과제정보
We thank all Lee laboratory members for helpful comments and discussion. This research was supported by the KAIST Key Research Institutes Project (Interdisciplinary Research Group) to S.J.V.L.
참고문헌
- Amrit, F.R., Steenkiste, E.M., Ratnappan, R., Chen, S.W., McClendon, T.B., Kostka, D., Yanowitz, J., Olsen, C.P., and Ghazi, A. (2016). DAF-16 and TCER1 facilitate adaptation to germline loss by restoring lipid homeostasis and repressing reproductive physiology in C. elegans. PLoS Genet. 12, e1005788.
- Amrit, F.R.G., Naim, N., Ratnappan, R., Loose, J., Mason, C., Steenberge, L., McClendon, B.T., Wang, G., Driscoll, M., Yanowitz, J.L., et al. (2019). The longevity-promoting factor, TCER-1, widely represses stress resistance and innate immunity. Nat. Commun. 10, 3042.
- Angarola, B.L. and Anczukow, O. (2021). Splicing alterations in healthy aging and disease. Wiley Interdiscip. Rev. RNA 12, e1643.
- Barmada, S.J., Ju, S., Arjun, A., Batarse, A., Archbold, H.C., Peisach, D., Li, X., Zhang, Y., Tank, E.M., Qiu, H., et al. (2015). Amelioration of toxicity in neuronal models of amyotrophic lateral sclerosis by hUPF1. Proc. Natl. Acad. Sci. U. S. A. 112, 7821-7826. https://doi.org/10.1073/pnas.1509744112
- Behm-Ansmant, I., Kashima, I., Rehwinkel, J., Sauliere, J., Wittkopp, N., and Izaurralde, E. (2007). mRNA quality control: an ancient machinery recognizes and degrades mRNAs with nonsense codons. FEBS Lett. 581, 2845-2853. https://doi.org/10.1016/j.febslet.2007.05.027
- Bhadra, M., Howell, P., Dutta, S., Heintz, C., and Mair, W.B. (2020). Alternative splicing in aging and longevity. Hum. Genet. 139, 357-369. https://doi.org/10.1007/s00439-019-02094-6
- Blackwell, T.K., Sewell, A.K., Wu, Z., and Han, M. (2019). TOR signaling in Caenorhabditis elegans development, metabolism, and aging. Genetics 213, 329-360. https://doi.org/10.1534/genetics.119.302504
- Brandman, O. and Hegde, R.S. (2016). Ribosome-associated protein quality control. Nat. Struct. Mol. Biol. 23, 7-15. https://doi.org/10.1038/nsmb.3147
- Cao, L., Qi, L., Zhang, L., Song, W., Yu, Y., Xu, C., Li, L., Guo, Y., Yang, L., Liu, C., et al. (2017). Human nonsense-mediated RNA decay regulates EMT by targeting the TGF-β signaling pathway in lung adenocarcinoma. Cancer Lett. 403, 246-259. https://doi.org/10.1016/j.canlet.2017.06.021
- Charizanis, K., Lee, K.Y., Batra, R., Goodwin, M., Zhang, C., Yuan, Y., Shiue, L., Cline, M., Scotti, M.M., Xia, G., et al. (2012). Muscleblind-like 2-mediated alternative splicing in the developing brain and dysregulation in myotonic dystrophy. Neuron 75, 437-450. https://doi.org/10.1016/j.neuron.2012.05.029
- Chu, J., Hong, N.A., Masuda, C.A., Jenkins, B.V., Nelms, K.A., Goodnow, C.C., Glynne, R.J., Wu, H., Masliah, E., Joazeiro, C.A., et al. (2009). A mouse forward genetics screen identifies LISTERIN as an E3 ubiquitin ligase involved in neurodegeneration. Proc. Natl. Acad. Sci. U. S. A. 106, 2097-2103. https://doi.org/10.1073/pnas.0812819106
- Curran, S.P. and Ruvkun, G. (2007). Lifespan regulation by evolutionarily conserved genes essential for viability. PLoS Genet. 3, e56.
