Heme degrading protein hems is involved in oxidative stress response of Bartonella henselae

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Liu, MaFeng ^a,b   Boulouis, Henri Jean ^a   Biville, Francis ^a,c  

^a ECOLE NATIONALE VÉTÉRINAIRE D ALFORT   (France)

^b JILIN UNIVERSITY   (China)

^c INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ASCORBIC ACID; BACTERIAL PROTEIN; FERRIC ION; HEME; HYDROGEN PEROXIDE; IRON; PROTEIN HEMS; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE FERRIHEMOPROTEIN REDUCTASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL METABOLISM; BACTERIAL STRAIN; BACTERIUM MUTANT; BARTONELLA HENSELAE; CELL MEMBRANE TRANSPORT; CONTROLLED STUDY; CYTOPLASM; ELECTRON; ESCHERICHIA COLI; GENE CLUSTER; GENE EXPRESSION; GENE SILENCING; GENETIC CODE; GENETIC COMPLEMENTATION; GENOME; HEME SYNTHESIS; IRON TRANSPORT; NONHUMAN; OXIDATIVE STRESS; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PURIFICATION; SEQUENCE HOMOLOGY; DRUG EFFECT; GENETICS; IMMUNOBLOTTING; METABOLISM; PROTEIN BINDING;

ALPHAPROTEOBACTERIA; BARTONELLA; BARTONELLA HENSELAE;

BACTERIAL PROTEINS; BARTONELLA HENSELAE; HEME; HYDROGEN PEROXIDE; IMMUNOBLOTTING; OXIDATIVE STRESS; PROTEIN BINDING;

EID: 84861674953     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037630     Document Type: Article

References (52)

