Degranulation of natural killer cells following interaction with HIV-1-infected cells is hindered by downmodulation of NTB-A by Vpu

Cell Host and Microbe

Volumn 8, Issue 5, 2010, Pages 397-409

  Shah, Ankur H ^a   Sowrirajan, Bharatwaj ^a   Davis, Zachary B ^a   Ward, Jeffrey P ^b   Campbell, Edward M ^c   Planelles, Vicente ^d   Barker, Edward ^a  

^a RUSH UNIVERSITY MEDICAL CENTER   (United States)

^b State University of New York Upstate Medical University: College of Medicine   (United States)

^c LOYOLA UNIVERSITY CHICAGO   (United States)

^d UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD14 ANTIGEN; CD20 ANTIGEN; CD3 ANTIGEN; CD4 ANTIGEN; CD56 ANTIGEN; CD69 ANTIGEN; LIGAND; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; NATURAL KILLER CELL COACTIVATION RECEPTOR NKT AND B CELL ANTIGEN; NATURAL KILLER CELL RECEPTOR; NATURAL KILLER CELL RECEPTOR NKG2D; UNCLASSIFIED DRUG; VPR PROTEIN; VPU PROTEIN;

ANIMAL CELL; ARTICLE; CD4+ T LYMPHOCYTE; CELL ACTIVATION; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; CYTOLYSIS; DEGRANULATION; DOWN REGULATION; ENDOCYTOSIS; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RECEPTOR BINDING;

ANTIGENS, CD; CELL DEGRANULATION; CELL LINE; CYTOTOXICITY, IMMUNOLOGIC; DOWN-REGULATION; HELA CELLS; HIV-1; HUMAN IMMUNODEFICIENCY VIRUS PROTEINS; HUMANS; JURKAT CELLS; KILLER CELLS, NATURAL; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K; RECEPTORS, CELL SURFACE; T-LYMPHOCYTES; VIRAL REGULATORY AND ACCESSORY PROTEINS;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 78349264184     PISSN: 19313128     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chom.2010.10.008     Document Type: Article

References (51)

