Potential role for snoRNAs in PKR activation during metabolic stress

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 16, 2015, Pages 5023-5028

  Osama, A Youssef ^a   Sarah, A Safran ^a   Takahisa, Nakamura ^b   David, A Nix ^c   Gökhan, S Hotamisligil ^d   Brenda, L Bass ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^c UNIVERSITY OF UTAH   (United States)

^d HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Metabolic stress; Phosphorylation; RNA binding protein; SnoRNA

Indexed keywords

5' MONOPHOSPHATE; 5' TRIPHOSPHATE; DOUBLE STRANDED RNA; PALMITIC ACID; PHOSPHATE; PROTEIN KINASE; PROTEIN KINASE RNA ACTIVATED; SMALL NUCLEOLAR RNA; UNCLASSIFIED DRUG; CELL EXTRACT; PROTEIN KINASE R;

ANIMAL CELL; ARTICLE; AUTOPHOSPHORYLATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FIBROBLAST; GENETIC TRANSFECTION; IMMUNOPRECIPITATION; METABOLIC STRESS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN RNA BINDING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WILD TYPE; ANIMAL; CHO CELL LINE; CRICETULUS; DRUG EFFECTS; ENZYME ACTIVATION; HAMSTER; METABOLISM; PHYSIOLOGICAL STRESS; REPRODUCIBILITY;

MAMMALIA; MUS;

ANIMALS; CELL EXTRACTS; CHO CELLS; CRICETINAE; CRICETULUS; EIF-2 KINASE; ENZYME ACTIVATION; IMMUNOPRECIPITATION; MICE; PALMITIC ACID; REPRODUCIBILITY OF RESULTS; RNA, SMALL NUCLEOLAR; STRESS, PHYSIOLOGICAL;

EID: 84928137393     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1424044112     Document Type: Article

References (40)

1. Donnelly N, Gorman AM, Gupta S, Samali A (2013) The eIF2α kinases: Their structures and functions. Cell Mol Life Sci 70(19):3493-3511.
2. Hotamisligil GS (2010) Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 140(6):900-917.
3. Toth AM, Zhang P, Das S, George CX, Samuel CE (2006) Interferon action and the double-stranded RNA-dependent enzymes ADAR1 adenosine deaminase and PKR protein kinase. Prog Nucleic Acid Res Mol Biol 81:369-434.
4. Dabo S, Meurs EF (2012) dsRNA-dependent protein kinase PKR and its role in stress, signaling and HCV infection. Viruses 4(11):2598-2635.
5. Dauber B, Wolff T (2009) Activation of the antiviral kinase PKR and viral countermeasures. Viruses 1(3):523-544.
6. Meurs E, et al. (1990) Molecular cloning and characterization of the human doublestranded RNA-activated protein kinase induced by interferon. Cell 62(2):379-390.
7. Taylor DR, et al. (1996) Autophosphorylation sites participate in the activation of the double-stranded-RNA-activated protein kinase PKR. Mol Cell Biol 16(11):6295-6302.
8. Romano PR, et al. (1998) Autophosphorylation in the activation loop is required for full kinase activity in vivo of human and yeast eukaryotic initiation factor 2alpha kinases PKR and GCN2. Mol Cell Biol 18(4):2282-2297.
9. McMillan NA, et al. (1995) Mutational analysis of the double-stranded RNA (dsRNA) binding domain of the dsRNA-activated protein kinase, PKR. J Biol Chem 270(6):2601-2606.
10. Cole JL (2007) Activation of PKR: An open and shut case? Trends Biochem Sci 32(2): 57-62.
11. Holcik M, Sonenberg N (2005) Translational control in stress and apoptosis. Nat Rev Mol Cell Biol 6(4):318-327.
12. Bonnet MC, Weil R, Dam E, Hovanessian AG, Meurs EF (2000) PKR stimulates NF-kappaB irrespective of its kinase function by interacting with the IkappaB kinase complex. Mol Cell Biol 20(13):4532-4542.
13. Nakamura T, et al. (2010) Double-stranded RNA-dependent protein kinase links pathogen sensing with stress and metabolic homeostasis. Cell 140(3):338-348.
14. Davis S, Watson JC (1996) In vitro activation of the interferon-induced, double-stranded RNA-dependent protein kinase PKR by RNA from the 3' untranslated regions of human alpha-tropomyosin. Proc Natl Acad Sci USA 93(1):508-513.
15. Osman F, Jarrous N, Ben-Asouli Y, Kaempfer R (1999) A cis-acting element in the 3'-untranslated region of human TNF-alpha mRNA renders splicing dependent on the activation of protein kinase PKR. Genes Dev 13(24):3280-3293.
16. Nussbaum JM, Gunnery S, Mathews MB (2002) The 3'-untranslated regions of cytoskeletal muscle mRNAs inhibit translation by activating the double-stranded RNA-dependent protein kinase PKR. Nucleic Acids Res 30(5):1205-1212.
17. Carvalho BM, et al. (2013) Modulation of double-stranded RNA-activated protein kinase in insulin sensitive tissues of obese humans. Obesity (Silver Spring) 21(12): 2452-2457.
18. Nakamura T, Arduini A, Baccaro B, Furuhashi M, Hotamisligil GS (2014) Small-molecule inhibitors of PKR improve glucose homeostasis in obese diabetic mice. Diabetes 63(2):526-534.
19. Carvalho-Filho MA, et al. (2012) Double-stranded RNA-activated protein kinase is a key modulator of insulin sensitivity in physiological conditions and in obesity in mice. Endocrinology 153(11):5261-5274.
20. Nix DA, Courdy SJ, Boucher KM (2008) Empirical methods for controlling false positives and estimating confidence in ChIP-Seq peaks. BMC Bioinformatics 9:523.
21. Nicol JW, Helt GA, Blanchard SG, Jr, Raja A, Loraine AE (2009) The Integrated Genome Browser: Free software for distribution and exploration of genome-scale datasets. Bioinformatics 25(20):2730-2731.
22. Lafontaine DL, Tollervey D (1998) Birth of the snoRNPs: The evolution of the modification-guide snoRNAs. Trends Biochem Sci 23(10):383-388.
23. Pellé R, Murphy NB (1993) In vivo UV-cross-linking hybridization: A powerful technique for isolating RNA binding proteins. Application to trypanosome mini-exon derived RNA. Nucleic Acids Res 21(10):2453-2458.
24. Ule J, Jensen K, Mele A, Darnell RB (2005) CLIP: A method for identifying protein-RNA interaction sites in living cells. Methods 37(4):376-386.
25. Michel CI, et al. (2011) Small nucleolar RNAs U32a, U33, and U35a are critical mediators of metabolic stress. Cell Metab 14(1):33-44.
26. Nallagatla SR, et al. (2007) 5'-Triphosphate-dependent activation of PKR by RNAs with short stem-loops. Science 318(5855):1455-1458.
27. Kiss T, Fayet E, Jády BE, Richard P, Weber M (2006) Biogenesis and intranuclear trafficking of human box C/D and H/ACA RNPs. Cold Spring Harb Symp Quant Biol 71: 407-417.
28. Nakamura T, et al. (2015) A critical role for PKR complexes with TRBP in immunometabolic regulation and eIF2a phosphorylation in obesity. Cell Rep, 10.1016/j.celrep.2015.03.021.
29. Kim Y, et al. (2014) PKR is activated by cellular dsRNAs during mitosis and acts as a mitotic regulator. Genes Dev 28(12):1310-1322.
30. Zhang J, Yang Y, Wu J (2010) Palmitate impairs cytokinesis associated with RhoA inhibition. Cell Res 20(4):492-494.
31. Toroney R, Hull CM, Sokoloski JE, Bevilacqua PC (2012) Mechanistic characterization of the 5'-triphosphate-dependent activation of PKR: Lack of 5'-end nucleobase specificity, evidence for a distinct triphosphate binding site, and a critical role for the dsRBD. RNA 18(10):1862-1874.
32. Tycowski KT, Shu MD, Steitz JA (1993) A small nucleolar RNA is processed from an intron of the human gene encoding ribosomal protein S3. Genes Dev 7(7A):1176-1190.
33. Dieci G, Preti M, Montanini B (2009) Eukaryotic snoRNAs: A paradigm for gene expression flexibility. Genomics 94(2):83-88.
34. Otsuka Y, Kedersha NL, Schoenberg DR (2009) Identification of a cytoplasmic complex that adds a cap onto 5'-monophosphate RNA. Mol Cell Biol 29(8):2155-2167.
35. Goubau D, et al. (2014) Antiviral immunity via RIG-I-mediated recognition of RNA bearing 5'-diphosphates. Nature 514(7522):372-375.
36. Schubert T, et al. (2012) Df31 protein and snoRNAs maintain accessible higher-order structures of chromatin. Mol Cell 48(3):434-444.
37. Fong YW, Ho JJ, Inouye C, Tjian R (2014) The dyskerin ribonucleoprotein complex as an OCT4/SOX2 coactivator in embryonic stem cells. eLife 3:3.
38. Rybak-Wolf A, et al. (2014) A variety of dicer substrates in human and C. elegans. Cell 159(5):1153-1167.
39. Esteller M (2011) Non-coding RNAs in human disease. Nat Rev Genet 12(12):861-874.
40. Scruggs BS, Michel CI, Ory DS, Schaffer JE (2012) SmD3 regulates intronic noncoding RNA biogenesis. Mol Cell Biol 32(20):4092-4103.