Analysis of albumen gland proteins suggests survival strategies of developing embryos of Pomacea canaliculata

References

• Allam, B., Pales Espinosa, E., Tanguy, A., Jeffroy, F., Le Bris, C. & Paillard, C. (2014) Transcriptional changes in manila clam (Ruditapes philippinarum) in response to brown ring disease. Fish & Shellfish Immunology 41, 2–11. doi: 10.1016/j.fsi.2014.05.022
   PubMed Web of Science ®Google Scholar
• Arockiaraj, J., Vanaraja, P., Easwvaran, S., Singh, A., Alinejaid, T., Othman, R.Y. & Bhassu, S. (2011) Gene profiling and characterization of arginine kinase-1 (MrAK-1) from freshwater giant prawn (Macrobrachium rosenbergii). Fish & Shellfish Immunology 31, 81–89. doi: 10.1016/j.fsi.2011.04.004
   PubMed Web of Science ®Google Scholar
• Baibai, T., Oukhattar, L., Mountassif, D., Assobhei, O., Serrano, A. & Soukri, A. (2010) Comparative molecular analysis of evolutionarily distant glyceraldehydes-3-phosphate dehydrogenase from Sardina pilchardus and Octopus vulgaris. Acta Biochimica et Biophysica Sinica 42, 863–872. doi: 10.1093/abbs/gmq103
   PubMed Web of Science ®Google Scholar
• Benkendorff, K., Davis, A.R. & Bremner, J.B. (2001) Chemical defense in the egg masses of benthic invertebrates: an assessment of antibacterial activity in 39 mollusks and 4 polychaetes. Journal of Invertebrate Pathology 78, 109–118. doi: 10.1006/jipa.2001.5047
   PubMed Web of Science ®Google Scholar
• Bulat, T., Smidak, R., Sialana, F.J., Jung, G., Rattei, T., Bilban, M., Sattmann, H., Lubec, G., Aradska, J. & Song, L. (2016) Transcriptomic and proteomic analysis of Arion vulgaris—proteins for probably successful survival strategies? PLOS ONE 11, e0150614. doi: 10.1371/journal.pone.0150614
   PubMed Web of Science ®Google Scholar
• Burks, R.L., Kyle, C.H. & Trawick, M.K. (2010) Pink eggs and snails: field oviposition patterns of an invasive snail, Pomacea insularum, indicate a preference for an invasive macrophyte. Hydrobiologia 646, 243–251. doi: 10.1007/s10750-010-0167-1
   Web of Science ®Google Scholar
• Carland, T.M. & Gerwick, L. (2010) The C1q domain containing proteins: where do they come from and what do they do? Developmental & Comparative Immunology 34, 785–790. doi: 10.1016/j.dci.2010.02.014
   PubMed Web of Science ®Google Scholar
• Chen, G.F., Zhang, C.Y., Wang, Y.Y., Guo, C.L., Sang, F.M. & Wang, C.M. (2016) Identification and characterization of a ferritin gene involved in the immune defense response of scallop Chlamys farreri. Fish & Shellfish Immunology 55, 1–9. doi: 10.1016/j.fsi.2016.04.128
   PubMed Web of Science ®Google Scholar
• Christeller, J.T. (2005) Evolutionary mechanisms acting on proteinase inhibitor variability. FEBS Journal 272, 5710–5722. doi: 10.1111/j.1742-4658.2005.04975.x
   PubMed Web of Science ®Google Scholar
• Chye, M.-L., Sin, S.-F., Xu, Z.-F. & Yeung, E.C. (2006) Serine proteinase inhibitor proteins: exogenous and endogenous functions. In Vitro Cellular & Developmental Biology—Plant 42, 100–108. doi: 10.1079/IVP2005741
   Web of Science ®Google Scholar
• Dreon, M.S., Schinella, G., Heras, H. & Pollero, R.J. (2004) Antioxidant defense system in the apple snail eggs, the role of ovorubin. Archives of Biochemistry and Biophysics 422, 1–8. doi: 10.1016/j.abb.2003.11.018
   PubMed Web of Science ®Google Scholar
• Dreon, M.S., Ituarte, S., Heras, H. & Hofmann, A. (2010) The role of the proteinase inhibitor ovorubin in apple snail eggs resembles plant embryo defense against predation. PLOS ONE 5, 1–9. doi: 10.1371/journal.pone.0015059
   Web of Science ®Google Scholar
• Dreon, M.S., Frassa, M.V., Ceolín, M., Ituarte, S., Qiu, J.-W., Sun, J., Fernández, P.E., Heras, H. & van der Goot, F.G. (2013) 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, 1–11. doi: 10.1371/journal.pone.0063782
   Web of Science ®Google Scholar
• Dreon, M.S., Fernández, P.E., Gimeno, E.J., & Heras, H. (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, 1–10. doi: 10.1371/journal.pntd.0002961
   Web of Science ®Google Scholar
• Estebenet, A.L. & Martin, P.R. (2002) Pomacea canaliculata (Gastropoda: Ampullariidae): life-history traits and their plasticity. Biocell 26, 83–89.
