CUGBP1 is required for IFNβ-mediated induction of dominant-negative CEBPβ and suppression of SIV replication in macrophages

Journal of Immunology

Volumn 179, Issue 11, 2007, Pages 7262-7269

  Dudaronek, Justyna M ^a   Barber, Sheila A ^b   Clements, Janice E ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BOOZ ALLEN HAMILTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; BINDING PROTEIN; MESSENGER RNA; PROTEIN CUGBP1; PROTEIN INHIBITOR; PROTEIN LIP; UNCLASSIFIED DRUG; CCAAT ENHANCER BINDING PROTEIN BETA; CUGBP1 PROTEIN, HUMAN; RNA BINDING PROTEIN; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN; CONTROLLED STUDY; CYTOKINE PRODUCTION; HUMAN; HUMAN CELL; INNATE IMMUNITY; MACACA; MACROPHAGE; MONOCYTE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; RNA TRANSLATION; SIGNAL TRANSDUCTION; SIMIAN IMMUNODEFICIENCY VIRUS; VIRUS INFECTION; VIRUS REPLICATION; ACQUIRED IMMUNE DEFICIENCY SYNDROME; ANIMAL; BIOSYNTHESIS; CELL CULTURE; CELL STRAIN U937; DISEASE MODEL; DRUG ANTAGONISM; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; PHOSPHORYLATION; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIROLOGY;

AIDS DEMENTIA COMPLEX; ANIMALS; CCAAT-ENHANCER-BINDING PROTEIN-BETA; CELLS, CULTURED; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; HUMANS; INTERFERON-BETA; MACACA MULATTA; MACROPHAGES; PHOSPHORYLATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS; SIMIAN IMMUNODEFICIENCY VIRUS; U937 CELLS; VIRUS REPLICATION;

EID: 38849119807     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.179.11.7262     Document Type: Article

References (62)

