I (2008a) Transthyretin protects against A-β peptide toxicity by proteolytic cleavage of the peptide: a mechanism sensitive to the Kunitz protease inhibitor. PLoS ONE 3:e2899. https://doi.org/10.1371/journal.pone.0002899
Costa R, Gonçalves A, Saraiva MJ, Cardoso I (2008b) Transthyretin binding to A-β peptide–impact on A-β fibrillogenesis and toxicity. FEBS Lett 582:936–942. https://doi.org/10.1016/j.febslet.2008.02.034
Du J, Cho PY, Yang DT, Murphy RM (2012) Identification of β-amyloid-binding sites on transthyretin. Protein Eng Des Sel 25:337–345. https://doi.org/10.1093/protein/gzs026
Dyke B, Hegenauer J, Saltman P, Laurs RM (1987) Isolation and characterization of a new zinc-binding protein from albacore tuna plasma. Biochemistry 26:3228–3234. https://doi.org/10.1021/bi00385a044
Eneqvist T, Lundberg E, Nilsson L, Abagyan R, Sauer-Eriksson AE (2003) The transthyretin-related protein family. Eur J Biochem 270:518–532. https://doi.org/10.1046/j.1432-1033.2003.03408.x
Ernström U, Pettersson T, Jörnvall H (1995) A yellow component associated with human transthyretin has properties like a pterin derivative, 7,8-dihydropterin-6-carboxaldehyde. FEBS Lett 360:177–182. https://doi.org/10.1016/0014-5793(95)00095-q
Fleming CE, Saraiva MJ, Sousa MM (2007) Transthyretin enhances nerve regeneration. J Neurochem 103:831–839. https://doi.org/10.1111/j.1471-4159.2007.04828.x
Fleming CE, Nunes AF, Sousa MM (2009) Transthyretin: more than meets the eye. Prog Neurobiol 89:266–276. https://doi.org/10.1016/j.pneurobio.2009.07.007
Fletcher PE, Fletcher GL (1978) The binding of zinc to the plasma of winter flounder (Pseudopleuronectes americanus): affinity and specificity. Can J Zool 56:114–120. https://doi.org/10.1139/z78-016
Fletcher PE, Fletcher GL (1980) Zinc- and copper-binding proteins in the plasma of winter flounder (Pseudopleuronectes americanus). Can J Zool 58:609–613. https://doi.org/10.1139/z80-086
Fletcher GL, Watts EG, King MJ (1975) Copper, zinc, and total protein levels in the plasma of sockeye salmon (Oncorhynchus nerka) during their spawning migration. J Fish Res Bd Can 32:78–82. https://doi.org/10.1139/f75-012
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. https://doi.org/10.1016/s0014-5793(03)01248-1
Fukada T, Yamasaki S, Nishida K, Murakami M, Hirano T (2011) Zinc homeostasis and signaling in health and diseases: zinc signaling. J Biol Inorg Chem 16:1123–1134. https://doi.org/10.1007/s00775-011-0797-4
Gonçalves I, Quintela T, Baltazar G, Almeida MR, Saraiva MJ, Santos CR (2008) Transthyretin interacts with metallothionein 2. Biochemistry 47:2244–2251. https://doi.org/10.1021/bi7016377
Hamilton JA, Steinrauf LK, Braden BC, Liepnieks J, Benson MD, Holmgren G, Sandgren O, Steen L (1993) The X-ray crystal structure refinements of normal human transthyretin and the amyloidogenic Val-30→Met variant to 1.7-Å resolution. J Biol Chem 268:2416–2424
Hennebry SC, Law RH, Richardson SJ, Buckle AM, Whisstock JC (2006a) The crystal structure of the transthyretin-like protein from Salmonella dublin, a prokaryote 5-hydroxyisourate hydrolase. J Mol Biol 359:1389–1399. https://doi.org/10.1016/j.jmb.2006.04.057
Hennebry SC, Wright HM, Likic VA, Richardson SJ (2006b) Structural and functional evolution of transthyretin and transthyretin-like proteins. Proteins 64:1024–1045. https://doi.org/10.1002/prot.21033
Henze A, Homann T, Serteser M, Can O, Sezgin O, Coskun A, Unsal I, Schweigert FJ, Ozpinar A (2015) Post-translational modifications of transthyretin affect the triiodonine-binding potential. J Cell Mol Med 19:359–370. https://doi.org/10.1111/jcmm.12446
