Characterization of the gene encoding component C3 of the complement system from the spider Loxosceles laeta venom glands: Phylogenetic implications

Immunobiology

Volumn 221, Issue 9, 2016, Pages 953-963

  Myamoto, D T ^a   Pidde Queiroz, G ^a   Pedroso, A ^a   Goncalves de Andrade R M ^a   van den Berg, C W ^b   Tambourgi, D V ^a  

^a INSTITUTO BUTANTAN   (Brazil)

^b CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

C3; Complement system; Gene; Loxosceles; Phylogenetic analysis; Spider

Indexed keywords

ALTERNATIVE COMPLEMENT PATHWAY C3 C5 CONVERTASE; AMINO ACID; COMPLEMENT COMPONENT C3; COMPLEMENTARY DNA; RNA; SPIDER VENOM; THIOESTER; ARTHROPOD PROTEIN; LOXOSCELES VENOM; PHOSPHODIESTERASE;

AMINO ACID SEQUENCE; ARTICLE; COMPLEMENT SYSTEM; CONTROLLED STUDY; DNA SEQUENCE; FEMALE; HASARIUS ADANSONI; INNATE IMMUNITY; LOXOSCELES LAETA; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA ISOLATION; SEQUENCE HOMOLOGY; SPIDER; ANIMAL; EXOCRINE GLAND; GENETICS; IMMUNOLOGY; NUCLEOTIDE SEQUENCE;

AMINO ACID SEQUENCE; ANIMALS; ARTHROPOD PROTEINS; BASE SEQUENCE; COMPLEMENT C3; DNA, COMPLEMENTARY; EXOCRINE GLANDS; FEMALE; PHOSPHORIC DIESTER HYDROLASES; PHYLOGENY; SEQUENCE ANALYSIS, DNA; SPIDER VENOMS; SPIDERS;

EID: 84973537489     PISSN: 01712985     EISSN: 18783279     Source Type: Journal    
DOI: 10.1016/j.imbio.2016.05.009     Document Type: Article

References (58)

