Abstract
We have characterized the amino acid sequences of over 20 endogenous peptides bound by a soluble analog of H-2Dd, H-2Dds. Synthetic analogs corresponding to self, viral, tumor, or motif peptides were then tested for their ability to bind to H-2Dd by serologic epitope induction assays using both purified soluble protein and cell surface H-2Dd. The dominant primary sequence motif included glycine at position 2, proline at position 3, and a hydrophobic COOH terminus: leucine, isoleucine, or phenylalanine at position 9 or 10. Ancillary support for high affinity binding was contributed by a positively charged residue at position 5. Three-dimensional computer models of H-2Dds/peptide complexes, based on the crystallographic structure of the human HLA-B27/peptide complex, showed that the basic residue at position 5 was in position to form a salt bridge with aspartic acid at position 156, a polymorphic residue of the H-2Dd heavy (H) chain. Analysis of 28 such models, including 17 based on nonamer self-peptides, revealed considerable variation in the structure of the major histocompatibility complex (MHC) surrounding peptide residue 1, depending on the size and charge of the side chain. Interactions between the side chains of peptide residues 5 and 7, and 6 and 8 commonly occurred. Those peptide positions with limited sequence variability and least solvent accessibility may satisfy structural requirements for high affinity binding of the peptide to the MHC class I H chain, whereas the highly variable positions of the peptide (such as positions 4, 6, and 8) may contribute more to the T cell epitopes.
Full Text
The Full Text of this article is available as a PDF (5.6 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Abastado J. P., Darche S., Jouin H., Delarbre C., Gachelin G., Kourilsky P. A monoclonal antibody recognizes a subset of the H-2Dd mouse major class I antigens. Res Immunol. 1989 Jun-Aug;140(5-6):581–594. doi: 10.1016/0923-2494(89)90121-1. [DOI] [PubMed] [Google Scholar]
- Abastado J. P., Jaulin C., Schutze M. P., Langlade-Demoyen P., Plata F., Ozato K., Kourilsky P. Fine mapping of epitopes by intradomain Kd/Dd recombinants. J Exp Med. 1987 Aug 1;166(2):327–340. doi: 10.1084/jem.166.2.327. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
- Bikoff E. K., Jaffe L., Ribaudo R. K., Otten G. R., Germain R. N., Robertson E. J. MHC class I surface expression in embryo-derived cell lines inducible with peptide or interferon. Nature. 1991 Nov 21;354(6350):235–238. doi: 10.1038/354235a0. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- Bluestone J. A., Jameson S., Miller S., Dick R., 2nd Peptide-induced conformational changes in class I heavy chains alter major histocompatibility complex recognition. J Exp Med. 1992 Dec 1;176(6):1757–1761. doi: 10.1084/jem.176.6.1757. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Catipović B., Dal Porto J., Mage M., Johansen T. E., Schneck J. P. Major histocompatibility complex conformational epitopes are peptide specific. J Exp Med. 1992 Dec 1;176(6):1611–1618. doi: 10.1084/jem.176.6.1611. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Corr M., Boyd L. F., Frankel S. R., Kozlowski S., Padlan E. A., Margulies D. H. Endogenous peptides of a soluble major histocompatibility complex class I molecule, H-2Lds: sequence motif, quantitative binding, and molecular modeling of the complex. J Exp Med. 1992 Dec 1;176(6):1681–1692. doi: 10.1084/jem.176.6.1681. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cossins J., Gould K. G., Smith M., Driscoll P., Brownlee G. G. Precise prediction of a Kk-restricted cytotoxic T cell epitope in the NS1 protein of influenza virus using an MHC allele-specific motif. Virology. 1993 Mar;193(1):289–295. doi: 10.1006/viro.1993.1124. [DOI] [PubMed] [Google Scholar]
