Multi-component complement system of Cnidaria: C3, Bf, and MASP genes expressed in the endodermal tissues of a sea anemone, Nematostella vectensis

Immunobiology

Volumn 214, Issue 3, 2009, Pages 165-178

  Kimura, Ayuko ^a   Sakaguchi, Eri ^a   Nonaka, Masaru ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

C3; Cnidaria; Complement; Evolution; Factor B; Innate immunity; MASP

Indexed keywords

ALTERNATIVE COMPLEMENT PATHWAY C3 C5 CONVERTASE; COMPLEMENT COMPONENT C3; COMPLEMENT COMPONENT C6; FIBRINOGEN; MANNAN BINDING LECTIN ASSOCIATED SERINE PROTEINASE;

AMINO ACID SEQUENCE; ANIMAL TISSUE; ARTICLE; COELENTERATE; COMPLEMENT SYSTEM; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENDODERM; FEMALE; GENE EXPRESSION; GENE IDENTIFICATION; GENE SEQUENCE; GENETIC CONSERVATION; IMMUNOGENETICS; IN SITU HYBRIDIZATION; LAST COMMON ANCESTOR; MESENTERY; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHARYNX; PRIORITY JOURNAL; PROTEIN DOMAIN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEA ANEMONE;

ANIMALS; CLONING, MOLECULAR; COMPLEMENT C3; COMPLEMENT FACTOR B; COMPLEMENT SYSTEM PROTEINS; ENDODERM; EVOLUTION, MOLECULAR; GENE EXPRESSION PROFILING; HUMANS; MANNOSE-BINDING PROTEIN-ASSOCIATED SERINE PROTEASES; ORGAN SPECIFICITY; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; SEA ANEMONES; SEQUENCE ANALYSIS, DNA;

EID: 59649085305     PISSN: 01712985     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.imbio.2009.01.003     Document Type: Article

References (42)

