Immunological dysfunction in HIV-1-infected individuals caused by impairment of adenosine deaminase-induced costimulation of T-cell activation

Immunology

Volumn 128, Issue 3, 2009, Pages 393-404

  Martinez Navio, José M ^a   Climent, Núria ^a,b   Pacheco, Rodrigo ^a   Garcia, Felipe ^a   Plana, Montserrat ^a   Nomdedeu, Meritxell ^a   Oliva, Harold ^a,b   Rovira, Cristina ^a   Miralles, Laia ^a   Gatell, José M ^a   Gallart, Teresa ^a   Mallol, Josefa ^a   Lluis, Carme ^a   Franco, Rafael ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b HOSPITAL CLÍNIC   (Spain)

Author keywords

Activation; Costimulation; Cytokines; Human immunodeficiency virus; T cells

Indexed keywords

ADENOSINE DEAMINASE; CD3 ANTIBODY; DIPEPTIDYL PEPTIDASE IV; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 6; PROTEINASE INHIBITOR; RECOMBINANT GLYCOPROTEIN GP 120;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ADULT; AGED; ARTICLE; CD4 LYMPHOCYTE COUNT; CLINICAL ARTICLE; CONTROLLED STUDY; CORRELATIONAL STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENZYME ACTIVATION; ENZYME ASSAY; FEMALE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; IMMUNITY; IMMUNOPATHOLOGY; LYMPHOCYTE PROLIFERATION; MALE; PATHOGENESIS; PRIORITY JOURNAL; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; VIRUS LOAD; VOLUNTEER;

ADENOSINE DEAMINASE; ADULT; AGED; ANTIGENS, CD26; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CYTOKINES; DISEASE PROGRESSION; FEMALE; HIV ENVELOPE PROTEIN GP120; HIV INFECTIONS; HIV-1; HUMANS; LYMPHOCYTE ACTIVATION; MALE; MIDDLE AGED; PROTEIN BINDING; VIRAL LOAD;

EID: 70349675871     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/j.1365-2567.2009.03121.x     Document Type: Article

References (75)

