1887

Abstract

The is a diverse and growing family of viruses that already includes more than 25 distinct species. While some of these viruses have a significant impact on public health, others appear to be non-pathogenic. At present little is known about the host cell responses to infection with different arenaviruses, particularly those found in the New World; however, apoptosis is known to play an important role in controlling infection of many viruses. Here we show that infection with Tacaribe virus (TCRV), which is widely considered the prototype for non-pathogenic arenaviruses, leads to stronger induction of apoptosis than does infection with its human-pathogenic relative Junín virus. TCRV-induced apoptosis occurred in several cell types during late stages of infection and was shown to be caspase-dependent, involving the activation of caspases 3, 7, 8 and 9. Further, UV-inactivated TCRV did not induce apoptosis, indicating that the activation of this process is dependent on active viral replication/transcription. Interestingly, when apoptosis was inhibited, growth of TCRV was not enhanced, indicating that apoptosis does not have a direct negative effect on TCRV infection . Taken together, our data identify and characterize an important virus–host cell interaction of the prototypic, non-pathogenic arenavirus TCRV, which provides important insight into the growing field of arenavirus research aimed at better understanding the diversity in responses to different arenavirus infections and their functional consequences.

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2016-04-01
2024-03-28
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References

  1. Abraham J., Kwong J. A., Albariño C. G., Lu J. G., Radoshitzky S. R., Salazar-Bravo J., Farzan M., Spiropoulou C. F., Choe H. 2009; Host-species transferrin receptor 1 orthologs are cellular receptors for nonpathogenic New World clade B arenaviruses. PLoS Pathog 5:e1000358 [View Article][PubMed]
    [Google Scholar]
  2. Acrani G. O., Gomes R., Proença-Módena J. L., da Silva A. F., Carminati P. O., Silva M. L., Santos R. I. M., Arruda E. 2010; Apoptosis induced by Oropouche virus infection in HeLa cells is dependent on virus protein expression. Virus Res 149:56–63 [View Article][PubMed]
    [Google Scholar]
  3. Amara A., Mercer J. 2015; Viral apoptotic mimicry. Nat Rev Microbiol 13:461–469 [View Article][PubMed]
    [Google Scholar]
  4. Ashkenazi A., Dixit V. M. 1998; Death receptors: signaling and modulation. Science 281:1305–1308 [View Article][PubMed]
    [Google Scholar]
  5. Balachandran S., Kim C. N., Yeh W. C., Mak T. W., Bhalla K., Barber G. N. 1998; Activation of the dsRNA-dependent protein kinase (PKR), induces apoptosis through FADD-mediated death signaling. EMBO J 17:6888–6902 [View Article][PubMed]
    [Google Scholar]
  6. Banos-Lara M. R., Méndez E. 2010; Role of individual caspases induced by astrovirus on the processing of its structural protein and its release from the cell through a non-lytic mechanism. Virology 401:322–332 [View Article][PubMed]
    [Google Scholar]
  7. Best S. M., Shelton J. F., Pompey J. M., Wolfinbarger J. B., Bloom M. E. 2003; Caspase cleavage of the nonstructural protein NS1 mediates replication of Aleutian mink disease parvovirus. J Virol 77:5305–5312 [View Article][PubMed]
    [Google Scholar]
  8. Bitzer M., Prinz F., Bauer M., Spiegel M., Neubert W. J., Gregor M., Schulze-Osthoff K., Lauer U. 1999; Sendai virus infection induces apoptosis through activation of caspase-8 (FLICE) and caspase-3 (CPP32). J Virol 73:702–708[PubMed]
    [Google Scholar]
  9. Bitzer M., Armeanu S., Prinz F., Ungerechts G., Wybranietz W., Spiegel M., Bernlöhr C., Cecconi F., Gregor M., other authors. 2002; Caspase-8 and Apaf-1-independent caspase-9 activation in Sendai virus-infected cells. J Biol Chem 277:29817–29824 [View Article][PubMed]
