Differential contribution of the repeats to heparin binding of HBHA, a major adhesin of Mycobacterium tuberculosis

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Lebrun, Pierre ^a,b   Raze, Dominique ^a,b   Fritzinger, Bernd ^b,c   Wieruszeski, Jean Michel ^b,c   Biet, Franck ^e   Dose, Alexander ^d   Carpentier, Mathieu ^b,c   Schwarzer, Dirk ^d   Allain, Fabrice ^b,c   Lippens, Guy ^b,c   Locht, Camille ^a,b  

^a INSERM U1019   (France)

^b UNIV LILLE   (France)

^c UNIVERSITÉ DES SCIENCES ET TECHNOLOGIES DE LILLE   (France)

^d UNIVERSITY OF TÜBINGEN   (Germany)

^e UR1282   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; GLYCOSAMINOGLYCAN; HEPARIN BINDING HEMAGGLUTININ; HEPARIN DERIVATIVE; LYSINE; PROLINE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; HBHA PROTEIN, MYCOBACTERIUM TUBERCULOSIS; HEPARIN; MEMBRANE PROTEIN; OLIGOSACCHARIDE;

ALPHA HELIX; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; EVOLUTIONARY ADAPTATION; GENE SEQUENCE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN DETERMINATION; PROTEIN POLYMORPHISM; PROTEIN STABILITY; PROTEIN STRUCTURE; STRUCTURAL HOMOLOGY; CHEMISTRY; METABOLISM; MOLECULAR GENETICS; MOLECULAR WEIGHT; PROTEIN TERTIARY STRUCTURE; SPECIES DIFFERENCE; THERMODYNAMICS;

MYCOBACTERIUM TUBERCULOSIS;

ADHESINS, BACTERIAL; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; HEPARIN; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; MYCOBACTERIUM TUBERCULOSIS; OLIGOSACCHARIDES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; REPETITIVE SEQUENCES, AMINO ACID; SPECIES SPECIFICITY; THERMODYNAMICS;

EID: 84857754823     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0032421     Document Type: Article

References (42)

