Live or let die: Posttranscriptional gene regulation in cell stress and cell death

Immunological Reviews

Volumn 253, Issue 1, 2013, Pages 237-252

  Thomas, Marshall P ^a   Lieberman, Judy ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Apoptosis; MiRNA; Pre mRNA splicing; Stress; Translation

Indexed keywords

MICRORNA; RNA INDUCED SILENCING COMPLEX;

ALTERNATIVE RNA SPLICING; APOPTOSIS; CELL CYCLE ARREST; CELL STRESS; ENDOPLASMIC RETICULUM STRESS; GENE CONTROL; GENOTOXICITY; HEAT SHOCK; HEAT SHOCK RESPONSE; HUMAN; INTERNAL RIBOSOME ENTRY SITE; MEMBRANE PERMEABILITY; NONHUMAN; OSMOTIC STRESS; PRIORITY JOURNAL; REVIEW; RNA STABILITY; TRANSLATION INITIATION; TRANSLATION REGULATION; UNFOLDED PROTEIN RESPONSE;

EID: 84875794702     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/imr.12052     Document Type: Review

References (128)

1. Tani H, et al. Genome-wide determination of RNA stability reveals hundreds of short-lived noncoding transcripts in mammals. Genome Res 2012;22:947-956.
2. Selinger DW, Saxena RM, Cheung KJ, Church GM, Rosenow C. Global RNA Half-Life Analysis in Escherichia coli reveals positional patterns of transcript degradation. Genome Res 2003;13:216-223.
3. Richter K, Haslbeck M, Buchner J. The heat shock response: life on the verge of death. Mol Cell 2010;40:253-266.
4. Green DR, Kroemer G. Cytoplasmic functions of the tumour suppressor p53. Nature 2009;458:1127-1130.
5. Lord CJ, Ashworth A. The DNA damage response and cancer therapy. Nature 2012;481:287-294.
6. Merksamer PI, Papa FR. The UPR and cell fate at a glance. J Cell Sci 2010;123:1003-1006.
7. Rutkowski DT, Kaufman RJ. That which does not kill me makes me stronger: adapting to chronic ER stress. Trends Biochem Sci 2007;32:469-476.
8. Papa FR. Endoplasmic reticulum stress, pancreatic β-cell degeneration, and diabetes. Cold Spring Harb Perspect Med 2012;2:a007666.
9. Taylor RC, Cullen SP, Martin SJ. Apoptosis: controlled demolition at the cellular level. Nat Rev Mol Cell Biol 2008;9:231-241.
10. Danial NN, Korsmeyer SJ. Cell death: critical control points. Cell 2004;116:205-219.
11. Llambi F, et al. A unified model of mammalian BCL-2 protein family interactions at the mitochondria. Mol Cell 2011;44:517-531.
12. Riedl SJ, Shi Y. Molecular mechanisms of caspase regulation during apoptosis. Nat Rev Mol Cell Biol 2004;5:897-907.
13. Bouchier-Hayes L, Green DR. Caspase-2: the orphan caspase. Cell Death Differe 2012;19:51-57.
14. Thiery J, et al. Perforin pores in the endosomal membrane trigger the release of endocytosed granzyme B into the cytosol of target cells. Nat Immunol 2011;12:770-777.
15. Chowdhury D, Lieberman J. Death by a thousand cuts: granzyme pathways of programmed cell death. Annu Rev Immunol 2008;26:389-420.
16. Bots M, Medema JP. Granzymes at a glance. J Cell Sci 2006;119:5011-5014.
17. Fan Z, et al. Cleaving the oxidative repair protein Ape1 enhances cell death mediated by granzyme A. Nat Immunol 2003;4:145-153.
18. Jans DA, Jans P, Briggs LJ, Sutton V, Trapani JA. Nuclear transport of granzyme B (Fragmentin-2). J Biol Chem 1996;271:30781-30789.
19. Albeck JG, Burke JM, Aldridge BB, Zhang M, Lauffenburger DA, Sorger PK. Quantitative Analysis of Pathways Controlling Extrinsic Apoptosis in Single Cells. Mol Cell 2008;30:11-25.
20. Morley SJ, Jeffrey I, Bushell M, Pain VM, Clemens MJ. Differential requirements for caspase-8 activity in the mechanism of phosphorylation of eIF2α, cleavage of eIF4GI and signaling events associated with the inhibition of protein synthesis in apoptotic Jurkat T cells. FEBS Let 2000;477:229-236.
21. Jurica MS, Moore MJ. Pre-mRNA splicing: awash in a sea of proteins. Mol Cell 2003;12:5-14.
22. Hoskins AA, Moore MJ. The spliceosome: a flexible, reversible macromolecular machine. Trends Biochem Sci 2012;37:179-188.
23. Wang Z, Burge CB. Splicing regulation: from a parts list of regulatory elements to an integrated splicing code. RNA 2008;14:802-813.
