Article information
Resumen
El monofosfato de adenosina cíclico (AMPc) induce la activación de la proteína cinasa A, la cual regula negativamente la activación, la proliferación celular y la producción de IL-2, en células T. En células infectadas con el virus de inmunodeficiencia humana, el monofosfato de adenosina cíclico suprime la actividad de transcripción del promotor del virus y el paso del ADN viral del citoplasma al núcleo. El incremento del monofosfato de adenosina cíclico mediado por células T reguladoras CD4+, empleando la inyección de esta molécula en células blanco a través de las uniones comunicantes o empleando el eje CD39-CD73 para generar adenosina es utilizado para suprimir otras poblaciones celulares.
En esta revisión se propone que la modulación del monofosfato de adenosina cíclico por las células T reguladoras CD4+ podría tener un papel dual durante la evolución de la infección por el virus de inmunodeficiencia humana. Su papel benéfico se centraría principalmente en el control de la replicación viral y factores de transcripción, o evitando la infección de nuevas células blanco por disminución en la expresión de los receptores virales. Paradójicamente, la segunda posibilidad es que el aumento del monofosfato de adenosina cíclico podría tener un papel perjudicial, debido al efecto negativo sobre la proliferación, activación, respuesta citotóxica y en la producción de citocinas que se observa durante la infección viral.
Palabras clave:
AMP cíclico
VIH
células T
replicación viral
uniones comunicantes
adenosina
Abstract
Cyclic adenosine monophosphate induces the activation of protein kinase A, which negatively regulates activation, proliferation and IL-2 production in T cells. In cells infected with human immunodeficiency virus, cyclic adenosine monophosphate suppresses the transcriptional activity of long terminal repeats and the amount of viral DNA from the cytoplasm to the nucleus. The increase in cyclic adenosine monophosphate mediated by CD4+ regulatory T cells, using either the influx of this molecule in target cells through the GAP junctions or by CD39-CD73 to generate adenosine, is used by CD4+ regulatory T cells to suppress other cell populations. In this review, we suggest that modulation of cyclic adenosine monophosphate by CD4+ regulatory T cells may have a dual role during the evolution of human immunodeficiency virus infection. The beneficial role would be mainly focused on the control of viral replication and transcription factors to replicate the virus, and/or preventing the infection of new target cells, decreasing the expression of the viral co-receptors. Paradoxically to this beneficial role, the second possibility is that increased cyclic adenosine monophosphate could have a detrimental role, due to the negative effect on proliferation, activation, cytotoxic response and cytokine production, which occurs during viral infection.
Key words:
Cyclic AMP
HIV
T cells
virus replication
Gap junctions
adenosine
Full text is only aviable in PDF
Referencias
[1.]
S. Gerlo, P. Verdood, R. Kooijman.
Modulation of cytokine production by cyclic adenosine monophosphate analogs in human leukocytes.
J Interferon Cytokine Res, 30 (2010), pp. 883-891
[2.]
T. Bopp, C. Becker, M. Klein, S. Klein-Hessling, A. Palmetshofer, E. Serfling, et al.
Cyclic adenosine monophosphate is a key component of regulatory T cell-mediated suppression.
J Exp Med, 204 (2007), pp. 1303-1310
[3.]
R. Bacchetta, E. Gambineri, M.G. Roncarolo.
Role of regulatory T cells and FOXP3 in human diseases.
J Allergy ClinImmunol, 120 (2007), pp. 227-235
[4.]
J. Schulze, A. Thomssen, P. Hartjen, I. Toth, C. Lehmann, D. Meyer-Olson, et al.
Comprehensive analysis of frequency and phenotype of T regulatory cells in HIV infection: CD39 expression of FoxP3+ T regulatory cells correlates with progressive disease.
J Virol, 85 (2010), pp. 1287-1297
[5.]
B. Hofmann, P. Nishanian, T. Nguyen, M. Liu, J.L. Fahey.
Restoration of T-cell function in HIV infection by reduction of intracellular cAMP levels with adenosine analogues.
