Gold nanoparticles as a vaccine platform: Influence of size and shape on immunological responses in vitro and in vivo

ACS Nano

Volumn 7, Issue 5, 2013, Pages 3926-3938

  Niikura, Kenichi ^a   Matsunaga, Tatsuya ^a   Suzuki, Tadaki ^b   Kobayashi, Shintaro ^a   Yamaguchi, Hiroki ^a   Orba, Yasuko ^a   Kawaguchi, Akira ^b   Hasegawa, Hideki ^b   Kajino, Kiichi ^a   Ninomiya, Takafumi ^c   Ijiro, Kuniharu ^a   Sawa, Hirofumi ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^c SAPPORO MEDICAL UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

antibody; colloid; cytokine; gold nanoparticle; shape dependence; vaccine; west nile virus

Indexed keywords

CYTOKINE PRODUCTION; CYTOKINES; GOLD NANOPARTICLES; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTORS; IMMUNOLOGICAL RESPONSE; SHAPE DEPENDENCE; TUMOR NECROSIS FACTORS; WEST NILE VIRUS;

COLLOIDS; GOLD; MACROPHAGES; METAL NANOPARTICLES; PHYSIOLOGY; SPHERES; VACCINES;

ANTIBODIES;

CYTOKINE; DRUG CARRIER; GOLD; METAL NANOPARTICLE; VACCINE; VIRUS ENVELOPE PROTEIN;

ANIMAL; ARTICLE; BIOSYNTHESIS; BONE MARROW CELL; CELL LINE; CHEMISTRY; CYTOLOGY; DENDRITIC CELL; DRUG STABILITY; FEMALE; IMMUNOLOGY; INTRACELLULAR SPACE; MACROPHAGE; METABOLISM; MOUSE; PARTICLE SIZE; PROTEIN TRANSPORT; STRUCTURE ACTIVITY RELATION; VACCINATION; WEST NILE FLAVIVIRUS;

ANIMALS; BONE MARROW CELLS; CELL LINE; CYTOKINES; DENDRITIC CELLS; DRUG CARRIERS; DRUG STABILITY; FEMALE; GOLD; INTRACELLULAR SPACE; MACROPHAGES; METAL NANOPARTICLES; MICE; PARTICLE SIZE; PROTEIN TRANSPORT; STRUCTURE-ACTIVITY RELATIONSHIP; VACCINATION; VACCINES; VIRAL ENVELOPE PROTEINS; WEST NILE VIRUS;

EID: 84878326767     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn3057005     Document Type: Article

References (63)

1. Harris, J. R.; Markl, J. Keyhole Limpet Hemocyanin (KLH): A Biomedical Review Micron 1999, 30, 597-623
2. Ragupathi, G.; Meyers, M.; Adluri, S.; Howard, L.; Musselli, C.; Livingston, P. O. Induction of Antibodies against GD3 Ganglioside in Melanoma Patients by Vaccination with GD3-Lactone-KLH Conjugate Plus Immunological Adjuvant QS-21 Int. J. Cancer 2000, 85, 659-666
3. Hou, Y.; Gu, X. X. Development of Peptide Mimotopes of Lipooligosaccharide from Nontypeable Haemophilus influenza as Vaccine Candidates J. Immunol. 2003, 170, 4373-4379
4. May, R. J.; Beenhouwer, D. O.; Scharff, M. D. Antibodies to Keyhole Limpet Homecyanin Cross-React with an Epitope on the Polysaccharide Capsule of Cryptococcus neoformans and Other Carbohydrates: Implications for Vaccine Development J. Immunol. 2003, 171, 4905-4912
5. Gharavi, A. E.; Pierangeli, S. S.; Stanfield, M. C.; Liu, X. W.; Espinola, R. G.; Harris, E. N. GDKV-Induced Antiphospholipid Antibodies Enhance Thrombosis and Activate Endothelial Cells in Vivo and in Vitro J. Immunol. 1999, 163, 2922-2927
6. Chen, Y. S.; Hung, Y. C.; Lin, W. H.; Huang, G. S. Assessment of Gold Nanoparticles as a Size-Dependent Vaccine Carrier for Enhancing the Antibody Response against Synthetic Foot-and-Mouth Disease Virus Peptide Nanotechnology 2010, 21, 195101-1951018
7. Rana, S.; Bajaj, A.; Mout, R.; Rotello, V. M. Monolayer Coated Gold Nanoparticles for Delivery Applications Adv. Drug Delivery Rev. 2012, 64, 200-216
8. De, M.; Ghosh, P. S.; Rotello, V. M. Applications of Nanoparticles in Biology Adv. Mater. 2008, 20, 4225-4241
9. Bastús, N. G.; Sánchez-Tilló, E.; Pujals, S.; Farrera, C.; López, C.; Giralt, E.; Celada, A.; Lloberas, J.; Puntes, V. Homogeneous Conjugation of Peptides onto Gold Nanoparticles Enhances Macrophage Response ACS Nano 2009, 3, 1335-1344
10. Shukla, R.; Bansal, V.; Chaudhary, M.; Basu, A.; Bhonde, R. R.; Sastry, M. Biocompatibility of Gold Nanoparticles and Their Endocytotic Fate Inside the Cellular Compartment: A Microscopic Overview Langmuir 2005, 21, 10644-10654
11. Dykman, L.; Khlebtsov, N. Gold Nanoparticles in Biomedical Applications: Recent Advances and Perspectives Chem. Soc. Rev. 2013, 41, 2256-2282
12. Perrault, S. D.; Chan, W. C. W. Synthesis and Surface Modification of Highly Monodispersed, Spherical Gold Nanoparticles of 50-200 nm J. Am. Chem. Soc. 2009, 131, 17042-17043
13. Sau, T. K.; Murphy, C. J. Room Temperature, High-Yield Synthesis of Multiple Shapes of Gold Nanoparticles in Aqueous Solution J. Am. Chem. Soc. 2004, 126, 8648-8649
14. Shiosaka, S.; Kiyami, H.; Wanaka, A.; Tohyama, M. A New Method for Producing a Specific and High Titre Antibody against Glutamate Using Colloidal Gold as a Carrier Brain Res. 1986, 382, 399-403
15. Chen, Y. S.; Hung, Y. C.; Liau, I.; Huang, G. S. Assessment of the In Vivo Toxicity of Gold Nanoparticles Nanoscale Res. Lett. 2009, 4, 858-864
16. Jiang, W.; Kim, B. Y. S.; Rutka, J. T.; Chan, W. C. W. Nanoparticle-Mediated Cellular Response Is Size-Dependent Nat. Nanotechnol. 2008, 3, 145-150
17. Mottram, P. L.; Leong, D.; Irwin, B. C.; Gloster, S.; Xiang, S. D.; Meanger, J.; Ghildyal, R.; Vardaxis, N.; Plebanski, M. Type 1 and 2 Immunity Following Vaccination Is Influenced by Nanoparticle Size: Formulation of a Model Vaccine for Respiratory Syncytial Virus Mol. Pharmaceutics 2007, 4, 73-84
18. Wang, Y. T.; Lu, X. M.; Zhu, F.; Huang, P.; Yu, Y.; Zeng, L.; Long, Z. Y.; Wu, Y. M. The Use of a Gold Nanoparticle-Based Adjuvant To Improve the Therapeutic Efficacy of hNgR-Fc Protein Immunization in Spinal Cord-Injured Rats Biomaterials 2011, 32, 7988-7998
19. Banchereau, J.; Briere, F.; Caux, C.; Davoust, J.; Lebecque, S.; Liu, Y. J.; Pulendran, B.; Palucka, K. Immunobiology of Dendritic Cells Annu. Rev. Immunol. 2000, 18, 767-811
20. Janeway, C. A., Jr.; Medzhitov, R. Innate Immune Recognition Annu. Rev. Immunol. 2002, 20, 197-216
21. Hubbell, J. A.; Thomas, S. N.; Swartz, M. A. Materials Engineering for Immunomodulation Nature 2009, 462, 449-460
22. Yen, H. J.; Hsu, S. H.; Tsai, C. L. Cytotoxicity and Immunological Response of Gold and Silver Nanoparticles of Different Sizes Small 2009, 5, 1553-1561
23. Hutter, E.; Boridy, S.; Labrecque, S.; Hebert, M. L.; Kriz, J.; Winnik, F. M.; Maysinger, D. Microglial Response to Gold Nanoparticles ACS Nano 2010, 4, 2595-2606
24. Dauphin, G.; Zientara, S. West Nile Virus: Recent Trends in Diagnosis and Vaccine Development Vaccine 2007, 25, 5563-5576
25. Chithrani, B. D.; Chan, W. C. W. Elucidating the Mechanism of Cellular Uptake and Removal of Protein-Coated Gold Nanoparticles of Different Sizes and Shapes Nano Lett. 2007, 7, 1542-1550
26. Fifis, T.; Gamvrellis, A.; Irwin, B. C.; Pietersz, G. A.; Li, J.; Mottram, P. L.; Mckenzie, I. F. C.; Plebanski, M. Size-Dependent Immunogenicity: Therapeutic and Protective Properties of Nano-Vaccines against Tumors J. Immunol. 2004, 173, 3148-3154
27. Chithrani, B. D.; Ghazani, A. A.; Chan, W. C. W. Determining the Size and Shape Dependence of Gold Nanoparticle Uptake into Mammalian Cells Nano Lett. 2006, 6, 662-668
28. Mukhopadhyay, S.; Kim, B. S.; Chipman, P. R.; Rossmann, M. G.; Kuhn, R. J. Structure of West Nile Virus Science 2003, 302, 248
29. Chen, H.; Kou, X.; Yang, Z.; Ni, W.; Wang, J. Shape- and Size-Dependent Refractive Index Sensitivity of Gold Nanoparticles Langmuir 2008, 24, 5233-5237
30. Gole, A.; Murphy, C. J. Azide-Derivatized Gold Nanorods: Functional Materials for "Click" Chemistry Langmuir 2008, 24, 266-272
31. Kanai, R.; Kar, K.; Anthony, K.; Gould, L. H.; Ledizet, M.; Fikrig, E.; Marasco, W. A.; Koski, R. A.; Modis, Y. Crystal Structure of West Nile Virus Envelope Glycoprotein Reveals Viral Surface Epitopes J. Virol. 2006, 80, 11000-11008
32. Walkey, C. D.; Chan, W. C. W. Understanding and Controlling the Interaction of Nanomaterials with Proteins in a Physiological Environment Chem. Soc. Rev. 2012, 41, 2780-2799
33. Casal, E.; Pfaller, T.; Duschl, A.; Oostingh, G. J.; Puntes, V. Time Evolution of the Nanoparticle Protein Corona ACS Nano 2010, 4, 3623-3632
34. Monopoli, M.; Åberg, C.; Salvati, A.; Dawson, K. A. Biomolecular Coronas Provide the Biological Identity of Nanosized Materials Nat. Nanotechnol. 2012, 7, 779-786
35. Maiorano, G.; Sabella, S.; Sorce, B.; Brunetti, V.; Malvindi, M. A.; Cingolani, R.; Pompa, P. P. Effects of Cell Culture Media on the Dynamic Formation of Protein-Nanoparticle Complexes and Influence on the Cellular Response ACS Nano 2010, 4, 7481-7491
36. Gil, P. R.; Oberdörster, G.; Elder, A.; Puntes, V.; Parak, W. J. Correlating Physico-Chemical with Toxicological Properties of Nanoparticles: The Present and the Future ACS Nano 2010, 4, 5527-5531
37. Ohatki, N.; Takahashi, H.; Kaneko, K.; Gomi, Y.; Ishikawa, T.; Higashi, Y.; Kurata, T.; Sata, T.; Kojima, A. Immunogenicity and Efficacy of Two Types of West Nile Virus-like Particles Different in Size and Maturation as a Second-Generation Vaccine Candidate Vaccine 2010, 28, 6588-6596
38. Raschke, W. C.; Baird, S.; Ralph, P.; Nakoinz, I. Functional Macrophage Cell Lines Transformed by Abelson Leukemia Virus Cell 1978, 15, 261-267
39. Hauck, T. S.; Ghazani, A. A.; Chan, W. C. W. Assessing the Effect of Surface Chemistry on Gold Nanorod Uptake, Toxicity, and Gene Expression in Mammalian Cells Small 2008, 4, 153-159
40. Walkey, C. D.; Olsen, J. B.; Guo, H.; Emili, A.; Chan, W. C. W. Nanoparticle Size and Surface Chemistry Determine Serum Protein Adsorption and Macrophage Uptake J. Am. Chem. Soc. 2012, 134, 2139-2147
41. Arnida; Janát-Amsbury, M. M.; Ray, A.; Peterson, C. M.; Ghandehari, H. Geometry and Surface Characteristics of Gold Nanoparticles Influence Their Biodistribution and Uptake by Macrophages Eur. J. Pharm. Biopharm. 2011, 77, 417-423
42. Vácha, R.; Martinez-Veracoechaea, F. J.; Frenkel, D. Receptor-Mediated Endocytosis of Nanoparticles of Various Shapes Nano Lett. 2011, 11, 5391-5395
43. Ghiringhelli, F.; Apetoh, L.; Tesniere, A.; Aymeric, L.; Ma, Y.; Ortiz, C.; Vermaelen, K.; Panaretakis, T.; Mignot, G.; Ullrich, E. et al. Activation of the NLRP3 Inflammasome in Dendritic Cells Induces IL-1β-Dependent Adaptive Immunity against Tumors Nat. Med. 2009, 15, 1170-1178
44. Martinon, F.; Mayor, A.; Tschopp, J. The Inflammasomes: Guardians of the Body Annu. Rev. Immunol. 2009, 27, 229-265
45. Lunov, O.; Syrovets, T.; Loos, C.; Nienhaus, G. U.; Mailänder, V.; Landfester, K.; Rouis, M.; Simmet, T. Amino-Functionalized Polystyrene Nanoparticles Activate the NLRP3 Inflammasome in Human Macrophages ACS Nano 2011, 5, 9648-9657
46. Yang, E. J.; Kim, S.; Kim, J. S.; Choi, I. H. Inflammasome Formation and IL-1β Release by Human Blood Monocytes in Response to Silver Nanoparticles Biomaterials 2012, 33, 6858-6867
47. Hornung, V.; Bauernfeind, F.; Halle, A.; Samstad, E. O.; Kono, H.; Rock, K. L.; Fitzgerald, K. A.; Latz, E. Silica Crystals and Aluminum Salts Activate the NALP3 Inflammasome through Phagosomal Destabilization Nat. Immunol. 2008, 9, 847-856
48. Vácha, R.; Martinez-Veracoechaea, F. J.; Frenkel, D. Intracellular Release of Endocytosed Nanoparticles upon a Change of Ligand-Receptor Interaction ACS Nano 2012, 6, 10598-10605
49. Dinarello, C. A. Biologic Basis for Interleukin-1 in Disease Blood 1996, 87, 2095-2147
50. Zhou, R.; Yazdi, A. S.; Menu, P.; Tschopp, J. A Role for Mitochondria in NLRP3 Inflammasome Activation Nat. Immunol. 2011, 12, 199-200
51. Eisenbarth, S. C.; Colegio, O. R.; O'Connor, W., Jr.; Sutterwala, F. S.; Flavell, R. A. Crucial Role for the Nalp3 Inflammasome in the Immunostimulatory Properties of Aluminium Adjuvants Nature 2008, 453, 1122-1126
52. Li, H.; Willingham, S. B.; Ting, J. P. Y.; Re, F. Cutting Edge: Inflammasome Activation by Alum and Alum's Adjuvant Effect are Mediated by NLRP3 J. Immunol. 2008, 181, 17-21
53. Wickliffe, K. E.; Leppla, S. H.; Moayeri, M. Anthrax Lethal Toxin-Induced Inflammasome Formation and Caspase-1 Activation Are Late Events Dependent on Ion Fluxes and the Proteasome Cell. Microbiol. 2008, 10, 332-343
54. Wajant, H.; Pfizenmaier, K.; Scheurich, P. Tumor Necrosis Factor Signaling Cell Death Differ. 2003, 10, 45-65
55. Franchi, L.; Núñez, G. The Nlrp3 Inflammasome Is Critical for Aluminiumhydroxide-Mediated IL-1β Secretion but Dispensable for Adjuvant Activity Eur. J. Immunol. 2008, 38, 2085-2089
56. Bon, A. L.; Schiavoni, G.; D'Agostin, G.; Gresser, I.; Belardelli, F.; Tough, D. F. Type I Interferons Potently Enhance Humoral Immunity and Can Promote Isotype Switching by Stimulating Dendritic Cells in Vivo Immunity 2001, 14, 461-470
57. Thakor, A. S.; Jokerst, J.; Zavaleta, C.; Massoud, T. F.; Gambhir, S. S. Gold Nanoparticles: A Revival in Precious Metal Administration to Patients Nano Lett. 2011, 11, 4029-4036
58. Alkilany, A. M.; Lohse, S. E.; Murphy, C. J. The Gold Standard: Gold Nanoparticle Libraries To Understand the Nano-Bio Interface Acc. Chem. Res. 2013, 46, 650-661
59. Alkilany, A. M.; Murphy, C. J. Toxicity and Cellular Uptake of Gold Nanoparticles: What We Have Learned So Far? J. Nanopart. Res. 2010, 12, 2313-2333
60. Zhou, C.; Long, M.; Qin, Y.; Sun, X.; Zheng, J. Luminescent Gold Nanoparticles with Efficient Renal Clearance Angew. Chem., Int. Ed. 2011, 50, 3168-3172
61. Sharp, F. A.; Ruane, D.; Claass, B.; Creagh, E.; Harris, J.; Malyala, P.; Singh, M.; O'Hagan, D. T.; Pétrilli, V.; Tschopp, J. et al. Uptake of Particulate Vaccine Adjuvants by Dendritic Cells Activates the NALP3 Inflammasome Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 870-875
62. Inaba, K.; Inaba, M.; Romani, N.; Aya, H.; Deguchi, M.; Ikehara, S.; Muramatsu, S.; Steinman, R. M. Generation of Large Numbers of Dendritic Cells from Mouse Bone Marrow Cultures Supplemented with Granulocyte/Macrophage Colony-Stimulating Factor J. Exp. Med. 1992, 176, 1693-1702
63. Kajino, K.; Nakamura, I.; Bamba, H.; Sawai, T.; Ogasawara, K. Involvement of IL-10 in Exhaustion of Myeloid Dendritic Cells and Rescue by CD40 Stimulation Immunology 2007, 120, 28-37