Biology:Perivitellins

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Perivitellins are egg proteins found in the perivitelline fluid of many gastropods. They are multifunctional complexes providing the developing embryo with nutrition, protection from the environment, and defense against predators.[1] Despite the central role perivitellins play in reproduction and development, there is little information about their role in gastropod Molluscs. Most studies of perivitellins have been performed in eggs of Ampullaridae, a family of freshwater snails (Caenogastropoda), notably the Pomacea genus, mostly those of Pomacea canaliculata, Pomacea scalaris and Pomacea maculata.[2][3]

Synthesis

Perivitellins are almost exclusively synthesized in the albumen gland (also known as albumen gland-capsule gland complex or uterine gland), an accessory gland from the female reproductive system of gastropods.[4][5] This has been experimentally confirmed for the perivitellins ovorubin (PcOvo) and PcPV2, which were only found in the albumen gland with no extra-gland synthesis, circulation or storage.[6][7][8] During the reproductive season, these perivitellins are transferred to eggs. After oviposition, they are rapidly restored in the albumen gland, decreasing their total amount in the gland only after repeated ovipositions.[4][9] In Pomacea canaliculata snails, perivitellins would act, together with the polysaccharide galactogen, as a limiting factor of the reproductive effort during reproduction.[4]

Types of perivitellins

The first studies performed in Pomacea canaliculata identified two proteins named perivitellin-1, PV1 or ovorubin (now called PcOvo) and perivitellin-2 or PV2 massively accumulated in eggs, comprising 60-70% of total protein, respectively, and a heterogeneous fraction dubbed perivitellin-3 or PV3 fraction.[10] Recent proteomic analyses of perivitelline fluids, however, identified a total of 34 proteins from Pomacea canaliculata, 38 in Pomacea maculata, and 32 in Pomacea diffusa.[11][12][13][14]

Perivitellin-1 or PcOvo (former ovorubin) and perivitellin-2 or PcPV2 are probably the best characterized from snails.[5][8][10][15][16][17][18][19] Both perivitellins are multimeric and glycosylated proteins with remarkable thermal stability up to 100°C and 60°C, respectively, and over a wide range of pH.[20][21] They are also highly resistant to the combined action of pepsin and trypsin proteases.[17][18][21]

The perivitelline fluid of Pomacea scalaris and Pomacea diffusa contain one major perivitellin, PsSC (also named scalarin) and PdPV1, respectively, which are structurally and phylogenetically related to PcOvo.[19][22][23][24] The perivitelline fluid of P. maculata is also similar, with two major perivitellins, PmPV1 and PmPV2, structurally and functionally similar to PcOvo and PcPV2, respectively.[25][26][27]

The rest of Pomacea perivitellins (over 25) have been characterized at the transcriptomic and proteomic levels, but biochemical studies are still largely missing.[28]

Perivitellin functions

Perivitellins provide nutrition, energy storage, defense against predation, and protection from the environment to the developing embryo.

A functional classification of the perivitellin aminoacid sequences based on the Kyoto Encyclopedia of Genes and Genomes (KEGG), classified them in "environmental information processing", among which several immune proteins are included, "metabolism", "organismal systems", "cellular processes", "other", and a considerable number of "unknown" proteins.

The first functional studies performed in Pomacea canaliculata, considered them mostly as storage proteins that provided energetic and structural precursors for the embryos, since they are consumed during development.[16]

Later research on PV1s (PcOvo, PmPV1, and PsSC) reported that their carotenoid cofactor, notably astaxanthin, serves as a potent antioxidant and provides the reddish color to the eggs.[1][20][25][29] These carotenoproteins are also highly resistant to gastrointestinal digestion, and withstand the passage through the digestive system without significant modifications; this characteristic was related to embryo defenses, deterring predators by lowering the nutritional value of the eggs.[8][22][26] PcOvo and PsSC also carry phosphate groups attached to serine residues that may serve as a phosphorus reserve for the embryo.[19] Unlike PcOvo and PmPV1, PsSC is also an active lectin that agglutinates bacteria and alters the gastrointestinal mucosa of rats, functions associated with embryo protection against both pathogens and predators.[19][23]

PV2s are toxins only found in Pomacea canaliculata (PcPV2) and Pomacea maculata (PmPV2) perivitelline fluid.[25][30][31] They are potent neurotoxins when intraperitoneally injected to mice, while exerting enterotoxic functions when ingested.[27][30][32] Each of the two dimeric units of either PcPV2 or PmPV2 consists of a carbohydrate-binding protein of the tachylectin family (acting as a targeting module) disulfide-linked to a pore-forming subunit of the Membrane Attack Complex and Perforin (MACPF) subfamily (toxic module).[18][27] These toxins bear a structural resemblance to botulinic and ricin heterodimeric toxins, the so-called “AB toxins” previously known only in bacteria and plants. Perivitellin-2 is also resistant to gastrointestinal digestion, which contributes to lowering the egg nutritional value.[18][32]

