Elucidation of Medusozoan (Jellyfish) Venom Constituent Activities Using Constellation Pharmacology
Within the phylum Cnidaria, sea anemones (class Anthozoa) express a rich diversity of ion-channel peptide modulators with biomedical applications, but corollary discoveries from jellyfish (subphylum Medusozoa) are lacking. To bridge this gap, bioactivities of previously unexplored proteinaceous and...
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| Published in: | Toxins Vol. 16; no. 10; p. 447 |
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| Abstract | Within the phylum Cnidaria, sea anemones (class Anthozoa) express a rich diversity of ion-channel peptide modulators with biomedical applications, but corollary discoveries from jellyfish (subphylum Medusozoa) are lacking. To bridge this gap, bioactivities of previously unexplored proteinaceous and small molecular weight (~15 kDa to 5 kDa) venom components were assessed in a mouse dorsal root ganglia (DRG) high-content calcium-imaging assay, known as constellation pharmacology. While the addition of crude venom led to nonspecific cell death and Fura-2 signal leakage due to pore-forming activity, purified small molecular weight fractions of venom demonstrated three main, concentration-dependent and reversible effects on defined heterogeneous cell types found in the primary cultures of mouse DRG. These three phenotypic responses are herein referred to as phenotype A, B and C: excitatory amplification (A) or inhibition (B) of KCl-induced calcium signals, and test compound-induced disturbances to baseline calcium levels (C). Most notably, certain
venom fractions showed phenotype A effects in all DRG neurons;
and
fractions predominantly showed phenotype B effects in small- and medium-diameter neurons. Finally, specific
and
venom components induced direct excitatory responses (phenotype C) in glial cells. These findings demonstrate a diversity of neuroactive compounds in jellyfish venom potentially targeting a constellation of ion channels and ligand-gated receptors with broad physiological implications. |
|---|---|
| AbstractList | Within the phylum Cnidaria, sea anemones (class Anthozoa) express a rich diversity of ion-channel peptide modulators with biomedical applications, but corollary discoveries from jellyfish (subphylum Medusozoa) are lacking. To bridge this gap, bioactivities of previously unexplored proteinaceous and small molecular weight (~15 kDa to 5 kDa) venom components were assessed in a mouse dorsal root ganglia (DRG) high-content calcium-imaging assay, known as constellation pharmacology. While the addition of crude venom led to nonspecific cell death and Fura-2 signal leakage due to pore-forming activity, purified small molecular weight fractions of venom demonstrated three main, concentration-dependent and reversible effects on defined heterogeneous cell types found in the primary cultures of mouse DRG. These three phenotypic responses are herein referred to as phenotype A, B and C: excitatory amplification (A) or inhibition (B) of KCl-induced calcium signals, and test compound-induced disturbances to baseline calcium levels (C). Most notably, certain Alatina alata venom fractions showed phenotype A effects in all DRG neurons; Physalia physalis and Chironex fleckeri fractions predominantly showed phenotype B effects in small- and medium-diameter neurons. Finally, specific Physalia physalis and Alatina alata venom components induced direct excitatory responses (phenotype C) in glial cells. These findings demonstrate a diversity of neuroactive compounds in jellyfish venom potentially targeting a constellation of ion channels and ligand-gated receptors with broad physiological implications. Within the phylum Cnidaria, sea anemones (class Anthozoa) express a rich diversity of ion-channel peptide modulators with biomedical applications, but corollary discoveries from jellyfish (subphylum Medusozoa) are lacking. To bridge this gap, bioactivities of previously unexplored proteinaceous and small molecular weight (~15 kDa to 5 kDa) venom components were assessed in a mouse dorsal root ganglia (DRG) high-content calcium-imaging assay, known as constellation pharmacology. While the addition of crude venom led to nonspecific cell death and Fura-2 signal