Skip to main content
SpringerLink
Log in

Developmental and tissue-specific expression of the Q5 k gene

  • Original Articles
  • Published:
Immunogenetics Aims and scope Submit manuscript

Abstract

Expression of the Q5 k gene was examined by northern blot analysis and polymerase chain reaction (PCR) in the AKR mouse and various cell lines, each of the H-2 k haplotype. Our results show that Q5 k mRNA is present during the whole postimplantational development of the AKR embryo/fetus (gestation day 6 to 15). In the juvenile mouse (week 2 to 4) transcription of the Q5 k gene persisted in all organs examined. In contrast, in the adult animal expression of the Q5 k gene was limited to the thymus and uterus of the pregnant mouse. Upon malignant transformation, the amount of Q5 k-specific mRNA increased dramatically in thymus and could also be observed in the spleen of thymoma bearing animals. Expression of the Q5 k gene was also detectable in several transformed mouse cell lines. Mitogen stimulation or treatment with cytokines induced Q5 k expression in primary spleen cell cultures. A possible explanation for the tissue-restricted expression in the adult AKR mouse is discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Allen, H., Fraser, J., Flyer, D., Calvin, S.,and Flavell, R.: β2-microglobulin is not required for cell surface expression of the murine class I histocompatibility antigen H-2Db or of a truncated H-2Db. Proc Natl Acad Sci USA 83: 7447–7451, 1986

    Google Scholar 

  • Baeuerle, P. A. and Baltimore, D.: Activation of a DNA-binding activity in an apparently cytoplasmic precursor of the NF-kB transcription factor. Cell 53: 211–217, 1988

    Google Scholar 

  • Baeuerle, P. A. and Baltimore, D.: A subunit of active NF-kB is required for inhibition of NF-kB by IkB. Genes Dev 3: 1689–1698, 1989

    Google Scholar 

  • Baldwin, A. S. and Sharp, P. A.: Binding of a nuclear factor to a regulatory sequence in the promoter of the mouse H-2Kb class I major histocompatibility gene. Mol Cell Biol 7: 305–313, 1987

    Google Scholar 

  • Baldwin, A. S. and Sharp, P. A.: Two transcription factors, NF-kB and H2TF1, interact with a single regulatory sequence in the class I major histocompatibility complex promoter. Proc Natl Acad Sci USA 85: 723–727, 1988

    Google Scholar 

  • Burlingham, W. J., Ceman, S. S., and DeMars, R.: Secretion and cell surface expression of IgG1 are impaired in human B lymphoblasts that lack HLA-A, −B, and −C antigens. Proc Natl Acad Sci USA 86: 8005–8009, 1989

    Google Scholar 

  • Cate, R. L., Mattalino, R. J., Hession, C., Tizard, R., Farber, N. M., Cheung, A., Ninta, E. G., Frey, A. Z., Gash, D. J., Chow, E. P., Fisher, R. A., Bertonis, J. M., Torres, G., Wallner, B. P., Ramachandran, K. L., Ragin, R. C., Manganaro, T. F., MacLaughlin, D., and Donahoe, P. K.: Isolation of the bovine and human genes for Mullerian inhibiting substance and expression of the human gene in animal cells. Cell 45: 685–698, 1986

    Google Scholar 

  • Chirgwin, J. M., Przybyla, A. E., MacDonald, R. J., and Rutter, W.: Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18: 5294–5299, 1979

    CAS  PubMed  Google Scholar 

  • Chomczynski, P. and Sacchi, N.: Single step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156–159, 1987

    Article  CAS  PubMed  Google Scholar 

  • Church, G. M. and Gilbert, W.: Genomic sequencing. Proc Natl Acad Sci USA 81: 1991–1995, 1984

    CAS  PubMed  Google Scholar 

  • Collins, M. L., and Hunsaker, W. R.: Improved hybridization assays employing tailed oligonucleotide probes: a direct comparison with 5'end labeled oligonucleotide probes and nick-translated plasmid probes. Anal Biochem 151: 211–224, 1985

    Google Scholar 

  • Devlin, J. J., Lew, A. M., Flavell, R. A., and Coligan, J. E.: Secretion of a soluble class I molecule encoded by the Q10 gene of the C57BL/10 mouse. EMBO J 4: 369–374, 1985a

