Polar invasion and translocation of neisseria meningitidis and streptococcus suis in a novel human model of the blood-cerebrospinal fluid barrier

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Schwerk, Christian ^a   Papandreou, Thalia ^a   Schuhmann, Daniel ^a   Nickol, Laura ^a   Borkowski, Julia ^a   Steinmann, Ulrike ^a   Quednau, Natascha ^a   Stump, Carolin ^a   Weiss, Christel ^a   Berger, Jürgen ^b   Wolburg, Hartwig ^c   Claus, Heike ^d   Vogel, Ulrich ^d   Ishikawa, Hiroshi ^e,f   Tenenbaum, Tobias ^a   Schroten, Horst ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

^c UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^d UNIVERSITY OF WÜRZBURG   (Germany)

^e JIKEI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^f NIPPON DENTAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

APICAL MEMBRANE; ARTICLE; BACTERIAL INVASION; BACTERIAL KINETICS; BACTERIAL TRANSLOCATION; BACTERIUM COLONY; BASOLATERAL MEMBRANE; BLOOD CEREBROSPINAL FLUID BARRIER; CELL POLARITY; ELECTRIC RESISTANCE; FLOW KINETICS; HUMAN; HUMAN CELL; HUMAN CHOROID PLEXUS PAPILLOMA CELL; MACROMOLECULE; MOLECULAR MECHANICS; NEISSERIA MENINGITIDIS; NONHUMAN; PROTEIN EXPRESSION; STREPTOCOCCUS SUIS; TIGHT JUNCTION; TUMOR CELL; ANIMAL; BACTERIAL COUNT; BACTERIAL MEMBRANE; BACTERIUM ADHERENCE; BIOLOGICAL MODEL; BLOOD BRAIN BARRIER; CELL MEMBRANE; CEREBROSPINAL FLUID; CHOROID PLEXUS; CYTOLOGY; EPITHELIUM; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMPEDANCE; METABOLISM; MICROBIOLOGY; MOVEMENT (PHYSIOLOGY); PAPILLOMA; PATHOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE; ULTRASTRUCTURE;

BACTERIA (MICROORGANISMS); NEISSERIA MENINGITIDIS; STREPTOCOCCUS SUIS;

FLUORESCEIN ISOTHIOCYANATE; INULIN; MEMBRANE PROTEIN;

ANIMALS; BACTERIAL ADHESION; BACTERIAL CAPSULES; BLOOD-BRAIN BARRIER; CELL LINE, TUMOR; CELL MEMBRANE; CELL POLARITY; CEREBROSPINAL FLUID; CHOROID PLEXUS; COLONY COUNT, MICROBIAL; ELECTRIC IMPEDANCE; EPITHELIUM; FLUORESCEIN-5-ISOTHIOCYANATE; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; INULIN; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; MOVEMENT; NEISSERIA MENINGITIDIS; PAPILLOMA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STREPTOCOCCUS SUIS; TIGHT JUNCTIONS;

EID: 84855716594     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0030069     Document Type: Article

References (61)

