These ~172-kDa proteins are dimers of AB toxins, each composed of a carbohydrate-binding protein of the tachylectin family (targeting module) disulfide-linked to a pore-forming protein of the Membrane Attack Complex and Perforin (MACPF) family (toxic unit).[2][3] Like most other studied perivitellins from Pomacea snails, PV2s are highly stable in a wide range of pH values and withstand gastrointestinal digestion, characteristics associated with an antinutritive defense system that deters predation by lowering the nutritional value of the eggs.[2][1][4]
Functionsedit
As part of the perivitelline fluid, perivitellin-2 constitutes a nutrient source for the developing embryo, notably in the last stages where it is probably used as an endogenous source of energy and structural molecules during the transition to the free life.[5] PV2s also play a role in a complex defense system that protects the embryos against predation.[2][6][1]
Pomacea maculata perivitellin-2
Identifiers
Organism
Pomacea maculata (giant apple snail)
Symbol
PmPV2
Alt. symbols
PV2
PV2s have both lectin and perforin activities, associated to the two subunits of their particular structures.[2][3] As a lectin, PV2s can agglutinate rabbit red blood cells and bind to the plasma membrane of intestinal cells both in vitro and in vivo.[2][1][7] As a perforin, PV2s are able to disrupt intestinal cells altering the plasma membraneconductance and to form large pores in artificial lipid bilayers.[3] An interesting issue with these perivitellins is that the combination of two immune proteins (lectin and perforin) gave rise to a new toxic entity, an excellent example of protein exaptation.[2][3] This binary structure includes PV2s within “AB-toxins”, a group of toxins mostly described in bacteria and plants. In PV2 toxins, the lectin would bind to target membranes through the recognition of specific glycans, acting as a delivery “B” subunit, and then the pore-forming “A” subunit would disrupt lipid bilayers forming large pores and leading to cell death, therefore constituting a true pore-forming toxin.[3]
Toxicity toward mammalsedit
PV2 toxins proved to be highly toxic to mice when it enters the bloodstream (LD50, 96 h 0.25 mg/kg, i.p.) and those receiving sublethal doses displayed neurological signs including weakness and lethargy, low head and bent down position (ortopneic), half-closed eyes, taquipnea, hirsute hair, extreme abduction of the rear limbs, paresia and were not able to support their body weight (tetraplegic), among others.[3][6] Histopathological analyses of affected mice showed that PV2 toxins affect the dorsal horn of the spinal cord, particularly on the 2nd and 3rd gray matter laminas, where alters the calcium metabolism and causes neuronapoptosis.[6] Apart from its neurotoxicity, it has been recently shown that PV2s are also enterotoxic to mice when ingested, a function that had never been ascribed to animal proteins.[1] At the cellular level, PV2 is cytotoxic to intestinal cells, on which it causes changes in their surface morphology increasing the membrane roughness. At the system level, oral administration of PV2 induces large morphological changes on mice intestine mucosa, reducing its absorptive surface. Additionally, PV2 reaches the Peyer's patches where it activates lymphoid follicles and triggers apoptosis.[1]
Evolution of a pore-forming toxinedit
Schematic illustration of the evolution of the MACPF–tachylectin complex in ampullariids. Based on the genomic arrangements of the MACPF and tachylectin genes, the model proposes that a single copy of MACPF–tachylectin complex was present in the common ancestor of ampullariids. Only in the two species of Pomacea has it become highly diversified, with both MACPF-tachylectin genes that are conserved across Ampullariidae, and multiple Pomacea specific MACPF-tachylectin genes that were generated by tandem duplication. The final 1-MACPF and 2-tachylectin configuration is exclusively expressed in the albumen gland of Pomacea and the proteins detected in their eggs. Numbers below and inside gene diagram boxes are scaffold numbers and gene numbers in the scaffold, respectively. For instance, Lanistes nyassanus contains a MACPF gene (Lny_22924_0.25) and a tachylectin gene (Lny_22924_0.27) in scaffold Lny_22924. For Pomacea canaliculata, the chromosome numbers are shown above the gene diagram boxes. More details can be found in Sun et al., 2019.[8]
Proteomic analysis indicates that the MACPF and the Tachylectins are among the most abundant proteins in Pomacea eggs but are minor proteins in the genera laying eggs below the water.[9][10] According to the fossil record, some 3 MYA, when Pomacea diverged from Marisa and began laying eggs above the water, these two genes were subjected to extensive duplication and these unrelated proteins were combined by a covalent bond resulting in the dimerization into PV2 AB toxin that co-opted to new roles. This new structure rendered a novel toxin that is non-digestible, enterotoxic and neurotoxic.[3][1]
Referencesedit
^ abcdefgGiglio ML, Ituarte S, Ibañez AE, Dreon MS, Prieto E, Fernández PE, Heras H (2020). "Novel Role for Animal Innate Immune Molecules: Enterotoxic Activity of a Snail Egg MACPF-Toxin". Frontiers in Immunology. 11: 428. doi:10.3389/fimmu.2020.00428. PMC7082926. PMID 32231667.
