Identification and molecular characterization of a mucosal lectin (MeML) from the blue mussel Mytilus edulis and its potential role in particle capture

Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology

Volumn 156, Issue 4, 2010, Pages 495-501

  Pales Espinosa, Emmanuelle ^a   Perrigault, Mickael ^a   Allam, Bassem ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

Gene expression; Lectin; Mollusk; Mucocyte; Real time PCR; Suspension feeding bivalve

Indexed keywords

CALCIUM; CARBOHYDRATE; COMPLEMENTARY DNA; GLUTAMINE; LECTIN; PROLINE; PROTEIN MEML; SERINE; SIGNAL PEPTIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLOOD CELL; CALCIUM BINDING; CONTROLLED STUDY; FOOD DEPRIVATION; GILL; INTESTINE; LIP; MOLECULAR BIOLOGY; MOLECULAR RECOGNITION; MUCOSA CELL; MUSSEL; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN MOTIF; UPREGULATION;

ANIMALIA; BIVALVIA; MYTILUS EDULIS;

EID: 77953022374     PISSN: 10956433     EISSN: 15314332     Source Type: Journal    
DOI: 10.1016/j.cbpa.2010.04.004     Document Type: Article

References (68)

1. Allen P.G., and Dawidowicz E.A. Phagocytosis in Acanthamoeba. 1. A mannose receptor is responsible for the binding and phagocytosis of yeast. J. Cell. Physiol. 145 (1990) 508-513
2. Barille L., Heral M., and BarilleBoyer A.L. Ecophysiological deterministic model for Crassostrea gigas in an estuarine environment. Aquat. Living Resour. 10 (1997) 31-48
3. Beninger P.G., and Decottignies P. What makes diatoms attractive for suspensivores? The organic casing and associated organic molecules of Coscinodiscus perforatus are quality cues for the bivalve Pecten maximus. J. Plankton Res. 27 (2005) 11-17
4. Beninger P.G., Decottignies P., and Rince Y. Localization of qualitative particle selection sites in the heterorhabdic filibranch Pecten maximus (Bivalvia: Pectinidae). Mar. Ecol. Prog. Ser. 275 (2004) 163-173
5. Beninger P.G., and StJean S.D. Particle processing on the labial palps of Mytilus edulis and Placopecten magellanicus (Mollusca: Bivalvia). Mar. Ecol. Prog. Ser. 147 (1997) 117-127
6. Blobel G., and Dobberstein B. Transfer of proteins across membranes.1. Presence of proteolytically processed and unprocessed nascent immunoglobulin light-chains on membrane-bound ribosomes of Murine myeloma. J Cell Biol 67 (1975) 835-851
7. Braissant O., and Wahli W. A simplified in situ hybridization protocol using non-radioactively labeled probes to detect abundant and rare mRNAs on tissue sections. Biochemica 1 (1998) 10-16
8. Bulgheresi S., Schabussova I., Chen T., Mullin N.P., Maizels R.M., and Ott J.A. A new C-type lectin similar to the human immunoreceptor DC-SIGN mediates symbiont acquisition by a marine nematode. Appl. Environ. Microb. 72 (2006) 2950-2956
9. Childs R.A., Wright J.R., Ross G.F., Yuen C.T., Lawson A.M., Chai W.G., Drickamer K., and Feizi T. Specificity of lung surfactant protein Sp-a for both the carbohydrate and the lipid moieties of certain neutral glycolipids. J. Biol. Chem. 267 (1992) 9972-9979
10. Cognie B., Barille L., Masse G., and Beninger P.G. Selection and processing of large suspended algae in the oyster Crassostrea gigas. Mar. Ecol. Prog. Ser. 250 (2003) 145-152
11. Cognie B., Barille L., and Rince E. Selective feeding of the oyster Crassostrea gigas fed on a natural microphytobenthos assemblage. Estuaries 24 (2001) 126-134