1. Ayala F.J., and Rzhetsky A. Origin of the metazoan phyla: molecular clocks confirm paleontological estimates. Proc. Natl. Acad. Sci. USA 95 (1998) 606-611
2. Azumi K., De Santis R., De Tomaso A., Rigoutsos I., Yoshizaki F., Pinto M.R., Marino R., Shida K., Ikeda M., Arai M., Inoue Y., Shimizu T., Satoh N., Rokhsar D.S., Du Pasquier L., Kasahara M., Satake M., and Nonaka M. Genomic analysis of immunity in a Urochordate and the emergence of the vertebrate immune system: "waiting for Godot". Immunogenetics 55 (2003) 570-581
3. Chen C.B., and Wallis R. Two mechanisms for mannose-binding protein modulation of the activity of its associated serine proteases. J. Biol. Chem. 279 (2004) 26058-26065
4. Clow L.A., Raftos D.A., Gross P.S., and Smith L.C. The sea urchin complement homologue, SpC3, functions as an opsonin. J. Exp. Biol. 207 (2004) 2147-2155
5. De Smet K., and Contreras R. Human antimicrobial peptides: defensins, cathelicidins and histatins. Biotechnol. Lett. 27 (2005) 1337-1347
6. Dishaw L.J., Smith S.L., and Bigger C.H. Characterization of a C3-like cDNA in a coral: phylogenetic implications. Immunogenetics 57 (2005) 535-548
7. Dolmer K., and Sottrup-Jensen L. Disulfide bridges in human complement component C3b. FEBS Lett. 315 (1993) 85-90
8. Endo Y., Nonaka M., Saiga H., Kakinuma Y., Matsushita A., Takahashi M., Matsushita M., and Fujita T. Origin of mannose-binding lectin-associated serine protease (MASP)-1 and MASP-3 involved in the lectin complement pathway traced back to the invertebrate, amphioxus. J. Immunol. 170 (2003) 4701-4707
9. Endo Y., Takahashi M., Nakao M., Saiga H., Sekine H., Matsushita M., Nonaka M., and Fujita T. Two lineages of mannose-binding lectin-associated serine protease (MASP) in vertebrates [published erratum appears in J. Immunol. 2000;164(10):5330]. J. Immunol. 161 (1998) 4924-4930
10. Fautin D.G., and Mariscal R.N. Capter 6 Cnidaria: Anthozoa. Microscopic Anatomy of Invertebrates vol. 2 (1991), Academic Press, New York 267-357
11. Frank P., and Bleakney J.S. Histology and sexual reproduction of the anemone Nematostella vectensis (Stephenson, 1935). J. Nat. Hist. 10 (1976) 441-449
12. Gal P., Barna L., Kocsis A., and Zavodszky P. Serine proteases of the classical and lectin pathways: similarities and differences. Immunobiology 212 (2007) 267-277
13. He Y., Tang B., Zhang S., Liu Z., Zhao B., and Chen L. Molecular and immunochemical demonstration of a novel member of Bf/C2 homolog in amphioxus Branchiostoma belcheri: implications for involvement of hepatic cecum in acute phase response. Fish Shellfish Immunol. 24 (2008) 768-778
14. Hemmrich G., and Bosch T.C. Compagen, a comparative genomics platform for early branching metazoan animals, reveals early origins of genes regulating stem-cell differentiation. Bioessays 30 (2008) 1010-1018
15. Janssen B.J., Huizinga E.G., Raaijmakers H.C., Roos A., Daha M.R., Nilsson-Ekdahl K., Nilsson B., and Gros P. Structures of complement component C3 provide insights into the function and evolution of immunity. Nature 437 (2005) 505-511
16. Kimura A., Ikeo K., and Nonaka M. Evolutionary origin of the vertebrate blood complement and coagulation systems inferred from liver EST analysis of lamprey. Dev. Comp. Immunol. 33 (2009) 77-87
17. King N., Westbrook M.J., Young S.L., Kuo A., Abedin M., Chapman J., Fairclough S., Hellsten U., Isogai Y., Letunic I., Marr M., Pincus D., Putnam N., Rokas A., Wright K.J., Zuzow R., Dirks W., Good M., Goodstein D., Lemons D., Li W., Lyons J.B., Morris A., Nichols S., Richter D.J., Salamov A., Sequencing J.G., Bork P., Lim W.A., Manning G., Miller W.T., McGinnis W., Shapiro H., Tjian R., Grigoriev I.V., and Rokhsar D. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451 (2008) 783-788
18. Krishnan V., Xu Y., Macon K., Volanakis J.E., and Narayana S.V. The crystal structure of C2a, the catalytic fragment of classical pathway C3 and C5 convertase of human complement. J. Mol. Biol. 367 (2007) 224-233
19. Marino R., Kimura Y., De Santis R., Lambris J.D., and Pinto M.R. Complement in urochordates: cloning and characterization of two C3-like genes in the ascidian Ciona intestinalis. Immunogenetics 53 (2002) 1055-1064
