The Adhesion G Protein-Coupled Receptor GPR56/ADGRG1 Is an Inhibitory Receptor on Human NK Cells

Cell Reports

Volumn 15, Issue 8, 2016, Pages 1757-1770

  Chang, Gin Wen ^a   Hsiao, Cheng Chih ^b   Peng, Yen Ming ^a   Vieira Braga, Felipe A ^b   Kragten, Natasja A M ^b   Remmerswaal, Ester B M ^b   van de Garde, Martijn D B ^b   Straussberg, Rachel ^c   König, Gabriele M ^d   Kostenis, Evi ^d   Knäuper, Vera ^e   Meyaard, Linde ^f   van Lier, René A W ^b   van Gisbergen, Klaas P J M ^b   Lin, Hsi Hsien ^a,g   Hamann, Jörg ^b  

^a CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c TEL AVIV UNIVERSITY   (Israel)

^d UNIVERSITY OF BONN   (Germany)

^e CARDIFF UNIVERSITY   (United Kingdom)

^f UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^g CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

Author keywords

Adhesion GPCRs; Cytotoxicity; Immune regulation; NK cells; Transcription factor

Indexed keywords

B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; CD81 ANTIGEN; CELL PROTEIN; CYTOKINE; G PROTEIN COUPLED RECEPTOR; PROTEIN ADGRG1; PROTEIN GPR56; PROTEIN HOBIT; TETRASPANIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; AUTACOID; GPR56 PROTEIN, HUMAN;

ARTICLE; CELL ADHESION; CELL KILLING; CYTOKINE PRODUCTION; DEGRANULATION; ECTOPIC EXPRESSION; HUMAN; HUMAN CELL; MICROGYRIA; MUTATIONAL ANALYSIS; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; SEQUENCE HOMOLOGY; T LYMPHOCYTE ACTIVATION; CELL CULTURE; CELL DIFFERENTIATION; CELL DIVISION; CELL LINE; CORTICAL DYSPLASIA; CYTOLOGY; CYTOTOXICITY; DEFICIENCY; DOWN REGULATION; DRUG EFFECTS; IMMUNOLOGICAL SYNAPSE; METABOLISM; PATHOLOGY;

CELL DIFFERENTIATION; CELL DIVISION; CELL LINE; CELLS, CULTURED; CYTOKINES; CYTOTOXICITY, IMMUNOLOGIC; DOWN-REGULATION; HUMANS; IMMUNOLOGICAL SYNAPSES; INFLAMMATION MEDIATORS; KILLER CELLS, NATURAL; MALFORMATIONS OF CORTICAL DEVELOPMENT; RECEPTORS, G-PROTEIN-COUPLED; TETRASPANIN 28; TRANSCRIPTION FACTORS;

EID: 84966692466     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.04.053     Document Type: Article

References (64)

1. Ackerman S.D., Garcia C., Piao X., Gutmann D.H., Monk K.R. The adhesion GPCR Gpr56 regulates oligodendrocyte development via interactions with Gα12/13 and RhoA. Nat. Commun. 2015, 6:6122.
2. Araç D., Boucard A.A., Bolliger M.F., Nguyen J., Soltis S.M., Südhof T.C., Brunger A.T. A novel evolutionarily conserved domain of cell-adhesion GPCRs mediates autoproteolysis. EMBO J. 2012, 31:1364-1378.
3. Baala L., Briault S., Etchevers H.C., Laumonnier F., Natiq A., Amiel J., Boddaert N., Picard C., Sbiti A., Asermouh A., et al. Homozygous silencing of T-box transcription factor EOMES leads to microcephaly with polymicrogyria and corpus callosum agenesis. Nat. Genet. 2007, 39:454-456.
4. Bae B.-I., Tietjen I., Atabay K.D., Evrony G.D., Johnson M.B., Asare E., Wang P.P., Murayama A.Y., Im K., Lisgo S.N., et al. Evolutionarily dynamic alternative splicing of GPR56 regulates regional cerebral cortical patterning. Science 2014, 343:764-768.
5. Björkström N.K., Riese P., Heuts F., Andersson S., Fauriat C., Ivarsson M.A., Björklund A.T., Flodström-Tullberg M., Michaëlsson J., Rottenberg M.E., et al. Expression patterns of NKG2A, KIR, and CD57 define a process of CD56dim NK-cell differentiation uncoupled from NK-cell education. Blood 2010, 116:3853-3864.
6. Caligiuri M.A. Human natural killer cells. Blood 2008, 112:461-469.
7. Chen G., Yang L., Begum S., Xu L. GPR56 is essential for testis development and male fertility in mice. Dev. Dyn. 2010, 239:3358-3367.
8. Chiang N.-Y., Hsiao C.-C., Huang Y.-S., Chen H.-Y., Hsieh I.-J., Chang G.-W., Lin H.-H. Disease-associated GPR56 mutations cause bilateral frontoparietal polymicrogyria via multiple mechanisms. J. Biol. Chem. 2011, 286:14215-14225.
9. Crotta S., Stilla A., Wack A., D'Andrea A., Nuti S., D'Oro U., Mosca M., Filliponi F., Brunetto R.M., Bonino F., et al. Inhibition of natural killer cells through engagement of CD81 by the major hepatitis C virus envelope protein. J. Exp. Med. 2002, 195:35-41.
10. Crotty S., Johnston R.J., Schoenberger S.P. Effectors and memories: Bcl-6 and Blimp-1 in T and B lymphocyte differentiation. Nat. Immunol. 2010, 11:114-120.
11. Daussy C., Faure F., Mayol K., Viel S., Gasteiger G., Charrier E., Bienvenu J., Henry T., Debien E., Hasan U.A., et al. T-bet and Eomes instruct the development of two distinct natural killer cell lineages in the liver and in the bone marrow. J. Exp. Med. 2014, 211:563-577.
12. Della Chiesa M., Falco M., Parolini S., Bellora F., Petretto A., Romeo E., Balsamo M., Gambarotti M., Scordamaglia F., Tabellini G., et al. GPR56 as a novel marker identifying the CD56dull CD16+ NK cell subset both in blood stream and in inflamed peripheral tissues. Int. Immunol. 2010, 22:91-100.
13. Doody G.M., Stephenson S., McManamy C., Tooze R.M. PRDM1/BLIMP-1 modulates IFN-gamma-dependent control of the MHC class I antigen-processing and peptide-loading pathway. J. Immunol. 2007, 179:7614-7623.
14. Elsen G.E., Hodge R.D., Bedogni F., Daza R.A.M., Nelson B.R., Shiba N., Reiner S.L., Hevner R.F. The protomap is propagated to cortical plate neurons through an Eomes-dependent intermediate map. Proc. Natl. Acad. Sci. USA 2013, 110:4081-4086.
15. Fauriat C., Long E.O., Ljunggren H.-G., Bryceson Y.T. Regulation of human NK-cell cytokine and chemokine production by target cell recognition. Blood 2010, 115:2167-2176.
16. Fehniger T.A., Shah M.H., Turner M.J., VanDeusen J.B., Whitman S.P., Cooper M.A., Suzuki K., Wechser M., Goodsaid F., Caligiuri M.A. Differential cytokine and chemokine gene expression by human NK cells following activation with IL-18 or IL-15 in combination with IL-12: implications for the innate immune response. J. Immunol. 1999, 162:4511-4520.
17. Fehniger T.A., Cai S.F., Cao X., Bredemeyer A.J., Presti R.M., French A.R., Ley T.J. Acquisition of murine NK cell cytotoxicity requires the translation of a pre-existing pool of granzyme B and perforin mRNAs. Immunity 2007, 26:798-811.
18. Freud A.G., Caligiuri M.A. Human natural killer cell development. Immunol. Rev. 2006, 214:56-72.
19. Giera S., Deng Y., Luo R., Ackerman S.D., Mogha A., Monk K.R., Ying Y., Jeong S.-J., Makinodan M., Bialas A.R., et al. The adhesion G protein-coupled receptor GPR56 is a cell-autonomous regulator of oligodendrocyte development. Nat. Commun. 2015, 6:6121.
20. Hamann J., Aust G., Araç D., Engel F.B., Formstone C., Fredriksson R., Hall R.A., Harty B.L., Kirchhoff C., Knapp B., et al. International Union of Basic and Clinical Pharmacology. XCIV. Adhesion G protein-coupled receptors. Pharmacol. Rev. 2015, 67:338-367.
21. Iguchi T., Sakata K., Yoshizaki K., Tago K., Mizuno N., Itoh H. Orphan G protein-coupled receptor GPR56 regulates neural progenitor cell migration via a G alpha 12/13 and Rho pathway. J. Biol. Chem. 2008, 283:14469-14478.
22. Jin Z., Tietjen I., Bu L., Liu-Yesucevitz L., Gaur S.K., Walsh C.A., Piao X. Disease-associated mutations affect GPR56 protein trafficking and cell surface expression. Hum. Mol. Genet. 2007, 16:1972-1985.
23. Karpus O.N., Veninga H., Hoek R.M., Flierman D., van Buul J.D., Vandenakker C.C., vanBavel E., Medof M.E., van Lier R.A.W., Reedquist K.A., Hamann J. Shear stress-dependent downregulation of the adhesion-G protein-coupled receptor CD97 on circulating leukocytes upon contact with its ligand CD55. J. Immunol. 2013, 190:3740-3748.
24. Kishore A., Purcell R.H., Nassiri-Toosi Z., Hall R.A. Stalk-dependent and stalk-independent signaling by the adhesion G protein-coupled receptors GPR56 (ADGRG1) and BAI1 (ADGRB1). J. Biol. Chem. 2016, 291:3385-3394.
25. Knox J.J., Cosma G.L., Betts M.R., McLane L.M. Characterization of T-bet and eomes in peripheral human immune cells. Front. Immunol. 2014, 5:217.
26. Krementsov D.N., Rassam P., Margeat E., Roy N.H., Schneider-Schaulies J., Milhiet P.-E., Thali M. HIV-1 assembly differentially alters dynamics and partitioning of tetraspanins and raft components. Traffic 2010, 11:1401-1414.
27. Langenhan T., Aust G., Hamann J. Sticky signaling-adhesion class G protein-coupled receptors take the stage. Sci. Signal. 2013, 6:re3.
28. Lanier L.L. Up on the tightrope: natural killer cell activation and inhibition. Nat. Immunol. 2008, 9:495-502.
29. Lawrence P.A., Struhl G., Casal J. Planar cell polarity: A bridge too far?. Curr. Biol. 2008, 18:R959-R961.
30. Lee J., Zhang T., Hwang I., Kim A., Nitschke L., Kim M., Scott J.M., Kamimura Y., Lanier L.L., Kim S. Epigenetic modification and antibody-dependent expansion of memory-like NK cells in human cytomegalovirus-infected individuals. Immunity 2015, 42:431-442.
31. Liebscher I., Schön J., Petersen S.C., Fischer L., Auerbach N., Demberg L.M., Mogha A., Cöster M., Simon K.-U., Rothemund S., et al. A tethered agonist within the ectodomain activates the adhesion G protein-coupled receptors GPR126 and GPR133. Cell Rep. 2014, 9:2018-2026.
32. Lin H.-H., Chang G.-W., Davies J.Q., Stacey M., Harris J., Gordon S. Autocatalytic cleavage of the EMR2 receptor occurs at a conserved G protein-coupled receptor proteolytic site motif. J. Biol. Chem. 2004, 279:31823-31832.
33. Little K.D., Hemler M.E., Stipp C.S. Dynamic regulation of a GPCR-tetraspanin-G protein complex on intact cells: central role of CD81 in facilitating GPR56-Galpha q/11 association. Mol. Biol. Cell 2004, 15:2375-2387.
34. Lopez-Vergès S., Milush J.M., Pandey S., York V.A., Arakawa-Hoyt J., Pircher H., Norris P.J., Nixon D.F., Lanier L.L. CD57 defines a functionally distinct population of mature NK cells in the human CD56dimCD16+ NK-cell subset. Blood 2010, 116:3865-3874.
35. Luo R., Jeong S.-J., Jin Z., Strokes N., Li S., Piao X. G protein-coupled receptor 56 and collagen III, a receptor-ligand pair, regulates cortical development and lamination. Proc. Natl. Acad. Sci. USA 2011, 108:12925-12930.
36. Monk K.R., Hamann J., Langenhan T., Nijmeijer S., Schöneberg T., Liebscher I. Adhesion G protein-coupled receptors: from in vitro pharmacology to in vivo mechanisms. Mol. Pharmacol. 2015, 88:617-623.
37. Nagler A., Lanier L.L., Cwirla S., Phillips J.H. Comparative studies of human FcRIII-positive and negative natural killer cells. J. Immunol. 1989, 143:3183-3191.
38. Ono A. Relationships between plasma membrane microdomains and HIV-1 assembly. Biol. Cell 2010, 102:335-350.
39. Paavola K.J., Hall R.A. Adhesion G protein-coupled receptors: signaling, pharmacology, and mechanisms of activation. Mol. Pharmacol. 2012, 82:777-783.
40. Paavola K.J., Stephenson J.R., Ritter S.L., Alter S.P., Hall R.A. The N terminus of the adhesion G protein-coupled receptor GPR56 controls receptor signaling activity. J. Biol. Chem. 2011, 286:28914-28921.
41. Paavola K.J., Sidik H., Zuchero J.B., Eckart M., Talbot W.S. Type IV collagen is an activating ligand for the adhesion G protein-coupled receptor GPR126. Sci. Signal. 2014, 7:ra76.
42. Pegram H.J., Andrews D.M., Smyth M.J., Darcy P.K., Kershaw M.H. Activating and inhibitory receptors of natural killer cells. Immunol. Cell Biol. 2011, 89:216-224.
43. Peng Y.-M., van de Garde M.D.B., Cheng K.-F., Baars P.A., Remmerswaal E.B.M., van Lier R.A.W., Mackay C.R., Lin H.-H., Hamann J. Specific expression of GPR56 by human cytotoxic lymphocytes. J. Leukoc. Biol. 2011, 90:735-740.
44. Piao X., Hill R.S., Bodell A., Chang B.S., Basel-Vanagaite L., Straussberg R., Dobyns W.B., Qasrawi B., Winter R.M., Innes A.M., et al. G protein-coupled receptor-dependent development of human frontal cortex. Science 2004, 303:2033-2036.
45. Piao X., Chang B.S., Bodell A., Woods K., Benzeev B., Topçu M., Guerrini R., Goldberg-Stern H., Sztriha L., Dobyns W.B., et al. Genotype-phenotype analysis of human frontoparietal polymicrogyria syndromes. Ann. Neurol. 2005, 58:680-687.
46. Pierce K.L., Premont R.T., Lefkowitz R.J. Seven-transmembrane receptors. Nat. Rev. Mol. Cell Biol. 2002, 3:639-650.
47. Romee R., Foley B., Lenvik T., Wang Y., Zhang B., Ankarlo D., Luo X., Cooley S., Verneris M., Walcheck B., Miller J. NK cell CD16 surface expression and function is regulated by a disintegrin and metalloprotease-17 (ADAM17). Blood 2013, 121:3599-3608.
48. Saito Y., Kaneda K., Suekane A., Ichihara E., Nakahata S., Yamakawa N., Nagai K., Mizuno N., Kogawa K., Miura I., et al. Maintenance of the hematopoietic stem cell pool in bone marrow niches by EVI1-regulated GPR56. Leukemia 2013, 27:1637-1649.
49. Schlums H., Cichocki F., Tesi B., Theorell J., Beziat V., Holmes T.D., Han H., Chiang S.C.C., Foley B., Mattsson K., et al. Cytomegalovirus infection drives adaptive epigenetic diversification of NK cells with altered signaling and effector function. Immunity 2015, 42:443-456.