- DiBrino M., Parker K. C., Shiloach J., Knierman M., Lukszo J., Turner R. V., Biddison W. E., Coligan J. E. Endogenous peptides bound to HLA-A3 possess a specific combination of anchor residues that permit identification of potential antigenic peptides. Proc Natl Acad Sci U S A. 1993 Feb 15;90(4):1508–1512. doi: 10.1073/pnas.90.4.1508. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dupree P., Olkkonen V. M., Chavrier P. Sequence of a canine cDNA clone encoding a Ran/TC4 GTP-binding protein. Gene. 1992 Oct 21;120(2):325–326. doi: 10.1016/0378-1119(92)90118-9. [DOI] [PubMed] [Google Scholar]
- Eggertsen G., Hudson G., Shiels B., Reed D., Fey G. H. Sequence of rat alpha 1-macroglobulin, a broad-range proteinase inhibitor from the alpha-macroglobulin-complement family. Mol Biol Med. 1991 Apr;8(2):287–302. [PubMed] [Google Scholar]
- Falk K., Rötzschke O., Deres K., Metzger J., Jung G., Rammensee H. G. Identification of naturally processed viral nonapeptides allows their quantification in infected cells and suggests an allele-specific T cell epitope forecast. J Exp Med. 1991 Aug 1;174(2):425–434. doi: 10.1084/jem.174.2.425. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Falk K., Rötzschke O., Rammensee H. G. A self peptide naturally presented by both H-2Kb and H-2Kbm1 molecules demonstrates MHC restriction of self tolerance at the molecular level. Int Immunol. 1992 Mar;4(3):321–325. doi: 10.1093/intimm/4.3.321. [DOI] [PubMed] [Google Scholar]
- Falk K., Rötzschke O., Rammensee H. G. Cellular peptide composition governed by major histocompatibility complex class I molecules. Nature. 1990 Nov 15;348(6298):248–251. doi: 10.1038/348248a0. [DOI] [PubMed] [Google Scholar]
- Falk K., Rötzschke O., Stevanović S., Jung G., Rammensee H. G. Allele-specific motifs revealed by sequencing of self-peptides eluted from MHC molecules. Nature. 1991 May 23;351(6324):290–296. doi: 10.1038/351290a0. [DOI] [PubMed] [Google Scholar]
- Flores-Riveros J. R., Sibley E., Kastelic T., Lane M. D. Substrate phosphorylation catalyzed by the insulin receptor tyrosine kinase. Kinetic correlation to autophosphorylation of specific sites in the beta subunit. J Biol Chem. 1989 Dec 25;264(36):21557–21572. [PubMed] [Google Scholar]
- Fremont D. H., Matsumura M., Stura E. A., Peterson P. A., Wilson I. A. Crystal structures of two viral peptides in complex with murine MHC class I H-2Kb. Science. 1992 Aug 14;257(5072):919–927. doi: 10.1126/science.1323877. [DOI] [PubMed] [Google Scholar]
- 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]
- Gates F. T., 3rd, Coligan J. E., Kindt T. J. Complete amino acid sequence of murine beta 2-microglobulin: structural evidence for strain-related polymorphism. Proc Natl Acad Sci U S A. 1981 Jan;78(1):554–558. doi: 10.1073/pnas.78.1.554. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gould K. G., Scotney H., Brownlee G. G. Characterization of two distinct major histocompatibility complex class I Kk-restricted T-cell epitopes within the influenza A/PR/8/34 virus hemagglutinin. J Virol. 1991 Oct;65(10):5401–5409. doi: 10.1128/jvi.65.10.5401-5409.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grantham R. Amino acid difference formula to help explain protein evolution. Science. 1974 Sep 6;185(4154):862–864. doi: 10.1126/science.185.4154.862. [DOI] [PubMed] [Google Scholar]
