1932

Abstract

Butyrophilin molecules (commonly contracted to BTN), collectively take their name from the eponymous protein in cow's milk. They are considered to be members of the B7 family of costimulatory receptors, which includes B7.1 (CD80), B7.2 (CD86), and related molecules, such as PD-L1 (B7-H1, CD274), ICOS-L (CD275), and B7-H3 (CD276). These coreceptors modulate T cell responses upon antigen presentation by major histocompatibility complex and cognate αβ T cell receptor engagement. Molecules such as BTN3A1 (CD277), myelin oligodendrocyte glycoprotein, and mouse Skint1 and Btnl2, all members of the butyrophilin family, show greater structural and functional diversity than the canonical B7 receptors. Some butyrophilins mediate complex interactions between antigen-presenting cells and conventional αβ T cells, and others regulate the immune responses of specific γδ T cell subsets by mechanisms that have characteristics of both innate and adaptive immunity.

Keyword(s): B30.2BTN1ABTN2ABTN3APRYSPRY
Loading

Article metrics loading...

/content/journals/10.1146/annurev-immunol-041015-055435
2016-05-20
2024-04-17
Loading full text...

Full text loading...

/deliver/fulltext/immunol/34/1/annurev-immunol-041015-055435.html?itemId=/content/journals/10.1146/annurev-immunol-041015-055435&mimeType=html&fmt=ahah

Literature Cited

  1. Sharma P, Allison JP. 1.  2015. Immune checkpoint targeting in cancer therapy: toward combination strategies with curative potential. Cell 161:205–14 [Google Scholar]
  2. Quezada SA, Peggs KS, Simpson TR, Allison JP. 2.  2011. Shifting the equilibrium in cancer immunoediting: from tumor tolerance to eradication. Immunol. Rev. 241:104–18 [Google Scholar]
  3. Podojil JR, Miller SD. 3.  2013. Targeting the B7 family of co-stimulatory molecules: successes and challenges. BioDrugs 27:1–13 [Google Scholar]
  4. Sharma P, Allison JP. 4.  2015. The future of immune checkpoint therapy. Science 348:56–61 [Google Scholar]
  5. Arnett HA, Escobar SS, Viney JL. 5.  2009. Regulation of costimulation in the era of butyrophilins. Cytokine 46:370–75 [Google Scholar]
  6. Abeler-Dorner L, Swamy M, Williams G, Hayday AC, Bas A. 6.  2012. Butyrophilins: an emerging family of immune regulators. Trends Immunol. 33:34–41 [Google Scholar]
  7. Afrache H, Gouret P, Ainouche S, Pontarotti P, Olive D. 7.  2012. The butyrophilin (BTN) gene family: from milk fat to the regulation of the immune response. Immunogenetics 64:781–94 [Google Scholar]
  8. Arnett HA, Viney JL. 8.  2014. Immune modulation by butyrophilins. Nat. Rev. Immunol. 14:559–69 [Google Scholar]
  9. Henry J, Miller MM, Pontarotti P. 9.  1999. Structure and evolution of the extended B7 family. Immunol. Today 20:285–88 [Google Scholar]
  10. Rhodes DA, Stammers M, Malcherek G, Beck S, Trowsdale J. 10.  2001. The cluster of BTN genes in the extended major histocompatibility complex. Genomics 71:351–62 [Google Scholar]
  11. Compte E, Pontarotti P, Collette Y, Lopez M, Olive D. 11.  2004. Frontline: characterization of BT3 molecules belonging to the B7 family expressed on immune cells. Eur. J. Immunol. 34:2089–99 [Google Scholar]
  12. Arnett HA, Escobar SS, Gonzalez-Suarez E, Budelsky AL, Steffen LA. 12.  et al. 2007. BTNL2, a butyrophilin/B7-like molecule, is a negative costimulatory molecule modulated in intestinal inflammation. J. Immunol. 178:1523–33 [Google Scholar]
  13. Smith IA, Knezevic BR, Ammann JU, Rhodes DA, Aw D. 13.  et al. 2010. BTN1A1, the mammary gland butyrophilin, and BTN2A2 are both inhibitors of T cell activation. J. Immunol. 184:3514–25 [Google Scholar]