50. Schrage R., Schmitz A.-L., Gaffal E., Annala S., Kehraus S., Wenzel D., Büllesbach K.M., Bald T., Inoue A., Shinjo Y., et al. The experimental power of FR900359 to study Gq-regulated biological processes. Nat. Commun. 2015, 6:10156.
51. Solaimani Kartalaei P., Yamada-Inagawa T., Vink C.S., de Pater E., van der Linden R., Marks-Bluth J., van der Sloot A., van den Hout M., Yokomizo T., van Schaick-Solernó M.L., et al. Whole-transcriptome analysis of endothelial to hematopoietic stem cell transition reveals a requirement for Gpr56 in HSC generation. J. Exp. Med. 2015, 212:93-106.
52. Stephenson J.R., Paavola K.J., Schaefer S.A., Kaur B., Van Meir E.G., Hall R.A. Brain-specific angiogenesis inhibitor-1 signaling, regulation, and enrichment in the postsynaptic density. J. Biol. Chem. 2013, 288:22248-22256.
53. Stoveken H.M., Hajduczok A.G., Xu L., Tall G.G. Adhesion G protein-coupled receptors are activated by exposure of a cryptic tethered agonist. Proc. Natl. Acad. Sci. USA 2015, 112:6194-6199.
54. Tseng C.-T.K., Klimpel G.R. Binding of the hepatitis C virus envelope protein E2 to CD81 inhibits natural killer cell functions. J. Exp. Med. 2002, 195:43-49.
55. van Gisbergen K.P.J.M., Kragten N.A.M., Hertoghs K.M.L., Wensveen F.M., Jonjic S., Hamann J., Nolte M.A., van Lier R.A.W. Mouse Hobit is a homolog of the transcriptional repressor Blimp-1 that regulates NKT cell effector differentiation. Nat. Immunol. 2012, 13:864-871.
56. Vieira Braga F.A., Hertoghs K.M.L., Kragten N.A.M., Doody G.M., Barnes N.A., Remmerswaal E.B.M., Hsiao C.-C., Moerland P.D., Wouters D., Derks I.A.M., et al. Blimp-1 homolog Hobit identifies effector-type lymphocytes in humans. Eur. J. Immunol. 2015, 45:2945-2958.
57. Vivier E., Tomasello E., Baratin M., Walzer T., Ugolini S. Functions of natural killer cells. Nat. Immunol. 2008, 9:503-510.
58. Voehringer D., Koschella M., Pircher H. Lack of proliferative capacity of human effector and memory T cells expressing killer cell lectinlike receptor G1 (KLRG1). Blood 2002, 100:3698-3702.
59. Walzer T., Vivier E. G-protein-coupled receptors in control of natural killer cell migration. Trends Immunol. 2011, 32:486-492.
60. White J.P., Wrann C.D., Rao R.R., Nair S.K., Jedrychowski M.P., You J.-S., Martínez-Redondo V., Gygi S.P., Ruas J.L., Hornberger T.A., et al. G protein-coupled receptor 56 regulates mechanical overload-induced muscle hypertrophy. Proc. Natl. Acad. Sci. USA 2014, 111:15756-15761.
61. Xu L., Begum S., Hearn J.D., Hynes R.O. GPR56, an atypical G protein-coupled receptor, binds tissue transglutaminase, TG2, and inhibits melanoma tumor growth and metastasis. Proc. Natl. Acad. Sci. USA 2006, 103:9023-9028.
62. Yang L., Chen G., Mohanty S., Scott G., Fazal F., Rahman A., Begum S., Hynes R.O., Xu L. GPR56 Regulates VEGF production and angiogenesis during melanoma progression. Cancer Res. 2011, 71:5558-5568.
63. Yang T.-Y., Chiang N.-Y., Tseng W.-Y., Pan H.-L., Peng Y.-M., Shen J.-J., Wu K.-A., Kuo M.-L., Chang G.-W., Lin H.-H. Expression and immunoaffinity purification of recombinant soluble human GPR56 protein for the analysis of GPR56 receptor shedding by ELISA. Protein Expr. Purif. 2015, 109:85-92.
64. Zhang T., Scott J.M., Hwang I., Kim S. Cutting edge: antibody-dependent memory-like NK cells distinguished by FcRγ deficiency. J. Immunol. 2013, 190:1402-1406.