Multiomic single-cell sequencing defines tissue-specific responses in Stevens-Johnson syndrome and toxic epidermal necrolysis.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
08 Oct 2024
Historique:
received: 12 12 2023
accepted: 27 09 2024
medline: 9 10 2024
pubmed: 9 10 2024
entrez: 8 10 2024
Statut: epublish

Résumé

Stevens-Johnson syndrome and toxic epidermal necrolysis (SJS/TEN) is a rare but life-threatening cutaneous drug reaction mediated by human leukocyte antigen (HLA) class I-restricted CD8

Identifiants

pubmed: 39379371
doi: 10.1038/s41467-024-52990-3
pii: 10.1038/s41467-024-52990-3
doi:

Substances chimiques

Receptors, Antigen, T-Cell 0
Granzymes EC 3.4.21.-
GNLY protein, human 0
Perforin 126465-35-8
Histocompatibility Antigens Class I 0
Antigens, Differentiation, T-Lymphocyte 0
GZMB protein, human EC 3.4.21.-

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

8722

Subventions

Organisme : U.S. Department of Health & Human Services | National Institutes of Health (NIH)
ID : U01AI154659
Organisme : U.S. Department of Health & Human Services | National Institutes of Health (NIH)
ID : P50GM115305
Organisme : U.S. Department of Health & Human Services | National Institutes of Health (NIH)
ID : R01HG010863
Organisme : U.S. Department of Health & Human Services | National Institutes of Health (NIH)
ID : R21AI139021
Organisme : U.S. Department of Health & Human Services | National Institutes of Health (NIH)
ID : R01AI152183
Organisme : U.S. Department of Health & Human Services | National Institutes of Health (NIH)
ID : 2 D43 TW010559
Organisme : NIAID NIH HHS
ID : P30 AI110527
Pays : United States
Organisme : NIAID NIH HHS
ID : P30 AI110527
Pays : United States
Organisme : U.S. Department of Health & Human Services | National Institutes of Health (NIH)
ID : 2 D43 TW010559
Organisme : U.S. Department of Health & Human Services | National Institutes of Health (NIH)
ID : K43 TW011178-01
Organisme : U.S. Department of Health & Human Services | National Institutes of Health (NIH)
ID : R01AI152183
Organisme : U.S. Department of Health & Human Services | National Institutes of Health (NIH)
ID : 2 D43 TW010559
Organisme : NIAID NIH HHS
ID : P30 AI110527
Pays : United States
Organisme : U.S. Department of Health & Human Services | National Institutes of Health (NIH)
ID : P50GM115305
Organisme : Department of Health | National Health and Medical Research Council (NHMRC)
ID : GNT1123499
Organisme : Department of Health | National Health and Medical Research Council (NHMRC)
ID : GNT2028952
Organisme : Department of Health | National Health and Medical Research Council (NHMRC)
ID : GNT2028952
Organisme : Department of Health | National Health and Medical Research Council (NHMRC)
ID : GNT2028952
Organisme : Department of Health | National Health and Medical Research Council (NHMRC)
ID : GNT2028952

Investigateurs

Jason Trubiano (J)

Informations de copyright

© 2024. The Author(s).

