Cellular transcription factors induced in trigeminal ganglia during dexamethasone-induced reactivation from latency stimulate bovine herpesvirus 1 productive infection and certain viral promoters

Journal of Virology

Volumn 86, Issue 5, 2012, Pages 2459-2473

  Workman, Aspen ^a,b,c   Eudy, James ^d   Smith, Lynette ^d   da Silva, Leticia Frizzo ^a,b   Sinani, Devis ^a,b   Bricker, Halie ^e   Cook, Emily ^a   Doster, Alan ^b,c   Jones, Clinton ^a,b,c  

^a UNIVERSITY OF NEBRASKA   (United States)

^b UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^c Morrison Life Science Center   (United States)

^d UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^e NEBRASKA WESLEYAN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEXAMETHASONE; PENTRAXIN 3; PROMYELOCYTIC LEUKEMIA ZINC FINGER PROTEIN; PROTEIN C; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SLUG; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BOVINE HERPES VIRUS; CALF (BOVINE); CONTROLLED STUDY; GENE EXPRESSION; GENE INDUCTION; GENE LOCATION; HERPES VIRUS INFECTION; LATENT PERIOD; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; SENSORY NERVE CELL; TRIGEMINUS GANGLION; VIRUS REACTIVATION; VIRUS VIRULENCE;

ANIMALS; CATTLE; CATTLE DISEASES; CELL LINE; DEXAMETHASONE; GENE EXPRESSION REGULATION, VIRAL; HERPESVIRIDAE INFECTIONS; HERPESVIRUS 1, BOVINE; MICE; PROMOTER REGIONS, GENETIC; RABBITS; TRANSCRIPTION FACTORS; TRIGEMINAL GANGLION; UP-REGULATION; VIRUS ACTIVATION; VIRUS LATENCY;

ALPHAHERPESVIRINAE; ANIMALIA; BOVINAE; BOVINE HERPESVIRUS 1;

EID: 84863396946     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.06143-11     Document Type: Article

References (101)