1. Adams M.D., Celniker S.E., Holt R.A., Evanus C.A., Gocaynej D., Amanatides P.G., Scherer S.E., Li P.W., Hoskins R.A., Galle R.F. The genome sequence of Drosophila melanogaster. Science 2000, 287:85-95.
2. Al-Sharif W.Z., Sunyer J.O., Lambris J.D., Smith L.C. Sea urchin coelomocytes specifically express a homologue of the complement component C3. J. Immunol. 1998, 160:2983-2997.
3. Alper C.A., Balavitch D. Cobra venom factor: evidence for its being altered Cobra C3 (the third component of complement). Science 1976, 191:1275-1276.
4. Ariki S., Takahara S., Shibata T., Fukuoka T., Ozaki A., Endo Y., Fujita T., Koshiba T., Kawabata S. Factor C acts a lipopolysaccharide-responsive C3 convertase in horseshoe crab complement activation. J. Immunol. 2008, 181:7994-8001.
5. Ausubel F.A. Curr. Protoc. Mol. Biol. 1995, vol. 2. John Wiley and Sons, New York.
6. Boshra H., Gelman A.E., Sunyer J.O. Structural and functional characterization of complement C4 and C1s-like molecules in teleost fish: insights into the evolution of classical and alternative pathways. J. Immunol. 2004, 173:349-359.
7. Buresova V., Hajdusek O., Franta Z., Loosova G., Grunclova L., Levashina E.A., Kopacek P. Functional genomics of tick thioester-containing proteins reveal the ancient origin of the complement system. J. Innate. Immun. 2011, 3:623-630.
8. Castillo M.G., Goodson M.S., McFall-Ngai M. Identification and molecular characterization of a complement C3 molecule in a lophotrochozoan, the Hawaiian bobtail squid Euprymna scolopes. Dev. Comp. Immunolol. 2009, 33:69-76.
9. Clow L.A., Raftos D.A., Gross P.S., Smith L.C. The sea urchin complement homologue, SpC3, functions as an opsonin. J. Exp. Biol. 2004, 207:2147-2155.
10. Dishaw L.J., Smith S.L., Bigger C.H. Characterization of a C3-like cDNA in a coral: phylogenetic implications. Immunogenetics 2005, 57:535-548.
11. Doods A.W. Which came first, the lectin/classical pathway or the alternative pathway of complement?. Immunobiology 2002, 205:340-354.
12. Fernandes-Pedrosa M., Junqueira-de-Azevedo I.L.M., Gonçalves-de-Andrade R.M., Kobashi L.S., Almeida D.D., Lee Ho P., Tambourgi D.V. Transcriptome analysis of Loxosceles laeta (Araneae, Sicariidae) spider venomous gland using expressed sequence tags. BMC Genom. 2008, 9:1-12.
13. Fritzinger D.C., Bredehorst R., Vogel C.W. Molecular cloning and derived primary structure of cobra venom factor. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:12775-12779.
14. Fujito N.T., Sugimoto S., Nonaka M. Evolution of thioester-containing proteins revealed by cloning and characterization of their genes from a cnidarian sea anemone, Haliplanela lineate. Dev. Comp. Immunol. 2010, 34:775-784.
15. Futrell J. Loxoscelism. Am. J. Med. Sci. 1992, 304:261-267.
16. Gadjeva M., Doods A.W., Taniguchi-Sidle A., Willis A.C., Isenman D.E., Law S.K. The covalent binding reaction of complement component C3. J. Immunol. 1998, 161:985-990.
17. Gao Z., Li M., Wu J., Zhang S. Interplay between invertebrate C3a with vertebrate macrophages: functional characterization of immune activities of amphioxus C3a. Fish Shellfish Immunol. 2013, 35:1249-1259.
18. Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 1999, 41:95-98.
19. Hogan C.J.H., Barbaro K.C., Winkel K. Loxoscelism old obstacles, new directions. Ann. Emerg. Med. 2004, 44:608-624.
20. Holmes D.S., Quigley M. A rapid boiling method for the preparation of bacterial plasmids. Anal. Biochem. 1991, 114:193-197.
21. Isaac L., 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. 1992, 267:10062-10069.
22. Janssen B.J.C., Huizinga E.G., Raaijmakers H.C.A., Roos A., Daha M.R., Nilsson-Ekdahl K., Nilsson B., Gros P. Structures of complement component C3 provides insights into the function and evolution of immunity. Nature 2005, 437:505-511.
23. Kimura A., Sakaguchi E., Nonaka M. Multi-component complement system of Cnidaria: c3, Bf, and MASP genes expressed in the endodermal tissues of a sea anemone, Nematostela vectensis. Immunobiology 2009, 214:165-178.
24. Krishnan V., Ponnuraj K., Xu Y., Macon K., Volanakis J.E., Narayana S.V.L. The crystal structure of cobra venom factor, a cofactor for C3 and C5 convertase CVFBb. Structure 2009, 17:611-619.
25. Levashina E.A., Moita L.F., Blandin S., Vriend G., Lagueux M., 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 2001, 104:709-718.
26. Marino R., Kimura Y., De Santis R., Lambris J.D., Pinto M.R. Complement in urochordates: cloning and characterization of two C3-like genes in the ascidian Ciona intestinalis. Immunogenetics 2002, 53:1055-1064.
27. Miller D.J., Hemmrich G., Ball E.E., Hayward D.C., Khalturin K., Funayama N., Agata K., Bosch T.C.G. The innate immune repertoire in Cnidaria-ancestral complexity and stochastic gene loss. Genome Biol. 2007, 8:R59.
28. Myamoto D.T., Pidde-Queiroz G., Gonçalves-de-Andrade R.M., Pedroso A., van den Berg C.W., Tambourgi D.V. Characterization of a gene coding for the complement system component FB from Loxosceles laeta spider venom glands. PLoS One 2016, 11(1):e0146992.
29. Nonaka M. The complement C3 protein family in invertebrates. Invertebr. Surviv. J. 2011, 8:21-32.
30. Nonaka M. Evolution of complement system. Subcell. Biochem. 2014, 80:31-43.
31. Nonaka M., Azumi K. Opsonic complement system of the solitary ascidian: halocynthia roretzi. Dev. Comp. Immunol. 1999, 23:421-427.
