Identification, molecular characterization and expression analysis of a mucosal C-type lectin in the eastern oyster, Crassostrea virginica

Fish and Shellfish Immunology

Volumn 30, Issue 3, 2011, Pages 851-858

  Jing, Xing ^a,b   Espinosa, Emmanuelle Pales ^a   Perrigault, Mickael ^a   Allam, Bassem ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b OCEAN UNIVERSITY OF CHINA   (China)

Author keywords

Bivalve; Gene expression; Lectin; Mucocyte; QPCR

Indexed keywords

BACTERIA (MICROORGANISMS); BIVALVIA; CRASSOSTREA VIRGINICA; INVERTEBRATA; OSTREIDAE; VERTEBRATA;

EID: 79952188597     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2011.01.007     Document Type: Article

References (73)

1. Nyholm S.V., McFall-Ngai M.J. The winnowing: establishing the squid-Vibrio symbiosis. Nat Rev Microbiol 2004, 2:632-642.
2. Sperandio V., Torres A.G., Jarvis B., Nataro J.P., Kaper J.B. Bacteria-host communication: the language of hormones. Proc Natl Acad Sci U S A 2003, 100:8951-8956.
3. Cummins S.F., Degnan B.M., Nagle G.T. Characterization of Aplysia Alb-1, a candidate water-borne protein pheromone released during egg laying. Peptides 2008, 29:152-161.
4. Ferrer R.P., Zimmer R.K. The scent of danger: arginine as an olfactory cue of reduced predation risk. J Exp Biol 2007, 210:1768-1775.
5. Griffiths C.L., Richardson C.A. Chemically induced predator avoidance behaviour in the burrowing bivalve Macoma balthica. J Exp Mar Biol Ecol 2006, 331:91-98.
6. Sharon N., Lis H. History of lectins: from hemagglutinins to biological recognition molecules. Glycobiology 2004, 14:53R-62R.
7. Vasta G.R., Ahmed H. Animal lectins: a functional view 2008, CRC Press, Boca Raton.
8. Vasta G.R. Roles of galectins in infection. Nat Rev Microbiol 2009, 7:424-438.
9. Naganuma T., Ogawa T., Hirabayashi J., Kasai K., Kamiya H., Muramoto K. Isolation, characterization and molecular evolution of a novel pearl shelf lectin from a marine bivalve, Pteria penguin. Mol Divers 2006, 10:607-618.
10. Kenjo A., Takahashi M., Matsushita M., Endo Y., Nakata M., Mizuochi T., et al. Cloning and characterization of novel ficolins from the solitary ascidian, Halocynthia roretzi. J Biol Chem 2001, 276:19959-19965.
11. Tasumi S., 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 2007, 179:3086-3098.
12. Tasumi S., Ohira T., Kawazoe I., Suetake H., Suzuki Y., Aida K. Primary structure and characteristics of a lectin from skin mucus of the Japanese eel Anguilla japonica. J Biol Chem 2002, 277:27305-27311.
13. Hager K.M., Carruthers V.B. MARveling at parasite invasion. Trends Parasitol 2008, 24:51-54.
14. Rabinovich G.A., Gruppi A. Galectins as immunoregulators during infectious processes: from microbial invasion to the resolution of the disease. Parasite Immunol 2005, 27:103-114.
15. Bulgheresi S., Schabussova I., Chen T., Mullin N.P., Maizels R.M., 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 2006, 72:2950-2956.
16. Wood-Charlson E.M., Hollingsworth L.L., Krupp D.A., Weis V.M. Lectin/glycan interactions play a role in recognition in a coral/dinoflagellate symbiosis. Cell Microbiol 2006, 8:1985-1993.
17. Springer S.A., Moy G.W., Friend D.S., Swanson W.J., Vacquier V.D. Oyster sperm bindin is a combinatorial fucose lectin with remarkable intra-species diversity. Int J Dev Biol 2008, 52:759-768.
18. Pales Espinosa E., Perrigault M., Ward J.E., Shumway S.E., Allam B. Lectins associated with the feeding organs of the oyster, Crassostrea virginica, can mediate particle selection. Biol Bull 2009, 217:130-141.
19. Pales Espinosa E., Perrigault M., Ward J.E., Shumway S.E., Allam B. Microalgal cell surface carbohydrates as recognition sites for particle sorting in suspension-feeding bivalves. Biol Bull 2010, 218:75-86.
20. Fisher W.S., Dinuzzo A.R. Agglutination of bacteria and erythrocytes by serum from 6 species of marine mollusks. J Invertebr Pathol 1991, 57:380-394.
21. Koizumi N., Imai Y., Morozumi A., Imamura M., Kadotani T., Yaoi K., et al. Lipopolysaccharide-binding protein of Bombyx mori participates in a hemocyte-mediated defense reaction against gram-negative bacteria. J Insect Physiol 1999, 45:853-859.
22. Yu X.Q., Kanost M.R. Immulectin-2, a pattern recognition receptor that stimulates hemocyte encapsulation and melanization in the tobacco hornworm, Manduca sexta. Dev Comp Immunol 2004, 28:891-900.
23. Holmskov U., Thiel S., Jensenius J.C. Collectins and ficolins: humoral lectins of the innate immune defense. Annu Rev Immunol 2003, 21:547-578.
24. Yu X.Q., Gan H., Kanost M.R. Immulectin, an inducible C-type lectin from an insect, Manduca sexta, stimulates activation of plasma prophenol oxidase. Insect Biochem Mol Biol 1999, 29:585-597.
25. Suzuki T., Takagi T., Furukohri T., Kawamura K., Nakauchi M. A calcium-dependent galactose-binding lectin from the tunicate Polyandrocarpa misakiensis. Isolation, characterization and amino acid sequence. J Biol Chem 1990, 265:1274-1281.
26. Wang H., Song L.S., Li C.H., Zhao J.M., Zhang H., Ni D.J., et al. Cloning and characterization of a novel C-type lectin from zhikong scallop Chlamys farreri. Mol Immunol 2007, 44:722-731.
27. Zhu L., Song L.S., Xu W., Qian P.Y. Molecular cloning and immune responsive expression of a novel C-type lectin gene from bay scallop Argopecten irradians. Fish Shellfish Immunol 2008, 25:231-238.
28. Gourdine J.P., Markiv A., Smith-Ravin J. The three-dimensional structure of codakine and related marine C-type lectins. Fish Shellfish Immunol 2007, 23:831-839.
29. Moy G.W., Springer S.A., Adams S.L., Swanson W.J., Vacquier V.D. Extraordinary intraspecific diversity in oyster sperm bindin. Proc Natl Acad Sci U S A 2008, 105:1993-1998.
30. Springer S.A., Crespi B.J. Adaptive gamete-recognition divergence in a hybridizing Mytilus population. Evolution 2007, 61:772-783.
31. Wootton E.C., Zubkov M.V., Jones D.H., Jones R.H., Martel C.M., Thornton C.A., et al. Biochemical prey recognition by planktonic protozoa. Environ Microbiol 2007, 9:216-222.
32. Allen P.G., Dawidowicz E.A. Phagocytosis in Acanthamoeba .1. A mannose receptor is responsible for the binding and phagocytosis of yeast. J Cell Physiol 1990, 145:508-513.
33. Fisher W.S. Occurrence of agglutinins in the pallial cavity mucus of oysters. J Exp Mar Biol Ecol 1992, 162:1-13.
34. Pales Espinosa E., Perrigault M., Shumway S.E., Ward J.E., Wikfors G., 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 2008, 27:1006-1007.
35. Pales Espinosa E., Perrigault M., Allam B. Identification and molecular characterization of a mucosal lectin (MeML) from the blue mussel Mytilus edulis and its potential role in particle capture. Comp Biochem Physiol A-Mol Integr Physiol 2010, 156:495-501.
36. Pales Espinosa E., Hassan D., Ward J.E., Shumway S.E., Allam B. Role of epicellular molecules in the selection of particles by the blue mussel, Mytilus edulis. Biol Bull 2011, 219:50-60.
37. Yamaura K., Takahashi K.G., Suzuki T. Identification and tissue expression analysis of C-type lectin and galectin in the pacific oyster, Crassostrea gigas. Comp Biochem Physiol B 2008, 149:168-175.
38. Scotto-Lavino E., Du G.W., Frohman M.A. 5′ end cDNA amplification using classic RACE. Nat Protoc 2006, 1:2555-2562.
39. Scotto-Lavino E., Du G.W., Frohman M.A. 3′ End cDNA amplification using classic RACE. Nat Protoc 2006, 1:2742-2745.
40. Braissant O., Wahli W. A simplified in situ hybridization protocol using non-radioactively labeled probes to detect abundant and rare mRNAs on tissue sections. Biochemica 1998, 1:10-16.
41. Pales Espinosa E., Allam B. Comparative growth and survival of juvenile hard clams, Mercenaria mercenaria, fed commercially available diets. Zoo Biol 2006, 25:513-525.
42. Cognie B., Barille L. Does bivalve mucus favour the growth of their main food source, microalgae?. Oceanol Acta 1999, 22:441-450.
43. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-delta delta C) method. Methods 2001, 25:402-408.
44. +-dependent animal lectins. Prog Nucleic Acid Res Mol Biol 1993, 45:207-232.
45. Drickamer K. 2 distinct classes of carbohydrate-recognition domains in animal lectins. J Biol Chem 1988, 263:9557-9560.
46. Blobel G., 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 1975, 67:835-851.
47. Hegde R.S., Bernstein H.D. The surprising complexity of signal sequences. Trends Biochem Sci 2006, 31:563-571.
48. Tsutsui S., Iwamoto K., Nakamura O., Watanabe T. Yeast-binding C-type lectin with opsonic activity from conger eel (Conger myriaster) skin mucus. Mol Immunol 2007, 44:691-702.
49. Suzuki Y., Kaneko T. Demonstration of the mucous hemagglutinin in the club cells of eel skin. Dev Comp Immunol 1986, 10:509-518.
50. Tsutsui S., Yamaguchi M., Hirasawa A., Nakamura O., Watanabe T. Common skate (Raja kenojei) secretes pentraxin into the cutaneous secretion: the first skin mucus lectin in cartilaginous fish. J Biochem 2009, 146:295-306.
51. Okamoto M., Tsutsui S., Tasumi S., Suetake H., Kikuchi K., Suzuki Y. Tandem repeat l-rhamnose-binding lectin from the skin mucus of ponyfish, Leiognathus nuchalis. Biochem Biophys Res Commun 2005, 333:463-469.
52. Suzuki Y., Tasumi S., Tsutsui S., Okamoto M., Suetake H. Molecular diversity of skin mucus lectins in fish. Comp Biochem Physiol B 2003, 136:723-730.
53. Kvennefors E.C.E., Leggat W., Hoegh-Guldberg O., Degnan B.M., Barnes A.C. An ancient and variable mannose-binding lectin from the coral Acropora millepora binds both pathogens and symbionts. Dev Comp Immunol 2008, 32:1582-1592.
54. Furuta E., Takagi T., Yamaguchi K., Shimozawa A. Incilaria mucus agglutinated human erythrocytes. J Exp Zool 1995, 271:340-347.
55. Fountain D.W., Campbell B.A. A lectin isolate from mucus of Helix aspersa. Comp Biochem Physiol B 1984, 77:419-425.
56. + and monosaccharide binding to a C-type carbohydrate-recognition domain of the macrophage mannose receptor. J Biol Chem 1997, 272:5668-5681.
57. Kolatkar A.R., Weis W.I. Structural basis of galactose recognition by C-type animal lectins. J Biol Chem 1996, 271:6679-6685.
58. Drickamer K. Engineering galactose-binding activity into a C-type mannose-binding protein. Nature 1992, 360:183-186.
59. Childs R.A., Wright J.R., Ross G.F., Yuen C.T., Lawson A.M., Chai W.G., et al. Specificity of lung surfactant protein Sp-A for both the carbohydrate and the lipid moieties of certain neutral glycolipids. J Biol Chem 1992, 267:9972-9979.
60. Ward J.E., Levinton J.S., Shumway S.E., Cucci T. Particle sorting in bivalves: in vivo determination of the pallial organs of selection. Mar Biol 1998, 131:283-292.
61. Defossez J.M., Daguzan J. About preferential ingestion of organic matter by bivalves. J Mollus Stud 1996, 62:394-397.
62. Luo T., Yang H.J., Li F., Zhang X.B., Xu X. Purification, characterization and cDNA cloning of a novel lipopolysaccharide-binding lectin from the shrimp Penaeus monodon. Dev Comp Immunol 2006, 30:607-617.
63. Kondo M., Matsuyama H., Yano T. The opsonic effect of lectin on phagocytosis by hemocytes of kuruma prawn, Penaeus japonicus. Fish Pathol 1992, 27:217-222.
64. Kim Y.M., Park K.I., Choi K.S., Alvarez R.A., Cummings R.D., Cho M. Lectin from the manila clam Ruditapes philippinarum is induced upon infection with the protozoan parasite Perkinsus olseni. J Biol Chem 2006, 281:26854-26864.
65. Schroder H.C., Ushijima H., Krasko A., Gamulin V., Thakur N.L., Diehl-Seifert B., et al. Emergence and disappearance of an immune molecule, an antimicrobial lectin, in basal Metazoa - a tachylectin-related protein in the sponge Suberites domuncula. J Biol Chem 2003, 278:32810-32817.
66. Hatakeyama T., Suenaga T., Eto S., Niidome T., Aoyagi H. Antibacterial activity of peptides derived from the C-terminal region of a hemolytic lectin, CEL-III, from the marine invertebrate Cucumaria echinata. J Biochem 2004, 135:65-70.
67. Chen C.L., Durrant H.J., Newton R.P., Ratcliffe N.A. A study of novel lectins and their involvement in the activation of the prophenoloxidase system in Blaberus discoidalis. Biochem J 1995, 310:23-31.
68. Ling E.J., Yu X.Q. Cellular encapsulation and melanization are enhanced by immulectins, pattern recognition receptors from the tobacco hornworm Manduca sexta. Dev Comp Immunol 2006, 30:289-299.
69. Ma T.H.T., Benzie J.A.H., He J.G., Chan S.M. PmLT, a C-type lectin specific to hepatopancreas is involved in the innate defense of the shrimp Penaeus monodon. J Invertebr Pathol 2008, 99:332-341.
70. Kim J.Y., Kim Y.M., Cho S.K., Choi K.S., Cho M. Noble tandem-repeat galectin of Manila clam Ruditapes philippinarum is induced upon infection with the protozoan parasite Perkinsus olseni. Dev Comp Immunol 2008, 32:1131-1141.
71. Kang Y.S., Kim Y.M., Park K.I., Cho S.K., Choi K.S., Cho M. Analysis of EST and lectin expressions in hemocytes of Manila clams (Ruditapes philippinarum) (Bivalvia: Mollusca) infected with Perkinsus olseni. Dev Comp Immunol 2006, 30:1119-1131.
72. Perrigault M., Tanguy A., Allam B. Identification and expression of differentially expressed genes in the hard clam, Mercenaria mercenaria, in response to quahog parasite unknown (QPX). BMC Genomics 2009, 10:17.
73. Allam B., Paillard C., Auffret M. Alterations in hemolymph and extrapallial fluid parameters in the Manila clam, Ruditapes philippinarum, challenged with the pathogen Vibrio tapetis. J Invertebr Pathol 2000, 76:63-69.