^ abcdefDreon MS, Frassa MV, Ceolín M, Ituarte S, Qiu JW, Sun J, et al. (2013-05-30). "Novel animal defenses against predation: a snail egg neurotoxin combining lectin and pore-forming chains that resembles plant defense and bacteria attack toxins". PLOS ONE. 8 (5): e63782. Bibcode:2013PLoSO...863782D. doi:10.1371/journal.pone.0063782. PMC3667788. PMID 23737950.
^ abcdefgGiglio ML, Ituarte S, Milesi V, Dreon MS, Brola TR, Caramelo J, et al. (August 2020). "Exaptation of two ancient immune proteins into a new dimeric pore-forming toxin in snails". Journal of Structural Biology. 211 (2): 107531. doi:10.1016/j.jsb.2020.107531. hdl:11336/143650. PMID 32446810. S2CID 218873723.
^Frassa MV, Ceolín M, Dreon MS, Heras H (July 2010). "Structure and stability of the neurotoxin PV2 from the eggs of the apple snail Pomacea canaliculata". Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics. 1804 (7): 1492–1499. doi:10.1016/j.bbapap.2010.02.013. PMID 20215051.
^Heras H, Garin CF, Pollero RJ (1998). "Biochemical composition and energy sources during embryo development and in early juveniles of the snail Pomacea canaliculata (Mollusca: Gastropoda)". Journal of Experimental Zoology. 280 (6): 375–383. doi:10.1002/(SICI)1097-010X(19980415)280:6<375::AID-JEZ1>3.0.CO;2-K. ISSN 1097-010X.
^ abcHeras H, Frassa MV, Fernández PE, Galosi CM, Gimeno EJ, Dreon MS (September 2008). "First egg protein with a neurotoxic effect on mice". Toxicon. 52 (3): 481–488. doi:10.1016/j.toxicon.2008.06.022. PMID 18640143.
^Dreon MS, Fernández PE, Gimeno EJ, Heras H (June 2014). "Insights into embryo defenses of the invasive apple snail Pomacea canaliculata: egg mass ingestion affects rat intestine morphology and growth". PLOS Neglected Tropical Diseases. 8 (6): e2961. doi:10.1371/journal.pntd.0002961. PMC4063725. PMID 24945629.
^Sun J, Mu H, Ip JC, Li R, Xu T, Accorsi A, et al. (July 2019). Russo C (ed.). "Signatures of Divergence, Invasiveness, and Terrestrialization Revealed by Four Apple Snail Genomes". Molecular Biology and Evolution. 36 (7): 1507–1520. doi:10.1093/molbev/msz084. PMC6573481. PMID 30980073.
^Sun J, Zhang H, Wang H, Heras H, Dreon MS, Ituarte S, et al. (August 2012). "First proteome of the egg perivitelline fluid of a freshwater gastropod with aerial oviposition". Journal of Proteome Research. 11 (8): 4240–4248. doi:10.1021/pr3003613. hdl:11336/94414. PMID 22738194.
^Mu H, Sun J, Heras H, Chu KH, Qiu JW (February 2017). "An integrated proteomic and transcriptomic analysis of perivitelline fluid proteins in a freshwater gastropod laying aerial eggs". Journal of Proteomics. 155: 22–30. doi:10.1016/j.jprot.2017.01.006. hdl:11336/100499. PMID 28095328. S2CID 19632393.
