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2,3,7,8-Tetrachlorodibenzo-p-dioxin regulates Bovine Herpesvirus type 1 induced apoptosis by modulating Bcl-2 family members

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Abstract

Exposure to environmental contaminants, like 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD), leads to an increased susceptibility to infectious agents. Infection of bovine cells (MDBK) with Bovine Herpesvirus 1 (BHV-1) anticipates virus-induced apoptosis, suggesting an involvement of TCDD in virus infection. Herein we analyzed the effects of TCDD on apoptotic pathway in MDBK cells infected with BHV-1. After 12 h of infection, TCDD induced a significant increase in apoptotic cells. TCDD caused a dose-dependent up-regulation and anticipated activation of caspases 3, 8 and 9, with respect to unexposed groups. TCDD anticipated cleavage of PARP, compared to controls. Furthermore TCDD increased Bax and Bid levels, and decreased Bcl-2 and Bcl-XL levels. Such events took place earlier in exposed than unexposed cells. These results showed that TCDD influences BHV-1 induced apoptosis through members of Bcl-2 family and up-regulating activation of caspases.

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Abbreviations

TCDD:

2,3,7,8-Tetrachlorodibenzo-p-dioxin

BHV-1:

Bovine Herpesvirus 1

MDBK:

Madin-Darby bovine kidney cells

PARP:

Poly-(ADP-ribose) polymerase

References

  1. Kerkvliet NI (1995) Immunological effects of chlorinated dibenzo-p-dioxins. Environ Health Perspect 103:47–53. doi:10.2307/3432722

    Article  PubMed  CAS  Google Scholar 

  2. Mandal PK (2005) Dioxin: a review of its environmental effects and its aryl hydrocarbon receptor biology. J Comp Physiol [B] 175:221–230. doi:10.1007/s00360-005-0483-3

    CAS  Google Scholar 

  3. Burleson GR, Lebrec H, Yang YG, Ibanes JD, Pennington KN, Birnbaum LS (1996) Effect of 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin (TCDD) on influenza virus host resistance in mice. Fundam Appl Toxicol 29:40–47. doi:10.1006/faat.1996.0004

    Article  PubMed  CAS  Google Scholar 

  4. Gollapudi S, Kim CH, Patel A, Sindhu R, Gupta S (1996) Dioxin activates human immunodeficiency virus-1 expression in chronically infected promonocytic U1 cells by enhancing NF-kappa B activity and production of tumor necrosis factor-alpha. Biochem Biophys Res Commun 226:889–894. doi:10.1006/bbrc.1996.1445

    Article  PubMed  CAS  Google Scholar 

  5. Murayama T, Inoue M, Nomura T, Mori S, Eizuru Y (2002) 2,3,7,8-Tetrachlorodibenzo-p-dioxin is a possible activator of human cytomegalovirus replication in a human fibroblast cell line. Biochem Biophys Res Commun 296:651–656. doi:10.1016/S0006-291X(02)00921-X

    Article  PubMed  CAS  Google Scholar 

  6. Ohata H, Tetsuka T, Hayashi H, Onozaki K, Okamoto T (2003) 3-Methylcholanthrene activates human immunodeficiency virus type 1 replication via aryl hydrocarbon receptor. Microbiol Immunol 47:363–370

    PubMed  CAS  Google Scholar 

  7. Fiorito F, Pagnini U, De Martino L, Montagnaro S, Ciarcia R, Florio S et al (2008) 2,3,7,8-Tetrachlorodibenzo-p-dioxin increases Bovine Herpesvirus type-1 (BHV-1) replication in Madin-Darby bovine kidney (MDBK) cells in vitro. J Cell Biochem 103:221–233. doi:10.1002/jcb.21398

    Article  PubMed  CAS  Google Scholar 

  8. Diletti G, Torreti L, De Massis MR, Migliorati G, Scortichini G (2003) A case of milk contamination by PCDD/Fs in Italy: analytical levels and contamination source identification. Organohalogen Compd 64:1–4

    CAS  Google Scholar 

  9. Santelli F, Boscaino F, Cautela D, Castaldo D, Malorni A (2006) Determination of polychlorinated dibenzo-p-dioxins (PCDDs), polychlorinated dibenzo-p-furans (PCDFs) and polychlorinated biphenyls (PCBs) in buffalo milk and mozzarella cheese. Eur Food Res Technol 223:51–56. doi:10.1007/s00217-005-0112-0

