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. 1989 Apr 1;108(4):1317–1329. doi: 10.1083/jcb.108.4.1317

Endocytosis of the class I major histocompatibility antigen via a phorbol myristate acetate-inducible pathway is a cell-specific phenomenon and requires the cytoplasmic domain [published erratum appears in J Cell Biol 1989 Sep;109(3):1381]

PMCID: PMC2115514  PMID: 2925787

Abstract

Class I major histocompatibility (MHC) antigens are expressed by virtually all mammalian cells, yet their levels of expression and behavior on the cell surface vary in a cell-specific fashion. A panel of lymphoid (both B and T) and nonlymphoid cell lines was used to study the kinetics of internalization of the H-2Ld class I MHC in different cell types. These studies revealed that endocytosis of H-2Ld occurs by both constitutive and PMA-regulated pathways in lymphoid cells, but only by a PMA-refractory pathway in the nonlymphoid cells tested. Transfectant derivatives of the T lymphoma, EL4, which express wild- type or mutant H-2Ld class I MHC antigens, were used to investigate the requirement for the cytoplasmic domain of the class I MHC antigen for its endocytosis in T lymphocytes. These studies showed that modification or deletion of the cytoplasmic domain of H-2Ld abrogates endocytosis via a PMA-regulated pathway. The role of cytoplasmic domain phosphorylation in PMA-inducible endocytosis was examined. The wild- type H-2Ld antigen is phosphorylated in all cell types examined, and this phosphorylation is up-regulated by PMA treatment. In contrast, cytoplasmic domain mutants of H-2Ld fail to be phosphorylated in vivo, in the presence or absence of PMA. The universality of PMA-inducible hyperphosphorylation of the class I MHC antigen among diverse cell types leads us to conclude that phosphorylation of the cytoplasmic domain, while perhaps necessary, is not sufficient for triggering endocytosis via a PMA-inducible pathway. Furthermore, the results with the cytoplasmic domain mutants of H-2Ld suggest that a structural conformation of the class I MHC cytoplasmic domain is required for endocytosis via this route.

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Selected References

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  1. Aragnol D., Malissen B., Schiff C., Piron M. A., Leserman L. D. Endocytosis of MHC molecules by B cell-B lymphoma and B cell-T lymphoma hybrids. J Immunol. 1986 Nov 15;137(10):3347–3353. [PubMed] [Google Scholar]
  2. Beguinot L., Hanover J. A., Ito S., Richert N. D., Willingham M. C., Pastan I. Phorbol esters induce transient internalization without degradation of unoccupied epidermal growth factor receptors. Proc Natl Acad Sci U S A. 1985 May;82(9):2774–2778. doi: 10.1073/pnas.82.9.2774. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Berridge M. J., Irvine R. F. Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature. 1984 Nov 22;312(5992):315–321. doi: 10.1038/312315a0. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. 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]
  6. 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]
  7. Buys S. S., Keogh E. A., Kaplan J. Fusion of intracellular membrane pools with cell surfaces of macrophages stimulated by phorbol esters and calcium ionophores. Cell. 1984 Sep;38(2):569–576. doi: 10.1016/0092-8674(84)90511-7. [DOI] [PubMed] [Google Scholar]
  8. Castagna M., Takai Y., Kaibuchi K., Sano K., Kikkawa U., Nishizuka Y. Direct activation of calcium-activated, phospholipid-dependent protein kinase by tumor-promoting phorbol esters. J Biol Chem. 1982 Jul 10;257(13):7847–7851. [PubMed] [Google Scholar]
  9. Coggeshall K. M., Cambier J. C. B cell activation. VIII. Membrane immunoglobulins transduce signals via activation of phosphatidylinositol hydrolysis. J Immunol. 1984 Dec;133(6):3382–3386. [PubMed] [Google Scholar]
