Fol. Biol. 2018, 64, 46-58

https://doi.org/10.14712/fb2018064020046

ALKB-8, a 2-Oxoglutarate-Dependent Dioxygenase and S-Adenosine Methionine-Dependent Methyltransferase Modulates Metabolic Events Linked to Lysosome-Related Organelles and Aging in C. elegans

J. Kollárová1, Marta Kostrouchová1,2, A. Benda3, Markéta Kostrouchová1

1BIOCEV, First Faculty of Medicine, Charles University, Vestec, Czech Republic
2Department of Pathology, Third Faculty of Medicine, Charles University, Prague, Czech Republic
3Imaging Methods Core Facility, BIOCEV, Faculty of Science, Charles University, Prague, Czech Republic

Received May 2018
Accepted May 2018

References

1. Aravind, L., Koonin, E. V. (2001) The DNA-repair protein AlkB, EGL-9, and leprecan define new families of 2-oxoglutarate- and iron-dependent dioxygenases. Genome Biol. 2, research0007. <https://doi.org/10.1186/gb-2001-2-3-research0007>
2. Ashrafi, K., Chang, F. Y., Watts, J. L., Fraser, A. G., Kamath, R. S., Ahringer, J., Ruvkun, G. (2003) Genome-wide RNAi analysis of Caenorhabditis elegans fat regulatory genes. Nature 421, 268-272. <https://doi.org/10.1038/nature01279>
3. Brenner, S. (1974) The genetics of Caenorhabditis elegans. Genetics 77, 71-94. <https://doi.org/10.1093/genetics/77.1.71>
4. Buettner, C., Harney, J. W., Berry, M. J. (1999) The Caenorhabditis elegans homologue of thioredoxin reductase contains a selenocysteine insertion sequence (SECIS) element that differs from mammalian SECIS elements but directs selenocysteine incorporation. J. Biol. Chem. 274, 21598-21602. <https://doi.org/10.1074/jbc.274.31.21598>
5. Byrne, A. B., Weirauch, M. T., Wong, V., Koeva, M., Dixon, S. J., Stuart, J. M., Roy, P. J. (2007) A global analysis of genetic interactions in Caenorhabditis elegans. J. Biol. 6, 8. <https://doi.org/10.1186/jbiol58>
6. Chan, C. T. , Dyavaiah, M., DeMott, M. S., Taghizadeh, K., Dedon, P. C., Begley, T. J. (2010) A quantitative systems approach reveals dynamic control of tRNA modifications during cellular stress. PLoS Genet. 6, e1001247. <https://doi.org/10.1371/journal.pgen.1001247>
7. Chan, C. T., Pang, Y. L., Deng, W., Babu, I. R., Dyavaiah, M., Begley, T. J., Dedon, P. C. (2012) Reprogramming of tRNA modifications controls the oxidative stress response by codon- biased translation of proteins. Nat. Commun. 3, 937. <https://doi.org/10.1038/ncomms1938>
8. Church, C., Moir, L., McMurray, F., Girard, C., Banks, G. T., Teboul, L., Wells, S., Bruning, J. C., Nolan, P. M., Ashcroft, F. M., Cox, R. D. (2010) Overexpression of Fto leads to increased food intake and results in obesity. Nat. Genet. 42, 1086-1092. <https://doi.org/10.1038/ng.713>
9. Cunniff, B., Snider, G. W., Fredette, N., Stumpff, J., Hondal, R.J., Heintz, N. H. (2014) Resolution of oxidative stress by thioredoxin reductase: cysteine versus selenocysteine. Redox Biol. 2, 475-484. <https://doi.org/10.1016/j.redox.2014.01.021>
10. Deng, W., Babu, I. R., Su, D., Yin, S., Begley, T.J., Dedon, P. C. (2015) Trm9-catalyzed tRNA modifications regulate global protein expression by codon-biased translation. PLoS Genet. 11, e1005706. <https://doi.org/10.1371/journal.pgen.1005706>
11. Endres, L., Begley, U., Clark, R., Gu, C., Dziergowska, A., Malkiewicz, A., Melendez, J. A., Dedon, P. C., Begley, T. J. (2015) Alkbh8 regulates selenocysteine-protein expression to protect against reactive oxygen species damage. PLoS One 10, e0131335. <https://doi.org/10.1371/journal.pone.0131335>
12. Fabrizio, P., Hoon, S., Shamalnasab, M., Galbani, A., Wei, M., Giaever, G., Nislow, C., Longo, V. D. (2010) Genomewide screen in Saccharomyces cerevisiae identifies vacuolar protein sorting, autophagy, biosynthetic, and tRNA methylation genes involved in life span regulation. PLoS Genet. 6, e1001024. <https://doi.org/10.1371/journal.pgen.1001024>
13. Fedeles, B. I., Singh, V., Delaney, J. C., Li, D., Essigmann, J. M. (2015) The AlkB family of Fe(II)/α-ketoglutarate-de- pendent dioxygenases: repairing nucleic acid alkylation damage and beyond. J. Biol. Chem. 290, 20734-20742. <https://doi.org/10.1074/jbc.R115.656462>
14. Fire, A., Xu, S., Montgomery, M. K., Kostas, S. A., Driver, S. E., Mello, C. C. (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391, 806-811. <https://doi.org/10.1038/35888>
15. Frayling, T. M., Timpson, N. J., Weedon, M. N., Zeggini, E., Freathy, R. M., Lindgren, C. M., Perry, J. R., Elliott, K. S., Lango, H., Rayner, N. W., Shields, B., Harries, L. W., Barrett, J. C., Ellard, S., Groves, C. J., Knight, B., Patch, A. M., Ness, A. R., Ebrahim, S., Lawlor, D. A., Ring, S. M., Ben-Shlomo, Y., Jarvelin, M. R., Sovio, U., Bennett, A. J., Melzer, D., Ferrucci, L., Loos, R. J., Barroso, I., Wareham, N. J., Karpe, F., Owen, K. R., Cardon, L. R., Walker, M., Hitman, G. A., Palmer, C. N., Doney, A. S., Morris, A. D., Smith, G. D., Hattersley, A. T., McCarth,y M. I. (2007) A common variant in the FTO gene is associated with body mass index and predisposes to childhood and adult obesity. Science 316, 889-894. <https://doi.org/10.1126/science.1141634>
16. Fu, D., Brophy, J. A., Chan, C. T., Atmore, K. A., Begley, U., Paules, R. S., Dedon, P. C., Begley, T. J., Samson, L. D. (2010a) Human AlkB homolog ABH8 is a tRNA methyltransferase required for wobble uridine modification and DNA damage survival. Mol. Cell. Biol. 30, 2449-2459. <https://doi.org/10.1128/MCB.01604-09>
17. Fu, Y., Dai, Q., Zhang, W., Ren, J., Pan, T., He, C. (2010b) The AlkB domain of mammalian ABH8 catalyzes hydroxylation of 5-methoxycarbonylmethyluridine at the wobble position of tRNA. Angew Chem. Int. Ed. Engl. 49, 8885-8888. <https://doi.org/10.1002/anie.201001242>
18. Gerken, T., Girard, C. A., Tung, Y. C., Webby, C. J., Saudek, V., Hewitson, K. .S, Yeo, G. S., McDonough, M. A., Cunliffe, S., McNeill, L. A., Galvanovskis, J., Rorsman, P., Robins P, Prieur X, Coll AP, Ma M, Jovanovic Z, Farooqi IS, Sedgwick B, Barroso I, Lindahl, T., Ponting, C. P., Ashcroft, F. M., O’Rahilly, S., Schofield, C. J. (2007) The obesity- associated FTO gene encodes a 2-oxoglutarate-dependent nucleic acid demethylase. Science 318, 1469-1472. <https://doi.org/10.1126/science.1151710>
19. Gu, C., Begley, T. J., Dedon, P. C. (2014) tRNA modifications regulate translation during cellular stress. FEBS Lett. 588, 4287-4296. <https://doi.org/10.1016/j.febslet.2014.09.038>
20. Jee, C., Vanoaica, L., Lee, J., Park, B. .J, Ahnn, J. (2005) Thioredoxin is related to life span regulation and oxidative stress response in Caenorhabditis elegans. Genes Cells 10, 1203-1210. <https://doi.org/10.1111/j.1365-2443.2005.00913.x>
21. Kalhor, H. R., Clarke, S. (2003) Novel methyltransferase for modified uridine residues at the wobble position of tRNA. Mol. Cell. Biol. 23, 9283-9292. <https://doi.org/10.1128/MCB.23.24.9283-9292.2003>
22. Leihne, V., Kirpekar, F., Vagbo, C. B., van den Born, E., Krokan, H. E., Grini, P. E., Meza, T. J., Falnes, P. O. (2011) Roles of Trm9- and ALKBH8-like proteins in the formation of modified wobble uridines in Arabidopsis tRNA. Nucleic Acids Res. 39, 7688-7701. <https://doi.org/10.1093/nar/gkr406>
23. Li, W., Bandyopadhyay, J., Hwaang, H. S., Park, B. J., Cho, J. H., Lee, J. I., Ahnn, J., Lee, S. K. (2012) Two thioredoxin reductases, trxr-1 and trxr-2, have differential physiological roles in Caenorhabditis elegans. Mol. Cells 34, 209-218. <https://doi.org/10.1007/s10059-012-0155-6>
24. Miranda-Vizuete, A., Fierro Gonzalez, J. C., Gahmon, G., Burghoorn, J., Navas, P., Swoboda, P. (2006) Lifespan decrease in a Caenorhabditis elegans mutant lacking TRX-1, a thioredoxin expressed in ASJ sensory neurons. FEBS Lett. 580, 484-490. <https://doi.org/10.1016/j.febslet.2005.12.046>
25. Pastore, C., Topalidou, I., Forouhar, F., Yan, A. C., Levy, M., Hunt, J. F. (2012) Crystal structure and RNA binding properties of the RNA recognition motif (RRM) and AlkB domains in human AlkB homolog 8 (ABH8), an enzyme catalyzing tRNA hypermodification. J. Biol. Chem. 287, 2130-2143. <https://doi.org/10.1074/jbc.M111.286187>
26. Patil, A., Chan, C. T., Dyavaiah, M., Rooney, J. P., Dedon, P. C., Begley, T. J. (2012) Translational infidelity-induced protein stress results from a deficiency in Trm9-catalyzed tRNA modifications. RNA Biol. 9, 990-1001. <https://doi.org/10.4161/rna.20531>
27. Peters, T., Ausmeier, K., Ruther, U. (1999) Cloning of Fatso (Fto), a novel gene deleted by the Fused toes (Ft) mouse mutation. Mamm. Genome 10, 983-986. <https://doi.org/10.1007/s003359901121>
28. Porta-de-la-Riva, M., Fontrodona, L., Villanueva, A., Ceron, J. (2012) Basic Caenorhabditis elegans methods: synchronization and observation. J. Vis. Exp. 64, e4019.
29. Shimada, K., Nakamura, M., Anai, S., De Velasco, M., Tanaka, M., Tsujikawa, K., Ouji, Y., Konishi, N. (2009) A novel human AlkB homologue, ALKBH8, contributes to human bladder cancer progression. Cancer Res. 69, 3157-3164. <https://doi.org/10.1158/0008-5472.CAN-08-3530>
30. Simmer, F., Tijsterman, M., Parrish, S., Koushika, S. P., Nonet, M. L., Fire, A, Ahringer, J., Plasterk, R. H. (2002) Loss of the putative RNA-directed RNA polymerase RRF-3 makes C. elegans hypersensitive to RNAi. Curr. Biol. 12, 1317-1319. <https://doi.org/10.1016/S0960-9822(02)01041-2>
31. Smemo, S., Tena, J. J., Kim, K. H., Gamazon, E. R., Sakabe, N. J., Gomez-Marin, C., Aneas, I., Credidio, F. L., Sobreira, D. R., Wasserman, N. F., Lee, J. H., Puviindran, V., Tam, D., Shen, M., Son, J. E., Vakili, N. A., Sung, H. K., Naranjo, S., Acemel, R. D., Manzanares, M., Nagy, A., Cox, N. J., Hui, C. C., Gomez-Skarmeta, J. L., Nobrega, M. A. (2014) Obesity-associated variants within FTO form long-range functional connections with IRX3. Nature 507, 371-375. <https://doi.org/10.1038/nature13138>
32. Songe-Moller, L., van den Born, E., Leihne, V., Vagbo, C. B., Kristoffersen, T., Kroka,n H. E., Kirpekar, F., Falnes, P. O., Klungland, A. (2010) Mammalian ALKBH8 possesses tRNA methyltransferase activity required for the biogenesis of multiple wobble uridine modifications implicated in translational decoding. Mol. Cell. Biol. 30, 1814-1827. <https://doi.org/10.1128/MCB.01602-09>
33. Soukas, A. A., Carr, C. E., Ruvkun, G. (2013) Genetic regulation of Caenorhabditis elegans lysosome related organelle function. PLoS Genet. 9, e1003908. <https://doi.org/10.1371/journal.pgen.1003908>
34. Tabara, H., Sarkissian, M., Kelly, W. G., Fleenor, J., Grishok, A., Timmons, L., Fire, A., Mello, C. C. (1999) The rde-1 gene, RNA interference, and transposon silencing in C. elegans. Cell 99, 123-132. <https://doi.org/10.1016/S0092-8674(00)81644-X>
35. Timmons, L., Court, D. L., Fire, A. (2001) Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263, 103-112. <https://doi.org/10.1016/S0378-1119(00)00579-5>
36. van den Born, E., Vagbo, C. B., Songe-Moller, L., Leihne, V., Lien, G. F., Leszczynsk,a G., Malkiewicz, A., Krokan, H. E., Kirpekar, F., Klungland, A., Falnes, P. O. (2011) ALKBH8-mediated formation of a novel diastereomeric pair of wobble nucleosides in mammalian tRNA. Nat. Commun. 2, 172. <https://doi.org/10.1038/ncomms1173>
37. Van Gilst, M. R., Hadjivassiliou, H., Yamamoto, K. R. (2005) A Caenorhabditis elegans nutrient response system partially dependent on nuclear receptor NHR-49. Proc. Natl. Acad. Sci. USA 102, 13496-13501. <https://doi.org/10.1073/pnas.0506234102>
38. Vohanka, J., Simeckova, K., Machalova, E., Behensky, F., Krause, M. W., Kostrouch, Z., Kostrouchova, M. (2010) Diversification of fasting regulated transcription in a cluster of duplicated nuclear hormone receptors in C. elegans. Gene Expr. Patterns 10, 227-236. <https://doi.org/10.1016/j.gep.2010.05.001>
39. Wilhelm, T., Byrne, J., Medina, R., Kolundzic, E., Geisinger, J., Hajduskova, M., Tursun, B., Richly, H. (2017) Neuronal inhibition of the autophagy nucleation complex extends life span in post-reproductive C. elegans. Genes Dev. 31, 1561-1572. <https://doi.org/10.1101/gad.301648.117>
40. Yajnik, C. S., Janipalli, C. S., Bhaskar, S., Kulkarni, S. R., Freathy, R. M., Prakash, S., Mani, K. R., Weedon, M. N., Kale, S. D., Deshpande, J., Krishnaveni, G. V., Veena, S. R., Fall, C. H., McCarthy, M. I., Frayling, T. M., Hattersley, A. T., Chandak, G. R. (2009) FTO gene variants are strongly associated with type 2 diabetes in South Asian Indians. Diabetologia 52, 247-252. <https://doi.org/10.1007/s00125-008-1186-6>
41. Zdzalik, D., Vagbo, C. B., Kirpekar, F., Davydova, E., Puscian, A., Maciejewska, A. M., Krokan, H. E., Klungland, A., Tudek, B., van den Born, E., Falnes, P. O. (2014) Protozoan ALKBH8 oxygenases display both DNA repair and tRNA modification activities. PLoS One 9, e98729. <https://doi.org/10.1371/journal.pone.0098729>
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