Skin microbiota analysis in human 3D skin models—“Free your mice”
Open accessAbstract
In the May issue of Experimental Dermatology 2018, we published a review article focusing on human 3D skin models in the context of microbiota research. The principal intention was to provide an overview of present and future concepts to use skin models in microbiota analyses. With the present viewpoint, we would like to draw the reader's attention again to the use of human skin models in microbiota research with the aim to highlight the benefits and necessity of human skin models to analyse the human skin‐microbiota interaction. This is accompanied by a critical view on mice models that often are not suitable to analyse the functional impact of the human skin microbiota. In addition, we present novel and future concepts highlighting the benefits of human 3D skin models in microbiota research.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Rodent skin has its own microbiota that differs from human skin microbial communities, and attempts to model human microbiota on animal skin are prevented by competition from the native flora, in addition to intrinsic morphological differences with human skin.
“Indeed, besides having intrinsic morphological differences with human skin, disadvantaging germ-free animal models, rodent skin is characterized by its own microbiota, which obviously differs from the microbial communities of human skin; thus, the attempts to model human microbiota on animal skin are prevented due to the competition exerted by the native flora [133,134].”
From Recreating Human Skin In Vitro: Should the Microbiota Be Taken into Account? (2024) · cites this paper as [134]
Split into 2 atoms — 1 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Weidinger, S., & Novak, N. (2016) · The Lancet · doi:10.1016/s0140-6736(15)00149-x · Cited by 1,908 · see citing works
Nakatsuji, T., Chen, T. H., Narala, S., Chun, K. A., Two, A. M., Yun, T., Shafiq, F., Kotol, P. F., Bouslimani, A., Melnik, A. V., et al. (2017) · Science Translational Medicine · doi:10.1126/scitranslmed.aah4680 · Cited by 1,095 · see citing works
The microbiome of uncontacted Amerindians
Clemente, J. C., Pehrsson, E. C., Blaser, M. J., Sandhu, K., Gao, Z., Wang, B., Magris, M., Hidalgo, G., Contreras, M., Noya-Alarcón, Ó., et al. (2015) · Science Advances · doi:10.1126/sciadv.1500183 · Cited by 851 · see citing works
Meslier, V., Laiola, M., Roager, H. M., De Filippis, F., Roume, H., Quinquis, B., Giacco, R., Mennella, I., Ferracane, R., Pons, N., et al. (2020) · Gut · doi:10.1136/gutjnl-2019-320438 · Cited by 583 · see citing works
Hair-bearing human skin generated entirely from pluripotent stem cells
Lee, J., Rabbani, C. C., Gao, H., Steinhart, M. R., Woodruff, B. M., Pflum, Z. E., Kim, A., Heller, S., Liu, Y., Shipchandler, T. Z., et al. (2020) · Nature · doi:10.1038/s41586-020-2352-3 · Cited by 487 · see citing works
Changes in the Ceramide Profile of Atopic Dermatitis Patients
Ishikawa, J., Narita, H., Kondo, N., Hotta, M., Takagi, Y., Masukawa, Y., Kitahara, T., Takema, Y., Koyano, S., Yamazaki, S., et al. (2010) · Journal of Investigative Dermatology · doi:10.1038/jid.2010.161 · Cited by 372 · see citing works
Flagged first, then by citations
Research works printed but not linked: 54
- F. Rademacher, M. Simanski, R. Gläser, J. Harder, Exp. Dermatol. 2018, 27, 489.
- H. Niehues, J. A. Bouwstra, A. El Ghalbzouri, J. M. Brandner, P. Zeeuwen, E. H. van den Bogaard, Exp. Dermatol. 2018, 27, 501.
- A. Pupovac, B. Senturk, C. Griffoni, K. Maniura-Weber, M. Rottmar, S. L. McArthur, Adv. Healthc. Mater. 2018, 7, e1701405.
- P. A. Gerber, B. A. Buhren, H. Schrumpf, B. Homey, A. Zlotnik, P. Hevezi, Biol. Chem. 2014, 395, 577.
- E. A. Brettmann, C. de Guzman Strong, Exp. Dermatol. 2018, 27, 859.
- M. Pasparakis, I. Haase, F. O. Nestle, Nat. Rev. Immunol. 2014, 14, 289.
- J. Harder, J. M. Schröder, R. Gläser, Exp. Dermatol. 2013, 22, 1.
- K. Kwiecien, A. Zegar, J. Jung, P. Brzoza, M. Kwitniewski, U. Godlewska, B. Grygier, P. Kwiecinska, A. Morytko, J. Cichy, Cytokine Growth Factor Rev. 2019, 49, 70.
- F. Rademacher, M. Simanski, J. Harder, Int. J. Mol. Sci. 2016, 17, 560.
- V. Dimitrov, J. H. White, J. Steroid Biochem. Mol. Biol. 2016, 164, 246.
- S. Holtfreter, F. J. Radcliff, D. Grumann, H. Read, S. Johnson, S. Monecke, S. Ritchie, F. Clow, C. Goerke, B. M. Broker, J. D. Fraser, S. Wiles, PLoS One 2013, 8, e71142.
- N. Nagase, A. Sasaki, K. Yamashita, A. Shimizu, Y. Wakita, S. Kitai, J. Kawano, J. Vet. Med. Sci. 2002, 64, 245.
- A. A. Ross, K. M. Muller, J. S. Weese, J. D. Neufeld, Proc. Natl Acad. Sci. USA 2018, 115, E5786.
- F. Hugenholtz, W. M. de Vos, Cell Mol. Life Sci. 2018, 75, 149.
- H. K. Kim, D. Missiakas, O. Schneewind, J. Immunol. Methods 2014, 410, 88.
- A. Schulz, L. Jiang, L. de Vor, M. Ehrstrom, F. Wermeling, L. Eidsmo, K. Melican, Cell Rep. 2019, 29, 1074.
- P. A. Dimitriu, B. Iker, K. Malik, H. Leung, W. W. Mohn, G. G. Hillebrand, mBio 2019, 10(4):e00839-19. https://doi.org/10.1128/ mBio.00839 -19 · DOI
- H. J. Kim, J. J. Kim, N. R. Myeong, T. Kim, D. Kim, S. An, H. Kim, T. Park, S. I. Jang, J. H. Yeon, I. Kwack, W. J. Sul, Sci. Rep. 2019, 9, 16748.
- M. Brandwein, I. Katz, A. Katz, R. Kohen, Hum. Microbiome J. 2019, 13, 100063.
- R. Vongsa, D. Hoffman, K. Shepard, D. Koenig, BMC Microbiol. 2019, 19, 16.
- A. A. Ross, A. Rodrigues Hoffmann, J. D. Neufeld, Microbiome 2019, 7, 79.
- P. L. Zeeuwen, T. H. Ederveen, D. A. van der Krieken, H. Niehues, J. Boekhorst, S. Kezic, D. A. Hanssen, M. E. Otero, I. M. van Vlijmen- Willems, D. Rodijk-Olthuis, D. Falcone, E. H. van den Bogaard, M. Kamsteeg, H. D. de Koning, M. E. Zeeuwen-Franssen, M. A. van Steensel, M. Kleerebezem, H. M. Timmerman, S. A. van Hijum, J. Schalkwijk, J. Allergy Clin. Immunol. 2017, 139, 1368.
- N. Fyhrquist, G. Muirhead, S. Prast-Nielsen, M. Jeanmougin, P. Olah, T. Skoog, G. Jules-Clement, M. Feld, M. Barrientos-Somarribas, H. Sinkko, E. H. van den Bogaard, P. Zeeuwen, G. Rikken, J. Schalkwijk, H. Niehues, W. Daubener, S. K. Eller, H. Alexander, D. Pennino, S. Suomela, I. Tessas, E. Lybeck, A. M. Baran, H. Darban, R. S. Gangwar, U. Gerstel, K. Jahn, P. Karisola, L. Yan, B. Hansmann, S. Katayama, S. Meller, M. Bylesjo, P. Hupe, F. Levi-Schaffer, D. Greco, A. Ranki, J. M. Schroder, J. Barker, J. Kere, S. Tsoka, A. Lauerma, V. Soumelis, F. O. Nestle, B. Homey, B. Andersson, H. Alenius, Nat. Commun. 2019, 10, 4703.
- E. van den Bogaard, D. Ilic, S. Dubrac, M. Tomic-Canic, J. Bouwstra, A. Celli, T. Mauro, J. Invest. Dermatol. 2020. https://doi. org/10.1016/j.jid.2020.04.023 [Online ahead of print] · DOI
- H. Niehues, J. Schalkwijk, I. van Vlijmen-Willems, D. Rodijk-Olthuis, M. M. van Rossum, E. Wladykowski, J. M. Brandner, E. H. J. van den Bogaard, P. Zeeuwen, J Allergy Clin. Immunol. 1979, 2017, 139.
- W. David Boothe, J. A. Tarbox, M. B. Tarbox, Adv. Exp. Med. Biol. 2017, 1027, 21.
- S. Weidinger, N. Novak, Lancet 2016, 387, 1109.
- H. Baurecht, M. C. Ruhlemann, E. Rodriguez, F. Thielking, I. Harder, A. S. Erkens, D. Stolzl, E. Ellinghaus, M. Hotze, W. Lieb, S. Wang, F. A. Heinsen-Groth, A. Franke, S. Weidinger, J. Allergy Clin. Immunol. 2018, 141, 1668.
- M. Burian, B. Schittek, Int. J. Med. Microbiol. 2015, 305, 283.
- C. Tam, J. J. Mun, D. J. Evans, S. M. Fleiszig, J. Clin. Invest. 2012, 122, 3665.
- J. Ishikawa, H. Narita, N. Kondo, M. Hotta, Y. Takagi, Y. Masukawa, T. Kitahara, Y. Takema, S. Koyano, S. Yamazaki, A. Hatamochi, J. Invest. Dermatol. 2010, 130, 2511.
- S. Li, M. Villarreal, S. Stewart, J. Choi, G. Ganguli-Indra, D. C. Babineau, C. Philpot, G. David, T. Yoshida, M. Boguniewicz, J. M. Hanifin, L. A. Beck, D. Y. Leung, E. L. Simpson, A. K. Indra, Br. J. Dermatol. 2017, 177, e125.
- M. Mildner, J. Jin, L. Eckhart, S. Kezic, F. Gruber, C. Barresi, C. Stremnitzer, M. Buchberger, V. Mlitz, C. Ballaun, B. Sterniczky, D. Fodinger, E. Tschachler, J. Invest. Dermatol. 2010, 130, 2286.
- V. van Drongelen, E. M. Haisma, J. J. Out-Luiting, P. H. Nibbering, A. El Ghalbzouri, Clin. Exp. Allergy 2014, 44, 1515.
- D. Fangmann, E. M. Theismann, K. Turk, D. M. Schulte, I. Relling, K. Hartmann, J. K. Keppler, J. R. Knipp, A. Rehman, F. A. Heinsen, A. Franke, L. Lenk, S. Freitag-Wolf, E. Appel, S. Gorb, C. Brenner, D. Seegert, G. H. Waetzig, P. Rosenstiel, S. Schreiber, K. Schwarz, M. Laudes, Diab. Care 2018, 41, 398.
- D. Houghton, T. Hardy, C. Stewart, L. Errington, C. P. Day, M. I. Trenell, L. Avery, Diabetologia 2018, 61, 1700.
- V. Meslier, M. Laiola, H. M. Roager, F. De Filippis, H. Roume, B. Quinquis, R. Giacco, I. Mennella, R. Ferracane, N. Pons, E. Pasolli, A. Rivellese, L. O. Dragsted, P. Vitaglione, S. D. Ehrlich, D. Ercolini, Gut 2020, 69, 1258.
- C. Clemente, E. C. Pehrsson, M. J. Blaser, K. Sandhu, Z. Gao, B. Wang, M. Magris, G. Hidalgo, M. Contreras, Ó. Noya-Alarcón, O. Lander, J. McDonald, M. Cox, J. Walter, P. L. Oh, J. F. Ruiz, S. Rodriguez, N. Shen, S. J. Song, J. Metcalf, R. Knight, G. Dantas, M. G. Dominguez-Bello, Sci. Adv. 2015, 1, e1500183.
- Y. Nodake, S. Matsumoto, R. Miura, H. Honda, G. Ishibashi, I. Dekio, R. Sakakibara, J. Dermatol. Sci. 2015, 79, 119.
- A. Myles, N. J. Earland, E. D. Anderson, I. N. Moore, M. D. Kieh, K. W. Williams, A. Saleem, N. M. Fontecilla, P. A. Welch, D. A. Darnell, L. A. Barnhart, A. A. Sun, G. Uzel, S. K. Datta, JCI Insight 2018, 3, e120608.
- C. Schmidt, Nat. Biotechnol. 2020, 38, 392.
- B. Paetzold, J. R. Willis, J. Pereira de Lima, N. Knodlseder, H. Bruggemann, S. R. Quist, T. Gabaldon, M. Guell, Microbiome 2019, 7, 95.
- D. Hoeller, B. Huppertz, T. C. Roos, P. Poblete Gutierrez, H. F. Merk, J. Frank, F. K. Jugert, Exp. Dermatol. 2001, 10, 264.
- T. Wagner, M. Gschwandtner, A. Strajeriu, A. Elbe-Burger, J. Grillari, R. Grillari-Voglauer, G. Greiner, B. Golabi, E. Tschachler, M. Mildner, Sci. Rep. 2018, 8, 13434.
- N. Obara, S. Tohgi, Y. Mii, N. Hamada, R. Arakawa, S. R. Aki, R. M. Singh, Y. A. Hoffman, Sci. Rep. 2019, 9, 9326.
- A. Berroth, J. Kuhnl, N. Kurschat, A. Schwarz, F. Stab, T. Schwarz, H. Wenck, R. Fölster-Holst, G. Neufang, J. Allergy Clin. Immunol. 2013, 131, 1547.
- E. Desmet, A. Ramadhas, J. Lambert, M. Van Gele, Exp. Biol. Med. (Maywood) 2017, 242, 1158.
- E. H. van den Bogaard, G. S. Tjabringa, I. Joosten, M. Vonk-Bergers, E. van Rijssen, H. J. Tijssen, M. Erkens, J. Schalkwijk, H. Koenen, J. Invest. Dermatol. 2014, 134, 719.
- K. Ouwehand, S. W. Spiekstra, T. Waaijman, M. Breetveld, R. J. Scheper, T. D. de Gruijl, S. Gibbs, Eur. J. Cell Biol. 2012, 91, 765.
- V. Facy, V. Flouret, M. Regnier, R. Schmidt, Toxicol. In Vitro 2005, 19, 787.
- J. Lee, C. C. Rabbani, H. Gao, M. R. Steinhart, B. M. Woodruff, Z. E. Pflum, A. Kim, S. Heller, Y. Liu, T. Z. Shipchandler, K. R. Koehler, Nature 2020, 582, 399.
- S. Ishack, S. R. Lipner, Dermatol. Surg. 2020. https://doi.org/10.1097/ DSS.00000 00000 002378 [Online ahead of print] · DOI
- S. Xu, X. Zheng, L. Hu, W. Li, R. Li, Y. Parungao, Y. Wang, Y. Nie, T. Liu, K. Song, Polymers (Basel) 2020, 12, 1237.
- B. S. Kim, G. Gao, J. Y. Kim, D. W. Cho, Adv. Healthc. Mater. 2019, 8, e1801019. How to cite this article: Emmert H, Rademacher F, Gläser R, Harder J. Skin microbiota analysis in human 3D skin models- "Free your mice". Exp Dermatol. 2020;29:1133-1139. https:// doi.org/10.1111/exd.14164
Cited by
Sorted by citations
Recreating Human Skin In Vitro: Should the Microbiota Be Taken into Account?
Galvan, A., Pellicciari, C., & Calderan, L. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25021165 · Cited by 11 · see citing works
- Authors
- Emmert, H., Rademacher, F., Gläser, R., & Harder, J.
- Affiliations
- Christian-Albrechts-Universität zu Kiel (DE)
- Corresponding author
- Harder, Jürgen
- Venue
- Experimental Dermatology
- Publisher
- Wiley
- Published
- 2020-08-27
- Volume
- 29
- Issue
- 11
- Pages
- 1133-1139
- ISSN
- 0906-6705 (ISSN-L)
- 1600-0625
- OpenAlex
- W3047285247
- Cited by
- 32
- References
- 6
- Citations by year
- 2026: 5 · 2025: 7 · 2024: 6 · 2023: 7 · 2022: 4 · 2021: 3
- FWCI
- 2.55
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Experimental Dermatology (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Dermatology › Dermatology and Skin Diseases
- Health Sciences › Medicine › Dermatology › Contact Dermatitis and Allergies
- Health Sciences › Medicine › Epidemiology › Nail Diseases and Treatments
- Keywords
- skin microbiome, mouse model, animal model limitations, in vitro skin model
- MeSH terms
- Host Microbial Interactions, Animals, Humans, Models, Biological, Skin, Skin Physiological Phenomena, Biomedical Research, Mice, Precision Medicine, Microbiota
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
