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Robert Sanchez Rodriguez, … , Abul K. Abbas, Michael D. Rosenblum
Published February 10, 2014
Citation Information: J Clin Invest. 2014;124(3):1027-1036. https://doi.org/10.1172/JCI72932.
Citation Information: J Clin Invest. 2014;124(3):1027-1036. https://doi.org/10.1172/JCI72932.
Abstract
Regulatory T cells (Tregs), which are characterized by expression of the transcription factor Foxp3, are a dynamic and heterogeneous population of cells that control immune responses and prevent autoimmunity. We recently identified a subset of Tregs in murine skin with properties typical of memory cells and defined this population as memory Tregs (mTregs). Due to the importance of these cells in regulating tissue inflammation in mice, we analyzed this cell population in humans and found that almost all Tregs in normal skin had an activated memory phenotype. Compared with mTregs in peripheral blood, cutaneous mTregs had unique cell surface marker expression and cytokine production. In normal human skin, mTregs preferentially localized to hair follicles and were more abundant in skin with high hair density. Sequence comparison of TCRs from conventional memory T helper cells and mTregs isolated from skin revealed little homology between the two cell populations, suggesting that they recognize different antigens. Under steady-state conditions, mTregs were nonmigratory and relatively unresponsive; however, in inflamed skin from psoriasis patients, mTregs expanded, were highly proliferative, and produced low levels of IL-17. Taken together, these results identify a subset of Tregs that stably resides in human skin and suggest that these cells are qualitatively defective in inflammatory skin disease.
Authors
Robert Sanchez Rodriguez, Mariela L. Pauli, Isaac M. Neuhaus, Siegrid S. Yu, Sarah T. Arron, Hobart W. Harris, Sara Hsin-Yi Yang, Bryan A. Anthony, Francis M. Sverdrup, Elisabeth Krow-Lucal, Tippi C. MacKenzie, David S. Johnson, Everett H. Meyer, Andrea Löhr, Andro Hsu, John Koo, Wilson Liao, Rishu Gupta, Maya G. Debbaneh, Daniel Butler, Monica Huynh, Ethan C. Levin, Argentina Leon, William Y. Hoffman, Mary H. McGrath, Michael D. Alvarado, Connor H. Ludwig, Hong-An Truong, Megan M. Maurano, Iris K. Gratz, Abul K. Abbas, Michael D. Rosenblum
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Citation information
Citations to this article (179)
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N Malhotra, JM Leyva-Castillo, U Jadhav, O Barreiro, C Kam, NK ONeill, F Meylan, P Chambon, UH von Andrian, RM Siegel, EC Wang, R Shivdasani, RS Geha |
Science Immunology | 2018 |
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Taking the lead – how keratinocytes orchestrate skin T cell immunity
MM Klicznik, AB Szenes-Nagy, DJ Campbell, IK Gratz |
Immunology Letters | 2018 |
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Targeting Regulatory T Cells to Treat Patients With Systemic Lupus Erythematosus
M Mizui, GC Tsokos |
Frontiers in immunology | 2018 |
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Regulatory T-Cells: Potential Regulator of Tissue Repair and Regeneration
J Li, J Tan, MM Martino, KO Lui |
Frontiers in immunology | 2018 |
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Innate immunity and effector and regulatory mechanisms involved in allergic contact dermatitis
MC Silvestre, MN Sato, VM dos Reis |
Anais Brasileiros de Dermatologia | 2018 |
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T Regulatory Cell Subpopulations Associated with Recent Ultraviolet Radiation Exposure in a Skin Cancer Screening Cohort
RS Hesterberg, RP Amorrortu, Y Zhao, S Hampras, AA Akuffo, N Fenske, B Cherpelis, J Balliu, L Vijayan, PK Epling-Burnette, DE Rollison |
Journal of immunology (Baltimore, Md. : 1950) | 2018 |