May 04, 2024
perivitellin, pore, forming, toxin, present, perivitelline, fluid, apple, snails, pomacea, maculata, pmpv2, pomacea, canaliculata, pcpv2, this, protein, called, perivitellin, massively, accumulated, eggs, total, protein, toxin, protects, eggs, from, predators,. Perivitellin 2 PV2 is a pore forming toxin present in the egg perivitelline fluid of the apple snails Pomacea maculata PmPV2 and Pomacea canaliculata PcPV2 This protein called perivitellin is massively accumulated in the eggs 20 total protein As a toxin PV2 protects eggs from predators but it also nourishes the developing snail embryos 1 Pomacea canaliculata perivitellin 2IdentifiersOrganismPomacea canaliculata golden apple snail SymbolPcPV2Alt symbolsPV2 Contents 1 Structure and stability 2 Functions 3 Toxicity toward mammals 4 Evolution of a pore forming toxin 5 ReferencesStructure and stability editThese 172 kDa proteins are dimers of AB toxins each composed of a carbohydrate binding protein of the tachylectin family targeting module disulfide linked to a pore forming protein of the Membrane Attack Complex and Perforin MACPF family toxic unit 2 3 Like most other studied perivitellins from Pomacea snails PV2s are highly stable in a wide range of pH values and withstand gastrointestinal digestion characteristics associated with an antinutritive defense system that deters predation by lowering the nutritional value of the eggs 2 1 4 Functions editAs part of the perivitelline fluid perivitellin 2 constitutes a nutrient source for the developing embryo notably in the last stages where it is probably used as an endogenous source of energy and structural molecules during the transition to the free life 5 PV2s also play a role in a complex defense system that protects the embryos against predation 2 6 1 Pomacea maculata perivitellin 2 nbsp IdentifiersOrganismPomacea maculata giant apple snail SymbolPmPV2Alt symbolsPV2 PV2s have both lectin and perforin activities associated to the two subunits of their particular structures 2 3 As a lectin PV2s can agglutinate rabbit red blood cells and bind to the plasma membrane of intestinal cells both in vitro and in vivo 2 1 7 As a perforin PV2s are able to disrupt intestinal cells altering the plasma membrane conductance and to form large pores in artificial lipid bilayers 3 An interesting issue with these perivitellins is that the combination of two immune proteins lectin and perforin gave rise to a new toxic entity an excellent example of protein exaptation 2 3 This binary structure includes PV2s within AB toxins a group of toxins mostly described in bacteria and plants In PV2 toxins the lectin would bind to target membranes through the recognition of specific glycans acting as a delivery B subunit and then the pore forming A subunit would disrupt lipid bilayers forming large pores and leading to cell death therefore constituting a true pore forming toxin 3 Toxicity toward mammals editPV2 toxins proved to be highly toxic to mice when it enters the bloodstream LD50 96 h 0 25 mg kg i p and those receiving sublethal doses displayed neurological signs including weakness and lethargy low head and bent down position ortopneic half closed eyes taquipnea hirsute hair extreme abduction of the rear limbs paresia and were not able to support their body weight tetraplegic among others 3 6 Histopathological analyses of affected mice showed that PV2 toxins affect the dorsal horn of the spinal cord particularly on the 2nd and 3rd gray matter laminas where alters the calcium metabolism and causes neuron apoptosis 6 Apart from its neurotoxicity it has been recently shown that PV2s are also enterotoxic to mice when ingested a function that had never been ascribed to animal proteins 1 At the cellular level PV2 is cytotoxic to intestinal cells on which it causes changes in their surface morphology increasing the membrane roughness At the system level oral administration of PV2 induces large morphological changes on mice intestine mucosa reducing its absorptive surface Additionally PV2 reaches the Peyer s patches where it activates lymphoid follicles and triggers apoptosis 1 Evolution of a pore forming toxin edit nbsp Schematic illustration of the evolution of the MACPF tachylectin complex in ampullariids Based on the genomic arrangements of the MACPF and tachylectin genes the model proposes that a single