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. 1983 Oct 11;11(19):6775–6785. doi: 10.1093/nar/11.19.6775

The structure of the mouse immunoglobulin in gamma 3 membrane gene segment.

M Komaromy, L Clayton, J Rogers, S Robertson, J Kettman, R Wall
PMCID: PMC326413  PMID: 6314258

Abstract

The genomic region containing the mouse immunoglobulin gamma 3 heavy chain membrane (M) exons has been located and sequenced. The exon structure is highly similar to that of the other mouse gamma chains, with strong sequence conservation in the coding regions and the intron 5' to the M1 exon. The intron between M1 and M2 shows moderate sequence homology but very strong conservation of size. RNA blots suggest that gamma 3 membrane exon usage is similar to that seen in other immunoglobulin membrane heavy chain mRNAs. The transmembrane region contains the invariant residues which have been noted in all other heavy chain sequences and which were previously proposed to be interactive in a two-chain model for insertion through the lymphocyte membrane. Conserved residues with similar spacing have been seen in class II histocompatibility antigens, which are also two-chain transmembrane molecules, but not in class I antigens, which span cell membranes with a single chain.

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Selected References

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

  1. Adams J. M., Gough N. M., Webb E. A., Tyler B. M., Jackson J., Cory S. Molecular cloning of mouse immunoglobulin heavy chain messenger ribonucleic acids coding for mu, alpha, gamma 1, gamma 2a, and gamma 3 chains. Biochemistry. 1980 Jun 10;19(12):2711–2719. doi: 10.1021/bi00553a027. [DOI] [PubMed] [Google Scholar]
  2. Alt F. W., Bothwell A. L., Knapp M., Siden E., Mather E., Koshland M., Baltimore D. Synthesis of secreted and membrane-bound immunoglobulin mu heavy chains is directed by mRNAs that differ at their 3' ends. Cell. 1980 Jun;20(2):293–301. doi: 10.1016/0092-8674(80)90615-7. [DOI] [PubMed] [Google Scholar]
  3. Auffray C., Korman A. J., Roux-Dosseto M., Bono R., Strominger J. L. cDNA clone for the heavy chain of the human B cell alloantigen DC1: strong sequence homology to the HLA-DR heavy chain. Proc Natl Acad Sci U S A. 1982 Oct;79(20):6337–6341. doi: 10.1073/pnas.79.20.6337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Benoist C. O., Mathis D. J., Kanter M. R., Williams V. E., 2nd, McDevitt H. O. The murine Ia alpha chains, E alpha and A alpha, show a surprising degree of sequence homology. Proc Natl Acad Sci U S A. 1983 Jan;80(2):534–538. doi: 10.1073/pnas.80.2.534. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Brégégère F., Abastado J. P., Kvist S., Rask L., Lalanne J. L., Garoff H., Cami B., Wiman K., Larhammar D., Peterson P. A. Structure of C-terminal half of two H-2 antigens from cloned mRNA. Nature. 1981 Jul 2;292(5818):78–81. doi: 10.1038/292078a0. [DOI] [PubMed] [Google Scholar]
  6. Coligan J. E., Kindt T. J., Uehara H., Martinko J., Nathenson S. G. Primary structure of a murine transplantation antigen. Nature. 1981 May 7;291(5810):35–39. doi: 10.1038/291035a0. [DOI] [PubMed] [Google Scholar]
  7. Darnell J. E., Jr Variety in the level of gene control in eukaryotic cells. Nature. 1982 Jun 3;297(5865):365–371. doi: 10.1038/297365a0. [DOI] [PubMed] [Google Scholar]
  8. Early P., Rogers J., Davis M., Calame K., Bond M., Wall R., Hood L. Two mRNAs can be produced from a single immunoglobulin mu gene by alternative RNA processing pathways. Cell. 1980 Jun;20(2):313–319. doi: 10.1016/0092-8674(80)90617-0. [DOI] [PubMed] [Google Scholar]