Huang X, Atwood CS, Moir RD, Hartshorn MA, Vonsattel JP, Tanzi RE, Bush AI (1997) Zinc-induced Alzheimer’s Aβ1-40 aggregation is mediated by conformational factors. J Biol Chem 272:26464–26470. https://doi.org/10.1074/jbc.272.42.26464
Hyung SJ, Deroo S, Robinson CV (2010) Retinol and retinol-binding protein stabilize transthyretin via formation of retinol transport complex. ACS Chem Biol 5:1137–1146. https://doi.org/10.1021/cb100144v
Ingbar SH (1958) Pre-albumin: a thyroxine-binding protein of human plasma. Endocrinology 63:256–259. https://doi.org/10.1210/endo-63-2-256
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. https://doi.org/10.1172/JCI101335
Kasai K, Nishiyama N, Yamauchi K (2018) Molecular and thyroid hormone binding properties of lamprey transthyretins: the role of an N-terminal histidine-rich segment in hormone binding with high affinity. Mol Cell Endocrinol 474:74–88. https://doi.org/10.1016/j.mce.2018.02.012
King JC, Shames DM, Woodhouse LR (2000) Zinc homeostasis in humans. J Nutr 130(5S Suppl):1360S-1366S. https://doi.org/10.1093/jn/130.5.1360S
Lance VA, Joanen T, McNease L (1983) Selenium, vitamin E, and trace elements in the plasma of wild and farm-reared alligators during the reproductive cycle. Can J Zool 61:1744–1751. https://doi.org/10.1139/z83-225
Lance VA, Cort T, Masuoka J, Lawson R, Saltman P (1995) Unusually high zinc concentrations in snake plasma, with observations on plasma zinc concentrations in lizards, turtles and alligators. J Zool Lond 235:577–585. https://doi.org/10.1111/j.1469-7998.1995.tb01769.x
Liz MA, Faro CJ, Saraiva MJ, Sousa MM (2004) Transthyretin, a new cryptic protease. J Biol Chem 279:21431–21438. https://doi.org/10.1074/jbc.M402212200
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. https://doi.org/10.1194/jlr.M700158-JLR200
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. https://doi.org/10.1042/BJ20082090
Liz MA, Leite SC, Juliano L, Saraiva MJ, Damas AM, Bur D, Sousa MM (2012) Transthyretin is a metallopeptidase with an inducible active site. Biochem J 443:769–778. https://doi.org/10.1042/BJ20111690
Lundberg E, Bäckström S, Sauer UH, Sauer-Eriksson AE (2006) The transthyretin-related protein: structural investigation of a novel protein family. J Struct Biol 155:445–457. https://doi.org/10.1016/j.jsb.2006.04.002
Malpeli G, Folli C, Berni R (1996) Retinoid binding to retinol-binding protein and the interference with the interaction with transthyretin. Biochim Biophys Acta 1294:48–54. https://doi.org/10.1016/0167-4838(95)00264-2
Mangrolia P, Yang DT, Murphy RM (2016) Transthyretin variants with improved inhibition of β-amyloid aggregation. Protein Eng Des Sel 29:209–218. https://doi.org/10.1093/protein/gzw008
Maret W (2017) Zinc in cellular regulation: the nature and significance of “zinc signals.” Int J Mol Sci 8:2285. https://doi.org/10.3390/ijms18112285
Martinho A, Gonçalves I, Cardoso I, Almeida MR, Quintela T, Saraiva MJ, Santos CRA (2010) Human metallothioneins 2 and 3 differentially affect amyloid-β binding by transthyretin. FEBS J 277:3427–3436. https://doi.org/10.1111/j.1742-4658.2010.07749.x
Masuoka J, Hegenauer J, Van Dyke BR, Saltman P (1993) Intrinsic stoichiometric equilibrium constants for the binding of zinc(II) and copper(II) to the high affinity site of serum albumin. J Biol Chem 268:21533–21537
McCammon MG, Scott DJ, Keetch CA, Greene LH, Purkey HE, Petrassi HM, Kelly JW, Robinson CV (2002) Screening transthyretin amyloid fibril inhibitors: characterization of novel multiprotein, multiligand complexes by mass spectrometry. Structure 10:851–863. https://doi.org/10.1016/s0969-2126(02)00771-2
Miroy GJ, Lai Z, Lashuel HA, Peterson SA, Strang C, Kelly JW (1996) Inhibiting transthyretin amyloid fibril formation via protein stabilization. Proc Natl Acad Sci USA 93:15051–15056. https://doi.org/10.1073/pnas.93.26.15051
