Human metallothioneins 2 and 3 differentially affect amyloid-beta binding by transthyretin

FEBS Journal

Volumn 277, Issue 16, 2010, Pages 3427-3436

  Martinho, Ana ^a   Gonçalves, Isabel ^a   Cardoso, Isabel ^b   Almeida, Maria R ^b,c   Quintela, Telma ^a   Saraiva, Maria J ^b,c   Santos, Cecília R A ^a  

^a UNIVERSITY OF BEIRA INTERIOR   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

^c UNIVERSITY OF PORTO   (Portugal)

Author keywords

amyloid beta; metallothionein 2; metallothionein 3; protein interactions; transthyretin

Indexed keywords

AMYLOID BETA PROTEIN; METALLOTHIONEIN II; METALLOTHIONEIN III; PREALBUMIN;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; BINDING COMPETITION; HUMAN; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RAT; TWO HYBRID SYSTEM;

AMYLOID BETA-PROTEIN; ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; GROWTH INHIBITORS; HUMANS; METALLOTHIONEIN; MICROSCOPY, CONFOCAL; NERVE TISSUE PROTEINS; PREALBUMIN; PROTEIN BINDING; RATS; RATS, WISTAR; TWO-HYBRID SYSTEM TECHNIQUES;

ANIMALIA;

EID: 77955239777     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2010.07749.x     Document Type: Article

References (44)