    Article  CAS  Google Scholar 

  10. 2004/558/EC. Official Journal of the European Union L 249 volume 47, 23 July 2004. Commission Decision of 15 July 2004 implementing Council Directive 64/432/EEC as regards additional guarantees for intra-Community trade in bovine animals relating to infectious bovine rhinotracheitis and the approval of the eradication programmes presented by certain Member States

  11. Ackermann M, Engels M (2006) Pro and contra IBR-eradication. Vet Microbiol 113:293–302. doi:10.1016/j.vetmic.2005.11.043

    Article  PubMed  Google Scholar 

  12. Tikoo SK, Campos M, Babiuk LA (1995) Bovine Herpesvirus 1 (BHV-1): biology, pathogenesis, and control. Adv Virus Res 45:191–223. doi:10.1016/S0065-3527(08)60061-5

    Article  PubMed  CAS  Google Scholar 

  13. Jones C (2003) Herpes simplex virus type-1 and Bovine Herpesvirus-1 latency. Clin Microbiol Rev 16:79–95. doi:10.1128/CMR.16.1.79-95.2003

    Article  PubMed  CAS  Google Scholar 

  14. Griebel PJ, Qualtiere L, Davis WC, Lawman MJ, Babiuk LA (1987) Bovine peripheral blood leukocyte subpopulation dynamics following a primary Bovine Herpesvirus-1 infection. Viral Immunol 1:267–286

    Article  PubMed  Google Scholar 

  15. Carter JJ, Weinberg AD, Pollard A, Reeves R, Magnuson JA, Magnuson NS (1989) Inhibition of T-lymphocyte mitogenic responses and effects on cell functions by Bovine Herpesvirus 1. J Virol 63:1525–1530

    PubMed  CAS  Google Scholar 

  16. 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

    PubMed  CAS  Google Scholar 

  17. Huang P, Tofighi R, Emgard M, Ceccatelli S (2005) Cell death induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin (2,3,7,8-TCDD) in AtT-20 pituitary cells. Toxicology 207:391–399. doi:10.1016/j.tox.2004.10.013

    Article  PubMed  CAS  Google Scholar 

  18. Schwarz M, Buchmann A, Stinchcombe S, Kalkuhl A, Bock K (2000) Ah receptor ligands and tumor promotion: survival of neoplastic cells. Toxicol Lett 112–113:69–77. doi:10.1016/S0378-4274(99)00247-7

    Article  PubMed  Google Scholar 

  19. Hossain A, Tsuchiya S, Minegishi M, Osada M, Ikawa S, Tezuka FA et al (1998) The Ah receptor is not involved in 2,3,7,8-tetrachlorodibenzo-p-dioxin-mediated apoptosis in human leukemic T cell lines. J Biol Chem 273:19853–19858. doi:10.1074/jbc.273.31.19853

    Article  PubMed  CAS  Google Scholar 

  20. Everett H, McFadden G (1999) Apoptosis: an innate immune response to virus infection. Trends Microbiol 7:160–165. doi:10.1016/S0966-842X(99)01487-0

    Article  PubMed  CAS  Google Scholar 

  21. Devireddy LR, Jones CJ (1999) Activation of caspases and p53 by Bovine Herpesvirus 1 infection results in programmed cell death and efficient virus release. J Virol 73:3778–3788

    PubMed  CAS  Google Scholar 

  22. Lovato L, Inman M, Henderson G, Doster A, Jones C (2003) Infection of cattle with a Bovine Herpesvirus 1 strain that contains a mutation in the latency-related gene leads to increased apoptosis in trigeminal ganglia during the transition from acute infection to latency. J Virol 77:4848–4857. doi:10.1128/JVI.77.8.4848-4857.2003

    Article  PubMed  CAS  Google Scholar 

  23. Henderson G, Perng GC, Nesburn AB, Wechsler SL, Jones C (2004) The latency-related gene encoded by Bovine Herpesvirus 1 can suppress caspase 3 and caspase 9 cleavage during productive infection. J Neurovirol 10:64–70. doi:10.1080/13550280490261716

    Article  PubMed  CAS  Google Scholar 

  24. Henderson G, Zhang Y, Inman M, Jones D, Jones C (2004) Infected cell protein 0 encoded by Bovine Herpesvirus 1 can activate caspase 3 when overexpressed in transfected cells. J Gen Virol 85:3511–3516. doi:10.1099/vir.0.80371-0

    Article  PubMed  CAS  Google Scholar 

  25. Geiser V, Rose S, Jones C (2008) Bovine Herpesvirus type 1 induces cell death by a cell-type-dependent fashion. Microb Pathog 44:459–466. doi:10.1016/j.micpath.2007.10.014

