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In vivo effects of dexamethasone on blood gene expression in ataxia telangiectasia

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Abstract

Ataxia telangiectasia (AT) is a rare incurable genetic disease caused by biallelic mutations in the Ataxia telangiectasia-mutated gene. Intra-erythrocyte infusion of dexamethasone improves clinical outcomes in AT patients; however, the molecular mechanisms that lead to this improvement remain unknown. Hence, to gain a better understanding of these mechanisms, we assessed the effects of glucocorticoid administration on gene expression in the blood of AT patients. Whole blood was obtained from nine children enrolled in a phase two clinical trial, who were being treated with dexamethasone (AT Dexa), from six untreated AT patients (AT) and from six healthy volunteers (WT). CodeLink Whole Genome Bioarrays were used to assess transcript expression. The reliability of the differentially expressed genes (DEGs) was verified by qRT-PCR analysis. The enriched Gene Ontology (GO) terms and the pathways of the Kyoto Encyclopedia of Genes and Genomes (KEGG) of DEGs obtained by group comparisons were achieved using the Database for Annotation, Visualization and Integrated Discovery (DAVID). Functional network analyses were computed by Reactome FI. The likely involved transcription factors were revealed by iRegulon. Among the identified DEGs influenced by the pathology and restored by dexamethasone, we detected 522 upregulated probes coding for known proteins, while 22 probes were downregulated, as they were in healthy subjects. These results provide useful information and represent a first step towards gaining a better understanding of the underlying mechanisms of the effects of dexamethasone on AT patients.

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Acknowledgements

We would like to thank the patients and their families who participated in the study. We are also very grateful to the clinicians and nurses, fully listed in the original paper describing the study results (Refs. [15] and [51]), who allowed the collection of the blood samples for the study. The study was partially financed by FanoAteneo and Sparks, the A-T Society and Action for A-T (Grant Ref. 14SAP01). EryDel S.p.A. financed the study, but was not involved in its design, execution or management, nor was it involved in the analysis or interpretation of data, or the preparation, review, or approval of the manuscript.

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Authors and Affiliations

  1. Department of Biomolecular Sciences, University of Urbino “Carlo Bo”, Via Saffi 2, 61029, Urbino, PU, Italy

    Michele Menotta, Sara Biagiotti, Sara Orazi, Luigia Rossi & Mauro Magnani

  2. Department of Clinical and Molecular Medicine, Sapienza Università di Roma, Rome, Italy

    Luciana Chessa

  3. Department of Pediatrics and Child Neurology and Psychiatry, Sapienza Università di Roma, Rome, Italy

    Vincenzo Leuzzi & Daniela D’Agnano

  4. Department of Clinical and Experimental Sciences, Pediatrics Clinic and Institute of Molecular Medicine “A. Nocivelli”, Spedali Civili and University of Brescia, Brescia, Italy

    Alessandro Plebani & Annarosa Soresina

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  1. Michele Menotta
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  2. Sara Biagiotti
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  3. Sara Orazi
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Correspondence to Michele Menotta.

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Conflict of interest

MMa and LR hold stock ownership in EryDel S.p.A. None of the authors have competing interests.

Ethics approval

The study was approved by the Ethics Committee of the participating healthcare facility (Comitato Etico Azienda Policlinico Umberto I, Pres. Prof. Aldo Isidori ref. #636/11), and all patients provided informed consent (along with the consent of their parents or legal guardian, as required).

Electronic supplementary material

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Supplementary Fig. 1

Full image of HLC outcome reported in Fig. 5 (TIFF 21476 kb)

Supplementary Fig. 2

Full image of HLC outcome reported in Fig. 6 (TIFF 3994 kb)

Supplementary data 1

Gene expression comparison among WT, AT and AT Dexa. The file contains the gene lists with matching fold change values obtained by statistical analysis of the three compared groups (WT vs AT, AT Dexa vs AT, WT vs AT Dexa). Fold change in linear scale (XLSX 214 kb)

Supplementary data 2

DAVID output. The file contains three Excel sheets with the DAVID functional pathway enrichment (FPE) numerical data set which were networked and visualised by Enrichment Map plugin for Cytoscape. (XLSX 91 kb)

Supplementary data 3

Reactome FI output. The file contains six Excel sheets showing the molecular functions (MF) and the biological processes (BP) of the Reactome FI assigned modules of the gene lists obtained by the three compared groups (WT vs AT, AT Dexa vs AT, WT vs AT Dexa). The probability p values and the FDR values are also shown (XLSX 48 kb)

Supplementary data 4

Reactome FI output of AT Dexa exclusive gene list. The file contains two Excel sheets showing the molecular functions (MF) and the biological processes (BP) of the Reactome FI assigned modules of the gene list exclusive to the AT Dexa group. The probability p values and the FDR values are also shown (XLSX 18 kb)

Supplementary data 5

Re-established gene expression in AT after Dexa treatment. The file contains the list of the transcripts differentially regulated in healthy people from AT patients. Some of them were re-established after Dexa treatment. Log2 Fold change scale. (XLSX 56 kb)

Supplementary data 6

AT, WT, AT NR and AT R hierarchical tree. The file contains the probes, gene symbol list and arranged expression levels from the outcome of the clusterization and hierarchical tree (HLC) among AT, WT, AT Dexa “Non Responder” (AT NR) and AT Dexa “Responder” (AT R). (XLSX 128 kb)

Supplementary data 7

AT R Vs AT NR comparison and hierarchical tree. The file contains the probes, gene symbol list and arranged expression levels after performing a direct evaluation of AT NR and AT R data also used in the clusterization and hierarchical tree (HLC) building (XLSX 39 kb)

Supplementary data 8

iRegulon outcome. The file contains six Excel sheets of the iRegulon outcome data for each compared group using the gene lists of the upregulated or downregulated transcripts as input (XLSX 226 kb)

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Menotta, M., Biagiotti, S., Orazi, S. et al. In vivo effects of dexamethasone on blood gene expression in ataxia telangiectasia. Mol Cell Biochem 438, 153–166 (2018). https://doi.org/10.1007/s11010-017-3122-x

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