Winner of the Student Award in the Hospital Intern Category, 10th World Biomaterials Congress, May 17-22, 2016, Montreal QC, Canada: Peptide biomaterials raising adaptive immune responses in wound healing contexts: Immunogenic Materials in Healing Wounds
Open accessAbstract
Biomaterials used in the context of tissue engineering or wound repair are commonly designed to be "nonimmunogenic." However, previously it has been observed that self-assembled peptide nanofiber materials are noninflammatory despite their immunogenicity, suggesting that they may be appropriate for use in wound-healing contexts. To test this hypothesis, mice were immunized with epitope-containing peptide self-assemblies until they maintained high antibody titers against the material, then gels of the same peptide assemblies were applied within full-thickness dermal wounds. In three different murine dermal-wounding models with different baseline healing rates, even significantly immunogenic peptide assemblies did not delay healing. Conversely, adjuvanted peptide assemblies, while raising similar antibody titers to unadjuvanted assemblies, did delay wound healing. Analysis of the healing wounds indicated that compared to adjuvanted peptide assemblies, the unadjuvanted assemblies exhibited a progression of the dominant T-cell subset from CD4(+) to CD8(+) cells in the wound, and CD4(+) cell populations displayed a more Th2-slanted response. These findings illustrate an example of a significant antibiomaterial adaptive immune response that does not adversely affect wound healing despite ongoing antibody production. This material would thus be considered "immunologically compatible" in this specific context rather than "nonimmunogenic," a designation that is expected to apply to a range of other protein- and peptide-based biomaterials in wound-healing and tissue-engineering applications. © 2016 Wiley Periodicals, Inc. J Biomed Mater Res Part A: 104A: 1853-1862, 2016.
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Certain recombinant proteins and self-assembling peptides are immunogenic.
“Certain recombinant proteins and self-assembling peptides are immunogenic214–218.”
From Towards organoid culture without Matrigel (2021) · cites this paper as [214]
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Cites
Inflammation in Wound Repair: Molecular and Cellular Mechanisms
Eming, S. A., Krieg, T., & Davidson, J. M. (2007) · Journal of Investigative Dermatology · doi:10.1038/sj.jid.5700701 · Cited by 2,429 · see citing works
Selective Differentiation of Neural Progenitor Cells by High-Epitope Density Nanofibers
Silva, G. A., Czeisler, C. M., Niece, K. L., Beniash, E., Harrington, D. A., Kessler, J. A., & Stupp, S. I. (2004) · Science · doi:10.1126/science.1093783 · Cited by 2,169 · see citing works
Mesenchymal Stem Cells Enhance Wound Healing Through Differentiation and Angiogenesis
Wu, Y., Chen, L., Scott, P. G., & Tredget, E. E. (2007) · Stem Cells · doi:10.1634/stemcells.2007-0226 · Cited by 1,680 · see citing works
Nanotechnological strategies for engineering complex tissues
Dvir, T., Timko, B. P., Kohane, D. S., & Langer, R. (2011) · Nature Nanotechnology · doi:10.1038/nnano.2010.246 · Cited by 1,367 · see citing works
Designing peptide based nanomaterials
Ulijn, R. V., & Smith, A. M. (2008) · Chemical Society Reviews · doi:10.1039/b609047h · Cited by 1,139 · see citing works
Kisiday, J. D., Jin, M. M., Kurz, B., Hung, H.-H. K., Semino, C. E., Zhang, S., & Grodzinsky, A. J. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.142309999 · Cited by 1,045 · see citing works
Immune response to biologic scaffold materials
Badylak, S. F., & Gilbert, T. W. (2008) · Seminars in Immunology · doi:10.1016/j.smim.2007.11.003 · Cited by 857 · see citing works
Quantitative and reproducible murine model of excisional wound healing
Galiano, R. D., Michaels, V. J., Dobryansky, M., Levine, J. P., & Gurtner, G. C. (2004) · Wound Repair and Regeneration · doi:10.1111/j.1067-1927.2004.12404.x · Cited by 743 · see citing works
PDGF and FGF stimulate wound healing in the genetically diabetic mouse.
Greenhalgh, D. G., Sprugel, K. H., Murray, M. J., & Ross, R. (1990) · Europe PMC (PubMed Central) · Cited by 681 · see citing works
Hamley, I. W. (2007) · Angewandte Chemie International Edition · doi:10.1002/anie.200700861 · Cited by 619 · see citing works
Understanding the role of immune regulation in wound healing
Park, J. E., & Barbul, A. (2004) · The American Journal of Surgery · doi:10.1016/s0002-9610(03)00296-4 · Cited by 590 · see citing works
A self-assembling peptide acting as an immune adjuvant
Rudra, J. S., Tian, Y. F., Jung, J. P., & Collier, J. H. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0912124107 · Cited by 523 · see citing works
Self-citationSelf-assembling peptide scaffolds for regenerative medicine
Matson, J. B., & Stupp, S. I. (2011) · Chemical Communications · doi:10.1039/c1cc15551b · Cited by 502 · see citing works
Aguilar, J. C., & Rodríguez, E. G. (2007) · Vaccine · doi:10.1016/j.vaccine.2007.01.111 · Cited by 499 · see citing works
The mouse excisional wound splinting model, including applications for stem cell transplantation
Wang, X., Ge, J., Tredget, E. E., & Wu, Y. (2013) · Nature Protocols · doi:10.1038/nprot.2013.002 · Cited by 439 · see citing works
XENOGENEIC EXTRACELLULAR MATRIX GRAFTS ELICIT A TH2-RESTRICTED IMMUNE RESPONSE1
Allman, A. J., McPherson, T. B., Badylak, S. F., Merrill, L. C., Kallakury, B., Sheehan, C., Raeder, R. H., & Metzger, D. W. (2001) · Transplantation · doi:10.1097/00007890-200106150-00024 · Cited by 388 · see citing works
Interrelation of immunity and tissue repair or regeneration
Eming, S. A., Hammerschmidt, M., Krieg, T., & Roers, A. (2009) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2009.04.009 · Cited by 321 · see citing works
Schierle, C. F., De la Garza, M., Mustoe, T. A., & Galiano, R. D. (2009) · Wound Repair and Regeneration · doi:10.1111/j.1524-475x.2009.00489.x · Cited by 311 · see citing works
Modulating Adaptive Immune Responses to Peptide Self-Assemblies
Rudra, J. S., Sun, T., Bird, K., Daniels, M. D., Gasiorowski, J. Z., Chong, A. S., & Collier, J. H. (2012) · ACS Nano · doi:10.1021/nn204530r · Cited by 277 · see citing works
Self-citationGradated assembly of multiple proteins into supramolecular nanomaterials
Hudalla, G. A., Sun, T., Gasiorowski, J. Z., Han, H., Tian, Y., Chong, A. S., & Collier, J. H. (2014) · Nature Materials · doi:10.1038/nmat3998 · Cited by 268 · see citing works
Self-citationThe Th1/Th2 paradigm and the allograft response
Strom, T. B. (1996) · Current Opinion in Immunology · doi:10.1016/s0952-7915(96)80087-2 · Cited by 265 · see citing works
Black, M., Trent, A. M., Kostenko, Y., et al. (2012) · Advanced Materials · doi:10.1002/adma.201200209 · Cited by 239 · see citing works
Peptide-directed self-assembly of hydrogels
Kopec̆ek, J., & Yang, J. (2008) · Acta Biomaterialia · doi:10.1016/j.actbio.2008.10.001 · Cited by 222 · see citing works
Co-assembling peptides as defined matrices for endothelial cells
Jung, J. P., Nagaraj, A. K., Fox, E. K., Rudra, J. S., Devgun, J. M., & Collier, J. H. (2009) · Biomaterials · doi:10.1016/j.biomaterials.2009.01.033 · Cited by 219 · see citing works
Self-citationSelf-assembled peptide nanofibers raising durable antibody responses against a malaria epitope
Rudra, J. S., Mishra, S., Chong, A. S., Mitchell, R. A., Nardin, E. H., Nussenzweig, V., & Collier, J. H. (2012) · Biomaterials · doi:10.1016/j.biomaterials.2012.05.041 · Cited by 176 · see citing works
Self-citationChen, J., Pompano, R. R., Santiago, F. W., Maillat, L., Sciammas, R., Sun, T., Han, H., Topham, D. J., Chong, A. S., & Collier, J. H. (2013) · Biomaterials · doi:10.1016/j.biomaterials.2013.07.063 · Cited by 169 · see citing works
Self-citationThe Effect of In Vivo T Helper and T Suppressor Lymphocyte Depletion on Wound Healing
Barbul, A., Breslin, R. J., WOODYARD, J. P., Wasserkrug, H. L., & Efron, G. (1989) · Annals of Surgery · doi:10.1097/00000658-198904000-00015 · Cited by 156 · see citing works
Jung, J. P., Jones, J. L., Cronier, S. A., & Collier, J. H. (2008) · Biomaterials · doi:10.1016/j.biomaterials.2008.01.008 · Cited by 151 · see citing works
Self-citationFibrillar peptide gels in biotechnology and biomedicine
Jung, J. P., Gasiorowski, J. Z., & Collier, J. H. (2010) · Biopolymers · doi:10.1002/bip.21326 · Cited by 145 · see citing works
Self-citationSelf-assembling Peptides: From Bio-inspired Materials to Bone Regeneration
Semino, C. E. (2008) · Journal of Dental Research · doi:10.1177/154405910808700710 · Cited by 142 · see citing works
Pompano, R. R., Chen, J., Verbus, E. A., et al. (2014) · Advanced Healthcare Materials · doi:10.1002/adhm.201400137 · Cited by 127 · see citing works
Scarless skin repair in immunodeficient mice
Gawrońska‐Kozak, B., Bogacki, M., Rim, J., Monroe, W. T., & Manuel, J. A. (2006) · Wound Repair and Regeneration · doi:10.1111/j.1743-6109.2006.00121.x · Cited by 127 · see citing works
Significance of T-lymphocytes in wound healing.
Peterson, J. M., Barbul, A., Breslin, R. J., Wasserkrug, H. L., & Efron, G. (1987) · PubMed · Cited by 127 · see citing works
Systemically and Topically Administered Leptin Both Accelerate Wound Healing in Diabetic ob/ob Mice
Ring, B. D., Scully, S. A., Davis, C. R., Baker, M. B., Cullen, M. J., Pelleymounter, M. A., & Danilenko, D. M. (2000) · Endocrinology · doi:10.1210/endo.141.1.7373 · Cited by 121 · see citing works
Jung, J. P., Moyano, J. V., & Collier, J. H. (2011) · Integrative Biology · doi:10.1039/c0ib00112k · Cited by 116 · see citing works
Self-citationIwata, Y., Yoshizaki, A., Komura, K., Shimizu, K., Ogawa, F., Hara, T., Muroi, E., Bae, S., Takenaka, M., Yukami, T., et al. (2009) · The American Journal of Pathology · doi:10.2353/ajpath.2009.080355 · Cited by 107 · see citing works
The role of lymphocytes in wound healing
Martin, C., & Muir, I. F. K. (1990) · British Journal of Plastic Surgery · doi:10.1016/0007-1226(90)90185-3 · Cited by 106 · see citing works
Inflammatory cell subpopulations in keloid scars
Boyce, D. E., Ciampolini, J., Ruge, F., Harding, K. G., & Murison, M. S. C. (2001) · British Journal of Plastic Surgery · doi:10.1054/bjps.2001.3638 · Cited by 104 · see citing works
Morphologic Assessment Using Monoclonal Antibodies
Fishel, R. S., Barbul, A., Beschorner, W. E., Wasserkrug, H. L., & Efron, G. (1987) · Annals of Surgery · doi:10.1097/00000658-198707000-00004 · Cited by 103 · see citing works
Immune Response to Small Intestinal Submucosa (Surgisis) Implant in Humans: Preliminary Observations
Ansaloni, L., Cambrini, P., Catena, F., Saverio, S. D., GAGLIARDI, S., Gazzotti, F., Hodde, J. P., Metzger, D. W., D'Alessandro, L., & Pinna, A. D. (2007) · Journal of Investigative Surgery · doi:10.1080/08941930701481296 · Cited by 99 · see citing works
Wound healing and T-lymphocytes
Efron, J. E., Frankel, H. L., Lazarou, S. A., et al. (1990) · Journal of Surgical Research · doi:10.1016/0022-4804(90)90013-r · Cited by 98 · see citing works
Local delivery of proteins and the use of self-assembling peptides
Segers, V. F. M., & Lee, R. T. (2007) · Drug Discovery Today · doi:10.1016/j.drudis.2007.05.003 · Cited by 92 · see citing works
Peptide Amphiphile Micelles Self-Adjuvant Group A Streptococcal Vaccination
Trent, A. M., Ulery, B. D., Black, M., et al. (2014) · The AAPS Journal · doi:10.1208/s12248-014-9707-3 · Cited by 92 · see citing works
Effect of CD4+ and CD8+ cell depletion on wound healing
Davis, P. A., Corless, D., Aspinall, R., et al. (2001) · British journal of surgery · doi:10.1046/j.1365-2168.2001.01665.x · Cited by 83 · see citing works
Validation of a Model for the Study of Multiple Wounds in the Diabetic Mouse (db/db)
Sullivan, S. R., Underwood, R. A., Gibran, N. S., et al. (2004) · Plastic & Reconstructive Surgery · doi:10.1097/01.prs.0000105044.03230.f4 · Cited by 82 · see citing works
Antibodies to wounded tissue enhance cutaneous wound healing
Nishio, N., Ito, S., Suzuki, H., & Isobe, K. (2009) · Immunology · doi:10.1111/j.1365-2567.2009.03119.x · Cited by 69 · see citing works
A Wound Healing Model Using Healing‐impaired Diabetic Mice
Tsuboi, R., Shi, C., Rifkin, D. B., & Ogawa, H. (1992) · The Journal of Dermatology · doi:10.1111/j.1346-8138.1992.tb03757.x · Cited by 67 · see citing works
Fibrillized peptide microgels for cell encapsulation and 3D cell culture
Tian, Y. F., Devgun, J. M., & Collier, J. H. (2011) · Soft Matter · doi:10.1039/c1sm05504f · Cited by 62 · see citing works
Self-citationRodriguez, A., Voskerician, G., Meyerson, H. J., MacEwan, S. R., & Anderson, J. M. (2007) · Journal of Biomedical Materials Research Part A · doi:10.1002/jbm.a.31562 · Cited by 54 · see citing works
Controllably degradable β-sheet nanofibers and gels from self-assembling depsipeptides
Tian, Y., Hudalla, G. A., Han, H., & Collier, J. H. (2013) · Biomaterials Science · doi:10.1039/c3bm60161g · Cited by 46 · see citing works
Self-citationThe Regulatory Role of T Lymphocytes in Wound Healing
Barbul, A., & REGAN, M. C. (1990) · The Journal of Trauma: Injury, Infection, and Critical Care · doi:10.1097/00005373-199012001-00021 · Cited by 45 · see citing works
The potential role of the lymphocyte in fetal wound healing
Adolph, V. R., DiSanto, S. K., Bleacher, J. C., Dillon, P. W., & Krummel, T. M. (1993) · Journal of Pediatric Surgery · doi:10.1016/s0022-3468(05)80320-3 · Cited by 39 · see citing works
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Towards organoid culture without Matrigel
Kozlowski, M. T., Crook, C. J., & Ku, H. T. (2021) · Communications Biology · doi:10.1038/s42003-021-02910-8 · Cited by 409 · see citing works
Peptide-Based Functional Biomaterials for Soft-Tissue Repair
Hosoyama, K., Lazurko, C., Muñoz, M., McTiernan, C. D., & Alarcon, E. I. (2019) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2019.00205 · Cited by 118 · see citing works
- Authors
- Vigneswaran, Y., Han, H., De Loera, R., Wen, Y., Zhang, X., Sun, T., Mora-Solano, C., & Collier, J. H.
- Affiliations
- University of Chicago (US)
- Department of Surgery; University of Chicago; Chicago Illinois
- Duke University (US)
- Corresponding author
- Collier, Joel H.
- Venue
- Journal of Biomedical Materials Research Part A
- Publisher
- Wiley
- Published
- 2016-05-26
- Volume
- 104
- Issue
- 8
- Pages
- 1853-1862
- ISSN
- 1549-3296 (ISSN-L)
- PMC
- PMC4988660
- OpenAlex
- W2766172417
- Cited by
- 26
- References
- 52
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 5 · 2022: 1 · 2021: 4 · 2020: 1 · 2019: 1 · 2018: 2 · 2017: 4 · 2016: 2
- FWCI
- 3.21
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Biomedical Materials Research Part A (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Biomedical Imaging and Bioengineering (1R01EB009701)
- National Institute of Allergy and Infectious Diseases (1R01AI118182)
- Topics
- Health Sciences › Medicine › Rehabilitation › Wound Healing and Treatments
- Physical Sciences › Materials Science › Biomaterials › Supramolecular Self-Assembly in Materials
- Physical Sciences › Materials Science › Biomaterials › Electrospun Nanofibers in Biomedical Applications
- Keywords
- adaptive immune response, wound healing, immunogenicity, adjuvants, skin wounds, T cell subsets, Th2 immune response, tissue engineering scaffolds
- MeSH terms
- Adjuvants, Immunologic, Amino Acid Sequence, Animals, Antibody Formation, Awards and Prizes, Biocompatible Materials, Freund's Adjuvant, Internship and Residency, Mice, Inbred C57BL, Ovalbumin, Peptides, Phenotype, T-Lymphocytes, Wound Healing, Cytokines, Tissue Scaffolds, Adaptive Immunity, Nanofibers
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