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The Translational Regulators GCN-1 and ABCF-3 Act Together to Promote Apoptosis in
Apoptosis, also referred to as programmed cell death, is a crucial cellular process that eliminates unwanted cells during animal development and tissue homeostasis. Abnormal regulation of apoptosis can cause developmental defects and a variety of other human disorders, including cancer, neurodegenerative diseases and autoimmune diseases. Therefore, it is important to identify regulatory mechanisms that control apoptosis. Previous studies have demonstrated that the transcriptional induction of apoptotic genes can be crucial to initiating an apoptotic program. Less is known about translational controls of apoptosis. Here we report that the evolutionarily conserved C. elegans translational regulators GCN-1 and ABCF-3 promote apoptosis generally and act independently of the anti-apoptotic BCL-2 homolog CED-9. GCN-1 and ABCF-3 physically interact and maintain the phosphorylation level of eukaryotic initiation factor 2α, suggesting that GCN-1 and ABCF-3 act together to regulate the initiation of translation. We propose that the translational regulators GCN-1 and ABCF-3 maternally contribute to the proper execution of the apoptotic program.
Vyšlo v časopise: The Translational Regulators GCN-1 and ABCF-3 Act Together to Promote Apoptosis in. PLoS Genet 10(8): e32767. doi:10.1371/journal.pgen.1004512
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004512Souhrn
Apoptosis, also referred to as programmed cell death, is a crucial cellular process that eliminates unwanted cells during animal development and tissue homeostasis. Abnormal regulation of apoptosis can cause developmental defects and a variety of other human disorders, including cancer, neurodegenerative diseases and autoimmune diseases. Therefore, it is important to identify regulatory mechanisms that control apoptosis. Previous studies have demonstrated that the transcriptional induction of apoptotic genes can be crucial to initiating an apoptotic program. Less is known about translational controls of apoptosis. Here we report that the evolutionarily conserved C. elegans translational regulators GCN-1 and ABCF-3 promote apoptosis generally and act independently of the anti-apoptotic BCL-2 homolog CED-9. GCN-1 and ABCF-3 physically interact and maintain the phosphorylation level of eukaryotic initiation factor 2α, suggesting that GCN-1 and ABCF-3 act together to regulate the initiation of translation. We propose that the translational regulators GCN-1 and ABCF-3 maternally contribute to the proper execution of the apoptotic program.
Zdroje
1. FuchsY, StellerH (2011) Programmed cell death in animal development and disease. Cell 147 : 742–758 doi:10.1016/j.cell.2011.10.033
2. ConradtB (2009) Genetic control of programmed cell death during animal development. Annu Rev Genet 43 : 493–523 doi:10.1146/annurev.genet.42.110807.091533
3. HymanBT, YuanJ (2012) Apoptotic and non-apoptotic roles of caspases in neuronal physiology and pathophysiology. Nat Rev Neurosci 13 : 395–406 doi:10.1038/nrn3228
4. HipfnerDR, CohenSM (2004) Connecting proliferation and apoptosis in development and disease. Nat Rev Mol Cell Biol 5 : 805–815 doi:10.1038/nrm1491
5. MiyashitaT, ReedJC (1995) Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 80 : 293–299.
6. OdaE, OhkiR, MurasawaH, NemotoJ, ShibueT, et al. (2000) Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis. Science 288 : 1053–1058.
7. SaxJK, FeiP, MurphyME, BernhardE, KorsmeyerSJ, et al. (2002) BID regulation by p53 contributes to chemosensitivity. Nat Cell Biol 4 : 842–849 doi:10.1038/ncb866
8. MoroniMC, HickmanES, Lazzerini DenchiE, CapraraG, ColliE, et al. (2001) Apaf-1 is a transcriptional target for E2F and p53. Nat Cell Biol 3 : 552–558 doi:10.1038/35078527
9. WuGS, BurnsTF, McDonaldER3rd, JiangW, MengR, et al. (1997) KILLER/DR5 is a DNA damage-inducible p53-regulated death receptor gene. Nat Genet 17 : 141–143 doi:10.1038/ng1097-141
10. NakanoK, VousdenKH (2001) PUMA, a novel proapoptotic gene, is induced by p53. Mol Cell 7 : 683–694.
11. SchulerM, GreenDR (2005) Transcription, apoptosis and p53: catch-22. Trends Genet 21 : 182–187 doi:10.1016/j.tig.2005.01.001
12. NehmeR, ConradtB (2008) egl-1: a key activator of apoptotic cell death in C. elegans. Oncogene 27 Suppl 1: S30–40 doi:10.1038/onc.2009.41
13. WinnJ, CarterM, AveryL, CameronS (2011) Hox and a newly identified E2F co-repress cell death in Caenorhabditis elegans. Genetics 188 : 897–905 doi:10.1534/genetics.111.128421
14. PottsMB, WangDP, CameronS (2009) Trithorax, Hox, and TALE-class homeodomain proteins ensure cell survival through repression of the BH3-only gene egl-1. Dev Biol 329 : 374–385 doi:10.1016/j.ydbio.2009.02.022
15. HiroseT, GalvinBD, HorvitzHR (2010) Six and Eya promote apoptosis through direct transcriptional activation of the proapoptotic BH3-only gene egl-1 in Caenorhabditis elegans. Proc Natl Acad Sci USA 107 : 15479–15484 doi:10.1073/pnas.1010023107
16. MaurerCW, ChiorazziM, ShahamS (2007) Timing of the onset of a developmental cell death is controlled by transcriptional induction of the C. elegans ced-3 caspase-encoding gene. Development 134 : 1357–1368 doi:10.1242/dev.02818
17. HiroseT, HorvitzHR (2013) An Sp1 transcription factor coordinates caspase-dependent and -independent apoptotic pathways. Nature 500 : 354–358 doi:10.1038/nature12329
18. HolcikM, SonenbergN (2005) Translational control in stress and apoptosis. Nat Rev Mol Cell Biol 6 : 318–327 doi:10.1038/nrm1618
19. NevinsTA, HarderZM, KornelukRG, HolcíkM (2003) Distinct regulation of internal ribosome entry site-mediated translation following cellular stress is mediated by apoptotic fragments of eIF4G translation initiation factor family members eIF4GI and p97/DAP5/NAT1. J Biol Chem 278 : 3572–3579 doi:10.1074/jbc.M206781200
20. HolcikM, LefebvreC, YehC, ChowT, KornelukRG (1999) A new internal-ribosome-entry-site motif potentiates XIAP-mediated cytoprotection. Nat Cell Biol 1 : 190–192 doi:10.1038/11109
21. SchumacherB, HanazawaM, LeeM-H, NayakS, VolkmannK, et al. (2005) Translational repression of C. elegans p53 by GLD-1 regulates DNA damage-induced apoptosis. Cell 120 : 357–368 doi:10.1016/j.cell.2004.12.009
22. ContrerasV, FridayAJ, MorrisonJK, HaoE, KeiperBD (2011) Cap-independent translation promotes C. elegans germ cell apoptosis through Apaf-1/CED-4 in a caspase-dependent mechanism. PLoS ONE 6: e24444 doi:10.1371/journal.pone.0024444
23. ContrerasV, RichardsonMA, HaoE, KeiperBD (2008) Depletion of the cap-associated isoform of translation factor eIF4G induces germline apoptosis in C. elegans. Cell Death Differ 15 : 1232–1242 doi:10.1038/cdd.2008.46
24. HuangC-Y, ChenJ-Y, WuS-C, TanC-H, TzengR-Y, et al. (2012) C. elegans EIF-3.K promotes programmed cell death through CED-3 caspase. PLoS ONE 7: e36584 doi:10.1371/journal.pone.0036584
25. AveryL, HorvitzHR (1987) A cell that dies during wild-type C. elegans development can function as a neuron in a ced-3 mutant. Cell 51 : 1071–1078.
26. SulstonJE, SchierenbergE, WhiteJG, ThomsonJN (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 100 : 64–119.
27. Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282 : 2012–2018.
28. NukazukaA, FujisawaH, InadaT, OdaY, TakagiS (2008) Semaphorin controls epidermal morphogenesis by stimulating mRNA translation via eIF2alpha in Caenorhabditis elegans. Genes Dev 22 : 1025–1036 doi:10.1101/gad.1644008
29. Vazquez de AldanaCR, MartonMJ, HinnebuschAG (1995) GCN20, a novel ATP binding cassette protein, and GCN1 reside in a complex that mediates activation of the eIF-2 alpha kinase GCN2 in amino acid-starved cells. EMBO J 14 : 3184–3199.
30. MartonMJ, CrouchD, HinnebuschAG (1993) GCN1, a translational activator of GCN4 in Saccharomyces cerevisiae, is required for phosphorylation of eukaryotic translation initiation factor 2 by protein kinase GCN2. Mol Cell Biol 13 : 3541–3556.
31. HansonPI, WhiteheartSW (2005) AAA+ proteins: have engine, will work. Nat Rev Mol Cell Biol 6 : 519–529 doi:10.1038/nrm1684
32. MartonMJ, Vazquez de AldanaCR, QiuH, ChakraburttyK, HinnebuschAG (1997) Evidence that GCN1 and GCN20, translational regulators of GCN4, function on elongating ribosomes in activation of eIF2alpha kinase GCN2. Mol Cell Biol 17 : 4474–4489.
33. DavisonEM, SafferAM, HuangLS, DeModenaJ, SternbergPW, et al. (2011) The LIN-15A and LIN-56 transcriptional regulators interact to negatively regulate EGF/Ras signaling in Caenorhabditis elegans vulval cell-fate determination. Genetics 187 : 803–815 doi:10.1534/genetics.110.124487
34. IngoliaNT, GhaemmaghamiS, NewmanJRS, WeissmanJS (2009) Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324 : 218–223 doi:10.1126/science.1168978
35. RajA, RifkinSA, AndersenE, Van OudenaardenA (2010) Variability in gene expression underlies incomplete penetrance. Nature 463 : 913–918 doi:10.1038/nature08781
36. ReddienPW, CameronS, HorvitzHR (2001) Phagocytosis promotes programmed cell death in C. elegans. Nature 412 : 198–202 doi:10.1038/35084096
37. GumiennyTL, LambieE, HartwiegE, HorvitzHR, HengartnerMO (1999) Genetic control of programmed cell death in the Caenorhabditis elegans hermaphrodite germline. Development 126 : 1011–1022.
38. LettreG, KritikouEA, JaeggiM, CalixtoA, FraserAG, et al. (2004) Genome-wide RNAi identifies p53-dependent and -independent regulators of germ cell apoptosis in C. elegans. Cell Death Differ 11 : 1198–1203 doi:10.1038/sj.cdd.4401488
39. GartnerA, MilsteinS, AhmedS, HodgkinJ, HengartnerMO (2000) A conserved checkpoint pathway mediates DNA damage–induced apoptosis and cell cycle arrest in C. elegans. Mol Cell 5 : 435–443.
40. MetzsteinMM, StanfieldGM, HorvitzHR (1998) Genetics of programmed cell death in C. elegans: past, present and future. Trends Genet 14 : 410–416.
41. HengartnerMO, EllisRE, HorvitzHR (1992) Caenorhabditis elegans gene ced-9 protects cells from programmed cell death. Nature 356 : 494–499 doi:10.1038/356494a0
42. HengartnerMO, HorvitzHR (1994) Activation of C. elegans cell death protein CED-9 by an amino-acid substitution in a domain conserved in Bcl-2. Nature 369 : 318–320 doi:10.1038/369318a0
43. EberhardR, StergiouL, HofmannER, HofmannJ, HaenniS, et al. (2013) Ribosome synthesis and MAPK activity modulate ionizing radiation-induced germ cell apoptosis in Caenorhabditis elegans. PLoS Genet 9: e1003943 doi:10.1371/journal.pgen.1003943
44. SchumacherB, HofmannK, BoultonS, GartnerA (2001) The C. elegans homolog of the p53 tumor suppressor is required for DNA damage-induced apoptosis. Curr Biol 11 : 1722–1727.
45. HofmannER, MilsteinS, BoultonSJ, YeM, HofmannJJ, et al. (2002) Caenorhabditis elegans HUS-1 is a DNA damage checkpoint protein required for genome stability and EGL-1-mediated apoptosis. Curr Biol 12 : 1908–1918.
46. MillerPF, HinnebuschAG (1990) cis-acting sequences involved in the translational control of GCN4 expression. Biochim Biophys Acta 1050 : 151–154.
47. RousakisA, VlassisA, VlantiA, PateraS, ThireosG, et al. (2013) The general control nonderepressible-2 kinase mediates stress response and longevity induced by target of rapamycin inactivation in Caenorhabditis elegans. Aging Cell 12 : 742–51 doi:10.1111/acel.12101
48. BrennerS (1974) The genetics of Caenorhabditis elegans. Genetics 77 : 71–94.
49. WicksSR, YehRT, GishWR, WaterstonRH, PlasterkRH (2001) Rapid gene mapping in Caenorhabditis elegans using a high density polymorphism map. Nat Genet 28 : 160–164 doi:10.1038/88878
50. TroemelER, ChouJH, DwyerND, ColbertHA, BargmannCI (1995) Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans. Cell 83 : 207–218.
51. ThellmannM, HatzoldJ, ConradtB (2003) The Snail-like CES-1 protein of C. elegans can block the expression of the BH3-only cell-death activator gene egl-1 by antagonizing the function of bHLH proteins. Development 130 : 4057–4071.
52. SmitRB, SchnabelR, GaudetJ (2008) The HLH-6 transcription factor regulates C. elegans pharyngeal gland development and function. PLoS Genet 4: e1000222 doi:10.1371/journal.pgen.1000222
53. MelloCC, KramerJM, StinchcombD, AmbrosV (1991) Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J 10 : 3959–3970.
54. ClarkSG, LuX, HorvitzHR (1994) The Caenorhabditis elegans locus lin-15, a negative regulator of a tyrosine kinase signaling pathway, encodes two different proteins. Genetics 137 : 987–997.
55. HermanMA, VassilievaLL, HorvitzHR, ShawJE, HermanRK (1995) The C. elegans gene lin-44, which controls the polarity of certain asymmetric cell divisions, encodes a Wnt protein and acts cell nonautonomously. Cell 83 : 101–110.
56. KnopM, SiegersK, PereiraG, ZachariaeW, WinsorB, et al. (1999) Epitope tagging of yeast genes using a PCR-based strategy: more tags and improved practical routines. Yeast 15 : 963–972 doi:;10.1002/(SICI)1097-0061(199907)15 : 10B<963::AID-YEA399>3.0.CO;2-W
57. YoungmanMJ, RogersZN, KimDH (2011) A decline in p38 MAPK signaling underlies immunosenescence in Caenorhabditis elegans. PLoS Genet 7: e1002082 doi:10.1371/journal.pgen.1002082
58. RajA, Van den BogaardP, RifkinSA, Van OudenaardenA, TyagiS (2008) Imaging individual mRNA molecules using multiple singly labeled probes. Nat Methods 5 : 877–879 doi:10.1038/nmeth.1253
59. SubramanianV, MazumderA, SurfaceLE, ButtyVL, FieldsPA, et al. (2013) H2A.Z acidic patch couples chromatin dynamics to regulation of gene expression programs during ESC differentiation. PLoS Genet 9: e1003725 doi:10.1371/journal.pgen.1003725
60. IngoliaNT, BrarGA, RouskinS, McGeachyAM, WeissmanJS (2012) The ribosome profiling strategy for monitoring translation in vivo by deep sequencing of ribosome-protected mRNA fragments. Nat Protoc 7 : 1534–1550 doi:10.1038/nprot.2012.086
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