The V4 and V5 variable loops of HIV-1 envelope glycoprotein are tolerant to insertion of green fluorescent protein and are useful targets for labeling

Journal of Biological Chemistry

Volumn 290, Issue 24, 2015, Pages 15279-15291

  Nakane, Shuhei ^a,b   Iwamoto, Aikichi ^a   Matsuda, Zene ^a,b  

^a UNIVERSITY OF TOKYO   (Japan)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES; CYTOLOGY; GLYCOPROTEINS; OLIGOMERS; PROTEINS; VIRUSES;

CELL SURFACE EXPRESSION; ENVELOPE GLYCOPROTEINS; FUNCTIONAL EVALUATION; GREEN FLUORESCENT PROTEIN; HUMAN IMMUNODEFICIENCY VIRUS TYPE-1; INSERTIONAL MUTAGENESIS; STRUCTURAL MODELS; VIRUS-LIKE PARTICLES;

DISEASES;

GREEN FLUORESCENT PROTEIN; HIV 1 ENVELOPE GLYCOPROTEIN; HUMAN IMMUNODEFICIENCY VIRUS PROTEIN; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN; GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 41;

ARTICLE; CELL FUSION; CELL SURFACE; CELL VACUOLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; MOLECULAR IMAGING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN QUATERNARY STRUCTURE; PROTEIN TARGETING; VIRUS CELL INTERACTION; VIRUS LIKE AGENT; AMINO ACID SEQUENCE; CHEMISTRY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; HEK293 CELL LINE; HUMAN IMMUNODEFICIENCY VIRUS; METABOLISM; WESTERN BLOTTING;

HUMAN IMMUNODEFICIENCY VIRUS 1;

AMINO ACID SEQUENCE; BLOTTING, WESTERN; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HIV; HIV ENVELOPE PROTEIN GP120; HIV ENVELOPE PROTEIN GP41; HUMANS; MUTAGENESIS, INSERTIONAL;

EID: 84931291964     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.628610     Document Type: Article

References (53)