Références

Marks, M. E. et al. Updates in SJS/TEN: collaboration, innovation, and community. Front. Med. 10, 1213889 (2023).
doi: 10.3389/fmed.2023.1213889
Krantz, M., Yoon, B., Stone, C., Yu, R. & Phillips, E. Stevens-Johnson syndrome and toxic epidermal necrolysis in the FDA adverse event reporting system (FAERS) from 1995-2020. J. Allergy Clin. Immunol. 149, AB62 (2022).
doi: 10.1016/j.jaci.2021.12.233
Posadas, S. J. et al. Delayed reactions to drugs show levels of perforin, granzyme B, and Fas-L to be related to disease severity. J. Allergy Clin. Immunol. 109, 155–161 (2002).
doi: 10.1067/mai.2002.120563
Chung, W.-H. et al. Granulysin is a key mediator for disseminated keratinocyte death in Stevens-Johnson syndrome and toxic epidermal necrolysis. Nat. Med. 14, 1343–1350 (2008).
doi: 10.1038/nm.1884
Clayberger, C. et al. 15 kDa granulysin causes differentiation of monocytes to dendritic cells but lacks cytotoxic activity. J. Immunol. 188, 6119–6126 (2012).
doi: 10.4049/jimmunol.1200570
Chung, W. H. et al. Medical genetics: a marker for Stevens-Johnson syndrome. Nature 428, 486 (2004).
doi: 10.1038/428486a
Pan, R. Y. et al. Identification of drug-specific public TCR driving severe cutaneous adverse reactions. Nat. Commun. 10, 3569 (2019).
doi: 10.1038/s41467-019-11396-2
Chung, W.-H. et al. Oxypurinol-specific T cells possess preferential TCR clonotypes and express granulysin in allopurinol-induced severe cutaneous adverse reactions. J. Invest. Dermatol. 135, 2237–2248 (2015).
doi: 10.1038/jid.2015.165
Lee, H. Y., Fook-Chong, S., Koh, H. Y., Thirumoorthy, T. & Pang, S. M. Cyclosporine treatment for Stevens-Johnson syndrome/toxic epidermal necrolysis: Retrospective analysis of a cohort treated in a specialized referral center. J. Am. Acad. Dermatol. 76, 106–113 (2017).
doi: 10.1016/j.jaad.2016.07.048
Zhang, J. et al. Evaluation of combination therapy with etanercept and systemic corticosteroids for Stevens-Johnson syndrome and toxic epidermal necrolysis: A multicenter observational study. J. Allergy Clin. Immunology Pract. 10, 1295–1304 (2022).
doi: 10.1016/j.jaip.2022.01.038
Mukherjee, E. M. & Phillips, E. J. Where to place etanercept and combination treatment for Stevens-Johnson syndrome and toxic epidermal necrolysis? Ann. Allergy Asthma Immunol. 129, 269–270 (2022).
doi: 10.1016/j.anai.2022.06.025
Brüggen, M. C. et al. Supportive care in the acute phase of Stevens–Johnson syndrome and toxic epidermal necrolysis: an international, multidisciplinary Delphi‐based consensus. Br. J. Dermatol. 185, 616–626 (2021).
doi: 10.1111/bjd.19893
Chen, S. et al. Macrophages in immunoregulation and therapeutics. Signal Transduct. Target. Ther. 8, 207 (2023).
doi: 10.1038/s41392-023-01452-1
Morris, D. L. et al. CD40 promotes MHC class II expression on adipose tissue macrophages and regulates adipose tissue CD4+ T cells with obesity. J. Leukoc. Biol. 99, 1107–1119 (2015).
doi: 10.1189/jlb.3A0115-009R
Chakarov, S. et al. Two distinct interstitial macrophage populations coexist across tissues in specific subtissular niches. Science 363, eaau0964 (2019).
doi: 10.1126/science.aau0964
Bailin, S. S., et al. Changes in subcutaneous white adipose tissue cellular composition and molecular programs underlie glucose intolerance in persons with HIV. Front. immunol. 14, https://doi.org/10.3389/fimmu.2023.1152003 (2023).
Büttner, M., Ostner, J., Müller, C. L., Theis, F. J. & Schubert, B. scCODA is a Bayesian model for compositional single-cell data analysis. Nat. Commun. 12, 6876 (2021).
