Impairment of T cell development and acute inflammatory response in HIV-1 Tat transgenic mice

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Fiume, Giuseppe ^a   Scialdone, Annarita ^a   Albano, Francesco ^a   Rossi, Annalisa ^a   Tuccillo, Franca Maria ^b   Rea, Domenica ^b   Palmieri, Camillo ^a   Caiazzo, Elisabetta ^c   Cicala, Carla ^c   Bellevicine, Claudio ^c   Falcone, Cristina ^a   Vecchio, Eleonora ^a   Pisano, Antonio ^a   Ceglia, Simona ^a   Mimmi, Selena ^a   Iaccino, Enrico ^a   Laurentiis, Annamaria De ^a   Pontoriero, Marilena ^a   Agosti, Valter ^a   Troncone, Giancarlo ^c   Mignogna, Chiara ^a   Palma, Giuseppe ^b   Arra, Claudio ^b   Mallardo, Massimo ^c   Maria Buonaguro, Franco ^b   Scala, Giuseppe ^a   Quinto, Ileana ^a   more..

^a UNIVERSITY MAGNA GRAECIA OF CATANZARO   (Italy)

^b NATIONAL CANCER INSTITUTE   (Italy)

^c UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; MICRORNA; TRANSACTIVATOR PROTEIN;

ANIMAL; BLOOD; CELL DIFFERENTIATION; CLUSTER ANALYSIS; CYTOLOGY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; LYMPHOCYTE COUNT; LYMPHOCYTE DEPLETION; LYMPHOPOIESIS; METABOLISM; MOUSE; T LYMPHOCYTE SUBPOPULATION; THYMOCYTE; THYMUS; TRANSGENIC MOUSE; VIROLOGY;

ANIMALS; CELL DIFFERENTIATION; CLUSTER ANALYSIS; CYTOKINES; GENE EXPRESSION; GENE EXPRESSION PROFILING; HIV INFECTIONS; HIV-1; LIPOPOLYSACCHARIDES; LYMPHOCYTE COUNT; LYMPHOCYTE DEPLETION; LYMPHOPOIESIS; MICE; MICE, TRANSGENIC; MICRORNAS; NF-KAPPA B; T-LYMPHOCYTE SUBSETS; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; THYMOCYTES; THYMUS GLAND;

EID: 84979872873     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep13864     Document Type: Article

References (76)

1. Ben Haij, N., Leghmari, K., Planes, R., Thieblemont, N. & Bahraoui, E. HIV-1 Tat protein binds to TLR4-MD2 and signals to induce TNF-alpha and IL-10. Retrovirology 10, 123, doi: 10.1186/1742-4690-10-123 (2013).
2. Brenchley, J. M. et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat. med. 12, 1365-1371, doi: 10.1038/nm1511 (2006).
3. Bagashev, A. & Sawaya, B. E. Roles and functions of HIV-1 Tat protein in the CNS: an overview. Virol. J. 10, 358, doi: 10.1186/1743-422X-10-358 (2013).
4. Cupp, C., Taylor, J. P., Khalili, K. & Amini, S. Evidence for stimulation of the transforming growth factor beta 1 promoter by HIV-1 Tat in cells derived from CNS. Oncogene 8, 2231-2236 (1993).
5. Ganju, R. K. et al. Human immunodeficiency virus tat modulates the Flk-1/KDR receptor, mitogen-activated protein kinases, and components of focal adhesion in Kaposi's sarcoma cells. J. Virol. 72, 6131-6137 (1998).
6. Kim, T. A. et al. HIV-1 Tat-mediated apoptosis in human brain microvascular endothelial cells. J. Immunol. 170, 2629-2637 (2003).
7. Nath, A. & Geiger, J. Neurobiological aspects of human immunodeficiency virus infection: neurotoxic mechanisms. Prog. Neurobiol. 54, 19-33 (1998).
8. Li, C. J., Friedman, D. J., Wang, C., Metelev, V. & Pardee, A. B. Induction of apoptosis in uninfected lymphocytes by HIV-1 Tat protein. Science 268, 429-431 (1995).
9. Sabatier, J. M. et al. Evidence for neurotoxic activity of tat from human immunodeficiency virus type 1. J. Virol. 65, 961-967 (1991).
10. Lepelley, A. et al. Innate sensing of HIV-infected cells. PLoS Pathog. 7, e1001284, doi: 10.1371/journal.ppat.1001284 (2011).
11. Schmidt, B., Ashlock, B. M., Foster, H., Fujimura, S. H. & Levy, J. A. HIV-infected cells are major inducers of plasmacytoid dendritic cell interferon production, maturation, and migration. Virology 343, 256-266, doi: 10.1016/j.virol.2005.09.059 (2005).
12. Ishii, K. J., Koyama, S., Nakagawa, A., Coban, C. & Akira, S. Host innate immune receptors and beyond: making sense of microbial infections. Cell Host Microbe 3, 352-363, doi: 10.1016/j.chom.2008.05.003 (2008).
13. Scala, G. et al. The expression of the interleukin 6 gene is induced by the human immunodeficiency virus 1 TAT protein. J. Exp. Med. 179, 961-971 (1994).
14. Li, J. C., Yim, H. C. & Lau, A. S. Role of HIV-1 Tat in AIDS pathogenesis: its effects on cytokine dysregulation and contributions to the pathogenesis of opportunistic infection. Aids 24, 1609-1623, doi: 10.1097/QAD.0b013e32833ac6a0 (2010).
15. Gerondakis, S., Fulford, T. S., Messina, N. L. & Grumont, R. J. NF-kappaB control of T cell development. Nat. Immunol. 15, 15-25, doi: 10.1038/ni.2785 (2014).
16. Baldwin, A. S., Jr. The NF-kappa B and I kappa B proteins: new discoveries and insights. Annu. Rev. Immunol. 14, 649-683, doi: 10.1146/annurev.immunol.14.1.649 (1996).
17. Kanarek, N., London, N., Schueler-Furman, O. & Ben-Neriah, Y. Ubiquitination and degradation of the inhibitors of NF-kappaB. Cold Spring Harb Perspect Biol. 2, a000166, doi: 10.1101/cshperspect.a000166 (2010).
18. Fiume, G. et al. Human immunodeficiency virus-1 Tat activates NF-kappaB via physical interaction with IkappaB-alpha and p65. Nucleic Acids Res. 40, 3548-3562, doi: 10.1093/nar/gkr1224 (2012).
19. Katsikis, P. D., Mueller, Y. M. & Villinger, F. The cytokine network of acute HIV infection: a promising target for vaccines and therapy to reduce viral set-point? PLoS Pathog. 7, e1002055, doi: 10.1371/journal.ppat.1002055 (2011).
20. Reuter, M. A., Pombo, C. & Betts, M. R. Cytokine production and dysregulation in HIV pathogenesis: lessons for development of therapeutics and vaccines. Cytokine Growth Factor Rev 23, 181-191, doi: 10.1016/j.cytogfr.2012.05.005 (2012).
21. Jeang, K. T., Giam, C. Z., Majone, F. & Aboud, M. Life, death, and tax: role of HTLV-I oncoprotein in genetic instability and cellular transformation. J Biol Chem. 279, 31991-31994, doi: 10.1074/jbc.R400009200 (2004).
22. Sun, S. C. & Yamaoka, S. Activation of NF-kappaB by HTLV-I and implications for cell transformation. Oncogene 24, 5952-5964, doi: 10.1038/sj.onc.1208969 (2005).
23. Yoshida, M. Multiple viral strategies of HTLV-1 for dysregulation of cell growth control. Annu. Rev. Immunol. 19, 475-496, doi: 10.1146/annurev.immunol.19.1.475 (2001).
24. de Meis, J. et al. Thymus atrophy and double-positive escape are common features in infectious diseases. J Parasitol Res. 2012, 574020, doi: 10.1155/2012/574020 (2012).
25. Love, P. E. & Bhandoola, A. Signal integration and crosstalk during thymocyte migration and emigration. Nat Rev Immunol. 11, 469-477, doi: 10.1038/nri2989 (2011).
26. Trampont, P. C. et al. CXCR4 acts as a costimulator during thymic beta-selection. Nat. Immunol. 11, 162-170, doi: 10.1038/ni.1830 (2010).
27. Wickremasinghe, M. I., Thomas, L. H., O'Kane, C. M., Uddin, J. & Friedland, J. S. Transcriptional mechanisms regulating alveolar epithelial cell-specific CCL5 secretion in pulmonary tuberculosis. J Biol Chem. 279, 27199-27210, doi: 10.1074/jbc.M403107200 (2004).
28. Cao, S., Zhang, X., Edwards, J. P. & Mosser, D. M. NF-kappaB1 (p50) homodimers differentially regulate pro-and antiinflammatory cytokines in macrophages. J Biol Chem 281, 26041-26050, doi: 10.1074/jbc.M602222200 (2006).
29. Belkaya, S. et al. Dynamic modulation of thymic microRNAs in response to stress. PloS one 6, e27580, doi: 10.1371/journal. pone.0027580 (2011).
30. Kuchen, S. et al. Regulation of microRNA expression and abundance during lymphopoiesis. Immunity 32, 828-839, doi: 10.1016/j.immuni.2010.05.009 (2010).
31. Li, Q. J. et al. miR-181a is an intrinsic modulator of T cell sensitivity and selection. Cell 129, 147-161, doi: 10.1016/j. cell.2007.03.008 (2007).
32. Sanchez-Del Cojo, M., Lopez-Huertas, M. R., Mateos, E., Alcami, J. & Coiras, M. Mechanisms of RNA interference in the HIV-1-host cell interplay. AIDS Rev 13, 149-160 (2011).
33. Bennasser, Y., Le, S. Y., Benkirane, M. & Jeang, K. T. Evidence that HIV-1 encodes an siRNA and a suppressor of RNA silencing. Immunity 22, 607-619, doi: 10.1016/j.immuni.2005.03.010 (2005).
34. Herbein, G. et al. Apoptosis of CD8+ T cells is mediated by macrophages through interaction of HIV gp120 with chemokine receptor CXCR4. Nature 395, 189-194, doi: 10.1038/26026 (1998).
35. Copeland, S. et al. Acute inflammatory response to endotoxin in mice and humans. Clin Diagn Lab Immun 12, 60-67, doi: 10.1128/CDLI.12.1.60-67.2005 (2005).
36. Godin, P. J. et al. Experimental human endotoxemia increases cardiac regularity: results from a prospective, randomized, crossover trial. Crit Care Med 24, 1117-1124 (1996).
37. van der Poll, T. et al. Endotoxin induces downregulation of tumor necrosis factor receptors on circulating monocytes and granulocytes in humans. Blood 86, 2754-2759 (1995).
38. Buonaguro, L., Buonaguro, F. M., Giraldo, G. & Ensoli, B. The human immunodeficiency virus type 1 Tat protein transactivates tumor necrosis factor beta gene expression through a TAR-like structure. J. Virol. 68, 2677-2682 (1994).
39. Kovanen, P. E. et al. T-cell development and function are modulated by dual specificity phosphatase DUSP5. J. Biol. Chem. 283, 17362-17369, doi: 10.1074/jbc.M709887200 (2008).
40. Pircher, H., Burki, K., Lang, R., Hengartner, H. & Zinkernagel, R. M. Tolerance induction in double specific T-cell receptor transgenic mice varies with antigen. Nature 342, 559-561, doi: 10.1038/342559a0 (1989).
41. Pircher, H. et al. T cell tolerance to Mlsa encoded antigens in T cell receptor V beta 8.1 chain transgenic mice. EMBO J. 8, 719-727 (1989).
42. Germeraad, W. T. et al. Development of thymic microenvironments in vitro is oxygen-dependent and requires permanent presence of T-cell progenitors. J Histochem Cytochem 51, 1225-1235 (2003).
43. Gaulton, G. N., Scobie, J. V. & Rosenzweig, M. HIV-1 and the thymus. Aids 11, 403-414 (1997).
44. Motohara, M. et al. Impaired T-cell differentiation in the thymus at the early stages of acute pathogenic chimeric simian-human immunodeficiency virus (SHIV) infection in contrast to less pathogenic SHIV infection. Microbes Infect. 8, 1539-1549, doi: 10.1016/j.micinf.2006.01.011 (2006).
45. McCune, J. M. Thymic function in HIV-1 disease. Sem Immunol 9, 397-404, doi: 10.1006/smim.1997.0098 (1997).
46. Joshi, V. V. et al. Pathology of suspected acquired immune deficiency syndrome in children: a study of eight cases. Pediatr Pathol 2, 71-87 (1984).
47. Rosenzweig, M., Clark, D. P. & Gaulton, G. N. Selective thymocyte depletion in neonatal HIV-1 thymic infection. Aids 7, 1601-1605 (1993).
48. Reimann, K. A. et al. A chimeric simian/human immunodeficiency virus expressing a primary patient human immunodeficiency virus type 1 isolate env causes an AIDS-like disease after in vivo passage in rhesus monkeys. J. Virol. 70, 6922-6928 (1996).
49. Joshi, V. V. & Oleske, J. M. Pathologic appraisal of the thymus gland in acquired immunodeficiency syndrome in children. A study of four cases and a review of the literature. Arch Pathol Lab Med 109, 142-146 (1985).
50. Kourtis, A. P. et al. Early progression of disease in HIV-infected infants with thymus dysfunction. N Engl J Med 335, 1431-1436, doi: 10.1056/NEJM199611073351904 (1996).
51. Muller, J. G. et al. Alterations of thymus cortical epithelium and interdigitating dendritic cells but no increase of thymocyte cell death in the early course of simian immunodeficiency virus infection. Am. J. Pathol. 143, 699-713 (1993).
52. Wykrzykowska, J. J. et al. Early regeneration of thymic progenitors in rhesus macaques infected with simian immunodeficiency virus. J. Exp. Med. 187, 1767-1778 (1998).
53. Prakash, O. et al. Human Kaposi's sarcoma cell-mediated tumorigenesis in human immunodeficiency type 1 tat-expressing transgenic mice. J. Natl. Cancer Inst 92, 721-728 (2000).
54. Vogel, J., Hinrichs, S. H., Reynolds, R. K., Luciw, P. A. & Jay, G. The HIV tat gene induces dermal lesions resembling Kaposi's sarcoma in transgenic mice. Nature 335, 606-611, doi: 10.1038/335606a0 (1988).
55. Hasegawa, H. et al. Thymus-derived leukemia-lymphoma in mice transgenic for the Tax gene of human T-lymphotropic virus type I. Nat. med. 12, 466-472, doi: 10.1038/nm1389 (2006).
56. Chang, J. R. et al. HIV-1 Tat protein promotes neuronal dysfunction through disruption of microRNAs. J. Biol. Chem. 286, 41125-41134, doi: 10.1074/jbc.M111.268466 (2011).
57. Eletto, D. et al. Inhibition of SNAP25 expression by HIV-1 Tat involves the activity of mir-128a. J. Cell. Physio. 216, 764-770, doi: 10.1002/jcp.21452 (2008).
58. Triboulet, R. et al. Suppression of microRNA-silencing pathway by HIV-1 during virus replication. Science 315, 1579-1582, doi: 10.1126/science.1136319 (2007).
59. Liu, G., Min, H., Yue, S. & Chen, C. Z. Pre-miRNA loop nucleotides control the distinct activities of mir-181a-1 and mir-181c in early T cell development. PloS one 3, e3592, doi: 10.1371/journal.pone.0003592 (2008).
60. Stacey, A. R. et al. Induction of a striking systemic cytokine cascade prior to peak viremia in acute human immunodeficiency virus type 1 infection, in contrast to more modest and delayed responses in acute hepatitis B and C virus infections. J. Virol. 83, 3719-3733, doi: 10.1128/JVI.01844-08 (2009).
61. Deeks, S. G., Tracy, R. & Douek, D. C. Systemic effects of inflammation on health during chronic HIV infection. Immunity 39, 633-645, doi: 10.1016/j.immuni.2013.10.001 (2013).
62. Hammer, R. E. et al. Genetic engineering of mammalian embryos. J. Anim. Sci. 63, 269-278 (1986).
63. Chisari, F. V. et al. Expression of hepatitis B virus large envelope polypeptide inhibits hepatitis B surface antigen secretion in transgenic mice. J. Virol. 60, 880-887 (1986).
64. Corallini, A. et al. Systemic expression of HIV-1 tat gene in transgenic mice induces endothelial proliferation and tumors of different histotypes. Cancer Res 53, 5569-5575 (1993).
65. Fiume, G. et al. Eukaryotic Initiation Factor 4H Is under Transcriptional Control of p65/NF-kappaB. PloS one 8, e66087, doi: 10.1371/journal.pone.0066087 (2013).
66. Fiume, G. et al. Computational analysis and in vivo validation of a microRNA encoded by the IBTK gene, a regulator of B-lymphocytes differentiation and survival. Comput. Biol. Chem. 33, 434-439, doi: 10.1016/j.compbiolchem.2009.08.001 (2009).
67. Spatuzza, C. et al. Physical and functional characterization of the genetic locus of IBtk, an inhibitor of Bruton's tyrosine kinase: evidence for three protein isoforms of IBtk. Nucleic Acids Res. 36, 4402-4416, doi: 10.1093/nar/gkn413 (2008).
68. de Laurentiis, A. et al. Mass spectrometry-based identification of the tumor antigen UN1 as the transmembrane CD43 sialoglycoprotein. Mol. Cell. Proteomics. 10, M111 007898, doi: 10.1074/mcp.M111.007898 (2011).
69. Janda, E. et al. Btk regulation in human and mouse B cells via protein kinase C phosphorylation of IBtkgamma. Blood 117, 6520-6531, doi: 10.1182/blood-2010-09-308080 (2011).
70. Puca, A. et al. IkappaB-alpha represses the transcriptional activity of the HIV-1 Tat transactivator by promoting its nuclear export. J. Biol. Chem. 282, 37146-37157, doi: 10.1074/jbc.M705815200 (2007).
71. Migliaccio, N. et al. B-cell receptor-guided delivery of peptide-siRNA complex for B-cell lymphoma therapy. Cancer Cell Int. 15, 50, doi: 10.1186/s12935-015-0202-4 (2015).
72. Pisano, A. et al. CRL3IBTK Regulates the Tumor Suppressor Pdcd4 through Ubiquitylation Coupled to Proteasomal Degradation. J. Biol. Chem. doi: 10.1074/jbc.M114.634535 (2015).
73. Schiavone, M. et al. Design and Characterization of a Peptide Mimotope of the HIV-1 gp120 Bridging Sheet. Int. J. Mol. Sci. 13, 5674-5699, doi: 10.3390/ijms13055674 (2012).
74. Vitagliano, L. et al. Structural and functional insights into IkappaB-alpha/HIV-1 Tat interaction. Biochimie 93, 1592-1600, doi: 10.1016/j.biochi.2011.05.025 (2011).
75. Palmieri, C. et al. Inhibition of HIV-1 replication in primary human monocytes by the IkappaB-alphaS32/36A repressor of NFkappaB. Retrovirology 1, 45, doi: 10.1186/1742-4690-1-45 (2004).
76. Tuccillo, F. M. et al. Cancer-associated CD43 glycoforms as target of immunotherapy. Mol. Cancer Ther. 13, 752-762, doi: 10.1158/1535-7163.MCT-13-0651 (2014).