1. Kim KS, (2010) Acute bacterial meningitis in infants and children. Lancet Infect Dis 10: 32-42.
2. Koedel U, Klein M, Pfister HW, (2010) New understandings on the pathophysiology of bacterial meningitis. Curr Opin Infect Dis 23: 217-223.
3. Engelhardt B, Sorokin L, (2009) The blood-brain and the blood-cerebrospinal fluid barriers: function and dysfunction. Semin Immunopathol 31: 497-511.
4. Matter K, Balda MS, (2007) Epithelial tight junctions, gene expression and nucleo-junctional interplay. J Cell Sci 120: 1505-1511.
5. Matter K, Balda MS, (2003) Signalling to and from tight junctions. Nat Rev Mol Cell Biol 4: 225-236.
6. Hartsock A, Nelson WJ, (2008) Adherens and tight junctions: structure, function and connections to the actin cytoskeleton. Biochim Biophys Acta 1778: 660-669.
7. Abbott NJ, Patabendige AA, Dolman DE, Yusof SR, Begley DJ, (2010) Structure and function of the blood-brain barrier. Neurobiol Dis 37: 13-25.
8. Wolburg H, Paulus W, (2010) Choroid plexus: biology and pathology. Acta Neuropathol 119: 75-88.
9. Engelhardt B, Wolburg-Buchholz K, Wolburg H, (2001) Involvement of the choroid plexus in central nervous system inflammation. Microsc Res Tech 52: 112-129.
10. Stins MF, Badger J, Sik Kim K, (2001) Bacterial invasion and transcytosis in transfected human brain microvascular endothelial cells. Microb Pathog 30: 19-28.
11. Weksler BB, Subileau EA, Perriere N, Charneau P, Holloway K, et al. (2005) Blood-brain barrier-specific properties of a human adult brain endothelial cell line. FASEB J 19: 1872-1874.
12. Muruganandam A, Herx LM, Monette R, Durkin JP, Stanimirovic DB, (1997) Development of immortalized human cerebromicrovascular endothelial cell line as an in vitro model of the human blood-brain barrier. FASEB J 11: 1187-1197.
13. Shi LZ, Zheng W, (2005) Establishment of an in vitro brain barrier epithelial transport system for pharmacological and toxicological study. Brain Res 1057: 37-48.
14. Haselbach M, Wegener J, Decker S, Engelbertz C, Galla HJ, (2001) Porcine Choroid plexus epithelial cells in culture: regulation of barrier properties and transport processes. Microsc Res Tech 52: 137-152.
15. Gath U, Hakvoort A, Wegener J, Decker S, Galla HJ, (1997) Porcine choroid plexus cells in culture: expression of polarized phenotype, maintenance of barrier properties and apical secretion of CSF-components. Eur J Cell Biol 74: 68-78.
16. Kitazawa T, Hosoya K, Watanabe M, Takashima T, Ohtsuki S, et al. (2001) Characterization of the amino acid transport of new immortalized choroid plexus epithelial cell lines: a novel in vitro system for investigating transport functions at the blood-cerebrospinal fluid barrier. Pharm Res 18: 16-22.
17. Zheng W, Zhao Q, (2002) Establishment and characterization of an immortalized Z310 choroidal epithelial cell line from murine choroid plexus. Brain Res 958: 371-380.
18. Strazielle N, Ghersi-Egea J-F, (2011) In Vitro Models of the Blood-Cerebrospinal Fluid Barrier and Their Use in Neurotoxicological Research. Neuromethods 56: 161-184.
19. Kumabe T, Tominaga T, Kondo T, Yoshimoto T, Kayama T, (1996) Intraoperative radiation therapy and chemotherapy for huge choroid plexus carcinoma in an infant-case report. Neurol Med Chir (Tokyo) 36: 179-184.
20. Takahashi K, Satoh F, Hara E, Murakami O, Kumabe T, et al. (1997) Production and secretion of adrenomedullin by cultured choroid plexus carcinoma cells. J Neurochem 68: 726-731.
21. Szmydynger-Chodobska J, Pascale CL, Pfeffer AN, Coulter C, Chodobski A, (2007) Expression of junctional proteins in choroid plexus epithelial cell lines: a comparative study. Cerebrospinal Fluid Res 4: 11.
22. Ishiwata I, Ishiwata C, Ishiwata E, Sato Y, Kiguchi K, et al. (2005) Establishment and characterization of a human malignant choroids plexus papilloma cell line (HIBCPP). Hum Cell 18: 67-72.
