Early and late HIV-1 membrane fusion events are impaired by sphinganine lipidated peptides that target the fusion site

Biochemical Journal

Volumn 461, Issue 2, 2014, Pages 213-222

  Klug, Yoel A ^a   Ashkenazi, Avraham ^a,d   Viard, Mathias ^b,c   Porat, Ziv ^a   Blumenthal, Robert ^b   Shai, Yechiel ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b NATIONAL CANCER INSTITUTE   (United States)

^c FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Biophysics; HIV; HIV entry inhibitor; Membrane fusion; Membrane protein; Protein folding

Indexed keywords

CD4 ANTIGEN; DIHYDROSPHINGOMYELIN; HYBRID PROTEIN; LIPOPEPTIDE; SPHINGANINE; UNCLASSIFIED DRUG;

ANTIVIRAL ACTIVITY; ARTICLE; BINDING SITE; CELL CONTACT; CELL MEMBRANE; CONJUGATION; CONTROLLED STUDY; DIFFUSION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; MEMBRANE FUSION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN SECONDARY STRUCTURE;

ANTIGENS, CD4; GENE EXPRESSION; GENES, REPORTER; HELA CELLS; HIV ENVELOPE PROTEIN GP120; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; LUCIFERASES; MEMBRANE FUSION; PEPTIDES; PROTEIN FOLDING; SPHINGOSINE; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; TRANSGENES; VIRUS INTERNALIZATION;

EID: 84903265715     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20140189     Document Type: Article

References (46)

1. Rawat, S. S., Viard, M., Gallo, S. A., Blumenthal, R. and Puri, A. (2006) Sphingolipids, cholesterol, and HIV-1: a paradigm in viral fusion. Glycoconj. J. 23, 189-197 CrossRef PubMed (Pubitemid 43725198)
2. Liao, Z., Cimakasky, L. M., Hampton, R., Nguyen, D. H. and Hildreth, J. E. (2001) Lipid rafts and HIV pathogenesis: host membrane cholesterol is required for infection by HIV type 1. AIDS Res. Hum. Retroviruses 17, 1009-1019 CrossRef PubMed (Pubitemid 32881320)
3. Simons, K. and Ikonen, E. (1997) Functional rafts in cell membranes. Nature 387, 569-572 CrossRef PubMed (Pubitemid 27248754)
4. Nguyen, D. H. and Hildreth, J. E. (2000) Evidence for budding of human immunodeficiency virus type 1 selectively from glycolipid-enriched membrane lipid rafts. J. Virol. 74, 3264-3272 CrossRef PubMed (Pubitemid 30143751)
5. Ono, A. and Freed, E. O. (2001) Plasma membrane rafts play a critical role in HIV-1 assembly and release. Proc. Natl. Acad. Sci. U.S.A. 98, 13925-13930 CrossRef PubMed (Pubitemid 33116000)
6. Viard, M., Parolini, I., Sargiacomo, M., Fecchi, K., Ramoni, C., Ablan, S., Ruscetti, F. W., Wang, J. M. and Blumenthal, R. (2002) Role of cholesterol in human immunodeficiency virus type 1 envelope protein-mediated fusion with host cells. J. Virol. 76, 11584-11595 CrossRef PubMed (Pubitemid 35231314)
7. Simons, K. and Warren, G. (1984) Semliki Forest virus: a probe for membrane traffic in the animal cell. Adv. Protein Chem. 36, 79-132 CrossRef PubMed
8. Simons, K. and Garoff, H. (1980) The budding mechanisms of enveloped animal viruses. J. Gen. Virol. 50, 1-21 CrossRef PubMed
9. Kielian, M. and Helenius, A. (1986) In The Togaviridae and Flaviviridae (Schlesinger, S. and Schlesinger, M. J., eds), pp. 91-119, Springer, New York CrossRef
10. White, J. M. (1990) Viral and cellular membrane fusion proteins. Annu. Rev. Physiol. 52, 675-697 CrossRef PubMed
11. Blumenthal, R., Clague, M. J., Durell, S. R. and Epand, R. M. (2003) Membrane fusion. Chem. Rev. 103, 53-69 CrossRef PubMed
12. Finzi, A., Xiang, S. H., Pacheco, B., Wang, L., Haight, J., Kassa, A., Danek, B., Pancera, M., Kwong, P. D. and Sodroski, J. (2010) Topological layers in the HIV-1 gp120 inner domain regulate gp41 interaction and CD4-triggered conformational transitions. Mol. Cell 37, 656-667 CrossRef PubMed
13. Buzon, V., Natrajan, G., Schibli, D., Campelo, F., Kozlov, M. M. and Weissenhorn, W. (2010) Crystal structure of HIV-1 gp41 including both fusion peptide and membrane proximal external regions. PLoS Pathog. 6, e1000880 CrossRef PubMed
14. Gallo, S. A., Finnegan, C. M., Viard, M., Raviv, Y., Dimitrov, A., Rawat, S. S., Puri, A., Durell, S. and Blumenthal, R. (2003) The HIV Env-mediated fusion reaction. Biochim. Biophys. Acta 1614, 36-50 CrossRef PubMed (Pubitemid 36857094)
15. Melikyan, G. B., Markosyan, R. M., Hemmati, H., Delmedico, M. K., Lambert, D. M. and Cohen, F. S. (2000) Evidence that the transition of HIV-1 gp41 into a six-helix bundle, not the bundle configuration, induces membrane fusion. J. Cell Biol. 151, 413-423 CrossRef PubMed
16. Chan, D. C., Chutkowski, C. T. and Kim, P. S. (1998) Evidence that a prominent cavity in the coiled coil of HIV type 1 gp41 is an attractive drug target. Proc. Natl. Acad. Sci. U.S.A. 95, 15613-15617 CrossRef PubMed (Pubitemid 29018748)
17. Furuta, R. A., Wild, C. T., Weng, Y. and Weiss, C. D. (1998) Capture of an early fusion-active conformation of HIV-1 gp41. Nat. Struct. Biol. 5, 276-279 CrossRef PubMed (Pubitemid 28164878)
18. Munoz-Barroso, I., Durell, S., Sakaguchi, K., Appella, E. and Blumenthal, R. (1998) Dilation of the human immunodeficiency virus-1 envelope glycoprotein fusion pore revealed by the inhibitory action of a synthetic peptide from gp41. J. Cell Biol. 140, 315-323 CrossRef PubMed (Pubitemid 28078395)
19. Wexler-Cohen, Y. and Shai, Y. (2009) Membrane-anchored HIV-1 N-heptad repeat peptides are highly potent cell fusion inhibitors via an altered mode of action. PLoS Pathog. 5, e1000509 CrossRef PubMed
20. Liu, S., Lu, H., Niu, J., Xu, Y., Wu, S. and Jiang, S. (2005) Different from the HIV fusion inhibitor C34, the anti-HIV drug Fuzeon (T-20) inhibits HIV-1 entry by targeting multiple sites in gp41 and gp120. J. Biol. Chem. 280, 11259-11273 CrossRef PubMed (Pubitemid 40418432)
21. Brugger, B., Glass, B., Haberkant, P., Leibrecht, I., Wieland, F. T. and Krausslich, H. G. (2006) The HIV lipidome: a raft with an unusual composition. Proc. Natl. Acad. Sci. U.S.A. 103, 2641-2646 CrossRef PubMed
22. Epand, R. M. (2003) Cholesterol in bilayers of sphingomyelin or dihydrosphingomyelin at concentrations found in ocular lens membranes. Biophys. J. 84, 3102-3110 CrossRef PubMed
23. Goni, F. M. and Alonso, A. (2006) Biophysics of sphingolipids I. Membrane properties of sphingosine, ceramides and other simple sphingolipids. Biochim. Biophys. Acta 1758, 1902-1921 CrossRef PubMed (Pubitemid 44879372)
24. Kuikka, M., Ramstedt, B., Ohvo-Rekila, H., Tuuf, J. and Slotte, J. P. (2001) Membrane properties of D-erythro-N-acyl sphingomyelins and their corresponding dihydro species. Biophys. J. 80, 2327-2337 CrossRef PubMed (Pubitemid 32401996)
25. Ashkenazi, A., Viard, M., Unger, L., Blumenthal, R. and Shai, Y. (2012) Sphingopeptides: dihydrosphingosine-based fusion inhibitors against wild-type and enfuvirtide-resistant HIV-1. FASEB J. 26, 4628-4636 CrossRef PubMed
26. Merrifield, R. B., Vizioli, L. D. and Boman, H. G. (1982) Synthesis of the antibacterial peptide cecropin A (1-33). Biochemistry 21, 5020-5031 CrossRef PubMed (Pubitemid 13203097)
27. Wexler-Cohen, Y., Ashkenazi, A., Viard, M., Blumenthal, R. and Shai, Y. (2010) Virus-cell and cell-cell fusion mediated by the HIV-1 envelope glycoprotein is inhibited by short gp41 N-terminal membrane-anchored peptides lacking the critical pocket domain. FASEB J. 24, 4196-4202 CrossRef PubMed
28. George, T. C., Fanning, S. L., Fitzgerald-Bocarsly, P., Medeiros, R. B., Highfill, S., Shimizu, Y., Hall, B. E., Frost, K., Basiji, D., Ortyn, W. E. et al. (2006) Quantitative measurement of nuclear translocation events using similarity analysis of multispectral cellular images obtained in flow. J. Immunol. Methods 311, 117-129 CrossRef PubMed
29. Finnegan, C. M., Rawat, S. S., Cho, E. H., Guiffre, D. L., Lockett, S., Merrill, Jr, A. H. and Blumenthal, R. (2007) Sphingomyelinase restricts the lateral diffusion of CD4 and inhibits human immunodeficiency virus fusion. J. Virol. 81, 5294-5304 CrossRef PubMed (Pubitemid 46744438)
30. Popik, W. and Alce, T. M. (2004) CD4 receptor localized to non-raft membrane microdomains supports HIV-1 entry. Identification of a novel raft localization marker in CD4. J. Biol. Chem. 279, 704-712 CrossRef PubMed (Pubitemid 38044875)
31. Lippincott-Schwartz, J., Presley, J. F., Zaal, K. J., Hirschberg, K., Miller, C. D. and Ellenberg, J. (1999) Monitoring the dynamics and mobility of membrane proteins tagged with green fluorescent protein. Methods Cell Biol. 58, 261-281 CrossRef PubMed
32. McAuliffe, M. J., Lalonde, F. M., McGarry, D., Gandler, W., Csaky, K. and Trus, B. L. (2005) Medical image processing, analysis and visualization in clinical research. In Proceeding CBMS '01 Proceedings of the Fourteenth IEEE Symposium on Computer-Based Medical Systems, pp. 381, IEEE Computer Society, Washington
33. Rajendran, L., Schneider, A., Schlechtingen, G., Weidlich, S., Ries, J., Braxmeier, T., Schwille, P., Schulz, J. B., Schroeder, C., Simons, M. et al. (2008) Efficient inhibition of the Alzheimer's disease β-secretase by membrane targeting. Science 320, 520-523 CrossRef PubMed (Pubitemid 351590663)
34. Ingallinella, P., Bianchi, E., Ladwa, N. A., Wang, Y. J., Hrin, R., Veneziano, M., Bonelli, F., Ketas, T. J., Moore, J. P., Miller, M. D. and Pessi, A. (2009) Addition of a cholesterol group to an HIV-1 peptide fusion inhibitor dramatically increases its antiviral potency. Proc. Natl. Acad. Sci. U.S.A. 106, 5801-5806 CrossRef PubMed
35. Ashkenazi, A., Faingold, O., Kaushansky, N., Ben-Nun, A. and Shai, Y. (2013) A highly conserved sequence associated with the HIV gp41 loop region is an immunomodulator of antigen-specific T cells in mice. Blood 121, 2244-2252 CrossRef PubMed
36. Bolte, S. and Cordelieres, F. P. (2006) A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc. 224, 213-232 CrossRef (Pubitemid 46010930)
37. Gallaher, W. R. (1987) Detection of a fusion peptide sequence in the transmembrane protein of human immunodeficiency virus. Cell 50, 327-328 CrossRef PubMed
38. Hubner, W., McNerney, G. P., Chen, P., Dale, B. M., Gordon, R. E., Chuang, F. Y., Li, X. D., Asmuth, D. M., Huser, T. and Chen, B. K. (2009) Quantitative 3D video microscopy of HIV transfer across T cell virological synapses. Science 323, 1743-1747 CrossRef PubMed
39. McDonald, D., Wu, L., Bohks, S. M., KewalRamani, V. N., Unutmaz, D. and Hope, T. J. (2003) Recruitment of HIV and its receptors to dendritic cell-T cell junctions. Science 300, 1295-1297 CrossRef PubMed (Pubitemid 36618241)
40. Carr, C. M. and Kim, P. S. (1993) A spring-loaded mechanism for the conformational change of influenza hemagglutinin. Cell 73, 823-832 CrossRef PubMed (Pubitemid 23159019)
41. Vieira, C. R., Munoz-Olaya, J. M., Sot, J., Jimenez-Baranda, S., Izquierdo-Useros, N., Abad, J. L., Apellaniz, B., Delgado, R., Martinez-Picado, J., Alonso, A. et al. (2010) Dihydrosphingomyelin impairs HIV-1 infection by rigidifying liquid-ordered membrane domains. Chem. Biol. 17, 766-775 CrossRef PubMed
42. St Vincent, M. R., Colpitts, C. C., Ustinov, A. V., Muqadas, M., Joyce, M. A., Barsby, N. L., Epand, R. F., Epand, R. M., Khramyshev, S. A., Valueva, O. A. et al. (2010) Rigid amphipathic fusion inhibitors, small molecule antiviral compounds against enveloped viruses. Proc. Natl. Acad. Sci. U.S.A. 107, 17339-17344 CrossRef PubMed
43. Wolf, M. C., Freiberg, A. N., Zhang, T., Akyol-Ataman, Z., Grock, A., Hong, P. W., Li, J., Watson, N. F., Fang, A. Q., Aguilar, H. C. et al. (2009) A broad-spectrum antiviral targeting entry of enveloped viruses. Proc. Natl. Acad. Sci. U.S.A. 107, 3157-3162 CrossRef
44. Volmer, R., van der Ploeg, K. and Ron, D. (2012) Membrane lipid saturation activates endoplasmic reticulum unfolded protein response transducers through their transmembrane domains. Proc. Natl. Acad. Sci. U.S.A. 110, 4628-4633 CrossRef
45. Lorizate, M., Sachsenheimer, T., Glass, B., Habermann, A., Gerl, M. J., Krausslich, H. G. and Brugger, B. (2013) Comparative lipidomics analysis of HIV-1 particles and their preducer cell membrane in different cell lines. Cell. Microbiol 15, 292-304 CrossRef PubMed
46. Ernst, A. M. and Brugger, B. (2013) Sphingolipids as modulators of membrane proteins. Biochim. Biophys. Acta 1841, 665-670 CrossRef PubMed