Skip to main content
PMC home page
Immunology logoLink to Immunology
. 1990 Mar;69(3):361–366.

Bovine IgG1, but not IgG2, binds to human B cells and inhibits antibody secretion.

G S Nash 1, R P MacDermott 1, S Schloemann 1, M J Bertovich 1, J O'Neal 1, L Porter 1, A Kulczycki 1
PMCID: PMC1385952  PMID: 2312161

Abstract

We previously observed that milk-derived bovine IgG, but not serum-derived bovine IgG, strongly inhibits antibody secretion by pokeweed mitogen (PWM)-stimulated human peripheral blood mononuclear cells (PBMC). Bovine milk contains a greater percentage of IgG1 (90%) than does bovine serum (53%). To determine whether bovine IgG subclasses have different functional capabilities, we have examined the effects of bovine IgG1 and IgG2 subclasses upon not only antibody secretion but also mitogenesis by human PBMC. Both bovine IgG subclasses markedly inhibited PWM-stimulated mitogenesis. However, only bovine IgG1, and not IgG2, inhibited antibody secretion during a 14-day in vitro culture period. Also, antibody secretion was inhibited following a 24-hr preincubation of human PBMC with bovine IgG1, but not with IgG2. To determine whether these differences corresponded to specificities of human Fc gamma receptors on subsets of mononuclear cells, fluorescence-activated cell sorter (FACS) analyses were performed. Both bovine IgG subclasses bound to human monocytes. However, only bovine IgG1 bound to human B cells, and bovine IgG1 bound more avidly to human B cells than did human IgG. One model to explain these findings is that inhibition of mitogenesis may be due to the binding of both bovine IgG1 and IgG2 subclasses to monocytes; whereas subclass-specific inhibition of antibody secretion may result from the selective binding of bovine IgG1, but not bovine IgG2, to B cells. The observation that bovine IgG1 has a greater avidity for human B lymphocyte Fc receptors than human IgG may have important implications for future studies of Fc gamma receptors on human leucocytes.

