Engineering vaccines and niches for immune modulation

Acta Biomaterialia

Volumn 10, Issue 4, 2014, Pages 1728-1740

  Purwada, Alberto ^a   Roy, Krishnendu ^b   Singh, Ankur ^a  

^a Cornell University   (United States)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Biomaterials; Immunoengineering; Immunomodulation; Niches; Vaccines

Indexed keywords

CELL ENGINEERING; CELLS; CYTOLOGY; DISEASES; MODULATION; MOLECULAR BIOLOGY; REGENERATIVE MEDICINE; VACCINES;

AUTOIMMUNE DISORDER; B CELLS; CLINICAL APPLICATION; IMMUNE MODULATION; IMMUNE RESPONSE; IMMUNO MODULATIONS; IMMUNOENGINEERING; INFECTIOUS DISEASE; NICHE; REGENERATIVE MEDICINE;

IMMUNE SYSTEM;

ANTIGEN; BIOMATERIAL; NANOPARTICLE; POLYMER; VACCINE;

AUTOIMMUNE DISEASE; BIOMEDICAL ENGINEERING; DRUG DELIVERY SYSTEM; DRUG DESIGN; HUMAN; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNITY; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; IMMUNOSTIMULATION; IMMUNOTHERAPY; IN VITRO STUDY; IN VIVO STUDY; INFECTION; NEOPLASM; NONHUMAN; PARTICLE SIZE; PRIORITY JOURNAL; REVIEW; SURFACE PROPERTY;

BIOMATERIALS; IMMUNOENGINEERING; IMMUNOMODULATION; NICHES; VACCINES;

ANIMALS; BIOCOMPATIBLE MATERIALS; BIOENGINEERING; CROSS-PRIMING; HUMANS; IMMUNOMODULATION; IMMUNOTHERAPY; VACCINES;

EID: 84896404260     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2013.12.036     Document Type: Review

References (138)

1. F.H. Igney, and P.H. Krammer Immune escape of tumors: Apoptosis resistance and tumor counterattack J Leukoc Biol 71 6 2002 907 920
2. B. Hahm, M.J. Trifilo, E.I. Zuniga, and M.B. Oldstone Viruses evade the immune system through type I interferon-mediated STAT2-dependent, but STAT1-independent, signaling Immunity 22 2 2005 247 257
3. I. Mellman, G. Coukos, and G. Dranoff Cancer immunotherapy comes of age Nature 480 7378 2011 480 489
4. L.W. Kwak, R. Pennington, L. Boni, A.C. Ochoa, R.J. Robb, and M.C. Popescu Liposomal formulation of a self lymphoma antigen induces potent protective antitumor immunity J Immunol 160 8 1998 3637 3641
5. Z. Yu, M.R. Theoret, C.E. Touloukian, D.R. Surman, S.C. Garman, and L. Feigenbaum et al. Poor immunogenicity of a self/tumor antigen derives from peptide-MHC-I instability and is independent of tolerance J Clin Invest 114 4 2004 551 559 PMCID: 503773
6. M. Wick, P. Dubey, H. Koeppen, C.T. Siegel, P.E. Fields, and L. Chen et al. Antigenic cancer cells grow progressively in immune hosts without evidence for T cell exhaustion or systemic anergy J Exp Med 186 2 1997 229 238 PMCID: 2198977
7. P. Yu, Y. Lee, W. Liu, T. Krausz, A. Chong, and H. Schreiber et al. Intratumor depletion of CD4+ cells unmasks tumor immunogenicity leading to the rejection of late-stage tumors J Exp Med 201 5 2005 779 791 PMCID: 2212829
8. S.A. Rosenberg A new era for cancer immunotherapy based on the genes that encode cancer antigens Immunity 10 3 1999 281 287
9. P.A. Monach, S.C. Meredith, C.T. Siegel, and H. Schreiber A unique tumor antigen produced by a single amino acid substitution Immunity 2 1 1995 45 59
10. T. Wolfel, M. Hauer, J. Schneider, M. Serrano, C. Wolfel, and E. Klehmann-Hieb et al. A p16INK4a-insensitive CDK4 mutant targeted by cytolytic T lymphocytes in a human melanoma Science 269 5228 1995 1281 1284
11. P.G. Coulie, F. Lehmann, B. Lethe, J. Herman, C. Lurquin, and M. Andrawiss et al. A mutated intron sequence codes for an antigenic peptide recognized by cytolytic T lymphocytes on a human melanoma Proc Natl Acad Sci U S A 92 17 1995 7976 7980 PMCID: 41269
12. S.J. Piersma Immunosuppressive tumor microenvironment in cervical cancer patients Cancer Microenviron 4 3 2011 361 375 PMCID: 3234326
13. C.C. Tong, J. Kao, and A.G. Sikora Recognizing and reversing the immunosuppressive tumor microenvironment of head and neck cancer Immunol Res 54 1-3 2012 266 274
14. A.F. Ochsenbein, P. Klenerman, U. Karrer, B. Ludewig, M. Pericin, and H. Hengartner et al. Immune surveillance against a solid tumor fails because of immunological ignorance Proc Natl Acad Sci U S A 96 5 1999 2233 2238 PMCID: 26766
15. A.Y. Savinov, F.S. Wong, A.C. Stonebraker, and A.V. Chervonsky Presentation of antigen by endothelial cells and chemoattraction are required for homing of insulin-specific CD8+ T cells J Exp Med 197 5 2003 643 656 PMCID: 2193823
16. K. Pietras, A. Ostman, M. Sjoquist, E. Buchdunger, R.K. Reed, and C.H. Heldin et al. Inhibition of platelet-derived growth factor receptors reduces interstitial hypertension and increases transcapillary transport in tumors Cancer Res 61 7 2001 2929 2934
17. D.L. Barber, E.J. Wherry, D. Masopust, B. Zhu, J.P. Allison, and A.H. Sharpe et al. Restoring function in exhausted CD8 T cells during chronic viral infection Nature 439 7077 2006 682 687
18. H. Nishimura, M. Nose, H. Hiai, N. Minato, and T. Honjo Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor Immunity 11 2 1999 141 151
19. S.L. Topalian, F.S. Hodi, J.R. Brahmer, S.N. Gettinger, D.C. Smith, and D.F. McDermott et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer N Engl J Med 366 26 2012 2443 2454 PMCID: 3544539
20. J.R. Brahmer, S.S. Tykodi, L.Q. Chow, W.J. Hwu, S.L. Topalian, and P. Hwu et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer N Engl J Med 366 26 2012 2455 2465 PMCID: 3563263
21. K.S. Peggs, S.A. Quezada, and J.P. Allison Cell intrinsic mechanisms of T-cell inhibition and application to cancer therapy Immunol Rev 224 2008 141 165
22. M. Vanneman, and G. Dranoff Combining immunotherapy and targeted therapies in cancer treatment Nat Rev Cancer 12 4 2012 237 251
23. D.M. Pardoll The blockade of immune checkpoints in cancer immunotherapy Nat Rev Cancer 12 4 2012 252 264
24. T. Sun, T. Holowka, Y. Song, S. Zierow, L. Leng, and Y. Chen et al. A Plasmodium-encoded cytokine suppresses T-cell immunity during malaria Proc Natl Acad Sci U S A 109 31 2012 E2117 E2126 PMCID: 3411961
25. J.J. Moon, H. Suh, A.V. Li, C.F. Ockenhouse, A. Yadava, and D.J. Irvine Enhancing humoral responses to a malaria antigen with nanoparticle vaccines that expand Tfh cells and promote germinal center induction Proc Natl Acad Sci U S A 109 4 2012 1080 1085 PMCID: 3268296
26. Khan T, Reddy ST. Immunological principles regulating immunomodulation with biomaterials. Acta Biomater [in press]. http://dx.doi.org/10.1016/j.actbio. 2013.12.01
27. J.H. Hoofnagle, and A.M. di Bisceglie The treatment of chronic viral hepatitis N Engl J Med 336 5 1997 347 356
28. C. Flexner, A. Hugin, and B. Moss Prevention of vaccinia virus infection in immunodeficient mice by vector-directed IL-2 expression Nature 330 6145 1987 259 262
29. I.A. Ramshaw, M.E. Andrew, S.M. Phillips, D.B. Boyle, and B.E. Coupar Recovery of immunodeficient mice from a vaccinia virus/IL-2 recombinant infection Nature 329 6139 1987 545 546
30. G. Parmiani, L. Rivoltini, G. Andreola, and M. Carrabba Cytokines in cancer therapy Immunol Lett 74 1 2000 41 44
31. H. Kawamura, S.A. Rosenberg, and J.A. Berzofsky Immunization with antigen and interleukin 2 in vivo overcomes Ir gene low responsiveness J Exp Med 162 1 1985 381 386
32. A. Singh, S. Suri, and K. Roy In-situ crosslinking hydrogels for combinatorial delivery of chemokines and siRNA-DNA carrying microparticles to dendritic cells Biomaterials 30 28 2009 5187 5200
33. J.A. Hubbell, S.N. Thomas, and M.A. Swartz Materials engineering for immunomodulation Nature 462 7272 2009 449 460
34. Y. Hori, A.M. Winans, and D.J. Irvine Modular injectable matrices based on aglinate solution/microsphere mixtures that gel in situ and co-deliver immunomodulatory factors Acta Biomater 5 2009 969 982
35. O.A. Ali, N. Huebsch, L. Cao, G. Dranoff, and D.J. Mooney Infection-mimicking materials to program dendritic cells in situ Nat Mater 8 2 2009 151 158
36. A. Singh, H. Nie, B. Ghosn, H. Qin, L.W. Kwak, and K. Roy Efficient modulation of T-cell response by dual-mode, single-carrier delivery of cytokine-targeted siRNA and DNA vaccine to antigen-presenting cells Mol Ther 16 12 2008 2011 2021
37. D. Nguyen, J. Green, M. Chan, R. Langer, and D. Anderson Polymeric materials for gene delivery and DNA vaccination Adv Mater 20 2008 1 21
38. S.R. Little, D.M. Lynn, Q. Ge, D.G. Anderson, S.V. Puram, and J. Chen et al. Poly-beta amino ester-containing microparticles enhance the activity of nonviral genetic vaccines Proc Natl Acad Sci U S A 101 26 2004 9534 9539
39. S.P. Sullivan, D.G. Koutsonanos, M. Del Pilar Martin, J.W. Lee, V. Zarnitsyn, and S.O. Choi et al. Dissolving polymer microneedle patches for influenza vaccination Nat Med 16 8 2010 915 920 PMCID: 2917494
40. Y.C. Kim, F.S. Quan, D.G. Yoo, R.W. Compans, S.M. Kang, and M.R. Prausnitz Improved influenza vaccination in the skin using vaccine coated microneedles Vaccine 27 49 2009 6932 6938 PMCID: 2913971
41. M.R. Prausnitz, and R. Langer Transdermal drug delivery Nat Biotechnol 26 11 2008 1261 1268 PMCID: 2700785
42. O. Boussif, F. Lezoualc'h, M.A. Zanta, M.D. Mergny, D. Scherman, and B. Demeneix et al. A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: Polyethylenimine Proc Natl Acad Sci U S A 92 16 1995 7297 7301
43. M. Neu, D. Fischer, and T. Kissel Recent advances in rational gene transfer vector design based on poly(ethylene imine) and its derivatives J Gene Med 7 8 2005 992 1009
44. C. de Chastellier, and L. Thilo Phagosome maturation and fusion with lysosomes in relation to surface property and size of the phagocytic particle Eur J Cell Biol 74 1 1997 49 62
45. S. Jilek, H.P. Merkle, and E. Walter DNA-loaded biodegradable microparticles as vaccine delivery systems and their interaction with dendritic cells Adv Drug Deliv Rev 57 3 2005 377 390
46. Y. Tabata, and Y. Ikada Macrophage activation through phagocytosis of muramyl dipeptide encapsulated in gelatin microspheres J Pharm Pharmacol 39 9 1987 698 704
47. J.C. Sunshine, and J.J. Green Nanoengineering approaches to the design of artificial antigen-presenting cells Nanomedicine (Lond) 8 7 2013 1173 1189
48. E.R. Steenblock, and T.M. Fahmy A comprehensive platform for ex vivo T-cell expansion based on biodegradable polymeric artificial antigen-presenting cells Mol Ther 16 4 2008 765 772
49. L. Thiele, H.P. Merkle, and E. Walter Phagocytosis and phagosomal fate of surface-modified microparticles in dendritic cells and macrophages Pharm Res 20 2 2003 221 228
50. Y. Tabata, Y. Inoue, and Y. Ikada Size effect on systemic and mucosal immune responses induced by oral administration of biodegradable microspheres Vaccine 14 17-18 1996 1677 1685
51. Y. Tabata, and Y. Ikada Effect of the size and surface charge of polymer microspheres on their phagocytosis by macrophage Biomaterials 9 4 1988 356 362
52. J.A. Champion, A. Walker, and S. Mitragotri Role of particle size in phagocytosis of polymeric microspheres Pharm Res 25 8 2008 1815 1821 PMCID: 2793372
53. K.K. Tran, and H. Shen The role of phagosomal pH on the size-dependent efficiency of cross-presentation by dendritic cells Biomaterials 30 7 2009 1356 1362 PMCID: 2735406
54. S.E. Gratton, P.A. Ropp, P.D. Pohlhaus, J.C. Luft, V.J. Madden, and M.E. Napier et al. The effect of particle design on cellular internalization pathways Proc Natl Acad Sci U S A 105 33 2008 11613 11618 PMCID: 2575324
55. S.T. Reddy, A.J. van der Vlies, E. Simeoni, V. Angeli, G.J. Randolph, and C.P. O'Neil et al. Exploiting lymphatic transport and complement activation in nanoparticle vaccines Nat Biotechnol 25 10 2007 1159 1164
56. S.P. Kasturi, K. Sachaphibulkij, and K. Roy Covalent conjugation of polyethyleneimine on biodegradable microparticles for delivery of plasmid DNA vaccines Biomaterials 26 32 2005 6375 6385
57. D. O'Hagan, M. Singh, and J. Ulmer Microparticle-based technologies for vaccines Methods 40 2006 10 19
58. M. Singh, M. Briones, G. Ott, and D. O'Hagan Cationic microparticles: A potent delivery system for DNA vaccines Proc Natl Acad Sci U S A 97 2 2000 811 816
59. M.L. Hedley Formulations containing poly(lactide-co-glycolide) and plasmid DNA expression vectors Expert Opin Biol Ther 3 6 2003 903 910
60. L. Thiele, B. Rothen-Rutishauser, S. Jilek, H. Wunderli-Allenspach, H.P. Merkle, and E. Walter Evaluation of particle uptake in human blood monocyte-derived cells in vitro. Does phagocytosis activity of dendritic cells measure up with macrophages? J Control Release 76 1-2 2001 59 71
61. R. Agarwal, V. Singh, P. Jurney, L. Shi, S.V. Sreenivasan, and K. Roy Mammalian cells preferentially internalize hydrogel nanodiscs over nanorods and use shape-specific uptake mechanisms Proc Natl Acad Sci U S A 110 43 2013 17247 17252
62. C. Zuany-Amorim, J. Hastewell, and C. Walker Toll-like receptors as potential therapeutic targets for multiple diseases Nat Rev Drug Discov 1 10 2002 797 807
63. W. Cao, S. Manicassamy, H. Tang, S.P. Kasturi, A. Pirani, and N. Murthy et al. Toll-like receptor-mediated induction of type I interferon in plasmacytoid dendritic cells requires the rapamycin-sensitive PI(3)K-mTOR-p70S6K pathway Nat Immunol 9 10 2008 1157 1164
64. M. Kwissa, S.P. Kasturi, and B. Pulendran The science of adjuvants Expert Rev Vaccines 6 5 2007 673 684
65. U. Hasan, C. Chaffois, C. Gaillard, V. Saulnier, E. Merck, and S. Tancredi et al. Human TLR10 is a functional receptor, expressed by B cells and plasmacytoid dendritic cells, which activates gene transcription through MyD88 J Immunol 174 5 2005 2942 2950
66. M. Gilliet, W. Cao, and Y.J. Liu Plasmacytoid dendritic cells: Sensing nucleic acids in viral infection and autoimmune diseases Nat Rev Immunol 8 8 2008 594 606
67. D.T. O'Hagan, and N.M. Valiante Recent advances in the discovery and delivery of vaccine adjuvants Nat Rev Drug Discov 2 9 2003 727 735
68. M. Singh, and D. O'Hagan Advances in vaccine adjuvants Nat Biotechnol 17 11 1999 1075 1081
69. M. Singh, and D.T. O'Hagan Recent advances in vaccine adjuvants Pharm Res 19 6 2002 715 728
70. A. Singh, P. Pradhan, and K. Roy Immunobioengineering approaches towards combinatorial delivery of immune-modulators and antigens. Novel immune potentiators and delivery technologies for next generation vaccines 2013 Springer New York 161 181
71. H.C. Chen, B. Sun, K.K. Tran, and H. Shen Effects of particle size on toll-like receptor 9-mediated cytokine profiles Biomaterials 32 6 2011 1731 1737 PMCID: 3031083
72. J.A. Champion, Y.K. Katare, and S. Mitragotri Particle shape: A new design parameter for micro- and nanoscale drug delivery carriers J Control Release 121 1-2 2007 3 9
73. J.A. Champion, and S. Mitragotri Shape induced inhibition of phagocytosis of polymer particles Pharm Res 26 1 2009 244 249 PMCID: 2810499
74. N. Doshi, and S. Mitragotri Macrophages recognize size and shape of their targets PLoS One 5 4 2010 e10051 PMCID: 2850372
75. G. Sharma, D.T. Valenta, Y. Altman, S. Harvey, H. Xie, and S. Mitragotri et al. Polymer particle shape independently influences binding and internalization by macrophages J Control Release 147 3 2010 408 412 PMCID: 2975856
76. R. Agarwal, and K. Roy Intracellular delivery of polymeric nanocarriers: A matter of size, shape, charge, elasticity and surface composition Ther Deliv 4 6 2013 705 723
77. M. Caldorera-Moore, N. Guimard, L. Shi, and K. Roy Designer nanoparticles: Incorporating size, shape and triggered release into nanoscale drug carriers Expert Opin Drug Deliv 7 4 2010 479 495 PMCID: 2845970
78. L.C. Glangchai, M. Caldorera-Moore, L. Shi, and K. Roy Nanoimprint lithography based fabrication of shape-specific, enzymatically-triggered smart nanoparticles J Control Release 125 3 2008 263 272
79. L.K. Petersen, L. Xue, M.J. Wannemuehler, K. Rajan, and B. Narasimhan The simultaneous effect of polymer chemistry and device geometry on the in vitro activation of murine dendritic cells Biomaterials 30 28 2009 5131 5142
80. P. Decuzzi, B. Godin, T. Tanaka, S.Y. Lee, C. Chiappini, and X. Liu et al. Size and shape effects in the biodistribution of intravascularly injected particles J Control Release 141 3 2010 320 327
81. V.P. Chauhan, Z. Popovic, O. Chen, J. Cui, D. Fukumura, and M.G. Bawendi et al. Fluorescent nanorods and nanospheres for real-time in vivo probing of nanoparticle shape-dependent tumor penetration Angew Chem 50 48 2011 11417 11420 PMCID: 3260125
82. J. Doh, and D.J. Irvine Immunological synapse arrays: Patterned protein surfaces that modulate immunological synapse structure formation in T cells Proc Natl Acad Sci U S A 103 15 2006 5700 5705 PMCID: 1458636
83. J.C. Sunshine, K. Perica, J.P. Schneck, and J.J. Green Particle shape dependence of CD8+ T cell activation by artificial antigen presenting cells Biomaterials 35 1 2014 269 277
84. C.J. Turtle, and S.R. Riddell Artificial antigen-presenting cells for use in adoptive immunotherapy Cancer J 16 4 2010 374 381 PMCID: 2929753
85. G.P. Downey, R.J. Botelho, J.R. Butler, Y. Moltyaner, P. Chien, and A.D. Schreiber et al. Phagosomal maturation, acidification, and inhibition of bacterial growth in nonphagocytic cells transfected with FcgammaRIIA receptors J Biol Chem 274 40 1999 28436 28444
86. K.A. Howard, and H.O. Alpar The development of polyplex-based DNA vaccines J Drug Target 10 2 2002 143 151
87. M.L. Hedley, J. Curley, and R. Urban Microspheres containing plasmid-encoded antigens elicit cytotoxic T-cell responses Nat Med 4 3 1998 365 368
88. B. Klencke, M. Matijevic, R.G. Urban, J.L. Lathey, M.L. Hedley, and M. Berry et al. Encapsulated plasmid DNA treatment for human papillomavirus 16-associated anal dysplasia: A Phase I study of ZYC101 Clin Cancer Res 8 5 2002 1028 1037
89. E. Mathiowitz, J.S. Jacob, Y.S. Jong, G.P. Carino, D.E. Chickering, and P. Chaturvedi et al. Biologically erodable microspheres as potential oral drug delivery systems Nature 386 6623 1997 410 414
90. D. Wang, M.E. Christopher, L.P. Nagata, M.A. Zabielski, H. Li, and J.P. Wong et al. Intranasal immunization with liposome-encapsulated plasmid DNA encoding influenza virus hemagglutinin elicits mucosal, cellular and humoral immune responses J Clin Virol 31 Suppl. 1 2004 S99 106
91. T.M. Luby, G. Cole, L. Baker, J.S. Kornher, U. Ramstedt, and M.L. Hedley Repeated immunization with plasmid DNA formulated in poly(lactide-co-glycolide) microparticles is well tolerated and stimulates durable T cell responses to the tumor-associated antigen cytochrome P450 1B1 Clin Immunol 112 1 2004 45 53
92. J. Luten, C.F. van Nostrum, S.C. De Smedt, and W.E. Hennink Biodegradable polymers as non-viral carriers for plasmid DNA delivery J Control Release 126 2 2008 97 110
93. S. Ando, D. Putnam, D.W. Pack, and R. Langer PLGA microspheres containing plasmid DNA: Preservation of supercoiled DNA via cryopreparation and carbohydrate stabilization J Pharm Sci 88 1 1999 126 130
94. E. Walter, K. Moelling, J. Pavlovic, and H.P. Merkle Microencapsulation of DNA using poly(DL-lactide-co-glycolide): Stability issues and release characteristics J Control Release 61 3 1999 361 374
95. K. Fu, D.W. Pack, A.M. Klibanov, and R. Langer Visual evidence of acidic environment within degrading poly(lactic-co-glycolic acid) (PLGA) microspheres Pharm Res 17 1 2000 100 106
96. E. Wagner, M. Ogris, and W. Zauner Polylysine-based transfection systems utilizing receptor-mediated delivery Adv Drug Deliv Rev 30 1-3 1998 97 113
97. K. Regnstrom, E.G. Ragnarsson, M. Koping-Hoggard, E. Torstensson, H. Nyblom, and P. Artursson PEI - a potent, but not harmless, mucosal immuno-stimulator of mixed T-helper cell response and FasL-mediated cell death in mice Gene Ther 10 18 2003 1575 1583
98. G.W. Bos, T. Kanellos, D.J. Crommelin, W.E. Hennink, and C.R. Howard Cationic polymers that enhance the performance of HbsAg DNA in vivo Vaccine 23 4 2004 460 469
99. K. Roy, H.Q. Mao, S.K. Huang, and K.W. Leong Oral gene delivery with chitosan-DNA nanoparticles generates immunologic protection in a murine model of peanut allergy Nat Med 5 4 1999 387 391
100. S.C. Richardson, H.V. Kolbe, and R. Duncan Potential of low molecular mass chitosan as a DNA delivery system: Biocompatibility, body distribution and ability to complex and protect DNA Int J Pharm 178 2 1999 231 243
101. L. Illum, I. Jabbal-Gill, M. Hinchcliffe, A.N. Fisher, and S.S. Davis Chitosan as a novel nasal delivery system for vaccines Adv Drug Deliv Rev 51 1-3 2001 81 96
102. G.P. Li, Z.G. Liu, B. Liao, and N.S. Zhong Induction of Th1-type immune response by chitosan nanoparticles containing plasmid DNA encoding house dust mite allergen Der p 2 for oral vaccination in mice Cell Mol Immunol 6 1 2009 45 50
103. Y. Luo, D. O'Hagan, H. Zhou, M. Singh, J. Ulmer, and R.A. Reisfeld et al. Plasmid DNA encoding human carcinoembryonic antigen (CEA) adsorbed onto cationic microparticles induces protective immunity against colon cancer in CEA-transgenic mice Vaccine 21 17-18 2003 1938 1947
104. H.J. Mollenkopf, G. Dietrich, J. Fensterle, L. Grode, K.D. Diehl, and B. Knapp et al. Enhanced protective efficacy of a tuberculosis DNA vaccine by adsorption onto cationic PLG microparticles Vaccine 22 21-22 2004 2690 2695
105. X. He, L. Jiang, F. Wang, Z. Xiao, J. Li, and L.S. Liu et al. Augmented humoral and cellular immune responses to hepatitis B DNA vaccine adsorbed onto cationic microparticles J Control Release 107 2 2005 357 372
106. C.H. Pan, N. Nair, R.J. Adams, M.C. Zink, E.Y. Lee, and F.P. Polack et al. Dose-dependent protection against or exacerbation of disease by a polylactide glycolide microparticle-adsorbed, alphavirus-based measles virus DNA vaccine in rhesus macaques Clin Vaccine Immunol 15 4 2008 697 706
107. S. Pai Kasturi, H. Qin, K.S. Thomson, S. El-Bereir, S.C. Cha, and S. Neelapu et al. Prophylactic anti-tumor effects in a B cell lymphoma model with DNA vaccines delivered on polyethylenimine (PEI) functionalized PLGA microparticles J Control Release 113 3 2006 261 270
108. T. Nochi, Y. Yuki, H. Takahashi, S. Sawada, M. Mejima, and T. Kohda et al. Nanogel antigenic protein-delivery system for adjuvant-free intranasal vaccines Nat Mater 9 7 2010 572 578
109. M. Yoshida, and J.E. Babensee Poly(lactic-co-glycolic acid) enhances maturation of human monocyte-derived dendritic cells J Biomed Mater Res A 71 1 2004 45 54
110. N.L. Bennewitz, and J.E. Babensee The effect of the physical form of poly(lactic-co-glycolic acid) carriers on the humoral immune response to co-delivered antigen Biomaterials 26 16 2005 2991 2999
111. R.L. Hunter Overview of vaccine adjuvants: Present and future Vaccine 20 Suppl 3 2002 S7 12
112. S.T. Reddy, A. Rehor, H.G. Schmoekel, J.A. Hubbell, and M.A. Swartz In vivo targeting of dendritic cells in lymph nodes with poly(propylene sulfide) nanoparticles J Control Release 112 1 2006 26 34
113. S.Y. Seong, and P. Matzinger Hydrophobicity: An ancient damage-associated molecular pattern that initiates innate immune responses Nat Rev Immunol 4 6 2004 469 478
114. J.S. Lewis, T.D. Zaveri, C.P. Crooks 2nd, and B.G. Keselowsky Microparticle surface modifications targeting dendritic cells for non-activating applications Biomaterials 33 29 2012 7221 7232 PMCID: 3428206
115. A. Singh, H. Qin, I. Fernandez, J. Wei, J. Lin, and L.W. Kwak et al. An injectable synthetic immune-priming center mediates efficient T-cell class switching and T-helper 1 response against B cell lymphoma J Control Release 155 2 2011 184 192
116. S. Jhunjhunwala, G. Raimondi, A.J. Glowacki, S.J. Hall, D. Maskarinec, and S.H. Thorne et al. Bioinspired controlled release of CCL22 recruits regulatory T cells in vivo Adv Mater 24 35 2012 4735 4738 PMCID: 3491880
117. T. Kumamoto, E.K. Huang, H.J. Paek, A. Morita, H. Matsue, and R.F. Valentini et al. Induction of tumor-specific protective immunity by in situ Langerhans cell vaccine Nat Biotechnol 20 1 2002 64 69
118. Y. Hori, A.M. Winans, and D.J. Irvine Modular injectable matrices based on alginate solution/microsphere mixtures that gel in situ and co-deliver immunomodulatory factors Acta Biomater 5 4 2009 969 982
119. J.J. Moon, H. Suh, M.E. Polhemus, C.F. Ockenhouse, A. Yadava, and D.J. Irvine Antigen-displaying lipid-enveloped PLGA nanoparticles as delivery agents for a Plasmodium vivax malaria vaccine PLoS One 7 2 2012 e31472 PMCID: 3273465
120. J.S. Rudra, S. Mishra, A.S. Chong, R.A. Mitchell, E.H. Nardin, and V. Nussenzweig et al. Self-assembled peptide nanofibers raising durable antibody responses against a malaria epitope Biomaterials 33 27 2012 6476 6484 PMCID: 3392361
121. S.P. Kasturi, I. Skountzou, R.A. Albrecht, D. Koutsonanos, T. Hua, and H.I. Nakaya et al. Programming the magnitude and persistence of antibody responses with innate immunity Nature 470 7335 2011 543 547
122. J. Park, S.H. Wrzesinski, E. Stern, M. Look, J. Criscione, and R. Ragheb et al. Combination delivery of TGF-beta inhibitor and IL-2 by nanoscale liposomal polymeric gels enhances tumour immunotherapy Nat Mater 11 10 2012 895 905 PMCID: 3601683
123. A. Yeste, M. Nadeau, E.J. Burns, H.L. Weiner, and F.J. Quintana Nanoparticle-mediated codelivery of myelin antigen and a tolerogenic small molecule suppresses experimental autoimmune encephalomyelitis Proc Natl Acad Sci U S A 109 28 2012 11270 11275 PMCID: 3396465
124. B.G. Keselowsky, D.M. Collard, and A.J. Garcia Integrin binding specificity regulates biomaterial surface chemistry effects on cell differentiation Proc Natl Acad Sci U S A 102 17 2005 5953 5957 PMCID: 1087905
125. B.G. Keselowsky, D.M. Collard, and A.J. Garcia Surface chemistry modulates focal adhesion composition and signaling through changes in integrin binding Biomaterials 25 28 2004 5947 5954
126. S. Chen, J.A. Jones, Y. Xu, H.Y. Low, J.M. Anderson, and K.W. Leong Characterization of topographical effects on macrophage behavior in a foreign body response model Biomaterials 31 13 2010 3479 3491 PMCID: 2837101
127. H. Shin, S. Jo, and A.G. Mikos Biomimetic materials for tissue engineering Biomaterials 24 24 2003 4353 4364
128. U. Hersel, C. Dahmen, and H. Kessler RGD modified polymers: Biomaterials for stimulated cell adhesion and beyond Biomaterials 24 24 2003 4385 4415
129. T.A. Petrie, J.E. Raynor, D.W. Dumbauld, T.T. Lee, S. Jagtap, and K.L. Templeman et al. Multivalent integrin-specific ligands enhance tissue healing and biomaterial integration Sci Transl Med 2 45 2010 45ra60 PMCID: 3128787
130. W.J. Kao, D. Lee, J.C. Schense, and J.A. Hubbell Fibronectin modulates macrophage adhesion and FBGC formation: The role of RGD, PHSRN, and PRRARV domains J Biomed Mater Res 55 1 2001 79 88
131. W.J. Kao, and Y. Liu Utilizing biomimetic oligopeptides to probe fibronectin-integrin binding and signaling in regulating macrophage function in vitro and in vivo Front Biosci 6 2001 D992 D999
132. M.J. Smith, D.C. Smith, G.L. Bowlin, and K.L. White Modulation of murine innate and acquired immune responses following in vitro exposure to electrospun blends of collagen and polydioxanone J Biomed Mater Res 93 2 2010 793 806
133. A.J. Allman, T.B. McPherson, S.F. Badylak, L.C. Merrill, B. Kallakury, and C. Sheehan et al. Xenogeneic extracellular matrix grafts elicit a TH2-restricted immune response Transplantation 71 11 2001 1631 1640
134. A.B. Blom, P.M. van der Kraan, and W.B. van den Berg Cytokine targeting in osteoarthritis Curr Drug Targets 8 2 2007 283 292
135. M.K. Haynes, E.L. Hume, and J.B. Smith Phenotypic characterization of inflammatory cells from osteoarthritic synovium and synovial fluids Clin Immunol 105 3 2002 315 325
136. R.E. Whitmire, D.S. Wilson, A. Singh, M.E. Levenston, N. Murthy, and A.J. Garcia Self-assembling nanoparticles for intra-articular delivery of anti-inflammatory proteins Biomaterials 33 30 2012 7665 7675 PMCID: 3418443
137. S. Franz, S. Rammelt, D. Scharnweber, and J.C. Simon Immune responses to implants - a review of the implications for the design of immunomodulatory biomaterials Biomaterials 32 28 2011 6692 6709
138. F.Y. McWhorter, T. Wang, P. Nguyen, T. Chung, and W.F. Liu Modulation of macrophage phenotype by cell shape Proc Natl Acad Sci U S A 110 43 2013 17253 17258