    [Google Scholar]
  10. Borner C., Monney L. 1999; Apoptosis without caspases: an inefficient molecular guillotine?. Cell Death Differ 6:497–507 [View Article][PubMed]
    [Google Scholar]
  11. Briese T., Paweska J. T., McMullan L. K., Hutchison S. K., Street C., Palacios G., Khristova M. L., Weyer J., Swanepoel R., other authors. 2009; Genetic detection and characterization of Lujo virus, a new hemorrhagic fever-associated arenavirus from southern Africa. PLoS Pathog 5:e1000455 [View Article][PubMed]
    [Google Scholar]
  12. Candé C., Cecconi F., Dessen P., Kroemer G. 2002; Apoptosis-inducing factor (AIF): key to the conserved caspase-independent pathways of cell death?. J Cell Sci 115:4727–4734 [View Article][PubMed]
    [Google Scholar]
  13. Carballal G., Calello M. A., Laguens R. P., Weissenbacher M. C. 1987; Tacaribe virus: a new alternative for Argentine hemorrhagic fever vaccine. J Med Virol 23:257–263 [View Article][PubMed]
    [Google Scholar]
  14. Carter M. F., Murphy F. A., Brunschwig J. P., Noonan C., Rawls W. E. 1973; Effects of actinomycin D and ultraviolet and ionizing radiation on Pichinde virus. J Virol 12:33–38[PubMed]
    [Google Scholar]
  15. Chattopadhyay S., Marques J. T., Yamashita M., Peters K. L., Smith K., Desai A., Williams B. R., Sen G. C. 2010; Viral apoptosis is induced by IRF-3-mediated activation of Bax. EMBO J 29:1762–1773 [View Article][PubMed]
    [Google Scholar]
  16. Chattopadhyay S., Yamashita M., Zhang Y., Sen G. C. 2011; The IRF-3/Bax-mediated apoptotic pathway, activated by viral cytoplasmic RNA and DNA, inhibits virus replication. J Virol 85:3708–3716 [View Article][PubMed]
    [Google Scholar]
  17. Daugas E., Nochy D., Ravagnan L., Loeffler M., Susin S. A., Zamzami N., Kroemer G. 2000; Apoptosis-inducing factor (AIF): a ubiquitous mitochondrial oxidoreductase involved in apoptosis. FEBS Lett 476:118–123 [View Article][PubMed]
    [Google Scholar]
  18. Desmyter J., Melnick J. L., Rawls W. E. 1968; Defectiveness of interferon production and of rubella virus interference in a line of African green monkey kidney cells (Vero). J Virol 2:955–961[PubMed]
    [Google Scholar]
  19. Downs W. G., Anderson C. R., Spence L., Aitken T. H., Greenhall A. H. 1963; Tacaribe virus, a new agent isolated from Artibeus bats and mosquitoes in Trinidad, West Indies. Am J Trop Med Hyg 12:640–646[PubMed]
    [Google Scholar]
  20. Eleouet J. F., Chilmonczyk S., Besnardeau L., Laude H. 1998; Transmissible gastroenteritis coronavirus induces programmed cell death in infected cells through a caspase-dependent pathway. J Virol 72:4918–4924[PubMed]
    [Google Scholar]
  21. Elliott L. H., McCormick J. B., Johnson K. M. 1982; Inactivation of Lassa, Marburg, and Ebola viruses by gamma irradiation. J Clin Microbiol 16:704–708[PubMed]
    [Google Scholar]
  22. Fischer U., Jänicke R. U., Schulze-Osthoff K. 2003; Many cuts to ruin: a comprehensive update of caspase substrates. Cell Death Differ 10:76–100 [View Article][PubMed]
    [Google Scholar]
  23. Gadaleta P., Vacotto M., Coulombié F. 2002; Vesicular stomatitis virus induces apoptosis at early stages in the viral cycle and does not depend on virus replication. Virus Res 86:87–92 [View Article][PubMed]
    [Google Scholar]
  24. Gil J., Esteban M. 2000; The interferon-induced protein kinase (PKR), triggers apoptosis through FADD-mediated activation of caspase 8 in a manner independent of Fas and TNF-α receptors. Oncogene 19:3665–3674 [View Article][PubMed]
    [Google Scholar]
  25. Gliedman J. B., Smith J. F., Brown D. T. 1975; Morphogenesis of Sindbis virus in cultured Aedes albopictus cells. J Virol 16:913–926[PubMed]
    [Google Scholar]
  26. Granville D. J., Gottlieb R. A. 2002; Mitochondria: regulators of cell death and survival. Scientific World J 2:1569–1578 [View Article][PubMed]
