Conserved arginine residue in the membrane-spanning domain of HIV-1 gp41 is required for efficient membrane fusion

Protein and Cell

Volumn 2, Issue 5, 2011, Pages 369-376

  Long, Yufei ^a,b   Meng, Fanxia ^a   Kondo, Naoyuki ^a,c   Iwamoto, Aikichi ^d   Matsuda, Zene ^a,d  

^a INSTITUTE OF BIOPHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF TOKYO   (Japan)

Author keywords

arginine; gp41; human immunodeficiency virus; membrane fusion; membrane spanning domain (MSD); type 1 (HIV 1)

Indexed keywords

ALANINE; ARGININE; ASPARAGINE; ASPARTIC ACID; GLUTAMIC ACID; GLUTAMINE; GLYCOPROTEIN GP 41; HUMAN IMMUNODEFICIENCY VIRUS PROTEIN; ISOLEUCINE; LEUCINE; LYSINE; MUTANT PROTEIN; VIRUS ENVELOPE PROTEIN;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; ASSAY; CELL BASED DUAL SPLIT PROTEIN ASSAY; CELL FUSION; CONSENSUS SEQUENCE; CONTROLLED STUDY; MEMBRANE FUSION; MEMBRANE SPANNING DOMAIN; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROCESSING; SYNCYTIA FORMATION ASSAY; SYNCYTIUM;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 80053064868     PISSN: 1674800X     EISSN: 16748018     Source Type: Journal    
DOI: 10.1007/s13238-011-1051-0     Document Type: Article

References (33)

