Caenorhabditis elegans: A versatile platform for drug discovery

Biotechnology Journal

Volumn 1, Issue 12, 2006, Pages 1405-1418

  Artal Sanz, Marta ^a   de Jong, Liesbeth ^a   Tavernarakis, Nektarios ^a  

^a INSTITUTE OF COMPUTER SCIENCE   (Greece)

Author keywords

Chemical genetics; Compound screening; Drug target identification; Mode of action; Nematode; Rnai

Indexed keywords

CHEMICAL GENETICS; DRUG TARGET IDENTIFICATION; MODE-OF-ACTION; NEMATODE; RNAI;

DIAGNOSIS;

BIOLOGY;

CAENORHABDITIS ELEGANS PROTEIN; DRUG;

ANIMAL; ANIMAL MODEL; CAENORHABDITIS ELEGANS; DISEASE MODEL; DRUG DELIVERY SYSTEM; DRUG DESIGN; DRUG EFFECT; DRUG SCREENING; METABOLISM; METHODOLOGY; REVIEW;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DISEASE MODELS, ANIMAL; DRUG DELIVERY SYSTEMS; DRUG DESIGN; DRUG EVALUATION, PRECLINICAL; MODELS, ANIMAL; PHARMACEUTICAL PREPARATIONS;

EID: 34249736779     PISSN: 18606768     EISSN: 18607314     Source Type: Journal    
DOI: 10.1002/biot.200600176     Document Type: Review

References (70)

1. Riddle, D. L., C. elegans II. Cold Spring Harbor Laboratory Press: Plainview, N.Y. 1997.
2. Baumeister, R., Ge, L., The worm in us - Caenorhabditis elegans as a model of human disease. Trends Biotechnol. 2002, 20, 147-148.
3. Poulin, G., Nandakumar, R., Ahringer, J., Genome-wide RNAi screens in Caenorhabditis elegans: impact on cancer research. Oncogene 2004, 23, 8340-8345.
4. Kenyon C., The plasticity of aging: insights from long-lived mutants. Cell 2005, 120, 449-460.
5. Sulston, J. E., Schierenberg, E., White, J. G., Thomson, J. N., The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 1983, 100, 64-119.
6. White. J. G., Southgate, E., Thomson, J. N., Brenner, S., The structure of the ventral nerve cord of Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 1976, 275, 327-348.
7. Harris, T. W., Chen, N., Cunningham, F., Tello-Ruiz, M. et al., Worm-Base: a multi-species resource for nematode biology and genomics. Nucleic Acids Res. 2004, 32, D411-417.
8. Chen, N., Harris, T. W., Antoshechkin, I., Bastiani, C. et al., Worm-Base: a comprehensive data resource for Caenorhabditis biology and genomics. Nucleic Acids Res. 2005, 33, D383-389.
9. Bargmann, C. I., Neurobiology of the Caenorhabditis elegans genome. Science 1998, 282, 2028-2033.
10. Kaletta, T., Hengartner, M. O., Finding function in novel targets: C. elegans as a model organism. Nat. Rev. Drug Discov. 2006, 5, 387-399.
11. Ashrafi, K., Chang, F. Y., Watts, J. L., Fraser, A. G. et al., Genomewide RNAi analysis of Caenorhabditis elegans fat regulatory genes. Nature 2003, 421, 268-272.
12. Kamath, R. S., Fraser, A. G., Dong, Y., Poulin, G. et al., Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 2003, 421, 231-237.
13. Kaletta, T. B. L., Bogaert, T., Caenorhabditis elegans Functional Genomics in Drug Discovery: Expanding Paradigms. In: Carroll PMF, K. (ed.), Model Organisms in Drug Discovery. John Wiley & Sons, West Sussex, England 2003, vol. 57.
14. Feichtinger, R., Bogaert, T., Compound screens relating to insulin deficiency or insulin resistance patent 01/93669. 2001.
15. Wicks, S. R., Yeh, R. T., Gish, W. R., Waterston, R. H., Plasterk, R. H., Rapid gene mapping in Caenorhabditis elegans using a high density polymorphism map. Nat. Genet. 2001, 28, 160-164.
16. Swan, K. A., Curtis, D. E., McKusick, K. B., Voinov, A. V. et al., Highthroughput gene mapping in Caenorhabditis elegans. Genome Res. 2002, 12, 1100-1105.
17. Zipperlen, P., Nairz, K., Rimann, I., Basler, K. et al., A universal method for automated gene mapping. Genome Biol 2005, 6, R19.
18. Ranganathan, R., Sawin, E. R., Trent, C., Horvitz, H. R., Mutations in the Caenorhabditis elegans serotonin reuptake transporter MOD-5 reveal serotonin-dependent and -independent activities of fluoxetine. J. Neurosci. 2001, 21, 5871-5884.
19. Dempsey, C. M., Mackenzie, S. M., Gargus, A., Blanco, G., Sze, J. Y., Serotonin (5HT), fluoxetine, imipramine and dopamine target distinct 5HT receptor signaling to modulate Caenorhabditis elegans egg-laying behavior. Genetics 2005, 169, 1425-1436.
20. Choy, R. K., Kemner, J. M., Thomas, J. H., Fluoxetine-resistance genes in Caenorhabditis elegans function in the intestine and may act in drug transport. Genetics 2006, 172, 885-892.
21. Jones, A. K., Buckingham, S. D., Sattelle, D. B., Chemistry-to-gene screens in Caenorhabditis elegans. Nat. Rev. Drug Discov. 2005, 4, 321-330.
22. Brown, L. A., Jones, A. K., Buckingham, S. D., Mee, C. J., Sattelle, D. B., Contributions from Caenorhabditis elegans functional genetics to antiparasitic drug target identification and validation: Nicotinic acetylcholine receptors, a case study. Int. J. Parasitol. 2006, 36, 617-624.
23. Waggoner, L. E., Dickinson, K. A., Poole, D. S., Tabuse, Y. et al., Longterm nicotine adaptation in Caenorhabditis elegans involves PKCdependent changes in nicotinic receptor abundance. J. Neurosci. 2000, 20, 8802-8811.
24. Gottschalk, A., Almedom, R. B., Schedletzky, T., Anderson, S. D., Yates, J. R., 3rd, Schafer WR. Identification and characterization of novel nicotinic receptor-associated proteins in Caenorhabditis elegans. Embo J. 2005, 24, 2566-2578.
25. Davies, A. G., Pierce-Shimomura, J. T., Kim, H., VanHoven, M. K. et al., A central role of the BK potassium channel in behavioral responses to ethanol in C. elegans. Cell 2003, 115, 655-666.
26. Hawasli, A. H., Saifee, O., Liu, C., Nonet, M. L., Crowder, C. M., Resistance to volatile anesthetics by mutations enhancing excitatory neurotransmitter release in Caenorhabditis elegans. Genetics 2004, 168, 831-843.
27. Lackner, M. R., Kindt, R. M., Carroll, P. M., Brown, K. et al., Chemical genetics identifies Rab geranylgeranyl transferase as an apoptotic target of farnesyl transferase inhibitors. Cancer Cell 2005, 7, 325-336.
28. Kwok, T. C., Ricker, N., Fraser, R., Chan, A. W. et al., A small-molecule screen in C. elegans yields a new calcium channel antagonist. Nature 2006, 441, 91-95.
29. Peterson, R. T., Link, B. A., Dowling, J. E., Schreiber, S. L., Small molecule developmental screens reveal the logic and timing of vertebrate development. Proc. Natl. Acad. Sci. USA 2000, 97, 12965-12969.
30. Fitzgerald, K., Tertyshnikova, S., Moore, L., Bjerke, L. et al., Chemical genetics reveals an RGS/G-protein role in the action of a compound. PLoS Genet 2006, 2, e57.
31. Fire, A., Xu, S., Montgomery, M. K., Kostas, S. A. et al., Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 1998, 391, 806-811.
32. Tabara, H., Grishok, A., Mello, C. C., RNAi in C. elegans: soaking in the genome sequence. Science 1998, 282, 430-431.
33. Timmons, L., Fire, A., Specific interference by ingested dsRNA. Nature 1998, 395, 854.
34. Fraser, A. G., Kamath, R. S., Zipperlen, P., Martinez-Campos, M. et al., Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature 2000, 408, 325-330.
35. Gonczy, P., Echeverri, C., Oegema, K., Coulson, A. et al. Functional genomic analysis of cell division in C. elegans using RNAi of genes on chromosome III. Nature 2000, 408, 331-336.
36. Lee, S. S., Lee, R. Y., Fraser, A. G., Kamath, R. S. et al., A systematic RNAi screen identifies a critical role for mitochondria in C. elegans longevity. Nat. Genet. 2003, 33, 40-48.
37. Kennedy, S., Wang, D., Ruvkun, G., A conserved siRNA-degrading RNase negatively regulates RNA interference in C. elegans. Nature 2004, 427, 645-649.
38. Wang, D., Kennedy, S., Conte, D. Jr., Kim, J. K. et al., Somatic misexpression of germline P granules and enhanced RNA interference in retinoblastoma pathway mutants. Nature 2005, 436, 593-597.
39. Sieburth, D., Ch'ng, Q., Dybbs, M., Tavazoie, M. et al., Systematic analysis of genes required for synapse structure and function. Nature 2005, 436, 510-517.
40. Gill, M. S., Olsen, A., Sampayo, J. N., Lithgow, G. J., An automated high-throughput assay for survival of the nematode Caenorhabditis elegans. Free Radic. Biol. Med. 2003, 35, 558-565.
41. Ellerbrock, B. R., Coscarelli, E. M., Gurney, M. E., Geary, T. G., Screening for presenilin inhibitors using the free-living nematode, Caenorhabditis elegans. J. Biomol. Screen. 2004, 9, 147-152.
42. Verwaerde, P., Anthonissen, C., Deprez, B., Bonnet, B., Bogaert, T., Lipid uptake assays patent 09/861,881. 2001.
43. Kaletta, T. J., Dewulf, N. E., Plaetinck, G. K. M., Methods for identifying and developing compounds that interact with voltage-gated potassium channels of the kv4 family patent Patent pending. 2003.
44. Morris, C. E., Juranka, P. F., Lin, W., Morris, T. J., Laitko, U., Studying the mechanosensitivity of voltage-gated channels using oocyte patches. In: Clifton, N. J. (ed.), Methods mol. biol. 2006, 322, 315-329.
45. Pierce, S. B., Costa, M., Wisotzkey, R., Devadhar, S. et al., Regulation of DAF-2 receptor signaling by human insulin and ins-1, a member of the unusually large and diverse C. elegans insulin gene family. Genes Dev. 2001, 15, 672-686.
46. Levitan, D., Greenwald, I., Facilitation of lin-12-mediated signalling by sel-12, a Caenorhabditis elegans S182 Alzheimer's disease gene. Nature 1995, 377, 351-354.
47. Link, C. D., Expression of human beta-amyloid peptide in transgenic Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 1995, 92, 9368-9372.
48. Sherrington, R., Rogaev, E. I., Liang, Y., Rogaeva, E. A. et al., Cloning of a gene bearing missense mutations in early-onset familial Alzheimer's disease. Nature 1995, 375, 754-760.
49. Lakso, M., Vartiainen, S., Moilanen, A. M., Sirvio, J. et al., Dopaminergic neuronal loss and motor deficits in Caenorhabditis elegans overexpressing human alpha-synuclein. J. Neurochem. 2003, 86, 165-172.
50. Faber, P. W., Alter, J. R., MacDonald, M. E., Hart, A. C., Polyglutamine-mediated dysfunction and apoptotic death of a Caenorhabditis elegans sensory neuron. Proc. Natl. Acad. Sci. USA 1999, 96, 179-184.
51. Hara, M., Han, M., Ras farnesyltransferase inhibitors suppress the phenotype resulting from an activated ras mutation in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 1995, 92, 3333-3337.
52. Barr, M. M., Sternberg, P. W., A polycystic kidney-disease gene homologue required for male mating behaviour in C. elegans. Nature 1999, 401, 386-389.
53. Gaud, A., Simon, J. M., Witzel, T., Carre-Pierrat, M. et al., Prednisone reduces muscle degeneration in dystrophin-deficient Caenorhabditis elegans. Neuromuscul. Disord. 2004, 14, 365-370.
54. Kim, H., Rogers, M. J., Richmond, J. E., McIntire, S. L., SNF-6 is an acetylcholine transporter interacting with the dystrophin complex in Caenorhabditis elegans. Nature 2004, 430, 891-896.
55. Petersen, C. I., McFarland, T. R., Stepanovic, S. Z., Yang, P. et al., In vivo identification of genes that modify ether-a-go-go-related gene activity in Caenorhabditis elegans may also affect human cardiac arrhythmia. Proc. Natl. Acad. Sci. USA 2004, 101, 11773-11778.
56. Nollen, E. A., Garcia, S. M., van Haaften, G., Kim, S. et al., Genomewide RNA interference screen identifies previously undescribed regulators of polyglutamine aggregation. Proc. Natl. Acad. Sci. USA 2004, 101, 6403-6408.
57. Nass, R., Hall, D. H., Miller, D. M. 3rd, Blakely, R. D., Neurotoxin-induced degeneration of dopamine neurons in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 2002, 99, 3264-3269.
58. Crowder, C. M., Ethanol targets: a BK channel cocktail in C. elegans. Trends Neurosci. 2004, 27, 579-582.
59. Moy, T. I., Ball, A. R., Anklesaria, Z., Casadei, G. et al., Identification of novel antimicrobials using a live-animal infection model. Proc. Natl. Acad. Sci. USA 2006, 103, 10414-10419.
60. Reboul, J., Vaglio, P., Rual, J. F., Lamesch, P. et al., C. elegans ORFeome version 1.1: experimental verification of the genome annotation and resource for proteome-scale protein expression. Nat. Genet. 2003, 34, 35-41.
61. Luan, C. H., Qiu, S., Finley, J. B., Carson, M. et al., High-throughput expression of C. elegans proteins. Genome Res. 2004, 14, 2102-2110.
62. Li, S., Armstrong, C. M., Bertin, N., Ge, H. et al., A map of the interactome network of the metazoan C. elegans. Science 2004, 303, 540-543.
63. Nguyen, M., Alfonso, A., Johnson, C. D., Rand, J. B., Caenorhabditis elegans mutants resistant to inhibitors of acetylcholinesterase. Genetics 1995, 140, 527-535.
64. Vassilatis, D. K., Arena, J. P., Plasterk, R. H., Wilkinson, H. A. et al., Genetic and biochemical evidence for a novel avermectin-sensitive chloride channel in Caenorhabditis elegans. Isolation and characterization. J. Biol. Chem. 1997, 272, 33167-33174.
65. Dent, J. A., Smith, M. M., Vassilatis, D. K., Avery, L., The genetics of ivermectin resistance in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 2000, 97, 2674-2679.
66. Brenner, S., The genetics of Caenorhabditis elegans. Genetics 1974, 77, 71-94.
67. Lewis, J. A., Wu, C. H., Levine, J. H., Berg, H., Levamisole-resistant mutants of the nematode Caenorhabditis elegans appear to lack pharmacological acetylcholine receptors. Neuroscience 1980, 5, 967-989.
68. Parker, J. A., Arango, M., Abderrahmane, S., Lambert, E. et al. Resveratrol rescues mutant polyglutamine cytotoxicity in nematode and mammalian neurons. Nat. Genet. 2005, 37, 349-350.
69. Evason, K., Huang, C., Yamben, I., Covey, D. F., Kornfeld, K., Anticonvulsant medications extend worm life-span. Science 2005, 307, 258-262.
70. Braungart, E., Gerlach, M., Riederer, P., Baumeister, R., Hoener, M. C., Caenorhabditis elegans MPP Model of Parkinson's Disease for High-Throughput Drug Screenings. Neurodegener. Dis. 2004, 1, 175-183.