Lipid raft/caveolae signaling is required for Cryptococcus neoformans invasion into human brain microvascular endothelial cells

Journal of Biomedical Science

Volumn 19, Issue 1, 2012, Pages

  Long, Min ^b   Huang, Sheng He ^a   Wu, Chun Hua ^a   Shackleford, Gregory M ^a   Jong, Ambrose ^a  

^a CHILDREN S HOSPITAL LOS ANGELES   (United States)

^b SOUTHERN MEDICAL UNIVERSITY   (China)

Author keywords

brain microvascular endothelial cells; caveolin 1; CD44; Cryptococcus neoformans; lipid raft

Indexed keywords

CAVEOLIN 1; CD44V ANTIGEN; FILIPIN; MEMBRANE LIPID; SMALL INTERFERING RNA; CD44 PROTEIN, HUMAN; HERMES ANTIGEN;

ACTIN FILAMENT; ARTICLE; BLOOD BRAIN BARRIER; CAVEOLA; CONTROLLED STUDY; CRYPTOCOCCUS NEOFORMANS; IMMUNOFLUORESCENCE MICROSCOPY; LIPID RAFT; MEMBRANE STRUCTURE; MICROVASCULAR ENDOTHELIAL CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; CELL CULTURE; CELL MEMBRANE; CENTRAL NERVOUS SYSTEM INFECTION; CYTOLOGY; DRUG EFFECT; ENDOCYTOSIS; ENDOTHELIUM CELL; GENE SILENCING; GENETICS; HUMAN; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHOSPHORYLATION;

FILOBASIDIELLA NEOFORMANS;

ACTIN CYTOSKELETON; ANTIGENS, CD44; BLOOD-BRAIN BARRIER; CAVEOLAE; CAVEOLIN 1; CELL MEMBRANE; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM INFECTIONS; CRYPTOCOCCUS NEOFORMANS; ENDOCYTOSIS; ENDOTHELIAL CELLS; FILIPIN; GENE KNOCKDOWN TECHNIQUES; HUMANS; MEMBRANE MICRODOMAINS; PHOSPHORYLATION; RNA, SMALL INTERFERING;

EID: 84862817605     PISSN: 10217770     EISSN: 14230127     Source Type: Journal    
DOI: 10.1186/1423-0127-19-19     Document Type: Article

References (36)

1. Host-pathogen interactions: the attributes of virulence. Casadevall A, Pirofski L, J Infect Dis 2001 184 337 344 10.1086/322044 11443560 (Pubitemid 32662181)
2. The biology of the Cryptococcus neoformans species complex. Lin X, Heitman J, Annu Rev Microbiol 2006 60 69 105 69-105 10.1146/annurev.micro.60. 080805.142102 16704346 (Pubitemid 44627941)
3. Estimation of the current global burden of cryptococcal meningitis among persons living with HIV/AIDS. Park BJ, Wannemuehler KA, Marston BJ, Govender N, Pappas PG, Chiller TM, AIDS 2009 23 525 530 10.1097/QAD.0b013e328322ffac 19182676
4. The cell biology of the blood-brain barrier. Rubin LL, Staddon JM, Annu Rev Neurosci 1999 22 11 28 10.1146/annurev.neuro.22.1.11 10202530 (Pubitemid 29144879)
5. The capsule of the fungal pathogen Cryptococcus neoformans. Zaragoza O, Rodrigues ML, De Jesus M, Frases S, Dadachova E, Casadevall A, Adv Appl Microbiol 2009 68 133 216 133-216 19426855
6. Real-time imaging of trapping and urease-dependent transmigration of Cryptococcus neoformans in mouse brain. Shi M, Li SS, Zheng C, Jones GJ, Kim KS, Zhou H, Kubes P, Mody CH, J Clin Invest 2010 120 1683 1693 10.1172/JCI41963 20424328
7. Capsule structure changes associated with Cryptococcus neoformans crossing of the blood-brain barrier. Charlier C, Chretien F, Baudrimont M, Mordelet E, Lortholary O, Dromer F, Am J Pathol 2005 166 421 432 10.1016/S0002-9440(10)62265-1 15681826 (Pubitemid 40189039)
8. Pathogenesis of cerebral Cryptococcus neoformans infection after fungemia. Chretien F, Lortholary O, Kansau I, Neuville S, Gray F, Dromer F, J Infect Dis 2002 186 522 530 10.1086/341564 12195380 (Pubitemid 34876262)
9. Identification and characterization of CPS1 as a hyaluronic acid synthase contributing to the pathogenesis of C. neoformans infection. Jong A, Wu CH, Chen HM, Luo F, Kwon-Chung KJ, Chang YC, Lamunyon CW, Plaas A, Huang SH, Eukaryot Cell 2007 6 1486 1496 10.1128/EC.00120-07 17545316 (Pubitemid 47257717)
10. Invasion of Cryptococcus neoformans into human brain microvascular endothelial cells requires protein kinase C-alpha activation. Jong A, Wu CH, Prasadarao NV, Kwon-Chung KJ, Chang YC, Ouyang Y, Shackleford GM, Huang SH, Cell Microbiol 2008 10 1854 1865 10.1111/j.1462-5822.2008.01172.x 18489726
11. Urease expression by Cryptococcus neoformans promotes microvascular sequestration, thereby enhancing central nervous system invasion. Olszewski MA, Noverr MC, Chen GH, Toews GB, Cox GM, Perfect JR, Huffnagle GB, Am J Pathol 2004 164 1761 1771 10.1016/S0002-9440(10)63734-0 15111322 (Pubitemid 38529778)
12. Role of extracellular phospholipases and mononuclear phagocytes in dissemination of cryptococcosis in a murine model. Santangelo R, Zoellner H, Sorrell T, Wilson C, Donald C, Djordjevic J, Shounan Y, Wright L, Infect Immun 2004 72 2229 2239 10.1128/IAI.72.4.2229-2239.2004 15039347 (Pubitemid 38419938)
13. CPS1, a homolog of the Streptococcus pneumoniae type 3 polysaccharide synthase gene, is important for the pathobiology of Cryptococcus neoformans. Chang YC, Jong A, Huang S, Zerfas P, Kwon-Chung KJ, Infect Immun 2006 74 3930 3938 10.1128/IAI.00089-06 16790766 (Pubitemid 43993325)
14. Involvement of human CD44 during Cryptococcus neoformans infection of brain microvascular endothelial cells. Jong A, Wu CH, Shackleford GM, Kwon-Chung KJ, Chang YC, Chen HM, Ouyang Y, Huang SH, Cell Microbiol 2008 10 1313 1326 10.1111/j.1462-5822.2008.01128.x 18248627 (Pubitemid 351663922)
15. Cryptococcus neoformans induces alterations in cytoskeleton of human brain microvascular endothelial cells. Chen HM, Stins SF, Huang HS, Chen YH, Kwon-Chung KJ, Chang YC, Kim KSJA, J Med Microbiol 2003 52 961 970 10.1099/jmm.0.05230-0 14532340 (Pubitemid 38648135)
16. Invasion of Cryptococcus neoformans into Human Brain Microvascular Endothelial Cells Is Mediated through the Lipid Rafts-Endocytic Pathway via the Dual Specificity Tyrosine Phosphorylation-regulated Kinase 3 (DYRK3). Huang SH, Long M, Wu CH, Kwon-Chung KJ, Chang YC, Chi F, Lee S, Jong A, J Biol Chem 2011 286 34761 34769 10.1074/jbc.M111.219378 21693704
17. Regulation of raft-dependent endocytosis. Lajoie P, Nabi IR, J Cell Mol Med 2007 11 644 653 10.1111/j.1582-4934.2007.00083.x 17760830 (Pubitemid 47313313)
18. Caveolae/raft-dependent endocytosis. Nabi IR, Le PU, J Cell Biol 2003 161 673 677 10.1083/jcb.200302028 12771123 (Pubitemid 36648749)