  10. Dasgupta J. D., Cemach K., Dubey D. P., Yunis E. J., Amos D. B. The role of class I histocompatibility antigens in the regulation of T-cell activation. Proc Natl Acad Sci U S A. 1987 Feb;84(4):1094–1098. doi: 10.1073/pnas.84.4.1094. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dasgupta J. D., Watkins S., Slayter H., Yunis E. J. Receptor-like nature of class I HLA: endocytosis via coated pits. J Immunol. 1988 Oct 15;141(8):2577–2580. [PubMed] [Google Scholar]
  12. Davis C. G., Lehrman M. A., Russell D. W., Anderson R. G., Brown M. S., Goldstein J. L. The J.D. mutation in familial hypercholesterolemia: amino acid substitution in cytoplasmic domain impedes internalization of LDL receptors. Cell. 1986 Apr 11;45(1):15–24. doi: 10.1016/0092-8674(86)90533-7. [DOI] [PubMed] [Google Scholar]
  13. Davis C. G., van Driel I. R., Russell D. W., Brown M. S., Goldstein J. L. The low density lipoprotein receptor. Identification of amino acids in cytoplasmic domain required for rapid endocytosis. J Biol Chem. 1987 Mar 25;262(9):4075–4082. [PubMed] [Google Scholar]
  14. Davis R. J., Czech M. P. Tumor-promoting phorbol diesters mediate phosphorylation of the epidermal growth factor receptor. J Biol Chem. 1984 Jul 10;259(13):8545–8549. [PubMed] [Google Scholar]
  15. De Felice M., Turco M. C., Giarrusso P. C., Corbo L., Pizzano R., Martinelli V., Ferrone S., Venuta S. Differential regulatory role of monomorphic and polymorphic determinants of histocompatibility leukocyte antigen class I antigens in monoclonal antibody OKT3-induced T cell proliferation. J Immunol. 1987 Oct 15;139(8):2683–2689. [PubMed] [Google Scholar]
  16. Dobberstein B., Garoff H., Warren G., Robinson P. J. Cell-free synthesis and membrane insertion of mouse H-2Dd histocompatibility antigen and beta 2-microglobulin. Cell. 1979 Aug;17(4):759–769. doi: 10.1016/0092-8674(79)90316-7. [DOI] [PubMed] [Google Scholar]
  17. Edidin M., Zuniga M. Lateral diffusion of wild-type and mutant Ld antigens in L cells. J Cell Biol. 1984 Dec;99(6):2333–2335. doi: 10.1083/jcb.99.6.2333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Evans G. A., Margulies D. H., Shykind B., Seidman J. G., Ozato K. Exon shuffling: mapping polymorphic determinants on hybrid mouse transplantation antigens. Nature. 1982 Dec 23;300(5894):755–757. doi: 10.1038/300755a0. [DOI] [PubMed] [Google Scholar]
  19. Farrar W. L., Ruscetti F. W. Association of protein kinase C activation with IL 2 receptor expression. J Immunol. 1986 Feb 15;136(4):1266–1273. [PubMed] [Google Scholar]
  20. Germain R. N. Antigen processing and CD4+ T cell depletion in AIDS. Cell. 1988 Aug 12;54(4):441–444. doi: 10.1016/0092-8674(88)90062-1. [DOI] [PubMed] [Google Scholar]
  21. Germain R. N. Immunology. The ins and outs of antigen processing and presentation. Nature. 1986 Aug 21;322(6081):687–689. doi: 10.1038/322687a0. [DOI] [PubMed] [Google Scholar]
  22. Goldstein J. L., Brown M. S., Anderson R. G., Russell D. W., Schneider W. J. Receptor-mediated endocytosis: concepts emerging from the LDL receptor system. Annu Rev Cell Biol. 1985;1:1–39. doi: 10.1146/annurev.cb.01.110185.000245. [DOI] [PubMed] [Google Scholar]
  23. Guild B. C., Strominger J. L. Human and murine class I MHC antigens share conserved serine 335, the site of HLA phosphorylation in vivo. J Biol Chem. 1984 Jul 25;259(14):9235–9240. [PubMed] [Google Scholar]
  24. Huet C., Ash J. F., Singer S. J. The antibody-induced clustering and endocytosis of HLA antigens on cultured human fibroblasts. Cell. 1980 Sep;21(2):429–438. doi: 10.1016/0092-8674(80)90479-1. [DOI] [PubMed] [Google Scholar]
  25. Huet S., Boumsell L., Raynal B., Degos L., Dausset J., Bernard A. Role in T-cell activation for HLA class I molecules from accessory cells: further distinction between activation signals delivered to T cells via CD2 and CD3 molecules. Proc Natl Acad Sci U S A. 1987 Oct;84(20):7222–7226. doi: 10.1073/pnas.84.20.7222. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hunter T., Ling N., Cooper J. A. Protein kinase C phosphorylation of the EGF receptor at a threonine residue close to the cytoplasmic face of the plasma membrane. Nature. 1984 Oct 4;311(5985):480–483. doi: 10.1038/311480a0. [DOI] [PubMed] [Google Scholar]
