Artículo

Jurado, J.O.; Alvarez, I.B.; Pasquinelli, V.; Martínez, G.J.; Quiroga, M.F.; Abbate, E.; Musella, R.M.; Chuluyan, H.E.; García, V.E. "Programmed death (PD)-1:PD-ligand 1/PD-ligand 2 pathway inhibits T cell effector functions during human tuberculosis" (2008) Journal of Immunology. 181(1):116-125
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Abstract:

Protective immunity against Mycobacterium tuberculosis requires the generation of cell-mediated immunity. We investigated the expression and role of programmed death 1 (PD-1) and its ligands, molecules known to modulate T cell activation, in the regulation of IFN-γ production and lytic degranulation during human tuberculosis. We demonstrated that specific Ag-stimulation increased CD3+PD-1+ lymphocytes in peripheral blood and pleural fluid from tuberculosis patients in direct correlation with IFN-γ production from these individuals. Moreover, M. tuberculosis-induced IFN-γ participated in the up-regulation of PD-1 expression. Blockage of PD-1 or PD-1 and its ligands (PD-Ls: PD-L1, PD-L2) enhanced the specific degranulation of CD8+ T cells and the percentage, of specific IFN-γ-producing lymphocytes against the pathogen, demonstrating that the PD-1:PD-Ls pathway inhibits T cell effector functions during active M. tuberculosis infection. Furthermore, the simultaneous blockage of the inhibitory receptor PD-1 together with the activation of the costimulatory protein signaling lymphocytic activation molecule led to the promotion of protective IFN-γ responses to M. tuberculosis, even in patients with weak cell-mediated immunity against the bacteria. Together, we demonstrated that PD-1 interferes with T cell effector functions against M. tuberculosis, suggesting that PD-1 has a key regulatory role during the immune response of the host to the pathogen. Copyright © 2008 by The American Association of Immunologists, Inc.

Registro:

Documento: Artículo
Título:Programmed death (PD)-1:PD-ligand 1/PD-ligand 2 pathway inhibits T cell effector functions during human tuberculosis
Autor:Jurado, J.O.; Alvarez, I.B.; Pasquinelli, V.; Martínez, G.J.; Quiroga, M.F.; Abbate, E.; Musella, R.M.; Chuluyan, H.E.; García, V.E.
Filiación:Department of Biological Chemistry, School of Sciences, University of Buenos Aires, Buenos Aires, Argentina
Laboratorio de Inmunogenética, Hospital de Clíni-cas José de San Martín, University of Buenos Aires, Buenos Aires, Argentina
Division de Tisioneumonología, Hospital F. J. Muñiz, Buenos Aires, Argentina
Department of Biological Chemistry, School of Sciences, University of Buenos Aires, Intendente Guiraldes 2160, Pabellón II, Capital Federal, 1428, Buenos Aires, Argentina
Palabras clave:gamma interferon; inhibitor protein; ligand; pd 1 ligand; pd 2 ligand; programmed death 1 protein; receptor protein; unclassified drug; antigen; apoptosis regulatory protein; CD150 antigen; CD274 protein, human; cell surface receptor; gamma interferon; leukocyte antigen; PDCD1 protein, human; PDCD1LG2 protein, human; signal peptide; article; CD3+ T lymphocyte; CD8+ T lymphocyte; cellular immunity; cytokine production; degranulation; human; priority journal; protein expression; protein function; signal transduction; T lymphocyte activation; tuberculosis; biosynthesis; cell culture; immunology; lymphocyte activation; metabolism; Mycobacterium tuberculosis; protein binding; signal transduction; T lymphocyte; Antigens; Antigens, CD; Apoptosis Regulatory Proteins; Cells, Cultured; Humans; Intercellular Signaling Peptides and Proteins; Interferon Type II; Lymphocyte Activation; Mycobacterium tuberculosis; Protein Binding; Receptors, Cell Surface; Signal Transduction; T-Lymphocytes; Tuberculosis
Año:2008
Volumen:181
Número:1
Página de inicio:116
Página de fin:125
DOI: http://dx.doi.org/10.4049/jimmunol.181.1.116
Título revista:Journal of Immunology
Título revista abreviado:J. Immunol.
