Human brown fat inducible thioesterase variant 2 cellular localization and catalytic function

Biochemistry

Volumn 51, Issue 35, 2012, Pages 6990-6999

  Chen, Danqi ^a   Latham, John ^a   Zhao, Hong ^a   Bisoffi, Marco ^b   Farelli, Jeremiah ^c   Dunaway Mariano, Debra ^a  

^a UNIVERSITY OF NEW MEXICO   (United States)

^b UNIVERSITY OF NEW MEXICO HEALTH SCIENCES CENTER   (United States)

^c USA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL-COA; ACYL-COA; CATALYTIC FUNCTIONS; CELLULAR LOCALIZATION; HEK293 CELLS; IN-VITRO; LIPID TRANSFER; LONG CHAINS; MITOCHONDRIAL MATRIX; MULTI-MODULAR; N-TERMINALS; PARALOGS; PHOSPHATIDYLINOSITOL 4 PHOSPHATES; SIGNAL SEQUENCE; THIOESTERASES; THIOESTERS;

CYTOLOGY; MAMMALS;

CATALYSIS;

BROWN FAT INDUCIBLE THIOESTERASE VARIANT 2; PALMITOYL COENZYME A HYDROLASE; THIOL ESTER HYDROLASE; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME BINDING; ENZYME LOCALIZATION; HUMAN; HUMAN CELL; IN VITRO STUDY; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN PROCESSING; SIGNAL TRANSDUCTION;

ACYL COENZYME A; AMINO ACID SEQUENCE; HEK293 CELLS; HUMANS; MITOCHONDRIA; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PALMITOYL-COA HYDROLASE; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT;

MAMMALIA;

EID: 84865718191     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi3008824     Document Type: Article

References (57)