Monaco HL (2000) The transthyretin-retinol-binding protein complex. Biochim Biophys Acta 1482:65–72. https://doi.org/10.1016/s0167-4838(00)00140-0
Monaco HL, Rizzi M, Coda A (1995) Structure of a complex of two plasma proteins: transthyretin and retinol-binding protein. Science 268:1039–1041. https://doi.org/10.1126/science
Montorzi M, Falchuk KH, Vallee BL (1995) Vitellogenin and lipovitellin: zinc proteins of Xenopus laevis oocytes. Biochemistry 34:10851–10858. https://doi.org/10.1021/bi00034a018
Muñoz EC, Rosado JL, López P, Furr HC, Allen LH (2000) Iron and zinc supplementation improves indicators of vitamin A status of Mexican preschoolers. Am J Clin Nutr 71:789–794. https://doi.org/10.1093/ajcn/71.3.789
Nakamura O, Suzuki R, Asai K, Kaji H, Kaneko T, Takahashi Y, Takahagi A, Tsutsui S (2020) Transport of maternal transthyretin to the fetus in the viviparous teleost Neoditrema ransonnetii (Perciformes, Embiotocidae). J Comp Physiol B 190:231–241. https://doi.org/10.1007/s00360-020-01261-w
Nunes AF, Saraiva MJ, Sousa MM (2006) Transthyretin knockouts are a new mouse model for increased neuropeptide Y. FASEB J 20:166–168. https://doi.org/10.1096/fj.05-4106fje
Palmieri Lde C, Lima LM, Freire JB, Bleicher L, Polikarpov I, Almeida FCL, Foguel D (2010) Novel Zn2+-binding sites in human transthyretin: implications for amyloidogenesis and retinol-binding protein recognition. J Biol Chem 285:31731–31741. https://doi.org/10.1074/jbc.M110.157206
Pettersson T, Ernström U, Griffiths W, Sjövall J, Bergman T, Jörnvall H (1995) Lutein associated with a transthyretin indicates carotenoid derivation and novel multiplicity of transthyretin ligands. FEBS Lett 365:23–26. https://doi.org/10.1016/0014-5793(95)00389-q
Poltash ML, Shirzadeh M, McCabe JW, Moghadamchargari Z, Laganowsky A, Russell DH (2019) New insights into the metal-induced oxidative degradation pathways of transthyretin. Chem Commun (Camb) 55:4091–4094. https://doi.org/10.1039/c9cc00682f
Quintas A, Saraiva MJ, Brito RM (1999) The tetrameric protein transthyretin dissociates to a non-native monomer in solution. A novel model for amyloidogenesis. J Biol Chem 274:32943–32949. https://doi.org/10.1074/jbc.274.46.32943
Quintas A, Vaz DC, Cardoso I, Saraiva MJ, Brito RM (2001) Tetramer dissociation and monomer partial unfolding precedes protofibril formation in amyloidogenic transthyretin variants. J Biol Chem 276:27207–27213. https://doi.org/10.1074/jbc.M101024200
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
Refai E, Dekki N, Yang SN, Imreh G, Cabrera O, Yu L, Yang G, Norgren S, Rössner SM, Inverardi L, Ricordi C, Olivecrona G, Andersson M, Jörnvall H, Berggren PO, Juntti-Berggren L (2005) Transthyretin constitutes a functional component in pancreatic β-cell stimulus-secretion coupling. Proc Natl Acad Sci USA 102:17020–17025. https://doi.org/10.1073/pnas.0503219102
Richardson SJ (2007) Cell and molecular biology of transthyretin and thyroid hormones. Int Rev Cytol 258:137–193. https://doi.org/10.1016/S0074-7696(07)58003-4
Robbins J (2000) Thyroid hormone transport proteins and the physiology of hormone binding. In: Braverman LE, Utiger RD (eds) The thyroid—a fundamental and clinical text, 8th edn. Lippincott Williams & Wilkins, Philadelphia, pp 105–120
Savage JE (1968) Trace minerals and avian reproduction. Fed Proc Am Soc Exp Biol 27:927–931
Schreiber G, Richardson SJ (1997) The evolution of gene expression, structure and function of transthyretin. Comp Biochem Physiol B Biochem Mol Biol 116:137–160. https://doi.org/10.1016/s0305-0491(96)00212-x