1. G. Alter, J.M. Malenfant, and M. Altfeld CD107a as a functional marker for the identification of natural killer cell activity J. Immunol. Methods 294 2004 15 22 (Pubitemid 39626587)
2. J.L. Andersen, J.L. DeHart, E.S. Zimmerman, O. Ardon, B. Kim, G. Jacquot, S. Benichou, and V. Planelles HIV-1 Vpr-induced apoptosis is cell cycle dependent and requires Bax but not ANT PLoS Pathog. 2 2006 e127 10.1371/journal.ppat.0020127
3. S. Bauer, V. Groh, J. Wu, A. Steinle, J.H. Phillips, L.L. Lanier, and T. Spies Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA Science 285 1999 727 729
4. M.I. Bonaparte, and E. Barker Inability of natural killer cells to destroy autologous HIV-infected T lymphocytes AIDS 17 2003 487 494
5. M.I. Bonaparte, and E. Barker Killing of human immunodeficiency virus-infected primary T-cell blasts by autologous natural killer cells is dependent on the ability of the virus to alter the expression of major histocompatibility complex class I molecules Blood 104 2004 2087 2094
6. F. Borrego, J. Kabat, D.K. Kim, L. Lieto, K. Maasho, J. Pena, R. Solana, and J.E. Coligan Structure and function of major histocompatibility complex (MHC) class I specific receptors expressed on human natural killer (NK) cells Mol. Immunol. 38 2002 637 660
7. A. Bosque, and V. Planelles Induction of HIV-1 latency and reactivation in primary memory CD4+ T cells Blood 113 2009 58 65
8. C. Bottino, M. Falco, S. Parolini, E. Marcenaro, R. Augugliaro, S. Sivori, E. Landi, R. Biassoni, L.D. Notarangelo, and L. Moretta NTB-A [correction of GNTB-A], a novel SH2D1A-associated surface molecule contributing to the inability of natural killer cells to kill Epstein-Barr virus-infected B cells in X-linked lymphoproliferative disease J. Exp. Med. 194 2001 235 246
9. S. Bour, and K. Strebel The human immunodeficiency virus (HIV) type 2 envelope protein is a functional complement to HIV type 1 Vpu that enhances particle release of heterologous retroviruses J. Virol. 70 1996 8285 8300
10. V.M. Braud, D.S. Allan, C.A. O'Callaghan, K. Soderstrom, A. D'Andrea, G.S. Ogg, S. Lazetic, N.T. Young, J.I. Bell, and J.H. Phillips HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C Nature 391 1998 795 799
11. Y.T. Bryceson, M.E. March, D.F. Barber, H.G. Ljunggren, and E.O. Long Cytolytic granule polarization and degranulation controlled by different receptors in resting NK cells J. Exp. Med. 202 2005 1001 1012
12. Y.T. Bryceson, M.E. March, H.G. Ljunggren, and E.O. Long Activation, coactivation, and costimulation of resting human natural killer cells Immunol. Rev. 214 2006 73 91
13. Y.T. Bryceson, M.E. March, H.G. Ljunggren, and E.O. Long Synergy among receptors on resting NK cells for the activation of natural cytotoxicity and cytokine secretion Blood 107 2006 159 166
14. Y.T. Bryceson, H.G. Ljunggren, and E.O. Long Minimal requirement for induction of natural cytotoxicity and intersection of activation signals by inhibitory receptors Blood 114 2009 2657 2666
15. E. Ciccone, D. Pende, O. Viale, A. Than, C. Di Donato, A.M. Orengo, R. Biassoni, S. Verdiani, A. Amoroso, and A. Moretta Involvement of HLA class I alleles in natural killer (NK) cell-specific functions: expression of HLA-Cw3 confers selective protection from lysis by alloreactive NK clones displaying a defined specificity (specificity 2) J. Exp. Med. 176 1992 963 971
16. G.B. Cohen, R.T. Gandhi, D.M. Davis, O. Mandelboim, B.K. Chen, J.L. Strominger, and D. Baltimore The selective downregulation of class I major histocompatibility complex proteins by HIV-1 protects HIV-infected cells from NK cells Immunity 10 1999 661 671
17. K.L. Collins, B.K. Chen, S.A. Kalams, B.D. Walker, and D. Baltimore HIV-1 Nef protein protects infected primary cells against killing by cytotoxic T lymphocytes Nature 391 1998 397 401
