Skip to main content
PMC home page
The Journal of Experimental Medicine logoLink to The Journal of Experimental Medicine
. 1992 Oct 1;176(4):937–950. doi: 10.1084/jem.176.4.937

Distinctive polymorphism at the HLA-C locus: implications for the expression of HLA-C

PMCID: PMC2119399  PMID: 1383381

Abstract

The HLA-C locus remains an enigma. The serological polymorphism is poorly defined, HLA-C molecules are expressed at the cell surface at about 10% the levels of HLA-A and -B, and their importance for antigen presentation to either CD8-bearing T cells or natural killer cells is unclear. Our understanding of HLA-C polymorphism has also lagged behind that of HLA-A and -B. We have applied the polymerase chain reaction to the characterization of cDNA encoding HLA-C antigens. Combining the recent results with previously characterized HLA-C alleles gives a data base of 26 sequences, which was used to analyze the nature of HLA-C polymorphism and compare it to the variation seen in HLA-A and -B. The sequences form 10 families of alleles that correlate well with the patterns of serological crossreactivity, including the C blanks, and all major HLA-C allelic families appear to have been sampled. The families further divide into two groups of HLA-C alleles defined on the basis of linked substitutions in the 3' exons. In comparison with HLA-A and -B, HLA-C alleles are more closely related to each other, there being less variation in residues of the antigen recognition site and more variation at other positions. In particular, the helix of the alpha 1 domain of HLA-C molecules is unusually conserved. Despite the reduced diversity in the antigen recognition site, it is evident that HLA-C genes have been the target of past selection for polymorphism. Within the antigen recognition site, it is the alpha 1 domain that is most diagnostic of HLA-C, whereas the alpha 2 domain is similar to that of HLA-B, the locus to which HLA-C is most closely related. In particular, conserved motifs in the alpha 1 helix and the conserved glycine at the base of the B pocket (position 45) provide a combination of features that is uniquely found in HLA-C molecules. We hypothesize that these features restrict the peptides bound by HLA-C molecules and in this manner reduce the efficiency of HLA-C assembly and expression at the cell surface. The overall picture HLA-C polymorphism obtained from this sampling of HLA-C alleles is unlikely to change as further alleles are characterized.

Full Text

The Full Text of this article is available as a PDF (1.2 MB).

Selected References

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

  1. Asahina A., Akazaki S., Nakagawa H., Kuwata S., Tokunaga K., Ishibashi Y., Juji T. Specific nucleotide sequence of HLA-C is strongly associated with psoriasis vulgaris. J Invest Dermatol. 1991 Aug;97(2):254–258. doi: 10.1111/1523-1747.ep12480361. [DOI] [PubMed] [Google Scholar]
  2. Beck J. C., Hansen T. H., Cullen S. E., Lee D. R. Slower processing, weaker beta 2-M association, and lower surface expression of H-2Ld are influenced by its amino terminus. J Immunol. 1986 Aug 1;137(3):916–923. [PubMed] [Google Scholar]
