Cloning and Characterization of Mannose-Binding Lectin from Lamprey (Agnathans)12

The recognition of pathogens is mediated by a set of pattern recognition molecules that recognize conserved pathogen-associated molecular patterns shared by broad classes of microorganisms. Mannose-binding lectin (MBL) is one of the pattern recognition molecules and activates complement in association with MBL-associated serine protease (MASP) via the lectin pathway. Recently, an MBL-like lectin was isolated from the plasma of a urochordate, the solitary ascidian. This ascidian lectin has a carbohydrate recognition domain, but the collagen-like domain was replaced by another sequence. To elucidate the origin of MBLs, the aim of this study is to determine the structure and function of the MBL homolog in lamprey, the most primitive vertebrate. Using an N-acetylglucosamine (GlcNAc)-agarose column, MBL-like lectin (p25) was isolated from lamprey serum and cDNA cloning was conducted. From the deduced amino acid sequence this lectin has a collagenous region and a typical carbohydrate recognition domain. This lectin also binds mannose, glucose, and GlcNAc, but not galactose, indicating that it is structurally and functionally similar to the mammalian MBLs. Furthermore, it associated with lamprey MASPs, and the MBL-MASP activated lamprey C3 in fluid-phase and on the surface of pathogens. In conjunction with the phylogenetic analysis, it seems likely that the lamprey MBL is an ortholog of the mammalian MBL. Because acquired immunity seems to have been established only from jawed vertebrates onward, the lectin complement pathway in lamprey, as one of the major contributors to innate immunity, plays a pivotal role in defending the body against microorganisms.

[1]  T. Fujita.  Evolution of the lectin–complement pathway and its role in innate immunity , 2002, Nature Reviews Immunology.

[2]  T. Fujita,et al.  Origin of Mannose-Binding Lectin-Associated Serine Protease (MASP)-1 and MASP-3 Involved in the Lectin Complement Pathway Traced Back to the Invertebrate, Amphioxus12 , 2003, The Journal of Immunology.

[3]  M. Nonaka,et al.  Primitive complement system of invertebrates , 2004, Immunological reviews.

[4]  N. Saitou,et al.  The neighbor-joining method: a new method for reconstructing phylogenetic trees. , 1987, Molecular biology and evolution.

[5]  K. Drickamer,et al.  Mannose-binding proteins isolated from rat liver contain carbohydrate-recognition domains linked to collagenous tails. Complete primary structures and homology with pulmonary surfactant apoprotein. , 1986, The Journal of biological chemistry.

[6]  T. Fujita,et al.  Primitive complement system--recognition and activation. , 2004, Molecular immunology.

[7]  T. Yano,et al.  Expansion of genes encoding complement components in bony fish: biological implications of the complement diversity. , 2003, Developmental and comparative immunology.

[8]  T. Fujita,et al.  Cleavage of the third component of complement (C3) by mannose-binding protein-associated serine protease (MASP) with subsequent complement activation. , 1995, Immunobiology.

[9]  T. Fujita,et al.  The lectin‐complement pathway – its role in innate immunity and evolution , 2004, Immunological reviews.

[10]  M. Nonaka.  Evolution of the complement system. , 2001, Current opinion in immunology.

[11]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[12]  Teizo Fujita,et al.  Origin of the classical complement pathway: Lamprey orthologue of mammalian C1q acts as a lectin. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[13]  T. Fujita,et al.  Opsonic complement component C3 in the solitary ascidian, Halocynthia roretzi. , 1999, Journal of immunology.

[14]  S. Thiel,et al.  Collections and ficolins: humoral lectins of the innate immune defense. , 2003, Annual review of immunology.

[15]  J. L. Ding,et al.  The ancient origin of the complement system , 2005, The EMBO journal.

[16]  T. Fujita,et al.  An Ancient Lectin-Dependent Complement System in an Ascidian: Novel Lectin Isolated from the Plasma of the Solitary Ascidian, Halocynthia roretzi1 2 , 2001, The Journal of Immunology.

[17]  S. Thiel,et al.  A second serine protease associated with mannan-binding lectin that activates complement , 1997, Nature.

[18]  T. Fujita,et al.  Cloning and Characterization of Novel Ficolins from the Solitary Ascidian, Halocynthia roretzi* , 2001, The Journal of Biological Chemistry.

[19]  K. Drickamer.  Engineering galactose-binding activity into a C-type mannose-binding protein , 1992, Nature.

[20]  M. Walport.  Complement. First of two parts. , 2001, The New England journal of medicine.

[21]  S. Thiel,et al.  MASP-3 and its association with distinct complexes of the mannan-binding lectin complement activation pathway. , 2001, Immunity.

[22]  N. Yamaguchi,et al.  Purification of a lamprey complement protein homologous to the third component of the mammalian complement system. , 1984, Journal of immunology.

[23]  J. Jensenius,et al.  Collectins: collagenous C-type lectins of the innate immune defense system. , 1994, Immunology today.

[24]  T. Fujita,et al.  Activation of the classical complement pathway by mannose-binding protein in association with a novel C1s-like serine protease , 1992, The Journal of experimental medicine.

[25]  M. Nonaka,et al.  Characterization of novel ascidian β integrins as primitive complement receptor subunits , 2004, Immunogenetics.

[26]  L. Smith,et al.  The ancestral complement system in sea urchins , 2001, Immunological reviews.

[27]  T. Fujita,et al.  A Short Consensus Repeat-Containing Complement Regulatory Protein of Lamprey That Participates in Cleavage of Lamprey Complement 31 , 2004, The Journal of Immunology.

[28]  R. A. Ezekowitz,et al.  Role of the mannose-binding lectin in innate immunity. , 2003, The Journal of infectious diseases.

[29]  D. Jack,et al.  Mannose‐binding lectin: targeting the microbial world for complement attack and opsonophagocytosis , 2001, Immunological reviews.

[30]  M. Walport,et al.  Complement. Second of two parts. , 2001, The New England journal of medicine.

[31]  D. Cleveland.  Peptide mapping in one dimension by limited proteolysis of sodium dodecyl sulfate-solubilized proteins. , 1983, Methods in enzymology.

[32]  M. Nonaka,et al.  Cloning and Characterization of Integrin α Subunits from the Solitary Ascidian, Halocynthia roretzi1 , 2001, The Journal of Immunology.

[33]  K. Drickamer,et al.  Two distinct classes of carbohydrate-recognition domains in animal lectins. , 1988, The Journal of biological chemistry.

[34]  Wayne A. Hendrickson,et al.  Structure of a C-type mannose-binding protein complexed with an oligosaccharide , 1992, Nature.

[35]  T. Fujita,et al.  The role of ficolins in innate immunity. , 2002, Immunobiology.

[36]  F C Kafatos,et al.  Phylogenetic perspectives in innate immunity. , 1999, Science.