Abstract
Dendritic cells form the link between the innate and adaptative immune response, particularly on mucosal and epidermal surfaces. The Langerhans, an epidermal dendritic cell subpopulation, play a key role in the skin immune response across several species. Scarse immune cell subpopulations, including Langerhans-like cells, have been identified in endangered green turtles thereby complicating the understanding of the pathogenesis of diseases such as fibropapillomatosis, which induces skin tumours in this species worldwide. In biopsies from green turtle skin, we demonstrated that the polyclonal anti-human Langerin antibodies strongly stained a Langerin+ cell population in epidermal sheets, the suprabasal layer of the epidermis in cryosections and in cells from cytospin preparation of migration assays. The morphology of these cells was round to amoeboid in normal skin; however, in skin with ulcerative dermatitis, Langerin+ cells aggregated around ulcers and adopted a more pleomorphic morphology. To our knowledge, this is the first identification of Langerin+ cells with a molecular marker in a reptile species.
This is a preview of subscription content, log in via an institution to check access.
Data availability
Not applicable.
Code availability
Not applicable.
References
Armando P-T, Millan-Aldaco Diana R-ZA (1995) Epidermal Langerhans cells in the terrestrial turtle Kinosternum integrum. Dev Comp Immunol 19:225–236
Bursch LS, Wang L, Igyarto B et al (2007) Identification of a novel population of Langerin + dendritic cells. J Exp Med 204:3147–3156. https://doi.org/10.1084/jem.20071966
Costanzo JP, Lee RE, Ultsch GR (2008) Physiological ecology of overwintering in hatchling turtles. J Exp Zool Part A Ecol Genet Physiol 309:297–379. https://doi.org/10.1002/jez.460
Deckers J, Hammad H, Hoste E (2018) Langerhans cells: sensing the environment in health and disease. Front Immunol 9:1–14. https://doi.org/10.3389/fimmu.2018.00093
Duffy DJ, Schnitzler C, Karpinski L et al (2018) Sea turtle fibropapilloma tumors share genomic drivers and therapeutic vulnerabilities with human cancers. Commun Biol 1:63. https://doi.org/10.1038/s42003-018-0059-x
Geissmann F, Dieu-Nosjean MC, Dezutter C et al (2002) Accumulation of immature Langerhans cells in human lymph nodes draining chronically inflamed skin. J Exp Med 196:417–430. https://doi.org/10.1084/jem.20020018
Glazebrook JS, Campbell RSF (1990) A survey of the diseases of marine turtles in northern Australia.I Farmed turtles. Dis Aquat Organ 9:83–95. https://doi.org/10.3354/dao009083
Lovy J, Savidant GP, Speare DJ, Wright GM (2009) Langerin/CD207 positive dendritic-like cells in the haemopoietic tissues of salmonids. Fish Shellfish Immunol 27:365–368. https://doi.org/10.1016/j.fsi.2009.01.006
Muñoz FA, Estrada-Parra S, Romero-Rojas A et al (2009) Identification of CD3+ T lymphocytes in the green turtle Chelonia mydas. Vet Immunol Immunopathol 131. https://doi.org/10.1016/j.vetimm.2009.04.015
Muñoz FA, Estrada-Parra S, Romero-Rojas A et al (2013) Immunological evaluation of captive green sea turtle (chelonia mydas) with ulcerative dermatitis. J Zoo Wildl Med 44. https://doi.org/10.1638/2010-0228R4.1
Nagy N, Bódi I, Oláh I (2016) Avian dendritic cells: phenotype and ontogeny in lymphoid organs. Dev Comp Immunol. https://doi.org/10.1016/j.dci.2015.12.020
Nishibu A, Ward BR, Jester JV et al (2006) Behavioral responses of epidermal Langerhans cells in situ to local pathological stimuli. J Invest Dermatol 126:787–796. https://doi.org/10.1038/sj.jid.5700107
Quesada-Pascual F, Jimenez-Flores R, Flores-Langarica A et al (2008) Characterization of langerhans cells in epidermal sheets along the body of Armadillo (Dasypus novemcinctus). Vet Immunol Immunopathol 124:220–229. https://doi.org/10.1016/j.vetimm.2008.03.011
Schuler BYG, Steinman RM (1985) Murine epidermal langerhans cells mature into potent immunostimulatory dendritic cells in vitro. J Exp Med 161:526–546
Van Der Vlist M, Geijtenbeek TBH (2010) Langerin functions as an antiviral receptor on Langerhans cells. Immunol Cell Biol 88:410–415
Work TM, Rameyer RA, Balazs GH et al (2001) Immune status of free-ranging green turtles with Fibropapillomatosis from Hawaii. J Wildl Dis 37:574–581. https://doi.org/10.7589/0090-3558-37.3.574
Work TM, Dagenais J, Balazs GH et al (2015) Dynamics of virus shedding and in situ confirmation of Chelonid herpesvirus 5 in Hawaiian green turtles with Fibropapillomatosis. Vet Pathol 52:1195–1201. https://doi.org/10.1177/0300985814560236
Yetsko K, Farrell JA, Blackburn NB et al (2021) Molecular characterization of a marine turtle tumor epizootic, profiling external, internal and postsurgical regrowth tumors. Commun Biol 4. https://doi.org/10.1038/s42003-021-01656-7
Zimmerman LM (2020) The reptilian perspective on vertebrate immunity: 10 years of progress. J Exp Biol 223. https://doi.org/10.1242/jeb.214171
Acknowledgements
To the staff of Laboratory 15 of the Cell Biology Department of CINVESTAV for all their technical support. To Xcaret Park and especially to the Corporate Direction of Conservation.
Xcaret Group for providing the biological samples for this study. A very special posthumous thanks to Dr. Leopoldo Flores, who was a great intellectual and spiritual leader of our group. This work was funded in part by the CONACyT postdoctoral fellowship.
Funding
This work was funded in part by the CONACyT postdoctoral fellowship.
Author information
Authors and Affiliations
Contributions
The authors of the submitted manuscript participated equally in the conception and design of the research (Leopoldo Flores-Romo, Fernando Alberto Muñoz Tenería), design and execution of the fieldwork and biological sampling (Ana Cecilia Negrete-Philippe, Fernando Alberto Muñoz Tenería), laboratory work and data acquisition and analysis (Juana Calderón-Amador, Fernando Alberto Muñoz Tenería), writing of the first draft (Fernando Alberto Muñoz Tenería), supervision, revision and editing of the manuscript (Leopoldo Flores-Romo).
Corresponding author
Ethics declarations
Ethical approval
The skin biopsies of the specimens were obtained by the veterinary staff of Xcaret Park, under the medical and welfare protocols and internal legislation of the Institution.
Consent to participate
All authors read the manuscript and approved their participation.
Consent for publication
All authors approved the publication of the manuscript.
Conflicts to interest
The authors declare that there are no conflicts of interest.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Muñoz Tenería, F.A., Calderón-Amador, J., Negrete-Philippe, A.C. et al. A subpopulation of green turtle suprabasal epidermal cells are Langerin+ and migrate under in vitro stimulation of the chemokine CCL21. Vet Res Commun 46, 939–945 (2022). https://doi.org/10.1007/s11259-021-09883-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11259-021-09883-3