A gatekeeper helix determines the substrate specificity of Sjögren-Larsson Syndrome enzyme fatty aldehyde dehydrogenase

Nature Communications

Volumn 5, Issue , 2014, Pages

  Keller, Markus A ^a,b   Zander, Ulrich ^c   Fuchs, Julian E ^d   Kreutz, Christoph ^d   Watschinger, Katrin ^a   Mueller, Thomas ^d   Golderer, Georg ^a   Liedl, Klaus R ^d   Ralser, Markus ^b,e   Kräutler, Bernhard ^d   Werner, Ernst R ^a   Marquez, Jose A ^c,f  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

^d UNIVERSITY OF INNSBRUCK   (Austria)

^e NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^f UNIV GRENOBLE ALPES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE; ALDEHYDE DEHYDROGENASE; COMPLEMENTARY DNA; FATTY ALDEHYDE DEHYDROGENASE; HYDROGEN; UNCLASSIFIED DRUG; LONG-CHAIN-ALDEHYDE DEHYDROGENASE;

BIOACCUMULATION; BIOASSAY; CATALYSIS; ENZYME; FATTY ACID; GENE EXPRESSION; HOMINID; MEMBRANE; MUTATION; NERVOUS SYSTEM DISORDER; SKIN DISORDER; SUBSTRATE; TOXICITY;

AFFINITY CHROMATOGRAPHY; ARTICLE; BINDING SITE; CIRCULAR DICHROISM; CONTROLLED STUDY; COVALENT BOND; CRYSTAL STRUCTURE; CRYSTALLIZATION; CRYSTALLOGRAPHY; DIMERIZATION; ENZYMATIC ASSAY; ENZYME ACTIVE SITE; ENZYME ASSAY; ENZYME SPECIFICITY; ENZYME STRUCTURE; ESCHERICHIA COLI; GATEKEEPER HELIX; HUMAN; HYDROGEN BOND; HYDROPHOBICITY; LIPID BILAYER; MASS SPECTROMETRY; MISSENSE MUTATION; MOLECULAR CLONING; NONHUMAN; NUCLEOPHILICITY; OLIGOMERIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; REACTION ANALYSIS; STOP CODON; X RAY DIFFRACTION; CELL MEMBRANE; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR MODEL; MUTATION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; SJOEGREN LARSSON SYNDROME; X RAY CRYSTALLOGRAPHY;

PYRONIA TITHONUS;

ALDEHYDE OXIDOREDUCTASES; CELL MEMBRANE; CRYSTALLOGRAPHY, X-RAY; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MUTATION; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; SJOGREN-LARSSON SYNDROME; SUBSTRATE SPECIFICITY;

EID: 84921469183     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5439     Document Type: Article

References (70)