1. Dalgleish AG, Beverley PC, Clapham PR, Crawford DH, Greaves MF, Weiss RA. The CD4 (T4) antigen is an essential component of the receptor for the AIDS retrovirus. Nature 1984 312 : 763 767.
2. Klatzmann D, Barre-Sinoussi F, Nugeyre MT et al. Selective tropism of lymphadenopathy associated virus (LAV) for helper-inducer T lymphocytes. Science 1984 225 : 59 63. (Pubitemid 14123409)
3. Roederer M, Dubs JG, Anderson MT, Raju PA, Herzenberg LA, Herzenberg LA. CD8 naive T cell counts decrease progressively in HIV-infected adults. J Clin Invest 1995 95 : 2061 2066.
4. Zhang D, Shankar P, Xu Z et al. Most antiviral CD8 T cells during chronic viral infection do not express high levels of perforin and are not directly cytotoxic. Blood 2003 101 : 226 235.
5. Zhu T, Muthui D, Holte S et al. Evidence for human immunodeficiency virus type 1 replication in vivo in CD14(+) monocytes and its potential role as a source of virus in patients on highly active antiretroviral therapy. J Virol 2002 76 : 707 716.
6. Meltzer MS, Nakamura M, Hansen BD, Turpin JA, Kalter DC, Gendelman HE. Macrophages as susceptible targets for HIV infection, persistent viral reservoirs in tissue, and key immunoregulatory cells that control levels of virus replication and extent of disease. AIDS Res Hum Retroviruses 1990 6 : 967 971.
7. Moir S, Malaspina A, Ogwaro KM et al. HIV-1 induces phenotypic and functional perturbations of B cells in chronically infected individuals. Proc Natl Acad Sci USA 2001 98 : 10362 10367.
8. Gabrilovich DI, Vassilev V, Nosikov VV, Serebrovskaya LV, Ivanova LA, Pokrovsky VV. Clinical significance of HIV DNA in polymorphonuclear neutrophils from patients with HIV infection. J Acquir Immune Defic Syndr 1993 6 : 587 591.
9. Macatonia SE, Lau R, Patterson S, Pinching AJ, Knight SC. Dendritic cell infection, depletion and dysfunction in HIV-infected individuals. Immunology 1990 71 : 38 45.
10. Foley P, Kazazi F, Biti R, Sorrell TC, Cunningham AL. HIV infection of monocytes inhibits the T-lymphocyte proliferative response to recall antigens, via production of eicosanoids. Immunology 1992 75 : 391 397.
11. Veiga AP, Casseb J, Duarte AJ. Humoral response to hepatitis B vaccination and its relationship with T CD45RA+ (naive) and CD45RO+ (memory) subsets in HIV-1-infected subjects. Vaccine 2006 24 : 7124 7128.
12. Opravil M, Fierz W, Matter L, Blaser J, Luthy R. Poor antibody response after tetanus and pneumococcal vaccination in immunocompromised, HIV-infected patients. Clin Exp Immunol 1991 84 : 185 189.
13. Boasso A, Shearer GM. Chronic innate immune activation as a cause of HIV-1 immunopathogenesis. Clin Immunol 2008 126 : 235 242.
14. Hunt PW. Role of immune activation in HIV pathogenesis. Curr HIV/AIDS Rep 2007 4 : 42 7.
15. Liu Z, Cumberland WG, Hultin LE, Kaplan AH, Detels R, Giorgi JV. CD8+ T-lymphocyte activation in HIV-1 disease reflects an aspect of pathogenesis distinct from viral burden and immunodeficiency. J Acquir Immune Defic Syndr Hum Retrovirol 1998 18 : 332 340.
16. Kestens L, Vanham G, Vereecken C et al. Selective increase of activation antigens HLA-DR and CD38 on CD4+ CD45RO+ T lymphocytes during HIV-1 infection. Clin Exp Immunol 1994 95 : 436 441.
17. Sousa AE, Carneiro J, Meier-Schellersheim M, Grossman Z, Victorino RM. CD4 T cell depletion is linked directly to immune activation in the pathogenesis of HIV-1 and HIV-2 but only indirectly to the viral load. J Immunol 2002 169 : 3400 3406.
18. Gruters RA, Terpstra FG, De Jong R, Van Noesel CJ, Van Lier RA, Miedema F. Selective loss of T cell functions in different stages of HIV infection. Early loss of anti-CD3-induced T cell proliferation followed by decreased anti-CD3-induced cytotoxic T lymphocyte generation in AIDS-related complex and AIDS. Eur J Immunol 1990 20 : 1039 1044.