1. Locht C, Rouanet C, Hougardy JM, Mascart F, (2007) How a different look at latency can help to develop novel diagnostics and vaccines against tuberculosis. Expert Opin Biol Ther 7: 1665-1677.
2. Locht C, Raze D, Rouanet C, Genisset C, Segers J, et al. (2008) The Mycobacterial Heparin-Binding Hemagglutinin: a Virulence Factor and Antigen Useful For Diagnostics and Vaccine Development In: Daffé M, Reyrat JM, editors. The Mycobacterial Cell Envelope pp. 305-322 ASM Press ed. Washington, DC.
3. Menozzi FD, Rouse JH, Alavi M, Laude-Sharp M, Muller J, et al. (1996) Identification of a heparin-binding hemagglutinin present in mycobacteria. J Exp Med 184: 993-1001.
4. Menozzi FD, Bischoff R, Fort E, Brennan MJ, Locht C, (1998) Molecular characterization of the mycobacterial heparin-binding hemagglutinin, a mycobacterial adhesin. Proc Natl Acad Sci U S A 95: 12625-12630.
5. Pethe K, Aumercier M, Fort E, Gatot C, Locht C, et al. (2000) Characterization of the heparin-binding site of the mycobacterial heparin-binding hemagglutinin adhesin. J Biol Chem 275: 14273-14280.
6. Pethe K, Alonso S, Biet F, Delogu G, Brennan MJ, et al. (2001) The heparin-binding haemagglutinin of M. tuberculosis is required for extrapulmonary dissemination. Nature 412: 190-194.
7. Verbelen C, Dupres V, Raze D, Bompard C, Locht C, et al. (2008) Interaction of the mycobacterial heparin-binding hemagglutinin with actin, as evidenced by single-molecule force spectroscopy. J Bacteriol 190: 7614-7620.
8. Menozzi FD, Reddy VM, Cayet D, Raze D, Debrie AS, et al. (2006) Mycobacterium tuberculosis heparin-binding haemagglutinin adhesin (HBHA) triggers receptor-mediated transcytosis without altering the integrity of tight junctions. Microbes Infect 8: 1-9.
9. Temmerman S, Pethe K, Parra M, Alonso S, Rouanet C, et al. (2004) Methylation-dependent T cell immunity to Mycobacterium tuberculosis heparin-binding hemagglutinin. Nat Med 10: 935-941.
10. Parra M, Pickett T, Delogu G, Dheenadhayalan V, Debrie AS, et al. (2004) The mycobacterial heparin-binding hemagglutinin is a protective antigen in the mouse aerosol challenge model of tuberculosis. Infect Immun 72: 6799-6805.
11. Hougardy JM, Schepers K, Place S, Drowart A, Lechevin V, et al. (2007) Heparin-binding-hemagglutinin-induced IFN-gamma release as a diagnostic tool for latent tuberculosis. PLoS One 2: e926.
12. Rouanet C, Locht C, (2010) Boosting BCG to protect against TB. Expert Rev Respir Med 4: 339-348.
13. Rouanet C, Debrie AS, Lecher S, Locht C, (2009) Subcutaneous boosting with heparin binding haemagglutinin increases BCG-induced protection against tuberculosis. Microbes Infect 11: 995-1001.
14. Guerrero GG, Debrie AS, Locht C, (2010) Boosting with mycobacterial heparin-binding haemagglutinin enhances protection of Mycobacterium bovis BCG-vaccinated newborn mice against M. tuberculosis. Vaccine 28: 4340-4347.
15. Esposito C, Carullo P, Pedone E, Graziano G, Del Vecchio P, et al. (2010) Dimerisation and structural integrity of Heparin Binding Hemagglutinin A from Mycobacterium tuberculosis: implications for bacterial agglutination. FEBS Lett 584: 1091-1096.
16. Esposito C, Pethoukov MV, Svergun DI, Ruggiero A, Pedone C, et al. (2008) Evidence for an elongated dimeric structure of heparin-binding hemagglutinin from Mycobacterium tuberculosis. J Bacteriol 190: 4749-4753.
17. Lomino JV, Tripathy A, Redinbo MR, (2011) Triggered Mycobacterium tuberculosis Heparin Binding Hemagglutinin Adhesin Folding and Dimerization. J Bacteriol 193: 2089-2096.
18. Blaum BS, Deakin JA, Johansson CM, Herbert AP, Barlow PN, et al. (2010) Lysine and Arginine Side Chains in Glycosaminoglycan-Protein Complexes Investigated by NMR, Cross-Linking, and Mass Spectrometry: A Case Study of the Factor H-Heparin Interaction. J Am Chem Soc 132: 6374-6381.
19. Dull RO, Dinavahi R, Schwartz L, Humphries DE, Berry D, et al. (2003) Lung endothelial heparan sulfates mediate cationic peptide-induced barrier dysfunction: a new role for the glycocalyx. Am J Physiol Lung Cell Mol Physiol 285: L986-995.
20. Pethe K, Puech V, Daffe M, Josenhans C, Drobecq H, et al. (2001) Mycobacterium smegmatis laminin-binding glycoprotein shares epitopes with Mycobacterium tuberculosis heparin-binding haemagglutinin. Mol Microbiol 39: 89-99.
