Hypomorphic mutation in the site-1 protease Mbtps1 endows resistance to persistent viral infection in a cell-specific manner

Cell Host and Microbe

Volumn 9, Issue 3, 2011, Pages 212-222

  Popkin, Daniel L ^a   Teijaro, John R ^a   Sullivan, Brian M ^a   Urata, Shuzo ^a   Rutschmann, Sophie ^a   De La Torre, Juan Carlos ^a   Kunz, Stefan ^a,b   Beutler, Bruce ^a   Oldstone, Michael ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE BOUND TRANSCRIPTION FACTOR PEPTIDASE SITE 1; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN;

ALLELE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARENAVIRUS INFECTION; ARTICLE; CELL SPECIFICITY; CONTROLLED STUDY; DENDRITIC CELL; ENZYME ACTIVITY; ENZYME SPECIFICITY; GENE EXPRESSION; GENE MUTATION; GENE TARGETING; GENETIC CODE; HEPATITIS B VIRUS; HEPATITIS C VIRUS; HUMAN IMMUNODEFICIENCY VIRUS; LYMPHOCYTIC CHORIOMENINGITIS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MOUSE; NONHUMAN; PERSISTENT VIRUS INFECTION; PRIORITY JOURNAL; VIRUS TITRATION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTIGENS, VIRAL; ARENAVIRIDAE INFECTIONS; B-LYMPHOCYTES; BONE MARROW CELLS; DENDRITIC CELLS; IMMUNITY, INNATE; IMMUNOCOMPROMISED HOST; KIDNEY; LIVER; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MICE; MICE, INBRED C57BL; MUTATION; PLAQUE ASSAY; PROPROTEIN CONVERTASES; SERINE ENDOPEPTIDASES; SPLEEN; T-LYMPHOCYTES; VIRAL TROPISM;

ARENAVIRUS; HEPATITIS B VIRUS; HEPATITIS C VIRUS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MUS; RODENTIA;

EID: 79952660523     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2011.02.006     Document Type: Article

References (43)

