Cell membrane-coated nanoparticles as an emerging antibacterial vaccine platform

Vaccines

Volumn 3, Issue 4, 2015, Pages 814-828

  Angsantikul, Pavimol ^a   Thamphiwatana, Soracha ^a   Gao, Weiwei ^a   Zhang, Liangfang ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Biomimetic nanoparticle; Infectious disease; Membrane coating; Nanomedicine; Nanovaccine

Indexed keywords

ALPHA HEMOLYSIN; ANTIBACTERIAL VACCINE; BACTERIAL TOXIN; GAMMA INTERFERON; GLYCOPROTEIN P 15095; GOLD NANOPARTICLE; INTERLEUKIN 17; NANOPARTICLE; POLYGLACTIN; STREPTOLYSIN O; UNCLASSIFIED DRUG; VACCINE; VIRULENCE FACTOR;

ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; CELL MEMBRANE; DENDRITIC CELL; ERYTHROCYTE MEMBRANE; EXOSOME; MEMBRANE VESICLE; NONHUMAN; REVIEW; STAPHYLOCOCCUS AUREUS; VACCINATION;

EID: 84979232441     PISSN: None     EISSN: 2076393X     Source Type: Journal    
DOI: 10.3390/vaccines3040814     Document Type: Review

References (78)

1. Plotkin, S.A. Vaccines, vaccination, and vaccinology. J. Infect. Dis.2003, 187, 1349–1359.
2. Mendoza, N.; Ravanfar, P.; Satyaprakah, A.; Pillai, S.; Creed, R. Existing antibacterial vaccines. Dermatol. Ther. 2009, 22, 129–142.
3. Fauci, A.S.; Morens, D.M. The perpetual challenge of infectious diseases. N. Engl. J. Med. 2012, 366, 454–461.
4. Hancock, R.E.W.; Nijnik, A.; Philpott, D.J. Modulating immunity as a therapy for bacterial infections. Nat. Rev. Microbiol. 2012, 10, 243–254.
5. Berendonk, T.U.; Manaia, C.M.; Merlin, C.; Fatta-Kassinos, D.; Cytryn, E.; Walsh, F.; Buergmann, H.; Sorum, H.; Norstrom, M.; Pons, M.-N.; et al. Tackling antibiotic resistance: The environmental framework. Nat. Rev. Microbiol.2015, 13, 310–317.
6. Blair, J.M.A.; Webber, M.A.; Baylay, A.J.; Ogbolu, D.O.; Piddock, L.J.V. Molecular mechanisms of antibiotic resistance. Nat. Rev. Microbiol. 2015, 13, 42–51.
7. Irvine, D.J.; Swartz, M.A.; Szeto, G.L. Engineering synthetic vaccines using cues from natural immunity. Nat. Mater. 2013, 12, 978–990.
8. Swartz, M.A.; Hirosue, S.; Hubbell, J.A. Engineering approaches to immunotherapy. Sci. Transl. Med. 2012, doi:10.1126/scitranslmed.3003763.
9. Moon, J.J.; Huang, B.; Irvine, D.J. Engineering nano- and microparticles to tune immunity. Adv. Mater. 2012, 24, 3724–3746.
10. Zhao, L.; Seth, A.; Wibowo, N.; Zhao, C.-X.; Mitter, N.; Yu, C.; Middelberg, A.P.J. Nanoparticle vaccines. Vaccine2014, 32, 327–337.
11. Yoo, J.-W.; Irvine, D.J.; Discher, D.E.; Mitragotri, S. Bio-inspired, bioengineered and biomimetic drug delivery carriers. Nat. Rev. Drug Discov.2011, 10, 521–535.
12. Demento, S.L.; Cui, W.; Criscione, J.M.; Stern, E.; Tulipan, J.; Kaech, S.M.; Fahmy, T.M. Role of sustained antigen release from nanoparticle vaccines in shaping the T cell memory phenotype. Biomaterials2012, 33, 4957–4964.
13. Silva, A.L.; Rosalia, R.A.; Sazak, A.; Carstens, M.G.; Ossendorp, F.; Oostendorp, J.; Jiskoot, W. Optimization of encapsulation of a synthetic long peptide in PLGA nanoparticles: Low-burst release is crucial for efficient CD8+ T cell activation. Eur. J. Pharm. Biopharm. 2013, 83, 338–345.
14. Lutsiak, M.E.; Kwon, G.S.; Samuel, J. Biodegradable nanoparticle delivery of a Th2-biased peptide for induction of Th1 immune responses. J. Pharm. Pharmacol. 2006, 58, 739–747.
15. Demento, S.L.; Siefert, A.L.; Bandyopadhyay, A.; Sharp, F.A.; Fahmy, T.M. Pathogen-associated molecular patterns on biomaterials: A paradigm for engineering new vaccines. Trends Biotechnol. 2011, 29, 294–306.
16. Demento, S.L.; Eisenbarth, S.C.; Foellmer, H.G.; Platt, C.; Caplan, M.J.; Saltzman, W.M.; Mellman, I.; Ledizet, M.; Fikrig, E.; Flavell, R.A.; et al. Inflammasome-activating nanoparticles as modular systems for optimizing vaccine efficacy. Vaccine2009, 27, 3013–3021.
17. Nochi, T.; Yuki, Y.; Takahashi, H.; Sawada, S.-I.; Mejima, M.; Kohda, T.; Harada, N.; Kong, I.G.; Sato, A.; Kataoka, N.; et al. Nanogel antigenic protein-delivery system for adjuvant-free intranasal vaccines. Nat. Mater. 2010, 9, 572–578.
18. Yoo, J.-W.; Mitragotri, S. Polymer particles that switch shape in response to a stimulus. Proc. Natl. Acad. Sci. USA2010, 107, 11205–11210.
19. Wilson, J.T.; Keller, S.; Manganiello, M.J.; Cheng, C.; Lee, C.-C.; Opara, C.; Convertine, A.; Stayton, P.S. pH-responsive nanoparticle vaccines for dual-delivery of antigens and immunostimulatory oligonucleotides. ACS Nano2013, 7, 3912–3925.
20. Hu, Y.; Litwin, T.; Nagaraja, A.R.; Kwong, B.; Katz, J.; Watson, N.; Irvine, D.J. Cytosolic delivery of membrane-impermeable molecules in dendritic cells using pH-responsive core-shell nanoparticles. Nano Lett. 2007, 7, 3056–3064.
21. Moon, J.J.; Suh, H.; Bershteyn, A.; Stephan, M.T.; Liu, H.; Huang, B.; Sohail, M.; Luo, S.; Um, S.H.; Khant, H.; et al. Interbilayer-crosslinked multilamellar vesicles as synthetic vaccines for potent humoral and cellular immune responses. Nat. Mater. 2011, 10, 243–251.
22. Moon, J.J.; Suh, H.; Li, A.V.; Ockenhouse, C.F.; Yadava, A.; Irvine, D.J. Enhancing humoral responses to a malaria antigen with nanoparticle vaccines that expand Tfh cells and promote germinal center induction. Proc. Natl. Acad. Sci. USA2012, 109, 1080–1085.
23. Li, A.V.; Moon, J.J.; Abraham, W.; Suh, H.; Elkhader, J.; Seidman, M.A.; Yen, M.; Im, E.-J.; Foley, M.H.; Barouch, D.H.; et al. Generation of effector memory T cell-based mucosal and systemic immunity with pulmonary nanoparticle vaccination. Sci. Transl. Med.2013, doi:10.1126/scitranslmed.3006516.
24. Hu, C.-M.J.; Zhang, L.; Aryal, S.; Cheung, C.; Fang, R.H.; Zhang, L. Erythrocyte membrane-camouflaged polymeric nanoparticles as a biomimetic delivery platform. Proc. Natl. Acad. Sci. USA2011, 108, 10980–10985.
25. Hu, C.-M.J.; Fang, R.H.; Copp, J.; Luk, B.T.; Zhang, L. A biomimetic nanosponge that absorbs pore-forming toxins. Nat. Nanotechnol.2013, 8, 336–340.
26. Hu, C.-M.J.; Fang, R.H.; Luk, B.T.; Zhang, L. Nanoparticle-detained toxins for safe and effective vaccination. Nat. Nanotechnol. 2013, 8, 933–938.
27. Hu, C.-M.J.; Zhang, L. Nanotoxoid vaccines. Nano Today2014, 9, 401–404.
28. Lee, V.T.; Schneewind, O. Protein secretion and the pathogenesis of bacterial infections. Genes Dev. 2001, 15, 1725–1752.
29. Kitchin, N.R. Review of diphtheria, tetanus and pertussis vaccines in clinical development. Expert Rev. Vaccines2011, 10, 605–615.
30. Holmgren, J.; Svennerholm, A.-M.; Lonnroth, I.; Fall-Persson, M.; Markman, B.; Lundbeck, H. Development of improved cholera vaccine based on subunit toxoid. Nature1977, 269, 602–604.
31. Greenberg, R.N.; Marbury, T.C.; Foglia, G.; Warny, M. Phase I dose finding studies of an adjuvanted clostridium difficile toxoid vaccine. Vaccine2012, 30, 2245–2249.
32. Cryz, S.J., Jr.; Furer, E.; Germanier, R. Effect of chemical and heat inactivation on the antigenicity and immunogenicity of Vibrio cholerae. Infect. Immun. 1982, 38, 21–26.
33. Metz, B.; Kersten, G.F.; Hoogerhout, P.; Brugghe, H.F.; Timmermans, H.A.; de Jong, A.; Meiring, H.; ten Hove, J.; Hennink, W.E.; Crommelin, D.J.; et al. Identification of formaldehyde-induced modifications in proteins: Reactions with model peptides. J. Biol. Chem. 2004, 279, 6235–6243.
34. Parish, H.J.; Cannon, D.A. Staphylococcal infection: Antitoxic immunity. Br. Med. J. 1960, 1, 743–747.
35. Kernodle, D.S. Expectations regarding vaccines and immune therapies directed against Staphylococcus aureus alpha-hemolysin. J. Infect. Dis. 2011, 203, 1692–1693.
36. Kennedy, A.D.; Wardenburg, J.B.; Gardner, D.J.; Long, D.; Whitney, A.R.; Braughton, K.R.; Schneewind, O.; DeLeo, F.R. Targeting of alpha-hemolysin by active or passive immunization decreases severity of USA300 skin infection in a mouse model. J. Infect. Dis. 2010, 202, 1050–1058.
37. Kirkham, L.A.; Kerr, A.R.; Douce, G.R.; Paterson, G.K.; Dilts, D.A.; Liu, D.F.; Mitchell, T.J. Construction and immunological characterization of a novel nontoxic protective pneumolysin mutant for use in future pneumococcal vaccines. Infect. Immun. 2006, 74, 586–593.
38. Jang, S.I.; Lillehoj, H.S.; Lee, S.-H.; Lee, K.W.; Lillehoj, E.P.; Hong, Y.H.; An, D.-J.; Jeong, W.; Chun, J.-E.; Bertrand, F.; et al. Vaccination with clostridium perfringens recombinant proteins in combination with Montanide™ ISA 71 VG adjuvant increases protection against experimental necrotic enteritis in commercial broiler chickens. Vaccine2012, 30, 5401–5406.
39. Adhikari, R.P.; Karauzum, H.; Sarwar, J.; Abaandou, L.; Mahmoudieh, M.; Boroun, A.R.; Vu, H.; Nguyen, T.; Devi, V.S.; Shulenin, S.; et al. Novel structurally designed vaccine for S. Aureus alpha-hemolysin: Protection against bacteremia and pneumonia. PLoS ONE2012, 7, e38567.
40. Los, F.C.O.; Randis, T.M.; Aroian, R.V.; Ratner, A.J. Role of pore-forming toxins in bacterial infectious diseases. Microbiol. Mol. Biol. Rev. 2013, 77, 173–207.
41. Dobrovolskaia, M.A.; McNeil, S.E. Immunological properties of engineered nanomaterials. Nat. Nanotechnol. 2007, 2, 469–478.
42. Ivarsson, M.E.; Leroux, J.C.; Castagner, B. Targeting bacterial toxins. Angew. Chem. Int. Ed. 2012, 51, 4024–4045.
43. Hoshino, Y.; Kodama, T.; Okahata, Y.; Shea, K.J. Peptide imprinted polymer nanoparticles: A plastic antibody. J. Am. Chem. Soc. 2008, 130, 15242–15243.
44. Elamanchili, P.; Lutsiak, C.M.; Hamdy, S.; Diwan, M.; Samuel, J. “Pathogen-mimicking” nanoparticles for vaccine delivery to dendritic cells. J. Immunother.2007, 30, 378–395.
45. McCarthy, D.P.; Hunter, Z.N.; Chackerian, B.; Shea, L.D.; Miller, S.D. Targeted immunomodulation using antigen-conjugated nanoparticles. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 2014, 6, 298–315.
46. Little, S.R. Reorienting our view of particle-based adjuvants for subunit vaccines. Proc. Natl. Acad. Sci. USA2012, 109, 999–1000.
47. Espuelas, S.; Roth, A.; Thumann, C.; Frisch, B.; Schuber, F. Effect of synthetic lipopeptides formulated in liposomes on the maturation of human dendritic cells. Mol. Immunol. 2005, 42, 721–729.
48. Zaman, M.; Toth, I. Immunostimulation by synthetic lipopeptide based vaccine candidates: Structure-activity relationships. Front. Immunol. 2013, doi:10.3389/fimmu.2013.00318.
49. Rudra, J.S.; Tian, Y.F.; Jung, J.P.; Collier, J.H. A self-assembling peptide acting as an immune adjuvant. Proc. Natl. Acad. Sci. USA2010, 107, 622–627.
50. Li, L.L.; Xu, J.H.; Qi, G.B.; Zhao, X.Z.; Yu, F.Q.; Wang, H. Core-shell supramolecular gelatine nanoparticles for adaptive and “on-demand” antibiotic delivery. ACS Nano2014, 8, 4975–4983.
51. Gregory, A.E.; Titball, R.; Williamson, D. Vaccine delivery using nanoparticles. Front. Cell. Infect. Microbiol.2013, doi:10.3389/fcimb.2013.00013.
52. Gao, W.; Fang, R.H.; Thamphiwatana, S.; Luk, B.T.; Li, J.; Angsantikul, P.; Zhang, Q.; Hu, C.-M.J.; Zhang, L. Modulating antibacterial immunity via bacterial membrane-coated nanoparticles. Nano Lett. 2015, 15, 1403–1409.
53. Poetsch, A.; Wolters, D. Bacterial membrane proteomics. Proteomics2008, 8, 4100–4122.
54. Lee, E.Y.; Bang, J.Y.; Park, G.W.; Choi, D.S.; Kang, J.S.; Kim, H.J.; Park, K.S.; Lee, J.O.; Kim, Y.K.; Kwon, K.H.; et al. Global proteomic profiling of native outer membrane vesicles derived from Escherichia coli. Proteomics2007, 7, 3143–3153.
55. Kuehn, M.J.; Kesty, N.C. Bacterial outer membrane vesicles and the host-pathogen interaction. Genes Dev. 2005, 19, 2645–2655.
56. Hu, C.-M.J.; Fang, R.H.; Luk, B.T.; Chen, K.N.H.; Carpenter, C.; Gao, W.; Zhang, K.; Zhang, L. “Marker-of-self” functionalization of nanoscale particles through a top-down cellular membrane coating approach. Nanoscale2013, 5, 2664–2668.
57. Luk, B.T.; Hu, C.-M.J.; Fang, R.H.; Dehaini, D.; Carpenter, C.; Gao, W.; Zhang, L. Interfacial interactions between natural RBC membranes and synthetic polymeric nanoparticles. Nanoscale2014, 6, 2730–2737.
58. Unal, C.M.; Schaar, V.; Riesbeck, K. Bacterial outer membrane vesicles in disease and preventive medicine. Semin. Immunopathol. 2011, 33, 395–408.
59. Acevedo, R.; Fernandez, S.; Zayas, C.; Acosta, A.; Sarmiento, M.E.; Ferro, V.A.; Rosenqvist, E.; Campa, C.; Cardoso, D.; Garcia, L.; et al. Bacterial outer membrane vesicles and vaccine applications. Front. Immunol. 2014, doi:10.3389/fimmu.2014.00121
60. Camacho, A.; Irache, J.; de Souza, J.; Sánchez-Gómez, S.; Gamazo, C. Nanoparticle-based vaccine for mucosal protection against shigella flexneri in mice. Vaccine2013, 31, 3288–3294.
61. Hurst, S.J.; Lytton-Jean, A.K.R.; Mirkin, C.A. Maximizing DNA loading on a range of gold nanoparticle sizes. Anal. Chem. 2006, 78, 8313–8318.
62. 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.
63. Kim, J.H.; Lee, J.; Park, J.; Gho, Y.S. Gram-negative and gram-positive bacterial extracellular vesicles. Sem. Cell. Dev. Biol. 2015, 40, 97–104.
64. Gurung, M.; Moon, D.C.; Choi, C.W.; Lee, J.H.; Bae, Y.C.; Kim, J.; Lee, Y.C.; Seol, S.Y.; Cho, D.T.; Kim, S.I.; et al. Staphylococcus aureus produces membrane-derived vesicles that induce host cell death. PLoS ONE2011, 6, e27958.
65. Thay, B.; Wai, S.N.; Oscarsson, J. Staphylococcus aureus alpha-toxin-dependent induction of host cell death by membrane-derived vesicles. PLoS ONE2013, 8, e54661.
66. Chen, D.J.; Osterrieder, N.; Metzger, S.M.; Buckles, E.; Doody, A.M.; DeLisa, M.P.; Putnam, D. Delivery of foreign antigens by engineered outer membrane vesicle vaccines. Proc. Natl. Acad. Sci. USA2010, 107, 3099–3104.
67. Gujrati, V.; Kim, S.; Kim, S.-H.; Min, J.J.; Choy, H.E.; Kim, S.C.; Jon, S. Bioengineered bacterial outer membrane vesicles as cell-specific drug-delivery vehicles for cancer therapy. ACS Nano2014, 8, 1525–1537.
68. Berlanda Scorza, F.; Colucci, A.M.; Maggiore, L.; Sanzone, S.; Rossi, O.; Ferlenghi, I.; Pesce, I.; Caboni, M.; Norais, N.; di Cioccio, V.; et al. High yield production process for shigella outer membrane particles. PLoS ONE2012, 7, e35616.
69. Gao, W.W.; Hu, C.-M.J.; Fang, R.H.; Luk, B.T.; Su, J.; Zhang, L.F. Surface functionalization of gold nanoparticles with red blood cell membranes. Adv. Mater. 2013, 25, 3549–3553.
70. Piao, J.G.; Wang, L.M.; Gao, F.; You, Y.Z.; Xiong, Y.J.; Yang, L.H. Erythrocyte membrane is an alternative coating to polyethylene glycol for prolonging the circulation lifetime of gold nanocages for photothermal therapy. ACS Nano2014, 8, 10414–10425.
71. Parodi, A.; Quattrocchi, N.; van de Ven, A.L.; Chiappini, C.; Evangelopoulos, M.; Martinez, J.O.; Brown, B.S.; Khaled, S.Z.; Yazdi, I.K.; Vittoria Enzo, M.; et al. Synthetic nanoparticles functionalized with biomimetic leukocyte membranes possess cell-like functions. Nat. Nanotechnol. 2013, 8, 61–68.
72. Fang, R.H.; Hu, C.-M.J.; Luk, B.T.; Gao, W.; Copp, J.A.; Tai, Y.; O’Connor, D.E.; Zhang, L. Cancer cell membrane-coated nanoparticles for anticancer vaccination and drug delivery. Nano Lett. 2014, 14, 2181–2188.
73. DeMuth, P.C.; Moon, J.J.; Suh, H.; Hammond, P.T.; Irvine, D.J. Releasable layer-by-layer assembly of stabilized lipid nanocapsules on microneedles for enhanced transcutaneous vaccine delivery. ACS Nano2012, 6, 8041–8051.
74. Ishii, Y.; Nakae, T.; Sakamoto, F.; Matsuo, K.; Matsuo, K.; Quan, Y.-S.; Kamiyama, F.; Fujita, T.; Yamamoto, A.; Nakagawa, S.; et al. A transcutaneous vaccination system using a hydrogel patch for viral and bacterial infection. J. Control. Release2008, 131, 113–120.
75. Kim, J.; Li, W.A.; Choi, Y.; Lewin, S.A.; Verbeke, C.S.; Dranoff, G.; Mooney, D.J. Injectable, spontaneously assembling, inorganic scaffolds modulate immune cells in vivo and increase vaccine efficacy. Nat. Biotechnol. 2015, 33, 64–72.
76. Stephan, S.B.; Taber, A.M.; Jileaeva, I.; Pegues, E.P.; Sentman, C.L.; Stephan, M.T. Biopolymer implants enhance the efficacy of adoptive T-cell therapy. Nat. Biotechnol. 2015, 33, 97–101.
77. Wang, F.; Gao, W.; Thamphiwatana, S.; Luk, B.T.; Angsantikul, P.; Zhang, Q.; Hu, C.-M.J.; Fang, R.H.; Copp, J.A.; Pornpattananangkul, D.; et al. Engineering red blood cell membrane-coated nanoparticles for broad biomedical applications. Adv. Mater. 2015, 27, 3437–3443.
78. Zhang, J.; Gao, W.; Fang, R.H.; Dong, A.; Zhang, L. Synthesis of nanogels via cell membrane-templated polymerization. Small2015, 11, 4309–4313.