leakage due to pore-forming activity, purified small molecular weight fractions of venom demonstrated three main, concentration-dependent and reversible effects on defined heterogeneous cell types found in the primary cultures of mouse DRG. These three phenotypic responses are herein referred to as phenotype A, B and C: excitatory amplification (A) or inhibition (B) of KCl-induced calcium signals, and test compound-induced disturbances to baseline calcium levels (C). Most notably, certain venom fractions showed phenotype A effects in all DRG neurons; and fractions predominantly showed phenotype B effects in small- and medium-diameter neurons. Finally, specific and venom components induced direct excitatory responses (phenotype C) in glial cells. These findings demonstrate a diversity of neuroactive compounds in jellyfish venom potentially targeting a constellation of ion channels and ligand-gated receptors with broad physiological implications. Within the phylum Cnidaria, sea anemones (class Anthozoa) express a rich diversity of ion-channel peptide modulators with biomedical applications, but corollary discoveries from jellyfish (subphylum Medusozoa) are lacking. To bridge this gap, bioactivities of previously unexplored proteinaceous and small molecular weight (~15 kDa to 5 kDa) venom components were assessed in a mouse dorsal root ganglia (DRG) high-content calcium-imaging assay, known as constellation pharmacology. While the addition of crude venom led to nonspecific cell death and Fura-2 signal leakage due to pore-forming activity, purified small molecular weight fractions of venom demonstrated three main, concentration-dependent and reversible effects on defined heterogeneous cell types found in the primary cultures of mouse DRG. These three phenotypic responses are herein referred to as phenotype A, B and C: excitatory amplification (A) or inhibition (B) of KCl-induced calcium signals, and test compound-induced disturbances to baseline calcium levels (C). Most notably, certain Alatina alata venom fractions showed phenotype A effects in all DRG neurons; Physalia physalis and Chironex fleckeri fractions predominantly showed phenotype B effects in small- and medium-diameter neurons. Finally, specific Physalia physalis and Alatina alata venom components induced direct excitatory responses (phenotype C) in glial cells. These findings demonstrate a diversity of neuroactive compounds in jellyfish venom potentially targeting a constellation of ion channels and ligand-gated receptors with broad physiological implications.Within the phylum Cnidaria, sea anemones (class Anthozoa) express a rich diversity of ion-channel peptide modulators with biomedical applications, but corollary discoveries from jellyfish (subphylum Medusozoa) are lacking. To bridge this gap, bioactivities of previously unexplored proteinaceous and small molecular weight (~15 kDa to 5 kDa) venom components were assessed in a mouse dorsal root ganglia (DRG) high-content calcium-imaging assay, known as constellation pharmacology. While the addition of crude venom led to nonspecific cell death and Fura-2 signal leakage due to pore-forming activity, purified small molecular weight fractions of venom demonstrated three main, concentration-dependent and reversible effects on defined heterogeneous cell types found in the primary cultures of mouse DRG. These three phenotypic responses are herein referred to as phenotype A, B and C: excitatory amplification (A) or inhibition (B) of KCl-induced calcium signals, and test compound-induced disturbances to baseline calcium levels (C). Most notably, certain Alatina alata venom fractions showed phenotype A effects in all DRG neurons; Physalia physalis and Chironex fleckeri fractions predominantly showed phenotype B effects in small- and medium-diameter neurons. Finally, specific Physalia physalis and Alatina alata venom components induced direct excitatory responses (phenotype C) in glial cells. These findings demonstrate a diversity of neuroactive compounds in jellyfish venom potentially targeting a constellation of ion channels and ligand-gated receptors with broad physiological implications. Within the phylum Cnidaria, sea anemones (class Anthozoa) express a rich diversity of ion-channel peptide modulators with