Endocytosis and intracellular trafficking of human natural killer cell receptors

Traffic

Volumn 10, Issue 12, 2009, Pages 1735-1744

  Masilamani, Madhan ^a   Peruzzi, Giovanna ^b   Borrego, Francisco ^c   Coligan, John E ^b  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

Endocytosis; Intra cellular trafficking; NK cell receptors

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; CD16 ANTIGEN; CD94 ANTIGEN; CELL PROTEIN; CYTOCHROME P450 2B4; DYNAMIN; GAMMA INTERFERON; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; NATURAL KILLER CELL RECEPTOR; NATURAL KILLER CELL RECEPTOR NKG2G; PROTEIN KINASE C DELTA; UNCLASSIFIED DRUG;

BINDING AFFINITY; CD8+ T LYMPHOCYTE; CELL MIGRATION; CELL SURFACE; CYTOKINE PRODUCTION; DOWN REGULATION; ENDOCYTOSIS; GENE ACTIVATION; GENE EXPRESSION; GENE FUNCTION; GENE LOCATION; HUMAN; LIGAND BINDING; NATURAL KILLER CELL; NONHUMAN; PHAGOCYTOSIS; PINOCYTOSIS; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; TARGET CELL; UBIQUITINATION;

ENDOCYTOSIS; HUMANS; PROTEIN TRANSPORT; RECEPTORS, NATURAL KILLER CELL;

EID: 70649110088     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2009.00973.x     Document Type: Review

References (173)

1. Alcover A, Alarcon B. Internalization and intracellular fate of TCR-CD3 complexes. Crit Rev Immunol 2000, 20:325-346.
2. Geisler C. TCR trafficking in resting and stimulated T cells. Crit Rev Immunol 2004, 24:67-86.
3. Barr VA, Balagopalan L, Barda-Saad M, Polishchuk R, Boukari H, Bunnell SC, Bernot KM, Toda Y, Nossal R, Samelson LE. T-cell antigen receptor-induced signaling complexes: internalization via a cholesterol-dependent endocytic pathway. Traffic 2006, 7:1143-1162.
4. Rodriguez-Pinto D. B cells as antigen presenting cells. Cell Immunol 2005, 238:67-75.
5. von Zastrow M, Sorkin A. Signaling on the endocytic pathway. Curr Opin Cell Biol 2007, 19:436-445.
6. Miaczynska M, Pelkmans L, Zerial M. Not just a sink: endosomes in control of signal transduction. Curr Opin Cell Biol 2004, 16:400-406.
7. McPherson PS, Kay BK, Hussain NK. Signaling on the endocytic pathway. Traffic 2001, 2:375-384.
8. Watts C, Zaru R, Prescott AR, Wallin RP, West MA. Proximal effects of Toll-like receptor activation in dendritic cells. Curr Opin Immunol 2007, 19:73-78.
9. Swanson JA. Shaping cups into phagosomes and macropinosomes. Nat Rev Mol Cell Biol 2008, 9:639-649.
10. Swanson JA, Hoppe AD. The coordination of signaling during Fc receptor-mediated phagocytosis. J Leukoc Biol 2004, 76:1093-1103.
11. Amigorena S, Bonnerot C. Fc receptor signaling and trafficking: a connection for antigen processing. Immunol Rev 1999, 172:279-284.
12. Caplan S, Naslavsky N, Hartnell LM, Lodge R, Polishchuk RS, Donaldson JG, Bonifacino JS. A tubular EHD1-containing compartment involved in the recycling of major histocompatibility complex class I molecules to the plasma membrane. EMBO J 2002, 21:2557-2567.
13. Vyas JM, Van der Veen AG, Ploegh HL. The known unknowns of antigen processing and presentation. Nat Rev Immunol 2008, 8:607-618.
14. Naslavsky N, Weigert R, Donaldson JG. Characterization of a nonclathrin endocytic pathway: membrane cargo and lipid requirements. Mol Biol Cell 2004, 15:3542-3552.
15. Conner SD, Schmid SL. Regulated portals of entry into the cell. Nature 2003, 422:37-44.
16. Doherty GJ, McMahon HT. Mechanisms of endocytosis. Annu Rev Biochem 2009, 78:857-902.
17. Rappoport JZ. Focusing on clathrin-mediated endocytosis. Biochem J 2008, 412:415-423.
18. Mayor S, Pagano RE. Pathways of clathrin-independent endocytosis. Nat Rev Mol Cell Biol 2007, 8:603-612.
19. Kirkham M, Parton RG. Clathrin-independent endocytosis: new insights into caveolae and non-caveolar lipid raft carriers. Biochim Biophys Acta 2005, 1746:349-363.
20. Le Roy C, Wrana JL. Clathrin- and non-clathrin-mediated endocytic regulation of cell signalling. Nat Rev Mol Cell Biol 2005, 6:112-126.