    Google Scholar 

  • Devlin, J. J., Weiss, E. H., Paulson, M., and Flavell, R. A.: Duplicated gene pairs and alleles of class I genes in the Qa 2 region of the murine major histocompatibility complex: a comparison. EMBO J 4: 3203–3207, 1985b

    Google Scholar 

  • Dignam, J. D., Lebovitz, R. M., and Roeder, R. G.: Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res 11: 1475–1489, 1983

    Google Scholar 

  • Doyle, A., Martin, W. J., Fuma, K., Gazadar, A., Carney, D., Martin, S. E., Linnoila, I., Cuttia, F., Mulshine, J., Bunn, P., and Minna, J.: Markedly decreased expression of class I histocompatibility antigens, protein, and mRNA in human small cell lung cancer. J Exp Med 161: 1135–1151, 1985

    Google Scholar 

  • Fahrner, K., Hogan, B. L. M., and Flavell, R. A.: Transcription of H-2 and Qa genes in embryonic and adult mice. EMBO J 6: 1265–1271, 1987

    Google Scholar 

  • Feinberg, A. P. and Vogelstein, B.: Addendum: A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 137: 266–267, 1984

    CAS  PubMed  Google Scholar 

  • Festenstein, H. and Schmidt, W.: Variation in MHC antigenic profiles of tumor cells and its biological effects. Immunol Rev 60: 85–127, 1981

    Google Scholar 

  • Flaherty, L., Elliot, E., Tine, J. A., Walsh, A. C., and Waters, J. B.: Immunogenetics of the Q and TL regions of the mouse. Crit Rev Immunol 10: 131–175, 1990

    Google Scholar 

  • Ghosh, S., Gifford, A. M., Riviere, L. R., Tempst, P., Nolan, G. P., and Baltimore, D.: Cloning of the DNA binding subunit of NF-kB: Homology to rel and dorsal. Cell 62: 1019–1029, 1990

    Google Scholar 

  • Haas, W., Kaufmann, S., and Martinex-A., C.: The development and function of γδ T cells. Immunol Today 11: 340–343, 1990

    Google Scholar 

  • Handy, D. E., Burke, P. A., Ozato, K., and Coligan, J. E.: Site-specific mutagenesis of the class I regulatory element of the Q10 gene allows expression in non-liver tissues. J Immunol 142: 1015–1021, 1989

    Google Scholar 

  • Hansen, T., Stagsted, J., Pedersen, L., Roth, R. A., Goldstein, A., and Olsson, L.: Inhibition of insulin receptor phosphorylation by peptides derived from major histocompatibility complex class I antigens. Proc Natl Acad Sci USA 86: 3123–3126, 1989

    Google Scholar 

  • Henseling, U., Schmidt, W., Schöler, H. R., Gruss, P., and Hatzopouslos, A. K.: A transcription factor interacting with the class I gene enhancer is inactive in tumorigenic cell lines which suppress major histocompatibility complex class I genes. Mol Cell Biol 10: 4100–4109, 1990

    Google Scholar 

  • Israel, A., Kimura, A., Kieran, M., Yano, O., Kanellopoulos, J., Le Bail, O., and Kourilsky, P.: A common positive transacting factor binds to enhancer sequences in the promoters of mouse H-2 and β2-microglobulin genes. Proc Natl Acad Sci USA 84: 2653–2657, 1987

    Google Scholar 

  • Israel, A., Le Bail, O., Piette, J., Kieran, M., Logeeat, F., Wallach, D., Fellous, M., and Kourilsky, P.: TNF stimulates expression of mouse MHC class I genes by inducing an NF-kB-like enhancer binding activity which displaces constitutive factors. EMBO J 8: 3793–3800, 1989

    Google Scholar 

  • Ito, K., Van Kaer, L., Bonneville, M., Hsu, S., Murphy, D. B., and Tonegawa, S.: Recognition of the product of a novel MHC-TL region gene (27 b) by a mouse γδ T cell receptor. Cell 62: 549–561, 1990

    Google Scholar 

  • Janeway, C. A., Jr., Jones, B., and Hayday, A.: Specificity and function of T cells bearing γδ receptors. Immunol Today 9: 73–79, 1988