- Guo H. C., Jardetzky T. S., Garrett T. P., Lane W. S., Strominger J. L., Wiley D. C. Different length peptides bind to HLA-Aw68 similarly at their ends but bulge out in the middle. Nature. 1992 Nov 26;360(6402):364–366. doi: 10.1038/360364a0. [DOI] [PubMed] [Google Scholar]
- Hill A. V., Elvin J., Willis A. C., Aidoo M., Allsopp C. E., Gotch F. M., Gao X. M., Takiguchi M., Greenwood B. M., Townsend A. R. Molecular analysis of the association of HLA-B53 and resistance to severe malaria. Nature. 1992 Dec 3;360(6403):434–439. doi: 10.1038/360434a0. [DOI] [PubMed] [Google Scholar]
- Hunt D. F., Henderson R. A., Shabanowitz J., Sakaguchi K., Michel H., Sevilir N., Cox A. L., Appella E., Engelhard V. H. Characterization of peptides bound to the class I MHC molecule HLA-A2.1 by mass spectrometry. Science. 1992 Mar 6;255(5049):1261–1263. doi: 10.1126/science.1546328. [DOI] [PubMed] [Google Scholar]
- Hérissé J., Galibert F. Nucleotide sequence of the EcoRI E fragment of adenovirus 2 genome. Nucleic Acids Res. 1981 Mar 11;9(5):1229–1240. doi: 10.1093/nar/9.5.1229. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Kirkpatrick S., Gelatt C. D., Jr, Vecchi M. P. Optimization by simulated annealing. Science. 1983 May 13;220(4598):671–680. doi: 10.1126/science.220.4598.671. [DOI] [PubMed] [Google Scholar]
- Kornblihtt A. R., Umezawa K., Vibe-Pedersen K., Baralle F. E. Primary structure of human fibronectin: differential splicing may generate at least 10 polypeptides from a single gene. EMBO J. 1985 Jul;4(7):1755–1759. doi: 10.1002/j.1460-2075.1985.tb03847.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kozlowski S., Corr M., Takeshita T., Boyd L. F., Pendleton C. D., Germain R. N., Berzofsky J. A., Margulies D. H. Serum angiotensin-1 converting enzyme activity processes a human immunodeficiency virus 1 gp160 peptide for presentation by major histocompatibility complex class I molecules. J Exp Med. 1992 Jun 1;175(6):1417–1422. doi: 10.1084/jem.175.6.1417. [DOI] [PMC free article] [PubMed] [Google Scholar]
- LaRosa G. J., Davide J. P., Weinhold K., Waterbury J. A., Profy A. T., Lewis J. A., Langlois A. J., Dreesman G. R., Boswell R. N., Shadduck P. Conserved sequence and structural elements in the HIV-1 principal neutralizing determinant. Science. 1990 Aug 24;249(4971):932–935. doi: 10.1126/science.2392685. [DOI] [PubMed] [Google Scholar]
- Lerch K., Ammer D. Amino acid sequence of copper-zinc superoxide dismutase from horse liver. J Biol Chem. 1981 Nov 25;256(22):11545–11551. [PubMed] [Google Scholar]
- MacArthur M. W., Thornton J. M. Influence of proline residues on protein conformation. J Mol Biol. 1991 Mar 20;218(2):397–412. doi: 10.1016/0022-2836(91)90721-h. [DOI] [PubMed] [Google Scholar]
- 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]
- Madden D. R., Gorga J. C., Strominger J. L., Wiley D. C. The three-dimensional structure of HLA-B27 at 2.1 A resolution suggests a general mechanism for tight peptide binding to MHC. Cell. 1992 Sep 18;70(6):1035–1048. doi: 10.1016/0092-8674(92)90252-8. [DOI] [PubMed] [Google Scholar]
