1. bookVolume 62 (2018): Issue 1 (March 2018)
Journal Details
License
Format
Journal
eISSN
2453-7837
First Published
30 Mar 2016
Publication timeframe
4 times per year
Languages
English
access type Open Access

Crossing the Blood-Brain Barrier by Neuroinvasive Pathogens

Published Online: 11 Apr 2018
Volume & Issue: Volume 62 (2018) - Issue 1 (March 2018)
Page range: 44 - 51
Received: 04 Dec 2017
Accepted: 17 Jan 2018
Journal Details
License
Format
Journal
eISSN
2453-7837
First Published
30 Mar 2016
Publication timeframe
4 times per year
Languages
English
Abstract

The penetration of the blood-brain barrier (BBB) and invasion of the central nervous system (CNS) are important steps for all neuroinvasive pathogens. All of the ways of pathogens passing through the BBB are still unclear. Among known pathways, pathogen traversal can occur paracellularly, transcellularly or using a “Trojan horse” mechanism. The first step of translocation across the BBB is the interactions of the pathogen’s ligands with the receptors of the host brain cells. Lyme disease, the most common vector-borne disease in the temperate zones of Europe and North America, are caused by Borreliella species (former Borrelia burgdorferi sensu lato) that affects the peripheral and the CNS. In this review, we have presented various pathogen interactions with endothelial cells, which allow the disruption of the BBB so that the pathogens can pass across the BBB.

Keywords

1. Abbott, N. J., Ronnback, L., Hansson, E., 2006: Astrocyteendothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci., 7, 41—53.10.1038/nrn1824Search in Google Scholar

2. Archer, D. P., Ravussin, P. A., 1994: Role of blood-brain barrier in cerebral homeostasis. Ann. Fr. Anesth. Reanim., 13, 57—61.10.1016/S0750-7658(94)80187-8Search in Google Scholar

3. Badger, J. L., Stins, M. F., Kim, K. S., 1999: Citrobacter freundii invades and replicates in human brain microvascular endothelial cells. Infect. Immunol., 67, 4208—4215.10.1128/IAI.67.8.4208-4215.1999Search in Google Scholar

4. Berge, A., Sjobring, U., 1993: PAM, a novel plasminogenbinding protein from Streptococcus pyogenes. J. Biol. Chem., 268, 25417—25424.10.1016/S0021-9258(19)74408-1Search in Google Scholar

5. Braun, L., Ohayon, H., Cossart, P., 1998: The InIB protein of Listeria monocytogenes is sufficient to promote entry into mammalian cells. Mol. Microbiol., 27, 1077—1087.10.1046/j.1365-2958.1998.00750.xOpen DOISearch in Google Scholar

6. Cabanes, D., Sousa, S., Cebria, A., Lecuit, M., Garcia-del Portillo, F., Cossart, P., 2005: Gp96 is a receptor for a novel Listeria monocytogenes virulence factor, Vip, a surface protein. EMBO J., 24, 2827—2838.10.1038/sj.emboj.7600750Open DOISearch in Google Scholar

7. Coleman, J. L., Roemer, E. J., Benach, J. L., 1999: Plasmincoated Borrelia burgdorferi degrades soluble and insoluble components of the mammalian extracellular matrix. Infect. Immunol., 67, 3929—3936.10.1128/IAI.67.8.3929-3936.1999Search in Google Scholar

8. Coleman, J. L., Gebbia, J. A., Benach, J. L., 2001:Borrelia burgdorferi and other bacterial products induce expression and release of the urokinase receptor (CD87). J. Immunol., 166, 473—480.10.4049/jimmunol.166.1.473Search in Google Scholar

9. Comstock, L. E., Thomas, D. D., 1991: Characterization of Borrelia burgdorferi invasion of cultured endothelial cells. Microb. Pathog., 10, 137—148.10.1016/0882-4010(91)90074-KSearch in Google Scholar

10. Coureuil, M., Mikaty, G., Miller, F., Bourdoulous, S., Duménil, G., Mège, R. M., et al., 2009: Meningococcal type IV pili recruit the polarity complex to cross the brain endothelium. Science, 325, 83—87.10.1126/science.1173196Search in Google Scholar

11. Chang, Y. C., Stins, M. F., McCaffery, M. J., Miller, G. F., Pare, D. R., Dam, T., et al., 2004: Cryptococcal yeast cells invade the central nervous system via transcellular penetration of the blood-brain barrier. Infect. Immunol., 72, 4985—4995.10.1128/IAI.72.9.4985-4995.2004Search in Google Scholar

12. Charlier, C., Chretien, F., Baudrimont, M., Mordelet, E., Lortholary, O., Dromer, F., 2005: Capsule structure changes associated with Cryptococcus neoformans crossing of the blood-brain barrier. Am. J. Pathol., 166, 421—432 C.10.1016/S0002-9440(10)62265-1Search in Google Scholar

13. Chauhan, V. S., Kluttz, J. M., Bost, K. L., Marriott, I., 2011: Prophylactic and therapeutic targeting of the neurokinin-1 receptor limits neuroinflammation in a murine model of pneumococcal meningitis. J. Immunol., 186, 7255—7263.10.4049/jimmunol.1100721Search in Google Scholar

14. Chung, J. W., Hong, S. J., Kim, K. J., Goti, D., Stins, M. F., Shin, S., et al., 2003: 37-kDa laminin receptor precursor modulates cytotoxic necrotizing factor 1-mediated RhoA activation and bacterial uptake. J. Biol. Chem., 278, 16857—16862.10.1074/jbc.M301028200Search in Google Scholar

15. Drevets, D. A., Dillon, M. J., Schawang, J. S., Van Rooijen, N., Ehrchen, J., Sunderkotter, C., et al., 2004: The Ly-6Chigh monocyte subpopulation transports Listeria monocytogenes into the brain during systemic infection of mice. J. Immunol., 172, 4418—4424.10.4049/jimmunol.172.7.4418Search in Google Scholar

16. Fuchs, H., Wallich, R., Simon, M. M., Kramer, M. D., 1994: The outer surface protein A of the spirochete Borrelia burgdorferi is a plasmin(ogen) receptor. Proc. Natl. Acad. Sci. USA, 91, 12594—12598.10.1073/pnas.91.26.12594Open DOISearch in Google Scholar

17. Furuse, M., Itoh, M., Hirase, T., Nagafuchi, A., Yonemura, S., Tsukita, S., 1994: Direct association of occludin with ZO-1 and its possible involvement in the localization of occludin at tight junctions. J. Cell Biol., 127, 1617—1626.10.1083/jcb.127.6.1617Search in Google Scholar

18. Furuse, M., Fujita, K., Hiiragi, T., Fujimoto, K., Tsukita, S., 1998: Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin. J. Cell Biol., 141, 1539—1550.10.1083/jcb.141.7.1539Search in Google Scholar

19. Gebbia, J. A., Coleman, J. L., Benach, J. L., 2001:Borrelia spirochetes upregulate release and activation of matrix metalloproteinase gelatinase B (MMP-9) and collagenase 1 (MMP-1) in human cells. Infect. Immunol., 69, 456—462.10.1128/IAI.69.1.456-462.2001Search in Google Scholar

20. Grab, D. J., Nikolskaia, O., Kim, Y. V., Lonsdale-Eccles, J. D., Ito, S., Hara, T., et al., 2004: African trypanosome interactions with an in vitro model of the human blood-brain barrier. J. Parasitol., 90, 970—979.10.1645/GE-287ROpen DOISearch in Google Scholar

21. Greiffenberg, L., Goebel, W., Kim, K. S., Weiglein, I., Bubert, A., Engelbrecht, F., et al., 1998: Interaction of Listeria monocytogenes with human brain microvascular endothelial cells: InlB-dependent invasion, long-term intracellular growth, and spread from macrophages to endothelial cells. Infect. Immunol., 66, 5260—5267.10.1128/IAI.66.11.5260-5267.1998Search in Google Scholar

22. Haake, D. A., Lovett, M. A., 1994: Interjunctional invasion of endothelial cell monolayers. Methods Enzymol., 236, 447—463.10.1016/0076-6879(94)36033-2Search in Google Scholar

23. Hawkins, B. T., Davis, T. P., 2005: The blood-brain barrier/neurovascular unit in health and disease. Pharmacol. Rev., 57, 173—185.10.1124/pr.57.2.4Open DOISearch in Google Scholar

24. Hoffman, O., Weber, R. J., 2009: Pathophysiology and treatment of bacterial meningitis. Advances in Neurological Disorders, 2, 1—7.10.1177/1756285609337975Search in Google Scholar

25. Hu, L. T., Pratt, S. D., Perides, G., Katz, L., Rogers, R. A., Klempner, M. S., 1997: Isolation, cloning, and expression of a 70-kilodalton plasminogen binding protein of Borrelia burgdorferi. Infect. Immunol., 65, 4989—4995.10.1128/iai.65.12.4989-4995.1997Search in Google Scholar

26. Huang, S. H., Wass, C., Fu, Q., Prasadarao, N. V., Stins, M., Kim, K. S., 1995:Escherichia coli invasion of brain microvascular endothelial cells in vitro and in vivo: molecular cloning and characterization of invasion gene ibe10. Infect. Immunol., 63, 4470—4475.10.1128/iai.63.11.4470-4475.1995Search in Google Scholar

27. Jain, S. K., Paul-Satyaseela, M., Lamichhane, G., Kim, K. S., Bishai, W. R., 2006: Mycobacterium tuberculosis invasion and traversal across an in vitro human blood-brain barrier as a pathogenic mechanism for central nervous system tuberculosis. J. Infect. Dis., 193, 1287—1295.10.1086/502631Search in Google Scholar

28. Jong, A. Y., Stins, M. F., Huang, S. H., Chen, S. H., Kim, K. S., 2001: Traversal of Candida albicans across human blood-brain barrier in vitro. Infect. Immunol., 69, 4536—4544.10.1128/IAI.69.7.4536-4544.2001Search in Google Scholar

29. Khan, N. A., Kim, Y., Shin, S., Kim, K. S., 2007: FimH-mediated Escherichia coli K1 invasion of human brain microvascular endothelial cells. Cell Microbiol., 9, 169—178.10.1111/j.1462-5822.2006.00779.xSearch in Google Scholar

30. Kim, K. S., 2008: Mechanisms of microbial traversal of the blood-brain barrier. Nat. Rev. Microbiol., 6, 625—634.10.1038/nrmicro1952Open DOISearch in Google Scholar

31. Klempner, M. S., Noring, R., Epstein, M. P., McCloud, B., Hu, R., Limentani, S. A., et al., 1995: Binding of human plasminogen and urokinase-type plasminogen activator to the Lyme disease spirochete, Borrelia burgdorferi. J. Infect. Dis., 171, 1258—1265.10.1093/infdis/171.5.1258Search in Google Scholar

32. Mach, F., Schonbeck, U., Bonnefoy, J. Y., Pober, J. S., Libby, P., 1997: Activation of monocyte/macrophage functions related to acute atheroma complication by ligation of CD40: induction of collagenase, stromelysin, and tissue factor. Circulation, 96, 396—9.10.1161/01.CIR.96.2.396Open DOISearch in Google Scholar

33. Maisey, H. C., Hensler, M., Nizet, V., Doran, K. S., 2007: Group B streptococcal pilus proteins contribute to adherence to and invasion of brain microvascular endothelial cells. J. Bacteriol., 189, 1464—1467.10.1128/JB.01153-06Search in Google Scholar

34. Martin-Padura, I., Lostaglio, S., Schneemann, M., Williams, L., Romano, M., Fruscella, P., et al., 1998: Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration. J. Cell Biol., 142, 117—127.10.1083/jcb.142.1.117Search in Google Scholar

35. Miyoshi, J., Takai, Y., 2005: Molecular perspective on tightjunction assembly and epithelial polarity. Advances Drug Delivery Reviews, 57, 815—855.10.1016/j.addr.2005.01.008Open DOISearch in Google Scholar

36. Nasdala, I., Wolburg-Buchholz, K., Wolburg, H., Kuhn, A., Ebnet, K., Brachtendorf, G., et al., 2002: A transmembrane tight junction protein selectively expressed on endothelial cells and platelets. J. Biol. Chem., 277, 16294—16303.10.1074/jbc.M111999200Search in Google Scholar

37. Nassif, X., Pujol, C., Morand, P., Eugene, E., 1999: Interactions of pathogenic Neisseria with host cells. Is it possible to assemble the puzzle ? Mol. Microbiol., 32, 1124—1132.10.1046/j.1365-2958.1999.01416.xSearch in Google Scholar

38. Nassif, X., Bourdoulous, S., Eugene, E., Couraud, P. O., 2002: How do extracellular pathogens cross the blood-brain barrier ? Trends Microbiol., 10, 227—232.10.1016/S0966-842X(02)02349-1Search in Google Scholar

39. Nguyen, L., Pieters, J., 2005: The Trojan horse: survival tactics of pathogenic mycobacteria in macrophages. Trends Cell Biol., 15, 269—276.10.1016/j.tcb.2005.03.009Open DOISearch in Google Scholar

40. Nizet, V., Kim, K. S., Stins, M., Jonas, M., Chi, E. Y., Nguyen, D., et al., 1997: Invasion of brain microvascular endothelial cells by group B streptococci. Infect. Immunol., 65, 5074—5081.10.1128/iai.65.12.5074-5081.1997Search in Google Scholar

41. Orihuela, C. J., Mahdavi, J., Thornton, J., Mann, B., Wooldridge, K. G., Abouseada, N., et al., 2009: Laminin receptor initiates bacterial contact with the blood brain barrier in experimental meningitis models. J. Clin. Invest., 119, 1638—1646.10.1172/JCI36759Search in Google Scholar

42. Perides, G., Noring, R., Klempner, M. S., 1996: Inhibition of Borrelia burgdorferi-bound fibrinolytic enzymes by alpha2-antiplasmin, PAI-1 and PAI-2. Biochem. Bioph. Res. Comm., 219, 690—695.10.1006/bbrc.1996.0296Search in Google Scholar

43. Plant, L., Sundqvist, J., Zughaier, S., Lovkvist, L., Stephens, D. S, Jonsson, A. B., 2006: Lipooligosaccharide structure contributes to multiple steps in the virulence of Neisseria meningitidis. Infect. Immunol., 74, 1360—1367.10.1128/IAI.74.2.1360-1367.2006Search in Google Scholar

44. Prasadarao, N. V., Srivastava, P. K., Rudrabhatla, R. S., Kim, K. S., Huang, S. H., Sukumaran, S. K., 2003: Cloning and expression of the Escherichia coli K1 outer membrane protein A receptor, a gp96 homologue. Infect. Immunol., 71, 1680—1688.10.1128/IAI.71.4.1680-1688.2003Search in Google Scholar

45. Ring, A., Weiser, J. N., Tuomanen, E. I., 1998: Pneumococcal trafficking across the blood-brain barrier. Molecular analysis of a novel bidirectional pathway. J. Clin. Invest., 102, 347—360.10.1172/JCI2406Open DOISearch in Google Scholar

46. Rupprecht, T. A., Koedel, U., Heimerl, C., Fingerle, V., Paul, R., Wilske, B., et al., 2006: Adhesion of Borrelia garinii to neuronal cells is mediated by the interaction of OspA with proteoglycans. J. Neuroimmunol., 175, 5—11.10.1016/j.jneuroim.2006.02.007Search in Google Scholar

47. Shen, Y., Naujokas, M., Park, M., Ireton, K., 2000: InIBdependent internalization of Listeria is mediated by the Met receptor tyrosine kinase. Cell, 103, 501—510.10.1016/S0092-8674(00)00141-0Search in Google Scholar

48. Schonbeck, U., Mach, F., Sukhova, G. K., Murphy, C., Bonnefoy, J. Y., Fabunmi, R. P., Libby, P., 1997: Regulation of matrix metalloproteinase expression in human vascular smooth muscle cells by T lymphocytes: a role for CD40 signaling in plaque rupture? Circ. Res., 81, 448—54.10.1161/01.RES.81.3.448Search in Google Scholar

49. Steere, A. C., 2001: Lyme disease. N. Engl. J. Med., 345, 115—125.10.1056/NEJM200107123450207Search in Google Scholar

50. Sukhova, G. K., Schönbeck, U., Rabkin, E., Schoen, F. J., Poole, A. R., Billinghurst, R. C., Libby, P., 1999: Evidence for increased collagenolysis by interstitial collagenases-1 and -3 in vulnerable human atheromatous plaques. Circulation, 99, 2503—2509.10.1161/01.CIR.99.19.2503Search in Google Scholar

51. Szczepanski, A., Furie, M. B., Benach, J. L., Lane, B. P., Fleit, H. B., 1990: Interaction between Borrelia burgdorferi and endothelium in vitro. J. Clin. Invest., 85, 1637—1647.10.1172/JCI114615Search in Google Scholar

52. Tao-Cheng, J. H., Brightman, M. W., 1988: Development of membrane interactions between brain endothelial cells and astrocytes in vitro. Int. J. Dev. Neurosci., 6, 25—37.10.1016/0736-5748(88)90026-3Open DOISearch in Google Scholar

53. Tenenbaum, T., Bloier, C., Adam, R., Reinscheid, D. J., Schroten, H., 2005: Adherence to and invasion of human brain microvascular endothelial cells are promoted by fibrinogen-binding protein FbsA of Streptococcus agalactiae. Infect. Immunol., 73, 4404—4409.10.1128/IAI.73.7.4404-4409.2005Search in Google Scholar

54. Thomas, D. D., Navab, M., Haake, D. A., Fogelman, A. M., Miller, J. N., Lovett, M. A., 1988: Treponema pallidum invades intercellular junctions of endothelial cell monolayers. Proc. Natl. Acad. Sci. USA, 85, 3608—3612.10.1073/pnas.85.10.3608Search in Google Scholar

55. Tuomanen, E., 1996: Entry of pathogens into the central nervous system. FEMS Microbiol. Rev., 18, 289—299.10.1111/j.1574-6976.1996.tb00245.xSearch in Google Scholar

56. Unkmeir, A., Latsch, K., Dietrich, G., Wintermeyer, E., Schinke, B., Schwender, S., 2002: Fibronectin mediates Opcdependent internalization of Neisseria meningitidis in human brain microvascular endothelial cells. Mol. Microbiol., 46, 933—946.10.1046/j.1365-2958.2002.03222.xOpen DOISearch in Google Scholar

Recommended articles from Trend MD

Plan your remote conference with Sciendo