12. Drickamer K. 2 distinct classes of carbohydrate-recognition domains in animal Lectins. J. Biol. Chem. 263 (1988) 9557-9560
13. Drickamer K. Engineering galactose-binding activity into a C-type mannose-binding protein. Nature 360 (1992) 183-186
14. Drickamer K. Evolution of Ca2+-dependent animal lectins. Prog. Nucleic Acid Res. Mol. Biol. 45 (1993) 207-232
15. Faulkner D.J. Marine natural products. Nat. Prod. Rep. 19 (2002) 1-48
16. Fisher W.S. Occurrence of agglutinins in the pallial cavity mucus of oysters. J. Exp. Mar. Biol. Ecol. 162 (1992) 1-13
17. Fisher W.S., and Dinuzzo A.R. Agglutination of bacteria and erythrocytes by serum from 6 species of marine mollusks. J. Invertebr. Pathol. 57 (1991) 380-394
18. Fountain D.W., and Campbell B.A. A lectin isolate from mucus of Helix aspersa. Comp. Biochem. Phys. B 77 (1984) 419-425
19. Frenkiel L., and Moueza M. Gill ultrastructure and symbiotic bacteria in Codakia orbicularis (Bivalvia, Lucinidae). Zoomorphology 115 (1995) 51-61
20. Furuta E., Takagi T., Yamaguchi K., and Shimozawa A. Incilaria mucus agglutinated human erythrocytes. J. Exp. Zool. 271 (1995) 340-347
21. Gourdine J.P., Markiv A., and Smith-Ravin J. The three-dimensional structure of codakine and related marine C-type lectins. Fish. Shellfish Immunol. 23 (2007) 831-839
22. Gourdine J.P., and Smith-Ravin E.J. Electrophoretic separation of gill proteins of the clam Codakia orbicularis. Prep. Biochem. Biotechnol. 32 (2002) 341-353
23. Hager K.M., and Carruthers V.B. MARveling at parasite invasion. Trends Parasitol. 24 (2008) 51-54
24. Hay M.E. Marine chemical ecology: what's known and what's next?. J. Exp. Mar. Biol. Ecol. 200 (1996) 103-134
25. Hegde R.S., and Bernstein H.D. The surprising complexity of signal sequences. Trends Biochem. Sci. 31 (2006) 563-571
26. Holmskov U., Thiel S., and Jensenius J.C. Collectins and ficolins: humoral lectins of the innate immune defense. Annu. Rev. Immunol. 21 (2003) 547-578
27. Iglesias J.I.P., Urrutia M.B., Navarro E., AlvarezJorna P., Larretxea X., Bougrier S., and Heral M. Variability of feeding processes in the cockle Cerastoderma edule (L) in response to changes in seston concentration and composition. J. Exp. Mar. Biol. Ecol. 197 (1996) 121-143
28. Jing, X., Perrigault, M., Pales Espinosa, E., Allam, B., submitted for publication. Identification and tissue expression analysis of C-type lectin in the eastern oyster, Crassostrea virginica.
29. Kenjo A., Takahashi M., Matsushita M., Endo Y., Nakata M., Mizuochi T., and Fujita T. Cloning and characterization of novel ficolins from the solitary ascidian, Halocynthia roretzi. J. Biol. Chem. 276 (2001) 19959-19965
30. Kiorboe T., and Mohlenberg F. Particle selection in suspension-feeding bivalves. Mar. Ecol. Prog. Ser. 5 (1981) 291-296
31. Koizumi N., Imai Y., Morozumi A., Imamura M., Kadotani T., Yaoi K., Iwahana H., and Sato R. Lipopolysaccharide-binding protein of Bombyx mori participates in a hemocyte-mediated defense reaction against gram-negative bacteria. J. Insect Physiol. 45 (1999) 853-859
32. Kolatkar A.R., and Weis W.I. Structural basis of galactose recognition by C-type animal lectins. J. Biol. Chem. 271 (1996) 6679-6685
33. Kvennefors E.C.E., Leggat W., Hoegh-Guldberg O., Degnan B.M., and Barnes A.C. An ancient and variable mannose-binding lectin from the coral Acropora millepora binds both pathogens and symbionts. Dev. Comp. Immunol. 32 (2008) 1582-1592