  9. Evans G. A., Margulies D. H., Camerini-Otero R. D., Ozato K., Seidman J. G. Structure and expression of a mouse major histocompatibility antigen gene, H-2Ld. Proc Natl Acad Sci U S A. 1982 Mar;79(6):1994–1998. doi: 10.1073/pnas.79.6.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Galfre G., Howe S. C., Milstein C., Butcher G. W., Howard J. C. Antibodies to major histocompatibility antigens produced by hybrid cell lines. Nature. 1977 Apr 7;266(5602):550–552. doi: 10.1038/266550a0. [DOI] [PubMed] [Google Scholar]
  11. Gilmore-Hebert M., Wall R. Nuclear RNA precursors in the processing pathway to MOPC 21 kappa light chain messenger RNA. J Mol Biol. 1979 Dec 25;135(4):879–891. doi: 10.1016/0022-2836(79)90517-5. [DOI] [PubMed] [Google Scholar]
  12. Heidecker G., Messing J., Gronenborn B. A versatile primer for DNA sequencing in the M13mp2 cloning system. Gene. 1980 Jun;10(1):69–73. doi: 10.1016/0378-1119(80)90145-6. [DOI] [PubMed] [Google Scholar]
  13. Honjo T., Obata M., Yamawaki-Katoaka Y., Kataoka T., Kawakami T., Takahashi N., Mano Y. Cloning and complete nucleotide sequence of mouse immunoglobulin gamma 1 chain gene. Cell. 1979 Oct;18(2):559–568. doi: 10.1016/0092-8674(79)90072-2. [DOI] [PubMed] [Google Scholar]
  14. Hood L., Steinmetz M., Malissen B. Genes of the major histocompatibility complex of the mouse. Annu Rev Immunol. 1983;1:529–568. doi: 10.1146/annurev.iy.01.040183.002525. [DOI] [PubMed] [Google Scholar]
  15. Korman A. J., Auffray C., Schamboeck A., Strominger J. L. The amino acid sequence and gene organization of the heavy chain of the HLA-DR antigen: homology to immunoglobulins. Proc Natl Acad Sci U S A. 1982 Oct;79(19):6013–6017. doi: 10.1073/pnas.79.19.6013. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kvist S., Bregegere F., Rask L., Cami B., Garoff H., Daniel F., Wiman K., Larhammar D., Abastado J. P., Gachelin G. cDNA clone coding for part of a mouse H-2d major histocompatibility antigen. Proc Natl Acad Sci U S A. 1981 May;78(5):2772–2776. doi: 10.1073/pnas.78.5.2772. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. LITTLEFIELD J. W. SELECTION OF HYBRIDS FROM MATINGS OF FIBROBLASTS IN VITRO AND THEIR PRESUMED RECOMBINANTS. Science. 1964 Aug 14;145(3633):709–710. doi: 10.1126/science.145.3633.709. [DOI] [PubMed] [Google Scholar]
  19. Lai C. J., Dhar R., Khoury G. Mapping the spliced and unspliced late lytic SV40 RNAs. Cell. 1978 Aug;14(4):971–982. doi: 10.1016/0092-8674(78)90351-3. [DOI] [PubMed] [Google Scholar]
  20. Lalanne J. L., Delarbre C., Gachelin G., Kourilsky P. A cDNA clone containing the entire coding sequence of a mouse H-2Kd histocompatibility antigen. Nucleic Acids Res. 1983 Mar 11;11(5):1567–1577. doi: 10.1093/nar/11.5.1567. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Larhammar D., Schenning L., Gustafsson K., Wiman K., Claesson L., Rask L., Peterson P. A. Complete amino acid sequence of an HLA-DR antigen-like beta chain as predicted from the nucleotide sequence: similarities with immunoglobulins and HLA-A, -B, and -C antigens. Proc Natl Acad Sci U S A. 1982 Jun;79(12):3687–3691. doi: 10.1073/pnas.79.12.3687. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lee J. S., Trowsdale J., Travers P. J., Carey J., Grosveld F., Jenkins J., Bodmer W. F. Sequence of an HLA-DR alpha-chain cDNA clone and intron-exon organization of the corresponding gene. Nature. 1982 Oct 21;299(5885):750–752. doi: 10.1038/299750a0. [DOI] [PubMed] [Google Scholar]