1. Breitschwerdt EB, Maggi RG, Chomel BB, Lappin MR, (2010) Bartonellosis: an emerging infectious disease of zoonotic importance to animals and human beings. J Vet Emerg Crit Care (San Antonio) 20: 8-30.
2. Guptill L, (2010) Bartonellosis. Vet Microbiol 140: 347-359.
3. Edouard S, Raoult D, (2010) Bartonella henselae, an ubiquitous agent of proteiform zoonotic disease. Med Mal Infect 40: 319-330.
4. Klotz SA, Ianas V, Elliott SP, (2011) Cat-scratch Disease. Am Fam Physician 83: 152-155.
5. Scherer DC, DeBuron-Connors I, Minnick MF, (1993) Characterization of Bartonella bacilliformis flagella and effect of antiflagellin antibodies on invasion of human erythrocytes. Infect Immun 61: 4962-4971.
6. Derrick SC, Ihler GM, (2001) Deformin, a substance found in Bartonella bacilliformis culture supernatants, is a small, hydrophobic molecule with an affinity for albumin. Blood Cells Mol Dis 27: 1013-1019.
7. Mitchell SJ, Minnick MF, (1995) Characterization of a two-gene locus from Bartonella bacilliformis associated with the ability to invade human erythrocytes. Infect Immun 63: 1552-1562.
8. Seubert A, Hiestand R, de la Cruz F, Dehio C, (2003) A bacterial conjugation machinery recruited for pathogenesis. Mol Microbiol 49: 1253-1266.
9. Vayssier-Taussat M, Le Rhun D, Deng HK, Biville F, Cescau S, et al. (2010) The Trw type IV secretion system of Bartonella mediates host-specific adhesion to erythrocytes. PLoS Pathog 6: e1000946.
10. Sander A, Kretzer S, Bredt W, Oberle K, Bereswill S, (2000) Hemin-dependent growth and hemin binding of Bartonella henselae. FEMS Microbiol Lett 189: 55-59.
11. Alsmark CM, Frank AC, Karlberg EO, Legault BA, Ardell DH, et al. (2004) The louse-borne human pathogen Bartonella quintana is a genomic derivative of the zoonotic agent Bartonella henselae. Proc Natl Acad Sci U S A 101: 9716-9721.
12. Perry RD, Mier I, Fetherston JD, (2007) Roles of the Yfe and Feo transporters of Yersinia pestis in iron uptake and intracellular growth. Biometals 20: 699-703.
13. Watson RJ, Millichap P, Joyce SA, Reynolds S, Clarke DJ, (2010) The role of iron uptake in pathogenicity and symbiosis in Photorhabdus luminescens TT01. BMC Microbiol 10: 177.
14. Parrow NL, Abbott J, Lockwood AR, Battisti JM, Minnick MF, (2009) Function, regulation, and transcriptional organization of the hemin utilization locus of Bartonella quintana. Infect Immun 77: 307-316.
15. Anzaldi LL, Skaar EP, (2010) Overcoming the heme paradox: heme toxicity and tolerance in bacterial pathogens. Infect Immun 78: 4977-4989.
16. Schmitt MP, (1997) Utilization of host iron sources by Corynebacterium diphtheriae: identification of a gene whose product is homologous to eukaryotic heme oxygenases and is required for acquisition of iron from heme and hemoglobin. J Bacteriol 179: 838-845.
17. Ratliff M, Zhu W, Deshmukh R, Wilks A, 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.
18. Bruggemann H, Bauer R, Raffestin S, Gottschalk G, (2004) Characterization of a heme oxygenase of Clostridium tetani and its possible role in oxygen tolerance. Arch Microbiol 182: 259-263.
19. Skaar EP, Gaspar AH, Schneewind O, (2006) Bacillus anthracis IsdG, a heme-degrading monooxygenase. J Bacteriol 188: 1071-1080.
20. Puri S, O'Brian MR, (2006) The hmuQ and hmuD genes from Bradyrhizobium japonicum encode heme-degrading enzymes. J Bacteriol 188: 6476-6482.
21. Stojiljkovic I, Hantke K, (1994) Transport of haemin across the cytoplasmic membrane through a haemin- specific periplasmic binding-protein-dependent transport system in Yersinia enterocolitica. Mol Microbiol 13: 719-732.
22. Wyckoff EE, Schmitt M, Wilks A, Payne SM, (2004) HutZ is required for efficient heme utilization in Vibrio cholerae. J Bacteriol 186: 4142-4151.
23. Lansky IB, Lukat-Rodgers GS, Block D, Rodgers KR, Ratliff M, et al. (2006) The cytoplasmic heme-binding protein (PhuS) from the heme uptake system of Pseudomonas aeruginosa is an intracellular heme-trafficking protein to the delta-regioselective heme oxygenase. J Biol Chem 281: 13652-13662.
24. Letoffe S, Heuck G, Delepelaire P, Lange N, Wandersman C, (2009) Bacteria capture iron from heme by keeping tetrapyrrol skeleton intact. Proc Natl Acad Sci U S A 106: 11719-11724.
25. Dailey HA, Septer AN, Daugherty L, Thames D, Gerdes S, et al. The Escherichia coli protein YfeX functions as a porphyrinogen oxidase, not a heme dechelatase. MBio 2: e00248-00211.
