Identification and molecular characterization of a complement C3 molecule in a lophotrochozoan, the Hawaiian bobtail squid Euprymna scolopes

Developmental and Comparative Immunology

Volumn 33, Issue 1, 2009, Pages 69-76

  Castillo, Maria G ^a   Goodson, Michael S ^b   McFall Ngai, Margaret ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF DAYTON   (United States)

Author keywords

Cephalopod; Immunocytochemistry; Innate immunity; Invertebrate immunity; Lophotrochozoa; Mollusk; Symbiosis

Indexed keywords

COMPLEMENT COMPONENT C3;

AMINO ACID SEQUENCE; ANIMAL TISSUE; ARTICLE; GENE; GENE EXPRESSION; IMMUNOCYTOCHEMISTRY; INNATE IMMUNITY; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN ANALYSIS; SEQUENCE HOMOLOGY; SQUID;

ANIMALIA; CEPHALOPODA; EUPRYMNA SCOLOPES; INVERTEBRATA; LOPHOTROCHOZOA; SEPIOLIDAE;

AMINO ACID SEQUENCE; ANIMALS; COMPLEMENT C3; DECAPODIFORMES; MOLECULAR SEQUENCE DATA; ORGAN SPECIFICITY; PHYLOGENY;

EID: 53849091298     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2008.07.013     Document Type: Article

References (43)