    Google Scholar 

  • Jones, E. A. and Bodmer, W. F.: Lack of expression of HLA antigens on choriocarcinoma cell lines. Tissue Antigens 16: 195–201, 1980

    Google Scholar 

  • Kieran, M., Blank, V., Logeat, F., Vandekerckhove, J., Lottspeich, F., Le Bail, O., Urban, M. B., Kourilsky, P., Naeuerle, P., and Israel, A.: The DNA binding subunit of NF-kB is identical to factor KBF1 and homologous to the rel oncogene product. Cell 62: 1007–1018, 1990

    Google Scholar 

  • Kimura, A., Israel, A., Le Bail, B., and Kourilsky, P.: Detailed analysis of the mouse H-2Kb promoter: enhancer-like sequences and their role in the regulation of class I expression. Cell 44: 261–271, 1986

    Google Scholar 

  • Kittur, D., Shimizu, Y., DeMars, R., and Edidin, M.: Insulin binding to human B lymphoblasts is a function of HLA haplotype. Proc Natl Acad Sci USA 84: 1351–1355, 1987

    Google Scholar 

  • Klein, J.: Natural History of the Major Histocompatibility Complex. Wiley, New York, 1986

    Google Scholar 

  • Korber, B., Hood, L., and Stroynowski, I.: Regulation of murine class I genes by interferons is controlled by regions located both 5' and 3' to the transcription initiation site. Proc Natl Acad Sci USA 84: 3380–3384, 1987

    CAS  PubMed  Google Scholar 

  • Kress, M., Cosman, D., Khoury, G., and Jay, G.: Secretion of a transplantation-related antigen. Cell 34: 189–196, 1983

    Google Scholar 

  • Labeta, M. O., Fernandez, N., Reyes, A., Ferrara, P., Marelli, O., Le Roy, E., Houlihang, J., and Festenstein, H.: Biochemical analysis of a novel H-2 class I-like glycoprotein expressed in five AKR-(gross virus) derived spontaneous T cell leukemias. J Immunol 143: 1245–1253, 1989

    Google Scholar 

  • Lampson, L. A., Fisher, C. A., and Whealan, J. P.: Striking paucity of HLA-A, −B, −C and β2-microglobulin on human neuroblastoma cell lines. J Immunol 130: 2471–2478, 1983

    Google Scholar 

  • Mellor, A. L., Weiss, E. H., Kress, M., Jay, G., and Flavell, R. A.: A nonpolymorphic class I gene in the murine major histocompatibility complex. Cell 36: 139–144, 1984

    Google Scholar 

  • Messer, G., Weiss, E. H., and Baeuerle, P. A.: Tumor necrosis factor-β (TNF-β) induces binding of the NF-kB transcription factor to a high-affinity kB element in the TNF-β promoter. Cytokine 2: 389–397, 1990

    Google Scholar 

  • Michaelson, J., Flaherty, L., Vitetta, E., and Ponlik, M. D.: Molecular similarities between the Qa-2 alloantigen and other gene products of the 17th chromosome of the mouse. J Exp Med 145: 1066–1070, 1977

    Google Scholar 

  • Morello, D., Daniel, F., Baldacci, P., Cayre, Y., Gachelin, G., and Kourilsky, P.: Absence of significant H-2 and β2-microglobulin mRNA expression by mouse embryonal carcinoma cells. Nature 296: 260–262, 1982

    Google Scholar 

  • Morello, D., Duprey, P., Israel, A., and Babinet, C.: Asynchronous regulation of mouse H-2D and beta-2 microglobulin RNA transcripts. Immunogenetics 22: 441–452, 1985

    Google Scholar 

  • Ozato, K., Wan, Y., and Orrison, B.: Mouse major histocompatibility class I gene expression begins at midsomite stage and is inducible in earlier stage embryos by interferon. Proc Natl Acad Sci USA 82: 2427–2431, 1985

    Google Scholar 

  • Ruano, G., Fenton, W., and Kidd, K. K.: Biphasic amplification of very dilute DNA samples via ‘booster’ PCR. Nucleic Acids Res 17: 5407, 1989

