Combined proteomic and transcriptomic interrogation of the venom gland of Conus geographus uncovers novel components and functional compartmentalization

Helena Safavi-Hemami, Hao Hu, Dhana G Gorasia, Pradip K Bandyopadhyay, Paul D Veith, Neil D Young, Eric C Reynolds, Mark Yandell, Baldomero M Olivera, Anthony W Purcell

Research output: Contribution to journalArticleResearchpeer-review

33 Citations (Scopus)

Abstract

Cone snails are highly successful marine predators that use complex venoms to capture prey. At any given time, hundreds of toxins (conotoxins) are synthesized in the secretory epithelial cells of the venom gland, a long and convoluted organ that can measure 4 times the length of the snail s body. In recent years a number of studies have begun to unveil the transcriptomic, proteomic and peptidomic complexity of the venom and venom glands of a number of cone snail species. By using a combination of DIGE, bottom-up proteomics and next-generation transcriptome sequencing the present study identifies proteins involved in envenomation and conotoxin maturation, significantly extending the repertoire of known (poly)peptides expressed in the venom gland of these remarkable animals. We interrogate the molecular and proteomic composition of different sections of the venom glands of 3 specimens of the fish hunter Conus geographus and demonstrate regional variations in gene expression and protein abundance. DIGE analysis identified 1204 gel spots of which 157 showed significant regional differences in abundance as determined by biological variation analysis. Proteomic interrogation identified 342 unique proteins including those that exhibited greatest fold change. The majority of these proteins also exhibited significant changes in their mRNA expression levels validating the reliability of the experimental approach. Transcriptome sequencing further revealed a yet unknown genetic diversity of several venom gland components. Interestingly, abundant proteins that potentially form part of the injected venom mixture, such as echotoxins, phospholipase A2 and con-ikots-ikots, classified into distinct expression clusters with expression peaking in different parts of the gland. Our findings significantly enhance the known repertoire of venom gland polypeptides and provide molecular and biochemical evidence for the compartmentalization of this organ into distinct functional entities.
Original languageEnglish
Pages (from-to)938 - 953
Number of pages16
JournalMolecular & Cellular Proteomics
Volume13
Issue number4
DOIs
Publication statusPublished - 2014

Cite this

Safavi-Hemami, Helena ; Hu, Hao ; Gorasia, Dhana G ; Bandyopadhyay, Pradip K ; Veith, Paul D ; Young, Neil D ; Reynolds, Eric C ; Yandell, Mark ; Olivera, Baldomero M ; Purcell, Anthony W. / Combined proteomic and transcriptomic interrogation of the venom gland of Conus geographus uncovers novel components and functional compartmentalization. In: Molecular & Cellular Proteomics. 2014 ; Vol. 13, No. 4. pp. 938 - 953.
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abstract = "Cone snails are highly successful marine predators that use complex venoms to capture prey. At any given time, hundreds of toxins (conotoxins) are synthesized in the secretory epithelial cells of the venom gland, a long and convoluted organ that can measure 4 times the length of the snail s body. In recent years a number of studies have begun to unveil the transcriptomic, proteomic and peptidomic complexity of the venom and venom glands of a number of cone snail species. By using a combination of DIGE, bottom-up proteomics and next-generation transcriptome sequencing the present study identifies proteins involved in envenomation and conotoxin maturation, significantly extending the repertoire of known (poly)peptides expressed in the venom gland of these remarkable animals. We interrogate the molecular and proteomic composition of different sections of the venom glands of 3 specimens of the fish hunter Conus geographus and demonstrate regional variations in gene expression and protein abundance. DIGE analysis identified 1204 gel spots of which 157 showed significant regional differences in abundance as determined by biological variation analysis. Proteomic interrogation identified 342 unique proteins including those that exhibited greatest fold change. The majority of these proteins also exhibited significant changes in their mRNA expression levels validating the reliability of the experimental approach. Transcriptome sequencing further revealed a yet unknown genetic diversity of several venom gland components. Interestingly, abundant proteins that potentially form part of the injected venom mixture, such as echotoxins, phospholipase A2 and con-ikots-ikots, classified into distinct expression clusters with expression peaking in different parts of the gland. Our findings significantly enhance the known repertoire of venom gland polypeptides and provide molecular and biochemical evidence for the compartmentalization of this organ into distinct functional entities.",
author = "Helena Safavi-Hemami and Hao Hu and Gorasia, {Dhana G} and Bandyopadhyay, {Pradip K} and Veith, {Paul D} and Young, {Neil D} and Reynolds, {Eric C} and Mark Yandell and Olivera, {Baldomero M} and Purcell, {Anthony W}",
year = "2014",
doi = "10.1074/mcp.M113.031351",
language = "English",
volume = "13",
pages = "938 -- 953",
journal = "Molecular & Cellular Proteomics",
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Safavi-Hemami, H, Hu, H, Gorasia, DG, Bandyopadhyay, PK, Veith, PD, Young, ND, Reynolds, EC, Yandell, M, Olivera, BM & Purcell, AW 2014, 'Combined proteomic and transcriptomic interrogation of the venom gland of Conus geographus uncovers novel components and functional compartmentalization', Molecular & Cellular Proteomics, vol. 13, no. 4, pp. 938 - 953. https://doi.org/10.1074/mcp.M113.031351

Combined proteomic and transcriptomic interrogation of the venom gland of Conus geographus uncovers novel components and functional compartmentalization. / Safavi-Hemami, Helena; Hu, Hao; Gorasia, Dhana G; Bandyopadhyay, Pradip K; Veith, Paul D; Young, Neil D; Reynolds, Eric C; Yandell, Mark; Olivera, Baldomero M; Purcell, Anthony W.

In: Molecular & Cellular Proteomics, Vol. 13, No. 4, 2014, p. 938 - 953.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Combined proteomic and transcriptomic interrogation of the venom gland of Conus geographus uncovers novel components and functional compartmentalization

AU - Safavi-Hemami, Helena

AU - Hu, Hao

AU - Gorasia, Dhana G

AU - Bandyopadhyay, Pradip K

AU - Veith, Paul D

AU - Young, Neil D

AU - Reynolds, Eric C

AU - Yandell, Mark

AU - Olivera, Baldomero M

AU - Purcell, Anthony W

PY - 2014

Y1 - 2014

N2 - Cone snails are highly successful marine predators that use complex venoms to capture prey. At any given time, hundreds of toxins (conotoxins) are synthesized in the secretory epithelial cells of the venom gland, a long and convoluted organ that can measure 4 times the length of the snail s body. In recent years a number of studies have begun to unveil the transcriptomic, proteomic and peptidomic complexity of the venom and venom glands of a number of cone snail species. By using a combination of DIGE, bottom-up proteomics and next-generation transcriptome sequencing the present study identifies proteins involved in envenomation and conotoxin maturation, significantly extending the repertoire of known (poly)peptides expressed in the venom gland of these remarkable animals. We interrogate the molecular and proteomic composition of different sections of the venom glands of 3 specimens of the fish hunter Conus geographus and demonstrate regional variations in gene expression and protein abundance. DIGE analysis identified 1204 gel spots of which 157 showed significant regional differences in abundance as determined by biological variation analysis. Proteomic interrogation identified 342 unique proteins including those that exhibited greatest fold change. The majority of these proteins also exhibited significant changes in their mRNA expression levels validating the reliability of the experimental approach. Transcriptome sequencing further revealed a yet unknown genetic diversity of several venom gland components. Interestingly, abundant proteins that potentially form part of the injected venom mixture, such as echotoxins, phospholipase A2 and con-ikots-ikots, classified into distinct expression clusters with expression peaking in different parts of the gland. Our findings significantly enhance the known repertoire of venom gland polypeptides and provide molecular and biochemical evidence for the compartmentalization of this organ into distinct functional entities.

AB - Cone snails are highly successful marine predators that use complex venoms to capture prey. At any given time, hundreds of toxins (conotoxins) are synthesized in the secretory epithelial cells of the venom gland, a long and convoluted organ that can measure 4 times the length of the snail s body. In recent years a number of studies have begun to unveil the transcriptomic, proteomic and peptidomic complexity of the venom and venom glands of a number of cone snail species. By using a combination of DIGE, bottom-up proteomics and next-generation transcriptome sequencing the present study identifies proteins involved in envenomation and conotoxin maturation, significantly extending the repertoire of known (poly)peptides expressed in the venom gland of these remarkable animals. We interrogate the molecular and proteomic composition of different sections of the venom glands of 3 specimens of the fish hunter Conus geographus and demonstrate regional variations in gene expression and protein abundance. DIGE analysis identified 1204 gel spots of which 157 showed significant regional differences in abundance as determined by biological variation analysis. Proteomic interrogation identified 342 unique proteins including those that exhibited greatest fold change. The majority of these proteins also exhibited significant changes in their mRNA expression levels validating the reliability of the experimental approach. Transcriptome sequencing further revealed a yet unknown genetic diversity of several venom gland components. Interestingly, abundant proteins that potentially form part of the injected venom mixture, such as echotoxins, phospholipase A2 and con-ikots-ikots, classified into distinct expression clusters with expression peaking in different parts of the gland. Our findings significantly enhance the known repertoire of venom gland polypeptides and provide molecular and biochemical evidence for the compartmentalization of this organ into distinct functional entities.

UR - http://www.mcponline.org/content/13/4/938.full.pdf+html

U2 - 10.1074/mcp.M113.031351

DO - 10.1074/mcp.M113.031351

M3 - Article

VL - 13

SP - 938

EP - 953

JO - Molecular & Cellular Proteomics

JF - Molecular & Cellular Proteomics

SN - 1535-9476

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