1. Perozich, J., Nicholas, H., Wang, B. C., Lindahl, R. & Hempel, J. Relationships within the aldehyde dehydrogenase extended family. Protein Sci. 8, 137-146 (1999).
2. Demozay, D., Mas, J.-C., Rocchi, S. & Van Obberghen, E. FALDH reverses the deleterious action of oxidative stress induced by lipid peroxidation product 4-hydroxynonenal on insulin signaling in 3T3-L1 adipocytes. Diabetes 57, 1216-1226 (2008).
3. Nakahara, K. et al. The Sjögren-Larsson syndrome gene encodes a hexadecenal dehydrogenase of the sphingosine 1-phosphate degradation pathway. Mol. Cell 46, 461-471 (2012).
4. Rizzo, W. B. & Carney, G. Sjögren-Larsson syndrome: diversity of mutations and polymorphisms in the fatty aldehyde dehydrogenase gene (ALDH3A2). Hum. Mutat. 26, 1-10 (2005).
5. Gordon, N. Sjögren-Larsson syndrome. Dev. Med. Child Neurol. 49, 152-154 (2007).
6. Kihara, A., Mitsutake, S., Mizutani, Y. & Igarashi, Y. Metabolism and biological functions of two phosphorylated sphingolipids, sphingosine 1-phosphate and ceramide 1-phosphate. Prog. Lipid Res. 46, 126-144 (2007).
7. Hait, N. C. et al. Regulation of histone acetylation in the nucleus by sphingosine-1-phosphate. Science 325, 1254-1257 (2009).
8. Warner, H. R. & Lands, W. E. The metabolism of plasmalogen: enzymatic hydrolysis of the vinyl ether. J. Biol. Chem. 236, 2404-2409 (1961).
9. Centemeri, C., Colli, S., Tosarello, D., Ciceri, P. & Nicosia, S. Heterogeneous platelet-activating factor (PAF) receptors and calcium increase in platelets and macrophages. Biochem. Pharmacol. 57, 263-271 (1999).
10. Cheminade, C. et al. 1-O-alkylglycerols improve boar sperm motility and fertility. Biol. Reprod. 66, 421-428 (2002).
11. Mandal, A., Wang, Y., Ernsberger, P. & Kester, M. Interleukin-1-induced ether-linked diglycerides inhibit calcium-insensitive protein kinase C isotypes. Implications for growth senescence. J. Biol. Chem. 272, 20306-20311 (1997).
12. Watschinger, K. et al. Identification of the gene encoding alkylglycerol monooxygenase defines a third class of tetrahydrobiopterin-dependent enzymes. Proc. Natl Acad. Sci. USA 107, 13672-13677 (2010).
13. Ashibe, B., Hirai, T., Higashi, K., Sekimizu, K. & Motojima, K. Dual subcellular localization in the endoplasmic reticulum and peroxisomes and a vital role in protecting against oxidative stress of fatty aldehyde dehydrogenase are achieved by alternative splicing. J. Biol. Chem. 282, 20763-20773 (2007).
14. Liu, Z. J. et al. The first structure of an aldehyde dehydrogenase reveals novel interactions between NAD and the Rossmann fold. Nat. Struct. Biol. 4, 317-326 (1997).
15. Rogers, G. R., Markova, N. G., De Laurenzi, V., Rizzo, W. B. & Compton, J. G. Genomic organization and expression of the human fatty aldehyde dehydrogenase gene (FALDH). Genomics 39, 127-135 (1997).
16. Khanna, M. et al. Discovery of a novel class of covalent inhibitor for aldehyde dehydrogenases. J. Biol. Chem. 286, 43486-43494 (2011).
17. Masaki, R., Yamamoto, A. & Tashiro, Y. Microsomal aldehyde dehydrogenase is localized to the endoplasmic reticulum via its carboxyl-terminal 35 amino acids. J. Cell Biol. 126, 1407-1420 (1994).
18. Keller, M. A. et al. Monitoring of fatty aldehyde dehydrogenase by formation of pyrenedecanoic acid from pyrenedecanal. J. Lipid Res. 51, 1554-1559 (2010).
19. Lloyd, M. D. et al. Characterisation of recombinant human fatty aldehyde dehydrogenase: implications for Sjögren-Larsson syndrome. J. Enzyme Inhib. Med. Chem. 22, 584-590 (2007).
20. Johansson, K. et al. Structure of betaine aldehyde dehydrogenase at 2.1 A resolution. Protein Sci. 7, 2106-2117 (1998).
21. Parajuli, B., Georgiadis, T. M., Fishel, M. L. & Hurley, T. D. Development of selective inhibitors for human aldehyde dehydrogenase 3A1 (ALDH3A1) for the enhancement of cyclophosphamide cytotoxicity. Chembiochem 15, 701-712 (2014).
22. Keller, M. A. et al. Studying fatty aldehyde metabolism in living cells with pyrene-labeled compounds. J. Lipid Res. 53, 1410-1416 (2012).
23. Jones, K. H., Lindahl, R., Baker, D. C. & Timkovich, R. Hydride transfer stereospecificity of rat liver aldehyde dehydrogenases. J. Biol. Chem. 262, 10911-10913 (1987).