    Article  PubMed  CAS  Google Scholar 

  26. De Martino L, Marfé G, Di Stefano C, Pagnini U, Florio S, Crispino L et al (2003) Interference of Bovine Herpesvirus 1 (BHV-1) in sorbitol-induced apoptosis. J Cell Biochem 89:373–380. doi:10.1002/jcb.10518

    Article  PubMed  CAS  Google Scholar 

  27. Winkler MT, Doster A, Jones C (1999) Bovine Herpesvirus 1 can infect CD4(+) T lymphocytes and induce programmed cell death during acute infection of cattle. J Virol 73:8657–8668

    PubMed  CAS  Google Scholar 

  28. Fiorito F, Granato GE, De Blasio E, Longo M, Marfè G, Florio S, et al (2008) 2,3,7,8-Tetrachlorodibenzo-p-dioxin anticipates Bovine Herpesvirus type 1 induced apoptosis. Ann NY Acad Sci (submitted)

  29. Ahn NS, Hu H, Park JS, Park JS, Kim JS, An S et al (2005) Molecular mechanisms of the 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced inverted U-shaped dose responsiveness in anchorage independent growth and cell proliferation of human breast epithelial cells with stem cell characteristics. Mutat Res 579:189–199. doi:10.1016/j.mrfmmm.2005.03.026

    PubMed  CAS  Google Scholar 

  30. Elmore S (2007) Apoptosis: a review of programmed cell death. Toxicol Pathol 35:495–516. doi:10.1080/01926230701320337

    Article  PubMed  CAS  Google Scholar 

  31. Cory S, Adams JM (2002) The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer 2:647–656. doi:10.1038/nrc883

    Article  PubMed  CAS  Google Scholar 

  32. Sperandio S, de Belle I, Bredesen DE (2000) An alternative, nonapoptotic form of programmed cell death. Proc Natl Acad Sci USA 97:14376–14381. doi:10.1073/pnas.97.26.14376

    Article  PubMed  CAS  Google Scholar 

  33. Wesselborg S, Janssen O, Kabelitz D (1993) Induction of activation-driven death (apoptosis) in activated but not resting peripheral blood T cells. J Immunol 150:4338–4345

    PubMed  CAS  Google Scholar 

  34. Ciacci-Zanella J, Stone M, Henderson G, Jones C (1999) The latency-related gene of Bovine Herpesvirus 1 inhibits programmed cell death. J Virol 73:9734–9740

    PubMed  CAS  Google Scholar 

  35. Meyer F, Perez S, Geiser V, Sintek M, Inman M, Jones C (2007) A protein encoded by the Bovine Herpesvirus 1 latency-related gene interacts with specific cellular regulatory proteins, including CCAAT enhancer binding protein alpha. J Virol 81:59–67. doi:10.1128/JVI.01171-06

    Article  PubMed  CAS  Google Scholar 

  36. Marfè G, De Martino L, Filomeni G, Di Stefano C, Giganti MG, Pagnini U et al (2006) Degenerate PCR method for identification of an antiapoptotic gene in BHV-1. J Cell Biochem 97:813–823. doi:10.1002/jcb.20636

    Article  PubMed  CAS  Google Scholar 

  37. De Martino L, Marfe G, Consalvo MI, Di Stefano C, Pagnini U, Sinibaldi-Salimei P (2007) Antiapoptotic activity of Bovine Herpesvirus type-1 (BHV-1) UL14 protein. Vet Microbiol 123:210–216. doi:10.1016/j.vetmic.2007.02.026

    Article  PubMed  CAS  Google Scholar 

  38. Jones C, Geiser V, Henderson G, Jiang Y, Meyer F, Perez S et al (2006) Functional analysis of Bovine Herpesvirus 1 (BHV-1) genes expressed during latency. Vet Microbiol 113:199–210. doi:10.1016/j.vetmic.2005.11.009

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by grants by Regione Campania for the project entitled: “Contaminanti organici persistenti nell’ambiente: Studio di coorte sullo stato sanitario e sui livelli di accumulo nel latte materno in gruppi di popolazione a differente rischio di esposizione nella Regione Campania”.

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Correspondence to Filomena Fiorito.

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Fiorito, F., Marfè, G., De Blasio, E. et al. 2,3,7,8-Tetrachlorodibenzo-p-dioxin regulates Bovine Herpesvirus type 1 induced apoptosis by modulating Bcl-2 family members. Apoptosis 13, 1243–1252 (2008). https://doi.org/10.1007/s10495-008-0249-y

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  • DOI: https://doi.org/10.1007/s10495-008-0249-y

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