doi: 10.1038/s41467-021-27150-6
Chen, S. H. et al. Predominance of CD14+ cells in burn blister fluids. Ann. Plast. Surg. 80, S70–s74 (2018).
doi: 10.1097/SAP.0000000000001305
Le Cleach, L. et al. Blister fluid T lymphocytes during toxic epidermal necrolysis are functional cytotoxic cells which express human natural killer (NK) inhibitory receptors. Clin. Exp. Immunol. 119, 225–230 (2000).
doi: 10.1046/j.1365-2249.2000.01119.x
Zou, Z. et al. A single-cell transcriptomic atlas of human skin aging. Dev. Cell 56, 383–397 (2021).
doi: 10.1016/j.devcel.2020.11.002
Denu, R. A. et al. Fibroblasts and mesenchymal stromal/stem cells are phenotypically indistinguishable. Acta Haematol. 136, 85–97 (2016).
doi: 10.1159/000445096
Mayassi, T., Barreiro, L. B., Rossjohn, J. & Jabri, B. A multilayered immune system through the lens of unconventional T cells. Nature 595, 501–510 (2021).
doi: 10.1038/s41586-021-03578-0
Hao, Y. et al. Integrated analysis of multimodal single-cell data. Cell 184, 3573–3587 (2021).
doi: 10.1016/j.cell.2021.04.048
Hu, Y. et al. γδ T cells: origin and fate, subsets, diseases and immunotherapy. Signal Transduct. Target. Ther. 8, 434 (2023).
doi: 10.1038/s41392-023-01653-8
Kanbar, J. N., et al. The long noncoding RNA Malat1 regulates CD8+ T cell differentiation by mediating epigenetic repression. J. Exp. Med. 219, e20211756 (2022).
Menon, M. P. & Hua, K. F. The long non-coding RNAs: Paramount regulators of the NLRP3 inflammasome. Front. Immunol. 11, 569524 (2020).
doi: 10.3389/fimmu.2020.569524
Correia, M. P. et al. Distinct human circulating NKp30(+)FcεRIγ(+)CD8(+) T cell population exhibiting high natural killer-like antitumor potential. Proc. Natl. Acad. Sci. USA 115, E5980–e5989 (2018).
doi: 10.1073/pnas.1720564115
Burel, J. G. et al. Circulating T cell-monocyte complexes are markers of immune perturbations. ELife 8, e46045 (2019).
doi: 10.7554/eLife.46045
Schluns, K. S., Kieper, W. C., Jameson, S. C. & Lefrançois, L. Interleukin-7 mediates the homeostasis of naïve and memory CD8 T cells in vivo. Nat. Immunol. 1, 426–432 (2000).
doi: 10.1038/80868
Cheuk, S. et al. CD49a Expression defines tissue-resident CD8+ T cells poised for cytotoxic function in human skin. Immunity 46, 287–300 (2017).
doi: 10.1016/j.immuni.2017.01.009
He, H. et al. Single-cell transcriptome analysis of human skin identifies novel fibroblast subpopulation and enrichment of immune subsets in atopic dermatitis. J. Allergy Clin. Immunol. 145, 1615–1628 (2020).
doi: 10.1016/j.jaci.2020.01.042
Rojahn, T. B. et al. Single-cell transcriptomics combined with interstitial fluid proteomics defines cell type–specific immune regulation in atopic dermatitis. J. Allergy Clin. Immunol. 146, 1056–1069 (2020).
doi: 10.1016/j.jaci.2020.03.041
Park, S. L. et al. Local proliferation maintains a stable pool of tissue-resident memory T cells after antiviral recall responses. Nat. Immunol. 19, 183–191 (2018).
doi: 10.1038/s41590-017-0027-5
Mackay, L. K. et al. The developmental pathway for CD103+CD8+ tissue-resident memory T cells of skin. Nat. Immunol. 14, 1294–1301 (2013).
doi: 10.1038/ni.2744
Clark, R. A. et al. The vast majority of CLA+ T cells are resident in normal skin. J. Immunol. (Baltim., Md.: 1950) 176, 4431–4439 (2006).
doi: 10.4049/jimmunol.176.7.4431
Tokura, Y., Phadungsaksawasdi, P., Kurihara, K., Fujiyama, T. & Honda, T. Pathophysiology of Skin Resident Memory T Cells. Front. Immunol. 11, 618897 (2020).
doi: 10.3389/fimmu.2020.618897