  14. Swanson RM, Gavin MA, Escobar SS, Rottman JB, Lipsky BP. 14.  et al. 2013. Butyrophilin-like 2 modulates B7 costimulation to induce Foxp3 expression and regulatory T cell development in mature T cells. J. Immunol. 190:2027–35 [Google Scholar]
  15. Vantourout P, Hayday A. 15.  2013. Six-of-the-best: unique contributions of γδ T cells to immunology. Nat. Rev. Immunol. 13:88–100 [Google Scholar]
  16. Bonneville M, O’Brien RL, Born WK. 16.  2010. γδ T cell effector functions: a blend of innate programming and acquired plasticity. Nat. Rev. Immunol. 10:467–78 [Google Scholar]
  17. Hayday AC. 17.  2009. γδ T cells and the lymphoid stress-surveillance response. Immunity 31:184–96 [Google Scholar]
  18. Chien YH, Meyer C, Bonneville M. 18.  2014. γδ T cells: first line of defense and beyond. Annu. Rev. Immunol. 32:121–55 [Google Scholar]
  19. Pennington DJ, Silva-Santos B, Hayday AC. 19.  2005. γδ T cell development—having the strength to get there. Curr. Opin. Immunol. 17:108–15 [Google Scholar]
  20. Ribot JC, Debarros A, Silva-Santos B. 20.  2011. Searching for “signal 2”: costimulation requirements of γδ T cells. Cell Mol. Life Sci. 68:2345–55 [Google Scholar]
  21. Ribot JC, Debarros A, Mancio-Silva L, Pamplona A, Silva-Santos B. 21.  2012. B7-CD28 costimulatory signals control the survival and proliferation of murine and human γδ T cells via IL-2 production. J. Immunol. 189:1202–8 [Google Scholar]
  22. Boyden LM, Lewis JM, Barbee SD, Bas A, Girardi M. 22.  et al. 2008. Skint1, the prototype of a newly identified immunoglobulin superfamily gene cluster, positively selects epidermal γδ T cells. Nat. Genet. 40:656–62 [Google Scholar]
  23. Harly C, Guillaume Y, Nedellec S, Peigne CM, Monkkonen H. 23.  et al. 2012. Key implication of CD277/butyrophilin-3 (BTN3A) in cellular stress sensing by a major human γδ T-cell subset. Blood 120:2269–79 [Google Scholar]
  24. Ruddy DA, Kronmal GS, Lee VK, Mintier GA, Quintana L. 24.  et al. 1997. A 1.1-Mb transcript map of the hereditary hemochromatosis locus. Genome Res. 7:441–56 [Google Scholar]
  25. Tazi-Ahnini R, Henry J, Offer C, Bouissou-Bouchouata C, Mather IH, Pontarotti P. 25.  1997. Cloning, localization, and structure of new members of the butyrophilin gene family in the juxta-telomeric region of the major histocompatibility complex. Immunogenetics 47:55–63 [Google Scholar]
  26. Henry J, Ribouchon M, Depetris D, Mattei M, Offer C. 26.  et al. 1997. Cloning, structural analysis, and mapping of the B30 and B7 multigenic families to the major histocompatibility complex (MHC) and other chromosomal regions. Immunogenetics 46:383–95 [Google Scholar]
  27. Viken MK, Blomhoff A, Olsson M, Akselsen HE, Pociot F. 27.  et al. 2009. Reproducible association with type 1 diabetes in the extended class I region of the major histocompatibility complex. Genes Immun. 10:323–33 [Google Scholar]
  28. Valentonyte R, Hampe J, Huse K, Rosenstiel P, Albrecht M. 28.  et al. 2005. Sarcoidosis is associated with a truncating splice site mutation in BTNL2. Nat. Genet. 37:357–64 [Google Scholar]
  29. Pathan S, Gowdy RE, Cooney R, Beckly JB, Hancock L. 29.  et al. 2009. Confirmation of the novel association at the BTNL2 locus with ulcerative colitis. Tissue Antigens 74:322–29 [Google Scholar]
  30. Prescott NJ, Lehne B, Stone K, Lee JC, Taylor K. 30.  et al. 2015. Pooled sequencing of 531 genes in inflammatory bowel disease identifies an associated rare variant in BTNL2 and implicates other immune related genes. PLOS Genet. 11:e1004955 [Google Scholar]
  31. Orozco G, Eerligh P, Sanchez E, Zhernakova S, Roep BO. 31.  et al. 2005. Analysis of a functional BTNL2 polymorphism in type 1 diabetes, rheumatoid arthritis, and systemic lupus erythematosus. Hum. Immunol. 66:1235–41 [Google Scholar]
