Rapid expansion of the protein disulfide isomerase gene family facilitates the folding of venom peptides

Helena Safavi-Hemami; Qing Li; Ronneshia L. Jackson; Albert S. Song; Wouter Krogh Boomsma; Pradip K. Bandyopadhyay; Christian W. Gruber; Anthony W. Purcell; Mark Yandell; Baldomero M. Olivera; Lars Ellgaard

doi:10.1073/pnas.1525790113

Rapid expansion of the protein disulfide isomerase gene family facilitates the folding of venom peptides

Helena Safavi-Hemami, Qing Li, Ronneshia L. Jackson, Albert S. Song, Wouter Krogh Boomsma, Pradip K. Bandyopadhyay, Christian W. Gruber, Anthony W. Purcell, Mark Yandell, Baldomero M. Olivera, Lars Ellgaard

Biomolecular Sciences

26 Citations (Scopus)

Abstract

Formation of correct disulfide bonds in the endoplasmic reticulum is a crucial step for folding proteins destined for secretion. Protein disulfide isomerases (PDIs) play a central role in this process. We report a previously unidentified, hypervariable family of PDIs that represents the most diverse gene family of oxidoreductases described in a single genus to date. These enzymes are highly expressed specifically in the venom glands of predatory cone snails, animals that synthesize a remarkably diverse set of cysteine-rich peptide toxins (conotoxins). Enzymes in this PDI family, termed conotoxin-specific PDIs, significantly and differentially accelerate the kinetics of disulfide-bond formation of several conotoxins. Our results are consistent with a unique biological scenario associated with protein folding: The diversification of a family of foldases can be correlated with the rapid evolution of an unprecedented diversity of disulfide-rich structural domains expressed by venomous marine snails in the superfamily Conoidea.

Original language	English
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	113
Issue number	12
Pages (from-to)	3227-3232
Number of pages	6
ISSN	0027-8424
DOIs	https://doi.org/10.1073/pnas.1525790113
Publication status	Published - 22 Mar 2016

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Safavi-Hemami, H., Li, Q., Jackson, R. L., Song, A. S., Boomsma, W. K., Bandyopadhyay, P. K., Gruber, C. W., Purcell, A. W., Yandell, M., Olivera, B. M., & Ellgaard, L. (2016). Rapid expansion of the protein disulfide isomerase gene family facilitates the folding of venom peptides. Proceedings of the National Academy of Sciences of the United States of America, 113(12), 3227-3232. https://doi.org/10.1073/pnas.1525790113

Rapid expansion of the protein disulfide isomerase gene family facilitates the folding of venom peptides. / Safavi-Hemami, Helena; Li, Qing; Jackson, Ronneshia L. et al.
In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 113, No. 12, 22.03.2016, p. 3227-3232.

Research output: Contribution to journal › Journal article › Research › peer-review

Safavi-Hemami, H, Li, Q, Jackson, RL, Song, AS, Boomsma, WK, Bandyopadhyay, PK, Gruber, CW, Purcell, AW, Yandell, M, Olivera, BM & Ellgaard, L 2016, 'Rapid expansion of the protein disulfide isomerase gene family facilitates the folding of venom peptides', Proceedings of the National Academy of Sciences of the United States of America, vol. 113, no. 12, pp. 3227-3232. https://doi.org/10.1073/pnas.1525790113

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abstract = "Formation of correct disulfide bonds in the endoplasmic reticulum is a crucial step for folding proteins destined for secretion. Protein disulfide isomerases (PDIs) play a central role in this process. We report a previously unidentified, hypervariable family of PDIs that represents the most diverse gene family of oxidoreductases described in a single genus to date. These enzymes are highly expressed specifically in the venom glands of predatory cone snails, animals that synthesize a remarkably diverse set of cysteine-rich peptide toxins (conotoxins). Enzymes in this PDI family, termed conotoxin-specific PDIs, significantly and differentially accelerate the kinetics of disulfide-bond formation of several conotoxins. Our results are consistent with a unique biological scenario associated with protein folding: The diversification of a family of foldases can be correlated with the rapid evolution of an unprecedented diversity of disulfide-rich structural domains expressed by venomous marine snails in the superfamily Conoidea.",

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AU - Safavi-Hemami, Helena

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AU - Jackson, Ronneshia L.

AU - Song, Albert S.

AU - Boomsma, Wouter Krogh

AU - Bandyopadhyay, Pradip K.

AU - Gruber, Christian W.

AU - Purcell, Anthony W.

AU - Yandell, Mark

AU - Olivera, Baldomero M.

AU - Ellgaard, Lars

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N2 - Formation of correct disulfide bonds in the endoplasmic reticulum is a crucial step for folding proteins destined for secretion. Protein disulfide isomerases (PDIs) play a central role in this process. We report a previously unidentified, hypervariable family of PDIs that represents the most diverse gene family of oxidoreductases described in a single genus to date. These enzymes are highly expressed specifically in the venom glands of predatory cone snails, animals that synthesize a remarkably diverse set of cysteine-rich peptide toxins (conotoxins). Enzymes in this PDI family, termed conotoxin-specific PDIs, significantly and differentially accelerate the kinetics of disulfide-bond formation of several conotoxins. Our results are consistent with a unique biological scenario associated with protein folding: The diversification of a family of foldases can be correlated with the rapid evolution of an unprecedented diversity of disulfide-rich structural domains expressed by venomous marine snails in the superfamily Conoidea.

AB - Formation of correct disulfide bonds in the endoplasmic reticulum is a crucial step for folding proteins destined for secretion. Protein disulfide isomerases (PDIs) play a central role in this process. We report a previously unidentified, hypervariable family of PDIs that represents the most diverse gene family of oxidoreductases described in a single genus to date. These enzymes are highly expressed specifically in the venom glands of predatory cone snails, animals that synthesize a remarkably diverse set of cysteine-rich peptide toxins (conotoxins). Enzymes in this PDI family, termed conotoxin-specific PDIs, significantly and differentially accelerate the kinetics of disulfide-bond formation of several conotoxins. Our results are consistent with a unique biological scenario associated with protein folding: The diversification of a family of foldases can be correlated with the rapid evolution of an unprecedented diversity of disulfide-rich structural domains expressed by venomous marine snails in the superfamily Conoidea.

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DO - 10.1073/pnas.1525790113

M3 - Journal article

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JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

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ER -

Rapid expansion of the protein disulfide isomerase gene family facilitates the folding of venom peptides

Abstract

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