   PubMed Web of Science ®Google Scholar
• Gestal, C., Pallavicini, A., Venier, P., Novoa, B. & Figueras, A. (2010) MgC1q, a novel C1q-domain-containing protein involved in the immune response of Mytilus galloprovincialis. Developmental & Comparative Immunology 34, 926–934. doi: 10.1016/j.dci.2010.02.012
   PubMed Web of Science ®Google Scholar
• Hayes, K.A., Cowie, R.H., Thiengo, S.C. & Strong, E.E. (2012) Comparing apples with apples: clarifying the identities of two highly invasive Neotropical Ampullariidae (Caenogastropoda). Zoological Journal of the Linnean Society 166, 723–753. doi: 10.1111/j.1096-3642.2012.00867.x
   Web of Science ®Google Scholar
• Heras, H., Garin, C.F. & Pollero, R.J. (1998) Biochemical composition and energy sources during embryo development and in early juveniles of the snail Pomacea canaliculata (Mollusca: Gastropoda). The Journal of Experimental Zoology 280, 375–383. doi: 10.1002/(SICI)1097-010X(19980415)280:6<375::AID-JEZ1>3.0.CO;2-K
   Google Scholar
• Heras, H., Frassa, M.V., Fernández, P.E., Galosi, C.M., Gimeno, E.J. & Dreon, M.S. (2008) First egg protein with a neurotoxic effect on mice. Toxicon 52, 481–488. doi: 10.1016/j.toxicon.2008.06.022
   PubMed Web of Science ®Google Scholar
• Joza, N., Susin, S.A., Daugas, E., Stanford, W.L., Cho, S.K., Li, C.Y.J., Sasaki, T., Elia, A.J., Cheng, H.-Y.M., Ravagnan, L., Ferri, K.F., Zamzami, N., Wakeham, A., Hakem, R., Yoshida, H., Kong, Y.-Y., Mak, T.W., Zúñiga-Pflucker, J.C., Kroemer, G. & Penninger, J.M. (2001) Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death. Nature 410, 549–554. doi: 10.1038/35069004
   PubMed Web of Science ®Google Scholar
• Kamiya, H., Sakai, R. & Jimbo, M. (2006) Bioactive molecules from sea hares. Progress in Molecular and Subcellular Biology 43, 215–239. doi: 10.1007/978-3-540-30880-5_10
   PubMedGoogle Scholar
• Kamler, E. (2005) Parent–egg–progeny relationships in teleost fishes: an energetics perspective. Reviews in Fish Biology and Fisheries 15, 399–421. doi: 10.1007/s11160-006-0002-y
   Web of Science ®Google Scholar
• Kong, P., Zhang, H., Wang, L., Zhou, Z., Yang, J., Zhang, Y., Qiu, L., Wang, L. & Song, L. (2010) AiC1qDC-1, a novel gC1q-domain-containing protein from bay scallop Argopecten irradians with fungi agglutinating activity. Developmental & Comparative Immunology 34, 837–846. doi: 10.1016/j.dci.2010.03.006
   PubMed Web of Science ®Google Scholar
• Mukai, S.T., Hoque, T., Morishita, F. & Saleuddin, A.S.M. (2004) Cloning and characterization of a candidate nutritive glycoprotein from the albumen gland of the freshwater snail, Helisoma duryi (Mollusca: Pulmonata). Invertebrate Biology 1, 83–92.
   Google Scholar
• Nagle, G.T., de Jong-Brink, M., Painter, S.D. & Li, K.W. (2001) Structure, localization and potential role of a novel molluscan trypsin inhibitor in Lymnaea. European Journal of Biochemistry 268, 1213–1221. doi: 10.1046/j.1432-1327.2001.01972.x
   PubMedGoogle Scholar
• Norden, D.A. (1972) The inhibition of trypsin and some other proteases by ovorubin, a protein from the eggs of Pomacea canaliculata. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 42, 569–576. doi: 10.1016/0305-0491(72)90319-7
   PubMed Web of Science ®Google Scholar
• Pasquevich, M.Y., Dreon, M.S. & Heras, H. (2014) 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 and Molecular Biology 169, 63–71. doi: 10.1016/j.cbpb.2013.11.008
   PubMed Web of Science ®Google Scholar
• Qiu, Y., Xi, J., Du, L. & Poovaiah, B.W. (2012) The function of calreticulin in plant immunity. Plant Signaling & Behavior 7, 907–910. doi: 10.4161/psb.20721
   PubMedGoogle Scholar
• Sanchez, J.-F., Lescar, J., Chazalet, V., Audfray, A., Gagnon, J., Alvarez, R., Breton, C., Imberty, A. & Mitchell, E.P. (2006) Biochemical and structural analysis of Helix pomatia agglutinin: a hexameric lectin with a novel fold. Journal of Biological Chemistry 281, 20171–20180. doi: 10.1074/jbc.M603452200
   PubMed Web of Science ®Google Scholar
• Santoro, M.G. (2000) Heat shock factors and the control of the stress response. Biochemical Pharmacology 59, 55–63. doi: 10.1016/S0006-2952(99)00299-3