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Herpes simplex virus-2 dynamics as a probe to measure the extremely rapid and spatially localized tissue-resident T-cell response
JT Schiffer, DA Swan, M Prlic, JM Lund |
Immunological Reviews | 2018 |
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Langerhans Cells Prevent Autoimmunity via Expansion of Keratinocyte Antigen-Specific Regulatory T Cells
DY Kitashima, T Kobayashi, T Woodring, K Idouchi, T Doebel, B Voisin, T Adachi, T Ouchi, H Takahashi, K Nishifuji, DH Kaplan, BE Clausen, M Amagai, K Nagao |
EBioMedicine | 2018 |
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Foxp3 + T reg cells control psoriasiform inflammation by restraining an IFN-I–driven CD8 + T cell response
K Stockenhuber, AN Hegazy, NR West, NE Ilott, A Stockenhuber, SJ Bullers, EE Thornton, IC Arnold, A Tucci, H Waldmann, GS Ogg, F Powrie |
Journal of Experimental Medicine | 2018 |
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CD4+ Memory T Cells at Home in the Tissue: Mechanisms for Health and Disease
D Schreiner, CG King |
Frontiers in immunology | 2018 |
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SJS/TEN 2017: Building Multidisciplinary Networks to Drive Science and Translation
KD White, R Abe, M Ardern-Jones, T Beachkofsky, C Bouchard, B Carleton, J Chodosh, R Cibotti, R Davis, JC Denny, RP Dodiuk-Gad, EN Ergen, JL Goldman, JH Holmes, SI Hung, ME Lacouture, RJ Lehloenya, S Mallal, TA Manolio, RG Micheletti, CM Mitchell, M Mockenhaupt, DA Ostrov, R Pavlos, M Pirmohamed, E Pope, A Redwood, M Rosenbach, MD Rosenblum, JC Roujeau, AP Saavedra, HN Saeed, JP Struewing, H Sueki, C Sukasem, C Sung, JA Trubiano, J Weintraub, LM Wheatley, KB Williams, B Worley, WH Chung, NH Shear, EJ Phillips |
The Journal of Allergy and Clinical Immunology: In Practice | 2018 |
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Oral immunotherapy with omalizumab reverses the Th2 cell-like programme of regulatory T cells and restores their function
A Abdel-Gadir, L Schneider, A Casini, LM Charbonnier, SV Little, T Harrington, DT Umetsu, R Rachid, TA Chatila |
Cell | 2018 |
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Human T Cell Development, Localization, and Function throughout Life
BV Kumar, TJ Connors, DL Farber |
Immunity | 2018 |
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Identification of Casz1 as a Regulatory Protein Controlling T Helper Cell Differentiation, Inflammation, and Immunity
N Bhaskaran, Z Liu, SS Saravanamuthu, C Yan, Y Hu, L Dong, P Zelenka, L Zheng, V Bletsos, R Harris, B Harrington, A Weinberg, CJ Thiele, F Ye, P Pandiyan |
Frontiers in immunology | 2018 |
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The Role of Skin and Orogenital Microbiota in Protective Immunity and Chronic Immune-Mediated Inflammatory Disease
YJ Park, HK Lee |
Frontiers in immunology | 2018 |
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Immunological memory cells
W Ratajczak, P Niedźwiedzka-Rystwej, B Tokarz-Deptuła, W Deptuła |
CENT EUR J IMMUNOL | 2018 |
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CCR8 Expression Defines Tissue-Resident Memory T Cells in Human Skin
ML McCully, K Ladell, R Andrews, RE Jones, KL Miners, L Roger, DM Baird, MJ Cameron, ZM Jessop, IS Whitaker, EL Davies, DA Price, B Moser |
Journal of immunology (Baltimore, Md. : 1950) | 2018 |
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Altered expression of regulatory molecules in the skin of psoriasis
AD Sabag, D Dias-Polak, J Bejar, H Sheffer, R Bergman, Z Vadasz |
Immunologic Research | 2018 |
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Partially Exhausted Tumor Infiltrating Lymphyctes Predict Response to Combination Immunotherapy
