Immune roles of a rhamnose-binding lectin in the colonial ascidian Botryllus schlosseri

Immunobiology

Volumn 216, Issue 6, 2011, Pages 725-736

  Franchi, Nicola ^a   Schiavon, Filippo ^a   Carletto, Matteo ^a   Gasparini, Fabio ^a   Bertoloni, Giulio ^b   Tosatto, Silvio C E ^a   Ballarin, Loriano ^a  

^a UNIVERSITY OF PADOVA   (Italy)

^b Department of Histology Microbiology and Medical Biotechnology ^*  (Italy)

Author keywords

Botryllus; Compound ascidians; Haemocytes; Rhamnose binding lectin; Tunicates

Indexed keywords

INTERLEUKIN 1ALPHA; LECTIN; MONOPHENOL MONOOXYGENASE; PEROXIDE; REACTIVE OXYGEN METABOLITE; RHAMNOSE BINDING LECTIN; SUPEROXIDE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; ASCIDIACEA; BOTRYLLUS SCHLOSSERI; CELL AGGLUTINATION; CONTROLLED STUDY; CYTOKINE RESPONSE; CYTOSKELETON; DEGRANULATION; ENZYME RELEASE; FEMALE; IMMUNE RESPONSE; INNATE IMMUNITY; MOLECULAR INTERACTION; MORULA; NONHUMAN; PHAGOCYTE; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RESPIRATORY BURST;

AGGLUTINATION; AMINO ACID SEQUENCE; ANIMALS; BACTERIA; CELL DEGRANULATION; CELLS, CULTURED; ERYTHROCYTES; INTERLEUKIN-1ALPHA; LECTINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHAGOCYTES; PROTEIN BINDING; PROTEIN CONFORMATION; RABBITS; RHAMNOSE; SEQUENCE ALIGNMENT; TUMOR NECROSIS FACTOR-ALPHA; UROCHORDATA; YEASTS;

EID: 79955536128     PISSN: 01712985     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.imbio.2010.10.011     Document Type: Article

References (79)

