Bryostatin activates HIV-1 latent expression in human astrocytes through a PKC and NF-κB-dependent mechanism

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Díaz, Laura ^a,b   Martínez Bonet, Marta ^a   Sánchez, Javier ^a   Fernández Pineda, Alejandra ^a   Jiménez, José Luis ^a   Muñoz, Eduardo ^c   Moreno, Santiago ^d   Álvarez, Susana ^a   Muñoz Fernández, Ma Ángeles ^a  

^a HOSPITAL GENERAL UNIVERSITARIO GREGORIO MARAÑÓN   (Spain)

^b BIOMATERIALES Y NANOMEDICINA CIBER BBN   (Spain)

^c UNIVERSITY OF CÓRDOBA   (Spain)

^d HOSPITAL RAMÓN Y CAJAL   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BRYOSTATIN; BRYOSTATIN 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN KINASE C;

ASTROCYTE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; LONG TERMINAL REPEAT; METABOLISM; PROMOTER REGION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TUMOR CELL LINE; VIROLOGY; VIRUS LATENCY;

ASTROCYTES; BRYOSTATINS; CELL LINE, TUMOR; GENE EXPRESSION REGULATION, VIRAL; HIV INFECTIONS; HIV LONG TERMINAL REPEAT; HIV-1; HUMANS; NF-KAPPA B; PROMOTER REGIONS, GENETIC; PROTEIN KINASE C; SIGNAL TRANSDUCTION; TRANSCRIPTIONAL ACTIVATION; VIRUS LATENCY;

EID: 84937423781     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep12442     Document Type: Article

References (58)