  23. Maki R., Roeder W., Traunecker A., Sidman C., Wabl M., Raschke W., Tonegawa S. The role of DNA rearrangement and alternative RNA processing in the expression of immunoglobulin delta genes. Cell. 1981 May;24(2):353–365. doi: 10.1016/0092-8674(81)90325-1. [DOI] [PubMed] [Google Scholar]
  24. Malissen M., Malissen B., Jordan B. R. Exon/intron organization and complete nucleotide sequence of an HLA gene. Proc Natl Acad Sci U S A. 1982 Feb;79(3):893–897. doi: 10.1073/pnas.79.3.893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. McNicholas J., Steinmetz M., Hunkapiller T., Jones P., Hood L. DNA sequence of the gene encoding the E alpha Ia polypeptide of the BALB/c mouse. Science. 1982 Dec 17;218(4578):1229–1232. doi: 10.1126/science.6815800. [DOI] [PubMed] [Google Scholar]
  26. Miyata T., Yasunaga T., Yamawaki-Kataoka Y., Obata M., Honjo T. Nucleotide sequence divergence of mouse immunoglobulin gamma 1 and gamma 2b chain genes and the hypothesis of intervening sequence-mediated domain transfer. Proc Natl Acad Sci U S A. 1980 Apr;77(4):2143–2147. doi: 10.1073/pnas.77.4.2143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Moore K. W., Rogers J., Hunkapiller T., Early P., Nottenburg C., Weissman I., Bazin H., Wall R., Hood L. E. Expression of IgD may use both DNA rearrangement and RNA splicing mechanisms. Proc Natl Acad Sci U S A. 1981 Mar;78(3):1800–1804. doi: 10.1073/pnas.78.3.1800. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Moore K. W., Sher B. T., Sun Y. H., Eakle K. A., Hood L. DNA sequence of a gene encoding a BALB/c mouse Ld transplantation antigen. Science. 1982 Feb 5;215(4533):679–682. doi: 10.1126/science.7058332. [DOI] [PubMed] [Google Scholar]
  29. Mushinski J. F., Blattner F. R., Owens J. D., Finkelman F. D., Kessler S. W., Fitzmaurice L., Potter M., Tucker P. W. Mouse immunoglobulin D: construction and characterization of a cloned delta chain cDNA. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7405–7409. doi: 10.1073/pnas.77.12.7405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Nevins J. R., Darnell J. E., Jr Steps in the processing of Ad2 mRNA: poly(A)+ nuclear sequences are conserved and poly(A) addition precedes splicing. Cell. 1978 Dec;15(4):1477–1493. doi: 10.1016/0092-8674(78)90071-5. [DOI] [PubMed] [Google Scholar]
  31. Ollo R., Auffray C., Morchamps C., Rougeon F. Comparison of mouse immunoglobulin gamma 2a and gamma 2b chain genes suggests that exons can be exchanged between genes in a multigenic family. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2442–2446. doi: 10.1073/pnas.78.4.2442. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Ollo R., Rougeon F. Gene conversion and polymorphism: generation of mouse immunoglobulin gamma 2a chain alleles by differential gene conversion by gamma 2b chain gene. Cell. 1983 Feb;32(2):515–523. doi: 10.1016/0092-8674(83)90471-3. [DOI] [PubMed] [Google Scholar]
  33. Reyes A. A., Schöld M., Itakura K., Wallace R. B. Isolation of a cDNA clone for the murine transplantation antigen H-2Kb. Proc Natl Acad Sci U S A. 1982 May;79(10):3270–3274. doi: 10.1073/pnas.79.10.3270. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Robertson S. M., Clayton L., Dev V. G., Wall R., Capra J. D., Kettman J. R. Antiarsonate antibody response: a model for studying antibody diversity. Fed Proc. 1982 Jul;41(9):2502–2506. [PubMed] [Google Scholar]
  35. Rogers J., Choi E., Souza L., Carter C., Word C., Kuehl M., Eisenberg D., Wall R. Gene segments encoding transmembrane carboxyl termini of immunoglobulin gamma chains. Cell. 1981 Oct;26(1 Pt 1):19–27. doi: 10.1016/0092-8674(81)90029-5. [DOI] [PubMed] [Google Scholar]
