HIV-1 gp41 ectodomain enhances Cryptococcus neoformans binding to human brain microvascular endothelial cells via gp41 core-induced membrane activities

Biochemical Journal

Volumn 438, Issue 3, 2011, Pages 457-466

  Huang, Sheng He ^a   Wu, Chu Hua ^a   Jiang, Shibo ^b   Bahner, Ingrid ^c   Lossinsky, Albert S ^d   Jong, Ambrose Y ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b FUDAN UNIVERSITY   (China)

^c UNIVERSITY OF SOUTH FLORIDA   (United States)

^d NEW YORK STATE INSTITUTE FOR BASIC RESEARCH IN DEVELOPMENTAL DISABILITIES   (United States)

Author keywords

Blood brain barrier; Brain microvascular endothelial cell; Cryptococcus neoformans; HIV 1 gp41; Membrane ruffling

Indexed keywords

BETA ACTIN; CORE PROTEIN; GLYCOPROTEIN GP 41; GLYCOPROTEIN GP 41 I90; HERMES ANTIGEN; INTERCELLULAR ADHESION MOLECULE 1; PEPTIDE; PROTEIN KINASE C ALPHA; UNCLASSIFIED DRUG;

ARTICLE; BINDING KINETICS; BLOOD BRAIN BARRIER; BRAIN TISSUE; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; CYTOPATHOLOGY; ECTODOMAIN; ENZYME PHOSPHORYLATION; HUMAN; HUMAN BRAIN MICROVASCULAR ENDOTHELIAL CELL; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; IMMUNOFLUORESCENCE MICROSCOPY; LIPID RAFT; MEMBRANE BIOLOGY; MEMBRANE RUFFLING; MICROVASCULAR ENDOTHELIAL CELL; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SCANNING TRANSMISSION ELECTRON MICROSCOPY; SYNCYTIUM; UPREGULATION;

ACTINS; BINDING SITES; BRAIN; CELL MEMBRANE; CELLS, CULTURED; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; HIV ENVELOPE PROTEIN GP41; HIV-1; HUMANS; INTERCELLULAR ADHESION MOLECULE-1; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, FLUORESCENCE; MUTATION; PROTEIN KINASE C-ALPHA;

FILOBASIDIELLA NEOFORMANS; FUNGI; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 80052150017     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20110218     Document Type: Article

References (56)

