Abstract
The murine major histocompatibility complex encodes H-2K and H-2D transplantation antigens and other class I-like proteins called Qa and Tla molecules; the functions of the Qa/Tla molecules are not known. That they may participate in embryonic cell-cell interactions and/or play a role in immune responses against tumors has been speculated. We have studied two murine embryonal carcinoma tumors, 402AX and PCC4, that are rejected in vivo immunologically, although they do not express H-2K or H-2D antigens. Transplantation studies with these cells suggest that rejection is mediated by class-I-like major histocompatibility complex antigens. As a first step in evaluating Qa/Tla function(s), we have characterized expression of class I-like genes and proteins in 402AX and PCC4 cells. Northern (RNA) blot hybridizations, polymerase chain reaction studies, and cDNA cloning experiments demonstrate that EC lines transcribe genes allelic to the Tla region gene "37", Qa-2 region gene "Q7", and another, previously uncharacterized, class I-like gene. Immunoprecipitation studies show that the embryonal carcinoma tumor cells contain low levels of beta 2-microglobulin expressed in association with non-H-2K, non-H-2D class I-like proteins.
Full text
PDFImages in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Allen H., Fraser J., Flyer D., Calvin S., Flavell R. Beta 2-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 U S A. 1986 Oct;83(19):7447–7451. doi: 10.1073/pnas.83.19.7447. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- Cole G. A., Cole G. A., Clements V. K., Garcia E. P., Ostrand-Rosenberg S. Allogeneic H-2 antigen expression is insufficient for tumor rejection. Proc Natl Acad Sci U S A. 1987 Dec;84(23):8613–8617. doi: 10.1073/pnas.84.23.8613. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Croce C. M., Linnenbach A., Huebner K., Parnes J. R., Margulies D. H., Appella E., Seidman J. G. Control of expression of histocompatibility antigens (H-2) and beta 2-microglobulin in F9 teratocarcinoma stem cells. Proc Natl Acad Sci U S A. 1981 Sep;78(9):5754–5758. doi: 10.1073/pnas.78.9.5754. [DOI] [PMC free article] [PubMed] [Google Scholar]
- De Plaen E., Lurquin C., Van Pel A., Mariamé B., Szikora J. P., Wölfel T., Sibille C., Chomez P., Boon T. Immunogenic (tum-) variants of mouse tumor P815: cloning of the gene of tum- antigen P91A and identification of the tum- mutation. Proc Natl Acad Sci U S A. 1988 Apr;85(7):2274–2278. doi: 10.1073/pnas.85.7.2274. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Devlin J. J., Weiss E. H., Paulson M., Flavell R. A. Duplicated gene pairs and alleles of class I genes in the Qa2 region of the murine major histocompatibility complex: a comparison. EMBO J. 1985 Dec 1;4(12):3203–3207. doi: 10.1002/j.1460-2075.1985.tb04066.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Démant P., Oudshoorn-Snoek M. H-2 class I antigen expression on mouse teratocarcinoma cell lines. Immunogenetics. 1985;22(6):543–552. doi: 10.1007/BF00430302. [DOI] [PubMed] [Google Scholar]
- Efstratiadis A., Kafatos F. C., Maxam A. M., Maniatis T. Enzymatic in vitro synthesis of globin genes. Cell. 1976 Feb;7(2):279–288. doi: 10.1016/0092-8674(76)90027-1. [DOI] [PubMed] [Google Scholar]