  3. Belich M. P., Madrigal J. A., Hildebrand W. H., Zemmour J., Williams R. C., Luz R., Petzl-Erler M. L., Parham P. Unusual HLA-B alleles in two tribes of Brazilian Indians. Nature. 1992 May 28;357(6376):326–329. doi: 10.1038/357326a0. [DOI] [PubMed] [Google Scholar]
  4. Beretta A., Grassi F., Pelagi M., Clivio A., Parravicini C., Giovinazzo G., Andronico F., Lopalco L., Verani P., Buttò S. HIV env glycoprotein shares a cross-reacting epitope with a surface protein present on activated human monocytes and involved in antigen presentation. Eur J Immunol. 1987 Dec;17(12):1793–1798. doi: 10.1002/eji.1830171218. [DOI] [PubMed] [Google Scholar]
  5. Bjorkman P. J., Parham P. Structure, function, and diversity of class I major histocompatibility complex molecules. Annu Rev Biochem. 1990;59:253–288. doi: 10.1146/annurev.bi.59.070190.001345. [DOI] [PubMed] [Google Scholar]
  6. Bjorkman P. J., Saper M. A., Samraoui B., Bennett W. S., Strominger J. L., Wiley D. C. Structure of the human class I histocompatibility antigen, HLA-A2. Nature. 1987 Oct 8;329(6139):506–512. doi: 10.1038/329506a0. [DOI] [PubMed] [Google Scholar]
  7. Bjorkman P. J., Saper M. A., Samraoui B., Bennett W. S., Strominger J. L., Wiley D. C. The foreign antigen binding site and T cell recognition regions of class I histocompatibility antigens. Nature. 1987 Oct 8;329(6139):512–518. doi: 10.1038/329512a0. [DOI] [PubMed] [Google Scholar]
  8. Bodmer J. G., Marsh S. G., Albert E. D., Bodmer W. F., Dupont B., Erlich H. A., Mach B., Mayr W. R., Parham P., Sasazuki T. Nomenclature for factors of the HLA system, 1991. WHO Nomenclature Committee for factors of the HLA system. Tissue Antigens. 1992 Apr;39(4):161–173. doi: 10.1111/j.1399-0039.1992.tb01932.x. [DOI] [PubMed] [Google Scholar]
  9. Bonneville M., Moreau J. F., Blokland E., Pool J., Moisan J. P., Goulmy E., Soulillou J. P. T lymphocyte cloning from rejected human kidney allograft. Recognition repertoire of alloreactive T cell clones. J Immunol. 1988 Dec 15;141(12):4187–4195. [PubMed] [Google Scholar]
  10. Bronson S. K., Pei J., Taillon-Miller P., Chorney M. J., Geraghty D. E., Chaplin D. D. Isolation and characterization of yeast artificial chromosome clones linking the HLA-B and HLA-C loci. Proc Natl Acad Sci U S A. 1991 Mar 1;88(5):1676–1680. doi: 10.1073/pnas.88.5.1676. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Buxton S. E., Benjamin R. J., Clayberger C., Parham P., Krensky A. M. Anchoring pockets in human histocompatibility complex leukocyte antigen (HLA) class I molecules: analysis of the conserved B ("45") pocket of HLA-B27. J Exp Med. 1992 Mar 1;175(3):809–820. doi: 10.1084/jem.175.3.809. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Chen B. P., Lam V., Kraus E. E., DeMars R., Sondel P. M. Restriction of Epstein-Barr virus-specific cytotoxic T cells by HLA-A, -B, and -C molecules. Hum Immunol. 1989 Oct;26(2):137–147. doi: 10.1016/0198-8859(89)90099-2. [DOI] [PubMed] [Google Scholar]
  13. Cianetti L., Testa U., Scotto L., La Valle R., Simeone A., Boccoli G., Giannella G., Peschle C., Boncinelli E. Three new class I HLA alleles: structure of mRNAs and alternative mechanisms of processing. Immunogenetics. 1989;29(2):80–91. doi: 10.1007/BF00395855. [DOI] [PubMed] [Google Scholar]