ISSN:00221767
CODEN:JOIMA
CAS:gamma interferon, 82115-62-6; Antigens; Antigens, CD; Apoptosis Regulatory Proteins; CD150 antigen, 169535-43-7; CD274 protein, human; Intercellular Signaling Peptides and Proteins; Interferon Type II, 82115-62-6; PDCD1 protein, human, 146588-21-8; PDCD1LG2 protein, human; Receptors, Cell Surface
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00221767_v181_n1_p116_Jurado

Referencias:

  • Kaufmann, S.H., How can immunology contribute to the control of tuberculosis? (2001) Nat. Rev. Immunol, 1, pp. 20-30
  • Tascon, R.E., Stavropoulos, E., Lukaes, K.V., Colston, M.J., Protection against Mycobacterium tuberculosis infection by CDS + T cells requires the production of 7 interferon (1998) Infect. Immun, 66, pp. 830-834
  • Zhang, M., Gong, J., Iyer, D.V., Jones, B.E., Modlin, R.L., Barnes, P.F., T cell cytokine responses in persons wilh tuberculosis and human immunodeficiency virus infection (1994) J. Clin. Invest, 94, pp. 2435-2442
  • Zhang, M., Lin, Y., Iyer, D.V., Gong, J., Abrams, J.S., Barnes, P.F., T-cell cytokine responses in human infection with Mycobacterium tuberculosis (1995) Infect. Immun, 63, pp. 3231-3234
  • Newman, D.K., Hamilton, C., Newman, P.J., Inhibition of antigen-receptor signaling by platelet endothelial cell adhesion molecule-1 (CD31) requires functional ITIMs, SHP-2, and p56tck (2001) Blood, 97, pp. 2351-2357
  • Thompson, C.B., Allison, J.P., The emerging role of CTLA-4 as an immune attenuator (1997) Immunity, 7, pp. 445-450
  • Oosterwegel, M.A., Greenwald, R.J., Mandelbrot, D.A., Lorsbach, R.B., Sharpe, A.H., CTLA-4 and T cell activation (1999) Curr. Opin. Immunol, 11, pp. 294-300
  • Pasquinelli, V., Quiroga, M.F., Martinez, G.J., Zorrilla, L.C., Musella, R.M., Bracco, M.M., Belmonte, L., Garcia, V.E., Expression of signaling lymphocytic activation molecule-associated protein interrupts IFN-γ production in human tuberculosis (2004) J. Immunol, 172, pp. 1177-1185
  • Quiroga, M.F., Pasquinelli, V., Martinez, G.J., Jurado, J.O., Zorrilla, L.C., Musella, R.M., Abbate, E., Garcia, V.E., Inducible costimulator: A modulator of IFN-γ production in human tuberculosis (2006) J. Immunol, 176, pp. 5965-5974
  • Quiroga, M.F., Jurado, J.O., Martinez, G.J., Pasquinelli, V., Musella, R.M., Abbate, E., Issekutz, A.C., Sieling, P.A., Cross-talk between CD31 and the signaling lymphocytic activation molecule-associated protein during interferon-γ production against Mycobacterium tuberculosis (2007) J. Infect. Dis, 196, pp. 1369-1378
  • Ishida, Y., Agata, Y., Shibahara, K., Honjo, T., Induced expression of PD-1, a novel member of the immunoglobulin gene superfamily, upon programmed cell death (1992) EMBO J, 11, pp. 3887-3895
  • Agata, Y., Kawasaki, A., Nishimura, H., Ishida, Y., Tsubata, T., Yagita, H., Honjo, T., Expression of the PD-1 antigen on the surface of stimulated mouse T and B lymphocytes (1996) Int. Immunol, 8, pp. 765-77Z
  • Freeman, G.J., Long, A.J., Iwai, Y., Bourque, K., Chemova, T., Nishimura, H., Fitz, L.J., el al, Engagement of the PD-I immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation (2000) J. Exp. Med, 192, pp. 1027-1034
