Peptides Derived from the Tight Junction Protein CLDN1 Disrupt the Skin Barrier and Promote Responsiveness to an Epicutaneous Vaccine
Keratinocytes express many pattern recognition receptors that enhance the skin’s adaptive immune response to epicutaneous antigens. We have shown that these pattern recognition receptors are expressed below tight junctions (TJ), strongly implicating TJ disruption as a critical step in antigen respon...
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| Published in: | Journal of investigative dermatology Vol. 140; no. 2; pp. 361 - 369.e3 |
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01-02-2020
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| Abstract | Keratinocytes express many pattern recognition receptors that enhance the skin’s adaptive immune response to epicutaneous antigens. We have shown that these pattern recognition receptors are expressed below tight junctions (TJ), strongly implicating TJ disruption as a critical step in antigen responsiveness. To disrupt TJs, we designed peptides inspired by the first extracellular loop of the TJ transmembrane protein CLDN1. These peptides transiently disrupted TJs in the human lung epithelial cell line 16HBE and delayed TJ formation in primary human keratinocytes. Building on these observations, we tested whether vaccinating mice with an epicutaneous influenza patch containing TJ-disrupting peptides was an effective strategy to elicit an immunogenic response. Application of a TJ-disrupting peptide patch resulted in barrier disruption as measured by increased transepithelial water loss. We observed a significant increase in antigen-specific antibodies when we applied patches with TJ-disrupting peptide plus antigen (influenza hemagglutinin) in either a patch-prime or a patch-boost model. Collectively, these observations demonstrate that our designed peptides perturb TJs in human lung as well as human and murine skin epithelium, enabling epicutaneous vaccine delivery. We anticipate that this approach could obviate currently used needle-based vaccination methods that require administration by health care workers and biohazard waste removal. |
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| AbstractList | Keratinocytes express many pattern recognition receptors that enhance the skin's adaptive immune response to epicutaneous antigens. We have shown that these pattern recognition receptors are expressed below tight junctions (TJ), strongly implicating TJ disruption as a critical step in antigen responsiveness. To disrupt TJs, we designed peptides inspired by the first extracellular loop of the TJ transmembrane protein CLDN1. These peptides transiently disrupted TJs in the human lung epithelial cell line 16HBE and delayed TJ formation in primary human keratinocytes. Building on these observations, we tested whether vaccinating mice with an epicutaneous influenza patch containing TJ-disrupting peptides was an effective strategy to elicit an immunogenic response. Application of a TJ-disrupting peptide patch resulted in barrier disruption as measured by increased transepithelial water loss. We observed a significant increase in antigen-specific antibodies when we applied patches with TJ-disrupting peptide plus antigen (influenza hemagglutinin) in either a patch-prime or a patch-boost model. Collectively, these observations demonstrate that our designed peptides perturb TJs in human lung as well as human and murine skin epithelium, enabling epicutaneous vaccine delivery. We anticipate that this approach could obviate currently used needle-based vaccination methods that require administration by health care workers and biohazard waste removal. |
| Author | Beck, Lisa A. De Benedetto, Anna Pandya, Radha P. Miller, Benjamin L. Hilimire, Thomas A. Brewer, Matthew G. Yoshida, Takeshi Martinez-Sobrido, Luis Anderson, Elizabeth A. |
| Author_xml | – sequence: 1 givenname: Matthew G. orcidid: 0000-0001-7631-5234 surname: Brewer fullname: Brewer, Matthew G. organization: Department of Dermatology, University of Rochester Medical Center, Rochester, New York, USA – sequence: 2 givenname: Elizabeth A. orcidid: 0000-0002-6425-5278 surname: Anderson fullname: Anderson, Elizabeth A. organization: Department of Dermatology, University of Rochester Medical Center, Rochester, New York, USA – sequence: 3 givenname: Radha P. orcidid: 0000-0002-3105-1666 surname: Pandya fullname: Pandya, Radha P. organization: Department of Dermatology, University of Rochester Medical Center, Rochester, New York, USA – sequence: 4 givenname: Anna orcidid: 0000-0001-6293-435X surname: De Benedetto fullname: De Benedetto, Anna organization: Department of Dermatology, University of Rochester Medical Center, Rochester, New York, USA – sequence: 5 givenname: Takeshi orcidid: 0000-0003-0133-5067 surname: Yoshida fullname: Yoshida, Takeshi organization: Department of Dermatology, University of Rochester Medical Center, Rochester, New York, USA – sequence: 6 givenname: Thomas A. orcidid: 0000-0001-7677-3016 surname: Hilimire fullname: Hilimire, Thomas A. organization: Department of Microbiology and Immunology, University of Rochester Medical Center, Rochester, New York, USA – sequence: 7 givenname: Luis orcidid: 0000-0001-7084-0804 surname: Martinez-Sobrido fullname: Martinez-Sobrido, Luis organization: Department of Microbiology and Immunology, University of Rochester Medical Center, Rochester, New York, USA – sequence: 8 givenname: Lisa A. orcidid: 0000-0002-8452-667X surname: Beck fullname: Beck, Lisa A. email: lisa_beck@URMC.rochester.edu organization: Department of Dermatology, University of Rochester Medical Center, Rochester, New York, USA – sequence: 9 givenname: Benjamin L. orcidid: 0000-0001-9168-8047 surname: Miller fullname: Miller, Benjamin L. email: benjamin_miller@URMC.rochester.edu organization: Department of Dermatology, University of Rochester Medical Center, Rochester, New York, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31381894$$D View this record in MEDLINE/PubMed |
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| Title | Peptides Derived from the Tight Junction Protein CLDN1 Disrupt the Skin Barrier and Promote Responsiveness to an Epicutaneous Vaccine |
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