Hydra and the hair follicle - An unconventional comparative biology approach to exploring the human holobiont.
antimicrobial peptides
microbial ecology
microbiome
model organisms
Journal
BioEssays : news and reviews in molecular, cellular and developmental biology
ISSN: 1521-1878
Titre abrégé: Bioessays
Pays: United States
ID NLM: 8510851
Informations de publication
Date de publication:
05 2022
05 2022
Historique:
revised:
02
02
2022
received:
01
10
2021
accepted:
17
02
2022
pubmed:
10
3
2022
medline:
26
4
2022
entrez:
9
3
2022
Statut:
ppublish
Résumé
The microbiome of human hair follicles (HFs) has emerged as an important player in different HF and skin pathologies, yet awaits in-depth exploration. This raises questions regarding the tightly linked interactions between host environment, nutrient dependency of host-associated microbes, microbial metabolism, microbe-microbe interactions and host immunity. The use of simple model systems facilitates addressing generally important questions and testing overarching, therapeutically relevant principles that likely transcend obvious interspecies differences. Here, we evaluate the potential of the freshwater polyp Hydra, to dissect fundamental principles of microbiome regulation by the host, that is the human HF. In particular, we focus on therapeutically targetable host-microbiome interactions, such as nutrient dependency, microbial interactions and host defence. Offering a new lens into the study of HF - microbiota interactions, we argue that general principles of how Hydra manages its microbiota can inform the development of novel, microbiome-targeting therapeutic interventions in human skin disease.
Identifiants
pubmed: 35261041
doi: 10.1002/bies.202100233
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e2100233Informations de copyright
© 2022 The Authors. BioEssays published by Wiley Periodicals LLC.
Références
Bertolini, M., McElwee, K., Gilhar, A., Bulfone-Paus, S., & Paus, R. (2020). Hair follicle immune privilege and its collapse in alopecia areata. Experimental Dermatology, 29(8), 703-725.
Polak-Witka, K., Rudnicka, L., Blume-Peytavi, U., & Vogt, A. (2020). The role of the microbiome in scalp hair follicle biology and disease. Experimental Dermatology, 29(3), 286-294. https://doi.org/10.1111/exd.13935.
Lousada, M. B., Lachnit, T., Edelkamp, J., Rouillé, T., Ajdic, D., Uchida, Y., Di Nardo, A., Bosch, T. C. G., & Paus, R. (2020). Exploring the human hair follicle microbiome. The British Journal of Dermatology, 184(5), 802-815. https://doi.org/10.1111/bjd.19461.
Limbu, S. L., Purba, T. S., Harries, M., Wikramanayake, T. C., Miteva, M., Bhogal, R. K., O'Neill, C. A., & Paus, R. (2021). A folliculocentric perspective of dandruff pathogenesis: Could a troublesome condition be caused by changes to a natural secretory mechanism? BioEssays, 43(10), 2100005. https://doi.org/10.1002/bies.202100005.
Constantinou, A., Polak-Witka, K., Tomazou, M., Oulas, A., Kanti, V., Schwarzer, R., Helmuth, J., Edelmann, A., Blume-Peytavi, U., Spyrou, G. M., & Vogt, A. (2021). Dysbiosis and enhanced beta-defensin production in hair follicles of patients with lichen planopilaris and frontal fibrosing alopecia. Biomedicines, 9(3), 266. https://doi.org/10.3390/biomedicines9030266.
Johnston, D. G. W., Kirby, B., & Tobin, D. J. (2021). Hidradenitis suppurativa: A folliculotropic disease of innate immune barrier dysfunction? Experimental Dermatology, 30(10), 1554-1568. https://doi.org/10.1111/exd.14451.
Lousada, M. B., Edelkamp, J., Lachnit, T., Erdmann, H., & Paus, R. (2021). Can antibiotic-induced changes in the composition of the hair follicle microbiome regulate human hair growth? Experimental Dermatology, 30(10), 1440-1441. https://doi.org/10.1111/exd.14364.
Sakamoto, K., Jin, S.-P., Goel, S., Jo, J.-H., Voisin, B., Kim, D., Nadella, V., Liang, H., Kobayashi, T., Huang, X., Deming, C., Horiuchi, K., Segre, J. A., Kong, H. H., & Nagao, K. (2021). Disruption of the endopeptidase ADAM10-Notch signaling axis leads to skin dysbiosis and innate lymphoid cell-mediated hair follicle destruction. Immunity, 54(10), 2321-2337.e10. https://doi.org/10.1016/j.immuni.2021.09.001.
Migacz-Gruszka, K., Branicki, W., Obtulowicz, A., Pirowska, M., Gruszka, K., & Wojas-Pelc, A. (2019). What's new in the pathophysiology of Alopecia Areata? The possible contribution of skin and gut microbiome in the pathogenesis of alopecia - big opportunities, big challenges, and novel perspectives. International Journal of Trichology, 11(5), 185-188. https://doi.org/10.4103/ijt.ijt_76_19.
Yu, Y., Champer, J., Agak, G. W., Kao, S., Modlin, R. L., & Kim, J. (2016). Different Propionibacterium acnes phylotypes induce distinct immune responses and express unique surface and secreted proteomes. Journal of Investigative Dermatology, 136(11), 2221-2228. https://doi.org/10.1016/j.jid.2016.06.615.
Lee, Y. B., Byun, E. J., & Kim, H. S. (2019). Potential role of the microbiome in acne: A comprehensive review. Journal of Clinical Medicine, 8(7), 987-1012. https://doi.org/10.3390/jcm8070987.
SanMiguel, A. J., Meisel, J. S., Horwinski, J., Zheng, Q., Bradley, C. W., & Grice, E. A. (2018). Antiseptic agents elicit short-term, personalized, and body site-specific shifts in resident skin bacterial communities. The Journal of Investigative Dermatology, 138(10), 2234-2243. https://doi.org/10.1016/j.jid.2018.04.022.
Fyhrquist, N., Muirhead, G., Prast-Nielsen, S., Jeanmougin, M., Olah, P., Skoog, T., Jules-Clement, G., Feld, M., Barrientos-Somarribas, M., Sinkko, H., van den Bogaard, E. H., Zeeuwen, P. L. J. M., Rikken, G., Schalkwijk, J., Niehues, H., Däubener, W., Eller, S. K., Alexander, H., Pennino, D., … & Alenius, H. (2019). Microbe-host interplay in atopic dermatitis and psoriasis. Nature Communications, 10, 4703.
Wikramanayake, T. C., Borda, L. J., Miteva, M., & Paus, R. (2019). Seborrheic dermatitis-looking beyond Malassezia. Experimental Dermatology, 28(9), 991-1001. https://doi.org/10.1111/exd.14006.
Knackstedt, R., Knackstedt, T., & Gatherwright, J. (2020). The role of topical probiotics on skin conditions: A systematic review of animal and human studies and implications for future therapies. Experimental Dermatology, 29(1), 15-21. https://doi.org/10.1111/exd.14032.
Bosch, T. C. G., & Miller, D. J. (2016). The holobiont imperative: Perspectives from early emerging animals. Springer-Verlag. The Hydra Holobiont: A Tale of Several Symbiotic Lineages 79. https://doi.org/10.1007/978-3-7091-1896-2.
Postler, T. S., & Ghosh, S. (2017). Understanding the holobiont: How microbial metabolites affect human health and shape the immune system. Cell Metabolism, 26(1), 110-130.
van de Guchte, M., Blottière, H. M., & Doré, J. (2018). Humans as holobionts: Implications for prevention and therapy. Microbiome, 6(1), 81. https://doi.org/10.1186/s40168-018-0466-8.
Philpott, M. P., Sanders, D. A., & Kealey, T. (1996). Whole hair follicle culture. Dermatologic Clinics, 14(4), 595-607. https://doi.org/10.1016/s0733-8635(05)70387-9.
Philpott, M. P. (2018). Culture of the human pilosebaceous unit, hair follicle and sebaceous gland. Experimental Dermatology, 27(5), 571-577. https://doi.org/10.1111/exd.13669.
Langan, E. A., Philpott, M. P., Kloepper, J. E., & Paus, R. (2015). Human hair follicle organ culture: Theory, application and perspectives. Experimental Dermatology, 24(12), 903-911. https://doi.org/10.1111/exd.12836.
Scharschmidt, T. C., Vasquez, K. S., Pauli, M. L., Leitner, E. G., Chu, K., Truong, H.-A., Lowe, M. M., Sanchez Rodriguez, R., Ali, N., Laszik, Z. G., Sonnenburg, J. L., Millar, S. E., & Rosenblum, M. D. (2017). Commensal microbes and hair follicle morphogenesis coordinately drive treg migration into neonatal skin. Cell Host & Microbe, 21(4), 467-477. https://doi.org/10.1016/j.chom.2017.03.001.
Meisel, J. S., Sfyroera, G., Bartow-McKenney, C., Gimblet, C., Bugayev, J., Horwinski, J., Kim, B., Brestoff, J. R., Tyldsley, A. S., Zheng, Q., Hodkinson, B. P., Artis, D., & Grice, E. A. (2018). Commensal microbiota modulate gene expression in the skin, Microbiome, 6(1), 20.