  32. Traherne JA, Barcellos LF, Sawcer SJ, Compston A, Ramsay PP. 32.  et al. 2006. Association of the truncating splice site mutation in BTNL2 with multiple sclerosis is secondary to HLA-DRB1*15. Hum. Mol. Genet. 15:155–61 [Google Scholar]
  33. Schwartz JC, Zhang X, Fedorov AA, Nathenson SG, Almo SC. 33.  2001. Structural basis for co-stimulation by the human CTLA-4/B7-2 complex. Nature 410:604–8 [Google Scholar]
  34. Stamper CC, Zhang Y, Tobin JF, Erbe DV, Ikemizu S. 34.  et al. 2001. Crystal structure of the B7-1/CTLA-4 complex that inhibits human immune responses. Nature 410:608–11 [Google Scholar]
  35. Rhodes DA, de Bono B, Trowsdale J. 35.  2005. Relationship between SPRY and B30.2 protein domains. Evolution of a component of immune defence?. Immunology 116:411–17 [Google Scholar]
  36. Stremlau M, Owens CM, Perron MJ, Kiessling M, Autissier P, Sodroski J. 36.  2004. The cytoplasmic body component TRIM5α restricts HIV-1 infection in Old World monkeys. Nature 427:848–53 [Google Scholar]
  37. James LC, Keeble AH, Khan Z, Rhodes DA, Trowsdale J. 37.  2007. Structural basis for PRYSPRY-mediated tripartite motif (TRIM) protein function. PNAS 104:6200–5 [Google Scholar]
  38. Xu H, Yang J, Gao W, Li L, Li P. 38.  et al. 2014. Innate immune sensing of bacterial modifications of Rho GTPases by the Pyrin inflammasome. Nature 513:237–41 [Google Scholar]
  39. de Zoete MR, Flavell RA. 39.  2014. Detecting “different”: Pyrin senses modified GTPases. Cell Res. 24:1286–87 [Google Scholar]
  40. Caruso R, Warner N, Inohara N, Nunez G. 40.  2014. NOD1 and NOD2: signaling, host defense, and inflammatory disease. Immunity 41:898–908 [Google Scholar]
  41. Reymond A, Meroni G, Fantozzi A, Merla G, Cairo S. 41.  et al. 2001. The tripartite motif family identifies cell compartments. EMBO J. 20:2140–51 [Google Scholar]
  42. Nisole S, Stoye JP, Saib A. 42.  2005. TRIM family proteins: retroviral restriction and antiviral defence. Nat. Rev. Microbiol. 3:799–808 [Google Scholar]
  43. Ozato K, Shin DM, Chang TH, Morse HC 3rd. 43.  2008. TRIM family proteins and their emerging roles in innate immunity. Nat. Rev. Immunol. 8:849–60 [Google Scholar]
  44. Rhodes DA, Trowsdale J. 44.  2007. TRIM21 is a trimeric protein that binds IgG Fc via the B30.2 domain. Mol. Immunol. 44:2406–14 [Google Scholar]
  45. McEwan WA, Mallery DL, Rhodes DA, Trowsdale J, James LC. 45.  2011. Intracellular antibody-mediated immunity and the role of TRIM21. BioEssays 33:803–9 [Google Scholar]
  46. McEwan WA, Tam JC, Watkinson RE, Bidgood SR, Mallery DL, James LC. 46.  2013. Intracellular antibody-bound pathogens stimulate immune signaling via the Fc receptor TRIM21. Nat. Immunol. 14:327–36 [Google Scholar]
  47. Uchil PD, Hinz A, Siegel S, Coenen-Stass A, Pertel T. 47.  et al. 2013. TRIM protein-mediated regulation of inflammatory and innate immune signaling and its association with antiretroviral activity. J. Virol. 87:257–72 [Google Scholar]
  48. Pertel T, Hausmann S, Morger D, Zuger S, Guerra J. 48.  et al. 2011. TRIM5 is an innate immune sensor for the retrovirus capsid lattice. Nature 472:361–65 [Google Scholar]
  49. Nguyen T, Liu XK, Zhang Y, Dong C. 49.  2006. BTNL2, a butyrophilin-like molecule that functions to inhibit T cell activation. J. Immunol. 176:7354–60 [Google Scholar]
  50. Ammann JU, Cooke A, Trowsdale J. 50.  2013. Butyrophilin Btn2a2 inhibits TCR activation and phosphatidylinositol 3-kinase/Akt pathway signaling and induces Foxp3 expression in T lymphocytes. J. Immunol. 190:5030–6 [Google Scholar]
  51. Sarter K, Leimgruber E, Gobet F, Agrawal V, Dunand-Sauthier I. 51.  et al. 2016. Btn2a2, a T-cell immunomodulatory molecule coregulated with MHC class II genes. J. Exp. Med 213:177–87 [Google Scholar]
  52. Malcherek G, Mayr L, Roda-Navarro P, Rhodes D, Miller N, Trowsdale J. 52.  2007. The B7 homolog butyrophilin BTN2A1 is a novel ligand for DC-SIGN. J. Immunol. 179:3804–11 [Google Scholar]
  53. Reith W, LeibundGut-Landmann S, Waldburger JM. 53.  2005. Regulation of MHC class II gene expression by the class II transactivator. Nat. Rev. Immunol. 5:793–806 [Google Scholar]
  54. Cubillos-Ruiz JR, Martinez D, Scarlett UK, Rutkowski MR, Nesbeth YC. 54.  et al. 2010. CD277 is a negative co-stimulatory molecule universally expressed by ovarian cancer microenvironmental cells. Oncotarget 1:329–38 [Google Scholar]
  55. Le Page C, Marineau A, Bonza PK, Rahimi K, Cyr L. 55.  et al. 2012. BTN3A2 expression in epithelial ovarian cancer is associated with higher tumor infiltrating T cells and a better prognosis. PLOS ONE 7:e38541 [Google Scholar]
  56. Bas A, Swamy M, Abeler-Dorner L, Williams G, Pang DJ. 56.  et al. 2011. Butyrophilin-like 1 encodes an enterocyte protein that selectively regulates functional interactions with T lymphocytes. PNAS 108:4376–81 [Google Scholar]
  57. Yamazaki T, Goya I, Graf D, Craig S, Martin-Orozco N, Dong C. 57.  2010. A butyrophilin family member critically inhibits T cell activation. J. Immunol. 185:5907–14 [Google Scholar]
  58. Chapoval AI, Smithson G, Brunick L, Mesri M, Boldog FL. 58.  et al. 2013. BTNL8, a butyrophilin-like molecule that costimulates the primary immune response. Mol. Immunol. 56:819–28 [Google Scholar]
  59. Lewis JM, Girardi M, Roberts SJ, Barbee SD, Hayday AC, Tigelaar RE. 59.  2006. Selection of the cutaneous intraepithelial γδ+ T cell repertoire by a thymic stromal determinant. Nat. Immunol. 7:843–50 [Google Scholar]
  60. Barbee SD, Woodward MJ, Turchinovich G, Mention JJ, Lewis JM. 60.  et al. 2011. Skint-1 is a highly specific, unique selecting component for epidermal T cells. PNAS 108:3330–35 [Google Scholar]
  61. Turchinovich G, Hayday AC. 61.  2011. Skint-1 identifies a common molecular mechanism for the development of interferon-γ-secreting versus interleukin-17-secreting γδ T cells. Immunity 35:59–68 [Google Scholar]
  62. Bonneville M. 62.  2006. Selection of intraepithelial γδ cells: the Holy GrIEL at last?. Nat. Immunol. 7:791–92 [Google Scholar]
  63. Tanaka Y, Sano S, Nieves E, De Libero G, Rosa D. 63.  et al. 1994. Nonpeptide ligands for human γδ T cells. PNAS 91:8175–79 [Google Scholar]
  64. Sandstrom A, Peigne CM, Leger A, Crooks JE, Konczak F. 64.  et al. 2014. The intracellular B30.2 domain of butyrophilin 3a1 binds phosphoantigens to mediate activation of human Vγ9Vδ2 T cells. Immunity 40:490–500 [Google Scholar]
  65. Hsiao CH, Lin X, Barney RJ, Shippy RR, Li J. 65.  et al. 2014. Synthesis of a phosphoantigen prodrug that potently activates Vγ9Vδ2 T-lymphocytes. Chem. Biol. 21:945–54 [Google Scholar]
  66. Rhodes DA, Chen HC, Price AJ, Keeble AH, Davey MS. 66.  et al. 2015. Activation of human γδ T cells by cytosolic interactions of BTN3A1 with soluble phosphoantigens and the cytoskeletal adaptor periplakin. J. Immunol. 194:2390–98 [Google Scholar]
  67. Vavassori S, Kumar A, Wan GS, Ramanjaneyulu GS, Cavallari M. 67.  et al. 2013. Butyrophilin 3A1 binds phosphorylated antigens and stimulates human γδ T cells. Nat. Immunol. 14:908–16 [Google Scholar]
  68. Gober HJ, Kistowska M, Angman L, Jeno P, Mori L, De Libero G. 68.  2003. Human T cell receptor γδ cells recognize endogenous mevalonate metabolites in tumor cells. J. Exp. Med. 197:163–68 [Google Scholar]
  69. Poggi A, Boero S, Musso A, Zocchi MR. 69.  2013. Selective role of mevalonate pathway in regulating perforin but not FasL and TNFα release in human natural killer cells. PLOS ONE 8e62932
  70. Eberl M, Hintz M, Reichenberg A, Kollas AK, Wiesner J, Jomaa H. 70.  2003. Microbial isoprenoid biosynthesis and human γδ T cell activation. FEBS Lett. 544:4–10 [Google Scholar]
  71. Kistowska M, Rossy E, Sansano S, Gober HJ, Landmann R. 71.  et al. 2008. Dysregulation of the host mevalonate pathway during early bacterial infection activates human TCR γδ cells. Eur. J. Immunol. 38:2200–9 [Google Scholar]
  72. Blanc M, Hsieh WY, Robertson KA, Watterson S, Shui G. 72.  et al. 2011. Host defense against viral infection involves interferon mediated down-regulation of sterol biosynthesis. PLOS Biol. 9:e1000598 [Google Scholar]
  73. Wang X, Hinson ER, Cresswell P. 73.  2007. The interferon-inducible protein viperin inhibits influenza virus release by perturbing lipid rafts. Cell Host Microbe 2:96–105 [Google Scholar]
  74. Seo JY, Yaneva R, Cresswell P. 74.  2011. Viperin: a multifunctional, interferon-inducible protein that regulates virus replication. Cell Host Microbe 10:534–39 [Google Scholar]
  75. Freed-Pastor WA, Mizuno H, Zhao X, Langerod A, Moon SH. 75.  et al. 2012. Mutant p53 disrupts mammary tissue architecture via the mevalonate pathway. Cell 148:244–58 [Google Scholar]
  76. Weekes MP, Tomasec P, Huttlin EL, Fielding CA, Nusinow D. 76.  et al. 2014. Quantitative temporal viromics: an approach to investigate host–pathogen interaction. Cell 157:1460–72 [Google Scholar]
  77. Fielding CA, Aicheler R, Stanton RJ, Wang EC, Han S. 77.  et al. 2014. Two novel human cytomegalovirus NK cell evasion functions target MICA for lysosomal degradation. PLOS Pathog. 10:e1004058 [Google Scholar]
  78. Hsu JL, van den Boomen DJ, Tomasec P, Weekes MP, Antrobus R. 78.  et al. 2015. Plasma membrane profiling defines an expanded class of cell surface proteins selectively targeted for degradation by HCMV US2 in cooperation with UL141. PLOS Pathog. 11:e1004811 [Google Scholar]
  79. De Libero G, Lau SY, Mori L. 79.  2014. Phosphoantigen presentation to TCR γδ cells, a conundrum getting less gray zones. Front. Immunol. 5:679 [Google Scholar]
  80. Harly C, Peigne CM, Scotet E. 80.  2014. Molecules and mechanisms implicated in the peculiar antigenic activation process of human Vγ9Vδ2 T cells. Front. Immunol. 5:657 [Google Scholar]
  81. Karunakaran MM, Herrmann T. 81.  2014. The Vγ9Vδ2 T cell antigen receptor and butyrophilin-3 A1: models of interaction, the possibility of co-evolution, and the case of dendritic epidermal T cells. Front. Immunol. 5:648 [Google Scholar]
  82. Gu S, Nawrocka W, Adams EJ. 82.  2014. Sensing of pyrophosphate metabolites by Vγ9Vδ2 T cells. Front. Immunol. 5:688 [Google Scholar]
  83. Kjer-Nielsen L, Patel O, Corbett AJ, Le Nours J, Meehan B. 83.  et al. 2012. MR1 presents microbial vitamin B metabolites to MAIT cells. Nature 491:717–23 [Google Scholar]
  84. Le Bourhis L, Dusseaux M, Bohineust A, Bessoles S, Martin E. 84.  et al. 2013. MAIT cells detect and efficiently lyse bacterially-infected epithelial cells. PLOS Pathog. 9:e1003681 [Google Scholar]
  85. Gold MC, Lewinsohn DM. 85.  2013. Co-dependents: MR1-restricted MAIT cells and their antimicrobial function. Nat. Rev. Microbiol. 11:14–19 [Google Scholar]
  86. Borg NA, Wun KS, Kjer-Nielsen L, Wilce MC, Pellicci DG. 86.  et al. 2007. CD1d-lipid-antigen recognition by the semi-invariant NKT T-cell receptor. Nature 448:44–49 [Google Scholar]