Soler, D., Humphreys, T. L., Spinola, S. M. & Campbell, J. J. CCR4 versus CCR10 in human cutaneous TH lymphocyte trafficking. Blood 101, 1677–1682 (2003).
doi: 10.1182/blood-2002-07-2348
Mackay, L. K. et al. Cutting edge: CD69 interference with sphingosine-1-phosphate receptor function regulates peripheral T cell retention. J. Immunol. 194, 2059–2063 (2015).
doi: 10.4049/jimmunol.1402256
Skon, C. N. et al. Transcriptional downregulation of S1pr1 is required for the establishment of resident memory CD8+ T cells. Nat. Immunol. 14, 1285–1293 (2013).
doi: 10.1038/ni.2745
El Hajj, Y. et al. Pregnenolone sulfate induces transcriptional and immunoregulatory effects on T cells. Sci. Rep. 14, 6782 (2024).
doi: 10.1038/s41598-024-57327-0
He, Y. et al. Mediators of capillary-to-venule conversion in the chronic inflammatory skin disease psoriasis. J. Invest. Dermatol. 142, 3313–3326 (2022).
doi: 10.1016/j.jid.2022.05.1089
Litvak, V. et al. Function of C/EBPδ in a regulatory circuit that discriminates between transient and persistent TLR4-induced signals. Nat. Immunol. 10, 437–443 (2009).
doi: 10.1038/ni.1721
Hammond, S. et al. Checkpoint inhibition reduces the threshold for drug-specific T-cell priming and increases the incidence of sulfasalazine hypersensitivity. Toxicol. Sci. 186, 58–69 (2021).
doi: 10.1093/toxsci/kfab144
Mazurek, N. et al. Cell-surface galectin-3 confers resistance to TRAIL by impeding trafficking of death receptors in metastatic colon adenocarcinoma cells. Cell Death Differ. 19, 523–533 (2012).
doi: 10.1038/cdd.2011.123
Bae, J. et al. Targeting LAG3/GAL-3 to overcome immunosuppression and enhance anti-tumor immune responses in multiple myeloma. Leukemia 36, 138–154 (2022).
doi: 10.1038/s41375-021-01301-6
Huang, H., Wang, C., Rubelt, F., Scriba, T. J. & Davis, M. M. Analyzing the Mycobacterium tuberculosis immune response by T-cell receptor clustering with GLIPH2 and genome-wide antigen screening. Nat. Biotechnol. 38, 1194–1202 (2020).
doi: 10.1038/s41587-020-0505-4
Hwang, S. S. et al. mRNA destabilization by BTG1 and BTG2 maintains T cell quiescence. Science 367, 1255–1260 (2020).
doi: 10.1126/science.aax0194
Sun, B. et al. Double-jeopardy: scRNA-seq doublet/multiplet detection using multi-omic profiling. Cell Rep. Methods 1, 100008 (2021).
doi: 10.1016/j.crmeth.2021.100008
Ji, Q., Perchellet, A. & Goverman, J. M. Viral infection triggers central nervous system autoimmunity via activation of CD8+ T cells expressing dual TCRs. Nat. Immunol. 11, 628–634 (2010).
doi: 10.1038/ni.1888
Lee, H., Jeong, S. & Shin, E.-C. Significance of bystander T cell activation in microbial infection. Nat. Immunol. 23, 13–22 (2022).
doi: 10.1038/s41590-021-00985-3
Jin, S. et al. Inference and analysis of cell-cell communication using CellChat. Nat. Commun. 12, 1088 (2021).
doi: 10.1038/s41467-021-21246-9
Morel, E. et al. CD94/NKG2C is a killer effector molecule in patients with Stevens-Johnson syndrome and toxic epidermal necrolysis. J. Allergy Clin. Immunol. 125, 703–710 (2010).
doi: 10.1016/j.jaci.2009.10.030
Grant, E. J. et al. The unconventional role of HLA-E: The road less traveled. Mol. Immunol. 120, 101–112 (2020).
doi: 10.1016/j.molimm.2020.02.011
Walters, L. C. et al. Pathogen-derived HLA-E bound epitopes reveal broad primary anchor pocket tolerability and conformationally malleable peptide binding. Nat. Commun. 9, 3137 (2018).
doi: 10.1038/s41467-018-05459-z
Tamada, M. et al. Modulation of glucose metabolism by CD44 contributes to antioxidant status and drug resistance in cancer cells. Cancer Res. 72, 1438–1448 (2012).
