Intron Retention as a Posttranscriptional Regulatory Mechanism of Neurotoxin Expression at Early Life Stages of the Starlet Anemone Nematostella vectensis

Yehu Moran; Hagar Weinberger; Adam M. Reitzel; James C. Sullivan; Roy Kahn; Dalia Gordon; John R. Finnerty; Michael Gurevitz

doi:10.1016/j.jmb.2008.05.011

Intron Retention as a Posttranscriptional Regulatory Mechanism of Neurotoxin Expression at Early Life Stages of the Starlet Anemone Nematostella vectensis

Yehu Moran^*, Hagar Weinberger, Adam M. Reitzel, James C. Sullivan, Roy Kahn, Dalia Gordon, John R. Finnerty, Michael Gurevitz

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

37 Scopus citations

Abstract

Sea anemones use an arsenal of peptide neurotoxins accumulated in special stinging cells (nematocytes) for defense and predation. Intriguingly, genomic analysis of Nematostella vectensis revealed only a single toxin, Nv1 (N. vectensis toxin 1), encoded by multiple extremely conserved genes. We examined the toxic potential of Nv1 and whether it is produced by the three developmental stages (embryo, planula, and polyp) of Nematostella. Nv1 was expressed in recombinant form and, similarly to Type I sea anemone toxins, inhibited the inactivation of voltage-gated sodium channels. However, in contrast to the other toxins, Nv1 revealed high specificity for insect over mammalian voltage-gated sodium channels. Transcript analysis indicated that multiple Nv1 loci are transcribed at all developmental stages of N. vectensis, whereas splicing of these transcripts is restricted to the polyp stage. This finding suggests that regulation of Nv1 synthesis is posttranscriptional and that the embryo and planula stages do not produce the Nv1 toxin. This rare phenomenon of intron retention at the early developmental stages is intriguing and raises the question as to the mechanism enabling such differential expression in sea anemones.

Original language	English
Pages (from-to)	437-443
Number of pages	7
Journal	Journal of Molecular Biology
Volume	380
Issue number	3
DOIs	https://doi.org/10.1016/j.jmb.2008.05.011
State	Published - 11 Jul 2008
Externally published	Yes

Bibliographical note

Funding Information:
This article is dedicated to the memory of Prof. Andre Menez. M.G. and D.G. were supported by United States–Israel Binational Agricultural Research and Development Grants IS-3928-06 and IS-4066-07 and by Israeli Science Foundation Grant 909/04. J.R.F. was supported by Environmental Protection Agency Grant F5E11155 (together with A.M.R.) and National Science Foundation Grant FP-91656101-0 (together with J.C.S.). A.M.R. was supported by a Postdoctoral Scholar Program at the Woods Hole Oceanographic Institution, with funding provided by The Beacon Institute for Rivers and Estuaries and the J. Seward Johnson Fund.

Keywords

Nematostella vectensis
intron retention
recombinant expression
sea anemone toxins
splicing

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10.1016/j.jmb.2008.05.011

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title = "Intron Retention as a Posttranscriptional Regulatory Mechanism of Neurotoxin Expression at Early Life Stages of the Starlet Anemone Nematostella vectensis",

abstract = "Sea anemones use an arsenal of peptide neurotoxins accumulated in special stinging cells (nematocytes) for defense and predation. Intriguingly, genomic analysis of Nematostella vectensis revealed only a single toxin, Nv1 (N. vectensis toxin 1), encoded by multiple extremely conserved genes. We examined the toxic potential of Nv1 and whether it is produced by the three developmental stages (embryo, planula, and polyp) of Nematostella. Nv1 was expressed in recombinant form and, similarly to Type I sea anemone toxins, inhibited the inactivation of voltage-gated sodium channels. However, in contrast to the other toxins, Nv1 revealed high specificity for insect over mammalian voltage-gated sodium channels. Transcript analysis indicated that multiple Nv1 loci are transcribed at all developmental stages of N. vectensis, whereas splicing of these transcripts is restricted to the polyp stage. This finding suggests that regulation of Nv1 synthesis is posttranscriptional and that the embryo and planula stages do not produce the Nv1 toxin. This rare phenomenon of intron retention at the early developmental stages is intriguing and raises the question as to the mechanism enabling such differential expression in sea anemones.",

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Intron Retention as a Posttranscriptional Regulatory Mechanism of Neurotoxin Expression at Early Life Stages of the Starlet Anemone Nematostella vectensis

Abstract

Bibliographical note

Keywords

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