1. Griffin, D. E. 2003. Immune responses to RNA-virus infections of the CNS. Nat. Rev. Immunol. 3: 493-502.
2. Honda, Y., L. Rogers, K. Nakata, B. Y. Zhao, R. Pine, Y. Nakai, K. Kurosu, W. N. Rom, and M. Weiden. 1998. Type I interferon induces inhibitory 16-kD CCAAT/enhancer binding protein (C/EBP)β, repressing the HIV-1 long terminal repeat in macrophages: pulmonary tuberculosis alters C/EBP expression, enhancing HIV-1 replication. J. Exp. Med. 188: 1255-1265.
3. Kornbluth, R. S., P. S. Oh, J. R. Munis, P. H. Cleveland, and D. D. Richman. 1990. The role of interferons in the control of HIV replication in macrophages. Clin. Immunol. Immunopathol. 54: 200-219.
4. Barber, S. A., D. S. Herbst, B. T. Bullock, L. Gama, and J. E. Clements. 2004. Innate immune responses and control of acute simian immunodeficiency virus replication in the central nervous system. J. Neurovirol. 10(Suppl. 1): 15-20.
5. Williams, K. C., S. Corey, S. V. Westmoreland, D. Pauley, H. Knight, C. deBakker, X. Alvarez, and A. A. Lackner. 2001. Perivascular macrophages are the primary cell type productively infected by simian immunodeficiency virus in the brains of macaques: implications for the neuropathogenesis of AIDS. J. Exp. Med. 193: 905-915.
6. Davis, L. E., B. L. Hjelle, V. E. Miller, D. L. Palmer, A. L. Llewellyn, T. L. Merlin, S. A. Young, R. G. Mills, W. Wachsman, and C. A. Wiley. 1992. Early viral brain invasion in iatrogenic human immunodeficiency virus infection. Neurology 42: 1736-1739.
7. An, S. F., M. Groves, F. Gray, and F. Scaravilli. 1999. Early entry and widespread cellular involvement of HIV-1 DNA in brains of HIV-1 positive asymptomatic individuals. J. Neuropathol. Exp. Neurol. 58: 1156-1162.
8. Flaherty, M. T., D. A. Hauer, J. L. Mankowski, M. C. Zink, and J. E. Clements. 1997. Molecular and biological characterization of a neurovirulent molecular clone of simian immunodeficiency virus. J. Virol. 71: 5790-5798.
9. Mankowski, J. L., M. T. Flaherty, J. P. Spelman, D. A. Hauer, P. J. Didier, A. M. Amedee, M. Murphey-Corb, L. M. Kirstein, A. Munoz, J. E. Clements, and M. C. Zink. 1997. Pathogenesis of simian immunodeficiency virus encephalitis: viral determinants of neurovirulence. J. Virol. 71: 6055-6060.
10. Zink, M. C., A. M. Amedee, J. L. Mankowski, L. Craig, P. Didier, D. L. Carter, A. Munoz, M. Murphey-Corb, and J. E. Clements. 1997. Pathogenesis of SIV encephalitis: selection and replication of neurovirulent SIV. Am. J. Pathol. 151: 793-803.
11. Clements, J. E., M. Li, L. Gama, B. Bullock, L. M. Carruth, J. L. Mankowski, and M. C. Zink. 2005. The central nervous system is a viral reservoir in simian immunodeficiency virus, infected macaques on combined antiretroviral therapy: a model for human immunodeficiency virus patients on highly active antiretroviral therapy. J. Neurovirol. 11: 180-189.
12. Barber, S. A., L. Gama, J. M. Dudaronek, T. Voelker, P. M. Tarwater, and J. E. Clements. 2006. Mechanism for the establishment of transcriptional HIV latency in the brain in a simian immunodeficiency virus-macaque model. J. Infect. Dis. 193: 963-970.
13. Clements, J. E., T. Babas, J. L. Mankowski, K. Suryanarayana, M. Piatak, Jr., P. M. Tarwater, J. D. Lifson, and M. C. Zink. 2002. The central nervous system as a reservoir for simian immunodeficiency virus (SIV): steady-state levels of SIV DNA in brain from acute through asymptomatic infection. J. Infect. Dis. 186: 905-913.
14. Gessani, S., P. Puddu, B. Varano, P. Borghi, L. Conti, L. Fantuzzi, G. Gherardi, and F. Belardelli. 1994. Role of endogenous interferon-β in the restriction of HIV replication in human monocyte/macrophages. J. Leukocyte Biol. 56: 358-361.
15. Gessani, S., P. Puddu, B. Varano, P. Borghi, L. Conti, L. Fantuzzi, M. Papacchini, and F. Belardelli. 1994. Role of interferons in the restriction of HIV replication in human monocytes/macrophages. Res. Immunol. 145: 659-662; discussion 662-653.
16. Gessani, S., P. Puddu, B. Varano, P. Borghi, L. Conti, L. Fantuzzi, and F. Belardelli. 1994. Induction of β interferon by human immunodeficiency virus type 1 and its gp120 protein in human monocytes-macrophages: role of β interferon in restriction of virus replication. J. Virol. 68: 1983-1986.
17. Weiden, M., N. Tanaka, Y. Qiao, B. Y. Zhao, Y. Honda, K. Nakata, A. Canova, D. E. Levy, W. N. Rom, and R. Pine. 2000. Differentiation of monocytes to macrophages switches the Mycobacterium tuberculosis effect on HIV-1 replication from stimulation to inhibition: modulation of interferon response and CCAAT/enhancer binding protein β expression. J. Immunol. 165: 2028-2039.
18. Ossipow, V., P. Descombes, and U. Schibler. 1993. CCAAT/enhancer-binding protein mRNA is translated into multiple proteins with different transcription activation potentials. Proc. Natl. Acad. Sci. USA 90: 8219-8223.
19. Henderson, A. J., X. Zou, and K. L. Calame. 1995. C/EBP proteins activate transcription from the human immunodeficiency virus type 1 long terminal repeat in macrophages/monocytes. J. Virol. 69: 5337-5344.
20. Henderson, A. J., R. I. Connor, and K. L. Calame. 1996. C/EBP activators are required for HIV-1 replication and proviral induction in monocytic cell lines. Immunity 5: 91-101.
21. + T cells. Proc. Natl. Acad. Sci. USA 94: 8714-8719.
22. Descombes, P., and U. Schibler. 1991. A liver-enriched transcriptional activator protein, LAP, and a transcriptional inhibitory protein, LIP, are translated from the same mRNA. Cell 67: 569-579.
23. Timchenko, N. A., A. L. Welm, X. Lu, and L. T. Timchenko. 1999. CUG repeat binding protein (CUGBP1) interacts with the 5′ region of C/EBPβ mRNA and regulates translation of C/EBPβ isoforms. Nucleic Acids Res. 27: 4517-4525.
24. Timchenko, N. A., G. L. Wang, and L. T. Timchenko. 2005. RNA CUG-binding protein 1 increases translation of 20-kDa isoform of CCAAT/enhancer-binding protein β by interacting with the α and β subunits of eukaryotic initiation translation factor 2. J. Biol. Chem. 280: 20549-20557.
25. Baldwin, B. R., N. A. Timchenko, and C. A. Zahnow. 2004. Epidermal growth factor receptor stimulation activates the RNA binding protein CUG-BP1 and increases expression of C/EBPβ-LIP in mammary epithelial cells. Mol. Cell. Biol. 24: 3682-3691.
26. Timchenko, N. A., Z. J. Cai, A. L. Welm, S. Reddy, T. Ashizawa, and L. T. Timchenko. 2001. RNA CUG repeats sequester CUGBP1 and alter protein levels and activity of CUGBP1. J. Biol. Chem. 276: 7820-7826.
27. Welm, A. L., S. L. Mackey, L. T. Timchenko, G. J. Darlington, and N. A. Timchenko. 2000. Translational induction of liver-enriched transcriptional inhibitory protein during acute phase response leads to repression of CCAAT/enhancer binding protein α mRNA. J. Biol. Chem. 275: 27406-27413.
28. Zink, M. C., K. Suryanarayana, J. L. Mankowski, A. Shen, M. Piatak, Jr., J. P. Spelman, D. L. Carter, R. J. Adams, J. D. Lifson, and J. E. Clements. 1999. High viral load in the cerebrospinal fluid and brain correlates with severity of simian immunodeficiency virus encephalitis. J. Virol. 73: 10480-10488.
29. Niranjanakumari, S., E. Lasda, R. Brazas, and M. A. Garcia-Blanco. 2002. Reversible crosslinking combined with immunoprecipitation to study RNA-protein interactions in vivo. Methods 26: 182-190.
30. Hoshino, Y., K. Nakata, S. Hoshino, Y. Honda, D. B. Tse, T. Shioda, W. N. Rom, and M. Weiden. 2002. Maximal HIV-1 replication in alveolar macrophages during tuberculosis requires both lymphocyte contact and cytokines. J. Exp. Med. 195: 495-505.
31. Korth, M. J., M. D. Taylor, and M. G. Katze. 1998. Interferon inhibits the replication of HIV-1, SIV, and SHIV chimeric viruses by distinct mechanisms. Virology 247: 265-273.
32. Sears, R. C., and L. Sealy. 1994. Multiple forms of C/EBP β bind the EFII enhancer sequence in the Rous sarcoma virus long terminal repeat. Mol. Cell. Biol. 14: 4855-4871.
33. Silverman, R. H. 1997. 2-5A-Dependent RNase L: a regulated endoribonuclease in the interferon system. In Ribonucleases: Structure and Functions. G. D' Alessio and J. F. Riordan, eds. Academic Press, New York, NY, pp. 515-551.
34. de Veer, M. J., M. Holko, M. Frevel, E. Walker, S. Der, J. M. Paranjape, R. H. Silverman, and B. R. Williams. 2001. Functional classification of interferon-stimulated genes identified using microarrays. J. Leukocyte Biol. 69: 912-920.
35. Sebastian, T., and P. F. Johnson. 2006. Stop and go: anti-proliferative and mitogenic functions of the transcription factor C/EBPβ. Cell Cycle 5: 953-957.
36. Sebastian, T., R. Malik, S. Thomas, J. Sage, and P. F. Johnson. 2005. C/EBPβ cooperates with RB:E2F to implement Ras(V12)-induced cellular senescence. EMBO J. 24: 3301-3312.
37. Zahnow, C. A., R. D. Cardiff, R. Laucirica, D. Medina, and J. M. Rosen. 2001. A role for CCAAT/enhancer binding protein β-liver-enriched inhibitory protein in mammary epithelial cell proliferation. Cancer Res. 61: 261-269.
38. Zahnow, C. A., P. Younes, R. Laucirica, and J. M. Rosen. 1997. Overexpression of C/EBPβ-LIP, a naturally occurring, dominant-negative transcription factor, in human breast cancer. J. Natl. Cancer Inst. 89: 1887-1891.
39. Bae, E. J., and S. G. Kim. 2005. Enhanced CCAAT/enhancer-binding protein β-liver-enriched inhibitory protein production by Oltipraz, which accompanies CUG repeat-binding protein-1 (CUGBP1) RNA-binding protein activation, leads to inhibition of preadipocyte differentiation. Mol. Pharmacol. 68: 660-669.
40. Samuel, C. E. 2001. Antiviral actions of interferons. Clin. Microbiol. Rev. 14: 778-809, table of contents.
41. Peng, G., K. J. Lei, W. Jin, T. Greenwell-Wild, and S. M. Wahl. 2006. Induction of APOBEC3 family proteins, a defensive maneuver underlying interferon-induced anti-HIV-1 activity. J. Exp. Med. 203: 41-46.
42. Sheehy, A. M., N. C. Gaddis, J. D. Choi, and M. H. Malim. 2002. Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 418: 646-650.
43. Stremlau, M., C. M. Owens, M. J. Perron, M. Kiessling, P. Autissier, and J. Sodroski. 2004. The cytoplasmic body component TRIM5α restricts HIV-1 infection in Old World monkeys. Nature 427: 848-853.
44. Musunuru, K. 2003. Cell-specific RNA-binding proteins in human disease. Trends Cardiovasc. Med. 13: 188-195.
45. Krishnan, V., and S. L. Zeichner. 2004. Alterations in the expression of DEAD-box and other RNA binding proteins during HIV-1 replication. Retrovirology 1: 42.
46. Dayton, A. I. 2004. Within you, without you: HIV-1 rev and RNA export. Retrovirology 1: 35.
47. Jacquenet, S., A. Mereau, P. S. Bilodeau, L. Damier, C. M. Stoltzfus, and C. Branlant. 2001. A second exon splicing silencer within human immunodeficiency virus type 1 tat exon 2 represses splicing of Tat mRNA and binds protein hnRNP H. J. Biol. Chem. 276: 40464-40475.
48. Marchand, V., A. Mereau, S. Jacquenet, D. Thomas, A. Mougin, R. Gattoni, J. Stevenin, and C. Branlant. 2002. A Janus splicing regulatory element modulates HIV-1 tat and rev mRNA production by coordination of hnRNP A1 cooperative binding. J. Mol. Biol. 323: 629-652.
49. Mouland, A. J., H. Xu, H. Cui, W. Krueger, T. P. Munro, M. Prasol, J. Mercier, D. Rekosh, R. Smith, E. Barbarese, et al. 2001. RNA trafficking signals in human immunodeficiency virus type 1. Mol. Cell. Biol. 21: 2133-2143.
50. Valente, S. T., and S. P. Goff. 2006. Inhibition of HIV-1 gene expression by a fragment of hnRNP U. Mol. Cell. 23: 597-605.
51. Constantoulakis, P., M. Campbell, B. K. Felber, G. Nasioulas, E. Afonina, and G. N. Pavlakis. 1993. Inhibition of rev-mediated HIV-1 expression by an RNA binding protein encoded by the interferon-inducible 9-27 gene. Science 259: 1314-1318.
52. Timchenko, L. T., E. Salisbury, G. L. Wang, H. Nguyen, J. H. Albrecht, J. W. Hershey, and N. A. Timchenko. 2006. Age-specific CUGBP1-eIF2 complex increases translation of CCAAT/enhancer-binding protein β in old liver. J. Biol. Chem. 281: 32806-32819.
53. Roberts, R., N. A. Timchenko, J. W. Miller, S. Reddy, C. T. Caskey, M. S. Swanson, and L. T. Timchenko. 1997. Altered phosphorylation and intracellular distribution of a (CUG)n triplet repeat RNA-binding protein in patients with myotonic dystrophy and in myotonin protein kinase knockout mice. Proc. Natl. Acad. Sci. USA 94: 13221-13226.
54. Tanaka, N., Y. Hoshino, J. Gold, S. Hoshino, F. Martiniuk, T. Kurata, R. Pine, D. Levy, W. N. Rom, and M. Weiden. 2005. Interleukin-10 induces inhibitory C/EBPβ through STAT-3 and represses HIV-1 transcription in macrophages. Am. J. Respir. Cell Mol. Biol. 33: 406-411.
55. Natsuka, S., S. Akira, Y. Nishio, S. Hashimoto, T. Sugita, H. Isshiki, and T. Kishimoto. 1992. Macrophage differentiation-specific expression of NF-IL6, a transcription factor for interleukin-6. Blood 79: 460-466.
56. Kaisho, T., and S. Akira. 2006. Toll-like receptor function and signaling. J. Allergy Clin. Immunol. 117: 979-987; quiz 988.
57. Wedel, A., G. Sulski, and H. W. Ziegler-Heitbrock. 1996. CCAAT/enhancer binding protein is involved in the expression of the tumour necrosis factor gene in human monocytes. Cytokine 8: 335-341.
58. Pope, R. M., A. Leutz, and S. A. Ness. 1994. C/EBP β regulation of the tumor necrosis factor α gene. J. Clin. Invest. 94: 1449-1455.
59. Shirakawa, F., K. Saito, C. A. Bonagura, D. L. Galson, M. J. Fenton, A. C. Webb, and P. E. Auron. 1993. The human prointerleukin 1 β gene requires DNA sequences both proximal and distal to the transcription start site for tissue-specific induction. Mol. Cell. Biol. 13: 1332-1344.
60. Akira, S., H. Isshiki, T. Sugita, O. Tanabe, S. Kinoshita, Y. Nishio, T. Nakajima, T. Hirano, and T. Kishimoto. 1990. A nuclear factor for IL-6 expression (NF-IL6) is a member of a C/EBP family. EMBO J. 9: 1897-1906.
61. Orandle, M. S., A. G. MacLean, V. G. Sasseville, X. Alvarez, and A. A. Lackner. 2002. Enhanced expression of proinflammatory cytokines in the central nervous system is associated with neuroinvasion by simian immunodeficiency virus and the development of encephalitis. J. Virol. 76: 5797-5802.
62. Mankowski, J. L., S. E. Queen, J. E. Clements, and M. C. Zink. 2004. Cerebrospinal fluid markers that predict SIV CNS disease. J. Neuroimmunol. 157: 66 -70.