26. Miller JH, (1972) Experiments in molecular genetics. Cold Spring Harbor, N.Y Cold Spring Harbor laboratory Press.
27. Riess T, Dietrich F, Schmidt KV, Kaiser PO, Schwarz H, et al. (2008) Analysis of a novel insect cell culture medium-based growth medium for Bartonella species. Appl Environ Microbiol 74: 5224-5227.
28. Maniatis T, Fritch EF, Sanbrook J, (1989) Molecular Cloning. A Laboratory Manual; In: Harbor CS, editors. editor New York Cold Spring Harbor Laboratory Press.
29. Riess T, Anderson B, Fackelmayer A, Autenrieth IB, Kempf VA, (2003) Rapid and efficient transposon mutagenesis of Bartonella henselae by transposome technology. Gene 313: 103-109.
30. Derbise A, Lesic B, Dacheux D, Ghigo JM, Carniel E, (2003) A rapid and simple method for inactivating chromosomal genes in Yersinia. FEMS Immunol Med Microbiol 38: 113-116.
31. Oshima T, Biville F, (2006) Functional identification of YgiP as a positive regulator of the ttdA-ttdB-ygjE operon. Microbiology 152: 2129-2135.
32. Vargas C, McEwan AG, Downie JA, (1993) Detection of c-type cytochromes using enhanced chemiluminescence. Anal Biochem 209: 323-326.
33. Towbin H, Staehelin T, Gordon J, (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A 76: 4350-4354.
34. Carroll JA, Coleman SA, Smitherman LS, Minnick MF, (2000) Hemin-binding surface protein from Bartonella quintana. Infect Immun 68: 6750-6757.
35. Zhu W, Wilks A, 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.
36. Laemmli UK, (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
37. Perrotte-Piquemal M, Danchin A, Biville F, (1999) Pyrophosphate increases the efficiency of enterobactin-dependent iron uptake in Escherichia coli. Biochimie 81: 245-253.
38. Letoffe S, Delepelaire P, Wandersman C, (2006) The housekeeping dipeptide permease is the Escherichia coli heme transporter and functions with two optional peptide binding proteins. Proc Natl Acad Sci U S A 103: 12891-12896.
39. Wilks A, Schmitt MP, (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.
40. Skaar EP, Gaspar AH, Schneewind O, (2004) IsdG and IsdI, heme-degrading enzymes in the cytoplasm of Staphylococcus aureus. J Biol Chem 279: 436-443.
41. Gillaspie D, Perkins I, Larsen K, McCord A, Pangonis S, et al. (2009) Plasmid-based system for high-level gene expression and antisense gene knockdown in Bartonella henselae. Appl Environ Microbiol 75: 5434-5436.
42. Liu MF, Cescau S, Mechold U, Wang J, Cohen D, et al. (2012) Identification of a new nanoRNase in Bartonella. Microbiology 158: 886-895.
43. Wyckoff EE, Lopreato GF, Tipton KA, Payne SM, (2005) Shigella dysenteriae ShuS promotes utilization of heme as an iron source and protects against heme toxicity. J Bacteriol 187: 5658-5664.
44. Imlay JA, (2008) Cellular defenses against superoxide and hydrogen peroxide. Annu Rev Biochem 77: 755-776.
45. Coleman SA, Minnick MF, (2003) Differential expression of the invasion-associated locus B (ialB) gene of Bartonella bacilliformis in response to environmental cues. Microb Pathog 34: 179-186.
46. Suits MD, Pal GP, Nakatsu K, Matte A, Cygler M, et al. (2005) Identification of an Escherichia coli O157:H7 heme oxygenase with tandem functional repeats. Proc Natl Acad Sci U S A 102: 16955-16960.
47. Thompson JM, Jones HA, Perry RD, (1999) Molecular characterization of the hemin uptake locus (hmu) from Yersinia pestis and analysis of hmu mutants for hemin and hemoprotein utilization. Infect Immun 67: 3879-3892.
48. Silver GM, Gaines PJ, Hunter SW, Maddux JD, Thomas RE, et al. (2002) Identification, characterization, and cloning of an immunoglobulin degrading enzyme in the cat flea, Ctenocephalides felis. Arch Insect Biochem Physiol 51: 136-150.
49. Chaveroche MK, Ghigo JM, d'Enfert C, (2000) A rapid method for efficient gene replacement in the filamentous fungus Aspergillus nidulans. Nucleic Acids Res 28: E97.
50. Guzman LM, Belin D, Carson MJ, Beckwith J, (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177: 4121-4130.
51. Letoffe S, Debarbieux L, Izadi N, Delepelaire P, Wandersman C, (2003) Ligand delivery by haem carrier proteins: the binding of Serratia marcescens haemophore to its outer membrane receptor is mediated by two distinct peptide regions. Mol Microbiol 50: 77-88.
52. Kaur AP, Lansky IB, Wilks A, (2009) The role of the cytoplasmic heme-binding protein (PhuS) of Pseudomonas aeruginosa in intracellular heme trafficking and iron homeostasis. J Biol Chem 284: 56-66.