Orchestrating immune responses: How size, shape and rigidity affect the immunogenicity of particulate vaccines

Journal of Controlled Release

Volumn 234, Issue , 2016, Pages 124-134

  Benne, Naomi ^a   van Duijn, Janine ^a   Kuiper, Johan ^a   Jiskoot, Wim ^a   Slütter, Bram ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

Author keywords

Microparticle; Nanoparticle; Rigidity; T cells; Vaccination

Indexed keywords

ANTIGENS; CELLS; CRASHWORTHINESS; CYTOLOGY; NANOPARTICLES; PARTICLE SIZE; RIGIDITY; T-CELLS; VACCINES;

ANTIGEN PRESENTING CELLS; ANTIGEN PROCESSING; DRUG DELIVERY VEHICLES; MICRO PARTICLES; MULTIPLE PROCESS; PHYSICOCHEMICAL CHARACTERISTICS; T-CELL RESPONSE; VACCINATION;

IMMUNE SYSTEM;

VACCINE; DRUG CARRIER; NANOPARTICLE;

ANTIGEN PRESENTATION; DRUG DESIGN; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOGENICITY; IMMUNOSTIMULATION; LYMPHOID TISSUE; NONHUMAN; PARTICLE SIZE; PARTICULATE MATTER; PATHOGENESIS; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; REVIEW; RIGIDITY; SYSTEMATIC REVIEW; T LYMPHOCYTE; ANIMAL; CHEMISTRY; HUMAN; IMMUNOLOGY; SURFACE PROPERTY;

ANIMALS; ANTIGEN PRESENTATION; DRUG CARRIERS; HUMANS; NANOPARTICLES; PARTICLE SIZE; SURFACE PROPERTIES; VACCINES;

EID: 84982179547     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2016.05.033     Document Type: Review

References (103)

