The atomic resolution structure of human alkb homolog 7 (ALKBH7), a key protein for programmed necrosis and fat metabolism

Journal of Biological Chemistry

Volumn 289, Issue 40, 2014, Pages 27924-27936

  Wang, Guoqiang ^a   He, Qingzhong ^b   Feng, Chong ^a   Liu, Yang ^a   Deng, Zengqin ^a   Qi, Xiaoxuan ^a   Wu, Wei ^a   Mei, Pinchao ^b   Chen, Zhongzhou ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b PEKING UNION MEDICAL COLLEGE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALKYLATION; CELL DEATH; CELL MEMBRANES; HYDROXYLATION; MANGANESE; METABOLISM; MITOCHONDRIA; NUCLEIC ACIDS; PROTEINS; SUBSTRATES;

ATOMIC RESOLUTION STRUCTURES; FAT METABOLISM; GENETIC ABLATION; METABOLIC DISEASE; MITOCHONDRIAL MEMBRANE POTENTIAL; NEGATIVELY CHARGED; PROTEIN SUBSTRATE; STRUCTURAL BASIS;

CRYSTAL ATOMIC STRUCTURE;

ALKB HOMOLOG 7; DIOXYGENASE; GLYCINE DERIVATIVE; IRON; LEUCINE; MANGANESE; MITOCHONDRIAL PROTEIN; N OXALYLGLYCINE; NUCLEIC ACID; NUCLEIC ACID BASE; PROTEIN; UNCLASSIFIED DRUG; 2 OXOGLUTARIC ACID; ALKBH7 PROTEIN, HUMAN; FAT;

ALKYLATION; ARTICLE; BETA SHEET; BODY WEIGHT; CELL DEATH; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA DAMAGE; DRUG DESIGN; ENZYME SUBSTRATE; FAT MASS; HYDROXYLATION; LIPID METABOLISM; METABOLIC DISORDER; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; NUCLEOTIDE RECOGNITION LID; OXIDATION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN STRUCTURE; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME ACTIVE SITE; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; NECROSIS; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE; SEQUENCE ALIGNMENT; X RAY CRYSTALLOGRAPHY; X RAY DIFFRACTION;

AMINO ACID SEQUENCE; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; FATS; HUMANS; KETOGLUTARIC ACIDS; MANGANESE; MITOCHONDRIAL PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NECROSIS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; SEQUENCE ALIGNMENT; X-RAY DIFFRACTION;

EID: 84907482246     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.590505     Document Type: Article

References (54)