Schwarzman AL, Gregori L, Vitek MP, Lyubski S, Strittmatter WJ, Enghilde JJ, Bhasin R, Silverman J, Weisgraber KH, Coyle PK, Zagorski MG, Talafous J, Eisenberg M, Saunders AM, Roses AD, Goldgaber D (1994) Transthyretin sequesters amyloid β protein and prevents amyloid formation. Proc Natl Acad Sci USA 91:8368–8372. https://doi.org/10.1073/pnas.91.18.8368
Scott BJ, Bradwell AR (1983) Identification of the serum binding proteins for iron, zinc, cadmium, nickel, and calcium. Clin Chem 29:629–633. https://doi.org/10.1093/clinchem/29.4.629
Seibert FB, Nelson JW (1942) Electrophoretic study of the blood protein response in tuberculosis. J Biol Chem 143:29–38
Sekijima Y, Kelly JW, Ikeda S (2008) Pathogenesis of and therapeutic strategies to ameliorate the transthyretin amyloidoses. Curr Pharm Des 14:3219–3230. https://doi.org/10.2174/138161208786404155
Shidoji Y, Muto Y (1977) Vitamin A transport in plasma of the non-mammalian vertebrates: isolation and partial characterization of piscine retinol-binding protein. J Lipid Res 18:679–691
Stadtman ER, Levine RL (2003) Free radical-mediated oxidation of free amino acids and amino acid residues in proteins. Amino Acids 25:207–218. https://doi.org/10.1007/s00726-003-0011-2
Sturrock AM, Hunter E, Milton JA, Trueman CN (2013) Analysis methods and reference concentrations of 12 minor and trace elements in fish blood plasma. J Trace Elem Med Biol 27:273–285. https://doi.org/10.1016/j.jtemb.2013.03.001
Susuki S, Ando Y, Sato T, Nishiyama M, Miyata M, Suico MA, Shuto T, Kai H (2008) Multi-elemental analysis of serum and amyloid fibrils in familial amyloid polyneuropathy patients. Amyloid 15:108–116. https://doi.org/10.1080/13506120802006013
Suzuki S, Kasai K, Yamauchi K (2015) Characterization of little skate (Leucoraja erinacea) recombinant transthyretin: zinc-dependent 3,3’,5-triiodo-L-thyronine binding. Gen Comp Endocrinol 217–218:43–53. https://doi.org/10.1016/j.ygcen.2015.04.006
Suzuki S, Kasai K, Nishiyama N, Ishihara A, Yamauchi K (2017) Characteristics of the brown hagfish Paramyxine atami transthyretin: metal ion-dependent thyroid hormone binding. Gen Comp Endocrinol 249:1–14. https://doi.org/10.1016/j.ygcen.2017.02.011
Takaoka Y, Ohta M, Miyakawa K, Nakamura O, Suzuki M, Takahashi K, Yamamura K, Sakaki Y (2004) Cysteine 10 is a key residue in amyloidogenesis of human transthyretin Val30Met. Am J Pathol 164:337–345. https://doi.org/10.1016/s0002-9440(10)63123-9
Thompson ED, Mayer GD, Glover CN, Capo T, Walsh PJ, Hogstrand C (2012) Zinc hyperaccumulation in squirrelfish (Holocentrus adscenscionis) and its role in embryo viability. PLoS ONE 7:46127. https://doi.org/10.1371/journal.pone.0046127
Tola AJ, Leelawatwattana L, Prapunpoj P (2019) The catalytic kinetics of chicken transthyretin towards human Aβ1-42. Comp Biochem Physiol C Toxicol Pharmacol 226:108610. https://doi.org/10.1016/j.cbpc.2019.108610
van Bennekum AM, Wei S, Gamble MV, Vogel S, Piantedosi R, Gottesman M, Episkopou V, Blaner WS (2001) Biochemical basis for depressed serum retinol levels in transthyretin-deficient mice. J Biol Chem 276:1107–1113. https://doi.org/10.1074/jbc.M008091200
Vergauwen L, Cavallin JE, Ankley GT, Bars C, Gabriëls IJ, Michiels EDG, Fitzpatrick KR, Periz-Stanacev J, Randolph EC, Robinson SL, Saari TW, Schroeder AL, Stinckens E, Swintek J, Van Cruchten SJ, Verbueken E, Villeneuve DL, Knapen D (2018) Gene transcription ontogeny of hypothalamic-pituitary-thyroid axis development in early-life stage fathead minnow and zebrafish. Gen Comp Endocrinol 266:87–100. https://doi.org/10.1016/j.ygcen.2018.05.001
Versieck J, Barbier F, Speecke A, Hoste J (1974) Manganese, copper, and zinc concentrations in serum and packed blood cells during acute hepatitis, chronic hepatitis, and posthepatitic cirrhosis. Clin Chem 20:1141–1145. https://doi.org/10.1093/clinchem/20.9.1141
