Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-28T17:55:20.828Z Has data issue: false hasContentIssue false
  • English
  • Français

Caenorhabditis elegans: nature and nurture gift to nematode parasitologists

Published online by Cambridge University Press:  06 December 2017

Gustavo Salinas  and
Gastón Risi
Gustavo Salinas*
Affiliation:
Worm Biology Laboratory, Institut Pasteur de Montevideo, Mataojo 2020, Montevideo 11400, Uruguay Departamento de Biociencias, Facultad de Química, Universidad de la República, Avda. gral Flores 2124, Montevideo 11300, Uruguay
Gastón Risi
Affiliation:
Worm Biology Laboratory, Institut Pasteur de Montevideo, Mataojo 2020, Montevideo 11400, Uruguay Departamento de Biociencias, Facultad de Química, Universidad de la República, Avda. gral Flores 2124, Montevideo 11300, Uruguay
*
Author for correspondence: Gustavo Salinas, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The free-living nematode Caenorhabditis elegans is the simplest animal model organism to work with. Substantial knowledge and tools have accumulated over 50 years of C. elegans research. The use of C. elegans relating to parasitic nematodes from a basic biology standpoint or an applied perspective has increased in recent years. The wealth of information gained on the model organism, the use of the powerful approaches and technologies that have advanced C. elegans research to parasitic nematodes and the enormous success of the omics fields have contributed to bridge the divide between C. elegans and parasite nematode researchers. We review key fields, such as genomics, drug discovery and genetics, where C. elegans and nematode parasite research have convened. We advocate the use of C. elegans as a model to study helminth metabolism, a neglected area ready to advance. How emerging technologies being used in C. elegans can pave the way for parasitic nematode research is discussed.

Keywords

Caenorhabditis elegansdrug discoverygeneticsgenomicshelminthmetabolismnematodeva
Type
Review Article
Information
Parasitology , Volume 145 , Issue 8 , July 2018 , pp. 979 - 987
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Besier, B (2007) New anthelmintics for livestock: the time is right. Trends in Parasitology 23, 21–24.CrossRefGoogle ScholarPubMed
Blaxter, M and Koutsovoulos, G (2015) The evolution of parasitism in Nematoda. Parasitology 142(suppl. 1), S26–S39.Google Scholar
Braeckman, BP, Houthoofd, K and Vanfleteren, JR (2009) Intermediary metabolism. In Wormbook The C. elegans Research Community, pp. 1–24. doi: 10.1895/wormbook.1.146.1.Google Scholar
Brenner, S. (2002). Nature's Gift to Science. Nobel Lecture, December 8, 2002. Available at http://www.nobelprize.org/nobel_prizes/medicine/laureates/20.Google Scholar
Britton, C, Roberts, B and Marks, ND (2016) Functional genomics tools for Haemonchus contortus and lessons from other helminths. Advances in Parasitology 93, 599–623.Google Scholar
Buckingham, SD, Partridge, FA and Sattelle, DB (2014) Automated, high-throughput, motility analysis in Caenorhabditis elegans and parasitic nematodes: applications in the search for new anthelmintics. International Journal for Parasitology: Drugs and Drug Resistance 4, 226–232.Google Scholar
Burns, AR. and Roy, PJ. (2012). To kill a mocking worm: strategies to improve Caenorhabditis elegans as a model system for use in anthelmintic discovery. In Caffrey, CR (ed). Parasitic Helminths: Targets, Screens, Drugs and Vaccines. Weinheim: Wiley-VCH Verlag GmbH & Co. KGaA, pp. 201–216.CrossRefGoogle Scholar
Burns, AR, Luciani, GM, Musso, G, Bagg, R, Yeo, M, Zhang, Y, Rajendran, L, Glavin, J, Hunter, R, Redman, E, Stasiuk, S, Schertzberg, M, Angus McQuibban, G, Caffrey, CR, Cutler, SR, Tyers, M, Giaever, G, Nislow, C, Fraser, AG, MacRae, CA, Gilleard, J and Roy, PJ (2015) Caenorhabditis elegans is a useful model for anthelmintic discovery. Nature Communications 6, 7485.CrossRefGoogle ScholarPubMed
Butcher, RA (2017) Small-molecule pheromones and hormones controlling nematode development. Nature Chemical Biology 13, 577–586.Google Scholar
Consortium, CES (1998) Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282, 2012–2018.Google Scholar
Corsi, AK, Wightman, B and Chalfie, M (2015) A transparent window into biology: a primer on Caenorhabditis elegans. Genetics 200, 387–407.Google Scholar
Chalfie, M, Tu, Y, Euskirchen, G, Ward, WW and Prasher, DC (1994) Green fluorescent protein as a marker for gene expression. Science 263, 802–805.CrossRefGoogle ScholarPubMed
Chitwood, DJ (1999) Biochemistry and function of nematode steroids. Critical Reviews in Biochemistry and Molecular Biology 34, 273–284.Google Scholar
Cragg, GM and Newman, DJ (2013) Natural products: a continuing source of novel drug leads. Biochimica et Biophysica Acta 1830, 3670–3695.CrossRefGoogle ScholarPubMed
Crook, M (2014) The dauer hypothesis and the evolution of parasitism: 20 years on and still going strong. International Journal for Parasitology 44, 1–8.Google Scholar
Davies, M, Nowotka, M, Papadatos, G, Dedman, N, Gaulton, A, Atkinson, F, Bellis, L and Overington, JP (2015) ChEMBL web services: streamlining access to drug discovery data and utilities. Nucleic Acids Research 43, W612–W620.Google Scholar
Dickinson, DJ and Goldstein, B (2016) CRISPR-Based Methods for Caenorhabditis elegans genome engineering. Genetics 202, 885–901.Google Scholar
Doitsidou, M, Jarriault, S and Poole, RJ (2016) Next-Generation sequencing-based approaches for mutation mapping and identification in Caenorhabditis elegans. Genetics 204, 451–474.Google Scholar
Duguet, TB, Charvet, CL, Forrester, SG, Wever, CM, Dent, JA, Neveu, C and Beech, RN (2016) Recent duplication and functional divergence in parasitic nematode levamisole-sensitive acetylcholine receptors. PLoS Neglected Tropical Diseases 10, e0004826.CrossRefGoogle ScholarPubMed
Erkut, C., Gade, V. R., Laxman, S. and Kurzchalia, T. V. (2016). The glyoxylate shunt is essential for desiccation tolerance in C. Elegans and budding yeast. Elife 5.Google Scholar
Farelli, JD, Galvin, BD, Li, Z, Liu, C, Aono, M, Garland, M, Hallett, OE, Causey, TB, Ali-Reynolds, A, Saltzberg, DJ, Carlow, CK, Dunaway-Mariano, D and Allen, KN (2014) Structure of the trehalose-6-phosphate phosphatase from Brugia malayi reveals key design principles for anthelmintic drugs. PLoS Pathogens 10, e1004245.Google Scholar
Felix, MA and Braendle, C (2010) The natural history of Caenorhabditis elegans. Current Biology 20, R965–R969.Google Scholar
Ferreira, SR, Mendes, TA, Bueno, LL, de Araujo, JV, Bartholomeu, DC and Fujiwara, RT (2015) A new methodology for evaluation of nematode viability. BioMed Research International 2015, 879263.Google Scholar
Fire, A, Xu, S, Montgomery, MK, Kostas, SA, Driver, SE and Mello, CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391, 806–811.Google Scholar
Gang, SS, Castelletto, ML, Bryant, AS, Yang, E, Mancuso, N, Lopez, JB, Pellegrini, M and Hallem, EA (2017) Targeted mutagenesis in a human-parasitic nematode. PLoS Pathogens 13, e1006675.Google Scholar
Hall, DH and Altun, ZF (2008) C. elegans Atlas, 1st edn., Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.Google Scholar
Hashimshony, T, Feder, M, Levin, M, Hall, BK and Yanai, I (2015) Spatiotemporal transcriptomics reveals the evolutionary history of the endoderm germ layer. Nature 519, 219–222.Google Scholar
Hedgecock, EM, Sulston, JE and Thomson, JN (1983) Mutations affecting programmed cell deaths in the nematode Caenorhabditis elegans. Science 220, 1277–1279.Google Scholar
Holden-Day, L. and Walker, R. J. (2014). Anthelmintic drugs and nematicides: studies in Caenorhabditis elegans. In Wormbook The C. elegans Research Community, pp. 1–13. doi: 10.1895/wormbook.1.143.2.Google Scholar
Howe, KL, Bolt, BJ, Cain, S, Chan, J, Chen, WJ, Davis, P, Done, J, Down, T, Gao, S, Grove, C, Harris, TW, Kishore, R, Lee, R, Lomax, J, Li, Y, Muller, HM, Nakamura, C, Nuin, P, Paulini, M, Raciti, D, Schindelman, G, Stanley, E, Tuli, MA, Van Auken, K, Wang, D, Wang, X, Williams, G, Wright, A, Yook, K, Berriman, M, Kersey, P, Schedl, T, Stein, L and Sternberg, PW (2016) Wormbase 2016: expanding to enable helminth genomic research. Nucleic Acids Research 44, D774–D780.Google Scholar
Howe, KL, Bolt, BJ, Shafie, M, Kersey, P and Berriman, M (2017) Wormbase ParaSite – a comprehensive resource for helminth genomics. Molecular & Biochemical Parasitology 215, 2–10.Google Scholar
Hutter, H and Moerman, D (2015) Big data in Caenorhabditis elegans: quo vadis? Molecular Biology of the Cell 26, 3909–3914.Google Scholar
Iwata, F, Shinjyo, N, Amino, H, Sakamoto, K, Islam, MK, Tsuji, N and Kita, K (2008) Change of subunit composition of mitochondrial complex II (succinate-ubiquinone reductase/quinol-fumarate reductase) in Ascaris suum during the migration in the experimental host. Parasitology International 57, 54–61.Google Scholar
James, CE and Davey, MW (2007) A rapid colorimetric assay for the quantitation of the viability of free-living larvae of nematodes in vitro. Parasitology Research 101, 975–980.Google Scholar
Kaminsky, R, Ducray, P, Jung, M, Clover, R, Rufener, L, Bouvier, J, Weber, SS, Wenger, A, Wieland-Berghausen, S, Goebel, T, Gauvry, N, Pautrat, F, Skripsky, T, Froelich, O, Komoin-Oka, C, Westlund, B, Sluder, A and Mäser, P (2008) A new class of anthelmintics effective against drug-resistant nematodes. Nature 452, 176–180.Google Scholar
Keiser, J and Utzinger, J (2010) The drugs we have and the drugs we need against major helminth infections. Advances in Parasitology 73, 197–230.CrossRefGoogle ScholarPubMed
Kita, K (2016) Current trend of drug development for neglected tropical diseases (NTDs). Yakugaku Zasshi 136, 205–211.CrossRefGoogle ScholarPubMed
Kita, K and Takamiya, S (2002) Electron-transfer complexes in Ascaris mitochondria. Advances in Parasitology 51, 95–131.Google Scholar
Kormish, JD and McGhee, JD (2005) The C. elegans lethal gut-obstructed gob-1 gene is trehalose-6-phosphate phosphatase. Developmental Biology 287, 35–47.CrossRefGoogle Scholar
Lazetic, V and Fay, DS (2017) Molting in C. elegans. Worm 6, e1330246.CrossRefGoogle ScholarPubMed
Li, X, Shao, H, Junio, A, Nolan, TJ, Massey, HC Jr, Pearce, EJ, Viney, ME and Lok, JB (2011) Transgenesis in the parasitic nematode Strongyloides ratti. Molecular & Biochemical Parasitology 179, 114–119.Google Scholar
Lo, NC, Addiss, DG, Hotez, PJ, King, CH, Stothard, JR, Evans, DS, Colley, DG, Lin, W, Coulibaly, JT, Bustinduy, AL, Raso, G, Bendavid, E, Bogoch, II, Fenwick, A, Savioli, L, Molyneux, D, Utzinger, J and Andrews, JR (2016) A call to strengthen the global strategy against schistosomiasis and soil-transmitted helminthiasis: the time is now. The Lancet Infectious Diseases. doi: 10.1016/S1473-3099(16)30535-7.Google Scholar
Lok, JB, Shao, H, Massey, HC and Li, X (2017) Transgenesis in Strongyloides and related parasitic nematodes: historical perspectives, current functional genomic applications and progress towards gene disruption and editing. Parasitology 144, 327–342.Google Scholar
Lonjers, ZT, Dickson, EL, Chu, TP, Kreutz, JE, Neacsu, FA, Anders, KR and Shepherd, JN (2012) Identification of a new gene required for the biosynthesis of rhodoquinone in Rhodospirillum rubrum. Journal of Bacteriology 194, 965–971.Google Scholar
Luck, AN, Yuan, X, Voronin, D, Slatko, BE, Hamza, I and Foster, JM (2016) Heme acquisition in the parasitic filarial nematode Brugia malayi. FASEB Journal 30, 3501–3514.Google Scholar
Mathew, MD, Mathew, ND, Miller, A, Simpson, M, Au, V, Garland, S, Gestin, M, Edgley, ML, Flibotte, S, Balgi, A, Chiang, J, Giaever, G, Dean, P, Tung, A, Roberge, M, Roskelley, C, Forge, T, Nislow, C and Moerman, D (2016) Using C. elegans forward and reverse genetics to identify New compounds with anthelmintic activity. PLoS Neglected Tropical Diseases 10, e0005058. 10.1371/journal.pntd.0005058.Google Scholar
Mentel, M, Rottger, M, Leys, S, Tielens, AG and Martin, WF (2014) Of early animals, anaerobic mitochondria, and a modern sponge. BioEssays 36, 924–932.CrossRefGoogle Scholar
Panic, G, Duthaler, U, Speich, B and Keiser, J (2014) Repurposing drugs for the treatment and control of helminth infections. International Journal for Parasitology: Drugs and Drug Resistance 4, 185–200.Google Scholar
Parkinson, J, Mitreva, M, Whitton, C, Thomson, M, Daub, J, Martin, J, Schmid, R, Hall, N, Barrell, B, Waterston, RH, McCarter, JP and Blaxter, ML (2004) A transcriptomic analysis of the phylum Nematoda. Nature Genetics 36, 1259–1267.Google Scholar
Rao, AU, Carta, LK, Lesuisse, E and Hamza, I (2005) Lack of heme synthesis in a free-living eukaryote. Proceedings of the National Academy of Sciences USA 102, 4270–4275.Google Scholar
San-Miguel, A and Lu, H (2013) Microfluidics as a tool for C. elegans research. In Wormbook The C. elegans Research Community, pp. 1–19. doi: 10.1895/wormbook.1.162.1.Google Scholar
Shao, H, Li, X, Nolan, TJ, Massey, HC Jr, Pearce, EJ and Lok, JB (2012) Transposon-mediated chromosomal integration of transgenes in the parasitic nematode Strongyloides ratti and establishment of stable transgenic lines. PLoS Pathogens 8, e1002871.CrossRefGoogle ScholarPubMed
Sloan, MA, Reaves, BJ, Maclean, MJ, Storey, BE and Wolstenholme, AJ (2015) Expression of nicotinic acetylcholine receptor subunits from parasitic nematodes in Caenorhabditis elegans. Molecular & Biochemical Parasitology 204, 44–50.Google Scholar
Streit, A (2017) Genetics: modes of reproduction and genetic analysis. Parasitology 144, 316–326.Google Scholar
Sulston, JE and Horvitz, HR (1977) Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Developmental Biology 56, 110–156.Google Scholar
Sutherland, IA and Leathwick, DM (2011) Anthelmintic resistance in nematode parasites of cattle: a global issue? Trends in Parasitology 27, 176–181.CrossRefGoogle ScholarPubMed
Thompson, O, Edgley, M, Strasbourger, P, Flibotte, S, Ewing, B, Adair, R, Au, V, Chaudhry, I, Fernando, L, Hutter, H, Kieffer, A, Lau, J, Lee, N, Miller, A, Raymant, G, Shen, B, Shendure, J, Taylor, J, Turner, EH, Hillier, LW, Moerman, DG and Waterston, RH (2013) The million mutation project: a new approach to genetics in Caenorhabditis elegans. Genome Research 23, 1749–1762.Google Scholar
Tielens, AG and Van Hellemond, JJ (1998) The electron transport chain in anaerobically functioning eukaryotes. Biochimica et Biophysica Acta 1365, 71–78.CrossRefGoogle ScholarPubMed
Van Hellemond, JJ, Klockiewicz, M, Gaasenbeek, CP, Roos, MH and Tielens, AG (1995) Rhodoquinone and complex II of the electron transport chain in anaerobically functioning eukaryotes. Journal of Biological Chemistry 270, 31065–31070.Google Scholar
Ward, JD (2015) Rendering the intractable more tractable: tools from Caenorhabditis elegans ripe for import into parasitic nematodes. Genetics 201, 1279–1294.Google Scholar
Weaver, KJ, May, CJ and Ellis, BL (2017) Using a health-rating system to evaluate the usefulness of Caenorhabditis elegans as a model for anthelmintic study. PLoS ONE 12, e0179376.CrossRefGoogle Scholar
Wever, CM, Farrington, D and Dent, JA (2015) The validation of nematode-specific acetylcholine-gated chloride channels as potential anthelmintic drug targets. PLoS ONE 10, e0138804.Google Scholar
White, JG, Southgate, E, Thomson, JN and Brenner, S (1986) The structure of the nervous system of the nematode Caenorhabditis elegans. Philosophical Transactions of the Royal Society of London B, Biological Sciences 314, 1–340.Google Scholar
Zamanian, M and Andersen, EC (2016) Prospects and challenges of CRISPR/Cas genome editing for the study and control of neglected vector-borne nematode diseases. FEBS Journal 283, 3204–3221.CrossRefGoogle Scholar