Skip to main content
The EMBO Journal logoLink to The EMBO Journal
. 1992 Mar;11(3):829–837. doi: 10.1002/j.1460-2075.1992.tb05120.x

Isolation of a hagfish gene that encodes a complement component.

H Ishiguro 1, K Kobayashi 1, M Suzuki 1, K Titani 1, S Tomonaga 1, Y Kurosawa 1
PMCID: PMC556522  PMID: 1372251

Abstract

It has been widely accepted that cyclostomes are the most primitive vertebrates extant with the ability to produce antibodies. We isolated cDNA clones that encode a putative 'antibody' from one of the cyclostomes, Eptatretus burgeri. The amino acid sequence predicted from the nucleotide sequences of the cDNA clones indicated that this gene does actually encode the proteins isolated as hagfish 'antibodies' by various investigators. However, these proteins are not similar to mammalian immunoglobulins but have some characteristics common to complements C3, C4 and C5 in higher vertebrates. We discuss the relationships of the isolated gene for hagfish complement with the mammalian genes for complements C3, C4 and C5. We also discuss the possibility of the presence of antibodies in cyclostomes.

Full text

PDF
829

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ardavín C. F., Zapata A. Ultrastructure and changes during metamorphosis of the lympho-hemopoietic tissue of the larval anadromous sea lamprey Petromyzon marinus. Dev Comp Immunol. 1987 Winter;11(1):79–93. doi: 10.1016/0145-305x(87)90010-3. [DOI] [PubMed] [Google Scholar]
  2. Becherer J. D., Alsenz J., Lambris J. D. Molecular aspects of C3 interactions and structural/functional analysis of C3 from different species. Curr Top Microbiol Immunol. 1990;153:45–72. doi: 10.1007/978-3-642-74977-3_3. [DOI] [PubMed] [Google Scholar]
  3. Belt K. T., Carroll M. C., Porter R. R. The structural basis of the multiple forms of human complement component C4. Cell. 1984 Apr;36(4):907–914. doi: 10.1016/0092-8674(84)90040-0. [DOI] [PubMed] [Google Scholar]
  4. Benton W. D., Davis R. W. Screening lambdagt recombinant clones by hybridization to single plaques in situ. Science. 1977 Apr 8;196(4286):180–182. doi: 10.1126/science.322279. [DOI] [PubMed] [Google Scholar]
  5. Braciak T. A., Northemann W., Hudson G. O., Shiels B. R., Gehring M. R., Fey G. H. Sequence and acute phase regulation of rat alpha 1-inhibitor III messenger RNA. J Biol Chem. 1988 Mar 15;263(8):3999–4012. [PubMed] [Google Scholar]
  6. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  7. Daoudaki M. E., Becherer J. D., Lambris J. D. A 34-amino acid peptide of the third component of complement mediates properdin binding. J Immunol. 1988 Mar 1;140(5):1577–1580. [PubMed] [Google Scholar]
  8. Day N. K., Gewurz H., Johannsen R., Finstad J., Good R. A. Complement and complement-like activity in lower vertebrates and invertebrates. J Exp Med. 1970 Nov;132(5):941–950. doi: 10.1084/jem.132.5.941. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Devriendt K., Van den Berghe H., Cassiman J. J., Marynen P. Primary structure of pregnancy zone protein. Molecular cloning of a full-length PZP cDNA clone by the polymerase chain reaction. Biochim Biophys Acta. 1991 Jan 17;1088(1):95–103. doi: 10.1016/0167-4781(91)90157-h. [DOI] [PubMed] [Google Scholar]
  10. Farries T. C., Atkinson J. P. Evolution of the complement system. Immunol Today. 1991 Sep;12(9):295–300. doi: 10.1016/0167-5699(91)90002-B. [DOI] [PubMed] [Google Scholar]
  11. Fujii T. Electron microscopy of the leucocytes of the typhlosole in ammocoetes, with special attention to the antibody-producing cells. J Morphol. 1982 Jul;173(1):87–100. doi: 10.1002/jmor.1051730108. [DOI] [PubMed] [Google Scholar]
  12. Gordon A. H. The alpha macroglobulins of rat serum. Biochem J. 1976 Dec 1;159(3):643–650. doi: 10.1042/bj1590643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gross-Bellard M., Oudet P., Chambon P. Isolation of high-molecular-weight DNA from mammalian cells. Eur J Biochem. 1973 Jul 2;36(1):32–38. doi: 10.1111/j.1432-1033.1973.tb02881.x. [DOI] [PubMed] [Google Scholar]
  14. Grossberger D., Marcuz A., Du Pasquier L., Lambris J. D. Conservation of structural and functional domains in complement component C3 of Xenopus and mammals. Proc Natl Acad Sci U S A. 1989 Feb;86(4):1323–1327. doi: 10.1073/pnas.86.4.1323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gubler U., Hoffman B. J. A simple and very efficient method for generating cDNA libraries. Gene. 1983 Nov;25(2-3):263–269. doi: 10.1016/0378-1119(83)90230-5. [DOI] [PubMed] [Google Scholar]
  16. Hagen M., Filosa M. F., Youson J. H. Immunocytochemical localization of antibody-producing cells in adult lamprey. Immunol Lett. 1983 Feb;6(2):87–92. doi: 10.1016/0165-2478(83)90086-x. [DOI] [PubMed] [Google Scholar]
  17. Hanley P. J., Seppelt I. M., Gooley A. A., Hook J. W., Raison R. L. Distinct Ig H chains in a primitive vertebrate, Eptatretus stouti. J Immunol. 1990 Dec 1;145(11):3823–3828. [PubMed] [Google Scholar]
