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. 1993 Jun 1;177(6):1651–1662. doi: 10.1084/jem.177.6.1651

KBF1 (p50 NF-kappa B homodimer) acts as a repressor of H-2Kb gene expression in metastatic tumor cells

PMCID: PMC2191052  PMID: 8496683

Abstract

Downregulation of major histocompatibility complex class I expression is causally related to high malignancy and low immunogenicity of certain murine tumors. In this study, we have analyzed the roles of the nuclear factors KBF1/p50 and p65 in regulation of class I expression in high and low metastatic tumor cells. Low class I-expressing cells show at higher levels of KBF1/p50 and NF-kappa B (p50/p65) binding activity than high class I-expressing cells. However, an excess of KBF1 over NF- kappa B is observed in low expressing cells, while an excess of NF- kappa B over KBF1 is observed in high expressing cells. Stable transfection of a p65 expression vector into low class I-expressing cells activated H-2 transcription and cell surface expression, while stable transfection of p50 expression vector into high expressing cells suppressed H-2Kb transcription and cell surface expression. Our studies suggest that KBF1 has the potential of downregulating class I gene expression, whereas dimers containing the p65 subunit are activators of class I gene expression.

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Selected References

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  1. Baeuerle P. A., Baltimore D. A 65-kappaD subunit of active NF-kappaB is required for inhibition of NF-kappaB by I kappaB. Genes Dev. 1989 Nov;3(11):1689–1698. doi: 10.1101/gad.3.11.1689. [DOI] [PubMed] [Google Scholar]
  2. Baeuerle P. A., Baltimore D. I kappa B: a specific inhibitor of the NF-kappa B transcription factor. Science. 1988 Oct 28;242(4878):540–546. doi: 10.1126/science.3140380. [DOI] [PubMed] [Google Scholar]
  3. Baeuerle P. A. The inducible transcription activator NF-kappa B: regulation by distinct protein subunits. Biochim Biophys Acta. 1991 Apr 16;1072(1):63–80. doi: 10.1016/0304-419x(91)90007-8. [DOI] [PubMed] [Google Scholar]
  4. Baldwin A. S., Jr, 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. 1987 Jan;7(1):305–313. doi: 10.1128/mcb.7.1.305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Baldwin A. S., Jr, Sharp P. A. Two transcription factors, NF-kappa B and H2TF1, interact with a single regulatory sequence in the class I major histocompatibility complex promoter. Proc Natl Acad Sci U S A. 1988 Feb;85(3):723–727. doi: 10.1073/pnas.85.3.723. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bernards R., Schrier P. I., Houweling A., Bos J. L., van der Eb A. J., Zijlstra M., Melief C. J. Tumorigenicity of cells transformed by adenovirus type 12 by evasion of T-cell immunity. 1983 Oct 27-Nov 2Nature. 305(5937):776–779. doi: 10.1038/305776a0. [DOI] [PubMed] [Google Scholar]
  7. Blanchet O., Bourge J. F., Zinszner H., Israel A., Kourilsky P., Dausset J., Degos L., Paul P. Altered binding of regulatory factors to HLA class I enhancer sequence in human tumor cell lines lacking class I antigen expression. Proc Natl Acad Sci U S A. 1992 Apr 15;89(8):3488–3492. doi: 10.1073/pnas.89.8.3488. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Blanchet O., Bourge J. F., Zinszner H., Tatari Z., Degos L., Paul P. DNA binding of regulatory factors interacting with MHC-class-I gene enhancer correlates with MHC-class-I transcriptional level in class-I-defective cell lines. Int J Cancer Suppl. 1991;6:138–145. doi: 10.1002/ijc.2910470725. [DOI] [PubMed] [Google Scholar]