1. Ackermann M, Peterhans E, Wyler R. 1982. DNA of bovine herpesvirus type 1 in the trigeminal ganglia of latently infected calves. Am. J. Vet. Res. 43:36-40.
2. Adam PJ, Reagan CP, Hautmann MB, Owens GK. 2000. Positive- and negative-acting Kruppel-like transcription factors bind a transforming growth factor beta control element required for expression of the smooth muscle cell differentiation marker SM22-alpha in vivo. J. Biol. Chem. 275:37798-37806.
3. Barnes PJ. 1998. Anti-inflammatory actions of glucocorticoids: molecular mechanisms. Clin. Sci. 94:557-572.
4. Bieker JJ. 2001. Kruppel-like factors: three fingers in many pies. J. Biol. Chem. 276:34355-34358.
5. Bozza S, et al. 2006. Pentraxin 3 protects from MCMV infection and reactivation through TLR sensing pathways leading to IRF3 activation. Blood 108:3387-3396.
6. Bratanich AC, Hanson ND, Jones CJ. 1992. The latency-related gene of bovine herpesvirus 1 inhibits the activity of immediate-early transcription unit 1. Virology 191:988-991.
7. Bray SJ. 2006. Notch signaling: a simple pathway becomes complex. Nat. Rev. Mol. Cell Biol. 7:678-689.
8. Brown GA, Field HJ. 1990. Experimental reactivation of bovine herpesvirus 1 (BHV-1) by means of corticosteroids in an intranasal rabbit model. Arch. Virol. 112:81-101.
9. Cantin EM, Hinton DR, Chen J, Openshaw H. 1995. Gamma interferon expression during acute and latent nervous system infection by herpes simplex virus type 1. J. Virol. 69:4898-4905.
10. Carballo E, WSL, Blackshear PJ. 1988. Feedback inhibition of macrophage tumor necrosis factor-alpha production by tristetraprolin. Science 281:1001-1005.
11. Ciacci-Zanella J, Stone M, Henderson G, Jones C. 1999. The latencyrelated gene of bovine herpesvirus 1 inhibits programmed cell death. J. Virol. 73:9734-9740.
12. Dang DT, Zhao W, Mahatan CS, Geiman DE, Yang VW. 2002. Opposing effects of Kruppel-like factor 4 (gut-enriched Kruppel-like factor) and Kruppel-like factor 5 (intestinal-enriched Kruppel-like factor) on the promoter of the Kruppel-like factor 4 gene. Nucleic Acids Res. 30:2736-2741.
13. de Hoon M, Imoto S, Miyano S. 2002. Cluster 3.0. University of Tokyo, Human Genome Center, Tokyo, Japan.
14. DuBois RN, Ryder MWMK, Lau LF, Nathans DD. 2000. A growth factor-inducible nuclear protein with a novel cysteine/histidine repetitive sequence. J. Biol. Chem. 265:19185-19191.
15. Ehebauer M, Penelope P, Arias AM. 2006. Notch, a universal arbiter of cell fate decisions. Science 314:1414-1415.
16. Eisen M. 2002. Gene cluster 3.0. Stanford University, Stanford, CA.
17. Fahenenstich J, et al. 2003. Promyelocytic leukaemia zinc finger protein (PLZF) is a glucocorticoid- and progesterone-induced transcription factor in human endometrial stromal cells and myometrial smooth muscle cells. Mol. Hum. Reprod. 9:611-623.
18. Feinberg MW, et al. 2005. Kruppel-like factor 4 is a mediator of proinflammatory signaling in macrophages. J. Biol. Chem. 280:38247-38268.
19. Fillipponi D, et al. 2007. Repression of kit expression by Plzf in germ cells. Mol. Cell Biol. 27:6770-6781.
20. Garlanda C, Bottazzi B, Bastone A, Mantovani A. 2005. Pentraxins at the crossroads between innate immunity, inflammation, matrix deposition, and female fertility. Annu. Rev. Immunol. 23:337-366.
21. Geiser V, Jones C. 2003. Stimulation of bovine herpesvirus 1 productive infection by the adenovirus E1A gene and a cell cycle regulatory gene, E2F-4. J. Gen. Virol. 84:929-938.
22. Geiser V, Inman M, Zhang Y, Jones C. 2002. The latency related (LR) gene of bovine herpesvirus 1 (BHV-1) can inhibit the ability of bICP0 to activate productive infection. J. Gen. Virol. 83:2965-2971.
23. Gutierrez-Hartmann A, Duval DL, Bradford AP. 2007. ETS transcription factors in endocrine systems. Trends Endocrinol. Metab. 18:150-158.
24. Hage JJ, et al. 1998. Reactivation of latent bovine herpesvirus 1 in cattle seronegative to glycoproteins gB and gE. Vet. Microbiol. 60:87-98.
25. Halford WP, Gebhardt BM, Carr DJ. 1996. Persistent cytokine expression in trigeminal ganglion latently infected with herpes simplex virus type 1. J. Immunol. 157:3542-3549.
26. Hayden MS, Ghosh S. 2008. Shared principles in NF-κB signaling. Cell 132:344-362.
27. Homan EJ, Easterday BC. 1983. Experimental latent and recrudescent bovine herpesvirus-1 infections in calves. Am. J. Vet. Res. 44:309-313.
