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. 1996 Mar 5;93(5):1886–1891. doi: 10.1073/pnas.93.5.1886

The joining (J) chain is present in invertebrates that do not express immunoglobulins.

T Takahashi 1, T Iwase 1, N Takenouchi 1, M Saito 1, K Kobayashi 1, Z Moldoveanu 1, J Mestecky 1, I Moro 1
PMCID: PMC39877  PMID: 8700853

Abstract

Joining (J) chain is a component of polymeric, but not monomeric, immunoglobulin (Ig) molecules and may play a role in their polymerization and transport across epithelial cells. To date, study of the J chain has been confined to vertebrates that produce Ig and in which the J chain displays a considerable degree of structural homology. The role of the J chain in Ig polymerization has been questioned and, since the J chain can be expressed in lymphoid cells that do not produce Ig, it is possible that the J chain may have other functions. To explore this possibility, we have surveyed J-chain gene, mRNA, and protein expression by using reverse transcriptase-coupled PCR, Northern blot analysis, and immunoblot analysis in invertebrate species that do not produce Ig. We report that the J-chain gene is expressed in invertebrates (Mollusca, Annelida, Arthropoda, Echinodermata, and Holothuroidea), as well as in representative vertebrates (Mammalia, Teleostei, Amphibia). Furthermore, J-chain cDNA from the earthworm has a high degree of homology (68-76%) to human, mouse, and bovine J chains. Immunohistochemical studies reveal that the J chain is localized in the mucous cells of body surfaces, intestinal epithelial cells, and macrophage-like cells of the earthworm and slug. This study suggests that the J chain is a primitive polypeptide that arose before the evolution of Ig molecules and remains highly conserved in extent invertebrates and vertebrates.