32. Nonaka M., Kimura A. Genomic view of the evolution of the complement system. Immunogenetics 2006, 58:701-713.
33. Nonaka M., Fujii T., Kaidoh T., Natsuume-Sakai S., Nonaka M., Yamaguchi N., Takahashi M. Purification of a lamprey complement protein homologous to the third component of the mammalian complement system. J. Immunol. 1984, 133:3242-3249.
34. Nonaka M., Nakayama K., Yeul Y.D., Takahashi M. Complete nucleotide and derived amino acid sequences of the fourth component of mouse complement (C4). J. Biol. Chem. 1985, 260:10936-10943.
35. Parkison J., Blaxter M. Expressed sequence tags: an overview. Methods Mol. Biol. 2009, 533:1-12.
36. Pasupuleti M., Walse B., Nordahl E.A., Mörgelin M., Malmsten M., Schmidchen A. Preservation of antimicrobial properties of complement peptide C3a: from invertebrates to humans. J. Biol. Chem. 2006, 282:2520-2528.
37. Pinto M.R., Chinnici C.M., Kimura Y., Mellilo D., Marino R., Spruce L.A., De Santis R., Parrinelo N., Lambris J.D. CiC3-1a-mediated chemotaxis in the deuterostome invertebrate Ciona intestinalis (Urochordata). J. Immunol. 2003, 171:5521-5528.
38. Prado-Alvarez M., Rotland J., Gestal C., Novoa B., Figueras A. Characterization of a C3 and a factor B-like protein in the carpet-shell clam: Ruditapes decussatus. Fish Shellfish Immunol. 2009, 26:305-315.
39. Sahu A., Lambrism J.D. Structure and biology of complement protein C3: a connecting link between innate and acquired immunity. Immunol. Rev. 2001, 180:35-48.
40. Schmid E., Warner R.L., Crouch L.D., Friedl H.P., Till G.O., Hugli T.E., Ward P.A. Neutrophil chemotactic activity and C5a following systemic activation of complement in rats. Inflammation 1997, 21:325-333.
41. Sekiguchi R., Nonaka M. Evolution of the complement system in protostomes revealed by de novo transcriptome analysis of six species of Arthropoda. Dev. Comp. Immunol. 2015, 50:58-67.
42. Sekiguchi R., Fujito N.T., Nonaka M. Evolution of the thioester-containing proteins (TEPs) of the arthropoda revealed by molecular cloning of TEP genes from a spider, Hasarius adansoni. Dev. Comp. Immunol. 2012, 36:483-489.
43. Smith L.C., Shih C., Dachenhausen S.G. Coelomocytes express SpBf, a homologue of factor B, the second component in the sea urchin complement system. J. Immunol. 1998, 161:6784-6793.
44. Suzuki M.M., Satoh N., Nonaka M. C6-like and C3-like molecules from the Cephalochordate, amphioxus, suggest a cytolytic complement system in invertebrates. J. Mol. Evol. 2002, 54:671-679.
45. Tambourgi D.V., Magnoli F.C., Von Eickstedt V.R., Benedetti Z.C., Petricevich V.L., da Silva W.D. Incorporation of a 35-kilodalton purified protein from Loxosceles intermedia spider venom transforms human erythrocytes into activators of autologous complement alternative pathway. J. Immunol. 1995, 155:4459-4466.
46. Tambourgi D.V., Magnoli F.C., van der Berg C.W., Morgan B.P., de Araujo P.S., Alves E.W., da Silva W.D. Sphingomyelinases in the venom of the spider Loxosceles intermedia are responsible for both dermonecrosis and complement-dependent hemolysis. Biochem. Biophys. Res. Commun. 1998, 251:366-373.
47. Tambourgi D.V., Morgan B.P., Gonçalves-de-Andrade R.M., Magnoli F.C., van den berg C.W. Loxosceles intermedia spider envenomation induces activation of an endogenous metalloproteinase, resulting in cleavage of glycophorins from erythrocyte surface and facilitating complement-mediated lysis. Blood 2000, 95:683-691.
48. Tambourgi D.V., Paixão-Cavalcante D., Gonçalves-de-Andrade R.M., Fernandes-Pedrosa M., Magnoli F.C., Morgan B.P., van den Berg C.W. Loxosceles sphingomyelinase induces complement-dependent dermonecrosis, neutrophil infiltration, and endogenous gelatinase expression. J. Invest. Dermatol. 2005, 124:725-731.
49. Tambourgi D.V., Gonçalves de Andrade R.M., van den Berg C.W. Loxoscelism: from basic research to the proposal of new therapies. Toxicon 2010, 56:1113-1119.
50. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 2013, 30:2725-2729.
51. The C.elegans Sequencing Consortium Genome Sequence of the nematode C. elegans: a platform for investigating biology. Science 1999, 282:2012-2018.
52. Vogel C.W., Smith C.A., Müller-Eberhard H.J. Cobra venom factor: structural homology with the third component of human complement. J. Immunol. 1984, 133:3235-3241.
53. Walport M.J. Complement. First of two parts. N. Engl. J. Med. 2001, 344:1058-1066.
54. Xu T., Xie J., Li J., Luo M., Ye S., Wu X. Identification of expressed genes in cDNA library of hemocytes from the RLO-challenged oyster Crassostrea ariakensis Gould with special functional implication of three complement-related fragments (CaC1q1, CaC1q2 and CaC3). Fish Shellfish Immunol. 2012, 32:1106-1116.
55. Yoshizaki F.Y., Ikawa S., Satake M., Satoh N., Nonaka M. Structure and the evolutionary implication of the triplicated complement factor B genes of a urochordate ascidian, Ciona intestinalis. Immunogenetics 2005, 56:930-942.
56. Zarkadis I.K., Mastellos D., Lambris J. Phylogenetic aspects of the complement system. Dev. Comp. Immunol. 2001, 25:745-762.
57. Zhang H., Song L., Li C., Zhao J., Wang H., Qiang G., Xu W. Molecular cloning and characterization of a thioester-containing protein from Zhikong scallop Chlamys farreri. Mol. Immunol. 2007, 44:3492-3500.
58. Zhu Y., Thangamani S., Ho B., Ding L.D. The ancient origin of the complement system. EMBO J. 2005, 24:382-394.