doi: 10.1158/0008-5472.CAN-11-3024
Schubert, M. et al. Perturbation-response genes reveal signaling footprints in cancer gene expression. Nat. Commun. 9, 20 (2018).
doi: 10.1038/s41467-017-02391-6
Salehi, R. et al. Granulosa cell-derived miR-379-5p regulates macrophage polarization in polycystic ovarian syndrome. Front. Immunol. 14, 1104550 (2023).
doi: 10.3389/fimmu.2023.1104550
Timms, K., Guo, H., Arkwright, P. & Pennock, J. Keratinocyte EGF signalling dominates in atopic dermatitis lesions: A comparative RNAseq analysis. Exp. Dermatol. 31, 1373–1384 (2022).
doi: 10.1111/exd.14605
Wu, F. et al. Signaling pathways in cancer-associated fibroblasts and targeted therapy for cancer. Signal Transduct. Target. Ther. 6, 218 (2021).
doi: 10.1038/s41392-021-00641-0
Villani, A. P. et al. Massive clonal expansion of polycytotoxic skin and blood CD8(+) T cells in patients with toxic epidermal necrolysis. Sci. Adv. 7, https://doi.org/10.1126/sciadv.abe0013 (2021).
Martos, S. N. et al. Single-cell analyses identify dysfunctional CD16(+) CD8 T cells in smokers. Cell Rep. Med. 1, 100054 (2020).
Milner, J. J. et al. Delineation of a molecularly distinct terminally differentiated memory CD8 T cell population. Proc. Natl. Acad. Sci. USA 117, 25667–25678 (2020).
doi: 10.1073/pnas.2008571117
Rapaport, A. S. et al. The inhibitory receptor NKG2A sustains virus-specific CD8
doi: 10.1016/j.immuni.2015.11.005
Joachims, M. L. et al. Dysregulated long non-coding RNA in Sjögren’s disease impacts both interferon and adaptive immune responses. RMD Open 8, e002672 (2022).
doi: 10.1136/rmdopen-2022-002672
Kersh, G. J. & Allen, P. M. Structural basis for T cell recognition of altered peptide ligands: a single T cell receptor can productively recognize a large continuum of related ligands. J. Exp. Med. 184, 1259–1268 (1996).
doi: 10.1084/jem.184.4.1259
Evavold, B. D., Sloan-Lancaster, J. & Allen, P. M. Tickling the TCR: selective T-cell functions stimulated by altered peptide ligands. Immunol. Today 14, 602–609 (1993).
doi: 10.1016/0167-5699(93)90200-5
Corrêa, M. P. et al. Expression pattern and immunoregulatory roles of galectin-1 and galectin-3 in atopic dermatitis and psoriasis. Inflammation 45, 1133–1145 (2022).
doi: 10.1007/s10753-021-01608-7
Ellis, J. et al. Depletion of LAG-3(+) T cells translated to pharmacology and improvement in psoriasis disease activity: A phase I randomized study of mAb GSK2831781. Clin. Pharmacol. Ther. 109, 1293–1303 (2021).
doi: 10.1002/cpt.2091
Poirier, N. et al. Antibody-mediated depletion of lymphocyte-activation gene-3 (LAG-3+)-activated T lymphocytes prevents delayed-type hypersensitivity in non-human primates. Clin. Exp. Immunol. 164, 265–274 (2011).
doi: 10.1111/j.1365-2249.2011.04329.x
Bloom, B. R. & Bennett, B. Mechanism of a reaction in vitro associated with delayed-type hypersensitivity. Science 153, 80–82 (1966).
doi: 10.1126/science.153.3731.80
Chen, J. et al. MIF inhibition alleviates vitiligo progression by suppressing CD8(+) T cell activation and proliferation. J. Pathol. 260, 84–96 (2023).
doi: 10.1002/path.6073
Mitchell, R. A., Metz, C. N., Peng, T. & Bucala, R. Sustained mitogen-activated protein kinase (MAPK) and cytoplasmic phospholipase A2 activation by macrophage migration inhibitory factor (MIF): REGULATORY ROLE IN CELL PROLIFERATION AND GLUCOCORTICOID ACTION*. J. Biol. Chem. 274, 18100–18106 (1999).
doi: 10.1074/jbc.274.25.18100
