Multiple Functions of the New Cytokine-Based Antimicrobial Peptide Thymic Stromal Lymphopoietin (TSLP)
"> Figure 1
<p>TSLP transcript variants and protein isoforms. (<b>A</b>) Graphics showing the TSLP gene (green), the long form, and short form transcripts (blue), and the protein products (red). Long (NM_033035.4, NP_149024.1) and short (NM_138551.3, NP_612561.2) transcript and protein variants, respectively, are indicated (NCBI). (<b>B</b>) Amino acid sequence of human TSLP isoforms. The putative signal sequences of the TSLP isoforms are marked in blue, and the mature protein in black. N-linked glycosylation sites are marked green, and methionine start codons are marked red. Bold black characters indicate the position of MKK34. (<b>C</b>) JNet secondary structure prediction of lfTSLP based on the amino acid sequence. Helices are marked as red tubes, and sheets are marked as green arrows. JNETCONF: The confidence estimate for the prediction, high values indicate high confidence. Modified from the web-based application Jpred (The Barton Group, School of Life Sciences, University of Dundee, UK). (<b>D</b>) Three-dimensional structure (Swiss-model, [<a href="#B9-pharmaceuticals-09-00041" class="html-bibr">9</a>]) of lfTSLP (<b>left</b>) and sfTSLP (<b>right</b>).</p> "> Figure 1 Cont.
<p>TSLP transcript variants and protein isoforms. (<b>A</b>) Graphics showing the TSLP gene (green), the long form, and short form transcripts (blue), and the protein products (red). Long (NM_033035.4, NP_149024.1) and short (NM_138551.3, NP_612561.2) transcript and protein variants, respectively, are indicated (NCBI). (<b>B</b>) Amino acid sequence of human TSLP isoforms. The putative signal sequences of the TSLP isoforms are marked in blue, and the mature protein in black. N-linked glycosylation sites are marked green, and methionine start codons are marked red. Bold black characters indicate the position of MKK34. (<b>C</b>) JNet secondary structure prediction of lfTSLP based on the amino acid sequence. Helices are marked as red tubes, and sheets are marked as green arrows. JNETCONF: The confidence estimate for the prediction, high values indicate high confidence. Modified from the web-based application Jpred (The Barton Group, School of Life Sciences, University of Dundee, UK). (<b>D</b>) Three-dimensional structure (Swiss-model, [<a href="#B9-pharmaceuticals-09-00041" class="html-bibr">9</a>]) of lfTSLP (<b>left</b>) and sfTSLP (<b>right</b>).</p> "> Figure 2
<p>Immunohistochemical (IHC) staining and in situ hybridization (ISH) of sections of oral mucosa (<b>A</b>–<b>C</b>), skin (<b>D</b>–<b>F</b>), salivary gland (<b>G</b>–<b>I</b>), and smokeless tobacco (“snus”; <b>J</b>,<b>K</b>) for TSLP variants. Left column: IHC staining with anti-TSLP antibody recognizing both lfTSLP and sfTSLP (brown color). Middle column: IHC staining with anti-TSLP antibody recognizing lfTSLP only. As no specific staining is detected in (<b>B</b>,<b>E</b>,<b>H</b>), this means that the staining in (<b>A</b>,<b>D</b>,<b>G</b>) represents sfTSLP. In oral mucosa exposed to smokeless tobacco, lfTSLP is seen (<b>K</b>). Right column: ISH staining by use of sfTSLP-specific probe (blue color) which confirms strong expression of sfTSLP in oral mucosa and salivary gland, and weak expression in skin. Modified from [<a href="#B5-pharmaceuticals-09-00041" class="html-bibr">5</a>].</p> "> Figure 3