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Selected References

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

  1. Brandtzaeg P. Presence of J chain in human immunocytes containing various immunoglobulin classes. Nature. 1974 Nov 29;252(5482):418–420. doi: 10.1038/252418a0. [DOI] [PubMed] [Google Scholar]
  2. Brandtzaeg P. Role of J chain and secretory component in receptor-mediated glandular and hepatic transport of immunoglobulins in man. Scand J Immunol. 1985 Aug;22(2):111–146. doi: 10.1111/j.1365-3083.1985.tb01866.x. [DOI] [PubMed] [Google Scholar]
  3. Carayannopoulos L., Max E. E., Capra J. D. Recombinant human IgA expressed in insect cells. Proc Natl Acad Sci U S A. 1994 Aug 30;91(18):8348–8352. doi: 10.1073/pnas.91.18.8348. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cattaneo A., Neuberger M. S. Polymeric immunoglobulin M is secreted by transfectants of non-lymphoid cells in the absence of immunoglobulin J chain. EMBO J. 1987 Sep;6(9):2753–2758. doi: 10.1002/j.1460-2075.1987.tb02569.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. 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]
  6. Cooper E. L., Rinkevich B., Uhlenbruck G., Valembois P. Invertebrate immunity: another viewpoint. Scand J Immunol. 1992 Mar;35(3):247–266. doi: 10.1111/j.1365-3083.1992.tb02857.x. [DOI] [PubMed] [Google Scholar]
  7. Davis A. C., Roux K. H., Pursey J., Shulman M. J. Intermolecular disulfide bonding in IgM: effects of replacing cysteine residues in the mu heavy chain. EMBO J. 1989 Sep;8(9):2519–2526. doi: 10.1002/j.1460-2075.1989.tb08389.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Eskeland T., Brandtzaeg P. Does J chain mediate the combination of 19S IgM and dimeric IgA with the secretory component rather than being necessary for their polymerization? Immunochemistry. 1974 Mar;11(3):161–163. doi: 10.1016/0019-2791(74)90214-6. [DOI] [PubMed] [Google Scholar]
  9. Furuta E., Yamaguchi K., Aikawa M., Shimozawa A. Phagocytosis by hemolymph cells of the land slug, Incilaria fruhstorferi Collinge (Gastropoda: Pulmonata). Anat Anz. 1987;163(2):89–99. [PubMed] [Google Scholar]
  10. Hajdu I., Moldoveanu Z., Cooper M. D., Mestecky J. Ultrastructural studies of human lymphoid cells. mu and J chain expression as a function of B cell differentiation. J Exp Med. 1983 Dec 1;158(6):1993–2006. doi: 10.1084/jem.158.6.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hughes G. J., Frutiger S., Paquet N., Jaton J. C. The amino acid sequence of rabbit J chain in secretory immunoglobulin A. Biochem J. 1990 Nov 1;271(3):641–647. doi: 10.1042/bj2710641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kaji H., Parkhouse R. M. Intracellular J chain in mouse plasmacytomas secreting IgA, IgM and IgG. Nature. 1974 May 3;249(452):45–47. doi: 10.1038/249045a0. [DOI] [PubMed] [Google Scholar]
  13. Kobayashi K., Vaerman J. P., Bazin H., LeBacq-Verheyden A. M., Heremans J. F. Identification of J-chain in polymeric immunoglobulins from a variety of species by cross-reaction with rabbit antisera to human J-chain. J Immunol. 1973 Nov;111(5):1590–1594. [PubMed] [Google Scholar]
  14. Koshland M. E. The coming of age of the immunoglobulin J chain. Annu Rev Immunol. 1985;3:425–453. doi: 10.1146/annurev.iy.03.040185.002233. [DOI] [PubMed] [Google Scholar]
  15. Kubagawa H., Burrows P. D., Grossi C. E., Mestecky J., Cooper M. D. Precursor B cells transformed by Epstein-Barr virus undergo sterile plasma-cell differentiation: J-chain expression without immunoglobulin. Proc Natl Acad Sci U S A. 1988 Feb;85(3):875–879. doi: 10.1073/pnas.85.3.875. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kutteh W. H., Moldoveanu Z., Prince S. J., Kulhavy R., Alonso F., Mestecky J. Biosynthesis of J-chain in human lymphoid cells producing immunoglobulins of various isotypes. Mol Immunol. 1983 Sep;20(9):967–976. doi: 10.1016/0161-5890(83)90037-8. [DOI] [PubMed] [Google Scholar]
  17. Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
  18. Ma J. K., Hiatt A., Hein M., Vine N. D., Wang F., Stabila P., van Dolleweerd C., Mostov K., Lehner T. Generation and assembly of secretory antibodies in plants. Science. 1995 May 5;268(5211):716–719. doi: 10.1126/science.7732380. [DOI] [PubMed] [Google Scholar]
  19. Mansour M. H., DeLange R., Cooper E. L. Isolation, purification, and amino acid composition of the tunicate hemocyte Thy-1 homolog. J Biol Chem. 1985 Mar 10;260(5):2681–2686. [PubMed] [Google Scholar]