1. [1] Smith, K.A., Smallpox: can we still learn from the journey to eradication?. Indian J. Med. Res. 137 (2013), 895–899.
2. [2] Milstien, J.B., Gibson, J.J., Quality control of BCG vaccine by WHO: a review of factors that may influence vaccine effectiveness and safety. Bull. World Health Organ. 68 (1990), 93–108.
3. [3] Guillot, S., Caro, V., Cuervo, N., Korotkova, E., Combiescu, M., Persu, A., Aubert-Combiescu, A., Delpeyroux, F., Crainic, R., Natural genetic exchanges between vaccine and wild poliovirus strains in humans. J. Virol. 74 (2000), 8434–8443.
4. [4] Donnelly, S., Loscher, C.E., Lynch, M.A., Mills, K.H., Whole-cell but not acellular pertussis vaccines induce convulsive activity in mice: evidence of a role for toxin-induced interleukin-1beta in a new murine model for analysis of neuronal side effects of vaccination. Infect. Immun. 69 (2001), 4217–4223.
5. [5] Murphy, T.V., Gargiullo, P.M., Massoudi, M.S., Nelson, D.B., Jumaan, A.O., Okoro, C.A., Zanardi, L.R., Setia, S., Fair, E., LeBaron, C.W., Schwartz, B., Wharton, M., Livingood, J.R., Intussusception among infants given an oral rotavirus vaccine. N. Engl. J. Med. 344 (2001), 564–572.
6. [6] Cherkasova, E.A., Korotkova, E.A., Yakovenko, M.L., Ivanova, O.E., Eremeeva, T.P., Chumakov, K.M., Agol, V.I., Long-term circulation of vaccine-derived poliovirus that causes paralytic disease. J. Virol. 76 (2002), 6791–6799.
7. [7] Moyle, P.M., Toth, I., Modern subunit vaccines: development, components, and research opportunities. ChemMedChem 8 (2013), 360–376.
8. [8] Slutter, B., Soema, P.C., Ding, Z., Verheul, R., Hennink, W., Jiskoot, W., Conjugation of ovalbumin to trimethyl chitosan improves immunogenicity of the antigen. J. Control. Release 143 (2010), 207–214.
9. [9] O'Hagan, D.T., Singh, M., Microparticles as vaccine adjuvants and delivery systems. Expert Rev. Vaccines 2 (2003), 269–283.
10. [10] Sharp, F.A., Ruane, D., Claass, B., Creagh, E., Harris, J., Malyala, P., Singh, M., O'Hagan, D.T., Petrilli, V., Tschopp, J., O'Neill, L.A., Lavelle, E.C., Uptake of particulate vaccine adjuvants by dendritic cells activates the NALP3 inflammasome. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 870–875.
11. [11] De Temmerman, M.-L., Rejman, J., Demeester, J., Irvine, D.J., Gander, B., De Smedt, S.C., Particulate vaccines: on the quest for optimal delivery and immune response. Drug Discov. Today 16 (2011), 569–582.
12. [12] Brewer, J.M., Pollock, K.G., Tetley, L., Russell, D.G., Vesicle size influences the trafficking, processing, and presentation of antigens in lipid vesicles. J. Immunol. 173 (2004), 6143–6150.
13. [13] Vila, A., Sanchez, A., Evora, C., Soriano, I., McCallion, O., Alonso, M.J., PLA-PEG particles as nasal protein carriers: the influence of the particle size. Int. J. Pharm. 292 (2005), 43–52.
14. [14] Shakweh, M., Besnard, M., Nicolas, V., Fattal, E., Poly (lactide-co-glycolide) particles of different physicochemical properties and their uptake by Peyer's patches in mice. Eur. J. Pharm. Biopharm. 61 (2005), 1–13.
15. [15] Cohen, J.A., Beaudette, T.T., Tseng, W.W., Bachelder, E.M., Mende, I., Engleman, E.G., Frechet, J.M., T-cell activation by antigen-loaded pH-sensitive hydrogel particles in vivo: the effect of particle size. Bioconjug. Chem. 20 (2009), 111–119.
16. [16] Kumar, S., Anselmo, A.C., Banerjee, A., Zakrewsky, M., Mitragotri, S., Shape and size-dependent immune response to antigen-carrying nanoparticles. J. Control. Release, 2015.
17. [17] Gratton, S.E., Pohlhaus, P.D., Lee, J., Guo, J., Cho, M.J., Desimone, J.M., Nanofabricated particles for engineered drug therapies: a preliminary biodistribution study of PRINT nanoparticles. J. Control. Release 121 (2007), 10–18.
18. [18] Nakano, K., Tozuka, Y., Yamamoto, H., Kawashima, Y., Takeuchi, H., A novel method for measuring rigidity of submicron-size liposomes with atomic force microscopy. Int. J. Pharm. 355 (2008), 203–209.
19. [19] Best, J.P., Cui, J., Mullner, M., Caruso, F., Tuning the mechanical properties of nanoporous hydrogel particles via polymer cross-linking. Langmuir 29 (2013), 9824–9831.
20. [20] Sun, H., Wong, E.H.H., Yan, Y., Cui, J., Dai, Q., Guo, J., Qiao, G.G., Caruso, F., The role of capsule stiffness on cellular processing. Chem. Sci. 6 (2015), 3505–3514.
21. [21] Albanese, A., Tang, P.S., Chan, W.C., The effect of nanoparticle size, shape, and surface chemistry on biological systems. Annu. Rev. Biomed. Eng. 14 (2012), 1–16.
22. [22] Watson, D.S., Endsley, A.N., Huang, L., Design considerations for liposomal vaccines: influence of formulation parameters on antibody and cell-mediated immune responses to liposome associated antigens. Vaccine 30 (2012), 2256–2272.
23. [23] Wang, J., Byrne, J.D., Napier, M.E., DeSimone, J.M., More effective nanomedicines through particle design. Small 7 (2011), 1919–1931.
24. [24] Geijtenbeek, T.B.H., Gringhuis, S.I., Signalling through C-type lectin receptors: shaping immune responses. Nat. Rev. Immunol. 9 (2009), 465–479.
25. [25] Kawai, T., Akira, S., The role of pattern-recognition receptors in innate immunity: update on toll-like receptors. Nat. Immunol. 11 (2010), 373–384.
26. [26] Alving, C.R., Liposomes as carriers of antigens and adjuvants. J. Immunol. Methods 140 (1991), 1–13.
27. [27] Zaks, K., Jordan, M., Guth, A., Sellins, K., Kedl, R., Izzo, A., Bosio, C., Dow, S., Efficient immunization and cross-priming by vaccine adjuvants containing TLR3 or TLR9 agonists complexed to cationic liposomes. J. Immunol. 176 (2006), 7335–7345.
28. [28] Smith, D.M., Simon, J.K., Baker, J.R. Jr., Applications of nanotechnology for immunology. Nat. Rev. Immunol. 13 (2013), 592–605.
29. [29] Moon, J.J., Huang, B., Irvine, D.J., Engineering nano- and microparticles to tune immunity. Adv. Mater. 24 (2012), 3724–3746.
30. [30] Kamaly, N., Xiao, Z., Valencia, P.M., Radovic-Moreno, A.F., Farokhzad, O.C., Targeted polymeric therapeutic nanoparticles: design, development and clinical translation. Chem. Soc. Rev. 41 (2012), 2971–3010.
31. [31] Moyer, T.J., Zmolek, A.C., Irvine, D.J., Beyond antigens and adjuvants: formulating future vaccines. J. Clin. Invest. 126 (2016), 799–808.
32. [32] Banchereau, J., Steinman, R.M., Dendritic cells and the control of immunity. Nature 392 (1998), 245–252.
33. [33] von Andrian, U.H., Mempel, T.R., Homing and cellular traffic in lymph nodes. Nat. Rev. Immunol. 3 (2003), 867–878.
34. [34] Reddy, S.T., van der Vlies, A.J., Simeoni, E., Angeli, V., Randolph, G.J., O'Neil, C.P., Lee, L.K., Swartz, M.A., Hubbell, J.A., Exploiting lymphatic transport and complement activation in nanoparticle vaccines. Nat. Biotechnol. 25 (2007), 1159–1164.
35. [35] Reddy, S.T., Rehor, A., Schmoekel, H.G., Hubbell, J.A., Swartz, M.A., In vivo targeting of dendritic cells in lymph nodes with poly(propylene sulfide) nanoparticles. J. Control. Release 112 (2006), 26–34.
36. [36] Manolova, V., Flace, A., Bauer, M., Schwarz, K., Saudan, P., Bachmann, M.F., Nanoparticles target distinct dendritic cell populations according to their size. Eur. J. Immunol. 38 (2008), 1404–1413.
37. [37] Martín-Fontecha, A., Sebastiani, S., Höpken, U.E., Uguccioni, M., Lipp, M., Lanzavecchia, A., Sallusto, F., Regulation of dendritic cell migration to the draining lymph node: impact on T lymphocyte traffic and priming. J. Exp. Med. 198 (2003), 615–621.
38. [38] Oussoren, C., Zuidema, J., Crommelin, D.J., Storm, G., Lymphatic uptake and biodistribution of liposomes after subcutaneous injection. II. Influence of liposomal size, lipid compostion and lipid dose. Biochim. Biophys. Acta 1328 (1997), 261–272.
39. [39] Oussoren, C., Velinova, M., Scherphof, G., van der Want, J.J., van Rooijen, N., Storm, G., Lymphatic uptake and biodistribution of liposomes after subcutaneous injection. IV. Fate of liposomes in regional lymph nodes. Biochim. Biophys. Acta 1370 (1998), 259–272.
40. [40] Merad, M., Sathe, P., Helft, J., Miller, J., Mortha, A., The dendritic cell lineage: ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Annu. Rev. Immunol., 31, 2013, 10.1146/annurev-immunol-020711-074950.
41. [41] Tabata, Y., Inoue, Y., Ikada, Y., Size effect on systemic and mucosal immune responses induced by oral administration of biodegradable microspheres. Vaccine 14 (1996), 1677–1685.
42. [42] Jani, P., Halbert, G.W., Langridge, J., Florence, A.T., The uptake and translocation of latex nanospheres and microspheres after oral administration to rats. J. Pharm. Pharmacol. 41 (1989), 809–812.
43. [43] Desai, M.P., Labhasetwar, V., Amidon, G.L., Levy, R.J., Gastrointestinal uptake of biodegradable microparticles: effect of particle size. Pharm. Res. 13 (1996), 1838–1845.
44. [44] Schroeder, H.W., Cavacini, L., Structure and function of immunoglobulins. J. Allergy Clin. Immunol. 125 (2010), S41–S52.
45. [45] Jung, T., Kamm, W., Breitenbach, A., Hungerer, K.D., Hundt, E., Kissel, T., Tetanus toxoid loaded nanoparticles from sulfobutylated poly(vinyl alcohol)-graft-poly(lactide-co-glycolide): evaluation of antibody response after oral and nasal application in mice. Pharm. Res. 18 (2001), 352–360.
46. [46] Slütter, B., Bal, S.M., Que, I., Kaijzel, E., Löwik, C., Bouwstra, J., Jiskoot, W., Antigen–adjuvant nanoconjugates for nasal vaccination: an improvement over the use of nanoparticles?. Mol. Pharm. 7 (2010), 2207–2215.
47. [47] Mellman, I., Steinman, R.M., Dendritic cells: specialized and regulated antigen processing machines. Cell 106 (2001), 255–258.
48. [48] Trombetta, E.S., Mellman, I., Cell biology of antigen processing in vitro and in vivo. Annu. Rev. Immunol. 23 (2005), 975–1028.
49. [49] Joshi, V.B., Geary, S.M., Salem, A.K., Biodegradable particles as vaccine delivery systems: size matters. AAPS J. 15 (2013), 85–94.
50. [50] Mathaes, R., Winter, G., Siahaan, T.J., Besheer, A., Engert, J., Influence of particle size, an elongated particle geometry, and adjuvants on dendritic cell activation. Eur. J. Pharm. Biopharm. 94 (2015), 542–549.
51. [51] Foged, C., Brodin, B., Frokjaer, S., Sundblad, A., Particle size and surface charge affect particle uptake by human dendritic cells in an in vitro model. Int. J. Pharm. 298 (2005), 315–322.
52. [52] Shima, F., Uto, T., Akagi, T., Baba, M., Akashi, M., Size effect of amphiphilic poly(γ-glutamic acid) nanoparticles on cellular uptake and maturation of dendritic cells in vivo. Acta Biomater. 9 (2013), 8894–8901.
53. [53] Blank, F., Stumbles, P.A., Seydoux, E., Holt, P.G., Fink, A., Rothen-Rutishauser, B., Strickland, D.H., von Garnier, C., Size-dependent uptake of particles by pulmonary antigen-presenting cell populations and trafficking to regional lymph nodes. Am. J. Respir. Cell Mol. Biol. 49 (2013), 67–77.
54. [54] le Guével, X., Palomares, F., Torres, M.J., Blanca, M., Fernandez, T.D., Mayorga, C., Nanoparticle size influences the proliferative responses of lymphocyte subpopulations. RSC Adv. 5 (2015), 85305–85309.
55. [55] Kanchan, V., Panda, A.K., Interactions of antigen-loaded polylactide particles with macrophages and their correlation with the immune response. Biomaterials 28 (2007), 5344–5357.
56. [56] Thomas, C., Gupta, V., Ahsan, F., Particle size influences the immune response produced by hepatitis B vaccine formulated in inhalable particles. Pharm. Res. 27 (2010), 905–919.
57. [57] Janeway, C.A. Jr., Medzhitov, R., Innate immune recognition. Annu. Rev. Immunol. 20 (2002), 197–216.
58. [58] Villadangos, J.A., Schnorrer, P., Intrinsic and cooperative antigen-presenting functions of dendritic-cell subsets in vivo. Nat. Rev. Immunol. 7 (2007), 543–555.
59. [59] Varkouhi, A.K., Scholte, M., Storm, G., Haisma, H.J., Endosomal escape pathways for delivery of biologicals. J. Control. Release 151 (2011), 220–228.
60. [60] Mant, A., Chinnery, F., Elliott, T., Williams, A.P., The pathway of cross-presentation is influenced by the particle size of phagocytosed antigen. Immunology 136 (2012), 163–175.
61. [61] Silva, A.L., Rosalia, R.A., Varypataki, E., Sibuea, S., Ossendorp, F., Jiskoot, W., Poly-(lactic-co-glycolic-acid)-based particulate vaccines: particle uptake by dendritic cells is a key parameter for immune activation. Vaccine 33 (2015), 847–854.
62. [62] Seydoux, E., Rothen-Rutishauser, B., Nita, I.M., Balog, S., Gazdhar, A., Stumbles, P.A., Petri-Fink, A., Blank, F., von Garnier, C., Size-dependent accumulation of particles in lysosomes modulates dendritic cell function through impaired antigen degradation. Int. J. Nanomedicine 9 (2014), 3885–3902.
63. [63] Nolz, J.C., Molecular mechanisms of CD8 + T cell trafficking and localization. Cell. Mol. Life Sci. 72 (2015), 2461–2473.
64. [64] Tscharke, D.C., Croft, N.P., Doherty, P.C., La Gruta, N.L., Sizing up the key determinants of the CD8 + T cell response. Nat. Rev. Immunol. 15 (2015), 705–716.
65. [65] Geginat, J., Paroni, M., Facciotti, F., Gruarin, P., Kastirr, I., Caprioli, F., Pagani, M., Abrignani, S., The CD4-centered universe of human T cell subsets. Semin. Immunol. 25 (2013), 252–262.
66. [66] Mottram, P.L., Leong, D., Crimeen-Irwin, B., 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. Pharm. 4 (2007), 73–84.
67. [67] Fifis, T., Gamvrellis, A., Crimeen-Irwin, B., Pietersz, G.A., Li, J., Mottram, P.L., McKenzie, I.F., Plebanski, M., Size-dependent immunogenicity: therapeutic and protective properties of nano-vaccines against tumors. J. Immunol. 173 (2004), 3148–3154.
68. [68] Li, X., Sloat, B.R., Yanasarn, N., Cui, Z., Relationship between the size of nanoparticles and their adjuvant activity: data from a study with an improved experimental design. Eur. J. Pharm. Biopharm. 78 (2011), 107–116.
69. [69] Mann, J.F., Shakir, E., Carter, K.C., Mullen, A.B., Alexander, J., Ferro, V.A., Lipid vesicle size of an oral influenza vaccine delivery vehicle influences the Th1/Th2 bias in the immune response and protection against infection. Vaccine 27 (2009), 3643–3649.
70. [70] Henriksen-Lacey, M., Devitt, A., Perrie, Y., The vesicle size of DDA:TDB liposomal adjuvants plays a role in the cell-mediated immune response but has no significant effect on antibody production. J. Control. Release 154 (2011), 131–137.
71. [71] Tran, K.K., Shen, H., The role of phagosomal pH on the size-dependent efficiency of cross-presentation by dendritic cells. Biomaterials 30 (2009), 1356–1362.