21. Masilamani M, Narayanan S, Prieto M, Borrego F, Coligan JE. Uncommon endocytic and trafficking pathway of the natural killer cell CD94/NKG2A inhibitory receptor. Traffic 2008, 9:1019-1034.
22. Di Guglielmo GM, Le Roy C, Goodfellow AF, Wrana JL. Distinct endocytic pathways regulate TGF-beta receptor signalling and turnover. Nat Cell Biol 2003, 5:410-421.
23. Sigismund S, Argenzio E, Tosoni D, Cavallaro E, Polo S, Di Fiore PP. Clathrin-mediated internalization is essential for sustained EGFR signaling but dispensable for degradation. Dev Cell 2008, 15:209-219.
24. Benmerah A, Lamaze C. Clathrin-coated pits: vive la difference?. Traffic 2007, 8:970-982.
25. Brodsky FM, Chen CY, Knuehl C, Towler MC, Wakeham DE. Biological basket weaving: formation and function of clathrin-coated vesicles. Annu Rev Cell Dev Biol 2001, 17:517-568.
26. Sorkin A. Cargo recognition during clathrin-mediated endocytosis: a team effort. Curr Opin Cell Biol 2004, 16:392-399.
27. Schmid EM, McMahon HT. Integrating molecular and network biology to decode endocytosis. Nature 2007, 448:883-888.
28. Donaldson JG, Porat-Shliom N, Cohen LA. Clathrin-independent endocytosis: a unique platform for cell signaling and PM remodeling. Cell Signal 2009, 21:1-6.
29. Sengelov H, Voldstedlund M, Vinten J, Borregaard N. Human neutrophils are devoid of the integral membrane protein caveolin. J Leukoc Biol 1998, 63:563-566.
30. Fra AM, Williamson E, Simons K, Parton RG. Detergent-insoluble glycolipid microdomains in lymphocytes in the absence of caveolae. J Biol Chem 1994, 269:30745-30748.
31. Kiss AL, Turi A, Mullner N, Timar J. Caveolin isoforms in resident and elicited rat peritoneal macrophages. Eur J Cell Biol 2000, 79:343-349.
32. Lei MG, Morrison DC. Differential expression of caveolin-1 in lipopolysaccharide-activated murine macrophages. Infect Immun 2000, 68:5084-5089.
33. Gargalovic P, Dory L. Caveolin-1 and caveolin-2 expression in mouse macrophages. High density lipoprotein 3-stimulated secretion and a lack of significant subcellular co-localization. J Biol Chem 2001, 276:26164-26170.
34. Medina FA, Williams TM, Sotgia F, Tanowitz HB, Lisanti MP. A novel role for caveolin-1 in B lymphocyte function and the development of thymus-independent immune responses. Cell Cycle 2006, 5:1865-1871.
35. Stoddart A, Jackson AP, Brodsky FM. Plasticity of B cell receptor internalization upon conditional depletion of clathrin. Mol Biol Cell 2005, 16:2339-2348.
36. Fattakhova G, Masilamani M, Borrego F, Gilfillan AM, Metcalfe DD, Coligan JE. The high-affinity immunoglobulin-E receptor (FcepsilonRI) is endocytosed by an AP-2/clathrin-independent, dynamin-dependent mechanism. Traffic 2006, 7:673-685.
37. Lamaze C, Dujeancourt A, Baba T, Lo CG, Benmerah A, Dautry-Varsat A. Interleukin 2 receptors and detergent-resistant membrane domains define a clathrin-independent endocytic pathway. Mol Cell 2001, 7:661-671.
38. Grassart A, Dujeancourt A, Lazarow PB, Dautry-Varsat A, Sauvonnet N. Clathrin-independent endocytosis used by the IL-2 receptor is regulated by Rac1, Pak1 and Pak2. EMBO Rep 2008, 9:356-362.
39. Glebov OO, Bright NA, Nichols BJ. Flotillin-1 defines a clathrin-independent endocytic pathway in mammalian cells. Nat Cell Biol 2006, 8:46-54.
40. Nichols BJ, Kenworthy AK, Polishchuk RS, Lodge R, Roberts TH, Hirschberg K, Phair RD, Lippincott-Schwartz J. Rapid cycling of lipid raft markers between the cell surface and Golgi complex. J Cell Biol 2001, 153:529-541.
41. Putnam MA, Moquin AE, Merrihew M, Outcalt C, Sorge E, Caballero A, Gondre-Lewis TA, Drake JR. Lipid raft-independent B cell receptor-mediated antigen internalization and intracellular trafficking. J Immunol 2003, 170:905-912.
42. Santini F, Keen JH. Endocytosis of activated receptors and clathrin-coated pit formation: deciphering the chicken or egg relationship. J Cell Biol 1996, 132:1025-1036.
