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A Shope Fibroma virus PYRIN-only protein modulates the host immune response

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Abstract

PYRIN domain (PYD) proteins have recently emerged as important signaling molecules involved in the development of innate immunity to intracellular pathogens through activation of inflammatory mediator pathways. ASC is the central adaptor protein, which links pathogen recognition by PYD-containing pathogen recognition receptors to the activation of downstream effectors, including activation of Caspase-1 and NF-κB. The cellular PYD-only protein 1 (cPOP1) can block the recruitment of ASC to activated PAN receptors and thereby functions as an endogenous inhibitor of the PYD-mediated signal transduction pathway. Here we describe the identification and characterization of a Shope Fibroma homolog to cPOP1. Like cPOP1, a Shope Fibroma virus-encoded POP (vPOP), co-localizes and directly associates with ASC and inhibits PYD-mediated signal transduction. Poxviruses are known to encode immune evasive proteins to promote host cell infection and suppression of the host immune response. Poxvirus-encoded vPOPs represent a novel class of immune evasive proteins and impair the host response by blocking Cryopyrin and ASC inflammasome-mediated activation of pro-Caspase-1 and subsequent processing of pro-interleukin (IL)-1β, and expression of vPOPs causes activation of NF-κB.

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References

  1. C. Stehlik, J.C. Reed, J. Exp. Med. 200, 551–558 (2004)

    Article  CAS  Google Scholar 

  2. J. Tschopp, F. Martinon, K. Burns, Nat. Rev. Mol. Cell Biol. 4, 95–104 (2003)

    Article  CAS  Google Scholar 

  3. J.P. Ting, B.K. Davis, Annu. Rev. Immunol. 23, 387–414 (2004)

    Article  Google Scholar 

  4. N. Inohara, G. Nunez, Nat. Rev. Immunol. 3, 371–381 (2003)

    Article  CAS  Google Scholar 

  5. K.E. Conway, B.B. McConnell, C.E. Bowring, C.D. Donald, S.T. Warren, P.M. Vertino, Cancer Res. 60, 6236–6242 (2000)

    CAS  PubMed  Google Scholar 

  6. J. Masumoto, S. Taniguchi, K. Ayukawa, H. Sarvotham, T. Kishino, N. Niikawa, E. Hidaka, T. Katsuyama, T. Higuchi, J. Sagara, J. Biol. Chem. 274, 33835–33838 (1999)

    Article  CAS  Google Scholar 

  7. F. Martinon, K. Burns, J. Tschopp, Mol. Cell. 10, 417–426 (2002)

    Article  CAS  Google Scholar 

  8. S. Brydges, D.L. Kastner, Curr. Top. Microbiol. Immunol. 305, 127–160 (2006)

    CAS  PubMed  Google Scholar 

  9. S.-H. Lee, C. Stehlik, J.C. Reed, J. Biol. Chem. 276, 34495–34500 (2001)

    Article  CAS  Google Scholar 

  10. E.W. Humke, S.K. Shriver, M.A. Starovasnik, W.J. Fairbrother, V.M. Dixit, Cell 103, 99–111 (2000)

    Article  CAS  Google Scholar 

  11. A. Druilhe, S.M. Srinivasula, M. Razmara, M. Ahmad, E.S. Alnemri, Cell Death Differ. 8, 649–657 (2001)

    Article  CAS  Google Scholar 

  12. M. Lamkanfi, G. Denecker, M. Kalai, K. D’Hondt, A. Meeus, W. Declercq, X. Saelens, P. Vandenabeele, J. Biol. Chem. 279, 51729–51738 (2004)

    Article  CAS  Google Scholar 

  13. G. Condorelli, G. Vigliotta, A. Cafieri, A. Trencia, P. Andalo, F. Oriente, C. Miele, M. Caruso, P. Formisano, F. Beguinot, Oncogene 18, 4409–4415 (1999)

    Article  CAS  Google Scholar 

  14. A. Krueger, I. Schmitz, S. Baumann, P.H. Krammer, S. Kirchhoff, J. Biol. Chem. 276, 20633–20640 (2001)

    Article  CAS  Google Scholar 

  15. C. Stehlik, M. Krajewska, K. Welsh, S. Krajewski, A. Godzik, J.C. Reed, Biochem. J. 373, 101–113 (2003)

    Article  CAS  Google Scholar 

  16. J.B. Johnston, J.W. Barrett, S.H. Nazarian, M. Goodwin, D. Ricuttio, G. Wang, G. McFadden, Immunity 23, 587–598 (2005)

    Article  CAS  Google Scholar 

  17. C. Stehlik, L. Fiorentino, A. Dorfleutner, J.M. Bruey, E.M. Ariza, J. Sagara, J.C. Reed, J. Exp. Med. 196, 1605–1615 (2002)

    Article  CAS  Google Scholar 

  18. C. Stehlik, S.H. Lee, A. Dorfleutner, A. Stassinopoulos, J. Sagara, J.C. Reed, J. Immunol. 171, 6154–6163 (2003)

    Article  CAS  Google Scholar 

  19. E. Liepinsh, R. Barbals, E. Dahl, A. Sharipo, E. Staub, G. Otting, J. Mol. Biol. 332, 1155–1163 (2003)

    Article  CAS  Google Scholar 

  20. C. Cameron, S. Hota-Mitchell, L. Chen, J. Barrett, J.X. Cao, C. Macaulay, D. Willer, D. Evans, G. McFadden, Virology 264, 298–318 (1999)

    Article  CAS  Google Scholar 

  21. D.O. Willer, G. McFadden, D.H. Evans, Virology 264, 319–343 (1999)

    Article  CAS  Google Scholar 

  22. C.L. Afonso, E.R. Tulman, Z. Lu, L. Zsak, F.A. Osorio, C. Balinsky, G.F. Kutish, D.L. Rock, J. Virol. 76, 783–790 (2002)

    Article  CAS  Google Scholar 

  23. H.J. Lee, K. Essani, G.L. Smith, Virology 281, 170–192 (2001)

    Article  CAS  Google Scholar 

  24. C.L. Afonso, G. Delhon, E.R. Tulman, Z. Lu, A. Zsak, V.M. Becerra, L. Zsak, G.F. Kutish, D.L. Rock, J. Virol. 79, 966–977 (2005)

    Article  CAS  Google Scholar 

  25. T.A. Dowds, J. Masumoto, L. Zhu, N. Inohara, G. Nunez, J. Biol. Chem. 279, 21924–21928 (2004)

    Article  CAS  Google Scholar 

  26. G.A. Manji, L. Wang, B.J. Geddes, M. Brown, S. Merriam, A. Al-Garawi, S. Mak, J.M. Lora, M. Briskin, M. Jurman, J. Cao, P.S. DiStefano, J. Bertin, J. Biol. Chem. 277, 11570–11575 (2002)

    Article  CAS  Google Scholar 

  27. F.S. Sutterwala, Y. Ogura, M. Szczepanik, M. Lara-Tejero, G.S. Lichtenberger, E.P. Grant, J. Bertin, A.J. Coyle, J.E. Galan, P.W. Askenase, R.A. Flavell, Immunity 24, 317–327 (2006)

    Article  CAS  Google Scholar 

  28. T.D. Kanneganti, N. Ozoren, M. Body-Malapel, A. Amer, J.H. Park, L. Franchi, J. Whitfield, W. Barchet, M. Colonna, P. Vandenabeele, J. Bertin, A. Coyle, E.P. Grant, S. Akira, G. Nunez, Nature 440, 232–236 (2006)

    Article  Google Scholar 

  29. F. Martinon, V. Petrilli, A. Mayor, A. Tardivel, J. Tschopp, Nature 440, 237–241 (2006)

    Article  CAS  Google Scholar 

  30. S. Mariathasan, D.S. Weiss, K. Newton, J. McBride, K. O’Rourke, M. Roose-Girma, W.P. Lee, Y. Weinrauch, D.M. Monack, V.M. Dixit, Nature 440, 228–232 (2006)

    Article  CAS  Google Scholar 

  31. T.D. Kanneganti, M. Body-Malapel, A. Amer, J.H. Park, J. Whitfield, Z.F. Taraporewala, D. Miller, J.T. Patton, N. Inohara, G. Nunez, J. Biol. Chem.281, 36560–36568 (2006)

    Article  CAS  Google Scholar 

  32. J.W. Yu, J. Wu, Z. Zhang, P. Datta, I. Ibrahimi, S. Taniguchi, J. Sagara, T. Fernandes-Alnemri, E.S. Alnemri, Cell Death Differ. 13, 236–249 (2006)

    Article  CAS  Google Scholar 

  33. S. Mariathasan, K. Newton, D.M. Monack, D. Vucic, D.M. French, W.P. Lee, M. Roose-Girma, S. Erickson, V.M. Dixit, Nature 430, 213–218 (2004)

    Article  CAS  Google Scholar 

  34. M. Yamamoto, K. Yaginuma, H. Tsutsui, J. Sagara, X. Guan, E. Seki, K. Yasuda, M. Yamamoto, S. Akira, K. Nakanishi, T. Noda, S. Taniguchi, Genes Cells 9, 1055–1067 (2004)

    Article  CAS  Google Scholar 

  35. B.T. Seet, J.B. Johnston, C.R. Brunetti, J.W. Barrett, H. Everett, C. Cameron, J. Sypula, S.H. Nazarian, A. Lucas, G. McFadden, Annu. Rev. Immunol. 21, 377–423 (2003)

    Article  CAS  Google Scholar 

  36. B. Moss, J.L. Shisler, Semin. Immunol. 13, 59–66 (2001)

    Article  CAS  Google Scholar 

  37. G. Fantuzzi, C.A. Dinarello, J. Clin. Immunol. 19, 1–11 (1999)

    Article  CAS  Google Scholar 

  38. J. Schmitz, A. Owyang, E. Oldham, Y. Song, E. Murphy, T.K. McClanahan, G. Zurawski, M. Moshrefi, J. Qin, X. Li, D.M. Gorman, J.F. Bazan, R.A. Kastelein, Immunity 23, 479–490 (2005)

    Article  CAS  Google Scholar 

  39. A. Sarkar, M. Duncan, J. Hart, E. Hertlein, D.C. Guttridge, M.D. Wewers, J. Immunol. 176, 4979–4986 (2006)

    Article  CAS  Google Scholar 

  40. C. Camus-Bouclainville, L. Fiette, S. Bouchiha, B. Pignolet, D. Counor, C. Filipe, J. Gelfi, F. Messud-Petit, J. Virol. 78, 2510–2516 (2004)

    Article  CAS  Google Scholar 

  41. L. Wang, G.A. Manji, J.M. Grenier, A. Al-Garawi, S. Merriam, J.M. Lora, B.J. Geddes, M. Briskin, P.S. DiStefano, J. Bertin, J. Biol. Chem. 277, 29874–29880 (2002)

    Article  CAS  Google Scholar 

  42. M. Hasegawa, R. Imamura, T. Kinoshita, N. Matsumoto, J. Masumoto, N. Inohara, T. Suda, J. Biol. Chem. 280, 15122–15130 (2005)

    Article  CAS  Google Scholar 

  43. J. Hiscott, H. Kwon, P. Genin, J. Clin. Invest. 107, 143–151 (2001)

    Article  CAS  Google Scholar 

  44. M. Karin, Y. Cao, F.R. Greten, Z.-W. Li, Nat. Rev. Cancer 2, 301–310 (2002)

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The project described was supported by Grant Number 5P20-RR-016440 (CS, DCF) from the National Center for Research Resources (NCRR), a component of the National Institutes of Health (NIH) and Grant Numbers 1R21-AI-067680 (CS), 1R03-AI-067806 (CS), and R 01-AI-56324 (JCR) from NIAID/NIH. Its contents are solely the responsibility of the authors and do not necessarily represent the official views of NCRR or NIH. We are also grateful to the support from the Alexander Bland Osborn Cancer Center Endowment (CS).

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Authors and Affiliations

  1. Mary Babb Randolph Cancer Center and Department of Microbiology, Immunology & Cell Biology, West Virginia University School of Medicine, 1826 MBRCC, 1 Medical Center Drive, Morgantown, WV, 26506-9300, USA

    Andrea Dorfleutner, Siera J. Talbott, Nicole B. Bryan, Kristin N. Funya, Stephanie L. Rellick, Daniel C. Flynn & Christian Stehlik

  2. Burnham Institute for Medical Research, 10901 North Torrey Pines Road, La Jolla, CA, 92037, USA

    John C. Reed

  3. Pathology and Physiology Research Branch, Health Effects Laboratory Division, National Institute for Occupational Safety and Health, Morgantown, WV, 26505, USA

    Xianglin Shi

  4. Department of Pharmaceutical Sciences, School of Pharmacy, West Virginia University, 1 Medical Center Drive, Morgantown, WV, 26506-9500, USA

    Yon Rojanasakul

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  1. Andrea Dorfleutner
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Correspondence to Christian Stehlik.

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Andrea Dorfleutner and Siera J. Talbott contributed equally to this work.

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Dorfleutner, A., Talbott, S.J., Bryan, N.B. et al. A Shope Fibroma virus PYRIN-only protein modulates the host immune response. Virus Genes 35, 685–694 (2007). https://doi.org/10.1007/s11262-007-0141-9

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  • DOI: https://doi.org/10.1007/s11262-007-0141-9

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