Insights into the Protein–Lipid Interaction of Perivitellin-2, an Unusual Snail Pore-Forming Toxin

The perivitellin-2 (PV2) from snails is an unusual neuro and enterotoxin comprising a pore-forming domain of the Membrane Attack Complex and Perforin Family (MACPF) linked to a lectin. While both domains have membrane binding capabilities, PV2’s mechanism of action remains unclear. We studied the ap...

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Main Authors: Romina F. Vázquez, M. Antonieta Daza Millone, Matías L. Giglio, Tabata R. Brola, Sabina M. Maté, Horacio Heras
Format: Article
Language:English
Published: MDPI AG 2025-04-01
Series:Toxins
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Online Access:https://www.mdpi.com/2072-6651/17/4/183
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author Romina F. Vázquez
M. Antonieta Daza Millone
Matías L. Giglio
Tabata R. Brola
Sabina M. Maté
Horacio Heras
author_facet Romina F. Vázquez
M. Antonieta Daza Millone
Matías L. Giglio
Tabata R. Brola
Sabina M. Maté
Horacio Heras
author_sort Romina F. Vázquez
collection DOAJ
description The perivitellin-2 (PV2) from snails is an unusual neuro and enterotoxin comprising a pore-forming domain of the Membrane Attack Complex and Perforin Family (MACPF) linked to a lectin. While both domains have membrane binding capabilities, PV2’s mechanism of action remains unclear. We studied the apple snail <i>Pomacea maculata</i> PV2’s (PmPV2’s) interaction with lipid membranes using various biophysical and cell biology approaches. In vitro studies showed that PmPV2 toxicity decreased when cholesterol (Chol) was diminished from enterocyte cell membranes. Chol enhanced PmPV2 association with phosphatidylcholine membranes but did not induce pore formation. In contrast, using rat brain lipid models, rich in glycolipids, PmPV2 exhibited high affinity and induced vesicle permeabilization. Negative stain electron microscopy and atomic force microscopy confirmed the formation of pore-like structures in brain lipid vesicles. Our findings suggest that Chol is a necessary lipid component and point to PmPV2–glycolipid interactions as potential activators critical to triggering PmPV2’s pore-forming activity, providing insights into this novel toxin’s mechanism.
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spelling doaj-art-18f97bda7d1941b1a0367333467067952025-08-20T02:18:10ZengMDPI AGToxins2072-66512025-04-0117418310.3390/toxins17040183Insights into the Protein–Lipid Interaction of Perivitellin-2, an Unusual Snail Pore-Forming ToxinRomina F. Vázquez0M. Antonieta Daza Millone1Matías L. Giglio2Tabata R. Brola3Sabina M. Maté4Horacio Heras5Instituto de Investigaciones Bioquímicas de La Plata “Prof. Dr. Rodolfo R. Brenner”, INIBIOLP, CCT-La Plata, CONICET, Facultad de Ciencias Médicas, Universidad Nacional de La Plata, 60 y 120, La Plata 1900, ArgentinaInstituto de Investigaciones Fisicoquímicas Teóricas y Aplicadas, INIFTA, CCT-La Plata, CONICET, Universidad Nacional de La Plata, Diagonal 113 y 64, La Plata 1900, ArgentinaInstituto de Investigaciones Bioquímicas de La Plata “Prof. Dr. Rodolfo R. Brenner”, INIBIOLP, CCT-La Plata, CONICET, Facultad de Ciencias Médicas, Universidad Nacional de La Plata, 60 y 120, La Plata 1900, ArgentinaInstituto de Investigaciones Bioquímicas de La Plata “Prof. Dr. Rodolfo R. Brenner”, INIBIOLP, CCT-La Plata, CONICET, Facultad de Ciencias Médicas, Universidad Nacional de La Plata, 60 y 120, La Plata 1900, ArgentinaInstituto de Investigaciones Bioquímicas de La Plata “Prof. Dr. Rodolfo R. Brenner”, INIBIOLP, CCT-La Plata, CONICET, Facultad de Ciencias Médicas, Universidad Nacional de La Plata, 60 y 120, La Plata 1900, ArgentinaInstituto de Investigaciones Bioquímicas de La Plata “Prof. Dr. Rodolfo R. Brenner”, INIBIOLP, CCT-La Plata, CONICET, Facultad de Ciencias Médicas, Universidad Nacional de La Plata, 60 y 120, La Plata 1900, ArgentinaThe perivitellin-2 (PV2) from snails is an unusual neuro and enterotoxin comprising a pore-forming domain of the Membrane Attack Complex and Perforin Family (MACPF) linked to a lectin. While both domains have membrane binding capabilities, PV2’s mechanism of action remains unclear. We studied the apple snail <i>Pomacea maculata</i> PV2’s (PmPV2’s) interaction with lipid membranes using various biophysical and cell biology approaches. In vitro studies showed that PmPV2 toxicity decreased when cholesterol (Chol) was diminished from enterocyte cell membranes. Chol enhanced PmPV2 association with phosphatidylcholine membranes but did not induce pore formation. In contrast, using rat brain lipid models, rich in glycolipids, PmPV2 exhibited high affinity and induced vesicle permeabilization. Negative stain electron microscopy and atomic force microscopy confirmed the formation of pore-like structures in brain lipid vesicles. Our findings suggest that Chol is a necessary lipid component and point to PmPV2–glycolipid interactions as potential activators critical to triggering PmPV2’s pore-forming activity, providing insights into this novel toxin’s mechanism.https://www.mdpi.com/2072-6651/17/4/183MACPFsnail pore-forming toxinneurotoxin/enterotoxinlectinlipid membranesprotein–lipid interaction
spellingShingle Romina F. Vázquez
M. Antonieta Daza Millone
Matías L. Giglio
Tabata R. Brola
Sabina M. Maté
Horacio Heras
Insights into the Protein–Lipid Interaction of Perivitellin-2, an Unusual Snail Pore-Forming Toxin
Toxins
MACPF
snail pore-forming toxin
neurotoxin/enterotoxin
lectin
lipid membranes
protein–lipid interaction
title Insights into the Protein–Lipid Interaction of Perivitellin-2, an Unusual Snail Pore-Forming Toxin
title_full Insights into the Protein–Lipid Interaction of Perivitellin-2, an Unusual Snail Pore-Forming Toxin
title_fullStr Insights into the Protein–Lipid Interaction of Perivitellin-2, an Unusual Snail Pore-Forming Toxin
title_full_unstemmed Insights into the Protein–Lipid Interaction of Perivitellin-2, an Unusual Snail Pore-Forming Toxin
title_short Insights into the Protein–Lipid Interaction of Perivitellin-2, an Unusual Snail Pore-Forming Toxin
title_sort insights into the protein lipid interaction of perivitellin 2 an unusual snail pore forming toxin
topic MACPF
snail pore-forming toxin
neurotoxin/enterotoxin
lectin
lipid membranes
protein–lipid interaction
url https://www.mdpi.com/2072-6651/17/4/183
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