Browse > Article
http://dx.doi.org/10.14348/molcells.2017.0017

Survival assays using Caenorhabditis elegans  

Park, Hae-Eun H. (Department of Life Sciences, Pohang University of Science and Technology)
Jung, Yoonji (Department of Life Sciences, Pohang University of Science and Technology)
Lee, Seung-Jae V. (Department of Life Sciences, Pohang University of Science and Technology)
Publication Information
Molecules and Cells / v.40, no.2, 2017 , pp. 90-99 More about this Journal
Abstract
Caenorhabditis elegans is an important model organism with many useful features, including rapid development and aging, easy cultivation, and genetic tractability. Survival assays using C. elegans are powerful methods for studying physiological processes. In this review, we describe diverse types of C. elegans survival assays and discuss the aims, uses, and advantages of specific assays. C. elegans survival assays have played key roles in identifying novel genetic factors that regulate many aspects of animal physiology, such as aging and lifespan, stress response, and immunity against pathogens. Because many genetic factors discovered using C. elegans are evolutionarily conserved, survival assays can provide insights into mechanisms underlying physiological processes in mammals, including humans.
Keywords
aging; C. elegans; immunity; lifespan; pathogen; stress; survival;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
연도 인용수 순위
1 Beanan, M.J., and Strome, S. (1992). Characterization of a germ-line proliferation mutation in C. elegans. Development 116, 755-766.
2 Cabreiro, F., Au, C., Leung, K.Y., Vergara-Irigaray, N., Cocheme, H.M., Noori, T., Weinkove, D., Schuster, E., Greene, N.D., and Gems, D. (2013). Metformin retards aging in C. elegans by altering microbial folate and methionine metabolism. Cell 153, 228-239.   DOI
3 Choe, K.P., and Strange, K. (2007). Molecular and genetic characterization of osmosensing and signal transduction in the nematode Caenorhabditis elegans. FEBS J. 274, 5782-5789.   DOI
4 Cleland, W.W. (1964). DITHIOTHREITOL, A NEW PROTECTIVE REAGENT FOR SH GROUPS. Biochemistry 3, 480-482.   DOI
5 Corsi, A.K., Wightman, B., and Chalfie, M. (2015). A transparent window into biology: a primer on Caenorhabditis elegans. Worm-Book, 1-31.
6 Darby, C. (2005). Interactions with microbial pathogens. WormBook, 1-15.
7 Doonan, R., McElwee, J.J., Matthijssens, F., Walker, G.A., Houthoofd, K., Back, P., Matscheski, A., Vanfleteren, J.R., and Gems, D. (2008). Against the oxidative damage theory of aging: superoxide dismutases protect against oxidative stress but have little or no effect on life span in Caenorhabditis elegans. Genes Dev. 22, 3236-3241.   DOI
8 Ewbank, J.J. (2006). Signaling in the immune response. WormBook, 1-12.
9 Samuelson, A.V., Carr, C.E., and Ruvkun, G. (2007). Gene activities that mediate increased life span of C. elegans insulin-like signaling mutants. Genes Dev. 21, 2976-2994.   DOI
10 Savory, F.R., Sait, S.M., and Hope, I.A. (2011). DAF-16 and Δ9 desaturase genes promote cold tolerance in long-lived Caenorhabditis elegans age-1 mutants. PLoS One 6, e24550.   DOI
11 Scott, B.A., Avidan, M.S., and Crowder, C.M. (2002). Regulation of hypoxic death in C. elegans by the insulin/IGF receptor homolog DAF-2. Science 296, 2388-2391.   DOI
12 Shen, X., Ellis, R.E., Lee, K., Liu, C.Y., Yang, K., Solomon, A., Yoshida, H., Morimoto, R., Kurnit, D.M., Mori, K., et al. (2001). Complementary signaling pathways regulate the unfolded protein response and are required for C. elegans development. Cell 107, 893-903.   DOI
13 Sies, H. (1985). Oxidative stress: introductory remarks. Oxidative Stress, 1-8.
14 Sonoda, S., Ohta, A., Maruo, A., Ujisawa, T., and Kuhara, A. (2016). Sperm affects head sensory neuron in temperature tolerance of Caenorhabditis elegans. Cell Rep. 16, 56-65.   DOI