28. Hunsperger EA, Wilcox CL. 2003. Caspase-3-dependent reactivation of latent herpes simplex virus type 1 in sensory neuronal cultures. J. Neurovirol. 9:390-398.
29. Inman M, Lovato L, Doster A, Jones C. 2002. A mutation in the latency-related gene of bovine herpesvirus 1 interferes with the latency reactivation cycle of latency in calves. J. Virol. 76:6771-6779.
30. Inman M, Lovato L, Doster A, Jones C. 2001. A mutation in the latency-related gene of bovine herpesvirus 1 leads to impaired ocular shedding in acutely infected calves. J. Virol. 75:8507-8515.
31. Irizarry RA, Gautier LBM, Cope L. 2002. An r package for analyses of Affymetrix oligonucleotide arrays, p 102-119. In Parmigiani ESGG, Irizarry RA, Zeger SL (ed), Analysis of gene expression of gene expression data: methods and software. Springer, New York, NY.
32. Jaber T, Workman A, Jones C. 2010. Small noncoding RNAs encoded within the bovine herpesvirus 1 latency-related gene can reduce steadystate levels of infected cell protein 0 (bICP0). J. Virol. 84:6297-6307.
33. Jones C. 1998. Alphaherpesvirus latency: its role in disease and survival of the virus in nature. Adv. Virus Res. 51:81-133.
34. Jones C. 2003. Herpes simplex virus type 1 and bovine herpesvirus 1 latency. Clin. Microbiol. Rev. 16:79-95.
35. Jones C. 2009. Regulation of innate immune responses by bovine herpesvirus 1 and infected cell protein 0. Viruses 1:255-275.
36. Jones C, Delhon G, Bratanich A, Kutish G, Rock D. 1990. Analysis of the transcriptional promoter which regulates the latency-related transcript of bovine herpesvirus 1. J. Virol. 64:1164-1170.
37. Jones C, et al. 2000. Analysis of latency in cattle after inoculation with a temperature sensitive mutant of bovine herpesvirus 1 (RLB106). Vaccine 18:3185-3195.
38. Jones C, et al. 2006. Functional analysis of bovine herpesvirus 1 (BHV-1) genes expressed during latency. Vet. Microbiol. 113:199-210.
39. Jones C, Chowdhury S. 2007. A review of the biology of bovine herpesvirus type 1 (BHV-1), its role as a cofactor in the bovine respiratory disease complex, and development of improved vaccines. Adv. Anim. Health 8:187-205.
40. Kaashoek MJ, Rijsewijk FA, Oirschot JT. 1996. Persistence of antibodies against bovine herpesvirus 1 and virus reactivation two to three years after infection. Vet. Microbiol. 53:103-110.
41. + T cells are selectively activated and retained in latently infected sensory ganglia. Immunity 18:593-603.
42. + T cell inhibition of HSV-1 reactivation from neuronal latency. Science 322:268-272.
43. KosZ-Vnenchak JJ, Coen DM, Knipe DM. 1993. Evidence for a novel regulatory pathway for herpes simplex virus gene expression in trigeminal ganglion neurons. J. Virol. 67:5383-5393.
44. Lee K, Gjorevski N, Boghaert E, Radisky DC, Nelson CM. 2011. Snail1, Snail2, and E46 promote mammary epithelial branching morphogenesis. EMBO J. 30:2662-2674.
45. Leroy P, Mostov KE. 2007. Slug is required for cell survival during partial epithelial-mesenchymal transition of HGF-induced tubulogenesis. Mol. Biol. Cell 18:1943-1952.
46. Liu T, Khanna KM, Carriere BN, Hendricks RL. 2001. Gamma interferon can prevent herpes simplex virus type 1 reactivation from latency in sensory neurons. J. Virol. 75:11178-11184.
47. + T cells can block herpes simplex virus type 1 (HSV-1) reactivation from latency in sensory neurons. J. Exp. Med. 191:1459-1466.
48. Liu T, Tang Q, Hendricks RL. 1996. Inflammatory infiltration of the trigeminal ganglion after herpes simplex virus type 1 corneal infection. J. Virol. 70:264-271.
49. Liu Y, et al. 2006. Induction of KLF4 in response to heat stress. Cell Stress Chaperones 11:379-389.
50. Lovato L, Inman M, Henderson G, Doster A, Jones C. 2003. Infection of cattle with a bovine herpesvirus 1 (BHV-1) strain that contains a mutation in the latency related gene leads to increased apoptosis in tri- geminal ganglia during the transition from acute infection to latency. J. Virol. 77:4848-4857.
51. Martin JP, Delmotte M-H, Formstecher P, Lefebvre P. 2003. PLZF is a negative regulator of retinoic acid receptor transcriptional activity. Nuclear Recept. 1:1-11.
52. Masuno K, et al. 2011. Expression profiling identifies Klf15 as a glucocorticoid target that regulates airway hyperresponsiveness. Am. J. Respir. Cell Mol. Biol. 45:642-649.
53. McConnell MJ, et al. 2003. Growth suppression by acute promyelocytic leukemia-associated protein PLZF is mediated by repression of c-myc expression. Mol. Cell Biol. 23:9375-9388.