Kimberly Loo, Katy Tsai, Kelly Mahuron, Jacqueline Liu, Mariela L. Pauli, Priscila Sandoval, Adi Nosrati, James Lee, lawrence chen, Jimmy Hwang, Lauren Levine, Matthew Krummel, Alain Algazi, Miguel Pampaloni, Michael D. Alvarado, Michael D. Rosenblum, Adil Daud |
JCI Insight | 2017 |
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Therapeutic application of T regulatory cells in composite tissue allotransplantation
JH Yang, SC Eun |
Journal of Translational Medicine | 2017 |
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Heterogeneity and Stability in Foxp3+ Regulatory T Cells
B Min |
Journal of Interferon & Cytokine Research | 2017 |
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Regulatory T Cell and Forkhead Box Protein 3 as Modulators of Immune Homeostasis
LM Pereira, ST Gomes, R Ishak, AC Vallinoto |
Frontiers in immunology | 2017 |
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Immune-Mediated Repair: A Matter of Plasticity
T Pradeu, P Laurent, V Jolivel, P Manicki, L Chiu, C Contin-Bordes, ME Truchetet |
Frontiers in immunology | 2017 |
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Homeostatic Immunity and the Microbiota
Y Belkaid, OJ Harrison |
Immunity | 2017 |
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Emerging Skin T-Cell Functions in Response to Environmental Insults
J Suwanpradid, ZE Holcomb, AS MacLeod |
Journal of Investigative Dermatology | 2017 |
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IL-17A-Producing Foxp3 + Regulatory T Cells and Human Diseases
MK Jung, JE Kwak, EC Shin |
Immune Network | 2017 |
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Regulatory T cells in skin
N Ali, MD Rosenblum |
Immunology | 2017 |
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Regulatory T-cell heterogeneity and the cancer immune response
KA Ward-Hartstonge, RA Kemp |
IBMS BoneKEy | 2017 |
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Establishing Tolerance to Commensal Skin Bacteria
TC Scharschmidt |
Dermatologic Clinics | 2017 |
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CD49a Expression Defines Tissue-Resident CD8+ T Cells Poised for Cytotoxic Function in Human Skin
S Cheuk, H Schlums, IG Sérézal, E Martini, SC Chiang, N Marquardt, A Gibbs, E Detlofsson, A Introini, M Forkel, C Höög, A Tjernlund, J Michaëlsson, L Folkersen, J Mjösberg, L Blomqvist, M Ehrström, M Ståhle, YT Bryceson, L Eidsmo |
Immunity | 2017 |
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Analysis of FOXP3+ regulatory T cell subpopulations in peripheral blood and tissue of patients with systemic lupus erythematosus
A Schmidt, CC Rieger, RK Venigalla, S Éliás, R Max, HM Lorenz, HJ Gröne, PH Krammer, A Kuhn |
Immunologic Research | 2017 |
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Commensal Microbes and Hair Follicle Morphogenesis Coordinately Drive Treg Migration into Neonatal Skin
TC Scharschmidt, KS Vasquez, ML Pauli, EG Leitner, K Chu, HA Truong, MM Lowe, RS Rodriguez, N Ali, ZG Laszik, JL Sonnenburg, SE Millar, MD Rosenblum |
Cell Host & Microbe | 2017 |
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Regulatory T Cells in Skin Facilitate Epithelial Stem Cell Differentiation
N Ali, B Zirak, RS Rodriguez, ML Pauli, HA Truong, K Lai, R Ahn, K Corbin, MM Lowe, TC Scharschmidt, K Taravati, MR Tan, RR Ricardo-Gonzalez, A Nosbaum, M Bertolini, W Liao, FO Nestle, R Paus, G Cotsarelis, AK Abbas, MD Rosenblum |
Cell | 2017 |
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Genomic analysis of atypical fibroxanthoma
K Lai, CA Harwood, KJ Purdie, CM Proby, IM Leigh, N Ravi, TW Mully, L Brooks, PM Sandoval, MD Rosenblum, ST Arron, OR Bandapalli |
PloS one | 2017 |
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Erosive Pustular Dermatosis: A Manifestation of Immunosenescence A Report of 8 Cases
T Thuraisingam, P Mirmirani |
Skin Appendage Disorders | 2017 |
