Mechanism of multivalent nanoparticle encounter with HIV-1 for potency enhancement of peptide triazole virus inactivation

Journal of Biological Chemistry

Volumn 290, Issue 1, 2015, Pages 529-543

  Bastian, Arangassery Rosemary ^a,b   Nangarlia, Aakansha ^a,b   Bailey, Lauren D ^a   Holmes, Andrew ^a   Sundaram, R Venkat Kalyana ^a,b   Ang, Charles ^a,b   Moreira, Diogo R M ^c   Freedman, Kevin ^d   Duffy, Caitlin ^a   Contarino, Mark ^a   Abrams, Cameron ^d   Root, Michael ^e   Chaiken, Irwin ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b DREXEL UNIVERSITY   (United States)

^c INSTITUTO OSWALDO CRUZ   (Brazil)

^d Drexel University   (United States)

^e THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRAL AGENTS; BINDING SITES; CELL MEMBRANES; DISEASES; GOLD NANOPARTICLES; NANOPARTICLES; PEPTIDES;

ANTI-VIRAL EFFECTS; ENVELOPED VIRUS; METASTABILITIES; NANOPARTICLE CONJUGATE; PICOMOLAR LEVELS; RESISTANT MUTANTS; SPIKE PROTEIN; VIRUS INACTIVATION;

VIRUSES;

GLYCOPROTEIN GP 120; GOLD NANOPARTICLE; PEPTIDE TRIAZOLE; TRIAZOLE DERIVATIVE; UNCLASSIFIED DRUG; ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; GOLD; NANOCONJUGATE; PEPTIDE; PROTEIN BINDING;

ANTIVIRAL ACTIVITY; ARTICLE; BINDING AFFINITY; CONJUGATION; CONTROLLED STUDY; DISPERSION; DRUG POTENCY; DRUG PROTEIN BINDING; GROWTH INHIBITION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PARTICLE SIZE; PHYSICAL PHENOMENA; PROTEIN FUNCTION; VIRUS INACTIVATION; VIRUS INHIBITION; VIRUS SHEDDING; ANTAGONISTS AND INHIBITORS; CHEMISTRY; DOSE RESPONSE; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; SYNTHESIS; TUMOR CELL LINE; ULTRASTRUCTURE; VIRUS ENTRY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

ANTI-HIV AGENTS; CELL LINE, TUMOR; DOSE-RESPONSE RELATIONSHIP, DRUG; GOLD; HIV ENVELOPE PROTEIN GP120; HIV-1; HUMANS; NANOCONJUGATES; PARTICLE SIZE; PEPTIDES; PROTEIN BINDING; TRIAZOLES; VIRUS INACTIVATION; VIRUS INTERNALIZATION;

EID: 84920545972     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.608315     Document Type: Article

References (75)