1. Soprano DR, Herbert J, Soprano KJ, Schon EA Goodman DS (1985) Demonstration of transthyretin mRNA in the brain and other extrahepatic tissues in the rat. J Biol Chem 260, 11793 11798.
2. 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.
3. Monaco HL (2000) The transthyretin-retinol-binding protein complex. Biochim Biophys Acta 1482, 65 72.
4. Herbert J, Wilcox JN, Pham KT, Fremeau RT Jr., Zeviani M, Dwork A, Soprano DR, Makover A, Goodman DS, Zimmerman EA et al. (1986) Transthyretin: a choroid plexus-specific transport protein in human brain. The 1986 S. Weir Mitchell award. Neurology 36, 900 911.
5. Choi SH, Leight SN, Lee VM, Li T, Wong PC, Johnson JA, Saraiva MJ Sisodia SS (2007) Accelerated Abeta deposition in APPswe/PS1deltaE9 mice with hemizygous deletions of TTR (transthyretin). J Neurosci 27, 7006 7010.
6. Stein TD Johnson JA (2002) Lack of neurodegeneration in transgenic mice overexpressing mutant amyloid precursor protein is associated with increased levels of transthyretin and the activation of cell survival pathways. J Neurosci 22, 7380 7388.
7. Schwarzman AL Goldgaber D (1996) Interaction of transthyretin with amyloid beta-protein: binding and inhibition of amyloid formation. Ciba Found Symp 199, 146 160. discussion 160-144.
8. Stein TD, Anders NJ, DeCarli C, Chan SL, Mattson MP Johnson JA (2004) Neutralization of transthyretin reverses the neuroprotective effects of secreted amyloid precursor protein (APP) in APPSW mice resulting in tau phosphorylation and loss of hippocampal neurons: support for the amyloid hypothesis. J Neurosci 24, 7707 7717.
9. Merched A, Serot JM, Visvikis S, Aguillon D, Faure G Siest G (1998) Apolipoprotein E, transthyretin and actin in the CSF of Alzheimer's patients: relation with the senile plaques and cytoskeleton biochemistry. FEBS Lett 425, 225 228.
10. Serot JM, Christmann D, Dubost T Couturier M (1997) Cerebrospinal fluid transthyretin: aging and late onset Alzheimer's disease. J Neurol Neurosurg Psychiatry 63, 506 508.
11. 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 sensitive to the Kunitz protease inhibitor. PLoS ONE 3, e2899.
12. Costa R, Goncalves A, Saraiva MJ Cardoso I (2008) Transthyretin binding to A-Beta peptide - impact on A-Beta fibrillogenesis and toxicity. FEBS Lett 582, 936 942.
13. Vasak M (2005) Advances in metallothionein structure and functions. J Trace Elem Med Biol 19, 13 17.
14. Moffatt P Denizeau F (1997) Metallothionein in physiological and physiopathological processes. Drug Metab Rev 29, 261 307.
15. Palmiter RD, Findley SD, Whitmore TE Durnam DM (1992) MT-III, a brain-specific member of the metallothionein gene family. Proc Natl Acad Sci USA 89, 6333 6337.
16. Uchida Y, Takio K, Titani K, Ihara Y Tomonaga M (1991) The growth inhibitory factor that is deficient in the Alzheimer's disease brain is a 68 amino acid metallothionein-like protein. Neuron 7, 337 347.
17. Hozumi I, Suzuki JS, Kanazawa H, Hara A, Saio M, Inuzuka T, Miyairi S, Naganuma A Tohyama C (2008) Metallothionein-3 is expressed in the brain and various peripheral organs of the rat. Neurosci Lett 438, 54 58.
18. Moffatt P Seguin C (1998) Expression of the gene encoding metallothionein-3 in organs of the reproductive system. DNA Cell Biol 17, 501 510.
19. West AK, Hidalgo J, Eddins D, Levin ED Aschner M (2008) Metallothionein in the central nervous system: roles in protection, regeneration and cognition. Neurotoxicology 29, 489 503.
20. Carrasco J, Penkowa M, Giralt M, Camats J, Molinero A, Campbell IL, Palmiter RD Hidalgo J (2003) Role of metallothionein-III following central nervous system damage. Neurobiology Dis 13, 22 36.
21. Penkowa M (2006) Metallothioneins are multipurpose neuroprotectants during brain pathology. FEBS J 273, 1857 1870.
22. Hozumi I, Uchida Y, Watabe K, Sakamoto T Inuzuka T (2006) Growth inhibitory factor (GIF) can protect from brain damage due to stab wounds in rat brain. Neurosci Lett 395, 220 223.
23. Irie Y Keung WM (2001) Metallothionein-III antagonizes the neurotoxic and neurotrophic effects of amyloid beta peptides. Biochem Biophys Res Commun 282, 416 420.
24. 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. Neurobiology Dis 5, 349 356.
25. Carrasco J, Adlard P, Cotman C, Quintana A, Penkowa M, Xu F, Van Nostrand WE Hidalgo J (2006) Metallothionein-I and -III expression in animal models of Alzheimer disease. Neuroscience 143, 911 922.
26. Yu WH, Lukiw WJ, Bergeron C, Niznik HB Fraser PE (2001) Metallothionein III is reduced in Alzheimer's disease. Brain Res 894, 37 45.
27. Tsuji S, Kobayashi H, Uchida Y, Ihara Y Miyatake T (1992) Molecular-cloning of human growth inhibitory factor cDNA and its down-regulation in Alzheimer's disease. EMBO J 11, 4843 4850.
28. Carrasco J, Giralt M, Molinero A, Penkowa M, Moos T Hidalgo J (1999) Metallothionein (MT)-III: generation of polyclonal antibodies, comparison with MT-I+II in the freeze lesioned rat brain and in a bioassay with astrocytes, and analysis of Alzheimer's disease brains. J Neurotrauma 16, 1115 1129.
29. Amoureux MC, Van Gool D, Herrero MT, Dom R, Colpaert FC Pauwels PJ (1997) Regulation of metallothionein-III (GIF) mRNA in the brain of patients with Alzheimer disease is not impaired. Mol Chem Neuropathol, sponsored by the International Society for Neurochemistry and the World Federation of Neurology and research groups on neurochemistry and cerebrospinal fluid 32, 101 121.
30. Goncalves I, Quintela T, Baltazar G, Almeida MR, Saraiva MJ Santos CR (2008) Transthyretin interacts with metallothionein 2. Biochemistry 47, 2244 2251.
31. Ito T, Tashiro K, Muta S, Ozawa R, Chiba T, Nishizawa M, Yamamoto K, Kuhara S Sakaki Y (2000) Toward a protein-protein interaction map of the budding yeast: A comprehensive system to examine two-hybrid interactions in all possible combinations between the yeast proteins. Proc Natl Acad Sci USA 97, 1143 1147.
32. Raghu P Sivakumar B (2004) Interactions amongst plasma retinol-binding protein, transthyretin and their ligands: implications in vitamin A homeostasis and transthyretin amyloidosis. Biochim Biophys Acta 1703, 1 9.
33. Palmiter RD, Brinster RL, Hammer RE, Trumbauer ME, Rosenfeld MG, Birnberg NC Evans RM (1992) Dramatic growth of mice that develop from eggs microinjected with metallothionein-growth hormone fusion genes. 1982. Biotechnology 24, 429 433.
34. Hamer DH (1986) Metallothionein. Annu Rev Biochem 55, 913 951.
35. Kagi JHR Schaffer A (1988) Biochemistry of metallothionein. Biochemistry 27, 8509 8515.
36. Braun W, Wagner G, Worgotter E, Vasak M, Kagi JHR Wuthrich K (1986) Polypeptide fold in the 2 metal-clusters of metallothionein-2 by nuclear-magnetic-resonance in solution. J Mol Biol 187, 125 129.
37. Kagi JHR, Vasak M, Lerch K, Gilg DEO, Hunziker P, Bernhard WR Good M (1984) Structure of mammalian metallothionein. Environ Health Perspect 54, 93 103.
38. Chen CF, Wang SH Lin LY (1996) Identification and characterization of metallothionein III (growth inhibitory factor) from porcine brain. Comp Biochem Physiol B Biochem Mol Biol 115, 27 32.
39. Sewell AK, Jensen LT, Erickson JC, Palmiter RD Winge DR (1995) Bioactivity of metallothionein-3 correlates with its novel beta domain sequence rather than metal binding properties. Biochemistry 34, 4740 4747.
40. Crossgrove JS, Li GJ Zheng W (2005) The choroid plexus removes beta-amyloid from brain cerebrospinal fluid. Exp Biol Med (Maywood) 230, 771 776.
41. Crossgrove JS, Smith EL Zheng W (2007) Macromolecules involved in production and metabolism of beta-amyloid at the brain barriers. Brain Res 1138, 187 195.
42. Almeida MR, Damas AM, Lans MC, Brouwer A Saraiva MJ (1997) Thyroxine binding to transthyretin Met 119. Comparative studies of different heterozygotic carriers and structural analysis. Endocrine 6, 309 315.
43. Klotz IM Hunston DL (1984) Mathematical-models for ligand-receptor binding - real sites, ghost sites. J Biol Chem 259, 60 62.
44. Sousa MM, Yan SD, Stern D Saraiva MJ (2000) Interaction of the receptor for advanced glycation end products (RAGE) with transthyretin triggers nuclear transcription factor kB (NF-kB) activation. Lab Invest 80, 1101 1110.