24. Spies N, Nielsen CB, Padgett RA, Burge CB. Biased chromatin signatures around polyadenylation sites and exons. Mol Cell 2009;36:245-254.
25. Nilsen TW, Graveley BR. Expansion of the eukaryotic proteome by alternative splicing. Nature 2010;463:457-463.
26. Biamonti G, Caceres JF. Cellular stress and RNA splicing. Trends Biochem Sci 2009;34:146-153.
27. Zhu J, Mayeda A, Krainer AR. Exon identity established through differential antagonism between exonic splicing silencer-bound hnRNP A1 and enhancer-bound SR proteins. Mol Cell 2001;8:1351-1361.
28. Mayeda A, Krainer AR. Regulation of alternative pre-mRNA splicing by hnRNP A1 and splicing factor SF2. Cell 1992;68:365-375.
29. Konig J, et al. iCLIP reveals the function of hnRNP particles in splicing at individual nucleotide resolution. Nat Struct Mol Biol 2010;17:909-915.
30. Huelga SC, et al. Integrative genome-wide analysis reveals cooperative regulation of alternative splicing by hnRNP proteins. Cell Rep 2012;1:167-178.
31. Martinez-Contreras R, Fisette J-F, Nasim FH, Madden R, Cordeau M, Chabot B. Intronic binding sites for hnRNP A/B and hnRNP F/H proteins stimulate pre-mRNA splicing. PLoS Biol 2006;4:e21.
32. Wang ET, et al. Alternative isoform regulation in human tissue transcriptomes. Nature 2008;456:470-476.
33. Yeo G, Holste D, Kreiman G, Burge CB. Variation in alternative splicing across human tissues. Genome Biol 2004;5:R74.
34. Bond U. Heat shock but not other stress inducers leads to the disruption of a sub-set of snRNPs and inhibition of in vitro splicing in HeLa cells. EMBO J 1988;7:3509.
35. Shin C, Feng Y, Manley JL. Dephosphorylated SRp38 acts as a splicing repressor in response to heat shock. Nature 2004;427:553-558.
36. Shi Y, Nishida K, Giammartino DCD, Manley JL. Heat shock-induced SRSF10 dephosphorylation displays thermotolerance mediated by Hsp27. Mol Cell Biol 2011;31:458-465.
37. Mitchell JA, Fraser P. Transcription factories are nuclear subcompartments that remain in the absence of transcription. Genes Dev 2008;22:20-25.
38. Tilgner H, et al. Deep sequencing of subcellular RNA fractions shows splicing to be predominantly co-transcriptional in the human genome but inefficient for lncRNAs. Genome Res 2012;22:1616-1625.
39. Nevo Y, et al. Genome-wide activation of latent donor splice sites in stress and disease. Nucl Acids Res 2012;40:10980-10994.
40. Rebbapragada I, Lykke-Andersen J. Execution of nonsense-mediated mRNA decay: what defines a substrate? Curr Opin Cell Biol 2009;21:394-402.
41. Rajani DK, Walch M, Martinvalet D, Thomas MP, Lieberman J. Alterations in RNA processing during immune-mediated programmed cell death. Proc Natl Acad Sci USA 2012;109:8688-8693.
42. Gazave E, Marqués-Bonet T, Fernando O, Charlesworth B, Navarro A. Patterns and rates of intron divergence between humans and chimpanzees. Genome Biol 2007;8:R21.
43. Xiao SH, Manley JL. Phosphorylation of the ASF/SF2 RS domain affects both protein-protein and protein-RNA interactions and is necessary for splicing. Genes Dev 1997;11:334-344.
44. de la Mata M, et al. A slow RNA polymerase II affects alternative splicing in vivo. Mol Cell 2003;12:525-532.
45. Proudfoot NJ, Furger A, Dye MJ. Integrating mRNA processing with transcription. Cell 2002;108:501-512.
46. Buratowski S. Connections between mRNA 3′ end processing and transcription termination. Curr Opin Cell Biol 2005;17:257-261.
47. Kornblihtt AR, Mata MDL, Fededa JP, Muñoz MJ, Nogués G. Multiple links between transcription and splicing. RNA 2004;10:1489-1498.
48. Muñoz MJ, et al. DNA damage regulates alternative splicing through inhibition of RNA polymerase II elongation. Cell 2009;137:708-720.
49. Ip JY, et al. Global impact of RNA polymerase II elongation inhibition on alternative splicing regulation. Genome Res 2011;21:390-401.
50. Das R, et al. SR proteins function in coupling RNAP II transcription to pre-mRNA splicing. Mol Cell 2007;26:867-881.
