Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1991 Jul 15;88(14):6077–6081. doi: 10.1073/pnas.88.14.6077

Human chromosome 16 encodes a factor involved in induction of class II major histocompatibility antigens by interferon gamma.

M R Bono 1, C Alcaïde-Loridan 1, P Couillin 1, B Letouzé 1, M C Grisard 1, H Jouin 1, M Fellous 1
PMCID: PMC52025  PMID: 1906174

Abstract

Interferon gamma (IFN-gamma) induces expression of class II major histocompatibility complex (MHC)-encoded antigens in immunocompetent cells. To gain further insight into the mechanism of this induction, we prepared somatic cell hybrids between different human cell lines and a murine cell line, RAG, that does not express murine class II MHC antigens before or after treatment with murine IFN-gamma. Some of the resulting cell hybrids express murine class II MHC antigens when treated with murine IFN-gamma. This inducible phenotype is correlated with the presence of human chromosome 16. It has been shown previously that the induction of class I MHC antigens by human IFN-gamma in human-rodent hybrids requires the presence of species-specific factors encoded by chromosome 6, which bears the gene for the human IFN-gamma receptor, and chromosome 21, whose product(s) is necessary for the transduction of human IFN-gamma signals. In this report, we show that the induction of murine class II MHC antigens by human IFN-gamma in the human-RAG cell hybrids requires, likewise, the presence of human chromosomes 6 and 21, in addition to chromosome 16. In some of these hybrids, when all three of these human chromosomes were present, induction of cell-surface HLA-DR antigens was also observed. Our results demonstrate that human chromosome 16 encodes a non-species-specific factor involved in the induction of class II MHC antigens by IFN-gamma.