15 Stiernagle, T. (2006). Maintenance of C. elegans. WormBook, 1-11.
16 Stroustrup, N., Ulmschneider, B.E., Nash, Z.M., Lopez-Moyado, I.F., Apfeld, J., and Fontana, W. (2013). The Caenorhabditis elegans lifespan machine. Nat. Methods 10, 665-670.   DOI
17 Stroustrup, N., Anthony, W.E., Nash, Z.M., Gowda, V., Gomez, A., Lopez-Moyado, I.F., Apfeld, J., and Fontana, W. (2016). The temporal scaling of Caenorhabditis elegans ageing. Nature 530, 103-107.   DOI
18 Van Raamsdonk, J.M., and Hekimi, S. (2011). FUdR causes a twofold increase in the lifespan of the mitochondrial mutant gas-1. Mech. Ageing Dev. 132, 519-521.   DOI
19 Ewbank, J.J., and Pujol, N. (2016). Local and long-range activation of innate immunity by infection and damage in C. elegans. Curr. Opin. Immunol 38, 1-7.   DOI
20 Felix, M.A., Ashe, A., Piffaretti, J., Wu, G., Nuez, I., Belicard, T., Jiang, Y., Zhao, G., Franz, C.J., Goldstein, L.D., et al. (2011). Natural and experimental infection of Caenorhabditis nematodes by novel viruses related to nodaviruses. PLoS Biol. 9, e1000586.   DOI
21 Wang, Y., and Hekimi, S. (2015). Mitochondrial dysfunction and longevity in animals: Untangling the knot. Science 350, 1204-1207.   DOI
22 Van Raamsdonk, J.M., and Hekimi, S. (2012). Superoxide dismutase is dispensable for normal animal lifespan. Proc. Natl. Acad. Sci. USA 109, 5785-5790.   DOI
23 Vilchez, D., Saez, I., and Dillin, A. (2014). The role of protein clearance mechanisms in organismal ageing and age-related diseases. Nat. Commun. 5, 5659.   DOI
24 Walter, P., and Ron, D. (2011). The unfolded protein response: from stress pathway to homeostatic regulation. Science 334, 1081-1086.   DOI
25 Wang, D., Liu, P., and Xing, X. (2010). Pre-treatment with mild UV irradiation increases the resistance of nematode Caenorhabditis elegans to toxicity on locomotion behaviors from metal exposure. Environ Toxicol Pharmacol 29, 213-222.   DOI
26 Sun, A.Y., and Lambie, E.J. (1997). gon-2, a gene required for gonadogenesis in Caenorhabditis elegans. Genetics 147, 1077-1089.
27 Szewczyk, N.J., Udranszky, I.A., Kozak, E., Sunga, J., Kim, S.K., Jacobson, L.A., and Conley, C.A. (2006). Delayed development and lifespan extension as features of metabolic lifestyle alteration in C. elegans under dietary restriction. J. Exp. Biol. 209, 4129-4139.   DOI
28 Troemel, E.R. (2016). Host-microsporidia interactions in Caenorhabditis elegans, a model nematode host. Microbiol Spectr 4.
29 Troemel, E.R., Felix, M.A., Whiteman, N.K., Barriere, A., and Ausubel, F.M. (2008). Microsporidia are natural intracellular parasites of the nematode Caenorhabditis elegans. PLoS Biol. 6, 2736-2752.
30 Fisher, R.A. (1990). Statistical methods, experimental design, and scientific inference (Oxford Univ. Press).
31 Ford, S.A., Kao, D., Williams, D., and King, K.C. (2016). Microbemediated host defence drives the evolution of reduced pathogen virulence. Nat. Commun. 7, 13430.   DOI
32 Franz, C.J., Zhao, G., Felix, M.A., and Wang, D. (2012). Complete genome sequence of Le Blanc virus, a third Caenorhabditis nematode-infecting virus. J. Virol. 86, 11940.   DOI
33 Freedman, J.H., Slice, L.W., Dixon, D., Fire, A., and Rubin, C.S. (1993). The novel metallothionein genes of Caenorhabditis elegans. Structural organization and inducible, cell-specific expression. J. Biol. Chem. 268, 2554-2564.