51. van der Houven van Oordt W, et al. The Mkk3/6-p38-Signaling Cascade Alters the Subcellular Distribution of Hnrnp A1 and Modulates Alternative Splicing Regulation. J Cell Biol 2000;149:307-316.
52. Dutertre M, et al. Cotranscriptional exon skipping in the genotoxic stress response. Nat Struct Mol Biol 2010;17:1358-1366.
53. Wei W-J, et al. YB-1 binds to CAUC motifs and stimulates exon inclusion by enhancing the recruitment of U2AF to weak polypyrimidine tracts. Nucl Acids Res 2012;40:8622-8636.
54. Merdzhanova G, et al. E2F1 controls alternative splicing pattern of genes involved in apoptosis through upregulation of the splicing factor SC35. Cell Death Differ 2008;15:1815-1823.
55. Shkreta L, Michelle L, Toutant J, Tremblay ML, Chabot B. The DNA Damage Response Pathway Regulates the Alternative Splicing of the Apoptotic Mediator Bcl-x. J Biol Chem 2011;286:331-340.
56. Munchel SE, Shultzaberger RK, Takizawa N, Weis K. Dynamic profiling of mRNA turnover reveals gene-specific and system-wide regulation of mRNA decay. Mol Biol Cell 2011;22:2787-2795.
57. Rabani M, et al. Metabolic labeling of RNA uncovers principles of RNA production and degradation dynamics in mammalian cells. Nat Biotech 2011;29:436-442.
58. Schwerk C, Schulze-Osthoff K. Regulation of apoptosis by alternative pre-mRNA splicing. Mol Cell 2005;19:1-13.
59. Edmond V, et al. Acetylation and phosphorylation of SRSF2 control cell fate decision in response to cisplatin. EMBO J 2011;30:510-523.
60. Hua Y, Vickers TA, Okunola HL, Bennett CF, Krainer AR. Antisense masking of an hnRNP A1/A2 intronic splicing silencer corrects SMN2 splicing in transgenic mice. Am J Human Gen 2008;82:834-848.
61. Holcik M, Sonenberg N. Translational control in stress and apoptosis. Nat Rev Mol Cell Biol 2005;6:318-327.
62. Morley SJ, Coldwell MJ, Clemens MJ. Initiation factor modifications in the preapoptotic phase. Cell Death Differ 2005;12:571-584.
63. Wouters BG, van den Beucken T, Magagnin MG, Koritzinsky M, Fels D, Koumenis C. Control of the hypoxic response through regulation of mRNA translation. Sem Cell Dev Biol 2005;16:487-501.
64. Wek RC, Jiang H-Y, Anthony TG. Coping with stress: eIF2 kinases and translational control. Biochem Soc Trans 2006;34:7.
65. Harding HP, et al. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell 2003;11:619-633.
66. Gingras A-C, Raught B, Sonenberg N. Regulation of translation initiation by FRAP/mTOR. Genes Dev 2001;15:807-826.
67. Silvera D, Formenti SC, Schneider RJ. Translational control in cancer. Nature Rev Cancer 2010;10:254-266.
68. Cuesta R, Laroia G, Schneider RJ. Chaperone Hsp27 inhibits translation during heat shock by binding eIF4G and facilitating dissociation of cap-initiation complexes. Genes Dev 2000;14:1460-1470.
69. Yamasaki S, Ivanov P, Hu G, Anderson P. Angiogenin cleaves tRNA and promotes stress-induced translational repression. J Cell Biol 2009;185:35-42.
70. Ivanov P, Emara MM, Villen J, Gygi SP, Anderson P. Angiogenin-Induced tRNA Fragments Inhibit Translation Initiation. Mol Cell 2011;43:613-623.
71. Bevilacqua E, et al. eIF2alpha phosphorylation tips the balance to apoptosis during osmotic stress. J Biol Chem 2010;285:17098-17111.
72. Allemand E, Guil S, Myers M, Moscat J, Cáceres JF, Krainer AR. Regulation of heterogenous nuclear ribonucleoprotein A1 transport by phosphorylation in cells stressed by osmotic shock. Proc Natl Acad Sci USA 2005;102:3605-3610.
73. Cammas A, et al. Cytoplasmic relocalization of heterogeneous nuclear ribonucleoprotein A1 controls translation initiation of specific mRNAs. Mol Biol Cell 2007;18:5048-5059.
74. Teske BF, et al. The eIF2 kinase PERK and the integrated stress response facilitate activation of ATF6 during endoplasmic reticulum stress. Mol Biol Cell 2011;22:4390-4405.
75. Bi M, et al. ER stress-regulated translation increases tolerance to extreme hypoxia and promotes tumor growth. EMBO J 2005;24:3470-3481.
76. Yamaguchi H, Wang H-G. CHOP is involved in endoplasmic reticulum stress-induced apoptosis by enhancing DR5 expression in human carcinoma cells. J Biol Chem 2004;279:45495-45502.
77. Puthalakath H, et al. ER Stress Triggers Apoptosis by Activating BH3-Only Protein Bim. Cell 2007;129:1337-1349.
78. Zinszner H, et al. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev 1998;12:982-995.
79. Palam LR, Baird TD, Wek RC. Phosphorylation of eIF2 facilitates ribosomal bypass of an inhibitory upstream ORF to enhance CHOP translation. J Biol Chem 2011;286:10939-10949.
80. Szegezdi E, Logue SE, Gorman AM, Samali A. Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep 2006;7:880-885.
81. Harding HP, et al. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 2000;6:1099-1108.
82. Fawcett TW, Martindale JL, Guyton KZ, Hai T, Holbrook NJ. Complexes containing activating transcription factor (ATF)/cAMP-responsive-element-binding protein (CREB) interact with the CCAAT/enhancer-binding protein (C/EBP)-ATF composite site to regulate Gadd153 expression during the stress response. Biochem. J 1999;339:135-141.
83. Ingolia NT, Ghaemmaghami S, Newman JRS, Weissman JS. Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 2009;324:218-223.
84. Clemens MJ, Bushell M, Morley SJ. Degradation of eukaryotic polypeptide chain initiation factor (eIF) 4G in response to induction of apoptosis in human lymphoma cell lines. Oncogene 1998;17:2921-2931.
85. Saelens X, Kalai M, Vandenabeele P. Translation inhibition in apoptosis. J Biol Chem 2001;276:41620-41628.
86. Bushell M, Stoneley M, Sarnow P, Willis AE. Translation inhibition during the induction of apoptosis: RNA or protein degradation? Biochem Soc Trans 2004;32:606-610.
87. Bushell M, et al. Polypyrimidine Tract Binding Protein Regulates IRES-Mediated Gene Expression during Apoptosis. Mol Cell 2006;23:401-412.
88. Kalai M, et al. The caspase-generated fragments of PKR cooperate to activate full-length PKR and inhibit translation. Cell Death Differ 2007;14:1050-1059.
89. Jeffrey IW, Bushell M, Tilleray VJ, Morley S, Clemens MJ. Inhibition of protein synthesis in apoptosis differential requirements by the tumor necrosis factor α family and a DNA-damaging agent for caspases and the double-stranded RNA-dependent protein kinase. Cancer Res 2002;62:2272-2280.
90. Clemens MJ, Bushell M, Jeffrey IW, Pain VM, Morley SJ. Translation initiation factor modifications and the regulation of protein synthesis in apoptotic cells. Cell Death Differ 2000;7:603-615.
91. Marissen WE, Lloyd RE. Eukaryotic translation initiation factor 4G is targeted for proteolytic cleavage by caspase 3 during inhibition of translation in apoptotic cells. Mol Cell Biol 1998;18:7565-7574.
92. Spencer SL, Gaudet S, Albeck JG, Burke JM, Sorger PK. Non-genetic origins of cell-to-cell variability in TRAIL-induced apoptosis. Nature 2009;459:428-432.
93. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009;136:215-233.
94. Fabian MR, Sonenberg N. The mechanics of miRNA-mediated gene silencing: a look under the hood of miRISC. Nat Struct Mol Biol 2012;19:586-593.
95. Thomas M, Lieberman J, Lal A. Desperately seeking microRNA targets. Nat Struct Mol Biol 2010;17:1169-1174.
96. Mendell JT, Olson EN. MicroRNAs in stress signaling and human disease. Cell 2012;148:1172-1187.
97. Cimmino A, et al. miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc Natl Acad Sci USA 2005;102:13944-13949.
98. Hullinger TG, et al. Inhibition of miR-15 protects against cardiac ischemic injury. Circulation Res 2012;110:71-81.
99. Aurora AB, et al. MicroRNA-214 protects the mouse heart from ischemic injury by controlling Ca2 + overload and cell death. J Clin Invest 2012;122:1222-1232.
100. Chang T-C, et al. Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol Cell 2007;26:745-752.
101. He L, et al. A microRNA component of the p53 tumour suppressor network. Nature 2007;447:1130-1134.