72. [72] Huang, X., Li, L., Liu, T., Hao, N., Liu, H., Chen, D., Tang, F., The shape effect of mesoporous silica nanoparticles on biodistribution, clearance, and biocompatibility in vivo. ACS Nano 5 (2011), 5390–5399.
73. [73] Geng, Y., Dalhaimer, P., Cai, S., Tsai, R., Tewari, M., Minko, T., Discher, D.E., Shape effects of filaments versus spherical particles in flow and drug delivery. Nat. Nanotechnol. 2 (2007), 249–255.
74. [74] Li, L., Liu, T., Fu, C., Tan, L., Meng, X., Liu, H., Biodistribution, excretion, and toxicity of mesoporous silica nanoparticles after oral administration depend on their shape. Nanomed.: Nanotechnol., Biol. Med. 11 (2015), 1915–1924.
75. [75] Champion, J.A., Mitragotri, S., Shape induced inhibition of phagocytosis of polymer particles. Pharm. Res. 26 (2009), 244–249.
76. [76] Niikura, K., Matsunaga, T., Suzuki, T., Kobayashi, S., Yamaguchi, H., Orba, Y., Kawaguchi, A., Hasegawa, H., Kajino, K., Ninomiya, T., Ijiro, K., Sawa, H., Gold nanoparticles as a vaccine platform: influence of size and shape on immunological responses in vitro and in vivo. ACS Nano 7 (2013), 3926–3938.
77. [77] Sharma, G., Valenta, D.T., Altman, Y., Harvey, S., Xie, H., Mitragotri, S., Smith, J.W., Polymer particle shape independently influences binding and internalization by macrophages. J. Control. Release 147 (2010), 408–412.
78. [78] Champion, J.A., Mitragotri, S., Role of target geometry in phagocytosis. Proc. Natl. Acad. Sci. U. S. A. 103 (2006), 4930–4934.
79. [79] Huang, X., Teng, X., Chen, D., Tang, F., He, J., The effect of the shape of mesoporous silica nanoparticles on cellular uptake and cell function. Biomaterials 31 (2010), 438–448.
80. [80] Yi, X., Gao, H., Phase diagrams and morphological evolution in wrapping of rod-shaped elastic nanoparticles by cell membrane: a two-dimensional study. Phys. Rev. E, 89, 2014.
81. [81] Merkel, T.J., Jones, S.W., Herlihy, K.P., Kersey, F.R., Shields, A.R., Napier, M., Luft, J.C., Wu, H., Zamboni, W.C., Wang, A.Z., Bear, J.E., DeSimone, J.M., Using mechanobiological mimicry of red blood cells to extend circulation times of hydrogel microparticles. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 586–591.
82. [82] Anselmo, A.C., Zhang, M., Kumar, S., Vogus, D.R., Menegatti, S., Helgeson, M.E., Mitragotri, S., Elasticity of nanoparticles influences their blood circulation, phagocytosis, endocytosis, and targeting. ACS Nano 9 (2015), 3169–3177.
83. [83] Gabizon, A., Papahadjopoulos, D., Liposome formulations with prolonged circulation time in blood and enhanced uptake by tumors. Proc. Natl. Acad. Sci. 85 (1988), 6949–6953.
84. [84] Allen, T.M., Hansen, C., Rutledge, J., Liposomes with prolonged circulation times: factors affecting uptake by reticuloendothelial and other tissues. Biochim. Biophys. Acta 981 (1989), 27–35.
85. [85] Senior, J., Gregoriadis, G., Stability of small unilamellar liposomes in serum and clearance from the circulation: the effect of the phospholipid and cholesterol components. Life Sci. 30 (1982), 2123–2136.
86. [86] Wróblewska, M., Czyżewska, M., Wolska, A., Kortas-Stempak, B., Szutowicz, A., Apo A-II participates in HDL–liposome interaction by the formation of new pre-β mobility particles and the modification of liposomes. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1801 (2010), 1323–1329.
87. [87] Christensen, D., Henriksen-Lacey, M., Kamath, A.T., Lindenstrøm, T., Korsholm, K.S., Christensen, J.P., Rochat, A.-F., Lambert, P.-H., Andersen, P., Siegrist, C.-A., Perrie, Y., Agger, E.M., A cationic vaccine adjuvant based on a saturated quaternary ammonium lipid have different in vivo distribution kinetics and display a distinct CD4 T cell-inducing capacity compared to its unsaturated analog. J. Control. Release 160 (2012), 468–476.
88. [88] Kaur, R., Henriksen-Lacey, M., Wilkhu, J., Devitt, A., Christensen, D., Perrie, Y., Effect of incorporating cholesterol into DDA:TDB liposomal adjuvants on bilayer properties, biodistribution, and immune responses. Mol. Pharm. 11 (2014), 197–207.
89. [89] Yi, X., Shi, X., Gao, H., Cellular uptake of elastic nanoparticles. Phys. Rev. Lett., 107, 2011.
90. [90] Sun, J., Zhang, L., Wang, J., Feng, Q., Liu, D., Yin, Q., Xu, D., Wei, Y., Ding, B., Shi, X., Jiang, X., Tunable rigidity of (polymeric core)-(lipid shell) nanoparticles for regulated cellular uptake. Adv. Mater. 27 (2015), 1402–1407.
91. [91] Beningo, K.A., Wang, Y.L., Fc-receptor-mediated phagocytosis is regulated by mechanical properties of the target. J. Cell Sci. 115 (2002), 849–856.
92. [92] Hartmann, R., Weidenbach, M., Neubauer, M., Fery, A., Parak, W.J., Stiffness-dependent in vitro uptake and lysosomal acidification of colloidal particles. Angew. Chem. Int. Ed. Eng. 54 (2015), 1365–1368.
93. [93] Cui, J., De Rose, R., Best, J.P., Johnston, A.P., Alcantara, S., Liang, K., Such, G.K., Kent, S.J., Caruso, F., Mechanically tunable, self-adjuvanting nanoengineered polypeptide particles. Adv. Mater. 25 (2013), 3468–3472.
94. [94] Yasuda, T., Dancey, G.F., Kinsky, S.C., Immunogenicity of liposomal model membranes in mice: dependence on phospholipid composition. Proc. Natl. Acad. Sci. U. S. A. 74 (1977), 1234–1236.
95. [95] Dancey, G.F., Yasuda, T., Kinsky, S.C., Effect of liposomal model membrane composition on immunogenicity. J. Immunol. 120 (1978), 1109–1113.
96. [96] Kersten, G.F., van de Put, A.M., Teerlink, T., Beuvery, E.C., Crommelin, D.J., Immunogenicity of liposomes and iscoms containing the major outer membrane protein of Neisseria gonorrhoeae: influence of protein content and liposomal bilayer composition. Infect. Immun. 56 (1988), 1661–1664.
97. [97] Bakouche, O., Gerlier, D., Enhancement of immunogenicity of tumour virus antigen by liposomes: the effect of lipid composition. Immunology 58 (1986), 507–513.
98. [98] Garnier, F., Forquet, F., Bertolino, P., Gerlier, D., Enhancement of in vivo and in vitro T cell response against measles virus haemagglutinin after its incorporation into liposomes: effect of the phospholipid composition. Vaccine 9 (1991), 340–345.
99. [99] Mazumdar, T., Anam, K., Ali, N., Influence of phospholipid composition on the adjuvanticity and protective efficacy of liposome-encapsulated Leishmania donovani antigens. J. Parasitol. 91 (2005), 269–274.
100. [100] Arnal, L., Serra, D.O., Cattelan, N., Castez, M.F., Vazquez, L., Salvarezza, R.C., Yantorno, O.M., Vela, M.E., Adhesin contribution to nanomechanical properties of the virulent Bordetella pertussis envelope. Langmuir 28 (2012), 7461–7469.
101. [101] Mokrozub, V.V., Lazarenko, L.M., Sichel, L.M., Babenko, L.P., Lytvyn, P.M., Demchenko, O.M., Melnichenko, Y.O., Boyko, N.V., Biavati, B., DiGioia, D., Bubnov, R.V., Spivak, M.Y., The role of beneficial bacteria wall elasticity in regulating innate immune response. EPMA J., 6, 2015, 13.
102. [102] Kol, N., Shi, Y., Tsvitov, M., Barlam, D., Shneck, R.Z., Kay, M.S., Rousso, I., A stiffness switch in human immunodeficiency virus. Biophys. J. 92 (2007), 1777–1783.
103. [103] Kol, N., Gladnikoff, M., Barlam, D., Shneck, R.Z., Rein, A., Rousso, I., Mechanical properties of murine leukemia virus particles: effect of maturation. Biophys. J. 91 (2006), 767–774.