  9. Blank V., Kourilsky P., Israël A. NF-kappa B and related proteins: Rel/dorsal homologies meet ankyrin-like repeats. Trends Biochem Sci. 1992 Apr;17(4):135–140. doi: 10.1016/0968-0004(92)90321-y. [DOI] [PubMed] [Google Scholar]
  10. Braciale T. J., Braciale V. L. Antigen presentation: structural themes and functional variations. Immunol Today. 1991 Apr;12(4):124–129. doi: 10.1016/0167-5699(91)90096-C. [DOI] [PubMed] [Google Scholar]
  11. Burke P. A., Hirschfeld S., Shirayoshi Y., Kasik J. W., Hamada K., Appella E., Ozato K. Developmental and tissue-specific expression of nuclear proteins that bind the regulatory element of the major histocompatibility complex class I gene. J Exp Med. 1989 Apr 1;169(4):1309–1321. doi: 10.1084/jem.169.4.1309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Collart M. A., Baeuerle P., Vassalli P. Regulation of tumor necrosis factor alpha transcription in macrophages: involvement of four kappa B-like motifs and of constitutive and inducible forms of NF-kappa B. Mol Cell Biol. 1990 Apr;10(4):1498–1506. doi: 10.1128/mcb.10.4.1498. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Cordon-Cardo C., Fuks Z., Drobnjak M., Moreno C., Eisenbach L., Feldman M. Expression of HLA-A,B,C antigens on primary and metastatic tumor cell populations of human carcinomas. Cancer Res. 1991 Dec 1;51(23 Pt 1):6372–6380. [PubMed] [Google Scholar]
  15. Daniel-Vedele F., Israel A., Benicourt C., Kourilsky P. Functional analysis of the mouse H-2Kb gene promoter in embryonal carcinoma cells. Immunogenetics. 1985;21(6):601–611. doi: 10.1007/BF00395884. [DOI] [PubMed] [Google Scholar]
  16. Daniel-Vedele F., Morello D., Benicourt C., Transy C., Le Bail O., Plata F., Kourilsky P. Functional expression of a mouse H-2Kb gene isolated from non-expressing teratocarcinoma cells. EMBO J. 1984 Mar;3(3):597–601. doi: 10.1002/j.1460-2075.1984.tb01854.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. De Baetselier P., Katzav S., Gorelik E., Feldman M., Segal S. Differential expression of H-2 gene products in tumour cells in associated with their metastatogenic properties. Nature. 1980 Nov 13;288(5787):179–181. doi: 10.1038/288179a0. [DOI] [PubMed] [Google Scholar]
  18. Doyle A., Martin W. J., Funa K., Gazdar A., Carney D., Martin S. E., Linnoila I., Cuttitta F., Mulshine J., Bunn P. Markedly decreased expression of class I histocompatibility antigens, protein, and mRNA in human small-cell lung cancer. J Exp Med. 1985 May 1;161(5):1135–1151. doi: 10.1084/jem.161.5.1135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Eisenbach L., Hollander N., Greenfeld L., Yakor H., Segal S., Feldman M. The differential expression of H-2K versus H-2D antigens, distinguishing high-metastatic from low-metastatic clones, is correlated with the immunogenic properties of the tumor cells. Int J Cancer. 1984 Oct 15;34(4):567–573. doi: 10.1002/ijc.2910340421. [DOI] [PubMed] [Google Scholar]
  20. Eisenbach L., Segal S., Feldman M. MHC imbalance and metastatic spread in Lewis lung carcinoma clones. Int J Cancer. 1983 Jul 15;32(1):113–120. doi: 10.1002/ijc.2910320118. [DOI] [PubMed] [Google Scholar]
  21. Franzoso G., Bours V., Park S., Tomita-Yamaguchi M., Kelly K., Siebenlist U. The candidate oncoprotein Bcl-3 is an antagonist of p50/NF-kappa B-mediated inhibition. Nature. 1992 Sep 24;359(6393):339–342. doi: 10.1038/359339a0. [DOI] [PubMed] [Google Scholar]
  22. Fujita T., Nolan G. P., Ghosh S., Baltimore D. Independent modes of transcriptional activation by the p50 and p65 subunits of NF-kappa B. Genes Dev. 1992 May;6(5):775–787. doi: 10.1101/gad.6.5.775. [DOI] [PubMed] [Google Scholar]
  23. Ghosh S., Gifford A. M., Riviere L. R., Tempst P., Nolan G. P., Baltimore D. Cloning of the p50 DNA binding subunit of NF-kappa B: homology to rel and dorsal. Cell. 1990 Sep 7;62(5):1019–1029. doi: 10.1016/0092-8674(90)90276-k. [DOI] [PubMed] [Google Scholar]
  24. Hamada K., Gleason S. L., Levi B. Z., Hirschfeld S., Appella E., Ozato K. H-2RIIBP, a member of the nuclear hormone receptor superfamily that binds to both the regulatory element of major histocompatibility class I genes and the estrogen response element. Proc Natl Acad Sci U S A. 1989 Nov;86(21):8289–8293. doi: 10.1073/pnas.86.21.8289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Haskill S., Beg A. A., Tompkins S. M., Morris J. S., Yurochko A. D., Sampson-Johannes A., Mondal K., Ralph P., Baldwin A. S., Jr Characterization of an immediate-early gene induced in adherent monocytes that encodes I kappa B-like activity. Cell. 1991 Jun 28;65(7):1281–1289. doi: 10.1016/0092-8674(91)90022-q. [DOI] [PubMed] [Google Scholar]
  26. Henkel T., Zabel U., van Zee K., Müller J. M., Fanning E., Baeuerle P. A. Intramolecular masking of the nuclear location signal and dimerization domain in the precursor for the p50 NF-kappa B subunit. Cell. 1992 Mar 20;68(6):1121–1133. doi: 10.1016/0092-8674(92)90083-o. [DOI] [PubMed] [Google Scholar]
  27. Henseling U., Schmidt W., Schöler H. R., Gruss P., Hatzopoulos 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. 1990 Aug;10(8):4100–4109. doi: 10.1128/mcb.10.8.4100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Holden C. A., Sanderson A. R., MacDonald D. M. Absence of human leukocyte antigen molecules in skin tumors and some cutaneous appendages: evidence using monoclonal antibodies. J Am Acad Dermatol. 1983 Dec;9(6):867–871. doi: 10.1016/s0190-9622(83)70200-8. [DOI] [PubMed] [Google Scholar]
  29. Hémar A., Barrand P., Ferrer M., Cornet V., Buttin G., Dautry-Varsat A. Activity of the kappa B enhancer of the interleukin-2 receptor alpha chain in somatic cell hybrids is accompanied by the nuclear localization of NF-kappa B. New Biol. 1991 Nov;3(11):1097–1105. [PubMed] [Google Scholar]
  30. Inoue J., Kerr L. D., Kakizuka A., Verma I. M. I kappa B gamma, a 70 kd protein identical to the C-terminal half of p110 NF-kappa B: a new member of the I kappa B family. Cell. 1992 Mar 20;68(6):1109–1120. doi: 10.1016/0092-8674(92)90082-n. [DOI] [PubMed] [Google Scholar]
  31. Isakov N., Katzav S., Feldman M., Segal S. Loss of expression of transplantation antigens encoded by the H-2K locus on Lewis lung carcinoma cells and its relevance to the tumor's metastatic properties. J Natl Cancer Inst. 1983 Jul;71(1):139–145. [PubMed] [Google Scholar]
  32. Israel A., Kimura A., Fournier A., Fellous M., Kourilsky P. Interferon response sequence potentiates activity of an enhancer in the promoter region of a mouse H-2 gene. Nature. 1986 Aug 21;322(6081):743–746. doi: 10.1038/322743a0. [DOI] [PubMed] [Google Scholar]
  33. Israel A., Yano O., Logeat F., Kieran M., Kourilsky P. Two purified factors bind to the same sequence in the enhancer of mouse MHC class I genes: one of them is a positive regulator induced upon differentiation of teratocarcinoma cells. Nucleic Acids Res. 1989 Jul 11;17(13):5245–5257. doi: 10.1093/nar/17.13.5245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Israël A., Kimura A., Kieran M., Yano O., Kanellopoulos J., Le Bail O., Kourilsky P. A common positive trans-acting factor binds to enhancer sequences in the promoters of mouse H-2 and beta 2-microglobulin genes. Proc Natl Acad Sci U S A. 1987 May;84(9):2653–2657. doi: 10.1073/pnas.84.9.2653. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Israël A., Le Bail O., Hatat D., Piette J., Kieran M., Logeat F., Wallach D., Fellous M., Kourilsky P. TNF stimulates expression of mouse MHC class I genes by inducing an NF kappa B-like enhancer binding activity which displaces constitutive factors. EMBO J. 1989 Dec 1;8(12):3793–3800. doi: 10.1002/j.1460-2075.1989.tb08556.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Kang S. M., Tran A. C., Grilli M., Lenardo M. J. NF-kappa B subunit regulation in nontransformed CD4+ T lymphocytes. Science. 1992 Jun 5;256(5062):1452–1456. doi: 10.1126/science.1604322. [DOI] [PubMed] [Google Scholar]
  37. Kanno M., Fromental C., Staub A., Ruffenach F., Davidson I., Chambon P. The SV40 TC-II(kappa B) and the related H-2Kb enhansons exhibit different cell type specific and inducible proto-enhancer activities, but the SV40 core sequence and the AP-2 binding site have no enhanson properties. EMBO J. 1989 Dec 20;8(13):4205–4214. doi: 10.1002/j.1460-2075.1989.tb08606.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Katoh S., Ozawa K., Kondoh S., Soeda E., Israel A., Shiroki K., Fujinaga K., Itakura K., Gachelin G., Yokoyama K. Identification of sequences responsible for positive and negative regulation by E1A in the promoter of H-2Kbm1 class I MHC gene. EMBO J. 1990 Jan;9(1):127–135. doi: 10.1002/j.1460-2075.1990.tb08088.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Kieran M., Blank V., Logeat F., Vandekerckhove J., Lottspeich F., Le Bail O., Urban M. B., Kourilsky P., Baeuerle P. A., Israël A. The DNA binding subunit of NF-kappa B is identical to factor KBF1 and homologous to the rel oncogene product. Cell. 1990 Sep 7;62(5):1007–1018. doi: 10.1016/0092-8674(90)90275-j. [DOI] [PubMed] [Google Scholar]
  40. Kimura A., Israël A., Le Bail O., Kourilsky P. Detailed analysis of the mouse H-2Kb promoter: enhancer-like sequences and their role in the regulation of class I gene expression. Cell. 1986 Jan 31;44(2):261–272. doi: 10.1016/0092-8674(86)90760-9. [DOI] [PubMed] [Google Scholar]
  41. Korber B., Hood L., 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 U S A. 1987 May;84(10):3380–3384. doi: 10.1073/pnas.84.10.3380. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Korber B., Mermod N., Hood L., Stroynowski I. Regulation of gene expression by interferons: control of H-2 promoter responses. Science. 1988 Mar 11;239(4845):1302–1306. doi: 10.1126/science.3125612. [DOI] [PubMed] [Google Scholar]
  43. Kretzschmar M., Meisterernst M., Scheidereit C., Li G., Roeder R. G. Transcriptional regulation of the HIV-1 promoter by NF-kappa B in vitro. Genes Dev. 1992 May;6(5):761–774. doi: 10.1101/gad.6.5.761. [DOI] [PubMed] [Google Scholar]
  44. Kushtai G., Barzilay J., Feldman M., Eisenbach L. The c-fos proto-oncogene in murine 3LL carcinoma clones controls the expression of MHC genes. Oncogene. 1988 Feb;2(2):119–127. [PubMed] [Google Scholar]
  45. Kushtai G., Feldman M., Eisenbach L. c-fos transfection of 3LL tumor cells turns on MHC gene expression and consequently reduces their metastatic competence. Int J Cancer. 1990 Jun 15;45(6):1131–1136. doi: 10.1002/ijc.2910450624. [DOI] [PubMed] [Google Scholar]
  46. Lampson L. A., Fisher C. A., Whelan J. P. Striking paucity of HLA-A, B, C and beta 2-microglobulin on human neuroblastoma cell lines. J Immunol. 1983 May;130(5):2471–2478. [PubMed] [Google Scholar]
  47. Liou H. C., Nolan G. P., Ghosh S., Fujita T., Baltimore D. The NF-kappa B p50 precursor, p105, contains an internal I kappa B-like inhibitor that preferentially inhibits p50. EMBO J. 1992 Aug;11(8):3003–3009. doi: 10.1002/j.1460-2075.1992.tb05370.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. López-Nevot M. A., Esteban F., Ferrón A., Gutiérrez J., Oliva M. R., Romero C., Huelin C., Ruiz-Cabello F., Garrido F. HLA class I gene expression on human primary tumours and autologous metastases: demonstration of selective losses of HLA antigens on colorectal, gastric and laryngeal carcinomas. Br J Cancer. 1989 Feb;59(2):221–226. doi: 10.1038/bjc.1989.45. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Macchi M., Bornert J. M., Davidson I., Kanno M., Rosales R., Vigneron M., Xiao J. H., Fromental C., Chambon P. The SV40 TC-II(kappa B) enhanson binds ubiquitous and cell type specifically inducible nuclear proteins from lymphoid and non-lymphoid cell lines. EMBO J. 1989 Dec 20;8(13):4215–4227. doi: 10.1002/j.1460-2075.1989.tb08607.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Maryanski J. L., Pala P., Corradin G., Jordan B. R., Cerottini J. C. H-2-restricted cytolytic T cells specific for HLA can recognize a synthetic HLA peptide. Nature. 1986 Dec 11;324(6097):578–579. doi: 10.1038/324578a0. [DOI] [PubMed] [Google Scholar]
  51. Maschek U., Pülm W., Segal S., Hämmerling G. J. Major histocompatibility complex class I genes in murine fibrosarcoma IC9 are down regulated at the level of the chromatin structure. Mol Cell Biol. 1989 Jul;9(7):3136–3142. doi: 10.1128/mcb.9.7.3136. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Masucci M. G., Torsteindottir S., Colombani J., Brautbar C., Klein E., Klein G. Down-regulation of class I HLA antigens and of the Epstein-Barr virus-encoded latent membrane protein in Burkitt lymphoma lines. Proc Natl Acad Sci U S A. 1987 Jul;84(13):4567–4571. doi: 10.1073/pnas.84.13.4567. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Momburg F., Ziegler A., Harpprecht J., Möller P., Moldenhauer G., Hämmerling G. J. Selective loss of HLA-A or HLA-B antigen expression in colon carcinoma. J Immunol. 1989 Jan 1;142(1):352–358. [PubMed] [Google Scholar]
  54. Nagata T., Segars J. H., Levi B. Z., Ozato K. Retinoic acid-dependent transactivation of major histocompatibility complex class I promoters by the nuclear hormone receptor H-2RIIBP in undifferentiated embryonal carcinoma cells. Proc Natl Acad Sci U S A. 1992 Feb 1;89(3):937–941. doi: 10.1073/pnas.89.3.937. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Natali P. G., Nicotra M. R., Bigotti A., Venturo I., Marcenaro L., Giacomini P., Russo C. Selective changes in expression of HLA class I polymorphic determinants in human solid tumors. Proc Natl Acad Sci U S A. 1989 Sep;86(17):6719–6723. doi: 10.1073/pnas.86.17.6719. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Nielsen D. A., Chou J., MacKrell A. J., Casadaban M. J., Steiner D. F. Expression of a preproinsulin-beta-galactosidase gene fusion in mammalian cells. Proc Natl Acad Sci U S A. 1983 Sep;80(17):5198–5202. doi: 10.1073/pnas.80.17.5198. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Nolan G. P., Ghosh S., Liou H. C., Tempst P., Baltimore D. DNA binding and I kappa B inhibition of the cloned p65 subunit of NF-kappa B, a rel-related polypeptide. Cell. 1991 Mar 8;64(5):961–969. doi: 10.1016/0092-8674(91)90320-x. [DOI] [PubMed] [Google Scholar]
  58. Nudel U., Zakut R., Shani M., Neuman S., Levy Z., Yaffe D. The nucleotide sequence of the rat cytoplasmic beta-actin gene. Nucleic Acids Res. 1983 Mar 25;11(6):1759–1771. doi: 10.1093/nar/11.6.1759. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Ozato K., Sachs D. H. Monoclonal antibodies to mouse MHC antigens. III. Hybridoma antibodies reacting to antigens of the H-2b haplotype reveal genetic control of isotype expression. J Immunol. 1981 Jan;126(1):317–321. [PubMed] [Google Scholar]
  60. Plaksin D., Gelber C., Eisenbach L. H-2Db gene transfer into highly metastatic D122 cells results in tumor rejection in allogeneic recipients, but does not affect metastasis in syngeneic recipients. Implications for mechanisms of allorejection. Int J Cancer. 1992 Nov 11;52(5):771–777. doi: 10.1002/ijc.2910520517. [DOI] [PubMed] [Google Scholar]
  61. Plaksin D., Gelber C., Feldman M., Eisenbach L. Reversal of the metastatic phenotype in Lewis lung carcinoma cells after transfection with syngeneic H-2Kb gene. Proc Natl Acad Sci U S A. 1988 Jun;85(12):4463–4467. doi: 10.1073/pnas.85.12.4463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Rees R. C., Buckle A. M., Gelsthorpe K., James V., Potter C. W., Rogers K., Jacob G. Loss of polymorphic A and B locus HLA antigens in colon carcinoma. Br J Cancer. 1988 Apr;57(4):374–377. doi: 10.1038/bjc.1988.85. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Ruben S. M., Dillon P. J., Schreck R., Henkel T., Chen C. H., Maher M., Baeuerle P. A., Rosen C. A. Isolation of a rel-related human cDNA that potentially encodes the 65-kD subunit of NF-kappa B. Science. 1991 Mar 22;251(5000):1490–1493. doi: 10.1126/science.2006423. [DOI] [PubMed] [Google Scholar]
  64. Schmid R. M., Perkins N. D., Duckett C. S., Andrews P. C., Nabel G. J. Cloning of an NF-kappa B subunit which stimulates HIV transcription in synergy with p65. Nature. 1991 Aug 22;352(6337):733–736. doi: 10.1038/352733a0. [DOI] [PubMed] [Google Scholar]
  65. Schmidt W., Festenstein H. Resistance to cell-mediated cytotoxicity is correlated with reduction of H-2K gene products in AKR leukemia. Immunogenetics. 1982;16(3):257–264. doi: 10.1007/BF00343314. [DOI] [PubMed] [Google Scholar]
  66. Schmitz M. L., Baeuerle P. A. The p65 subunit is responsible for the strong transcription activating potential of NF-kappa B. EMBO J. 1991 Dec;10(12):3805–3817. doi: 10.1002/j.1460-2075.1991.tb04950.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Schreiber E., Matthias P., Müller M. M., Schaffner W. Rapid detection of octamer binding proteins with 'mini-extracts', prepared from a small number of cells. Nucleic Acids Res. 1989 Aug 11;17(15):6419–6419. doi: 10.1093/nar/17.15.6419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Schrier P. I., Bernards R., Vaessen R. T., Houweling A., van der Eb A. J. Expression of class I major histocompatibility antigens switched off by highly oncogenic adenovirus 12 in transformed rat cells. 1983 Oct 27-Nov 2Nature. 305(5937):771–775. doi: 10.1038/305771a0. [DOI] [PubMed] [Google Scholar]
  69. Schüle R., Muller M., Kaltschmidt C., Renkawitz R. Many transcription factors interact synergistically with steroid receptors. Science. 1988 Dec 9;242(4884):1418–1420. doi: 10.1126/science.3201230. [DOI] [PubMed] [Google Scholar]
  70. Singh H., LeBowitz J. H., Baldwin A. S., Jr, Sharp P. A. Molecular cloning of an enhancer binding protein: isolation by screening of an expression library with a recognition site DNA. Cell. 1988 Feb 12;52(3):415–423. doi: 10.1016/s0092-8674(88)80034-5. [DOI] [PubMed] [Google Scholar]
  71. Smith M. E., Bodmer W. F., Bodmer J. G. Selective loss of HLA-A,B,C locus products in colorectal adenocarcinoma. Lancet. 1988 Apr 9;1(8589):823–824. doi: 10.1016/s0140-6736(88)91682-0. [DOI] [PubMed] [Google Scholar]
  72. Ten R. M., Paya C. V., Israël N., Le Bail O., Mattei M. G., Virelizier J. L., Kourilsky P., Israël A. The characterization of the promoter of the gene encoding the p50 subunit of NF-kappa B indicates that it participates in its own regulation. EMBO J. 1992 Jan;11(1):195–203. doi: 10.1002/j.1460-2075.1992.tb05042.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Townsend A. R., Rothbard J., Gotch F. M., Bahadur G., Wraith D., McMichael A. J. The epitopes of influenza nucleoprotein recognized by cytotoxic T lymphocytes can be defined with short synthetic peptides. Cell. 1986 Mar 28;44(6):959–968. doi: 10.1016/0092-8674(86)90019-x. [DOI] [PubMed] [Google Scholar]
  74. Urban M. B., Baeuerle P. A. The role of the p50 and p65 subunits of NF-kappa B in the recognition of cognate sequences. New Biol. 1991 Mar;3(3):279–288. [PubMed] [Google Scholar]
  75. Urban M. B., Schreck R., Baeuerle P. A. NF-kappa B contacts DNA by a heterodimer of the p50 and p65 subunit. EMBO J. 1991 Jul;10(7):1817–1825. doi: 10.1002/j.1460-2075.1991.tb07707.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Watts S., Vogel J. M., Harriman W. D., Itoh T., Stauss H. J., Goodenow R. S. DNA sequence analysis of the C3H H-2Kk and H-2Dk loci. Evolutionary relationships to H-2 genes from four other mouse strains. J Immunol. 1987 Dec 1;139(11):3878–3885. [PubMed] [Google Scholar]
  77. Yano O., Kanellopoulos J., Kieran M., Le Bail O., Israël A., Kourilsky P. Purification of KBF1, a common factor binding to both H-2 and beta 2-microglobulin enhancers. EMBO J. 1987 Nov;6(11):3317–3324. doi: 10.1002/j.1460-2075.1987.tb02652.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Zabel U., Henkel T., Silva M. S., Baeuerle P. A. Nuclear uptake control of NF-kappa B by MAD-3, an I kappa B protein present in the nucleus. EMBO J. 1993 Jan;12(1):201–211. doi: 10.1002/j.1460-2075.1993.tb05646.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Zachow K. R., Orr H. T. Regulation of HLA class I transcription in T cells. J Immunol. 1989 Nov 15;143(10):3385–3389. [PubMed] [Google Scholar]
  80. van Bleek G. M., Nathenson S. G. Presentation of antigenic peptides by MHC class I molecules. Trends Cell Biol. 1992 Jul;2(7):202–207. doi: 10.1016/0962-8924(92)90247-k. [DOI] [PubMed] [Google Scholar]

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