24. Shimizu, Y. et al. L-Threonine dehydrogenase from the hyperthermophilic archaeon Pyrococcus horikoshii OT3: gene cloning and enzymatic characterization. Extremophiles 9, 317-324 (2005).
25. Mostad, S. B. & Glasfeld, A. Using high field NMR to determine dehydrogenase stereospecificity with respect to NADH: An undergraduate biochemistry lab. J. Chem. Educ. 70, 504 (1993).
26. Hammen, P. K., Allali-Hassani, A., Hallenga, K., Hurley, T. D. & Weiner, H. Multiple conformations of NAD and NADH when bound to human cytosolic and mitochondrial aldehyde dehydrogenase. Biochemistry 41, 7156-7168 (2002).
27. Esaki, N. et al. Enzymatic in situ determination of stereospecificity of NAD-dependent dehydrogenases. J. Biol. Chem. 264, 9750-9752 (1989).
28. You, K. S. Stereospecificity for nicotinamide nucleotides in enzymatic and chemical hydride transfer reactions. CRC Crit. Rev. Biochem. 17, 313-451 (1985).
29. Marchal, S., Rahuel-Clermont, S. & Branlant, G. Role of glutamate-268 in the catalytic mechanism of nonphosphorylating glyceraldehyde-3-phosphate dehydrogenase from Streptococcus mutans. Biochemistry 39, 3327-3335 (2000).
30. Cobessi, D., Tête-Favier, F., Marchal, S., Branlant, G. & Aubry, A. Structural and biochemical investigations of the catalytic mechanism of an NADPdependent aldehyde dehydrogenase from Streptococcus mutans. J. Mol. Biol. 300, 141-152 (2000).
31. Moore, S. A. et al. Sheep liver cytosolic aldehyde dehydrogenase: the structure reveals the basis for the retinal specificity of class 1 aldehyde dehydrogenases. Structure 6, 1541-1551 (1998).
32. Steinmetz, C. G., Xie, P., Weiner, H. & Hurley, T. D. Structure of mitochondrial aldehyde dehydrogenase: the genetic component of ethanol aversion. Structure 5, 701-711 (1997).
33. Wang, X. & Weiner, H. Involvement of glutamate 268 in the active site of human liver mitochondrial (class 2) aldehyde dehydrogenase as probed by site-directed mutagenesis. Biochemistry 34, 237-243 (1995).
34. Hempel, J. et al. Aldehyde dehydrogenase catalytic mechanism. A proposal. Adv. Exp. Med. Biol. 463, 53-59 (1999).
35. Hempel, J. et al. Aldehyde dehydrogenase. Maintaining critical active site geometry at motif 8 in the class 3 enzyme. Eur. J. Biochem. 268, 722-726 (2001).
36. Mann, C. J. & Weiner, H. Differences in the roles of conserved glutamic acid residues in the active site of human class 3 and class 2 aldehyde dehydrogenases. Protein Sci. 8, 1922-1929 (1999).
37. Sheikh, S., Ni, L., Hurley, T. D. & Weiner, H. The potential roles of the conserved amino acids in human liver mitochondrial aldehyde dehydrogenase. J. Biol. Chem. 272, 18817-18822 (1997).
38. Cho, S. W., Yoon, H. Y., Ahn, J. Y., Choi, S. Y. & Kim, T. U. Identification of an NAD+ binding site of brain glutamate dehydrogenase isoproteins by photoaffinity labeling. J. Biol. Chem. 273, 31125-31130 (1998).
39. Abriola, D. P., Fields, R., Stein, S., MacKerell, Jr. AD & Pietruszko, R. Active site of human liver aldehyde dehydrogenase. Biochemistry 26, 5679-5684 (1987).
40. Farrés, J., Wang, T. T., Cunningham, S. J. & Weiner, H. Investigation of the active site cysteine residue of rat liver mitochondrial aldehyde dehydrogenase by site-directed mutagenesis. Biochemistry 34, 2592-2598 (1995).
41. Hempel, J., Nicholas, H. & Lindahl, R. Aldehyde dehydrogenases: widespread structural and functional diversity within a shared framework. Protein Sci. 2, 1890-1900 (1993).
42. Petrek, M., Kosinová, P., Koca, J. & Otyepka, M. MOLE: a Voronoi diagram-based explorer of molecular channels, pores, and tunnels. Structure 15, 1357-1363 (2007).
43. Rizzo, W. B., Carney, G. & Lin, Z. The molecular basis of Sjögren-Larsson syndrome: mutation analysis of the fatty aldehyde dehydrogenase gene. Am. J. Hum. Genet. 65, 1547-1560 (1999).
44. Duester, G. Genetic dissection of retinoid dehydrogenases. Chem. Biol. Interact.s 130-132, 469-480 (2001).
45. Picot, D., Loll, P. J. & Garavito, R. M. The X-ray crystal structure of the membrane protein prostaglandin H2 synthase-1. Nature 367, 243-249 (1994).