  87. Wang H, Henry O, Distefano MD, Wang YC, Raikkonen J. 87.  et al. 2013. Butyrophilin 3A1 plays an essential role in prenyl pyrophosphate stimulation of human Vγ9Vδ2 T cells. J. Immunol. 191:1029–42 [Google Scholar]
  88. Leung CL, Green KJ, Liem RK. 88.  2002. Plakins: a family of versatile cytolinker proteins. Trends Cell Biol. 12:37–45 [Google Scholar]
  89. Jefferson JJ, Leung CL, Liem RK. 89.  2004. Plakins: Goliaths that link cell junctions and the cytoskeleton. Nat. Rev. Mol. Cell Biol. 5:542–53 [Google Scholar]
  90. Bouameur JE, Favre B, Borradori L. 90.  2014. Plakins, a versatile family of cytolinkers: roles in skin integrity and in human diseases. J. Investig. Dermatol. 134:885–94 [Google Scholar]
  91. Karashima T, Watt FM. 91.  2002. Interaction of periplakin and envoplakin with intermediate filaments. J. Cell Sci. 115:5027–37 [Google Scholar]
  92. Boczonadi V, McInroy L, Maatta A. 92.  2007. Cytolinker cross-talk: Periplakin N-terminus interacts with plectin to regulate keratin organisation and epithelial migration. Exp. Cell Res. 313:3579–91 [Google Scholar]
  93. Groot KR, Sevilla LM, Nishi K, DiColandrea T, Watt FM. 93.  2004. Kazrin, a novel periplakin-interacting protein associated with desmosomes and the keratinocyte plasma membrane. J. Cell Biol. 166:653–59 [Google Scholar]
  94. Kalinin AE, Aho M, Uitto J, Aho S. 94.  2005. Breaking the connection: caspase 6 disconnects intermediate filament-binding domain of periplakin from its actin-binding N-terminal region. J. Investig. Dermatol. 124:46–55 [Google Scholar]
  95. Beekman JM, Bakema JE, van de Winkel JG, Leusen JH. 95.  2004. Direct interaction between FcγRI (CD64) and periplakin controls receptor endocytosis and ligand binding capacity. PNAS 101:10392–97 [Google Scholar]
  96. van den Heuvel AP, de Vries-Smits AM, van Weeren PC, Dijkers PF, de Bruyn KM. 96.  et al. 2002. Binding of protein kinase B to the plakin family member periplakin. J. Cell Sci. 115:3957–66 [Google Scholar]
  97. DiColandrea T, Karashima T, Maatta A, Watt FM. 97.  2000. Subcellular distribution of envoplakin and periplakin: insights into their role as precursors of the epidermal cornified envelope. J. Cell Biol. 151:573–86 [Google Scholar]
  98. Sevilla LM, Nachat R, Groot KR, Klement JF, Uitto J. 98.  et al. 2007. Mice deficient in involucrin, envoplakin, and periplakin have a defective epidermal barrier. J. Cell Biol. 179:1599–612 [Google Scholar]
  99. Cipolat S, Hoste E, Natsuga K, Quist SR, Watt FM. 99.  2014. Epidermal barrier defects link atopic dermatitis with altered skin cancer susceptibility. eLife 3:e01888 [Google Scholar]
  100. Ortega E, Buey RM, Sonnenberg A, de Pereda JM. 100.  2011. The structure of the plakin domain of plectin reveals a non-canonical SH3 domain interacting with its fourth spectrin repeat. J. Biol. Chem. 286:12429–38 [Google Scholar]
  101. Miyashita Y, Ozawa M. 101.  2007. Increased internalization of p120-uncoupled E-cadherin and a requirement for a dileucine motif in the cytoplasmic domain for endocytosis of the protein. J. Biol. Chem. 282:11540–48 [Google Scholar]
  102. Ishiyama N, Lee SH, Liu S, Li GY, Smith MJ. 102.  et al. 2010. Dynamic and static interactions between p120 catenin and E-cadherin regulate the stability of cell–cell adhesion. Cell 141:117–28 [Google Scholar]
  103. Palakodeti A, Sandstrom A, Sundaresan L, Harly C, Nedellec S. 103.  et al. 2012. The molecular basis for modulation of human Vγ9Vδ2 T cell responses by CD277/butyrophilin-3 (BTN3A)-specific antibodies. J. Biol. Chem. 287:32780–90 [Google Scholar]
  104. Jeong J, Lisinski I, Kadegowda AK, Shin H, Wooding FB. 104.  et al. 2013. A test of current models for the mechanism of milk-lipid droplet secretion. Traffic 14:974–86 [Google Scholar]
  105. Ogg SL, Weldon AK, Dobbie L, Smith AJ, Mather IH. 105.  2004. Expression of butyrophilin (Btn1a1) in lactating mammary gland is essential for the regulated secretion of milk-lipid droplets. PNAS 101:10084–89 [Google Scholar]
  106. Decaup E, Duault C, Bezombes C, Poupot M, Savina A. 106.  et al. 2014. Phosphoantigens and butyrophilin 3A1 induce similar intracellular activation signaling in human TCRVγ9+ γδ T lymphocytes. Immunol. Lett. 161:133–37 [Google Scholar]
  107. Yamashiro H, Yoshizaki S, Tadaki T, Egawa K, Seo N. 107.  2010. Stimulation of human butyrophilin 3 molecules results in negative regulation of cellular immunity. J. Leukoc. Biol. 88:757–67 [Google Scholar]
  108. Simone R, Barbarat B, Rabellino A, Icardi G, Bagnasco M. 108.  et al. 2010. Ligation of the BT3 molecules, members of the B7 family, enhance the proinflammatory responses of human monocytes and monocyte-derived dendritic cells. Mol. Immunol. 48:109–18 [Google Scholar]
  109. Messal N, Mamessier E, Sylvain A, Celis-Gutierrez J, Thibult ML. 109.  et al. 2011. Differential role for CD277 as co-regulator of the immune signal in T and NK cells. Eur. J. Immunol. 41:3443–54 [Google Scholar]
  110. Jack LJ, Mather IH. 110.  1990. Cloning and analysis of cDNA encoding bovine butyrophilin, an apical glycoprotein expressed in mammary tissue and secreted in association with the milk-fat globule membrane during lactation. J. Biol. Chem. 265:14481–86 [Google Scholar]
  111. Vorbach C, Harrison R, Capecchi MR. 111.  2003. Xanthine oxidoreductase is central to the evolution and function of the innate immune system. Trends Immunol. 24:512–17 [Google Scholar]
  112. Jeong J, Rao AU, Xu J, Ogg SL, Hathout Y. 112.  et al. 2009. The PRY/SPRY/B30.2 domain of butyrophilin 1A1 (BTN1A1) binds to xanthine oxidoreductase: implications for the function of BTN1A1 in the mammary gland and other tissues. J. Biol. Chem. 284:22444–56 [Google Scholar]
  113. Sargeant TJ, Lloyd-Lewis B, Resemann HK, Ramos-Montoya A, Skepper J, Watson CJ. 113.  2014. Stat3 controls cell death during mammary gland involution by regulating uptake of milk fat globules and lysosomal membrane permeabilization. Nat. Cell Biol. 16:1057–68 [Google Scholar]
  114. Gardinier MV, Amiguet P, Linington C, Matthieu JM. 114.  1992. Myelin/oligodendrocyte glycoprotein is a unique member of the immunoglobulin superfamily. J. Neurosci. Res. 33:177–87 [Google Scholar]
  115. Pagany M, Jagodic M, Bourquin C, Olsson T, Linington C. 115.  2003. Genetic variation in myelin oligodendrocyte glycoprotein expression and susceptibility to experimental autoimmune encephalomyelitis. J. Neuroimmunol. 139:1–8 [Google Scholar]
  116. Reindl M, Di Pauli F, Rostasy K, Berger T. 116.  2013. The spectrum of MOG autoantibody-associated demyelinating diseases. Nat. Rev. Neurol. 9:455–61 [Google Scholar]
  117. Guggenmos J, Schubart AS, Ogg S, Andersson M, Olsson T. 117.  et al. 2004. Antibody cross-reactivity between myelin oligodendrocyte glycoprotein and the milk protein butyrophilin in multiple sclerosis. J. Immunol. 172:661–68 [Google Scholar]
  118. Linington C, Berger T, Perry L, Weerth S, Hinze-Selch D. 118.  et al. 1993. T cells specific for the myelin oligodendrocyte glycoprotein mediate an unusual autoimmune inflammatory response in the central nervous system. Eur. J. Immunol. 23:1364–72 [Google Scholar]
  119. Delarasse C, Daubas P, Mars LT, Vizler C, Litzenburger T. 119.  et al. 2003. Myelin/oligodendrocyte glycoprotein-deficient (MOG-deficient) mice reveal lack of immune tolerance to MOG in wild-type mice. J. Clin. Investig. 112:544–53 [Google Scholar]
  120. Stefferl A, Schubart A, Storch M, Amini A, Mather I. 120.  et al. 2000. Butyrophilin, a milk protein, modulates the encephalitogenic T cell response to myelin oligodendrocyte glycoprotein in experimental autoimmune encephalomyelitis. J. Immunol. 165:2859–65 [Google Scholar]
  121. Bruno R, Sabater L, Sospedra M, Ferrer-Francesch X, Escudero D. 121.  et al. 2002. Multiple sclerosis candidate autoantigens except myelin oligodendrocyte glycoprotein are transcribed in human thymus. Eur. J. Immunol. 32:2737–47 [Google Scholar]
  122. Garcia-Vallejo JJ, Ilarregui JM, Kalay H, Chamorro S, Koning N. 122.  et al. 2014. CNS myelin induces regulatory functions of DC-SIGN-expressing, antigen-presenting cells via cognate interaction with MOG. J. Exp. Med. 211:1465–83 [Google Scholar]
  123. Ye TZ, Gordon CT, Lai YH, Fujiwara Y, Peters LL. 123.  et al. 2000. Ermap, a gene coding for a novel erythroid specific adhesion/receptor membrane protein. Gene 242:337–45 [Google Scholar]
  124. Su YY, Gordon CT, Ye TZ, Perkins AC, Chui DH. 124.  2001. Human ERMAP: an erythroid adhesion/receptor transmembrane protein. Blood Cells Mol. Dis. 27:938–49 [Google Scholar]
  125. Wagner FF, Poole J, Flegel WA. 125.  2003. Scianna antigens including Rd are expressed by ERMAP. Blood 101:752–7 [Google Scholar]
  126. Kaufman J, Skjodt K, Salomonsen J. 126.  1991. The B-G multigene family of the chicken major histocompatibility complex. Crit. Rev. Immunol. 11:113–43 [Google Scholar]
  127. Kaufman J, Salomonsen J. 127.  1992. B-G: we know what it is, but what does it do?. Immunol. Today 13:1–3 [Google Scholar]
  128. Salomonsen J, Chattaway JA, Chan AC, Parker A, Huguet S. 128.  et al. 2014. Sequence of a complete chicken BG haplotype shows dynamic expansion and contraction of two gene lineages with particular expression patterns. PLOS Genet. 10:e1004417 [Google Scholar]
  129. Salomonsen J, Dunon D, Skjodt K, Thorpe D, Vainio O, Kaufman J. 129.  1991. Chicken major histocompatibility complex-encoded B-G antigens are found on many cell types that are important for the immune system. PNAS 88:1359–63 [Google Scholar]
  130. Salomonsen J, Eriksson H, Skjodt K, Lundgreen T, Simonsen M, Kaufman J. 130.  1991. The “adjuvant effect” of the polymorphic B-G antigens of the chicken major histocompatibility complex analyzed using purified molecules incorporated in liposomes. Eur. J. Immunol. 21:649–58 [Google Scholar]
  131. Goto RM, Wang Y, Taylor RL Jr, Wakenell PS, Hosomichi K. 131.  et al. 2009. BG1 has a major role in MHC-linked resistance to malignant lymphoma in the chicken. PNAS 106:16740–45 [Google Scholar]
  132. Elleder D, Stepanets V, Melder DC, Senigl F, Geryk J. 132.  et al. 2005. The receptor for the subgroup C avian sarcoma and leukosis viruses, Tvc, is related to mammalian butyrophilins, members of the immunoglobulin superfamily. J. Virol. 79:10408–19 [Google Scholar]
  133. Greenwald RJ, Freeman GJ, Sharpe AH. 133.  2005. The B7 family revisited. Annu. Rev. Immunol. 23:515–48 [Google Scholar]
  134. Schwartz JC, Zhang X, Nathenson SG, Almo SC. 134.  2002. Structural mechanisms of costimulation. Nat. Immunol. 3:427–34 [Google Scholar]
  135. Dong H, Zhu G, Tamada K, Chen L. 135.  1999. B7-H1, a third member of the B7 family, co-stimulates T-cell proliferation and interleukin-10 secretion. Nat. Med. 5:1365–69 [Google Scholar]
/content/journals/10.1146/annurev-immunol-041015-055435
Loading
/content/journals/10.1146/annurev-immunol-041015-055435
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error