18. C. Dohring, D. Scheidegger, J. Samaridis, M. Cella, and M. Colonna A human killer inhibitory receptor specific for HLA-A1,2 J. Immunol. 156 1996 3098 3101 (Pubitemid 26123520)
19. J.L. Douglas, J.K. Gustin, K. Viswanathan, M. Mansouri, A.V. Moses, and K. Fruh The great escape: viral strategies to counter BST-2/tetherin PLoS Pathog. 6 2010 e1000913 10.1371/journal.ppat.1000913
20. M. Falco, E. Marcenaro, E. Romeo, F. Bellora, D. Marras, F. Vely, G. Ferracci, L. Moretta, A. Moretta, and C. Bottino Homophilic interaction of NTBA, a member of the CD2 molecular family: induction of cytotoxicity and cytokine release in human NK cells Eur. J. Immunol. 34 2004 1663 1672
21. R.M. Flaig, S. Stark, and C. Watzl Cutting edge: NTB-A activates NK cells via homophilic interaction J. Immunol. 172 2004 6524 6527
22. M. Fogli, D. Mavilio, E. Brunetta, S. Varchetta, K. Ata, G. Roby, C. Kovacs, D. Follmann, D. Pende, and J. Ward Lysis of endogenously infected CD4+ T cell blasts by rIL-2 activated autologous natural killer cells from HIV-infected viremic individuals PLoS Pathog. 4 2008 e1000101 10.1371/journal.ppat.1000101
23. J.V. Garcia, and A.D. Miller Serine phosphorylation-independent downregulation of cell-surface CD4 by nef Nature 350 1991 508 511
24. T. Kerkau, I. Bacik, J.R. Bennink, J.W. Yewdell, T. Hunig, A. Schimpl, and U. Schubert The human immunodeficiency virus type 1 (HIV-1) Vpu protein interferes with an early step in the biosynthesis of major histocompatibility complex (MHC) class I molecules J. Exp. Med. 185 1997 1295 1305
25. L.L. Lanier NK cell recognition Annu. Rev. Immunol. 23 2005 225 274
26. L.L. Lanier Up on the tightrope: natural killer cell activation and inhibition Nat. Immunol. 9 2008 495 502
27. F. Margottin, S.P. Bour, H. Durand, L. Selig, S. Benichou, V. Richard, D. Thomas, K. Strebel, and R. Benarous A novel human WD protein, h-beta TrCp, that interacts with HIV-1 Vpu connects CD4 to the ER degradation pathway through an F-box motif Mol. Cell 1 1998 565 574
28. R.S. Mitchell, C. Katsura, M.A. Skasko, K. Fitzpatrick, D. Lau, A. Ruiz, E.B. Stephens, F. Margottin-Goguet, R. Benarous, and J.C. Guatelli Vpu antagonizes BST-2-mediated restriction of HIV-1 release via beta-TrCP and endo-lysosomal trafficking PLoS Pathog. 5 2009 e1000450 10.1371/journal.ppat. 1000450
29. M. Moll, S.K. Andersson, A. Smed-Sorensen, and J.K. Sandberg Inhibition of lipid antigen presentation in dendritic cells by HIV-1 Vpu interference with CD1d recycling from endosomal compartments Blood 116 2010 1876 1884
30. L. Moretta, and A. Moretta Unravelling natural killer cell function: triggering and inhibitory human NK receptors EMBO J. 23 2004 255 259 (Pubitemid 38294490)
31. A. Moretta, S. Sivori, M. Vitale, D. Pende, L. Morelli, R. Augugliaro, C. Bottino, and L. Moretta Existence of both inhibitory (p58) and activatory (p50) receptors for HLA-C molecules in human natural killer cells J. Exp. Med. 182 1995 875 884
32. A. Moretta, R. Biassoni, C. Bottino, D. Pende, M. Vitale, A. Poggi, M.C. Mingari, and L. Moretta Major histocompatibility complex class I-specific receptors on human natural killer and T lymphocytes Immunol. Rev. 155 1997 105 117
33. A. Moretta, C. Bottino, M. Vitale, D. Pende, C. Cantoni, M.C. Mingari, R. Biassoni, and L. Moretta Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis Annu. Rev. Immunol. 19 2001 197 223
34. K. Natarajan, N. Dimasi, J. Wang, R.A. Mariuzza, and D.H. Margulies Structure and function of natural killer cell receptors: multiple molecular solutions to self, nonself discrimination Annu. Rev. Immunol. 20 2002 853 885
35. S.J. Neil, T. Zang, and P.D. Bieniasz Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu Nature 451 2008 425 430
36. D. Pende, S. Parolini, A. Pessino, S. Sivori, R. Augugliaro, L. Morelli, E. Marcenaro, L. Accame, A. Malaspina, and R. Biassoni Identification and molecular characterization of NKp30, a novel triggering receptor involved in natural cytotoxicity mediated by human natural killer cells J. Exp. Med. 190 1999 1505 1516
37. A. Pessino, S. Sivori, C. Bottino, A. Malaspina, L. Morelli, L. Moretta, R. Biassoni, and A. Moretta Molecular cloning of NKp46: a novel member of the immunoglobulin superfamily involved in triggering of natural cytotoxicity J. Exp. Med. 188 1998 953 960
38. P.J. Peters, J. Borst, V. Oorschot, M. Fukuda, O. Krahenbuhl, J. Tschopp, J.W. Slot, and H.J. Geuze Cytotoxic T lymphocyte granules are secretory lysosomes, containing both perforin and granzymes J. Exp. Med. 173 1991 1099 1109
39. J. Richard, S. Sindhu, T.N. Pham, J.P. Belzile, and E.A. Cohen HIV-1 Vpr upregulates expression of ligands for the activating NKG2D receptor and promotes NK cell-mediated killing Blood 115 2010 1354 1363
40. F.W. Ruscetti, J.A. Mikovits, V.S. Kalyanaraman, R. Overton, H. Stevenson, K. Stromberg, R.B. Herberman, W.L. Farrar, and J.R. Ortaldo Analysis of effector mechanisms against HTLV-I- and HTLV-III/LAV-infected lymphoid cells J. Immunol. 136 1986 3619 3624
41. U. Schubert, A.V. Ferrer-Montiel, M. Oblatt-Montal, P. Henklein, K. Strebel, and M. Montal Identification of an ion channel activity of the Vpu transmembrane domain and its involvement in the regulation of virus release from HIV-1-infected cells FEBS Lett. 398 1996 12 18
42. U. Schubert, L.C. Anton, I. Bacik, J.H. Cox, S. Bour, J.R. Bennink, M. Orlowski, K. Strebel, and J.W. Yewdell CD4 glycoprotein degradation induced by human immunodeficiency virus type 1 Vpu protein requires the function of proteasomes and the ubiquitin-conjugating pathway J. Virol. 72 1998 2280 2288
43. O. Schwartz, V. Marechal, S. Le Gall, F. Lemonnier, and J.M. Heard Endocytosis of major histocompatibility complex class I molecules is induced by the HIV-1 Nef protein Nat. Med. 2 1996 338 342
44. C. Tomescu, J. Chehimi, V.C. Maino, and L.J. Montaner N. cell lysis of HIV-1-infected autologous CD4 primary T cells: requirement for IFN-mediated NK activation by plasmacytoid dendritic cells J. Immunol. 179 2007 2097 2104
45. B. Tycko, C.H. Keith, and F.R. Maxfield Rapid acidification of endocytic vesicles containing asialoglycoprotein in cells of a human hepatoma line J. Cell Biol. 97 1983 1762 1776
46. N. Van Damme, D. Goff, C. Katsura, R.L. Jorgenson, R. Mitchell, M.C. Johnson, E.B. Stephens, and J. Guatelli The interferon-induced protein BST-2 restricts HIV-1 release and is downregulated from the cell surface by the viral Vpu protein Cell Host Microbe 3 2008 245 252
47. J. Ward, M. Bonaparte, J. Sacks, J. Guterman, M. Fogli, D. Mavilio, and E. Barker HIV modulates the expression of ligands important in triggering natural killer cell cytotoxic responses on infected primary T-cell blasts Blood 110 2007 1207 1214
48. J. Ward, Z. Davis, J. DeHart, E. Zimmerman, A. Bosque, E. Brunetta, D. Mavilio, V. Planelles, and E. Barker HIV-1 Vpr triggers natural killer cell-mediated lysis of infected cells through activation of the ATR-mediated DNA damage response PLoS Pathog. 5 2009 e1000613 10.1371/journal.ppat.1000613
49. R.L. Willey, F. Maldarelli, M.A. Martin, and K. Strebel Human immunodeficiency virus type 1 Vpu protein induces rapid degradation of CD4 J. Virol. 66 1992 7193 7200
50. Z.Y. Zheng, and D. Zucker-Franklin Apparent ineffectiveness of natural killer cells vis-a-vis retrovirus-infected targets J. Immunol. 148 1992 3679 3685
51. S.F. Ziegler, F. Ramsdell, and M.R. Alderson The activation antigen CD69 Stem Cells 12 1994 456 465