The nematode Caenorhabditis elegans, stress and aging: Identifying the complex interplay of genetic pathways following the treatment with humic substances

Frontiers in Genetics

Volumn 3, Issue APR, 2012, Pages

  Menzel, Ralph ^a   Menzel, Stefanie ^a,b   Swain, Suresh C ^c,d   Pietsch, Kerstin ^a   Tiedt, Sophie ^a   Witczak, Jördis ^a   Stürzenbaum, Stephen R ^c   Steinberg, Christian E W ^a  

^a HUMBOLDT UNIVERSITY   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d ABERYSTWYTH UNIVERSITY   (United Kingdom)

Author keywords

Aging; Caenorhabditis elegans; Gene expression; Humic substances; Hydroxybenzene; Longevity; Stress; TGF beta

Indexed keywords

CAENORHABDITIS ELEGANS; NEMATODA;

EID: 84876066913     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2012.00050     Document Type: Article

References (60)

1. Aitlhadj, L., and Stürzenbaum, S. R. (2010). The use of FUdR can cause prolonged longevity in mutant nematodes. Mech. Ageing Dev. 131, 364-365.
2. Akagawa, M., Shigemitsu, T., and Suyama, K. (2003). Production of hydrogen peroxide by polyphenols and polyphenol-rich beverages under quasi-physiological conditions. Biosci. Biotechnol. Biochem. 67, 2632-2640.
3. An, J. H., and Blackwell, T. K. (2003). SKN-1 links C. elegans mesendodermal specification to a conserved oxidative stress response. Genes Dev. 17, 1882-1893.
4. Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., Harris, M. A., Hill, D. P., Issel-Tarver, L., Kasarskis, A., Lewis, S., Matese, J. C., Richardson, J. E., Ringwald, M., Rubin, G. M., and Sherlock, G. (2000). Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25, 25-29.
5. Azen, S. P., Roy, S., Pike, M. C., Casagrande, J., and Mishell, D. R. Jr. (1977). A new procedure for the statistical evaluation of intrauterine contraception. Am. J. Obstet. Gynecol. 128, 329-335.
6. Benjamini, Y., and Hochberg, Y. (1995). Controlling the false discovery rate - a practical and powerful approach to multiple testing. J. R. Stat. Soc. Series B Stat. Methodol. 57, 289-300.
7. Berdichevsky, A., Viswanathan, M., Horvitz, H. R., and Guarente, L. (2006). C. elegans SIR-2.1 interacts with 14-3-3 proteins to activate DAF-16 and extend life span. Cell 125, 1165-1177.
8. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
9. Budovskaya, Y. V., Wu, K., Southworth, L. K., Jiang, M., Tedesco, P., Johnson, T. E., and Kim, S. K. (2008). An elt-3/elt-5/elt-6 GATA transcription circuit guides aging in C. elegans. Cell 134, 291-303.
10. Coolon, J. D., Jones, K. L., Todd, T. C., Carr, B. C., and Herman, M. A. (2009). Caenorhabditis elegans genomic response to soil bacteria predicts environment-specific genetic effects on life history traits. PLoS Genet. 5, e1000503. doi:10.1371/journal.pgen.1000503
11. Dalma-Weiszhausz, D. D., Warrington, J., Tanimoto, E. Y., and Miyada, C. G. (2006). The Affymetrix GeneChip platform: an overview. Meth. Enzymol. 410, 3-28.
12. Davies, S. K., Leroi, A. M., and Bundy, J. G. (2012). Fluorodeoxyuridine affects the identification of metabolic responses to daf-2 status in Caenorhabditis elegans. Mech. Ageing Dev. 133, 46-49.
13. Evans, E. A., Kawli, T., and Tan, M. W. (2008). Pseudomonas aeruginosa suppresses host immunity by activating the DAF-2 insulin-like signaling pathway in Caenorhabditis elegans. PLoS Pathog. 4, e1000175. doi:10.1371/journal.ppat.1000175
14. Fisher, A. L., and Lithgow, G. J. (2006). The nuclear hormone receptor DAF-12 has opposing effects on Caenorhabditis elegans lifespan and regulates genes repressed in multiple long-lived worms. Aging Cell 5, 127-138.
15. Gems, D., and McElwee, J. J. (2005). Broad spectrum detoxification: the major longevity assurance process regulated by insulin/IGF-1 signaling Mech. Ageing Dev. 126, 381-387.
16. Granato, M., Schnabel, H., and Schnabel, R. (1994a). Genesis of an organ: molecular analysis of the pha-1 gene. Development 120, 3005-3017.
17. Granato, M., Schnabel, H., and Schnabel, R. (1994b). pha-1, a selectable marker for gene transfer in C. elegans. Nucleic Acids Res. 22, 1762-1763.
18. Grigoryev, D. N., Ma, S. F., Irizarry, R. A., Ye, S. Q., Quackenbush, J., and Garcia, J. G. (2004). Orthologous gene-expression profiling in multi-species models: search for candidate genes. Genome Biol. 5, R34.
19. Halaschek-Wiener, J., Khattra, J. S., Mckay, S., Pouzyrev, A., Stott, J. M., Yang, G. S., Holt, R. A., Jones, S. J. M., Marra, M. A., Brooks-Wilson, A. R., and Riddle, D. L. (2005). Analysis of long-lived C. elegans daf-2 mutants using serial analysis of gene expression. Genome Res. 15, 603-615.
20. Hars, E. S., Qi, H., Ryazanov, A. G., Jin, S., Cai, L., Hu, C., and Liu, L. F. (2007). Autophagy regulates ageing in C. elegans. Autophagy 3, 93-95.
21. Herrero, J., Al-Shahrour, F., Diaz-Uriarte, R., Mateos, A., Vaquerizas, J. M., Santoyo, J., and Dopazo, J. (2003). GEPAS: a web-based resource for microarray gene expression data analysis. Nucleic Acids Res. 31, 3461-3467.
22. Hosokawa, H., Ishii, N., Ishida, H., Ichimori, K., Nakazawa, H., and Suzuki, K. (1994). Rapid accumulation of fluorescent material with aging in an oxygen-sensitive mutant mev-1 of Caenorhabditis elegans. Mech. Ageing Dev. 74, 161-170.
23. Huang, D. W., Sherman, B. T., Tan, Q., Kir, J., Liu, D., Bryant, D., Guo, Y., Stephens, R., Baseler, M. W., Lane, H. C., and Lempicki, R. A. (2007). DAVID Bioinformatics Resources: expanded annotation database and novel algorithms to better extract biology from large gene lists. Nucleic Acids Res. 35, W169-W175.
24. Ishii, N., Fujii, M., Hartman, P. S., Tsuda, M., Yasuda, K., Senoo-Matsuda, N., Yanase, S., Ayusawa, D., and Suzuki, K. (1998). A mutation in succinate dehydrogenase cytochrome b causes oxidative stress and ageing in nematodes. Nature 394, 694-697.
25. Kampkötter, A., Timpel, C., Zurawski, R. F., Ruhl, S., Chovolou, Y., Proksch, P., and Watjen, W. (2008). Increase of stress resistance and lifespan of Caenorhabditis elegans by quercetin. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 149, 314-323.
26. Kanehisa, M. (2002). The KEGG database. Novartis Found. Symp. 247, 91-101. [Discussion 101-103, 119-128, 244-152].
27. Kim, D. H., Feinbaum, R., Alloing, G., Emerson, F. E., Garsin, D. A., Inoue, H., Tanaka-Hino, M., Hisamoto, N., Matsumoto, K., Tan, M. W., and Ausubel, F. M. (2002). A conserved p38 MAP kinase pathway in Caenorhabditis elegans innate immunity. Science 297, 623-626.
28. Kim, S. K., Lund, J., Kiraly, M., Duke, K., Jiang, M., Stuart, J. M., Eizinger, A., Wylie, B. N., and Davidson, G. S. (2001). A gene expression map for Caenorhabditis elegans. Science 293, 2087-2092.
29. Kirkwood, T. B. L., and Austad, S. N. (2000). Why do we age Nature 408, 233-238.
30. Kourtis, N., and Tavernarakis, N. (2011). Cellular stress response pathways and ageing: intricate molecular relationships. EMBO J. 30, 2520-2531.
31. Levine, M. T., Eckert, M. L., and Begun, D. J. (2011). Whole-genome expression plasticity across tropical and temperate Drosophila melanogaster populations from Eastern Australia. Mol. Biol. Evol. 28, 249-256.
32. Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) Method. Methods 25, 402-408.
33. Mao, C., and Obeid, L. M. (2008). Ceramidases: regulators of cellular responses mediated by ceramide, sphingosine, and sphingosine-1-phosphate. Biochim. Biophys. Acta 1781, 424-434.
34. McCarthy, D. J., and Smyth, G. K. (2009). Testing significance relative to a fold-change threshold is a TREAT. Bioinformatics 25, 765-771.
35. Meinelt, T., Paul, A., Phan, T. M., Zwirnmann, E., Krüger, A., Wienke, A., and Steinberg, C. E. W. (2007). Reduction in vegetative growth of the water mold Saprolegnia parasitica (Coker) by humic substance of different qualities. Aquat. Toxicol. 83, 93-103.
36. Melendez, A., Talloczy, Z., Seaman, M., Eskelinen, E. L., Hall, D. H., and Levine, B. (2003). Autophagy genes are essential for dauer development and life-span extension in C. elegans. Science 301, 1387-1391.
37. Menzel, R., Menzel, S., Tiedt, S., Kubsch, G., Stößer, R., Bährs, H., Putschew, A., Saul, N., and Steinberg, C. E. W. (2011). Enrichment of humic material with hydroxybenzene moieties intensifies its physiological effects on the nematode Caenorhabditis elegans. Environ. Sci. Technol. 45, 8707-8715.
38. Menzel, R., Rödel, M., Kulas, J., and Steinberg, C. E. W. (2005). CYP35: xenobiotically induced gene expression in the nematode Caenorhabditis elegans. Arch. Biochem. Biophys. 438, 93-102.
39. Murphy, C. T., Mccarroll, S. A., Bargmann, C. I., Fraser, A., Kamath, R. S., Ahringer, J., Li, H., and Kenyon, C. (2003). Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 424, 277-283.
40. Pietsch, K., Saul, N., Chakrabarti, S., Stürzenbaum, S. R., Menzel, R., and Steinberg, C. E. W. (2011). Hormetins, antioxidants and prooxidants: defining quercetin-, caffeic acid- and rosmarinic acid-mediated life extension in C. elegans. Biogerontology 12, 329-347.
41. Pietsch, K., Saul, N., Menzel, R., Stürzenbaum, S. R., and Steinberg, C. E. W. (2009). Quercetin mediated lifespan extension in Caenorhabditis elegans is modulated by age-1, daf-2, sek-1 and unc-43. Biogerontology 10, 565-578.
42. Pietsch, K., Saul, N., Swain, S., Menzel, R., Steinberg, C. E. W., and Stürzenbaum, S. R. (2012). Ruling aging with polyphenols: meta-analysis of global transcriptional responses reveals conserved genetic pathways as mediators for quercetin and tannic acid effected longevity in C. elegans. Front. Genet. 3, 48.
43. Rainer, J., Sanchez-Cabo, F., Stocker, G., Sturn, A., and Trajanoski, Z. (2006). CARMAweb: comprehensive R- and bioconductor-based web service for microarray data analysis. Nucleic Acids Res. 34, W498-W503.
44. Rhee, S. Y., Wood, V., Dolinski, K., and Draghici, S. (2008). Use and misuse of the gene ontology annotations. Nat. Rev. Genet. 9, 509-515.
45. Saul, N., Pietsch, K., Menzel, R., Stürzenbaum, S. R., and Steinberg, C. E. W. (2009). Catechin induced longevity in C. elegans: from key regulator genes to disposable soma. Mech. Ageing Dev. 130, 477-486.
46. Saul, N., Pietsch, K., Menzel, R., Stürzenbaum, S. R., and Steinberg, C. E. W. (2010). The longevity effect of tannic acid in Caenorhabditis elegans: disposable soma meets hormesis. J. Gerontol. A Biol. Sci. Med. Sci. 65, 626-635.
47. Senoo-Matsuda, N., Yasuda, K., Tsuda, M., Ohkubo, T., Yoshimura, S., Nakazawa, H., Hartman, P. S., and Ishii, N. (2001). A defect in the cytochrome b large subunit in complex II causes both superoxide anion overproduction and abnormal energy metabolism in Caenorhabditis elegans. J. Biol. Chem. 276, 41553-41558.
48. Shaw, W. M., Luo, S., Landis, J., Ashraf, J., and Murphy, C. T. (2007). The C. elegans TGF-beta dauer pathway regulates longevity via insulin signaling. Curr. Biol. 17, 1635-1645.
49. Shin, H., Lee, H., Fejes, A. P., Baillie, D. L., Koo, H. S., and Jones, S. J. (2011). Gene expression profiling of oxidative stress response of C. elegans aging defective AMPK mutants using massively parallel transcriptome sequencing. BMC Res. Notes 4, 34. doi:10.1186/1756-0500-4-34
50. Solomon, A., Bandhakavi, S., Jabbar, S., Shah, R., Beitel, G. J., and Morimoto, R. I. (2004). Caenorhabditis elegans OSR-1 regulates behavioral and physiological responses to hyperosmotic environments. Genetics 167, 161-170.
51. Steinberg, C. E. W., Saul, N., Pietsch, K., Meinelt, T., Rienau, S., and Menzel, R. (2007). Dissolved humic substances facilitate fish life in extreme aquatic environments and have the potential to extend lifespan of Caenorhabditis elegans. Ann. Environ. Sci. 1, 81-90.
52. Sulston, J. E., and Hodgkin, J. (1988). "Methods," in The nematode Caenorhabditis elegans, ed. W. B. Wood (Cold Spring Harbor: CSHL Press), 587-606.
53. Swain, S., Wren, J. F., Stürzenbaum, S. R., Kille, P., Morgan, A. J., Jager, T., Jonker, M. J., Hankard, P. K., Svendsen, C., Owen, J., Hedley, B. A., Blaxter, M., and Spurgeon, D. J. (2010). Linking toxicant physiological mode of action with induced gene expression changes in Caenorhabditis elegans. BMC Syst. Biol. 4, 32. doi:10.1186/1752-0509-4-32
54. 2+ signaling to determine neuronal asymmetric development in Caenorhabditis elegans. EMBO Rep. 3, 56-62.
55. Tissenbaum, H. A., and Guarente, L. (2001). Increased dosage of a sir-2 gene extends lifespan in Caenorhabditis elegans. Nature 410, 227-230.
56. 38 MAPK regulates expression of immune response genes and contributes to longevity in C. elegans. PLoS Genet. 2, e183. doi:10.1371/journal.pgen.0020183
57. Van Straalen, N. M., and Feder, M. E. (2012). Ecological and evolutionary functional genomics-how can it contribute to the risk assessment of chemicals Environ. Sci. Technol. 46, 3-9.
58. Viswanathan, M., Kim, S. K., Berdichevsky, A., and Guarente, L. (2005). A role for SIR-2.1 regulation of ER stress response genes in determining C. elegans life span. Dev. Cell 9, 605-615.
59. Wiegant, F. A. C., Surinova, S., Ytsma, E., Langelaar-Makkinje, M., Wikman, G., and Post, J. A. (2009). Plant adaptogens increase lifespan and stress resistance in C. elegans. Biogerontology 10, 27-42.
60. Wilson, M. A., Shukitt-Hale, B., Kalt, W., Ingram, D. K., Joseph, J. A., and Wolkow, C. A. (2006). Blueberry polyphenols increase lifespan and thermotolerance in Caenorhabditis elegans. Aging Cell 5, 59-68.