19. Lipid rafts and caveolae as portals for endocytosis: new insights and common mechanisms. Parton RG, Richards AA, Traffic 2003 4 724 738 10.1034/j.1600-0854.2003.00128.x 14617356 (Pubitemid 37361854)
20. The multiple faces of caveolae. Parton RG, Simons K, Nat Rev Mol Cell Biol 2007 8 185 194 17318224
21. Dual control of caveolar membrane traffic by microtubules and the actin cytoskeleton. Mundy DI, Machleidt T, Ying YS, Anderson RG, Bloom GS, J Cell Sci 2002 115 4327 4339 10.1242/jcs.00117 12376564 (Pubitemid 35460703)
22. The caveolin proteins. Williams TM, Lisanti MP, Genome Biol 2004 5 214 10.1186/gb-2004-5-3-214 15003112 (Pubitemid 38444510)
23. Caveolins: structure and function in signal transduction. Krajewska WM, Maslowska I, Cell Mol Biol Lett 2004 9 195 220 15213803 (Pubitemid 38902217)
24. Palmitoylation of caveolin-1 at a single site (Cys-156) controls its coupling to the c-Src tyrosine kinase: targeting of dually acylated molecules (GPI-linked, transmembrane, or cytoplasmic) to caveolae effectively uncouples c-Src and caveolin-1 (TYR-14). Lee H, Woodman SE, Engelman JA, Volonte D, Galbiati F, Kaufman HL, Lublin DM, Lisanti MP, J Biol Chem 2001 276 35150 35158 10.1074/jbc.M104530200 11451957
25. Constitutive and growth factor-regulated phosphorylation of caveolin-1 occurs at the same site (Tyr-14) in vivo: identification of a c-Src/Cav-1/Grb7 signaling cassette. Lee H, Volonte D, Galbiati F, Iyengar P, Lublin DM, Bregman DB, Wilson MT, Campos-Gonzalez R, Bouzahzah B, Pestell RG, Scherer PE, Lisanti MP, Mol Endocrinol 2000 14 1750 1775 10.1210/me.14.11.1750 11075810
26. The essential role of Saccharomyces cerevisiae CDC6 nucleotide-binding site in cell growth, DNA synthesis, and Orc1 association. Wang B, Feng L, Hu Y, Huang SH, Reynolds CP, Wu L, Jong AY, J Biol Chem 1999 274 8291 8298 10.1074/jbc.274.12.8291 10075735 (Pubitemid 29144308)
27. Phosphorylated caveolin-1 regulates Rho/ROCK-dependent focal adhesion dynamics and tumor cell migration and invasion. Joshi B, Strugnell SS, Goetz JG, Kojic LD, Cox ME, Griffith OL, Chan SK, Jones SJ, Leung SP, Masoudi H, Leung S, Wiseman SM, Nabi IR, Cancer Res 2008 68 8210 8220 10.1158/0008-5472.CAN-08-0343 18922892
28. Progestin-induced caveolin-1 expression mediates breast cancer cell proliferation. Salatino M, Beguelin W, Peters MG, Carnevale R, Proietti CJ, Galigniana MD, Vedoy CG, Schillaci R, Charreau EH, Sogayar MC, Elizalde PV, Oncogene 2006 25 7723 7739 10.1038/sj.onc.1209757 16799639 (Pubitemid 44967967)
29. The caveolin proteins. Williams TM, Lisanti MP, Genome Biol 2004 5 214 10.1186/gb-2004-5-3-214 15003112 (Pubitemid 38444510)
30. Caveosomes and endocytosis of lipid rafts. Nichols B, J Cell Sci 2003 116 4707 4714 10.1242/jcs.00840 14600257 (Pubitemid 37541214)
31. Cryptococcal yeast cells invade the central nervous system via transcellular penetration of the blood-brain barrier. Chang YC, Stins MF, McCaffery MJ, Miller GF, Pare DR, Dam T, Paul-Satyaseela M, Kim KS, Kwon-Chung KJ, Infect Immun 2004 72 4985 4995 10.1128/IAI.72.9.4985-4995.2004 15321990 (Pubitemid 39223381)
32. Caveolin interaction with protein kinase C. Isoenzyme-dependent regulation of kinase activity by the caveolin scaffolding domain peptide. Oka N, Yamamoto M, Schwencke C, Kawabe J, Ebina T, Ohno S, Couet J, Lisanti MP, Ishikawa Y, J Biol Chem 1997 272 33416 33421 10.1074/jbc.272.52.33416 9407137 (Pubitemid 28023695)
33. Simian Virus 40 depends on ER protein folding and quality control factors for entry into host cells. Schelhaas M, Malmstrom J, Pelkmans L, Haugstetter J, Ellgaard L, Grunewald K, Helenius A, Cell 2007 131 516 529 10.1016/j.cell.2007. 09.038 17981119 (Pubitemid 350017762)
34. Caveolin-stabilized membrane domains as multifunctional transport and sorting devices in endocytic membrane traffic. Pelkmans L, Burli T, Zerial M, Helenius A, Cell 2004 118 767 780 10.1016/j.cell.2004.09.003 15369675 (Pubitemid 39221735)
35. Filamins: promiscuous organizers of the cytoskeleton. Popowicz GM, Schleicher M, Noegel AA, Holak TA, Trends Biochem Sci 2006 31 411 419 10.1016/j.tibs.2006.05.006 16781869 (Pubitemid 44038918)
36. Identification of filamin as a novel ligand for caveolin-1: evidence for the organization of caveolin-1-associated membrane domains by the actin cytoskeleton. Stahlhut M, van Deurs B, Mol Biol Cell 2000 11 325 337 10637311 (Pubitemid 30075526)