54. Meyer F, et al. 2007. Identification of a novel protein encoded by the latency-related gene of bovine herpesvirus 1. J. Neurovirol. 13:569-578.
55. Meyer F, et al. 2007. A protein encoded by the bovine herpesvirus 1 (BHV-1) latency related gene interacts with specific cellular regulatory proteins, including the CCAAT enhancer binding protein alpha (C/EBP-α). J. Virol. 81:59-67.
56. Misra V, Bratanich AC, Carpenter D, O'Hare P. 1994. Protein and DNA elements involved in transactivation of the promoter of the bovine herpesvirus (BHV) 1 IE-1 transcription unit by the BHV alpha gene trans-inducing factor. J. Virol. 68:4898-4909.
57. Nakatake Y, et al. 2006. Klf4 cooperates with Oct3/4 and Sox2 to activate the Lefty1 core promoter in embryonic stem cells. Mol. Cell Biol. 26:7772-7782.
58. Nichol PF, Chang JY, Johnson EM Jr, Olivo PD. 1996. Herpes simplex virus gene expression in neurons: viral DNA synthesis is a critical regulatory event in the branch point between lytic and latent pathways. J. Virol. 5476-5486.
59. Otteson DC, Lai H, Liu Y, Zack DJ. 2005. Zinc-finger domains of the transcriptional repressor KLF15 binds multiple sites in rhodopsin and IRBP promoters including the CRS-1 and G-rich elements. BMC Mol. Biol. 6:15.
60. Perez S, et al. 2007. A protein encoded by the bovine herpesvirus 1 ORF E gene induces neurite-like morphological changes in mouse neuroblastoma cells and is expressed in trigeminal ganglionic neurons. J. Neurovirol. 13:139-149.
61. Perez S, Meyer F, Saira K, Doster A, Jones C. 2008. Premature expression of the latency-related RNA encoded by bovine herpesvirus 1 correlates with higher levels of beta interferon RNA expression in productively infected cells. J. Gen. Virol. 89:1338-1345.
62. Perez S, Lovato L, Zhou J, Doster A, Jones C. 2006. Comparison of inflammatory infiltrates in trigeminal ganglia of cattle infected with wild type BHV-1 versus a virus strain containing a mutation in the LR (latency-related) gene. J. Neurovirol. 12:392-397.
63. Perez S, Inman M, Doster A, Jones C. 2005. Latency-related gene encoded by bovine herpesvirus 1 promotes virus growth and reactivation from latency in tonsils of infected calves. J. Clin. Microbiol. 43:393-401.
64. Perng G-C, Jones C. 2010. Towards an understanding of the herpes simplex virus type 1 latency reactivation cycle. Interdisc. Persp. Infect. Dis. 2010:1-18.
65. Pesola JM, Zhu J, Knipe DM, Coen DM. 2005. Herpes simplex virus 1 immediate-early and early gene expression during reactivation from latency under conditions that prevent infectious virus production. J. Virol. 79:14516-14525.
66. + T cells in controlling HSV-1 latency ex vivo. Immunity 23:515-523.
67. Rhen T, Cidlowski JA. 2005. Anti-inflammatory action of glucocorticoids: new mechanisms of old drugs. N. Engl. J. Med. 353:1711-1723.
68. Rock D, Lokensgard J, Lewis T, Kutish G. 1992. Characterization of dexamethasone-induced reactivation of latent bovine herpesvirus 1. J. Virol. 66:2484-2490.
69. Rodrigues R, Cuddington B, Mossman K. 2010. Bovine herpesvirus type 1 as a novel oncolytic virus. Cancer Gene Ther. 17:344-345.
70. Roizman B, Sears AE. 1996. Herpes simplex viruses and their replication, p 2231-2295. In Fields BE, et al. (ed), Fields virology, 3rd ed. Lippincott-Raven Publishers, New York, NY.
71. Sanalkumar R, Dhanesh SB, James J. 2010. Non-canonical activation of Notch signaling/target genes in vertebrates. Cell. Mol. Life Sci. 67:2957-2968.
72. Sawtell NM, Thompson RL. 1992. Rapid in vivo reactivation of herpes simplex virus in latently infected murine ganglionic neurons after transient hyperthermia. J. Virol. 66:2150-2156.
73. Schang L, Jones C. 1997. Analysis of bovine herpesvirus 1 transcripts during a primary infection of trigeminal ganglia of cattle. J. Virol. 71:6786-6795.
74. Sharrocks AD. 2001. The ETS-domain transcription factor family. Nat. Rev. Mol. Cell. Biol. 2:827-837.
75. Sheffy BE, Davies DH. 1972. Reactivation of a bovine herpesvirus after corticosteroid treatment. Proc. Soc. Exp. Biol. Med. 140:974-976.
76. Shen W, Jones C. 2008. Open reading frame 2 encoded by the latency related gene of bovine herpesvirus 1 has anti-apoptosis activity in transiently transfected neuroblastoma cells. J. Virol. 82:10940-10945.
77. Shimeld C, et al. 1995. Immune cell infiltration and persistence in the mouse trigeminal ganglion after infection of the cornea with herpes simplex virus type 1. J. Neuroimmunol. 61:7-16.