23. Stephens DS, (2009) Biology and pathogenesis of the evolutionarily successful, obligate human bacterium Neisseria meningitidis. Vaccine 27 (Suppl 2): B71-77.
24. Sanford SE, (1987) Gross and histopathological findings in unusual lesions caused by Streptococcus suis in pigs. II. Central nervous system lesions. Can J Vet Res 51: 486-489.
25. Dominguez-Punaro MC, Segura M, Plante MM, Lacouture S, Rivest S, et al. (2007) Streptococcus suis serotype 2, an important swine and human pathogen, induces strong systemic and cerebral inflammatory responses in a mouse model of infection. J Immunol 179: 1842-1854.
26. Williams AE, Blakemore WF, (1990) Pathogenesis of meningitis caused by Streptococcus suis type 2. J Infect Dis 162: 474-481.
27. Madsen LW, Svensmark B, Elvestad K, Aalbaek B, Jensen HE, (2002) Streptococcus suis serotype 2 infection in pigs: new diagnostic and pathogenetic aspects. J Comp Pathol 126: 57-65.
28. Tenenbaum T, Papandreou T, Gellrich D, Friedrichs U, Seibt A, et al. (2009) Polar bacterial invasion and translocation of Streptococcus suis across the blood-cerebrospinal fluid barrier in vitro. Cell Microbiol 11: 323-336.
29. Lun ZR, Wang QP, Chen XG, Li AX, Zhu XQ, (2007) Streptococcus suis: an emerging zoonotic pathogen. Lancet Infect Dis 7: 201-209.
30. Mai NT, Hoa NT, Nga TV, Linh le D, Chau TT, et al. (2008) Streptococcus suis meningitis in adults in Vietnam. Clin Infect Dis 46: 659-667.
31. Guarner J, Greer PW, Whitney A, Shieh WJ, Fischer M, et al. (2004) Pathogenesis and diagnosis of human meningococcal disease using immunohistochemical and PCR assays. Am J Clin Pathol 122: 754-764.
32. Pron B, Taha MK, Rambaud C, Fournet JC, Pattey N, et al. (1997) Interaction of Neisseria maningitidis with the components of the blood-brain barrier correlates with an increased expression of PilC. J Infect Dis 176: 1285-1292.
33. Tenenbaum T, Matalon D, Adam R, Seibt A, Wewer C, et al. (2008) Dexamethasone prevents alteration of tight junction-associated proteins and barrier function in porcine choroid plexus epithelial cells after infection with Streptococcus suis in vitro. Brain Res 1229: 1-17.
34. Adam RA, Tenenbaum T, Valentin-Weigand P, Laryea M, Schwahn B, et al. (2004) Porcine choroid plexus epithelial cells induce Streptococcus suis bacteriostasis in vitro. Infect Immun 72: 3084-3087.
35. Vorbrodt AW, Dobrogowska DH, (2003) Molecular anatomy of intercellular junctions in brain endothelial and epithelial barriers: electron microscopist's view. Brain Res Brain Res Rev 42: 221-242.
36. Chodobski A, Szmydynger-Chodobska J, (2001) Choroid plexus: target for polypeptides and site of their synthesis. Microsc Res Tech 52: 65-82.
37. Dickson PW, Schreiber G, (1986) High levels of messenger RNA for transthyretin (prealbumin) in human choroid plexus. Neurosci Lett 66: 311-315.
38. Stylianopoulou F, Herbert J, Soares MB, Efstratiadis A, (1988) Expression of the insulin-like growth factor II gene in the choroid plexus and the leptomeninges of the adult rat central nervous system. Proc Natl Acad Sci U S A 85: 141-145.
39. Lim L, Zhou H, Costa RH, (1997) The winged helix transcription factor HFH-4 is expressed during choroid plexus epithelial development in the mouse embryo. Proc Natl Acad Sci U S A 94: 3094-3099.
40. Smith HE, Damman M, van der Velde J, Wagenaar F, Wisselink HJ, et al. (1999) Identification and characterization of the cps locus of Streptococcus suis serotype 2: the capsule protects against phagocytosis and is an important virulence factor. Infect Immun 67: 1750-1756.
41. Carbonnelle E, Hill DJ, Morand P, Griffiths NJ, Bourdoulous S, et al. (2009) Meningococcal interactions with the host. Vaccine 27 (Suppl 2): B78-89.
42. McGuinness BT, Clarke IN, Lambden PR, Barlow AK, Poolman JT, et al. (1991) Point mutation in meningococcal por A gene associated with increased endemic disease. Lancet 337: 514-517.
43. Vogel U, Morelli G, Zurth K, Claus H, Kriener E, et al. (1998) Necessity of molecular techniques to distinguish between Neisseria meningitidis strains isolated from patients with meningococcal disease and from their healthy contacts. J Clin Microbiol 36: 2465-2470.
44. Seiler A, Reinhardt R, Sarkari J, Caugant DA, Achtman M, (1996) Allelic polymorphism and site-specific recombination in the opc locus of Neisseria meningitidis. Mol Microbiol 19: 841-856.
45. Saito Y, Wright EM, (1983) Bicarbonate transport across the frog choroid plexus and its control by cyclic nucleotides. J Physiol 336: 635-648.
46. Villalobos AR, Miller DS, Renfro JL, (2002) Transepithelial organic anion transport by shark choroid plexus. Am J Physiol Regul Integr Comp Physiol 282: R1308-1316.
47. Virji M, Makepeace K, Peak IR, Ferguson DJ, Jennings MP, et al. (1995) Opc- and pilus-dependent interactions of meningococci with human endothelial cells: molecular mechanisms and modulation by surface polysaccharides. Mol Microbiol 18: 741-754.
48. Unkmeir A, Latsch K, Dietrich G, Wintermeyer E, Schinke B, et al. (2002) Fibronectin mediates Opc-dependent internalization of Neisseria meningitidis in human brain microvascular endothelial cells. Mol Microbiol 46: 933-946.
49. Charland N, Harel J, Kobisch M, Lacasse S, Gottschalk M, (1998) Streptococcus suis serotype 2 mutants deficient in capsular expression. Microbiology(144 (Pt 2): 325-332.
50. Segura M, Gottschalk M, Olivier M, (2004) Encapsulated Streptococcus suis inhibits activation of signaling pathways involved in phagocytosis. Infect Immun 72: 5322-5330.
51. Hammerschmidt S, Wolff S, Hocke A, Rosseau S, Muller E, et al. (2005) Illustration of pneumococcal polysaccharide capsule during adherence and invasion of epithelial cells. Infect Immun 73: 4653-4667.
52. Deghmane AE, Giorgini D, Larribe M, Alonso JM, Taha MK, (2002) Down-regulation of pili and capsule of Neisseria meningitidis upon contact with epithelial cells is mediated by CrgA regulatory protein. Mol Microbiol 43: 1555-1564.
53. Cunha CS, Griffiths NJ, Virji M, (2010) Neisseria meningitidis Opc invasin binds to the sulphated tyrosines of activated vitronectin to attach to and invade human brain endothelial cells. PLoS Pathog 6: e1000911.
54. Virji M, Makepeace K, Ferguson DJ, Achtman M, Sarkari J, et al. (1992) Expression of the Opc protein correlates with invasion of epithelial and endothelial cells by Neisseria meningitidis. Mol Microbiol 6: 2785-2795.
55. de Vries FP, Cole R, Dankert J, Frosch M, van Putten JP, (1998) Neisseria meningitidis producing the Opc adhesin binds epithelial cell proteoglycan receptors. Mol Microbiol 27: 1203-1212.
56. Doulet N, Donnadieu E, Laran-Chich MP, Niedergang F, Nassif X, et al. (2006) Neisseria meningitidis infection of human endothelial cells interferes with leukocyte transmigration by preventing the formation of endothelial docking structures. J Cell Biol 173: 627-637.
57. Mikaty G, Soyer M, Mairey E, Henry N, Dyer D, et al. (2009) Extracellular bacterial pathogen induces host cell surface reorganization to resist shear stress. PLoS Pathog 5: e1000314.
58. Lappann M, Haagensen JA, Claus H, Vogel U, Molin S, (2006) Meningococcal biofilm formation: structure, development and phenotypes in a standardized continuous flow system. Mol Microbiol 62: 1292-1309.
59. Benga L, Goethe R, Rohde M, Valentin-Weigand P, (2004) Non-encapsulated strains reveal novel insights in invasion and survival of Streptococcus suis in epithelial cells. Cell Microbiol 6: 867-881.
60. Spandidos A, Wang X, Wang H, Seed B, (2010) PrimerBank: a resource of human and mouse PCR primer pairs for gene expression detection and quantification. Nucleic Acids Res 38: D792-799.
61. Ram S, Cox AD, Wright JC, Vogel U, Getzlaff S, et al. (2003) Neisserial lipooligosaccharide is a target for complement component C4b. Inner core phosphoethanolamine residues define C4b linkage specificity. J Biol Chem 278: 50853-50862.