- Margulies D. H., Ramsey A. L., Boyd L. F., McCluskey J. Genetic engineering of an H-2Dd/Q10b chimeric histocompatibility antigen: purification of soluble protein from transformant cell supernatants. Proc Natl Acad Sci U S A. 1986 Jul;83(14):5252–5256. doi: 10.1073/pnas.83.14.5252. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maryanski J. L., Verdini A. S., Weber P. C., Salemme F. R., Corradin G. Competitor analogs for defined T cell antigens: peptides incorporating a putative binding motif and polyproline or polyglycine spacers. Cell. 1990 Jan 12;60(1):63–72. doi: 10.1016/0092-8674(90)90716-r. [DOI] [PubMed] [Google Scholar]
- Matsumura M., Fremont D. H., Peterson P. A., Wilson I. A. Emerging principles for the recognition of peptide antigens by MHC class I molecules. Science. 1992 Aug 14;257(5072):927–934. doi: 10.1126/science.1323878. [DOI] [PubMed] [Google Scholar]
- Matunis M. J., Michael W. M., Dreyfuss G. Characterization and primary structure of the poly(C)-binding heterogeneous nuclear ribonucleoprotein complex K protein. Mol Cell Biol. 1992 Jan;12(1):164–171. doi: 10.1128/mcb.12.1.164. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McCluskey J., Boyd L. F., Highet P. F., Inman J., Margulies D. H. T cell activation by purified, soluble, class I MHC molecules. Requirement for polyvalency. J Immunol. 1988 Sep 1;141(5):1451–1455. [PubMed] [Google Scholar]
- McMichael A. J., Gotch F. M., Santos-Aguado J., Strominger J. L. Effect of mutations and variations of HLA-A2 on recognition of a virus peptide epitope by cytotoxic T lymphocytes. Proc Natl Acad Sci U S A. 1988 Dec;85(23):9194–9198. doi: 10.1073/pnas.85.23.9194. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nakanishi O., Oyanagi M., Kuwano Y., Tanaka T., Nakayama T., Mitsui H., Nabeshima Y., Ogata K. Molecular cloning and nucleotide sequences of cDNAs specific for rat liver ribosomal proteins S17 and L30. Gene. 1985;35(3):289–296. doi: 10.1016/0378-1119(85)90007-1. [DOI] [PubMed] [Google Scholar]
- Nathenson S. G., Geliebter J., Pfaffenbach G. M., Zeff R. A. Murine major histocompatibility complex class-I mutants: molecular analysis and structure-function implications. Annu Rev Immunol. 1986;4:471–502. doi: 10.1146/annurev.iy.04.040186.002351. [DOI] [PubMed] [Google Scholar]
- Noguchi T., Inoue H., Tanaka T. The M1- and M2-type isozymes of rat pyruvate kinase are produced from the same gene by alternative RNA splicing. J Biol Chem. 1986 Oct 15;261(29):13807–13812. [PubMed] [Google Scholar]
- Oleinikov A. V., Jokhadze G. G., Alakhov YuB Primary structure of rat liver elongation factor 2 deduced from the cDNA sequence. FEBS Lett. 1989 May 8;248(1-2):131–136. doi: 10.1016/0014-5793(89)80447-8. [DOI] [PubMed] [Google Scholar]
- Otten G. R., Bikoff E., Ribaudo R. K., Kozlowski S., Margulies D. H., Germain R. N. Peptide and beta 2-microglobulin regulation of cell surface MHC class I conformation and expression. J Immunol. 1992 Jun 15;148(12):3723–3732. [PubMed] [Google Scholar]
- Ozato K., Mayer N. M., Sachs D. H. Monoclonal antibodies to mouse major histocompatibility complex antigens. Transplantation. 1982 Sep;34(3):113–120. doi: 10.1097/00007890-198209000-00001. [DOI] [PubMed] [Google Scholar]
- Padlan E. A. On the nature of antibody combining sites: unusual structural features that may confer on these sites an enhanced capacity for binding ligands. Proteins. 1990;7(2):112–124. doi: 10.1002/prot.340070203. [DOI] [PubMed] [Google Scholar]
- Padlan E. A. Structural implications of sequence variability in immunoglobulins. Proc Natl Acad Sci U S A. 1977 Jun;74(6):2551–2555. doi: 10.1073/pnas.74.6.2551. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Parnes J. R., Seidman J. G. Structure of wild-type and mutant mouse beta 2-microglobulin genes. Cell. 1982 Jun;29(2):661–669. doi: 10.1016/0092-8674(82)90182-9. [DOI] [PubMed] [Google Scholar]
- Pissowotzki K., Mansouri K., Piepersberg W. Genetics of streptomycin production in Streptomyces griseus: molecular structure and putative function of genes strELMB2N. Mol Gen Genet. 1991 Dec;231(1):113–123. doi: 10.1007/BF00293829. [DOI] [PubMed] [Google Scholar]
- Ray D., Culine S., Tavitain A., Moreau-Gachelin F. The human homologue of the putative proto-oncogene Spi-1: characterization and expression in tumors. Oncogene. 1990 May;5(5):663–668. [PubMed] [Google Scholar]
- Reddy A. B., Chatterjee A., Rothblum L. I., Black A., Busch H. Isolation and characterization of complementary DNA to proliferating cell nucleolar antigen P40. Cancer Res. 1989 Apr 1;49(7):1763–1767. [PubMed] [Google Scholar]
- Ribaudo R. K., Margulies D. H. Independent and synergistic effects of disulfide bond formation, beta 2-microglobulin, and peptides on class I MHC folding and assembly in an in vitro translation system. J Immunol. 1992 Nov 1;149(9):2935–2944. [PubMed] [Google Scholar]
- Riddles P. W., Whan V., Blakeley R. L., Zerner B. Cloning and sequencing of a jack bean urease-encoding cDNA. Gene. 1991 Dec 15;108(2):265–267. doi: 10.1016/0378-1119(91)90443-f. [DOI] [PubMed] [Google Scholar]
- Roberts K. P., Griswold M. D. Characterization of rat transferrin receptor cDNA: the regulation of transferrin receptor mRNA in testes and in Sertoli cells in culture. Mol Endocrinol. 1990 Apr;4(4):531–542. doi: 10.1210/mend-4-4-531. [DOI] [PubMed] [Google Scholar]
- Rötzschke O., Falk K., Deres K., Schild H., Norda M., Metzger J., Jung G., Rammensee H. G. Isolation and analysis of naturally processed viral peptides as recognized by cytotoxic T cells. Nature. 1990 Nov 15;348(6298):252–254. doi: 10.1038/348252a0. [DOI] [PubMed] [Google Scholar]
- 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]
- Schad P. A., Iglewski B. H. Nucleotide sequence and expression in Escherichia coli of the Pseudomonas aeruginosa lasA gene. J Bacteriol. 1988 Jun;170(6):2784–2789. doi: 10.1128/jb.170.6.2784-2789.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shimizu S., Malik K., Sejima H., Kishi J., Hayakawa T., Koiwai O. Cloning and sequencing of the cDNA encoding a mouse tissue inhibitor of metalloproteinase-2. Gene. 1992 May 15;114(2):291–292. doi: 10.1016/0378-1119(92)90591-c. [DOI] [PubMed] [Google Scholar]
- Shirai M., Pendleton C. D., Berzofsky J. A. Broad recognition of cytotoxic T cell epitopes from the HIV-1 envelope protein with multiple class I histocompatibility molecules. J Immunol. 1992 Mar 15;148(6):1657–1667. [PubMed] [Google Scholar]
- Stewart M. A., Warnock M., Wheeler A., Wilkie N., Mullins J. I., Onions D. E., Neil J. C. Nucleotide sequences of a feline leukemia virus subgroup A envelope gene and long terminal repeat and evidence for the recombinational origin of subgroup B viruses. J Virol. 1986 Jun;58(3):825–834. doi: 10.1128/jvi.58.3.825-834.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sutton J., Rowland-Jones S., Rosenberg W., Nixon D., Gotch F., Gao X. M., Murray N., Spoonas A., Driscoll P., Smith M. A sequence pattern for peptides presented to cytotoxic T lymphocytes by HLA B8 revealed by analysis of epitopes and eluted peptides. Eur J Immunol. 1993 Feb;23(2):447–453. doi: 10.1002/eji.1830230222. [DOI] [PubMed] [Google Scholar]
- Szikora J. P., Van Pel A., Boon T. Tum- mutation P35B generates the MHC-binding site of a new antigenic peptide. Immunogenetics. 1993;37(2):135–138. doi: 10.1007/BF00216837. [DOI] [PubMed] [Google Scholar]
- Szikora J. P., Van Pel A., Brichard V., André M., Van Baren N., Henry P., De Plaen E., Boon T. Structure of the gene of tum- transplantation antigen P35B: presence of a point mutation in the antigenic allele. EMBO J. 1990 Apr;9(4):1041–1050. doi: 10.1002/j.1460-2075.1990.tb08208.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Takahashi H., Cohen J., Hosmalin A., Cease K. B., Houghten R., Cornette J. L., DeLisi C., Moss B., Germain R. N., Berzofsky J. A. An immunodominant epitope of the human immunodeficiency virus envelope glycoprotein gp160 recognized by class I major histocompatibility complex molecule-restricted murine cytotoxic T lymphocytes. Proc Natl Acad Sci U S A. 1988 May;85(9):3105–3109. doi: 10.1073/pnas.85.9.3105. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Torres R. M., Clark E. A. Differential increase of an alternatively polyadenylated mRNA species of murine CD40 upon B lymphocyte activation. J Immunol. 1992 Jan 15;148(2):620–626. [PubMed] [Google Scholar]
- Utz U., Koenig S., Coligan J. E., Biddison W. E. Presentation of three different viral peptides, HTLV-1 Tax, HCMV gB, and influenza virus M1, is determined by common structural features of the HLA-A2.1 molecule. J Immunol. 1992 Jul 1;149(1):214–221. [PubMed] [Google Scholar]
- Van Bleek G. M., Nathenson S. G. Isolation of an endogenously processed immunodominant viral peptide from the class I H-2Kb molecule. Nature. 1990 Nov 15;348(6298):213–216. doi: 10.1038/348213a0. [DOI] [PubMed] [Google Scholar]
- Watts S., Wheeler C., Morse R., Goodenow R. S. Amino acid comparison of the class I antigens of mouse major histocompatibility complex. Immunogenetics. 1989;30(5):390–392. doi: 10.1007/BF02425281. [DOI] [PubMed] [Google Scholar]
- Wei M. L., Cresswell P. HLA-A2 molecules in an antigen-processing mutant cell contain signal sequence-derived peptides. Nature. 1992 Apr 2;356(6368):443–446. doi: 10.1038/356443a0. [DOI] [PubMed] [Google Scholar]
- Wilson J. M., Kelley W. N. Molecular basis of hypoxanthine-guanine phosphoribosyltransferase deficiency in a patient with the Lesch-Nyhan syndrome. J Clin Invest. 1983 May;71(5):1331–1335. doi: 10.1172/JCI110884. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wilson S. R., Cui W. L. Applications of simulated annealing to peptides. Biopolymers. 1990 Jan;29(1):225–235. doi: 10.1002/bip.360290127. [DOI] [PubMed] [Google Scholar]
- 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]
- Zhang W., Young A. C., Imarai M., Nathenson S. G., Sacchettini J. C. Crystal structure of the major histocompatibility complex class I H-2Kb molecule containing a single viral peptide: implications for peptide binding and T-cell receptor recognition. Proc Natl Acad Sci U S A. 1992 Sep 1;89(17):8403–8407. doi: 10.1073/pnas.89.17.8403. [DOI] [PMC free article] [PubMed] [Google Scholar]