Metabolite-driven regulation of heme uptake by the biliverdin IXβ/δ-selective heme oxygenase (HemO) of Pseudomonas aeruginosa

Journal of Biological Chemistry

Volumn 291, Issue 39, 2016, Pages 20503-20515

  Mouriño, Susana ^a   Giardina, Bennett J ^a   Reyes Caballero, Hermes ^a,b   Wilks, Angela ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF PHARMACY   (United States)

^b Johns Hopkins University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; CELL MEMBRANES; CELL SIGNALING; ENZYME ACTIVITY; PIGMENTS;

ASSIMILATION SYSTEM; ENZYMATIC ACTIVITIES; EXTRACELLULAR LEVELS; FEEDBACK REGULATION; ISOTOPIC LABELING; PSEUDOMONAS AERUGINOSA; SIGNALING SYSTEMS; TRANSPORT PROTEINS;

PORPHYRINS;

BILIVERDIN; BILIVERDIN IX BETA; BILIVERDIN IX DELTA; HEME OXYGENASE; MEMBRANE PROTEIN; PROTEIN HASA; PROTEIN HASR; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; CARRIER PROTEIN; HASAP PROTEIN, PSEUDOMONAS AERUGINOSA; HEME; HOLOENZYME; IRON;

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; CONTROLLED STUDY; HASA GENE; HASR GENE; ISOTHERMAL TITRATION CALORIMETRY; ISOTOPE LABELING; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PSEUDOMONAS AERUGINOSA; REGULATORY MECHANISM; TRANSCRIPTION REGULATION; AMINO ACID SUBSTITUTION; ANALOGS AND DERIVATIVES; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; MISSENSE MUTATION;

AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; BILIVERDINE; CARRIER PROTEINS; HEME; HEME OXYGENASE (DECYCLIZING); HOLOENZYMES; IRON; MUTATION, MISSENSE; PSEUDOMONAS AERUGINOSA;

EID: 84988603231     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.728527     Document Type: Article

References (28)