34. Livak K.J., and Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(- Delta Delta C) method. Methods 25 (2001) 402-408
35. Mann K., Weiss I.M., Andre S., Gabius H.J., and Fritz M. The amino-acid sequence of the abalone (Haliotis laevigata) nacre protein perlucin - Detection of a functional C-type lectin domain with galactose/mannose specificity. Eur. J. Biochem. 267 (2000) 5257-5264
36. Minamikawa M., Hine M., Russell S., Huber P., Duignan P., and Lumsden J.S. Isolation and partial characterization of a calcium-dependent lectin (chiletin) from the haemolymph of the flat oyster, Ostrea chilensis. Fish. Shellfish Immunol. 17 (2004) 463-476
37. Mistry A.C., Honda S., and Hirose S. Structure, properties and enhanced expression of galactose-binding C-type lectins in mucous cells of gills from freshwater Japanese eels (Anguilla japonica). Biochem. J. 360 (2001) 107-115
38. Mullin N.P., Hitchen P.G., and Taylor M.E. Mechanism of Ca2+ and monosaccharide binding to a C-type carbohydrate-recognition domain of the macrophage mannose receptor. J. Biol. Chem. 272 (1997) 5668-5681
39. Nakamura O., Watanabe T., Kamiya H., and Muramoto K. Galectin containing cells in the skin and mucosal tissues in Japanese conger eel, Conger myriaster: an immunohistochemical study. Dev. Comp. Immunol. 25 (2001) 431-437
40. Newell R.I.E., and Jordan S.J. Preferential ingestion of organic material by the american oyster Crassostrea virginica. Mar. Ecol. Prog. Ser. 13 (1983) 47-53
41. Nyholm S.V., and McFall-Ngai M.J. The winnowing: establishing the squid-vibrio symbiosis. Nat. Rev. Microbiol. 2 (2004) 632-642
42. Okamoto M., Tsutsui S., Tasumi S., Suetake H., Kikuchi K., and Suzuki Y. Tandem repeat L-rhamnose-binding lectin from the skin mucus of ponyfish, Leiognathus nuchalis. Biochem. Bioph. Res. Commun. 333 (2005) 463-469
43. Pales Espinosa E., and Allam B. Comparative growth and survival of juvenile hard clams, Mercenaria mercenaria, fed commercially available diets. Zoo Biol. 25 (2006) 513-525
44. Pales Espinosa E., Barille L., and Allam B. Use of encapsulated live microalgae to investigate pre-ingestive selection in the oyster Crassostrea gigas. J. Exp. Mar. Biol. Ecol. 343 (2007) 118-126
45. Pales Espinosa E., Perrigault M., Shumway S.E., Ward J.E., Wikfors G., and Allam B. The sweet relationship between microalgae and Crassostrea virginica: implication of carbohydrate and lectin interactions in particle selection in suspension feeding bivalves. J. Shellfish Res. 27 (2008) 1006-1007
46. Pales Espinosa E., Perrigault M., Ward J.E., Shumway S.E., and Allam B. Lectins associated with the feeding organs of the oyster Crassostrea virginica can mediate particle selection. Biol. Bull. 217 (2009) 130-141
47. Pales Espinosa, E., Perrigault, M., Shumway, S.E., Ward, J.E., Allam, B., 2010. Lectin binding patterns of microalgae: role in particle selection in suspension feeding bivalves. Biol. Bull. 218, 75-86.
48. Sharon N., and Lis H. History of lectins: from hemagglutinins to biological recognition molecules. Glycobiology 14 (2004) 53R-62R
49. Shumway S.E., Cucci T.L., Newell R.C., and Yentsch C.M. Particle selection, ingestion, and absorption in filter-feeding bivalves. J. Exp. Mar. Biol. Ecol. 91 (1985) 77-92
50. Springer S.A., Moy G.W., Friend D.S., Swanson W.J., and Vacquier V.D. Oyster sperm bindin is a combinatorial fucose lectin with remarkable intra-species diversity. Int. J. Dev. Biol. 52 (2008) 759-768
51. Stevens J., Blixt O., Glaser L., Taubenberger J.K., Palese P., Paulson J.C., and Wilson I.A. Glycan microarray analysis of the hemagglutinins from modern and pandemic influenza viruses reveals different receptor specificities. J. Mol. Biol. 355 (2006) 1143-1155
52. Tasumi S., Ohira T., Kawazoe I., Suetake H., Suzuki Y., and Aida K. Primary structure and characteristics of a lectin from skin mucus of the Japanese eel Anguilla japonica. J. Biol. Chem. 277 (2002) 27305-27311
53. Tasumi S., and Vasta G.R. A galectin of unique domain organization from hemocytes of the eastern oyster (Crassostrea virginica) is a receptor for the protistan parasite Perkinsus marinus. J. Immunol. 179 (2007) 3086-3098
54. Tripp M.R. Agglutinins in the hemolymph of the hard clam, Mercenaria mercenaria. J. Invertebr. Pathol. 59 (1992) 228-234
55. Tsutsui S., Iwamoto K., Nakamura O., and Watanabe T. Yeast-binding C-type lectin with opsonic activity from conger eel (Conger myriaster) skin mucus. Mol. Immunol. 44 (2007) 691-702
56. Tsutsui S., Yamaguchi M., Hirasawa A., Nakamura O., and Watanabe T. Common skate (Raja kenojei) secretes pentraxin into the cutaneous secretion: the first skin mucus lectin in cartilaginous fish. J. Biochem. 146 (2009) 295-306
57. Vasta G.R. Roles of galectins in infection. Nat. Rev. Microbiol. 7 (2009) 424-438
58. Vasta G.R., and Ahmed H. Animal Lectins: A Functional View (2008), Taylor and Francis (CRC Press, Boca Raton, Fl
59. Vasta G.R., Cheng T.C., and Marchalonis J.J. A lectin on the hemocyte membrane of the oyster (Crassostrea virginica). Cell. Immunol. 88 (1984) 475-488
60. Ward J.E., Levinton J.S., Shumway S.E., and Cucci T. Site of particle selection in a bivalve mollusc. Nature 390 (1997) 131-132
61. Ward J.E., Levinton J.S., Shumway S.E., and Cucci T. Particle sorting in bivalves: in vivo determination of the pallial organs of selection. Mar. Biol. 131 (1998) 283-292
62. Ward J.E., and Shumway S.E. Separating the grain from the chaff: particle selection in suspension- and deposit-feeding bivalves. J. Exp. Mar. Biol. Ecol. 300 (2004) 83-130
63. Ward J.E., and Targett N.M. Influence of marine microalgal metabolites on the feeding-behavior of the blue mussel Mytilus edulis. Mar. Biol. 101 (1989) 313-321
64. Wood-Charlson E.M., Hollingsworth L.L., Krupp D.A., and Weis V.M. Lectin/glycan interactions play a role in recognition in a coral/dinoflagellate symbiosis. Cell. Microbiol. 8 (2006) 1985-1993
65. Wootton E.C., Zubkov M.V., Jones D.H., Jones R.H., Martel C.M., Thornton C.A., and Roberts E.C. Biochemical prey recognition by planktonic protozoa. Environ. Microbiol. 9 (2007) 216-222
66. Yamaura K., Takahashi K.G., and Suzuki T. Identification and tissue expression analysis of C-type lectin and galectin in the Pacific oyster, Crassostrea gigas. Comp. Biochem. Phys. B 149 (2008) 168-175
67. Zhang H., Wang H., Wang L.L., Song X.Y., Zhao J.M., Qiu L.M., Li L., Cong M., and Song L.S. A novel C-type lectin (Cflec-3) from Chlamys farreri with three carbohydrate-recognition domains. Fish. Shellfish Immunol. 26 (2009) 707-715
68. Zheng P.L., Wang H., Zhao J.M., Song L.S., Qiu L.M., Dong C.H., Wang B., Gai Y.C., Mu C.K., Li C.H., Ni D.J., and Xing K.Z. A lectin (CfLec-2) aggregating Staphylococcus haemolyticus from scallop Chlamys farreri. Fish. Shellfish Immunol. 24 (2008) 286-293