1. Mitchell, T. G. and Perfect, J. R. (1995) Cryptococcosis in the era of AIDS: 100 years after the discovery of Cryptococcus neoformans. Clin. Microbiol. Rev. 8, 515-548
2. Oursler, K. A., Moore, R. D. and Chaisson, R. E. (1999) Risk factors for cryptococcal meningitis in HIV-infected patients. AIDS Res. Hum. Retroviruses 15, 625-631
3. Powderly, W. G. (1993) Cryptococcal meningitis and AIDS. Clin. Infect. Dis. 17, 842
4. Eckert, D. M. and Kim, P. S. (2001) Mechanisms of viral membrane fusion and its inhibition. Annu. Rev. Biochem. 70, 777-810
5. Moore, J. P. and Doms, R. W. (2003) The entry of entry inhibitors: a fusion of science and medicine. Proc. Natl. Acad. Sci. U.S.A. 100, 10598-10602
6. Lu, M., Blacklow, S. C. and Kim, P. S. (1995) A trimeric structural domain of the HIV-1 transmembrane glycoprotein. Nat. Struct. Biol. 2, 1075-1082
7. Pan, C., Liu, S. and Jiang, S. (2010) HIV-1 gp41 fusion intermediate: a target for HIV therapeutics. J. Formos Med. Assoc. 109, 94-105
8. Cai, L. and Jiang, S. (2010) Development of peptide and small-molecule HIV-1 fusion inhibitors that target gp41. ChemMedChem 5, 1813-1824
9. Qi, Z., Pan, C., Lu, H., Shui, Y., Li, L., Li, X., Xu, X., Liu, S. and Jiang, S. (2010) A recombinant mimetics of the HIV-1 gp41 prehairpin fusion intermediate fused with human IgG Fc fragment elicits neutralizing antibody response in the vaccinated mice. Biochem. Biophys. Res. Commun. 398, 506-512
10. Chan, D. C., Fass, D., Berger, J. M. and Kim, P. S. (1997) Core structure of gp41 from the HIV envelope glycoprotein. Cell 89, 263-273 (Pubitemid 27199898)
11. Weissenhorn, W., Dessen, A., Harrison, S. C., Skehel, J. J. and Wiley, D. C. (1997) Atomic structure of the ectodomain from HIV-1 gp41. Nature 387, 426-428
12. Tan, K., Liu, J., Wang, J., Shen, S. and Liu, M. (1997) Atomic structure of a thermostable subdomain of HIV-1 gp41. Proc. Natl. Acad. Sci. U.S.A. 94, 12303-12308
13. Chan, D. C. and Kim, P. S. (1998) HIV entry and its inhibition. Cell 93, 681-684 (Pubitemid 28257575)
14. Jiang, S., Lin, K., Strick, N. and Neurath, A. R. (1993) HIV-1 inhibition by a peptide. Nature 365, 113
15. Wild, C. T., Shugars, D. C., Greenwell, T. K., McDanal, C. B. and Matthews, T. J. (1994) Peptides corresponding to a predictive α-helical domain of human immunodeficiency virus type 1 gp41 are potent inhibitors of virus infection. Proc. Natl. Acad. Sci. U.S.A. 91, 9770-9774
16. Lu, M. and Kim, P.S (1997) A trimeric structural subdomain of the HIV-1 transmembrane glycoprotein. J. Biomol. Struct. Dyn. 15, 465-471
17. Lalezari, J. P., Henry, K., O'Hearn, M., Montaner, J. S., Piliero, P. J., Trottier, B., Walmsley, S., Cohen, C., Kuritzkes, D. R., Eron, Jr, J. J. et al. (2003) Enfuvirtide, an HIV-1 fusion inhibitor, for drug-resistant HIV infection in north and south America. N. Engl. J. Med. 348, 2175-2185
18. Shu, W., Ji, H. and Lu, M. (2000) Interactions between HIV-1 gp41 core and detergents and their implications for membrane fusion. J. Biol. Chem. 275, 1839-1845
19. Markosyan, R. M., Cohen, F. S. and Melikyan, G. B. (2003) HIV-1 envelope proteins complete their folding into six-helix bundles immediately after fusion pore formation. Mol. Biol. Cell 14, 926-938
20. Shnaper, S., Sackett, K., Gallo, S. A., Blumenthal, R. and Shai, Y. (2004) The C- and the N-terminal regions of glycoprotein 41 ectodomain fuse membranes enriched and not enriched with cholesterol, respectively. J. Biol. Chem. 279, 18526-18534
21. Tan, K., Liu, J., Wang, J., Shen, S. and Lu, M. (1997) Atomic structure of a thermostable subdomain of HIV-1 gp41. Proc. Natl. Acad. Sci. U.S.A. 94, 12303-12308
22. Korazim, O., Sackett, K. and Shai, Y. (2006) Functional and structural characterization of HIV-1 gp41 ectodomain regions in phospholipid membranes suggests that the fusion-active conformation is extended. J. Mol. Biol. 364, 1103-1117
23. Lev, N., Fridmann-Sirkis, Y., Blank, L., Bitler, A., Epand, R. F., Epand, R. M. and Shai, Y. (2009) Conformational stability and membrane interaction of the full-length ectodomain of HIV-1 gp41: implication for mode of action. Biochemistry 48, 3166-3175
24. Huang, J. H., Qi, Z., Wu, F., Kotula, L., Jiang, S. and Chen, Y. H. (2008) Interaction of HIV-1 gp41 core with NPF motif in Epsin: implication in endocytosis of HIV. J. Biol. Chem. 283, 14994-15002
25. Huang, J. H., Lu, L., Lu, H., Chen, X., Jiang, S. and Chen, Y. H. (2007) Identification of the HIV-1 gp41 core-binding motif in the scaffolding domain of caveolin-1. J. Biol. Chem. 282, 6143-6152
26. Chen, Y. H., Bock, G., Vornhagen, R., Steindl, F., Katinger, H. and Dierich, M. P. (1994) HIV-1 gp41 enhances major histocompatibility complex class I and ICAM-1 expression on H9 and U937 cells. Int. Arch. Allergy Immunol. 104, 227-231
27. Zhu, Y., Lu, L., Xu, L., Yang, H., Jiang, S. and Chen, Y. H. (2010) Identification of a gp41 core-binding molecule with homologous sequence of human TNNI3K like protein as a novel human immunodeficiency viruses type 1 entry inhibitor. J. Virol. 84, 9359-9368
28. Le, Y., Jiang, S., Hu, J., Gong, W., Su, S., Dunlop, N. M., Shen, W., Li, B. and Ming, W. J. (2000) N36, a synthetic N-terminal heptad repeat domain of the HIV-1 envelope protein gp41, is an activator of human phagocytes. Clin. Immunol. 96, 236-242
29. Langford, D. and Masliah, E. (2001) Crosstalk between components of the blood brain barrier and cells of the CNS in microglial activation in AIDS. Brain Pathol. 11, 306-312 (Pubitemid 32494573)
30. Moses, A. V. and Nelson, J. A. (1994) HIV infection of human brain capillary endothelial cells: implications for AIDS dementia. Adv. Neuroimmunol. 4, 239-247
31. An, S. F., Groves, M., Gray, F. and Scaravilli, F. (1999) Early entry and widespread cellular involvement of HIV-1 DNA in brains of HIV-1 positive asymptomatic individuals. J. Neuropathol. Exp. Neurol. 58, 1156-1162
32. Resnick, L., Berger, J. R., Shapshak, P. and Tourtellotte, W. W. (1988) Early penetration of the blood-brain-barrier by HIV. Neurology 38, 9-14
33. Liu, N. Q., Lossinsky, A. S., Popik, W., Li, X., Gujuluva, C., Kriederman, B., Roberts, J., Pushkarsky, T., Bukrinsky, M., Witte, M. et al. (2002) Human immunodeficiency virus type 1 enters brain microvascular endothelia by macropinocytosis dependent on lipid rafts and the mitogen-activated protein kinase signaling pathway. J. Virol. 76, 6689-6700 (Pubitemid 34633535)
34. Chen, H. M., Stins, S. F., Huang, H. S., Chen, Y. H., Kwon-Chung, K. J., Chang, Y. C. and Kim, K. S. (2003) Crytptococcus neoformans induces alterations in cytoskeleton of human rain microvascular endothelial cells. J. Med. Microbiol. 52, 961-970
35. Jong, A. Y., Wu, C. H., Jiang, S., Feng, L., Chen, H. M. and Huang, S. H. (2007) HIV-1 gp41 ectodomain enhances Cryptococcus neoformans binding to HBMEC. Biochem. Biophys. Res. Commun. 356, 899-905
36. Chang, Y. C., Penoyer, L. A. and Kwon-Chung, K. J. (1996) The second capsule gene of Cryptococcus neoformans, CAP64, is essential for virulence. Infect. Immun. 64, 1977-1983
37. Chang, Y. C. and Kwon-Chung, K. J. (1998) Isolation of the third capsule-associated gene, CAP60, required for virulence in Cryptococcus neoformans. Infect. Immun. 66, 2230-2236
38. Chang, Y. C. and Kwon-Chung, K. J. (1999) Isolation, characterization, and localization of a capsule-associated gene, CAP10, of Cryptococcus neoformans. J. Bacteriol. 181, 5636-5643 (Pubitemid 29437133)
39. Huang, S. H. and Jong, A. Y. (2001) Cellular mechanisms of microbial proteins contributing to invasion of the blood-brain barrier. Cell. Microbiol. 3, 277-287