Full text

PDF
361

Selected References

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

  1. Allen J. M., Seed B. Isolation and expression of functional high-affinity Fc receptor complementary DNAs. Science. 1989 Jan 20;243(4889):378–381. doi: 10.1126/science.2911749. [DOI] [PubMed] [Google Scholar]
  2. Anderson C. L. Isolation of the receptor for IgG from a human monocyte cell line (U937) and from human peripheral blood monocytes. J Exp Med. 1982 Dec 1;156(6):1794–1806. doi: 10.1084/jem.156.6.1794. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bock S. A., Remigio L. K., Gordon B. Immunochemical localization of proteins in the intestinal mucosa of children with diarrhea. J Allergy Clin Immunol. 1983 Sep;72(3):262–268. doi: 10.1016/0091-6749(83)90030-1. [DOI] [PubMed] [Google Scholar]
  4. Butler J. E., Maxwell C. F., Pierce C. S., Hylton M. B., Asofsky R., Kiddy C. A. Studies on the relative synthesis and distribution of IgA and IgG1 in various tissues and body fluids of the cow. J Immunol. 1972 Jul;109(1):38–46. [PubMed] [Google Scholar]
  5. Cohen L., Sharp S., Kulczycki A., Jr Human monocytes, B lymphocytes, and non-B lymphocytes each have structurally unique Fc gamma receptors. J Immunol. 1983 Jul;131(1):378–383. [PubMed] [Google Scholar]
  6. Cunningham-Rundles C., Carr R. I., Good R. A. Dietary protein antigenemia in humoral immunodeficiency. Correlation with splenomegaly. Am J Med. 1984 Feb;76(2):181–185. doi: 10.1016/0002-9343(84)90771-x. [DOI] [PubMed] [Google Scholar]
  7. Jones D. H., Looney R. J., Anderson C. L. Two distinct classes of IgG Fc receptors on a human monocyte line (U937) defined by differences in binding of murine IgG subclasses at low ionic strength. J Immunol. 1985 Nov;135(5):3348–3353. [PubMed] [Google Scholar]
  8. Julius M. H., Janusz M., Lisowski J. A colostral protein that induces the growth and differentiation of resting B lymphocytes. J Immunol. 1988 Mar 1;140(5):1366–1371. [PubMed] [Google Scholar]
  9. Kulczycki A., Jr Bovine IgG can aggregate at conditions simulating pasteurization and binds to some human Fc gamma receptors. Mol Immunol. 1987 Mar;24(3):259–266. doi: 10.1016/0161-5890(87)90144-1. [DOI] [PubMed] [Google Scholar]
  10. Kulczycki A., Jr, Nash G. S., Bertovich M. J., Burack H. D., MacDermott R. P. Bovine milk IgG, but not serum IgG, inhibits pokeweed mitogen-induced antibody secretion by human peripheral blood mononuclear cells. J Clin Immunol. 1987 Jan;7(1):37–45. doi: 10.1007/BF00915423. [DOI] [PubMed] [Google Scholar]
  11. Kulczycki A., Jr, Solanki L., Cohen L. Isolation and partial characterization of Fc gamma-binding proteins of human leukocytes. J Clin Invest. 1981 Dec;68(6):1558–1565. doi: 10.1172/JCI110410. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kurlander R. J., Batker J. The binding of human immunoglobulin G1 monomer and small, covalently cross-linked polymers of immunoglobulin G1 to human peripheral blood monocytes and polymorphonuclear leukocytes. J Clin Invest. 1982 Jan;69(1):1–8. doi: 10.1172/JCI110419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Lowenstein H., Krasilnikoff P. A., Bjerrum O. J., Gudmand-Hoyer E. Occurrence of specific precipitins against bovine whey proteins in serum from children with gastrointestinal disorders. Int Arch Allergy Appl Immunol. 1977;55(1-6):514–525. doi: 10.1159/000231965. [DOI] [PubMed] [Google Scholar]
  14. Lubeck M. D., Steplewski Z., Baglia F., Klein M. H., Dorrington K. J., Koprowski H. The interaction of murine IgG subclass proteins with human monocyte Fc receptors. J Immunol. 1985 Aug;135(2):1299–1304. [PubMed] [Google Scholar]
  15. Mannhalter J. W., Wolf H. M., Ahmad R., Eibl M. M. The effect of Fc receptor modulation on human monocyte function. Mol Immunol. 1986 Nov;23(11):1225–1229. doi: 10.1016/0161-5890(86)90155-0. [DOI] [PubMed] [Google Scholar]
  16. May C. D., Remigio L., Feldman J., Bock S. A., Carr R. I. A study of serum antibodies to isolated milk proteins and ovalbumin in infants and children. Clin Allergy. 1977 Nov;7(6):583–595. doi: 10.1111/j.1365-2222.1977.tb01489.x. [DOI] [PubMed] [Google Scholar]
  17. Morgan E. L., Hobbs M. V., Thoman M. T., Weigle W. O. Lymphocyte activation by the Fc region of immunoglobulins. Immunol Invest. 1986 Nov;15(7):625–687. doi: 10.3109/08820138609048907. [DOI] [PubMed] [Google Scholar]
  18. Nash G. S., Seiden M. V., Beale M. G., MacDermott R. P. A rapid miniaturized solid-phase radioimmunoassay technique for secreted immunoglobulins, employing microtiter plates, antibody bound to polyacrylamide beads, and filter strip harvesting. J Immunol Methods. 1982 Mar 26;49(3):261–269. doi: 10.1016/0022-1759(82)90126-0. [DOI] [PubMed] [Google Scholar]
  19. Peltz G. A., Grundy H. O., Lebo R. V., Yssel H., Barsh G. S., Moore K. W. Human Fc gamma RIII: cloning, expression, and identification of the chromosomal locus of two Fc receptors for IgG. Proc Natl Acad Sci U S A. 1989 Feb;86(3):1013–1017. doi: 10.1073/pnas.86.3.1013. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Perussia B., Trinchieri G. Antibody 3G8, specific for the human neutrophil Fc receptor, reacts with natural killer cells. J Immunol. 1984 Mar;132(3):1410–1415. [PubMed] [Google Scholar]
  21. Perussia B., Trinchieri G., Jackson A., Warner N. L., Faust J., Rumpold H., Kraft D., Lanier L. L. The Fc receptor for IgG on human natural killer cells: phenotypic, functional, and comparative studies with monoclonal antibodies. J Immunol. 1984 Jul;133(1):180–189. [PubMed] [Google Scholar]
  22. Simmons D., Seed B. The Fc gamma receptor of natural killer cells is a phospholipid-linked membrane protein. Nature. 1988 Jun 9;333(6173):568–570. doi: 10.1038/333568a0. [DOI] [PubMed] [Google Scholar]
  23. Stengelin S., Stamenkovic I., Seed B. Isolation of cDNAs for two distinct human Fc receptors by ligand affinity cloning. EMBO J. 1988 Apr;7(4):1053–1059. doi: 10.1002/j.1460-2075.1988.tb02913.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Tomasi T. B., Jr, Katz L. Human antibodies against bovine immunoglobulin M in IgA deficient sera. Clin Exp Immunol. 1971 Jul;9(1):3–10. [PMC free article] [PubMed] [Google Scholar]
  25. Uher F., Dickler H. B. Independent ligand occupancy and cross-linking of surface Ig and Fc gamma receptors downregulates B-lymphocyte function. Evaluation in various B-lymphocyte populations. Mol Immunol. 1986 Nov;23(11):1177–1181. doi: 10.1016/0161-5890(86)90149-5. [DOI] [PubMed] [Google Scholar]

Articles from Immunology are provided here courtesy of British Society for Immunology

RESOURCES