Huynh, J., Chand, A., Gough, D. & Ernst, M. Therapeutically exploiting STAT3 activity in cancer — using tissue repair as a road map. Nat. Rev. Cancer 19, 82–96 (2019).
doi: 10.1038/s41568-018-0090-8
Kok, T. et al. Small-molecule inhibitors of macrophage migration inhibitory factor (MIF) as an emerging class of therapeutics for immune disorders. Drug Discov. Today 23, 1910–1918 (2018).
doi: 10.1016/j.drudis.2018.06.017
Rask-Andersen, M., Zhang, J., Fabbro, D. & Schiöth, H. B. Advances in kinase targeting: current clinical use and clinical trials. Trends Pharmacol. Sci. 35, 604–620 (2014).
doi: 10.1016/j.tips.2014.09.007
Mifsud, N. A. et al. The allopurinol metabolite, oxypurinol, drives oligoclonal expansions of drug-reactive T cells in resolved hypersensitivity cases and drug-naïve healthy donors. Allergy 78, 2980–2993 (2023).
Ostrov, D. A. et al. Drug hypersensitivity caused by alteration of the MHC-presented self-peptide repertoire. Proc. Natl. Acad. Sci. USA 109, 9959–9964 (2012).
doi: 10.1073/pnas.1207934109
Wohnhaas, C. T. et al. DMSO cryopreservation is the method of choice to preserve cells for droplet-based single-cell RNA sequencing. Sci. Rep. 9, 10699 (2019).
doi: 10.1038/s41598-019-46932-z
Guillaumet-Adkins, A. et al. Single-cell transcriptome conservation in cryopreserved cells and tissues. Genome Biol. 18, 45 (2017).
doi: 10.1186/s13059-017-1171-9
Salimi, M. et al. Enhanced isolation of lymphoid cells from human skin. Clin. Exp. Dermatol. 41, 552–556 (2016).
doi: 10.1111/ced.12802
Waise, S. et al. An optimised tissue disaggregation and data processing pipeline for characterising fibroblast phenotypes using single-cell RNA sequencing. Sci. Rep. 9, 9580 (2019).
doi: 10.1038/s41598-019-45842-4
Heaton, H. et al. Souporcell: robust clustering of single-cell RNA-seq data by genotype without reference genotypes. Nat. Methods 17, 615–620 (2020).
doi: 10.1038/s41592-020-0820-1
Osorio, D. & Cai, J. J. Systematic determination of the mitochondrial proportion in human and mice tissues for single-cell RNA-sequencing data quality control. Bioinformatics 37, 963–967 (2020).
doi: 10.1093/bioinformatics/btaa751
Korsunsky, I. et al. Fast, sensitive and accurate integration of single-cell data with Harmony. Nat. Methods 16, 1289–1296 (2019).
doi: 10.1038/s41592-019-0619-0
Xi, N. M. & Li, J. J. Benchmarking computational doublet-detection methods for single-cell RNA sequencing data. Cell Syst. 12, 176–194 (2021).
doi: 10.1016/j.cels.2020.11.008
McGinnis, C. S., Murrow, L. M. & Gartner, Z. J. Doubletfinder: Doublet detection in single-cell RNA sequencing data using artificial nearest neighbors. Cell Syst. 8, 329–337 (2019).
doi: 10.1016/j.cels.2019.03.003
Germain, P. L., Lun, A., Garcia Meixide, C., Macnair, W. & Robinson, M. D. Doublet identification in single-cell sequencing data using scDblFinder. F1000Res. https://doi.org/10.12688/f1000research.73600.2 (2021).
Bais, A. S. & Kostka, D. scds: computational annotation of doublets in single-cell RNA sequencing data. Bioinformatics 36, 1150–1158 (2019).
doi: 10.1093/bioinformatics/btz698
Hertzman, R. J. et al. Visual genomics analysis studio as a tool to analyze multiomic data. Front. Genet. 12, 642012 (2021).
doi: 10.3389/fgene.2021.642012
Xie, Z. et al. Gene set knowledge discovery with Enrichr. Curr. Protoc. 1, e90 (2021).
doi: 10.1002/cpz1.90
Dimitrov, D. et al. Comparison of methods and resources for cell-cell communication inference from single-cell RNA-Seq data. Nat. Commun. 13, 3224 (2022).
doi: 10.1038/s41467-022-30755-0