  20. Mather E. L., Alt F. W., Bothwell A. L., Baltimore D., Koshland M. E. Expression of J chain RNA in cell lines representing different stages of B lymphocyte differentiation. Cell. 1981 Feb;23(2):369–378. doi: 10.1016/0092-8674(81)90132-x. [DOI] [PubMed] [Google Scholar]
  21. Matsuuchi L., Cann G. M., Koshland M. E. Immunoglobulin J chain gene from the mouse. Proc Natl Acad Sci U S A. 1986 Jan;83(2):456–460. doi: 10.1073/pnas.83.2.456. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Max E. E., Korsmeyer S. J. Human J chain gene. Structure and expression in B lymphoid cells. J Exp Med. 1985 Apr 1;161(4):832–849. doi: 10.1084/jem.161.4.832. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. McCune J. M., Fu S. M., Kunkel H. G. J chain biosynthesis in pre-B cells and other possible precursor B cells. J Exp Med. 1981 Jul 1;154(1):138–145. doi: 10.1084/jem.154.1.138. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mestecky J., McGhee J. R. Immunoglobulin A (IgA): molecular and cellular interactions involved in IgA biosynthesis and immune response. Adv Immunol. 1987;40:153–245. doi: 10.1016/s0065-2776(08)60240-0. [DOI] [PubMed] [Google Scholar]
  25. Mestecky J., Preud'homme J. L., Crago S. S., Mihaesco E., Prchal J. T., Okos A. J. Presence of J chain in human lymphoid cells. Clin Exp Immunol. 1980 Feb;39(2):371–385. [PMC free article] [PubMed] [Google Scholar]
  26. Mestecky J., Winchester R. J., Hoffman T., Kunkel H. G. Parallel synthesis of immunoglobulins and J chain in pokeweed mitogen-stimulated normal cells and in lymphoblastoid cell lines. J Exp Med. 1977 Mar 1;145(3):760–765. doi: 10.1084/jem.145.3.760. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Mikoryak C. A., Margolies M. N., Steiner L. A. J chain in Rana catesbeiana high molecular weight Ig. J Immunol. 1988 Jun 15;140(12):4279–4285. [PubMed] [Google Scholar]
  28. Negm H. I., Mansour M. H., Cooper E. L. Serological characterization and partial purification of an Lyt-1 homolog in tunicate hemocytes. Biol Cell. 1991;72(3):249–257. doi: 10.1111/j.1768-322x.1991.tb03021.x. [DOI] [PubMed] [Google Scholar]
  29. Randall T. D., Brewer J. W., Corley R. B. Direct evidence that J chain regulates the polymeric structure of IgM in antibody-secreting B cells. J Biol Chem. 1992 Sep 5;267(25):18002–18007. [PubMed] [Google Scholar]
  30. Raschke W. C., Mather E. L., Koshland M. E. Assembly and secretion of pentameric IgM in a fusion between a nonsecreting B cell lymphoma and an IgG-secreting plasmacytoma. Proc Natl Acad Sci U S A. 1979 Jul;76(7):3469–3473. doi: 10.1073/pnas.76.7.3469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Roch P., Cooper E. L., Eskinazi D. P. Serological evidences for a membrane structure related to human beta 2-microglobulin expressed by certain earthworm leukocytes. Eur J Immunol. 1983 Dec;13(12):1037–1042. doi: 10.1002/eji.1830131216. [DOI] [PubMed] [Google Scholar]
  32. Saiuchi M., Nunoura N., Kim J. Preparation of a monoclonal antibody and expression of its antigen associated with myogenic differentiation on spontaneous and artificial myotubes derived from avian myoblasts. Cell Struct Funct. 1993 Oct;18(5):285–296. doi: 10.1247/csf.18.285. [DOI] [PubMed] [Google Scholar]
  33. Seeger M. A., Haffley L., Kaufman T. C. Characterization of amalgam: a member of the immunoglobulin superfamily from Drosophila. Cell. 1988 Nov 18;55(4):589–600. doi: 10.1016/0092-8674(88)90217-6. [DOI] [PubMed] [Google Scholar]
  34. Shalev A., Greenberg A. H., Lögdberg L., Björck L. beta 2-Microglobulin-like molecules in low vertebrates and invertebrates. J Immunol. 1981 Sep;127(3):1186–1191. [PubMed] [Google Scholar]
  35. Sun S. C., Lindström I., Boman H. G., Faye I., Schmidt O. Hemolin: an insect-immune protein belonging to the immunoglobulin superfamily. Science. 1990 Dec 21;250(4988):1729–1732. doi: 10.1126/science.2270488. [DOI] [PubMed] [Google Scholar]
  36. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wilde C. E., 3rd, Koshland M. E. Molecular size and shape of the J chain from polymeric immunoglobulins. Biochemistry. 1973 Aug 14;12(17):3218–3224. doi: 10.1021/bi00741a012. [DOI] [PubMed] [Google Scholar]
  38. Williams A. F., Tse A. G., Gagnon J. Squid glycoproteins with structural similarities to Thy-1 and Ly-6 antigens. Immunogenetics. 1988;27(4):265–272. doi: 10.1007/BF00376121. [DOI] [PubMed] [Google Scholar]
  39. Zikan J., Novotny J., Trapane T. L., Koshland M. E., Urry D. W., Bennett J. C., Mestecky J. Secondary structure of the immunoglobulin J chain. Proc Natl Acad Sci U S A. 1985 Sep;82(17):5905–5909. doi: 10.1073/pnas.82.17.5905. [DOI] [PMC free article] [PubMed] [Google Scholar]

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