- Fahrner K., Hogan B. L., Flavell R. A. Transcription of H-2 and Qa genes in embryonic and adult mice. EMBO J. 1987 May;6(5):1265–1271. doi: 10.1002/j.1460-2075.1987.tb02363.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ito K., Bonneville M., Takagaki Y., Nakanishi N., Kanagawa O., Krecko E. G., Tonegawa S. Different gamma delta T-cell receptors are expressed on thymocytes at different stages of development. Proc Natl Acad Sci U S A. 1989 Jan;86(2):631–635. doi: 10.1073/pnas.86.2.631. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jakob H., Boon T., Gaillard J., Nicolas J., Jacob F. Tératocarcinome de la spuris: isolement, culture et propriétés de cellules a potentialités multiples. Ann Microbiol (Paris) 1973 Oct;124(3):269–282. [PubMed] [Google Scholar]
- Janeway C. A., Jr Frontiers of the immune system. Nature. 1988 Jun 30;333(6176):804–806. doi: 10.1038/333804a0. [DOI] [PubMed] [Google Scholar]
- Janeway C. A., Jr, Jones B., Hayday A. Specificity and function of T cells bearing gamma delta receptors. Immunol Today. 1988 Mar;9(3):73–76. doi: 10.1016/0167-5699(88)91267-4. [DOI] [PubMed] [Google Scholar]
- Kourilsky P., Claverie J. M. MHC restriction, alloreactivity, and thymic education: a common link? Cell. 1989 Feb 10;56(3):327–329. doi: 10.1016/0092-8674(89)90233-x. [DOI] [PubMed] [Google Scholar]
- Kvist S., Roberts L., Dobberstein B. Mouse histocompatibility genes: structure and organisation of a Kd gene. EMBO J. 1983;2(2):245–254. doi: 10.1002/j.1460-2075.1983.tb01413.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lalanne J. L., Transy C., Guerin S., Darche S., Meulien P., Kourilsky P. Expression of class I genes in the major histocompatibility complex: identification of eight distinct mRNAs in DBA/2 mouse liver. Cell. 1985 Jun;41(2):469–478. doi: 10.1016/s0092-8674(85)80020-9. [DOI] [PubMed] [Google Scholar]
- Martin G. R. Teratocarcinomas and mammalian embryogenesis. Science. 1980 Aug 15;209(4458):768–776. doi: 10.1126/science.6250214. [DOI] [PubMed] [Google Scholar]
- Morello D., Daniel F., Baldacci P., Cayre Y., Gachelin G., Kourilsky P. Absence of significant H-2 and beta 2-microglobulin mRNA expression by mouse embryonal carcinoma cells. Nature. 1982 Mar 18;296(5854):260–262. doi: 10.1038/296260a0. [DOI] [PubMed] [Google Scholar]
- Morello D., Duprey P., Israel A., Babinet C. Asynchronous regulation of mouse H-2D and beta-2 microglobulin RNA transcripts. Immunogenetics. 1985;22(5):441–452. doi: 10.1007/BF00418090. [DOI] [PubMed] [Google Scholar]
- Moser A. R., Johnson L. L., Dove W. F. Mice coisogenically immunized against H-2 class I antigens on transfected L cells reject transplanted embryonal carcinoma cells. Immunogenetics. 1985;22(6):533–541. doi: 10.1007/BF00430301. [DOI] [PubMed] [Google Scholar]
- Nicolas J. F., Avner P., Gaillard J., Guenet J. L., Jakob H., Jacob F. Cell lines derived from teratocarcinomas. Cancer Res. 1976 Nov;36(11 Pt 2):4224–4231. [PubMed] [Google Scholar]
- Ostrand-Rosenberg S., Clements V. Resistance to 402AX teratocarcinoma involves immunity to minor histocompatibility antigens. Immunogenetics. 1987;26(1-2):1–5. doi: 10.1007/BF00345447. [DOI] [PubMed] [Google Scholar]
- Ostrand-Rosenberg S., Cohn A. L., Sandoz J. W. Multiple splenic lymphoid cell subpopulations regulate H-2 antigen expression on teratocarcinoma cells in vivo. J Immunol. 1983 Jun;130(6):2969–2973. [PubMed] [Google Scholar]
- Ozato K., Wan Y. J., Orrison B. M. Mouse major histocompatibility class I gene expression begins at midsomite stage and is inducible in earlier-stage embryos by interferon. Proc Natl Acad Sci U S A. 1985 Apr;82(8):2427–2431. doi: 10.1073/pnas.82.8.2427. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pierce G. B. Teratocarcinoma: model for a developmental concept of cancer. Curr Top Dev Biol. 1967;2:223–246. doi: 10.1016/s0070-2153(08)60289-6. [DOI] [PubMed] [Google Scholar]
