Lectin-like molecules in transcriptome of Littorina littorea hemocytes

Developmental and Comparative Immunology

Volumn 48, Issue 1, 2015, Pages 210-220

  Gorbushin, Alexander M ^a   Borisova, Elena A ^a  

^a SECHENOV INSTITUTE OF EVOLUTIONARY PHYSIOLOGY AND BIOCHEMISTRY   (Russian Federation)

Author keywords

Hemocytes; Innate immunity; Lectins; Mollusca; Transcriptome

Indexed keywords

C TYPE LIKE LECTIN; CALNEXIN; CALRETICULIN; CELL ADHESION MOLECULE; CHITINASE LIKE LECTIN; EPIDERMAL GROWTH FACTOR; F BOX LECTIN; FIBRINOGEN RELATED PROTEIN; FUCO LECTIN; GALECTIN; I TYPE LECTIN; L TYPE LECTIN; LECTIN; M TYPE LECTIN; P TYPE LECTIN; TRANSCRIPTOME; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BLOOD CELL; DNA LIBRARY; GENE FUNCTION; GENE SEQUENCE; GENETIC ASSOCIATION; IMMUNE RESPONSE; LITTORINA LITTOREA; MOLECULAR CLONING; MOLECULAR EVOLUTION; MOLECULAR RECOGNITION; NONHUMAN; PROTEIN EXPRESSION; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; AMINO ACID SEQUENCE; ANIMAL; CLASSIFICATION; CYTOLOGY; DNA SEQUENCE; GASTROPOD; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; NUCLEOTIDE SEQUENCE; SEQUENCE ALIGNMENT;

LITTORINA LITTOREA; MOLLUSCA;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CLONING, MOLECULAR; GASTROPODA; HEMOCYTES; IMMUNITY, INNATE; LECTINS; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; TRANSCRIPTOME;

EID: 84909954111     PISSN: 0145305X     EISSN: 18790089     Source Type: Journal    
DOI: 10.1016/j.dci.2014.10.007     Document Type: Article

References (82)

