44
Views
13
CrossRef citations to date
0
Altmetric
Article

LIN-35/Rb Causes Starvation-Induced Germ Cell Apoptosis via CED-9/Bcl2 Downregulation in Caenorhabditis elegans

, , &
Pages 2499-2516 | Received 21 Nov 2013, Accepted 16 Apr 2014, Published online: 20 Mar 2023

REFERENCES

  • Angelo G, Van Gilst MR. 2009. Starvation protects germline stem cells and extends reproductive longevity in C. elegans. Science 326:954–958. http://dx.doi.org/10.1126/science.1178343.
  • Seidel HS, Kimble J. 2011. The oogenic germline starvation response in C. elegans. PLoS One 6:e28074. http://dx.doi.org/10.1371/journal.pone.0028074.
  • Salinas LS, Maldonado E, Navarro RE. 2006. Stress-induced germ cell apoptosis by a p53 independent pathway in Caenorhabditis elegans. Cell Death Differ. 13:2129–2139. http://dx.doi.org/10.1038/sj.cdd.4401976.
  • Sulston JE, Horvitz HR. 1977. Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev. Biol. 56:110–156. http://dx.doi.org/10.1016/0012-1606(77)90158-0.
  • Sulston JE, Schierenberg E, White G, Thomson JN. 1983. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 100:64–119. http://dx.doi.org/10.1016/0012-1606(83)90201-4.
  • Gumienny TL, Lambie E, Hartwieg E, Horvitz HR, Hengartner MO. 1999. Genetic control of programmed cell death in the Caenorhabditis elegans hermaphrodite germline. Development 126:1011–1022.
  • Horvitz HR. 2003. Worms, life, and death (Nobel lecture). ChemBioChem 4:697–711. http://dx.doi.org/10.1002/cbic.200300614.
  • Lettre G, Hengartner MO. 2006. Developmental apoptosis in C. elegans: a complex CEDnario. Nat. Rev. Mol. Cell Biol. 7:97–108. http://dx.doi.org/10.1038/nrm1836.
  • Schertel C, Conradt B. 2007. C. elegans orthologs of components of the RB tumor suppressor complex have distinct pro-apoptotic functions. Development 134:3691–3701. http://dx.doi.org/10.1242/dev.004606.
  • Derry WB, Putzke AP, Rothman JH. 2001. Caenorhabditis elegans p53: role in apoptosis, meiosis, and stress resistance. Science 294:591–595. http://dx.doi.org/10.1126/science.1065486.
  • Schumacher B, Hofmann K, Boulton S, Gartner A. 2001. The C. elegans homolog of the p53 tumor suppressor is required for DNA damage-induced apoptosis. Curr. Biol. 11:1722–1727. http://dx.doi.org/10.1016/S0960-9822(01)00534-6.
  • Schumacher B, Schertel C, Wittenburg N, Tuck S, Mitani S, Gartner A, Conradt B, Shaham S. 2005. C. elegans ced-13 can promote apoptosis and is induced in response to DNA damage. Cell Death Differ. 12:153–161. http://dx.doi.org/10.1038/sj.cdd.4401539.
  • Brenner S. 1974. The genetics of Caenorhabditis elegans. Genetics 77:71–94.
  • Lu X, Horvitz HR. 1998. lin-35 and lin-53, Two genes that antagonize a C. elegans Ras pathway, encode proteins similar to Rb and its binding protein RbAp48. Cell 95:981–991. http://dx.doi.org/10.1016/S0092-8674(00)81722-5.
  • Ceol CJ, Horvitz RH. 2001. dpl-1 DP and efl-1 E2F act with lin-35 Rb to antagonize Ras signaling in C. elegans vulval development. Mol. Cell 7:461–473. http://dx.doi.org/10.1016/S1097-2765(01)00194-0.
  • Yuan J, Shaham S, Ledoux S, Ellis HM, Horvitz HR. 1993. The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 β-converting enzyme. Cell 75:641–652. http://dx.doi.org/10.1016/0092-8674(93)90485-9.
  • Petrella LN, Wang W, Spike CA, Rechtsteiner A, Reinke V, Strome S. 2011. synMuv B proteins antagonize germline fate in the intestine and ensure C. elegans survival. Development 138:1069–1079. http://dx.doi.org/10.1242/dev.059501.
  • Timmons L, Court DL, Fire A. 2001. Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263:103–112. http://dx.doi.org/10.1016/S0378-1119(00)00579-5.
  • Conte D, Mello CC. 2003. RNA interference in Caenorhabditis Elegans. Curr. Protoc. Mol. Biol. Chapter 26:Unit 26.3. http://dx.doi.org/10.1002/0471142727.mb2603s62.
  • Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expr. data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408. http://dx.doi.org/10.1006/meth.2001.1262.
  • Kawaguchi R, Girke T, Bray EA, Bailey-Serres J. 2004. Differential mRNA translation contributes to gene regulation under non-stress and dehydration stress conditions in Arabidopsis thaliana. Plant J. 38:823–839. http://dx.doi.org/10.1111/j.1365-313X.2004.02090.x.
  • Mangone M, MacMenamin P, Zegar C, Piano F, Gunsalus KC. 2008. UTRome.org: a platform for 3′ UTR biology in C. elegans. Nucleic Acids Res. 36:D57–D62. http://dx.doi.org/10.1093/nar/gkm946.
  • Markham NR, Zuker M. 2005. DINAMelt web server for nucleic acid melting prediction. Nucleic Acids Res. 33:W577–W581. http://dx.doi.org/10.1093/nar/gki591.
  • Holcik M, Sonenberg N. 2005. Translational control in stress and apoptosis. Nat. Rev. 6:318–327. http://dx.doi.org/10.1038/nrm1618.
  • Kaeberlein M, Kennedy BK. 2008. Protein translation. Aging Cell 7:777–782. http://dx.doi.org/10.1111/j.1474-9726.2008.00439.x.
  • Dinkova TD, Keiper BD, Korneeva NL, Aamodt EJ, Rhoads RE. 2005. Translation of a small subset of Caenorhabditis elegans mRNAs is dependent on a specific eukaryotic translation initiation factor 4E isoform. Mol. Cell. Biol. 25:100–113. http://dx.doi.org/10.1128/MCB.25.1.100-113.2005.
  • Kuznicki KA, Smith PA, Leung-Chiu WMA, Estevez AO, Scott HC, Bennett KL. 2000. Combinatorial RNA interference indicates GLH-4 can compensate for GLH-1; these two P granule components are critical for fertility in C. elegans. Development 127:2907–2916.
  • Xue D, Shaham S, Horvitz HR. 1996. The Caenorhabditis elegans cell-death protein CED-3 is a cysteine protease with substrate specificities similar to those of the human CPP32 protease. Genes Dev. 10:1073–1083. http://dx.doi.org/10.1101/gad.10.9.1073.
  • Yuan J, Shaham S, Ledoux S, Ellis HM, Horvitz HR. 1993. The C. elegans cell death Gene ced-3 encodes a protein similar to mammalian interleukin-1 p-converting enzyme. Cell 75:641–652. http://dx.doi.org/10.1016/0092-8674(93)90485-9.
  • Zhou Z, Hartwieg E, Horvitz HR. 2001. CED-1 is a transmembrane receptor that mediates cell corpse engulfment in C. elegans. Cell 104:43–56. http://dx.doi.org/10.1016/S0092-8674(01)00190-8.
  • Hengartner MO, Ellis RE, Horvitz HR. 1992. Caenorhabditis elegans gene ced-9 protects cells from programmed cell death. Nature 356:494–499. http://dx.doi.org/10.1038/356494a0.
  • Reece-Hoyes JS, Shingles J, Dupuy D, Grove CA, Walhout AJ, Vidal M, Hope IA. 2007. Insight into transcription factor gene duplication from Caenorhabditis elegans promoterome-driven expression patterns. BMC Genomics 8:27. http://dx.doi.org/10.1186/1471-2164-8-27.
  • Reddien PW, Andersen EC, Huang MC, Horvitz HR. 2007. DPL-1 DP, LIN-35 Rb and EFL-1 E2F act with the MCD-1 zinc-finger protein to promote programmed cell death in Caenorhabditis elegans. Genetics 175:1719–1733. http://dx.doi.org/10.1534/genetics.106.068148.
  • Harris C, Maroney AC, Johnson EMJ. 2002. Identification of JNK-dependent and -independent components of cerebellar granule neuron apoptosis. J. Neurochem. 83:992–1001. http://dx.doi.org/10.1046/j.1471-4159.2002.01219.x.
  • Lu C, Shi Y, Wang Z, Song Z, Zhu M, Cai Q, Chen T. 2008. Serum starvation induces H2AX phosphorylation to regulate apoptosis via p38 MAPK pathway. FEBS Lett. 582:2703–2708. http://dx.doi.org/10.1016/j.febslet.2008.06.051.
  • Ellis HM, Horvitz HR. 1986. Genetic control of programmed cell death in the nematode C. elegans. Cell 44:817–829. http://dx.doi.org/10.1016/0092-8674(86)90004-8.
  • Girling R, Partridge JF, Bandara LR, Burden N, Totty NF, Hsuan JJ, La Thangue NB. 1993. A new component of the transcription factor DRTF1/E2F. Nature 362:83–87. http://dx.doi.org/10.1038/362083a0.
  • Helin K, Wu C-L, Fattaey AR, Lees JA, Dynlacht BD, Ngwu C, Harlow E. 1993. Heterodimerization of the transcription factors E2F-1 and DP-1 leads to cooperative trans-activation. Genes Dev. 7:1850–1861. http://dx.doi.org/10.1101/gad.7.10.1850.
  • Attwooll C, Denchi EL, Helin K. 2004. The E2F family: specific functions and overlapping interests. EMBO J. 23:4709–4716. http://dx.doi.org/10.1038/sj.emboj.7600481.
  • Dimova DK, Dyson NJ. 2005. The E2F transcriptional network: old acquaintances with new faces. Oncogene 24:2810–2826. http://dx.doi.org/10.1038/sj.onc.1208612.
  • Boxem M, van den Heuvel S. 2002. C. elegans class B synthetic multivulva genes act in G1 regulation. Curr. Biol. 12:906–911. http://dx.doi.org/10.1016/S0960-9822(02)00844-8.
  • Sherrill KW, Byrd MP, Van Eden ME, Lloyd RE. 2004. BCL-2 translation is mediated via internal ribosome entry during cell stress. J. Biol. Chem. 279:29066–29074. http://dx.doi.org/10.1074/jbc.M402727200.
  • Bursch W, Karwana A, Mayer M, Dornetshubera J, Fröhweina U, Schulte-Hermanna R, Fazi B, Di Sanob F, Pireddab L, Piacentinib M, Petrovski G, Fésüsc L, Gernera C. 2008. Cell death and autophagy: cytokines, drugs, and nutritional factors. Toxicology 254:147–157. http://dx.doi.org/10.1016/j.tox.2008.07.048.
  • Liu S-Y, Chen C-L, Yang T-T, Huang W-C, Hsieh C-Y, Shen W-J, Tsai T-T, Shieh C-C, Lin C-F. 2012. Albumin prevents reactive oxygen species-induced mitochondrial damage, autophagy, and apoptosis during serum starvation. Apoptosis 17:1156–1169. http://dx.doi.org/10.1007/s10495-012-0758-6.
  • Seto M, Jaeger U, Hockett RD, Graninger W, Bennett S, Goldman P, Korsmeyer SJ. 1988. Alternative promoters and exons, somatic mutation and deregulation of the Bcl-2-Ig fusion gene in lymphoma. EMBO J. 7:123–131.
  • Smith MD, Ensor EA, Coffin RS, Boxer LM, Latchman DS. 1998. Bcl-2 transcription from the proximal P2 promoter is activated in neuronal cells by the Brn-3a POU family transcription factor. J. Biol. Chem. 273:16715–16722. http://dx.doi.org/10.1074/jbc.273.27.16715.
  • Young RL, Korsmeyer SJ. 1993. A negative regulatory element in the bcl-2 5′-untranslated region inhibits expression from an upstream promoter. Mol. Cell. Biol. 13:3686–3697.
  • Chi W, Reinke V. 2006. Promotion of oogenesis and embryogenesis in the C. elegans gonad by EFL-1/DPL-1 (E2F) does not require LIN-35 (pRB). Development 133:3147–3157. http://dx.doi.org/10.1242/dev.02490.
  • Ashe MP, De Long SK, Sachs AB. 2000. Glucose depletion rapidly inhibits translation initiation in yeast. Mol. Biol. Cell 11:833–848. http://dx.doi.org/10.1091/mbc.11.3.833.
  • Zid BM, Rogers AN, Katewa SD, Vargas MA, Kolipinski MC, Lu TA, Benzer S, Kapahi P. 2009. 4E-BP extends lifespan upon dietary restriction by enhancing mitochondrial activity in Drosophila. Cell 139:149–160. http://dx.doi.org/10.1016/j.cell.2009.07.034.
  • Davies E, Stankovicb B, Vianc A, Wood A. 2012. Where has all the message gone? Plant Sci. 185:23–32. http://dx.doi.org/10.1016/j.plantsci.2011.08.001.
  • Anderson P, Kedersha N. 2002. Stressful initiations. J. Cell Sci. 115:3227–3234.
  • Spriggs KA, Bushell M, Willis AE. 2010. Translational regulation of gene expression during conditions of cell stress. Mol. Cell 40:228–237. http://dx.doi.org/10.1016/j.molcel.2010.09.028.
  • Krishnamoorthy T, Pavitt GD, Zhang F, Dever TE, Hinnebusch AG. 2001. Tight binding of the phosphorylated a subunit of initiation factor 2 (eIF2a) to the regulatory subunits of guanine nucleotide exchange factor eIF2B is required for inhibition of translation initiation. Mol. Cell. Biol. 21:5018–5030. http://dx.doi.org/10.1128/MCB.21.15.5018-5030.2001.
  • Pan KZ, Palter JE, Rogers AN, Olsen A, Chen D, Lithgow GJ, Kapahi P. 2007. Inhibition of mRNA translation extends lifespan in Caenorhabditis elegans. Aging Cell 6:111–119. http://dx.doi.org/10.1111/j.1474-9726.2006.00266.x.
  • Rogers AN, Chen D, McColl G, Czerwieniec G, Felkey K, Gibson BW, Hubbard A, Melov S, Lithgow GJ, Kapahi P. 2011. Life span extension via eIF4G inhibition is mediated by posttranscriptional remodeling of stress response gene expression in C. elegans. Cell Metab. 14:55–66. http://dx.doi.org/10.1016/j.cmet.2011.05.010.
  • Contreras V, Friday AJ, Morrison JK, Hao E, Keiper BD. 2011. Cap-independent translation promotes C. elegans germ cell apoptosis through Apaf-1/CED-4 in a caspase-dependent mechanism. PLoS One 6:e24444. http://dx.doi.org/10.1371/journal.pone.0024444.
  • Song A, Labella S, Korneeva NL, Keiper BD, Aamodt EJ, Zetka M, Rhoads RE. 2010. A C. elegans eIF4E-family member upregulates translation at elevated temperatures of mRNAs encoding MSH-5 and other meiotic crossover proteins. J. Cell Sci. 123:2228–2237. http://dx.doi.org/10.1242/jcs.063107.
  • Syntichaki P, Troulinaki K, Tavernarakis N. 2007. eIF4E function in somatic cells modulates ageing in Caenorhabditis elegans. Nature 445:922–926. http://dx.doi.org/10.1038/nature05603.
  • Contreras V, Richardson M, Hao E, Keiper B. 2008. Depletion of the cap-associated isoform of translation factor eIF4G induces germline apoptosis in C. elegans. Cell Death Differ. 15:1232–1242. http://dx.doi.org/10.1038/cdd.2008.46.
  • Jackson R. 2005. Alternative mechanisms of initiating translation of mammalian mRNAs. Biochem. Soc. Trans. 33:1231–1241. http://dx.doi.org/10.1042/BST20051231.
  • Hellen CUT, Sarnow P. 2001. Internal ribosome entry sites in eukaryotic mRNA molecules. Genes Dev. 15:1593–1612. http://dx.doi.org/10.1101/gad.891101.
  • Spriggs KA, Stoneley M, Bushell M, Willis AE. 2008. Re-programming of translation following cell stress allows IRES mediated translation to predominate. Biol. Cell 100:27–38. http://dx.doi.org/10.1042/BC20070098.
  • Stoneley M, Willis AE. 2004. Cellular internal ribosome entry segments: structures, trans-acting factors and regulation of gene expression. Oncogene 23:3200–3207. http://dx.doi.org/10.1038/sj.onc.1207551.
  • Li D, Wang M. 2012. Construction of a bicistronic vector for the co-expression of two genes in Caenorhabditis elegans using a newly identified IRES. Biotechniques 52:173–176. http://dx.doi.org/10.2144/000113821.
  • Blumenthal T, Steward K. 1997. RNA processing and gene structure, p 117–145. In Riddle DL, Blumenthal T, Meyer BJ, Priess JR (ed), C. elegans II. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
  • Bektesh SL, Hirsh DI. 1988. C. elegans mRNAs acquire a spliced leader through a trans-splicing mechanism. Nucleic Acids Res. 16:5692. http://dx.doi.org/10.1093/nar/16.12.5692.
  • Eckmann CR, Kraemer B, Wickens M, Kimble J. 2002. GLD-3, a bicaudal-C homolog that inhibits FBF to control germline sex determination in C. elegans. Dev. Cell 3:697–710. http://dx.doi.org/10.1016/S1534-5807(02)00322-2.
  • Merritt C, Rasoloson D, Ko D, Seydoux G. 2008. 3′ UTRs are the primary regulators of gene expression in the C. elegans germline. Curr. Biol. 18:1476–1482. http://dx.doi.org/10.1016/j.cub.2008.08.013.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.