1. Doyle, T., and Geretti, A. M. (2012) Low-level viraemia on HAART: significance and management. Curr. Opin. Infect. Dis. 25, 17-25
2. Joint United Nations Programme on HIV/AIDS (2013) Global Report: UNAIDS Report on the Global AIDS Epidemic 2013, p 198, United Nations, Geneva
3. Kromdijk, W., Huitema, A. D., and Mulder, J. W. (2010) Treatment of HIV infection with the CCR5 antagonist maraviroc. Expert Opin. Pharmacother. 11, 1215-1223
4. Flores, A., and Quesada, E. (2013) Entry inhibitors directed towards glycoprotein gp120: an overview on a promising target for HIV-1 therapy. Curr. Med. Chem. 20, 751-771
5. Palmisano, L., and Vella, S. (2011) A brief history of antiretroviral therapy of HIV infection: success and challenges, Ann. Ist. Super. Sanita 47, 44-48
6. Granich, R., Crowley, S., Vitoria, M., Lo, Y. R., Souteyrand, Y., Dye, C., Gilks, C., Guerma, T., De Cock, K. M., and Williams, B. (2010) Highly active antiretroviral treatment for the prevention of HIV transmission, J. Int. AIDS Soc. 13, 1
7. Haqqani, A. A., and Tilton, J. C. (2013) Entry inhibitors and their use in the treatment of HIV-1 infection. Antiviral Res. 98, 158-170
8. Qiu, S., Yi, H., Hu, J., Cao, Z., Wu, Y., and Li, W. (2012) The binding mode of fusion inhibitor T20 onto HIV-1 gp41 and relevant T20-resistant mechanisms explored by computational study. Curr. HIV Res. 10, 182-194
9. Henrich, T. J., and Kuritzkes, D. R. (2013) HIV-1 entry inhibitors: recent development and clinical use. Curr. Opin. Virol. 3, 51-57
10. Wallace, B. J., Tan, K. B., Pett, S. L., Cooper, D. A., Kossard, S., and Whitfeld, M. J. (2011) Enfuvirtide injection site reactions: a clinical and histopathological appraisal. Australas. J. Dermatol. 52, 19-26
11. Perry, C. M. (2010) Maraviroc: a review of its use in the management of CCR5-tropic HIV-1 infection. Drugs 70, 1189-1213
12. 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
13. Champagne, K., Shishido, A., and Root, M. J. (2009) Interactions of HIV-1 inhibitory peptide T20 with the gp41 N-HR coiled coil. J. Biol. Chem. 284, 3619-3627
14. Emmelkamp, J. M., and Rockstroh, J. K. (2007) CCR5 antagonists: comparison of efficacy, side effects, pharmacokinetics and interactions: review of the literature. Eur. J. Med. Res. 12, 409-417
15. Chan, D. C., and Kim, P. S. (1998) HIV entry and its inhibition. Cell 93, 681-684
16. Wyatt, R., Kwong, P. D., Desjardins, E., Sweet, R. W., Robinson, J., Hendrickson, W. A., and Sodroski, J. G. (1998) The antigenic structure of the HIV gp120 envelope glycoprotein. Nature 393, 705-711
17. Kwong, P. D., Wyatt, R., Robinson, J., Sweet, R. W., Sodroski, J., and Hendrickson, W. A. (1998) Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393, 648-659
18. Wyatt, R., and Sodroski, J. (1998) The HIV-1 envelope glycoproteins: fusogens, antigens, and immunogens. Science 280, 1884-1888
19. Hermann, F. G., Egerer, L., Brauer, F., Gerum, C., Schwalbe, H., Dietrich, U., and von Laer, D. (2009) Mutations in gp120 contribute to the resistance of human immunodeficiency virus type 1 to membrane-anchored C-peptide maC46. J. Virol. 83, 4844-4853
20. Park, E. J., Vujcic, L. K., Anand, R., Theodore, T. S., and Quinnan, G. V., Jr. (1998) Mutations in both gp120 and gp41 are responsible for the broad neutralization resistance of variant human immunodeficiency virus type 1 MN to antibodies directed at V3 and non-V3 epitopes. J. Virol. 72, 7099-7107
21. Johnson, V. A., Calvez, V., Gunthard, H. F., Paredes, R., Pillay, D., Shafer, R. W., Wensing, A. M., and Richman, D. D. (2013) Update of the drug resistance mutations in HIV-1: March 2013. Top. Antivir. Med. 21, 6-14
22. Madani, N., Princiotto, A. M., Schön, A., LaLonde, J., Feng, Y., Freire, E., Park, J., Courter, J. R., Jones, D. M., Robinson, J., Liao, H. X., Moody, M. A., Permar, S., Haynes, B., Smith, A. B., 3rd, Wyatt, R., and Sodroski, J. (2014) CD4-mimetic small molecules sensitize human immunodeficiency virus (HIV-1) to vaccine-elicited antibodies. J. Virol. 88, 6542-6555
23. Nettles, R. E., Schürmann, D., Zhu, L., Stonier, M., Huang, S. P., Chang, I., Chien, C., Krystal, M., Wind-Rotolo, M., Ray, N., Hanna, G. J., Bertz, R., and Grasela, D. (2012) Pharmacodynamics, safety, and pharmacokinetics of BMS-663068, an oral HIV-1 attachment inhibitor in HIV-1-infected subjects. J. Infect. Dis. 206, 1002-1011
24. Zhao, Q., Ma, L., Jiang, S., Lu, H., Liu, S., He, Y., Strick, N., Neamati, N., and Debnath, A. K. (2005) Identification of N-phenyl-N′-(2,2,6,6-tetramethylpiperidin-4-yl)-oxalamides as a new class of HIV-1 entry inhibitors that prevent gp120 binding to CD4. Virology 339, 213-225
25. Hughes, A., Barber, T., and Nelson, M. (2008) New treatment options for HIV salvage patients: an overview of second generation PIs, NNRTIs, integrase inhibitors and CCR5 antagonists. J. Infect. 57, 1-10
26. Nichols, W. G., Steel, H. M., Bonny, T., Adkison, K., Curtis, L., Millard, J., Kabeya, K., and Clumeck, N. (2008) Hepatotoxicity observed in clinical trials of aplaviroc (GW873140). Antimicrob. Agents Chemother. 52, 858-865
27. Nichols, W. K., Mehta, R., Skordos, K., Macé, K., Pfeifer, A. M., Carr, B. A., Minko, T., Burchiel, S. W., and Yost, G. S. (2003) 3-Methylindole-induced toxicity to human bronchial epithelial cell lines, Toxicol. Sci. 71, 229-236
28. Madani, N., Schön, A., Princiotto, A. M., Lalonde, J. M., Courter, J. R., Soeta, T., Ng, D., Wang, L., Brower, E. T., Xiang, S. H., Kwon, Y. D., Huang, C. C., Wyatt, R., Kwong, P. D., Freire, E., Smith, A. B., 3rd, and Sodroski, J. (2008) Small-molecule CD4 mimics interact with a highly conserved pocket on HIV-1 gp120. Structure 16, 1689-1701
29. Cocklin, S., Gopi, H., Querido, B., Nimmagadda, M., Kuriakose, S., Cicala, C., Ajith, S., Baxter, S., Arthos, J., Martín-García, J., and Chaiken, I. M. (2007) Broad-spectrum anti-human immunodeficiency virus (HIV) potential of a peptide HIV type 1 entry inhibitor. J. Virol. 81, 3645-3648
30. Emileh, A., Tuzer, F., Yeh, H., Umashankara, M., Moreira, D. R., Lalonde, J. M., Bewley, C. A., Abrams, C. F., and Chaiken, I. M. (2013) A model of peptide triazole entry inhibitor binding to HIV-1 gp120 and the mechanism of bridging sheet disruption. Biochemistry 52, 2245-2261
31. Gopi, H. N., Tirupula, K. C., Baxter, S., Ajith, S., and Chaiken, I. M. (2006) Click chemistry on azidoproline: high-affinity dual antagonist for HIV-1 envelope glycoprotein gp120. ChemMedChem 1, 54-57
32. McFadden, K., Fletcher, P., Rossi, F., Kantharaju, Umashankara, M., Pirrone, V., Rajagopal, S., Gopi, H., Krebs, F. C., Martin-Garcia, J., Shattock, R. J., and Chaiken, I. (2012) Antiviral breadth and combination potential of peptide triazole HIV-1 entry inhibitors, Antimicrob. Agents Chemother. 56, 1073-1080
33. Tuzer, F., Madani, N., Kamanna, K., Zentner, I., LaLonde, J., Holmes, A., Upton, E., Rajagopal, S., McFadden, K., Contarino, M., Sodroski, J., and Chaiken, I. (2013) HIV-1 Env gp120 structural determinants for peptide triazole dual receptor site antagonism. Proteins 81, 271-290
34. Umashankara, M., McFadden, K., Zentner, I., Schön, A., Rajagopal, S., Tuzer, F., Kuriakose, S. A., Contarino, M., Lalonde, J., Freire, E., and Chaiken, I. (2010) The active core in a triazole peptide dual-site antagonist of HIV-1 gp120. ChemMedChem 5, 1871-1879
35. Ferrer, M., and Harrison, S. C. (1999) Peptide ligands to human immunodeficiency virus type 1 gp120 identified from phage display libraries. J. Virol. 73, 5795-5802
36. Biorn, A. C., Cocklin, S., Madani, N., Si, Z., Ivanovic, T., Samanen, J., Van Ryk, D. I., Pantophlet, R., Burton, D. R., Freire, E., Sodroski, J., and Chaiken, I. M. (2004) Mode of action for linear peptide inhibitors of HIV-1 gp120 interactions. Biochemistry 43, 1928-1938
37. Bastian, A. R., Contarino, M., Bailey, L. D., Aneja, R., Moreira, D. R., Freedman, K., McFadden, K., Duffy, C., Emileh, A., Leslie, G., Jacobson, J. M., Hoxie, J. A., and Chaiken, I. (2013) Interactions of peptide triazole thiols with Env gp120 induce irreversible breakdown and inactivation of HIV-1 virions. Retrovirology 10, 153
38. Bastian, A. R., Kantharaju, McFadden, K., Duffy, C., Rajagopal, S., Contarino, M. R., Papazoglou, E., and Chaiken, I. (2011) Cell-free HIV-1 virucidal action by modified peptide triazole inhibitors of Env gp120, ChemMedChem 6, 1335-1339, 1318
39. Gopi, H., Cocklin, S., Pirrone, V., McFadden, K., Tuzer, F., Zentner, I., Ajith, S., Baxter, S., Jawanda, N., Krebs, F. C., and Chaiken, I. M. (2009) Introducing metallocene into a triazole peptide conjugate reduces its off-rate and enhances its affinity and antiviral potency for HIV-1 gp120. J. Mol. Recognit. 22, 169-174
40. Frens, G. (1973) Controlled nucleation for the regulation of the particle size in monodisperse gold suspensions. Nature 10.1038/physci241020a0
41. Haiss, W., Thanh, N. T., Aveyard, J., and Fernig, D. G. (2007) Determination of size and concentration of gold nanoparticles from UV-vis spectra. Anal. Chem. 79, 4215-4221
42. Xie, H., Tkachenko, A. G., Glomm, W. R., Ryan, J. A., Brennaman, M. K., Papanikolas, J. M., Franzen, S., and Feldheim, D. L. (2003) Critical flocculation concentrations, binding isotherms, and ligand exchange properties of peptide-modified gold nanoparticles studied by UV-visible, fluorescence, and time-correlated single photon counting spectroscopies. Anal. Chem. 75, 5797-5805
43. He, J., Choe, S., Walker, R., Di Marzio, P., Morgan, D. O., and Landau, N. R. (1995) Human immunodeficiency virus type 1 viral protein R (Vpr) arrests cells in the G2 phase of the cell cycle by inhibiting p34cdc2 activity. J. Virol. 69, 6705-6711
44. Connor, R. I., Chen, B. K., Choe, S., and Landau, N. R. (1995) Vpr is required for efficient replication of human immunodeficiency virus type-1 in mononuclear phagocytes. Virology 206, 935-944
45. Xiang, S. H., Kwong, P. D., Gupta, R., Rizzuto, C. D., Casper, D. J., Wyatt, R., Wang, L., Hendrickson, W. A., Doyle, M. L., and Sodroski, J. (2002) Mutagenic stabilization and/or disruption of a CD4-bound state reveals distinct conformations of the human immunodeficiency virus type 1 gp120 envelope glycoprotein. J. Virol. 76, 9888-9899
46. Dey, B., Pancera, M., Svehla, K., Shu, Y., Xiang, S. H., Vainshtein, J., Li, Y., Sodroski, J., Kwong, P. D., Mascola, J. R., and Wyatt, R. (2007) Characterization of human immunodeficiency virus type 1 monomeric and trimeric gp120 glycoproteins stabilized in the CD4-bound state: antigenicity, biophysics, and immunogenicity. J. Virol. 81, 5579-5593
47. Flint, S. J., Enquist, L. W., and Racaniello, V. R. (2008) Principles of Virology, pp. 83-85, ASM Press, Washington, D. C.
48. Chojnacki, J., Staudt, T., Glass, B., Bingen, P., Engelhardt, J., Anders, M., Schneider, J., Müller, B., Hell, S. W., and Kräusslich, H. G. (2012) Maturation-dependent HIV-1 surface protein redistribution revealed by fluorescence nanoscopy. Science 338, 524-528
49. Muranyi, W., Malkusch, S., Müller, B., Heilemann, M., and Kräusslich, H. G. (2013) Super-resolution microscopy reveals specific recruitment of HIV-1 envelope proteins to viral assembly sites dependent on the envelope C-terminal tail. PLoS Pathog. 9, e1003198
50. Crooks, E. T., Tong, T., Osawa, K., and Binley, J. M. (2011) Enzyme digests eliminate nonfunctional Env from HIV-1 particle surfaces, leaving native Env trimers intact and viral infectivity unaffected. J. Virol. 85, 5825-5839
51. Summers, M. F., Henderson, L. E., Chance, M. R., Bess, J. W., Jr., South, T. L., Blake, P. R., Sagi, I., Perez-Alvarado, G., Sowder, R. C., 3rd, and Hare, D. R. (1992) Nucleocapsid zinc fingers detected in retroviruses: EXAFS studies of intact viruses and the solution-state structure of the nucleocapsid protein from HIV-1. Protein Sci. 1, 563-574
52. Vogt, V. M., and Simon, M. N. (1999) Mass determination of Rous sarcoma virus virions by scanning transmission electron microscopy. J. Virol. 73, 7050-7055
53. Kim, T., Lee, K., Gong, M. S., and Joo, S. W. (2005) Control of gold nanoparticle aggregates by manipulation of interparticle interaction. Langmuir 21, 9524-9528
54. Mao, Y., Wang, L., Gu, C., Herschhorn, A., Désormeaux, A., Finzi, A., Xiang, S. H., and Sodroski, J. G. (2013) Molecular architecture of the uncleaved HIV-1 envelope glycoprotein trimer. Proc. Natl. Acad. Sci. U.S.A. 110, 12438-12443
55. Mao, Y., Wang, L., Gu, C., Herschhorn, A., Xiang, S. H., Haim, H., Yang, X., and Sodroski, J. (2012) Subunit organization of the membrane-bound HIV-1 envelope glycoprotein trimer. Nat. Struct. Mol. Biol. 19, 893-899
56. Myszka, D. G., Sweet, R. W., Hensley, P., Brigham-Burke, M., Kwong, P. D., Hendrickson, W. A., Wyatt, R., Sodroski, J., and Doyle, M. L. (2000) Energetics of the HIV gp120-CD4 binding reaction. Proc. Natl. Acad. Sci. U.S.A. 97, 9026-9031
57. Dimitrov, A. S., Jacobs, A., Finnegan, C. M., Stiegler, G., Katinger, H., and Blumenthal, R. (2007) Exposure of the membrane-proximal external region of HIV-1 gp41 in the course of HIV-1 envelope glycoprotein-mediated fusion. Biochemistry 46, 1398-1401
58. White, J. M., Delos, S. E., Brecher, M., and Schornberg, K. (2008) Structures and mechanisms of viral membrane fusion proteins: multiple variations on a common theme. Crit. Rev. Biochem. Mol. Biol. 43, 189-219