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Skin-infiltrating, interleukin-22—producing T cells differentiate pediatric psoriasis from adult psoriasis
Cordoro KM, Hitraya-Low M, Taravati K, Sandoval PM, Kim E, Sugarman J, Pauli ML, Liao W, Rosenblum MD |
Journal of the American Academy of Dermatology | 2017 |
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Tumor immune profiling predicts response to anti-PD-1 therapy in human melanoma
Adil Daud, Kimberly Loo, Mariela L. Pauli, Robert Sanchez Rodriguez, Priscila Munoz Sandoval, Keyon Taravati, Katy Tsai, Adi Nosrati, Lorenzo Nardo, Michael D. Alvarado, Alain Algazi, Miguel Hernandez Pampaloni, Iryna Lobach, Jimmy Hwang, Robert Pierce, Iris Gratz, Matthew Krummel, Michael D. Rosenblum |
Journal of Clinical Investigation | 2016 |
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In Situ Detection of Regulatory T Cells in Human Genital Herpes Simplex Virus Type 2 (HSV-2) Reactivation and Their Influence on Spontaneous HSV-2 Reactivation
N Milman, J Zhu, C Johnston, A Cheng, A Magaret, DM Koelle, ML Huang, L Jin, A Klock, ED Layton, L Corey |
The Journal of Infectious Diseases | 2016 |
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Cutting Edge: Regulatory T Cells Facilitate Cutaneous Wound Healing
A Nosbaum, N Prevel, HA Truong, P Mehta, M Ettinger, TC Scharschmidt, NH Ali, ML Pauli, AK Abbas, MD Rosenblum |
Journal of immunology (Baltimore, Md. : 1950) | 2016 |
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Mechanisms of T cell organotropism
H Fu, EJ Ward, FM Marelli-Berg |
Cellular and Molecular Life Sciences | 2016 |
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Transition from inflammation to proliferation: a critical step during wound healing
NX Landén, D Li, M Ståhle |
Cellular and Molecular Life Sciences | 2016 |
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Regulatory T Cells in Systemic Sclerosis: a Comprehensive Review
G Slobodin, D Rimar |
Clinical Reviews in Allergy & Immunology | 2016 |
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Characterization of the human immune cell network at the gingival barrier
N Dutzan, JE Konkel, T Greenwell-Wild, NM Moutsopoulos |
Mucosal Immunology | 2016 |
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The distribution of cutaneous metastases correlates with local immunologic milieu
JM Schulman, ML Pauli, IM Neuhaus, RS Rodriguez, K Taravati, US Shin, TH McCalmont, MD Rosenblum |
Journal of the American Academy of Dermatology | 2016 |
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The influence of skin microorganisms on cutaneous immunity
Y Belkaid, S Tamoutounour |
Nature Reviews Immunology | 2016 |
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Network analysis of psoriasis reveals biological pathways and roles for coding and long non-coding RNAs
R Ahn, R Gupta, K Lai, N Chopra, ST Arron, W Liao |
BMC Genomics | 2016 |
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Novel perspectives on the role of the human microbiota in regenerative medicine and surgery
T Pellegatta, M Saler, V Bonfanti, G Nicoletti, A Faga |
Biomedical Reports | 2016 |
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Mechanisms of human autoimmunity
Michael D. Rosenblum, Kelly Remedios, Abul K. Abbas |
Journal of Clinical Investigation | 2015 |
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Requirement for CD28 in Effector Regulatory T Cell Differentiation, CCR6 Induction, and Skin Homing
R Zhang, CM Borges, MY Fan, JE Harris, LA Turka |
Journal of immunology (Baltimore, Md. : 1950) | 2015 |
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The emerging role of resident memory T cells in protective immunity and inflammatory disease
CO Park, TS Kupper |
Nature Medicine | 2015 |