40. Jong, A. Y., Stins, M. F., Huang, S. H., Chen, S. H. and Kim, K. S. (2001) Traversal of Candida albicans across human blood-brain barrier in vitro. Infect. Immun. 69, 4536-4544
41. Jong, A. Y., Chen, S. H., Stins, M. F. and Kim, K. (2003) Binding of Candida albicans enolase to human plasmin(ogen) results in enhanced invasion of brain microvascular endothelial cells. J. Med. Microbiol. 52, 622
42. Stins, M. F., Prasadarao, N. V., Zhou, J., Arditi, M. and Kim, K. S. (1997) Bovine brain microvascular endothelial cells transfected with SV40-large T antigen: development of an immortalized cell line to study pathophysiology of CNS disease. In Vitro Cell. Dev. Biol. Anim. 33, 243-247
43. Nizet, V., Kim, K. S., Stins, M., Jonas, M., Chi, E. Y., Nguyen, D. and Rubens, C. E. (1997) Invasion of brain microvascular endothelial cells by group B streptococci. Infect. Immun. 65, 5074-5081
44. Lossinsky, A. S. and Shivers, R. R. (2003) Studies of cerebral endothelium by scanning and high-voltage electron microscopy. Methods Mol. Med. 89, 67-82
45. Lossinsky, A. S., Buttle, K. F., Pluta, R., Mossakowski, M. J. and Wisniewski, H. M. (1999) Immunoultrastructural expression of intercellular adhesion molecule-1 in endothelial cell vesiculotubular structures and vesiculovacuolar organelles in blood-brain barrier development and injury. Cell Tissue Res. 295, 77-88
46. York, J. and Nunberg, J. H. (2004) Role of hydrophobic residues in the central ectodomain of gp41 in maintaining the association between human immunodeficiency virus type 1 envelope glycoprotein subunits gp120 and gp41. J. Virol. 78, 4921-4926
47. Jong, A., Wu, C. H., Prasadarao, N. V., Kwon-Chung, K. J., Chang, Y. C., Ouyang, Y., Shackleford, G. M. and Huang, S. H. (2008) Invasion of Cryptococcus neoformans into human brain microvascular endothelial cells requires protein kinase C-α activation. Cell. Microbiol. 10, 1854-1865
48. Jacobs, A., Sen, J., Rong, L. and Caffrey, M. (2005) Alanine scanning mutants of the HIV gp41 loop. J. Biol. Chem. 280, 27284-27288
49. Lu, M., Stoller, M. O., Wang, S., Liu, J., Fagan, M. B. and Nunberg, J. H. (2001) Structural and functional analysis of interhelical interactions in the human immunodeficiency virus type 1 gp41 envelope glycoprotein by alanine-scanning mutagenesis. J. Virol. 75, 11146-11156
50. Follis, K. E., Larson, S. J., Lu, M. and Nunberg, J. H. (2002) Genetic evidence that interhelical packing interactions in the gp41 core are critical for transition of the human immunodeficiency virus type 1 envelope glycoprotein to the fusion-active state. J. Virol. 76, 7356-7362
51. Gallaher, W. R., Ball, J. M., Garry, R. F., Martin-Amedee, A. M. and Montelaro, R. C. (1995) A general model for the surface glycoproteins of HIV and other retroviruses. AIDS Res. Hum. Retroviruses 11, 191-202
52. Cao, J., Bergeron, L., Helseth, E., Thali, M., Repke, H. and Sodroski, J. (1993) Effects of amino acid changes in the extracellular domain of the human immunodeficiency virus type 1 gp41 envelope glycoprotein. J. Virol. 67, 2747-2755 (Pubitemid 23118873)
53. Wang, S., York, J., Shu, W., Stoller, M. O., Nunberg, J. H. and Lu, M. (2002) Interhelical interactions in the gp41 core: implications for activation of HIV-1 membrane fusion. Biochemistry 41, 7283-7292 (Pubitemid 34602444)
54. Ha-Lee, Y. M., Lee, Y., Kim, Y. K. and Sohn, J. (2000) Cross-linking of CD4 induces cytoskeletal association of CD4 and p56lck. Exp. Mol. Med. 32, 18-22
55. Iyengar, S., Hildreth, J. E. and Schwartz, D. H. (1998) Actin-dependent receptor colocalization required for human immunodeficiency virus entry into host cells. J. Virol. 72, 5251-5255
56. Koyanagi, Y., Miles, S., Mitsuyasu, R. T., Merrill, J. E., Vinters, H. V. and Chen, I. S. (1987) Dual infection of the central nervous system by AIDS viruses with distinct cellular tropisms. Science 236, 819-822