46. Kitamura, T. et al. Substrate specificity, plasma membrane localization, and lipid modification of the aldehyde dehydrogenase ALDH3B1. Biochim. Biophys. Acta 1831, 1395-1401 (2013).
47. Kelson, T. L., Secor McVoy, J. R. & Rizzo, W. B. Human liver fatty aldehyde dehydrogenase: microsomal localization, purification, and biochemical characterization. Biochim. Biophys. Acta 1335, 99-110 (1997).
48. Marchitti, S. A., Orlicky, D. J. & Vasiliou, V. Expression and initial characterization of human ALDH3B1. Biochem. Biophys. Res. Commun. 356, 792-798 (2007).
49. Marchitti, S. A., Brocker, C., Orlicky, D. J. & Vasiliou, V. Molecular characterization, expression analysis, and role of ALDH3B1 in the cellular protection against oxidative stress. Free. Radic. Biol. Med. 49, 1432-1443 (2010).
50. Ikeda, M., Kihara, A. & Igarashi, Y. Sphingosine-1-phosphate lyase SPL is an endoplasmic reticulum-resident, integral membrane protein with the pyridoxal 5′-phosphate binding domain exposed to the cytosol. Biochem. Biophys. Res. Commun. 325, 338-343 (2004).
51. Pappa, A., Estey, T., Manzer, R., Brown, D. & Vasiliou, V. Human aldehyde dehydrogenase 3A1 (ALDH3A1): biochemical characterization and immunohistochemical localization in the cornea. Biochem. J. 376, 615-623 (2003).
52. Didona, B. et al. Novel and recurrent ALDH3A2 mutations in Italian patients with Sjögren-Larsson syndrome. J. Hum. Genet. 52, 865-870 (2007).
53. Engelstad, H. et al. Large contiguous gene deletions in Sjögren-Larsson syndrome. Mol. Genet. Metab. 104, 356-361 (2011).
54. Jean-François, E., Low, J. Y., Gonzales, C. R. & Sarraf, D. Sjögren-larsson syndrome and crystalline maculopathy associated with a novel mutation. Arch. Ophthalmol. 125, 1582-1583 (2007).
55. Nakano, H. et al. A novel homozygous missense mutation in the fatty aldehyde dehydrogenase gene causes Sjögren-Larsson syndrome. J. Dermatol. Sci. 52, 136-138 (2008).
56. Rafai, M. A. et al. [Sjögren-Larsson syndrome: a novel mutation in a Moroccan child]. Arch. Pediatr. 15, 1648-1651 (2008).
57. Sakai, K. et al. Novel ALDH3A2 heterozygous mutations in a Japanese family with Sjögren-Larsson syndrome. J. Invest. Dermatol. 126, 2545-2547 (2006).
58. Sakai, K. et al. An Indian family with Sjögren-Larsson syndrome caused by a novel ALDH3A2 mutation. Int. J. Dermatol. 49, 1031-1033 (2010).
59. Sarret, C. et al. Sjögren-Larsson syndrome: novel mutations in the ALDH3A2 gene in a French cohort. J. Neurol. Sci. 312, 123-126 (2012).
60. Shibaki, A., Akiyama, M. & Shimizu, H. Novel ALDH3A2 heterozygous mutations are associated with defective lamellar granule formation in a Japanese family of Sjögren-Larsson syndrome. J. Invest. Dermatol. 123, 1197-1199 (2004).
61. Yiş, U. & Terrinoni, A. Sjögren-Larsson syndrome: report of monozygote twins and a case with a novel mutation. Turk. J. Pediatr. 54, 64-66 (2012).
62. Davis, K. et al. Novel mutation in Sjogren-Larsson syndrome is associated with divergent neurologic phenotypes. J. Child Neurol. 28, 1259-1265 (2013).
63. Incecik, F., Herguner, O. M., Rizzo, W. B. & Altunbasak, S. A Turkish family with Sjögren-Larsson syndrome caused by a novel ALDH3A2 mutation. Ann. Indian Acad. Neurol. 16, 425-427 (2013).
64. Dimasi, N., Flot, D., Dupeux, F. & Marquez, J. A. Expression, crystallization and X-ray data collection from microcrystals of the extracellular domain of the human inhibitory receptor expressed on myeloid cells IREM-1. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 63, 204-208 (2007).
65. Kabsch, W. XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132 (2010).
66. McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007).
67. Murshudov, G. N. et al. REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. 67, 355-367 (2011).
68. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. 66, 486-501 (2010).
69. Schymkowitz, J. W. et al. Prediction of water and metal binding sites and their affinities by using the Fold-X force field. Proc. Natl Acad. Sci. USA 102, 10147-10152 (2005).
70. Schymkowitz, J. et al. The FoldX web server: an online force field. Nucleic Acids Res. 33, W382-W388 (2005).