<p>STAT5 phosphorylation in response to lfTSLP, 60 aa sfTSLP, 63 aa sfTSLP, or lfTSLP combined with sfTSLP in blood-derived CD1c myeloid DCs incubated with poly(I:C) for 24 h, and then treated with sfTSLP or/and lfTSLP for 15 min. Phosphorylation of STAT5 was assessed by flow cytometry. From [<a href="#B5-pharmaceuticals-09-00041" class="html-bibr">5</a>].</p> "> Figure 4
<p>Plot of hydrophobic moment (μH) for the mature lfTSLP (131 amino acids).</p> "> Figure 5
<p>Antimicrobial activity of short and long forms of thymic stromal lymphopoietin (sfTSLP and lfTSLP). (<b>A</b>) lfTSLP exhibited a larger zone of inhibition of growth of <span class="html-italic">Escherichia coli</span> ATCC 25922 in comparison with LL-37: (a) control; (b) 10 µM LL-37; and (c) 10µM TSLP. Mean values and standard deviations (n = 4). (<b>B</b>) In a viable count assay, indicated bacterial (<span class="html-italic">Escherichia coli, Pseudomonas aeruginosa, Staphylococcus aureus</span>, and <span class="html-italic">Staphylococcus epidermidis</span>) and fungal isolates (<span class="html-italic">Candida albicans</span> and <span class="html-italic">Candida parapsilosis</span>) were subjected to 2 µM of TSLP. The number of cfu was registered. (<b>C</b>) Suspensions of the indicated bacterial and fungal species were treated for 2 h with 60 amino acid (aa) sfTSLP, and 63 aa sfTSLP or lfTSLP peptide at a concentration of 1.35 mM before being plated on agar. Colony-forming units per ml were determined after incubation overnight. The values were normalized to the levels obtained without the addition of test peptides (broken line). (<b>D</b>) Suspensions of <span class="html-italic">Streptococcus mitis</span> were treated with equimolar concentrations of 60 aa sfTSLP, LL-37, or lfTSLP and analyzed as in C. From: [<a href="#B7-pharmaceuticals-09-00041" class="html-bibr">7</a>] (<b>A</b>,<b>B</b>) and [<a href="#B5-pharmaceuticals-09-00041" class="html-bibr">5</a>] (<b>C</b>,<b>D</b>).</p> "> Figure 6
<p>Helical structure of MKK34. A helical wheel projection was constructed using the amino acid sequence of MKK34.</p> "> Figure 7
<p>Enzymatic digestion of TSLP. (<b>A</b>) TSLP was digested with S. aureus V8 proteinase, and cleavage products were visualized by Western blot analysis using polyclonal antibodies against human TSLP. Products produced by V8 cleavage of TSLP revealed a major immunoreactive protein fragment at about 16 kDa. (<b>B</b>) TSLP and LL-37 were incubated with and without human neutrophil (leukocyte) elastase (HLE), <span class="html-italic">S. aureus</span> V8 proteinase or <span class="html-italic">Pseudomonas aeruginosa</span> elastase (PAE) and analyzed under non-reducing conditions by SDS-PAGE. From ref. [<a href="#B7-pharmaceuticals-09-00041" class="html-bibr">7</a>].</p> "> Figure 8
