Ryanodine receptor and FK506 binding protein 1 in the Atlantic killifish (Fundulus heteroclitus)

A phylogenetic and population-based comparison

Erika B. Holland, Jared V. Goldstone, Isaac N Pessah, Andrew Whitehead, Noah M. Reid, Sibel I. Karchner, Mark E. Hahn, Diane E. Nacci, Bryan W. Clark, John J. Stegeman

Research output: Contribution to journalArticle

1 Citation (Scopus)

Abstract

Non-dioxin-like polychlorinated biphenyls (NDL PCBs) activate ryanodine receptors (RyR), microsomal Ca2+ channels of broad significance. Teleost fish may be important models for NDL PCB neurotoxicity, and we used sequencing databases to characterize teleost RyR and FK506 binding protein 12 or 12.6 kDa (genes FKBP1A; FKBP1B), which promote NDL PCB-triggered Ca2+ dysregulation. Particular focus was placed on describing genes in the Atlantic killifish (Fundulus heteroclitus) genome and searching available RNA-sequencing datasets for single nucleotide variants (SNV) between PCB tolerant killifish from New Bedford Harbor (NBH) versus sensitive killifish from Scorton Creek (SC), MA. Consistent with the teleost whole genome duplication (tWGD), killifish have six RyR genes, corresponding to a and b paralogs of mammalian RyR1, 2 and 3. The presence of six RyR genes was consistent in all teleosts investigated including zebrafish. Killifish have four FKBP1; one FKBP1b and three FKBP1a named FKBP1aa, FKBP1ab, likely from the tWGD and a single gene duplicate FKBP1a3 suggested to have arisen in Atherinomorphae. The RyR and FKBP1 genes displayed tissue and developmental stage-specific mRNA expression, and the previously uncharacterized RyR3, herein named RyR3b, and all FKBP1 genes were prominent in brain. We identified a SNV in RyR3b encoding missense mutation E1458D. In NBH killifish, 57% were heterozygous and 28% were homozygous for this SNV, whereas almost all SC killifish (94%) lacked the variant (n ≥ 39 per population). The outlined sequence differences between mammalian and teleost RyR and FKBP1 together with outlined population differences in SNV frequency may contribute to our understanding of NDL PCB neurotoxicity.

Original languageEnglish (US)
Pages (from-to)105-115
Number of pages11
JournalAquatic Toxicology
Volume192
DOIs
StatePublished - 2017

Fingerprint

Tacrolimus Binding Protein 1A
Fundulidae
ryanodine receptors
Fundulus heteroclitus
Ryanodine Receptor Calcium Release Channel
binding proteins
teleost
polychlorinated biphenyls
Polychlorinated Biphenyls
phylogenetics
PCB
protein
gene
phylogeny
nucleotides
Population
neurotoxicity
genes
Nucleotides
Genes

Keywords

  • FK binding protein 1
  • Fundulus heteroclitus
  • Non-dioxin-like PCBs ryanodine receptor

ASJC Scopus subject areas

  • Aquatic Science
  • Health, Toxicology and Mutagenesis

Cite this

Ryanodine receptor and FK506 binding protein 1 in the Atlantic killifish (Fundulus heteroclitus) : A phylogenetic and population-based comparison. / Holland, Erika B.; Goldstone, Jared V.; Pessah, Isaac N; Whitehead, Andrew; Reid, Noah M.; Karchner, Sibel I.; Hahn, Mark E.; Nacci, Diane E.; Clark, Bryan W.; Stegeman, John J.

In: Aquatic Toxicology, Vol. 192, 2017, p. 105-115.

Research output: Contribution to journalArticle

Holland, EB, Goldstone, JV, Pessah, IN, Whitehead, A, Reid, NM, Karchner, SI, Hahn, ME, Nacci, DE, Clark, BW & Stegeman, JJ 2017, 'Ryanodine receptor and FK506 binding protein 1 in the Atlantic killifish (Fundulus heteroclitus): A phylogenetic and population-based comparison', Aquatic Toxicology, vol. 192, pp. 105-115. https://doi.org/10.1016/j.aquatox.2017.09.002
Holland, Erika B. ; Goldstone, Jared V. ; Pessah, Isaac N ; Whitehead, Andrew ; Reid, Noah M. ; Karchner, Sibel I. ; Hahn, Mark E. ; Nacci, Diane E. ; Clark, Bryan W. ; Stegeman, John J. / Ryanodine receptor and FK506 binding protein 1 in the Atlantic killifish (Fundulus heteroclitus) : A phylogenetic and population-based comparison. In: Aquatic Toxicology. 2017 ; Vol. 192. pp. 105-115.
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abstract = "Non-dioxin-like polychlorinated biphenyls (NDL PCBs) activate ryanodine receptors (RyR), microsomal Ca2+ channels of broad significance. Teleost fish may be important models for NDL PCB neurotoxicity, and we used sequencing databases to characterize teleost RyR and FK506 binding protein 12 or 12.6 kDa (genes FKBP1A; FKBP1B), which promote NDL PCB-triggered Ca2+ dysregulation. Particular focus was placed on describing genes in the Atlantic killifish (Fundulus heteroclitus) genome and searching available RNA-sequencing datasets for single nucleotide variants (SNV) between PCB tolerant killifish from New Bedford Harbor (NBH) versus sensitive killifish from Scorton Creek (SC), MA. Consistent with the teleost whole genome duplication (tWGD), killifish have six RyR genes, corresponding to a and b paralogs of mammalian RyR1, 2 and 3. The presence of six RyR genes was consistent in all teleosts investigated including zebrafish. Killifish have four FKBP1; one FKBP1b and three FKBP1a named FKBP1aa, FKBP1ab, likely from the tWGD and a single gene duplicate FKBP1a3 suggested to have arisen in Atherinomorphae. The RyR and FKBP1 genes displayed tissue and developmental stage-specific mRNA expression, and the previously uncharacterized RyR3, herein named RyR3b, and all FKBP1 genes were prominent in brain. We identified a SNV in RyR3b encoding missense mutation E1458D. In NBH killifish, 57{\%} were heterozygous and 28{\%} were homozygous for this SNV, whereas almost all SC killifish (94{\%}) lacked the variant (n ≥ 39 per population). The outlined sequence differences between mammalian and teleost RyR and FKBP1 together with outlined population differences in SNV frequency may contribute to our understanding of NDL PCB neurotoxicity.",
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AU - Pessah, Isaac N

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AU - Clark, Bryan W.

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