    Google Scholar 

  • Saiki, R. K., Gelfahd, D. H., Staffel, S., Scharf, S. J., Higuchi, R. G., Horn, T., Mullis, K. B., and Erlich, H. A.: Primer directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239: 487–491, 1988

    CAS  PubMed  Google Scholar 

  • Sawicki, J. A., Magnuson, T., and Epstein, C. J.: Evidence for expression of the paternal genome in the two-cell mouse embryo. Nature 294: 450–451, 1981

    Google Scholar 

  • Schmidt, W. and Festenstein, H.: Resistance to cell-mediated cytotoxicity is correlated with reduction of H-2K gene products in AKR leukemia. Immunogenetics 16: 257–264, 1982

    Google Scholar 

  • Schmidt, W., Henseling, U., Bevec, D., Alonzo, A. D. R., and Festenstein, H.: Control of synthesis and expression of H-2 heavy chain and beta-2 microglubulin in AKR leukemias. Immunogenetics 22: 483–494, 1985

    Google Scholar 

  • Schmidt, W., Noll, G., Bevec, D., and Henseling, U.: Aberrant MHC antigens in a sarcoma virus-induced mouse tumour. Immunogenetics 13: 123–132, 1986

    Google Scholar 

  • Schnabl, E., Stockinger, H., Majdic, O., Gangitsch, H., Lindley, I. J., Maurer, D., Hajek-Rosenmayer, A., and Knapp, W.: Activated human T lymphocytes express MHC class I heavy chains not associated with β2-microglobulin. J Exp Med 171: 1431–1442, 1990

    Google Scholar 

  • Searle, R. F., Sellens, M. H., Elson, J., Jenkinson, E. J., and Billington, D. W.: Detection of alloantigens during preimplantation development and early trophoblast differentiation in the mouse by immunoperoxidase labeling. J Exp Med 143: 348–359, 1976

    Google Scholar 

  • Sen, R. and Baltimore, D.: Multiple nuclear factors interact with the immunoglobulin enhancer. Cell 46: 705–716, 1986

    Google Scholar 

  • Sharon, M., Gnarra, J. R., Baniyash, M., and Leonard, W. J.: Possible association between IL-2 receptors and class I HLA molecules on T cells. J Immunol 141: 3512–3515, 1988

    Google Scholar 

  • Solano, A. R., Cremaschi, G., Sanchez, M. L., Borda, E., Sterin-Borda, L., and Podesta, E. J.: Molecular and biological interaction between major histocompatibility complex class I antigens and luteinizing hormone receptors of β-adrenergic receptors triggers cellular response in mice. Proc Natl Acad Sci USA 85: 5087–5091, 1988

    Google Scholar 

  • Soloski, M. J., Uhr, J. W., Flaherty, L., and Vitteta, E. S.: Qa-2, H-2K, and H-2D alloantigens evolved from a common ancestral gene. J Exp Med 153: 1080–1093, 1981

    Google Scholar 

  • Stagsted, J., Reaven, G. M., Hansen, T., Goldstein. A., and Olsson, L.: Regulation of insulin receptor functions by a peptide derived from a major histocompatibility complex class I antigen. Cell 62: 297–307, 1990

    Google Scholar 

  • Stanton, T. H. and Hood, L.: Biochemical identification of the Qa-1 alloantigen. Immunogenetics 11: 309–314, 1980

    Google Scholar 

  • Steinmetz, M., Moore, K. W., Frelinger, J. G., Sher, B. T., Shen, F. W., Boyse, E. A., and Hood, L.: A pseudogene homologous to mouse transplantation antigens: transplantation antigens are encoded by eight exons that correlate with protein domains. Cell 25: 683–692, 1981

    Google Scholar 

  • Stiernberg, J., Low, M. G., Flaherty, L., and Kincade, P. W.: Removal of lymphocyte surface molecules with phosphatidylinositol-specific phospholipase C: effects on mitogen responses and evidence that ThB and certain Qa antigens are membrane anchored via phosphatidylinositol. J Immunol 138: 3877–3884, 1987

    Google Scholar 

  • Stroynowski, I., Soloski, M., Low, M. G., and Hood, L.: A single gene encodes soluble and membrane-bound forms of the major histocompatibility Qa-2 antigen: anchoring of the product by a phospholipid tail. Cell 50: 759–768, 1987

