Engineering and exploitation of a fluorescent HIV-1 gp120 for live cell CD4 binding assays

Virology

Volumn 476, Issue , 2015, Pages 240-248

  Costantini, Lindsey M ^a   Irvin, Susan C ^a   Kennedy, Steven C ^a   Guo, Feng ^a   Goldstein, Harris ^a   Herold, Betsy C ^a   Snapp, Erik L ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

CD4; Diffusion; Envelope; Fluorescent protein; FRAP; Gp120; HIV 1; Inhibitory antibody; Laser scanning cytometry; Neutralizing antibody; Superfolder GFP

Indexed keywords

CD4 ANTIGEN; GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 120 GREEN FLUORESCENT FUSION PROTEIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; PROTEIN VARIANT; UNCLASSIFIED DRUG; VIRUS RECEPTOR;

ARTICLE; BINDING AFFINITY; BINDING ASSAY; CONTROLLED STUDY; FLUORESCENCE IMAGING; HUMAN; HUMAN CELL; LASER SCANNING CYTOMETRY; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN TRANSPORT; QUANTITATIVE ANALYSIS; CD4+ T LYMPHOCYTE; CELL TRACKING; EVALUATION STUDY; GENETIC ENGINEERING; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; METABOLISM; PROCEDURES; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

CD4-POSITIVE T-LYMPHOCYTES; CELL TRACKING; GENETIC ENGINEERING; GREEN FLUORESCENT PROTEINS; HIV ENVELOPE PROTEIN GP120; HIV INFECTIONS; HIV-1; HUMANS; RECEPTORS, VIRUS; RECOMBINANT FUSION PROTEINS;

EID: 84920137309     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2014.12.019     Document Type: Article

References (47)

1. Aronson D.E., Costantini L.M., Snapp E.L. Superfolder GFP is fluorescent in oxidizing environments when targeted via the Sec translocon. Traffic 2011, 12:543-548.
2. Binley J.M., Ngo-Abdalla S., Moore P., Bobardt M., Chatterji U., Gallay P., Burton D.R., Wilson I.A., Elder J.H., de Parseval A. Inhibition of HIV Env binding to cellular receptors by monoclonal antibody 2G12 as probed by Fc-tagged gp120. Retrovirology 2006, 3:39.
3. Bowley D.R., Labrijn A.F., Zwick M.B., Burton D.R. Antigen selection from an HIV-1 immune antibody library displayed on yeast yields many novel antibodies compared to selection from the same library displayed on phage. Protein Eng. Des. Sel. 2007, 20:81-90.
4. de Silva A., Braakman I., Helenius A. Posttranslational folding of vesicular stomatitis virus G protein in the ER: involvement of noncovalent and covalent complexes. J. Cell Biol. 1993, 120:647-655.
5. Einstein A. Über die von der molekularkinetischen Theorie der Wärme geforderte Bewegung von in ruhenden Flüssigkeiten suspendierten Teilchen. Ann. Phys. 1905, 17:549-560.
6. Felber B.K., Hadzopoulou-Cladaras M., Cladaras C., Copeland T., Pavlakis G.N. rev protein of human immunodeficiency virus type 1 affects the stability and transport of the viral mRNA. Proc. Natl. Acad. Sci. USA 1989, 86:1495-1499.
7. Finzi A., Pacheco B., Zeng X., Kwon Y.D., Kwong P.D., Sodroski J. Conformational characterization of aberrant disulfide-linked HIV-1 gp120 dimers secreted from overexpressing cells. J. Virol. Methods 2010, 168:155-161.
8. Haas J., Park E.C., Seed B. Codon usage limitation in the expression of HIV-1 envelope glycoprotein. Curr. Biol. 1996, 6:315-324.
9. Haim H., Si Z., Madani N., Wang L., Courter J.R., Princiotto A., Kassa A., DeGrace M., McGee-Estrada K., Mefford M., Gabuzda D., Smith A.B., Sodroski J. Soluble CD4 and CD4-mimetic compounds inhibit HIV-1 infection by induction of a short-lived activated state. PLoS Pathog. 2009, 5:e1000360.
10. Hewson T.J., Logie J.J., Simmonds P., Howie S.E. A CCR5-dependent novel mechanism for type 1 HIV gp120 induced loss of macrophage cell surface CD4. J. Immunol. 2001, 166:4835-4842.
11. Jain R.K., Joyce P.B., Molinete M., Halban P.A., Gorr S.U. Oligomerization of green fluorescent protein in the secretory pathway of endocrine cells. Biochem. J. 2001, 360:645-649.
12. Kappes, J., Wu, X., 2005. Cell-based method and assay for measuring the infectivity and drug sensitivity of immunodeficiency virus. Google Patents.
13. Klein F., Mouquet H., Dosenovic P., Scheid J.F., Scharf L., Nussenzweig M.C. Antibodies in HIV-1 vaccine development and therapy. Science 2013, 341:1199-1204.
14. Kong L., Sheppard N.C., Stewart-Jones G.B., Robson C.L., Chen H., Xu X., Krashias G., Bonomelli C., Scanlan C.N., Kwong P.D., Jeffs S.A., Jones I.M., Sattentau Q.J. Expression-system-dependent modulation of HIV-1 envelope glycoprotein antigenicity and immunogenicity. J. Mol. Biol. 2010, 403:131-147.
15. Kost T.A., Condreay J.P., Jarvis D.L. Baculovirus as versatile vectors for protein expression in insect and mammalian cells. Nat. Biotechnol. 2005, 23:567-575.
16. Li Y., Luo L., Rasool N., Kang C.Y. Glycosylation is necessary for the correct folding of human immunodeficiency virus gp120 in CD4 binding. J. Virol. 1993, 67:584-588.
17. Li Y., Migueles S.A., Welcher B., Svehla K., Phogat A., Louder M.K., Wu X., Shaw G.M., Connors M., Wyatt R.T., Mascola J.R. Broad HIV-1 neutralization mediated by CD4-binding site antibodies. Nat. Med. 2007, 13:1032-1034.
18. Lippincott-Schwartz J., Snapp E., Kenworthy A. Studying protein dynamics in living cells. Nat. Rev. Mol. Cell Biol. 2001, 2:444-456.
19. Louwagie J., Janssens W., Mascola J., Heyndrickx L., Hegerich P., van der Groen G., McCutchan F.E., Burke D.S. Genetic diversity of the envelope glycoprotein from human immunodeficiency virus type 1 isolates of African origin. J. Virol. 1995, 69:263-271.
20. Mach W.J., Thimmesch A.R., Orr J.A., Slusser J.G., Pierce J.D. Flow cytometry and laser scanning cytometry, a comparison of techniques. J. Clin. Monit. Comput. 2010, 24:251-259.
21. Mascola J.R., Haynes B.F. HIV-1 neutralizing antibodies: understanding nature[U+05F3]s pathways. Immunol. Rev. 2013, 254:225-244.
22. Moulard M., Lortat-Jacob H., Mondor I., Roca G., Wyatt R., Sodroski J., Zhao L., Olson W., Kwong P.D., Sattentau Q.J. Selective interactions of polyanions with basic surfaces on human immunodeficiency virus type 1 gp120. J. Virol. 2000, 74:1948-1960.
23. Nehls S., Snapp E.L., Cole N.B., Zaal K.J., Kenworthy A.K., Roberts T.H., Ellenberg J., Presley J.F., Siggia E., Lippincott-Schwartz J. Dynamics and retention of misfolded proteins in native ER membranes. Nat. Cell Biol. 2000, 2:288-295.
24. Page K.A., Landau N.R., Littman D.R. Construction and use of a human immunodeficiency virus vector for analysis of virus infectivity. J. Virol. 1990, 64:5270-5276.
25. Pedelacq J.D., Cabantous S., Tran T., Terwilliger T.C., Waldo G.S. Engineering and characterization of a superfolder green fluorescent protein. Nat. Biotechnol. 2006, 24:79-88.
26. Platt E.J., Gomes M.M., Kabat D. Kinetic mechanism for HIV-1 neutralization by antibody 2G12 entails reversible glycan binding that slows cell entry. Proc. Natl. Acad. Sci. USA 2012, 109:7829-7834.
27. Pozarowski P., Holden E., Darzynkiewicz Z. Laser scanning cytometry: principles and applications-an update. Methods Mol. Biol. 2013, 931:187-212.
28. Rao V.R., Ruiz A.P., Prasad V.R. Viral and cellular factors underlying neuropathogenesis in HIV associated neurocognitive disorders (HAND). AIDS Res. Ther. 2014, 11:13.
29. Saffman P.G., Delbruck M. Brownian motion in biological membranes. Proc. Natl. Acad. Sci. USA 1975, 72:3111-3113.
30. Sanders R.W., Venturi M., Schiffner L., Kalyanaraman R., Katinger H., Lloyd K.O., Kwong P.D., Moore J.P. The mannose-dependent epitope for neutralizing antibody 2G12 on human immunodeficiency virus type 1 glycoprotein gp120. J. Virol. 2002, 76:7293-7305.
31. Scanlan C.N., Pantophlet R., Wormald M.R., Ollmann Saphire E., Stanfield R., Wilson I.A., Katinger H., Dwek R.A., Rudd P.M., Burton D.R. The broadly neutralizing anti-human immunodeficiency virus type 1 antibody 2G12 recognizes a cluster of alpha1→2 mannose residues on the outer face of gp120. J. Virol. 2002, 76:7306-7321.
32. Schiffner T., Sattentau Q.J., Dorrell L. Development of prophylactic vaccines against HIV-1. Retrovirology 2013, 10:72.
33. Schon A., Madani N., Klein J.C., Hubicki A., Ng D., Yang X., Smith A.B., Sodroski J., Freire E. Thermodynamics of binding of a low-molecular-weight CD4 mimetic to HIV-1 gp120. Biochemistry 2006, 45:10973-10980.
34. Scordi-Bello I.A., Mosoian A., He C., Chen Y., Cheng Y., Jarvis G.A., Keller M.J., Hogarty K., Waller D.P., Profy A.T., Herold B.C., Klotman M.E. Candidate sulfonated and sulfated topical microbicides: comparison of anti-human immunodeficiency virus activities and mechanisms of action. Antimicrob. Agents Chemother. 2005, 49:3607-3615.
35. Shaner N.C., Lambert G.G., Chammas A., Ni Y., Cranfill P.J., Baird M.A., Sell B.R., Allen J.R., Day R.N., Israelsson M., Davidson M.W., Wang J. A bright monomeric green fluorescent protein derived from Branchiostoma lanceolatum. Nat. Methods 2013, 10:407-409.
36. Sherer N.M., Lehmann M.J., Jimenez-Soto L.F., Ingmundson A., Horner S.M., Cicchetti G., Allen P.G., Pypaert M., Cunningham J.M., Mothes W. Visualization of retroviral replication in living cells reveals budding into multivesicular bodies. Traffic 2003, 4:785-801.
37. Si Z., Madani N., Cox J.M., Chruma J.J., Klein J.C., Schon A., Phan N., Wang L., Biorn A.C., Cocklin S., Chaiken I., Freire E., Smith A.B., Sodroski J.G. Small-molecule inhibitors of HIV-1 entry block receptor-induced conformational changes in the viral envelope glycoproteins. Proc. Natl. Acad. Sci. USA 2004, 101:5036-5041.
38. Siggia E.D., Lippincott-Schwartz J., Bekiranov S. Diffusion in inhomogeneous media: theory and simulations applied to whole cell photobleach recovery. Biophys. J. 2000, 79:1761-1770.
39. Simek M.D., Rida W., Priddy F.H., Pung P., Carrow E., Laufer D.S., Lehrman J.K., Boaz M., Tarragona-Fiol T., Miiro G., Birungi J., Pozniak A., McPhee D.A., Manigart O., Karita E., Inwoley A., Jaoko W., Dehovitz J., Bekker L.G., Pitisuttithum P., Paris R., Walker L.M., Poignard P., Wrin T., Fast P.E., Burton D.R., Koff W.C. Human immunodeficiency virus type 1 elite neutralizers: individuals with broad and potent neutralizing activity identified by using a high-throughput neutralization assay together with an analytical selection algorithm. J. Virol. 2009, 83:7337-7348.
40. Snapp E.L., Sharma A., Lippincott-Schwartz J., Hegde R.S. Monitoring chaperone engagement of substrates in the endoplasmic reticulum of live cells. Proc. Natl. Acad. Sci. USA 2006, 103:6536-6541.
41. Swanson J. Fluorescent labeling of endocytic compartments. Methods Cell Biol. 1989, 29:137-151.
42. Trkola A., Dragic T., Arthos J., Binley J.M., Olson W.C., Allaway G.P., Cheng-Mayer C., Robinson J., Maddon P.J., Moore J.P. CD4-dependent, antibody-sensitive interactions between HIV-1 and its co-receptor CCR-5. Nature 1996, 384:184-187.
43. van Anken E., Sanders R.W., Liscaljet I.M., Land A., Bontjer I., Tillemans S., Nabatov A.A., Paxton W.A., Berkhout B., Braakman I. Only five of 10 strictly conserved disulfide bonds are essential for folding and eight for function of the HIV-1 envelope glycoprotein. Mol. Biol. Cell 2008, 19:4298-4309.
44. Vonderheit A., Helenius A. Rab7 associates with early endosomes to mediate sorting and transport of Semliki forest virus to late endosomes. PLoS Biol. 2005, 3:e233.
45. Wang Q., Pang S. An intercellular adhesion molecule-3 (ICAM-3) -grabbing nonintegrin (DC-SIGN) efficiently blocks HIV viral budding. FASEB J. 2008, 22:1055-1064.
46. Wu X., Yang Z.Y., Li Y., Hogerkorp C.M., Schief W.R., Seaman M.S., Zhou T., Schmidt S.D., Wu L., Xu L., Longo N.S., McKee K., O'Dell S., Louder M.K., Wycuff D.L., Feng Y., Nason M., Doria-Rose N., Connors M., Kwong P.D., Roederer M., Wyatt R.T., Nabel G.J., Mascola J.R. Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 2010, 329:856-861.
47. Zhou T., Georgiev I., Wu X., Yang Z.Y., Dai K., Finzi A., Kwon Y.D., Scheid J.F., Shi W., Xu L., Yang Y., Zhu J., Nussenzweig M.C., Sodroski J., Shapiro L., Nabel G.J., Mascola J.R., Kwong P.D. Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01. Science 2010, 329:811-817.