1. Bergeron, E., Vincent, M.J., and Nichol, S.T. (2007). Crimean-Congo hemorrhagic fever virus glycoprotein processing by the endoprotease SKI-1/S1P is critical for virus infectivity. J. Virol. 81, 13271-13276. (Pubitemid 350156967)
2. Borrow, P., Evans, C.F., and Oldstone, M.B. (1995). Virus-induced immunosuppression: immune system-mediated destruction of virus-infected dendritic cells results in generalized immune suppression. J. Virol. 69, 1059-1070.
3. Brandl, K., Rutschmann, S., Li, X., Du, X., Xiao, N., Schnabl, B., Brenner, D.A., and Beutler, B. (2009). Enhanced sensitivity to DSS colitis caused by a hypomorphic Mbtps1 mutation disrupting the ATF6-driven unfolded protein response. Proc. Natl. Acad. Sci. USA 106, 3300-3305.
4. Brown, M.S., Ye, J., Rawson, R.B., and Goldstein, J.L. (2000). Regulated intramembrane proteolysis: a control mechanism conserved from bacteria to humans. Cell 100, 391-398.
5. Buchmeier, M.J., Lewicki, H.A., Tomori, O., and Oldstone, M.B. (1981). Monoclonal antibodies to lymphocytic choriomeningitis and pichinde viruses: generation, characterization, and cross-reactivity with other arenaviruses. Virology 113, 73-85. (Pubitemid 11041742)
6. Bukrinsky, M., and Sviridov, D. (2006). Human immunodeficiency virus infection and macrophage cholesterol metabolism. J. Leukoc. Biol. 80, 1044-1051.
7. Carter, C.C., Onafuwa-Nuga, A., McNamara, L.A., Riddell, J., 4th, Bixby, D., Savona, M.R., and Collins, K.L. (2010). HIV-1 infects multipotent progenitor cells causing cell death and establishing latent cellular reservoirs. Nat. Med. 16, 446-451.
8. Chaput, N., Conforti, R., Viaud, S., Spatz, A., and Zitvogel, L. (2008). The Janus face of dendritic cells in cancer. Oncogene 27, 5920-5931.
9. Chen, X., Shen, J., and Prywes, R. (2002). The luminal domain of ATF6 senses endoplasmic reticulum (ER) stress and causes translocation of ATF6 from the ER to the Golgi. J. Biol. Chem. 277, 13045-13052.
10. de la Torre, J.C., and Oldstone, M.B. (1996). Anatomy of viral persistence: mechanisms of persistence and associated disease. Adv. Virus Res. 46, 311-343.
11. Emonet, S.F., Garidou, L., McGavern, D.B., and de la Torre, J.C. (2009). Generation of recombinant lymphocytic choriomeningitis viruses with trisegmented genomes stably expressing two additional genes of interest. Proc. Natl. Acad. Sci. USA 106, 3473-3478.
12. Evans, C.F., Borrow, P., de la Torre, J.C., and Oldstone, M.B. (1994). Virus-induced immunosuppression: kinetic analysis of the selection of a mutation associated with viral persistence. J. Virol. 68, 7367-7373. (Pubitemid 24328792)
13. Flatz, L., Bergthaler, A., de la Torre, J.C., and Pinschewer, D.D. (2006). Recovery of an arenavirus entirely from RNA polymerase I/II-driven cDNA. Proc. Natl. Acad. Sci. USA 103, 4663-4668.
14. Hawkins, J.L., Robbins, M.D., Warren, L.C., Xia, D., Petras, S.F., Valentine, J.J., Varghese, A.H., Wang, I.K., Subashi, T.A., Shelly, L.D., et al. (2008). Pharmacologic inhibition of site 1 protease activity inhibits sterol regulatory element-binding protein processing and reduces lipogenic enzyme gene expression and lipid synthesis in cultured cells and experimental animals. J. Pharmacol. Exp. Ther. 326, 801-808.
15. Hay, B.A., Abrams, B., Zumbrunn, A.Y., Valentine, J.J., Warren, L.C., Petras, S.F., Shelly, L.D., Xia, A., Varghese, A.H., Hawkins, J.L., et al. (2007). Aminopyrrolidineamide inhibitors of site-1 protease. Bioorg. Med. Chem. Lett. 17, 4411-4414.
16. Homann, D., Teyton, L., and Oldstone, M.B. (2001). Differential regulation of antiviral T-cell immunity results in stable CD8+ but declining CD4+ T-cell memory. Nat. Med. 7, 913-919.
17. Ilett, E.J., Prestwich, R.J., and Melcher, A.A. (2010). The evolving role of dendritic cells in cancer therapy. Expert Opin. Biol. Ther. 10, 369-379.
18. Jamieson, B.D., Butler, L.D., and Ahmed, R. (1987). Effective clearance of a persistent viral infection requires cooperation between virus-specific Lyt2+ T cells and nonspecific bone marrow-derived cells. J. Virol. 61, 3930-3937. (Pubitemid 18011494)
19. Lehman, T.L., O'Halloran, K.P., Hoover, E.A., and Avery, P.R. (2010). Utilizing the FIV model to understand dendritic cell dysfunction and the potential role of dendritic cell immunization in HIV infection. Vet. Immunol. Immunopathol. 134, 75-81.
20. Li, Q., Skinner, P.J., Ha, S.J., Duan, L., Mattila, T.L., Hage, A., White, C., Barber, D.L., O'Mara, L., Southern, P.J., et al. (2009). Visualizing antigen-specific and infected cells in situ predicts outcomes in early viral infection. Science 323, 1726-1729.
21. Liou, L.Y., Blasius, A.L., Welch, M.J., Colonna, M., Oldstone, M.B., and Zuniga, E.I. (2008). In vivo conversion of BM plasmacytoid DC into CD11b+ conventional DC during virus infection. Eur. J. Immunol. 38, 3388-3394.
