Abstract
Interactions of virulent Leptospira interrogans with murine monocyte-macrophage-like J774A.1 cells and Vero (African green monkey kidney fibroblasts) cells from attachment to internalization were investigated by a series of morphological analysis. Fontana silver staining revealed that only the pathogenic leptospires were able to attach to host cells and the attachment pattern varied depending on cell types that they interacted with. Transmission electron microscopy (TEM) analysis confirmed the formation of the leptospires-containing phagosomes and their colocalization with lysosomes in macrophages were verified by confocal microscopic analysis. Results of F-actin rearrangements examination indicated that virulent leptospires invaded host cells via a microfilament-independent pathway.
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References
Levett PN (2001) Leptospirosis. Clin Microbiol Rev 14:296–326
Meslin FX (1997) Global aspects of emerging and potential zoonoses: a WHO perspective. Emerg Infect Dis 3:223–228
Lomar AV, Diament D, Torres JR (2000) Leptospirosis in Latin America. Infect Dis Clin North Am 14:vii–viii
Dai B (1992) Advances in research on leptospira and human leptospirosis in China. Chin Med Sci J 7:239–243
Ko AI, Galvao Reis M, Ribeiro Dourado CM, Johnson WD Jr, Riley LW (1999) Urban epidemic of severe leptospirosis in Brazil. Salvador Leptospirosis study group. Lancet 354:820–825
Vieira OV, Botelho RJ, Grinstein S (2002) Phagosome maturation: aging gracefully. Biochem J 366:689–704
Underhill DM (2005) Phagosome maturation: steady as she goes. Immunity 23:343–344
Merien F, Baranton G, Perolat P (1997) Invasion of Vero cells and induction of apoptosis in macrophages by pathogenic Leptospira interrogans are correlated with virulence. Infect Immun 65:729–738
Barocchi MA, Ko AI, Reis MG, McDonald KL, Riley LW (2002) Rapid translocation of polarized MDCK cell monolayers by Leptospira interrogans, an invasive but nonintracellular pathogen. Infect Immun 70:6926–6932
Ooteman MC, Vago AR, Koury MC (2006) Evaluation of MAT, IgM ELISA and PCR methods for the diagnosis of human leptospirosis. J Microbiol Methods 65:247–257
Lewis J (1978) The routine application of a microtechnique for the demonstration of leptospiral antibodies. J Med Microbiol 11:355–358
Cirone SM, Riemann HP, Ruppanner R, Behymer DE, Franti CE (1978) Evaluation of the hemagglutination test for epidemiologic studies of leptospiral antibodies in wild mammals. J Wildl Dis 14:193–202
Thiermann AB (1977) Incidence of leptospirosis in the detroit rat population. Am J Trop Med Hyg 26:970–974
Yamada Y, Wang XD, Yokoyama S, Fukuda N, Takakura N (2006) Cardiac progenitor cells in brown adipose tissue repaired damaged myocardium. Biochem Biophys Res Commun 342:662–670
Fernandez-Mora E, Polidori M, Luhmann A, Schaible UE, Haas A (2005) Maturation of Rhodococcus equi-containing vacuoles is arrested after completion of the early endosome stage. Traffic 6:635–653
Wu Z, Wong K, Glogauer M, Ellen RP, McCulloch CA (1999) Regulation of stretch-activated intracellular calcium transients by actin filaments. Biochem Biophys Res Commun 261:419–425
Kotani K, Yonezawa K, Hara K, Ueda H, Kitamura Y, Sakaue H, Ando A, Chavanieu A, Calas B, Grigorescu F (1994) Involvement of phosphoinositide 3-kinase in insulin- or IGF-1-induced membrane ruffling. Embo J 13:2313–2321
Peiffer I, Servin AL, Bernet-Camard MF (1998) Piracy of decay-accelerating factor (CD55) signal transduction by the diffusely adhering strain Escherichia coli C1845 promotes cytoskeletal F-actin rearrangements in cultured human intestinal INT407 cells. Infect Immun 66:4036–4042
Ghigo E, Capo C, Tung CH, Raoult D, Gorvel JP, Mege JL (2002) Coxiella burnetii survival in THP-1 monocytes involves the impairment of phagosome maturation: IFN-gamma mediates its restoration and bacterial killing. J Immunol 169:4488–4495
Kuehnel MP, Goethe R, Habermann A, Mueller E, Rohde M, Griffiths G, Valentin-Weigand P (2001) Characterization of the intracellular survival of Mycobacterium avium ssp. paratuberculosis: phagosomal pH and fusogenicity in J774 macrophages compared with other mycobacteria. Cell Microbiol 3:551–566
Clemens DL (1996) Characterization of the Mycobacterium tuberculosis phagosome. Trends Microbiol 4:113–118
Boullier S, Tasca C, Milon A (2003) New flow cytometric method to quantify the inhibition of enteropathogenic Escherichia coli adhesion by anti-adhesin antibodies. Cytometry A 53:79–87
Frick IM, Schmidtchen A, Sjobring U (2003) Interactions between M proteins of Streptococcus pyogenes and glycosaminoglycans promote bacterial adhesion to host cells. Eur J Biochem 270:2303–2311
Kallstrom H, Hansson-Palo P, Jonsson AB (2000) Cholera toxin and extracellular Ca2+ induce adherence of non-piliated Neisseria: evidence for an important role of G-proteins and Rho in the bacteria–cell interaction. Cell Microbiol 2:341–351
Falkow S, Isberg RR, Portnoy DA (1992) The interaction of bacteria with mammalian cells. Annu Rev Cell Biol 8:333–363
Brumell JH, Grinstein S (2003) Role of lipid-mediated signal transduction in bacterial internalization. Cell Microbiol 5:287–297
Baldwin TJ, Knutton S, Haigh R, Williams PH, Palmer HM, Aitken A, Borriello SP (1996) Hijacking host cell signal transduction mechanisms during infection with enteropathogenic Escherichia coli. Biochem Soc Trans 24:552–558
Dawson JR, Ellen RP (1990) Tip-oriented adherence of Treponema denticola to fibronectin. Infect Immun 58:3924–3928
Wang HP, Yan J, Li LW, Mao YF, Li SP, Luo YH (2005) Phospholipase C activity and alteration of intracellular free Ca2+ levels during internalization of Leptospira interrogans. Zhejiang Da Xue Xue Bao Yi Xue Ban 34:15–20
Faine S, Shahar A, Aronson M (1964) Phagocytosis and its significance in leptospiral infection. Aust J Exp Biol Med Sci 42:579–588
Beuzon CR, Meresse S, Unsworth KE, Ruiz-Albert J, Garvis S, Waterman SR, Ryder TA, Boucrot E, Holden DW (2000) Salmonella maintains the integrity of its intracellular vacuole though the action of SifA. Embo J 19:3235–3249
Brumell JH, Goosney DL, Finlay BB (2002) SifA, a type III secreted effector of Salmonella typhimurium, directs Salmonella-induced filament (Sif) formation along microtubules. Traffic 3:407–415
Brumell JH, Rosenberger CM, Gotto GT, Marcus SL, Finlay BB (2001) SifA permits survival and replication of Salmonella typhimurium in murine macrophages. Cell Microbiol 3:75–84
Brumell JH, Tang P, Zaharik ML, Finlay BB (2002) Disruption of the Salmonella-containing vacuole leads to increased replication of Salmonella enterica serovar typhimurium in the cytosol of epithelial cells. Infect Immun 70:3264–3270
Fratti RA, Chua J, Deretic V (2002) Cellubrevin alterations and Mycobacterium tuberculosis phagosome maturation arrest. J Biol Chem 277:17320–17326
Acknowledgments
We thank Dr Dong Yu (currently at the Department of Molecular Microbiology, Washington University School of Medicine) and Dr Wenying An (School of International Studies, Zhejiang University) for providing critical review of the manuscript and Dr Shuang Qiu for the excellent technical assistance. This work was supported by a Grant (30370072) from National Natural Science Foundation of China.
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Liu, Y., Zheng, W., Li, L. et al. Pathogenesis of leptospirosis: interaction of Leptospira interrogans with in vitro cultured mammalian cells. Med Microbiol Immunol 196, 233–239 (2007). https://doi.org/10.1007/s00430-007-0047-0
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DOI: https://doi.org/10.1007/s00430-007-0047-0