102. Tarasov V, et al. Differential regulation of microRNAs by p53 revealed by massively parallel sequencing: miR-34a is a p53 target that induces apoptosis and G1-arrest. Cell Cycle 2007;6:1586-1593.
103. Bommer GT, et al. p53-mediated activation of miRNA34 candidate tumor-suppressor genes. Curr Biol 2007;17:1298-1307.
104. Raver-Shapira N, et al. Transcriptional activation of miR-34a contributes to p53-mediated apoptosis. Mol Cell 2007;26:731-743.
105. Lal A, et al. Capture of microRNA-bound mRNAs identifies the tumor suppressor miR-34a as a regulator of growth factor signaling. PLoS Genet 2011;7:e1002363.
106. Concepcion CP, et al. Intact p53-dependent responses in miR-34-deficient mice. PLoS Genet 2012;8:e1002797.
107. Navarro F, et al. miR-34a contributes to megakaryocytic differentiation of K562 cells independently of p53. Blood 2009;114:2181-2192.
108. Gantier MP, et al. Analysis of microRNA turnover in mammalian cells following Dicer1 ablation. Nucl Acids Res 2011;39:5692-5703.
109. Upton J-P, et al. Caspase-2 cleavage of BID is a critical apoptotic signal downstream of endoplasmic reticulum stress. Mol Cell Biol 2008;28:3943-3951.
110. Guo H, Ingolia NT, Weissman JS, Bartel DP. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 2010;466:835-840.
111. Han D, et al. IRE1α kinase activation modes control alternate endoribonuclease outputs to determine divergent cell fates. Cell 2009;138:562-575.
112. Upton J-P, et al. IRE1α cleaves select microRNAs during ER stress to derepress translation of proapoptotic caspase-2. Science 2012;338:818-822.
113. Chutkow WA, et al. Deletion of the α-arrestin protein Txnip in mice promotes adiposity and adipogenesis while preserving insulin sensitivity. Diabetes 2010;59:1424-1434.
114. Oslowski CM, et al. Thioredoxin-interacting protein mediates ER stress-induced β cell death through initiation of the inflammasome. Cell Metab 2012;16:265-273.
115. Ehses JA, et al. IL-1 antagonism reduces hyperglycemia and tissue inflammation in the type 2 diabetic GK rat. Proc Natl Acad Sci USA 2009;106:13998-14003.
116. Lerner AG, et al. IRE1α induces thioredoxin-interacting protein to activate the NLRP3 inflammasome and promote programmed cell death under irremediable ER stress. Cell Metab 2012;16:250-264.
117. Fritz D, Bergman N, Kilpatrick W, Wilusz C, Wilusz J. Messenger RNA decay in mammalian cells. Cell Biochem Biophys 2004;41:265-277.
118. Schoenberg DR, Maquat LE. Regulation of cytoplasmic mRNA decay. Nat Rev Genetics 2012;13:246.
119. Hollien J, Weissman JS. Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 2006;313:104-107.
120. Hollien J, Lin JH, Li H, Stevens N, Walter P, Weissman JS. Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J Cell Biol 2009;186:323-331.
121. Bouchecareilh M, Higa A, Fribourg S, Moenner M, Chevet E. Peptides derived from the bifunctional kinase/RNase enzyme IRE1α modulate IRE1α activity and protect cells from endoplasmic reticulum stress. FASEB J 2011;25:3115-3129.
122. Anderson P, Kedersha N. RNA granules: post-transcriptional and epigenetic modulators of gene expression. Nat Rev Mol Cell Biol 2009;10:430-436.
123. Buchan JR, Parker R. Eukaryotic stress granules: the ins and outs of translation. Mol Cell 2009;36:932-941.
124. Balagopal V, Parker R. Polysomes, P bodies and stress granules: states and fates of eukaryotic mRNAs. Curr Opin Cell Biol 2009;21:403-408.
125. Kedersha N, Anderson P. Mammalian stress granules and processing bodies. Meth. Enzymol. 2007;431:61-81.
126. Stöhr N, et al. ZBP1 regulates mRNA stability during cellular stress. J Cell Biol 2006;175:527-534.
127. Degen WG, Pruijn GJ, Raats JM, van Venrooij WJ. Caspase-dependent cleavage of nucleic acids. Cell Death Differ 2000;7:616-627.
128. Prete MD, Robles MS, Guáo A, Martínez-A C, Izquierdo M, Garcia-Sanz JA. Degradation of cellular mRNA is a general early apoptosis-induced event. FASEB J. 2002;16:2003-2005.