  36. Rogers J., Early P., Carter C., Calame K., Bond M., Hood L., Wall R. Two mRNAs with different 3' ends encode membrane-bound and secreted forms of immunoglobulin mu chain. Cell. 1980 Jun;20(2):303–312. doi: 10.1016/0092-8674(80)90616-9. [DOI] [PubMed] [Google Scholar]
  37. Rogers J., Wall R. A mechanism for RNA splicing. Proc Natl Acad Sci U S A. 1980 Apr;77(4):1877–1879. doi: 10.1073/pnas.77.4.1877. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Schibler U., Marcu K. B., Perry R. P. The synthesis and processing of the messenger RNAs specifying heavy and light chain immunoglobulins in MPC-11 cells. Cell. 1978 Dec;15(4):1495–1509. doi: 10.1016/0092-8674(78)90072-7. [DOI] [PubMed] [Google Scholar]
  39. Tucker P. W., Liu C. P., Mushinski J. F., Blattner F. R. Mouse immunoglobulin D: messenger RNA and genomic DNA sequences. Science. 1980 Sep 19;209(4463):1353–1360. doi: 10.1126/science.6968091. [DOI] [PubMed] [Google Scholar]
  40. Tucker P. W., Marcu K. B., Newell N., Richards J., Blattner F. R. Sequence of the cloned gene for the constant region of murine gamma 2b immunoglobulin heavy chain. Science. 1979 Dec 14;206(4424):1303–1306. doi: 10.1126/science.117549. [DOI] [PubMed] [Google Scholar]
  41. Tucker P. W., Slightom J. L., Blattner F. R. Mouse IgA heavy chain gene sequence: implications for evolution of immunoglobulin hinge axons. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7684–7688. doi: 10.1073/pnas.78.12.7684. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Tyler B. M., Cowman A. F., Adams J. M., Harris A. W. Generation of long mRNA for membrane immunoglobulin gamma 2a chains by differential splicing. Nature. 1981 Oct 1;293(5831):406–408. doi: 10.1038/293406a0. [DOI] [PubMed] [Google Scholar]
  43. Tyler B. M., Cowman A. F., Gerondakis S. D., Adams J. M., Bernard O. mRNA for surface immunoglobulin gamma chains encodes a highly conserved transmembrane sequence and a 28-residue intracellular domain. Proc Natl Acad Sci U S A. 1982 Mar;79(6):2008–2012. doi: 10.1073/pnas.79.6.2008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Wall R., Choi E., Carter C., Kuehl M., Rogers J. RNA processing in immunoglobulin gene expression. Cold Spring Harb Symp Quant Biol. 1981;45(Pt 2):879–885. doi: 10.1101/sqb.1981.045.01.105. [DOI] [PubMed] [Google Scholar]
  45. Williams P. B., Kubo R. T., Grey H. M. mu-Chains from a nonsecretor B cell line differ from secreted mu-chains at the C-terminal end. J Immunol. 1978 Dec;121(6):2435–2439. [PubMed] [Google Scholar]
  46. Yamawaki-Kataoka Y., Kataoka T., Takahashi N., Obata M., Honjo T. Complete nucleotide sequence of immunoglobulin gamma2b chain gene cloned from newborn nouse DNA. Nature. 1980 Feb 21;283(5749):786–789. doi: 10.1038/283786a0. [DOI] [PubMed] [Google Scholar]
  47. Yamawaki-Kataoka Y., Miyata T., Honjo T. The complete nucleotide sequence of mouse immunoglobin gamma 2a gene and evolution of heavy chain genes: further evidence for intervening sequence-mediated domain transfer. Nucleic Acids Res. 1981 Mar 25;9(6):1365–1381. doi: 10.1093/nar/9.6.1365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Yamawaki-Kataoka Y., Nakai S., Miyata T., Honjo T. Nucleotide sequences of gene segments encoding membrane domains of immunoglobulin gamma chains. Proc Natl Acad Sci U S A. 1982 Apr;79(8):2623–2627. doi: 10.1073/pnas.79.8.2623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Yaoita Y., Kumagai Y., Okumura K., Honjo T. Expression of lymphocyte surface IgE does not require switch recombination. Nature. 1982 Jun 24;297(5868):697–699. doi: 10.1038/297697a0. [DOI] [PubMed] [Google Scholar]

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