The RNA binding protein La/SS-B promotes RIG-I-mediated type I and type III IFN responses following Sendai viral infection

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Mahony, Rebecca ^a   Broadbent, Lindsay ^b   Maier Moore, Jacen S ^c   Power, Ultan F ^b   Jefferies, Caroline A ^a,d  

^a ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^b QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^c UNIVERSITY OF TEXAS AT EL PASO   (United States)

^d CEDARS SINAI MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; INTERFERON; INTERFERON TYPE III; RNA BINDING PROTEIN;

HEK293 CELL LINE; HUMAN; METABOLISM; RESPIROVIRUS INFECTION; SENDAI VIRUS; VIROLOGY;

CHEMOKINES; HEK293 CELLS; HUMANS; INTERFERON TYPE I; INTERFERONS; RESPIROVIRUS INFECTIONS; RNA-BINDING PROTEINS; SENDAI VIRUS;

EID: 85032996263     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-15197-9     Document Type: Article

References (71)

1. Yoneyama, M. et al. Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J Immunol 175, 2851-2858 (2005).
2. Kato, H. et al. Cell type-specific involvement of RIG-I in antiviral response. Immunity 23, 19-28 (2005).
3. Loo, Y. M. et al. Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity. J Virol 82, 335-345 (2008).
4. Kawai, T. et al. IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nature immunology 6, 981-988 (2005).
5. Meylan, E. et al. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437, 1167-1172 (2005).
6. Kumar, H. et al. Essential role of IPS-1 in innate immune responses against RNA viruses. J Exp Med 203, 1795-1803 (2006).
7. Sharma, S. et al. Triggering the interferon antiviral response through an IKK-related pathway. Science 300, 1148-1151 (2003).
8. Fitzgerald, K. A. et al. IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nature immunology 4, 491-496 (2003).
9. Lin, R., Mamane, Y. & Hiscott, J. Structural and Functional Analysis of Interferon Regulatory Factor 3: Localization of the Transactivation and Autoinhibitory Domains. Molecular and Cellular Biology 19, 2465-2474 (1999).
10. Kumar, K. P., McBride, K. M., Weaver, B. K., Dingwall, C. & Reich, N. C. Regulated Nuclear-Cytoplasmic Localization of Interferon Regulatory Factor 3, a Subunit of Double-Stranded RNA-Activated Factor 1. Molecular and Cellular Biology 20, 4159-4168 (2000).
11. Isaacs, A. & Lindenmann, J. Virus interference. I. The interferon. Proc R Soc Lond B Biol Sci 147, 258-267 (1957).
12. Isaacs, A., Lindenmann, J. & Valentine, R. C. Virus interference. II. Some properties of interferon. Proc R Soc Lond B Biol Sci 147, 268-273 (1957).
13. O'Shea, J. J., Notarangelo, L. D., Johnston, J. A. & Candotti, F. Advances in the understanding of cytokine signal transduction: the role of Jaks and STATs in immunoregulation and the pathogenesis of immunodeficiency. J Clin Immunol 17, 431-447 (1997).
14. Horvath, C. M., Stark, G. R., Kerr, I. M. & Darnell, J. E. Jr. Interactions between STAT and non-STAT proteins in the interferonstimulated gene factor 3 transcription complex. Mol Cell Biol 16, 6957-6964 (1996).
15. Sato, M. et al. Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-alpha/beta gene induction. Immunity 13, 539-548 (2000).
16. Honda, K. et al. IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 434, 772-777 (2005).
17. Clemens, M. J. & Elia, A. The double-stranded RNA-dependent protein kinase PKR: structure and function. J Interferon Cytokine Res 17, 503-524 (1997).
18. Stark, G. R., Kerr, I. M., Williams, B. R. G., Silverman, R. H. & Schreiber, R. D. How cells respond to interferons. Annual Review of Biochemistry 67, 227-264 (1998).
19. Le Bon, A. et al. Direct Stimulation of T Cells by Type I IFN Enhances the CD8+ T Cell Response during Cross-Priming. The Journal of Immunology 176, 4682-4689 (2006).
20. Le Bon, A. et al. Cutting Edge: Enhancement of Antibody Responses Through Direct Stimulation of B and T Cells by Type I IFN. The Journal of Immunology 176, 2074-2078 (2006).
21. Trinchieri, G., Santoli, D., Granato, D. & Perussia, B. Antagonistic effects of interferons on the cytotoxicity mediated by natural killer cells. Fed Proc 40, 2705-2710 (1981).
22. Salazar-Mather, T. P., Ishikawa, R. & Biron, C. A. NK cell trafficking and cytokine expression in splenic compartments after IFN induction and viral infection. J Immunol 157, 3054-3064 (1996).