1. Albrecht M., Tosatto S.C.E., Lengauer T., Valle G. Simple consensus procedures are effective and sufficient in secondary structure prediction. Protein Eng. 2003, 16:459-462.
2. Angata T., Brinkman-Van der Linden E.C.M. I-type lectins. Biochim. Biophys. Acta 2002, 1572:294-316.
3. Arason G.J. Lectins as defence molecules in vertebrates and invertebrates. Fish Shellfish Immunol. 1996, 6:277-289.
4. Ballarin L. Immunobiology of compound ascidians, with particular reference to Botryllus schlosseri: state of art. Invertebr. Survival J. 2008, 5:54-74.
5. Ballarin L., Cima F. Cytochemical properties of Botryllus schlosseri haemocytes: indications for morpho-functional characterisation. Eur. J. Histochem. 2005, 49:255-264.
6. Ballarin L., Cima F., Sabbadin A. Phagocytosis in the colonial ascidian Botryllus schlosseri. Dev. Comp. Immunol. 1994, 18:467-481.
7. Ballarin L., Cima F., Sabbadin A. Phenoloxidase and cytotoxicity in the compound ascidian Botryllus schlosseri. Dev. Comp. Immunol. 1998, 22:479-492.
8. Ballarin L., Tonello C., Sabbadin A. Humoral opsonin from the colonial ascidian Botryllus schlosseri as a member of the galectin family. Mar. Biol. 2000, 136:813-822.
9. Ballarin L., Franchini A., Ottaviani E., Sabbadin A. Morula cells as the main immunomodulatory haemocytes in ascidians: evidences from the colonial species Botryllus schlosseri. Biol. Bull. 2001, 201:59-64.
10. Ballarin L., Menin A., Franchi N., Bertoloni G., Cima F. Morula cells and non-self recognition in the compound ascidian Botryllus schlosseri. Invertebr. Survival J. 2005, 2:1-5.
11. Ballarin L., Menin A., Tallandini L., Matozzo V., Burighel P., Basso G., Fortunato E., Cima F. Haemocytes and blastogenetic cycle in the colonial ascidian Botryllus schlosseri: a matter of life and death. Cell Tissue Res. 2008, 331:555-564.
12. Ballarin L., Burighel P., Cima F. A tale of death and life: natural apoptosis in the colonial ascidian Botryllus schlosseri (Urochordata, Ascidiacea). Curr. Pharm. Des. 2008, 14:138-147.
13. Ballarin L., Cammarata M., Cima F., Grimaldi A., Lorenzon S., Malagoli D., Ottaviani E. Immune-neuroendocrine biology of invertebrates: a collection of methods. Invertebr. Survival J. 2008, 5:192-215.
14. Ballarin L., Schiavon F., Manni L. Natural apoptosis during the blastogenetic cycle of the colonial ascidian Botryllus schlosseri: a morphological analysis. Zool. Sci. 2010, 27:96-102.
15. Benkert P., Tosatto S.C., Schomburg D. QMEAN: a comprehensive scoring function for model quality assessment. Proteins 2008, 71:261-277.
16. Benkert P., Tosatto S.C., Schwede T. Global and local model quality estimation at CASP8 using the scoring functions QMEAN and QMEANclust. Proteins 2009, 77(Suppl. 9):173-180.
17. Berrill N.J. The development of the bud in Botryllus. Biol. Bull. 1941, 80:169-184.
18. Bindewald E., Cestaro A., Hesser J., Heiler M., Tosatto S.C.E. MANIFOLD: protein fold recognition based on secondary structure, sequence similarity and enzyme classification. Protein Eng. 2003, 16:785-789.
19. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal. Biochem. 1976, 72:248-254.
20. Brewer C.F. Binding and cross-linking properties of galectins. Biochim. Biophys. Acta 2002, 1575:255-262.
21. Brown F.D., Tiozzo S., Roux M.M., Ishizuka K., Swalla B.J., De Tomaso A.W. Early lineage specification of long-lived germline precursors in the colonial ascidian Botryllus schlosseri. Development 2009, 136:3485-3494.
22. Brunetti R., Burighel P. Sviluppo dell'apparato vascolare coloniale in Botryllus schlosseri (Pallas). Pubbl. Staz. Zool. Napoli 1969, 37:137-148.
23. Canutescu A.A., Shelenkov A.A., Dunbrack R.L. A graph-theory algorithm for rapid protein side-chain prediction. Protein Sci. 2003, 12:2001-2014.
24. Cima F., Ballarin L. Apoptosis and pattern of Bcl-2 and Bax expression in the alimentary tract during the colonial blastogenetic cycle of Botryllus schlosseri (Urochordata, Ascidiacea). Ital. J. Zool. 2009, 76:28-42.
25. Cima F., Basso G., Ballarin L. Apoptosis and phosphatidylserine-mediated recognition during the take-over phase of the colonial life-cycle in the ascidian Botryllus schlosseri. Cell Tissue Res. 2003, 312:369-376.
26. Cima F., Sabbadin A., Ballarin L. Cellular aspects of allorecognition in the compound ascidian Botryllus schlosseri. Dev. Comp. Immunol. 2004, 28:881-889.
27. Cima F., Sabbadin A., Zaniolo G., Ballarin L. Colony specificity and chemotaxis in the compound ascidian Botryllus schlosseri. Comp. Biochem. Physiol. 2006, 145A:376-382.
28. Cima F., Manni L., Basso G., Fortunato E., Accordi B., Schiavon F., Ballarin L. Hovering between death and life: haemocytes and natural apoptosis in the blastogenetic cycle of the colonial ascidian Botryllus schlosseri. Dev. Comp. Immunol. 2010, 34:272-285.