19. Sieg SF, Harding CV, Lederman MM. HIV-1 infection impairs cell cycle progression of CD4(+) T cells without affecting early activation responses. J Clin Invest 2001 108 : 757 764.
20. Pahwa R, McCloskey TW, Aroniadis OC, Strbo N, Krishnan S, Pahwa S. CD8+ T cells in HIV disease exhibit cytokine receptor perturbation and poor T cell receptor activation but are responsive to gamma-chain cytokine-driven proliferation. J Infect Dis 2006 193 : 879 887.
21. Pedersen C, Dickmeiss E, Gaub J et al. T-cell subset alterations and lymphocyte responsiveness to mitogens and antigen during severe primary infection with HIV: a case series of seven consecutive HIV seroconverters. AIDS 1990 4 : 523 526.
22. Schellekens PT, Roos MT, De Wolf F, Lange JM, Miedema F. Low T-cell responsiveness to activation via CD3/TCR is a prognostic marker for acquired immunodeficiency syndrome (AIDS) in human immunodeficiency virus-1 (HIV-1)-infected men. J Clin Immunol 1990 10 : 121 127.
23. Galati D, Bocchino M. New insights on the perturbations of T cell cycle during HIV infection. Curr Med Chem 2007 14 : 1920 1924.
24. Piedimonte G, Corsi D, Paiardini M et al. Unscheduled cyclin B expression and p34 cdc2 activation in T lymphocytes from HIV-infected patients. AIDS 1999 13 : 1159 1164.
25. Biancotto A, Grivel JC, Iglehart SJ et al. Abnormal activation and cytokine spectra in lymph nodes of people chronically infected with HIV-1. Blood 2007 109 : 4272 4279.
26. Barcellini W, Rizzardi GP, Borghi MO, Fain C, Lazzarin A, Meroni PL. TH1 and TH2 cytokine production by peripheral blood mononuclear cells from HIV-infected patients. AIDS 1994 8 : 757 762.
27. Shrivastav S, Kino T, Cunningham T et al. HIV-1 Vpr suppresses transcriptional activity of PPAR[gamma] and inhibits adipocyte differentiation: Implications for HIV-associated lipodystrophy. Mol Endocrinol 2008 22 : 234 247.
28. Brugger B, Krautkramer E, Tibroni N et al. Human Immunodeficiency Virus Type 1 Nef protein modulates the lipid composition of virions and host cell membrane microdomains. Retrovirology 2007 4 : 70.
29. Joseph AM, Ladha JS, Mojamdar M, Mitra D. Human immunodeficiency virus-1 Nef protein interacts with Tat and enhances HIV-1 gene expression. FEBS Lett 2003 548 : 37 42.
30. Roeth JF, Collins KL. Human immunodeficiency virus type 1 Nef: adapting to intracellular trafficking pathways. Microbiol Mol Biol Rev 2006 70 : 548 563.
31. Peruzzi F. The multiple functions of HIV-1 Tat: proliferation versus apoptosis. Front Biosci 2006 11 : 708 717.
32. Yoshizuka N, Yoshizuka-Chadani Y, Krishnan V, Zeichner SL. Human immunodeficiency virus type 1 Vpr-dependent cell cycle arrest through a mitogen-activated protein kinase signal transduction pathway. J Virol 2005 79 : 11366 11381.
33. Majumder B, Janket ML, Schafer EA et al. Human immunodeficiency virus type 1 Vpr impairs dendritic cell maturation and T-cell activation: implications for viral immune escape. J Virol 2005 79 : 7990 8003.
34. Majumder B, Venkatachari NJ, Schafer EA, Janket ML, Ayyavoo V. Dendritic cells infected with vpr-positive human immunodeficiency virus type 1 induce CD8+ T-cell apoptosis via upregulation of tumor necrosis factor alpha. J Virol 2007 81 : 7388 7399.
35. Venkatachari NJ, Majumder B, Ayyavoo V. Human immunodeficiency virus (HIV) type 1 Vpr induces differential regulation of T cell costimulatory molecules: direct effect of Vpr on T cell activation and immune function. Virol 2007 358 : 347 356.
36. Jones GJ, Barsby NL, Cohen EA et al. HIV-1 Vpr causes neuronal apoptosis and in vivo neurodegeneration. J Neurosci 2007 27 : 3703 3711.