  14. Connolly J. M., Hansen T. H., Ingold A. L., Potter T. A. Recognition by CD8 on cytotoxic T lymphocytes is ablated by several substitutions in the class I alpha 3 domain: CD8 and the T-cell receptor recognize the same class I molecule. Proc Natl Acad Sci U S A. 1990 Mar;87(6):2137–2141. doi: 10.1073/pnas.87.6.2137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. D'Amaro J., Bach F. H., Van Rood J. J., Rimm A. A., Bortin M. M. HLA C associations with acute leukaemia. Lancet. 1984 Nov 24;2(8413):1176–1178. doi: 10.1016/s0140-6736(84)92741-7. [DOI] [PubMed] [Google Scholar]
  16. Davidson W. F., Kress M., Khoury G., Jay G. Comparison of HLA class I gene sequences. Derivation of locus-specific oligonucleotide probes specific for HLA-A, HLA-B, and HLA-C genes. J Biol Chem. 1985 Nov 5;260(25):13414–13423. [PubMed] [Google Scholar]
  17. Degen E., Williams D. B. Participation of a novel 88-kD protein in the biogenesis of murine class I histocompatibility molecules. J Cell Biol. 1991 Mar;112(6):1099–1115. doi: 10.1083/jcb.112.6.1099. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Dill O., Kievits F., Koch S., Ivanyi P., Hämmerling G. J. Immunological function of HLA-C antigens in HLA-Cw3 transgenic mice. Proc Natl Acad Sci U S A. 1988 Aug;85(15):5664–5668. doi: 10.1073/pnas.85.15.5664. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Dower S. K., Segal D. M. Interaction of monoclonal antibodies with MHC class I antigens on mouse spleen cells. II. Levels of expression of H-2K, H-2D, and H-2L in different mouse strains. J Immunol. 1985 Jan;134(1):431–435. [PubMed] [Google Scholar]
  20. Duceman B. W., Ness D., Rende R., Chorney M. J., Srivastava R., Greenspan D. S., Pan J., Weissman S. M., Grumet F. C. HLA-JY328: mapping studies and expression of a polymorphic HLA class I gene. Immunogenetics. 1986;23(2):90–99. doi: 10.1007/BF00377967. [DOI] [PubMed] [Google Scholar]
  21. Ellis S. A., Strachan T., Palmer M. S., McMichael A. J. Complete nucleotide sequence of a unique HLA class I C locus product expressed on the human choriocarcinoma cell line BeWo. J Immunol. 1989 May 1;142(9):3281–3285. [PubMed] [Google Scholar]
  22. Ennis P. D., Zemmour J., Salter R. D., Parham P. Rapid cloning of HLA-A,B cDNA by using the polymerase chain reaction: frequency and nature of errors produced in amplification. Proc Natl Acad Sci U S A. 1990 Apr;87(7):2833–2837. doi: 10.1073/pnas.87.7.2833. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Garrett T. P., Saper M. A., Bjorkman P. J., Strominger J. L., Wiley D. C. Specificity pockets for the side chains of peptide antigens in HLA-Aw68. Nature. 1989 Dec 7;342(6250):692–696. doi: 10.1038/342692a0. [DOI] [PubMed] [Google Scholar]
  24. Green J., Montasser M., Low H. C., Woodrow J. C. Investigation of the associations of a number of HLA antigens with psoriasis and psoriatic arthritis. Stat Med. 1988 Mar;7(3):443–450. doi: 10.1002/sim.4780070310. [DOI] [PubMed] [Google Scholar]
  25. Groop L., Koskimies S., Pelkonen R., Tolppanen E. M. Increased frequency of HLA-Cw4 in type 2 diabetes. Acta Endocrinol (Copenh) 1983 Dec;104(4):475–478. doi: 10.1530/acta.0.1040475. [DOI] [PubMed] [Google Scholar]
  26. Grunnet N., Kristensen T., Kissmeyer-Nielsen F. Cell mediated lympholysis in man. The impact of HLA-C antigens. Tissue Antigens. 1976 May;7(5):301–309. doi: 10.1111/j.1399-0039.1976.tb01071.x. [DOI] [PubMed] [Google Scholar]
