Uncommon endocytic and trafficking pathway of the natural killer cell CD94/NKG2A inhibitory receptor

Traffic

Volumn 9, Issue 6, 2008, Pages 1019-1034

  Masilamani, Madhan ^a,b   Narayanan, Sriram ^a   Prieto, Martha ^a   Borrego, Francisco ^a   Coligan, John E ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

CD94 NKG2A; Endocytosis; Inhibitory receptor; Natural killer cells; Trafficking

Indexed keywords

ACTIN; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; AMILORIDE; CD94 ANTIGEN; CLATHRIN; DYNAMIN; EARLY ENDOSOME ANTIGEN 1; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; NATURAL KILLER CELL RECEPTOR NKG2A; PHOSPHATIDYLINOSITOL 3 KINASE; RAB PROTEIN; RAB11 PROTEIN; RAB4 PROTEIN; RAB5 PROTEIN; RAB7 PROTEIN; RAC1 PROTEIN;

ANIMAL CELL; ARTICLE; CELL COMPARTMENTALIZATION; CELL VACUOLE; CONTROLLED STUDY; CYTOSKELETON; ENDOCYTOSIS; ENDOSOME; INTRACELLULAR TRANSPORT; LIPID RAFT; LYSOSOME; NATURAL KILLER CELL; NONHUMAN; PINOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; RAT;

ANTIGENS, CD94; DYNAMINS; ENDOCYTOSIS; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GREEN FLUORESCENT PROTEINS; HUMANS; HYDRAZONES; KILLER CELLS, NATURAL; PROTEIN TRANSPORT; RECEPTORS, IMMUNOLOGIC; RNA INTERFERENCE; RNA, SMALL INTERFERING;

EID: 43149089544     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2008.00738.x     Document Type: Article

References (77)

