Angiogenin-cleaved tRNA halves interact with cytochrome c, protecting cells from apoptosis during osmotic stress

Molecular and Cellular Biology

Volumn 34, Issue 13, 2014, Pages 2450-2463

  Saikia, Mridusmita ^a   Jobava, Raul ^a   Parisien, Marc ^b   Putnam, Andrea ^a,c   Krokowski, Dawid ^a   Gao, Xing Huang ^a   Guan, Bo Jhih ^a   Yuan, Yiyuan ^a   Jankowsky, Eckhard ^a,c   Feng, Zhaoyang ^a   Hu, Guo fu ^d   Pusztai Carey, Marianne ^a   Gorla, Madhavi ^e   Sepuri, Naresh Babu V ^e   Pan, Tao ^b   Hatzoglou, Maria ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c CASE WESTERN RESERVE UNIVERSITY   (United States)

^d TUFTS MEDICAL CENTER   (United States)

^e UNIVERSITY OF HYDERABAD   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENIN; APOPTOSOME; APOPTOTIC PROTEASE ACTIVATING FACTOR 1; CASPASE 3; CASPASE 9; CYTOCHROME C; PROCASPASE 3; PROCASPASE 9; PROTEIN BCL 2; PROTEIN BCL XL; RIBONUCLEOPROTEIN; RNA; TRANSFER RNA; TUBULIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; BRAIN CELL; CELL PROTECTION; CELL STRESS; CELL SURVIVAL; CELL VIABILITY; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME RELEASE; FIBROBLAST; HYPEROSMOTIC STRESS; IN VITRO STUDY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN RNA BINDING; RNA CLEAVAGE;

ANIMALS; APOPTOSIS; APOPTOSOMES; APOPTOTIC PROTEASE-ACTIVATING FACTOR 1; BASE SEQUENCE; CASPASE 3; CASPASE 9; CELL SURVIVAL; CELLS, CULTURED; CYTOCHROMES C; ELECTROPHORETIC MOBILITY SHIFT ASSAY; FIBROBLASTS; MICE; MITOCHONDRIA; NEURONS; OSMOTIC PRESSURE; RIBONUCLEASE, PANCREATIC; RIBONUCLEOPROTEINS; RNA CLEAVAGE; RNA, TRANSFER; SEQUENCE ANALYSIS, RNA;

EID: 84901766882     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00136-14     Document Type: Article

References (55)