  27. Guild B. C., Erikson R. L., Strominger J. L. HLA-A2 and HLA-B7 antigens are phosphorylated in vitro by rous sarcoma virus kinase (pp60v-src) at a tyrosine residue encoded in a highly conserved exon of the intracellular domain. Proc Natl Acad Sci U S A. 1983 May;80(10):2894–2898. doi: 10.1073/pnas.80.10.2894. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Güssow D., Rein R. S., Meijer I., de Hoog W., Seemann G. H., Hochstenbach F. M., Ploegh H. L. Isolation, expression, and the primary structure of HLA-Cw1 and HLA-Cw2 genes: evolutionary aspects. Immunogenetics. 1987;25(5):313–322. doi: 10.1007/BF00404424. [DOI] [PubMed] [Google Scholar]
  29. Hajek-Rosenmayr A., Jungl L., Stammler M., Kirnbauer M. HLA-C "blank" alleles express class I gene products. Biochemical analysis of four different HLA-C "blank" polypeptides. Immunogenetics. 1989;30(6):399–404. doi: 10.1007/BF02421170. [DOI] [PubMed] [Google Scholar]
  30. Hajek-Rosenmayr A., Jungl L., Stammler M., Kirnbauer M. HLA-C locus antigens seen by one-dimensional isoelectric focusing: definition of the so far known HLA-C specificities and of two subtypes. Hum Immunol. 1989 Dec;26(4):227–236. doi: 10.1016/0198-8859(89)90001-3. [DOI] [PubMed] [Google Scholar]
  31. Hedrick P. W., Whittam T. S., Parham P. Heterozygosity at individual amino acid sites: extremely high levels for HLA-A and -B genes. Proc Natl Acad Sci U S A. 1991 Jul 1;88(13):5897–5901. doi: 10.1073/pnas.88.13.5897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Hildebrand W. H., Madrigal J. A., Little A. M., Parham P. HLA-Bw22: a family of molecules with identity to HLA-B7 in the alpha 1-helix. J Immunol. 1992 Feb 15;148(4):1155–1162. [PubMed] [Google Scholar]
  33. Hughes A. L., Nei M. Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature. 1988 Sep 8;335(6186):167–170. doi: 10.1038/335167a0. [DOI] [PubMed] [Google Scholar]
  34. Jardetzky T. S., Lane W. S., Robinson R. A., Madden D. R., Wiley D. C. Identification of self peptides bound to purified HLA-B27. Nature. 1991 Sep 26;353(6342):326–329. doi: 10.1038/353326a0. [DOI] [PubMed] [Google Scholar]
  35. Kariyone A., Tanabe M., Juji T., Kano K., Takiguchi M. Functional expression of HLA-C blank antigens on human blood lymphocytes. J Immunol. 1990 Dec 1;145(11):3714–3718. [PubMed] [Google Scholar]
  36. Koller B. H., Sidwell B., DeMars R., Orr H. T. Isolation of HLA locus-specific DNA probes from the 3'-untranslated region. Proc Natl Acad Sci U S A. 1984 Aug;81(16):5175–5178. doi: 10.1073/pnas.81.16.5175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Lawlor D. A., Warren E., Taylor P., Parham P. Gorilla class I major histocompatibility complex alleles: comparison to human and chimpanzee class I. J Exp Med. 1991 Dec 1;174(6):1491–1509. doi: 10.1084/jem.174.6.1491. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Lawlor D. A., Zemmour J., Ennis P. D., Parham P. Evolution of class-I MHC genes and proteins: from natural selection to thymic selection. Annu Rev Immunol. 1990;8:23–63. doi: 10.1146/annurev.iy.08.040190.000323. [DOI] [PubMed] [Google Scholar]
  39. Lie W. R., Myers N. B., Gorka J., Rubocki R. J., Connolly J. M., Hansen T. H. Peptide ligand-induced conformation and surface expression of the Ld class I MHC molecule. Nature. 1990 Mar 29;344(6265):439–441. doi: 10.1038/344439a0. [DOI] [PubMed] [Google Scholar]