  • Latchman, Y., Wood, C.R., Chemova, T., Chaudhary, D., Borde, M., Chemova, I., Iwai, Y., Nunes, R., PD-L2 is a second ligand for PD-1 and inhibits T cell activation (2001) Nat. Immunol, 2, pp. 261-268
  • Tseng, S.Y., Otsuji, M., Gorski, K., Huang, X., Slansky, J.E., Pai, S.I., Shalabi, A., Tsuchiya, H., B7-DC, a new dendritic cell molecule with potent costimulatory properties for T cells (2001) J. Exp. Med, 193, pp. 839-846
  • Sharpe, A.H., Wherry, E.J., Ahmed, R., Freeman, G.J., The function of programmed cell death 1 and its ligands in regulating autoimmunity and infection (2007) Nat. Immunol, 8, pp. 239-245
  • Garcia, V.E., Sieling, P.A., Gong, J., Barnes, P.F., Uyemura, K., Tanaka, Y., Bloom, B.R., Modlin, R.L., Single-cell cytokine analysis of γδ T cell responses to nonpeptide myeobacterial antigens (1997) J. Immunol, 159, pp. 1328-1335
  • Belts, M.R., Brenchley, J.M., Price, D.A., De Rosa, S.C., Douek, D.C., Roederer, M., Koup, R.A., Sensitive and viable identification of antigen-specific CDS+ T cells by a flow cytometric assay for degranulation (2003) J. Immunol. Methods, 281, pp. 65-78
  • Carter, L., Fouser, L.A., Jussif, J., Fitz, L., Deng, B., Wood, C.R., Collins, M., Carreno, B.M., PD-1: PD-L inhibitory pathway affects both CD4+ and CD8+ T cells and is overcome by IL-2 (2002) Eur. J. Immunol, 32, pp. 634-643
  • Spellberg, B., Edwards Jr., J.E., Type 1/type 2 immunity in infectious diseases (2001) Clin. Infect. Dis, 32, pp. 76-102
  • Chan, E.D., Chan, J., Schluger, N.W., What is the role of nitric oxide in murine and human host defense against tuberculosis: Current knowledge (2001) Am. J. Respir. Cell Mol. Biol, 25, pp. 606-612
  • Dorman, S.E., Holland, S.M., Interferon-y and interleukin-12 pathway defects and human disease (2000) Cytokine Growth Factor Rev, 11, pp. 321-333
  • Bennett, F., Luxenberg, D., Ling, V., Wang, I.M., Marquette, K., Lowe, D., Khan, N., Valge-Archer, V.E., Program death-1 engagement upon TCR activation has distinct effects on costimulation and cytokine-driven proliferation: Attenuation of ICOS, IL-4, and IL-21, but not CD28. IL-7, and IL-I5 responses (2003) J. Immunol, 170, pp. 711-718
  • Ellner, J.J., Barnes, P.F., Wallis, R.S., Modlin, R.L., The immunology of tuberculous pleurisy (1988) Semin. Respir. Infect, 3, pp. 335-342
  • Loke, P., Allison, J.P., PD-L1 and PD-L2 are differentially regulated by Th1 and Th2 cells (2003) Proc. Natl. Acad. Sci. USA, 100, pp. 5336-5341
  • Zhong, X., Tumang, J.R., Gao, W., Bai, C., Rothstein, T.L., PD-L2 expression extends beyond dendritic cells/macrophages to B1 cells enriched for VH11/VH12 and phosphatidylcholine binding (2007) Eur. J. Immunol, 37, pp. 2405-2410
  • Chen, L., Co-inhibitory molecules of the B7-CD28 family in the control of T-cell immunity (2004) Nat. Rev. Immunol, 4, pp. 336-347
  • Butte, M.J., Keir, M.E., Phamduy, T.B., Sharpe, A.H., Freeman, G.J., Programmed death-1 ligand 1 interacts specifically with the B7-1 costimulatory molecule to inhibit T cell responses (2007) Immunity, 27, pp. 111-122