1. Tait SW, Green DR. 2010. Mitochondria and cell death: outer membrane permeabilization and beyond. Nat. Rev. Mol. Cell Biol. 11:621-632. http://dx.doi.org/10.1038/nrm2952.
2. Li P, Nijhawan D, Wang X. 2004. Mitochondrial activation of apoptosis. Cell 116:S57-S59. http://dx.doi.org/10.1016/S0092-8674(04)00031-5.
3. Reubold TF, Eschenburg S. 2012. A molecular view on signal transduction by the apoptosome. Cell Signal. 24:1420-1425. http://dx.doi.org/10.1016/j.cellsig.2012.03.007.
4. Zou H, Li Y, Liu X, Wang X. 1999. An APAF-1.cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J. Biol. Chem. 274:11549-11556. http://dx.doi.org/10.1074/jbc.274.17.11549.
5. Adams JM, Cory S. 2002. Apoptosomes: engines for caspase activation. Curr. Opin. Cell Biol. 14:715-720. http://dx.doi.org/10.1016/S0955-0674(02)00381-2.
6. Jiang X, Wang X. 2000. Cytochrome c promotes caspase-9 activation by inducing nucleotide binding to Apaf-1. J. Biol. Chem. 275:31199-31203. http://dx.doi.org/10.1074/jbc.C000405200.
7. Purring-Koch C, Mclendon G. 2000. Cytochrome c binding to Apaf-1: the effects of dATP and ionic strength. Proc. Natl. Acad. Sci. U. S. A. 97:11928-11931. http://dx.doi.org/10.1073/pnas.220416197.
8. Kurokawa M, Zhao C, Reya T, Kornbluth S. 2008. Inhibition of apoptosome formation by suppression of Hsp90β phosphorylation in tyrosine kinase-induced leukemias. Mol. Cell. Biol. 28:5494-5506. http://dx.doi.org/10.1128/MCB.00265-08.
9. Pandey P, Saleh A, Nakazawa A, Kumar S, Srinivasula SM, Kumar V, Weichselbaum R, Nalin C, Alnemri ES, Kufe D, Kharbanda S. 2000. Negative regulation of cytochrome c-mediated oligomerization of Apaf-1 and activation of procaspase-9 by heat shock protein 90. EMBO J. 19: 4310-4322. http://dx.doi.org/10.1093/emboj/19.16.4310.
10. Favaloro B, Allocati N, Graziano V, Di Ilio C, De Laurenzi V. 2012. Role of apoptosis in disease. Aging (Albany, NY) 4:330-349.
11. Iwasaki Y, Ikeda K, Kinoshita M. 2002. Molecular and cellular mechanism of glutamate receptors in relation to amyotrophic lateral sclerosis. Curr. Drug Targets CNS Neurol. Disord. 1:511-518. http://dx.doi.org/10.2174/1568007023339021.
12. Kieran D, Sebastia J, Greenway MJ, King MA, Connaughton D, Concannon CG, Fenner B, Hardiman O, Prehn JH. 2008. Control of motoneuron survival by angiogenin. J. Neurosci. 28:14056-14061. http://dx.doi.org/10.1523/JNEUROSCI.3399-08.2008.
13. Aparicio-Erriu IM, Prehn JH. 2012. Molecular mechanisms in amyotrophic lateral sclerosis: the role of angiogenin, a secreted RNase. Front. Neurosci. 6:167. http://dx.doi.org/10.3389/fnins.2012.00167.
14. Thiyagarajan N, Ferguson R, Subramanian V, Acharya KR. 2012. Structural and molecular insights into the mechanism of action of human angiogenin-ALS variants in neurons. Nat. Commun. 3:1121. http://dx.doi.org/10.1038/ncomms2126.
15. Acharya KR, Shapiro R, Allen SC, Riordan JF, Vallee BL. 1994. Crystal structure of human angiogenin reveals the structural basis for its functional divergence from ribonuclease. Proc. Natl. Acad. Sci. U. S. A. 91: 2915-2919. http://dx.doi.org/10.1073/pnas.91.8.2915.
16. Li S, Hu GF. 2012. Emerging role of angiogenin in stress response and cell survival under adverse conditions. J. Cell Physiol. 227:2822-2826. http://dx.doi.org/10.1002/jcp.23051.
17. Tello-Montoliu A, Patel JV, Lip GY. 2006. Angiogenin: a review of the pathophysiology and potential clinical applications. J. Thromb. Haemost. 4:1864-1874. http://dx.doi.org/10.1111/j.1538-7836.2006.01995.x.
18. Yamasaki S, Ivanov P, Hu GF, Anderson P. 2009. Angiogenin cleaves tRNA and promotes stress-induced translational repression. J. Cell Biol. 185:35-42. http://dx.doi.org/10.1083/jcb.200811106.
19. Thompson DM, Parker R. 2009. Stressing out over tRNA cleavage. Cell 138:215-219. http://dx.doi.org/10.1016/j.cell.2009.07.001.
20. Saikia M, Krokowski D, Guan BJ, Ivanov P, Parisien M, Hu GF, Anderson P, Pan T, Hatzoglou M. 2012. Genome-wide identification and quantitative analysis of cleaved tRNA fragments induced by cellular stress. J. Biol. Chem. 287:42708-42725. http://dx.doi.org/10.1074/jbc.M112.371799.
21. Fu H, Feng J, Liu Q, Sun F, Tie Y, Zhu J, Xing R, Sun Z, Zheng X. 2009. Stress induces tRNA cleavage by angiogenin in mammalian cells. FEBS Lett. 583:437-442. http://dx.doi.org/10.1016/j.febslet.2008.12.043.
22. Thompson DM, Lu C, Green PJ, Parker R. 2008. tRNA cleavage is a conserved response to oxidative stress in eukaryotes. RNA 14:2095-2103. http://dx.doi.org/10.1261/rna.1232808.
23. Thompson DM, Parker R. 2009. The RNase Rny1p cleaves tRNAs and promotes cell death during oxidative stress in Saccharomyces cerevisiae. J. Cell Biol. 185:43-50. http://dx.doi.org/10.1083/jcb.200811119.
24. Lee SR, Collins K. 2005. Starvation-induced cleavage of the tRNA anticodon loop in Tetrahymena thermophila. J. Biol. Chem. 280:42744-42749. http://dx.doi.org/10.1074/jbc.M510356200.
25. Bevilacqua E, Wang X, Majumder M, Gaccioli F, Yuan CL, Wang C, Zhu X, Jordan LE, Scheuner D, Kaufman RJ, Koromilas AE, Snider MD, Holcik M, Hatzoglou M. 2010. eIF2α phosphorylation tips the balance to apoptosis during osmotic stress. J. Biol. Chem. 285:17098-17111. http://dx.doi.org/10.1074/jbc.M110.109439.
26. Burg MB, Ferraris JD, Dmitrieva NI. 2007. Cellular response to hyperosmotic stresses. Physiol. Rev. 87:1441-1474. http://dx.doi.org/10.1152/physrev.00056.2006.
27. Ivanov P, Emara MM, Villen J, Gygi SP, Anderson P. 2011. Angiogenininduced tRNA fragments inhibit translation initiation. Mol. Cell 43:613-623. http://dx.doi.org/10.1016/j.molcel.2011.06.022.
28. Mei Y, Stonestrom A, Hou YM, Yang X. 2010. Apoptotic regulation and tRNA. Protein Cell 1:795-801. http://dx.doi.org/10.1007/s13238-010-0107-x.
29. Mei Y, Yong J, Liu H, Shi Y, Meinkoth J, Dreyfuss G, Yang X. 2010. tRNA binds to cytochrome c and inhibits caspase activation. Mol. Cell 37:668-678. http://dx.doi.org/10.1016/j.molcel.2010.01.023.
30. Suryanarayana T, Uppala JK, Garapati UK. 2012. Interaction of cytochrome c with tRNA and other polynucleotides. Mol. Biol. Rep. 39:9187-9191. http://dx.doi.org/10.1007/s11033-012-1791-9.
31. Chan PP, Lowe TM. 2009. GtRNAdb: a database of transfer RNA genes detected in genomic sequence. Nucleic Acids Res. 37:D93-D97. http://dx.doi.org/10.1093/nar/gkn787.
32. Gorla M, Sepuri NB. 2014. Perturbation of apoptosis upon binding of tRNA to the heme domain of cytochrome c. Apoptosis 19:259-268. http://dx.doi.org/10.1007/s10495-013-0915-6.
33. Majumder M, Huang C, Snider MD, Komar AA, Tanaka J, Kaufman RJ, Krokowski D, Hatzoglou M. 2012. A novel feedback loop regulates the response to endoplasmic reticulum stress via the cooperation of cytoplasmic splicing and mRNA translation. Mol. Cell. Biol. 32:992-1003. http://dx.doi.org/10.1128/MCB.06665-11.
34. Skorupa A, King MA, Aparicio IM, Dussmann H, Coughlan K, Breen B, Kieran D, Concannon CG, Marin P, Prehn JH. 2012. Motoneurons secrete angiogenin to induce RNA cleavage in astroglia. J. Neurosci. 32: 5024-5038. http://dx.doi.org/10.1523/JNEUROSCI.6366-11.2012.
35. Jeon US, Kim JA, Sheen MR, Kwon HM. 2006. How tonicity regulates genes: story of TonEBP transcriptional activator. Acta Physiol. (Oxf.) 187: 241-247. http://dx.doi.org/10.1111/j.1748-1716.2006.01551.x.
36. Yang J, Liu X, Bhalla K, Kim CN, Ibrado AM, Cai J, Peng TI, Jones DP, Wang X. 1997. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275:1129-1132. http://dx.doi.org/10.1126/science.275.5303.1129.
37. Khandekar N, Willcox MD, Shih S, Simmons P, Vehige J, Garrett Q. 2013. Decrease in hyperosmotic stress-induced corneal epithelial cell apoptosis by L-carnitine. Mol. Vis. 19:1945-1956.