1. Brack-Werner, R. Astrocytes: HIV cellular reservoirs and important participants in neuropathogenesis. AIDS 13, 1-22 (1999).
2. Canki, M. et al. Highly productive infection with pseudotyped human immunodeficiency virus type 1 (HIV-1) indicates no intracellular restrictions to HIV-1 replication in primary human astrocytes. J Virol 75, 7925-7933 (2001).
3. Clarke, J. N. et al. Novel pathway of human immunodeficiency virus type 1 uptake and release in astrocytes. Virology 348, (2006).
4. Speth, C., Dierich, M. P. & Sopper, S. HIV-infection of the central nervous system: the tightrope walk of innate immunity. Mol Immunol 42, 213-228 (2005).
5. Gonzalez-Scarano, F. & Martin-Garcia, J. The neuropathogenesis of AIDS. Nat Rev Immunol 5, 69-81 (2005).
6. Kaul, M., Garden, G. A. & Lipton, S. A. Pathways to neuronal injury and apoptosis in HIV-associated dementia. Nature 410, 988-994 (2001).
7. Kramer-Hammerle, S., Rothenaigner, I., Wolff, H., Bell, J. E. & Brack-Werner, R. Cells of the central nervous system as targets and reservoirs of the human immunodeficiency virus. Virus Res 111, 194-213 (2005).
8. Minagar, A. et al. The role of macrophage/microglia and astrocytes in the pathogenesis of three neurologic disorders: HIV-associated dementia, Alzheimer disease, and multiple sclerosis. J Neurol Sci 202, 13-23 (2002).
9. Schnell, G., Price, R. W., Swanstrom, R. & Spudich, S. Compartmentalization and clonal amplification of HIV-1 variants in the cerebrospinal fluid during primary infection. J Virol 84, 2395-2407 (2010).
10. Schnell, G., Joseph, S., Spudich, S., Price, R. W. & Swanstrom, R. HIV-1 replication in the central nervous system occurs in two distinct cell types. PLoS Pathog 7, e1002286 (2011).
11. Lehrman, G. et al. Depletion of latent HIV-1 infection in vivo: a proof-of-concept study. Lancet 366, 549-555 (2005).
12. Lindkvist, A. et al. Reduction of the HIV-1 reservoir in resting CD4+ T-lymphocytes by high dosage intravenous immunoglobulin treatment: a proof-of-concept study. AIDS Res Ther 6, 15 (2009).
13. Prins, J. M. et al. Immuno-activation with anti-CD3 and recombinant human IL-2 in HIV-1-infected patients on potent antiretroviral therapy. AIDS 13, 2405-2410 (1999).
14. Bisgrove, D., Lewinski, M., Bushman, F. & Verdin, E. Molecular mechanisms of HIV-1 proviral latency. Expert Rev Anti Infect Ther 3, 805-814 (2005).
15. Han, Y., Wind-Rotolo, M., Yang, H. C., Siliciano, J. D. & Siliciano, R. F. Experimental approaches to the study of HIV-1 latency. Nat Rev Microbiol 5, 95-106 (2007).
16. Scripture-Adams, D. D., Brooks, D. G., Korin, Y. D. & Zack, J. A. Interleukin-7 induces expression of latent human immunodeficiency virus type 1 with minimal effects on T-cell phenotype. J Virol 76, 13077-13082 (2002).
17. van Praag, R. M. et al. OKT3 and IL-2 treatment for purging of the latent HIV-1 reservoir in vivo results in selective long-lasting CD4+ T cell depletion. J Clin Immunol 21, 218-226 (2001).
18. Davidson, S. K., Allen, S. W., Lim, G. E., Anderson, C. M. & Haygood, M. G. Evidence for the biosynthesis of bryostatins by the bacterial symbiont "Candidatus Endobugula sertula" of the bryozoan Bugula neritina. Appl Environ Microbiol 67, 4531-4537 (2001).
19. Newton, A. C. Protein kinase C: poised to signal. Am J Physiol Endocrinol Metab 298, E395-402 (2010).
20. Reyland, M. E. Protein kinase C isoforms: Multi-functional regulators of cell life and death. Front Biosci (Landmark Ed) 14, 2386-2399 (2009).
21. He, X. et al. Bryostatin-5 blocks stromal cell-derived factor-1 induced chemotaxis via desensitization and down-regulation of cell surface CXCR4 receptors. Cancer Res 68, 8678-8686 (2008).
22. Boto, W. M., Brown, L., Chrest, J. & Adler, W. H. Distinct modulatory effects of bryostatin 1 and staurosporine on the biosynthesis and expression of the HIV receptor protein (CD4) by T cells. Cell Regul 2, 95-103 (1991).
23. Mehla, R. et al. Bryostatin modulates latent HIV-1 infection via PKC and AMPK signaling but inhibits acute infection in a receptor independent manner. PLoS One 5, e11160 (2010).
24. Asiedu, C., Biggs, J., Lilly, M. & Kraft, A. S. Inhibition of leukemic cell growth by the protein kinase C activator bryostatin 1 correlates with the dephosphorylation of cyclin-dependent kinase 2. Cancer Res 55, 3716-3720 (1995).
25. Nekhai, S. et al. HIV-1 Tat-associated RNA polymerase C-terminal domain kinase, CDK2, phosphorylates CDK7 and stimulates Tat-mediated transcription. Biochem J 364, 649-657 (2002).
26. Vlach, J. & Pitha, P. M. Activation of human immunodeficiency virus type 1 provirus in T-cells and macrophages is associated with induction of inducer-specific NF-kappa B binding proteins. Virology 187, 63-72 (1992).
27. Mutter, R. & Wills, M. Chemistry and clinical biology of the bryostatins. Bioorg Med Chem 8, 1841-1860 (2000).
28. Propper, D. J. et al. A phase II study of bryostatin 1 in metastatic malignant melanoma. Br J Cancer 78, 1337-1341 (1998).
29. Varterasian, M. L. et al. Phase II trial of bryostatin 1 in patients with relapsed low-grade non-Hodgkin's lymphoma and chronic lymphocytic leukemia. Clin Cancer Res 6, 825-828 (2000).
30. Varterasian, M. L. et al. Phase I study of bryostatin 1 in patients with relapsed non-Hodgkin's lymphoma and chronic lymphocytic leukemia. J Clin Oncol 16, 56-62 (1998).
31. Varterasian, M. L. et al. Phase II study of bryostatin 1 in patients with relapsed multiple myeloma. Invest New Drugs 19, 245-247 (2001).
32. Mohammad, R. M. et al. Sequential treatment of human chronic lymphocytic leukemia with bryostatin 1 followed by 2-chlorodeoxyadenosine: preclinical studies. Clin Cancer Res 4, 445-453 (1998).
33. Etcheberrigaray, R. et al. Therapeutic effects of PKC activators in Alzheimer's disease transgenic mice. Proc Natl Acad Sci USA 101, 11141-11146 (2004).
34. Nelson, T. J., Sen, A., Alkon, D. L. & Sun, M. K. Adduct formation in liquid chromatography-triple quadrupole mass spectrometric measurement of bryostatin 1. J Chromatogr B Analyt Technol Biomed Life Sci 944, 55-62 (2014).
35. Reynolds, J. L. et al. Proteomic analysis of the effects of cocaine on the enhancement of HIV-1 replication in normal human astrocytes (NHA). Brain Res 1123, 226-236 (2006).
36. Folgueira, L. et al. Protein kinase C-zeta mediates NF-kappa B activation in human immunodeficiency virus-infected monocytes. J Virol 70, 223-231 (1996).
37. Alvarez, S., Serramia, M. J., Fresno, M. & Munoz-Fernandez, M. A. HIV-1 envelope glycoprotein 120 induces cyclooxygenase-2 expression in astrocytoma cells through a nuclear factor-kappaB-dependent mechanism. Neuromolecular Med 9, 179-193 (2007).
38. Alvarez, S., Blanco, A., Kern, F., Fresno, M. & Munoz-Fernandez, M. A. HIV-2 induces NF-kappaB activation and cyclooxygenase-2 expression in human astroglial cells. Virology 380, 144-151 (2008).
39. Jeeninga, R. E. et al. Functional differences between the long terminal repeat transcriptional promoters of human immunodeficiency virus type 1 subtypes A through G. J Virol 74, 3740-3751 (2000).
40. Kulkosky, J. et al. Expression of latent HAART-persistent HIV type 1 induced by novel cellular activating agents. AIDS Res Hum Retroviruses 20, 497-505 (2004).
41. Ghosh, S., May, M. J. & Kopp, E. B. NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu Rev Immunol 16, 225-260 (1998).
42. Han, Y., He, T., Huang, D. R., Pardo, C. A. & Ransohoff, R. M. TNF-alpha mediates SDF-1 alpha-induced NF-kappa B activation and cytotoxic effects in primary astrocytes. J Clin Invest 108, 425-435 (2001).
43. Thomas, C. Roadblocks in HIV research: five questions. Nat Med 15, 855-859 (2009).
44. Sabri, F. et al. Nonproductive human immunodeficiency virus type 1 infection of human fetal astrocytes: independence from CD4 and major chemokine receptors. Virology 264, 370-384 (1999).
45. Tornatore, C., Nath, A., Amemiya, K. & Major, E. O. Persistent human immunodeficiency virus type 1 infection in human fetal glial cells reactivated by T-cell factor(s) or by the cytokines tumor necrosis factor alpha and interleukin-1 beta. J Virol 65, 6094-6100 (1991).
46. Perez, M. et al. Bryostatin-1 synergizes with histone deacetylase inhibitors to reactivate HIV-1 from latency. Curr HIV Res 8, 418-429 (2010).
47. Kovochich, M., Marsden, M. D. & Zack, J. A. Activation of latent HIV using drug-loaded nanoparticles. PLoS One 6, e18270 (2011).
48. Tornatore, C., Meyers, K., Atwood, W., Conant, K. & Major, E. Temporal patterns of human immunodeficiency virus type 1 transcripts in human fetal astrocytes. J Virol 68, 93-102 (1994).
49. Scheid, C. et al. Immunomodulation in patients receiving intravenous Bryostatin 1 in a phase I clinical study: comparison with effects of Bryostatin 1 on lymphocyte function in vitro. Cancer Immunol Immunother 39, 223-230 (1994).
50. Jones, K. A. & Peterlin, B. M. Control of RNA initiation and elongation at the HIV-1 promoter. Annu Rev Biochem 63, 717-743 (1994).
51. Duh, E. J., Maury, W. J., Folks, T. M., Fauci, A. S. & Rabson, A. B. Tumor necrosis factor alpha activates human immunodeficiency virus type 1 through induction of nuclear factor binding to the NF-kappa B sites in the long terminal repeat. Proc Natl Acad Sci USA 86, 5974-5978 (1989).
52. Roebuck, K. A., Gu, D. S. & Kagnoff, M. F. Activating protein-1 cooperates with phorbol ester activation signals to increase HIV-1 expression. AIDS 10, 819-826 (1996).
53. Yang, X., Chen, Y. & Gabuzda, D. ERK MAP kinase links cytokine signals to activation of latent HIV-1 infection by stimulating a cooperative interaction of AP-1 and NF-kappaB. J Biol Chem 274, 27981-27988 (1999).
54. Warrilow, D., Gardner, J., Darnell, G. A., Suhrbier, A. & Harrich, D. HIV type 1 inhibition by protein kinase C modulatory compounds. AIDS Res Hum Retroviruses 22, 854-864 (2006).
55. Gulakowski, R. J., McMahon, J. B., Buckheit, R. W., Jr., Gustafson, K. R. & Boyd, M. R. Antireplicative and anticytopathic activities of prostratin, a non-tumor-promoting phorbol ester, against human immunodeficiency virus (HIV). Antiviral Res 33, 87-97 (1997).
56. Hezareh, M. et al. Mechanisms of HIV receptor and co-receptor down-regulation by prostratin: role of conventional and novel PKC isoforms. Antivir Chem Chemother 15, 207-222 (2004).
57. Wang, S., Wang, Z., Dent, P. & Grant, S. Induction of tumor necrosis factor by bryostatin 1 is involved in synergistic interactions with paclitaxel in human myeloid leukemia cells. Blood 101, 3648-3657 (2003).
58. Rhoades, K. L., Cai, S., Golub, S. H. & Economou, J. S. Granulocyte-macrophage colony-stimulating factor and interleukin-4 differentially regulate the human tumor necrosis factor-alpha promoter region. Cell Immunol 161, 125-131 (1995).