1. Kroemer, G., Galluzzi, L., Vandenabeele, P., Abrams, J., Alnemri, E. S., Baehrecke, E. H., Blagosklonny, M. V., El-Deiry, W. S., Golstein, P., Green, D. R, Hengartner, M., Knight, R. A., Kumar, S., Lipton, S. A., Malorni, W., Nuñez, G., Peter, M. E., Tschopp, J., Yuan, J., Piacentini, M., Zhivotovsky, B., Melino, G., and Nomenclature Committee on Cell Death 2009 (2009) Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death. Differ. 16, 3-11
2. Dunai, Z., Bauer, P. I., and Mihalik, R. (2011) Necroptosis: biochemical, physiological and pathological aspects. Pathol. Oncol. Res. 17, 791-800
3. Ha, H. C., and Snyder, S. H. (1999) Poly(ADP-ribose) polymerase is a mediator of necrotic cell death by ATP depletion. Proc. Natl. Acad. Sci. U.S.A. 96, 13978-13982
4. Cipriani, G., Rapizzi, E., Vannacci, A., Rizzuto, R., Moroni, F., and Chiarugi, A. (2005) Nuclear poly(ADP-ribose) polymerase-1 rapidly triggers mitochondrial dysfunction. J. Biol. Chem. 280, 17227-17234
5. Alano, C. C., Gamier, P., Ying, W., Higashi, Y., Kauppinen, T. M., and Swanson, R. A. (2010) NAD+ depletion is necessary and sufficient for poly(ADP-ribose) polymerase-1-mediated neuronal death.J. Neurosci. 30, 2967-2978
6. Kreuzaler, P., and Watson, C. J. (2012) Killing a cancer: what are the alternatives? Nat. Rev. Cancer 12, 411-424
7. Fu, D., Jordan, J. J., and Samson, L. D. (2013) Human ALKBH7 is required for alkylation- and oxidation-induced programmed necrosis. Gene Dev. 27,1089-1100
8. Solberg, A., Robertson, A. B., Aronsen, J. M., Rognmo, Ø., Sjaastad, I., Wisløff, U., and Klungland, A. (2013) Deletion of mouse Alkbh7 leads to obesity. J Mol. Cell Biol. 5,194-203
9. Kurowski, M. A., Bhagwat, A. S., Papaj, G., and Bujnicki, J. M. (2003) Phylogenomic identification of five new human homologs of the DNA repair enzyme AlkB. BMC Genomics 4, 48
10. Sanchez-Pulído, L, and Andrade-Navarro, M. A. (2007) The FTO (fat mass and obesity associated) gene codes for a novel member of the nonheme dioxygenase superfamily. BMC Biochem. 8, 23
11. Loenarz, C., and Schofield, C. J. (2011) Physiological and biochemical aspects of hydroxylations and demethylations catalyzed by human 2-oxo-glutarate oxygenases. Trends Biochem. Sci. 36, 7-18
12. Faines, P. Ø., Johansen, R. F., and Seeberg, E. (2002) AlkB-mediated oxidative demethylation reverses DNA damage in Escherichia coli. Nature 419,178-182
13. Delaney, J. C., and Essigmann, J. M. (2004) Mutagenesis, genotoxicity, and repair of 1-methyladenine, 3-alkylcytosines, 1 -methylguanine, and 3-methylthymine in alkB Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 101, 14051-14056
14. Delaney, J. C., Smeester, L., Wong, C., Frick, L. E., Taghizadeh, K., Wishnok, J. S., Drennan, C. L., Samson, L. D., and Essigmann, J. M. (2005) AlkB reverses etheno DNA lesions caused by lipid oxidation in vitro and in vivo. Nat. Struct. Mol. Biol. 12, 855-860
15. Westbye, M. P., Feyzi, E., Aas, P. A., Vågbø, C. B., Talstad, V. A., Kavli, B., Hagen, L., Sundheim, O., Akbari, M., Liabakk, N. B., Slupphaug, G., Otterlei, M., and Krokan, H. E. (2008) Human AlkB homolog lisa mitochondrial protein that demethylates 3-methylcytosine in DNA and RNA. J. Biol. Chem. 283, 25046-25056
16. Müller, T. A., Meek, K., and Hausinger, R. P. (2010) Human AlkB homologue 1 (ABH1) exhibits DNA lyase activity at abasic sites. DNA Repair 9, 58-65
17. Duncan, T., Trewick, S. C., Koivisto, P., Bates, P. A., Lindahl, T., and Sedgwick, B. (2002) Reversal of DNA alkylation damage by two human dioxygenases. Proc. Natl. Acad. Sci. U.S.A. 99, 16660-16665
18. Monsen, V. T., Sundheim, O., Aas, P. A., Westbye, M. P., Sousa, M. M., Slupphaug, G., and Krokan, H. E. (2010) Divergent ss-hairpins determine double-strand versus single-strand substrate recognition of human AlkB-homologues 2 and 3. Nucleic Acids Res. 38, 6447-6455