43. Finger EC, Lee NY, You HJ, Blobe GC. Endocytosis of the type III transforming growth factor-beta (TGF-beta) receptor through the clathrin-independent/lipid raft pathway regulates TGF-beta signaling and receptor down-regulation. J Biol Chem 2008, 283:34808-34818.
44. Rollason R, Korolchuk V, Hamilton C, Schu P, Banting G. Clathrin-mediated endocytosis of a lipid-raft-associated protein is mediated through a dual tyrosine motif. J Cell Sci 2007, 120:3850-3858.
45. Bonifacino JS, Traub LM. Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu Rev Biochem 2003, 72:395-447.
46. Hou P, Araujo E, Zhao T, Zhang M, Massenburg D, Veselits M, Doyle C, Dinner AR, Clark MR. B cell antigen receptor signaling and internalization are mutually exclusive events. PLoS Biol 2006, 4:e200.
47. Henley JR, Krueger EW, Oswald BJ, McNiven MA. Dynamin-mediated internalization of caveolae. J Cell Biol 1998, 141:85-99.
48. Praefcke GJ, McMahon HT. The dynamin superfamily: universal membrane tubulation and fission molecules?. Nat Rev Mol Cell Biol 2004, 5:133-147.
49. Mears JA, Hinshaw JE. Visualization of dynamins. Methods Cell Biol 2008, 88:237-256.
50. Marks B, Stowell MH, Vallis Y, Mills IG, Gibson A, Hopkins CR, McMahon HT. GTPase activity of dynamin and resulting conformation change are essential for endocytosis. Nature 2001, 410:231-235.
51. Damke H, Baba T, Warnock DE, Schmid SL. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J Cell Biol 1994, 127:915-934.
52. Macia E, Ehrlich M, Massol R, Boucrot E, Brunner C, Kirchhausen T. Dynasore, a cell-permeable inhibitor of dynamin. Dev Cell 2006, 10:839-850.
53. D'Souza-Schorey C, Chavrier P. ARF proteins: roles in membrane traffic and beyond. Nat Rev Mol Cell Biol 2006, 7:347-358.
54. Donaldson JG. Multiple roles for Arf6: sorting, structuring, and signaling at the plasma membrane. J Biol Chem 2003, 278:41573-41576.
55. Blagoveshchenskaya AD, Thomas L, Feliciangeli SF, Hung CH, Thomas G. HIV-1 Nef downregulates MHC-I by a PACS-1- and PI3K-regulated ARF6 endocytic pathway. Cell 2002, 111:853-866.
56. Naslavsky N, Weigert R, Donaldson JG. Convergence of non-clathrin- and clathrin-derived endosomes involves Arf6 inactivation and changes in phosphoinositides. Mol Biol Cell 2003, 14:417-431.
57. Radhakrishna H, Donaldson JG. ADP-ribosylation factor 6 regulates a novel plasma membrane recycling pathway. J Cell Biol 1997, 139:49-61.
58. Brown FD, Rozelle AL, Yin HL, Balla T, Donaldson JG. Phosphatidylinositol 4,5-bisphosphate and Arf6-regulated membrane traffic. J Cell Biol 2001, 154:1007-1017.
59. Swanson JA, Watts C. Macropinocytosis. Trends Cell Biol 1995, 5:424-428.
60. Amyere M, Mettlen M, Van Der Smissen P, Platek A, Payrastre B, Veithen A, Courtoy PJ. Origin, originality, functions, subversions and molecular signalling of macropinocytosis. Int J Med Microbiol 2002, 291:487-494.
61. Nichols BJ, Lippincott-Schwartz J. Endocytosis without clathrin coats. Trends Cell Biol 2001, 11:406-412.
62. Kerr MC, Teasdale RD. Defining macropinocytosis. Traffic 2009, 10:364-371.
63. von Delwig A, Hilkens CM, Altmann DM, Holmdahl R, Isaacs JD, Harding CV, Robertson H, McKie N, Robinson JH. Inhibition of macropinocytosis blocks antigen presentation of type II collagen in vitro and in vivo in HLA-DR1 transgenic mice. Arthritis Res Ther 2006, 8:R93.
64. Engqvist-Goldstein AE, Drubin DG. Actin assembly and endocytosis: from yeast to mammals. Annu Rev Cell Dev Biol 2003, 19:287-332.
65. West MA, Prescott AR, Eskelinen EL, Ridley AJ, Watts C. Rac is required for constitutive macropinocytosis by dendritic cells but does not control its downregulation. Curr Biol 2000, 10:839-848.
66. Garrett WS, Chen LM, Kroschewski R, Ebersold M, Turley S, Trombetta S, Galan JE, Mellman I. Developmental control of endocytosis in dendritic cells by Cdc42. Cell 2000, 102:325-334.
67. Keller HU. Diacylglycerols and PMA are particularly effective stimulators of fluid pinocytosis in human neutrophils. J Cell Physiol 1990, 145:465-471.
68. Ridley AJ, Paterson HF, Johnston CL, Diekmann D, Hall A. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 1992, 70:401-410.
69. Dharmawardhane S, Schurmann A, Sells MA, Chernoff J, Schmid SL, Bokoch GM. Regulation of macropinocytosis by p21-activated kinase-1. Mol Biol Cell 2000, 11:3341-3352.
70. Muro S, Wiewrodt R, Thomas A, Koniaris L, Albelda SM, Muzykantov VR, Koval M. A novel endocytic pathway induced by clustering endothelial ICAM-1 or PECAM-1. J Cell Sci 2003, 116:1599-1609.
71. Wienke DC, Knetsch ML, Neuhaus EM, Reedy MC, Manstein DJ. Disruption of a dynamin homologue affects endocytosis, organelle morphology, and cytokinesis in Dictyostelium discoideum. Mol Biol Cell 1999, 10:225-243.
72. Amyere M, Payrastre B, Krause U, Van Der Smissen P, Veithen A, Courtoy PJ. Constitutive macropinocytosis in oncogene-transformed fibroblasts depends on sequential permanent activation of phosphoinositide 3-kinase and phospholipase C. Mol Biol Cell 2000, 11:3453-3467.
73. Schafer DA, D'Souza-Schorey C, Cooper JA. Actin assembly at membranes controlled by ARF6. Traffic 2000, 1:892-903.
74. Nobes C, Marsh M. Dendritic cells: new roles for Cdc42 and Rac in antigen uptake?. Curr Biol 2000, 10:R739-R741.
75. Norbury CC. Drinking a lot is good for dendritic cells. Immunology 2006, 117:443-451.
76. Falcone S, Cocucci E, Podini P, Kirchhausen T, Clementi E, Meldolesi J. Macropinocytosis: regulated coordination of endocytic and exocytic membrane traffic events. J Cell Sci 2006, 119:4758-4769.
77. de Baey A, Lanzavecchia A. The role of aquaporins in dendritic cell macropinocytosis. J Exp Med 2000, 191:743-748.
78. Mettlen M, Platek A, Van Der Smissen P, Carpentier S, Amyere M, Lanzetti L, de Diesbach P, Tyteca D, Courtoy PJ. Src triggers circular ruffling and macropinocytosis at the apical surface of polarized MDCK cells. Traffic 2006, 7:589-603.
79. Araki N, Johnson MT, Swanson JA. A role for phosphoinositide 3-kinase in the completion of macropinocytosis and phagocytosis by macrophages. J Cell Biol 1996, 135:1249-1260.
80. Cao H, Chen J, Awoniyi M, Henley JR, McNiven MA. Dynamin 2 mediates fluid-phase micropinocytosis in epithelial cells. J Cell Sci 2007, 120:4167-4177.
81. Acconcia F, Sigismund S, Polo S. Ubiquitin in trafficking: the network at work. Exp Cell Res 2009, 315:1610-1618.
82. Ciechanover A, Orian A, Schwartz AL. The ubiquitin-mediated proteolytic pathway: mode of action and clinical implications. J Cell Biochem Suppl 2000, 34:40-51.
83. Weissman AM. Themes and variations on ubiquitylation. Nat Rev Mol Cell Biol 2001, 2:169-178.
84. Mukhopadhyay D, Riezman H. Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 2007, 315:201-205.
85. Pickart CM, Fushman D. Polyubiquitin chains: polymeric protein signals. Curr Opin Chem Biol 2004, 8:610-616.
86. Huang F, Kirkpatrick D, Jiang X, Gygi S, Sorkin A. Differential regulation of EGF receptor internalization and degradation by multiubiquitination within the kinase domain. Mol Cell 2006, 21:737-748.
87. Duncan LM, Piper S, Dodd RB, Saville MK, Sanderson CM, Luzio JP, Lehner PJ. Lysine-63-linked ubiquitination is required for endolysosomal degradation of class I molecules. EMBO J 2006, 25:1635-1645.
88. Sigismund S, Woelk T, Puri C, Maspero E, Tacchetti C, Transidico P, Di Fiore PP, Polo S. Clathrin-independent endocytosis of ubiquitinated cargos. Proc Natl Acad Sci U S A 2005, 102:2760-2765.
89. Molfetta R, Gasparrini F, Peruzzi G, Vian L, Piccoli M, Frati L, Santoni A, Paolini R. Lipid raft-dependent FcepsilonRI ubiquitination regulates receptor endocytosis through the action of ubiquitin binding adaptors. PLoS One 2009, 4:e5604.
90. Maxfield FR, McGraw TE. Endocytic recycling. Nat Rev Mol Cell Biol 2004, 5:121-132.
91. Gruenberg J. The endocytic pathway: a mosaic of domains. Nat Rev Mol Cell Biol 2001, 2:721-730.
92. Zoncu R, Perera RM, Balkin DM, Pirruccello M, Toomre D, De Camilli P. A phosphoinositide switch controls the maturation and signaling properties of APPL endosomes. Cell 2009, 136:1110-1121.
93. Sonnichsen B, De Renzis S, Nielsen E, Rietdorf J, Zerial M. Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J Cell Biol 2000, 149:901-914.
94. Hayakawa A, Leonard D, Murphy S, Hayes S, Soto M, Fogarty K, Standley C, Bellve K, Lambright D, Mello C, Corvera S. The WD40 and FYVE domain containing protein 2 defines a class of early endosomes necessary for endocytosis. Proc Natl Acad Sci U S A 2006, 103:11928-11933.
95. Lakadamyali M, Rust MJ, Zhuang X. Ligands for clathrin-mediated endocytosis are differentially sorted into distinct populations of early endosomes. Cell 2006, 124:997-1009.
96. Zerial M, McBride H. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2001, 2:107-117.
97. Miaczynska M, Zerial M. Mosaic organization of the endocytic pathway. Exp Cell Res 2002, 272:8-14.
98. Spang A. On the fate of early endosomes. Biol Chem 2009, 390:753-759.
99. Rink J, Ghigo E, Kalaidzidis Y, Zerial M. Rab conversion as a mechanism of progression from early to late endosomes. Cell 2005, 122:735-749.
100. Vonderheit A, Helenius A. Rab7 associates with early endosomes to mediate sorting and transport of Semliki forest virus to late endosomes. PLoS Biol 2005, 3:e233.
101. Lanier LL. Up on the tightrope: natural killer cell activation and inhibition. Nat Immunol 2008, 9:495-502.
102. Biassoni R. Human natural killer receptors, co-receptors, and their ligands. Curr Protoc Immunol 2009, 84:14.10.1-14.10.40.
103. Borrego F, Kabat J, Kim DK, Lieto L, Maasho K, Pena J, Solana R, Coligan JE. Structure and function of major histocompatibility complex (MHC) class I specific receptors expressed on human natural killer (NK) cells. Mol Immunol 2002, 38:637-660.
104. Long EO. Negative signaling by inhibitory receptors: the NK cell paradigm. Immunol Rev 2008, 224:70-84.
105. Meyaard L, Adema GJ, Chang C, Woollatt E, Sutherland GR, Lanier LL, Phillips JH. LAIR-1, a novel inhibitory receptor expressed on human mononuclear leukocytes. Immunity 1997, 7:283-290.
106. Tang X, Narayanan S, Peruzzi G, Apara A, Natarajan K, Margulies DH, Coligan JE, Borrego F. A single residue, arginine 65, is critical for the functional interaction of leukocyte-associated inhibitory receptor-1 with collagens. J Immunol 2009, 182:5446-5452.
107. Lebbink RJ, de Ruiter T, Adelmeijer J, Brenkman AB, van Helvoort JM, Koch M, Farndale RW, Lisman T, Sonnenberg A, Lenting PJ, Meyaard L. Collagens are functional, high affinity ligands for the inhibitory immune receptor LAIR-1. J Exp Med 2006, 203:1419-1425.
108. Cantoni C, Bottino C, Augugliaro R, Morelli L, Marcenaro E, Castriconi R, Vitale M, Pende D, Sivori S, Millo R, Biassoni R, Moretta L, Moretta A. Molecular and functional characterization of IRp60, a member of the immunoglobulin superfamily that functions as an inhibitory receptor in human NK cells. Eur J Immunol 1999, 29:3148-3159.
109. Ito M, Maruyama T, Saito N, Koganei S, Yamamoto K, Matsumoto N. Killer cell lectin-like receptor G1 binds three members of the classical cadherin family to inhibit NK cell cytotoxicity. J Exp Med 2006, 203:289-295.
110. Bryceson YT, March ME, Ljunggren HG, Long EO. Synergy among receptors on resting NK cells for the activation of natural cytotoxicity and cytokine secretion. Blood 2006, 107:159-166.
111. Maasho K, Opoku-Anane J, Marusina AI, Coligan JE, Borrego F. NKG2D is a costimulatory receptor for human naive CD8+ T cells. J Immunol 2005, 174:4480-4484.
112. Burgess SJ, Maasho K, Masilamani M, Narayanan S, Borrego F, Coligan JE. The NKG2D receptor: immunobiology and clinical implications. Immunol Res 2008, 40:18-34.
113. Doubrovina ES, Doubrovin MM, Vider E, Sisson RB, O'Reilly RJ, Dupont B, Vyas YM. Evasion from NK cell immunity by MHC class I chain-related molecules expressing colon adenocarcinoma. J Immunol 2003, 171:6891-6899.
114. Ogasawara K, Hamerman JA, Hsin H, Chikuma S, Bour-Jordan H, Chen T, Pertel T, Carnaud C, Bluestone JA, Lanier LL. Impairment of NK cell function by NKG2D modulation in NOD mice. Immunity 2003, 18:41-51.