1. Lanier LL. NK cell recognition. Annu Rev Immunol 2005;23:225-274.
2. Hallett WH, Murphy WJ. Positive and negative regulation of natural killer cells: Therapeutic implications. Semin Cancer Biol 2006;16:367-382.
3. 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.
4. Guma M, Angulo A, Lopez-Botet M. NK cell receptors involved in the response to human cytomegalovirus infection. Curr Top Microbiol Immunol 2006; 298:207-223.
5. 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.
6. 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.
7. 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.
8. 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.
9. 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.
10. Maxfield FR, McGraw TE. Endocytic recycling. Nat Rev Mol Cell Biol 2004;5:121-132.
11. 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.
12. Fujimoto LM, Roth R, Heuser JE, Schmid SL. Actin assembly plays a variable, but not obligatory role in receptor-mediated endocytosis in mammalian cells. Traffic 2000;1:161-171.
13. Kaksonen M, Toret CP, Drubin DG. Harnessing actin dynamics for clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 2006;7:404-414.
14. 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.
15. Lamaze C, Fujimoto LM, Yin HL, Schmid SL. The actin cytoskeleton is required for receptor-mediated endocytosis in mammalian cells. J Biol Chem 1997;272:20332-20335.
16. Bonifacino JS, Traub LM. Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu Rev Biochem 2003;72:395-447.
17. Conner SD, Schmid SL. Regulated portals of entry into the cell. Nature 2003;422:37-44.
18. Blitzer JT, Nusse R. A critical role for endocytosis in Wnt signaling. BMC Cell Biol 2006;7:28.
19. Jacquier V, Prummer M, Segura JM, Pick H, Vogel H. Visualizing odorant receptor trafficking in living cells down to the single-molecule level. Proc Natl Acad Sci U S A 2006;103:14325-14330.
20. 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.
21. Henley JR, Krueger EW, Oswald BJ, McNiven MA, Dynamin-mediated internalization of caveolae. J Cell Biol 1998;141:85-99.
22. Gomez TS, Hamann MJ, McCarney S, Savoy DN, Lubking CM, Heldebrant MP, Labno CM, McKean DJ, McNiven MA, Burkhardt JK, Billadeau DD. Dynamin 2 regulates T cell activation by controlling actin polymerization at the immunological synapse. Nat Immunol 2005;6:261-270.
23. 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.
24. 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.
25. 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.
26. Le Roy C, Wrana JL. Clathrin- and non-clathrin-mediated endocytic regulation of cell signalling. Nat Rev Mol Cell Biol 2005;6:112-126.
27. 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.
28. Glebov OO, Bright NA, Nichols BJ. Flotillin-1 defines a clathrin-independent endocytic pathway in mammalian cells. Nat Cell Biol 2006;8:46-54.
29. 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.
30. Crimeen-Irwin B, Ellis S, Christiansen D, Ludford-Menting MJ, Milland J, Lanteri M, Loveland BE, Gerlier D, Russell SM. Ligand binding determines whether CD46 is internalized by clathrin-coated pits or macropinocytosis. J Biol Chem 2003;278:46927-46937.
31. Baravalle G, Schober D, Huber M, Bayer N, Murphy RF, Fuchs R. Transferrin recycling and dextran transport to lysosomes is differentially affected by bafilomycin, nocodazole, and low temperature. Cell Tissue Res 2005;320:99-113.
32. van Dam EM, Ten Broeke T, Jansen K, Spijkers P, Stoorvogel W. Endocytosed transferrin receptors recycle via distinct dynamin and phosphatidylinositol 3-kinase-dependent pathways. J Biol Chem 2002;277:48876-48883.
33. West MA, Bretscher MS, Watts C. Distinct endocytotic pathways in epidermal growth factor-stimulated human carcinoma A431 cells. J Cell Biol 1989;109:2731-2739.
34. 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.
35. Ellis S, Mellor H. Regulation of endocytic traffic by rho family GTPases. Trends Cell Biol 2000;10:85-88.
36. 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.
37. 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.
38. Lamaze C, Chuang TH, Terlecky LJ, Bokoch GM, Schmid SL. Regulation of receptor-mediated endocytosis by Rho and Rac. Nature 1996;382:177-179.
39. 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.
40. Swanson JA, Watts C. Macropinocytosis. Trends Cell Biol 1995;5:424-428.
41. 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.
42. Radhakrishna H, Donaldson JG. ADP-ribosylation factor 6 regulates a novel plasma membrane recycling pathway. J Cell Biol 1997;139:49-61.
43. Carter LL, Redelmeier TE, Woollenweber LA, Schmid SL. Multiple GTP-binding proteins participate in clathrin-coated vesicle-mediated endocytosis. J Cell Biol 1993;120: 37-45.
44. Radhakrishna H, Klausner RD, Donaldson JG. Aluminum fluoride stimulates surface protrusions in cells overexpressing the ARF6 GTPase. J Cell Biol 1996;134:935-947.
45. Naslavsky N, Weigert R, Donaldson JG. Characterization of a nonclathrin endocytic pathway: Membrane cargo and lipid requirements. Mol Biol Cell 2004;15:3542-3552.
46. 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.
47. Holm PK, Eker P, Sandvig K, van Deurs B. Phorbol myristate acetate selectively stimulates apical endocytosis via protein kinase C in polarized MDCK cells. Exp Cell Res 1995;217:157-168.
48. Grimmer S, van Deurs B, Sandvig K. Membrane ruffling and macropinocytosis in A431 cells require cholesterol. J Cell Sci 2002;115:2953-2962.
49. Lindmo K, Stenmark H. Regulation of membrane traffic by phosphoinositide 3-kinases. J Cell Sci 2006;119:605-614.
50. Zerial M, McBride H. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2001;2:107-117.
51. Stenmark H, Parton RG, Steele-Mortimer O, Lutcke A, Gruenberg J, Zerial M. Inhibition of rab5 GTPase activity stimulates membrane fusion in endocytosis. EMBO J 1994;13:1287-1296.
52. Ceresa BP, Lotscher M, Schmid SL. Receptor and membrane recycling can occur with unaltered efficiency despite dramatic Rab5(q79l)-induced changes in endosome geometry. J Biol Chem 2001;276:9649-9654.
53. Alcover A, Alarcon B. Internalization and intracellular fate of TCR-CD3 complexes. Crit Rev Immunol 2000;20:325-346.
54. Stoddart A, Jackson AP, Brodsky FM. Plasticity of B cell receptor internalization upon conditional depletion of clathrin. Mol Biol Cell 2005;16:2339-2348.
55. Dikic I. Mechanisms controlling EGF receptor endocytosis and degradation. Biochem Soc Trans 2003;31:1178-1181.
56. 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.
57. Coudert JD, Zimmer J, Tomasello E, Cebecauer M, Colonna M, Vivier E, Held W. Altered NKG2D function in NK cells induced by chronic exposure to NKG2D ligand-expressing tumor cells. Blood 2005;106:1711-1717.
58. 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.
59. 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.
60. Jones AT. Macropinocytosis: Searching for an endocytic identity and role in the uptake of cell penetrating peptides. J Cell Mol Med 2007;11:670-684.
61. Mayor S, Pagano RE. Pathways of clathrin-independent endocytosis. Nat Rev Mol Cell Biol 2007;8:603-612.
62. Engqvist-Goldstein AE, Drubin DG. Actin assembly and endocytosis: From yeast to mammals. Annu Rev Cell Dev Biol 2003;19:287-332.
63. 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.
64. Damke H, Baba T, van der Bliek AM, Schmid SL. Clathrin-independent pinocytosis is induced in cells overexpressing a temperature-sensitive mutant of dynamin. J Cell Biol 1995;131:69-80.
65. Benmerah A, Lamaze C. Clathrin-coated pits: Vive la difference? Traffic 2007;8:970-982.
66. 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.
67. Long EO, Barber DF, Burshtyn DN, Faure M, Peterson M, Rajagopalan S, Renard V, Sandusky M, Stebbins CC, Wagtmann N, Watzl C. Inhibition of natural killer cell activation signals by killer cell immunoglobulin-like receptors (CD158). Immunol Rev 2001;181:223-233.
68. Maasho K, Masilamani M, Valas R, Basu S, Coligan JE, Borrego F. The inhibitory leukocyte-associated Ig-like receptor-1 (LAIR-1) is expressed at high levels by human naive T cells and inhibits TCR mediated activation. Mol Immunol 2005;42:1521-1530.
69. 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.
70. 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.
71. Ridley AJ. Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol 2006;16:522-529.
72. Hasegawa T. Production of a unique antibody specific for membrane ruffles and its use to characterize the behavior of two distinct types of ruffles. J Cell Biol 1993;120:1439-1448.
73. 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.
74. van der Goot FG, Gruenberg J. Intra-endosomal membrane traffic. Trends Cell Biol 2006;16:514-521.
75. Dietrich J, Menne C, Lauritsen JP, von Essen M, Rasmussen AB, Odum N, Geisler C. Ligand-induced TCR down-regulation is not dependent on constitutive TCR cycling. J Immunol 2002;168:5434-5440.
76. Maasho K, Marusina A, Reynolds NM, Coligan JE, Borrego F. Efficient gene transfer into the human natural killer cell line, NKL, using the Amaxa nucleofection system. J Immunol Methods 2004;284:133-140.
77. Costes SV, Daelemans D, Cho EH, Dobbin Z, Pavlakis G, Lockett S. Automatic and quantitative measurement of protein-protein colocalization in live cells. Biophys J 2004;86:3993-4003.