19. Sundheim, O., Vågbo, C. B., Bjørås, M., Sousa, M. M., Talstad, V., Aas, P. A., Drabløs, F., Krokan, H. E., Tainer, J. A., and Slupphaug, G. (2006) Human ABH3 structure and key residues for oxidative demethylation to reverse DNA/RNA damage. EMBO J. 25, 3389 -3397
20. Yang, C. G., Yi, C., Duguid, E. M., Sullivan, C. T., Jian, X., Rice, P. A., and He, C. (2008) Crystal structures of DNA/RNA repair enzymes AlkB and ABH2 bound to dsDNA. Nature 452, 961-965
21. Jia, G., Fu, Y., Zhao, X., Dai, Q., Zheng, G., Yang, Y., Yi, C., Lindahl, T., Pan, T., Yang, Y. G., and He, C. (2011) N6-Methyladenosine in nuclear RNA is a major substrate of the obesity-associated FTO. Nat. Chem. Biol. 7, 885-887
22. Zheng, G., Dahl, J. A., Niu, Y., Fedorcsak, P., Huang, C. M., Li, C. J., Vågbo, C. B., Shi, Y., Wang, W. L., Song, S. H., Lu, Z., Bosmans, R. P., Dai, Q., Hao, Y. J, Yang, X., Zhao, W. M., Tong, W. M., Wang, X. J., Bogdan, F., Furu, K., Fu, Y., Jia, G., Zhao, X., Liu, J., Krokan, H. E., Klungland, A., Yang, Y. G., and He, C. (2013) ALKBH5 is a mammalian RNA demethylase that impacts RNA metabolism and mouse fertility. Mol. Cell 49,18 -29
23. Fu, Y., Dai, Q., Zhang, W., Ren, J., Pan, T., and He, C. (2010) The AlkB domain of mammalian ABH8 catalyzes hydroxylation of 5-methoxycar-bonylmethyluridine at the wobble position of tRNA.Angew. Chem. Int. Ed. Engl. 49, 8885-8888
24. Lee, D. H., Jin, S. G., Cai, S., Chen, Y., Pfeifer, G. P., and O'Connor, T. R. (2005) Repair of methylation damage in DNA and RNA by mammalian AlkB homologues.J. Biol. Chem. 280, 39448-39459
25. Ringvoll, J., Nordstrand, L. M., Vågbø, C. B., Talstad, V., Reite, K., Aas, P. A., Lauritzen, K. H., Liabakk, N. B., Bjørk, A., Doughty, R. W., Faines, P. Ø., Krokan, H. E., and Klungland, A. (2006) Repair deficient mice reveal mABH2 as the primary oxidative demethylase for repairing ImeA and 3meC lesions in DNA. EMBO J. 25, 2189-2198
26. Johannessen, T. C., Prestegarden, L., Grudic, A., Hegi, M. E., Tysnes, B. B., and Bjerkvig, R. (2013) The DNA repair protein ALKBH2 mediates temozolomide resistance in human glioblastoma cells. Neuro-oncology 15, 269-278
27. Dango, S., Mosammaparast, N., Sowa, M. E., Xiong, L. J., Wu, F., Park, K., Rubin, M., Gygi, S., Harper, J. W., and Shi, Y. (2011) DNA unwinding by ASCC3 helicase is coupled to ALKBHS-dependent DNA alkylation repair and cancer cell proliferation. Mol. Cell 44, 373-384
28. Fu, D., Brophy, J. A., Chan, C. T., Atmore, K. A., Begley, U., Paules, R. S., Dedon, P. C., Begley, T. J., and Samson, L. D. (2010) Human AlkB homolog ABH8 is a tRNA methyltransferase required for wobble uridine modification and DNA damage survival. Mol. Cell. Biol. 30, 2449-2459
29. Fischer, J., Koch, L., Emmerling, C., Vierkotten, J., Peters, T., Brüning, J. C., and Rüther, U. (2009) Inactivation of the Fto gene protects from obesity. Nature 458, 894-898
30. Wang, J., Kamtekar, S., Berman, A. T-, and Steitz, T. A. (2005) Correction of x-ray intensities from single crystals containing lattice-translocation defects. Acta Crystallogr. D Biol. Crystallogr. 61, 67-74
31. Otwinowski, Z., and Minor, W. (1997) in Methods of Enzymology(Carter, C. W., Jr., ed) pp. 307-326, Academic Press
32. Terwilliger, T. C., and Berendzen, J. (1999) Automated MAD and MIR structure solution. Acta Crystallogr. D Biol. Crystallogr. 55, 849-861
33. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
34. Murshudov, G. N., Skubák, P., Lebedev, A. A., Pannu, N. S., Steiner, R. A., Nicholls, R. A., Winn, M. D., Long, F., and Vagin, A. A. (2011) REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr. 67, 355-367
35. Schrödinger, L. (2010) The PyMOL Molecular Graphics System, Version 1.3, Schrödinger, LLC, New York
36. McDonough, M. A., Loenarz, C., Chowdhury, R., Clifton, I. J., and Schofield, C. J. (2010) Structural studies on human 2-oxoglutarate dependent oxygenases. Curr. Opin. Struct. Biol. 20, 659-672
37. Aik, W., McDonough, M. A., Thalhammer, A., Chowdhury, R., and Schofield, C. J. (2012) Role of the jelly-roll fold in substrate binding by 2-oxo-glutarate oxygenases. Curr. Opin. Struct. Biol. 22, 691-700