1. Moulard, M., and Decroly, E. (2000) Maturation of HIV envelope glycoprotein precursors by cellular endoproteases. Biochim. Biophys. Acta 1469, 121-132
2. Curlin, M. E., Zioni, R., Hawes, S. E., Liu, Y., Deng, W., Gottlieb, G. S., Zhu, T., and Mullins, J. I. (2010) HIV-1 envelope subregion length variation during disease progression. PLoS Pathog. 6, e1001228
3. Zolla-Pazner, S., and Cardozo, T. (2010) Structure-function relationships of HIV-1 envelope sequence-variable regions refocus vaccine design. Nat. Rev. Immunol. 10, 527-535
4. Yuan, T., Li, J., and Zhang, M. Y. (2013) HIV-1 envelope glycoprotein variable loops are indispensable for envelope structural integrity and virus entry. PLoS One 8, e69789
5. Wyatt, R., Sullivan, N., Thali, M., Repke, H., Ho, D., Robinson, J., Posner, M., and Sodroski, J. (1993) Functional and immunologic characterization of human immunodeficiency virus type 1 envelope glycoproteins containing deletions of the major variable regions. J. Virol. 67, 4557-4565
6. Yang, X., Lipchina, I., Cocklin, S., Chaiken, I., and Sodroski, J. (2006) Antibody binding is a dominant determinant of the efficiency of human immunodeficiency virus type 1 neutralization. J. Virol. 80, 11404-11408
7. Leung, K., Kim, J. O., Ganesh, L., Kabat, J., Schwartz, O., and Nabel, G. J. (2008) HIV-1 assembly: viral glycoproteins segregate quantally to lipid rafts that associate individually with HIV-1 capsids and virions. Cell Host Microbe 3, 285-292
8. Wallace, A., and Stamatatos, L. (2009) Introduction of exogenous epitopes in the variable regions of the human immunodeficiency virus type 1 envelope glycoprotein: effect on viral infectivity and the neutralization phenotype. J. Virol. 83, 7883-7893
9. Ren, X., Sodroski, J., and Yang, X. (2005) An unrelated monoclonal antibody neutralizes human immunodeficiency virus type 1 by binding to an artificial epitope engineered in a functionally neutral region of the viral envelope glycoproteins. J. Virol. 79, 5616-5624
10. Pereira, C. F., Ellenberg, P. C., Jones, K. L., Fernandez, T. L., Smyth, R. P., Hawkes, D. J., Hijnen, M., Vivet-Boudou, V., Marquet, R., Johnson, I., and Mak, J. (2011) Labeling of multiple HIV-1 proteins with the biarsenicaltetracysteine system. PLoS One 6, e17016
11. Munro, J. B., Gorman, J., Ma, X., Zhou, Z., Arthos, J., Burton, D. R., Koff, W. C., Courter, J. R., Smith, A. B., 3rd, Kwong, P. D., Blanchard, S. C., and Mothes, W. (2014) Conformational dynamics of single HIV-1 envelope trimers on the surface of native virions. Science 346, 759-763
12. Julien, J. P., Cupo, A., Sok, D., Stanfield, R. L., Lyumkis, D., Deller, M. C., Klasse, P. J., Burton, D. R., Sanders, R. W., Moore, J. P., Ward, A. B., and Wilson, I. A. (2013) Crystal structure of a soluble cleaved HIV-1 envelope trimer. Science 342, 1477-1483
13. Lyumkis, D., Julien, J. P., de Val, N., Cupo, A., Potter, C. S., Klasse, P. J., Burton, D. R., Sanders, R. W., Moore, J. P., Carragher, B., Wilson, I. A., and Ward, A. B. (2013) Cryo-EM structure of a fully glycosylated soluble cleaved HIV-1 envelope trimer. Science 342, 1484-1490
14. Pancera, M., Zhou, T., Druz, A., Georgiev, I. S., Soto, C., Gorman, J., Huang, J., Acharya, P., Chuang, G. Y., Ofek, G., Stewart-Jones, G. B., Stuckey, J., Bailer, R. T., Joyce, M. G., Louder, M. K., Tumba, N., Yang, Y., Zhang, B., Cohen, M. S., Haynes, B. F., Mascola, J. R., Morris, L., Munro, J. B., Blanchard, S. C., Mothes, W., Connors, M., and Kwong, P. D. (2014) Structure and immune recognition of trimeric pre-fusion HIV-1 Env. Nature 514, 455-461
15. Tran, E. E., Borgnia, M. J., Kuybeda, O., Schauder, D. M., Bartesaghi, A., Frank, G. A., Sapiro, G., Milne, J. L., and Subramaniam, S. (2012) Structural mechanism of trimeric HIV-1 envelope glycoprotein activation. PLoS Pathog. 8, e1002797
16. Bartesaghi, A., Merk, A., Borgnia, M. J., Milne, J. L., and Subramaniam, S. (2013) Prefusion structure of trimeric HIV-1 envelope glycoprotein determined by cryo-electron microscopy. Nat. Struct. Mol. Biol. 20, 1352-1357