  • Bukczynski, J., Wen, T., Wang, C., Christie, N., Routy, J.P., Boulassel, M.R., Kovacs, C.M., Sekaly, R.P., Enhancement of HIV-spccific CD8 T cell responses by dual costimulation with CD80 and CD137L (2005) J. Immunol, 175, pp. 6378-6389
  • Lee, S.W., Park, Y., Song, A., Cheroutre, H., Kwon, B.S., Croft, M., Functional dichotomy between OX40 and 4-IBB in modulating effector CD8 T cell responses (2006) J. Immunol, 177, pp. 4464-4472
  • Dawicki, W., Bertram, E.M., Sharpe, A.H., Watts, T.H., 4-IBB and OX40 act independently to facilitate robust CDS and CD4 recall responses (2004) J. Immunol, 173, pp. 5944-5951
  • Hirano, F., Kaneko, K., Tamura, H., Dong, H., Wang, S., Ichikawa, M., Rietz, C., Zhu, G., Blockade of B7-HI and PD-1 by monoclonal antibodies potentiates cancer therapeutic immunity (2005) Cancer Res, 65, pp. 1089-1096
  • Loke, P., Allison, J.P., Emerging mechanisms of immune regulation: The extended B7 family and regulatory T cells (2004) Arthritis Res. Ther, 6, pp. 208-214
  • Dong, H., Zhu, G., Tamada, K., Chen, L., B7-H1, a third member of the B7 family, co-stimulates T-cell proliferation and interleukin-10 secretion (1999) Nat. Med, 5, pp. 1365-1369
  • Barber, D.L., Wherry, E.J., Masopust, D., Zhu, B., Allison, J.P., Sharpe, A.H., Freeman, G.J., Ahmed, R., Restoring function in exhausted CDS T cells during chronic viral infection (2006) Nature, 439, pp. 682-687
  • Day, C.L., Kaufmann, D.E., Kiepiela, P., Brown, J.A., Moodley, E.S., Reddy, S., Mackey, E.W., DePierres, C., PD-1 expression on HIV-spccific T cells is associated with T-cell exhaustion and disease progression (2006) Nature, 443, pp. 350-354
  • Boettler, T., Panther, E., Bengsch, B., Nazarova, N., Spangenberg, H.C., Blum, H.E., Thimme, R., Expression of the interleukin-7 receptor α chain (CD127) on virus-specific CDS+ T cells identifies functionally and phe-notypically defined memory T cells during acute resolving hepatitis B virus infection (2006) J. Virol, 80, pp. 3532-3540
  • Urbani, S., Amadei, B., Tola, D., Massari, M., Schivazappa, S., Missale, G., Ferrari, C., PD-1 expression in acute hepatitis C virus (HCV) infection is associated with HCV-spccific CDS exhaustion (2006) J. Virol, 80, pp. 11398-11403
  • Das, S., Suarez, G., Beswick, E.J., Sierra, J.C., Graham, D.Y., Reyes, V.E., Expression of B7-H1 on gastric epithelial cells: Its potential role in regulating T cells during Helicobacter pylori infection (2006) J. Immunol, 176, pp. 3000-3009
  • Cohen, N., Morisset, J., Emilie, D., Induction of tolerance by Porphy-romonas gingivalis on APCS: A mechanism implicated in periodontal infection (2004) J. Dent. Res, 83, pp. 429-433
  • Sable, S.B., Kumar, R., Kalra, M., Verma, I., Khuller, G.K., Dobos, K., Belisle, J.T., Peripheral blood and pleural fluid mononuclear cell responses to low-molecular-mass secretory polypeptides of Mycobacterium tuberculosis in human models of immunity to tuberculosis (2005) Infect. Immun, 73, pp. 3547-3558