38. Aik, W., Scotti, J- S., Choi, H., Gong, L., Demetriades, M., Schofield, C. J., and McDonough, M. A. (2014) Structure of human RNA N(6)-methyladenine demethylase ALKBH5 provides insights into its mechanisms of nucleic acid recognition and demethylation. Nucleic Acids Res. 42, 4741-4754
39. McDonough, M. A., Li, V., Flashman, E., Chowdhury, R., Mohr, C., Liénard, B. M., Zondlo, J., Oldham, N. J., Clifton, I. J., Lewis, J., McNeill, L. A., Kurzeja, R. J., Hewitson, K. S., Yang, E., Jordan, S., Syed, R. S., and Schofield, C. J. (2006) Cellular oxygen sensing: crystal structure of hypoxiainducible factor prolyl hydroxylase (PHD2). Proc. Natl. Acad. Sci. U.S.A. 103, 9814-9819
40. Ougland, R., Lando, D., Jonson, L, Dahl, J. A., Moen, M. N., Nordstrand, L. M., Rognes, T., Lee, J. T., Klungland, A., Kouzarides, T., and Larsen, E. (2012) ALKBH1 is a histone H2A dioxygenase involved in neural differentiation. Stem Cells 30, 2672-2682
41. Li, M. M., Nilsen, A., Shi, Y., Fusser, M., Ding, Y. H., Fu, Y., Liu, B., Niu, Y., Wu, Y. S., Huang, C. M., Olofsson, M., Jin, K. X., Lv, Y., Xu, X. Z., He, C., Dong, M. Q., Rendtlew Danielsen, J. M., Klungland, A., and Yang, Y. G. (2013) ALKBH4-dependent demethylation of actin regulates actomyosin dynamics. Nat. Commun. 4,1832
42. Yu, B., Edstrom, W. C., Benach, J., Hamuro, Y., Weber, P. C., Gibney, B. R., and Hunt, J. F. (2006) Crystal structures of catalytic complexes of the oxidative DNA/RNA repair enzyme AlkB. Nature 439, 879 - 884
43. Han, Z., Niu, T., Chang, J., Lei, X., Zhao, M., Wang, Q., Cheng, W., Wang, J., Feng, Y., and Chai, J. (2010) Crystal structure of the FTO protein reveals basis for its substrate specificity. Nature 464,1205-1209
44. Feng, C, Liu, Y., Wang, G., Deng, Z., Zhang, Q., Wu, W., Tong, Y., Cheng, C., and Chen, Z. (2014) Crystal structures of the human RNA demethylase Alkbh5 reveal basis for substrate recognition. J. Biol. Chem. 289, 11571-11583
45. Holland, P. J., and Hollis, T. (2010) Structural and mutational analysis of Escherichia coli AlkB provides insight into substrate specificity and DNA damage searching. PLoS ONE 5, e8680
46. Pastore, C., Topalidou, I., Forouhar, F., Yan, A. C., Levy, M., and 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
47. Holm, L., and Rosenström, P. (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res. 38, W545-W549
48. Chowdhury, R., McDonough, M. A., Mecinovic, J., Loenarz, C., Flashman, E., Hewitson, K. S., Domene, C., and Schofield, C. J. (2009) Structural basis for binding of hypoxia-inducible factor to the oxygen-sensing prolyl hydroxylases. Structure 17, 981-989
49. Bruick, R. K., and McKnight, S. L. (2001) A conserved family of prolyl-4-hydroxylases that modify HIF. Science 294, 1337-1340
50. Epstein, A. C., Gleadle, J. M., McNeill, L. A., Hewitson, K. S., O'Rourke, J., Mole, D. R., Mukherji, M., Metzen, E., Wilson, M. L, Dhanda, A., Tian, Y. M., Masson, N., Hamilton, D. L., Jaakkola, P., Barstead, R., Hodgkin,J., Maxwell, P. H., Pugh, C. W., Schofield, C. J., and Ratcliffe, P. J. (2001) C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 107, 43-54
51. Mantri, M., Zhang, Z., McDonough, M. A., and Schofield, C. J. (2012) Autocatalysed oxidative modifications to 2-oxoglutarate-dependent oxygenases. FEBS J. 279,1563-1575
52. Bjørnstad, L. G., Meza, T. J., Otterlei, M., Olafsrud, S. M., Meza-Zepeda, L. A., and Faines, P. Ø. (2012) Human ALKBH4 interacts with proteins associated with transcription. PLoS One 7, e49045
53. Nakagawa, T., Shimizu, S., Watanabe, T., Yamaguchi, O., Otsu, K., Yamagata, H., Inohara, H., Kubo, T., and Tsujimoto, Y. (2005) Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature 434, 652-658
54. Luvisetto, S., Basso, E., Petronilli, V., Bernardi, P., and Forte, M. (2008) Enhancement of anxiety, facilitation of avoidance behavior, and occurrence of adult-onset obesity in mice lacking mitochondrial cyclophilin D. Neuroscience 155, 585-596