17. Gallagher, J. R., Atanasiu, D., Saw, W. T., Paradisgarten, M. J., Whitbeck, J. C., Eisenberg, R. J., and Cohen, G. H. (2014) Functional fluorescent protein insertions in herpes simplex virus gB report on gB conformation before and after execution of membrane fusion. PLoS Pathog. 10, e1004373
18. Cabantous, S., Terwilliger, T. C., and Waldo, G. S. (2005) Protein tagging and detection with engineered self-assembling fragments of green fluorescent protein. Nat. Biotechnol. 23, 102-107
19. Pédelacq, J. D., Cabantous, S., Tran, T., Terwilliger, T. C., and Waldo, G. S. (2006) Engineering and characterization of a superfolder green fluorescent protein. Nat. Biotechnol. 24, 79-88
20. Ishikawa, H., Meng, F., Kondo, N., Iwamoto, A., and Matsuda, Z. (2012) Generation of a dual-functional split-reporter protein for monitoring membrane fusion using self-associating split GFP. Protein Eng. Des Sel. 25, 813-820
21. Patterson, G. H., and Lippincott-Schwartz, J. (2002) A photoactivatable GFP for selective photolabeling of proteins and cells. Science 297, 1873-1877
22. Lam, A. J., St-Pierre, F., Gong, Y., Marshall, J. D., Cranfill, P. J., Baird, M. A., McKeown, M. R., Wiedenmann, J., Davidson, M. W., Schnitzer, M. J., Tsien, R. Y., and Lin, M. Z. (2012) Improving FRET dynamic range with bright green and red fluorescent proteins. Nat. Methods 9, 1005-1012
23. Shaner, N. C., Campbell, R. E., Steinbach, P. A., Giepmans, B. N., Palmer, A. E., and Tsien, R. Y. (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol. 22, 1567-1572
24. Cavrois, M., De Noronha, C., and Greene, W. C. (2002) A sensitive and specific enzyme-based assay detecting HIV-1 virion fusion in primary T lymphocytes. Nat. Biotechnol. 20, 1151-1154
25. Stemmer, W. P. (1994) Rapid evolution of a protein in vitro by DNA shuffling. Nature 370, 389-391
26. Doucet, N., De Wals, P. Y., and Pelletier, J. N. (2004) Site-saturation mutagenesis of Tyr-105 reveals its importance in substrate stabilization and discrimination in TEM-1 β-lactamase. J. Biol. Chem. 279, 46295-46303
27. Wolf, M. C., Wang, Y., Freiberg, A. N., Aguilar, H. C., Holbrook, M. R., and Lee, B. (2009) A catalytically and genetically optimized β-lactamase-matrix based assay for sensitive, specific, and higher throughput analysis of native henipavirus entry characteristics. Virol. J. 6, 119
28. Taylor, M. J., Perrais, D., and Merrifield, C. J. (2011) A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis. PLoS Biol. 9, e1000604
29. Vonderheit, A., and Helenius, A. (2005) Rab7 associates with early endosomes to mediate sorting and transport of Semliki forest virus to late endosomes. PLoS Biol. 3, e233
30. Choudhury, A., Dominguez, M., Puri, V., Sharma, D. K., Narita, K., Wheatley, C. L., Marks, D. L., and Pagano, R. E. (2002) Rab proteins mediate Golgi transport of caveola-internalized glycosphingolipids and correct lipid trafficking in Niemann-Pick C cells. J. Clin. Investig. 109, 1541-1550
31. Falcón-Pérez, J. M., Nazarian, R., Sabatti, C., and Dell'Angelica, E. C. (2005) Distribution and dynamics of Lamp1-containing endocytic organelles in fibroblasts deficient in BLOC-3. J. Cell Sci. 118, 5243-5255
32. 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
33. Kimpton, J., and Emerman, M. (1992) Detection of replication-competent and pseudotyped human immunodeficiency virus with a sensitive cell line on the basis of activation of an integrated β-galactosidase gene. J. Virol. 66, 2232-2239
34. 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
35. Wang, H., Li, X., Nakane, S., Liu, S., Ishikawa, H., Iwamoto, A., and Matsuda, Z. (2014) Co-expression of foreign proteins tethered to HIV-1 envelope glycoprotein on the cell surface by introducing an intervening second membrane-spanning domain. PLoS One 9, e96790
36. Abacioglu, Y. H., Fouts, T. R., Laman, J. D., Claassen, E., Pincus, S. H., Moore, J. P., Roby, C. A., Kamin-Lewis, R., and Lewis, G. K. (1994) Epitope mapping and topology of baculovirus-expressed HIV-1 gp160 determined with a panel of murine monoclonal antibodies. AIDS Res. Hum. Retroviruses 10, 371-381
37. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J. Y., White, D. J., Hartenstein, V., Eliceiri, K., Tomancak, P., and Cardona, A. (2012) Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676-682
38. Clements, G. J., Price-Jones, M. J., Stephens, P. E., Sutton, C., Schulz, T. F., Clapham, P. R., McKeating, J. A., McClure, M. O., Thomson, S., and Marsh, M. (1991) The V3 loops of the HIV-1 and HIV-2 surface glycoproteins contain proteolytic cleavage sites: a possible function in viral fusion? AIDS Res. Hum. Retroviruses 7, 3-16
39. Du, S. X., Xu, L., Viswanathan, S., and Whalen, R. G. (2008) Inhibition of V3-specific cleavage of recombinant HIV-1 gp120 produced in Chinese hamster ovary cells. Protein Expr. Purif. 59, 223-231
40. Niwa, Y., Yano, M., Futaki, S., Okumura, Y., and Kido, H. (1996) T-cell membrane-associated serine protease, tryptase TL2, binds human immunodeficiency virus type 1 gp120 and cleaves the third-variable-domain loop of gp120. Neutralizing antibodies of human immunodeficiency virus type 1 inhibit cleavage of gp120. Eur. J. Biochem. 237, 64-70
41. Vollenweider, F., Benjannet, S., Decroly, E., Savaria, D., Lazure, C., Thomas, G., Chrétien, M., and Seidah, N. G. (1996) Comparative cellular processing of the human immunodeficiency virus (HIV-1) envelope glycoprotein gp160 by the mammalian subtilisin/kexin-like convertases. Biochem. J. 314, 521-532
42. Diaz-Aguilar, B., Dewispelaere, K., Yi, H. A., and Jacobs, A. (2013) Significant differences in cell-cell fusion and viral entry between strains revealed by scanning mutagenesis of the C-heptad repeat of HIV gp41. Biochemistry 52, 3552-3563
43. Zhang, M., Chang, H., Zhang, Y., Yu, J., Wu, L., Ji, W., Chen, J., Liu, B., Lu, J., Liu, Y., Zhang, J., Xu, P., and Xu, T. (2012) Rational design of true monomeric and bright photoactivatable fluorescent proteins. Nat. Methods 9, 727-729
44. Santos da Silva, E., Mulinge, M., and Perez Bercoff, D. (2013) The frantic play of the concealed HIV envelope cytoplasmic tail. Retrovirology 10, 54
45. Postler, T. S., and Desrosiers, R. C. (2013) The tale of the long tail: the cytoplasmic domain of HIV-1 gp41. J. Virol. 87, 2-15
46. Abrahamyan, L. G., Mkrtchyan, S. R., Binley, J., Lu, M., Melikyan, G. B., and Cohen, F. S. (2005) The cytoplasmic tail slows the folding of human immunodeficiency virus type 1 Env from a late prebundle configuration into the six-helix bundle. J. Virol. 79, 106-115
47. Bosch, V., and Pawlita, M. (1990) Mutational analysis of the human immunodeficiency virus type 1 env gene product proteolytic cleavage site. J. Virol. 64, 2337-2344
48. Chan, W. E., Wang, Y. L., Lin, H. H., and Chen, S. S. (2004) Effect of extension of the cytoplasmic domain of human immunodeficiency type 1 virus transmembrane protein gp41 on virus replication. J. Virol. 78, 5157-5169
49. Moore, P. L., Crooks, E. T., Porter, L., Zhu, P., Cayanan, C. S., Grise, H., Corcoran, P., Zwick, M. B., Franti, M., Morris, L., Roux, K. H., Burton, D. R., and Binley, J. M. (2006) Nature of nonfunctional envelope proteins on the surface of human immunodeficiency virus type 1. J. Virol. 80, 2515-2528
50. Bültmann, A., Muranyi, W., Seed, B., and Haas, J. (2001) Identification of two sequences in the cytoplasmic tail of the human immunodeficiency virus type 1 envelope glycoprotein that inhibit cell surface expression. J. Virol. 75, 5263-5276
51. Griffin, B. A., Adams, S. R., and Tsien, R. Y. (1998) Specific covalent labeling of recombinant protein molecules inside live cells. Science 281, 269-272
52. Royant, A., and Noirclerc-Savoye, M. (2011) Stabilizing role of glutamic acid 222 in the structure of enhanced green fluorescent protein. J. Struct. Biol. 174, 385-390
53. Helseth, E., Olshevsky, U., Furman, C., and Sodroski, J. (1991) Human immunodeficiency virus type 1 gp120 envelope glycoprotein regions important for association with the gp41 transmembrane glycoprotein. J. Virol. 65, 2119-2123