  18. Hashimoto K., Nakanishi T., Kurosawa Y. Isolation of carp genes encoding major histocompatibility complex antigens. Proc Natl Acad Sci U S A. 1990 Sep;87(17):6863–6867. doi: 10.1073/pnas.87.17.6863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hinds K. R., Litman G. W. Major reorganization of immunoglobulin VH segmental elements during vertebrate evolution. Nature. 1986 Apr 10;320(6062):546–549. doi: 10.1038/320546a0. [DOI] [PubMed] [Google Scholar]
  20. Kobayashi K., Tomonaga S., Hagiwara K. Isolation and characterization of immunoglobulin of hagfish, Eptatretus burgeri, a primitive vertebrate. Mol Immunol. 1985 Sep;22(9):1091–1097. doi: 10.1016/0161-5890(85)90112-9. [DOI] [PubMed] [Google Scholar]
  21. Linthicum D. S., Hildemann W. H. Immunologic responses of Pacific hagfish. 3. Serum antibodies to cellular antigens. J Immunol. 1970 Oct;105(4):912–918. [PubMed] [Google Scholar]
  22. Marchalonis J. J., Edelman G. M. Phylogenetic origins of antibody structure. 3. Antibodies in the primary immune response of the sea lamprey, Petromyzon marinus. J Exp Med. 1968 May 1;127(5):891–914. doi: 10.1084/jem.127.5.891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Marchalonis J. J., Schluter S. F. Immunoproteins in evolution. Dev Comp Immunol. 1989 Fall;13(4):285–301. doi: 10.1016/0145-305x(89)90039-6. [DOI] [PubMed] [Google Scholar]
  24. Matsudaira P. Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membranes. J Biol Chem. 1987 Jul 25;262(21):10035–10038. [PubMed] [Google Scholar]
  25. Müller-Eberhard H. J., Schreiber R. D. Molecular biology and chemistry of the alternative pathway of complement. Adv Immunol. 1980;29:1–53. doi: 10.1016/s0065-2776(08)60042-5. [DOI] [PubMed] [Google Scholar]
  26. 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 Dec;133(6):3242–3249. [PubMed] [Google Scholar]
  27. PILLEMER L., BLUM L., LEPOW I. H., WURZ L., TODD E. W. The properdin system and immunity. III. The zymosan assay of properdin. J Exp Med. 1956 Jan 1;103(1):1–13. doi: 10.1084/jem.103.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Raison R. L., Hull C. J., Hildemann W. H. Characterization of immunoglobulin from the Pacific hagfish, a primitive vertebrate. Proc Natl Acad Sci U S A. 1978 Nov;75(11):5679–5682. doi: 10.1073/pnas.75.11.5679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Saiki R. K., Gelfand D. H., Stoffel S., Scharf S. J., Higuchi R., Horn G. T., Mullis K. B., Erlich H. A. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988 Jan 29;239(4839):487–491. doi: 10.1126/science.2448875. [DOI] [PubMed] [Google Scholar]
  30. Sottrup-Jensen L., Stepanik T. M., Kristensen T., Lønblad P. B., Jones C. M., Wierzbicki D. M., Magnusson S., Domdey H., Wetsel R. A., Lundwall A. Common evolutionary origin of alpha 2-macroglobulin and complement components C3 and C4. Proc Natl Acad Sci U S A. 1985 Jan;82(1):9–13. doi: 10.1073/pnas.82.1.9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Stimler-Gerard N. P. Immunopharmacology of anaphylatoxin-induced bronchoconstrictor responses. Complement. 1986;3(3):137–151. doi: 10.1159/000467891. [DOI] [PubMed] [Google Scholar]
  32. Tack B. F. The beta-Cys-gamma-Glu thiolester bond in human C3, C4, and alpha 2-macroglobulin. Springer Semin Immunopathol. 1983;6(4):259–282. doi: 10.1007/BF02116276. [DOI] [PubMed] [Google Scholar]
  33. Varner J., Neame P., Litman G. W. A serum heterodimer from hagfish (Eptatretus stoutii) exhibits structural similarity and partial sequence identity with immunoglobulin. Proc Natl Acad Sci U S A. 1991 Mar 1;88(5):1746–1750. doi: 10.1073/pnas.88.5.1746. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Wetsel R. A., Lundwall A., Davidson F., Gibson T., Tack B. F., Fey G. H. Structure of murine complement component C3. II. Nucleotide sequence of cloned complementary DNA coding for the alpha chain. J Biol Chem. 1984 Nov 25;259(22):13857–13862. [PubMed] [Google Scholar]
  35. Wetsel R. A., Ogata R. T., Tack B. F. Primary structure of the fifth component of murine complement. Biochemistry. 1987 Feb 10;26(3):737–743. doi: 10.1021/bi00377a013. [DOI] [PubMed] [Google Scholar]
  36. Williams A. F., Barclay A. N. The immunoglobulin superfamily--domains for cell surface recognition. Annu Rev Immunol. 1988;6:381–405. doi: 10.1146/annurev.iy.06.040188.002121. [DOI] [PubMed] [Google Scholar]
  37. Wright S. D., Reddy P. A., Jong M. T., Erickson B. W. C3bi receptor (complement receptor type 3) recognizes a region of complement protein C3 containing the sequence Arg-Gly-Asp. Proc Natl Acad Sci U S A. 1987 Apr;84(7):1965–1968. doi: 10.1073/pnas.84.7.1965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. de Bruijn M. H., Fey G. H. Human complement component C3: cDNA coding sequence and derived primary structure. Proc Natl Acad Sci U S A. 1985 Feb;82(3):708–712. doi: 10.1073/pnas.82.3.708. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES