Cryptococcus neoformans phospholipase B1 activates host cell Rac1 for traversal across the blood-brain barrier

Cellular Microbiology

Volumn 14, Issue 10, 2012, Pages 1544-1553

  Maruvada, Ravi ^a   Zhu, Longkun ^a   Pearce, Donna ^a   Zheng, Yi ^b   Perfect, John ^c   Kwon Chung, Kyung J ^d   Kim, Kwang Sik ^a  

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

^b CINCINNATI CHILDREN S HOSPITAL RESEARCH FOUNDATION   (United States)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

ESTERASE; PHOSPHOLIPASE B1; RAC1 PROTEIN; STAT3 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; CELL ACTIVATION; CONTROLLED STUDY; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; FEMALE; FUNGUS TRANSMISSION; HUMAN; HUMAN CELL; MICROVASCULAR ENDOTHELIAL CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; TRANSCYTOSIS;

BLOOD-BRAIN BARRIER; CELL LINE; CRYPTOCOCCUS NEOFORMANS; ENDOTHELIAL CELLS; GENE EXPRESSION PROFILING; HOST-PATHOGEN INTERACTIONS; HUMANS; PHOSPHOLIPASES; PROTEIN BINDING; RAC1 GTP-BINDING PROTEIN; STAT3 TRANSCRIPTION FACTOR; TRANSCYTOSIS;

FILOBASIDIELLA NEOFORMANS;

EID: 84866312565     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2012.01819.x     Document Type: Article

References (35)

1. Akbar, H., Kim, J., Funk, K., Cancelas, J.A., Shang, X., Chen, L., etal. (2007) Genetic and pharmacologic evidence that Rac1 GTPase is involved in regulation of platelet secretion and aggregation. J Thromb Haemost 5: 1747-1755.
2. Casadevall, A., and Perfect, J.R. (1998) Cryptococcus neoformans. Washington, DC: American Society for Microbiology Press.
3. Chang, Y.C., Stins, M.F., McCaffery, M.J., Miller, G.F., Pare, D.R., Dam, T., etal. (2004) Cryptococcal yeast cells invade the central nervous system via transcellular penetration of the blood-brain barrier. Infect Immun 72: 4985-4995.
4. Charlier, C., Chretien, F., Baudrimont, M., Mordelet, E., Lortholary, O., and Dromer, F. (2005) Capsule structure changes associated with Cryptococcus neoformans crossing of the blood-brain barrier. Am J Pathol 166: 421-432.
5. Chin, S., Rozycki, G., Pugatch, D., and Harwell, J.I. (2004) Aetiology of meningitis in HIV-infected patients in a referral hospital in Phnom Penh, Cambodia. Int J STD AIDS 15: 48-50.
6. Chretien, F., Lortholary, O., Kansau, I., Neuville, S., Gray, F., and Dromer, F. (2002) Pathogenesis of cerebral Cryptococcus neoformans infection after fungemia. J Infect Dis 4: 522-530.
7. Chrisman, C.J., Albuquerque, P., Guimaraes, A.J., Nieves, E., and Casadevall, A. (2011) Phospholipids trigger Cryptococcus neoformans capsular enlargement during interactions with amoebae and macrophages. PLoS Pathog 7: e1002047. doi: 10.1371/journal.ppat.1002047.
8. Chuck, S.L., and Sande, M.A. (1989) Infections with Cryptococcus neoformans in the acquired immunodeficiency syndrome. N Engl J Med 321: 794-799.
9. Cox, G.M., McDade, H.C., Chen, S.C., Tucker, S.C., Gottfredsson, M., and Wright, L.C. (2001) Extracellular phospholipase activity is a virulence factor for Cryptococcus neoformans Mol Microbiol 39: 166-175.
10. Dromer, F., and Levitz, S. (2011) Chapter 34. Invasion of Cryptococcus into the central nervous system. In Cryptococcus, from Human Pathogen to Model Yeast. Heitman, J., Kozel, T.R., Kwon-Chung, K.J., Perfect, J.R., and Casadevall, A. (eds). Washington, DC: ASM Press: American Society of Microbiology, pp. 465-471.
11. French, N., Gray, K., Watera, C., Nakiyingi, J., Lugada, E., Moore, M., etal. (2002) Cryptococcal infection in a cohort of HIV-1-infected Ugandan adults. AIDS 16: 1031-1038.
12. Galan, J.E., and Zhou, D. (2000) Striking a balance: modulation of the actin cytoskeleton by Salmonella Proc Natl Acad Sci USA 97: 8754-8761.
13. Gao, Y., Dickerson, J.B., Guo, F., Zheng, J., and Zheng, Y. (2004) Rational design and characterization of a Rac GTPase-specific small molecule inhibitor. Proc Natl Acad Sci USA 101: 7618-7623.
14. Gordon, S.B., Walsh, A.L., Chaponda, M., Gordon, M.A., Soko, D., Mbwvinji, M., etal. (2000) Bacterial meningitis in Malawian adults: pneumococcal disease is common, severe, and seasonal. Clin Infect Dis 31: 53-57.
15. Hakim, J.G., Gangaidzo, I.T., Heyderman, R.S., Mielke, J., Mushangi, E., Taziwa, A., etal. (2000) Impact of HIV infection on meningitis in Harare, Zimbabwe: a prospective study of 406 predominantly adult patients. AIDS 14: 1401-1407.
16. Hall, A. (1998) Rho GTPases and the actin cytoskeleton. Science 279: 509-514.
17. Idnurm, A., Bahn, Y., Nielsen, K., Lin, X., Fraser, J.A., and Heitman, J. (2005) Deciphering the model pathogenic fungus Cryptococcus neoformans Nat Rev Microbiol 3: 753-764.
18. Kim, K.S. (2008) Mechanisms of microbial traversal of the blood-brain barrier. Nat Rev Microbiol 6: 625-634.
19. 2+ signaling by thrombin and protease-activated receptor-1-activating peptide in human brain microvascular endothelial cells. Am J Physiol Cell Physiol 286: C31-C42.
20. Lee, S.C., Dickson, D.W., and Casadevall, A. (1996) Pathology of cryptococcal meningoencephalitis: analysis of 27 patients with pathogenetic implications. Hum Pathol 8: 839-847.
21. Loftus, B.J., Fung, E., Roncaglia, P., Rowley, D., Amedeo, P., Bruno, D., etal. (2005) The genome of the basidiomycetous yeast and human pathogen Cryptococcus neoformans Science 307: 1321-1324.
22. Maruvada, R., and Kim, K.S. (2012) IbeA and OmpA of Escherichia coli K1 exploit Rac1 activation for invasion of human brain microvascular endothelial cells. Infect Immun 80: 2035-2041.
23. Mwaba, P., Mwansa, J., Chintu, C., Pobee, J., Scarborough, M., Portmouth, S., and Zumla, A. (2001) Clinical presentation, natural history, and cumulative death rates of 230 adults with primary cryptococcal meningitis in Zambian AIDS patients treated under local conditions. Postgrad Med J 77: 769-773.
24. Nhieu, G.T., and Sansonetti, P.J. (1999) Mechanism of shigella entry into epithelial cells. Curr Opin Microbiol 2: 51- 55.
25. Nichols, C.B., Perfect, Z.H., and Alspaugh, J.A. (2007) A Ras1-Cdc24 signal transduction pathway mediates thermotolerance in the fungal pathogen Cryptococcus neoformans Mol Microbiol 63: 1118-1130.
26. Olszewski, M.A., Noverr, M.C., Chen, G.-H., Toews, G.B., Cox, G.M., Perfect, J.R., and Huffnagle, G.B. (2004) Urease expression by Cryptococcus neoformans promotes microvascular sequestration, thereby enhancing central nervous system invasion. Am J Pathol 164: 1761-1771.
27. Perfect, J.R., and Casadevall, A. (2002) Cryptococcosis. Infect Dis Clin North Am 4: 837-874.
28. Rüffer, C., Strey, A., Janning, A., Kim, K.S., and Gerke, V. (2004) Cell-cell junctions of dermal microvascular endothelial cells contain tight and adherens junction proteins in spatial proximity. Biochemistry 43: 5360- 5369.
29. Shen, G., Zhou, E., Alspaugh, J.A., and Wang, P. (2012) Wsp1 is downstream of Cin1 and regulates vesicle transport and actin cytoskeleton as an effector of Cdc42 and Rac1 in Cryptococcus neoformans Eukaryot Cell 11: 471-481.
30. Shi, M., Li, S.S., Zheng, C., Jones, G.J., Kim, K.S., Zhou, H., etal. (2010) Real-time imaging of trapping and urease-dependent transmigration of Cryptococcus in the brain. J Clin Invest 120: 1683-1693.
31. Shin, S., and Kim, K.S. (2006) RhoA and Rac1 contribute to type III group B streptococcal invasion of human brain microvascular endothelial cells. Biochem Biophys Res Commun 345: 538-542.
32. Simon, A.R., Vikis, H.G., Stewart, S., Fanburg, B.L., Cochran, B.H., and Guan, K.L. (2000) Regulation of STAT3 by direct binding to the Rac1 GTPase. Science 290: 144-147.
33. Stins, M.F., Gilles, F., and Kim, K.S. (1997) Selective expression of adhesion molecules on human brain microvascular endothelial cells. J Neuroimmunol 76: 81-90.
34. Vallim, M.A., Nichols, C.B., Fernandes, L., Cramer, K.L., and Alspaugh, J.A. (2005) A Rac homolog functions downstream of Ras1 to control hyphal differentiation and high-temperature growth in the pathogenic fungus Cryptococcus neoformans Eukaryot Cell 4: 1066- 1078.
35. Zhu, L., Maruvada, R., Sapirstein, A., Malik, K.U., Peters-Golden, M., and Kim, K.S. (2010) Arachidonic acid metabolism regulates Escherichia coli penetration of the blood-brain barrier. Infect Immun 78: 4302- 4310.