21. Vanpouille C, Denys A, Carpentier M, Pakula R, Mazurier J, et al. (2004) Octasaccharide is the minimal length unit required for efficient binding of cyclophilin B to heparin and cell surface heparan sulphate. Biochem J 382: 733-740.
22. Wishart DS, Sykes BD, (1994) The 13C chemical-shift index: a simple method for the identification of protein secondary structure using 13C chemical-shift data. J Biomol NMR 4: 171-180.
23. Wishart DS, Sykes BD, Richards FM, (1991) Relationship between nuclear magnetic resonance chemical shift and protein secondary structure. J Mol Biol 222: 311-333.
24. Spera S, Bax A, (1991) Empirical Correlation between Protein Backbone Conformation and Cα and Cβ 13C Nuclear Magnetic Resonance Chemical Shift. J Am Chem Sot 113: 5490-5492.
25. Saito A, (1986) Conformation-dependent 13C chemical shifts: A new means of conformational characterization as obtained by high-resolution solid-state. 13C NMR Magn Reson Chem 24: 835-852.
26. Biet F, Angela de Melo Marques M, Grayon M, Xavier da Silveira EK, Brennan PJ, et al. (2007) Mycobacterium smegmatis produces an HBHA homologue which is not involved in epithelial adherence. Microbes Infect 9: 175-182.
27. Lefrancois LH, Pujol C, Bodier CC, Teixeira-Gomez AP, Drobecq H, et al. (2011) Characterization of the Mycobacterium avium subsp. paratuberculosis laminin-binding/histone-like protein (Lbp/Hlp) which reacts with sera from patients with Crohn's disease. Microbes Infect 13: 585-594.
28. Vidal Pessolani MC, Marques MA, Reddy VM, Locht C, Menozzi FD, (2003) Systemic dissemination in tuberculosis and leprosy: do mycobacterial adhesins play a role? Microbes Infect 5: 677-684.
29. Angulo J, Hricovini M, Gairi M, Guerrini M, de Paz JL, et al. (2005) Dynamic properties of biologically active synthetic heparin-like hexasaccharides. Glycobiology 15: 1008-1015.
30. Canales A, Lozano R, Lopez-Mendez B, Angulo J, Ojeda R, et al. (2006) Solution NMR structure of a human FGF-1 monomer, activated by a hexasaccharide heparin-analogue. FEBS J 273: 4716-4727.
31. Thompson LD, Pantoliano MW, Springer BA, (1994) Energetic characterization of the basic fibroblast growth factor-heparin interaction: identification of the heparin binding domain. Biochemistry 33: 3831-3840.
32. Rullo A, Nitz M, (2010) Importance of the spatial display of charged residues in heparin-peptide interactions. Biopolymers 93: 290-298.
33. Caldwell EE, Nadkarni VD, Fromm JR, Linhardt RJ, Weiler JM, (1996) Importance of specific amino acids in protein binding sites for heparin and heparan sulfate. Int J Biochem Cell Biol 28: 203-216.
34. Mizuno K, Inoue H, Hagiya M, Shimizu S, Nose T, et al. (1994) Hairpin loop and second kringle domain are essential sites for heparin binding and biological activity of hepatocyte growth factor. J Biol Chem 269: 1131-1136.
35. Shih PC, Yang MS, Lin SC, Ho Y, Hsiao JC, et al. (2009) A turn-like structure "KKPE" segment mediates the specific binding of viral protein A27 to heparin and heparan sulfate on cell surfaces. J Biol Chem 284: 36535-36546.
36. Vanwildemeersch M, Olsson AK, Gottfridsson E, Claesson-Welsh L, Lindahl U, et al. (2006) The anti-angiogenic His/Pro-rich fragment of histidine-rich glycoprotein binds to endothelial cell heparan sulfate in a Zn2+-dependent manner. J Biol Chem 281: 10298-10304.
37. Sauton B, (1912) Sur la nutrition minérale du bacille tuberculeux. C R Hebd Séances Acad Sci 155: 860-861.
38. Sambrook J, Fritsch FE, Maniatis T, eds. (1989) Molecular Cloning: a Laboratory Manual Cold Spring Harbor Cold Spring Harbor Laboratory Press.
39. Muhandiram DR, Kay LE, (1994) Gradient-Enhanced Triple-Resonance Three-Dimensional NMR Experiments with Improved Sensitivity. J Magn Reson B 103: 203-216.
40. Weisemann R, Ruterjans H, Bermel W, (1993) 3D triple-resonance NMR techniques for the sequential assignment of NH and 15N resonances in 15N- and 13C-labelled proteins. J Biomol NMR 3: 113-120.
41. Lassmann T, Frings O, Sonnhammer EL, (2009) Kalign2: high-performance multiple alignment of protein and nucleotide sequences allowing external features. Nucleic Acids Res 37: 858-865.
42. Tamiola K, Acar B, Mulder FA, (2010) Sequence-specific random coil chemical shifts of intrinsically disordered proteins. J Am Chem Soc 132: 18000-18003.