1. Lowell, B. B. and Spiegelman, B. M. (2000) Towards a molecular understanding of adaptive thermogenesis Nature 404, 652-660
2. Butow, R. A. and Bahassi, E. M. (1999) Adaptive thermogenesis: Orchestrating mitochondrial biogenesis Curr. Biol. 9, R767-R769
3. Lowell, B. B. (1998) Adaptive thermogenesis: Turning on the heat Curr. Biol. 8, R517-R520
4. Puigserver, P., Wu, Z., Park, C. W., Graves, R., Wright, M., and Spiegelman, B. M. (1998) A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis Cell 92, 829-839
5. Nedergaard, J., Golozoubova, V., Matthias, A., Asadi, A., Jacobsson, A., and Cannon, B. (2001) UCP1: The only protein able to mediate adaptive non-shivering thermogenesis and metabolic inefficiency Biochim. Biophys. Acta 1504, 82-106
6. Ricquier, D. (1998) Neonatal brown adipose tissue, UCP1 and the novel uncoupling proteins Biochem. Soc. Trans. 26, 120-123
7. Nedergaard, J., Matthias, A., Golozoubova, V., Jacobsson, A., and Cannon, B. (1999) UCP1: The original uncoupling protein - and perhaps the only one? New perspectives on UCP1, UCP2, and UCP3 in the light of the bioenergetics of the UCP1-ablated mice J. Bioenerg. Biomembr. 31, 475-491
8. Matthias, A., Ohlson, K. B., Fredriksson, J. M., Jacobsson, A., Nedergaard, J., and Cannon, B. (2000) Thermogenic responses in brown fat cells are fully UCP1-dependent. UCP2 or UCP3 do not substitute for UCP1 in adrenergically or fatty scid-induced thermogenesis J. Biol. Chem. 275, 25073-25081
9. Ribeiro, M. O., Lebrun, F. L., Christoffolete, M. A., Branco, M., Crescenzi, A., Carvalho, S. D., Negrao, N., and Bianco, A. C. (2000) Evidence of UCP1-independent regulation of norepinephrine-induced thermogenesis in brown fat Am. J. Physiol. 279, E314-E322
10. Yu, X. X., Lewin, D. A., Forrest, W., and Adams, S. H. (2002) Cold elicits the simultaneous induction of fatty acid synthesis and β-oxidation in murine brown adipose tissue: Prediction from differential gene expression and confirmation in vivo FASEB J. 16, 155-168
11. Watanabe, M., Yamamoto, T., Mori, C., Okada, N., Yamazaki, N., Kajimoto, K., Kataoka, M., and Shinohara, Y. (2008) Cold-induced changes in gene expression in brown adipose tissue: Implications for the activation of thermogenesis Biol. Pharm. Bull. 31, 775-784
12. Zhang, Y., Li, Y., Niepel, M. W., Kawano, Y., Han, S., Liu, S., Marsili, A., Larsen, P. R., Lee, C. H., and Cohen, D. E. (2012) Targeted deletion of thioesterase superfamily member 1 promotes energy expenditure and protects against obesity and insulin resistance Proc. Natl. Acad. Sci. U.S.A. 109, 5417-5422
13. Nedergaard, J., Bengtsson, T., and Cannon, B. (2007) Unexpected evidence for active brown adipose tissue in adult humans Am. J. Physiol. 293, E444-E452
14. Bartelt, A. and Heeren, J. (2012) The holy grail of metabolic disease: Brown adipose tissue Curr. Opin. Lipidol. 23, 190-195
15. Hu, H. H., Tovar, J. P., Pavlova, Z., Smith, M. L., and Gilsanz, V. (2012) Unequivocal identification of brown adipose tissue in a human infant Magn. Reson. Imaging 35, 938-942
16. Ponting, C. P. and Aravind, L. (1999) START: A lipid-binding domain in StAR, HD-ZIP and signalling proteins Trends Biochem. Sci. 24, 130-132
17. Alpy, F. and Tomasetto, C. (2005) Give lipids a START: The StAR-related lipid transfer (START) domain in mammals J. Cell Sci. 118, 2791-2801
18. Li, Z., Song, F., Zhuang, Z., Dunaway-Mariano, D., and Anderson, K. S. (2009) Monitoring enzyme catalysis in the multimeric state: Direct observation of Arthrobacter 4-hydroxybenzoyl-coenzyme A thioesterase catalytic complexes using time-resolved electrospray ionization mass spectrometry Anal. Biochem. 394, 209-216
19. Zhao, H., Martin, B. M., Bisoffi, M., and Dunaway-Mariano, D. (2009) The Akt C-terminal modulator protein is an acyl-CoA thioesterase of the hotdog-fold family Biochemistry 48, 5507-5509
20. Cao, J., Xu, H., Zhao, H., Gong, W., and Dunaway-Mariano, D. (2009) The mechanisms of human hotdog-fold thioesterase 2 (hTHEM2) substrate recognition and catalysis illuminated by a structure and function based analysis Biochemistry 48, 1293-1304
21. Zhuang, Z., Song, F., Zhao, H., Li, L., Cao, J., Eisenstein, E., Herzberg, O., and Dunaway-Mariano, D. (2008) Divergence of function in the hot dog fold enzyme superfamily: The bacterial thioesterase YciA Biochemistry 47, 2789-2796
22. Song, F., Zhuang, Z., Finci, L., Dunaway-Mariano, D., Kniewel, R., Buglino, J. A., Solorzano, V., Wu, J., and Lima, C. D. (2006) Structure, function, and mechanism of the phenylacetate pathway hot dog-fold thioesterase PaaI J. Biol. Chem. 281, 11028-11038
23. Zhuang, Z., Song, F., Takami, H., and Dunaway-Mariano, D. (2004) The BH1999 protein of Bacillus halodurans C-125 is gentisyl-coenzyme A thioesterase J. Bacteriol. 186, 393-399
24. Thoden, J. B., Zhuang, Z., Dunaway-Mariano, D., and Holden, H. M. (2003) The structure of 4-hydroxybenzoyl-CoA thioesterase from Arthrobacter sp. strain SU J. Biol. Chem. 278, 43709-43716
25. Zhuang, Z., Gartemann, K. H., Eichenlaub, R., and Dunaway-Mariano, D. (2003) Characterization of the 4-hydroxybenzoyl-coenzyme A thioesterase from Arthrobacter sp. strain SU Appl. Environ. Microbiol. 69, 2707-2711
26. Zhuang, Z., Song, F., Zhang, W., Taylor, K., Archambault, A., Dunaway-Mariano, D., Dong, J., and Carey, P. R. (2002) Kinetic, Raman, NMR, and site-directed mutagenesis studies of the Pseudomonas sp. strain CBS3 4-hydroxybenzoyl-CoA thioesterase active site Biochemistry 41, 11152-11160
27. Thoden, J. B., Holden, H. M., Zhuang, Z., and Dunaway-Mariano, D. (2002) X-ray crystallographic analyses of inhibitor and substrate complexes of wild-type and mutant 4-hydroxybenzoyl-CoA thioesterase J. Biol. Chem. 277, 27468-27476
28. Benning, M. M., Wesenberg, G., Liu, R., Taylor, K. L., Dunaway-Mariano, D., and Holden, H. M. (1998) The three-dimensional structure of 4-hydroxybenzoyl-CoA thioesterase from Pseudomonas sp. strain CBS-3 J. Biol. Chem. 273, 33572-33579
29. Zhuang, Z., Latham, J., Song, F., Zhang, W., Trujillo, M., and Dunaway-Mariano, D. (2012) Investigation of the catalytic mechanism of the hotdog-fold enzyme superfamily Pseudomonas sp. strain CBS3 4-hydroxybenzoyl-CoA thioesterase Biochemistry 51, 786-794
30. Willis, M. A., Zhuang, Z., Song, F., Howard, A., Dunaway-Mariano, D., and Herzberg, O. (2008) Structure of YciA from Haemophilus influenzae (HI0827), a hexameric broad specificity acyl-coenzyme A thioesterase Biochemistry 47, 2797-2805
31. Kirkby, B., Roman, N., Kobe, B., Kellie, S., and Forwood, J. K. (2010) Functional and structural properties of mammalian acyl-coenzyme A thioesterases Prog. Lipid Res. 49, 366-377
32. Adams, S. H., Chui, C., Schilbach, S. L., Yu, X. X., Goddard, A. D., Grimaldi, J. C., Lee, J., Dowd, P., Colman, S., and Lewin, D. A. (2001) BFIT, a unique acyl-CoA thioesterase induced in thermogenic brown adipose tissue: Cloning, organization of the human gene and assessment of a potential link to obesity Biochem. J. 360, 135-142
33. Li, J., Derewenda, U., Dauter, Z., Smith, S., and Derewenda, Z. S. (2000) Crystal structure of the Escherichia coli thioesterase II, a homolog of the human Nef binding enzyme Nat. Struct. Biol. 7, 555-559
34. Keatinge-Clay, A. (2008) Crystal structure of the erythromycin polyketide synthase dehydratase J. Mol. Biol. 384, 941-953
35. Kotaka, M., Kong, R., Qureshi, I., Ho, Q. S., Sun, H., Liew, C. W., Goh, L. P., Cheung, P., Mu, Y., Lescar, J., and Liang, Z. X. (2009) Structure and catalytic mechanism of the thioesterase CalE7 in enediyne biosynthesis J. Biol. Chem. 284, 15739-15749
36. Koski, M. K., Haapalainen, A. M., Hiltunen, J. K., and Glumoff, T. (2004) A two-domain structure of one subunit explains unique features of eukaryotic hydratase 2 J. Biol. Chem. 279, 24666-24672
37. Kato, J. Y., Funa, N., Watanabe, H., Ohnishi, Y., and Horinouchi, S. (2007) Biosynthesis of γ-butyrolactone autoregulators that switch on secondary metabolism and morphological development in Streptomyces Proc. Natl. Acad. Sci. U.S.A. 104, 2378-2383