- Robinson P. J., Bevec D., Mellor A. L., Weiss E. H. Sequence of the mouse Q4 class I gene and characterization of the gene product. Immunogenetics. 1988;27(2):79–86. doi: 10.1007/BF00351079. [DOI] [PubMed] [Google Scholar]
- Robinson P. J. Qb-1, a new class I polypeptide encoded by the Qa region of the mouse H-2 complex. Immunogenetics. 1985;22(3):285–289. doi: 10.1007/BF00404488. [DOI] [PubMed] [Google Scholar]
- STEVENS L. C. Studies on transplantable testicular teratomas of strain 129 mice. J Natl Cancer Inst. 1958 Jun;20(6):1257–1275. doi: 10.1093/jnci/20.6.1257. [DOI] [PubMed] [Google Scholar]
- Saiki R. K., Gelfand D. H., Stoffel S., Scharf S. J., Higuchi R., Horn G. T., Mullis K. B., Erlich H. A. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988 Jan 29;239(4839):487–491. doi: 10.1126/science.2448875. [DOI] [PubMed] [Google Scholar]
- Sanger F., Coulson A. R., Barrell B. G., Smith A. J., Roe B. A. Cloning in single-stranded bacteriophage as an aid to rapid DNA sequencing. J Mol Biol. 1980 Oct 25;143(2):161–178. doi: 10.1016/0022-2836(80)90196-5. [DOI] [PubMed] [Google Scholar]
- Seeburg P. H., Shine J., Martial J. A., Baxter J. D., Goodman H. M. Nucleotide sequence and amplification in bacteria of structural gene for rat growth hormone. Nature. 1977 Dec 8;270(5637):486–494. doi: 10.1038/270486a0. [DOI] [PubMed] [Google Scholar]
- Segal S., Khoury G. Differentiation as a requirement for simian virus 40 gene expression in F-9 embryonal carcinoma cells. Proc Natl Acad Sci U S A. 1979 Nov;76(11):5611–5615. doi: 10.1073/pnas.76.11.5611. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sher B. T., Nairn R., Coligan J. E., Hood L. E. DNA sequence of the mouse H-2Dd transplantation antigen gene. Proc Natl Acad Sci U S A. 1985 Feb;82(4):1175–1179. doi: 10.1073/pnas.82.4.1175. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Steinmetz M., Moore K. W., Frelinger J. G., Sher B. T., Shen F. W., Boyse E. A., Hood L. A pseudogene homologous to mouse transplantation antigens: transplantation antigens are encoded by eight exons that correlate with protein domains. Cell. 1981 Sep;25(3):683–692. doi: 10.1016/0092-8674(81)90175-6. [DOI] [PubMed] [Google Scholar]
- Stroynowski I., Soloski M., Low M. G., 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. 1987 Aug 28;50(5):759–768. doi: 10.1016/0092-8674(87)90334-5. [DOI] [PubMed] [Google Scholar]
- Transy C., Nash S. R., David-Watine B., Cochet M., Hunt S. W., 3rd, Hood L. E., Kourilsky P. A low polymorphic mouse H-2 class I gene from the Tla complex is expressed in a broad variety of cell types. J Exp Med. 1987 Aug 1;166(2):341–361. doi: 10.1084/jem.166.2.341. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Waneck G. L., Sherman D. H., Calvin S., Allen H., Flavell R. A. Tissue-specific expression of cell-surface Qa-2 antigen from a transfected Q7b gene of C57BL/10 mice. J Exp Med. 1987 May 1;165(5):1358–1370. doi: 10.1084/jem.165.5.1358. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Warner C. M., Gollnick S. O., Flaherty L., 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. 1987 Apr;36(3):611–616. doi: 10.1095/biolreprod36.3.611. [DOI] [PubMed] [Google Scholar]
- Wickens M. P., Buell G. N., Schimke R. T. Synthesis of double-stranded DNA complementary to lysozyme, ovomucoid, and ovalbumin mRNAs. Optimization for full length second strand synthesis by Escherichia coli DNA polymerase I. J Biol Chem. 1978 Apr 10;253(7):2483–2495. [PubMed] [Google Scholar]