Natural killer cells, dendritic cells, and the alarmin high-mobility group box 1 protein: A dangerous trio in HIV-1 infection?

Current Opinion in HIV and AIDS

Volumn 6, Issue 5, 2011, Pages 364-372

  Gougeon, Marie Lise ^a   Bras, Marlène ^a  

^a INSTITUT PASTEUR   (France)

Author keywords

dendritic cells; high mobility group box 1 protein; natural killer cells

Indexed keywords

ALARMIN; APOPTOSIS INHIBITOR; HIGH MOBILITY GROUP B1 PROTEIN; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 3; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG;

CD4+ T LYMPHOCYTE; CELL DAMAGE; CELL MATURATION; CELL STRESS; DENDRITIC CELL; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; LYSIS; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; SYNAPSE; UPREGULATION; VIRUS REPLICATION;

ADAPTIVE IMMUNITY; DENDRITIC CELLS; HIV INFECTIONS; HIV-1; HMGB1 PROTEIN; HUMANS; IMMUNE EVASION; IMMUNITY, INNATE; KILLER CELLS, NATURAL;

EID: 80051771760     PISSN: 1746630X     EISSN: 17466318     Source Type: Journal    
DOI: 10.1097/COH.0b013e328349b089     Document Type: Review

References (80)

1. Kuijpers TW, Baars PA, Dantin C, et al. Human NK cells can control CMV infection in the absence of T cells. Blood 2008; 112:914-915.
2. Biron CA, Byron KS, Sullivan JL. Severe herpesvirus infections in an adolescent without natural-killer cells. N Engl J Med 1989; 320:1731-1735. (Pubitemid 19163129)
3. Biron CA, Brossay L. NK cells and NKT cells in innate defense against viral infections. Curr Opin Immunol 2001; 13:458-464. (Pubitemid 32728479)
4. Bashirova AA, Thomas R, Carrington M. HLA/KIR restraint of HIV: surviving the fittest. Annu Rev Immunol 2011; 29:295-317.
5. Bryceson YT, March ME, Ljunggren HG, Long EO. Activation, coactivation, and costimulation of resting human natural killer cells. Immunol Rev 2006; 214:73-91. (Pubitemid 44707903)
6. Vivier E, Raulet DH, Moretta A, et al. Innate or adaptive immunity? The example of natural killer cells. Science 2011; 331:44-49.
7. Brandt CS, Baratin M, Yi EC, et al. The B7 family member B7-H6 is a tumor cell ligand for the activating natural killer cell receptor NKp30 in humans. J Exper Med 2009; 206:1495-1503.
8. Mandelboim O, Lieberman N, Lev M, et al. Recognition of haemagglutinins on virus-infected cells by NKp46 activates lysis by human NK cells. Nature 2001; 409:1055-1060. (Pubitemid 32204059)
9. Jarahian M, Watzl C, Fournier P, et al. Activation of natural killer cells by newcastle disease virus hemagglutinin-neuraminidase. J Virol 2009; 83:8108-8121.
10. Karre K, Ljunggren HG, Piontek G, Kiessling R. Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defense strategy. Nature 1986; 319:675-678. (Pubitemid 16119452)
11. Moretta A, Bottino C, Vitale M, et al. Receptors for HLA class-I molecules in human natural killer cells. Ann Rev Immunol 1996; 14:619-648. (Pubitemid 26130196)
12. Kim S, Poursine-Laurent J, Truscott SM, et al. Licensing of natural killer cells by host major histocompatibility complex class I molecules. Nature 2005; 436:709-713. (Pubitemid 41117274)
13. Fernandez NC, Treiner E, Vance RE, et al. A subset of natural killer cells achieves self-tolerance without expressing inhibitory receptors specific for self-MHC molecules. Blood 2005; 105:4416-4423. (Pubitemid 40720789)
14. Brodin P, Lakshmikanth T, Johansson S, et al. The strength of inhibitory input during education quantitatively tunes the functional responsiveness of individual natural killer cells. Blood 2009; 113:2434-2441.
15. Schwartz O, Marechal V, LeGall S, et al. Endocytosis of major histocompatibility complex class I molecules is induced by the HIV-1 Nef protein. Nat Med 1996; 2:338-342. (Pubitemid 26080655)
16. Cohen GB, Gandhi RT, Davis DM, et al. The selective downregulation of class I major histocompatibility complex proteins by HIV-1 protects HIV-infected cells from NK cells. Immunity 1999; 10:661-671. (Pubitemid 29302919)
17. Mavilio D, Benjamin J, Daucher M, et al. Natural killer cells in HIV-1 infection: dichotomous effects of viremia on inhibitory and activating receptors and their functional correlates. Proc Natl Acad Sci USA 2003; 100:15011-15016. (Pubitemid 37518008)
18. Mavilio D, Lombardo G, Benjamin J, et al. Characterization of CD56(-)/CD16+ natural killer (NK) cells: a highly dysfunctional NK subset expanded in HIVinfected viremic individuals. Proc Natl Acad Sci USA 2005; 102:2886-2891. (Pubitemid 40299886)
19. Qi Y, Martin MP, Gao X, et al. KIR/HLA pleiotropism: protection against both HIV and opportunistic infections. Plos Pathogens 2006; 2:741-745.
20. Martin MP, Gao XJ, Lee JH, et al. Epistatic interaction between KIR3DS1 and HLA-B delays the progression to AIDS. Nat Genet 2002; 31:429-434. (Pubitemid 35154456)
21. Alter G, Martin MP, Teigen N, et al. Differential natural killer cell-mediated inhibition of HIV-1 replication based on distinct KIR/HLA subtypes. J Exper Med 2007; 204:3027-3036. (Pubitemid 350179568)
22. Boulet S, Sharafi S, Simic N, et al. Increased proportion of KIR3DS1 homozygotes in HIV-exposed uninfected individuals. Aids 2008; 22:595-599. (Pubitemid 351640592)
23. Brackenridge S, Evans EJ, Toebes M, et al. An early HIV mutation within a HLA-B-57-restricted T cell epitope abrogates binding to the killer inhibitory receptor 3DL1 (KIR3DL1). J Virol 2011; 85:5415-5422.
24. Tiemessen CT, Paximadis M, Minevich G, et al. Natural killer cell responses to HIV-1 peptides are associated with more activating KIR genes and HLA-C genes of the C1 allotype. J Acquir Immune Defic Syndr 2011. [Epub ahead of print]
25. Caligiuri MA. Human natural killer cells. Blood 2008; 112:461-469.
26. Fauci AS, Mavilio D, Kottilil S. NK cells in HIV infection: paradigm for protection or targets for ambush. Nat Rev Immunol 2005; 5:835-843. (Pubitemid 41581665)
27. Alter G, Altfeld M. NK cells in HIV-1 infection: evidence for their role in the control of HIV-1 infection. J Intern Med 2009; 265:29-42.
28. Alter G, Teigen N, Davis BT, et al. Sequential deregulation of NK cell subset distribution and function starting in acute HIV-1 infection. Blood 2005; 106:3366-3369. (Pubitemid 41609166)
29. Brunetta E, Fogli M, Varchetta S, et al. The decreased expression of Siglec-7 represents an early marker of dysfunctional natural killer-cell subsets associated with high levels of HIV-1 viremia. Blood 2009; 114:3822-3830.
30. Brunetta E, Hudspeth KL, Mavilio D. Pathologic natural killer cell subset redistribution in HIV-1 infection: new insights in pathophysiology and clinical outcomes. J Leuk Biol 2010; 88:1119-1130.
31. Portales P, Reynes J, Pinet V, et al. Interferon-alpha restores HIV-induced alteration of natural killer cell perforin expression in vivo. Aids 2003; 17:495-504. (Pubitemid 36293102)
32. De Maria A, Fogli M, Costa P, et al. The impaired NK cell cytolytic function in viremic HIV-1 infection is associated with a reduced surface expression of natural cytotoxicity receptors (NKp46, NKp30 and NKp44). Eur J Immunol 2003; 33:2410-2418. (Pubitemid 37138973)
33. Mela CM, Burton CT, Imami N, et al. Switch from inhibitory to activating NKG2 receptor expression in HIV-1 infection: lack of reversion with highly active antiretroviral therapy. Aids 2005; 19:1761-1769. (Pubitemid 41546594)
34. Mela CM, Goodier MR. The contribution of cytomegalovirus to changes in NK cell receptor expression in HIV-1-infected individuals. J Infect Dis 2007; 195:158-159. (Pubitemid 44958238)
35. Fausther-Bovendo H, Sol-Foulon N, Candotti D, et al. HIV escape from natural killer cytotoxicity: Nef inhibits NKp44L expression on CD4(+) T cells. Aids 2009; 23:1077-1087.
36. Cerboni C, Neri F, Casartelli N, et al. Human immunodeficiency virus 1 Nef protein downmodulates the ligands of the activating receptor NKG2D and inhibits natural killer cell-mediated cytotoxicity. J Gen Virol 2007; 88:242-250. (Pubitemid 46085135)
37. Richard J, Sindhu S, Pham TNQ, et al. HIV-1 Vpr up-regulates expression of ligands for the activating NKG2D receptor and promotes NK cell-mediated killing. Blood 2010; 115:1354-1363.
38. Kottilil S, Shin K, Jackson JO, et al. Innate immune dysfunction in HIV infection: effect of HIV envelope-NK cell interactions. J Immunol 2006; 176:1107-1114. (Pubitemid 43099712)
39. Arthos J, Cicala C, Martinelli E, et al. HIV-1 envelope protein binds to and signals through integrin alpha(4)beta(7), the gut mucosal homing receptor for peripheral T cells. Nat Immunol 2008; 9:301-309. (Pubitemid 351267327)
40. Fernandez NC, Lozier A, Flament C, et al. Dendritic cells directly trigger NK cell functions: cross-talk relevant in innate antitumor immune responses in vivo. Nat Med 1999; 5:405-411. (Pubitemid 29180578)
41. Moretta A. Natural killer cells and dendritic cells: rendezvous in abused tissues. Nat Rev Immunol 2002; 2:957-964. (Pubitemid 37323216)
42. Piccioli D, Sbrana S, Melandri E, Valiante NM. Contact-dependent stimulation and inhibition of dendritic cells by natural killer cells. J Exp Med 2002; 195: 335-341. (Pubitemid 34461491)
43. Ferlazzo G, Tsang ML, Moretta L, et al. Human dendritic cells activate resting natural killer (NK) cells and are recognized via the NKp30 receptor by activated NK cells. J Exper Med 2002; 195:343-351. (Pubitemid 34461492)
44. Della Chiesa M, Vitale M, Carlomagno S, et al. The natural killer cell-mediated killing of autologous dendritic cells is confined to a cell subset expressing CD94/NKG2A, but lacking inhibitory killer Ig-like receptors. Eur J Immunol 2003; 33:2947-12947.
45. Tasca S, Tambussi G, Nozza S, et al. Escape of monocyte-derived dendritic cells of HIV-1 infected individuals from natural killer cell-mediated lysis. Aids 2003; 17:2291-2298. (Pubitemid 38147014)
46. Mavilio D, Lombardo G, Kinter A, et al. Characterization of the defective interaction between a subset of natural killer cells and dendritic cells in HIV-1 infection. J Exper Med 2006; 203:2339-2350. (Pubitemid 44498368)
47. Alter G, Kavanagh D, Rihn S, et al. IL-10 induces aberrant deletion of dendritic cells by natural killer cells in the context of HIV infection. J Clin Invest 2010; 120:1905-1913.
48. Melki MT, Saidi H, Dufour A, et al. Escape of HIV-1-infected dendritic cells from TRAIL-mediated NK cell cytotoxicity during NK-DC cross-talk: a pivotal role of HMGB1. Plos Pathogens 2010; 6:e1000862.
49. Saidi H, Melki MT, Gougeon ML. HMGB1-dependent triggering of HIV-1 replication and persistence in dendritic cells as a consequence of NK-DC cross-talk. Plos One 2008; 3:e3601.
50. Yanai H, Ban T, Wang ZC, et al. HMGB proteins function as universal sentinels for nucleic-acid-mediated innate immune responses. Nature 2009; 462:99-103.
51. Tian J, Avalos AM, Mao SY, et al. Toll-like receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE. Nat Immunol 2007; 8:487-496. (Pubitemid 46605917)
52. Scaffidi P, Misteli T, Bianchi ME. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 2002; 418:191-195. (Pubitemid 34773774)
53. Raucci A, Palumbo R, Bianchi ME. HMGB1: a signal of necrosis. Autoimmunity 2007; 40:285-289. (Pubitemid 46845522)
54. Wang HC, Bloom O, Zhang MH, et al. HMG-1 as a late mediator of endotoxin lethality in mice. Science 1999; 285:248-251. (Pubitemid 29329996)
55. Yang D, Chen Q, Yang H, et al. High mobility group box-1 protein induces the migration and activation of human dendritic cells and acts as an alarmin. J Leuk Biol 2007; 81:59-66. (Pubitemid 46021253)
56. Dumitriu IE, Bianchi ME, Bacci M, et al. The secretion of HMGB1 is required for the migration of maturing dendritic cells. J Leuk Biol 2007; 81:84-91. (Pubitemid 46021256)
57. Manfredi AA, Capobianco A, Esposito A, et al. Maturing dendritic cells depend onRAGEfor in vivohoming to lymph nodes. J Immunol2008; 180:2270-2275.
58. Messmer D, Yang H, Telusma G, et al. High mobility group box protein 1: an endogenous signal for dendritic cell maturation and Th1 polarization. J Immunol 2004; 173:307-313. (Pubitemid 38797355)
59. Dumitriu IE, Baruah P, Valentinis B, et al. Release of high mobility group box 1 by dendritic cells controls T cell activation via the receptor for advanced glycation end products. J Immunol 2005; 174:7506-7515. (Pubitemid 40806253)
60. Hu JJ, Gardner MB, Miller CJ. Simian immunodeficiency virus rapidly penetrates the cervicovaginal mucosa after intravaginal inoculation and infects intraepithelial dendritic cells. J Virol 2000; 74:6087-6095. (Pubitemid 30412980)
61. Steinman RM, Banchereau J. Taking dendritic cells into medicine. Nature 2007; 449:419-426. (Pubitemid 47509552)
62. McDonald D, Wu L, Bohks SM, et al. Recruitment of HIV and its receptors to dendritic cell-T cell junctions. Science 2003; 300:1295-1297. (Pubitemid 36618241)
63. Izquierdo-Useros N, Naranjo-GomezM, Archer J, et al. Capture and transfer of HIV-1 particles by mature dendritic cells converges with the exosomedissemination pathway. Blood 2009; 113:2732-2741.
64. Gould SJ, Booth AM, Hildreth JEK. The Trojan exosome hypothesis. Proc Natl Acad Sci USA 2003; 100:10592-10597. (Pubitemid 37140073)
65. Izquierdo-Useros N, Naranjo-Gomez M, Erkizia I, et al. HIV and mature dendritic cells: Trojan exosomes riding the Trojan horse? Plos Pathogens 2010; 6:e1000740.
66. Nowak P, Barqasho B, Treutiger CJ, et al. HMGB1 activates replication of latent HIV-1 in a monocytic cell-line, but inhibits HIV-1 replication in primary macrophages. Cytokine 2006; 34 (1-2):17-23. (Pubitemid 43817548)
67. Thierry S, Gozlan J, Jaulmes A, et al. High-mobility group box 1 protein induces HIV-1 expression from persistently infected cells. Aids 2007; 21:283-292. (Pubitemid 46175041)
68. Park JS, Svetkauskaite D, He QB, et al. Involvement of Toll-like receptors 2 and 4 in cellular activation by high mobility group box 1 protein. J Biol Chem 2004; 279:7370-7377. (Pubitemid 38294612)
69. Barqasho B, Nowak P, Abdurahman S, et al. Implications of the release of high-mobility group box 1 protein from dying cells during human immunodeficiency virus type 1 infection in vitro. J Gen Virol 2010; 91:1800-1809.
70. Gougeon ML. Apoptosis as an HIV strategy to escape immune attack. Nat Rev Immunol 2003; 3:392-404.
71. Gougeon ML, Lecoeur H, Dulioust A, et al. Programmed cell death in peripheral lymphocytes from HIV-infected persons: increased susceptibility to apoptosis of CD4 and CD8 T cells correlates with lymphocyte activation and with disease progression. J Immunol 1996; 156:3509-3520.
72. Nowak P, Barqasho B, Sonnerborg A. Elevated plasma levels of high mobility group box protein 1 in patients with HIV-1 infection. Aids 2007; 21:869-871. (Pubitemid 46573160)
73. Troseid M, Nowak P, Nystrom J, et al. Elevated plasma levels of lipopolysaccharide and high mobility group box-1 protein are associated with high viral load in HIV-1 infection: reduction by 2-year antiretroviral therapy. Aids 2010; 24:1733-1737.
74. Lamkanfi M, Sarkar A, Walle LV, et al. Inflammasome-dependent release of the alarmin HMGB1 in endotoxemia. J Immunol 2010; 185:4385-4392.
75. Zhu P, Duan L, Chen J, et al. Gene silencing of NALP3 protects against liver ischemia-reperfusion injury in mice. Hum Gene Ther 2011. [Epub ahead of print]
76. Yang Q, Zhong Q, Cao C, et al. AntiToll like receptor 4 monoclonal antibody attenuates cerebral ischemia-reperfusion injury. Cerebrovasc Dis 2008; 26:217-218.
77. Taguchi A, Blood DC, del Toro G, et al. Blockade of RAGE-amphoterin signalling suppresses tumour growth and metastases. Nature 2000; 405: 354-360. (Pubitemid 30337069)
78. Liliensiek B, Weigand MA, Bierhaus A, et al. Receptor for advanced glycation end products (RAGE) regulates sepsis but not the adaptive immune response. J Clin Invest 2004; 113:1641-1650. (Pubitemid 39071688)
79. Ulloa L, Ochani M, Yang H, et al. Ethyl pyruvate prevents lethality in mice with established lethal sepsis and systemic inflammation. Proc Natl Acad Sci USA 2002; 99:12351-12356.
80. Tang DL, Kang R, Xiao WM, et al. Quercetin prevents LPS-induced highmobility group box 1 release and proinflammatory function. Am J Respir Cell Mol Biol 2009; 41:651-660.