  27. Iacopetta B. J., Rothenberger S., Kühn L. C. A role for the cytoplasmic domain in transferrin receptor sorting and coated pit formation during endocytosis. Cell. 1988 Aug 12;54(4):485–489. doi: 10.1016/0092-8674(88)90069-4. [DOI] [PubMed] [Google Scholar]
  28. Imboden J. B., Stobo J. D. Transmembrane signalling by the T cell antigen receptor. Perturbation of the T3-antigen receptor complex generates inositol phosphates and releases calcium ions from intracellular stores. J Exp Med. 1985 Mar 1;161(3):446–456. doi: 10.1084/jem.161.3.446. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Klausner R. D., Harford J., van Renswoude J. Rapid internalization of the transferrin receptor in K562 cells is triggered by ligand binding or treatment with a phorbol ester. Proc Natl Acad Sci U S A. 1984 May;81(10):3005–3009. doi: 10.1073/pnas.81.10.3005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Krangel M. S., Orr H. T., Strominger J. L. Assembly and maturation of HLA-A and HLA-B antigens in vivo. Cell. 1979 Dec;18(4):979–991. doi: 10.1016/0092-8674(79)90210-1. [DOI] [PubMed] [Google Scholar]
  31. Lazarovits J., Roth M. A single amino acid change in the cytoplasmic domain allows the influenza virus hemagglutinin to be endocytosed through coated pits. Cell. 1988 Jun 3;53(5):743–752. doi: 10.1016/0092-8674(88)90092-x. [DOI] [PubMed] [Google Scholar]
  32. Lehrman M. A., Goldstein J. L., Brown M. S., Russell D. W., Schneider W. J. Internalization-defective LDL receptors produced by genes with nonsense and frameshift mutations that truncate the cytoplasmic domain. Cell. 1985 Jul;41(3):735–743. doi: 10.1016/s0092-8674(85)80054-4. [DOI] [PubMed] [Google Scholar]
  33. Machy P., Barbet J., Leserman L. D. Differential endocytosis of T and B lymphocyte surface molecules evaluated with antibody-bearing fluorescent liposomes containing methotrexate. Proc Natl Acad Sci U S A. 1982 Jul;79(13):4148–4152. doi: 10.1073/pnas.79.13.4148. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Machy P., Pierres M., Barbet J., Leserman L. D. Drug transfer into lymphoblasts mediated by liposomes bound to distinct sites on H-2 encoded I-A, I-E, and K molecules. J Immunol. 1982 Nov;129(5):2098–2102. [PubMed] [Google Scholar]
  35. Machy P., Truneh A., Gennaro D., Hoffstein S. Major histocompatibility complex class I molecules internalized via coated pits in T lymphocytes. Nature. 1987 Aug 20;328(6132):724–726. doi: 10.1038/328724a0. [DOI] [PubMed] [Google Scholar]
  36. Makowske M., Ballester R., Cayre Y., Rosen O. M. Immunochemical evidence that three protein kinase C isozymes increase in abundance during HL-60 differentiation induced by dimethyl sulfoxide and retinoic acid. J Biol Chem. 1988 Mar 5;263(7):3402–3410. [PubMed] [Google Scholar]
  37. May W. S., Jacobs S., Cuatrecasas P. Association of phorbol ester-induced hyperphosphorylation and reversible regulation of transferrin membrane receptors in HL60 cells. Proc Natl Acad Sci U S A. 1984 Apr;81(7):2016–2020. doi: 10.1073/pnas.81.7.2016. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. May W. S., Sahyoun N., Jacobs S., Wolf M., Cuatrecasas P. Mechanism of phorbol diester-induced regulation of surface transferrin receptor involves the action of activated protein kinase C and an intact cytoskeleton. J Biol Chem. 1985 Aug 5;260(16):9419–9426. [PubMed] [Google Scholar]
  39. McCluskey J., Boyd L. F., Maloy W. L., Coligan J. E., Margulies D. H. Alternative processing of H-2Dd pre-mRNAs results in membrane expression of differentially phosphorylated protein products. EMBO J. 1986 Oct;5(10):2477–2483. doi: 10.1002/j.1460-2075.1986.tb04524.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. McGraw T. E., Dunn K. W., Maxfield F. R. Phorbol ester treatment increases the exocytic rate of the transferrin receptor recycling pathway independent of serine-24 phosphorylation. J Cell Biol. 1988 Apr;106(4):1061–1066. doi: 10.1083/jcb.106.4.1061. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. 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]
  42. Morrison L. A., Lukacher A. E., Braciale V. L., Fan D. P., Braciale T. J. Differences in antigen presentation to MHC class I-and class II-restricted influenza virus-specific cytolytic T lymphocyte clones. J Exp Med. 1986 Apr 1;163(4):903–921. doi: 10.1084/jem.163.4.903. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Mostov K. E., de Bruyn Kops A., Deitcher D. L. Deletion of the cytoplasmic domain of the polymeric immunoglobulin receptor prevents basolateral localization and endocytosis. Cell. 1986 Nov 7;47(3):359–364. doi: 10.1016/0092-8674(86)90592-1. [DOI] [PubMed] [Google Scholar]
  44. Nishizuka Y. The molecular heterogeneity of protein kinase C and its implications for cellular regulation. Nature. 1988 Aug 25;334(6184):661–665. doi: 10.1038/334661a0. [DOI] [PubMed] [Google Scholar]
  45. Nishizuka Y. The role of protein kinase C in cell surface signal transduction and tumour promotion. Nature. 1984 Apr 19;308(5961):693–698. doi: 10.1038/308693a0. [DOI] [PubMed] [Google Scholar]
  46. Olefsky J. M., Kao M. Surface binding and rates of internalization of 125I-insulin in adipocytes and IM-9 lymphocytes. J Biol Chem. 1982 Aug 10;257(15):8667–8673. [PubMed] [Google Scholar]
  47. Owen M. J., Kissonerghis A. M., Lodish H. F. Biosynthesis of HLA-A and HLA-B antigens in vivo. J Biol Chem. 1980 Oct 25;255(20):9678–9684. [PubMed] [Google Scholar]
  48. Ozato K., Hansen T. H., Sachs D. H. Monoclonal antibodies to mouse MHC antigens. II. Antibodies to the H-2Ld antigen, the products of a third polymorphic locus of the mouse major histocompatibility complex. J Immunol. 1980 Dec;125(6):2473–2477. [PubMed] [Google Scholar]
  49. Pober J. S., Guild B. C., Strominger J. L. Phosphorylation in vivo and in vitro of human histocompatibility antigens (HLA-A and HLA-B) in the carboxy-terminal intracellular domain. Proc Natl Acad Sci U S A. 1978 Dec;75(12):6002–6006. doi: 10.1073/pnas.75.12.6002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Pober J. S., Guild B. C., Strominger J. L., Veatch W. R. Purification of HLA-A2 antigen, fluorescent labeling of its intracellular region, and demonstration of an interaction between fluorescently labeled HLA-A2 antigen and lymphoblastoid cell cytoskeleton proteins in vitro. Biochemistry. 1981 Sep 15;20(19):5625–5633. doi: 10.1021/bi00522a042. [DOI] [PubMed] [Google Scholar]
  51. Prywes R., Livneh E., Ullrich A., Schlessinger J. Mutations in the cytoplasmic domain of EGF receptor affect EGF binding and receptor internalization. EMBO J. 1986 Sep;5(9):2179–2190. doi: 10.1002/j.1460-2075.1986.tb04482.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Rothenberger S., Iacopetta B. J., Kühn L. C. Endocytosis of the transferrin receptor requires the cytoplasmic domain but not its phosphorylation site. Cell. 1987 May 8;49(3):423–431. doi: 10.1016/0092-8674(87)90295-9. [DOI] [PubMed] [Google Scholar]
  53. Rozengurt E., Rodriguez-Pena A., Coombs M., Sinnett-Smith J. Diacylglycerol stimulates DNA synthesis and cell division in mouse 3T3 cells: role of Ca2+-sensitive phospholipid-dependent protein kinase. Proc Natl Acad Sci U S A. 1984 Sep;81(18):5748–5752. doi: 10.1073/pnas.81.18.5748. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Samson M., Cousin J. L., Fehlmann M. Cross-linking of insulin receptors to MHC antigens in human B lymphocytes: evidence for selective molecular interactions. J Immunol. 1986 Oct 1;137(7):2293–2298. [PubMed] [Google Scholar]
  55. Sandri-Goldin R. M., Goldin A. L., Levine M., Glorioso J. C. High-frequency transfer of cloned herpes simplex virus type 1 sequences to mammalian cells by protoplast fusion. Mol Cell Biol. 1981 Aug;1(8):743–752. doi: 10.1128/mcb.1.8.743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Sege K., Rask L., Peterson P. A. Role of beta2-microglobulin in the intracellular processing of HLA antigens. Biochemistry. 1981 Aug 4;20(16):4523–4530. doi: 10.1021/bi00519a003. [DOI] [PubMed] [Google Scholar]
  57. Sterkers G., Henin Y., Kalil J., Bagot M., Levy J. P. Influence of HLA class I- and class II-specific monoclonal antibodies on DR-restricted lymphoproliferative responses. I. Unseparated populations of effector cells. J Immunol. 1983 Dec;131(6):2735–2740. [PubMed] [Google Scholar]
  58. Taylor D. S., Nowell P. C., Kornbluth J. Anti-HLA class I antibodies inhibit the T cell-independent proliferation of human B lymphocytes. J Immunol. 1987 Sep 15;139(6):1792–1796. [PubMed] [Google Scholar]
  59. Taylor D. S., Nowell P. C., Kornbluth J. Functional role of HLA class I cell-surface molecules in human T-lymphocyte activation and proliferation. Proc Natl Acad Sci U S A. 1986 Jun;83(12):4446–4450. doi: 10.1073/pnas.83.12.4446. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. 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]
  61. Truneh A., Mishal Z., Barbet J., Machy P., Leserman L. D. Endocytosis of liposomes bound to cell surface proteins measured by flow cytofluorometry. Biochem J. 1983 Jul 15;214(1):189–194. doi: 10.1042/bj2140189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Tse D. B., Pernis B. Spontaneous internalization of Class I major histocompatibility complex molecules in T lymphoid cells. J Exp Med. 1984 Jan 1;159(1):193–207. doi: 10.1084/jem.159.1.193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Turco M. C., De Felice M., Corbo L., Morrone G., Mertelsmann R., Ferrone S., Venuta S. Regulatory role of a monomorphic determinant of HLA Class I antigens in T cell proliferation. J Immunol. 1985 Oct;135(4):2268–2273. [PubMed] [Google Scholar]
  64. Turco M. C., de Felice M., Corbo L., Giarrusso P. C., Yang S. Y., Ferrone S., Venuta S. Enhancing effect of anti-HLA class I monoclonal antibodies on T cell proliferation induced via CD2 molecule. J Immunol. 1988 Oct 1;141(7):2275–2281. [PubMed] [Google Scholar]
  65. Unanue E. R. Antigen-presenting function of the macrophage. Annu Rev Immunol. 1984;2:395–428. doi: 10.1146/annurev.iy.02.040184.002143. [DOI] [PubMed] [Google Scholar]
  66. Veillette A., Bookman M. A., Horak E. M., Bolen J. B. The CD4 and CD8 T cell surface antigens are associated with the internal membrane tyrosine-protein kinase p56lck. Cell. 1988 Oct 21;55(2):301–308. doi: 10.1016/0092-8674(88)90053-0. [DOI] [PubMed] [Google Scholar]
  67. Veillette A., Horak I. D., Bolen J. B. Post-translational alterations of the tyrosine kinase p56lck in response to activators of protein kinase C. Oncogene Res. 1988 May;2(4):385–401. [PubMed] [Google Scholar]
  68. Yewdell J. W., Bennink J. R., Hosaka Y. Cells process exogenous proteins for recognition by cytotoxic T lymphocytes. Science. 1988 Feb 5;239(4840):637–640. doi: 10.1126/science.3257585. [DOI] [PubMed] [Google Scholar]
  69. Zerial M., Suomalainen M., Zanetti-Schneider M., Schneider C., Garoff H. Phosphorylation of the human transferrin receptor by protein kinase C is not required for endocytosis and recycling in mouse 3T3 cells. EMBO J. 1987 Sep;6(9):2661–2667. doi: 10.1002/j.1460-2075.1987.tb02557.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Zinkernagel R. M., Doherty P. C. MHC-restricted cytotoxic T cells: studies on the biological role of polymorphic major transplantation antigens determining T-cell restriction-specificity, function, and responsiveness. Adv Immunol. 1979;27:51–177. doi: 10.1016/s0065-2776(08)60262-x. [DOI] [PubMed] [Google Scholar]
  71. Zuniga M. C., Hood L. E. Clonal variation in cell surface display of an H-2 protein lacking a cytoplasmic tail. J Cell Biol. 1986 Jan;102(1):1–10. doi: 10.1083/jcb.102.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Zuniga M. C., Malissen B., McMillan M., Brayton P. R., Clark S. S., Forman J., Hood L. Expression and function of transplantation antigens with altered or deleted cytoplasmic domains. Cell. 1983 Sep;34(2):535–544. doi: 10.1016/0092-8674(83)90386-0. [DOI] [PubMed] [Google Scholar]

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