  • Nakae, S., Suto, H., Iikura, M., Kakurai, M., Sedgwick, J.D., Tsai, M., Galli, S.J., Mast cells enhance T cell activation: Importance of mast cell costimulatory molecules and secreted TNF (2006) J. Immunol, 176, pp. 2238-2248
  • Garcia, V.E., Quiroga, M.F., Ochoa, M.T., Ochoa, L., Pasquinelli, V., Fainboim, L., Olivares, L.M., Aversa, G., Signaling lymphocytic activation molecule expression and regulation in human intracellular infection correlate with Th1 cytokine patterns (2001) J. Immunol, 167, pp. 5719-5724
  • Okamoto, M., Hasegawa, Y., Hara, T., Hashimoto, N., Imaizumi, K., Shimokata, K., Kawabe, T., T-helpcr type 1/T-helper type 2 balance in malignant pleural effusions compared to tuberculous pleural effusions (2005) Chest, 128, pp. 4030-4035
  • Liang, S.C., Latchman, Y.E., Buhlmann, J.E., Tomczak, M.F., Horwitz, B.H., Freeman, G.J., Sharpe, A.H., Regulation of PD-1, PD-L1, and PD-L2 expression during normal and autoimmune responses (2003) Eur. J. Immunol, 33, pp. 2706-2716
  • Flies, D.B., Chen, L., The new B7s: Playing a pivotal role in tumor immunity (2007) J. Immunother, 30, pp. 251-260
  • Nishimura, H., Nose, M., Hiai, H., Minato, N., Honjo, T., Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor (1999) Immunity, 11, pp. 141-151
  • Latchman, Y.E., Liang, S.C., Wu, Y., Chemova, T., Sobel, R.A., Klemm, M., Kuchroo, V.K., Sharpe, A.H., PD-L1-deficient mice show that PD-L1 on T cells, antigen-presenting cells, and host tissues negatively regulates T cells (2004) Proc. Natl. Acad. Sci, USA, 101, pp. 10691-10696
  • Keir, M.E., Liang, S.C., Guleria, I., Latchman, Y.E., Qipo, A., Albacker, L.A., Koulmanda, M., Sharpe, A.H., Tissue expression of PD-L1 mediates peripheral T cell tolerance (2006) J. Exp. Med, 203, pp. 883-895
  • Kuipers, H., Muskens, F., Willart, M., Hijdra, D., van Assema, F.B., Coyle, A.J., Hoogsteden, H.C., Lambrecht, B.N., Contribution of the PD-1 ligands/PD-I signaling pathway to dendritic cell-mediated CD4+ T cell activation (2006) Eur. J. Immunol, 36, pp. 2472-2482
  • Blocki, F.A., Radhakrishnan, S., Van Keulen, V.P., Heckman, K.L., Ciric, B., Howe, C.L., Rodriguez, M., Pease, L.R., Induction of a gene expression program in dendritic cells with a cross-linking IgM antibody to the co-stimulatory molecule B7-DC (2006) FASEB J, 20, pp. 2408-2410
  • Rodig, N., T. Ryan, J. A. Allen, H. Pang, N. Grabie, T. Chemova, E. A. Greenfield, S. C. Liang, A. H. Sharpe, A. II. Lichtman, and G. J. Freeman. 2003. Endothelial expression of PD-L1 and PD-L2 down-regulates CD8+ Tcell activation and cytolysis. Eur. J. Immunol. 33: 3117-3126; Dong, H., S. E. Strome, D. R. Salomao, H. Tamura, F. Hirano, D. B. Flies, P. C. Roche, J. Lu, G. Zhu, K. Tamada, et al. 2002. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat. Med. 8: 793-800; Hadrup, S.R., Braendstrup, O., Jacobsen, G.K., Mortensen, S., Pedersen, L.O., Seremet, T., Andersen, M.H., Straten, P.T., Tumor infiltrating lymphocytes in seminoma lesions comprise clonally expanded cytotoxic T cells (2006) Int. J. Cancer, 119, pp. 831-838
  • Mittendorf, E.A., Storrer, C.E., Shriver, C.D., Ponniah, S., Peoples, G.E., Evaluation of the CD107 cytotoxicity assay for the detection of cytolytic CD8+ cells recognizing HER2/neu vaccine peptides (2005) Breast Cancer Res. Treat, 92, pp. 85-93
  • Petrovas, C., Casazza, J.P., Brenchley, J.M., Price, D.A., Gostick, E., Adams, W.C., Precopio, M.L., Koup, R.A., PD-1 is a regulator of virus-specific CDS+ T cell survival in HIV infection (2006) J. Exp. Med, 203, pp. 2281-2292
  • Trautmann, L., Janbazian, L., Chomont, N., Said, E.A., Gimmig, S., Bessette, B., Boulassel, M.R., Balderas, R.S., Upregulation of PD-1 expression on HIV-specific CDS+ T cells leads to reversible immune dysfunction (2006) Nat. Med, 12, pp. 1198-1202
  • Jun, H., Seo, S.K., Jeong, H.Y., Seo, H.M., Zhu, G., Chen, L., Choi, I.H., B7-H1 (CD274) inhibits the development of herpetic stromal keratitis (HSK) (2005) FEBS Lett, 579, pp. 6259-6264
  • Maier, H., Isogawa, M., Freeman, G.J., Chisari, F.V., PD-1: PD-L1 interactions contribute to the functional suppression of virus-specific CD8+ T lymphocytes in the liver (2007) J. Immunol, 178, pp. 2714-2720
  • Wolf, A.J., Desvignes, L., Linas, B., Banaiee, N., Tamura, T., Takatsu, K., Emst, J.D., Initiation of the adaptive immune response to Mycobacterium tuberculosis depends on antigen production in the local lymph node, not the lungs (2008) J. Exp. Med, 205, pp. 105-115
  • Alfaro, C., Murillo, O., Tirapu, I., Azpilicueta, A., Huarte, E., Anna, A., Arribillaga, L., Prieto, J., The im-munotherapy potential of agonistic anti-CD 137 (4-IBB) monoclonal antibodies for malignancies and chronic viral diseases] (2006) An. Sist. Sanit. Navar, 29, pp. 77-96

Citas:

---------- APA ----------
Jurado, J.O., Alvarez, I.B., Pasquinelli, V., Martínez, G.J., Quiroga, M.F., Abbate, E., Musella, R.M.,..., García, V.E. (2008) . Programmed death (PD)-1:PD-ligand 1/PD-ligand 2 pathway inhibits T cell effector functions during human tuberculosis. Journal of Immunology, 181(1), 116-125.
http://dx.doi.org/10.4049/jimmunol.181.1.116
---------- CHICAGO ----------
Jurado, J.O., Alvarez, I.B., Pasquinelli, V., Martínez, G.J., Quiroga, M.F., Abbate, E., et al. "Programmed death (PD)-1:PD-ligand 1/PD-ligand 2 pathway inhibits T cell effector functions during human tuberculosis" . Journal of Immunology 181, no. 1 (2008) : 116-125.
http://dx.doi.org/10.4049/jimmunol.181.1.116
---------- MLA ----------
Jurado, J.O., Alvarez, I.B., Pasquinelli, V., Martínez, G.J., Quiroga, M.F., Abbate, E., et al. "Programmed death (PD)-1:PD-ligand 1/PD-ligand 2 pathway inhibits T cell effector functions during human tuberculosis" . Journal of Immunology, vol. 181, no. 1, 2008, pp. 116-125.
http://dx.doi.org/10.4049/jimmunol.181.1.116
---------- VANCOUVER ----------
Jurado, J.O., Alvarez, I.B., Pasquinelli, V., Martínez, G.J., Quiroga, M.F., Abbate, E., et al. Programmed death (PD)-1:PD-ligand 1/PD-ligand 2 pathway inhibits T cell effector functions during human tuberculosis. J. Immunol. 2008;181(1):116-125.
http://dx.doi.org/10.4049/jimmunol.181.1.116