RNase L induces autophagy via c-Jun N-terminal kinase and double-stranded RNA-dependent protein kinase signaling pathways

Journal of Biological Chemistry

Volumn 287, Issue 52, 2012, Pages 43651-43664

  Siddiqui, Mohammad Adnan ^a   Malathi, Krishnamurthy ^a  

^a UNIVERSITY OF TOLEDO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-VIRAL EFFECTS; AUTOPHAGY; BAFILOMYCIN; C-JUN N-TERMINAL KINASE; CELLULAR PROTEINS; DIRECT ACTIVATION; HOST RESPONSE; INITIAL STAGES; KNOCK OUTS; LIGHT CHAIN; MICROTUBULE ASSOCIATED PROTEIN; MOUSE EMBRYONIC FIBROBLASTS; PARACRINE; PHARMACOLOGICAL INHIBITORS; RNA-DEPENDENT PROTEIN KINASE; SENDAI VIRUS; SIGNALING PATHWAYS; VIRAL INFECTIONS; VIRAL PATHOGENESIS; VIRAL REPLICATION; WILD TYPES;

CELL CULTURE; ENZYMES; PHOSPHORYLATION; PROTEINS; VIRUSES;

RNA;

BECLIN 1; INTERFERON; MICROTUBULE ASSOCIATED PROTEIN; MICROTUBULE ASSOCIATED PROTEIN LIGHT CHAIN 3 I; MICROTUBULE ASSOCIATED PROTEIN LIGHT CHAIN 3 II; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN BCL 2; PROTEIN KINASE R; PROTEIN P62; RIBONUCLEASE L; STRESS ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; AUTOPHAGY; CELL VACUOLE; CONTROLLED STUDY; ENCEPHALOMYOCARDITIS VIRUS; ENZYME ACTIVATION; ENZYME ACTIVITY; GROWTH INHIBITION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; SENDAI VIRUS; VIROGENESIS; VIRUS INFECTION; VIRUS REPLICATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; AUTOPHAGY; CARDIOVIRUS INFECTIONS; CELL LINE, TUMOR; EIF-2 KINASE; EMBRYO, MAMMALIAN; ENCEPHALOMYOCARDITIS VIRUS; ENDORIBONUCLEASES; FIBROBLASTS; HEAT-SHOCK PROTEINS; HUMANS; MAP KINASE SIGNALING SYSTEM; MICE; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; MITOGEN-ACTIVATED PROTEIN KINASE 8; MITOGEN-ACTIVATED PROTEIN KINASE 9; PROTO-ONCOGENE PROTEINS C-BCL-2; RESPIROVIRUS INFECTIONS; RNA, DOUBLE-STRANDED; SENDAI VIRUS; VIRUS REPLICATION;

ENCEPHALOMYOCARDITIS VIRUS; SENDAI VIRUS;

EID: 84871601752     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.399964     Document Type: Article

References (65)

1. Shoji-Kawata, S., and Levine, B. (2009) Autophagy, antiviral immunity, and viral countermeasures. Biochim. Biophys. Acta 1793, 1478-1484
2. Saitoh, T., and Akira, S. (2010) Regulation of innate immune responses by autophagy-related proteins. J. Cell Biol. 189, 925-935
3. Dreux, M., and Chisari, F. V. (2010) Viruses and the autophagy machinery. Cell Cycle 9, 1295-1307
4. Cao, Y., and Klionsky, D. J. (2007) Physiological functions of Atg6/Beclin 1: a unique autophagy-related protein. Cell Res. 17, 839-849 (Pubitemid 47585112)
5. Kang, R., Zeh, H. J., Lotze, M. T., and Tang, D. (2011) The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ. 18, 571-580
6. He, C., and Levine, B. (2010) The Beclin 1 interactome. Curr. Opin. Cell Biol. 22, 140-149
7. Liang, X. H., Kleeman, L. K., Jiang, H. H., Gordon, G., Goldman, J. E., Berry, G., Herman, B., and Levine, B. (1998) Protection against fatal Sindbis virus encephalitis by beclin, a novel Bcl-2-interacting protein. J. Virol. 72, 8586-8596 (Pubitemid 28471796)
8. Maiuri, M. C., Le Toumelin, G., Criollo, A., Rain, J. C., Gautier, F., Juin, P., Tasdemir, E., Pierron, G., Troulinaki, K., Tavernarakis, N., Hickman, J. A., Geneste, O., and Kroemer, G. (2007) Functional and physical interaction between Bcl-X(L) and a BH3-like domain in Beclin-1. EMBO J. 26, 2527-2539 (Pubitemid 46788315)
9. Oberstein, A., Jeffrey, P. D., and Shi, Y. (2007) Crystal structure of the Bcl-XL-Beclin 1 peptide complex: Beclin 1 is a novel BH3-only protein. J. Biol. Chem. 282, 13123-13132 (Pubitemid 47100641)
10. Pattingre, S., Tassa, A., Qu, X., Garuti, R., Liang, X. H., Mizushima, N., Packer, M., Schneider, M. D., and Levine, B. (2005) Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122, 927-939 (Pubitemid 41345209)
11. Wei, Y., Pattingre, S., Sinha, S., Bassik, M., and Levine, B. (2008) JNK1-mediated phosphorylation of Bcl-2 regulates starvation-induced autophagy. Mol. Cell 30, 678-688 (Pubitemid 351818252)
12. Wei, Y., Sinha, S., and Levine, B. (2008) Dual role of JNK1-mediated phosphorylation of Bcl-2 in autophagy and apoptosis regulation. Autophagy 4, 949-951
13. Zalckvar, E., Berissi, H., Mizrachy, L., Idelchuk, Y., Koren, I., Eisenstein, M., Sabanay, H., Pinkas-Kramarski, R., and Kimchi, A. (2009) DAP-kinase-mediated phosphorylation on the BH3 domain of beclin 1 promotes dissociation of beclin 1 from Bcl-XL and induction of autophagy. EMBO Rep. 10, 285-292
14. Lee, H. K., and Iwasaki, A. (2008) Autophagy and antiviral immunity. Curr. Opin. Immunol. 20, 23-29
15. Delgado, M. A., Elmaoued, R. A., Davis, A. S., Kyei, G., and Deretic, V. (2008) Toll-like receptors control autophagy. EMBO J. 27, 1110-1121 (Pubitemid 351508141)
16. Shi, C. S., and Kehrl, J. H. (2008) MyD88 and Trif target Beclin 1 to trigger autophagy in macrophages. J. Biol. Chem. 283, 33175-33182
17. Jounai, N., Takeshita, F., Kobiyama, K., Sawano, A., Miyawaki, A., Xin, K. Q., Ishii, K. J., Kawai, T., Akira, S., Suzuki, K., and Okuda, K. (2007) The Atg5 Atg12 conjugate associates with innate antiviral immune responses. Proc. Natl. Acad. Sci. U.S.A. 104, 14050-14055 (Pubitemid 350003333)
18. Lei, Y., Wen, H., Yu, Y., Taxman, D. J., Zhang, L., Widman, D. G., Swanson, K. V., Wen, K. W., Damania, B., Moore, C. B., Giguère, P. M., Siderovski, D. P., Hiscott, J., Razani, B., Semenkovich, C. F., Chen, X., and Ting, J. P. (2012) The mitochondrial proteins NLRX1 and TUFM form a complex that regulates type I interferon and autophagy. Immunity 36, 933-946
19. He, B. (2006) Viruses, endoplasmic reticulum stress, and interferon responses. Cell Death Differ. 13, 393-403
20. Ogata, M., Hino, S., Saito, A., Morikawa, K., Kondo, S., Kanemoto, S., Murakami, T., Taniguchi, M., Tanii, I., Yoshinaga, K., Shiosaka, S., Hammarback, J. A., Urano, F., and Imaizumi, K. (2006) Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol. Cell. Biol. 26, 9220-9231 (Pubitemid 44904418)
21. Kouroku, Y., Fujita, E., Tanida, I., Ueno, T., Isoai, A., Kumagai, H., Ogawa, S., Kaufman, R. J., Kominami, E., and Momoi, T. (2007) ER stress (PERK/eIF2alpha phosphorylation) mediates the polyglutamine-induced LC3 conversion, an essential step for autophagy formation. Cell Death Differ. 14, 230-239 (Pubitemid 46092226)
22. Høyer-Hansen, M., and Jäättelä, M. (2007) Connecting endoplasmic reticulum stress to autophagy by unfolded protein response and calcium. Cell Death Differ. 14, 1576-1582
23. Wong, C. H., Iskandar, K. B., Yadav, S. K., Hirpara, J. L., Loh, T., and Pervaiz, S. (2010) Simultaneous induction of non-canonical autophagy and apoptosis in cancer cells by ROS-dependent ERK and JNK activation. PloS One 5, e9996
24. Komiya, K., Uchida, T., Ueno, T., Koike, M., Abe, H., Hirose, T., Kawamori, R., Uchiyama, Y., Kominami, E., Fujitani, Y., and Watada, H. (2010) Free fatty acids stimulate autophagy in pancreatic β-cells via JNK pathway. Biochem. Biophys. Res. Commun. 401, 561-567
25. Tallóczy, Z., Jiang, W., Virgin, H. W., 4th, Leib, D. A., Scheuner, D., Kaufman, R. J., Eskelinen, E. L., and Levine, B. (2002) Regulation of starvation- and virus-induced autophagy by the eIF2α kinase signaling pathway. Proc. Natl. Acad. Sci. U.S.A. 99, 190-195 (Pubitemid 34060339)
26. Tallóczy, Z., Virgin, H. W., 4th, and Levine, B. (2006) PKR-dependent autophagic degradation of herpes simplex virus type 1. Autophagy 2, 24-29
27. Orvedahl, A., Alexander, D., Talloczy, Z., Sun, Q., Wei, Y., Zhang, W., Burns, D., Leib, D. A., and Levine, B. (2007) HSV-1 ICP34.5 confers neurovirulence by targeting the Beclin 1 autophagy protein. Cell Host Microbe 1, 23-35 (Pubitemid 46506007)
28. Kerr, I. M., Wreschner, D. H., Silverman, R. H., Cayley, P. J., and Knight, M. (1981) The 2-5A (pppA2′p5′A2′p5′A) and protein kinase systems in interferon-treated and control cells. Adv. Cyclic Nucleotide Res. 14, 469-478
29. Zhou, A., Hassel, B. A., and Silverman, R. H. (1993) Expression cloning of 2-5A-dependent RNAase: a uniquely regulated mediator of interferon action. Cell 72, 753-765 (Pubitemid 23093883)
30. Floyd-Smith, G., Slattery, E., and Lengyel, P. (1981) Interferon action: RNA cleavage pattern of a (2′-5′)oligoadenylate-dependent endonuclease. Science 212, 1030-1032 (Pubitemid 11078012)
31. Wreschner, D. H., James, T. C., Silverman, R. H., and Kerr, I. M. (1981) Ribosomal RNA cleavage, nuclease activation and 2-5A(ppp(A2′p)nA) in interferon-treated cells. Nucleic Acids Res. 9, 1571-1581 (Pubitemid 11002216)
32. Malathi, K., Dong, B., Gale, M., Jr., and Silverman, R. H. (2007) Small self-RNA generated by RNase L amplifies antiviral innate immunity. Nature 448, 816-819 (Pubitemid 47266340)
33. Silverman, R. H., Cayley, P. J., Knight, M., Gilbert, C. S., and Kerr, I. M. (1982) Control of the ppp(a2′p)nA system in HeLa cells. Effects of interferon and virus infection. Eur. J. Biochem. 124, 131-138 (Pubitemid 12094721)
34. Cebollero, E., Reggiori, F., and Kraft, C. (2012) Reticulophagy and ribophagy: regulated degradation of protein production factories. Int. J. Cell Biol. 2012, 182834
35. Iordanov, M. S., Paranjape, J. M., Zhou, A., Wong, J., Williams, B. R., Meurs, E. F., Silverman, R. H., and Magun, B. E. (2000) Activation of p38 mitogen-activated protein kinase and c-Jun NH(2)-terminal kinase by double-stranded RNA and encephalomyocarditis virus: involvement of RNase L, protein kinase R, and alternative pathways. Mol. Cell. Biol. 20, 617-627 (Pubitemid 30023103)
36. Li, G., Xiang, Y., Sabapathy, K., and Silverman, R. H. (2004) An apoptotic signaling pathway in the interferon antiviral response mediated by RNase L and c-Jun NH2-terminal kinase. J. Biol. Chem. 279, 1123-1131 (Pubitemid 38082634)
37. Malathi, K., Paranjape, J. M., Ganapathi, R., and Silverman, R. H. (2004) HPC1/RNASEL mediates apoptosis of prostate cancer cells treated with 2′,5′-oligoadenylates, topoisomerase I inhibitors, and tumor necrosis factor-related apoptosis-inducing ligand. Cancer Res. 64, 9144-9151 (Pubitemid 39665529)
38. Tanida, I., Yamaji, T., Ueno, T., Ishiura, S., Kominami, E., and Hanada, K. (2008) Consideration about negative controls for LC3 and expression vectors for four colored fluorescent protein-LC3 negative controls. Autophagy 4, 131-134
39. Hartmann, R., Justesen, J., Sarkar, S. N., Sen, G. C., and Yee, V. C. (2003) Crystal structure of the 2′-specific and double-stranded RNA-activated interferon-induced antiviral protein 2′-5′- oligoadenylate synthetase. Mol. Cell 12, 1173-1185 (Pubitemid 37487926)
40. Thakur, C. S., Jha, B. K., Dong, B., Das Gupta, J., Silverman, K. M., Mao, H., Sawai, H., Nakamura, A. O., Banerjee, A. K., Gudkov, A., and Silverman, R. H. (2007) Small-molecule activators of RNase L with broadspectrum antiviral activity. Proc. Natl. Acad. Sci. U.S.A. 104, 9585-9590 (Pubitemid 47175310)
41. Malathi, K., Paranjape, J. M., Bulanova, E., Shim, M., Guenther-Johnson, J. M., Faber, P. W., Eling, T. E., Williams, B. R., and Silverman, R. H. (2005) A transcriptional signaling pathway in the IFN system mediated by 2′-5′-oligoadenylate activation of RNase L. Proc. Natl. Acad. Sci. U.S.A. 102, 14533-14538 (Pubitemid 41457092)
42. Mizushima, N., Yoshimori, T., and Levine, B. (2010) Methods in mammalian autophagy research. Cell 140, 313-326
43. Silverman, R. H., Skehel, J. J., James, T. C., Wreschner, D. H., and Kerr, I. M. (1983) rRNA cleavage as an index of ppp(A2′p)nA activity in interferon-treated encephalomyocarditis virus-infected cells. J. Virol. 46, 1051-1055 (Pubitemid 13092515)
44. Samuel, C. E. (1993) The eIF-2α protein kinases, regulators of translation in eukaryotes from yeasts to humans. J. Biol. Chem. 268, 7603-7606
45. Gusella, G. L., Musso, T., Rottschafer, S. E., Pulkki, K., and Varesio, L. (1995) Potential requirement of a functional double-stranded RNA-dependent protein kinase (PKR) for the tumoricidal activation of macrophages by lipopolysaccharide or IFN-αβ, but not IFN-γ. J. Immunol. 154, 345-354
46. Pattingre, S., Bauvy, C., Carpentier, S., Levade, T., Levine, B., and Codogno, P. (2009) Role of JNK1-dependent Bcl-2 phosphorylation in ceramide-induced macroautophagy. J. Biol. Chem. 284, 2719-2728
47. Zhou, A., Paranjape, J., Brown, T. L., Nie, H., Naik, S., Dong, B., Chang, A., Trapp, B., Fairchild, R., Colmenares, C., and Silverman, R. H. (1997) Interferon action and apoptosis are defective in mice devoid of 2′,5′-oligoadenylate-dependent RNase L. EMBO J. 16, 6355-6363 (Pubitemid 27483262)
48. McKendry, R., John, J., Flavell, D., Müller, M., Kerr, I. M., and Stark, G. R. (1991) High-frequency mutagenesis of human cells and characterization of a mutant unresponsive to both α and γ interferons. Proc. Natl. Acad. Sci. U.S.A. 88, 11455-11459 (Pubitemid 21916060)
49. Deretic, V. (2012) Autophagy as an innate immunity paradigm: expanding the scope and repertoire of pattern recognition receptors. Curr. Opin. Immunol. 24, 21-31
50. Kraft, C., Deplazes, A., Sohrmann, M., and Peter, M. (2008) Mature ribosomes are selectively degraded upon starvation by an autophagy pathway requiring the Ubp3p/Bre5p ubiquitin protease. Nature Cell Biol. 10, 602-610 (Pubitemid 351627380)
51. MacIntosh, G. C., and Bassham, D. C. (2011) The connection between ribophagy, autophagy and ribosomal RNA decay. Autophagy 7, 662-663
52. Silverman, R. H. (2007) Viral encounters with 2′,5′- oligoadenylate synthetase and RNase L during the interferon antiviral response. J. Virol. 81, 12720-12729
53. Baltanás, F. C., Casafont, I., Weruaga, E., Alonso, J. R., Berciano, M. T., and Lafarga, M. (2011) Nucleolar disruption and cajal body disassembly are nuclear hallmarks of DNA damage-induced neurodegeneration in purkinje cells. Brain Pathol. 21, 374-388
54. Rusch, L., Zhou, A., and Silverman, R. H. (2000) Caspase-dependent apoptosis by 2′,5′-oligoadenylate activation of RNase L is enhanced by IFN-beta. J. Interferon Cytokine Res. 20, 1091-1100 (Pubitemid 32015249)
55. Kroemer, G., Mariño, G., and Levine, B. (2010) Autophagy and the integrated stress response. Mol. Cell 40, 280-293
56. Pattingre, S., Bauvy, C., Levade, T., Levine, B., and Codogno, P. (2009) Ceramide-induced autophagy: to junk or to protect cells? Autophagy 5, 558-560
57. Ku, B., Woo, J. S., Liang, C., Lee, K. H., Hong, H. S., E, X., Kim, K. S., Jung, J. U., and Oh, B. H. (2008) Structural and biochemical bases for the inhibition of autophagy and apoptosis by viral BCL-2 of murine γ-herpesvirus 68. PLoS pathogens 4, e25
58. Sinha, S., Colbert, C. L., Becker, N., Wei, Y., and Levine, B. (2008) Molecular basis of the regulation of Beclin 1-dependent autophagy by the γ-herpesvirus 68 Bcl-2 homolog M11. Autophagy 4, 989-997
59. Espert, L., Varbanov, M., Robert-Hebmann, V., Sagnier, S., Robbins, I., Sanchez, F., Lafont, V., and Biard-Piechaczyk, M. (2009) Differential role of autophagy in CD4 T cells and macrophages during X4 and R5 HIV-1 infection. PloS One 4, e5787
60. Dreux, M., Gastaminza, P., Wieland, S. F., and Chisari, F. V. (2009) The autophagy machinery is required to initiate hepatitis C virus replication. Proc. Natl. Acad. Sci. U.S.A. 106, 14046-14051
61. Williams, B. R. (2001) Signal integration via PKR. Science's STKE: Signal Transduction Knowledge Environment 2001, re2
62. Nakamura, T., Furuhashi, M., Li, P., Cao, H., Tuncman, G., Sonenberg, N., Gorgun, C. Z., and Hotamisligil, G. S. (2010) Double-stranded RNA-dependent protein kinase links pathogen sensing with stress and metabolic homeostasis. Cell 140, 338-348
63. Zhang, Y., Li, Z., Ge, X., Guo, X., and Yang, H. (2011) Autophagy promotes the replication of encephalomyocarditis virus in host cells. Autophagy 7, 613-628
64. Silverman, R. H. (2007) A scientific journey through the 2-5A/RNase L system. Cytokine Growth Factor Rev. 18, 381-388
65. Chakrabarti, A., Ghosh, P. K., Banerjee, S., Gaughan, C., and Silverman, R. H. (2012) RNase L Triggers Autophagy in Response to Viral Infections. J. Virol. 86, 11311-11321