Cryptococcal yeast cells invade the central nervous system via transcellular penetration of the blood-brain barrier

Infection and Immunity

Volumn 72, Issue 9, 2004, Pages 4985-4995

  Chang, Yun C ^a   Stins, Monique F ^c   McCaffery, Michael J ^d   Miller, Georgina F ^b   Pare, Dan R ^a   Dam, Tapen ^c   Paul Satyasee, Maneesh ^c   Kim, Kwang Sik ^c   Kwon Chung, Kyung J ^a,b  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; CENTRAL NERVOUS SYSTEM INFECTION; COLONY FORMING UNIT; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; ENDOTHELIUM CELL; FUNGAL MENINGITIS; HISTOPATHOLOGY; HUMAN; HUMAN CELL; MENINGITIS; MICROVASCULATURE; MOUSE; MYCOSIS; NONHUMAN; PRIORITY JOURNAL; YEAST CELL;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; CEREBROVASCULAR CIRCULATION; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; FEMALE; HUMANS; MICE; MICE, INBRED BALB C; MICROCIRCULATION; MICROSCOPY, ELECTRON, SCANNING;

EID: 4544298974     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.72.9.4985-4995.2004     Document Type: Article

References (42)

1. Badger, J. L., M. F. Stins, and K. S. Kim. 1999. Citrobacter freundii invades and replicates in human brain microvascular endothelial cells. Infect. Immun. 67:4208-4215.
2. Bogaerts, J., D. Rouvroy, H. Taelman, A. Kagame, M. A. Aziz, D. Swinne, and J. Verhaegen. 1999. AIDS-associated cryptococcal meningitis in Rwanda (1983-1992): epidemiologic and diagnostic features. J. Infect. 39:32-37.
3. Buchanan, K. L., and J. W. Murphy. 1998. What makes Cryptococcus neoformans a pathogen. Emerg. Infect. Dis. 4:71-83.
4. Chang, Y. C., R. Cherniak, T. R. Kozel, D. L. Granger, L. C. Morris, L. C. Weinhold, and K. J. Kwon-Chung. 1997. Structure and biological activities of acapsular Cryptococcus neoformans 602 complemented with the CAP64 gene. Infect. Immun. 65:1584-1592.
5. Chang, Y. C., and K. J. Kwon-Chung. 1994. Complementation of a capsule-deficient mutation of Cryptococcus neoformans restores its virulence. Mol. Cell. Biol. 14:4912-4919.
6. Chang, Y. C., and K. J. Kwon-Chung. 1998. Isolation of the third capsule-associated gene, CAP60, required for virulence in Cryptococcus neoformans. Infect. Immun. 66:2230-2236.
7. Chang, Y. C., and K. J. Kwon-Chung. 1999. Isolation, characterization, and localization of a capsule-associated gene, CAP10, of Cryptococcus neoformans. J. Bacteriol. 181:5636-5643.
8. Chang, Y. C., L. A. Penoyer, and K. J. Kwon-Chung. 1996. The second capsule gene of Cryptococcus neoformans, CAP64, is essential for virulence. Infect. Immun. 64:1977-1983.
9. Chen, S. H. M., M. F. Stins, S. H. Huang, Y. H. Chen, K. J. Kwon-Chung, Y. C. Chang, K. S. Kim, K. Suzuki, and A. Y. Jong. 2003. Cryptococcus neoformans induces alterations in cytoskeleton of human brain microvascular endothelial cells. J. Med. Microbiol. 52:961-970.
10. Chretien, F., O. Lortholary, I. Kansau, S. Neuville, F. Gray, and F. Dromer. 2002. Pathogenesis of cerebral Cyptococcus neoformans infection after fungemia. J. Infect. Dis. 186:522-530.
11. Cohen, Z., M. Ehret, M. Maitre, and E. Hamel. 1995. Ultrastructural analysis of tryptophan hydroxylase immunoreactive nerve terminals in the rat cerebral cortex and hippocampus: their associations with local blood vessels. Neuroscience 66:555-569.
12. Currie, B. P., and A. Casadevall. 1994. Estimation of the prevalence of cryptococcal infection among patients infected with the human immunodeficiency virus in New York City. Clin. Infect. Dis. 19:1029-1033.
13. Dallasta, L. M., L. A. Pisarov, J. E. Esplen, J. V. Werley, A. V. Moses, J. A. Nelson, and C. L. Achim. 1999. Blood-brain barrier tight junction distribution in human immunodeficiency virus-1 encephalitis. Am. J. Pathol. 155: 1915-1927.
14. Drevets, D. A., M. J. Dillon, J. S. Schawang, N. Van Rooijen, J. Ehrehen, C. Sunderkotter, and P. J. Leenen. 2004. The Ly-6C(high) monocyte subpopulation transports Listeria monocytogenes into the brain during systemic infection of mice. J. Immunol. 172:4418-4424.
15. Erlander, S. R. 1995. The solution to the seven mysteries of AIDS: the 'Trojan horse.' Med. Hypotheses 44:1-9.
16. Grab, D. J., O. Nikolskaia, Y. V. Kim, J. D. Lonsdale-Eccles, S. Ito, T. Hara, T. Fukuma, E. Nyarko, K. J. Kim, M. Stins, M. J. Delannoy, J. Rodgers, and K. S. Kim. African trypanosome interactions with an in vitro model of the human blood-brain barrier. J. Parasitol., in press.
17. Greiffenberg, L., W. Goebel, K. S. Kim, I. Weiglein, A. Bubert, F. Engelbrecht, M. Stins, and M. Kuhn. 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. Immun. 66:5260-5267.
18. Hakim, J. G., I. T. Gangaidzo, R. S. Heyderman, J. Mielke, E. Mushangi, A. Taziwa, V. J. Robertson, P. Musvaire, and P. R. Mason. 2000. Impact of HIV infection on meningitis in Harare, Zimbabwe: a prospective study of 406 predominantly adult patients. AIDS 14:1401-1407.
19. Huang, S. H., C. Wass, Q. Fu, N. V. Prasadarao, M. Stins, and K. S. Kim. 1995. Escherichia coli invasion of brain microvascular endothelial cells in vitro and in vivo: molecular cloning and characterization of invasion gene ibe10. Infect. Immun. 63:4470-4475.
20. Ibrahim, A. S., S. G. Filler, M. S. Alcouloumre, T. R. Kozel, J. E. J. Edwards, and M. A. Ghannoum. 1995. Adherence to and damage of endothelial cells by Cryptococcus neoformans in vitro: role of the capsule. Infect. Immun. 63:4368-4374.
21. Jaffe, E. A., L. W. Hoyer, and R. L. Nachman. 1973. Synthesis of antihemophilic factor by cultured endothelial cells. J. Clin. Investig. 52:2757-2764.
22. Jong, A. Y., M. F. Stins, S.-H. Huang, S. H. M. Chen, and K. S. Kim. 2001. Traversal of Candida albicans across human blood-brain barrier in vitro. Infect. Immun. 69:4536-4544.
23. Kim, K. S. 2000. E. coli invasion of brain microvascular endothelial cells as a pathogenetic basis of meningitis. Subcell. Biochem. 33:47-59.
24. Kim, K. S. 2003. Pathogenesis of bacterial meningitis: from bacteria to neuronal injury. Nat. Rev. Neurosci. 4:376-385.
25. Kwon-Chung, K. J., and J. E. Bennett. 1992. Medical mycology. Lea & Febiger, Philadelphia, Pa.
26. Lane, J. H., V. G. Sasseville, M. O. Smith, P. Vogel, D. R. Pauley, M. P. Heyes, and A. A. Lackner. 1996. Neuroinvasion by simian immunodeficiency virus coincides with increased numbers of perivascular macrophages/microglia and intrathecal immune activation. J. Neurovirol. 2:423-432.
27. Lonsdale-Eccles, J. D., and D. J. Grab. 2002. Trypanosome hydrolases and the blood-brain barrier. Trends Parasitol. 18:17-19.
28. McCaffery, J. M., and M. G. Farquhar. 1995. Localization of GTPases (GTP-binding proteins) by indirect immunofluorescence and immunoelectron microscopy. Methods Enzymol. 257:259-279.
29. Merkel, G., and B. A. Scofield. 1997. The in vitro interaction of Cryptococcus neoformans with primary rat lung cell cultures. FEMS Immunol. Med. Microbiol. 19:203-213.
30. Merkel, G. J., and B. A. Scofield. 1994. Comparisons between in vitro glial cell adherence and internalization of non-encapsulated and encapsulated strains of Cryptococcus neoformans. J. Med. Vet. Mycol. 32:361-372.
31. Nizet, V., K. S. Kim, M. Stins, M. Jonas, E. Y. Chi, D. Nguyen, and C. E. Rubens. 1997. Invasion of brain microvascular endothelial cells by group B streptococci. Infect. Immun. 65:5074-5081.
32. Pardridge, W. M. 1999. Blood-brain barrier biology and methodology. J. Neurovirol. 5:556-569.
33. Paspalas, C. D., and G. C. Papadopoulos. 1996. Ultrastructural relationships between noradrenergic nerve fibers and non-neural elements in the rat cerebral cortex. Glia 17:133-146.
34. Prasadarao, N. A., C. A. Wass, M. F. Stins, H. Shimada, and K. S. Kim. 1999. Outer membrane protein A-promoted actin condensation of brain microvasucular endothelial cells is required for Escherichia coli invasion. Infect. Immun. 67:5775-5783.
35. Prockop, L. D., and K. A. Naidu. 1997. Entry rate kinetics of D-mannitol and carboxy-inulin for transfer across the blood-cerebrospinal fluid barrier. J. Spinal Cord Med. 20:391-394.
36. Pujol, C., E. Eugene, L. de Saint Martin, and X. Nassif. 1997. Interaction of Neisseria meningitidis with a polarized monolayer of epithelial cells. Infect. Immun. 65:4836-4842.
37. Ring, A., J. N. Weiser, and E. I. Tuomanen. 1998. Pneumococcal trafficking across the blood-brain barrier. J. Clin. Investig. 102:347-360.
38. Rubin, L. L. 1999. The cell biology of the blood-brain barrier. Annu. Rev. Neurosci. 22:11-28.
39. Santangelo, R., H. Zoellner, T. Sorrell, C. Wilson, C. Donald, J. Djordjevic, Y. Shounan, and L. Wright. 2004. Role of extracellular pbospholipases and mononuclear pbagocytes in dissemination of cryptococcosis in a murine model. Infect. Immun. 72:2229-2239.
40. Stins, M. F., J. Badger, and K. S. Kim. 2001. Bacterial invasion and transcytosis in transfected human brain microvascular endothelial cells. Microb. Pathog. 30:19-28.
41. Stins, M. F., F. Gilles, and K. S. Kim. 1997. Selective expression of adhesion molecules on human brain microvascular endothelial cells. J. Neuroimmunol. 76:81-90.
42. Stins, M. F., Y. Shen, S. H. Huang, F. Gilles, V. K. Kalra, and K. S. Kim. 2001. Gp120 activates children's brain endothelial cells via CD4. J. Neurovirol. 7:125-134.