Vieira AV, Sanders EJ, Schneider WJ (1995) Transport of serum transthyretin into chicken oocytes. A receptor-mediated mechanism. J Biol Chem 270:2952–2956. https://doi.org/10.1074/jbc.270.7.2952
Wang F, Chmil C, Pierce F, Ganapathy K, Gump BB, MacKenzie JA, Metchref Y, Bendinskas K (2013) Immobilized metal affinity chromatography and human serum proteomics. J Chromatogr B Analyt Technol Biomed Life Sci 934:26–33. https://doi.org/10.1016/j.jchromb.2013.06.032
White JT, Kelly JW (2001) Support for the multigenic hypothesis of amyloidosis: the binding stoichiometry of retinol-binding protein, vitamin A, and thyroid hormone influences transthyretin amyloidogenicity in vitro. Proc Natl Acad Sci USA 98:13019–13024. https://doi.org/10.1073/pnas.241406698
Wilkinson-White LE, Easterbrook-Smith SB (2007) Characterization of the binding of Cu(II) and Zn(II) to transthyretin: effects on amyloid formation. Biochemistry 46:9123–9132. https://doi.org/10.1021/bi700607z
Williams RJP (2012) Zinc in evolution. J Inorg Biochem 111:104–109. https://doi.org/10.1016/j.jinorgbio.2012.01.004
Yamauchi K, Ishihara A (2006) Thyroid system-disrupting chemicals: interference with thyroid hormone binding to plasma proteins and the cellular thyroid hormone signaling pathway. Rev Environ Health 21:229–251. https://doi.org/10.1515/reveh.2006.21.4.229
Yamauchi K, Kasai K (2018) Sequential molecular events of functional trade-offs in 5-hydroxyisourate hydrolase before and after gene duplication led to the evolution of transthyretin during chordate diversification. J Mol Evol 86:457–469. https://doi.org/10.1007/s00239-018-9858-4
Yang DT, Joshi G, Cho PY, Johnson JA, Murphy RM (2013) Transthyretin as both a sensor and a scavenger of β-amyloid oligomers. Biochemistry 52:2849–2861. https://doi.org/10.1021/bi4001613
Yu WH, Lukiw WJ, Bergeron C, Niznik HB, Fraser PE (2001) Metallothionein III is reduced in Alzheimer’s disease. Brain Res 894:37–45. https://doi.org/10.1016/s0006-8993(00)03196-6
Zanotti G, Cendron L, Ramazzina I, Folli C, Percudani R, Berni R (2006) Structure of zebra fish HIUase: insights into evolution of an enzyme to a hormone transporter. J Mol Biol 363:1–9. https://doi.org/10.1016/j.jmb.2006.07.079
Zanotti G, Folli C, Cendron L, Alfieri B, Nishida SK, Gliubich F, Pasquato N, Negro A, Berni R (2008) Structural and mutational analyses of protein-protein interactions between transthyretin and retinol-binding protein. FEBS J 275:5841–5854. https://doi.org/10.1111/j.1742-4658.2008.06705.x
Zhang Q, Kelly JW (2003) Cys10 mixed disulfides make transthyretin more amyloidogenic under mildly acidic conditions. Biochemistry 42:8756–8761. https://doi.org/10.1021/bi030077a
Zhao L, Buxbaum JN, Reixach N (2013) Age-related oxidative modifications of transthyretin modulate its amyloidogenicity. Biochemistry 52:1913–1926. https://doi.org/10.1021/bi301313b
Zorn AM, Mason J (2001) Gene expression in the embryonic Xenopus liver. Mech Dev 103:153–157. https://doi.org/10.1016/s0925-4773(01)00341-0
Acknowledgements
We are grateful to Mr D. Suzuki, Mr K. Kasai, and Dr A. Ishihara for valuable discussions. This work was supported in part a Grant-in Aid of Science Research (C) (25340046 to K.Y.) from Japan Society for Promotion of Science.
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Yamauchi, K. The interaction of zinc with the multi-functional plasma thyroid hormone distributor protein, transthyretin: evolutionary and cross-species comparative aspects. Biometals 34, 423–437 (2021). https://doi.org/10.1007/s10534-021-00294-0
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DOI: https://doi.org/10.1007/s10534-021-00294-0