38. Akula, N., Midzak, A., Lecanu, L., and Papadopoulos, V. (2012) Identification of small-molecule inhibitors of the steroidogenic acute regulatory protein (STARD1) by structure-based design Bioorg. Med. Chem. Lett. 22, 4139-4143
39. Borthwick, F., Taylor, J. M., Bartholomew, C., and Graham, A. (2009) Differential regulation of the STARD1 subfamily of START lipid trafficking proteins in human macrophages FEBS Lett. 583, 1147-1153
40. Roderick, S. L., Chan, W. W., Agate, D. S., Olsen, L. R., Vetting, M. W., Rajashankar, K. R., and Cohen, D. E. (2002) Structure of human phosphatidylcholine transfer protein in complex with its ligand Nat. Struct. Biol. 9, 507-511
41. Rigotti, A., Cohen, D. E., and Zanlungo, S. (2010) STARTing to understand MLN64 function in cholesterol transport J. Lipid Res. 51, 2015-2017
42. Watari, H., Arakane, F., Moog-Lutz, C., Kallen, C. B., Tomasetto, C., Gerton, G. L., Rio, M. C., Baker, M. E., and Strauss, J. F., III (1997) MLN64 contains a domain with homology to the steroidogenic acute regulatory protein (StAR) that stimulates steroidogenesis Proc. Natl. Acad. Sci. U.S.A. 94, 8462-8467
43. Horibata, Y. and Sugimoto, H. (2010) StarD7 mediates the intracellular trafficking of phosphatidylcholine to mitochondria J. Biol. Chem. 285, 7358-7365
44. Angeletti, S., Maggio, B., and Genti-Raimondi, S. (2004) Surface activity and interaction of StarD7 with phospholipid monolayers Biochem. Biophys. Res. Commun. 314, 181-185
45. Kudo, N., Kumagai, K., Tomishige, N., Yamaji, T., Wakatsuki, S., Nishijima, M., Hanada, K., and Kato, R. (2008) Structural basis for specific lipid recognition by CERT responsible for nonvesicular trafficking of ceramide Proc. Natl. Acad. Sci. U.S.A. 105, 488-493
46. Thorsell, A. G., Lee, W. H., Persson, C., Siponen, M. I., Nilsson, M., Busam, R. D., Kotenyova, T., Schuler, H., and Lehtio, L. (2011) Comparative structural analysis of lipid binding START domains PLoS One 6, e19521
47. Chen, D., Wu, R., Bryan, T. L., and Dunaway-Mariano, D. (2009) In vitro kinetic analysis of substrate specificity in enterobactin biosynthetic lower pathway enzymes provides insight into the biochemical function of the hot dog-fold thioesterase EntH Biochemistry 48, 511-513
48. Suematsu, N. and Isohashi, F. (2006) Molecular cloning and functional expression of human cytosolic acetyl-CoA hydrolase Acta Biochim. Pol. 53, 553-561
49. von Heijne, G. (1986) Mitochondrial targeting sequences may form amphiphilic helices EMBO J. 5, 1335-1342
50. Omura, T. (1998) Mitochondria-targeting sequence, a multi-role sorting sequence recognized at all steps of protein import into mitochondria J. Biochem. 123, 1010-1016
51. Herrmann, J. M. and Hell, K. (2005) Chopped, trapped or tacked: Protein translocation into the IMS of mitochondria Trends Biochem. Sci. 30, 205-211
52. Klaus, S., Keipert, S., Rossmeisl, M., and Kopecky, J. (2012) Augmenting energy expenditure by mitochondrial uncoupling: A role of AMP-activated protein kinase Genes Nutr. 7, 369-386
53. Suematsu, N., Okamoto, K., and Isohashi, F. (2002) Mouse cytosolic acetyl-CoA hydrolase, a novel candidate for a key enzyme involved in fat metabolism: cDNA cloning, sequencing and functional expression Acta Biochim. Pol. 49, 937-945
54. Emsley, P. and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics Acta Crystallogr. D60, 2126-2132
55. Weeks, A. M., Coyle, S. M., Jinek, M., Doudna, J. A., and Chang, M. C. (2010) Structural and biochemical studies of a fluoroacetyl-CoA-specific thioesterase reveal a molecular basis for fluorine selectivity Biochemistry 49, 9269-9279
56. Brocker, C., Carpenter, C., Nebert, D. W., and Vasiliou, V. (2010) Evolutionary divergence and functions of the human acyl-CoA thioesterase gene (ACOT) family Hum. Genomics 4, 411-420
57. Kirkby, B., Roman, N., Kobe, B., Kellie, S., and Forwood, J. K. (2010) Functional and structural properties of mammalian acyl-coenzyme A thioesterases Prog. Lipid Res. 49, 366-377