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Figure 1.

Computational pipeline used to derive a set of 51 markers that identify GEP-NEN disease.

Step 1: Gene co-expression networks inferred from GEP-NEN-A and GEP-NEN-B datasets are intersected, producing the GEP-NEN network. Step 2: Co-expression networks from neoplastic and normal tissue microarray datasets are combined to produce the normal and neoplastic networks. Step 3: Links present in normal and neoplastic networks are subtracted from the GEP-NEN network. Step 4: Concordantly regulated genes in GEP-NEN-A and GEP-NEN-B networks are retained; other genes are eliminated from the GEP-NEN network, producing the Consensus GEP-NEN network. Step 5: Upregulated genes in both the GEP-NEN-A and GEP-NEN-B dataset are mapped to the Consensus GEP-NEN network. Step 6: Topological filtering, expression profiling, and literature-curation of putative tissue-based markers, yielding 21 putative genes further examined by RT-PCR. Step 7: Identification of mutually up-regulated genes in GEP-NEN blood transcriptome and GEP-NEN-A and GEP-NEN-B datasets, yielding 32 putative genes further examined by RT-PCR. Step 8: Literature-curation and cancer mutation database search, yielding a panel of 22 putative marker genes for further RT-PCR analysis.

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Table 1.

Characteristics of patient and controls (training and independent sets).

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Table 2.

Clinical characteristics of patients (test and independent sets).

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Figure 2.

GEP-NEN gene co-expression network.

A) Visualization of the GEP-NEN gene co-expression network (2545 genes, 30249 edges). Each node represents a gene, while a link represents a GEP-NEN-specific co-expression. Nodes that localized to the same network community are marked in the same color. The community structure of the GEP-NEN network is further visualized in the 3 dimensional inset, whereby each node represents a community while edges are drawn between communities that contain co-expressed genes. Larger nodes indicate bigger gene communities. B) Heatmap visualizing enrichment for over-represented Gene Ontology (GO) Biological Process (BP) terms assigned to the 10 largest clusters (>20 genes). Heatmap colors represent the significance of the enrichment.

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Table 3.

List of 51 marker genes.

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Figure 3.

Utility of the 51 marker gene signature for identification of GEP-NEN disease.

A) Unsupervised hierarchical clustering of the 130 samples in the training set (n = 67 controls, n = 63 GEP-NENs). Tree was generated with an average agglomeration method and 1-(sample correlation) was used as a measure of dissimilarity. Unique colors under the dendrogram represent sample cluster assignments, computed by cutting the hierarchical tree at height = 0.99 (black line), 0.85 (blue line), or 0.50 (red line) using a dynamic tree cutting approach [77]. B) Prediction accuracy of each classifier using sequential addition of 27 significantly up-regulated genes (p<0.05) in the GEP-NEN samples obtained using results of the 10-fold cross validation. C) Receiver operating characteristic (ROC) curves for “majority vote” classifier applied to validation sets 1 (AUC = 0.98, p<0.0001) and 2 (AUC = 0.95, p<0.0001) compared to ROC curve for utility of the plasma CgA values (AUC = 0.64, p<0.002). Direct comparisons of AUCs between set 1 or set 2 and CgA identified estimated Z-scores of 10.57 and 11.42 respectively, confirming the significant differences between the two detection systems (calculations detailed in Supplementary Methods).

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Figure 4.

Comparison of the 51 marker gene signature with Chromogranin A (CgA) for detecting GEP-NENs.

A) CgA levels were significantly elevated in the GEP-NEN group (n = 176; *p<0.002) but an overlap with normal values was identified. B) Comparison of the PCR-based approach with CgA protein measurement identified that call rates were significantly higher for the PCR-based test (*p<0.0005, χ2 = 12.3). The PCR blood test was significantly more accurate than measurement of CgA levels to detect GEP-NENs. ULN = upper limit of normal (19U/L – DAKO).

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Figure 5.

Utility of the 51 marker gene signature for detecting P-NENs, metastases and in patients with low Chromogranin A (CgA).

A) The sensitivity and specificity of the test to detect GI-NENs (90%, 94%) and P-NENs (80%, 94%) was similar. B) The PCR-based approach could detect patients with no metastases as well as patients with metastases. C) The PCR-based test could accurately identify GEP-NENs even when plasma CgA were low (<19U/L). Overall, the PCR blood test was significantly more accurate than measurement of CgA levels to detect GEP-NENs (*p<10−13, χ2>50).

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