Finally, a recent study of Pomacea canaliculata PV3 fraction identified and characterized two protease inhibitors from the Kunitz and Kazal families, a function also related to an antipredator defense since it would prevent predators to digest proteins from the eggs when ingested.[28]

References

  1. ↑ 1.0 1.1 "Egg carotenoproteins in neotropical Ampullariidae (Gastropoda: Arquitaenioglossa)". Comparative Biochemistry and Physiology. Toxicology & Pharmacology 146 (1–2): 158–67. 2007-07-01. doi:10.1016/j.cbpc.2006.10.013. PMID 17320485. 
  2. ↑ "Insights from an Integrated View of the Biology of Apple Snails (Caenogastropoda: Ampullariidae)". Malacologia 58 (1–2): 245–302. 2015. doi:10.4002/040.058.0209. https://www.arca.fiocruz.br/handle/icict/12732. 
  3. ↑ (in en) Apple snail perivitellins, multifunctional egg proteins. Philippine Rice Research Institute. 2017. ISBN 978-621-8022-25-6. http://sedici.unlp.edu.ar/handle/10915/72238. 
  4. ↑ 4.0 4.1 4.2 "Biosynthesis in the Albumen Gland-Capsule Gland Complex Limits Reproductive Effort in the Invasive Apple Snail Pomacea canaliculata". The Biological Bulletin 235 (1): 1–11. August 2018. doi:10.1086/699200. PMID 30160995. 
  5. ↑ 5.0 5.1 "De novo assembly of the transcriptome of an invasive snail and its multiple ecological applications". Molecular Ecology Resources 12 (6): 1133–44. November 2012. doi:10.1111/1755-0998.12014. PMID 22994926. 
  6. ↑ "Synthesis, distribution, and levels of an egg lipoprotein from the apple snail Pomacea canaliculata (Mollusca: Gastropoda)". The Journal of Experimental Zoology 292 (3): 323–30. February 2002. doi:10.1002/jez.10043. PMID 11857466. 
  7. ↑ "Metabolism of ovorubin, the major egg lipoprotein from the apple snail". Molecular and Cellular Biochemistry 243 (1–2): 9–14. January 2003. doi:10.1023/a:1021616610241. PMID 12619883. 
  8. ↑ 8.0 8.1 8.2 "Characterization of the major egg glycolipoproteins from the perivitellin fluid of the apple snail Pomacea canaliculata". Molecular Reproduction and Development 68 (3): 359–64. July 2004. doi:10.1002/mrd.20078. PMID 15112330. 
  9. ↑ "Biochemical Composition of the Eggs of the Freshwater Snail Lymnaea stagnalis and Oviposition-induced Restoration of Albumen Gland Secretion". International Journal of Invertebrate Reproduction and Development 12 (2): 199–212. 1987-09-01. doi:10.1080/01688170.1987.10510317. 
  10. ↑ 10.0 10.1 "Lipoproteins of the egg perivitelline fluid of Pomacea canaliculata snails (Mollusca: Gastropoda)". The Journal of Experimental Zoology 276 (5): 307–14. December 1996. doi:10.1002/(SICI)1097-010X(19961201)276:5<307::AID-JEZ1>3.0.CO;2-S. PMID 8972583. 
  11. ↑ "First proteome of the egg perivitelline fluid of a freshwater gastropod with aerial oviposition". Journal of Proteome Research 11 (8): 4240–8. August 2012. doi:10.1021/pr3003613. PMID 22738194. 
  12. ↑ "Comparative proteomics and codon substitution analysis reveal mechanisms of differential resistance to hypoxia in congeneric snails". Journal of Proteomics 172: 36–48. February 2018. doi:10.1016/j.jprot.2017.11.002. PMID 29122728. 
  13. ↑ "Egg perivitelline fluid proteome of a freshwater snail: Insight into the transition from aquatic to terrestrial egg deposition". Rapid Communications in Mass Spectrometry 34 (7): e8605. April 2020. doi:10.1002/rcm.8605. PMID 31657488. http://sedici.unlp.edu.ar/handle/10915/127372. 
  14. ↑ "Signatures of Divergence, Invasiveness, and Terrestrialization Revealed by Four Apple Snail Genomes". Molecular Biology and Evolution 36 (7): 1507–1520. July 2019. doi:10.1093/molbev/msz084. PMID 30980073. 
  15. ↑ "Ovorubin, a chromoprotein from the eggs of the gastropod mollusc Pomacea canaliculata". Proceedings of the Royal Society of London. Series B, Biological Sciences 149 (937): 571–87. December 1958. doi:10.1098/rspb.1958.0093. PMID 13623805. Bibcode: 1958RSPSB.149..571C. 
  16. ↑ 16.0 16.1 "Biochemical composition and energy sources during embryo development and in early juveniles of the snail Pomacea canaliculata (Mollusca: Gastropoda)" (in en). Journal of Experimental Zoology 280 (6): 375–383. 1998. doi:10.1002/(SICI)1097-010X(19980415)280:6<375::AID-JEZ1>3.0.CO;2-K. ISSN 1097-010X. 