29. Dahms N.M., Hancock M.K. P-type lectins. Biochim. Biophys. Acta 2002, 1572:317-340.
30. Delsuc F., Brinkmann H., Chourrout D., Philippe H. Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 2006, 439:965-968.
31. Gabius H.J. Animal lectins and life: a guided tour into the realm of the sugar code. Biochim. Biophys. Acta 2002, 1572:163-164.
32. Gasparini F., Longo F., Manni L., Burighel P., Zaniolo G. Tubular sprouting as a mode of vascular formation in a colonial ascidian (Tunicata). Dev. Dynam. 2007, 236:719-731.
33. Gasparini F., Franchi N., Spolaore B., Ballarin L. Novel rhamnose-binding lectins from the colonial ascidian Botryllus schlosseri. Dev. Comp. Immunol. 2008, 32:1177-1191.
34. Gorman A., McCarthy J., Finucane D., Reville W., Cotter T. Morphological assessment of apoptosis. Techniques in Apoptosis. A User's Guide 1997, 1-20. Portland, London. T.G. Cotter, S.J. Martin (Eds.).
35. Gouet P., Courcelle E., Stuart D.I., Métoz F. ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 1999, 15:305-308.
36. Jimbo M., Usui R., Sakai R., Muramoto K., Kamiya H. Purification, cloning and characterization of egg lectins from the teleost Tribolodon brandti. Comp. Biochem. Physiol. 2007, 147B:164-171.
37. Kaltner H., Stierstorfer B. Animal lectins as cell adhesion molecules. Acta Anat. 1998, 161:162-179.
38. Kilpatrick C.D. Animal lectins: a historical introduction and overview. Bioch. Biophys. Acta 2002, 1572:187-197.
39. Lam Y.W., Ng T.B. Purification and characterization of a rhamnose-binding lectin with immunoenhancing activity from grass carp (Ctenopharyngodon idellus) ovaries. Protein Expres. Purif. 2002, 26:378-385.
40. Landau M., Mayrose I., Rosenberg Y., Glaser F., Martz E., Pupko T., Ben-Tal N. ConSurf 2005: the projection of evolutionary conservation scores of residues on protein structures. Nucleic Acids Res. 2005, 33:W299-W302.
41. Lauzon R.J., Ishizuka K.J., Weissman I.L. A cyclical, developmentally-regulated death phenomenon in a colonial urochordate. Dev. Dynam. 1992, 194:71-83.
42. Lauzon R.J., Patton C.W., Weissman I.L. A morphological and immunohistochemical study of programmed cell death in Botryllus schlosseri (Tunicata, Ascidiacea). Cell Tissue Res. 1993, 272:115-127.
43. Loris R. Principles of structures of animal and plant lectins. Biochim. Biophys. Acta 2002, 1572:198-208.
44. Manni L., Zaniolo G., Cima F., Burighel P., Ballarin L. Botryllus schlosseri: a model ascidian for the study of asexual reproduction. Dev. Dynam. 2007, 236:335-352.
45. Matozzo V., Rova G., Marin M.G. Haemocytes of the cockle Cerastoderma glaucum: morphological characterisation and involvement in immune responses. Fish Shellfish Immunol. 2007, 23:732-746.
46. Matzinger P. The danger model: a renewed sense of self. Science 2002, 296:301-305.
47. Menin A., Ballarin L. Immunomodulatory molecules in the compound ascidian Botryllus schlosseri: evidence from conditioned media. J. Invertebr. Pathol. 2008, 99:275-280.
48. Menin A., Del Favero M., Cima F., Ballarin L. Release of phagocytosis-stimulating factor(s) by morula cells in a colonial ascidian. Mar. Biol. 2005, 148:225-230.
49. Naganuma T., Ogawa T., Hirabayashi J., Kasai K., Kamiya H., Muramoto K. Isolation, characterization and molecular evolution of a novel shell lectin from a marine bivalve, Pteria penguin. Mol. Div. 2006, 10:607-618.
50. Narvaez E., Berendsen J., Guzmán F., Gallardo J.A., Mercado L. An immunological method for quantifying antibacterial activity in Salmo salar (Linnaeus, 1758) skin mucus. Fish Shellfish Immunol. 2010, 28:235-239.
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. Ottaviani E., Sassi D., Kletsas D. PDGF- and TGF-β-induced changes in cell shape of invertebrate immunocytes: effect of calcium entry blockers. Eur. J. Cell Biol. 1997, 74:336-341.
53. Ozeki H., Ohwaki M., Fukuda T. Studies on lectins of amago (Oncorhynchus rhodurus). I. Amago ova lectin and its receptor on homologous macrophages. Dev. Comp. Immunol. 1983, 7:77-87.
54. Ozeki Y., Matsui T., Suzuki M., Titani K. Amino acid sequence and molecular characterization of a d-galactoside-specific lectin purified from sea urchin (Anthocidaris crassispina) eggs. Biochemistry 1991, 30:2391-2394.
55. Parrinello N., Canicattì C. Carbohydrate binding specificity and purification by biospecific affinity chromatography of Ascidia malaca Traust. hemagglutinins. Dev. Comp. Immunol. 1982, 6:53-64.
56. Raftos D.A., Stillman D.L., Cooper E.L. Chemotactic responses of tunicate (Urochordata, Ascidiacea) hemocytes in vitro. J. Invertebr. Pathol. 1998, 72:44-49.
57. Ruangsri J., Fernandes J.M.O., Brinchmann M., Kiron V. Antimicrobial activity in the tissues of Atlantic cod (Gadus morhua L.). Fish Shellfish Immunol. 2010, 28:879-886.
