Efficient Sensing of Infected Cells in Absence of Virus Particles by Blasmacytoid Dendritic Cells Is Blocked by the Viral Ribonuclease Erns

PLoS Pathogens

Volumn 9, Issue 6, 2013, Pages

  Python, Sylvie ^a   Gerber, Markus ^a   Suter, Rolf ^a   Ruggli, Nicolas ^a   Summerfield, Artur ^a  

^a INSTITUTE OF VIROLOGY AND IMMUNOLOGY   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; ALPHA1 INTERFERON; CHOLESTEROL; RIBONUCLEASE; VIRUS PROTEIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CELL CONTACT; CELL LINE; CELL STIMULATION; CONTROLLED STUDY; CYTOSKELETON; ENZYME LINKED IMMUNOSORBENT ASSAY; FLAVIVIRUS; FLOW CYTOMETRY; MONOCYTE; NONHUMAN; PLASMACYTOID DENDRITIC CELL; REAL TIME POLYMERASE CHAIN REACTION; SITE DIRECTED MUTAGENESIS; SWINE; SWINE DISEASE; VIRUS PARTICLE; VIRUS REPLICATION; VIRUS STRAIN; VIRUS TRANSMISSION;

ANIMALS; CELL LINE; CLASSICAL SWINE FEVER; CLASSICAL SWINE FEVER VIRUS; DENDRITIC CELLS; ENDORIBONUCLEASES; PLASMA CELLS; RNA, VIRAL; SWINE; TOLL-LIKE RECEPTOR 7; VIRAL PROTEINS;

CLASSICAL SWINE FEVER VIRUS; FLAVIVIRIDAE; HEPATITIS C VIRUS;

EID: 84879531380     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003412     Document Type: Article

References (63)

1. Reizis B, Bunin A, Ghosh HS, Lewis KL, Sisirak V, (2011) Plasmacytoid dendritic cells: recent progress and open questions. Annu Rev Immunol 29: 163-183.
2. Liu YJ, (2005) IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors. Annu Rev Immunol 23: 275-306.
3. Takahashi K, Asabe S, Wieland S, Garaigorta U, Gastaminza P, et al. (2010) Plasmacytoid dendritic cells sense hepatitis C virus-infected cells, produce interferon, and inhibit infection. Proc Natl Acad Sci U S A 107: 7431-7436.
4. Zhang S, Kodys K, Babcock GJ, Szabo G, (2012) CD81/CD9 tetraspanins aid plasmacytoid dendritic cells in recognition of HCV-infected cells and induction of IFNalpha. Hepatology 10.1002/hep.25827.
5. Lepelley A, Louis S, Sourisseau M, Law HK, Pothlichet J, et al. (2011) Innate sensing of HIV-infected cells. PLoS Pathog 7: e1001284.
6. Liess B, (1987) Pathogenesis and epidemiology of hog cholera. Ann Rech Vet 18: 139-145.
7. Balmelli C, Vincent IE, Rau H, Guzylack-Piriou L, McCullough K, et al. (2005) FcgammaRII-dependent sensitisation of natural interferon-producing cells for viral infection and interferon-alpha responses. Eur J Immunol 35: 2406-2415.
8. Fiebach AR, Guzylack-Piriou L, Python S, Summerfield A, Ruggli N, (2011) Classical Swine Fever virus npro limits type I interferon induction in plasmacytoid dendritic cells by interacting with interferon regulatory factor 7. J Virol 85: 8002-8011.
9. Summerfield A, (2012) Viewpoint: Factors involved in type I interferon responses during porcine virus infections. Vet Immunol Immunopathol 148: 168-171.
10. Schneider R, Unger G, Stark R, Schneider-Scherzer E, Thiel HJ, (1993) Identification of a structural glycoprotein of an RNA virus as a ribonuclease. Science 261: 1169-1171.
11. Peterhans E, Schweizer M, (2012) BVDV: A pestivirus inducing tolerance of the innate immune response. Biologicals 41 (1):: 39-51.
12. Meyer C, Von Freyburg M, Elbers K, Meyers G, (2002) Recovery of virulent and RNase-negative attenuated type 2 bovine viral diarrhea viruses from infectious cDNA clones. J Virol 76: 8494-8503.
13. Meyers G, Saalmuller A, Buttner M, (1999) Mutations abrogating the RNase activity in glycoprotein E(rns) of the pestivirus classical swine fever virus lead to virus attenuation. J Virol 73: 10224-10235.
14. Meyers G, Ege A, Fetzer C, von Freyburg M, Elbers K, et al. (2007) Bovine viral diarrhea virus: prevention of persistent fetal infection by a combination of two mutations affecting Erns RNase and Npro protease. J Virol 81: 3327-3338.
15. Meyer H, Liess B, Frey HR, Hermanns W, Trautwein G, (1981) Experimental transplacental transmission of hog cholera virus in pigs. IV. Virological and serological studies in newborn piglets. Zentralbl Veterinarmed B 28: 659-668.
16. Iqbal M, Poole E, Goodbourn S, McCauley JW, (2004) Role for bovine viral diarrhea virus Erns glycoprotein in the control of activation of beta interferon by double-stranded RNA. J Virol 78: 136-145.
17. Magkouras I, Matzener P, Rumenapf T, Peterhans E, Schweizer M, (2008) RNase-dependent inhibition of extracellular, but not intracellular, dsRNA-induced interferon synthesis by Erns of pestiviruses. J Gen Virol 89: 2501-2506.
18. Matzener P, Magkouras I, Rumenapf T, Peterhans E, Schweizer M, (2009) The viral RNase E(rns) prevents IFN type-I triggering by pestiviral single- and double-stranded RNAs. Virus Res 140: 15-23.
19. Husser L, Ruggli N, Summerfield A, (2012) N(pro) of Classical Swine Fever Virus Prevents Type I Interferon-Mediated Priming of Conventional Dendritic Cells for Enhanced Interferon-alpha Response. J Interferon Cytokine Res 32: 221-229.
20. Ruggli N, Tratschin JD, Schweizer M, McCullough KC, Hofmann MA, et al. (2003) Classical swine fever virus interferes with cellular antiviral defense: evidence for a novel function of N(pro). J Virol 77: 7645-7654.
21. Carrasco CP, Rigden RC, Vincent IE, Balmelli C, Ceppi M, et al. (2004) Interaction of classical swine fever virus with dendritic cells. J Gen Virol 85: 1633-1641.
22. Suter R, Summerfield A, Thomann-Harwood LJ, McCullough KC, Tratschin JD, et al. (2011) Immunogenic and replicative properties of classical swine fever virus replicon particles modified to induce IFN-alpha/beta and carry foreign genes. Vaccine 29: 1491-1503.
23. Barrat FJ, Meeker T, Gregorio J, Chan JH, Uematsu S, et al. (2005) Nucleic acids of mammalian origin can act as endogenous ligands for Toll-like receptors and may promote systemic lupus erythematosus. J Exp Med 202: 1131-1139.
24. Lannes N, Python S, Summerfield A, (2012) Interplay of foot-and-mouth disease virus, antibodies and plasmacytoid dendritic cells: virus opsonization under non-neutralizing conditions results in enhanced interferon-alpha responses. Vet Res 43: 64.
25. Burrack S, Aberle D, Burck J, Ulrich AS, Meyers G, (2012) A new type of intracellular retention signal identified in a pestivirus structural glycoprotein. FASEB J 26 (8):: 3292-305.
26. Rumenapf T, Unger G, Strauss JH, Thiel HJ, (1993) Processing of the envelope glycoproteins of pestiviruses. J Virol 67: 3288-3294.
27. Fetzer C, Tews BA, Meyers G, (2005) The carboxy-terminal sequence of the pestivirus glycoprotein E(rns) represents an unusual type of membrane anchor. J Virol 79: 11901-11913.
28. Bauhofer O, Summerfield A, Sakoda Y, Tratschin JD, Hofmann MA, et al. (2007) Classical swine fever virus Npro interacts with interferon regulatory factor 3 and induces its proteasomal degradation. J Virol 81: 3087-3096.
29. Flanagan MD, Lin S, (1980) Cytochalasins block actin filament elongation by binding to high affinity sites associated with F-actin. J Biol Chem 255: 835-838.
30. Ahmad FJ, Echeverri CJ, Vallee RB, Baas PW, (1998) Cytoplasmic dynein and dynactin are required for the transport of microtubules into the axon. J Cell Biol 140: 391-401.
31. Guzylack-Piriou L, Bergamin F, Gerber M, McCullough KC, Summerfield A, (2006) Plasmacytoid dendritic cell activation by foot-and-mouth disease virus requires immune complexes. Eur J Immunol 36: 1674-1683.
32. Krey T, Bontems F, Vonrhein C, Vaney MC, Bricogne G, et al. (2012) Crystal Structure of the Pestivirus Envelope Glycoprotein E(rns) and Mechanistic Analysis of Its Ribonuclease Activity. Structure 20: 862-873.
33. Hausmann Y, Roman-Sosa G, Thiel HJ, Rumenapf T, (2004) Classical swine fever virus glycoprotein E rns is an endoribonuclease with an unusual base specificity. J Virol 78: 5507-5512.
34. Windisch JM, Schneider R, Stark R, Weiland E, Meyers G, et al. (1996) RNase of classical swine fever virus: biochemical characterization and inhibition by virus-neutralizing monoclonal antibodies. J Virol 70: 352-358.
35. Tews BA, Schurmann EM, Meyers G, (2009) Mutation of cysteine 171 of pestivirus E rns RNase prevents homodimer formation and leads to attenuation of classical swine fever virus. J Virol 83: 4823-4834.
36. Lee HK, Lund JM, Ramanathan B, Mizushima N, Iwasaki A, (2007) Autophagy-dependent viral recognition by plasmacytoid dendritic cells. Science 315: 1398-1401.
37. Peterhans E, Bachofen C, Stalder H, Schweizer M, (2010) Cytopathic bovine viral diarrhea viruses (BVDV): emerging pestiviruses doomed to extinction. Vet Res 41: 44.
38. Baker JA, Sheffy BE, (1960) A persistent hog cholera viremia in young pigs. Proc Soc Exp Biol Med 105: 675-678.
39. Carbrey EA, (1965) THE ROLE OF IMMUNE TOLERANCE IN TRANSMISSION OF HOG CHOLERA. J Am Vet Med Assoc 146: 233-237.
40. Carbrey EA, Stewart WC, Kresse JI, Snyder ML, (1980) Persistent hog cholera infection detected during virulence typing of 135 field isolates 580. AmJVetRes 41: 946-949.
41. Van Oirschot JT, (1977) A congenital persistent swine fever infection. II. Immune response to swine fever virus and unrelated antigens. Veterinary Microbiology 2: 133-142.
42. Liess B, (1984) Persistent infections of hog cholera: A review. Preventive Veterinary Medicine 2: 109-113.
43. Frey HR, Liess B, Richter-Reichhelm HB, von Benten K, Trautwein G, (1980) Experimental transplacental transmission of hog cholera virus in pigs. I. Virological and serological studies. Zentralbl Veterinarmed B 27: 154-164.
44. Plateau E, Vannier P, Tillon JP, (1980) Atypical hog cholera infection: viral isolation and clinical study of in utero transmission. Am J Vet Res 41: 2012-2015.
45. Summerfield A, Alves M, Ruggli N, de Bruin MG, McCullough KC, (2006) High IFN-alpha responses associated with depletion of lymphocytes and natural IFN-producing cells during classical swine fever. JInterferon Cytokine Res 26: 248-255.
46. Peterhans E, Schweizer M, (2010) Pestiviruses: how to outmaneuver your hosts. Vet Microbiol 142: 18-25.
47. Kasza L, Shadduck JA, Christofinis GJ, (1972) Establishment, viral susceptibility and biological characteristics of a swine kidney cell line SK-6. Res Vet Sci 13: 46-51.
48. Seebach JD, Schneider MK, Comrack CA, LeGuern A, Kolb SA, et al. (2001) Immortalized bone-marrow derived pig endothelial cells. Xenotransplantation 8: 48-61.
49. Frey CF, Bauhofer O, Ruggli N, Summerfield A, Hofmann MA, et al. (2006) Classical swine fever virus replicon particles lacking the E(rns) gene: a potential marker vaccine for intradermal application. Vet Res 37: 655-670.
50. Knoetig SM, Summerfield A, Spagnuolo-Weaver M, McCullough KC, (1999) Immunopathogenesis of classical swine fever: role of monocytic cells. Immunology 97: 359-366.
51. Carrasco CP, Rigden RC, Schaffner R, Gerber H, Neuhaus V, et al. (2001) Porcine dendritic cells generated in vitro: morphological, phenotypic and functional properties. Immunology 104: 175-184.
52. Ruggli N, Tratschin JD, Mittelholzer C, Hofmann MA, (1996) Nucleotide sequence of classical swine fever virus strain Alfort/187 and transcription of infectious RNA from stably cloned full-length cDNA. J Virol 70: 3478-3487.
53. Moser C, Stettler P, Tratschin JD, Hofmann MA, (1999) Cytopathogenic and noncytopathogenic RNA replicons of classical swine fever virus. J Virol 73: 7787-7794.
54. Maurer R, Stettler P, Ruggli N, Hofmann MA, Tratschin JD, (2005) Oronasal vaccination with classical swine fever virus (CSFV) replicon particles with either partial or complete deletion of the E2 gene induces partial protection against lethal challenge with highly virulent CSFV. Vaccine 23: 3318-3328.
55. Charley B, Laude H, (1988) Induction of alpha interferon by transmissible gastroenteritis coronavirus: role of transmembrane glycoprotein E1 1234. J Virol 62: 8-11.
56. Alves MP, Guzylack-Piriou L, Juillard V, Audonnet JC, Doel T, et al. (2009) Innate immune defenses induced by CpG do not promote vaccine-induced protection against foot-and-mouth disease virus in pigs. Clin Vaccine Immunol 16: 1151-1157.
57. Hoffmann B, Beer M, Schelp C, Schirrmeier H, Depner K, (2005) Validation of a real-time RT-PCR assay for sensitive and specific detection of classical swine fever. J Virol Methods 130: 36-44.
58. Zufferey R, Nagy D, Mandel RJ, Naldini L, Trono D, (1997) Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat Biotechnol 15: 871-875.
59. Alves MP, Neuhaus V, Guzylack-Piriou L, Ruggli N, McCullough KC, et al. (2007) Toll-like receptor 7 and MyD88 knockdown by lentivirus-mediated RNA interference to porcine dendritic cell subsets. Gene Ther 14: 836-844.
60. Greiser-Wilke I, Moennig V, Coulibaly CO, Dahle J, Leder L, et al. (1990) Identification of conserved epitopes on a hog cholera virus protein. Arch Virol 111: 213-225.
61. Greiser-Wilke I, Dittmar KE, Liess B, Moennig V, (1992) Heterogeneous expression of the non-structural protein p80/p125 in cells infected with different pestiviruses. J Gen Virol 73: 47-52.
62. Ceppi M, de Bruin MG, Seuberlich T, Balmelli C, Pascolo S, et al. (2005) Identification of classical swine fever virus protein E2 as a target for cytotoxic T cells by using mRNA-transfected antigen-presenting cells. J Gen Virol 86: 2525-2534.
63. Guzylack-Piriou L, Balmelli C, McCullough KC, Summerfield A, (2004) Type-A CpG oligonucleotides activate exclusively porcine natural interferon-producing cells to secrete interferon-alpha, tumour necrosis factor-alpha and interleukin-12. Immunology 112: 28-37.