   PubMed Web of Science ®Google Scholar
• Sun, J., Zhang, H., Wang, H., Heras, H., Dreon, M.S., Ituarte, S., Ravasi, T., Qian, P.-Y. & Qiu, J.-W. (2012) First proteome of the egg perivitelline fluid of a freshwater gastropod with aerial oviposition. Journal of Proteome Research 11, 4240–4248. doi: 10.1021/pr3003613
   PubMed Web of Science ®Google Scholar
• Tahtouh, M., Croq, F., Vizioli, J., Sautiere, P.-E., Van Camp, C., Salzet, M., Daha, M.R., Pestel, J. & Lefebvre, C. (2009) Evidence for a novel chemotactic C1q domain-containing factor in the leech nerve cord. Molecular Immunology 46, 523–531. doi: 10.1016/j.molimm.2008.07.026
   PubMed Web of Science ®Google Scholar
• Thiyagarajan, V. & Qian, P.-Y. (2008) Proteomic analysis of larvae during development, attachment, and metamorphosis in the fouling barnacle, Balanus amphitrite. Proteomics 8, 3164–3172. doi: 10.1002/pmic.200700904
   PubMed Web of Science ®Google Scholar
• Vasta, G.R. (2009) Roles of galectins in infection. Nature Reviews Microbiology 7, 424–438. doi: 10.1038/nrmicro2146
   PubMed Web of Science ®Google Scholar
• Vasta, G.R., Ahmed, H., Tasumi, S., Odom, E.W. & Saito, K. (2007) Biological roles of lectins in innate immunity: molecular and structural basis for diversity in self/non-self recognition. Advances in Experimental Medicine and Biology 598, 389–406. doi: 10.1007/978-0-387-71767-8_27
   PubMed Web of Science ®Google Scholar
• Vasta, G.R., Feng, C., Bianchet, M.A., Bachvaroff, T.R. & Tasumi, S. (2015) Structural, functional, and evolutionary aspects of galectins in aquatic mollusks: from a sweet tooth to the Trojan horse. Fish & Shellfish Immunology 46, 94–106. doi: 10.1016/j.fsi.2015.05.012
   PubMed Web of Science ®Google Scholar
• Wang, L., Wang, L., Zhang, H., Zhou, Z., Siva, V.S. & Song, L. (2012) A C1q domain containing protein from scallop Chlamys farreri serving as pattern recognition receptor with heat-aggregated IgG binding activity. PLOS ONE 7, 1–12.
   Web of Science ®Google Scholar
• Wiśniewski, J.R., Zougman, A., Nagaraj, N. & Mann, M. (2009) Universal sample preparation method for proteome analysis. Nature Methods 6, 359–362. doi: 10.1038/nmeth.1322
   PubMed Web of Science ®Google Scholar
• Xu, T., Xie, J., Li, J., Luo, M., Ye, S. & Wu, X. (2012) Identification of expressed genes in cDNA library of hemocytes from the RLO-challenged oyster, Crassostrea ariakensis Gould with special functional implication of three complement-related fragments (CaC1q1, CaC1q2 and CaC3). Fish & Shellfish Immunology 32, 1106–1116. doi: 10.1016/j.fsi.2012.03.012
   PubMed Web of Science ®Google Scholar
• Youens, A.K. & Burks, R.L. (2008) Comparing apple snails with oranges: the need to standardize measuring techniques when studying Pomacea. Aquatic Ecology 42, 679–684. doi: 10.1007/s10452-007-9140-0
   Web of Science ®Google Scholar
• Yu, Y., Huang, H., Wang, Y., Yu, Y., Yuan, S., Huang, S., Pan, M., Feng, K. & Xu, A. (2008) A novel C1q family member of amphioxus was revealed to have a partial function of vertebrate C1q molecule. The Journal of Immunology 181, 7024–7032. doi: 10.4049/jimmunol.181.10.7024
   PubMed Web of Science ®Google Scholar
• Yusa, Y. (2001) Predation on eggs of the apple snail Pomacea canaliculata (Gastropoda: Ampullariidae) by the fire ant Solenopsis geminata. Journal of Molluscan Studies 67, 275–279. doi: 10.1093/mollus/67.3.275
   Web of Science ®Google Scholar
• Zhang, H., Song, L., Li, C., Zhao, J., Wang, H., Qiu, L., Ni, D. & Zhang, Y. (2008) A novel C1q-domain-containing protein from Zhikong scallop Chlamys farreri with lipopolysaccharide binding activity. Fish & Shellfish Immunology 25, 281–289. doi: 10.1016/j.fsi.2008.06.003
   PubMed Web of Science ®Google Scholar
• Zhang, Q., Wang, X.-Q., Jiang, H.-S., Jia, W.-M., Zhao, X.-F. & Wang, J.-X. (2014) Calnexin functions in antibacterial immunity of Marsupenaeus japonicus. Developmental & Comparative Immunology 46, 356–363. doi: 10.1016/j.dci.2014.05.009
   PubMed Web of Science ®Google Scholar