115. Groh V, Wu J, Yee C, Spies T. Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature 2002, 419:734-738.
116. Salih HR, Rammensee HG, Steinle A. Cutting edge: down-regulation of MICA on human tumors by proteolytic shedding. J Immunol 2002, 169:4098-4102.
117. Roda Navarro P, Reyburn HT. The traffic of the NKG2D/DAP10 receptor complex during NK cell activation. J Biol Chem 2009, 284:16463-16472.
118. Sivori S, Pende D, Bottino C, Marcenaro E, Pessino A, Biassoni R, Moretta L, Moretta A. NKp46 is the major triggering receptor involved in the natural cytotoxicity of fresh or cultured human NK cells. Correlation between surface density of NKp46 and natural cytotoxicity against autologous, allogeneic or xenogeneic target cells. Eur J Immunol 1999, 29:1656-1666.
119. Jarahian M, Watzl C, Fournier P, Arnold A, Djandji D, Zahedi S, Cerwenka A, Paschen A, Schirrmacher V, Momburg F. Activation of natural killer cells by Newcastle disease virus hemagglutinin-neuraminidase. J Virol 2009, 83:8108-8121.
120. Mandelboim O, Lieberman N, Lev M, Paul L, Arnon TI, Bushkin Y, Davis DM, Strominger JL, Yewdell JW, Porgador A. Recognition of haemagglutinins on virus-infected cells by NKp46 activates lysis by human NK cells. Nature 2001, 409:1055-1060.
121. Sivori S, Parolini S, Falco M, Marcenaro E, Biassoni R, Bottino C, Moretta L, Moretta A. 2B4 functions as a co-receptor in human NK cell activation. Eur J Immunol 2000, 30:787-793.
122. Sandusky MM, Messmer B, Watzl C. Regulation of 2B4 (CD244)-mediated NK cell activation by ligand-induced receptor modulation. Eur J Immunol 2006, 36:3268-3276.
123. Wang X, Ottosson A, Ji C, Feng X, Nordenskjold M, Henter JI, Fadeel B, Zheng C. Proteasome inhibition induces apoptosis in primary human natural killer cells and suppresses NKp46-mediated cytotoxicity. Haematologica 2009, 94:470-478.
124. Hazenbos WL, Gessner JE, Hofhuis FM, Kuipers H, Meyer D, Heijnen IA, Schmidt RE, Sandor M, Capel PJ, Daeron M, van de Winkel JG, Verbeek JS. Impaired IgG-dependent anaphylaxis and Arthus reaction in Fc gamma RIII (CD16) deficient mice. Immunity 1996, 5:181-188.
125. Vivier E, Morin P, O'Brien C, Druker B, Schlossman SF, Anderson P. Tyrosine phosphorylation of the Fc gamma RIII(CD16): zeta complex in human natural killer cells. Induction by antibody-dependent cytotoxicity but not by natural killing. J Immunol 1991, 146:206-210.
126. O'Shea JJ, Weissman AM, Kennedy IC, Ortaldo JR. Engagement of the natural killer cell IgG Fc receptor results in tyrosine phosphorylation of the zeta chain. Proc Natl Acad Sci U S A 1991, 88:350-354.
127. Cecchetti S, Spadaro F, Lugini L, Podo F, Ramoni C. Functional role of phosphatidylcholine-specific phospholipase C in regulating CD16 membrane expression in natural killer cells. Eur J Immunol 2007, 37:2912-2922.
128. Borrego F, Lopez-Beltran A, Pena J, Solana R. Downregulation of Fc gamma receptor IIIA alpha (CD16-II) on natural killer cells induced by anti-CD16 mAb is independent of protein tyrosine kinases and protein kinase C. Cell Immunol 1994, 158:208-217.
129. Harrison D, Phillips JH, Lanier LL. Involvement of a metalloprotease in spontaneous and phorbol ester-induced release of natural killer cell-associated Fc gamma RIII (CD16-II). J Immunol 1991, 147:3459-3465.
130. Paolini R, Serra A, Molfetta R, Piccoli M, Frati L, Santoni A. Tyrosine kinase-dependent ubiquitination of CD16 zeta subunit in human NK cells following receptor engagement. Eur J Immunol 1999, 29:3179-3187.
131. Morandi B, Costa R, Falco M, Parolini S, De Maria A, Ratto G, Mingari MC, Melioli G, Moretta A, Ferlazzo G. Distinctive lack of CD48 expression in subsets of human dendritic cells tunes NK cell activation. J Immunol 2005, 175:3690-3697.
132. Sivori S, Falco M, Marcenaro E, Parolini S, Biassoni R, Bottino C, Moretta L, Moretta A. Early expression of triggering receptors and regulatory role of 2B4 in human natural killer cell precursors undergoing in vitro differentiation. Proc Natl Acad Sci U S A 2002, 99:4526-4531.
133. Lee KM, McNerney ME, Stepp SE, Mathew PA, Schatzle JD, Bennett M, Kumar V. 2B4 acts as a non-major histocompatibility complex binding inhibitory receptor on mouse natural killer cells. J Exp Med 2004, 199:1245-1254.
134. Bhat R, Eissmann P, Endt J, Hoffmann S, Watzl C. Fine-tuning of immune responses by SLAM-related receptors. J Leukoc Biol 2006, 79:417-424.
135. Assarsson E, Kambayashi T, Persson CM, Ljunggren HG, Chambers BJ. 2B4 co-stimulation: NK cells and their control of adaptive immune responses. Mol Immunol 2005, 42:419-423.
136. McNerney ME, Lee KM, Kumar V. 2B4 (CD244) is a non-MHC binding receptor with multiple functions on natural killer cells and CD8+ T cells. Mol Immunol 2005, 42:489-494.
137. Boles KS, Stepp SE, Bennett M, Kumar V, Mathew PA. 2B4 (CD244) and CS1: novel members of the CD2 subset of the immunoglobulin superfamily molecules expressed on natural killer cells and other leukocytes. Immunol Rev 2001, 181:234-249.
138. Welstead GG, Hsu EC, Iorio C, Bolotin S, Richardson CD. Mechanism of CD150 (SLAM) down regulation from the host cell surface by measles virus hemagglutinin protein. J Virol 2004, 78:9666-9674.
139. Del Valle JM, Engel P, Martin M. The cell surface expression of SAP-binding receptor CD229 is regulated via its interaction with clathrin-associated adaptor complex 2 (AP-2). J Biol Chem 2003, 278:17430-17437.
140. Borrego F, Masilamani M, Marusina AI, Tang X, Coligan JE. The CD94/NKG2 family of receptors: from molecules and cells to clinical relevance. Immunol Res 2006, 35:263-278.
141. Brooks AG, Posch PE, Scorzelli CJ, Borrego F, Coligan JE. NKG2A complexed with CD94 defines a novel inhibitory natural killer cell receptor. J Exp Med 1997, 185:795-800.
142. Borrego F, Ulbrecht M, Weiss EH, Coligan JE, Brooks AG. Recognition of human histocompatibility leukocyte antigen (HLA)-E complexed with HLA class I signal sequence-derived peptides by CD94/NKG2 confers protection from natural killer cell-mediated lysis. J Exp Med 1998, 187:813-818.
143. Carretero M, Palmieri G, Llano M, Tullio V, Santoni A, Geraghty DE, Lopez-Botet M. Specific engagement of the CD94/NKG2-A killer inhibitory receptor by the HLA-E class Ib molecule induces SHP-1 phosphatase recruitment to tyrosine-phosphorylated NKG2-A: evidence for receptor function in heterologous transfectants. Eur J Immunol 1998, 28:1280-1291.
144. Kabat J, Borrego F, Brooks A, Coligan JE. Role that each NKG2A immunoreceptor tyrosine-based inhibitory motif plays in mediating the human CD94/NKG2A inhibitory signal. J Immunol 2002, 169:1948-1958.
145. Le Drean E, Vely F, Olcese L, Cambiaggi A, Guia S, Krystal G, Gervois N, Moretta A, Jotereau F, Vivier E. Inhibition of antigen-induced T cell response and antibody-induced NK cell cytotoxicity by NKG2A: association of NKG2A with SHP-1 and SHP-2 protein-tyrosine phosphatases. Eur J Immunol 1998, 28:264-276.
146. Borrego F, Masilamani M, Kabat J, Sanni TB, Coligan JE. The cell biology of the human natural killer cell CD94/NKG2A inhibitory receptor. Mol Immunol 2005, 42:485-488.
147. Masilamani M, Nguyen C, Kabat J, Borrego F, Coligan JE. CD94/NKG2A inhibits NK cell activation by disrupting the actin network at the immunological synapse. J Immunol 2006, 177:3590-3596.
148. Sanni TB, Masilamani M, Kabat J, Coligan JE, Borrego F. Exclusion of lipid rafts and decreased mobility of CD94/NKG2A receptors at the inhibitory NK cell synapse. Mol Biol Cell 2004, 15:3210-3223.
149. Borrego F, Kabat J, Sanni TB, Coligan JE. NK cell CD94/NKG2A inhibitory receptors are internalized and recycle independently of inhibitory signaling processes. J Immunol 2002, 169:6102-6111.
150. Lanier LL, Corliss B, Wu J, Phillips JH. Association of DAP12 with activating CD94/NKG2C NK cell receptors. Immunity 1998, 8:693-701.
151. Wood SA, Park JE, Brown WJ. Brefeldin A causes a microtubule-mediated fusion of the trans-Golgi network and early endosomes. Cell 1991, 67:591-600.