1. Bonifacino, J. S., Cosson, P., Shah, N., and Klausner, R. D. (1991). Role of potentially charged transmembrane residues in targeting proteins for retention and degradation within the endoplasmic reticulum. EMBO J 10, 2783-2793.
2. Ciczora, Y., Callens, N., Montpellier, C., Bartosch, B., Cosset, F. L., Op de Beeck, A., and Dubuisson, J. (2005). Contribution of the charged residues of hepatitis C virus glycoprotein E2 transmembrane domain to the functions of the E1E2 heterodimer. J Gen Virol 86, 2793-2798.
3. Colman, P. M., and Lawrence, M. C. (2003). The structural biology of type I viral membrane fusion. Nat Rev Mol Cell Biol 4, 309-319.
4. Davis, G. L., and Hunter, E. (1987). A charged amino acid substitution within the transmembrane anchor of the Rous sarcoma virus envelope glycoprotein affects surface expression but not intracellular transport. J Cell Biol 105, 1191-1203.
5. Dubay, J. W., Dubay, S. R., Shin, H. J., and Hunter, E. (1995). Analysis of the cleavage site of the human immunodeficiency virus type 1 glycoprotein: requirement of precursor cleavage for glycoprotein incorporation. J Virol 69, 4675-4682.
6. Freed, E. O., and Martin, M. A. (1996). Domains of the human immunodeficiency virus type 1 matrix and gp41 cytoplasmic tail required for envelope incorporation into virions. J Virol 70, 341-351.
7. Gangupomu, V. K., and Abrams, C. F. (2010). All-atom models of the membrane-spanning domain of HIV-1 gp41 from metadynamics. Biophys J 99, 3438-3444.
8. Gu, M., Rappaport, J., and Leppla, S. H. (1995). Furin is important but not essential for the proteolytic maturation of gp160 of HIV-1. FEBS Lett 365, 95-97.
9. Haffar, O. K., Dowbenko, D. J., and Berman, P. W. (1988). Topogenic analysis of the human immunodeficiency virus type 1 envelope glycoprotein, gp160, in microsomal membranes. J Cell Biol 107, 1677-1687.
10. Helseth, E., Olshevsky, U., Gabuzda, D., Ardman, B., Haseltine, W., and Sodroski, J. (1990). Changes in the transmembrane region of the human immunodeficiency virus type 1 gp41 envelope glycoprotein affect membrane fusion. J Virol 64, 6314-6318.
11. Hessa, T., Kim, H., Bihlmaier, K., Lundin, C., Boekel, J., Andersson, H., Nilsson, I., White, S. H., and von Heijne, G. (2005). Recognition of transmembrane helices by the endoplasmic reticulum translocon. Nature 433, 377-381.
12. Kabat, D., Kozak, S. L., Wehrly, K., and Chesebro, B. (1994). Differences in CD4 dependence for infectivity of laboratoryadapted and primary patient isolates of human immunodeficiency virus type 1. J Virol 68, 2570-2577.
13. Kim, J. H., Hartley, T. L., Curran, A. R., and Engelman, D. M. (2009). Molecular dynamics studies of the transmembrane domain of gp41 from HIV-1. Biochim Biophys Acta 1788, 1804-1812.
14. Kitchen, S. G., and Zack, J. A. (1997). CXCR4 expression during lymphopoiesis: implications for human immunodeficiency virus type 1 infection of the thymus. J Virol 71, 6928-6934.
15. Kondo, N., Miyauchi, K., and Matsuda, Z. (2011). Monitoring viralmediated membrane fusion using fluorescent reporter methods. Curr Protoc Cell Biol Chapter 26, Unit 26. 9.
16. Kondo, N., Miyauchi, K., Meng, F., Iwamoto, A., and Matsuda, Z. (2010). Conformational changes of the HIV-1 envelope protein during membrane fusion are inhibited by the replacement of its membrane-spanning domain. J Biol Chem 285, 14681-14688.
17. Li, L., Vorobyov, I., MacKerell, A. D. Jr, and Allen, T. W. (2008). Is arginine charged in a membrane? Biophys J 94, L11-L13.
18. Liu, S., Kondo, N., Long, Y., Xiao, D., Iwamoto, A., and Matsuda, Z. (2010). Membrane topology analysis of HIV-1 envelope glycoprotein gp41. Retrovirology 7, 100.
19. Melikyan, G. B. (2008). Common principles and intermediates of viral protein-mediated fusion: the HIV-1 paradigm. Retrovirology 5, 111.
20. Miyauchi, K., Curran, A. R., Long, Y., Kondo, N., Iwamoto, A., Engelman, D. M., and Matsuda, Z. (2010). The membranespanning domain of gp41 plays a critical role in intracellular trafficking of the HIV envelope protein. Retrovirology 7, 95.
21. Miyauchi, K., Komano, J., Yokomaku, Y., Sugiura, W., Yamamoto, N., and Matsuda, Z. (2005). Role of the specific amino acid sequence of the membrane-spanning domain of human immunodeficiency virus type 1 in membrane fusion. J Virol 79, 4720-4729.
22. Morton, H. C., van den Herik-Oudijk, I. E., Vossebeld, P., Snijders, A., Verhoeven, A. J., Capel, P. J., and van de Winkel, J. G. (1995). Functional association between the human myeloid immunoglobulin A Fc receptor (CD89) and FcR gamma chain. Molecular basis for CD89/FcR gamma chain association. J Biol Chem 270, 29781-29787.
23. Owens, R. J., Burke, C., and Rose, J. K. (1994). Mutations in the membrane-spanning domain of the human immunodeficiency virus envelope glycoprotein that affect fusion activity. J Virol 68, 570-574.
24. Pietschmann, T., Zentgraf, H., Rethwilm, A., and Lindemann, D. (2000). An evolutionarily conserved positively charged amino acid in the putative membrane-spanning domain of the foamy virus envelope protein controls fusion activity. J Virol 74, 4474-4482.
25. Reeves, J. D., Gallo, S. A., Ahmad, N., Miamidian, J. L., Harvey, P. E., Sharron, M., Pohlmann, S., Sfakianos, J. N., Derdeyn, C. A., Blumenthal, R., et al. (2002). Sensitivity of HIV-1 to entry inhibitors correlates with envelope/coreceptor affinity, receptor density, and fusion kinetics. Proc Natl Acad Sci U S A 99, 16249-16254.
26. Rowell, J. F., Stanhope, P. E., and Siliciano, R. F. (1995). Endocytosis of endogenously synthesized HIV-1 envelope protein. Mechanism and role in processing for association with class II MHC. J Immunol 155, 473-488.
27. Shang, L., and Hunter, E. (2010). Residues in the membranespanning domain core modulate conformation and fusogenicity of the HIV-1 envelope glycoprotein. Virology 404, 158-167.
28. Shang, L., Yue, L., and Hunter, E. (2008). Role of the membranespanning domain of human immunodeficiency virus type 1 envelope glycoprotein in cell-cell fusion and virus infection. J Virol 82, 5417-5428.
29. Weiss, C. D. (2003). HIV-1 gp41: mediator of fusion and target for inhibition. AIDS Rev 5, 214-221.
30. Welman, M., Lemay, G., and Cohen, E. A. (2007). Role of envelope processing and gp41 membrane spanning domain in the formation of human immunodeficiency virus type 1 (HIV-1) fusion-competent envelope glycoprotein complex. Virus Res 124, 103-112.
31. Wilk, T., Pfeiffer, T., Bukovsky, A., Moldenhauer, G., and Bosch, V. (1996). Glycoprotein incorporation and HIV-1 infectivity despite exchange of the gp160 membrane-spanning domain. Virology 218, 269-274.
32. Wyss, S., Dimitrov, A. S., Baribaud, F., Edwards, T. G., Blumenthal, R., and Hoxie, J. A. (2005). Regulation of human immunodeficiency virus type 1 envelope glycoprotein fusion by a membraneinteractive domain in the gp41 cytoplasmic tail. J Virol 79, 12231-12241.
33. Yang, C., Spies, C. P., and Compans, R. W. (1995). The human and simian immunodeficiency virus envelope glycoprotein transmembrane subunits are palmitoylated. Proc Natl Acad Sci U S A 92, 9871-9875.