20. Matus D.Q., Pang K., Daly M., and Martindale M.Q. Expression of Pax gene family members in the anthozoan cnidarian, Nematostella vectensis. Evol. Dev. 9 (2007) 25-38
21. Miller D.J., Hemmrich G., Ball E.E., Hayward D.C., Khalturin K., Funayama N., Agata K., and Bosch T.C. The innate immune repertoire in cnidaria-ancestral complexity and stochastic gene loss. Genome Biol. 8 (2007) R59
22. Nonaka M., Azumi K., Ji X., Namikawa-Yamada C., Sasaki M., Saiga H., Dodds A.W., Sekine H., Homma M.K., Matsushita M., Endo Y., and Fujita T. Opsonic complement component C3 in the solitary ascidian, Halocynthia roretzi. J. Immunol. 162 (1999) 387-391
23. Nonaka M., and Kimura A. Genomic view of the evolution of the complement system. Immunogenetics 58 (2006) 701-713
24. Nonaka M., and Takahashi M. Complete complementary DNA sequence of the third component of complement of lamprey. Implication for the evolution of thioester containing proteins. J. Immunol. 148 (1992) 3290-3295
25. Nonaka M., Takahashi M., and Sasaki M. Molecular cloning of a lamprey homologue of the mammalian MHC class III gene, complement factor B. J. Immunol. 152 (1994) 2263-2269
26. Nonaka M., and Yoshizaki F. Evolution of the complement system. Mol. Immunol. 40 (2004) 897-902
27. Page M.J., and Di Cera E. Serine peptidases: classification, structure and function. Cell Mol. Life Sci. 65 (2008) 1220-1236
28. Putnam N.H., Srivastava M., Hellsten U., Dirks B., Chapman J., Salamov A., Terry A., Shapiro H., Lindquist E., Kapitonov V.V., Jurka J., Genikhovich G., Grigoriev I.V., Lucas S.M., Steele R.E., Finnerty J.R., Technau U., Martindale M.Q., and Rokhsar D.S. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317 (2007) 86-94
29. Rossi V., Cseh S., Bally I., Thielens N.M., Jensenius J.C., and Arlaud G.J. Substrate specificities of recombinant mannan-binding lectin-associated serine proteases-1 and -2. J. Biol. Chem. 276 (2001) 40880-40887
30. Saitou N., and Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4 (1987) 406-425
31. Scholz C.B., and Technau U. The ancestral role of Brachyury: expression of NemBra1 in the basal cnidarian Nematostella vectensis (Anthozoa). Dev. Genes Evol. 212 (2003) 563-570
32. Smith L.C., Shih C.S., and Dachenhausen S.G. Coelomocytes express SpBf, a homologue of factor B, the second component in the sea urchin complement system. J. Immunol. 161 (1998) 6784-6793
33. Sullivan J.C., Ryan J.F., Watson J.A., Webb J., Mullikin J.C., Rokhsar D., and Finnerty J.R. StellaBase: the Nematostella vectensis Genomics Database. Nucleic Acids Res. 34 (2006) D495-499
34. Suzuki M.M., Satoh N., and Nonaka M. C6-like and C3-like molecules from the cephalochordate, amphioxus, suggest a cytolytic complement system in invertebrates. J. Mol. Evol. 54 (2002) 671-679
35. Takahashi M., Iwaki D., Kanno K., Ishida Y., Xiong J., Matsushita M., Endo Y., Miura S., Ishii N., Sugamura K., and Fujita T. Mannose-binding lectin (MBL)-associated serine protease (MASP)-1 contributes to activation of the lectin complement pathway. J. Immunol. 180 (2008) 6132-6138
36. Tamura K., Dudley J., Nei M., and Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24 (2007) 1596-1599
37. Terado T., Smith S.L., Nakanishi T., Nonaka M.I., Kimura H., and Nonaka M. Occurrence of structural specialization of the serine protease domain of complement factor B at the emergence of jawed vertebrates and adaptive immunity. Immunogenetics 53 (2001) 250-254
38. Thai C.T., and Ogata R.T. Complement components C5 and C7: recombinant factor I modules of C7 bind to the C345C domain of C5. J. Immunol. 173 (2004) 4547-4552
39. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., and Higgins D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25 (1997) 4876-4882
40. Volanakis J.E. Overview of the Complement System (1998), Marcel Dekker Inc., New York pp. 9-32
41. Yoshizaki F.Y., Ikawa S., Satake M., Satoh N., and Nonaka M. Structure and the evolutionary implication of the triplicated complement factor B genes of a urochordate ascidian, Ciona intestinalis. Immunogenetics 56 (2005) 930-942
42. Zhu Y., Thangamani S., Ho B., and Ding J.L. The ancient origin of the complement system. Embo J. 24 (2005) 382-394