37. Andersen JL, Planelles V. The role of Vpr in HIV-1 pathogenesis. Curr HIV Res 2005 3 : 43 51.
38. Tungaturthi PK, Sawaya BE, Singh SP et al. Role of HIV-1 Vpr in AIDS pathogenesis: relevance and implications of intravirion, intracellular and free Vpr. Biomed Pharmacother 2003 57 : 20 4.
39. Arriaga ME, Carr J, Li P, Wang B, Saksena NK. Interaction between HIV-1 and APOBEC3 sub-family of proteins. Curr HIV Res 2006 4 : 401 409.
40. Sakai K, Dimas J, Lenardo MJ. The Vif and Vpr accessory proteins independently cause HIV-1-induced T cell cytopathicity and cell cycle arrest. Proc Natl Acad Sci USA 2006 103 : 3369 3374.
41. Fantuzzi L, Purificato C, Donato K, Belardelli F, Gessani S. Human immunodeficiency virus type 1 gp120 induces abnormal maturation and functional alterations of dendritic cells: a novel mechanism for AIDS pathogenesis. J Virol 2004 78 : 9763 9772.
42. Metlas R, Veljkovic V. Does the HIV-1 manipulate immune network via gp120 immunoglobulin-like domain involving V3 loop? Vaccine 1995 13 : 355 359.
43. Valenzuela A, Blanco J, Callebaut C et al. Adenosine deaminase binding to human CD26 is inhibited by HIV-1 envelope glycoprotein gp120 and viral particles. J Immunol 1997 158 : 3721 3729. (Pubitemid 127488727)
44. Blanco J, Valenzuela A, Herrera C, Lluis C, Hovanessian AG, Franco R. The HIV-1 gp120 inhibits the binding of adenosine deaminase to CD26 by a mechanism modulated by CD4 and CXCR4 expression. FEBS Lett 2000 477 : 123 128.
45. Boyum A. Isolation of leucocytes from human blood. Further observations. Methylcellulose, dextran, and ficoll as erythrocyteaggregating agents. Scand J Clin Lab Invest Suppl 1968 97 : 31 50.
46. Boyum A. Isolation of lymphocytes, granulocytes and macrophages. Scand J Immunol 1976 5 : 9 15.
47. Franco R, Canela EI, Bozal J. Heterogeneous localization of some purine enzymes in subcellular fractions of rat brain and cerebellum. Neurochem Res 1986 11 : 423 435.
48. Kung P, Goldstein G, Reinherz EL, Schlossman SF. Monoclonal antibodies defining distinctive human T cell surface antigens. Science 1979 206 : 347 349.
49. Van Wauwe JP, De Mey JR, Goossens JG. OKT3: a monoclonal anti-human T lymphocyte antibody with potent mitogenic properties. J Immunol 1980 124 : 2708 2713.
50. Martin M, Huguet J, Centelles JJ, Franco R. Expression of ecto-adenosine deaminase and CD26 in human T cells triggered by the TCR-CD3 complex. Possible role of adenosine deaminase as costimulatory molecule. J Immunol 1995 155 : 4630 4643.
51. Pacheco R, Martinez-Navio JM, Lejeune M et al. CD26, adenosine deaminase, and adenosine receptors mediate costimulatory signals in the immunological synapse. Proc Natl Acad Sci USA 2005 102 : 9583 9588.
52. Pacheco R, Lluis C, Franco R. Role of CD26-adenosine deaminase interaction in T cell-mediated immunity. Inmunología 2005 24 : 235 245.
53. De Meester I, Vanham G, Kestens L et al. Binding of adenosine deaminase to the lymphocyte surface via CD26. Eur J Immunol 1994 24 : 566 570.
54. Ohnuma K, Takahashi N, Yamochi T, Hosono O, Dang NH, Morimoto C. Role of CD26/dipeptidyl peptidase IV in human T cell activation and function. Front Biosci 2008 13 : 2299 2310.
55. Phillips AN, Sabin CA, Elford J, Bofill M, Janossy G, Lee CA. Use of CD4 lymphocyte count to predict long-term survival free of AIDS after HIV infection. BMJ 1994 309 : 309 313.
56. Clerici M, Saresella M, Trabattoni D, Ferrante P, Vanzulli A, Vigano A. Thymic volume predicts long-term immune reconstitution in HIV-infected children treated with highly active antiretroviral therapy. AIDS 2002 16 : 2219 2221.