Kobayashi, T., Voisin, B., Kim, D. Y., Kennedy, E. A., Jo, J.-H., Shih, H.-Y., Truong, A., Doebel, T., Sakamoto, K., Cui, C.-Y., Schlessinger, D., Moro, K., Nakae, S., Horiuchi, K., Zhu, J., Leonard, W. J., Kong, H. H., & Nagao, K. (2019). Homeostatic control of sebaceous glands by innate lymphoid cells regulates commensal bacteria equilibrium. Cell, 176(5), 982-997.e16. https://doi.org/10.1016/j.cell.2018.12.031.
Stehlikova, Z., Kostovcikova, K., Kverka, M., Rossmann, P., Dvorak, J., Novosadova, I., Kostovcik, M., Coufal, S., Srutkova, D., Prochazkova, P., Hudcovic, T., Kozakova, H., Stepankova, R., Rob, F., Juzlova, K., Hercogova, J., Tlaskalova-Hogenova, H., & Jiraskova Zakostelska Z. (2019). Crucial role of microbiota in experimental psoriasis revealed by a gnotobiotic mouse model. Frontiers in Microbiology, 10, 236. https://doi.org/10.3389/fmicb.2019.00236.
Yang, J., Restori, K. H., Xu, M., Song, E. H., Zhao, L., Hu, S., Lyu, P., Wang, W.-B., & Xiong, N. (2020). Preferential perinatal development of skin-homing NK1.1 + innate lymphoid cells for regulation of cutaneous microbiota colonization, iScience, 23(4), 101014.
Patra, V., Wagner, K., Arulampalam, V., & Wolf, P. (2019). Skin microbiome modulates the effect of ultraviolet radiation on cellular response and immune function. iScience, 15, 211-222.
Oh, J. W., Kloepper, J., Langan, E. A., Kim, Y., Yeo, J., Kim, M. J., Hsi, T.-C., Rose, C., Yoon, G. S., Lee, S.-J., Seykora, J., Kim, J. C., Sung, Y. K., Kim, M., Paus, R., & Plikus, M. V. (2016). A guide to studying human hair follicle cycling in vivo. The Journal of Investigative Dermatology, 136(1), 34-44. https://doi.org/10.1038/JID.2015.354.
Fraune, S., Anton-Erxleben, F., Augustin, R., Franzenburg, S., Knop, M., Schröder, K., Willoweit-Ohl, D., & Bosch, T. C. (2014). Bacteria-bacteria interactions within the microbiota of the ancestral metazoan Hydra contribute to fungal resistance. The ISME Journal, 1543-1556. https://doi.org/10.1038/ismej.2014.239.
Schröder, K., & Bosch, T. C. G. (2016). The origin of mucosal immunity: Lessons from the holobiont Hydra. mBio, 7(6), e01184-16. https://doi.org/10.1128/mBio.01184-16.
Fraune, S., & Bosch, T. C. G. (2007). Long-term maintenance of species-specific bacterial microbiota in the basal metazoan Hydra. Proceedings of the National Academy of Sciences, 104(32), 13146-51. https://doi.org/10.1063/1.1599624.
Franzenburg, S., Walter, J., Künzel, S., Wang, J., Baines, J. F., Bosch, T. C. G., & Fraune, S. (2013). Distinct antimicrobial peptide expression determines host species-specific bacterial associations. Proceedings of the National Academy of Sciences of the United States of America, 110, E3730-8. https://doi.org/10.1073/pnas.1304960110/-/DCSupplemental.www.pnas.org/cgi/doi/10.1073/pnas.1304960110.
Bosch, T. C. G., & Zasloff, M. (2021). Antimicrobial peptides - or how our ancestors learned to control the microbiome. mBio, 12(5), e0184721.
Mergaert, P. (2018). Role of antimicrobial peptides in controlling symbiotic bacterial populations. Natural Product Reports, 35(4), 336-356.
Müller-Röver, S., Handjiski, B., van der Veen, C., Eichmüller, S., Foitzik, K., McKay, I. A., Stenn, K. S., & Paus, R. (2001). A comprehensive guide for the accurate classification of murine hair follicles in distinct hair cycle stages. The Journal of Investigative Dermatology, 117(1), 3-15. https://doi.org/10.1046/j.0022-202x.2001.01377.x.
Franzenburg, S., Fraune, S., Altrock, P. M., Künzel, S., Baines, J. F., Traulsen, A., & Bosch, T. C. G. (2013). Bacterial colonization of Hydra hatchlings follows a robust temporal pattern. The ISME Journal, 7(4), 781-790. https://doi.org/10.1038/ismej.2012.156.
Deines, P., Lachnit, T., & Bosch, T. C. G. (2017). Competing forces maintain the Hydra metaorganism. Immunological Reviews, 279(1), 123-136. https://doi.org/10.1111/imr.12564.
Lenhoff, H. M., & Brown, R. D. (1970). Mass culture of hydra: An improved method and its application to other aquatic invertebrates. Laboratorz Animals, 4(1), 139-154.
Schwentner, M., & Bosch, T. C. G. (2015). Revisiting the age, evolutionary history and species level diversity of the genus Hydra (Cnidaria: Hydrozoa). Molecular Phylogenetics and Evolution, 91, 41-55.
Lee, W.-S. (2011). Integral hair lipid in human hair follicle. Journal of Dermatological Science, 64(3), 153-158. https://doi.org/10.1016/j.jdermsci.2011.08.004.
Morinaga, H., Mohri, Y., Grachtchouk, M., Asakawa, K., Matsumura, H., Oshima, M., Takayama, N., Kato, T., Nishimori, Y., Sorimachi, Y., Takubo, K., Suganami, T., Iwama, A., Iwakura, Y., Dlugosz, A. A., & Nishimura, E. K. (2021). Obesity accelerates hair thinning by stem cell-centric converging mechanisms. Nature, 595(7866), 266-271. https://doi.org/10.1038/s41586-021-03624-x.
Palmer, M. A., Blakeborough, L., Harries, M., & Haslam, I. S. (2020). Cholesterol homeostasis: Links to hair follicle biology and hair disorders. Experimental Dermatology, 29(3), 299-311. https://doi.org/10.1111/exd.13993.
van Steensel, M. A. M., & Goh, B. C. (2021). Cutibacterium acnes: Much ado about maybe nothing much. Experimental Dermatology, 30(10), 1471-1476. https://doi.org/10.1111/exd.14394.
O'Neill, A. M., & Gallo, R. L. (2018). Host-microbiome interactions and recent progress into understanding the biology of acne vulgaris. Microbiome, 6(1), 177. https://doi.org/10.1186/s40168-018-0558-5.
Hansson, G. C. (2012). Role of mucus layers in gut infection and inflammation. Current Opinion in Microbiology, 15(1), 57-62. https://doi.org/10.1016/j.mib.2011.11.002.
Wein, T., Dagan, T., Fraune, S., Bosch, T. C. G., Reusch, T. B. H., & Hülter, N. F. (2018). Carrying capacity and colonization dynamics of curvibacter in the Hydra host habitat. Frontiers in Microbiology, 9, 443. https://doi.org/10.3389/fmicb.2018.00443.
Deines, P., Hammerschmidt, K., & Bosch, T. C. G. (2020). Microbial species coexistence depends on the host environment. mBio, 11(4), e00807-20. https://doi.org/10.1128/mBio.00807-20.
Lachnit, T., Bosch, T. C. G., & Deines, P. (2019). Exposure of the host-associated microbiome to nutrient-rich conditions may lead to dysbiosis and disease development-an evolutionary perspective. mBio, 10(3), e00355-19.
Nakamura, K., O'Neill, A. M., Williams, M. R., Cau, L., Nakatsuji, T., Horswill, A. R., & Gallo, R. L. (2020). Short chain fatty acids produced by Cutibacterium acnes inhibit biofilm formation by Staphylococcus epidermidis. Scientific Reports, 10, 21237.
Leech, J. M., Dhariwala, M. O., Lowe, M. M., Chu, K., Merana, G. R., Cornuot, C., Weckel, A., Ma, J. M., Leitner, E. G., Gonzalez, J. R., Vasquez, K. S., Diep, B. A., & Scharschmidt, T. C. (2019). Toxin-triggered interleukin-1 receptor signaling enables early-life discrimination of pathogenic versus commensal skin bacteria. Cell Host & Microbe, 26(6), 795-809.
Christensen, G. J. M., Scholz, C. F. P., Enghild, J., Rohde, H., Kilian, M., Thürmer, A., Brzuszkiewicz, E., Lomholt, H. B., & Brüggemann, H. (2016). Antagonism between Staphylococcus epidermidis and Propionibacterium acnes and its genomic basis. BMC Genomics, 17, 152. https://doi.org/10.1186/s12864-016-2489-5.
Lu, S.-E., Novak, J., Austin, F. W., Gu, G., Ellis, D., Kirk, M., Wilson-Stanford, S., Tonelli, M., & Smith, L. (2009). Occidiofungin, a unique antifungal glycopeptide produced by a strain of Burkholderia contaminans. Biochemistry, 48(35), 8312-8321. https://doi.org/10.1021/bi900814c.
Nguyen, M. T., Hanzelmann, D., Härtner, T., Peschel, A., & Götz, F. (2016). Skin-specific unsaturated fatty acids boost the staphylococcus aureus innate immune response. Infection and Immunity, 84(1), 205-215.
Coyte, K. Z., & Rakoff-Nahoum, S. (2019). Understanding competition and cooperation within the mammalian gut microbiome. Current Biology, 29(11), R538-R544. https://doi.org/10.1016/j.cub.2019.04.017.
Paetzold, B., Willis, J. R., de Lima, J. P., Knodlseder, N., Brüggemann, H., Quist, S. R., Gabaldon, T., & Guell, M. (2019). Skin microbiome modulation induced by probiotic solutions. Microbiome, 7(1), 95. https://doi.org/10.1186/s40168-019-0709-3.
Johnke, J., Dirksen, P., & Schulenburg, H. (2020). Community assembly of the native C. elegans microbiome is influenced by time, substrate and individual bacterial taxa. Environmental Microbiology, 22(4), 1265-1279. https://doi.org/10.1111/1462-2920.14932.
Simhadri, R. K., Fast, E. M., Guo, R., Schultz, M. J., Vaisman, N., Ortiz, L., Bybee, J., Slatko, B. E., & Frydman, H. M. (2017). The gut commensal microbiome of drosophila melanogaster is modified by the endosymbiont wolbachia. mSphere, 2(5), e00287-17. https://doi.org/10.1128/mSphere.00287-17.
Pinto, D., Sorbellini, E., Marzani, B., Rucco, M., Giuliani, G., & Rinaldi, F. (2019). Scalp bacterial shift in Alopecia areata. PLoS One, 14(4), e0215206. https://doi.org/10.1371/journal.pone.0215206.
Kang, H., Wu, W.-Y., Yu, M., Shapiro, J., & McElwee, K. J. (2020). Increased expression of TLR7 and TLR9 in alopecia areata. Experimental Dermatology, 29(3), 254-258. https://doi.org/10.1111/exd.14043.
Wang, J.-N., & Li, M. (2020). The immune function of keratinocytes in anti-pathogen infection in the skin. International Journal of Dermatology and Venereology, 3(4), 231-238. https://doi.org/10.1097/JD9.0000000000000094.
Lai, Y., & Gallo, R. L. (2008). Toll-like receptors in skin infectious and inflammatory diseases. Infectious Disorders Drug Targets, 8(3), 144-155.
Scharschmidt, T. C., Vasquez, K. S., Truong, H.-A., Gearty, S. V., Pauli, M. L., Nosbaum, A., Gratz, I. K., Otto, M., Moon, J. J., Liese, J., Abbas, A. K., Fischbach, M. A., & Rosenblum, M. D. (2015). A wave of regulatory T cells into neonatal skin mediates tolerance to commensal microbes. Immunity, 43(5), 1011-1021. https://doi.org/10.1016/j.immuni.2015.10.016.
Coombes, J. L., Siddiqui, K. R. R., Arancibia-Cárcamo, C. V., Hall, J., Sun, C.-M., Belkaid, Y., & Powrie, F. (2007). A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-β- and retinoic acid-dependent mechanism. The Journal of Experimental Medicine, 204(8), 1757-1764. https://doi.org/10.1084/jem.20070590.
Reithmayer, K., Meyer, K. C., Kleditzsch, P., Tiede, S., Uppalapati, S. K., Gläser, R., Harder, J., Schröder, J.-M., & Paus, R. (2009). Human hair follicle epithelium has an antimicrobial defence system that includes the inducible antimicrobial peptide psoriasin (S100A7) and RNase 7. The British Journal of Dermatology, 161(1), 78-89. https://doi.org/10.1111/j.1365-2133.2009.09154.x.
Chéret, J., Bertolini, M., Ponce, L., Lehmann, J., Tsai, T., Alam, M., Hatt, H., & Paus, R. (2018). Olfactory receptor OR2AT4 regulates human hair growth. Nature Communications, 9(1), 1-12. https://doi.org/10.1038/s41467-018-05973-0.
Schittek, B., Hipfel, R., Sauer, B., Bauer, J., Kalbacher, H., Stevanovic, S., Schirle, M., Schroeder, K., Blin, N., Meier, F., Rassner, G., & Garbe, C. (2001). Dermcidin: A novel human antibiotic peptide secreted by sweat glands. Nature Immunology, 2(12), 1133-1137. https://doi.org/10.1038/ni732.
Rademacher, F., Dreyer, S., Kopfnagel, V., Gläser, R., Werfel, T., & Harder, J. (2019). The antimicrobial and immunomodulatory function of RNase 7 in skin. Frontiers in Immunology, 10, 2553. https://doi.org/10.3389/fimmu.2019.02553.
Turner, J., Cho, Y., Dinh, N.-N., Waring, A. J., & Lehrer, R. I. (1998). Activities of LL-37, a cathelin-associated antimicrobial peptide of human neutrophils. Antimicrobial Agents and Chemotherapy, 42(9), 2206-2214.
Dürr, U. H. N., Sudheendra, U. S., & Ramamoorthy, A. (2006). LL-37, the only human member of the cathelicidin family of antimicrobial peptides. Biochimica et Biophysica Acta (BBA) - Biomembranes, 1758(9), 1408-1425. https://doi.org/10.1016/j.bbamem.2006.03.030.
Paulmann, M., Arnold, T., Linke, D., Özdirekcan, S., Kopp, A., Gutsmann, T., Kalbacher, H., Wanke, I., Schuenemann, V. J., Habeck, M., Bürck, J., Ulrich, A. S., & Schittek, B. (2012). Structure-activity analysis of the dermcidin-derived peptide DCD-1L, an anionic antimicrobial peptide present in human sweat*. Journal of Biological Chemistry, 287(11), 8434-8443. https://doi.org/10.1074/jbc.M111.332270.
Garreis, F., Gottschalt, M., Schlorf, T., Gläser, R., Harder, J., Worlitzsch, D., & Paulsen, F. P. (2011). Expression and regulation of antimicrobial peptide psoriasin (S100A7) at the ocular surface and in the lacrimal apparatus. Investigative Ophthalmology & Visual Science, 52(7), 4914-4922. https://doi.org/10.1167/iovs.10-6598.
Steffen, H., Rieg, S., Wiedemann, I., Kalbacher, H., Deeg, M., Sahl, H.-G., Peschel, A., Götz, F., Garbe, C., & Schittek, B. (2006). Naturally processed dermcidin-derived peptides do not permeabilize bacterial membranes and kill microorganisms irrespective of their charge. Antimicrobial Agents and Chemotherapy, 50(8), 2608-2620. https://doi.org/10.1128/AAC.00181-06.
Hata, T. R., & Gallo, R. L. (2008). Antimicrobial peptides, skin infections and atopic dermatitis. Seminars in Cutaneous Medicine and Surgery, 27(2), 144-150. https://doi.org/10.1016/j.sder.2008.04.002.
Cutuli, M., Cristiani, S., Lipton, J. M., & Catania, A. (2000). Antimicrobial effects of alpha-MSH peptides. Journal of Leukocyte Biology, 67(2), 233-239. https://doi.org/10.1002/jlb.67.2.233.
Paus, R. (2011). A neuroendocrinological perspective on human hair follicle pigmentation. Pigment Cell & Melanoma Research, 24(1), 89-106. https://doi.org/10.1111/j.1755-148X.2010.00808.x.
Kowalska, K., Carr, D. B., & Lipkowski, A. W. (2002). Direct antimicrobial properties of substance P. Life Sciences, 71(7), 747-750. https://doi.org/10.1016/S0024-3205(02)01740-X.
Racine, P.-J., Janvier, X., Clabaut, M., Catovic, C., Souak, D., Boukerb, A. M., Groboillot, A., Konto-Ghiorghi, Y., Duclairoir-Poc, C., Lesouhaitier, O., Orange, N., Chevalier, S., & Feuilloley, M. G. J. (2020). Dialog between skin and its microbiota: Emergence of “Cutaneous Bacterial Endocrinology”. Experimental Dermatology, 29(9), 790-800.
Augustin, R., Fraune, S., & Bosch, T. C. G. (2009). How Hydra senses and destroys microbes. Seminars in Immunology, 22(1), 54-58.
Fraune, S., Augustin, R., Anton-Erxleben, F., Wittlieb, J., Gelhaus, C., Klimovich, V. B., Samoilovich, M. P., & Bosch, T. C. G. (2010). In an early branching metazoan, bacterial colonization of the embryo is controlled by maternal antimicrobial peptides. Proceedings of the National Academy of Sciences, 107(42), 18067-18072. https://doi.org/10.1073/pnas.1008573107.
Jung, S., Dingley, A. J., Augustin, R., Anton-Erxleben, F., Stanisak, M., Gelhaus, C., Gutsmann, T., Hammer, M. U., Podschun, R., Bonvin, A. M. J. J., Leippe, M., Bosch, T. C. G., & Grötzinger, J. (2009). Hydramacin-1, structure and antibacterial activity of a protein from the basal metazoan hydra. Journal of Biological Chemistry, 1896-1905. https://doi.org/10.1074/jbc.M804713200.
Augustin, R., Anton-Erxleben, F., Jungnickel, S., Hemmrich, G., Spudy, B., Podschun, R., & Bosch, T. C. G. (2009). Activity of the novel peptide arminin against multiresistant human pathogens shows the considerable potential of phylogenetically ancient organisms as drug sources. Antimicrobial Agents and Chemotherapy, 53(12), 5245-5250. https://doi.org/10.1128/AAC.00826-09.
Augustin, R., Siebert, S., & Bosch, T. C. G. (2009). Identification of a kazal-type serine protease inhibitor with potent anti-staphylococcal activity as part of Hydra's innate immune system. Developmental and Comparative Immunology, 830-837. https://doi.org/10.1016/j.dci.2009.01.009.
Franzenburg, S., Fraune, S., Kunzel, S., Baines, J. F., Domazet-Loso, T., & Bosch, T. C. G. (2012). MyD88-deficient Hydra reveal an ancient function of TLR signaling in sensing bacterial colonizers. Proceedings of the National Academy of Sciences, 19374-19379. https://doi.org/10.1073/pnas.1213110109.
Mortzfeld, B. M., Taubenheim, J., Fraune, S., Klimovich, A. V., & Bosch, T. C. G. (2018). Stem cell transcription factor FoxO controls microbiome resilience in hydra. Frontiers in Microbiology, 9, 629. https://doi.org/10.3389/fmicb.2018.00629.
Bierkarre, H., Harder, J., Cuthbert, R., Emery, P., Leuschner, I., Mrowietz, U., Hedderich, J., McGonagle, D., & Gläser, R. (2016). Differential expression of antimicrobial peptides in psoriasis and psoriatic arthritis as a novel contributory mechanism for skin and joint disease heterogeneity. Scandinavian Journal of Rheumatology, 45(3), 188-196. https://doi.org/10.3109/03009742.2015.1091497.
Zhang, M., & Zhang, X. (2019). The role of PI3K/AKT/FOXO signaling in psoriasis. Archives of Dermatological Research, 311(2), 83-91. https://doi.org/10.1007/s00403-018-1879-8.
Constantinou, A., Kanti, V., Polak-Witka, K., Blume-Peytavi, U., Spyrou, G. M., & Vogt, A. (2021). The potential relevance of the microbiome to hair physiology and regeneration: The emerging role of metagenomics. Biomedicines, 9(3), 236. https://doi.org/10.3390/biomedicines9030236.
Nam, W., Kim, H., Bae, C., Kim, J., Nam, B., Kim, J., Park, S., Lee, J., & Sim, J. (2021). Lactobacillus paracasei HY7015 promotes hair growth in a telogenic mouse model. Journal of Medicinal Food, 24(7), 741-748. https://doi.org/10.1089/jmf.2020.4860.
Sanford, J. A., O'Neill, A. M., Zouboulis, C. C., & Gallo, R. L. (2019). Short-chain fatty acids from cutibacterium acnes activate both a canonical and epigenetic inflammatory response in human sebocytes. Journal of Immunology, 202(6), 1767-1776. https://doi.org/10.4049/jimmunol.1800893.
Paus, R., Langan, E. A., Vidali, S., Ramot, Y., & Andersen, B. (2014). Neuroendocrinology of the hair follicle: Principles and clinical perspectives. Trends in Molecular Medicine, 20(10), 559-570. https://doi.org/10.1016/j.molmed.2014.06.002.
Siebenhaar, F., Sharov, A. A., Peters, E. M. J., Sharova, T. Y., Syska, W., Mardaryev, A. N., Freyschmidt-Paul, P., Sundberg, J. P., Maurer, M., & Botchkarev, V. A. (2007). Substance P as an immunomodulatory neuropeptide in a mouse model for autoimmune hair loss (alopecia areata). The Journal of Investigative Dermatology, 127(6), 1489-1497. https://doi.org/10.1038/sj.jid.5700704.
Augustin, R., Schröder, K., Rincón, A. P. M., Fraune, S., Anton-Erxleben, F., Herbst, E.-M., Wittlieb, J., Schwentner, M., Grötzinger, J., Wassenaar, T. M., & Bosch, T. C. G. (2017). A secreted antibacterial neuropeptide shapes the microbiome of Hydra. Nature Communications, 8(1), 1-9. https://doi.org/10.1038/s41467-017-00625-1.
Murillo-Rincon, A. P., Klimovich, A., Pemöller, E., Taubenheim, J., Mortzfeld, B., Augustin, R., & Bosch, T. C. G. (2017). Spontaneous body contractions are modulated by the microbiome of Hydra. Scientific Reports, 7(1), 1-9. https://doi.org/10.1038/s41598-017-16191-x.
Klimovich, A., Giacomello, S., Björklund, Å., Faure, L., Kaucka, M., Giez, C., Murillo-Rincon, A. P., Matt, A.-S., Willoweit-Ohl, D., Crupi, G., Anda, J. d., Wong, G. C. L., D'Amato, M., Adameyko, I., & Bosch, T. C. G. (2020). Prototypical pacemaker neurons interact with the resident microbiota. Proceedings of the National Academy of Sciences, 117(30), 17854-17863. https://doi.org/10.1073/pnas.1920469117.
Krogh, A. (1929). The progress of physiology. Science, 70 200-204. https://doi.org/10.1126/science.70.1809.200.
Bosch, T. C. G., Guillemin, K., & McFall-Ngai, M. J. (2019). Evolutionary “experiments” in symbiosis: The study of model animals provides insights into the mechanisms underlying the diversity of host-microbe interactions. BioEssays, 41(10), 1800256.
Douglas, A. E. (2019). Simple animal models for microbiome research-PubMed. Nature Reviews. Microbiology, 17(12), 764-775.
McFall-Ngai, M., & Bosch, T. C. G. (2021). Chapter Eleven - Animal development in the microbial world: The power of experimental model systems. In S. F. Gilbert (Ed.), Current Topics in Developmental Biology (Vol. 141, pp. 371-397). Academic Press. https://doi.org/10.1016/bs.ctdb.2020.10.002.
George, S. M. C., Taylor, M. R., & Farrant, P. B. J. (2015). Psoriatic alopecia. Clinical and Experimental Dermatology, 40(7), 717-721.
O'Connell, T. M. (2020). The application of metabolomics to probiotic and prebiotic interventions in human clinical studies. Metabolites, 10(3), 120. https://doi.org/10.3390/metabo10030120.
Ring, H. C., Thorsen, J., Saunte, D. M., Lilje, B., Bay, L., Riis, P. T., Larsen, N., Andersen, L. O., Nielsen, H. V., Miller, I. M., Bjarnsholt, T., Fuursted, K., & Jemec, G. B. (2017). The follicular skin microbiome in patients with hidradenitis suppurativa and healthy controls. JAMA Dermatology, 153(9), 897-905. https://doi.org/10.1001/jamadermatol.2017.0904.
Ho, B. S.-Y., Ho, E. X. P., Chu, C. W., Ramasamy, S., Bigliardi-Qi M., de Sessions, P. F., & Bigliardi, P. L. (2019). Microbiome in the hair follicle of androgenetic alopecia patients. PLoS One, 14(5), e0216330. https://doi.org/10.1371/journal.pone.0216330.
Hall, J. B., Cong, Z., Imamura-Kawasawa, Y., Kidd, B. A., Dudley, J. T., Thiboutot, D. M., & Nelson, A. M. (2018). Isolation and identification of the follicular microbiome: Implications for acne research. The Journal of Investigative Dermatology, 138(9), 2033-2040. https://doi.org/10.1016/j.jid.2018.02.038.
Schneider, M. R., Schmidt-Ullrich, R., & Paus, R. (2009). The hair follicle as a dynamic miniorgan. Current Biology, 19(3), R132-R142. https://doi.org/10.1016/j.cub.2008.12.005.
Schröder, K., & Bosch, T. C. G. (2016). The origin of mucosal immunity: Lessons from the holobiont Hydra. mBio, 7(6), e01184-16.
Reddy, P. C., Gungi, A., & Unni, M. (2019). Cellular and molecular mechanisms of Hydra regeneration. Results and Problems in Cell Differentiation, 68, 259-290. https://doi.org/10.1007/978-3-030-23459-1_12.
Christoph, T., Müller-Röver, S., Audring, H., Tobin, D. J., Hermes, B., Cotsarelis, G., Rückert, R., & Paus, R. (2000). The human hair follicle immune system: Cellular composition and immune privilege. The British Journal of Dermatology, 142(5), 862-873. https://doi.org/10.1046/j.1365-2133.2000.03464.x.
Rathje, K., Mortzfeld, B., Hoeppner, M. P., Taubenheim, J., Bosch, T. C. G., & Klimovich, A. (2020). Dynamic interactions within the host-associated microbiota cause tumor formation in the basal metazoan Hydra. PLoS Pathogens, 16(3), e1008375. https://doi.org/10.1371/journal.ppat.1008375.
Sugawara, K., Bíró, T., Tsuruta, D., Tóth, B. I., Kromminga, A., Zákány, N., Zimmer, A., Funk, W., Gibbs, B. F., Zimmer, A., & Paus, R. (2012). Endocannabinoids limit excessive mast cell maturation and activation in human skin. The Journal of Allergy and Clinical Immunology, 129(3), 726-738.e8. https://doi.org/10.1016/j.jaci.2011.11.009.
Szymanski, J. R., & Yuste, R. (2019). Mapping the whole-body muscle activity of Hydra vulgaris. Current Biology, 29(11), 1807-1817.e3. https://doi.org/10.1016/j.cub.2019.05.012.
Emelianov, V., Bechara, F. G., Gläser, R., Langan, E. A., Taungjaruwinai, W. M., Schröder, J.-M., Meyer, K. C., & Paus, R. (2012). Immunohistological pointers to a possible role for excessive cathelicidin (LL-37) expression by apocrine sweat glands in the pathogenesis of hidradenitis suppurativa/acne inversa. The British Journal of Dermatology, 166, 1023-1034. https://doi.org/10.1111/j.1365-2133.2011.10765.x.
Technau, U., & Steele, R. E. (2011). Evolutionary crossroads in developmental biology. Cnidaria Development, 138(8), 1447-1458.