    [Google Scholar]
  27. Green D., Kroemer G. 1998; The central executioners of apoptosis: caspases or mitochondria?. Trends Cell Biol 8:267–271 [View Article][PubMed]
    [Google Scholar]
  28. Groseth A., Wolff S., Strecker T., Hoenen T., Becker S. 2010; Efficient budding of the Tacaribe virus matrix protein Z requires the nucleoprotein. J Virol 84:3603–3611 [View Article][PubMed]
    [Google Scholar]
  29. Groseth A., Hoenen T., Weber M., Wolff S., Herwig A., Kaufmann A., Becker S. 2011; Tacaribe virus but not Junin virus infection induces cytokine release from primary human monocytes and macrophages. PLoS Negl Trop Dis 5:e1137 [View Article][PubMed]
    [Google Scholar]
  30. Hay S., Kannourakis G. 2002; A time to kill: viral manipulation of the cell death program. J Gen Virol 83:1547–1564 [View Article][PubMed]
    [Google Scholar]
  31. Ho P. K., Hawkins C. J. 2005; Mammalian initiator apoptotic caspases. FEBS J 272:5436–5453 [View Article][PubMed]
    [Google Scholar]
  32. Iordanov M. S., Kirsch J. D., Ryabinina O. P., Wong J., Spitz P. N., Korcheva V. B., Thorburn A., Magun B. E. 2005; Recruitment of TRADD, FADD, and caspase 8 to double-stranded RNA-triggered death inducing signaling complexes (dsRNA-DISCs). Apoptosis 10:167–176 [CrossRef]
    [Google Scholar]
  33. Ivana Scovassi A., Diederich M. 2004; Modulation of poly(ADP-ribosylation) in apoptotic cells. Biochem Pharmacol 68:1041–1047 [View Article][PubMed]
    [Google Scholar]
  34. Jeurissen S. H., Wagenaar F., Pol J. M., van der Eb A. J., Noteborn M. H. 1992; Chicken anemia virus causes apoptosis of thymocytes after in vivo infection and of cell lines after in vitro infection. J Virol 66:7383–7388[PubMed]
    [Google Scholar]
  35. Karlberg H., Tan Y. J., Mirazimi A. 2011; Induction of caspase activation and cleavage of the viral nucleocapsid protein in different cell types during Crimean-Congo hemorrhagic fever virus infection. J Biol Chem 286:3227–3234 [View Article][PubMed]
    [Google Scholar]
  36. King A. M. Q., Adams M. J., Carstens E. B., Lefkowitz E. J. 2009 Virus Taxonomy: Classification and Nomenclature of Viruses: Ninth Report of the International Committee on Taxonomy of Viruses Amersterdam: Elsevier;
    [Google Scholar]
  37. Kleinschmidt M. C., Michaelis M., Ogbomo H., Doerr H. W., Cinatl J. Jr. 2007; Inhibition of apoptosis prevents West Nile virus induced cell death. BMC Microbiol 7:49 [View Article][PubMed]
    [Google Scholar]
  38. Kolokoltsova O. A., Grant A. M., Huang C., Smith J. K., Poussard A. L., Tian B., Brasier A. R., Peters C. J., Tseng C. T., other authors. 2014; RIG-I enhanced interferon independent apoptosis upon Junin virus infection. PLoS One 9:e99610 [View Article][PubMed]
    [Google Scholar]
  39. Kumar S. 2007; Caspase function in programmed cell death. Cell Death Differ 14:32–43 [View Article][PubMed]
    [Google Scholar]
  40. Li X. D., Kukkonen S., Vapalahti O., Plyusnin A., Lankinen H., Vaheri A. 2004; Tula hantavirus infection of Vero E6 cells induces apoptosis involving caspase 8 activation. J Gen Virol 85:3261–3268 [View Article][PubMed]
    [Google Scholar]
  41. Méndez E., Salas-Ocampo E., Arias C. F. 2004; Caspases mediate processing of the capsid precursor and cell release of human astroviruses. J Virol 78:8601–8608 [View Article][PubMed]
    [Google Scholar]
  42. Nuñez G., Benedict M. A., Hu Y., Inohara N. 1998; Caspases: the proteases of the apoptotic pathway. Oncogene 17:3237–3245 [View Article][PubMed]
    [Google Scholar]
  43. Olsen C. W., Kehren J. C., Dybdahl-Sissoko N. R., Hinshaw V. S. 1996; bcl-2 alters influenza virus yield, spread, and hemagglutinin glycosylation. J Virol 70:663–666[PubMed]
    [Google Scholar]
  44. Peters C. J., Buchmeier M., Rollin P. E., Ksiazek T. G. 1996; Arenaviruses. In Fields Virology, 3rd edn. pp 1521–1551Edited by Knipe D. M., Howley P. M. Philadelphia, PA: Lippincott-Raven;
    [Google Scholar]
  45. Pugazhenthi S., Gilden D. H., Nair S., McAdoo A., Wellish M., Brazeau E., Mahalingam R. 2009; Simian varicella virus induces apoptosis in monkey kidney cells by the intrinsic pathway and involves downregulation of Bcl-2 expression. J Virol 83:9273–9282 [View Article][PubMed]
    [Google Scholar]
  46. Ravindra P. V., Tiwari A. K., Ratta B., Chaturvedi U., Palia S. K., Subudhi P. K., Kumar R., Sharma B., Rai A., Chauhan R. S. 2008; Induction of apoptosis in Vero cells by Newcastle disease virus requires viral replication, de-novo protein synthesis and caspase activation. Virus Res 133:285–290 [View Article][PubMed]
    [Google Scholar]
  47. Richard A., Tulasne D. 2012; Caspase cleavage of viral proteins, another way for viruses to make the best of apoptosis. Cell Death Dis 3:e277 [View Article][PubMed]
    [Google Scholar]
  48. Rodrigues R., Paranhos-Baccalà G., Vernet G., Peyrefitte C. N. 2012; Crimean-Congo hemorrhagic fever virus-infected hepatocytes induce ER-stress and apoptosis crosstalk. PLoS One 7:e29712 [View Article][PubMed]
    [Google Scholar]
  49. Roulston A., Marcellus R. C., Branton P. E. 1999; Viruses and apoptosis. Annu Rev Microbiol 53:577–628 [View Article][PubMed]
    [Google Scholar]
  50. Sayler K. A., Barbet A. F., Chamberlain C., Clapp W. L., Alleman R., Loeb J. C., Lednicky J. A. 2014; Isolation of Tacaribe virus, a Caribbean arenavirus, from host-seeking Amblyomma americanum ticks in Florida. PLoS One 9:e115769 [View Article][PubMed]
    [Google Scholar]
  51. Shih S. R., Weng K. F., Stollar V., Li M. L. 2008; Viral protein synthesis is required for enterovirus 71 to induce apoptosis in human glioblastoma cells. J Neurovirol 14:53–61 [View Article][PubMed]
    [Google Scholar]
  52. Teodoro J. G., Branton P. E. 1997; Regulation of apoptosis by viral gene products. J Virol 71:1739–1746[PubMed]
    [Google Scholar]
  53. Thompson M. R., Kaminski J. J., Kurt-Jones E. A., Fitzgerald K. A. 2011; Pattern recognition receptors and the innate immune response to viral infection. Viruses 3:920–940 [View Article][PubMed]
    [Google Scholar]
  54. Timmer J. C., Salvesen G. S. 2007; Caspase substrates. Cell Death Differ 14:66–72 [View Article][PubMed]
    [Google Scholar]
  55. Urata S., Yasuda J., de la Torre J. C. 2009; The Z protein of the New World arenavirus Tacaribe virus has bona fide budding activity that does not depend on known late domain motifs. J Virol 83:12651–12655 [View Article][PubMed]
    [Google Scholar]
  56. Weissenbacher M. C., Coto C. E., Calello M. A. 1975-1976; Cross-protection between Tacaribe complex viruses. Presence of neutralizing antibodies against Junin virus (Argentine hemorrhagic fever) in guinea pigs infected with Tacaribe virus. Intervirology 6:42–49 [View Article][PubMed]
    [Google Scholar]
  57. Wolff S., Becker S., Groseth A. 2013a; Cleavage of the Junin virus nucleoprotein serves a decoy function to inhibit the induction of apoptosis during infection. J Virol 87:224–233 [View Article][PubMed]
    [Google Scholar]
  58. Wolff S., Ebihara H., Groseth A. 2013b; Arenavirus budding: a common pathway with mechanistic differences. Viruses 5:528–549 [View Article][PubMed]
    [Google Scholar]
  59. Wurzer W. J., Planz O., Ehrhardt C., Giner M., Silberzahn T., Pleschka S., Ludwig S. 2003; Caspase 3 activation is essential for efficient influenza virus propagation. EMBO J 22:2717–2728 [View Article][PubMed]
    [Google Scholar]
  60. Xing J., Ly H., Liang Y. 2015; The Z proteins of pathogenic but not nonpathogenic arenaviruses inhibit RIG-I-like receptor-dependent interferon production. J Virol 89:2944–2955 [View Article][PubMed]
    [Google Scholar]
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