  17. ↑ 17.0 17.1 "The role of the proteinase inhibitor ovorubin in apple snail eggs resembles plant embryo defense against predation". PLOS ONE 5 (12): e15059. December 2010. doi:10.1371/journal.pone.0015059. PMID 21151935. Bibcode: 2010PLoSO...515059D. 
  18. ↑ 18.0 18.1 18.2 18.3 "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. 2013-05-30. doi:10.1371/journal.pone.0063782. PMID 23737950. Bibcode: 2013PLoSO...863782D. 
  19. ↑ 19.0 19.1 19.2 19.3 "Carbohydrates and glycoforms of the major egg perivitellins from Pomacea apple snails (Architaenioglossa: Ampullariidae)". Comparative Biochemistry and Physiology. Part B, Biochemistry & Molecular Biology 157 (1): 66–72. September 2010. doi:10.1016/j.cbpb.2010.05.004. PMID 20471490. 
  20. ↑ 20.0 20.1 "Global shape and pH stability of ovorubin, an oligomeric protein from the eggs of Pomacea canaliculata". The FEBS Journal 275 (18): 4522–30. September 2008. doi:10.1111/j.1742-4658.2008.06595.x. PMID 18673387. 
  21. ↑ 21.0 21.1 "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): 1492–9. July 2010. doi:10.1016/j.bbapap.2010.02.013. PMID 20215051. 
  22. ↑ 22.0 22.1 "Agglutinating activity and structural characterization of scalarin, the major egg protein of the snail Pomacea scalaris (d'Orbigny, 1832)". PLOS ONE 7 (11): e50115. 2012-11-20. doi:10.1371/journal.pone.0050115. PMID 23185551. Bibcode: 2012PLoSO...750115I. 
  23. ↑ 23.0 23.1 "A lectin of a non-invasive apple snail as an egg defense against predation alters the rat gut morphophysiology". PLOS ONE 13 (6): e0198361. 2018-06-01. doi:10.1371/journal.pone.0198361. PMID 29856808. Bibcode: 2018PLoSO..1398361I. 
  24. ↑ Brola, T. R.; Dreon, M. S.; Qiu, J. W.; Heras, H. (2020-01-01). "A highly stable, nondigestible lectin from Pomacea diffusa unveils clade-related protection systems in apple snail eggs" (in en). Journal of Experimental Biology 223 (19): jeb.231878. doi:10.1242/jeb.231878. ISSN 0022-0949. PMID 32719049. https://jeb.biologists.org/content/early/2020/07/26/jeb.231878. 
  25. ↑ 25.0 25.1 25.2 "The major egg reserve protein from the invasive apple snail Pomacea maculata is a complex carotenoprotein related to those of Pomacea canaliculata and Pomacea scalaris". Comparative Biochemistry and Physiology. Part B, Biochemistry & Molecular Biology 169: 63–71. March 2014. doi:10.1016/j.cbpb.2013.11.008. PMID 24291422. 
  26. ↑ 26.0 26.1 "Convergent evolution of plant and animal embryo defences by hyperstable non-digestible storage proteins". Scientific Reports 7 (1): 15848. November 2017. doi:10.1038/s41598-017-16185-9. PMID 29158565. Bibcode: 2017NatSR...715848P. 
  27. ↑ 27.0 27.1 27.2 "Exaptation of two ancient immune proteins into a new dimeric pore-forming toxin in snails". Journal of Structural Biology 211 (2): 107531. August 2020. doi:10.1016/j.jsb.2020.107531. PMID 32446810. 
  28. ↑ 28.0 28.1 "Non-digestible proteins and protease inhibitors: implications for defense of the colored eggs of the freshwater apple snail Pomacea canaliculata". Canadian Journal of Zoology 97 (6): 558–566. 2019-02-01. doi:10.1139/cjz-2018-0210. ISSN 0008-4301. http://sedici.unlp.edu.ar/handle/10915/124301. 
  29. ↑ "Antioxidant defense system in the apple snail eggs, the role of ovorubin". Archives of Biochemistry and Biophysics 422 (1): 1–8. February 2004. doi:10.1016/j.abb.2003.11.018. PMID 14725852. 
  30. ↑ 30.0 30.1 "First egg protein with a neurotoxic effect on mice". Toxicon 52 (3): 481–8. September 2008. doi:10.1016/j.toxicon.2008.06.022. PMID 18640143. 
  31. ↑ "The eggs of the apple snail Pomacea maculata are defended by indigestible polysaccharides and toxic proteins". Canadian Journal of Zoology 94 (11): 777–785. 2016-09-12. doi:10.1139/cjz-2016-0049. 
  32. ↑ 32.0 32.1 "Novel Role for Animal Innate Immune Molecules: Enterotoxic Activity of a Snail Egg MACPF-Toxin" (in English). Frontiers in Immunology 11: 428. 2020. doi:10.3389/fimmu.2020.00428. PMID 32231667. 



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