Radiogenomic analysis of glioblastoma using protein-based amide proton transfer (APT) imaging and message RNA expression: A novel correlation in molecular imaging and gene characteristics
Shanshan Jiang1, Xianlong Wang1, Hao Yu1, Jiandong Xi1, Jingwen Wu1, Lisong Liang1, Shilong Lu1, Tianyu Zou1, Jinyuan Zhou2, and Zhibo Wen1

1Department of Radiology, Southern Medical University Zhujiang Hospital, Guangzhou, China, People's Republic of, 2Department of Radiology, Johns Hopkins University, Baltimore, MD, United States

Synopsis

The correlation between endogenous protein-based APT-weighted (APTw) imaging and gene expression in glioblastoma (GBM) was investigated. 16 patients with newly diagnosed GBM were studied. APTw/FLAIR hyperintensity area ratio (AFR), and APTw hyperintensity/gadolinium contrast-enhanced T1w enhancement area ratio (ATR) were calculated. Interoperative paired tumor and adjacent normal tissues were sampled for genomic analysis. BRCA1 and CDK4 were significantly downregulated in the high AFR group (adjusted P= 0.000953 and 0.025187), and SLAMF9 and MIA were significantly downregulated in the high ATR group (adjusted P= 1.08E-11 and 0.00997). APT imaging has great potential for unveiling some special genomic changes in GBM.

Target audience

Researchers and clinicians who are interested in novel diagnostic image methods and radiogenomics in gliomas.

Purpose

Glioblastoma (GBM) is the most dismal primary brain tumor that relentlessly defies therapy. New biological understanding helped to perfect treatment strategies, especially for targeted, molecular based therapies that are individualized on particular biological or genomic modifications in each unique patient. Amide proton transfer (APT) imaging is a novel MRI technique in which amide protons of endogenous mobile proteins in tissue (such as those in the cytoplasm) are detected [1]. The APT-weighted (APTw) signal is well correlated with the Ki-67 index and cell density, and may be a valuable imaging biomarker to identify the spatial extent and pathological grade of malignant gliomas [2,3]. The correlation between proteome and genome is fundamental duo to the central dogma of molecular biology. The research was designed to explore the differentially expressed genes (DEGs) related to the protein-based APT imaging phenotype of GBM.

Materials and Methods

MRI scanning:

16 patients with GBM were recruited and scanned on a Philips 3T MRI scanner. The sequences performed for each patient included T1w, T2w, FLAIR, APT imaging, and gadolinium contrast-enhanced T1w. A multi-offset, multi-acquisition imaging acquisition scheme was used for APT imaging (saturation power = 2 μT; saturation time = 800 msec; matrix = 128×128; field of view = 240×240 mm2; and slice thickness = 6 mm; scan time = 3 min) [2]. APTw images were calculated using a magnetization transfer ratio (MTR) asymmetry at ±3.5ppm.

APTw phenotype:

Two experienced neuro-oncologic radiologists assessed APTw imaging or conversional MR imaging morphologic features. APTw signal intensities and hyperintense area, FLAIR hyperintense area, and gadolinium contrast-enhanced T1w enhancement area were recorded. APTw/FLAIR hyperintense area ratio (AFR), as well as APTw hyperintense/gadolinium contrast-enhanced T1w enhancement area ratio (ATR) were calculated. The AFR cutoff value was 0.8, and all patients were divided into two groups: high AFR and low AFR. The ATR cutoff value was 0.9, and all patients were divided into two groups: high ATR and low ATR.

RNA extraction, library construction and sequencing:

Paired tumor and adjacent normal tissues were obtained intraoperatively. Global gene expression and genomic DNA measurements (RNA-seq) from the matched specimens with use of research identifiers were performed in these patients, as previously described [4]. [A1] A threshold of the FDR ≤ 0.05 and an absolute value of log2 Ratio ≥ 1 were used to identify differentially expressed genes (DEGs). GO and KEGG enrichment analyses were performed for DEGs as described by Zhang [5]. Workflow is showed in Fig. 1.

Results and Discussion

Radiogenomics analysis:

By analyzing the radiogenomic correlation between APTw image features and message RNA expression, BRCA1 and CDK4 genes were found to be significantly downregulated in the high AFR tumor tissue compared to the low AFR group. SLAMF9 and MIA genes were found to be significantly downregulated in the high ATR tumor tissues compared to the low ATR group (see Figs. 2 and 3).

Gene function interpretation:

BRCA1: BRCA1 (Breast Cancer 1, Early Onset) encodes a nuclear phosphoprotein that plays a role in maintaining genomic stability, and it also acts as a tumor suppressor. The BRCA1 protein is involved in repairing damaged DNA. BRCA1 protein expression may be an important predictive biomarker of overall survival in GBM [6].

CDK4: CDK4 (Cyclin-Dependent Kinase 4) is a Protein Coding gene. Among its related pathways are PI3K-Akt signaling pathway and Glioma. GO annotations related to this gene include protein complex binding and cyclin binding.

SLAMF9: SLAMF9 (SLAM Family Member 9) is a Protein Coding gene. GO annotations related to this gene include receptor activity. This gene may play a role in the immune response.

MIA: MIA (Melanoma Inhibitory Activity) is a Protein Coding gene. Among its related pathways is Neural Crest Differentiation. GO annotations related to this gene include growth factor activity [7].

Conclusion

Our initial findings demonstrated a novel correlation in molecular imaging and gene characteristics of gliomas, and revealed the potential genetic and biologic significance of the non-invasive protein-based APTw imaging features, which may facilitate the GBM precision medicine that depends on genomics.

Acknowledgements

No acknowledgement found.

References

[1] Zhou et al. Nature Med. 9, 1085 (2003).

[2] Wen et al. NeuroImage 51, 616 (2010).

[3] Togao et al. Neuro-Oncology 16, 441 (2014).

[4] Bredel et al. Cancer Res. 65, 8679 (2005).

[5] Zhang et al. BMC genomics. 14, 279 (2013).

[6] www.nrgoncology.org.

[7] www.genecards.org.

Figures

Fig. 1. The workflow of the radiogenomics study in patients with GBM. After each patient was scanned, MRI features were evaluated by two neuroradiologists. Tumor tissue was proceeded to RNA-seq analysis. DEGs were determined by t-Test.

Fig. 2. A typical patient with GBM with AFR=0.831 and ATR = 1.0257. The expression of BRCA1 and SLAMF9 were 1.00E-05, the expression of CDK4 was 7.37E-08, and the expression of MIA was 0.00056.

Fig.3. The difference of BRCA1 expression between high AFR and low AFR was significant (adjusted P = 0.000953), and the difference of CDK4 expression between high AFR and low AFR was significant (adjusted P = 0.025187). The difference of SLAMF9 expression between high ATR and low ATR was significant (adjusted P = 1.08E-11), and the difference of MIA expression between high ATR and low ATR was significant (adjusted P = 0.00997).



Proc. Intl. Soc. Mag. Reson. Med. 24 (2016)
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