    Google Scholar 

  • Tine, J. A., Walsh, A., Rathbun, D., Leonard, L., Wakeland, E. K., Dilwith, R., and Flaherty, L.: Genetic polymorphism of Q region genes from wild-derived mice: implications for Q region evolution. Immunogenetics 31: 315–325, 1990

    Google Scholar 

  • Waneck, G. L., Sherman, D. H., Kincade, P. W., Low, M. G., and Flavell, R. A.: Molecular mapping of signals in the Qa-2 antigen required for attachment of the phosphatidylinositol membrane anchor. Proc Natl Acad Sci USA 85: 577–581, 1988

    Google Scholar 

  • Warner, C. M., Gollnick, S. O., Flaherty, L., and Goldbard, S. B.: Analysis of Qa-2 antigen expression by preimplantation mouse embryos: Possible relationship to the preimplantation-embryo-development (Ped) gene product. Biol Reprod 36: 611–616, 1987

    Google Scholar 

  • Watts, S., Davis, A. C., Gant, B., Wheeler, C., Hill, L., and Goodenow, R. S.: Organization and structure of the Qa genes of the major histocompatibility complex of the C3H mouse: implications for Qa function and class I evolution. EMBO J 8: 1749–1759, 1989

    Google Scholar 

  • Webb, C. G., Gall, E., and Edelman, G. M.: Synthesis and distribution of H-2 antigens in preimplantation mouse embryos. J Exp Med 146: 923–932, 1977

    Google Scholar 

  • Weiss, E. H.: Molecular biology of the mouse Q region. Immunol Res 6: 179–191, 1987

    Google Scholar 

  • Weiss, E. H., Golden, L., Fahrner, K., Mellor, A. C., Devlin, J. J., Bullman, H., Tiddens, H., Bud, H., and Flavell, R. A.: Organization and evolution of the class I gene family in the major histocompatibility complex of the C57BL/10 mouse. Nature 310: 650–655, 1984

    Google Scholar 

  • Weiss, E. H., Bevec, D., Messer, G., Schwemmle, S., Grosshaus, C., Steinmetz, M., and Schmidt, W.: Organization of the AKR Qa region: structure of a divergent class I sequence, Q5k. J Immunogenet 16: 283–290, 1989

    Google Scholar 

  • Yano, O., Kanellopoulos, J., Kieran, M., Le Bail, O., Israel, A., and Kourilsky, P.: Purification of KBF1, a common factor binding to both H-2 and β2-microglobulin enhancers. EMBO J 6: 3317–3324, 1987

    Google Scholar 

  • Zabel, U., Schreck, R., and Baeuerle, P. A.: DNA-binding of purified transcription factor NF-kB: Affinity, specificity, Zn2+ dependence and differential half site recognition. J Biol Chem, in press, 1991

  • Zachow, K. R. and Orr, H. T.: Regulation of HLA class I transcription in T cells. J Immunol 143: 3385–3389, 1989

    Google Scholar 

  • Zijlstra, M., Bix, M., Simister, N. E., Loring, J. M., Raulet, D. H., and Jaenisch, R.: β2-microglobulin deficient mice lack CD4−8+ cytolytic T cells. Nature 344: 742–746, 1990

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut für Immunologie, W-8000, München, Federal Republic of Germany

    Sabine Schwemmle, Dorian Bevec & Elisabeth H. Weiss

  2. Lehrstuhl für Molekulare Tierzucht, W-8000, München, Federal Republic of Germany

    Gottfried Brem

  3. Genzentrum, Laboratorium für Molekulare Biologie, W-8033, Martinsried, Federal Republic of Germany

    Manuela B. Urban & Patrick A. Baeuerle

Authors
  1. Sabine Schwemmle
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dorian Bevec
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gottfried Brem
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Manuela B. Urban
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Patrick A. Baeuerle
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Elisabeth H. Weiss
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schwemmle, S., Bevec, D., Brem, G. et al. Developmental and tissue-specific expression of the Q5 k gene. Immunogenetics 34, 28–38 (1991). https://doi.org/10.1007/BF00212309

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00212309

Keywords

Search

Navigation