Full text

PDF
6077

Images in this article

6079Image
on p.6079

Selected References

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

  1. Aguet M., Dembić Z., Merlin G. Molecular cloning and expression of the human interferon-gamma receptor. Cell. 1988 Oct 21;55(2):273–280. doi: 10.1016/0092-8674(88)90050-5. [DOI] [PubMed] [Google Scholar]
  2. Aguet M., Merlin G. Purification of human gamma interferon receptors by sequential affinity chromatography on immobilized monoclonal antireceptor antibodies and human gamma interferon. J Exp Med. 1987 Apr 1;165(4):988–999. doi: 10.1084/jem.165.4.988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barnstable C. J., Bodmer W. F., Brown G., Galfre G., Milstein C., Williams A. F., Ziegler A. Production of monoclonal antibodies to group A erythrocytes, HLA and other human cell surface antigens-new tools for genetic analysis. Cell. 1978 May;14(1):9–20. doi: 10.1016/0092-8674(78)90296-9. [DOI] [PubMed] [Google Scholar]
  4. Basta P. V., Sherman P. A., Ting J. P. Detailed delineation of an interferon-gamma-responsive element important in human HLA-DRA gene expression in a glioblastoma multiform line. Proc Natl Acad Sci U S A. 1988 Nov;85(22):8618–8622. doi: 10.1073/pnas.85.22.8618. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Blanar M. A., Boettger E. C., Flavell R. A. Transcriptional activation of HLA-DR alpha by interferon gamma requires a trans-acting protein. Proc Natl Acad Sci U S A. 1988 Jul;85(13):4672–4676. doi: 10.1073/pnas.85.13.4672. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bono M. R., Benech P., Couillin P., Alcaide-Loridan C., Grisard M. C., Jouin H., Fischer D. G., Fellous M. Characterization of human IFN-gamma response using somatic cell hybrids of hematopoietic and nonhematopoietic origin. Somat Cell Mol Genet. 1989 Nov;15(6):513–523. doi: 10.1007/BF01534912. [DOI] [PubMed] [Google Scholar]
  7. Bono M. R., Strominger J. L. Direct evidence of homology between human DC-1 antigen and murine I-A molecules. Nature. 1982 Oct 28;299(5886):836–840. doi: 10.1038/299836a0. [DOI] [PubMed] [Google Scholar]
  8. Chen C., Okayama H. High-efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol. 1987 Aug;7(8):2745–2752. doi: 10.1128/mcb.7.8.2745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  10. Couillin P., Le Guern E., Ravise N., Grisard M. C., Oostra B. A., Boue A. Strategy for constructing somatic hybrids isolating the two derivative chromosomes in X;autosome translocations. Application to a female patient t(X;5) with Hunter syndrome. Ann Genet. 1990;33(4):196–207. [PubMed] [Google Scholar]
  11. Dedrick R. L., Jones P. P. Sequence elements required for activity of a murine major histocompatibility complex class II promoter bind common and cell-type-specific nuclear factors. Mol Cell Biol. 1990 Feb;10(2):593–604. doi: 10.1128/mcb.10.2.593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fan X. D., Goldberg M., Bloom B. R. Interferon-gamma-induced transcriptional activation is mediated by protein kinase C. Proc Natl Acad Sci U S A. 1988 Jul;85(14):5122–5125. doi: 10.1073/pnas.85.14.5122. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Fellous M., Nir U., Wallach D., Merlin G., Rubinstein M., Revel M. Interferon-dependent induction of mRNA for the major histocompatibility antigens in human fibroblasts and lymphoblastoid cells. Proc Natl Acad Sci U S A. 1982 May;79(10):3082–3086. doi: 10.1073/pnas.79.10.3082. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hemmi S., Peghini P., Metzler M., Merlin G., Dembic Z., Aguet M. Cloning of murine interferon gamma receptor cDNA: expression in human cells mediates high-affinity binding but is not sufficient to confer sensitivity to murine interferon gamma. Proc Natl Acad Sci U S A. 1989 Dec;86(24):9901–9905. doi: 10.1073/pnas.86.24.9901. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hume C. R., Lee J. S. Congenital immunodeficiencies associated with absence of HLA class II antigens on lymphocytes result from distinct mutations in trans-acting factors. Hum Immunol. 1989 Dec;26(4):288–309. doi: 10.1016/0198-8859(89)90007-4. [DOI] [PubMed] [Google Scholar]
  16. Jung V., Rashidbaigi A., Jones C., Tischfield J. A., Shows T. B., Pestka S. Human chromosomes 6 and 21 are required for sensitivity to human interferon gamma. Proc Natl Acad Sci U S A. 1987 Jun;84(12):4151–4155. doi: 10.1073/pnas.84.12.4151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kappes D., Strominger J. L. Human class II major histocompatibility complex genes and proteins. Annu Rev Biochem. 1988;57:991–1028. doi: 10.1146/annurev.bi.57.070188.005015. [DOI] [PubMed] [Google Scholar]