57. De PP, Bortolin MT, Zanussi S, Monzoni A, Pratesi C, Giacca M. Changes in thymic function in HIV-positive patients treated with highly active antiretroviral therapy and interleukin-2. Clin Exp Immunol 2001 125 : 440 446.
58. Fernandez S, Nolan RC, Price P et al. Thymic function in severely immunodeficient HIV type 1-infected patients receiving stable and effective antiretroviral therapy. AIDS Res Hum Retroviruses 2006 22 : 163 170.
59. Al-Harthi L, Landay A. Immune recovery in HIV disease: role of the thymus and T cell expansion in immune reconstitution strategies. J Hematother Stem Cell Res 2002 11 : 777 786.
60. Lange CG, Lederman MM. Immune reconstitution with antiretroviral therapies in chronic HIV-1 infection. J Antimicrob Chemother 2003 51 : 1 4.
61. Lange CG, Valdez H, Medvik K, Asaad R, Lederman MM. CD4+ T-lymphocyte nadir and the effect of highly active antiretroviral therapy on phenotypic and functional immune restoration in HIV-1 infection. Clin Immunol 2002 102 : 154 161.
62. Skiest DJ, Morrow P, Allen B et al. It is safe to stop antiretroviral therapy in patients with preantiretroviral CD4 cell counts > 250 cells/microL. J Acquir Immune Defic Syndr 2004 37 : 1351 1357.
63. Lederman HM, Williams PL, Wu JW et al. Incomplete immune reconstitution after initiation of highly active antiretroviral therapy in human immunodeficiency virus-infected patients with severe CD4+ cell depletion. J Infect Dis 2003 188 : 1794 1803.
64. Markowitz N, Bebchuk JD, Abrams DI. Nadir CD4+ T cell count predicts response to subcutaneous recombinant interleukin-2. Clin Infect Dis 2003 37 : e115 20.
65. Lange CG, Lederman MM, Medvik K et al. Nadir CD4+ T-cell count and numbers of CD28+ CD4+ T-cells predict functional responses to immunizations in chronic HIV-1 infection. AIDS 2003 17 : 2015 2023.
66. Salerno-Goncalves R, Sztein MB. Cell-mediated immunity and the challenges for vaccine development. Trends Microbiol 2006 14 : 536 542.
67. Lasky LA, Nakamura G, Smith DH et al. Delineation of a region of the human immunodeficiency virus type 1 gp120 glycoprotein critical for interaction with the CD4 receptor. Cell 1987 50 : 975 985.
68. Murray JL, Loftin KC, Munn CG, Reuben JM, Mansell PW, Hersh EM. Elevated adenosine deaminase and purine nucleoside phosphorylase activity in peripheral blood null lymphocytes from patients with acquired immune deficiency syndrome. Blood 1985 65 : 1318 1324.
69. Delia S, Mastroianni CM, Massetti AP et al. Adenosine deaminase activity and acquired immunodeficiency syndrome (AIDS). Clin Chem 1987 33 : 1675.
70. Tsuboi I, Sagawa K, Shichijo S, Yokoyama MM, Ou DW, Wiederhold MD. Adenosine deaminase isoenzyme levels in patients with human T-cell lymphotropic virus type 1 and human immunodeficiency virus type 1 infections. Clin Diagn Lab Immunol 1995 2 : 626 630.
71. Niedzwicki JG, Mayer KH, Abushanab E, Abernethy DR. Plasma adenosine deaminase2 is a marker for human immunodeficiency virus-1 seroconversion. Am J Hematol 1991 37 : 152 155.
72. Cowan MJ, Brady RO, Widder KJ. Elevated erythrocyte adenosine deaminase activity in patients with acquired immunodeficiency syndrome. Proc Natl Acad Sci USA 1986 83 : 1089 1091.
73. Chittiprol S, Satishchandra P, Bhimasenarao RS et al. Plasma adenosine deaminase activity among HIV1 Clade C seropositives: relation to CD4 T cell population and antiretroviral therapy. Clin Chim Acta 2007 377 : 133 137.
74. Fischer D, Van der Weyden MB, Snyderman R, Kelley WN. A role for adenosine deaminase in human monocyte maturation. J Clin Invest 1976 58 : 399 407.
75. Aldrich MB, Chen W, Blackburn MR, Martinez-Valdez H, Datta SK, Kellems RE. Impaired germinal center maturation in adenosine deaminase deficiency. J Immunol 2003 171 : 5562 5570.