Single-worm quantitative proteomics reveals aging heterogeneity in isogenic Caenorhabditis elegans.
aging
mass spectrometry
single worm proteomics
Journal
Aging cell
ISSN: 1474-9726
Titre abrégé: Aging Cell
Pays: England
ID NLM: 101130839
Informations de publication
Date de publication:
03 Dec 2023
03 Dec 2023
Historique:
revised:
14
11
2023
received:
26
06
2023
accepted:
17
11
2023
medline:
4
12
2023
pubmed:
4
12
2023
entrez:
4
12
2023
Statut:
aheadofprint
Résumé
The heterogeneity of aging has been investigated at cellular and organic levels in the mouse model and human, but the exploration of aging heterogeneity at whole-organism level is lacking. C. elegans is an ideal model organism for studying this question as they are self-fertilized and cultured in the same chamber. Despite the tremendous progress made in single-cell proteomic analysis, there is few single-worm proteomics studies about aging. Here, we apply single-worm quantitative mass spectrometry to quantify the heterogenous proteomic changes during aging across individuals, a total of 3524 proteins from 157 C. eleagns individuals were quantified. A reconstructed C. elegans aging trajectory and proteomic landscape of fast-aging individuals were used to analyze the heterogeneity of C. elegans aging. We characterized inter-individual proteomic variation during aging and revealed contributing factors that distinguish fast-aging individuals from their siblings.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e14055Subventions
Organisme : National Key Research and Development Program of China
ID : 2022YFF0608402
Organisme : National Natural Science Foundation of China
ID : 22074132
Organisme : National Natural Science Foundation of China
ID : 91953103
Organisme : National Natural Science Foundation of China
ID : C-0023
Organisme : National Natural Science Foundation of China
ID : 31972541
Organisme : Open Project Program of the State Key Laboratory of Proteomics, China
ID : SKLPO201806
Organisme : the outstanding youth fund of Zhejiang Province
ID : LR20B050001
Organisme : Open Project Program of Jiangsu Provincial Key Laboratory of Poultry Genetics and Breeding
Informations de copyright
© 2023 The Authors. Aging Cell published by Anatomical Society and John Wiley & Sons Ltd.
Références
Ba, Q., Hei, Y., Dighe, A., Li, W., Maziarz, J., Pak, I., Wang, S., Wagner, G. P., & Liu, Y. (2022). Proteotype coevolution and quantitative diversity across 11 mammalian species. Science Advances, 8(36), eabn0756. https://doi.org/10.1126/sciadv.abn0756
Bahar, R., Hartmann, C. H., Rodriguez, K. A., Denny, A. D., Busuttil, R. A., Dollé, M. E., Calder, R. B., Chisholm, G. B., Pollock, B. H., & Klein, C. A. (2006). Increased cell-to-cell variation in gene expression in ageing mouse heart. Nature, 441(7096), 1011-1014.
Bansal, A., Zhu, L. J., Yen, K., & Tissenbaum, H. A. (2015). Uncoupling lifespan and healthspan in Caenorhabditis elegans longevity mutants. Proceedings of the National Academy of Sciences, 112(3), E277-E286.
Bazopoulou, D., Knoefler, D., Zheng, Y., Ulrich, K., Oleson, B. J., Xie, L., Kim, M., Kaufmann, A., Lee, Y. T., Dou, Y., Chen, Y., Quan, S., & Jakob, U. (2019). Developmental ROS individualizes organismal stress resistance and lifespan. Nature, 576(7786), 301-305.
Bensaddek, D., Narayan, V., Nicolas, A., Murillo, A. B., Gartner, A., Kenyon, C. J., & Lamond, A. I. (2016). Micro-proteomics with iterative data analysis: Proteome analysis in C. Elegans at the single worm level. Proteomics, 16(3), 381-392. https://doi.org/10.1002/pmic.201500264
Castillo-Fernandez, J., Herrera-Puerta, E., Demond, H., Clark, S. J., Hanna, C. W., Hemberger, M., & Kelsey, G. (2020). Increased transcriptome variation and localised DNA methylation changes in oocytes from aged mice revealed by parallel single-cell analysis. Aging Cell, 19(12), e13278.
Cong, Y., Motamedchaboki, K., Misal, S. A., Liang, Y., Guise, A. J., Truong, T., Huguet R, Plower E. D, Zhu Y, Lopez Ferer D. &. Kelly, R. T. (2020). Ultrasensitive single-cell proteomics workflow identifies >1000 protein groups per mammalian cell. Chemical Science, 12(3), 1001-1006. https://doi.org/10.1039/d0sc03636f
Cox, J., & Mann, M. (2008). MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nature Biotechnology, 26(12), 1367-1372. https://doi.org/10.1038/nbt.1511
Ezcurra, M., Benedetto, A., Sornda, T., Gilliat, A. F., Au, C., Zhang, Q., Van Schelt S, Petrache AL, Wang H, de la Guardia, Y., Bar-Nun S, Tyler E, Wakelam MJ, & Gems D (2018). C. Elegans eats its own intestine to make yolk leading to multiple senescent pathologies. Current Biology, 28(16), 2544-2556. e2545.
Gladyshev, V. N. (2016). Aging: Progressive decline in fitness due to the rising deleteriome adjusted by genetic, environmental, and stochastic processes. Aging Cell, 15(4), 594-602.
Hemstreet, G. P., & Wang, W. (2004). Genotypic and phenotypic biomarker profiles for individual risk assessment and cancer detection (lessons from bladder cancer risk assessment in symptomatic patients and workers exposed to benzidine). Frontiers in Bioscience, 9, 2671-2679. https://doi.org/10.2741/1426
Herndon, L. A., Schmeissner, P. J., Dudaronek, J. M., Brown, P. A., Listner, K. M., Sakano, Y., Paupard, M. C., Hall, D. H., & Driscoll, M. (2002). Stochastic and genetic factors influence tissue-specific decline in ageing C. Elegans. Nature, 419(6909), 808-814. https://doi.org/10.1038/nature01135
Jones, O. R., Scheuerlein, A., Salguero-Gómez, R., Camarda, C. G., Schaible, R., Casper, B. B., Dahlgren, J. P., Ehrlén, J., García, M. B., Menges, E. S., Quintana-Ascencio, P. F., Caswell, H., Baudisch, A., & Vaupel, J. W. (2014). Diversity of ageing across the tree of life. Nature, 505(7482), 169-173.
Kenyon, C., Chang, J., Gensch, E., Rudner, A., & Tabtiang, R. (1993). A C. Elegans mutant that lives twice as long as wild type. Nature, 366(6454), 461-464. https://doi.org/10.1038/366461a0
Kenyon, C. J. (2010). The genetics of ageing. Nature, 464(7288), 504-512.
Kern, C. C., Townsend, S., Salzmann, A., Rendell, N. B., Taylor, G. W., Comisel, R. M., Foukas, L. C., Bähler, J., & Gems, D. (2021). C. Elegans feed yolk to their young in a form of primitive lactation. Nature Communications, 12(1), 1-11.
Kinser, H. E., Mosley, M. C., Plutzer, I. B., & Pincus, Z. (2021). Global, cell non-autonomous gene regulation drives individual lifespan among isogenic C. Elegans. eLife, 10, e65026.
Kirkwood, T. B., Feder, M., Finch, C. E., Franceschi, C., Globerson, A., Klingenberg, C. P., Lamarco, K., Omholt, S., & Westendorp, R. G. (2005). What accounts for the wide variation in life span of genetically identical organisms reared in a constant environment? Mechanisms of Ageing and Development, 126(3), 439-443.
Knoefler, D., Thamsen, M., Koniczek, M., Niemuth, N. J., Diederich, A.-K., & Jakob, U. (2012). Quantitative in vivo redox sensors uncover oxidative stress as an early event in life. Molecular Cell, 47(5), 767-776.
Labbadia, J., & Morimoto, R. I. (2015). Repression of the heat shock response is a programmed event at the onset of reproduction. Molecular Cell, 59(4), 639-650.
Li, S. T., Zhao, H. Q., Zhang, P., Liang, C. Y., Zhang, Y. P., Hsu, A. L., & Dong, M. Q. (2019). DAF-16 stabilizes the aging transcriptome and is activated in mid-aged Caenorhabditis elegans to cope with internal stress. Aging Cell, 18(3), e12896.
Liang, V., Ullrich, M., Lam, H., Chew, Y. L., Banister, S., Song, X., Zaw, T., Kassiou, M., Götz, J., & Nicholas, H. R. (2014). Altered proteostasis in aging and heat shock response in C. Elegans revealed by analysis of the global and de novo synthesized proteome. Cellular and Molecular Life Sciences, 71(17), 3339-3361. https://doi.org/10.1007/s00018-014-1558-7
Ljungquist, B., Berg, S., Lanke, J., McClearn, G. E., & Pedersen, N. L. (1998). The effect of genetic factors for longevity: A comparison of identical and fraternal twins in the Swedish twin registry. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, 53(6), M441-M446.
Narayan, V., Ly, T., Pourkarimi, E., Murillo, A. B., Gartner, A., Lamond, A. I., & Kenyon, C. (2016). Deep proteome analysis identifies age-related processes in C. Elegans. Cell Systems, 3(2), 144-159. https://doi.org/10.1016/j.cels.2016.06.011
Perez-Riverol, Y., Bai, J., Bandla, C., Garcia-Seisdedos, D., Hewapathirana, S., Kamatchinathan, S., Kundu, D. J., Prakash, A., Frericks-Zipper, A., Eisenacher, M., Walzer, M., Wang, S., Brazma, A., & Vizcaino, J. A. (2022). The PRIDE database resources in 2022: A hub for mass spectrometry-based proteomics evidences. Nucleic Acids Research, 50(D1), D543-D552. https://doi.org/10.1093/nar/gkab1038
Qiu, X., Mao, Q., Tang, Y., Wang, L., Chawla, R., Pliner, H. A., & Trapnell, C. (2017). Reversed graph embedding resolves complex single-cell trajectories. Nature Methods, 14(10), 979-982. https://doi.org/10.1038/nmeth.4402
Rappsilber, J., Mann, M., & Ishihama, Y. (2007). Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nature Protocols, 2(8), 1896-1906. https://doi.org/10.1038/nprot.2007.261
Rea, S. L., Wu, D., Cypser, J. R., Vaupel, J. W., & Johnson, T. E. (2005). A stress-sensitive reporter predicts longevity in isogenic populations of Caenorhabditis elegans. Nature Genetics, 37(8), 894-898.
Ruby, J. G., Wright, K. M., Rand, K. A., Kermany, A., Noto, K., Curtis, D., Varner, N., Garrigan, D., Slinkov, D., Dorfman, I., Granka, J. M., Byrnes, J., Myres, N., & Ball, C. (2018). Estimates of the heritability of human longevity are substantially inflated due to assortative mating. Genetics, 210(3), 1109-1124.
Sánchez-Blanco, A., & Kim, S. K. (2011). Variable pathogenicity determines individual lifespan in Caenorhabditis elegans. PLoS Genetics, 7(4), e1002047.
Shen, E.-Z., Song, C.-Q., Lin, Y., Zhang, W.-H., Su, P.-F., Liu, W.-Y., Zhang, P., Xu, J., Lin, N., Zhan, C., Wang, X., Shyr, Y., Cheng, H., & Dong, M. Q. (2014). Mitoflash frequency in early adulthood predicts lifespan in Caenorhabditis elegans. Nature, 508(7494), 128-132.
Steinbach, M. K., Leipert, J., Blurton, C., Leippe, M., & Tholey, A. (2022). Digital microfluidics supported microproteomics for quantitative proteome analysis of single Caenorhabditis elegans Nematodes. Journal of Proteome Research, 21(8), 1986-1996. https://doi.org/10.1021/acs.jproteome.2c00274
Stroustrup, N., Anthony, W. E., Nash, Z. M., Gowda, V., Gomez, A., López-Moyado, I. F., Apfeld, J., & Fontana, W. (2016). The temporal scaling of Caenorhabditis elegans ageing. Nature, 530(7588), 103-107.
Tajik, M., Baharfar, M., & Donald, W. A. (2022). Single-cell mass spectrometry. Trends in Biotechnology, 40(11), 1374-1392. https://doi.org/10.1016/j.tibtech.2022.04.004
Turek, M., Banasiak, K., Piechota, M., Shanmugam, N., Macias, M., Sliwinska, M. A., Niklewicz, M., Kowalski, K., Nowak, N., Chacinska, A., & Pokrzywa, W. (2021). Muscle-derived exophers promote reproductive fitness. EMBO Reports, 22(8), e52071. https://doi.org/10.15252/embr.202052071
Vellai, T., Takacs-Vellai, K., Zhang, Y., Kovacs, A. L., Orosz, L., & Muller, F. (2003). Genetics: Influence of TOR kinase on lifespan in C. Elegans. Nature, 426(6967), 620. https://doi.org/10.1038/426620a
Walther, D. M., Kasturi, P., Zheng, M., Pinkert, S., Vecchi, G., Ciryam, P., Morimoto, R. I., Dobson, C. M., Vendruscolo, M., Mann, M., & Hartl, F. U. (2015). Widespread proteome remodeling and aggregation in Aging C. Elegans. Cell, 161(4), 919-932. https://doi.org/10.1016/j.cell.2015.03.032
Wilhelm, T., Byrne, J., Medina, R., Kolundzic, E., Geisinger, J., Hajduskova, M., Tursun, B., & Richly, H. (2017). Neuronal inhibition of the autophagy nucleation complex extends life span in post-reproductive C. Elegans. Genes & Development, 31(15), 1561-1572. https://doi.org/10.1101/gad.301648.117
Wilson, K. A., Beck, J. N., Nelson, C. S., Hilsabeck, T. A., Promislow, D., Brem, R. B., & Kapahi, P. (2020). GWAS for lifespan and decline in climbing ability in flies upon dietary restriction reveal decima as a mediator of insulin-like peptide production. Current Biology, 30(14), 2749-2760 e2743. https://doi.org/10.1016/j.cub.2020.05.020
Xia, X., Chen, X., Wu, G., Li, F., Wang, Y., Chen, Y., Chen, M., Wang, X., Chen, W., Xian, B., Chen, W., Cao, Y., Xu, C., Gong, W., Chen, G., Cai, D., Wei, W., Yan, Y., & Xian, B. (2020). Three-dimensional facial-image analysis to predict heterogeneity of the human ageing rate and the impact of lifestyle. Nature Metabolism, 2(9), 946-957.
Yu, G., Wang, L. G., Han, Y., & He, Q. Y. (2012). clusterProfiler: An R package for comparing biological themes among gene clusters. Omics, 16(5), 284-287. https://doi.org/10.1089/omi.2011.0118
Zhang, W. B., Sinha, D. B., Pittman, W. E., Hvatum, E., Stroustrup, N., & Pincus, Z. (2016). Extended twilight among isogenic C. Elegans causes a disproportionate scaling between lifespan and health. Cell Systems, 3(4), 333-345.