Dressing up nanoparticles: A membrane wrap to induce formation of the virological synapse

ACS Nano

Volumn 9, Issue 4, 2015, Pages 4182-4192

  Yu, Xinwei ^a   Xu, Fangda ^a   Ramirez, Nora Guadalupe P ^b   Kijewski, Suzanne D G ^b   Akiyama, Hisashi ^b   Gummuluru, Suryaram ^b   Reinhard, Björn M ^a  

^a Boston University   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

biomimetics; drug delivery; glycosphingolipid; GM3; human immunodeficiency virus; Siglec1; stealth nanoparticles

Indexed keywords

BIOMIMETICS; CELLS; CYTOLOGY; DRUG DELIVERY; ENZYME ACTIVITY; IMMUNE SYSTEM; MOBILE SECURITY; NANOPARTICLES; PROTEINS; T-CELLS; VIRUSES;

GLYCOSPHINGOLIPIDS; GM3; HUMAN IMMUNODEFICIENCY VIRUS; SIGLEC1; STEALTH NANOPARTICLES;

DISEASES;

DRUG CARRIER; GANGLIOSIDE GM3; GOLD; METAL NANOPARTICLE; SIALOADHESIN;

CHEMISTRY; CYTOLOGY; DENDRITIC CELL; DRUG EFFECTS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGICAL SYNAPSE; IMMUNOLOGY; METABOLISM; SIGNAL TRANSDUCTION; T LYMPHOCYTE; VIRION;

DENDRITIC CELLS; DRUG CARRIERS; G(M3) GANGLIOSIDE; GOLD; HIV-1; HUMANS; IMMUNOLOGICAL SYNAPSES; METAL NANOPARTICLES; SIALIC ACID BINDING IG-LIKE LECTIN 1; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; VIRION;

EID: 84928975736     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/acsnano.5b00415     Document Type: Article

References (54)

1. Grakoui, A.; Bromley, S. K.; Sumen, C.; Davis, M. M.; Shaw, A. S.; Allen, P. M.; Dustin, M. L. The Immunological Synapse: A Molecular Machine Controlling T Cell Activation Science 1999, 285, 221-227
2. Chmielowski, B.; Ribas, A. Targeting Immunological Synapse: New Horizons in Immunotherapy for Cancer; Humana Press, 2009.
3. Wiendl, H.; Hohlfeld, R. Immune Regulation and Immunotherapy in Autoimmune Disease; Springer, 2007.
4. Jolly, C.; Kashefi, M.; Hollinshead, M.; Sattentau, Q. J. HIV-1 Cell to Cell Transfer Across an Env-Induced, Actin-Dependent Synapse J. Exp. Med. 2004, 199, 283-293
5. Hubner, W.; McNerney, G. P.; Chen, P.; Dale, B. M.; Gordon, R. E.; Chuang, F. Y.; Li, X. D.; Asmuth, D. M.; Huser, T.; Chen, B. K. Quantitative 3D Video Microscopy of HIV Transfer across T Cell Virological Synapses Science 2009, 323, 1743-1747
6. Vasiliver-Shamis, G.; Dustin, M. L.; Hioe, C. E. HIV-1 Virological Synapse Is Not Simply a Copycat of the Immunological Synapse Viruses 2010, 2, 1239-1260
7. Macdonald, D.; Wu, L.; Bohks, S. M.; Kewal Ramani, V. N.; Unutmaz, D.; Hope, T. J. Recruitment of HIV and Its Receptors to Dendritic Cell-Tcell Junctions Science 2003, 300, 1295-1297
8. Jolly, C.; Sattentau, Q. J. Retroviral Spread by Induction of Virological Synapses Traffic 2004, 5, 643-650
9. Haase, A. T. Population Biology of HIV-1 Infection: Viral and CD4+ T Cell Demographics and Dynamics in Lymphatic Tissue Annu. Rev. Immunol. 1999, 17, 625-656
10. Puryear, W. B.; Akiyama, H.; Geer, S. D.; Ramirez, N. P.; Yu, X.; Reinhard, B. M.; Gummuluru, S. Interferon-Inducible Mechanism of Dendritic Cell-Mediated HIV-1 Dissemination is Dependent on the Siglec, CD169 PloS Pathog. 2013, 9, e1003291
11. Izquierdo-Useros, N.; Lorizate, M.; Contreras, F.-X.; Rodriguez-Plata, M. T.; Glass, B.; Erkizia, I.; Prado, J. G.; Casas, J.; Fabrias, G.; Krausslich, H. G. et al. Sialyllactose in Viral Membrane Gangliosides Is a Novel Molecular Recognition Pattern for Mature Dendritic Cell Capture of HIV-1 PLoS Biol. 2012, 10, e1001315
12. Puryear, W. B.; Yu, X.; Ramirez, N. P.; Reinhard, B. M.; Gummuluru, S. HIV-1 Incorporation of Host-Cell-Derived Glycosphingolipid GM3 Allows for Capture by Mature Dendritic Cells Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 7475-7480
13. Izquierdo-Useros, N.; Lorizate, M.; Puertas, M. C.; Rodriguez-Plata, M. T.; Zangger, N.; Erikson, E.; Pino, M.; Erkizia, I.; Glass, B.; Clotet, B.; Keppler, O. T.; Telenti, A.; Krausslich, H. G.; Martinez-Picado, J. et al. Siglec-1 Is a Novel Dendritic Cell Receptor That Mediates HIV-1 Trans-Infection through Recognition of Viral Membrane Gangliosides PLoS Biol. 2012, 10, e1001448
14. Yameen, B.; Choi, W. I.; Vilos, C.; Swami, A.; Shi, J.; Farokhzad, O. C. Insight into Nanoparticle Cellular Uptake and Intracellular Targeting J. Controlled Release 2014, 190, 485-499
15. Niu, Y.; Yu, M.; Hartono, S. B.; Yang, J.; Xu, H.; Zhang, H.; Zhang, J.; Zou, J.; Dexter, A.; Gu, W. et al. Nanoparticles Mimicking Viral Surface Topography for Enhanced Cellular Delivery Adv. Mater. 2013, 25, 6233-6237
16. Aoyama, Y.; Kanamori, T.; Nakai, T.; Sasaki, T.; Horiuchi, S.; Sando, S.; Niidome, T. Artificial Viruses and Their Application to Gene Delivery. Size-Controlled Gene Coating with Glycocluster Nanoparticles J. Am. Chem. Soc. 2003, 125, 3455-3457
17. Mastrobattista, E.; van der Aa, A. E. M.; Hennink, W. E.; Crommelin, D. J. A. Artificial Viruses: A Nanotechnological Approach to Gene Delivery Nat. Rev. Drug Discovery 2006, 5, 115-121
18. van Schooneveld, M. M.; Vucic, E.; Koole, R.; Zhou, Y.; Stocks, J.; Cormode, D. P.; Tang, C. Y.; Gordon, R. E.; Nicolay, K.; Meijerink, A. et al. Improved Biocompatibility and Pharmacokinetics of Silica Nanoparticles by Means of a Lipid Coating: A Multimodality Investigation Nano Lett. 2008, 8, 2517-1525
19. Allijin, I. E.; Leong, W.; Tang, J.; Gianella, A.; Mieszawska, A. J.; Fay, F. S.; Ma, G.; Russel, S.; Callo, C. B.; Gordon, R. E. et al. Gold Nanocrystal Labeling Allows Low-Density Lipoprotein Imaging from the SubCellular to Macroscopic Level ACS Nano 2013, 7, 9761-9770
20. Thaxton, C. S.; Daniel, W. L.; Gilijohann, D. A.; Thomas, A. D.; Mirkin, C. A. Templated Spherical High Density Lipoprotein Nanoparticles J. Am. Chem. Soc. 2009, 131, 1384-1385
21. Ashley, C. E.; Carnes, E. C.; Phillips, G. K.; Padilla, D.; Durfee, P. N.; Brown, P. A.; Hanna, T. N.; Liu, J.; Phillips, B.; Carter, M. B. et al. The Targeted Delivery of Multicomponent Cargos to Cancer Cells by Nanoporous Particle-Supported Lipid Bilayers Nat. Mater. 2011, 10, 389-397
22. Yang, J. A.; Murphy, C. J. Evidence for Patchy Lipid Layers on Gold Nanoparticle Surfaces Langmuir 2012, 28, 5404-5416
23. Yu, X.; Feizpour, A.; Ramirez, N.-G. P.; Wu, L.; Akiyama, H.; Gummuluru, S.; Reinhard, B. M. Glycosphingolipid-Functionalized Nanoparticles Recapitulate CD169-dependent HIV-1 Uptake and Trafficking in Dendritic Cells Nat. Commun. 2014, 5, 4136
24. Hartnell, A.; Steel, J.; Turley, H.; Jones, M.; Jackson, D. G.; Crocker, P. R. Characterization of Human Sialoadhesin, a Sialic Acid Binding Receptor Expressed by Resident and Inflammatory Macrophage Populations Blood 2001, 97, 288-298
25. Chan, R.; Uchil, P. D.; Jin, J.; Shui, G.; Ott, D. E.; Mothes, W.; Wenk, M. R. Retroviruses Human Immunodeficiency Virus and Murin Leukemia Virus Are Enriched in Phosphoinositides J. Virol. 2008, 82, 11228-11238
26. Brugger, B.; Glass, B.; Haberkant, P.; Leibrecht, I.; Wieland, F. T.; Kräusslich, H.-G. The HIV Lipidome: A Raft with an Unusual Composition Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 2641-2646
27. Akiyama, H.; Ramirez, N. G.; Gudheti, M. V.; Gummuluru, S. CD169-Mediated Trafficking of HIV to Plasma Membrane Invaginations in Dendritic Cells Attenuates Efficacy of Anti-gp120 Broadly Neutralizing Antibodies PLoS Pathog. 2015, 11, e1004751
28. Izquierdo-Useros, N.; Lorizate, M.; McLaren, P. J.; Telenti, A.; Krausslich, H. G.; Martinez-Picado, J. HIV-1 Capture and Transmission by Dendritic Cells: The Role of Viral Glycolipids and the Cellular Receptor Siglec-1 PLoS Pathog. 2014, 10, e1004146
29. Gummuluru, S.; Ramirez, N.-G. P.; Akiyama, H. CD169-Dependent Cell Associated HIV-1 Transmission: A Driver of Virus Dissemination J. Infect. Dis. 2013, 210 (Suppl. 3) S641-S647
30. Kreibig, U.; Vollmer, M. Optical Properties of Metal Clusters; Springer: Berlin, 1995.
31. Wu, L.; Reinhard, B. M. Probing Subdiffraction Limit Separations with Plasmon Coupling Microscopy: Concepts and Applications Chem. Soc. Rev. 2014, 3884-3897
32. Sonnichsen, C.; Franzl, T.; Wilk, T.; von Plessen, G.; Feldmann, J. Plasmon Resonances in Large Noble-Metal Clusters New J. Phys. 2002, 4, 93.1-93.8
33. Lakadamyali, M.; Rust, M. J.; Babcock, H. P.; Zhuang, X. W. Visualizing Infection of Individual Influenza Viruses Proc. Natl. Acad. Sci. U.S.A. 2003, 100 (16) 9280-9285
34. Brandenburg, B.; Zhuang, X. W. Virus Trafficking-Learning from Single-Virus Tracking Nat. Rev. Microbiol. 2007, 5 (3) 197-208
35. Ewers, H.; Smith, A. E.; Sbalzarini, I. F.; Lilie, H.; Koumoutsakos, P.; Helenius, A. Single-Particle Tracking of Murine Polyoma Virus-like Particles on Live Cells and Artificial Membranes Proc. Natl. Acad. Sci. U.S.A. 2005, 102 (42) 15110-15115
36. Burckhardt, C. J.; Somalainen, M.; Schoenenberger, P.; Boucke, K.; Hemmi, S.; Greber, U. F. Drifting Motions of the Adenovirus Receptor CAR and Immobile Integrins Initiate Virus Uncoating and Membrane Lyctic Protein Exposure Cell Host Microbe 2011, 10, 105-117
37. Sherer, N. M.; Lehmann, M. J.; Jimenez-Soto, L. F.; Horensavitz, C.; Pypaert, M.; Mothes, W. Retroviruses Can Establish Filopodial Bridges for Efficient Cell-to-Cell Transmission Nat. Cell Biol. 2007, 9, 310-315
38. Ferrari, R.; Manfroi, A. J.; Young, W. R. Strongly and Weakly Self-Similar Diffusion Phys. D (Amsterdam, Neth.) 2001, 154, 111-137
39. Sbalzarini, I. F.; Koumoutsakos, P. Feature Point Tracking and Trajectory Analysis for Video Imaging in Cell Biology J. Struct. Biol. 2005, 151, 182-195
40. Schelhaas, M.; Ewers, H.; Rajamaeki, M. L.; Day, P. M.; Schiller, J. T.; Helenius, A. Human Papillomavirus Type 16 Entry: Retrograde Cell Surface Transport along Actin Rich Protrusions PLoS Pathog. 2008, 4, e1000148
41. Chen, T.; Reinhard, B. M. Characterizing the Lateral Friction of Nanoparticles on on-Chip Integrated Black Lipid Membranes Small 2013, 9, 876-884
42. Vaughan, J. C.; Brandenburg, B.; Hogle, J. M.; Zhuang, X. Rapid Actin-Dependent Viral Motility in Live Cells Biophys. J. 2009, 97, 1647-1656
43. Kusumi, A.; Nakada, C.; Ritchie, K.; Murase, K.; Suzuki, K.; Murakoshi, H.; Kasai, R. S.; Kondo, J.; Fujiwara, T. Paradigm Shift of the Plasma Membrane Concept from the Two-Dimensional Continuum Fluid to the Partitioned Fluid: High-Speed Single-Molecule Tracking of Membrane Molecules Annu. Rev. Biophys. Biomol. Struct. 2005, 34, 351-378
44. Saunderson, S. C.; Dunn, A. C.; Crocker, P. R.; McLellan, A. D. CD169 Mediates the Capture of Exosomes in Spleen and Lymph Node Blood 2014, 123, 208-216
45. Wang, J.-H.; Wells, C.; Wu, L. Macropinocytosis and Cytoskeleton Contribute to Dendritic-Mediated HIV-1 Transmission to CD4+ Cells Virology 2008, 381, 143-154
46. Garcia, E.; Pion, M.; Pelchen-Matthews, A.; Collinson, L.; Arrighi, J. F.; Blot, G.; Leuba, F.; Escola, J. M.; Demaurex, N.; Marsh, M. et al. HIV-1 Trafficking to the Dendritic Cell-T-Cell Infectious Synapse Uses a Pathway of Tetraspanin Sorting to the Immunological Synapse Traffic 2005, 6, 488-501
47. Mittelbrunn, M.; Yanez-Mo, M.; Sancho, D.; Ursa, A.; Sanchez-Madrid, F. Cutting Edge: Dynamic Redistribution of Tetraspanin CD81 at the Central Zone of the Immune Synapse in Both T Lymphocytes and APC J. Immunol. 2002, 169, 6691-6695
48. Felts, R. L.; Narayan, K.; Estes, J. D.; Shi, D.; Trubey, C. M.; Fu, J.; Hartnell, L. M.; Ruthel, G. T.; Schneider, D. K.; Nagashima, K. et al. 3D Visualization of HIV Transfer at the Virological Synapse between Dendritic Cells and Tcells Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 13336-13341
49. Miller, M. J.; Safrina, O.; Parker, I.; Cahalan, M. D. Imaging the Single Cell Dynamics of CD4+ T Cell Activation by Dendritic Cells in Lymph Nodes J. Exp. Med. 2004, 200, 847-856
50. Mempel, T. R.; Henrickson, S. E.; von Andrian, U. H. T-Cell Priming by Dendritic Cells in Lymph Nodes Occurs in Three Distinct Phases Nature 2004, 427, 154-159
51. Shakhar, G.; Lindquist, R. L.; Skokos, D.; Dudziak, D.; Huang, J. H.; Nussenzweig, M. C.; Dustin, M. L. Stable T Cell-Dendritic Cell Interactions Precede the Development of Both Tolerance and Immunity in Vivo Nat. Immunol. 2005, 6, 707-714
52. Yu, H. J.; Reuter, M. A.; McDonald, D. HIV Traffics through a Specialized, Surface-Accessible Intracellular Compartments during Trans-infection of T Cells by Mature Dendritic Cells PloS Pathog. 2008, 4, e10000134
53. Rong, G.; Wang, H.; Reinhard, B. M. Insights from a Nanoparticle Minuet: Two-Dimensional Membrane Profiling through Silver Plasmon Rulers Nano Lett. 2010, 10, 230-238
54. Wiley, R. D.; Gummuluru, S. Immature Dendritic Cell-Derived Exosomes Can Mediate HIV-1 Trans-infection Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 738-743