First proteome of the egg perivitelline fluid of a freshwater gastropod with aerial oviposition

Journal of Proteome Research

Volumn 11, Issue 8, 2012, Pages 4240-4248

  Sun, Jin ^a   Zhang, Huoming ^a,d   Wang, Hao ^b   Heras, Horacio ^c   Dreon, Marcos S ^c   Ituarte, Santiago ^c   Ravasi, Timothy ^d   Qian, Pei Yuan ^b   Qiu, Jian Wen ^a  

^a HONG KONG BAPTIST UNIVERSITY   (Hong Kong)

^b HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

^c INSTITUTO DE INVESTIGACIONES BIOQUÍMICAS DE LA PLATA INIBIOLP   (Argentina)

^d KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

Author keywords

apple snail; novel protein; perivitelline fluid; Pomacea canaliculata; proteomics

Indexed keywords

PROTEOME;

ARTICLE; BODY FLUID; EGG LAYING; GASTROPOD; INFORMATION PROCESSING; INNATE IMMUNITY; LIQUID CHROMATOGRAPHY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; PERIVITELLINE FLUID; POLYACRYLAMIDE GEL ELECTROPHORESIS; POMACEA CANALICULATA; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOMICS; SNAIL; SUPPRESSION SUBTRACTIVE HYBRIDIZATION; TANDEM MASS SPECTROMETRY;

AMINO ACID MOTIFS; ANIMALS; APOCRINE GLANDS; BAYES THEOREM; CONSERVED SEQUENCE; EGG PROTEINS; FEMALE; GENE EXPRESSION; LIKELIHOOD FUNCTIONS; MOLECULAR SEQUENCE DATA; OVIPOSITION; OVUM; PHYLOGENY; PROTEIN SUBUNITS; PROTEOME; SEQUENCE ANALYSIS, DNA; SNAILS;

BASOMMATOPHORA; GASTROPODA; MALUS X DOMESTICA; POMACEA CANALICULATA;

EID: 84864614809     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr3003613     Document Type: Article

References (41)

1. Dillon, R. T. The Ecology of Freshwater Mollusks; Cambridge University Press, Cambridge, U.K., 2000.
2. Heras, H.; Dreon, M. S.; Ituarte, S.; Pollero, R. J. Egg carotenoproteins in neotropical Ampullariidae (Gastropoda: Arquitaenioglossa) Comp. Biochem. Physiol., Part C: Toxicol. Pharmacol. 2007, 146, 158-167 (Pubitemid 47064523)
3. Hayes, K. A.; Cowie, R. H.; Jørgensen, A.; Schultheiß, R.; Albrecht, C.; Thiengo, S. C. Molluscan models in evolutionary biology: apple snails (Gastropoda: Ampullariidae) as a system for addressing fundamental questions Am. Malacol. Bull. 2009, 27, 47-58
4. Cowie, R. H. Apple snails as agricultural pests: their biology, impacts, and management. In Molluscs As Crop Pests; Barker, G. M., Ed.; CABI Publishing: Wallingford, New Zealand, 2002; pp 145-192.
5. Jørgensen, A.; Kristensen, T. K.; Madsen, H. A molecular phylogeny of apple snails (Gastropoda, Caenogastropoda, Ampullariidae) with an emphasis on African species Zool. Scr. 2008, 37, 245-252 (Pubitemid 351533454)
6. Hayes, K. A.; Cowie, R. H.; Thiengo, S. C. A global phylogeny of apple snails: Gondwanan origin, generic relationships, and the influence of outgroup choice (Caenogastropoda: Ampullariidae) Biol. J. Linn. Soc. 2009, 98, 61-76
7. Heras, H.; Garin, C. F.; Pollero, R. J. Biochemical composition and energy sources during embryo development and in early juveniles of the snail Pomacea canaliculata (Mollusca: Gastropoda) J. Exp. Zool. 1998, 280, 375-383 (Pubitemid 28159300)
8. Dreon, M. S.; Schinella, G.; Heras, H.; Pollero, R. J. Antioxidant defense system in the apple snail eggs, the role of ovorubin Arch. Biochem. Biophys. 2004, 422, 1-8 (Pubitemid 38064305)
9. Heras, H.; Frassa, M. V.; Fernández, P. E.; Galosi, C. M.; Gimeno, E. J.; Dreon, M. S. First egg protein with a neurotoxic effect on mice Toxicon 2008, 52, 481-488
10. Dreon, M. S.; Ituarte, S.; Heras, H. The role of the proteinase inhibitor ovorubin in apple snail eggs resembles plant embryo defense against predation PLoS One 2010, 5, e15059
11. Cheesman, D. F. Ovorubin, a chromoprotein from the eggs of the gastropod mollusc Pomacea canaliculata Proc. R. Soc. London, Ser. B 1958, 149, 571-587
12. Garín, C. F.; Heras, H.; Pollero, R. J. Lipoproteins of the egg perivitelline fluid of Pomacea canaliculata snails (Mollusca: Gastropoda) J. Exp. Zool. 1996, 276, 307-314
13. Frassa, M. V.; Ceolín, M.; Dreon, M. S.; Heras, H. Structure and stability of the neurotoxin PV2 from the eggs of the apple snail Pomacea canaliculata Biochim. Biophys. Acta, Proteins Proteomics 2010, 1804, 1492-1499
14. Hathaway, J. J. M.; Adema, C. M.; Stout, B. A.; Mobarak, C. D.; Loker, E. S. Identification of protein components of egg masses indicates parental investment in immunoprotection of offspring by Biomphalaria glabrata (Gastropoda, Mollusca) Dev. Comp. Immunol. 2010, 34, 425-435
15. Aagaard, J. E.; Yi, X.; MacCoss, M. J.; Swanson, W. J. Rapidly evolving zona pellucida domain proteins are a major component of the vitelline envelope of abalone eggs Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 17302-17307 (Pubitemid 44788964)
16. Sun, J.; Zhang, Y.; Thiyagarajan, V.; Qian, P.-Y.; Qiu, J.-W. Protein expression during the embryonic development of a gastropod Proteomics 2010, 10, 2701-2711
17. Neuhoff, V.; Arold, N.; Taube, D.; Ehrhardt, W. Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250 Electrophoresis 1988, 9, 255-262
18. Gan, C. S.; Guo, T.; Zhang, H.; Lim, S. K.; Sze, S. K. A comparative study of electrostatic repulsion-hydrophilic interaction chromatography (ERLIC) versus SCX-IMAC-based methods for phosphopeptide isolation/enrichment J. Proteome Res. 2008, 7, 4869-4877
19. Käll, L.; Storey, J. D.; MacCoss, M. J.; Noble, W. S. Assigning significance to peptides identified by tandem mass spectrometry using decoy databases J. Proteome Res. 2007, 7, 29-34 (Pubitemid 351171110)
20. Sun, J.; Wang, M.; Wang, H.; Zhang, H.; Thiyagarajan, V.; Qian, P.-Y.; Qiu, J.-W. De novo assembly of the transcriptome of an invasive snail and its multiple ecological applications. Mol. Ecol. Resour. (submitted).
21. Ishihama, Y.; Oda, Y.; Tabata, T.; Sato, T.; Nagasu, T.; Rappsilber, J.; Mann, M. Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein Mol. Cell. Proteomics 2005, 4, 1265-1272 (Pubitemid 41448714)
22. Wang, H.; Qian, P.-Y. Involvement of a novel p38 mitogen activated protein kinase in larval metamorphosis of the polychaete Hydroides elegans (Haswell) J. Exp. Zool., Part B 2010, 314, 390-402
23. Dreon, M. S.; Heras, H.; Pollero, R. J. Metabolism of ovorubin, the major egg lipoprotein from the apple snail Mol. Cell. Biochem. 2003, 243, 9-14 (Pubitemid 36240546)
24. Ituarte, S.; Dreon, M. S.; Pasquevich, M. Y.; Fernández, P. E.; Heras, H. Carbohydrates and glycoforms of the major egg perivitellins from Pomacea apple snails (Architaenioglossa: Ampullariidae) Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol. 2010, 157, 66-72
25. Petersen, T. N.; Brunak, S.; von Heijne, G.; Nielsen, H. SignalP 4.0: discriminating signal peptides from transmembrane regions Nat. Methods 2011, 8, 785-786
26. Ronquist, F.; Huelsenbeck, J. P. MrBayes 3: Bayesian phylogenetic inference under mixed models Bioinformatics 2003, 19, 1572-1574 (Pubitemid 37038874)
27. Tamura, K.; Peterson, D.; Peterson, N.; Stecher, G.; Nei, M.; Kumar, S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods Mol. Biol. Evol. 2011, 28, 2731-2739
28. Dreon, M. S.; Heras, H.; Pollero, R. J. Characterization of the major egg glycolipoproteins from the perivitelline fluid of the apple snail Pomacea canaliculata Mol. Reprod. Dev. 2004, 68, 359-364 (Pubitemid 38650042)
29. Zhang, H.; Song, L.; Li, C.; Zhao, J.; Wang, H.; Gao, Q.; Xu, W. Molecular cloning and characterization of a thioester-containing protein from Zhikong scallop Chlamys farreri Mol. Immunol. 2007, 44, 3492-3500 (Pubitemid 46754439)
30. Zhang, H.; Song, L.; Li, C.; Zhao, J.; Wang, H.; Qiu, L.; Ni, D.; Zhang, Y. A novel C1q-domain-containing protein from Zhikong scallop Chlamys farreri with lipopolysaccharide binding activity Fish Shellfish Immunol. 2008, 25, 281-289
31. Dziarski, R. Peptidoglycan recognition proteins (PGRPs) Mol. Immunol. 2004, 40, 877-886 (Pubitemid 38032811)
32. Ritchie, R. F.; Palomaki, G. E.; Neveux, L. M.; Navolotskaia, O.; Ledue, T. B.; Craig, W. Y. Reference distributions for the negative acute-phase serum proteins, albumin, transferrin and transthyretin: a practical, simple and clinically relevant approach in a large cohort J. Clin. Lab. Anal. 1999, 13, 273-279
33. Van Eijk, M.; van Roomen, C. P.; Renkema, G. H.; Bussink, A. P.; Andrews, L.; Blommaart, E. F.; Sugar, A.; Verhoeven, A. J.; Boot, R. G.; Aerts, J. M. Characterization of human phagocyte-derived chitotriosidase, a component of innate immunity Int. Immunol. 2005, 17, 1505-1512 (Pubitemid 41631326)
34. Kimura, A. Purification and physicochemical properties of chitinase extracted from digestive tract of Helix peliomphala Tokushima J. Exp. Med. 1977, 24, 1-8 (Pubitemid 8310285)
35. Swegle, M.; Kramer, K. J.; Muthukrishnan, S. Properties of barley seed chitinases and release of embryo-associated isoforms during early stages of imbibition Plant Physiol. 1992, 99, 1009-1014
36. Dreon, M. S.; Lavarias, S.; Garin, C. F.; Heras, H.; Pollero, R. J. Synthesis, distribution, and levels of an egg lipoprotein from the apple snail Pomacea canaliculata (Mollusca: Gastropoda) J. Exp. Zool. 2002, 292, 323-330 (Pubitemid 34166144)
37. 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.; Zuniga-Pflucker, J. C.; Kroemer, G.; Penninger, J. M. Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death Nature 2001, 410, 549-554 (Pubitemid 32267191)
38. Mann, K. The chicken egg white proteome Proteomics 2007, 7, 3558-3568 (Pubitemid 47597677)
39. Liou, H. L.; Dixit, S. S.; Xu, S.; Tint, G. S.; Stock, A. M.; Lobel, P. NPC2, the protein deficient in Niemann-Pick C2 disease, consists of multiple glycoforms that bind a variety of sterols J. Biol. Chem. 2006, 281, 36710-36723 (Pubitemid 46042138)
40. Dreon, M. S.; Ceolín, M.; Heras, H. Astaxanthin binding and structural stability of the apple snail carotenoprotein ovorubin Arch. Biochem. Biophys. 2007, 460, 107-112 (Pubitemid 46482419)
41. Clark, M. S.; Thorne, M. A. S.; Toullec, J.-Y.; Meng, Y.; Guan, L. L.; Peck, L. S.; Moore, S. Antarctic krill 454 pyrosequencing reveals chaperone and stress transcriptome PLoS One 2011, 6, e15919