1. Carroll M.C. The complement system in regulation of adaptive immunity. Nature Immunol 5 (2004) 981-986
2. Morgan B.P., Marchbank K.J., Longhi M.P., Harris C.L., and Gallimore A.M. Complement: central to innate immunity and bridging to adaptive responses. Immunol Lett 97 (2005) 171-179
3. Nielsen C.H., and Leslie R.G. Complement's participation in acquired immunity. J Leuk Biol 72 (2002) 249-261
4. Volanakis J. Overview of the complement system. In: Volanakis J., and Frank M. (Eds). The human complement system in health and disease (1998), Marcel Dekker, New York 9-32
5. Sahu A., and Lambris J.D. Structure and biology of complement protein C3, a connecting link between innate and acquired immunity. Immun Rev 180 (2001) 35-48
6. Blandin S., and Levashina E.A. Thioester-containing proteins and insect immunity. Mol Immunol 40 (2004) 903-908
7. Nair S.V., Del Valle H., Gross P.S., Terwilliger D.P., and 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 Gen 22 (2005) 33-47
8. Al-Sharif W.Z., Sunyer J.O., Lambris J.D., and Smith L.C. Sea urchin coelomocytes specifically express a homologue of the complement component C3. J Immunol 160 (1998) 2983-2997
9. Zhu Y., Thangamani S., Ho B., and Ding J.L. The ancient origin of the complement system. EMBO J 24 (2005) 382-394
10. 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
11. Fujita T., Matsushita M., and Endo Y. The lectin-complement pathway-its role in innate immunity and evolution. Immun Rev 198 (2004) 185-202
12. Nonaka M., and Yoshizaki F. Primitive complement system of invertebrates. Immun Rev 198 (2004) 203-215
13. Nonaka M., and Yoshizaki F. Evolution of the complement system. Mol Immunol 40 (2004) 897-902
14. Nonaka M., and Kimura A. Genomic view of the evolution of the complement system. Immunogenetics 58 (2006) 701-713
15. Pinto M.R., Melillo D., Giacomelli S., Sfyroera G., and Lambris J.D. Ancient origin of the complement system: emerging invertebrate models. Adv Exp Med Biol 598 (2007) 372-388
16. Janssen B.J., Huizinga E.G., Raaijmakers H.C., Roos A., Daha M.R., Nilsson-Ekdahl K., et al. Structures of complement component C3 provide insights into the function and evolution of immunity. Nature 437 (2005) 505-511
17. Nyholm S.V., and McFall-Ngai M.J. The winnowing: establishing the squid-Vibrio symbiosis. Nat Rev Microbiol 2 (2004) 632-642
18. Visick K.L., and Ruby E.G. Vibrio fischeri and its host: it takes two to tango. Curr Opin Microbiol 9 (2006) 632-638
19. Foster J.S., Apicella M.A., and McFall-Ngai M.J. Vibrio fischeri lipopolysaccharide induces developmental apoptosis, but not complete morphogenesis, of the Euprymna scolopes symbiotic light organ. Dev Biol 226 (2000) 242-254
20. Koropatnick T.A., Engle J.T., Apicella M.A., Stabb E.V., Goldman W.E., and McFall-Ngai M.J. Microbial factor-mediated development in a host-bacterial mutualism. Science 306 (2004) 1186-1188
21. Weis V.M., Small A.L., and McFall-Ngai M.J. A peroxidase related to the mammalian antimicrobial protein myeloperoxidase in the Euprymna-Vibrio mutualism. Proc Natl Acad Sci USA 93 (1996) 13683-13688
22. Small A.L., and McFall-Ngai M.J. A halide peroxidase in tissues that interact with bacteria in the host squid Euprymna scolopes. J Cell Biochem 72 (1999) 445-457
23. Davidson S.K., Koropatnick T.A., Kossmehl R., Sycuro L., and McFall-Ngai M.J. NO means 'yes' in the squid-vibrio symbiosis: nitric oxide (NO) during the initial stages of a beneficial association. Cell Microbiol 6 (2004) 1139-1151
24. Nyholm S.V., Stabb E.V., Ruby E.G., and McFall-Ngai M.J. Establishment of an animal-bacterial association: recruiting symbiotic vibrios from the environment. Proc Natl Acad Sci USA 97 (2000) 10231-10235
25. Nyholm S.V., Deplancke B., Gaskins H.R., Apicella M.A., and McFall-Ngai M.J. Roles of Vibrio fischeri and nonsymbiotic bacteria in the dynamics of mucus secretion during symbiont colonization of the Euprymna scolopes light organ. Appl Environ Microbiol 68 (2002) 5113-5122
26. Nyholm S.V., and McFall-Ngai M.J. Sampling the light-organ microenvironment of Euprymna scolopes: description of a population of host cells in association with the bacterial symbiont Vibrio fischeri. Biol Bull 195 (1998) 89-97
27. Koropatnick T.A., Kimbell J.R., and McFall-Ngai M.J. Responses of host hemocytes during the initiation of the squid-Vibrio symbiosis. Biol Bull 212 (2007) 29-39
28. Boettcher K.J., and Ruby E.G. Depressed light emission by symbiotic Vibrio fischeri of the sepiolid squid Euprymna scolopes. J Bacteriol 172 (1990) 3701-3706
29. Chun C.K., Scheetz T.E., Bonaldo M., de F., Brown B., Clemens A., et al. An annotated cDNA library of juvenile Euprymna scolopes with and without colonization by the symbiont Vibrio fischeri. BMC Genomics 7 (2006) 154-163
30. 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. Nucl Acids Res 25 (1997) 4876-4882
31. Felsenstein J. PHYLIP: phylogeny inference package (version 3.2). Cladistics 5 (1989) 164-166
32. Kishino H., and Hasegawa M. Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in Hominoidea. J Mol Evol 29 (1989) 170-179
33. 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
34. Dolmer K., and Sottrup-Jensen L. Disulfide bridges in human complement component C3b. FEBS Lett 315 (1993) 85-90
35. 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
36. Nonaka M., and Azumi K. Opsonic complement system of the solitary ascidian, Halocynthia roretzi. Dev Comp Immunol 23 (1999) 421-427
37. Law S.K., and Dodds A.W. The internal thioester and the covalent binding properties of the complement proteins C3 and C4. Protein Sci 6 (1997) 263-274
38. Nagar B., Jones R.G., Diefenbach R.J., Isenman D.E., and Rini J.M. X-ray crystal structure of C3d: a C3 fragment and ligand for complement receptor 2. Science 280 (1998) 1277-1281
39. Levashina E.A., Moita L.F., Blandin S., Vriend G., Lagueux M., and Kafatos F.C. Conserved role of a complement-like protein in phagocytosis revealed by dsRNA knockout in cultured cells of the mosquito, Anopheles gambiae. Cell 104 (2001) 709-718
40. Zhang H., Song L., Li C., Zhao J., Wang H., Gao Q., et al. Molecular cloning and characterization of a thioester-containing protein from Zhikong scallop Chlamys farreri. Mol Immunol 44 (2007) 3492-3500
41. 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
42. Botto M. Part 3. C3 family. In: Morley B.J., and Walport M.J. (Eds). The complement facts book (2000), Academic Press, San Diego, CA 87-94
43. Isaac L., and Isenman D.E. Structural requirements for thioester bond formation in human complement component C3. Reassessment of the role of thioester bond integrity on the conformation of C3. J Biol Chem 267 (1992) 10062-10069