<p>Electron microscopy analysis. <span class="html-italic">Staphylococcus aureus</span> and <span class="html-italic">Pseudomonas aeruginosa</span> were incubated with 30 μM of MKK34 and LL-37 for 2 h at 37 °C and visualized by negative staining. Scale bar 1 μm. Control: buffer control. From [<a href="#B7-pharmaceuticals-09-00041" class="html-bibr">7</a>], image courtesy of Matthias Mörgelin, Lund University, Lund, Sweden.</p> ">
Abstract
:1. Introduction
2. TSLP Variants
3. Expression and Regulation of TSLP Variants
4. Human TSLP Variants and Immunoregulation
4.1. Long-Form TSLP (lfTSLP)
4.2. Short-Form TSLP (sfTSLP)
5. Human TSLP Variants as Antimicrobial Peptides
6. Conclusions
Acknowledgments
Conflicts of Interest
References
- Friend, S.L.; Hosier, S.; Nelson, A.; Foxworthe, D.; Williams, D.E.; Farr, A. A thymic stromal cell line supports in vitro development of surface IgM+ B cells and produces a novel growth factor affecting B and T lineage cells. Exp. Hematol. 1994, 22, 321–328. [Google Scholar] [PubMed]
- Quentmeier, H.; Drexler, H.G.; Fleckenstein, D.; Zaborski, M.; Armstrong, A.; Sims, J.E.; Lyman, S.D. Cloning of human thymic stromal lymphopoietin (TSLP) and signaling mechanisms leading to proliferation. Leukemia 2001, 15, 1286–1292. [Google Scholar] [CrossRef] [PubMed]
- Reche, P.A.; Soumelis, V.; Gorman, D.M.; Clifford, T.; Liu, M.; Travis, M.; Zurawski, S.M.; Johnston, J.; Liu, Y.J.; Spits, H.; et al. Human thymic stromal lymphopoietin preferentially stimulates myeloid cells. J. Immunol. 2001, 167, 336–343. [Google Scholar] [CrossRef] [PubMed]
- Ziegler, S.F.; Roan, F.; Bell, B.D.; Stoklasek, T.A.; Kitajima, M.; Han, H. The biology of thymic stromal lymphopoietin (TSLP). Adv. Pharmacol. 2013, 66, 129–155. [Google Scholar] [PubMed]
- Bjerkan, L.; Schreurs, O.; Engen, S.A.; Jahnsen, F.L.; Baekkevold, E.S.; Blix, I.J.; Schenck, K. The short form of TSLP is constitutively translated in human keratinocytes and has characteristics of an antimicrobial peptide. Mucosal Immunol. 2015, 8, 49–56. [Google Scholar] [CrossRef] [PubMed]
- Fornasa, G.; Tsilingiri, K.; Caprioli, F.; Botti, F.; Mapelli, M.; Meller, S.; Kislat, A.; Homey, B.; Di Sabatino, A.; Sonzogni, A.; et al. Dichotomy of short and long thymic stromal lymphopoietin isoforms in inflammatory disorders of the bowel and skin. J. Allergy Clin. Immunol. 2015, 136, 413–422. [Google Scholar] [CrossRef] [PubMed]
- Sonesson, A.; Kasetty, G.; Olin, A.I.; Malmsten, M.; Mörgelin, M.; Sørensen, O.E.; Schmidtchen, A. Thymic stromal lymphopoietin exerts antimicrobial activities. Exp. Dermatol. 2011, 20, 1004–1010. [Google Scholar] [CrossRef] [PubMed]
- Petersen, T.N.; Brunak, S.; von Heijne, G.; Nielsen, H. SignalP 4.0: Discriminating signal peptides from transmembrane regions. Nat. Methods 2011, 8, 785–786. [Google Scholar] [CrossRef] [PubMed]
- Arnold, K.; Bordoli, L.; Kopp, J.; Schwede, T. The SWISS-MODEL workspace: A web-based environment for protein structure homology modelling. Bioinformatics 2006, 22, 195–201. [Google Scholar] [CrossRef] [PubMed]
- Harada, M.; Hirota, T.; Jodo, A.I.; Doi, S.; Kameda, M.; Fujita, K.; Miyatake, A.; Enomoto, T.; Noguchi, E.; Yoshihara, S.; et al. Functional analysis of the thymic stromal lymphopoietin variants in human bronchial epithelial cells. Am. J. Respir. Cell Mol. Biol. 2009, 40, 368–374. [Google Scholar] [CrossRef] [PubMed]
- Rothenberg, M.E.; Spergel, J.M.; Sherrill, J.D.; Annaiah, K.; Martin, L.J.; Cianferoni, A.; Gober, L.; Kim, C.; Glessner, J.; Frackelton, E.; et al. Common variants at 5q22 associate with pediatric eosinophilic esophagitis. Nat. Genet. 2010, 42, 289–291. [Google Scholar] [CrossRef] [PubMed]
- Mjösberg, J.; Bernink, J.; Golebski, K.; Karrich, J.J.; Peters, C.P.; Blom, B.; te Velde, A.A.; Fokkens, W.J.; van Drunen, C.M.; Spits, H. The transcription factor GATA3 is essential for the function of human type 2 innate lymphoid cells. Immunity 2012, 37, 649–659. [Google Scholar] [CrossRef] [PubMed]
- Melum, G.R.; Farkas, L.; Scheel, C.; Van Dieren, B.; Gran, E.; Liu, Y.J.; Johansen, F.E.; Jahnsen, F.L.; Baekkevold, E.S. A thymic stromal lymphopoietin-responsive dendritic cell subset mediates allergic responses in the upper airway mucosa. J. Allergy Clin. Immunol. 2014, 134, 613–621. [Google Scholar] [CrossRef] [PubMed]
- Soumelis, V.; Reche, P.A.; Kanzler, H.; Yuan, W.; Edward, G.; Homey, B.; Gilliet, M.; Ho, S.; Antonenko, S.; Lauerma, A.; et al. Human epithelial cells trigger dendritic cell mediated allergic inflammation by producing TSLP. Nat. Immunol. 2002, 3, 673–680. [Google Scholar] [CrossRef] [PubMed]
- Kinoshita, H.; Takai, T.; Le, T.A.; Kamijo, S.; Wang, X.L.; Ushio, H.; Hara, M.; Kawasaki, J.; Vu, A.T.; Ogawa, T.; et al. Cytokine milieu modulates release of thymic stromal lymphopoietin from human keratinocytes stimulated with double-stranded RNA. J. Allergy Clin. Immunol. 2009, 123, 179–186. [Google Scholar] [CrossRef] [PubMed]
- Kato, A.; Favoreto, S.; Avila, P.C.; Schleimer, R.P. TLR3- and Th2 cytokine-dependent production of thymic stromal lymphopoietin in human airway epithelial cells. J. Immunol. 2007, 179, 1080–1087. [Google Scholar] [CrossRef] [PubMed]
- Fontenot, D.; He, H.; Hanabuchi, S.; Nehete, P.N.; Zhang, M.; Chang, M.; Nehete, B.; Wang, Y.H.; Wang, Y.H.; Ma, Z.M.; et al. TSLP production by epithelial cells exposed to immunodeficiency virus triggers DC-mediated mucosal infection of CD4+ T cells. Proc. Natl. Acad. Sci. USA 2009, 106, 16776–16781. [Google Scholar] [CrossRef] [PubMed]
- Allakhverdi, Z.; Comeau, M.R.; Jessup, H.K.; Yoon, B.R.; Brewer, A.; Chartier, S.; Paquette, N.; Ziegler, S.F.; Sarfati, M.; Delespesse, G. Thymic stromal lymphopoietin is released by human epithelial cells in response to microbes, trauma, or inflammation and potently activates mast cells. J. Exp. Med. 2007, 204, 253–258. [Google Scholar] [CrossRef] [PubMed]
- Zhou, B.; Comeau, M.R.; De Smedt, T.; Liggitt, H.D.; Dahl, M.E.; Lewis, D.B.; Gyarmati, D.; Aye, T.; Campbell, D.J.; Ziegler, S.F. Thymic stromal lymphopoietin as a key initiator of allergic airway inflammation in mice. Nat. Immunol. 2005, 6, 1047–1053. [Google Scholar] [CrossRef] [PubMed]
- Headley, M.B.; Zhou, B.; Shih, W.X.; Aye, T.; Comeau, M.R.; Ziegler, S.F. TSLP conditions the lung immune environment for the generation of pathogenic innate and antigen-specific adaptive immune responses. J. Immunol. 2009, 182, 1641–1647. [Google Scholar] [CrossRef] [PubMed]
- Yoo, J.; Omori, M.; Gyarmati, D.; Zhou, B.; Aye, T.; Brewer, A.; Comeau, M.R.; Campbell, D.J.; Ziegler, S.F. Spontaneous atopic dermatitis in mice expressing an inducible thymic stromal lymphopoietin transgene specifically in the skin. J. Exp. Med. 2005, 202, 541–549. [Google Scholar] [CrossRef] [PubMed]
- Bergot, A.S.; Monnet, N.; Le Tran, S.; Mittal, D.; Al-Kouba, J.; Steptoe, R.J.; Grimbaldeston, M.A.; Frazer, I.H.; Wells, J.W. HPV16 E7 expression in skin induces TSLP secretion, type 2 ILC infiltration and atopic dermatitis-like lesions. Immunol. Cell Biol. 2015, 93, 540–547. [Google Scholar] [CrossRef] [PubMed]
- Mahmutovic-Persson, I.; Akbarshahi, H.; Bartlett, N.W.; Glanville, N.; Johnston, S.L.; Brandelius, A.; Uller, L. Inhaled dsRNA and rhinovirus evoke neutrophilic exacerbation and lung expression of thymic stromal lymphopoietin in allergic mice with established experimental asthma. Allergy 2014, 69, 348–358. [Google Scholar] [CrossRef] [PubMed]
- Li, M.; Messaddeq, N.; Teletin, M.; Pasquali, J.L.; Metzger, D.; Chambon, P. Retinoid X receptor ablation in adult mouse keratinocytes generates an atopic dermatitis triggered by thymic stromal lymphopoietin. Proc. Natl. Acad. Sci. USA 2005, 102, 14795–14800. [Google Scholar] [CrossRef] [PubMed]
- Lay, M.K.; Céspedes, P.F.; Palavecino, C.E.; León, M.A.; Díaz, R.A.; Salazar, F.J.; Méndez, G.P.; Bueno, S.M.; Kalergis, A.M. Human metapneumovirus infection activates the TSLP pathway that drives excessive pulmonary inflammation and viral replication in mice. Eur. J. Immunol. 2015, 45, 1680–1695. [Google Scholar] [CrossRef] [PubMed]
- He, R.; Geha, R.S. Thymic stromal lymphopoietin. Ann. N. Y. Acad. Sci. 2010, 1183, 13–24. [Google Scholar] [CrossRef] [PubMed]
- Nagata, Y.; Kamijuku, H.; Taniguchi, M.; Ziegler, S.; Seino, K. Differential role of thymic stromal lymphopoietin in the induction of airway hyperreactivity and Th2 immune response in antigen-induced asthma with respect to natural killer T cell function. Int. Arch. Allergy Immunol. 2007, 144, 305–314. [Google Scholar] [CrossRef] [PubMed]
- Rochman, I.; Watanabe, N.; Arima, K.; Liu, Y.J.; Leonard, W.J. Cutting edge: Direct action of thymic stromal lymphopoietin on activated human CD4+ T cells. J. Immunol. 2007, 178, 6720–6724. [Google Scholar] [CrossRef] [PubMed]
- Wong, C.K.; Hu, S.; Cheung, P.F.; Lam, C.W. Thymic stromal lymphopoietin induces chemotactic and prosurvival effects in eosinophils: Implications in allergic inflammation. Am. J. Respir. Cell Mol. Biol. 2010, 43, 305–315. [Google Scholar] [CrossRef] [PubMed]
- Ziegler, S.F.; Artis, D. Sensing the outside world: TSLP regulates barrier immunity. Nat. Immunol. 2010, 11, 289–293. [Google Scholar] [CrossRef] [PubMed]
- Reardon, C.; Lechmann, M.; Brüstle, A.; Gareau, M.G.; Shuman, N.; Philpott, D.; Ziegler, S.F.; Mak, T.W. Thymic stromal lymphopoetin-induced expression of the endogenous inhibitory enzyme SLPI mediates recovery from colonic inflammation. Immunity 2011, 35, 223–235. [Google Scholar] [CrossRef] [PubMed]
- Siracusa, M.C.; Saenz, S.A.; Hill, D.A.; Kim, B.S.; Headley, M.B.; Doering, T.A.; Wherry, E.J.; Jessup, H.K.; Siegel, L.A.; Kambayashi, T.; et al. TSLP promotes interleukin-3-independent basophil haematopoiesis and type 2 inflammation. Nature 2011, 477, 229–233. [Google Scholar] [CrossRef] [PubMed]
- Arima, K.; Watanabe, N.; Hanabuchi, S.; Chang, M.; Sun, S.C.; Liu, Y.J. Distinct signal codes generate dendritic cell functional plasticity. Sci. Signal. 2010, 3, ra4. [Google Scholar] [CrossRef] [PubMed]
- Roan, F.; Bell, B.D.; Stoklasek, T.A.; Kitajima, M.; Han, H.; Ziegler, S.F. The multiple facets of thymic stromal lymphopoietin (TSLP) during allergic inflammation and beyond. J. Leukoc. Biol. 2012, 91, 877–886. [Google Scholar] [CrossRef] [PubMed]
- Ito, T.; Wang, Y.H.; Duramad, O.; Hori, T.; Delespesse, G.J.; Watanabe, N.; Qin, F.X.; Yao, Z.; Cao, W.; Liu, Y.J. TSLP-activated dendritic cells induce an inflammatory T helper type 2 cell response through OX40 ligand. J. Exp. Med. 2005, 202, 1213–1223. [Google Scholar] [CrossRef] [PubMed]
- Rimoldi, M.; Chieppa, M.; Salucci, V.; Avogadri, F.; Sonzogni, A.; Sampietro, G.M.; Nespoli, A.; Viale, G.; Allavena, P.; Rescigno, M. Intestinal immune homeostasis is regulated by the crosstalk between epithelial cells and dendritic cells. Nat. Immunol. 2005, 6, 507–505. [Google Scholar] [CrossRef] [PubMed]
- Iliev, I.D.; Spadoni, I.; Mileti, E.; Matteoli, G.; Sonzogni, A.; Sampietro, G.M.; Foschi, D.; Caprioli, F.; Viale, G.; Rescigno, M. Human intestinal epithelial cells promote the differentiation of tolerogenic dendritic cells. Gut 2009, 58, 1481–1489. [Google Scholar] [CrossRef] [PubMed]
- Wang, G. Improved methods for classification, prediction, and design of antimicrobial peptides. Methods Mol. Biol. 2015, 1268, 43–66. [Google Scholar] [PubMed]
- Brogden, K.A. Antimicrobial peptides: Pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 2005, 3, 238–250. [Google Scholar] [CrossRef] [PubMed]
- Powers, J.P.; Hancock, R.E. The relationship between peptide structure and antibacterial activity. Peptides 2003, 24, 1681–1691. [Google Scholar] [CrossRef] [PubMed]
- Zasloff, M. Antimicrobial peptides of multicellular organisms. Nature 2002, 415, 389–395. [Google Scholar] [CrossRef] [PubMed]
- Schittek, B.; Hipfel, R.; Sauer, B.; Bauer, J.; Kalbacher, H.; Stevanovic, S.; Schirle, M.; Schroeder, K.; Blin, N.; Meier, F.; et al. Dermcidin: A novel human antibiotic peptide secreted by sweat glands. Nat. Immunol. 2001, 2, 1133–1137. [Google Scholar] [CrossRef] [PubMed]
- Diamond, G.; Beckloff, N.; Weinberg, A.; Kisich, K.O. The roles of antimicrobial peptides in innate host defense. Curr. Pharm. Des. 2009, 15, 2377–2392. [Google Scholar] [CrossRef] [PubMed]
- Guani-Guerra, E.; Santos-Mendoza, T.; Lugo-Reyes, S.O.; Teran, L.M. Antimicrobial peptides: General overview and clinical implications in human health and disease. Clin. Immunol. 2010, 135, 1–11. [Google Scholar] [CrossRef] [PubMed]
- Glaser, R.; Harder, J.; Lange, H.; Bartels, J.; Christophers, E.; Schroder, J.M. Antimicrobial psoriasin (S100A7) protects human skin from Escherichia coli infection. Nat. Immunol. 2005, 6, 57–64. [Google Scholar] [CrossRef] [PubMed]
- Sorensen, O.E.; Follin, P.; Johnsen, A.H.; Calafat, J.; Tjabringa, G.S.; Hiemstra, P.S.; Borregaard, N. Human cathelicidin, hCAP-18, is processed to the antimicrobial peptide LL-37 by extracellular cleavage with proteinase 3. Blood 2001, 97, 3951–3959. [Google Scholar] [CrossRef] [PubMed]
- Nordahl, E.A.; Rydengard, V.; Nyberg, P.; Nitsche, D.P.; Morgelin, M.; Malmsten, M.; Björck, L.; Schmidtchen, A. Activation of the complement system generates antibacterial peptides. Proc. Natl. Acad. Sci. USA 2004, 101, 16879–16884. [Google Scholar] [CrossRef] [PubMed]
- Papareddy, P.; Rydengard, V.; Pasupuleti, M.; Walse, B.; Morgelin, M.; Chalupka, A.; Malmsten, M.; Schmidtchen, A. Proteolysis of human thrombin generates novel host defense peptides. PLoS Pathog. 2010, 6, e1000857. [Google Scholar] [CrossRef] [PubMed]
- Papareddy, P.; Kalle, M.; Kasetty, G.; Mörgelin, M.; Rydengård, V.; Albiger, B.; Lundqvist, K.; Malmsten, M.; Schmidtchen, A. C-terminal peptides of tissue factor pathway inhibitor are novel host defense molecules. J. Biol. Chem. 2010, 285, 28387–28398. [Google Scholar] [CrossRef] [PubMed]
- Baker, B.S. The role of microorganisms in atopic dermatitis. Clin. Exp. Immunol. 2006, 144, 1–9. [Google Scholar] [CrossRef] [PubMed]
- Schroeder, B.O.; Wu, Z.; Nuding, S.; Groscurth, S.; Marcinowski, M.; Beisner, J.; Buchner, J.; Schaller, M.; Stange, E.F.; Wehkamp, J. Reduction of disulphide bonds unmasks potent antimicrobial activity of human β-defensin 1. Nature 2011, 469, 419–423. [Google Scholar] [CrossRef] [PubMed]
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Bjerkan, L.; Sonesson, A.; Schenck, K. Multiple Functions of the New Cytokine-Based Antimicrobial Peptide Thymic Stromal Lymphopoietin (TSLP). Pharmaceuticals 2016, 9, 41. https://doi.org/10.3390/ph9030041
Bjerkan L, Sonesson A, Schenck K. Multiple Functions of the New Cytokine-Based Antimicrobial Peptide Thymic Stromal Lymphopoietin (TSLP). Pharmaceuticals. 2016; 9(3):41. https://doi.org/10.3390/ph9030041
Chicago/Turabian StyleBjerkan, Louise, Andreas Sonesson, and Karl Schenck. 2016. "Multiple Functions of the New Cytokine-Based Antimicrobial Peptide Thymic Stromal Lymphopoietin (TSLP)" Pharmaceuticals 9, no. 3: 41. https://doi.org/10.3390/ph9030041