59. Xu, Y., Zhang, C., Jia, L., Wen, C., Liu, H., Wang, Y., Sun, Y., Huang, L., Zhou, Y., and Song, H. (2009) A novel approach to inhibit HIV-1 infection and enhance lysis of HIV by a targeted activator of complement. Virol. J. 6, 123
60. Nakamura, M., Terada, M., Sasaki, H., Kamada, M., and Ohno, T. (2000) Virolysis and in vitro neutralization of HIV-1 by humanized monoclonal antibody hNM-01. Hybridoma 19, 427-434
61. Contarino, M., Bastian, A. R., Kalyana Sundaram, R. V., McFadden, K., Duffy, C., Gangupomu, V., Baker, M., Abrams, C., and Chaiken, I. (2013) Chimeric Cyanovirin-MPER recombinantly engineered proteins cause cell-free virolysis of HIV-1. Antimicrob. Agents Chemother. 57, 4743-4750
62. Farokhzad, O. C., and Langer, R. (2009) Impact of nanotechnology on drug delivery. ACS Nano 3, 16-20
63. Zhang, L., Gu, F. X., Chan, J. M., Wang, A. Z., Langer, R. S., and Farokhzad, O. C. (2008) Nanoparticles in medicine: therapeutic applications and developments, Clin. Pharmacol. Ther. 83, 761-769
64. Hamidi, M., Azadi, A., Rafiei, P., and Ashrafi, H. (2013)Apharmacokinetic overview of nanotechnology-based drug delivery systems: an ADME-oriented approach. Crit. Rev. Ther. Drug Carrier Syst. 30, 435-467
65. Heidel, J. D., and Davis, M. E. (2011) Clinical developments in nanotechnology for cancer therapy. Pharm. Res. 28, 187-199
66. Jiang, W., Kim, B. Y., Rutka, J. T., and Chan, W. C. (2008) Nanoparticle-mediated cellular response is size-dependent. Nat. Nanotechnol. 3, 145-150
67. Mamo, T., Moseman, E. A., Kolishetti, N., Salvador-Morales, C., Shi, J., Kuritzkes, D. R., Langer, R., von Andrian, U., and Farokhzad, O. C. (2010) Emerging nanotechnology approaches for HIV/AIDS treatment and prevention. Nanomedicine 5, 269-285
68. Bowman, M. C., Ballard, T. E., Ackerson, C. J., Feldheim, D. L., Margolis, D. M., and Melander, C. (2008) Inhibition of HIV fusion with multivalent gold nanoparticles. J. Am. Chem. Soc. 130, 6896-6897
69. Mahmoud, K. A., and Luong, J. H. (2008) Impedance method for detecting HIV-1 protease and screening for its inhibitors using ferrocene-peptide conjugate/Au nanoparticle/single-walled carbon nanotube modified electrode. Anal. Chem. 80, 7056-7062
70. Chithrani, B. D., Ghazani, A. A., and Chan, W. C. (2006) Determining the size and shape dependence of gold nanoparticle uptake into mammalian cells. Nano Lett. 6, 662-668
71. Poignard, P., Moulard, M., Golez, E., Vivona, V., Franti, M., Venturini, S., Wang, M., Parren, P. W., and Burton, D. R. (2003) Heterogeneity of envelope molecules expressed on primary human immunodeficiency virus type 1 particles as probed by the binding of neutralizing and nonneutralizing antibodies. J. Virol. 77, 353-365
72. Bennett, A., Liu, J., Van Ryk, D., Bliss, D., Arthos, J., Henderson, R. M., and Subramaniam, S. (2007) Cryoelectron tomographic analysis of an HIV-neutralizing protein and its complex with native viral gp120. J. Biol. Chem. 282, 27754-27759
73. Deleted in proof
74. Kol, N., Shi, Y., Tsvitov, M., Barlam, D., Shneck, R. Z., Kay, M. S., and Rousso, I. (2007) A stiffness switch in human immunodeficiency virus. Biophys. J. 92, 1777-1783
75. Wallin, M., Ekstrom, M., and Garoff, H. (2005) The fusion-controlling disulfide bond isomerase in retrovirus Env is triggered by protein destabilization. J. Virol. 79, 1678-1685