1. Adema C.M., Hertel L.A., Miller R.D., Loker E.S. A family of fibrinogen-related proteins that precipitates parasite-derived molecules is produced by an invertebrate after infection. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:8691-8696.
2. Ashburner M., Ball C.A., Blake J.A., Botstein D., Butler H., Cherry J.M., et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet 2000, 25:25-29.
3. Badariotti F., Kypriotou M., Lelong C., Dubos M.P., Renard E., Galera P., et al. The phylogenetically conserved molluscan chitinase-like protein 1 (Cg-Clp1), homologue of human HC-gp39, stimulates proliferation and regulates synthesis of extracellular matrix components of mammalian chondrocytes. J. Biol. Chem 2006, 281:29583-29596.
4. Badariotti F., Lelong C., Dubos M.P., Favrel P. Characterization of chitinase-like proteins (Cg-Clp1 and Cg-Clp2) involved in immune defence of the mollusc Crassostrea gigas. FEBS J. 2007, 274:3646-3654.
5. Betran E., Thornton K., Long M. Retroposed new genes out of the X in Drosophila. Genome Res 2002, 12:1854-1859.
6. Brites D., McTaggart S., Morris K., Anderson J., Thomas K., Colson I., et al. The Dscam homologue of the crustacean Daphnia is diversified by alternative splicing like in insects. Mol. Biol. Evol 2008, 25:1429-1439.
7. Chang N.C., Hung S.I., Hwa K.Y., Kato I., Chen J.E., Liu C.H., et al. A macrophage protein, Ym1, transiently expressed during inflammation is a novel mammalian lectin. J. Biol. Chem 2001, 276:17497-17506.
8. Chou P.-H., Chang H.-S., Chen I.T., Lin H.-Y., Chen Y.-M., Yang H.-L., et al. The putative invertebrate adaptive immune protein Litopenaeus vannamei Dscam (LvDscam) is the first reported Dscam to lack a transmembrane domain and cytoplasmic tail. Dev. Comp. Immunol 2009, 33:1258-1267.
9. Chou P.H., Chang H.S., Chen I.T., Lee C.W., Hung H.Y., Han-Ching Wang K.C. Penaeus monodon Dscam (PmDscam) has a highly diverse cytoplasmic tail and is the first membrane-bound shrimp Dscam to be reported. Fish Shellfish Immunol 2011, 30:1109-1123.
10. Claessens A., Van de Vijver K., Van Bockstaele D.R., Wauters J., Berneman Z.N., Van Marck E., et al. Expression and localization of CHODLδE/CHODLfδE, the soluble isoform of chondrolectin. Cell Biol. Int 2007, 31:1323-1330.
11. Clark M.S., Thorne M.A.S., Vieira F.A., Cardoso J.C.R., Power D.M., Peck L.S. Insights into shell deposition in the Antarctic bivalve Laternula elliptica: gene discovery in the mantle transcriptome using 454 pyrosequencing. BMC Genomics 2010, 11:362.
12. Cooper D.N. Galectinomics: finding themes in complexity. Biochim. Biophys. Acta 2002, 1572:209-231.
13. Craft J.A., Gilbert J.A., Temperton B., Dempsey K.E., Ashelford K., Tiwari B., et al. Pyrosequencing of Mytilus galloprovincialis cDNAs: tissue-specific expression patterns. PLoS ONE 2010, 5:e8875.
14. Cuthbertson B., Shepard E., Chapman R., Gross P. Diversity of the penaeidin antimicrobial peptides in two shrimp species. Immunogenetics 2002, 54:442-445.
15. Dheilly N.M., Adema C., Raftos D.A., Gourbal B., Grunau C., Du Pasquier L. No more non-model species: the promise of next generation sequencing for comparative immunology. Dev. Comp. Immunol 2014, 45:56-66.
16. Feldmeyer B., Wheat C.W., Krezdorn N., Rotter B., Pfenninger M. Short read Illumina data for the de novo assembly of a non-model snail species transcriptome (Radix balthica, Basommatophora, Pulmonata), and a comparison of assembler performance. BMC Genomics 2011, 12:317.
17. Finn R.D., Bateman A., Clements J., Coggill P., Eberhardt R.Y., Eddy S.R., et al. Pfam: the protein families database. Nucleic Acids Res 2014, 42:D222-D230.
18. Flavell A.J. Retroelements, reverse transcriptase and evolution. Comp. Biochem. Physiol. B Biochem Mol. Biol 1995, 110:3-15.
19. Fullekrug J., Scheiffele P., Simons K. VIP36 localisation to the early secretory pathway. J. Cell Sci 1999, 112(Pt 17):2813-2821.