  40. Littaua R. A., Oldstone M. B., Takeda A., Debouck C., Wong J. T., Tuazon C. U., Moss B., Kievits F., Ennis F. A. An HLA-C-restricted CD8+ cytotoxic T-lymphocyte clone recognizes a highly conserved epitope on human immunodeficiency virus type 1 gag. J Virol. 1991 Aug;65(8):4051–4056. doi: 10.1128/jvi.65.8.4051-4056.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Little A. M., Madrigal J. A., Parham P. Molecular definition of an elusive third HLA-A9 molecule: HLA-A9.3. Immunogenetics. 1992;35(1):41–45. doi: 10.1007/BF00216625. [DOI] [PubMed] [Google Scholar]
  42. Lutz C. T., Jensen D. A., Schiffenbauer J., Didier D. K., Schwartz B. D., Davis C. S. Multiple mechanisms produce diversity of HLA-C alleles. Hum Immunol. 1990 May;28(1):27–31. doi: 10.1016/0198-8859(90)90099-b. [DOI] [PubMed] [Google Scholar]
  43. Madden D. R., Gorga J. C., Strominger J. L., Wiley D. C. The structure of HLA-B27 reveals nonamer self-peptides bound in an extended conformation. Nature. 1991 Sep 26;353(6342):321–325. doi: 10.1038/353321a0. [DOI] [PubMed] [Google Scholar]
  44. Malissen B., Kristensen T., Goridis C., Madsen M., Mawas C. Clones of human cytotoxic T lymphocytes derived from an allosensitized individual: HLA specificity and cell surface markers. Scand J Immunol. 1981 Sep;14(3):213–224. doi: 10.1111/j.1365-3083.1981.tb00558.x. [DOI] [PubMed] [Google Scholar]
  45. 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]
  46. Messer G., Zemmour J., Orr H. T., Parham P., Weiss E. H., Girdlestone J. HLA-J, a second inactivated class I HLA gene related to HLA-G and HLA-A. Implications for the evolution of the HLA-A-related genes. J Immunol. 1992 Jun 15;148(12):4043–4053. [PubMed] [Google Scholar]
  47. Mizuno S., Kang S. H., Lee H. W., Trapani J. A., Dupont B., Yang S. Y. Isolation and expression of a cDNA clone encoding HLA-Cw6: unique characteristics of HLA-C encoded gene products. Immunogenetics. 1989;29(5):323–330. doi: 10.1007/BF00352842. [DOI] [PubMed] [Google Scholar]
  48. Müller C. A., Hasmann R., Grosse-Wilde H., Vögeler U., Bei-Jun C., Dopfer R., Waller H. D. Significant association of acute lymphoblastic leukemia with HLA-Cw7. Genet Epidemiol. 1988;5(6):453–461. doi: 10.1002/gepi.1370050609. [DOI] [PubMed] [Google Scholar]
  49. Neefjes J. J., Ploegh H. L. Allele and locus-specific differences in cell surface expression and the association of HLA class I heavy chain with beta 2-microglobulin: differential effects of inhibition of glycosylation on class I subunit association. Eur J Immunol. 1988 May;18(5):801–810. doi: 10.1002/eji.1830180522. [DOI] [PubMed] [Google Scholar]
  50. Nei M., Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 1986 Sep;3(5):418–426. doi: 10.1093/oxfordjournals.molbev.a040410. [DOI] [PubMed] [Google Scholar]
  51. Nei M., Jin L. Variances of the average numbers of nucleotide substitutions within and between populations. Mol Biol Evol. 1989 May;6(3):290–300. doi: 10.1093/oxfordjournals.molbev.a040547. [DOI] [PubMed] [Google Scholar]
  52. Nössner E., Schendel D. J. HLA-Cw7-associated restriction fragment length polymorphism detected with an HLA-C locus-specific DNA probe. Tissue Antigens. 1991 Apr;37(4):168–170. doi: 10.1111/j.1399-0039.1991.tb01867.x. [DOI] [PubMed] [Google Scholar]
  53. Ozawa A., Ohkido M., Inoko H., Ando A., Tsuji K. Specific restriction fragment length polymorphism on the HLA-C region and susceptibility to psoriasis vulgaris. J Invest Dermatol. 1988 Mar;90(3):402–405. doi: 10.1111/1523-1747.ep12456500. [DOI] [PubMed] [Google Scholar]
  54. Parham P., Benjamin R. J., Chen B. P., Clayberger C., Ennis P. D., Krensky A. M., Lawlor D. A., Littman D. R., Norment A. M., Orr H. T. Diversity of class I HLA molecules: functional and evolutionary interactions with T cells. Cold Spring Harb Symp Quant Biol. 1989;54(Pt 1):529–543. doi: 10.1101/sqb.1989.054.01.063. [DOI] [PubMed] [Google Scholar]
  55. Parham P., Lawlor D. A., Lomen C. E., Ennis P. D. Diversity and diversification of HLA-A,B,C alleles. J Immunol. 1989 Jun 1;142(11):3937–3950. [PubMed] [Google Scholar]
  56. Parham P., Lomen C. E., Lawlor D. A., Ways J. P., Holmes N., Coppin H. L., Salter R. D., Wan A. M., Ennis P. D. Nature of polymorphism in HLA-A, -B, and -C molecules. Proc Natl Acad Sci U S A. 1988 Jun;85(11):4005–4009. doi: 10.1073/pnas.85.11.4005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Pohla H., Kuon W., Tabaczewski P., Doerner C., Weiss E. H. Allelic variation in HLA-B and HLA-C sequences and the evolution of the HLA-B alleles. Immunogenetics. 1989;29(5):297–307. doi: 10.1007/BF00352839. [DOI] [PubMed] [Google Scholar]
  58. Saper M. A., Bjorkman P. J., Wiley D. C. Refined structure of the human histocompatibility antigen HLA-A2 at 2.6 A resolution. J Mol Biol. 1991 May 20;219(2):277–319. doi: 10.1016/0022-2836(91)90567-p. [DOI] [PubMed] [Google Scholar]
  59. Snary D., Barnstable C. J., Bodmer W. F., Crumpton M. J. Molecular structure of human histocompatibility antigens: the HLA-C series. Eur J Immunol. 1977 Aug;7(8):580–585. doi: 10.1002/eji.1830070816. [DOI] [PubMed] [Google Scholar]
  60. Sodoyer R., Damotte M., Delovitch T. L., Trucy J., Jordan B. R., Strachan T. Complete nucleotide sequence of a gene encoding a functional human class I histocompatibility antigen (HLA-CW3). EMBO J. 1984 Apr;3(4):879–885. doi: 10.1002/j.1460-2075.1984.tb01900.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Sodoyer R., Damotte M., Delovitch T. L., Trucy J., Jordan B. R., Strachan T. Complete nucleotide sequence of a gene encoding a functional human class I histocompatibility antigen (HLA-CW3). EMBO J. 1984 Apr;3(4):879–885. doi: 10.1002/j.1460-2075.1984.tb01900.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Srivastava R., Duceman B. W., Biro P. A., Sood A. K., Weissman S. M. Molecular organization of the class I genes of human major histocompatibility complex. Immunol Rev. 1985 Jul;84:93–121. doi: 10.1111/j.1600-065x.1985.tb01127.x. [DOI] [PubMed] [Google Scholar]
  63. Stam N. J., Spits H., Ploegh H. L. Monoclonal antibodies raised against denatured HLA-B locus heavy chains permit biochemical characterization of certain HLA-C locus products. J Immunol. 1986 Oct 1;137(7):2299–2306. [PubMed] [Google Scholar]
  64. Storkus W. J., Howell D. N., Salter R. D., Dawson J. R., Cresswell P. NK susceptibility varies inversely with target cell class I HLA antigen expression. J Immunol. 1987 Mar 15;138(6):1657–1659. [PubMed] [Google Scholar]
  65. Storkus W. J., Salter R. D., Alexander J., Ward F. E., Ruiz R. E., Cresswell P., Dawson J. R. Class I-induced resistance to natural killing: identification of nonpermissive residues in HLA-A2. Proc Natl Acad Sci U S A. 1991 Jul 15;88(14):5989–5992. doi: 10.1073/pnas.88.14.5989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Takata H., Inoko H., Ando A., Haranaka M., Watanabe B., Tsuji K., Iri H. Cloning and analysis of HLA class I cDNA encoding a new HLA-C specificity Cx52. Immunogenetics. 1988;28(4):265–270. doi: 10.1007/BF00345504. [DOI] [PubMed] [Google Scholar]
  67. Takiguchi M., Nishimura I., Hayashi H., Karakl S., Kariyone A., Kano K. The structure and expression of genes encoding serologically undetected HLA-C locus antigens. J Immunol. 1989 Aug 15;143(4):1372–1378. [PubMed] [Google Scholar]
  68. Tibensky D., DeMars R., Holowachuk E. W., Delovitch T. L. Sequence and gene transfer analyses of HLA-CwBL18 (HLA-C blank) and HLA-Cw5 genes. Implications for the control of expression and immunogenicity of HLA-C antigens. J Immunol. 1989 Jul 1;143(1):348–355. [PubMed] [Google Scholar]
  69. Tibensky D., Decary F., Delovitch T. L. HLA-C genes are transcribed in HLA-C blank individuals. Immunogenetics. 1988;27(3):220–224. doi: 10.1007/BF00346590. [DOI] [PubMed] [Google Scholar]
  70. Townsend A., Bodmer H. Antigen recognition by class I-restricted T lymphocytes. Annu Rev Immunol. 1989;7:601–624. doi: 10.1146/annurev.iy.07.040189.003125. [DOI] [PubMed] [Google Scholar]
  71. Watkins D. I., McAdam S. N., Liu X., Strang C. R., Milford E. L., Levine C. G., Garber T. L., Dogon A. L., Lord C. I., Ghim S. H. New recombinant HLA-B alleles in a tribe of South American Amerindians indicate rapid evolution of MHC class I loci. Nature. 1992 May 28;357(6376):329–333. doi: 10.1038/357329a0. [DOI] [PubMed] [Google Scholar]
  72. Weis J. H., Murre C. Differential expression of H-2Dd and H-2Ld histocompatibility antigens. J Exp Med. 1985 Feb 1;161(2):356–365. doi: 10.1084/jem.161.2.356. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Wu T. T., Kabat E. A. An analysis of the sequences of the variable regions of Bence Jones proteins and myeloma light chains and their implications for antibody complementarity. J Exp Med. 1970 Aug 1;132(2):211–250. doi: 10.1084/jem.132.2.211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Zemmour J., Gumperz J. E., Hildebrand W. H., Ward F. E., Marsh S. G., Williams R. C., Parham P. The molecular basis for reactivity of anti-Cw1 and anti-Cw3 alloantisera with HLA-B46 haplotypes. Tissue Antigens. 1992 May;39(5):249–257. doi: 10.1111/j.1399-0039.1992.tb01943.x. [DOI] [PubMed] [Google Scholar]
  75. Zemmour J., Koller B. H., Ennis P. D., Geraghty D. E., Lawlor D. A., Orr H. T., Parham P. HLA-AR, an inactivated antigen-presenting locus related to HLA-A. Implications for the evolution of the MHC. J Immunol. 1990 May 1;144(9):3619–3629. [PubMed] [Google Scholar]
  76. Zemmour J., Little A. M., Schendel D. J., Parham P. The HLA-A,B "negative" mutant cell line C1R expresses a novel HLA-B35 allele, which also has a point mutation in the translation initiation codon. J Immunol. 1992 Mar 15;148(6):1941–1948. [PubMed] [Google Scholar]

Articles from The Journal of Experimental Medicine are provided here courtesy of The Rockefeller University Press

RESOURCES