1. Wilks, A., and Barker, K. D. (2011) in Handbook of Porphyrin Science (Kadish, K. M., Smith, K. M., and Guilard, R., eds) 1st Ed., pp. 357-398, World Scientific, Singapore
2. Wilks, A., and Burkhard, K. A. (2007) Heme and virulence: how bacterial pathogens regulate, transport and utilize heme. Nat. Prod. Rep. 24, 511-522
3. Contreras, H., Chim, N., Credali, A., and Goulding, C. W. (2014) Heme uptake in bacterial pathogens. Curr. Opin. Chem. Biol. 19, 34-41
4. Cornelis, P. (2010) Iron uptake and metabolism in Pseudomonads. Appl. Microbiol. Biotechnol. 86, 1637-1645
5. Cornelis, P., and Dingemans, J. (2013) Pseudomonas aeruginosa adapts its iron uptake strategies in function of the type of infections. Front. Cell Infect. Microbiol. 3, 75
6. Ochsner, U. A., Johnson, Z., and Vasil, M. L. (2000) Genetics and regulation of two distinct haem-uptake systems, phu and has, in Pseudomonas aeruginosa. Microbiology 146, 185-198
7. Létoffé, S., Delepelaire, P., and Wandersman, C. (1996) Protein secretion in Gram-negative bacteria: assembly of the three components of ABC protein-mediated exporters is ordered and promoted by substrate binding. EMBO J. 15, 5804-5811
8. Létoffé, S., Delepelaire, P., and Wandersman, C. (2004) Free and hemophore-bound heme acquisitions through the outer membrane receptor HasR have different requirements for the TonB-ExbB-ExbD complex. J. Bacteriol. 186, 4067-4074
9. Cescau, S., Cwerman, H., Létoffé, S., Delepelaire, P., Wandersman, C., and Biville, F. (2007) Heme acquisition by hemophores. Biometals 20, 603-613
10. Biville, F., Cwerman, H., Létoffé, S., Rossi, M. S., Drouet, V., Ghigo, J. M., and Wandersman, C. (2004) Haemophore-mediated signalling in Serratia marcescens: a new mode of regulation for an extra cytoplasmic function (ECF) σ factor involved in haem acquisition. Mol. Microbiol. 53, 1267-1277
11. Smith, A. D., and Wilks, A. (2015) Differential contributions of the outer membrane receptors PhuR and HasR to heme acquisition in Pseudomonas aeruginosa. J. Biol. Chem. 290, 7756-7766
12. O'Neill, M. J., and Wilks, A. (2013) The P. aeruginosa heme binding protein PhuS is a heme oxygenase titratable regulator of heme uptake. ACS Chem. Biol. 8, 1794-1802
13. Wegele, R., Tasler, R., Zeng, Y., Rivera, M., and Frankenberg-Dinkel, N. (2004) The heme oxygenase(s)-Phytochrome system of Pseudomonas aeruginosa. J. Biol. Chem. 279, 45791-45802
14. O'Neill, M. J., Bhakta, M. N., Fleming, K. G., and Wilks, A. (2012) Induced fit on heme binding to the Pseudomonas aeruginosa cytoplasmic protein (PhuS) drives interaction with heme oxygenase (HemO). Proc. Natl. Acad. Sci. U.S.A. 109, 5639-5644
15. Friedman, J., Lad, L., Li, H., Wilks, A., and Poulos, T. L. (2004) Structural basis for novel delta-regioselective heme oxygenation in the opportunistic pathogen Pseudomonas aeruginosa. Biochemistry 43, 5239-5245
16. Schuller, D. J., Zhu, W., Stojiljkovic, I., Wilks, A., and Poulos, T. L. (2001) Crystal structure of heme oxygenase from the gram-negative pathogen Neisseria meningitidis and a comparison with mammalian heme oxygenase-1. Biochemistry 40, 11552-11558
17. Hoang, T. T., Karkhoff-Schweizer, R. R., Kutchma, A. J., and Schweizer, H. P. (1998) A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212, 77-86
18. Hoang, T. T., Kutchma, A. J., Becher, A., and Schweizer, H. P. (2000) Integration-proficient plasmids for Pseudomonas aeruginosa: site-specific integration and use for engineering of reporter and expression strains. Plasmid 43, 59-72
19. Barker, K. D., Barkovits, K., and Wilks, A. (2012) Metabolic flux of extracellular heme uptake in Pseudomonas aeruginosa is driven by the iron-regulated heme oxygenase (HemO). J. Biol. Chem. 287, 18342-18350
20. Ratliff, M., Zhu, W., Deshmukh, R., Wilks, A., and Stojiljkovic, I. (2001) Homologues of neisserial heme oxygenase in gram-negative bacteria: degradation of heme by the product of the pigA gene of Pseudomonas aeruginosa. J. Bacteriol. 183, 6394-6403
21. Zhu, W., Wilks, A., and Stojiljkovic, I. (2000) Degradation of heme in gram-negative bacteria: the product of the hemO gene of Neisseriae is a heme oxygenase. J. Bacteriol. 182, 6783-6790
22. Wilks, A., and Schmitt, M. P. (1998) Expression and characterization of a heme oxygenase (Hmu O) from Corynebacterium diphtheriae. Iron acquisition requires oxidative cleavage of the heme macrocycle. J. Biol. Chem. 273, 837-841
23. Lansky, I. B., Lukat-Rodgers, G. S., Block, D., Rodgers, K. R., Ratliff, M., and Wilks, A. (2006) The cytoplasmic heme-binding protein (PhuS) from the heme uptake system of Pseudomonas aeruginosa is an intracellular hemetrafficking protein to the delta-regioselective heme oxygenase. J. Biol. Chem. 281, 13652-13662
24. Rivera, M., and Walker, F. A. (1995) Biosynthetic preparation of isotopically labeled heme. Anal. Biochem. 230, 295-302
25. Teale, F. W. (1959) Cleavage of the haem-protein link by acid methylethylketone. Biochim. Biophys. Acta 35, 543
26. Fuhrop, J. H., and Smith, K. M. (eds) (1975) Porphyrins and Metalloporphyrins, pp. 804-807, Elsevier, Amsterdam
27. de Lorenzo, V., and Timmis, K. N. (1994) Analysis and construction of stable phenotypes in Gram-negative bacteria with Tn5- and Tn10-derived minitransposons. Methods Enzymol. 235, 386-405
28. Holloway, B. W. (1955) Genetic recombination in Pseudomonas aeruginosa. J. Gen. Microbiol. 13, 572-581