152. Lippincott-Schwartz J, Yuan L, Tipper C, Amherdt M, Orci L, Klausner RD. Brefeldin A's effects on endosomes, lysosomes, and the TGN suggest a general mechanism for regulating organelle structure and membrane traffic. Cell 1991, 67:601-616.
153. Moretta L, Moretta A. Killer immunoglobulin-like receptors. Curr Opin Immunol 2004, 16:626-633.
154. Lanier LL, Corliss BC, Wu J, Leong C, Phillips JH. Immunoreceptor DAP12 bearing a tyrosine-based activation motif is involved in activating NK cells. Nature 1998, 391:703-707.
155. Kikuchi-Maki A, Yusa S, Catina TL, Campbell KS. KIR2DL4 is an IL-2-regulated NK cell receptor that exhibits limited expression in humans but triggers strong IFN-gamma production. J Immunol 2003, 171:3415-3425.
156. Rajagopalan S, Bryceson YT, Kuppusamy SP, Geraghty DE, van der Meer A, Joosten I, Long EO. Activation of NK cells by an endocytosed receptor for soluble HLA-G. PLoS Biol 2006, 4:e9.
157. Rajagopalan S, Fu J, Long EO. Cutting edge: induction of IFN-gamma production but not cytotoxicity by the killer cell Ig-like receptor KIR2DL4 (CD158d) in resting NK cells. J Immunol 2001, 167:1877-1881.
158. Kikuchi-Maki A, Catina TL, Campbell KS. Cutting edge: KIR2DL4 transduces signals into human NK cells through association with the Fc receptor gamma protein. J Immunol 2005, 174:3859-3863.
159. Miah SM, Hughes TL, Campbell KS. KIR2DL4 differentially signals downstream functions in human NK cells through distinct structural modules. J Immunol 2008, 180:2922-2932.
160. Huard B, Karlsson L. KIR expression on self-reactive CD8+ T cells is controlled by T-cell receptor engagement. Nature 2000, 403:325-328.
161. Huard B, Karlsson L, Triebel F. KIR down-regulation on NK cells is associated with down-regulation of activating receptors and NK cell inactivation. Eur J Immunol 2001, 31:1728-1735.
162. Chwae YJ, Lee JM, Kim EJ, Lee ST, Soh JW, Kim J. Activation-induced upregulation of inhibitory killer Ig-like receptors is regulated by protein kinase C. Immunol Cell Biol 2007, 85:220-228.
163. Chwae YJ, Lee JM, Kim HR, Kim EJ, Lee ST, Soh JW, Kim J. Amino-acid sequence motifs for PKC-mediated membrane trafficking of the inhibitory killer Ig-like receptor. Immunol Cell Biol 2008, 86:372-380.
164. Alvarez-Arias DA, Campbell KS. Protein kinase C regulates expression and function of inhibitory killer cell Ig-like receptors in NK cells. J Immunol 2007, 179:5281-5290.
165. van der Meer A, Lukassen HG, van Lierop MJ, Wijnands F, Mosselman S, Braat DD, Joosten I. Membrane-bound HLA-G activates proliferation and interferon-gamma production by uterine natural killer cells. Mol Hum Reprod 2004, 10:189-195.
166. Ortaldo JR, Mason AT, O'Shea JJ. Receptor-induced death in human natural killer cells: involvement of CD16. J Exp Med 1995, 181:339-344.
167. Poggi A, Massaro AM, Negrini S, Contini P, Zocchi MR. Tumor-induced apoptosis of human IL-2-activated NK cells: role of natural cytotoxicity receptors. J Immunol 2005, 174:2653-2660.
168. Lou Z, Jevremovic D, Billadeau DD, Leibson PJ. A balance between positive and negative signals in cytotoxic lymphocytes regulates the polarization of lipid rafts during the development of cell-mediated killing. J Exp Med 2000, 191:347-354.
169. Watzl C, Long EO. Natural killer cell inhibitory receptors block actin cytoskeleton-dependent recruitment of 2B4 (CD244) to lipid rafts. J Exp Med 2003, 197:77-85.
170. Krzewski K, Chen X, Orange JS, Strominger JL. Formation of a WIP- , WASp-, actin-, and myosin IIA-containing multiprotein complex in activated NK cells and its alteration by KIR inhibitory signaling. J Cell Biol 2006, 173:121-132.
171. May RC, Machesky LM. Phagocytosis and the actin cytoskeleton. J Cell Sci 2001, 114:1061-1077.
172. Welch MD, Mullins RD. Cellular control of actin nucleation. Annu Rev Cell Dev Biol 2002, 18:247-288.
173. Stebbins CC, Watzl C, Billadeau DD, Leibson PJ, Burshtyn DN, Long EO. Vav1 dephosphorylation by the tyrosine phosphatase SHP-1 as a mechanism for inhibition of cellular cytotoxicity. Mol Cell Biol 2003, 23:6291-6299.