23. Le Bon, A. et al. Cross-priming of CD8+ T cells stimulated by virus-induced type I interferon. Nature immunology 4, 1009-1015 (2003).
24. Le Bon, A. et al. Type i interferons potently enhance humoral immunity and can promote isotype switching by stimulating dendritic cells in vivo. Immunity 14, 461-470 (2001).
25. Zhou, L. et al. Activation of toll-like receptor-3 induces interferon-lambda expression in human neuronal cells. Neuroscience 159, 629-637 (2009).
26. Onoguchi, K. et al. Viral infections activate types I and III interferon genes through a common mechanism. J Biol Chem 282, 7576-7581 (2007).
27. Kotenko, S. V. et al. IFN-lambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nature immunology 4, 69-77 (2003).
28. Sheppard, P. et al. IL-28, IL-29 and their class II cytokine receptor IL-28R. Nature immunology 4, 63-68 (2003).
29. Sommereyns, C., Paul, S., Staeheli, P. & Michiels, T. IFN-lambda (IFN-lambda) is expressed in a tissue-dependent fashion and primarily acts on epithelial cells in vivo. PLoS Pathog 4, e1000017 (2008).
30. Dumoutier, L., Lejeune, D., Hor, S., Fickenscher, H. & Renauld, J. C. Cloning of a new type II cytokine receptor activating signal transducer and activator of transcription (STAT)1, STAT2 and STAT3. Biochem J 370, 391-396 (2003).
31. Chiu, Y. H., Macmillan, J. B. & Chen, Z. J. RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway. Cell 138, 576-591 (2009).
32. Ablasser, A. et al. RIG-I-dependent sensing of poly(dA:dT) through the induction of an RNA polymerase III-transcribed RNA intermediate. Nature immunology 10, 1065-1072 (2009).
33. Maraia, R. J. Transcription termination factor La is also an initiation factor for RNA polymerase III. Proc Natl Acad Sci USA 93, 3383-3387 (1996).
34. Gottlieb, E. & Steitz, J. A. The RNA binding protein La influences both the accuracy and the efficiency of RNA polymerase III transcription in vitro. EMBO J 8, 841-850 (1989).
35. Gottlieb, E. & Steitz, J. A. Function of the mammalian La protein: evidence for its action in transcription termination by RNA polymerase III. EMBO J 8, 851-861 (1989).
36. Stefano, J. E. Purified lupus antigen La recognizes an oligouridylate stretch common to the 3′ termini of RNA polymerase III transcripts. Cell 36, 145-154 (1984).
37. Maraia, R. J. & Intine, R. V. A. Recognition of Nascent RNA by the Human La Antigen: Conserved and Divergent Features of Structure and Function. Mol. Cell. Biol. 21, 367-379 (2001).
38. Fairley, J. A. et al. Human La is found at RNA polymerase III-transcribed genes in vivo. Proc Natl Acad Sci USA 102, 18350-18355 (2005).
39. Kurilla, M. G. & Keene, J. D. The leader RNA of vesicular stomatitis virus is bound by a cellular protein reactive with anti-La lupus antibodies. Cell 34, 837-845 (1983).
40. Kurilla, M. G., Cabradilla, C. D., Holloway, B. P. & Keene, J. D. Nucleotide sequence and host La protein interactions of rabies virus leader RNA. J Virol 50, 773-778 (1984).
41. Wilusz, J. & Keene, J. D. Interactions of plus and minus strand leader RNAs of the New Jersey serotype of vesicular stomatitis virus with the cellular La protein. Virology 135, 65-73 (1984).
42. Wilusz, J., Kurilla, M. G. & Keene, J. D. A host protein (La) binds to a unique species of minus-sense leader RNA during replication of vesicular stomatitis virus. Proc Natl Acad Sci USA 80, 5827-5831 (1983).
43. Bitko, V., Musiyenko, A., Bayfield, M. A., Maraia, R. J. & Barik, S. Cellular La protein shields nonsegmented negative-strand RNA viral leader RNA from RIG-I and enhances virus growth by diverse mechanisms. J Virol 82, 7977-7987 (2008).
44. Domitrovich, A. M., Diebel, K. W., Ali, N., Sarker, S. & Siddiqui, A. Role of La autoantigen and polypyrimidine tract-binding protein in HCV replication. Virology 335, 72-86 (2005).
45. Costa-Mattioli, M., Svitkin, Y. & Sonenberg, N. La Autoantigen Is Necessary for Optimal Function of the Poliovirus and Hepatitis C Virus Internal Ribosome Entry Site In Vivo and In Vitro. Mol. Cell. Biol. 24, 6861-6870 (2004).
46. Liu, Y. et al. Autoantigen La Promotes Efficient RNAi, Antiviral Response, and Transposon Silencing by Facilitating Multiple-Turnover RISC Catalysis. Mol Cell 44, 502-508 (2011).
47. Garcin, D., Itoh, M. & Kolakofsky, D. A Point Mutation in the Sendai Virus Accessory C Proteins Attenuates Virulence for Mice, but Not Virus Growth in Cell Culture. Virology 238, 424-431 (1997).
48. Itoh, M., Shibuta, H. & Homma, M. Single amino acid substitution of Sendai virus at the cleavage site of the fusion protein confers trypsin resistance. J Gen Virol 68 (Pt 11), 2939-2944 (1987).
49. Yamaguchi, R., Iwai, H. & Ueda, K. Variation of virulence and other properties among Sendai virus strains. Microbiol Immunol 32, 235-240 (1988).
50. Mochizuki, Y., Tashiro, M. & Homma, M. Pneumopathogenicity in mice of a Sendai virus mutant, TSrev-58, is accompanied by in vitro activation with trypsin. J Virol 62, 3040-3042 (1988).
51. Lopez, C. B., Garcia-Sastre, A., Williams, B. R. & Moran, T. M. Type I interferon induction pathway, but not released interferon, participates in the maturation of dendritic cells induced by negative-strand RNA viruses. J Infect Dis 187, 1126-1136 (2003).
52. Lopez, C. B. et al. TLR-independent induction of dendritic cell maturation and adaptive immunity by negative-strand RNA viruses. J Immunol 173, 6882-6889 (2004).
53. Baum, A. & García-Sastre, A. Differential recognition of viral RNA by RIG-I. Virulence 2, 166-169 (2011).
54. Baum, A., Sachidanandam, R. & García-Sastre, A. Preference of RIG-I for short viral RNA molecules in infected cells revealed by next-generation sequencing. Proceedings of the National Academy of Sciences of the United States of America 107, 16303-16308 (2010).
55. Melchjorsen, J. et al. Activation of innate defense against a paramyxovirus is mediated by RIG-I and TLR7 and TLR8 in a cell-typespecific manner. J Virol 79, 12944-12951 (2005).
56. Meerovitch, K. et al. La autoantigen enhances and corrects aberrant translation of poliovirus RNA in reticulocyte lysate. J Virol 67, 3798-3807 (1993).
57. Brierley, M. M., Marchington, K. L., Jurisica, I. & Fish, E. N. Identification of GAS-dependent interferon-sensitive target genes whose transcription is STAT2-dependent but ISGF3-independent. FEBS J 273, 1569-1581 (2006).
58. Ank, N. et al. Lambda interferon (IFN-lambda), a type III IFN, is induced by viruses and IFNs and displays potent antiviral activity against select virus infections in vivo. J Virol 80, 4501-4509 (2006).
59. Coccia, E. M. et al. Viral infection and Toll-like receptor agonists induce a differential expression of type I and lambda interferons in human plasmacytoid and monocyte-derived dendritic cells. Eur J Immunol 34, 796-805 (2004).
60. Gack, M. U., Nistal-Villan, E., Inn, K.-S., Garcia-Sastre, A. & Jung, J. U. Phosphorylation-Mediated Negative Regulation of RIG-I Antiviral Activity. J. Virol. 84, 3220-3229 (2010).
61. Gao, D. et al. REUL Is a Novel E3 Ubiquitin Ligase and Stimulator of Retinoic-Acid-Inducible Gene-I. PLoS ONE 4, e5760 (2009).
62. Oshiumi, H., Matsumoto, M., Hatakeyama, S. & Seya, T. Riplet/RNF135, a RING finger protein, ubiquitinates RIG-I to promote interferon-beta induction during the early phase of viral infection. J Biol Chem 284, 807-817 (2009).
63. Sun, Z., Ren, H., Liu, Y., Teeling, J. L. & Gu, J. Phosphorylation of RIG-I by Casein Kinase II Inhibits Its Antiviral Response. J. Virol. 85, 1036-1047 (2011).
64. Poeck, H. et al. Recognition of RNA virus by RIG-I results in activation of CARD9 and inflammasome signaling for interleukin 1 beta production. Nature immunology 11, 63-69 (2010).
65. Ling, Z., Tran, K. C. & Teng, M. N. Human respiratory syncytial virus nonstructural protein NS2 antagonizes the activation of beta interferon transcription by interacting with RIG-I. J Virol 83, 3734-3742 (2009).
66. Goswami, R. et al. Viral degradasome hijacks mitochondria to suppress innate immunity. Cell Res 23, 1025-1042 (2013).
67. Pruijn, G. J., Thijssen, J. P., Smith, P. R., Williams, D. G. & Van Venrooij, W. J. Anti-La monoclonal antibodies recognizing epitopes within the RNA-binding domain of the La protein show differential capacities to immunoprecipitate RNA-associated La protein. Eur J Biochem 232, 611-619 (1995).
68. Villenave, R. et al. Cytopathogenesis of Sendai Virus in Well-Differentiated Primary Pediatric Bronchial Epithelial Cells. Jsournal of Virology 84, 11718-11728 (2010).
69. Touzelet, O. et al. De novo generation of a non-segmented negative strand RNA virus with a bicistronic gene. Virus research 140, 40-48 (2009).
70. Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402-408 (2001).
71. Laemmli, U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685 (1970).