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Alpha-enolase is a potential prognostic marker in clear cell renal cell carcinoma

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Abstract

Clear cell renal cell carcinoma (ccRCC) is an aggressive disease with unpredictable behaviour. Clinical parameters are not always accurate for prognosis prediction. The integration of molecular markers to prognostic models can significantly improve prognostic assessment and consequently patient management. We assessed the expression of alpha-enolase (ENO1) protein by immunohistochemistry in 360 patients with primary ccRCC and correlated its expression with multiple clinicopathological parameters including stage, grade, tumor size, disease-free and overall survival. Cox proportional hazard regression models adjusted for clinicopathological factors were used to test for a link between ENO1 expression and both disease-free and overall survival. We correlated ENO1 mRNA expression with overall survival in an independent set of 428 ccRCC cases from The Cancer Genome Atlas. ENO1 showed cytoplasmic, membranous and nuclear staining patterns. There is a statistically significant negative correlation between ENO1 expression, tumor stage, and grade. ENO1 expression also shows a statistically significant direct correlation with disease-free survival (p = 0.011) and overall survival (p = 0.030) in ccRCC. Patients with higher ENO1 expression had lower hazard ratio of recurrence, although this was not statistically significant (HR = 0.330, p = 0.060). These findings were validated at the mRNA level in an independent set of 428 ccRCC cases which also showed that low ENO1 expression is associated with significantly shorter overall survival. Down-regulation of ENO1 can be a predictor of poor prognosis in ccRCC, and it can be a potential prognostic marker.

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Abbreviations

ENO1:

Alpha-enolase

ccRCC:

Clear cell renal cell carcinoma

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Acknowledgments

GMY is supported by grants from the Canadian Institute of Health Research (MOP 119606), Kidney Foundation of Canada (KFOC130030), Kidney Cancer Research Network of Canada, and Prostate Cancer Canada Movember Discovery Grants (D2013-39).

Conflict of interest

The author’s declare that they have no competing interests.

Author information

Authors and Affiliations

  1. Department of Laboratory Medicine, and the Keenan Research Centre for Biomedical Science at the Li Ka Shing Knowledge Institute, St. Michael’s Hospital, Toronto, Canada

    Nicole M. White-Al Habeeb, Ashley Di Meo, Fabio Rotondo, Annetta Seivwright, Andrew H. A. Girgis & George M. Yousef

  2. Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, M5S 1A8, Canada

    Nicole M. White-Al Habeeb, Ashley Di Meo & George M. Yousef

  3. Department of Biochemistry and Molecular Biology, Faculty of Biology, University of Athens, 15701, Athens, Greece

    Andreas Scorilas

  4. Department of Chemistry and Centre for Research in Mass Spectrometry, York University, 4700 Keele Street, Toronto, M3J 1P3, Canada

    Olena Masui

  5. Department of Pathology, London Health Sciences Center and Western University, London, N6A 5W9, Canada

    Manal Gabril

  6. Division of Urologic Oncology, Department of Surgery, Princess Margaret Hospital, University Health Network, University of Toronto, Toronto, ON, M5G 2M9, Canada

    Michael A. Jewett

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  1. Nicole M. White-Al Habeeb
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Electronic supplementary material

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10585_2015_9725_MOESM1_ESM.docx

Supplementary material 1 Correlation between cytoplasmic and nuclear intensity and frequency in cancerous kidney tissues. Both cytoplasmic and nuclear staining patterns showed significant positive correlation in cancerous kidney tissues. rs = spearman correlation coefficient (DOCX 50 kb)

10585_2015_9725_MOESM2_ESM.docx

Supplementary material 2 Correlation between cytoplasmic and membrane intensity and frequency in cancerous kidney tissues. Both cytoplasmic and membranous staining patterns showed significant positive correlation in cancerous kidney tissues. rs = spearman correlation coefficient (DOCX 44 kb)

10585_2015_9725_MOESM3_ESM.docx

Supplementary material 3 Correlation between cytoplasmic and nuclear intensity and frequency in kidney papillomas. Both cytoplasmic and nuclear staining patterns showed significant positive correlation in kidney papillomas. rs = spearman correlation coefficient (DOCX 41 kb)

10585_2015_9725_MOESM4_ESM.docx

Supplementary material 4 Correlation between cytoplasmic and membrane intensity and frequency in kidney papillomas. Both cytoplasmic and membranous staining patterns showed significant positive correlation in kidney papillomas. rs = spearman correlation coefficient (DOCX 41 kb)

10585_2015_9725_MOESM5_ESM.docx

Supplementary material 5 Kaplan–Meier survival curve for (a) DFS time and (b) OS time of patients with high and low cytoplasmic expression of alpha-enolase protein. a When using alpha-enolase as a dichotomous variable, patients with low alpha-enolase expression have a statistically significant decrease in disease free survival (p = 0.046) compared to those with high expression. b Patients with low alpha-enolase expression have a statistically significant decrease in overall survival (p = 0.048) compared to patients with high expression(DOCX 132 kb)

10585_2015_9725_MOESM6_ESM.tif

Supplementary material 6 Homozygous and heterozygous copy number loss at the ENO1 locus (ch1p36) was observed in 69 of 436 cases of ccRCC, indicating that chromosomal alterations are responsible, at least in part, of ENO1 dysregulation in kidney cancer. Blue indicates a copy number loss (TIFF 196 kb)

10585_2015_9725_MOESM7_ESM.docx

Supplementary material 7 miR-22 transfection. 786-O cells were successfully transfected with miR-22 mimic as there was a significant increase in the relative expression of miR-22 compared with untransfected and control cells. Untransfected cells display low endogenous expression of miR-22. Similar results were obtained for ACHN RCC cells (data not shown). Data are expressed as mean ± SEM. *p < 0.05 versus control. NC negative control, siPORT transfection agent (DOCX 76 kb)

10585_2015_9725_MOESM8_ESM.docx

Supplementary material 8 Endogenous miR-22 and ENO1 expression in two kidney cancer cell lines (786-O and ACHN) and a pool of normal kidney tissues (n = 5). Expression levels of miR-22 and ENO1 are inversely correlated. Data are expressed as mean ± SEM (DOCX 79 kb)

Supplementary material 9 (DOCX 13 kb)

Supplementary material 10 (DOCX 12 kb)

Supplementary material 11 (DOCX 12 kb)

Supplementary material 12 (DOCX 12 kb)

10585_2015_9725_MOESM13_ESM.xlsx

Supplementary material 13 Target prediction analysis showing a list of miRNAs that are predicted to target alpha-enolase. A value of 1 indicates that the miRNA was predicted to target alpha-enolase using the corresponding search algorithm. A value of 0 indicates that the miRNA was not predicted to target alpha-enolase using the corresponding search algorithm (XLSX 16 kb)

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White-Al Habeeb, N.M., Di Meo, A., Scorilas, A. et al. Alpha-enolase is a potential prognostic marker in clear cell renal cell carcinoma. Clin Exp Metastasis 32, 531–541 (2015). https://doi.org/10.1007/s10585-015-9725-2

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