AIDS, 7 (1993), pp. 659-664
[6.]
E.M. Aandahl, P. Aukrust, B.S. Skalhegg, F. Muller, S.S. Froland, V. Hansson, et al.
Protein kinase A type I antagonist restores immune responses of T cells from HIV-infected patients.
Faseb J, 12 (1998), pp. 855-862
[7.]
Y. Sun, L. Li, F. Lau, J.A. Beavo, E.A. Clark.
Infection of CD4+ memory T cells by HIV-1 requires expression of phosphodiesterase 4.
J Immunol, 165 (2000), pp. 1755-1761
[8.]
B. Banas, J. Eberle, D. Schlondorff, B. Luckow.
Modulation of HIV- 1 enhancer activity and virus production by cAMP.
FEBS Lett, 509 (2001), pp. 207-212
[9.]
A. Boasso, G.M. Shearer, C. Chougnet.
Immune dysregulation in human immunodeficiency virus infection: know it, fix it, prevent it?.
J InternMed, 265 (2009), pp. 78-96
[10.]
J.A. Martinson, A. Román-González, A.R. Tenorio, C.J. Montoya, C.N. Gichinga, M.T. Rugeles, et al.
Dendritic cells from HIV-1 infected individuals are less responsive to toll-like receptor (TLR) ligands.
Cell Immunol, 250 (2007), pp. 75-84
[11.]
K. Omori, J. Kotera.
Overview of PDEs and their regulation.
Circ Res, 100 (2007), pp. 309-327
[12.]
J.A. Beavo.
Cyclic nucleotide phosphodiesterases: Functional implications of multiple isoforms.
Physiol Rev, 75 (1995), pp. 725-748
[13.]
R.K. Sunahara, R. Taussig.
Isoforms of mammalian adenylyl cyclase: Multiplicities of signaling.
Mol Interv, 2 (2002), pp. 168-184
[14.]
C.W. Dessauer.
Adenylyl cyclase–A-kinase anchoring protein complexes: The next dimension in cAMP signaling.
Mol Pharmacol, 76 (2009), pp. 935-941
[15.]
S.H. Francis, M.A. Blount, J.D. Corbin.
Mammalian cyclic nucleotide phosphodiesterases: Molecular mechanisms and physiological functions.
Physiol Rev, 91 (2011), pp. 651-690
[16.]
H.P. Rang, M.M. Dale, J.M. Ritter, P.K. Moore.
Pharmacology.
5th, Elsevier, (2003),
[17.]
P. Borger, D.S. Postma, E. Vellenga, H.F. Kauffman.
Regulation of asthma- related T-cell cytokines by the cyclic AMP-dependent signalling pathway.
Clin Exp Allergy, 30 (2000), pp. 920-926
[18.]
R.P. Kwok, J.R. Lundblad, J.C. Chrivia, J.P. Richards, H.P. Bachinger, R.G. Brennan, et al.
Nuclear protein CBP is a coactivator for the transcription factor CREB.
Nature, 370 (1994), pp. 223-226
[19.]
A. Gupta, C. Terhorst.
CD3 delta enhancer. CREB interferes with the function of a murine CD3-delta A binding factor (M delta AF).
J Immunol, 152 (1994), pp. 3895-3903
[20.]
C.W. Chow, R.J. Davis.
Integration of calcium and cyclic AMP signaling pathways by 14-3-3.
Mol Cell Biol, 20 (2000), pp. 702-712
[21.]
K.M. Torgersen, T. Vang, H. Abrahamsen, S. Yaqub, K. Tasken.
Molecular mechanisms for protein kinase A-mediated modulation of immune function.
Cell Signal, 14 (2002), pp. 1-9
[22.]
K.J. Staples, M. Bergmann, K. Tomita, M.D. Houslay, I. McPhee, P.J. Barnes, et al.
Adenosine 3’,5’-cyclic monophosphate (cAMP)-dependent inhibition of IL-5 from human T lymphocytes is not mediated by the cAMP-dependent protein kinase A.
J Immunol, 167 (2001), pp. 2074-2080
[23.]
S.W. Henning, D.A. Cantrell.
GTPases in antigen receptor signalling.
Curr Opin Immunol, 10 (1998), pp. 322-329
[24.]
N. Seddiki, B. Santner-Nanan, J. Martinson, J. Zaunders, S. Sasson, A. Landay, et al.
Expression of interleukin (IL)-2 and IL-7 receptors discriminates between human regulatory and activated T cells.
J Exp Med, 203 (2006), pp. 1693-1700
[25.]
C.J. Workman, A.L. Szymczak-Workman, L.W. Collison, M.R. Pillai, D.A. Vignali.
The development and function of regulatory T cells.
Cell Mol Life Sci, 66 (2009), pp. 2603-2622
[26.]
T. Placke, H.G. Kopp, H.R. Salih.
Glucocorticoid-induced TNFR-related (GITR) protein and its ligand in antitumor immunity: Functional role and therapeutic modulation.
Clin Dev Immunol, (2010), pp. 239083
[27.]
B. Huang, J. Zhao, Z. Lei, S. Shen, D. Li, G.X. Shen, et al.
miR-142-3p restricts cAMP production in CD4+CD25- T cells and CD4+CD25+ TREG cells by targeting AC9 mRNA.
EMBO Rep, 10 (2009), pp. 180-185
[28.]
T. Barthlott, H. Moncrieffe, M. Veldhoen, C.J. Atkins, J. Christensen, A. O’Garra, et al.
CD25+ CD4+ T cells compete with naive CD4+ T cells for IL-2 and exploit it for the induction of IL-10 production.
Int Immunol, 17 (2005), pp. 279-288
[29.]
A.V. Bazhin, S. Kahnert, S. Kimpfler, D. Schadendorf, V. Umansky.
Distinct metabolism of cyclic adenosine monophosphate in regulatory and helper CD4+ T cells.
Mol Immunol, 47 (2010), pp. 678-684
[30.]
A. Marson, K. Kretschmer, G.M. Frampton, E.S. Jacobsen, J.K. Polansky, K.D. MacIsaac, et al.
Foxp3 occupancy and regulation of key target genes during T-cell stimulation.
Nature, 445 (2007), pp. 931-935
[31.]
Y. Zheng, S.Z. Josefowicz, A. Kas, T.T. Chu, M.A. Gavin, A.Y. Rudensky.
Genome-wide analysis of Foxp3 target genes in developing and mature regulatory T cells.
Nature, 445 (2007), pp. 936-940
[32.]
C.C. Johansson, T. Bryn, A. Yndestad, H.G. Eiken, V. Bjerkeli, S.S. Froland, et al.
Cytokine networks are pre-activated in T cells from HIV-infected patients on HAART and are under the control of cAMP.
AIDS, 18 (2004), pp. 171-179
[33.]
T. Bopp, N. Dehzad, S. Reuter, M. Klein, N. Ullrich, M. Stassen, et al.
Inhibition of cAMP degradation improves regulatory T cell-mediated suppression.
J Immunol, 182 (2009), pp. 4017-4024
[34.]
S. Yaqub, K. Tasken.
Role for the cAMP-protein kinase A signaling pathway in suppression of antitumor immune responses by regulatory T cells.
Crit Rev Oncog, 14 (2008), pp. 57-77
[35.]
S. Vendetti, M. Patrizio, A. Riccomi, M.T. De Magistris.
Human CD4+ T lymphocytes with increased intracellular cAMP levels exert regulatory functions by releasing extracellular cAMP.
J Leukoc Biol, 80 (2006), pp. 880-888
[36.]
S. Vendetti, A. Riccomi, A. Sacchi, L. Gatta, C. Pioli, M.T. De Magistris.
Cyclic adenosine 5’-monophosphate and calcium induce CD152 (CTLA-4) up-regulation in resting CD4+ T lymphocytes.
J Immunol, 169 (2002), pp. 6231-6235
[37.]
K. Li, K.J. Anderson, Q. Peng, A. Noble, B. Lu, A.P. Kelly, Cyclic AMP, et al.
plays a critical role in C3a-receptor-mediated regulation of dendritic cells in antigen uptake and T-cell stimulation.
Blood, 112 (2008), pp. 5084-5094
[38.]
T. Kambayashi, R.P. Wallin, H.G. Ljunggren.
cAMP-elevating agents suppress dendritic cell function.
J Leukoc Biol, 70 (2001), pp. 903-910
[39.]
A. la Sala, J. He, L. Laricchia-Robbio, S. Gorini, A. Iwasaki, M. Braun, et al.
Cholera toxin inhibits IL-12 production and CD8alpha+ dendritic cell differentiation by cAMP-mediated inhibition of IRF8 function.
J Exp Med, 206 (2009), pp. 1227-1235
[40.]
K.W. Moore, R. de Waal Malefyt, R.L. Coffman, A. O’Garra.
Interleukin- 10 and the interleukin-10 receptor.
Annu Rev Immunol, 19 (2001), pp. 683-765
[41.]
K. Steinbrink, E. Graulich, S. Kubsch, J. Knop, A.H. Enk.
CD4(+) and CD8(+) anergic T cells induced by interleukin-10-treated human dendritic cells display antigen-specific suppressor activity.
Blood, 99 (2002), pp. 2468-2476
[42.]
B. Koppelman, J.J. Neefjes, J.E. de Vries, R. de Waal Malefyt.
Interleukin- 10 down-regulates MHC class II alphabeta peptide complexes at the plasma membrane of monocytes by affecting arrival and recycling.
Immunity, 7 (1997), pp. 861-871
[43.]
C. Platzer, E. Fritsch, T. Elsner, M.H. Lehmann, H.D. Volk, S. Prosch.
Cyclic adenosine monophosphate-responsive elements are involved in the transcriptional activation of the human IL-10 gene in monocyticcells.
Eur J Immunol, 29 (1999), pp. 3098-3104
[44.]
W. Zhou, K. Hashimoto, K. Goleniewska, J.F. O’Neal, S. Ji, T.S. Blackwell, et al.
Prostaglandin I2 analogs inhibit proinflammatory cytokine production and T cell stimulatory function of dendritic cells.
J Immunol, 178 (2007), pp. 702-710
[45.]
Y. Son, T. Ito, Y. Ozaki, T. Tanijiri, T. Yokoi, K. Nakamura, et al.
Prostaglandin E2 is a negative regulator on human plasmacytoid dendritic cells.
Immunology, 119 (2006), pp. 36-42
[46.]
D. Sakata, C. Yao, S. Narumiya.
Prostaglandin E2, an immunoactivator.
J Pharmacol Sci, 112 (2010), pp. 1-5
[47.]
P.J. Bryce, M.J. Dascombe, I.V. Hutchinson.
Immunomodulatory effects of pharmacological elevation of cyclic AMP in T lymphocytes proceed via a protein kinase A independent mechanism.
Immunopharmacology, 41 (1999), pp. 139-146
[48.]
S. Fuld, G. Borland, S.J. Yarwood.
Elevation of cyclic AMP in Jurkat Tcells provokes distinct transcriptional responses through the protein kinase A (PKA) and exchange protein activated by cyclic AMP (EPAC) pathways.
Exp Cell Res, 309 (2005), pp. 161-173
[49.]
V.A. Boussiotis, G.J. Freeman, A. Berezovskaya, D.L. Barber, L.M. Nadler.
Maintenance of human T cell anergy: Blocking of IL-2 gene transcription by activated Rap1.
Science, 278 (1997), pp. 124-128
[50.]
J. Garay, J.A. D’Angelo, Y. Park, C.M. Summa, M.L. Aiken, E. Morales, et al.
Crosstalk between PKA and Epac regulates the phenotypic maturation and function of human dendritic cells.
J Immunol, 185 (2010), pp. 3227-3238
[51.]
M. Mandapathil, B. Hilldorfer, M.J. Szczepanski, M. Czystowska, M. Szajnik, J. Ren, et al.
Generation and accumulation of immunosuppressive adenosine by human CD4+CD25highFOXP3+ regulatory T cells.
J Biol Chem, 285 (2010), pp. 7176-7186
[52.]
M. Sitkovsky, D. Lukashev, S. Deaglio, K. Dwyer, S.C. Robson, A. Ohta.
Adenosine A2A receptor antagonists: Blockade of adenosinergic effects and T regulatory cells.
Br J Pharmacol, 153 (2008), pp. S457-S464
[53.]
R.P. Dong, J. Kameoka, M. Hegen, T. Tanaka, Y. Xu, S.F. Schlossman, et al.
Characterization of adenosine deaminase binding to human CD26 on T cells and its biologic role in immune response.
J Immunol, 156 (1996), pp. 1349-1355
[54.]
S. Majumdar, B.B. Aggarwal.
Adenosine suppresses activation of nuclear factor-kappaB selectively induced by tumor necrosis factor in different cell types.
Oncogene, 22 (2003), pp. 1206-1218
[55.]
G. Haskó, D.G. Kuhel, Z.H. Németh, J.G. Mabley, R.F. Stachlewitz, L. Virág, et al.
Inosine inhibits inflammatory cytokine production by a posttranscriptional mechanism and protects against endotoxin-induced shock.
J Immunol, 164 (2000), pp. 1013-1019
[56.]
F.G. Sajjadi, K. Takabayashi, A.C. Foster, R.C. Domingo, G.S. Firestein.
Inhibition of TNF-alpha expression by adenosine: Role of A3 adenosine receptors.
J Immunol, 156 (1996), pp. 3435-3442
[57.]
C.D. McWhinney, M.W. Dudley, T.L. Bowlin, N.P. Peet, L. Schook, M. Bradshaw, et al.
Activation of adenosine A3 receptors on macrophages inhibits tumor necrosis factor-alpha.
Eur J Pharmacol, 310 (1996), pp. 209-216
[58.]
X. Jin, R.K. Shepherd, B.R. Duling, J. Linden.
Inosine binds to A3 adenosine receptors and stimulates mast cell degranulation.
J Clin Invest, 100 (1997), pp. 2849-2857
[59.]
G. Borsellino, M. Kleinewietfeld, D. Di Mitri, A. Sternjak, A. Diamantini, R. Giometto, et al.
Expression of ectonucleotidase CD39 by Foxp3+ Treg cells: Hydrolysis of extracellular ATP and immune suppression.
Blood, 110 (2007), pp. 1225-1232
[60.]
H. Liao, M.C. Hyman, A.E. Baek, K. Fukase, D.J. Pinsky.
cAMP/CREBmediated transcriptional regulation of ectonucleoside triphosphate diphosphohydrolase 1 (CD39) expression.
J Biol Chem, 285 (2010), pp. 14791-14805
[61.]
S. Deaglio, K.M. Dwyer, W. Gao, D. Friedman, A. Usheva, A. Erat, et al.
Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression.
J Exp Med, 204 (2007), pp. 1257-1265
[62.]
J.J. Kobie, P.R. Shah, L. Yang, J.A. Rebhahn, D.J. Fowell, T.R. Mosmann.
T regulatory and primed uncommitted CD4 T cells express CD73, which suppresses effector CD4 T cells by converting 5’-adenosine monophosphate to adenosine.
J Immunol, 177 (2006), pp. 6780-6786
[63.]
A.A. Erdmann, Z.G. Gao, U. Jung, J. Foley, T. Borenstein, K.A. Jacobson, et al.
Activation of Th1 and Tc1 cell adenosine A2A receptors directly inhibits IL-2 secretion in vitro and IL-2-driven expansion in vivo.
Blood, 105 (2005), pp. 4707-4714
[64.]
T. Raskovalova, A. Lokshin, X. Huang, Y. Su, M. Mandic, H.M. Zarour, et al.
Inhibition of cytokine production and cytotoxic activity of human antimelanoma specific CD8+ and CD4+ T lymphocytes by adenosine-protein kinase A type I signaling.
Cancer Res, 67 (2007), pp. 5949-5956
[65.]
M.S. Alam, C.C. Kurtz, J.M. Wilson, B.R. Burnette, E.B. Wiznerowicz, W.G. Ross, et al.
A2A adenosine receptor (AR) activation inhibits pro-inflammatory cytokine production by human CD4+ helper T cells and regulates Helicobacter-induced gastritis and bacterial persistence.
Mucosal Immunol, 2 (2009), pp. 232-242
[66.]
W.H. Evans, S. Boitano.
Connexin mimetic peptides: Specific inhibitors of gap-junctional intercellular communication.
Biochem Soc Trans, 29 (2001), pp. 606-612
[67.]
P.C. Fonseca, O.K. Nihei, W. Savino, D.C. Spray, L.A. Alves.
Flow cytometry analysis of gap junction-mediated cell-cell communication: Advantages and pitfalls.
Cytometry A, 69 (2006), pp. 487-493
[68.]
M. Vaeth, T. Gogishvili, T. Bopp, M. Klein, F. Berberich-Siebelt, S. Gattenloehner, et al.
Regulatory T cells facilitate the nuclear accumulation of inducible cAMP early repressor (ICER) and suppress nuclear factor of activated T cell c1 (NFATc1).
Proc Natl Acad Sci U S A, 108 (2011), pp. 2480-2485
[69.]
M.E. Moreno-Fernández, C.M. Rueda, L.K. Rusie, C.A. Chougnet.
Regulatory T cells control HIV replication in activated T cells through a cAMP-dependent mechanism.
Blood, 117 (2011), pp. 5372-5380
[70.]
S. Ring, S. Karakhanova, T. Johnson, A.H. Enk, K. Mahnke.
Gap junctions between regulatory T cells and dendritic cells prevent sensitization of CD8(+) T cells.
J Allergy Clin Immunol, 125 (2010), pp. 237-246
[71.]
M. Fassbender, B. Gerlitzki, N. Ullrich, C. Lupp, M. Klein, M.P. Radsak, et al.
Cyclic adenosine monophosphate and IL-10 coordinately contribute to nTreg cell-mediated suppression of dendritic cell activation.
Cell Immunol, 265 (2010), pp. 91-96
[72.]
D.B. Leal, C.A. Streher, C. Bertoncheli, M. de, L.F. Carli, C.A. Leal, J.E. da Silva, et al.
HIV infection is associated with increased NTPDase activity that correlates with CD39-positive lymphocytes.
Biochim Biophys Acta, 1746 (2005), pp. 129-134
[73.]
P. Nigam, V. Velu, S. Kannanganat, L. Chennareddi, S. Kwa, M. Siddiqui, et al.
Expansion of FOXP3+ CD8 T cells with suppressive potential in colorectal mucosa following a pathogenic simian immunodeficiency virus infection correlates with diminished antiviral T cell response and viral control.
J Immunol, 184 (2010), pp. 1690-1701
[74.]
B. Hofmann, P. Nishanian, T. Nguyen, P. Insixiengmay, J.L. Fahey.
Human immunodeficiency virus proteins induce the inhibitory cAMP/protein kinase A pathway in normal lymphocytes.
Proc Natl Acad Sci U S A, 90 (1993), pp. 6676-6680
[75.]
A.M. Masci, M. Galgani, S. Cassano, S. De Simone, A. Gallo, V. De Rosa, et al.
HIV-1 gp120 induces anergy in naive T lymphocytes through CD4-independent protein kinase-A-mediated signaling.
J Leukoc Biol, 74 (2003), pp. 1117-1124
[76.]
C. Becker, C. Taube, T. Bopp, K. Michel, J. Kubach, S. Reuter, et al.
Protection from graft-versus-host disease by HIV-1 envelope protein gp120-mediated activation of human CD4+CD25+ regulatory T cells.
Blood, 114 (2009), pp. 1263-1269
[77.]
H.J. Epple, C. Loddenkemper, D. Kunkel, H. Troger, J. Maul, V. Moos, et al.
Mucosal but not peripheral FOXP3+ regulatory T cells are highly increased in untreated HIV infection and normalize after suppressive HAART.
Blood, 108 (2006), pp. 3072-3078
[78.]
J.M. Martínez-Navio, N. Climent, R. Pacheco, F. García, M. Plana, M. Nomdedeu, et al.
Immunological dysfunction in HIV-1-infected individuals caused by impairment of adenosine deaminase-induced costimulation of T-cell activation.
Immunology, 128 (2009), pp. 393-404
[79.]
A. Valenzuela, J. Blanco, C. Callebaut, E. Jacotot, C. Lluis, A.G. Hovanessian, et al.
HIV-1 envelope gp120 and viral particles block adenosine deaminase binding to human CD26.
Adv Exp Med Biol, 421 (1997), pp. 185-192
[80.]
J. Blanco, A. Valenzuela, C. Herrera, C. Lluis, A.G. Hovanessian, R. Franco.
The HIV-1 gp120 inhibits the binding of adenosine deaminase to CD26 by a mechanism modulated by CD4 and CXCR4 expression.
FEBS Lett, 477 (2000), pp. 123-128
[81.]
S. Wrenger, D. Reinhold, J. Faust, C. Mrestani-Klaus, W. Brandt, A. Fengler, et al.
Effects of nonapeptides derived from the N-terminal structure of human immunodeficiency virus-1 (HIV-1) Tat on suppression of CD26-dependent T cell growth.
Adv Exp Med Biol, 477 (2000), pp. 161-165
[82.]
J. Navarro, C. Punzon, J.L. Jiménez, E. Fernández-Cruz, A. Pizarro, M. Fresno, et al.
Inhibition of phosphodiesterase type IV suppresses human immunodeficiency virus type 1 replication and cytokine production in primary T cells: Involvement of NF-kappaB and NFAT.
J Virol, 72 (1998), pp. 4712-4720
[83.]
M. Rincón, A. Tugores, A. López-Rivas, A. Silva, M. Alonso, M.O. De Landazuri, et al.
Prostaglandin E2 and the increase of intracellular cAMP inhibit the expression of interleukin 2 receptors in human T cells.
Eur J Immunol, 18 (1988), pp. 1791-1796
[84.]
M.M. Hayes, B.R. Lane, S.R. King, D.M. Markovitz, M.J. Coffey.
Prostaglandin E(2) inhibits replication of HIV-1 in macrophages through activation of protein kinase A.
Cell Immunol, 215 (2002), pp. 61-71
[85.]
M. Thivierge, C. Le Gouill, M.J. Tremblay, J. Stankova, M. Rola-Pleszczynski.
Prostaglandin E2 induces resistance to human immunodeficiency virus-1 infection in monocyte-derived macrophages: Down-regulation of expression by cyclic adenosine monophosphate.
Blood, 92 (1998), pp. 40-45
[86.]
C. Barat, C. Gilbert, M. Imbeault, M.J. Tremblay.
Extracellular ATP reduces HIV-1 transfer from immature dendritic cells to CD4+ T lymphocytes.
Retrovirology, 5 (2008), pp. 30
[87.]
Y. By, J.M. Durand-Gorde, J. Condo, P.J. Lejeune, E. Fenouillet, R. Guieu, et al.
Monoclonal antibody-assisted stimulation of adenosine A2A receptors induces simultaneous down-regulation of CXCR4 and CCR5 on CD4+ T-cells.
Hum Immunol, 71 (2010), pp. 1073-1076
Copyright © 2012. Asociación Colombiana de Infectología (ACIN)
