Mycobacterium tuberculosis heparin-binding haemagglutinin adhesin (HBHA) triggers receptor-mediated transcytosis without altering the integrity of tight junctions

Microbes and Infection

Volumn 8, Issue 1, 2006, Pages 1-9

  Menozzi, Franco D ^a   Reddy, Venkata M ^b   Cayet, Delphine ^a,c   Raze, Dominique ^a   Debrie, Anne Sophie ^a   Dehouck, Marie Pierre ^a,c   Cecchelli, Roméo ^a,c   Locht, Camille ^a  

^a INSTITUT PASTEUR DE LILLE   (France)

^b UNIVERSITY OF ILLINOIS   (United States)

^c UNIVERSITÉ D'ARTOIS   (France)

Author keywords

Dissemination; HBHA; Transcytosis; Tuberculosis

Indexed keywords

ADHESIN; COLLOIDAL GOLD; HEMAGGLUTININ; HEPARAN SULFATE; HEPARIN BINDING PROTEIN; HEPARIN LYASE; LYSINE; PROTEIN HEPARIN BINDING HEMAGGLUTININ ADHESIN; PROTEOGLYCAN; RECEPTOR; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ARTICLE; CELL VACUOLE; CONTROLLED STUDY; COW; CYTOPLASM; ENDOCYTOSIS; ENDOTHELIUM CELL; EPITHELIUM CELL; FLUORESCENCE MICROSCOPY; HEP 2 CELL; HUMAN; HUMAN CELL; LARYNX MUCOSA; LUNG ALVEOLUS CELL TYPE 2; MYCOBACTERIUM TUBERCULOSIS; PRIORITY JOURNAL; PROTEIN BINDING; TIGHT JUNCTION; TRANSCYTOSIS;

MYCOBACTERIUM TUBERCULOSIS;

EID: 31344441136     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2005.03.023     Document Type: Article

References (38)

