Direct heme transfer reactions in the group A streptococcus heme acquisition pathway

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Lu, Chunmei ^a   Xie, Gang ^b   Liu, Mengyao ^b   Zhu, Hui ^a,b   Lei, Benfang ^b  

^a HARBIN MEDICAL UNIVERSITY   (China)

^b MONTANA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; HEME; MEMBRANE PROTEIN; METHEMOGLOBIN; PROTEIN HTSA; PROTEIN HTSABC; PROTEIN SHP; PROTEIN SHR; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; RECOMBINANT PROTEIN;

ARTICLE; CONTROLLED STUDY; KINETICS; NONHUMAN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN TRANSPORT; SPECTROSCOPY; STREPTOCOCCUS GROUP A; VELOCITY; BIOLOGICAL MODEL; ENZYME LINKED IMMUNOSORBENT ASSAY; METABOLISM; SPECTROPHOTOMETRY; STREPTOCOCCUS;

STREPTOCOCCUS SP. 'GROUP A';

ATP-BINDING CASSETTE TRANSPORTERS; BACTERIAL PROTEINS; ENZYME-LINKED IMMUNOSORBENT ASSAY; HEME; KINETICS; METHEMOGLOBIN; MODELS, BIOLOGICAL; PROTEIN INTERACTION MAPS; RECOMBINANT PROTEINS; SPECTROPHOTOMETRY; STREPTOCOCCUS;

EID: 84861399279     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037556     Document Type: Article

References (31)

1. Otto BR, Verweij-van Vught AM, MacLaren DM, (1992) Transferrins and heme-compounds as iron sources for pathogenic bacteria. Crit Rev Microbiol 18: 217-233.
2. Cescau S, Cwerman H, Létoffé S, Delepelaire P, Wandersman C, et al. (2007) Heme acquisition by hemophores. Biometals 20: 603-613.
3. Tullius MV, Harmston CA, Owens CP, Chim N, Morse RP, et al. (2011) Discovery and characterization of a unique mycobacterial heme acquisition system. Proc Natl Acad Sci USA 108: 5051-5056.
4. Torres VJ, Pishchany G, Humayun M, Schneewind O, Skaar EP, (2006) Staphylococcus aureus IsdB is a hemoglobin receptor required for heme iron utilization. J Bacteriol 188: 8421-8429.
5. Burkhard KA, Wilks A, (2007) Characterization of the outer membrane receptor ShuA from the heme uptake system of Shigella dysenteriae. Substrate specificity and identification of the heme protein ligands. 282: 15126-15136.
6. Zhu H, Liu M, Lei B, (2008) The surface protein Shr of Streptococcus pyogenes binds heme and transfers it to the streptococcal heme-binding protein Shp. BMC Microbiol 8: 15.
7. Klebba PE, Rutz JM, Liu J, Murphy CK, (1993) Mechanisms of TonB-catalyzed iron transport through the enteric bacterial cell envelope. J Bioenerg Biomembr 25: 603-611.
8. Mazmanian SK, Skaar EP, Gaspar AH, Humayun M, Gornicki P, et al. (2003) Passage of heme-iron across the envelope of Staphylococcus aureus. Science 299: 906-909.
9. Zhu H, Xie G, Liu M, Olson JS, Fabian M, et al. (2008) Pathway for heme uptake from human methemoglobin by the iron-regulated surface determinants (Isd) system of Staphylococcus aureus. J Biol Chem 283: 18450-18460.
10. Eichenbaum Z, Muller E, Morse SA, Scott JR, (1996) Acquisition of iron from host proteins by the group A Streptococcus. Infect Immun 64: 5428-5429.
11. Bates CS, Montañez GE, Woods CR, Vincent RM, Eichenbaum Z, (2003) Identification and characterization of a Streptococcus pyogenes operon involved in binding of hemoproteins and acquisition of iron. Infect Immun 71: 1042-1055.
12. Andrade MA, Ciccarelli FD, Perez-Iratxeta C, Bork P, (2002) NEAT: a domain duplicated in genes near the components of a putative Fe3+ siderophore transporter from Gram-positive pathogenic bacteria. Genome Biol 3: RESEARCH0047.
13. Lei B, Smoot LM, Menning HM, Voyich JM, Kala SV, et al. (2002) Identification and characterization of a novel heme-associated cell surface protein made by Streptococcus pyogenes. Infect Immun 70: 4494-4500.
14. Sook BR, Block DR, Sumithran S, Montañez GE, Rodgers KR, et al. (2008) Characterization of SiaA, a streptococcal heme-binding protein associated with a heme ABC transport system. Biochemistry 47: 2678-2688.
15. Ran Y, Liu M, Zhu H, Nygaard TK, Brown DE, et al. (2010) Spectroscopic identification of heme axial ligands in HtsA that are involved in heme acquisition by Streptococcus pyogenes. Biochemistry 49: 2834-2842.
16. Liu M, Lei B, (2005) Heme transfer from streptococcal cell-surface protein Shp to HtsA of transporter HtsABC. Infect Immun 73: 5086-5092.
17. Nygaard TK, Blouin GC, Liu M, Fukumura M, Olson JS, et al. (2006) The mechanism of direct heme transfer from the streptococcal cell surface protein Shp to HtsA of the HtsABC transporter. J Biol Chem 281: 20761-20771.
18. Hargrove MS, Singleton EW, Quillin ML, Ortiz LA, Phillips GN Jr, et al. (E7)→Tyr apomyoglobin as a reagent for measuring rates of hemin dissociation. J Biol Chem 269: 4207-4214.
19. Ouattara M, Cunha EB, Li X, Huang YS, Dixon D, et al. (2010) Shr of group A Streptococcus is a new type of composite NEAT protein involved in sequestering haem from methaemoglobin. Mol Microbiol 78: 739-756.
20. Dryla A, Hoffmann B, Gelbmann D, Giefing C, Hanner M, et al. (2007) High-affinity binding of the staphylococcal HarA protein to haptoglobin and hemoglobin involves a domain with an antiparallel eight-stranded beta-barrel fold. J Bacteriol 189: 254-264.
21. Honsa ES, Fabian M, Cardenas AM, Olson JS, Maresso AW, (2011) The five near-iron transporter (NEAT) domain anthrax hemophore, IsdX2, scavenges heme from hemoglobin and transfers heme to the surface protein IsdC. J Biol Chem 286: 33652-33660.
22. Liu M, Tanaka WN, Zhu H, Xie G, Dooley DM, et al. (2008) Direct hemin transfer from IsdA to IsdC in the iron-regulated surface determinant (Isd) heme acquisition system of Staphylococcus aureus. J Biol Chem 283: 6668-6676.
23. Ran Y, Zhu H, Liu M, Fabian M, Olson JS, et al. (2007) Bis-methionine ligation to heme iron in the streptococcal cell surface protein Shp facilitates rapid hemin transfer to HtsA of the HtsABC transporter. J Biol Chem 282: 31380-31388.
24. Villareal VA, Spirig T, Robson SA, Liu M, Lei B, Clubb RT, (2011) Transient weak protein-protein complexes transfer heme across the cell wall of Staphylococcus aureus. J Am Chem Soc 133: 14176-14179.
25. Muryoi N, Tiedemann MT, Pluym M, Cheung J, Heinrichs DE, Stillman MJ, (2008) Demonstration of the iron-regulated surface determinant (Isd) heme transfer pathway in Staphylococcus aureus. J Biol Chem 283: 28125-28136.
26. Nygaard TK, Liu M, McClure MJ, Lei B, (2006) Identification and characterization of the heme-binding proteins SeShp and SeHtsA of Streptococcus equi subspecies equi. BMC Microbiol 6: 82.
27. Maresso AW, Chapa TJ, Schneewind O, (2006) Surface protein IsdC and Sortase B are required for heme-iron scavenging of Bacillus anthracis. J Bacteriol 188: 8145-8152.
28. Fabian M, Solomaha E, Olson JS, Maresso AW, (2009) Heme transfer to the bacterial cell envelope occurs via a secreted hemophore in the Gram-positive pathogen Bacillus anthracis. J Biol Chem 284: 32138-32146.
29. Lei B, Liu M, Voyich JM, Prater CI, Kala SV, et al. (2003) Identification and characterization of HtsA, a second heme-binding protein made by Streptococcus pyogenes. Infect Immun 71: 5962-5969.
30. Ascoli F, Fanelli MR, Antonini E, (1981) Preparation and properties of apohemoglobin and reconstituted hemoglobins. Methods Enzymol 76: 72-87.
31. Fuhrhop JH, Smith KM, (1975) Porphyrins and Metalloporphyrins pp. 804-807.