20. Fusetti F., Pijning T., Kalk K.H., Bos E., Dijkstra B.W. Crystal structure and carbohydrate-binding properties of the human cartilage glycoprotein-39. J. Biol. Chem 2003, 278:37753-37760.
21. Gerardo R.V., Hafiz A. Animal Lectins: A Functional View 2008, CRC Press, US.
22. Gorbushin A.M., Iakovleva N.V. Haemogram of Littorina littorea. J. Mar. Biolog. Assoc. U.K. 2006, 86:1175-1181.
23. Gorbushin A.M., Iakovleva N.V. Functional characterization of Littorina littorea (Gastropoda: Prosobranchia) blood cells. J. Mar. Biolog. Assoc. U.K. 2007, 87:741-746.
24. Gorbushin A.M., Iakovleva N.V. The enigma of the haemogram "left-shift" in periwinkles infected with trematodes. Fish Shellfish Immunol 2008, 24:745-751.
25. Gorbushin A.M., Iakovleva N.V. A new gene family of single fibrinogen domain lectins in Mytilus. Fish Shellfish Immunol 2011, 30:434-438.
26. Gorbushin A.M., Iakovleva N.V. Dscam receptors from mollusca: multiple isoforms are lacking. Fish Shellfish Immunol 2013, 34:1653-1654.
27. Gorbushin A.M., Klimovich A.V., Iakovleva N.V. Himasthla elongata: effect of infection on expression of the LUSTR-like receptor mRNA in common periwinkle haemocytes. Exp. Parasitol 2009, 123:24-30.
28. Gorbushin A.M., Panchin Y.V., Iakovleva N.V. In search of the origin of FREPs: characterization of Aplysia californica fibrinogen-related proteins. Dev. Comp. Immunol 2010, 34:465-473.
29. Gourdine J.P., Smith-Ravin E.J. Analysis of a cDNA-derived sequence of a novel mannose-binding lectin, codakine, from the tropical clam Codakia orbicularis. Fish Shellfish Immunol 2007, 22:498-509.
30. Grabherr M.G., Haas B.J., Yassour M., Levin J.Z., Thompson D.A., Amit I., et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol 2011, 29:644-652.
31. Haas B.J., Papanicolaou A., Yassour M., Grabherr M., Blood P.D., Bowden J., et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protocols 2013, 8:1494-1512.
32. Hanington P.C., Zhang S.M. The primary role of fibrinogen-related proteins in invertebrates is defense, not coagulation. J. Innate Immun 2011, 3:17-27.
33. Hauri H.P., Kappeler F., Andersson H., Appenzeller C. ERGIC-53 and traffic in the secretory pathway. J. Cell Sci 2000, 113(Pt 4):587-596.
34. Heyland A., Vue Z., Voolstra C.R., Medina M., Moroz L.L. Developmental transcriptome of Aplysia californica. J. Exp. Zool. B Mol. Dev. Evol 2011, 316B:113-134.
35. Honda S., Kashiwagi M., Miyamoto K., Takei Y., Hirose S. Multiplicity, structures, and endocrine and exocrine natures of eel fucose-binding lectins. J. Biol. Chem 2000, 275:33151-33157.
36. Iakovleva N.V., Gorbushin A.M. Carbohydrate mimicry of the parasite in the Himasthla elongata (Trematoda: Echinostomatidae) - Littorina littorea (Mollusca: Prosobranchia) system. J. Evol. Biochem. Physiol 2005, 41:143-149.
37. Iakovleva N.V., Gorbushin A.M., Storey K.B. Modulation of mitogen-activated protein kinases (MAPK) activity in response to different immune stimuli in haemocytes of the common periwinkle Littorina littorea. Fish Shellfish Immunol 2006, 21:315-324.
38. Iakovleva N.V., Gorbushin A.M., Zelck U.E. Partial characterization of mitogen-activated protein kinases (MAPK) from haemocytes of the common periwinkle, Littorina littorea (Gastropoda: Prosobranchia). Fish Shellfish Immunol 2006, 20:665-668.
39. Iakovleva N.V., Shaposhnikova T.G., Gorbushin A.M. Rediae of echinostomatid and heterophyid trematodes suppress phagocytosis of haemocytes in Littorina littorea (Gastropoda: Prosobranchia). Exp. Parasitol 2006, 113:24-29.
40. Kong P., Wang L., Zhang H., Song X., Zhou Z., Yang J., et al. A novel C-type lectin from bay scallop Argopecten irradians (AiCTL-7) agglutinating fungi with mannose specificity. Fish Shellfish Immunol 2011, 30:836-844.
41. Kopacek P., Hajdusek O., Buresova V., Daffre S. Tick innate immunity. Adv. Exp. Med. Biol 2010, 708:137-162.
42. Langmead B., Trapnell C., Pop M., Salzberg S.L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009, 10:R25.
43. Letunic I., Doerks T., Bork P. SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res 2012, 40:D302-D305.
44. Li B., Dewey C.N. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 2011, 12:323.
45. Loker E.S. Gastropod imunobiology. Invertebrate Immunity 2011, 314. Springer, US. 1st ed. K. Söderhäll (Ed.).
46. Mann K., Weiss I.M., Andre S., Gabius H.J., 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 2000, 267:5257-5264.
47. Marchler-Bauer A., Lu S., Anderson J.B., Chitsaz F., Derbyshire M.K., DeWeese-Scott C., et al. CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 2011, 39:D225-D229.
48. Milan M., Coppe A., Reinhardt R., Cancela L.M., Leite R.B., Saavedra C., et al. Transcriptome sequencing and microarray development for the Manila clam, Ruditapes philippinarum: genomic tools for environmental monitoring. BMC Genomics 2011, 12:234.
49. Moné Y., Gourbal B., Duval D., Du Pasquier L., Kieffer-Jaquinod S., Mitta G. A large repertoire of parasite epitopes matched by a large repertoire of host immune receptors in an invertebrate host/parasite model. PLoS Negl. Trop. Dis 2010, 4:e813.
50. Nair S.V., Del Valle H., Gross P.S., Terwilliger D.P., Smith L.C. Macroarray analysis of coelomocyte gene expression in response to LPS in the sea urchin. Identification of unexpected immune diversity in an invertebrate. Physiol. Genomics 2005, 22:33-47.
51. Natarajan A., Yardimci G.G., Sheffield N.C., Crawford G.E., Ohler U. Predicting cell-type-specific gene expression from regions of open chromatin. Genome Res 2012, 22:1711-1722.
52. Odom E.W., Vasta G.R. Characterization of a binary tandem domain F-type lectin from striped bass (Morone saxatilis). J. Biol. Chem 2006, 281:1698-1713.
53. Romero A., Dios S., Poisa-Beiro L., Costa M.M., Posada D., Figueras A., et al. Individual sequence variability and functional activities of fibrinogen-related proteins (FREPs) in the Mediterranean mussel (Mytilus galloprovincialis) suggest ancient and complex immune recognition models in invertebrates. Dev. Comp. Immunol 2011, 35:334-344.
54. Smith P.H., Mwangi J.M., Afrane Y.A., Yan G., Obbard D.J., Ranford-Cartwright L.C., et al. Alternative splicing of the Anopheles gambiae Dscam gene in diverse Plasmodium falciparum infections. Malar. J. 2011, 10:156.
55. Song X., Zhang H., Zhao J., Wang L., Qiu L., Mu C., et al. An immune responsive multidomain galectin from bay scallop Argopectens irradians. Fish Shellfish Immunol 2010, 28:326-332.
56. Sun S.C., Lindstrom I., Boman H.G., Faye I., Schmidt O. Hemolin: an insect-immune protein belonging to the immunoglobulin superfamily. Science 1990, 250:1729-1732.
57. Tanguy M., McKenna P., Gauthier-Clerc S., Pellerin J., Danger J.-M., Siah A. Sequence analysis of a normalized cDNA library of Mytilus edulis hemocytes exposed to Vibrio splendidus LGP32 strain. Results Immunol 2013, 3:40-50.
58. 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.
59. Thomsen T., Schlosser A., Holmskov U., Sorensen G.L. Ficolins and FIBCD1: soluble and membrane bound pattern recognition molecules with acetyl group selectivity. Mol. Immunol 2011, 48:369-381.
60. Essentials of Glycobiology 2009, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 2nd ed. A. Varki, R.D. Cummings, J.D. Esko, H.H. Freeze, P. Stanley, C.R. Bertozzi (Eds.).
61. 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.
62. Vasta G.R., Ahmed H., Tasumi S., Odom E.W., Saito K. Biological roles of lectins in innate immunity: molecular and structural basis for diversity in self/non-self recognition. Adv. Exp. Med. Biol 2007, 598:389-406.
63. Vasta G.R., Ahmed H., Bianchet M.A., Fernandez-Robledo J.A., Amzel L.M. Diversity in recognition of glycans by F-type lectins and galectins: molecular, structural, and biophysical aspects. Ann. N. Y. Acad. Sci 2012, 1253:E14-E26.
64. Walker J.R., Nagar B., Young N.M., Hirama T., Rini J.M. X-ray crystal structure of a galactose-specific C-type lectin possessing a novel decameric quaternary structure. Biochemistry 2004, 43:3783-3792.
65. Wang N., Lee Y.H., Lee J. Recombinant perlucin nucleates the growth of calcium carbonate crystals: molecular cloning and characterization of perlucin from disk abalone, Haliotis discus discus. Comp. Biochem. Physiol. B Biochem Mol. Biol 2008, 149:354-361.
66. Wang X.W., Wang J.X. Diversity and multiple functions of lectins in shrimp immunity. Dev. Comp. Immunol 2013, 39:27-38.
67. Watson F.L., Puttmann-Holgado R., Thomas F., Lamar D.L., Hughes M., Kondo M., et al. Extensive diversity of Ig-superfamily proteins in the immune system of insects. Science 2005, 309:1874-1878.
68. Weiss I.M., Kaufmann S., Mann K., Fritz M. Purification and characterization of perlucin and perlustrin, two new proteins from the shell of the mollusc Haliotis laevigata. Biochem. Biophys. Res. Commun 2000, 267:17-21.
69. Weng L., Smits P., Wauters J., Merregaert J. Molecular cloning and characterization of human chondrolectin, a novel type I transmembrane protein homologous to C-type lectins. Genomics 2002, 80:62-70.
70. Werner G.A., Gemmell P., Grosser S., Hamer R., Shimeld S. Analysis of a deep transcriptome from the mantle tissue of Patella vulgata Linnaeus (Mollusca: Gastropoda: Patellidae) reveals candidate biomineralising genes. Mar. Biotechnol 2013, 15:230-243.
71. Williams D.B. Beyond lectins: the calnexin/calreticulin chaperone system of the endoplasmic reticulum. J. Cell Sci 2006, 119:615-623.
72. Yakovleva N.V., Samoilovich M.P., Gorbushin A.M. The diversity of strategies of defense from pathogens in molluscs. J. Evol. Biochem. Physiol 2001, 37:358-367.
73. Yoshida Y., Tokunaga F., Chiba T., Iwai K., Tanaka K., Tai T. Fbs2 is a new member of the E3 ubiquitin ligase family that recognizes sugar chains. J. Biol. Chem 2003, 278:43877-43884.
74. Zhang D., Jiang S., Hu Y., Cui S., Guo H., Wu K., et al. A multidomain galectin involved in innate immune response of pearl oyster Pinctada fucata. Dev. Comp. Immunol 2011, 35:1-6.
75. Zhang G., Fang X., Guo X., Li L., Luo R., Xu F., et al. The oyster genome reveals stress adaptation and complexity of shell formation. Nature 2012, 490:49-54.
76. Zhang H., Wang L., Song L., Song X., Wang B., Mu C., et al. A fibrinogen-related protein from bay scallop Argopecten irradians involved in innate immunity as pattern recognition receptor. Fish Shellfish Immunol 2009, 26:56-64.
77. Zhang H., Kong P., Wang L., Zhou Z., Yang J., Zhang Y., et al. Cflec-5, a pattern recognition receptor in scallop Chlamys farreri agglutinating yeast Pichia pastoris. Fish Shellfish Immunol 2010, 29:149-156.
78. Zhang L.L., Li L., Zhang G.F. Sequence variability of fibrinogen-related proteins (FREPs) in Crassostrea gigas. Chin. Sci. Bull 2012, 57:3312-3319.
79. Zhang S.M., Loker E.S. Representation of an immune responsive gene family encoding fibrinogen-related proteins in the freshwater mollusc Biomphalaria glabrata, an intermediate host for Schistosoma mansoni. Gene 2004, 341:255-266.
80. Zhang S.M., Nian H., Zeng Y., Dejong R.J. Fibrinogen-bearing protein genes in the snail Biomphalaria glabrata: characterization of two novel genes and expression studies during ontogenesis and trematode infection. Dev. Comp. Immunol 2008, 32:1119-1130.
81. Zhu L., Song L., Xu W., Qian P.Y. Identification of a C-type lectin from the bay scallop Argopecten irradians. Mol. Biol. Rep 2009, 36:1167-1173.
82. Zhu Y.Y., Machleder E.M., Chenchik A., Li R., Siebert P.D. Reverse transcriptase template switching: a SMART approach for full-length cDNA library construction. Biotechniques 2001, 30:892-897.