22. Liu, B., Woltman, A.M., Janssen, H.L., and Boonstra, A. (2009). Modulation of dendritic cell function by persistent viruses. J. Leukoc. Biol. 85, 205-214.
23. Matloubian, M., Kolhekar, S.R., Somasundaram, T., and Ahmed, R. (1993). Molecular determinants of macrophage tropism and viral persistence: importance of single amino acid changes in the polymerase and glycoprotein of lymphocytic choriomeningitis virus. J. Virol. 67, 7340-7349. (Pubitemid 23343862)
24. Nadanaka, S., Yoshida, H., Kano, F., Murata, M., and Mori, K. (2004). Activation of mammalian unfolded protein response is compatible with the quality control system operating in the endoplasmic reticulum. Mol. Biol. Cell 15, 2537-2548.
25. Oldstone, M.B. (2002). Arenaviruses. II. The molecular pathogenesis of arenavirus infections. Introduction. Curr. Top. Microbiol. Immunol. 263, V-XII.
26. Oldstone, M.B. (2009). Anatomy of viral persistence. PLoS Pathog. 5, e1000523.
27. Popkin, D.L., Watson, M.A., Karaskov, E., Dunn, G.P., Bremner, R., and Virgin, H.W., 4th. (2003). Murine cytomegalovirus paralyzes macrophages by blocking IFN gamma-induced promoter assembly. Proc. Natl. Acad. Sci. USA 100, 14309-14314.
28. Recher, M., Lang, K.S., Navarini, A., Hunziker, L., Lang, P.A., Fink, K., Freigang, S., Georgiev, P., Hangartner, L., Zellweger, R., et al. (2007). Extralymphatic virus sanctuaries as a consequence of potent T-cell activation. Nat. Med. 13, 1316-1323.
29. Riethmüller, J., Riehle, A., Grassmé, H., and Gulbins, E. (2006). Membrane rafts in host-pathogen interactions. Biochim. Biophys. Acta 1758, 2139-2147.
30. Rojek, J.M., and Kunz, S. (2008). Cell entry by human pathogenic arenaviruses. Cell. Microbiol. 10, 828-835.
31. Rojek, J.M., Perez, M., and Kunz, S. (2008). Cellular entry of lymphocytic choriomeningitis virus. J. Virol. 82, 1505-1517.
32. Rojek, J.M., Pasqual, G., Sanchez, A.B., Nguyen, N.T., de la Torre, J.C., and Kunz, S. (2010). Targeting the proteolytic processing of the viral glycoprotein precursor is a promising novel antiviral strategy against arenaviruses. J. Virol. 84, 573-584.
33. Ron, D., and Walter, P. (2007). Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 8, 519-529.
34. Sevilla, N., Kunz, S., Holz, A., Lewicki, H., Homann, D., Yamada, H., Campbell, K.P., de La Torre, J.C., and Oldstone, M.B. (2000). Immunosuppression and resultant viral persistence by specific viral targeting of dendritic cells. J. Exp. Med. 192, 1249-1260.
35. Sevilla, N., Kunz, S., McGavern, D., and Oldstone, M.B. (2003). Infection of dendritic cells by lymphocytic choriomeningitis virus. Curr. Top. Microbiol. Immunol. 276, 125-144.
36. Sevilla, N., McGavern, D.B., Teng, C., Kunz, S., and Oldstone, M.B. (2004a). Viral targeting of hematopoietic progenitors and inhibition of DC maturation as a dual strategy for immune subversion. J. Clin. Invest. 113, 737-745.
37. Sevilla, N., McGavern, D.B., Teng, C., Kunz, S., and Oldstone, M.B. (2004b). Viral targeting of hematopoietic progenitors and inhibition of DC maturation as a dual strategy for immune subversion. J. Clin. Invest. 113, 737-745.
38. van der Most, R.G., Sette, A., Oseroff, C., Alexander, J., Murali-Krishna, K., Lau, L.L., Southwood, S., Sidney, J., Chesnut, R.W., Matloubian, M., and Ahmed, R. (1996). Analysis of cytotoxic T cell responses to dominant and subdominant epitopes during acute and chronic lymphocytic choriomeningitis virus infection. J. Immunol. 157, 5543-5554. (Pubitemid 126448976)
39. Wu, C., Orozco, C., Boyer, J., Leglise, M., Goodale, J., Batalov, S., Hodge, C.L., Haase, J., Janes, J., Huss, J.W., 3rd, and Su, A.I. (2009). BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol. 10, R130.
40. Yang, J., Goldstein, J.L., Hammer, R.E., Moon, Y.A., Brown, M.S., and Horton, J.D. (2001). Decreased lipid synthesis in livers of mice with disrupted Site-1 protease gene. Proc. Natl. Acad. Sci. USA 98, 13607-13612.
41. Ye, J., Rawson, R.B., Komuro, R., Chen, X., Davé, U.P., Prywes, R., Brown, M.S., and Goldstein, J.L. (2000). ER stress induces cleavage of membranebound ATF6 by the same proteases that process SREBPs. Mol. Cell 6, 1355-1364. (Pubitemid 32045928)
42. Zuniga, E.I., McGavern, D.B., Pruneda-Paz, J.L., Teng, C., and Oldstone, M.B. (2004). Bone marrow plasmacytoid dendritic cells can differentiate into myeloid dendritic cells upon virus infection. Nat. Immunol. 5, 1227-1234.
43. Zwirner, N.W., Croci, D.O., Domaica, C.I., and Rabinovich, G.A. (2010). Overcoming the hurdles of tumor immunity by targeting regulatory pathways in innate and adaptive immune cells. Curr. Pharm. Des. 16, 255-267.