78. Shimeld C, Whiteland JL, Williams NA, Easty DL, Hill TJ. 1997. Cytokine production in the nervous system of mice during acute and latent infection with herpes simplex virus type 1. J. Gen. Virol. 78:3317-3325.
79. Shimeld C, Whiteland JL, Williams NA, Easty DL, Hill TJ. 1996. Reactivation of herpes simplex virus type 1 in the mouse trigeminal ganglion: an in vivo study of virus antigen and immune cell infiltration. J. Gen. Virol. 77:2583-2590.
80. Shimizu N, et al. 2011. Crosstalk between glucocorticoid receptor and nutritional sensor mTOR in skeletal muscle. Cell Metab. 13:170-182.
81. Tal-Singer R, et al. 1997. Gene expression during reactivation of herpes simplex virus type 1 from latency in the peripheral nervous system is different from that during lytic infection of tissue cultures. J. Virol. 71:5268-5276.
82. Theil D, et al. 2003. Latent herpesvirus infection in human trigeminal ganglia causes chronic immune response. Am. J. Pathol. 163:2179-2184.
83. Thompson RL, Preston CM, Sawtell NM. 2009. De novo synthesis of VP16 coordinates the exit form HSV latency in vivo. PLoS Pathog. 5:1-12.
84. Tikoo SK, Campos M, Babiuk LA. 1995. Bovine herpesvirus 1 (BHV-1): biology, pathogenesis, and control. Adv. Virus Res. 45:191-223.
85. Tsavachidou D, Podrzucki W, Seykora J, Berger SL. 2001. Gene array analysis reveals changes in peripheral nervous system gene expression following stimuli that result in reactivation of latent herpes simplex virus type 1: induction of transcription factor Bcl-3. J. Virol. 75:9909-9917.
86. Turin L, Russo S, Poli G. 1999. BHV-1: new molecular approaches to control a common and widespread infection. Mol. Med. 5:261-284.
87. Winkler MT, Doster A, Sur JH, Jones C. 2002. Analysis of bovine trigeminal ganglia following infection with bovine herpesvirus 1. Vet. Microbiol. 86:139-155.
88. Winkler MT, Schang LS, Doster A, Holt T, Jones C. 2000. Analysis of cyclins in trigeminal ganglia of calves infected with bovine herpesvirus 1. J. Gen. Virol. 81:2993-2998.
89. Winkler MTC, Doster A, Jones C. 2000. Persistence and reactivation of bovine herpesvirus 1 in the tonsil of latently infected calves. J. Virol. 74:5337-5346.
90. Wirth UV, et al. 1992. Immediate-early RNA 2.9 and early RNA 2.6 of bovine herpesvirus 1 are 3' coterminal and encode a putative zinc finger transactivator protein. J. Virol. 66:2763-2772.
91. Wirth UV, Gunkel K, Engels M, Schwyzer M. 1989. Spatial and temporal distribution of bovine herpesvirus 1 transcripts. J. Virol. 63:4882-4889.
92. Wirth UV, Vogt B, Schwyzer M. 1991. The three major immediate-early transcripts of bovine herpesvirus 1 arise from two divergent and spliced transcription units. J. Virol. 65:195-205.
93. Workman A, Sinani D, Pittayakhajonwut D, Jones C. 2011. A protein (ORF2) encoded by the latency-related gene of bovine herpesvirus 1 interacts with Notch1 and Notch3. J. Virol. 85:2536-2546.
94. Workman A, Perez S, Doster A, Jones C. 2009. Dexamethasone treatment of calves latently infected with bovine herpesvirus 1 (BHV-1) leads to activation of the bICP0 early promoter, in part by the cellular transcription factor C/EBP-alpha. J. Virol. 83:8800-8809.
95. Workman A, Jones C. 2010. Bovine herpesvirus 1 productive infection and bICP0 early promoter activity are stimulated by E2F1. J. Virol. 84:6308-6317.
96. Xu D, et al. 2009. Promyelocytic Leukemia zinc finger protein regulates interferon-mediated innate immunity. Immunity 30:802-816.
97. Yamamoto J, et al. 2004. A Kruppel-like factor KLF15 contributes fasting-induced transcriptional activation of mitochondrial acetyl-CoA synthase gene AceCS2. J. Biol. Chem. 279:16954-16962.
98. Yang L, Voytek CC, Margolis TP. 2000. Immunohistochemical analysis of primary sensory neurons latently infected with herpes simplex virus type 1. J. Virol. 74:209-217.
99. Yin F, Herring BP. 2005. GATA-6 can act as a positive or negative regulator of smooth muscle-specific gene expression. J. Biol. Chem. 280:4745-4752.
100. Li Z, et al. 2010. KLF4 promotes hydrogen-peroxide-induced apoptosis of chronic myeloid leukemia cells involving the bcl-2/bax pathway. Cell Stress and Chaperones 15:905-912.
101. Zhang Y, Jiang Y, Zhou J, Jones C. 2006. The bovine herpesvirus 1 (BHV-1) immediate-early protein (bICP0) interacts with the histone acetyltransferase p300, and these interactions correlate with stimulation of gC promoter activity. J. Gen. Virol. 87:1843-1851.