- Debes, C., Papadakis, A., Gronke, S., Karalay, O., Tain, L.S., Mizi, A., Nakamura, S., Hahn, O., Weigelt, C., Josipovic, N., et al. (2023). Ageingassociated changes in transcriptional elongation influence longevity. Nature 616, 814-821. https://doi.org/10.1038/s41586-023-05922-y
- Deschenes, M. and Chabot, B. (2017). The emerging role of alternative splicing in senescence and aging. Aging Cell 16, 918-933. https://doi.org/10.1111/acel.12646
- Fontana, L., Partridge, L., and Longo, V.D. (2010). Extending healthy life span--from yeast to humans. Science 328, 321-326. https://doi.org/10.1126/science.1172539
- Ghazi, A., Henis-Korenblit, S., and Kenyon, C. (2009). A transcription elongation factor that links signals from the reproductive system to lifespan extension in Caenorhabditis elegans. PLoS Genet. 5, e1000639.
- Giovannone, B., Tsiaras, W.G., de la Monte, S., Klysik, J., Lautier, C., Karashchuk, G., Goldwurm, S., and Smith, R.J. (2009). GIGYF2 gene disruption in mice results in neurodegeneration and altered insulin-like growth factor signaling. Hum. Mol. Genet. 18, 4629-4639. https://doi.org/10.1093/hmg/ddp430
- Ham, S., Kim, S.S., Park, S., Kim, E.J.E., Kwon, S., Park, H.H., Jung, Y., and Lee, S.V. (2022). Systematic transcriptome analysis associated with physiological and chronological aging in Caenorhabditis elegans. Genome Res. 32, 2003-2014. https://doi.org/10.1101/gr.276515.121
- Ham, S. and Lee, S.V. (2020). Advances in transcriptome analysis of human brain aging. Exp. Mol. Med. 52, 1787-1797. https://doi.org/10.1038/s12276-020-00522-6
- Haynes, C.M. and Hekimi, S. (2022). Mitochondrial dysfunction, aging, and the mitochondrial unfolded protein response in Caenorhabditis elegans. Genetics 222, iyac160.
- Heintz, C., Doktor, T.K., Lanjuin, A., Escoubas, C., Zhang, Y., Weir, H.J., Dutta, S., Silva-Garcia, C.G., Bruun, G.H., Morantte, I., et al. (2017). Splicing factor 1 modulates dietary restriction and TORC1 pathway longevity in C. elegans. Nature 541, 102-106. https://doi.org/10.1038/nature20789
- Hodgkin, J., Papp, A., Pulak, R., Ambros, V., and Anderson, P. (1989). A new kind of informational suppression in the nematode Caenorhabditis elegans. Genetics 123, 301-313. https://doi.org/10.1093/genetics/123.2.301
- Holly, A.C., Melzer, D., Pilling, L.C., Fellows, A.C., Tanaka, T., Ferrucci, L., and Harries, L.W. (2013). Changes in splicing factor expression are associated with advancing age in man. Mech. Ageing Dev. 134, 356-366. https://doi.org/10.1016/j.mad.2013.05.006
- Huang, W., Kew, C., Fernandes, S.A., Lohrke, A., Han, L., Demetriades, C., and Antebi, A. (2022). Decreased spliceosome fidelity and egl-8 intron retention inhibit mTORC1 signaling to promote longevity. Nat. Aging 2, 796-808. https://doi.org/10.1038/s43587-022-00275-z
- Hwang, A.B., Jeong, D.E., and Lee, S.J. (2012). Mitochondria and organismal longevity. Curr. Genomics 13, 519-532. https://doi.org/10.2174/138920212803251427
- Hwang, H.J., Park, Y., and Kim, Y.K. (2021). UPF1: from mRNA surveillance to protein quality control. Biomedicines 9, 995.
- Ishimura, R., Nagy, G., Dotu, I., Zhou, H., Yang, X.L., Schimmel, P., Senju, S., Nishimura, Y., Chuang, J.H., and Ackerman, S.L. (2014). RNA function. Ribosome stalling induced by mutation of a CNS-specific tRNA causes neurodegeneration. Science 345, 455-459. https://doi.org/10.1126/science.1249749
- Jackson, K.L., Dayton, R.D., Orchard, E.A., Ju, S., Ringe, D., Petsko, G.A., Maquat, L.E., and Klein, R.L. (2015). Preservation of forelimb function by UPF1 gene therapy in a rat model of TDP-43-induced motor paralysis. Gene Ther. 22, 20-28. https://doi.org/10.1038/gt.2014.101
- Jang, K.H., Heras, C.R., and Lee, G. (2022). m6A in the signal transduction network. Mol. Cells 45, 435-443. https://doi.org/10.14348/molcells.2022.0017
- Joazeiro, C.A.P. (2019). Mechanisms and functions of ribosome-associated protein quality control. Nat. Rev. Mol. Cell Biol. 20, 368-383. https://doi.org/10.1038/s41580-019-0118-2
- Ju, S., Tardiff, D.F., Han, H., Divya, K., Zhong, Q., Maquat, L.E., Bosco, D.A., Hayward, L.J., Brown, R.H., Jr., Lindquist, S., et al. (2011). A yeast model of FUS/TLS-dependent cytotoxicity. PLoS Biol. 9, e1001052.
- Junaid, M., Lee, A., Kim, J., Park, T.J., and Lim, S.B. (2022). Transcriptional heterogeneity of cellular senescence in cancer. Mol. Cells 45, 610-619. https://doi.org/10.14348/molcells.2022.0036
- Jung, Y., Kwon, S., Ham, S., Lee, D., Park, H.H., Yamaoka, Y., Jeong, D.E., Artan, M., Altintas, O., Park, S., et al. (2020). Caenorhabditis elegans Lipin 1 moderates the lifespan-shortening effects of dietary glucose by maintaining ω-6 polyunsaturated fatty acids. Aging Cell 19, e13150.
- Kanadia, R.N., Johnstone, K.A., Mankodi, A., Lungu, C., Thornton, C.A., Esson, D., Timmers, A.M., Hauswirth, W.W., and Swanson, M.S. (2003). A muscleblind knockout model for myotonic dystrophy. Science 302, 1978-1980. https://doi.org/10.1126/science.1088583
- Kenyon, C.J. (2010). The genetics of ageing. Nature 464, 504-512. https://doi.org/10.1038/nature08980
- Kim, E.J.E., Son, H.G., Park, H.H., Jung, Y., Kwon, S., and Lee, S.V. (2020). Caenorhabditis elegans algn-2 is critical for longevity conferred by enhanced nonsense-mediated mRNA decay. iScience 23, 101713.
- Kim, S. and Kim, C. (2021). Transcriptomic analysis of cellular senescence: one step closer to senescence atlas. Mol. Cells 44, 136-145. https://doi.org/10.14348/molcells.2021.2239
- Kim, S.S., Sohn, J., and Lee, S.V. (2022). Immunosenescence in Caenorhabditis elegans. Immun. Ageing 19, 56.
- Kim, Y.K. and Maquat, L.E. (2019). UPFront and center in RNA decay: UPF1 in nonsense-mediated mRNA decay and beyond. RNA 25, 407-422. https://doi.org/10.1261/rna.070136.118
- Lee, D., An, S.W.A., Jung, Y., Yamaoka, Y., Ryu, Y., Goh, G.Y.S., Beigi, A., Yang, J.S., Jung, G.Y., Ma, D.K., et al. (2019). MDT-15/MED15 permits longevity at low temperature via enhancing lipidostasis and proteostasis. PLoS Biol. 17, e3000415.
- Lee, G.Y., Sohn, J., and Lee, S.V. (2021). Combinatorial approach using Caenorhabditis elegans and mammalian systems for aging research. Mol. Cells 44, 425-432. https://doi.org/10.14348/molcells.2021.0080
- Lee, H. and Lee, S.V. (2022). Recent progress in regulation of aging by insulin/IGF-1 signaling in Caenorhabditis elegans. Mol. Cells 45, 763-770. https://doi.org/10.14348/molcells.2022.0097
- Lee, Y., An, S.W.A., Artan, M., Seo, M., Hwang, A.B., Jeong, D.E., Son, H.G., Hwang, W., Lee, D., Seo, K., et al. (2015). Genes and pathways that influence longevity in Caenorhabditis elegans. In Aging Mechanisms, N. Mori and I. Mook-Jung, eds. (Tokyo, Japan: Springer), pp. 123-169.
- Lopez-Otin, C., Blasco, M.A., Partridge, L., Serrano, M., and Kroemer, G. (2023). Hallmarks of aging: an expanding universe. Cell 186, 243-278. https://doi.org/10.1016/j.cell.2022.11.001
- Lu, R., Chen, J., Wang, F., Wang, L., Liu, J., and Lin, Y. (2022). Lysosome inhibition reduces basal and nutrient-induced fat accumulation in Caenorhabditis elegans. Mol. Cells 45, 649-659. https://doi.org/10.14348/molcells.2022.0073
- Ma, L., Gao, X., Luo, J., Huang, L., Teng, Y., and Horvitz, H.R. (2012). The Caenorhabditis elegans gene mfap-1 encodes a nuclear protein that affects alternative splicing. PLoS Genet. 8, e1002827.
- Mango, S.E. (2001). Stop making nonSense: the C. elegans smg genes. Trends Genet. 17, 646-653. https://doi.org/10.1016/S0168-9525(01)02479-9
- Martin, P.B., Kigoshi-Tansho, Y., Sher, R.B., Ravenscroft, G., Stauffer, J.E., Kumar, R., Yonashiro, R., Muller, T., Griffith, C., Allen, W., et al. (2020). NEMF mutations that impair ribosome-associated quality control are associated with neuromuscular disease. Nat. Commun. 11, 4625.
- Matilainen, O., Ribeiro, A.R.S., Verbeeren, J., Cetinbas, M., Sood, H., Sadreyev, R.I., and Garcia, S. (2021). Loss of muscleblind splicing factor shortens Caenorhabditis elegans lifespan by reducing the activity of p38 MAPK/PMK-1 and transcription factors ATF-7 and Nrf/SKN-1. Genetics 219, iyab114.
- Mazin, P., Xiong, J., Liu, X., Yan, Z., Zhang, X., Li, M., He, L., Somel, M., Yuan, Y., Phoebe Chen, Y.P., et al. (2013). Widespread splicing changes in human brain development and aging. Mol. Syst. Biol. 9, 633.
- Oh, C., Koh, D., Jeon, H.B., and Kim, K.M. (2022). The role of extracellular vesicles in senescence. Mol. Cells 45, 603-609. https://doi.org/10.14348/molcells.2022.0056
- Park, J., Park, J., Lee, J., and Lim, C. (2021). The trinity of ribosomeassociated quality control and stress signaling for proteostasis and neuronal physiology. BMB Rep. 54, 439-450. https://doi.org/10.5483/BMBRep.2021.54.9.097
- Park, S., Park, H.E.H., Son, H.G., and Lee, S.J.V. (2017). The role of RNA helicases in aging and lifespan regulation. Transl. Med. Aging 1, 24-31. https://doi.org/10.1016/j.tma.2017.08.001
- Powers, K.T., Szeto, J.A., and Schaffitzel, C. (2020). New insights into no-go, non-stop and nonsense-mediated mRNA decay complexes. Curr. Opin. Struct. Biol. 65, 110-118. https://doi.org/10.1016/j.sbi.2020.06.011
- Rimal, S., Li, Y., Vartak, R., Geng, J., Tantray, I., Li, S., Huh, S., Vogel, H., Glabe, C., Grinberg, L.T., et al. (2021). Inefficient quality control of ribosome stalling during APP synthesis generates CAT-tailed species that precipitate hallmarks of Alzheimer's disease. Acta Neuropathol. Commun. 9, 169.
- Rogalska, M.E., Vivori, C., and Valcarcel, J. (2023). Regulation of pre-mRNA splicing: roles in physiology and disease, and therapeutic prospects. Nat. Rev. Genet. 24, 251-269. https://doi.org/10.1038/s41576-022-00556-8
- Roux, A.E., Yuan, H., Podshivalova, K., Hendrickson, D., Kerr, R., Kenyon, C., and Kelley, D. (2023). Individual cell types in C. elegans age differently and activate distinct cell-protective responses. Cell Rep. 42, 112902.
- Sanchez-Hernandez, N., Boireau, S., Schmidt, U., Munoz-Cobo, J.P., Hernandez-Munain, C., Bertrand, E., and Sune, C. (2016). The in vivo dynamics of TCERG1, a factor that couples transcriptional elongation with splicing. RNA 22, 571-582. https://doi.org/10.1261/rna.052795.115
- Schweingruber, C., Rufener, S.C., Zund, D., Yamashita, A., and Muhlemann, O. (2013). Nonsense-mediated mRNA decay - mechanisms of substrate mRNA recognition and degradation in mammalian cells. Biochim. Biophys. Acta 1829, 612-623. https://doi.org/10.1016/j.bbagrm.2013.02.005
- Seo, M., Park, S., Nam, H.G., and Lee, S.J. (2016). RNA helicase SACY1 is required for longevity caused by various genetic perturbations in Caenorhabditis elegans. Cell Cycle 15, 1821-1829. https://doi.org/10.1080/15384101.2016.1183845
- Seo, M., Seo, K., Hwang, W., Koo, H.J., Hahm, J.H., Yang, J.S., Han, S.K., Hwang, D., Kim, S., Jang, S.K., et al. (2015). RNA helicase HEL-1 promotes longevity by specifically activating DAF-16/FOXO transcription factor signaling in Caenorhabditis elegans. Proc. Natl. Acad. Sci. U. S. A. 112, E4246-E4255. https://doi.org/10.1073/pnas.1505451112
- Son, H.G., Altintas, O., Kim, E.J.E., Kwon, S., and Lee, S.V. (2019). Agedependent changes and biomarkers of aging in Caenorhabditis elegans. Aging Cell 18, e12853.
- Son, H.G. and Lee, S.V. (2017). Longevity regulation by NMD-mediated mRNA quality control. BMB Rep. 50, 160-161. https://doi.org/10.5483/BMBRep.2017.50.4.045
- Son, H.G., Seo, M., Ham, S., Hwang, W., Lee, D., An, S.W., Artan, M., Seo, K., Kaletsky, R., Arey, R.N., et al. (2017). RNA surveillance via nonsensemediated mRNA decay is crucial for longevity in daf-2/insulin/IGF-1 mutant C. elegans. Nat. Commun. 8, 14749.
- Stein, K.C., Morales-Polanco, F., van der Lienden, J., Rainbolt, T.K., and Frydman, J. (2022). Ageing exacerbates ribosome pausing to disrupt cotranslational proteostasis. Nature 601, 637-642. https://doi.org/10.1038/s41586-021-04295-4
- Tabrez, S.S., Sharma, R.D., Jain, V., Siddiqui, A.A., and Mukhopadhyay, A. (2017). Differential alternative splicing coupled to nonsense-mediated decay of mRNA ensures dietary restriction-induced longevity. Nat. Commun. 8, 306.
- Tollervey, J.R., Wang, Z., Hortobagyi, T., Witten, J.T., Zarnack, K., Kayikci, M., Clark, T.A., Schweitzer, A.C., Rot, G., Curk, T., et al. (2011). Analysis of alternative splicing associated with aging and neurodegeneration in the human brain. Genome Res. 21, 1572-1582. https://doi.org/10.1101/gr.122226.111
- Vellai, T., Takacs-Vellai, K., Zhang, Y., Kovacs, A.L., Orosz, L., and Muller, F. (2003). Genetics: influence of TOR kinase on lifespan in C. elegans. Nature 426, 620.
- Wang, D., Zavadil, J., Martin, L., Parisi, F., Friedman, E., Levy, D., Harding, H., Ron, D., and Gardner, L.B. (2011). Inhibition of nonsense-mediated RNA decay by the tumor microenvironment promotes tumorigenesis. Mol. Cell. Biol. 31, 3670-3680. https://doi.org/10.1128/MCB.05704-11
- Wang, K., Wu, D., Zhang, H., Das, A., Basu, M., Malin, J., Cao, K., and Hannenhalli, S. (2018). Comprehensive map of age-associated splicing changes across human tissues and their contributions to age-associated diseases. Sci. Rep. 8, 10929.
- Wu, Z., Tantray, I., Lim, J., Chen, S., Li, Y., Davis, Z., Sitron, C., Dong, J., Gispert, S., Auburger, G., et al. (2019). MISTERMINATE mechanistically links mitochondrial dysfunction with proteostasis failure. Mol. Cell 75, 835-848.e8. https://doi.org/10.1016/j.molcel.2019.06.031
- Yan, L.L. and Zaher, H.S. (2019). How do cells cope with RNA damage and its consequences? J. Biol. Chem. 294, 15158-15171. https://doi.org/10.1074/jbc.REV119.006513