58. Sabbadin A. Osservazioni sullo sviluppo, l'accrescimento e la riproduzione di Botryllus schlosseri (Pallas), in condizioni di laboratorio. Boll. Zool. 1955, 22:243-265.
59. Shiina N., Tateno H., Ogawa T., Muramoto K., Saneyoshi M., Kamiya H. Isolation and characterization of l-rhamnose-binding lectins from chum salmon (Oncorhynchus keta) eggs. Fish. Sci. 2002, 68:1352-1366.
60. Shirai T., Watanabe Y., Lee M.S., Ogawa T., Muramoto K. Structure of rhamnose-binding lectin CSL3: unique pseudo-tetrameric architecture of a pattern recognition protein. J. Mol. Biol. 2009, 391:390-403.
61. Söderhäll K., Smith V.J. Separation of the hemocyte populations of Carcinus maenas and other marine decapods and prophenoloxidase distribution. Dev. Comp. Immunol. 1983, 7:229-239.
62. Sommer I., Toppo S., Sander O., Lengauer T., Tosatto S.C.E. Improving the quality of protein structure models by selecting from alignment alternatives. BMC Bioinform. 2006, 7:364.
63. Subramanian S., Ross N., MacKinnon S. Myxinidin, a novel antimicrobial peptide from the epidermal mucus of hagfish, Myxine glutinosa L. Mar. Biotechnol. 2009, 11:748-757.
64. Tateno H., Saneyoshi A., Ogawa T., Muramoto K., Kamiya H., Saneyoshi M. Isolation and characterization of rhamnose-binding lectins from eggs of steelhead trout (Oncorhynchus mykiss) homologous to low density lipoprotein receptor superfamily. J. Biol. Chem. 1998, 273:19190-19197.
65. Tateno H., Ogawa T., Muramoto K., Kamiya H., Saneyoshi M. Rhamnose-binding lectins from steelhead trout (Oncorhynchus mykiss) eggs recognize bacterial lipopolysaccharides and lipoteichoic acid. Biosci. Biotechnol. Biochem. 2002, 66:604-612.
66. Tateno H., Ogawa T., Muramoto K., Kamiya H., Saneyoshi M. Distribution and molecular evolution of rhamnose-binding lectins in Salmonidae: isolation and characterization of two lectins from white-spotted charr (Salvelinus leucomaenis) eggs. Biosci. Biotechnol. Biochem. 2002, 66:1356-1365.
67. Terada T., Watanabe Y., Tateno H., Naganuma T., Ogawa T., Muramoto K., Kamiya H. Structural characterization of a rhamnose-binding glycoprotein (lectin) from Spanish mackerel (Scomberomoronus niphonius) eggs. Biochim. Biophys. Acta 2006, 1770:617-629.
68. Terada T., Watanabe Y., Tateno H., Naganuma T., Ogawa T., Muramoto K., Kamiya H. Structural characterization of a rhamnose binding glycoprotein (lectin) from Spanish mackerel (Scomberomorous niphonius) eggs. Biochim. Biophys. Acta 2007, 1770:617-629.
69. Tosatto S.C. The victor/FRST function for model quality estimation. J. Comput. Biol. 2005, 12:1316-1327.
70. Tosatto S.C.E., Bindewald E., Hesser J., Männer R. A divide and conquer approach to fast loop modelling. Protein Eng. 2002, 15:279-286.
71. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. U. S. A. 1979, 76:4350-4354.
72. Trinchieri G., Kubin M., Bellone G., Cassatella M.A. Cytokine cross-talk between phagocytic cells and lymphocytes: relevance for differentiation/activation o phagocyic cells and regulation of adaptive immunity. J. Cell Biochem. 1993, 53:301-308.
73. Tymiak A.A., Norman J.A., Bolgar M., DiDonato G.C., Lee H., Parker W.L., Lo L.C., Berova N., Nakanishi K., Haber E. Physicochemical characterization of a ouabain isomer isolated from bovine hypothalamus. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:8189-8193.
74. Vasta G.R., Ahmed H. Animal lectins as cell surface receptors: current status for invertebrate species. Prog. Mol. Subcell. Biol. 1996, 17:158-182.
75. Vasta G.R., Ahmed H., Fink N.E., Ecola M.T., Marsh A.G., Snowden A., Odom E.W. Animal lectins as self/non-self recognition molecules. Ann. N. Y. Acad. Sci. 1994, 712:55-73.
76. Vasta G.R., Ahmed H., Odom E.W. Structural and functional diversity of lectin repertoires in invertebrates, protochordates and ectothermic vertebrates. Curr. Opin. Struct. Biol. 2004, 14:617-630.
77. Vakonakis I., Langenhan T., Prömel S., Russ A., Campbell I.D. Solution structure and sugar-binding mechanism of mouse latrophilin-1 RBL: a 7TM receptor-attached lectin-like domain. Structure 2008, 16:944-953.
78. Watanabe Y., Shiina N., Shinozaki F., Yokoyama H., Kominami J., Nakamura-Tsuruta S., Hirabayashi J., Sugahara K., Kamiya H., Matsubara H., Ogawa T., Muramoto K. Isolation and characterization of l-rhamnose-binding lectin, which binds to microsporidian Glugea plecoglossi, from ayu (Plecoglossus altivelis) eggs. Dev. Comp. Immunol. 2008, 32:487-499.
79. Watanabe Y., Tateno H., Nakamura-Tsuruta S., Kominami J., Hirabayashi J., Nakamura O., Watanabe T., Kamiya H., Naganuma T., Ogawa T., Muramoto K. The function of rhamnose-binding lectin in innate immunity by restricted binding to Gb3. Dev. Comp. Immunol. 2009, 33:187-197.