The importance of a gatekeeper residue on the aggregation of transthyretin

Background: Proteins have adopted negative design to diminish aggregation. Results: The replacement of Lys-35 by Leu increases the amyloidogenicity of the 26-57 segment of TTR as well as the entire protein. Conclusion: Lys-35 is as a gatekeeper residue in TTR, and its protective effect is suppressed...

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Detalles Bibliográficos
Autores: Sant'Anna, Ricardo, Braga, Carolina, Varejão, Nathalia|||0000-0002-6952-8896, Pimenta, Karinne M., Graña Montes, Ricardo|||0000-0003-1932-1077, Alves, Aline, Cortines, Juliana, Cordeiro, Yraima, Ventura, Salvador|||0000-0002-9652-6351, Foguel, Debora
Tipo de recurso: artículo
Fecha de publicación:2014
País:España
Institución:Universitat Autònoma de Barcelona
Repositorio:Dipòsit Digital de Documents de la UAB
Idioma:inglés
OAI Identifier:oai:ddd.uab.cat:185077
Acceso en línea:https://ddd.uab.cat/record/185077
https://dx.doi.org/urn:doi:10.1074/jbc.M114.563981
Access Level:acceso abierto
Palabra clave:Amyloid
Heparin
Peptides
Protein Aggregation
Protein Misfolding
Aggregation Propensity
Gatekeeper Residue
Rational Mutation
Transthyretin
Descripción
Sumario:Background: Proteins have adopted negative design to diminish aggregation. Results: The replacement of Lys-35 by Leu increases the amyloidogenicity of the 26-57 segment of TTR as well as the entire protein. Conclusion: Lys-35 is as a gatekeeper residue in TTR, and its protective effect is suppressed by heparin. Significance: The elucidation of the principles that govern protein aggregation is helpful for the design of strategies against amyloid diseases. Protein aggregation into β-sheet-enriched amyloid fibrils is associated with an increasing number of human disorders. The adoption of such amyloid conformations seems to constitute a generic property of polypeptide chains. Therefore, during evolution, proteins have adopted negative design strategies to diminish their intrinsic propensity to aggregate, including enrichment of gatekeeper charged residues at the flanks of hydrophobic aggregation-prone segments. Wild type transthyretin (TTR) is responsible for senile systemic amyloidosis, and more than 100 mutations in the TTR gene are involved in familial amyloid polyneuropathy. The TTR 26-57 segment bears many of these aggressive amyloidogenic mutations as well as the binding site for heparin. We demonstrate here that Lys-35 acts as a gatekeeper residue in TTR, strongly decreasing its amyloidogenic potential. This protective effect is sequence-specific because Lys-48 does not affect TTR aggregation. Lys-35 is part of the TTR basic heparin-binding motif. This glycosaminoglycan blocks the protective effect of Lys-35, probably by neutralization of its side chain positive charge. A K35L mutation emulates this effect and results in the rapid self-assembly of the TTR 26-57 region into amyloid fibrils. This mutation does not affect the tetrameric protein stability, but it strongly increases its aggregation propensity. Overall, we illustrate how TTR is yet another amyloidogenic protein exploiting negative design to prevent its massive aggregation, and we show how blockage of conserved protective features by endogenous factors or mutations might result in increased disease susceptibility.