  18. Kappler J. W., Skidmore B., White J., Marrack P. Antigen-inducible, H-2-restricted, interleukin-2-producing T cell hybridomas. Lack of independent antigen and H-2 recognition. J Exp Med. 1981 May 1;153(5):1198–1214. doi: 10.1084/jem.153.5.1198. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kern M. J., Stuart P. M., Omer K. W., Woodward J. G. Evidence that IFN-gamma does not affect MHC class II gene expression at the post-transcriptional level in a mouse macrophage cell line. Immunogenetics. 1989;30(4):258–265. doi: 10.1007/BF02421329. [DOI] [PubMed] [Google Scholar]
  20. Kobr M., Reith W., Herrero-Sanchez C., Mach B. Two DNA-binding proteins discriminate between the promoters of different members of the major histocompatibility complex class II multigene family. Mol Cell Biol. 1990 Mar;10(3):965–971. doi: 10.1128/mcb.10.3.965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Le Coniat M., Alcaide-Loridan C., Fellous M., Berger R. Human interferon gamma receptor 1 (IFNGR1) gene maps to chromosome region 6q23-6q24. Hum Genet. 1989 Dec;84(1):92–94. doi: 10.1007/BF00210682. [DOI] [PubMed] [Google Scholar]
  22. Oi V. T., Jones P. P., Goding J. W., Herzenberg L. A., Herzenberg L. A. Properties of monoclonal antibodies to mouse Ig allotypes, H-2, and Ia antigens. Curr Top Microbiol Immunol. 1978;81:115–120. doi: 10.1007/978-3-642-67448-8_18. [DOI] [PubMed] [Google Scholar]
  23. Ozato K., Mayer N., Sachs D. H. Hybridoma cell lines secreting monoclonal antibodies to mouse H-2 and Ia antigens. J Immunol. 1980 Feb;124(2):533–540. [PubMed] [Google Scholar]
  24. Piatier-Tonneau D., Turmel P., Auffray C., Charron D. Construction of chain- and locus-specific HLA class II DNA probes. Study of HLA-class II transcripts in leukemias. J Immunol. 1986 Sep 15;137(6):2050–2056. [PubMed] [Google Scholar]
  25. Radka S. F., Charron D. J., Brodsky F. M. Class II molecules of the major histocompatibility complex considered as differentiation markers. Hum Immunol. 1986 Aug;16(4):390–400. doi: 10.1016/0198-8859(86)90065-0. [DOI] [PubMed] [Google Scholar]
  26. Rosa F. M., Fellous M. Regulation of HLA-DR gene by IFN-gamma. Transcriptional and post-transcriptional control. J Immunol. 1988 Mar 1;140(5):1660–1664. [PubMed] [Google Scholar]
  27. Rubinstein M., Novick D., Fischer D. G. The human interferon-gamma receptor system. Immunol Rev. 1987 Jun;97:29–50. doi: 10.1111/j.1600-065x.1987.tb00515.x. [DOI] [PubMed] [Google Scholar]
  28. Schwartz R. H. T-lymphocyte recognition of antigen in association with gene products of the major histocompatibility complex. Annu Rev Immunol. 1985;3:237–261. doi: 10.1146/annurev.iy.03.040185.001321. [DOI] [PubMed] [Google Scholar]
  29. Seabright M. A rapid banding technique for human chromosomes. Lancet. 1971 Oct 30;2(7731):971–972. doi: 10.1016/s0140-6736(71)90287-x. [DOI] [PubMed] [Google Scholar]
  30. Slate D. L., Shulman L., Lawrence J. B., Revel M., Ruddle F. H. Presence of human chromosome 21 alone is sufficient for hybrid cell sensitivity to human interferon. J Virol. 1978 Jan;25(1):319–325. doi: 10.1128/jvi.25.1.319-325.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sood A. K., Pereira D., Weissman S. M. Isolation and partial nucleotide sequence of a cDNA clone for human histocompatibility antigen HLA-B by use of an oligodeoxynucleotide primer. Proc Natl Acad Sci U S A. 1981 Jan;78(1):616–620. doi: 10.1073/pnas.78.1.616. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Southern P. J., Berg P. Transformation of mammalian cells to antibiotic resistance with a bacterial gene under control of the SV40 early region promoter. J Mol Appl Genet. 1982;1(4):327–341. [PubMed] [Google Scholar]
  33. Steeg P. S., Johnson H. M., Oppenheim J. J. Regulation of murine macrophage Ia antigen expression by an immune interferon-like lymphokine: inhibitory effect of endotoxin. J Immunol. 1982 Dec;129(6):2402–2406. [PubMed] [Google Scholar]
  34. Steinmetz M., Minard K., Horvath S., McNicholas J., Srelinger J., Wake C., Long E., Mach B., Hood L. A molecular map of the immune response region from the major histocompatibility complex of the mouse. Nature. 1982 Nov 4;300(5887):35–42. doi: 10.1038/300035a0. [DOI] [PubMed] [Google Scholar]
  35. Woodward J. G., Omer K. W., Stuart P. M. MHC class II transcription in different mouse cell types. Differential requirement for protein synthesis between B cells and macrophages. J Immunol. 1989 Jun 1;142(11):4062–4069. [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES