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Mediators of Inflammation
Volume 2015, Article ID 120605, 11 pages
http://dx.doi.org/10.1155/2015/120605
Clinical Study

Administration of Panobinostat Is Associated with Increased IL-17A mRNA in the Intestinal Epithelium of HIV-1 Patients

1Department of Infectious Diseases, Aarhus University Hospital, 8200 Skejby, Denmark
2Department of Hepatology and Gastroenterology, Aarhus University Hospital, 8000 Aarhus, Denmark
3Department of Clinical Medicine, Aarhus University, 8000 Aarhus, Denmark
4Stereology and Electron Microscopy Laboratory, Centre for Stochastic Geometry and Advanced Bioimaging, Aarhus University Hospital, 8000 Aarhus, Denmark
5Aarhus Institute for Advanced Studies, Aarhus University, 8000 Aarhus, Denmark

Received 23 September 2015; Revised 10 November 2015; Accepted 15 November 2015

Academic Editor: Kong Chen

Copyright © 2015 Ane Bjerg Christensen et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. T. Blikslager, A. J. Moeser, J. L. Gookin, S. L. Jones, and J. Odle, “Restoration of barrier function in injured intestinal mucosa,” Physiological Reviews, vol. 87, no. 2, pp. 545–564, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. A. Kaser, S. Zeissig, and R. S. Blumberg, “Inflammatory bowel disease,” Annual Review of Immunology, vol. 28, pp. 573–621, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. J. M. Brenchley, T. W. Schacker, L. E. Ruff et al., “CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract,” Journal of Experimental Medicine, vol. 200, no. 6, pp. 749–759, 2004. View at Publisher · View at Google Scholar · View at Scopus
  4. E. J. Ciccone, S. W. Read, P. J. Mannon et al., “Cycling of gut mucosal CD4+T cells decreases after prolonged anti-retroviral therapy and is associated with plasma LPS levels,” Mucosal Immunology, vol. 3, no. 2, pp. 172–181, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. Q. Li, L. Dua, J. D. Estes et al., “Peak SIV replication in resting memory CD4+ T cells depletes gut lamina propria CD4+ T cells,” Nature, vol. 434, no. 7037, pp. 1148–1152, 2005. View at Publisher · View at Google Scholar · View at Scopus
  6. S. Mehandru, M. A. Poles, K. Tenner-Racz et al., “Primary HIV-1 infection is associated with preferential depletion of CD4+ T lymphocytes from effector sites in the gastrointestinal tract,” Journal of Experimental Medicine, vol. 200, no. 6, pp. 761–770, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. M. Guadalupe, E. Reay, S. Sankaran et al., “Severe CD4+ T-cell depletion in gut lymphoid tissue during primary human immunodeficiency virus type 1 infection and substantial delay in restoration following highly active antiretroviral therapy,” Journal of Virology, vol. 77, no. 21, pp. 11708–11717, 2003. View at Publisher · View at Google Scholar · View at Scopus
  8. J. J. Mattapallil, D. C. Douek, B. Hill, Y. Nishimura, M. Martin, and M. Roederer, “Massive infection and loss of memory CD4+ T cells in multiple tissues during acute SIV infection,” Nature, vol. 434, no. 7037, pp. 1093–1097, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. P. W. Denton, J. D. Estes, Z. Sun et al., “Antiretroviral pre-exposure prophylaxis prevents vaginal transmission of HIV-1 in humanized BLT mice,” PLoS Medicine, vol. 5, no. 1, article e16, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. Z. Sun, P. W. Denton, J. D. Estes et al., “Intrarectal transmission, systemic infection, and CD4+ T cell depletion in humanized mice infected with HIV-1,” Journal of Experimental Medicine, vol. 204, no. 4, pp. 705–714, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. J. M. Brenchley, D. A. Price, T. W. Schacker et al., “Microbial translocation is a cause of systemic immune activation in chronic HIV infection,” Nature Medicine, vol. 12, no. 12, pp. 1365–1371, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. J. M. Brenchley, M. Paiardini, K. S. Knox et al., “Differential Th17 CD4 T-cell depletion in pathogenic and nonpathogenic lentiviral infections,” Blood, vol. 112, no. 7, pp. 2826–2835, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. D. J. Cua and C. M. Tato, “Innate IL-17-producing cells: the sentinels of the immune system,” Nature Reviews Immunology, vol. 10, no. 7, pp. 479–489, 2010. View at Publisher · View at Google Scholar · View at Scopus
  14. N. R. Klatt and J. M. Brenchley, “Th17 cell dynamics in HIV infection,” Current Opinion in HIV and AIDS, vol. 5, no. 2, pp. 135–140, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. J. K. Kolls and A. Lindén, “Interleukin-17 family members and inflammation,” Immunity, vol. 21, no. 4, pp. 467–476, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. T. A. Rasmussen, M. Tolstrup, C. R. Brinkmann et al., “Panobinostat, a histone deacetylase inhibitor, for latent-virus reactivation in HIV-infected patients on suppressive antiretroviral therapy: a phase 1/2, single group, clinical trial,” The Lancet HIV, vol. 1, no. 1, pp. e13–e21, 2014. View at Publisher · View at Google Scholar · View at Scopus
  17. T. A. Rasmussen, O. S. Søgaard, C. Brinkmann et al., “Comparison of HDAC inhibitors in clinical development: effect on HIV production in latently infected cells and T-cell activation,” Human Vaccines and Immunotherapeutics, vol. 9, no. 5, pp. 993–1001, 2013. View at Publisher · View at Google Scholar · View at Scopus
  18. N. M. Archin, A. Espeseth, D. Parker, M. Cheema, D. Hazuda, and D. M. Margolis, “Expression of latent HIV induced by the potent HDAC inhibitor suberoylanilide hydroxamic acid,” AIDS Research and Human Retroviruses, vol. 25, no. 2, pp. 207–212, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. L. Shan, S. Xing, H.-C. Yang, H. Zhang, J. B. Margolick, and R. F. Siliciano, “Unique characteristics of histone deacetylase inhibitors in reactivation of latent HIV-1 in Bcl-2-transduced primary resting CD4+ T cells,” Journal of Antimicrobial Chemotherapy, vol. 69, no. 1, Article ID dkt338, pp. 28–33, 2014. View at Publisher · View at Google Scholar · View at Scopus
  20. F. Wightman, H. K. Lu, A. E. Solomon et al., “Entinostat is a histone deacetylase inhibitor selective for class 1 histone deacetylases and activates HIV production from latently infected primary T cells,” AIDS, vol. 27, no. 18, pp. 2853–2862, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. N. M. Archin, A. L. Liberty, A. D. Kashuba et al., “Administration of vorinostat disrupts HIV-1 latency in patients on antiretroviral therapy,” Nature, vol. 487, no. 7408, pp. 482–485, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. N. M. Archin, R. Bateson, M. K. Tripathy et al., “HIV-1 expression within resting CD4+ T cells after multiple doses of vorinostat,” Journal of Infectious Diseases, vol. 210, no. 5, pp. 728–735, 2014. View at Publisher · View at Google Scholar · View at Scopus
  23. J. H. Elliott, F. Wightman, A. Solomon et al., “Activation of HIV transcription with short-course vorinostat in HIV-infected patients on suppressive antiretroviral therapy,” PLoS Pathogens, vol. 10, no. 11, Article ID e1004473, 2014. View at Publisher · View at Google Scholar · View at Scopus
  24. C. A. Dinarello, G. Fossati, and P. Mascagni, “Histone deacetylase inhibitors for treating a spectrum of diseases not related to cancer,” Molecular Medicine, vol. 17, no. 5-6, pp. 333–352, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. A. S. Høgh Kølbæk Kjær, C. R. Brinkmann, C. A. Dinarello et al., “The histone deacetylase inhibitor panobinostat lowers biomarkers of cardiovascular risk and inflammation in HIV patients,” AIDS, vol. 29, no. 10, pp. 1195–1200, 2015. View at Publisher · View at Google Scholar
  26. M. C. Strain, S. M. Lada, T. Luong et al., “Highly precise measurement of HIV DNA by droplet digital PCR,” PLoS ONE, vol. 8, no. 4, Article ID e55943, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. O. S. Sogaard, M. E. Graversen, S. Leth et al., “The depsipeptide romidepsin reverses HIV-1 latency in vivo,” PLoS Pathogens, vol. 11, no. 9, Article ID e1005142, 2015. View at Publisher · View at Google Scholar
  28. S. Støy, A. Dige, T. D. Sandahl et al., “Cytotoxic T lymphocytes and natural killer cells display impaired cytotoxic functions and reduced activation in patients with alcoholic hepatitis,” American Journal of Physiology: Gastrointestinal and Liver Physiology, vol. 308, no. 4, pp. G269–G276, 2015. View at Publisher · View at Google Scholar · View at Scopus
  29. A. Brüel, T. E. H. Christoffersen, and J. R. Nyengaard, “Growth hormone increases the proliferation of existing cardiac myocytes and the total number of cardiac myocytes in the rat heart,” Cardiovascular Research, vol. 76, no. 3, pp. 400–408, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. K.-A. Dorph-Petersen, J. R. Nyengaard, and H. J. Gundersen, “Tissue shrinkage and unbiased stereological estimation of particle number and size,” Journal of Microscopy, vol. 204, no. 3, pp. 232–246, 2001. View at Publisher · View at Google Scholar · View at MathSciNet · View at Scopus
  31. M. Tolstrup, C. R. Brinkmann, T. A. Rasmussen et al., “Panobinostat dosing has broad but transient immunomodulatory effects in HIV patients,” in Proceedings of the Annual Conference on Retroviruses and Opportunistic Infections (CROI ’15), abstract 405, Seattle, Wash, USA, February 2015.
  32. P. L. Amlot, F. Tahami, D. Chinn, and E. Rawlings, “Activation antigen expression on human T cells. I. Analysis by two- colour flow cytometry of umbilical cord blood, adult blood and lymphoid tissue,” Clinical and Experimental Immunology, vol. 105, no. 1, pp. 176–182, 1996. View at Publisher · View at Google Scholar · View at Scopus
  33. R. De Maria, S. Fais, M. Silvestri et al., “Continuous in vivo activation and transient hyporesponsiveness to TcR/CD3 triggering of human gut lamina propria lymphocytes,” European Journal of Immunology, vol. 23, no. 12, pp. 3104–3108, 1993. View at Publisher · View at Google Scholar · View at Scopus
  34. C. T. Weaver, R. D. Hatton, P. R. Mangan, and L. E. Harrington, “IL-17 family cytokines and the expanding diversity of effector T cell lineages,” Annual Review of Immunology, vol. 25, pp. 821–852, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. F. Ragusa, “Th1 chemokines in ulcerative colitis,” La Clinica Terapeutica, vol. 166, no. 2, pp. e126–e131, 2015. View at Publisher · View at Google Scholar
  36. R. Olesen, S. Vigano, T. A. Rasmussen et al., “Innate immune activity correlates with CD4 T cell-associated HIV-1 DNA decline during latency-reversing treatment with panobinostat,” Journal of Virology, vol. 89, no. 20, pp. 10176–10189, 2015. View at Publisher · View at Google Scholar
  37. R. M. Onishi and S. L. Gaffen, “Interleukin-17 and its target genes: mechanisms of interleukin-17 function in disease,” Immunology, vol. 129, no. 3, pp. 311–321, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. M. Awane, P. G. Andres, D. J. Li, and H.-C. Reinecker, “NF-κB-inducing kinase is a common mediator of IL-17-, TNF-α-, and IL- 1β-induced chemokine promoter activation in intestinal epithelial cells,” Journal of Immunology, vol. 162, no. 9, pp. 5337–5344, 1999. View at Google Scholar · View at Scopus
  39. F. Fossiez, O. Djossou, P. Chomarat et al., “T cell interleukin-17 induces stromal cells to produce proinflammatory and hematopoietic cytokines,” The Journal of Experimental Medicine, vol. 183, no. 6, pp. 2593–2603, 1996. View at Publisher · View at Google Scholar · View at Scopus
  40. D. V. Jovanovic, J. A. Di Battista, J. Martel-Pelletier et al., “IL-17 stimulates the production and expression of proinflammatory cytokines, IL-β and TNF-α, by human macrophages,” Journal of Immunology, vol. 160, no. 7, pp. 3513–3521, 1998. View at Google Scholar · View at Scopus
  41. H. Park, Z. Li, X. O. Yang et al., “A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17,” Nature Immunology, vol. 6, no. 11, pp. 1133–1141, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. S. C. Liang, X.-Y. Tan, D. P. Luxenberg et al., “Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides,” The Journal of Experimental Medicine, vol. 203, no. 10, pp. 2271–2279, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. X. Guo, X. Jiang, Y. Xiao et al., “IL-17A signaling in colonic epithelial cells inhibits pro-inflammatory cytokine production by enhancing the activity of ERK and PI3K,” PLoS ONE, vol. 9, no. 2, Article ID e89714, 2014. View at Publisher · View at Google Scholar · View at Scopus
  44. W. O’Connor Jr., M. Kamanaka, C. J. Booth et al., “A protective function for interleukin 17A in T cell-mediated intestinal inflammation,” Nature Immunology, vol. 10, no. 6, pp. 603–609, 2009. View at Publisher · View at Google Scholar · View at Scopus