1. L.W. Poulter Basic concepts in lung immunology Res. Immunol. 148 1997 8 13
2. H.L. Ratcliffe Tuberculosis induced by droplet nuclei infection; pulmonary tuberculosis of predetermined initial intensity in mammals Am. J. Hyg. 55 1952 36 47
3. M.C. Vidal Pessolani, M.A. Marques, V.M. Reddy, C. Locht, and F.D. Menozzi Systemic dissemination in tuberculosis and leprosy: do mycobacterial adhesins play a role? Microbes Infect. 5 2003 677 684
4. R. Teitelbaum, W. Schubert, L. Gunther, Y. Kress, F. Macaluso, J.W. Pollard, D.N. McMurray, and B.R. Bloom The M cell as a portal of entry to the lung for the bacterial pathogen Mycobacterium tuberculosis Immunity 10 1999 641 650
5. L.E. Bermudez, and J. Goodman Mycobacterium tuberculosis invades and replicates within type II alveolar cells Infect. Immun. 64 1996 1400 1406
6. C.C. Shepard Growth characteristics of tubercle bacilli and certain other mycobacteria in HeLa cells J. Exp. Med. 105 1957 39 48
7. K.A. McDonough, and Y. Kress Cytotoxicity for lung epithelial cells is a virulence-associated phenotype of Mycobacterium tuberculosis Infect. Immun. 63 1995 4802 4811
8. Y. Lin, M. Zhang, and P.F. Barnes Chemokine production by a human alveolar epithelial cell line in response to Mycobacterium tuberculosis Infect. Immun. 66 1998 1121 1126
9. M. Zhang, K.J. Kim, D. Iyer, Y. Lin, J. Belisle, K. McEnery, E.D. Crandall, and F. Barnes Effects of Mycobacterium tuberculosis on the bioelectric properties of the alveolar epithelium Infect. Immun. 65 1997 692 698
10. P.K. Mehta, C.H. King, E.H. White, J.J. Murtagh Jr., and F.D. Quinn Comparison of in vitro models for the study of Mycobacterium tuberculosis invasion and intracellular replication Infect. Immun. 64 1996 2673 2679
11. K. Sato, H. Tomioka, T. Akaki, and S. Kawahara Antimicrobial activities of levofloxacin, clarithromycin, and KRM-1648 against Mycobacterium tuberculosis and Mycobacterium avium complex replicating within Mono Mac 6 human macrophage and A-549 type II alveolar cell lines Int. J. Antimicrob. Agents 16 2000 25 29
12. L.E. Bermudez, F.J. Sangari, P. Kolonoski, M. Petrofsky, and J. Goodman The efficiency of the translocation of Mycobacterium tuberculosis across a bilayer of epithelial and endothelial cells as a model of the alveolar wall is a consequence of transport within mononuclear phagocytes and invasion of alveolar epithelial cells Infect. Immun. 70 2002 140 146
13. V.M. Reddy, and D.A. Hayworth Interaction of Mycobacterium tuberculosis with human respiratory epithelial cells (HEp-2) Tuberculosis (Edinb.) 82 2002 31 36
14. F.D. Menozzi, J.H. Rouse, M. Alavi, M. Laude-Sharp, J. Muller, R. Bischoff, M.J. Brennan, and C. Locht Identification of a heparin-binding hemagglutinin present in mycobacteria J. Exp. Med. 184 1996 993 1001
15. F.D. Menozzi, R. Bischoff, E. Fort, M.J. Brennan, and C. Locht Molecular characterization of the mycobacterial heparin-binding hemagglutinin, a mycobacterial adhesin Proc. Natl. Acad. Sci. USA 95 1998 12625 12630
16. K. Pethe, S. Alonso, F. Biet, G. Delogu, M.J. Brennan, C. Locht, and F.D. Menozzi The heparin-binding haemagglutinin of M. tuberculosis is required for extrapulmonary dissemination Nature 412 2001 190 194
17. K. Pethe, M. Aumercier, E. Fort, C. Gatot, C. Locht, and F.D. Menozzi Characterization of the heparin-binding site of the mycobacterial heparin-binding hemagglutinin adhesin J. Biol. Chem. 275 2000 14273 14280
18. K. Pethe, P. Bifani, H. Drobecq, C. Sergheraert, A.S. Debrie, C. Locht, and F.D. Menozzi Mycobacterial heparin-binding hemagglutinin and laminin-binding protein share antigenic methyllysines that confer resistance to proteolysis Proc. Natl. Acad. Sci. USA 99 2002 10759 10764
19. S.L. Mueller-Ortiz, E. Sepulveda, M.R. Olsen, C. Jagannath, A.R. Wanger, and S.J. Norris Decreased infectivity despite unaltered C3 binding by a DeltahbhA mutant of Mycobacterium tuberculosis Infect. Immun. 70 2002 6751 6760
20. C. Masungi, S. Temmerman, J.P. Van Vooren, A. Drowart, K. Pethe, F.D. Menozzi, C. Locht, and F. Mascart Differential T and B cell responses against Mycobacterium tuberculosis heparin-binding hemagglutinin adhesin in infected healthy individuals and patients with tuberculosis J. Infect. Dis. 185 2002 513 520
21. D.L. Lohse, and R.J. Linhardt Purification and characterization of heparin lyases from Flavobacterium heparinum J. Biol. Chem. 267 1992 24347 24355
22. R.M. Albrecht, S.R. Simmons, and J.B. Pawley J.E. Beesely Immunocytochemistry. A Practical Approach 1993 Oxford University Press New York, NY 151 176
23. G.C. Manara, C. Ferrari, L.B. Giorgi, G. Pasquinelli, in: M.A. Hayat, Boca Raton, F.C.P. (Eds.) Immunogold-silver staining, 1995, pp. 247-255.
24. S. Meresse, M.P. Dehouck, P. Delorme, M. Bensaid, J.P. Tauber, C. Delbart, J.C. Fruchart, and R. Cecchelli Bovine brain endothelial cells express tight junctions and monoamine oxidase activity in long-term culture J. Neurochem. 53 1989 1363 1371
25. M.P. Dehouck, P. Jolliet-Riant, F. Bree, J.C. Fruchart, R. Cecchelli, and J.P. Tillement Drug transfer across the blood-brain barrier: correlation between in vitro and in vivo models J. Neurochem. 58 1992 1790 1797
26. R. Cecchelli, B. Dehouck, L. Descamps, L. Fenart, V.V. Buee-Scherrer, C. Duhem, S. Lundquist, M. Rentfel, G. Torpier, and M.P. Dehouck In vitro model for evaluating drug transport across the blood-brain barrier Adv. Drug Deliv. Rev. 36 1999 165 178
27. J.D. Huber, R.D. Egleton, and T.P. Davis Molecular physiology and pathophysiology of tight junctions in the blood-brain barrier Trends Neurosci. 24 2001 719 725
28. S.I. Rapoport, and P.J. Robinson Tight-junctional modification as the basis of osmotic opening of the blood-brain barrier Ann. New York Acad. Sci. 481 1986 250 267
29. M. Bernfield, M. Götte, P.W. Park, O. Reizes, M.L. Fitzgerald, J. Lincecum, and M. zako Functions of cell surface heparan sulfate proteoglycans Annu. Rev. Biochem. 68 1999 729 777
30. F.D. Menozzi, K. Pethe, P. Bifani, F. Soncin, M.J. Brennan, and C. Locht Enhanced bacterial virulence through exploitation of host glycosaminoglycans Mol. Microbiol. 43 2002 1379 1386
31. S.H. Huang, M.F. Stins, and K.S. Kim Bacterial penetration across the blood-brain barrier during the development of neonatal meningitis Microbes Infect. 2 2000 1237 1244
32. B.B. Finlay, and P. Cossart Exploitation of mammalian host cell functions by bacterial pathogens Science 276 1997 718 725
33. S. Dramsi, and P. Cossart Intracellular pathogens and the actin cytoskeleton Annu. Rev. Cell Dev. Biol. 14 1998 137 166
34. R.A. Carabeo, S.S. Grieshaber, E. Fischer, and T. Hackstadt Chlamydia trachomatis induces remodeling of the actin cytoskeleton during attachment and entry into HeLa cells Infect. Immun. 70 2002 3793 3803
35. K.A. McDonough, Y. Kress, and B.R. Bloom Pathogenesis of tuberculosis: interaction of Mycobacterium tuberculosis with macrophages Infect. Immun. 61 1993 2763 2773
36. Q.N. Myrvik, E.S. Leake, and M.J. Wright Disruption of phagosomal membranes of normal alveolar macrophages by the H37Rv strain of Mycobacterium tuberculosis A correlate of virulence Am. Rev. Respir. Dis. 129 1984 322 328
37. C. Alvarez-Dominguez, J.A. Vazquez-Boland, E. Carrasco-Marin, P. Lopez-Mato, and F. Leyva-Cobian Host cell heparan sulfate proteoglycans mediate attachment and entry of Listeria monocytogenes, and the listerial surface protein ActA is involved in heparan sulfate receptor recognition Infect. Immun. 65 1997 78 88
38. C. Dehio, E. Freissler, C. Lanz, O.G. Gomez-Duarte, G. David, and T.F. Meyer Ligation of cell surface heparan sulfate proteoglycans by antibody-coated beads stimulates phagocytic uptake into epithelial cells: a model for cellular invasion by Neisseria gonorrhoeae Exp. Cell Res. 242 1998 528 539