34 Garigan, D., Hsu, A.L., Fraser, A.G., Kamath, R.S., Ahringer, J., and Kenyon, C. (2002). Genetic analysis of tissue aging in Caenorhabditis elegans: a role for heat-shock factor and bacterial proliferation. Genetics 161, 1101-1112.
35 Gems, D., and Riddle, D.L. (1996). Longevity in Caenorhabditis elegans reduced by mating but not gamete production. Nature 379, 723-725.   DOI
36 Gill, M.S., Olsen, A., Sampayo, J.N., and Lithgow, G.J. (2003). An automated high-throughput assay for survival of the nematode Caenorhabditis elegans. Free Radic. Biol. Med. 35, 558-565.   DOI
37 Yang, W., and Hekimi, S. (2010). A mitochondrial superoxide signal triggers increased longevity in Caenorhabditis elegans. PLoS Biol. 8, e1000556.   DOI
38 Greer, E.L., Maures, T.J., Ucar, D., Hauswirth, A.G., Mancini, E., Lim, J.P., Benayoun, B.A., Shi, Y., and Brunet, A. (2011). Transgenerational epigenetic inheritance of longevity in Caenorhabditis elegans. Nature 479, 365-371.   DOI
39 Hall, J., Haas, K.L., and Freedman, J.H. (2012). Role of MTL-1, MTL-2, and CDR-1 in mediating cadmium sensitivity in Caenorhabditis elegans. Toxicol. Sci. 128, 418-426.   DOI
40 Xian, B., Shen, J., Chen, W., Sun, N., Qiao, N., Jiang, D., Yu, T., Men, Y., Han, Z., Pang, Y., et al. (2013). WormFarm: a quantitative control and measurement device toward automated Caenorhabditis elegans aging analysis. Aging Cell 12, 398-409.   DOI
41 Yang, J.S., Nam, H.J., Seo, M., Han, S.K., Choi, Y., Nam, H.G., Lee, S.J., and Kim, S. (2011). OASIS: online application for the survival analysis of lifespan assays performed in aging research. PLoS One 6, e23525.   DOI
42 Ziehm, M., Ivanov, D.K., Bhat, A., Partridge, L., and Thornton, J.M. (2015). SurvCurv database and online survival analysis platform update. Bioinformatics 31, 3878-3880.
43 Hwang, A.B., and Lee, S.J. (2011). Regulation of life span by mitochondrial respiration: the HIF-1 and ROS connection. Aging (Albany NY) 3, 304-310.
44 Han, S.K., Lee, D., Lee, H., Kim, D., Son, H.G., Yang, J.S., Lee, S.V., and Kim, S. (2016). OASIS 2: online application for survival analysis 2 with features for the analysis of maximal lifespan and healthspan in aging research. Oncotarget 7, 56147-56152.   DOI
45 Herndon, L.A., Schmeissner, P.J., Dudaronek, J.M., Brown, P.A., Listner, K.M., Sakano, Y., Paupard, M.C., Hall, D.H., and Driscoll, M. (2002). Stochastic and genetic factors influence tissue-specific decline in ageing C. elegans. Nature 419, 808-814.   DOI
46 Hodgkin, J., and Partridge, F.A. (2008). Caenorhabditis elegans meets microsporidia: the nematode killers from Paris. PLoS Biol. 6, 2634-2637.
47 Hwang, A.B., Jeong, D.E., and Lee, S.J. (2012). Mitochondria and organismal longevity. Curr. Genomics 13, 519-532.   DOI
48 Jiang, B., Ren, C., Li, Y., Lu, Y., Li, W., Wu, Y., Gao, Y., Ratcliffe, P.J., Liu, H., and Zhang, C. (2011). Sodium sulfite is a potential hypoxia inducer that mimics hypoxic stress in Caenorhabditis elegans. J. Biol. Inorg. Chem. 16, 267-274.   DOI
49 Hwang, A.B., Ryu, E.A., Artan, M., Chang, H.W., Kabir, M.H., Nam, H.J., Lee, D., Yang, J.S., Kim, S., Mair, W.B., et al. (2014). Feedback regulation via AMPK and HIF-1 mediates ROS-dependent longevity in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 111, E4458-4467.   DOI
50 Jaishankar, M., Tseten, T., Anbalagan, N., Mathew, B.B., and Beeregowda, K.N. (2014). Toxicity, mechanism and health effects of some heavy metals. Interdiscip Toxicol. 7, 60-72.   DOI
51 Kaplan, E.L., and Meier, P. (1958). Nonparametric estimation from incomplete observations. J. Am. Statistical Association 53, 457-481.   DOI
52 Kim, D.H., and Ewbank, J.J. (2015). Signaling in the innate immune response. WormBook, 1-51.
53 Keith, S.A., Amrit, F.R., Ratnappan, R., and Ghazi, A. (2014). The C. elegans healthspan and stress-resistance assay toolkit. Methods 68, 476-486.   DOI
54 Kenyon, C.J. (2010). The genetics of ageing. Nature 464, 504-512.   DOI
55 Kim, D.H., and Ausubel, F.M. (2005). Evolutionary perspectives on innate immunity from the study of Caenorhabditis elegans. Curr. Opin. Immunol. 17, 4-10.   DOI
56 Kirienko, N.V., Kirienko, D.R., Larkins-Ford, J., Wahlby, C., Ruvkun, G., and Ausubel, F.M. (2013). Pseudomonas aeruginosa disrupts Caenorhabditis elegans iron homeostasis, causing a hypoxic response and death. Cell Host Microbe 13, 406-416.   DOI
57 Kirienko, N.V., Cezairliyan, B.O., Ausubel, F.M., and Powell, J.R. (2014). Pseudomonas aeruginosa PA14 pathogenesis in Caenorhabditis elegans. Methods Mol. Biol. 1149, 653-669.
58 Labbadia, J., and Morimoto, R.I. (2015). The biology of proteostasis in aging and disease. Annu. Rev. Biochem. 84, 435-464.   DOI
59 Kourtis, N., Nikoletopoulou, V., and Tavernarakis, N. (2012). Small heatshock proteins protect from heat-stroke-associated neurodegeneration. Nature 490, 213-218.   DOI
60 Kuo, S.C., and Lampen, J.O. (1974). Tunicamycin--an inhibitor of yeast glycoprotein synthesis. Biochem. Biophys. Res. Commun. 58, 287-295.   DOI
61 Lamitina, T., Huang, C.G., and Strange, K. (2006). Genome-wide RNAi screening identifies protein damage as a regulator of osmoprotective gene expression. Proc. Natl. Acad. Sci. USA 103, 12173-12178.   DOI
62 Lee, S.J., Murphy, C.T., and Kenyon, C. (2009). Glucose shortens the life span of C. elegans by downregulating DAF-16/FOXO activity and aquaporin gene expression. Cell Metab. 10, 379-391.   DOI
63 Lu, N., and Goetsch, K. (1993). Carbohydrate requirement of Caenorhabditis elegans and the final development of a chemically defined medium. Nematologica 39, 303-311.   DOI
64 Lee, S.J., Hwang, A.B., and Kenyon, C. (2010). Inhibition of respiration extends C. elegans life span via reactive oxygen species that increase HIF-1 activity. Curr. Biol. 20, 2131-2136.   DOI
65 Lee, Y., An, S.W.A., Artan, M., Seo, M., Hwang, A.B., Jeong, D.-E., Son, H.G., Hwang, W., Lee, D., and Seo, K., et al. (2015). Genes and Pathways That Influence Longevity in Caenorhabditis elegans. In Aging Mechanisms (Springer), pp. 123-169.
66 Lithgow, G.J., White, T.M., Hinerfeld, D.A., and Johnson, T.E. (1994). Thermotolerance of a long-lived mutant of Caenorhabditis elegans. J. Gerontol. 49, B270-276.   DOI
67 Murray, P., Hayward, S.A., Govan, G.G., Gracey, A.Y., and Cossins, A.R. (2007). An explicit test of the phospholipid saturation hypothesis of acquired cold tolerance in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 104, 5489-5494.   DOI
68 Mantel, N. (1966). Evaluation of survival data and two new rank order statistics arising in its consideration. Cancer Chemother. Rep. 50, 163-170.
69 Mathew, M.D., Mathew, N.D., and Ebert, P.R. (2012). WormScan: a technique for high-throughput phenotypic analysis of Caenorhabditis elegans. PLoS One 7, e33483.   DOI
70 Murakami, S., and Johnson, T.E. (1996). A genetic pathway conferring life extension and resistance to UV stress in Caenorhabditis elegans. Genetics 143, 1207-1218.
71 Mylonakis, E., Ausubel, F.M., Perfect, J.R., Heitman, J., and Calderwood, S.B. (2002). Killing of Caenorhabditis elegans by Cryptococcus neoformans as a model of yeast pathogenesis. Proc. Natl. Acad. Sci. USA 99, 15675-15680.   DOI
72 Amrit, F.R., Ratnappan, R., Keith, S.A., and Ghazi, A. (2014). The C. elegans lifespan assay toolkit. Methods 68, 465-475.   DOI
73 Aitlhadj, L., and Sturzenbaum, S.R. (2010). The use of FUdR can cause prolonged longevity in mutant nematodes. Mech. Ageing Dev. 131, 364-365.   DOI
74 Alspaugh, J.A. (2015). Virulence mechanisms and Cryptococcus neoformans pathogenesis. Fungal Genet. Biol. 78, 55-58.   DOI
75 Altintas, O., Park, S., and Lee, S.J. (2016). The role of insulin/IGF-1 signaling in the longevity of model invertebrates, C. elegans and D. melanogaster. BMB Rep. 49, 81-92.   DOI
76 Papenfort, K., and Bassler, B.L. (2016). Quorum sensing signalresponse systems in Gram-negative bacteria. Nat. Rev. Microbiol. 14, 576-588.   DOI
77 Mylonakis, E., Casadevall, A., and Ausubel, F.M. (2007). Exploiting amoeboid and non-vertebrate animal model systems to study the virulence of human pathogenic fungi. PLoS Pathog. 3, e101.   DOI
78 O'Neil, N., and Rose, A. (2006). DNA repair. WormBook, 1-12.
79 Oliveira, R.P., Porter Abate, J., Dilks, K., Landis, J., Ashraf, J., Murphy, C.T., and Blackwell, T.K. (2009). Condition-adapted stress and longevity gene regulation by Caenorhabditis elegans SKN-1/Nrf. Aging Cell 8, 524-541.   DOI
80 Barsyte, D., Lovejoy, D.A., and Lithgow, G.J. (2001). Longevity and heavy metal resistance in daf-2 and age-1 long-lived mutants of Caenorhabditis elegans. FASEB J. 15, 627-634.   DOI
81 Powell-Coffman, J.A. (2010). Hypoxia signaling and resistance in C. elegans. Trends Endocrinol. Metab. 21, 435-440.   DOI
82 Pulak, R. (2006). Techniques for analysis, sorting, and dispensing of C. elegans on the COPAS flow-sorting system. Methods Mol. Biol. 351, 275-286.
83 Rechavi, O., Houri-Ze'evi, L., Anava, S., Goh, W.S., Kerk, S.Y., Hannon, G.J., and Hobert, O. (2014). Starvation-induced transgenerational inheritance of small RNAs in C. elegans. Cell 158, 277-287.   DOI
84 Reddy, K.C., Andersen, E.C., Kruglyak, L., and Kim, D.H. (2009). A polymorphism in npr-1 is a behavioral determinant of pathogen susceptibility in C. elegans. Science 323, 382-384.   DOI
85 Rodriguez, M., Snoek, L.B., De Bono, M., and Kammenga, J.E. (2013). Worms under stress: C. elegans stress response and its relevance to complex human disease and aging. Trends Genet. 29, 367-374.   DOI
86 Rohlfing, A.K., Miteva, Y., Hannenhalli, S., and Lamitina, T. (2010). Genetic and physiological activation of osmosensitive gene expression mimics transcriptional signatures of pathogen infection in C. elegans. PloS one 5, e9010.   DOI
87 Rooney, J.P., Luz, A.L., Gonzalez-Hunt, C.P., Bodhicharla, R., Ryde, I.T., Anbalagan, C., and Meyer, J.N. (2014). Effects of 5'-fluoro-2-deoxyuridine on mitochondrial biology in Caenorhabditis elegans. Exp. Gerontol. 56, 69-76.   DOI