A combination hydrogel microparticle-based vaccine prevents type 1 diabetes in non-obese diabetic mice

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Yoon, Young Mee ^a   Lewis, Jamal S ^b   Carstens, Matthew R ^b   Campbell Thompson, Martha ^a   Wasserfall, Clive H ^a   Atkinson, Mark A ^a   Keselowsky, Benjamin G ^b  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b University of Florida   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE BLOOD LEVEL; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HYDROGEL; IMMUNOLOGICAL ADJUVANT; INSULIN; INTERLEUKIN 10; LACTIC ACID; OLIGODEOXYRIBONUCLEOTIDE; POLYGLYCOLIC ACID; POLYLACTIC ACID-POLYGLYCOLIC ACID COPOLYMER; VACCINE;

ANALYSIS; ANIMAL; BONE MARROW CELL; CELL CULTURE; CELL MOTION; CHEMISTRY; CYTOLOGY; DIABETES MELLITUS, TYPE 1; FEMALE; GLUCOSE BLOOD LEVEL; GRANULOMA; HYDROGEL; IMMUNOLOGY; KAPLAN MEIER METHOD; METABOLISM; MOUSE; NONOBESE DIABETIC MOUSE; PATHOLOGY;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; BLOOD GLUCOSE; BONE MARROW CELLS; CELL MOVEMENT; CELLS, CULTURED; DIABETES MELLITUS, TYPE 1; FEMALE; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; GRANULOMA; HYDROGELS; INSULIN; INTERLEUKIN-10; KAPLAN-MEIER ESTIMATE; LACTIC ACID; MICE; MICE, INBRED NOD; OLIGODEOXYRIBONUCLEOTIDES; POLYGLYCOLIC ACID; VACCINES;

EID: 84939560665     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep13155     Document Type: Article

References (91)

1. Pinkse, G. G. et al. Autoreactive CD8 T cells associated with beta cell destruction in type 1 diabetes. Proc Natl Acad Sci USA 102, 18425-18430 (2005).
2. Gan, M. J., Albanese-O'Neill, A. & Haller, M. J. Type 1 diabetes: current concepts in epidemiology, pathophysiology, clinical care, and research. Curr Probl Pediatr Adolesc Health Care 42, 269-291 (2012).
3. Kantharidis, P., Wang, B., Carew, R. M. & Lan, H. Y. Diabetes complications: the microRNA perspective. Diabetes 60, 1832-1837 (2011).
4. Van Belle, T. L., Coppieters, K. T. & Von Herrath, M. G. Type 1 diabetes: etiology, immunology, and therapeutic strategies. Physiol Rev 91, 79-118 (2011).
5. Atkinson, M. A. & Eisenbarth, G. S. Type 1 diabetes: new perspectives on disease pathogenesis and treatment. Lancet 358, 221-229 (2001).
6. Waeckerle-Men, Y. & Groettrup, M. PLGA microspheres for improved antigen delivery to dendritic cells as cellular vaccines. Adv Drug Deliv Rev 57, 475-482 (2005).
7. Irvine, D. J., Swartz, M. A. & Szeto, G. L. Engineering synthetic vaccines using cues from natural immunity. Nat Mater 12, 978-990 (2013).
8. Rueckert, C. & Guzmán, C. A. Vaccines: from empirical development to rational design. PLoS Pathog 8, e1003001 (2012).
9. Lewis, J. S. et al. Combinatorial delivery of immunosuppressive factors to dendritic cells using dual-sized microspheres. J Mater Chem B Mater Biol Med 2, 2562-2574 (2014).
10. Satpute, S. R., Durai, M. & Moudgil, K. D. Antigen-specific tolerogenic and immunomodulatory strategies for the treatment of autoimmune arthritis. Semin Arthritis Rheum 38, 195-207 (2008).
11. Schwartz, R. H. T cell anergy. Annu Rev Immunol 21, 305-334 (2003).
12. Lewis, J. S., Roy, K. & Keselowsky, B. G. Materials that harness and modulate the immune system. MRS Bulletin 39, 25-34 (2014).
13. Keselowsky, B. G., Xia, C. Q. & Clare-Salzler, M. Multifunctional dendritic cell-targeting polymeric microparticles: engineering new vaccines for type 1 diabetes. Hum Vaccin 7, 37-44 (2011).
14. Zhao, K. et al. Preparation and efficacy of Newcastle disease virus DNA vaccine encapsulated in PLGA nanoparticles. PLoS One 8, e82648 (2013).
15. Hamdy, S. et al. Co-delivery of cancer-associated antigen and Toll-like receptor 4 ligand in PLGA nanoparticles induces potent CD8+ T cell-mediated anti-tumor immunity. Vaccine 26, 5046-5057 (2008).
16. Kirby, D. J. et al. PLGA microspheres for the delivery of a novel subunit TB vaccine. J Drug Target 16, 282-293 (2008).
17. Lewis, J. S., Zaveri, T. D., Crooks, C. P. & Keselowsky, B. G. Microparticle surface modifications targeting dendritic cells for nonactivating applications. Biomaterials 33, 7221-7232 (2012).
18. Yokoi, H., Kinoshita, T. & Zhang, S. Dynamic reassembly of peptide RADA16 nanofiber scaffold. Proc Natl Acad Sci USA 102, 8414-8419 (2005).
19. Kyle, S., Aggeli, A., Ingham, E. & McPherson, M. J. Production of self-assembling biomaterials for tissue engineering. Trends Biotechnol 27, 423-433 (2009).
20. Gelain, F., Bottai, D., Vescovi, A. & Zhang, S. Designer self-assembling peptide nanofiber scaffolds for adult mouse neural stem cell 3-dimensional cultures. PLoS One 1, e119 (2006).
21. Nishimura, A. et al. Controlled release of insulin from self-assembling nanofiber hydrogel, PuraMatrix™ : application for the subcutaneous injection in rats. Eur J Pharm Sci 45, 1-7 (2012).
22. Davis, M. E. et al. Local myocardial insulin-like growth factor 1 (IGF-1) delivery with biotinylated peptide nanofibers improves cell therapy for myocardial infarction. Proc Natl Acad Sci USA 103, 8155-8160 (2006).
23. Hsieh, P. C., MacGillivray, C., Gannon, J., Cruz, F. U. & Lee, R. T. Local controlled intramyocardial delivery of platelet-derived growth factor improves postinfarction ventricular function without pulmonary toxicity. Circulation 114, 637-644 (2006).
24. Petrovsky, N. & Aguilar, J. C. Vaccine adjuvants: current state and future trends. Immunol Cell Biol 82, 488-496 (2004).
25. Bode, C., Zhao, G., Steinhagen, F., Kinjo, T. & Klinman, D. M. CpG DNA as a vaccine adjuvant. Expert Rev Vaccines 10, 499-511 (2011).
26. Sparwasser, T. et al. Macrophages sense pathogens via DNA motifs: induction of tumor necrosis factor-alpha-mediated shock. Eur J Immunol 27, 1671-1679 (1997).
27. Jakob, T., Walker, P. S., Krieg, A. M., Udey, M. C. & Vogel, J. C. Activation of cutaneous dendritic cells by CpG-containing oligodeoxynucleotides: a role for dendritic cells in the augmentation of Th1 responses by immunostimulatory DNA. J Immunol 161, 3042-3049 (1998).
28. Klinman, D. M. et al. CpG DNA: recognition by and activation of monocytes. Microbes Infect 4, 897-901 (2002).
29. Lipford, G. B. et al. Immunostimulatory DNA: sequence-dependent production of potentially harmful or useful cytokines. Eur J Immunol 27, 3420-3426 (1997).
30. Stern, B. V., Boehm, B. O. & Tary-Lehmann, M. Vaccination with tumor peptide in CpG adjuvant protects via IFN-gammadependent CD4 cell immunity. J Immunol 168, 6099-6105 (2002).
31. Krieg, A. M., Love-Homan, L., Yi, A. K. & Harty, J. T. CpG DNA induces sustained IL-12 expression in vivo and resistance to Listeria monocytogenes challenge. J Immunol 161, 2428-2434 (1998).
32. Zonneveld-Huijssoon, E. et al. TLR9 agonist CpG enhances protective nasal HSP60 peptide vaccine efficacy in experimental autoimmune arthritis. Ann Rheum Dis 71, 1706-1715 (2012).
33. Quintana, F. J., Rotem, A., Carmi, P. & Cohen, I. R. Vaccination with empty plasmid DNA or CpG oligonucleotide inhibits diabetes in nonobese diabetic mice: modulation of spontaneous 60-kDa heat shock protein autoimmunity. J Immunol 165, 6148-6155 (2000).
34. Mellor, A. L. et al. Cutting edge: CpG oligonucleotides induce splenic CD19+ dendritic cells to acquire potent indoleamine 2,3-dioxygenase-dependent T cell regulatory functions via IFN Type 1 signaling. J Immunol 175, 5601-5605 (2005).
35. Shi, Y. et al. Granulocyte-macrophage colony-stimulating factor (GM-CSF) and T-cell responses: what we do and don't know. Cell Res 16, 126-133 (2006).
36. Hartoonian, C. et al. Effect of immunological adjuvants: GM-CSF (granulocyte-monocyte colony stimulating factor) and IL-23 (interleukin-23) on immune responses generated against hepatitis C virus core DNA vaccine. Cytokine 46, 43-50 (2009).
37. Koutsopoulos, S., Unsworth, L. D., Nagai, Y. & Zhang, S. Controlled release of functional proteins through designer selfassembling peptide nanofiber hydrogel scaffold. Proc Natl Acad Sci USA 106, 4623-4628 (2009).
38. Lü, J. M. et al. Current advances in research and clinical applications of PLGA-based nanotechnology. Expert Rev Mol Diagn 9, 325-341 (2009).
39. Preis, I. & Langer, R. S. A single-step immunization by sustained antigen release. J Immunol Methods 28, 193-197 (1979).
40. Ali, O. A., Huebsch, N., Cao, L., Dranoff, G. & Mooney, D. J. Infection-mimicking materials to program dendritic cells in situ. Nat Mater 8, 151-158 (2009).
41. Serhan, C. N. & Savill, J. Resolution of inflammation: the beginning programs the end. Nat Immunol 6, 1191-1197 (2005).
42. Serhan, C. N. et al. Resolution of inflammation: state of the art, definitions and terms. FASEB J 21, 325-332 (2007).
43. Singh, A., Suri, S. & Roy, K. In-situ crosslinking hydrogels for combinatorial delivery of chemokines and siRNA-DNA carrying microparticles to dendritic cells. Biomaterials 30, 5187-5200 (2009).
44. Singh, A. 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, 184-192 (2011).
45. Gower, R. M. et al. Modulation of leukocyte infiltration and phenotype in microporous tissue engineering scaffolds via vector induced IL-10 expression. Biomaterials 35, 2024-2031 (2014).
46. Hudalla, G. A. et al. A self-adjuvanting supramolecular vaccine carrying a folded protein antigen. Adv Healthc Mater 2, 1114-1119 (2013).
47. Hudalla, G. A. et al. Gradated assembly of multiple proteins into supramolecular nanomaterials. Nat Mater 13, 829-836 (2014).
48. Glowacki, A. J. et al. Prevention of inflammation-mediated bone loss in murine and canine periodontal disease via recruitment of regulatory lymphocytes. Proc Natl Acad Sci USA 110, 18525-18530 (2013).
49. Araujo-Pires, A. C. et al. IL-4/CCL22/CCR4 Axis Controls Regulatory T Cell Migration That Suppress Inflammatory Bone Loss in Murine Experimental Periodontitis. J Bone Miner Res 30, 400-410 (2015).
50. Stachowiak, A. N. & Irvine, D. J. Inverse opal hydrogel-collagen composite scaffolds as a supportive microenvironment for immune cell migration. J Biomed Mater Res A 85, 815-828 (2008).
51. Jain, S., Yap, W. T. & Irvine, D. J. Synthesis of protein-loaded hydrogel particles in an aqueous two-phase system for coincident antigen and CpG oligonucleotide delivery to antigen-presenting cells. Biomacromolecules 6, 2590-2600 (2005).
52. Shankar, S. P., Chen, I. I., Keselowsky, B. G., García, A. J. & Babensee, J. E. Profiles of carbohydrate ligands associated with adsorbed proteins on self-assembled monolayers of defined chemistries. J Biomed Mater Res A 92, 1329-1342 (2010).
53. Choe, S. W., Acharya, A. P., Keselowsky, B. G. & Sorg, B. S. Intravital microscopy imaging of macrophage localization to immunogenic particles and co-localized tissue oxygen saturation. Acta Biomater 6, 3491-3498 (2010).
54. Acharya, A. P., Dolgova, N. V., Clare-Salzler, M. J. & Keselowsky, B. G. Adhesive substrate-modulation of adaptive immune responses. Biomaterials 29, 4736-4750 (2008).
55. Acharya, A. P., Clare-Salzler, M. J. & Keselowsky, B. G. A high-throughput microparticle microarray platform for dendritic celltargeting vaccines. Biomaterials 30, 4168-4177 (2009).
56. Acharya, A. P. et al. The modulation of dendritic cell integrin binding and activation by RGD-peptide density gradient substrates. Biomaterials 31, 7444-7454 (2010).
57. Acharya, A. P., Dolgova, N. V., Xia, C. Q., Clare-Salzler, M. J. & Keselowsky, B. G. Adhesive substrates modulate the activation and stimulatory capacity of non-obese diabetic mouse-derived dendritic cells. Acta Biomater 7, 180-192 (2011).
58. Zaveri, T. D. et al. Contributions of surface topography and cytotoxicity to the macrophage response to zinc oxide nanorods. Biomaterials 31, 2999-3007 (2010).
59. Zaveri, T. D., Lewis, J. S., Dolgova, N. V., Clare-Salzler, M. J. & Keselowsky, B. G. Integrin-directed modulation of macrophage responses to biomaterials. Biomaterials 35, 3504-3515 (2014).
60. Lewis, J. S. et al. The effect of cyclic mechanical strain on activation of dendritic cells cultured on adhesive substrates. Biomaterials 34, 9063-9070 (2013).
61. Tsai, S. et al. Reversal of autoimmunity by boosting memory-like autoregulatory T cells. Immunity 32, 568-580 (2010).
62. Phillips, B. et al. A microsphere-based vaccine prevents and reverses new-onset autoimmune diabetes. Diabetes 57, 1544-1555 (2008).
63. Semino, C. E., Merok, J. R., Crane, G. G., Panagiotakos, G. & Zhang, S. Functional differentiation of hepatocyte-like spheroid structures from putative liver progenitor cells in three-dimensional peptide scaffolds. Differentiation 71, 262-270 (2003).
64. Holmes, T. C. et al. Extensive neurite outgrowth and active synapse formation on self-assembling peptide scaffolds. Proc Natl Acad Sci USA 97, 6728-6733 (2000).
65. Narmoneva, D. A. et al. Self-assembling short oligopeptides and the promotion of angiogenesis. Biomaterials 26, 4837-4846 (2005).
66. Hsieh, P. C., Davis, M. E., Gannon, J., MacGillivray, C. & Lee, R. T. Controlled delivery of PDGF-BB for myocardial protection using injectable self-assembling peptide nanofibers. J Clin Invest 116, 237-248 (2006).
67. Orban, T. et al. Autoantigen-specific regulatory T cells induced in patients with type 1 diabetes mellitus by insulin B-chain immunotherapy. J Autoimmun 34, 408-415 (2010).
68. Ludvigsson, J. et al. Extended evaluation of the safety and efficacy of GAD treatment of children and adolescents with recentonset type 1 diabetes: a randomised controlled trial. Diabetologia 54, 634-640 (2011).
69. Wherrett, D. K. et al. Antigen-based therapy with glutamic acid decarboxylase (GAD) vaccine in patients with recent-onset type 1 diabetes: a randomised double-blind trial. Lancet 378, 319-327 (2011).
70. Vollmer, J. & Krieg, A. M. Immunotherapeutic applications of CpG oligodeoxynucleotide TLR9 agonists. Adv Drug Deliv Rev 61, 195-204 (2009).
71. Barber, G. N. Cytoplasmic DNA innate immune pathways. Immunol Rev 243, 99-108 (2011).
72. Lambrecht, B. N., Kool, M., Willart, M. A. & Hammad, H. Mechanism of action of clinically approved adjuvants. Curr Opin Immunol 21, 23-29 (2009).
73. Nicholas, D., Odumosu, O. & Langridge, W. H. Autoantigen based vaccines for type 1 diabetes. Discov Med 11, 293-301 (2011).
74. Johansen, P. et al. Toll-like receptor ligands as adjuvants in allergen-specific immunotherapy. Clin Exp Allergy 35, 1591-1598 (2005).
75. Haddad, D. et al. Plasmid vaccine expressing granulocyte-macrophage colony-stimulating factor attracts infiltrates including immature dendritic cells into injected muscles. J Immunol 165, 3772-3781 (2000).
76. Sylvester, R. K. Clinical applications of colony-stimulating factors: a historical perspective. Am J Health Syst Pharm 59, S6-12 (2002).
77. Basak, S. K. et al. Increased dendritic cell number and function following continuous in vivo infusion of granulocyte macrophagecolony-stimulating factor and interleukin-4. Blood 99, 2869-2879 (2002).
78. Cheatem, D., Ganesh, B. B., Gangi, E., Vasu, C. & Prabhakar, B. S. Modulation of dendritic cells using granulocyte-macrophage colony-stimulating factor (GM-CSF) delays type 1 diabetes by enhancing CD4+ CD25+ regulatory T cell function. Clin Immunol 131, 260-270 (2009).
79. Steinbrink, K., Graulich, E., Kubsch, S., Knop, J. & Enk, A. H. CD4(+ ) and CD8(+ ) anergic T cells induced by interleukin-10-treated human dendritic cells display antigen-specific suppressor activity. Blood 99, 2468-2476 (2002).
80. Steinman, R. M., Hawiger, D. & Nussenzweig, M. C. Tolerogenic dendritic cells. Annu Rev Immunol 21, 685-711 (2003).
81. Gaudreau, S. et al. Granulocyte-macrophage colony-stimulating factor prevents diabetes development in NOD mice by inducing tolerogenic dendritic cells that sustain the suppressive function of CD4+ CD25+ regulatory T cells. J Immunol 179, 3638-3647 (2007).
82. Gaudreau, S. et al. GM-CSF induces bone marrow precursors of NOD mice to skew into tolerogenic dendritic cells that protect against diabetes. Cell Immunol 265, 31-36 (2010).
83. Yamaguchi, Y. et al. Insulin-loaded biodegradable PLGA microcapsules: initial burst release controlled by hydrophilic additives. J Control Release 81, 235-249 (2002).
84. Krieg, A. M. Therapeutic potential of Toll-like receptor 9 activation. Nat Rev Drug Discov 5, 471-484 (2006).
85. Flores, R. R., Diggs, K. A., Tait, L. M. & Morel, P. A. IFN-gamma negatively regulates CpG-induced IL-10 in bone marrowderived dendritic cells. J Immunol 178, 211-218 (2007).
86. Waibler, Z. et al. Excessive CpG 1668 stimulation triggers IL-10 production by cDC that inhibits IFN-alpha responses by pDC. Eur J Immunol 38, 3127-3137 (2008).
87. Beebe, A. M., Cua, D. J. & De Waal Malefyt, R. The role of interleukin-10 in autoimmune disease: systemic lupus erythematosus (SLE) and multiple sclerosis (MS). Cytokine Growth Factor Rev 13, 403-412 (2002).
88. Pennline, K. J., Roque-Gaffney, E. & Monahan, M. Recombinant human IL-10 prevents the onset of diabetes in the nonobese diabetic mouse. Clin Immunol Immunopathol 71, 169-175 (1994).
89. Goudy, K. et al. Adeno-associated virus vector-mediated IL-10 gene delivery prevents type 1 diabetes in NOD mice. Proc Natl Acad Sci USA 98, 13913-13918 (2001).
90. Slavin, A. J., Maron, R. & Weiner, H. L. Mucosal administration of IL-10 enhances oral tolerance in autoimmune encephalomyelitis and diabetes. Int Immunol 13, 825-833 (2001).
91. Zheng, X. X. et al. A noncytolytic IL-10/Fc fusion protein prevents diabetes, blocks autoimmunity, and promotes suppressor phenomena in NOD mice. J Immunol 158, 4507-4513 (1997).