38. Yoshida H, Kong YY, Yoshida R, Elia AJ, Hakem A, Hakem R, Pen-ninger JM, Mak TW. 1998. Apaf1 is required for mitochondrial pathways of apoptosis and brain development. Cell 94:739-750. http://dx.doi.org/10.1016/S0092-8674(00)81733-X.
39. Goldstein JC, Munoz-Pinedo C, Ricci JE, Adams SR, Kelekar A, Schuler M, Tsien RY, Green DR. 2005. Cytochrome c is released in a single step during apoptosis. Cell Death Differ. 12:453-462. http://dx.doi.org/10.1038/sj.cdd.4401596.
40. Novoa EM, Pavon-Eternod M, Pan T, Ribas de Pouplana L. 2012. A role for tRNA modifications in genome structure and codon usage. Cell 149: 202-213. http://dx.doi.org/10.1016/j.cell.2012.01.050.
41. Phizicky EM, Hopper AK. 2010. tRNA biology charges to the front. Genes Dev. 24:1832-1860. http://dx.doi.org/10.1101/gad.1956510.
42. El Yacoubi B, Bailly M, de Crecy-Lagard V. 2012. Biosynthesis and function of posttranscriptional modifications of transfer RNAs. Annu. Rev. Genet. 46: 69-95. http://dx.doi.org/10.1146/annurev-genet-110711-155641.
43. Von Ahsen O, Waterhouse NJ, Kuwana T, Newmeyer DD, Green DR. 2000. The "harmless" release of cytochrome c. Cell Death Differ. 7:1192-1199. http://dx.doi.org/10.1038/sj.cdd.4400782.
44. Emara MM, Ivanov P, Hickman T, Dawra N, Tisdale S, Kedersha N, Hu GF, Anderson P. 2010. Angiogenin-induced tRNA-derived stressinduced RNAs promote stress-induced stress granule assembly. J. Biol. Chem. 285:10959-10968. http://dx.doi.org/10.1074/jbc.M109.077560.
45. Czech A, Wende S, Morl M, Pan T, Ignatova Z. 2013. Reversible and rapid transfer-RNA deactivation as a mechanism of translational repression in stress. PLoS Genet. 9:e1003767. http://dx.doi.org/10.1371/journal.pgen.1003767.
46. Iordanov MS, Ryabinina OP, Wong J, Dinh TH, Newton DL, Rybak SM, Magun BE. 2000. Molecular determinants of apoptosis induced by the cytotoxic ribonuclease onconase: evidence for cytotoxic mechanisms different from inhibition of protein synthesis. Cancer Res. 60:1983-1994.
47. Machnicka MA, Milanowska K, Osman Oglou O, Purta E, Kurkowska M, Olchowik A, Januszewski W, Kalinowski S, Dunin-Horkawicz S, Rother KM, Helm M, Bujnicki JM, Grosjean H. 2013. MODOMICS: a database of RNA modification pathways-2013 update. Nucleic Acids Res. 41:D262-D267. http://dx.doi.org/10.1093/nar/gks1007.
48. Saikia M, Fu Y, Pavon-Eternod M, He C, Pan T. 2010. Genome-wide analysis of N1-methyl-adenosine modification in human tRNAs. RNA 16:1317-1327. http://dx.doi.org/10.1261/rna.2057810.
49. Sadagopan S, Veettil MV, Chakraborty S, Sharma-Walia N, Paudel N, Bottero V, Chandran B. 2012. Angiogenin functionally interacts with p53 and regulates p53-mediated apoptosis and cell survival. Oncogene 31: 4835-4847. http://dx.doi.org/10.1038/onc.2011.648.
50. Li S, Yu W, Kishikawa H, Hu GF. 2010. Angiogenin prevents serum withdrawal-induced apoptosis of P19 embryonal carcinoma cells. FEBS J. 277:3575-3587. http://dx.doi.org/10.1111/j.1742-4658.2010.07766.x.
51. Li S, Yu W, Hu GF. 2012. Angiogenin inhibits nuclear translocation of apoptosis inducing factor in a Bcl-2-dependent manner. J. Cell Physiol. 227:1639-1644. http://dx.doi.org/10.1002/jcp.22881.
52. Yuan S, Yu X, Asara JM, Heuser JE, Ludtke SJ, Akey CW. 2011. The holo-apoptosome: activation of procaspase-9 and interactions with caspase-3. Structure 19:1084-1096. http://dx.doi.org/10.1016/j.str.2011.07.001.
53. Bratton SB, Walker G, Srinivasula SM, Sun XM, Butterworth M, Alnemri ES, Cohen GM. 2001. Recruitment, activation and retention of caspases-9 and-3 by Apaf-1 apoptosome and associated XIAP complexes. EMBO J. 20:998-1009. http://dx.doi.org/10.1093/emboj/20.5.998.
54. Mcilwain DR, Berger T, Mak TW. 2013. Caspase functions in cell death and disease. Cold Spring Harb. Perspect. Biol. 5:a008656. http://dx.doi.org/10.1101/cshperspect.a008656.
55. National Institutes of Health. 1985. Guide for the care and use of laboratory animals. NIH publication 85-23. National Institutes of Health, Bethesda, MD.