biomedical applications, but corollary discoveries from jellyfish (subphylum Medusozoa) are lacking. To bridge this gap, bioactivities of previously unexplored proteinaceous and small molecular weight (~15 kDa to 5 kDa) venom components were assessed in a mouse dorsal root ganglia (DRG) high-content calcium-imaging assay, known as constellation pharmacology. While the addition of crude venom led to nonspecific cell death and Fura-2 signal leakage due to pore-forming activity, purified small molecular weight fractions of venom demonstrated three main, concentration-dependent and reversible effects on defined heterogeneous cell types found in the primary cultures of mouse DRG. These three phenotypic responses are herein referred to as phenotype A, B and C: excitatory amplification (A) or inhibition (B) of KCl-induced calcium signals, and test compound-induced disturbances to baseline calcium levels (C). Most notably, certain Alatina alata venom fractions showed phenotype A effects in all DRG neurons; Physalia physalis and Chironex fleckeri fractions predominantly showed phenotype B effects in small- and medium-diameter neurons. Finally, specific Physalia physalis and Alatina alata venom components induced direct excitatory responses (phenotype C) in glial cells. These findings demonstrate a diversity of neuroactive compounds in jellyfish venom potentially targeting a constellation of ion channels and ligand-gated receptors with broad physiological implications. |
| Author | Giglio, Matías L Yanagihara, Angel A Hurwitz, Kikiana Raghuraman, Shrinivasan Olivera, Baldomero M Espino, Samuel S Kadler, Raechel |
| AuthorAffiliation | 1 Pacific Biosciences Research Center, University of Hawaii at Manoa, Honolulu, HI 96822, USA; rkadler@hawaii.edu 3 Faculty of Sciences, Brigham Young University Hawaii, Laie, HI 96762, USA; kikiana.hurwitz@byuh.edu 2 Department of Biology, University of Utah, Salt Lake City, UT 84115, USA; matias.giglio@utah.edu (M.L.G.); samuel.espino@utah.edu (S.S.E.) |
| AuthorAffiliation_xml | – name: 1 Pacific Biosciences Research Center, University of Hawaii at Manoa, Honolulu, HI 96822, USA; rkadler@hawaii.edu – name: 2 Department of Biology, University of Utah, Salt Lake City, UT 84115, USA; matias.giglio@utah.edu (M.L.G.); samuel.espino@utah.edu (S.S.E.) – name: 3 Faculty of Sciences, Brigham Young University Hawaii, Laie, HI 96762, USA; kikiana.hurwitz@byuh.edu |
| Author_xml | – sequence: 1 givenname: Angel A orcidid: 0000-0001-6908-8176 surname: Yanagihara fullname: Yanagihara, Angel A organization: Pacific Biosciences Research Center, University of Hawaii at Manoa, Honolulu, HI 96822, USA – sequence: 2 givenname: Matías L orcidid: 0000-0002-6357-9772 surname: Giglio fullname: Giglio, Matías L organization: Department of Biology, University of Utah, Salt Lake City, UT 84115, USA – sequence: 3 givenname: Kikiana surname: Hurwitz fullname: Hurwitz, Kikiana organization: Faculty of Sciences, Brigham Young University Hawaii, Laie, HI 96762, USA – sequence: 4 givenname: Raechel orcidid: 0009-0000-6266-7941 surname: Kadler fullname: Kadler, Raechel organization: Pacific Biosciences Research Center, University of Hawaii at Manoa, Honolulu, HI 96822, USA – sequence: 5 givenname: Samuel S surname: Espino fullname: Espino, Samuel S organization: Department of Biology, University of Utah, Salt Lake City, UT 84115, USA – sequence: 6 givenname: Shrinivasan surname: Raghuraman fullname: Raghuraman, Shrinivasan organization: Department of Biology, University of Utah, Salt Lake City, UT 84115, USA – sequence: 7 givenname: Baldomero M surname: Olivera fullname: Olivera, Baldomero M organization: Department of Biology, University of Utah, Salt Lake City, UT 84115, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/39453223$$D View this record in MEDLINE/PubMed |
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| Keywords | glial cells box jellyfish ion-channel modulator venom cubozoa Fura-2 calcium imaging Physalia dorsal root ganglia constellation pharmacology neurons |
| Language | English |
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| Title | Elucidation of Medusozoan (Jellyfish) Venom Constituent Activities Using Constellation Pharmacology |
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