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The role of lymphocytes in the development and treatment of alopecia areata
H Guo, Y Cheng, J Shapiro, K McElwee |
Expert Review of Clinical Immunology | 2015 |
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New insights into the mechanisms of Treg function:
DM Rothstein, G Camirand |
Current Opinion in Organ Transplantation | 2015 |
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Tissue resident regulatory T cells: novel therapeutic targets for human disease
X Zhou, J Tang, H Cao, H Fan, B Li |
Cellular and Molecular Immunology | 2015 |
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High frequency of central memory regulatory T cells allows detection of liver recipients at risk of early acute rejection within the first month after transplantation
F Boix-Giner, O Millan, DS Segundo, P Muñoz-Cacho, E Mancebo, S Llorente, L Rafael-Valdivia, A Rimola, E Fábrega, A Mrowiec, L Allende, A Minguela, JM Bolarín, E Paz-Artal, M López-Hoyos, M Brunet, M Muro |
International Immunology | 2015 |
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Origin and functions of pro-inflammatory cytokine producing Foxp3+ regulatory T cells
P Pandiyan, J Zhu |
Cytokine | 2015 |
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Co-stimulation with TNF receptor superfamily 4/25 antibodies enhances in-vivo expansion of CD4+CD25+Foxp3+ T cells (Tregs) in a mouse study for active DNA Aβ42 immunotherapy
D Lambracht-Washington, RN Rosenberg |
Journal of Neuroimmunology | 2015 |
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Hair follicle–derived IL-7 and IL-15 mediate skin-resident memory T cell homeostasis and lymphoma
T Adachi, T Kobayashi, E Sugihara, T Yamada, K Ikuta, S Pittaluga, H Saya, M Amagai, K Nagao |
Nature Medicine | 2015 |
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Controlling the fire — tissue-specific mechanisms of effector regulatory T-cell homing
Z Chow, A Banerjee, MJ Hickey |
Immunology and Cell Biology | 2015 |
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Targeting the inflammasome in rheumatic diseases
SS McCoy, J Stannard, JM Kahlenberg |
Translational Research | 2015 |
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Regulatory T cell memory
MD Rosenblum, SS Way, AK Abbas |
Nature Reviews Immunology | 2015 |
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A Wave of Regulatory T Cells into Neonatal Skin Mediates Tolerance to Commensal Microbes
TC Scharschmidt, KS Vasquez, HA Truong, SV Gearty, ML Pauli, A Nosbaum, IK Gratz, M Otto, JJ Moon, J Liese, AK Abbas, MA Fischbach, MD Rosenblum |
Immunity | 2015 |
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Effects of the Staphylococcus aureus and Staphylococcus epidermidis Secretomes Isolated from the Skin Microbiota of Atopic Children on CD4+ T Cell Activation
E Laborel-Préneron, P Bianchi, F Boralevi, P Lehours, F Fraysse, F Morice-Picard, M Sugai, Y Sato'o, C Badiou, G Lina, AM Schmitt, D Redoulès, C Casas, C Davrinche, IC Allen |
PloS one | 2015 |
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Control of Regulatory T Cell Migration, Function, and Homeostasis
DJ Campbell |
Journal of immunology (Baltimore, Md. : 1950) | 2015 |
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Organ-specific and memory treg cells: specificity, development, function, and maintenance
IK Gratz, DJ Campbell |
Frontiers in immunology | 2014 |
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Microbiota in Healthy Skin and in Atopic Eczema
G Baviera, MC Leoni, L Capra, F Cipriani, G Longo, N Maiello, G Ricci, E Galli |
BioMed Research International | 2014 |
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Human skin residency
O Leavy |
Nature Reviews Immunology | 2014 |
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