Auteurs

Andrew Gibson (A)

Institute for Immunology and Infectious Diseases, Murdoch University, Perth, Australia.

Ramesh Ram (R)

Institute for Immunology and Infectious Diseases, Murdoch University, Perth, Australia.

Rama Gangula (R)

Department of Medicine, Vanderbilt University Medical Centre, Nashville, USA.

Yueran Li (Y)

Institute for Immunology and Infectious Diseases, Murdoch University, Perth, Australia.

Eric Mukherjee (E)

Department of Medicine, Vanderbilt University Medical Centre, Nashville, USA.

Amy M Palubinsky (AM)

Department of Medicine, Vanderbilt University Medical Centre, Nashville, USA.

Chelsea N Campbell (CN)

Department of Medicine, Vanderbilt University Medical Centre, Nashville, USA.

Michael Thorne (M)

Institute for Immunology and Infectious Diseases, Murdoch University, Perth, Australia.

Katherine C Konvinse (KC)

Department of Medicine, Vanderbilt University Medical Centre, Nashville, USA.

Phuti Choshi (P)

Department of Medicine, Groote Schuur Hospital, Cape Town, South Africa.

Pooja Deshpande (P)

Institute for Immunology and Infectious Diseases, Murdoch University, Perth, Australia.

Sarah Pedretti (S)

Allergy and Immunology Unit, University of Cape Town Lung Institute, Cape Town, South Africa.

Mark W Fear (MW)

School of Biomedical Sciences, University of Western Australia, Perth, Australia.

Fiona M Wood (FM)

School of Biomedical Sciences, University of Western Australia, Perth, Australia.
Burn Service of Western Australia, Fiona Stanley Hospital, Perth, Australia.

Richard T O'Neil (RT)

Ralph H Johnson VA Medical Center, Medical University of South Carolina, Charleston, USA.

Celestine N Wanjalla (CN)

Department of Medicine, Vanderbilt University Medical Centre, Nashville, USA.

Spyros A Kalams (SA)

Department of Medicine, Vanderbilt University Medical Centre, Nashville, USA.

Silvana Gaudieri (S)

Institute for Immunology and Infectious Diseases, Murdoch University, Perth, Australia.
Department of Medicine, Vanderbilt University Medical Centre, Nashville, USA.
School of Human Sciences, The University of Western Australia, Perth, Australia.

Rannakoe J Lehloenya (RJ)

Department of Medicine, University of Cape Town, Cape Town, South Africa.

Samuel S Bailin (SS)

Department of Medicine, Vanderbilt University Medical Centre, Nashville, USA.

Abha Chopra (A)

Institute for Immunology and Infectious Diseases, Murdoch University, Perth, Australia.
Department of Medicine, Vanderbilt University Medical Centre, Nashville, USA.

Jason A Trubiano (JA)

The Peter Doherty Institute for Infection and Immunity, University of Melbourne, Melbourne, Australia.
Centre for Antibiotic Allergy and Research, Austin Health, Melbourne, Australia.

Jonny G Peter (JG)

Department of Medicine, Groote Schuur Hospital, Cape Town, South Africa.
Allergy and Immunology Unit, University of Cape Town Lung Institute, Cape Town, South Africa.

Simon A Mallal (SA)

Institute for Immunology and Infectious Diseases, Murdoch University, Perth, Australia.
Department of Medicine, Vanderbilt University Medical Centre, Nashville, USA.

Elizabeth J Phillips (EJ)

Institute for Immunology and Infectious Diseases, Murdoch University, Perth, Australia. elizabeth.j.phillips@vumc.org.
Department of Medicine, Vanderbilt University Medical Centre, Nashville, USA. elizabeth.j.phillips@vumc.org.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH