Heterologous expression of mycobacterial proteins in Saccharomyces cerevisiae reveals two physiologically functional 3-hydroxyacyl-thioester dehydratases, HtdX and HtdY, in addition to HadABC and HtdZ

Journal of Bacteriology

Volumn 191, Issue 8, 2009, Pages 2683-2690

  Gurvitz, Aner ^a,b   Hiltunen, J Kalervo ^b   Kastaniotis, Alexander J ^b  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b UNIVERSITY OF OULU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

3 HYDROXYACYL THIOESTER DEHYDRATASE X; 3 HYDROXYACYL THIOESTER DEHYDRATASE Y; BACTERIAL PROTEIN; CARRIER PROTEIN; FATTY ACID SYNTHASE; GLYCEROL; HADAB PROTEIN; HADBC PROTEIN; HTDZ PROTEIN; THIOCTIC ACID; TRIPHENYLTETRAZOLIUM; UNCLASSIFIED DRUG; HTD2 PROTEIN, S CEREVISIAE; HYDROLYASE; RECOMBINANT PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; TETRAZOLIUM;

ARTICLE; BACTERIAL GROWTH; CARBON SOURCE; CONTROLLED STUDY; ENZYME ACTIVITY; MUTANT; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OPEN READING FRAME; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SACCHAROMYCES CEREVISIAE; WILD TYPE; BIOSYNTHESIS; ENZYMOLOGY; GENE DELETION; GENE EXPRESSION; GENETIC COMPLEMENTATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR CLONING;

EUKARYOTA; MYCOBACTERIUM TUBERCULOSIS; SACCHAROMYCES CEREVISIAE;

BACTERIAL PROTEINS; CLONING, MOLECULAR; GENE DELETION; GENE EXPRESSION; GENETIC COMPLEMENTATION TEST; GLYCEROL; HYDRO-LYASES; MYCOBACTERIUM TUBERCULOSIS; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TETRAZOLIUM SALTS; THIOCTIC ACID;

EID: 65249114632     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01046-08     Document Type: Article

References (43)

1. Arcus, V. L., J. S. Lott, J. M. Johnston, and E. N. Baker. 2006. The potential impact of structural genomics on tuberculosis drug discovery. Drug Discov. Today 11:28-34.
2. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl. 1989. Current protocols in molecular biology. John Wiley & Sons, Inc., New York, NY.
3. Autio, K. J., J. L. Guler, A. J. Kastaniotis, P. T. Englund, and J. K. Hiltunen. 2008. The 3-hydroxyacyl-ACP dehydratase of mitochondrial fatty acid synthesis in Trypanosoma brucei. FEBS Lett. 582:729-733.
4. Autio, K. J., A. J. Kastaniotis, H. Pospiech, I. J. Miinalainen, M. S. Scho- nauer, C. L. Dieckmann, and J. K. Hiltunen. 2008. An ancient genetic link between vertebrate mitochondrial fatty acid synthesis and RNA processing. FASEB J. 22:569-578.
5. Bloch, K. 1977. Control mechanisms for fatty acid synthesis in Mycobacterium smegmatis. Adv. Enzymol. 45:1-84.
6. Boker-Schmitt, E., S. Francisci, and R. J. Schweyen. 1982. Mutations releasing mitochondrial biogenesis from glucose repression in Saccharomyces cer- evisiae. J. Bacteriol. 151:303-310.
7. Boshoff, H. I., T. G. Myers, B. R. Copp, M. R. McNeil, M. A. Wilson, and C. E. Barry III. 2004. The transcriptional responses of Mycobacterium tuberculosis to inhibitors of metabolism: novel insights into drug mechanisms of action. J. Biol. Chem. 279:40174-10184.
8. Brody, S., C. Oh, U. Hoja, and E. Schweizer. 1997. Mitochondrial acyl carrier protein is involved in lipoic acid synthesis in Saccharomyces cerevisiae. FEBS Lett. 408:217-220.
9. Brown, A. K., A. Bhatt, A. Singh, E. Saparia, A. F. Evans, and G. S. Besra. 2007. Identification of the dehydratase component of the mycobacterial mycolic acid-synthesizing fatty acid synthase-II complex. Microbiology 153: 4166-4173.
10. Campbell, J. W., and J. E. Cronan, Jr. 2001. Bacterialfattyacidbiosynthesis: targets for antibacterial drug discovery. Annu. Rev. Microbiol. 55:305-332.
11. Castell, A., P. Johansson, T. Unge, T. A. Jones, and K. Bäckbro. 2005. Rv0216, a conserved hypothetical protein from Mycobacterium tuberculosis that is essential for bacterial survival during infection, has a double hotdog fold. Protein Sci. 14:1850-1862.
12. Chen, D.-C., B.-C. Yang, and T.-T. Kuo. 1992. One-step transformation of yeast in stationary phase. Curr. Genet. 21:83-84.
13. Dillon, S. C., and A. Bateman. 2004. The Hotdog fold: wrapping up a superfamily of thioesterases and dehydratases. BMC Bioinformatics 5:109.
14. Filppula, S. A., R. T. Sormunen, A. Hartig, W.-H. Kunau, and J. K. Hiltunen. 1995. Changing stereochemistry for a metabolic pathway in vivo. Experiments with the peroxisomal β-oxidation in yeast. J. Biol. Chem. 270:27453-27457.
15. Gerum, A. B., J. E. Ulmer, D. P. Jacobus, N. P. Jensen, D. R. Sherman, and C. H. Sibley. 2002. Novel Saccharomyces cerevisiae screen identifies WR99210 analogues that inhibit Mycobacterium tuberculosis dihydrofolate reductase. Antimicrob. Agents Chemother. 46:3362-3369.
16. Gietz, R. D., and A. Sugino. 1988. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74:527-534.
17. Goldman, P., and P. R. Vagelos. 1961. The specificity of triglyceride synthesis from diglycerides in chicken adipose tissue. J. Biol. Chem. 236:2620-2623.
18. Gu, S., J. Chen, K. M. Dobos, E. M. Bradbury, J. T. Belisle, and X. Chen. 2003. Comprehensive proteomic profiling of the membrane constituents of a Mycobacterium tuberculosis strain. Mol. Cell Proteomics 2:1284-1296.
19. Gueguen, V., D. Macherel, M. Jaquinod, R. Douce, and J. Bourguignon. 2000. Fatty acid and lipoic acid biosynthesis in higher plant mitochondria. J. Biol. Chem. 275:5016-5025.
20. 90mycolicacids, during de novo lipoic acid synthesis in Saccharomyces cerevisiae. Appl. Environ. Microbiol. 74:5078-5085.
21. Gurvitz, A., J. K. Hiltunen, and A. J. Kastaniotis. 2008. Identification of a novel mycobacterial 3-hydroxyacyl-thioester dehydratase HtdZ (Rv0130) by functional complementation in yeast. J. Bacteriol. 190:4088-4090.
22. Gurvitz, A., H. Rottensteiner, S. H. Kilpelainen, A. Hartig, J. K. Hiltunen, M. Binder, I. W. Dawes, and B. Hamilton. 1997. The Saccharomyces cerevi- siae peroxisomal 2,4-dienoyl-CoA reductase is encoded by the oleate-induc- ible gene SPS19. J. Biol. Chem. 272:22140-22147.
23. Hayden, M. A., I. Y. Huang, G. Iliopoulos, M. Orozco, and G. W. Ashley. 1993. Biosynthesis of lipoic acid: characterization of the lipoic acid auxo- trophs Escherichia coli W1485-lip2 and JRG33-lip9. Biochemistry 32:3778-3782.
24. Heath, R. J., Y. T. Yu, M. A. Shapiro, E. Olson, and C. O. Rock. 1998. Broad spectrum antimicrobial biocides target the FabI component of fatty acid synthesis. J. Biol. Chem. 273:30316-30320.
25. Herbert, A. A., and J. R. Guest. 1970. Turbidimetric and polarographic assays for lipoic acid using mutants of Escherichia coli. Methods Enzymol. 18:269-272.
26. Hill, J. E., A. M. Myers, T. J. Koerner, and A. Tzagoloff. 1986. Yeast/E. coli shuttle vectors with multiple unique restriction sites. Yeast 2:163-167.
27. Hiltunen, J. K., F. Okubo, V. A. Kursu, K. J. Autio, and A. J. Kastaniotis. 2005. Mitochondrial fatty acid synthesis and maintenance of respiratory competent mitochondria in yeast. Biochem. Soc. Trans. 33:1162-1165.
28. Hsu, A. Y., W. W. Poon, J. A. Shepherd, D. C. Myles, and C. F. Clarke. 1996. Complementation of coq3 mutant yeast by mitochondrial targeting of the Escherichia coli UbiG polypeptide: evidence that UbiG catalyzes both O- methylation steps in ubiquinone biosynthesis. Biochemistry 35:9797-9806.
29. Johansson, P., A. Castell, T. A. Jones, and K. Bäackbro. 2006. Structure and function of Rv0130, a conserved hypothetical protein from Mycobacterium tuberculosis. Protein Sci. 15:2300-2309.
30. Kastaniotis, A. J., K. J. Autio, R. T. Sormunen, and J. K. Hiltunen. 2004. Htd2p/Yhr067p is a yeast 3-hydroxyacyl-ACP dehydratase essential for mi- tochondrial function and morphology. Mol. Microbiol. 53:1407-1421.
31. Kimber, M. S., F. Martin, Y. Lu, S. Houston, M. Vedadi, A. Dharamsi, K. M. Fiebig, M. Schmid, and C. O. Rock. 2004. The structure of (3R)-hydroxyacyl- acyl carrier protein dehydratase (FabZ) from Pseudomonas aeruginosa. J. Biol. Chem. 279:52593-52602.
32. Malila, L. H., K. M. Siivari, M. J. Mäkelä, J. E. Jalonen, P. M. Latipää, W.-H. Kunau, and J. K. Hiltunen. 1993. Enzymes converting D-3-hydroxyacyl- CoAtotrans-2-enoyl-CoA. Microsomalandperoxisomalisoenzymesinratliver. J. Biol. Chem. 268:21578-21585.
33. Marmiesse, M., P. Brodin, C. Buchrieser, C. Gutierrez, N. Simoes, V. Vincent, P. Glaser, S. T. Cole, and R. Brosch. 2004. Macro-array and bioinfor- matic analyses reveal mycobacterial 'core' genes, variation in the ESAT-6 gene family and new phylogenetic markers for the Mycobacterium tuberculosis complex. Microbiology 150:483-496.
34. Parish, T., G. Roberts, F. Laval, M. Schaeffer, M. Daflé, and K. Duncan. 2007. Functional complementation of the essential gene fabGl of Mycobacterium tuberculosis by Mycobacterium smegmatis fabG but not Escherichia coli fabG. J. Bacteriol. 189:3721-3728.
35. Rose, M. D., F. Winston, and P. Heiter. 1990. Methods in yeast genetics: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
36. 16 fatty acyl substrate. J. Biol. Chem. 274:15582-15589.
37. Sacco, E., A. S. Covarrubias, H. M. O'Hare, P. Carroll, N. Eynard, T. A. Jones, T. Parish, M. Daflé, K. Bäckbro, and A. Quémard. 2007. The missing piece of the type II fatty acid synthase system from Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA 104:14628-14633.
38. Sacco, E., V. Legendre, F. Laval, D. Zerbib, H. Montrozier, N. Eynard, C. Guilhot, M. Daffé, and A. Quémard. 2007. Rv3389C from Mycobacterium tuberculosis, a member of the (R)-specific hydratase/dehydratase family. Bio-chim. Biophys. Acta 1774:303-311.
39. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
40. Sassetti, C. M., and E. J. Rubin. 2003. Genetic requirements for mycobac-terial survival during infection. Proc. Natl. Acad. Sci. USA 100:12989-12994.
41. Takayama, K., C. Wang, and G. S. Besra. 2005. Pathway to synthesis and processing of mycolic acids in Mycobacterium tuberculosis. Clin. Microbiol. Rev. 18:81-101.
42. Wang, F., R. Langley, G. Gulten, L. Wang, and J. C. Sacchettini. 2007. Identification of a type III thioesterase reveals the function of an operon crucial for Mtb virulence. Chem. Biol. 14:543-551.
43. World Health Organisation. 1997. Anti-tuberculosis drug resistance in the world: the WHO/IUATLD global project on anti-tuberculosis drug resistance surveillance. W. H. O. Global Tuberculosis Programme, Geneva, Switzerland.