Identification of an amphioxus intelectin homolog that preferably agglutinates gram-positive over gram-negative bacteria likely due to different binding capacity to LPS and PGN

Fish and Shellfish Immunology

Volumn 33, Issue 1, 2012, Pages 11-20

  Yan, Jie ^a   Wang, Jianfeng ^a   Zhao, Yaqi ^a   Zhang, Jingye ^a   Bai, Changcun ^a   Zhang, Changqing ^a   Zhang, Chao ^a   Li, Kailin ^a   Zhang, Haiqing ^b   Du, Xiumin ^c   Feng, Lijun ^a  

^a SHANDONG UNIVERSITY   (China)

^b Shandong Polytechnic   (China)

^c JINAN MILITARY GENERAL HOSPITAL   (China)

Author keywords

Amphioxus; Bacterial agglutination; Intelectin; LPS; PGN

Indexed keywords

BACTERIA (MICROORGANISMS); BRANCHIOSTOMA; BRANCHIOSTOMA LANCEOLATUM; ESCHERICHIA COLI; INVERTEBRATA; NEGIBACTERIA; POSIBACTERIA; STAPHYLOCOCCUS AUREUS; VERTEBRATA;

EID: 84861478693     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2012.03.023     Document Type: Article

References (37)

1. McGreal E.P., Martinez-Pomares L., Gordon S. Divergent roles for C-type lectins expressed by cells of the innate immune system. Mol Immunol 2004, 41:1109-1121.
2. Medzhitov R. Recognition of microorganisms and activation of the immune response. Nature 2007, 449(7164):819-826.
3. Yu Y., Yu Y., Huang H., Feng K., Pan M., Yuan S., et al. A short-form C-type lectin from amphioxus acts as a direct microbial killing protein via interaction with peptidoglycan and glucan. J Immunol 2007, 179:8425-8434.
4. Takano T., Sha Z., Peatman E., Terhune J., Liu H., Kucuktas H., et al. The two channel catfish intelectin genes exhibit highly differential patterns of tissue expression and regulation after infection with Edwardsiella ictaluri. Dev Comp Immunol 2008, 32:693-705.
5. Fujita T., Matsushita M., Endo Y. The lectin-complement pathway-its role in innate immunity and evolution. Immunol Rev 2004, 198:185-202.
6. Lee J.K., Buckhaults P., Wilkes C., Teilhet M., King M.L., Moremen K.W., et al. Cloning and expression of a Xenopus laevis oocyte lectin and characterization of its mRNA levels during early development. Glycobiology 1997, 7:367-372.
7. Pemberton A.D., Knight P.A., Gamble J., Colledge W.H., Lee J.K., Pierce M., et al. Innate BALB/c enteric epithelial responses to Trichinella spiralis: inducible expression of a novel goblet cell lectin, intelectin-2, and its natural deletion in C57BL/10 mice. J Immunol 2004, 173:1894-1901.
8. Lee J.K., Baum L.G., Moremen K., Pierce M. The X-lectins: a new family with homology to the Xenopus laevis oocyte lectin XL-35. Glycoconj J 2004, 21:443-450.
9. Russell S., Young K.M., Smith M., Hayes M.A., Lumsden J.S. Identification, cloning and tissue localization of a rainbow trout (Oncorhynchus mykiss) intelectin like protein that binds bacteria and chitin. Fish Shellfish Immunol 2008, 25:91-105.
10. Chang M.X., Nie P. Intelectin gene from the grass carp Ctenopharyngodon idella: cDNA cloning, tissue expression, and immunohistochemical localization. Fish Shellfish Immunol 2007, 23:128-140.
11. Lin B., Cao Z., Su P., Zhang H., Li M., Lin Y., et al. Characterization and comparative analyses of zebrafish intelectins: highly conserved sequences, diversified structures and functions. Fish Shellfish Immunol 2009, 26(3):396-405.
12. Abe Y., Tokuda M., Ishimoto R., Azumi K., Yokosawa H. A unique primary structure, cDNA cloning and function of a galactose-specific lectin from ascidian plasma. Eur J Biochem 1999, 261:33-39.
13. Lee J.K., Schnee J., Pang M., Wolfert M., Baum L.G., Moremen K.W., et al. Human homologs of the xenopus oocyte cortical granule lectin XL35. Glycobiology 2001, 11:65-73.
14. Komiya T., Tanigawa Y., Hirohashi S. Cloning of the novel gene intelectin, which is expressed in intestinal paneth cells in mice. Biochem Biophys Res Commun 1998, 251:759-762.
15. Lu Z.H., di Domenico A., Wright S.H., Knight P.A., Whitelaw C.B., Pemberton A.D. Strain-specific copy number variation in the intelectin locus on the 129 mouse chromosome 1. BMC Genomics 2011, 12:110.
16. Gerwick L., Corley-Smith G., Bayne C.J. Gene transcript changes in individual rainbow trout livers following an inflammatory stimulus. Fish Shellfish Immunol 2007, 22:157-171.
17. Tsuji S., Uehori J., Matsumoto M., Suzuki Y., Matsuhisa A., Toyoshima K., et al. Human intelectin is a novel soluble lectin that recognizes galactofuranose in carbohydrate chains of bacterial cell wall. J Biol Chem 2001, 276:23456-23463.
18. Tsuji S., Yamashita M., Hoffman D.R., Nishiyama A., Shinohara T., Ohtsu T., et al. Capture of heat-killed Mycobacterium bovis bacillus Calmette-Guérin by intelectin-1 deposited on cell surfaces. Glycobiology 2009, 19(5):518-526.
19. Tsutsui S., Komatsu Y., Sugiura T., Araki K., Nakamura O. A unique epidermal mucus lectin identified from catfish (Silurus asotus): first evidence of intelectin in fish skin slime. J Biochem 2011, 150(5):501-514.
20. Pemberton A.D., Verdon B., Inglis N.F., Pearson J.P. Sheep intelectin-2 co-purifies with the mucin Muc5ac from gastric mucus. Res Vet Sci 2011, 91(3):e53-e57.
21. Huang S., Yuan S., Guo L., Yu Y., Li J., Wu T., et al. Genomic analysis of the immune gene repertoire of amphioxus reveals extraordinary innate complexity and diversity. Genome Res 2008, 18(7):1112-1126.
22. Holland P.W. Whole mount in situ hybridization to amphioxus embryos. Methods Mol Biol 1999, 97:641-644.
23. Du X.J., Zhao X.F., Wang J.X. Molecular cloning and characterization of a lipopolysaccharide and beta-1, 3-glucan binding protein from fleshy prawn (Fenneropenaeus chinensis). Mol Immunol 2007, 44:1085-1094.
24. Wang X.W., Zhang X.W., Xu W.T., Zhao X.F., Wang J.X. A novel C-type lectin (FcLec4) facilitates the clearance of Vibrio anguillarum in vivo in Chinese white shrimp. Dev Comp Immunol 2009, 33(9):1039-1047.
25. Somboonwiwat K., Bachère E., Rimphanitchayakit V., Tassanakajon A. Localization of anti-lipopolysaccharide factor (ALFPm3) in tissues of the black tiger shrimp, Penaeus monodon, and characterization of its binding properties. Dev Comp Immunol 2008, 32(10):1170-1176.
26. Han Y., Huang G., Zhang Q., Yuan S., Liu J., Zheng T., et al. The primitive immune system of amphioxus provides insights into the ancestral structure of the vertebrate immune system. Dev Comp Immunol 2010, 34(8):791-796.
27. Tsuji S., Yamashita M., Nishiyama A., Shinohara T., Li Z., Myrvik Q.N., et al. Differential structure and activity between human and mouse intelectin-1: human intelectin-1 is a disulfide-linked trimer, whereas mouse homologue is a monomer. Glycobiology 2007, 17:1045-1051.
28. Zhang J. Evolution by gene duplication: an update. Trends Ecol Evol 2003, 18:292-298.
29. Liang Y., Pan A., Zhang S., Zhang Y., Liu M. Cloning, distribution and primary immune characteristics of amphioxus alpha-2 macroglobulin. Fish Shellfish Immunol 2011, 31(6):963-969.
30. Peatman E., Baoprasertkul P., Terhune J., Xu P., Nandi S., Kucuktas H., et al. Expression analysis of the acute phase response in channel catfish (Ictalurus punctatus) after infection with a gram-negative bacterium. Dev Comp Immunol 2007, 31(11):1183-1196.
31. Lin B., Chen S., Cao Z., Lin Y., Mo D., Zhang H., et al. Acute phase response in zebrafish upon Aeromonas salmonicida and Staphylococcus aureus infection: striking similarities and obvious differences with mammals. Mol Immunol 2007, 44(4):295-301.
32. Cash H.L., Whitham C.V., Behrendt C.L., Hooper L.V. Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science 2006, 313(5790):1126-1130.
33. Le Y., Lee S.H., Kon O.L., Lu J. Human L-ficolin: plasma levels, sugar specificity, and assignment of its lectin activity to the fibrinogen-like (FBG) domain. FEBS Lett 1998, 425(2):367-370.
34. Suzuki Y.A., Shin K., Lönnerdal B. Molecular cloning and functional expression of a human intestinal lactoferrin receptor. Biochemistry 2001, 40(51):15771-15779.
35. Orsi N. The antimicrobial activity of lactoferrin: current status and perspectives. Biometals 2004, 17(3):189-196.
36. Shin K., Wakabayashi H., Yamauchi K., Yaeshima T., Iwatsuki K. Recombinant human intelectin binds bovine lactoferrin and its peptides. Biol Pharm Bull 2008, 31(8):1605-1608.
37. Gu N., Kang G., Jin C., Xu Y., Zhang Z., Erle D.J., et al. Intelectin is required for IL-13-induced monocyte chemotactic protein-1 and -3 expression in lung epithelial cells and promotes allergic airway inflammation. Am J Physiol Lung Cell Mol Physiol 2010, 298(3):L290-L296.