Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
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Caffeine Induces High Expression of cyp-35A Family Genes and Inhibits the Early Larval Development in Caenorhabditis elegans

  • Min, Hyemin (Department of Bioscience and Biotechnology, Konkuk University) ;
  • Kawasaki, Ichiro (Department of Bioscience and Biotechnology, Konkuk University) ;
  • Gong, Joomi (Department of Bioscience and Biotechnology, Konkuk University) ;
  • Shim, Yhong-Hee (Department of Bioscience and Biotechnology, Konkuk University)
  • Received : 2014.10.24
  • Accepted : 2014.11.25
  • Published : 2015.03.31
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Abstract

Intake of caffeine during pregnancy can cause retardation of fetal development. Although the significant influence of caffeine on animal development is widely recognized, much remains unknown about its mode of action because of its pleiotropic effects on living organisms. In the present study, by using Caenorhabditis elegans as a model organism, the effects of caffeine on development were examined. Brood size, embryonic lethality, and percent larval development were investigated, and caffeine was found to inhibit the development of C. elegans at most of the stages in a dosage-dependent fashion. Upon treatment with 30 mM caffeine, the majority ($86.1{\pm}3.4%$) of the L1 larvae were irreversibly arrested without further development. In contrast, many of the late-stage larvae survived and grew to adults when exposed to the same 30 mM caffeine. These results suggest that early-stage larvae are more susceptible to caffeine than later-stage larvae. To understand the metabolic responses to caffeine treatment, the levels of expression of cytochrome P450 (cyp) genes were examined with or without caffeine treatment using comparative microarray, and it was found that the expression of 24 cyp genes was increased by more than 2-fold (p < 0.05). Among them, induction of the cyp-35A gene family was the most prominent. Interestingly, depletion of the cyp-35A family genes one-by-one or in combination through RNA interference resulted in partial rescue from early larval developmental arrest caused by caffeine treatment, suggesting that the high-level induction of cyp-35A family genes can be fatal to the development of early-stage larvae.

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References

  1. Aarnio, V., Lehtonen, M., Storvik, M., Callaway, J.C., Lakso, M., and Wong, G. (2011). Caenorhabditis elegans mutants predict regulation of fatty acids and endocannabinoids by the CYP-35A gene family. Front. Pharmacol. 2, 12.
  2. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
  3. Brent, R.L., Christian, M.S., and Diener, R.M. (2011). Evaluation of the reproductive and developmental risks of caffeine. Birth Defects Res. 92, 152-187 https://doi.org/10.1002/bdrb.20288
  4. Cnattingius, S., Signorello, L.B., Anneren, G., Clausson, B., Ekbom, A., Ljunger, E., Blot, W.J., McLaughlin, J.K., Petersson, G., Rane, A., et al. (2000). Caffeine intake and the risk of firsttrimester spontaneous abortion. N. Engl. J. Med. 343, 1839-1845. https://doi.org/10.1056/NEJM200012213432503
  5. Dostal, V., Roberts, C.M., and Link, C.D. (2010). Genetic mechanism of coffee extract protection in a Caenorhabditis elegans model of ${\alpha}$-amyloid peptide toxicity. Genetics 186, 857-866. https://doi.org/10.1534/genetics.110.120436
  6. Giannelli, M., Doyle, P., Roman, E., Pelerin, M., and Hermon, C. (2003). The effect of caffeine consumption and nausea on the risk of miscarriage. Paediatr. Perinat. Epidemiol. 17, 316-323. https://doi.org/10.1046/j.1365-3016.2003.00523.x
  7. Gilbert, R.M., Marshman, J.A., Schweider, M., and Berg, R. (1976). Caffeine content of beverages as consumed. Can. Med. Assoc. J. 114, 205-208
  8. Gotoh, O. (1998). Divergent structures of Caenorhabditis elegans cytochrome P450 genes suggest the frequent loss and gain of introns during the evolution of nematodes. Mol. Biol. Evol. 15, 1447-1459 https://doi.org/10.1093/oxfordjournals.molbev.a025872
  9. Hoyt, A.T., Browne, M., Richardson, S., Romitti, P., Druschel, D. (2014). Maternal caffeine consumption and small for gestational age births: results from a population-based case-control study. Matern. Child Health J. 18, 1540-1551. https://doi.org/10.1007/s10995-013-1397-4
  10. Kawasaki, I., Jeong, M.W., Yun, Y.J., Shin, Y.K., and Shim, Y.H. (2013). Cholesterol-responsive metabolic proteins are required for larval development in Caenorhabditis elegans. Mol. Cells 36, 410-416. https://doi.org/10.1007/s10059-013-0170-2
  11. Knutti, R., Rothweiler, H., and Schlatter, C. (1981). Effect of pregnancy on the pharmacokinetics of caffeine. Eur. J. Clin. Pharmacol. 21, 121-126.
  12. Kot, M., and Daniel, W.A. (2008). The relative contribution of human cytochrome P450 isoforms to the four caffeine oxidation pathways: an in vitro comparative study with cDNA-expressed P450s including CYP2C isoforms. Biochem. Pharmacol. 76, 543-551. https://doi.org/10.1016/j.bcp.2008.05.025
  13. Kwon, J.Y., Hong, M., Choi, M.S., Kang, S., Duke, K., Kim, S., Lee, S., and Lee J. (2004). Ethanol-response genes and their regulation analyzed by a microarray and comparative genomic approach in the nematode Caenorhabditis elegans. Genomics 83, 600-614. https://doi.org/10.1016/j.ygeno.2003.10.008
  14. Maeda, I., Kohara, Y., Yamamoto, M., and Sugimoto, A. (2001). Large-scale analysis of gene function in Caenorhabditis elegans by high-throughput RNAi. Curr. Biol. 11, 171-176. https://doi.org/10.1016/S0960-9822(01)00052-5
  15. Menzel, R., Bogaert, T., and Achazi, R. (2001). A systematic gene expression screen of Caenorhabditis elegans cytochrome P450 genes reveals CYP35 as strongly xenobiotic inducible. Arch. Biochem. Biophys. 395, 158-168 https://doi.org/10.1006/abbi.2001.2568
  16. Menzel, R., Rodel, 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. https://doi.org/10.1016/j.abb.2005.03.020
  17. Nehlig, A. (1999). Are we dependent upon coffee and caffeine? A review on human and animal data. Neurosci. Biobehav. Rev. 23, 563-576. https://doi.org/10.1016/S0149-7634(98)00050-5
  18. Nelson, D.R., Zeldin, D.C., Hoffman, S.M.G., Maltais, L.J., Wain, H.M., Nebert, D.W. (2004). Comparison of cytochrome P450 (CYP) genes from the mouse and human genomes, including nomenclature recommendations for genes, pseudogenes and alternative-splice variants. Pharmacogenetics. 14, 1-18 https://doi.org/10.1097/00008571-200401000-00001
  19. Pletonen, J., Aarnio, V., Heikkinen, L., Lakso, M., and Wong, G. (2013). Chronic ethalnol exprosure increases cytochrome P-450 and decreases activated in blocked unfolded protein response gene family transcripts in Caenorhabditis elegans. J. Biochem. Mol. Toxicol. 27, 219-228 https://doi.org/10.1002/jbt.21473
  20. Reinke, V., Smith, H.E., Nance, J., Wang, J., Van Doren, C., Begley, R., Jones, S.J.M., Davis, E.B., Schere,r St., Ward, S. et al. (2000). A global profile of germline gene expression in C. elegans. Mol. Cell 6, 605-616. https://doi.org/10.1016/S1097-2765(00)00059-9
  21. Reinke, V., Gil, I.S., Ward, S., and Kazmer, K. (2004). Genome-side germline-enriched and sex-biased expression profiles in Caenorhabditis elegans. Development 131, 311-323.
  22. Shakir, M.A., Fukushige, T., Yasuda, H., Miwa, J., and Siddiqui, S.S. (1993). C. elegans osm-3 gene mediating osmotic avoidance behavior encodes a kinesin-like protein. Neuroreport 4, 891-894. https://doi.org/10.1097/00001756-199307000-00013
  23. Shou, M., Gonzalez, F.J., and Gelboin, H.V. (1996). Stereoselective epoxidation and hydration at the K-region of polycyclic aromatic hydrocarbons by cDNA-expressed cytochromes P450 1A1, 1A2, and epoxide hydrolase. Biochemistry 35, 15807-15813. https://doi.org/10.1021/bi962042z
  24. Speith, J., and Blumenthal, T. (1985). The Caenorhabditis elegans vitellogenin gene family includes a gene encoding a distantly related protein. Mol. Cell. Biol. 5, 2495-2501. https://doi.org/10.1128/MCB.5.10.2495
  25. Sutphin, G.L., Bishop, E., Yanos, M.E., Moller, R.M., and Kaeberlein, M. (2012). Caffeine extends life span, improves healthspan, and delays age-associated pathology in Caenorhabditis elegans. Longev. Healthspan 1, 1-9 https://doi.org/10.1186/2046-2395-1-1
  26. The C. elegans Sequencing Consortium. (1998). Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282, 2012-2018 https://doi.org/10.1126/science.282.5396.2012
  27. Weinberg, B.A., and Bealer, B.K. (2002). The caffeine advantage (NY, USA: The Free press).
  28. Wicks, S.R., de Vries, C.J., van Luenen, H.G.A.M., and Plasterk, R.H.A. (2000). CHE-3, a cytosolic dynein heavy chain, is required for sensory cilia structure and function in Caenorhabditis elegans. Dev. Biol. 221, 295-307 https://doi.org/10.1006/dbio.2000.9686

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