copy of MACPF tachylectin complex was present in the common ancestor of ampullariids Only in the two species of Pomacea has it become highly diversified with both MACPF tachylectin genes that are conserved across Ampullariidae and multiple Pomacea specific MACPF tachylectin genes that were generated by tandem duplication The final 1 MACPF and 2 tachylectin configuration is exclusively expressed in the albumen gland of Pomacea and the proteins detected in their eggs Numbers below and inside gene diagram boxes are scaffold numbers and gene numbers in the scaffold respectively For instance Lanistes nyassanus contains a MACPF gene Lny 22924 0 25 and a tachylectin gene Lny 22924 0 27 in scaffold Lny 22924 For Pomacea canaliculata the chromosome numbers are shown above the gene diagram boxes More details can be found in Sun et al 2019 8 Proteomic analysis indicates that the MACPF and the Tachylectins are among the most abundant proteins in Pomacea eggs but are minor proteins in the genera laying eggs below the water 9 10 According to the fossil record some 3 MYA when Pomacea diverged from Marisa and began laying eggs above the water these two genes were subjected to extensive duplication and these unrelated proteins were combined by a covalent bond resulting in the dimerization into PV2 AB toxin that co opted to new roles This new structure rendered a novel toxin that is non digestible enterotoxic and neurotoxic 3 1 References edit a b c d e f g Giglio ML Ituarte S Ibanez AE Dreon MS Prieto E Fernandez PE Heras H 2020 Novel Role for Animal Innate Immune Molecules Enterotoxic Activity of a Snail Egg MACPF Toxin Frontiers in Immunology 11 428 doi 10 3389 fimmu 2020 00428 PMC 7082926 PMID 32231667 a b c d e f Dreon MS Frassa MV Ceolin M Ituarte S Qiu JW Sun J et al 2013 05 30 Novel animal defenses against predation a snail egg neurotoxin combining lectin and pore forming chains that resembles plant defense and bacteria attack toxins PLOS ONE 8 5 e63782 Bibcode 2013PLoSO 863782D doi 10 1371 journal pone 0063782 PMC 3667788 PMID 23737950 a b c d e f g Giglio ML Ituarte S Milesi V Dreon MS Brola TR Caramelo J et al August 2020 Exaptation of two ancient immune proteins into a new dimeric pore forming toxin in snails Journal of Structural Biology 211 2 107531 doi 10 1016 j jsb 2020 107531 hdl 11336 143650 PMID 32446810 S2CID 218873723 Frassa MV Ceolin M Dreon MS Heras H July 2010 Structure and stability of the neurotoxin PV2 from the eggs of the apple snail Pomacea canaliculata Biochimica et Biophysica Acta BBA Proteins and Proteomics 1804 7 1492 1499 doi 10 1016 j bbapap 2010 02 013 PMID 20215051 Heras H Garin CF Pollero RJ 1998 Biochemical composition and energy sources during embryo development and in early juveniles of the snail Pomacea canaliculata Mollusca Gastropoda Journal of Experimental Zoology 280 6 375 383 doi 10 1002 SICI 1097 010X 19980415 280 6 lt 375 AID JEZ1 gt 3 0 CO 2 K ISSN 1097 010X a b c Heras H Frassa MV Fernandez PE Galosi CM Gimeno EJ Dreon MS September 2008 First egg protein with a neurotoxic effect on mice Toxicon 52 3 481 488 doi 10 1016 j toxicon 2008 06 022 PMID 18640143 Dreon MS Fernandez PE Gimeno EJ Heras H June 2014 Insights into embryo defenses of the invasive apple snail Pomacea canaliculata egg mass ingestion affects rat intestine morphology and growth PLOS Neglected Tropical Diseases 8 6 e2961 doi 10 1371 journal pntd 0002961 PMC 4063725 PMID 24945629 Sun J Mu H Ip JC Li R Xu T Accorsi A et al July 2019 Russo C ed Signatures of Divergence Invasiveness and Terrestrialization Revealed by Four Apple Snail Genomes Molecular Biology and Evolution 36 7 1507 1520 doi 10 1093 molbev msz084 PMC 6573481 PMID 30980073 Sun J Zhang H Wang H Heras H Dreon MS Ituarte S et al August 2012 First proteome of the egg perivitelline fluid of a freshwater gastropod with aerial oviposition Journal of Proteome Research 11 8 4240 4248 doi 10 1021 pr3003613 hdl 11336 94414 PMID 22738194 Mu H Sun J Heras H Chu KH Qiu JW February 2017 An integrated proteomic and transcriptomic analysis of perivitelline fluid proteins in a freshwater gastropod laying aerial eggs Journal of Proteomics 155 22 30 doi 10 1016 j jprot 2017 01 006 hdl 11336 100499 PMID 28095328 S2CID 19632393 Retrieved from https en wikipedia org w index php title Perivitellin 2 amp oldid 1221319438, wikipedia, wiki, book, books, library,
