Volume 26, Issue 4 (7-2022)                   IBJ 2022, 26(4): 301-312 | Back to browse issues page


XML Print


Download citation:
BibTeX | RIS | EndNote | Medlars | ProCite | Reference Manager | RefWorks
Send citation to:

Hosein Yazdi A, Zarrinpour V, Moslemi E, Forghanifard M M. A Signature of Three microRNAs Is a Potential Diagnostic Biomarker for Glioblastoma. IBJ 2022; 26 (4) :301-312
URL: http://ibj.pasteur.ac.ir/article-1-3671-en.html
Abstract:  
Background: Glioblastoma is the most common primary malignant neoplasm of the central nervous system. Despite progress in diagnosis and treatment, glioblastoma still has a poor prognosis. This study aimed to examine whether a signature of three candidate miRNAs (i.e. hsa-let-7c-5p, hsa-miR-206-5p, and hsa-miR-1909-5p) can be used as a diagnostic biomarker for distinguishing glioblastoma from healthy brain tissues.
Methods: In this study, 50 formalin‐fixed paraffin‐embedded (FFPE) glioblastoma tissue samples and 50 healthy tissue samples adjacent to tumor were included. The expression of each candidate miRNA (i.e. hsa-let-7c-5p, hsa-miR-206-5p, and hsa-miR-1909-5p) was measured using quantitative reverse transcription PCR. To show the roles of each miRNA and their biological effects on glioblastoma development and clinicopathological characteristics, in silico tools were used. ROC curves were performed to assess the diagnostic accuracy of each miRNA.
Results: Based on the results, hsa-let-7c-5p and hsa-miR-206-5p were downregulated, while hsa-miR-1909-5p was upregulated in glioblastoma tumors compared to healthy samples. No association was detected between the expression of each candidate miRNA and sex. Except for hsa-let-7c-5p, other miRNAs did not correlate with age status. ROC curve analysis indicated that the signature of candidate miRNAs is a potential biomarker distinguishing between glioblastoma and healthy samples. Only hsa-miR-206-5p suggested the association with poor prognosis in glioblastoma patients.
Conclusion: Our findings revealed that the signature of three miRNAs is capable of distinguishing glioblastoma tumor and healthy tissues. These results are beneficial for the clinical management of glioblastoma patients.
Type of Study: Full Length | Subject: Cancer Biology

References
1. Brodbelt A, Greenberg D, Winters T, Williams M, Vernon S, Collins VP. Glioblastoma in England: 2007-2011. European journal of cancer r 2015; 51(4): 533-542. [DOI:10.1016/j.ejca.2014.12.014]
2. Song KS, Phi JH, Cho BK, Wang KC, Lee JY, Kim DG, Kim IH, Ahn HS, Park SH, Kim SK. Long-term outcomes in children with glioblastoma. Journal of neurosurgery. Pediatrics 2010; 6(2): 145-149. [DOI:10.3171/2010.5.PEDS09558]
3. Petr J, Platzek I, Seidlitz A, Mutsaerts HJMM, Hofheinz F, Schramm G, Maus J, Beuthien-Baumann B, Krause M, den Hoff Jv. Early and late effects of radiochemotherapy on cerebral blood flow in glioblastoma patients measured with non-invasive perfusion MRI. Radiotherapy and oncology 2016; 118(1): 24-28. [DOI:10.1016/j.radonc.2015.12.017]
4. Bastiancich C, Bianco J, Vanvarenberg K, Ucakar B, Joudiou N, Gallez B, Bastiat G, Lagarce F, V Préat V, Danhier F. Injectable nanomedicine hydrogel for local chemotherapy of glioblastoma after surgical resection. Journal of controlled release 2017; 264: 45-54. [DOI:10.1016/j.jconrel.2017.08.019]
5. Kaus M, Warfield SK, Nabavi A, E Chatzidakis, M Black P, Jolesz F A , Kikinis R. Segmentation of meningiomas and low grade gliomas in MRI. International conference on medical image computing and computer-assisted intervention 1999; 1679: 1-10. [DOI:10.1007/10704282_1]
6. Brandsma D, van den Bent MJ. Pseudoprogression and pseudoresponse in the treatment of gliomas. Current opinion in neurology 2009; 22(6): 633-638. [DOI:10.1097/WCO.0b013e328332363e]
7. Flegel T, Podell M, March PA, Chakeres DW. Use of a disposable real-time CT stereotactic navigator device for minimally invasive dog brain biopsy through a mini-burr hole. American journal of neuroradiology 2002; 23: 1160-1163.
8. Parker NR, Hudson AL, Khong P, Parkinson JF, Dwight T, Ikin RJ, Zhu Y, Cheng Z J, Vafaee F, Chen J, Wheeler HR, Howell VM. Intratumoral heterogeneity identified at the epigenetic, genetic and transcriptional level in glioblastoma. Scientific reports 2016; 6: 1-10. [DOI:10.1038/srep22477]
9. McNamara MG, Sahebjam S, Mason WP. Emerging biomarkers in glioblastoma. Cancers (Basel) 2013; 5(3): 1103-1119. [DOI:10.3390/cancers5031103]
10. Bitaraf A, Razmara E, Bakhshinejad B, Yousefi H, Vatanmakanian M, Garshasbi M, Cho WC, Babashah S. The oncogenic and tumor suppressive roles of RNA‐binding proteins in human cancers. Journal of cellular physiology 2021; 236(9): 6200-6224. [DOI:10.1002/jcp.30311]
11. Ghaffari-Makhmalbaf P, Sayyad M, Pakravan K, Razmara E, Bitaraf A, Bakhshinejad B, Goudarzi P, Yousefi H, Pournaghshband M, Nemati F, Fahimi H, Rohollah F, Hasanzad M, Hashemi M, Mousavi H, Babashah S. Docosahexaenoic acid reverses the promoting effects of breast tumor cell-derived exosomes on endothelial cell migration and angiogenesis. Life sciences 2021; 264: 118719. [DOI:10.1016/j.lfs.2020.118719]
12. Maminezhad H, Ghanadian S, Pakravan K, Razmara E, Rouhollah F, Mossahebi-Mohammadi M, Babashah S. A panel of six-circulating miRNA signature in serum and its potential diagnostic value in colorectal cancer. Life Sciences 2020; 258: 118226. [DOI:10.1016/j.lfs.2020.118226]
13. Poursheikhani A, Bahmanpour Z, Razmara E, Mashouri L, Taheri M, Morshedi Rad D, Yousefi H, Bitaraf A, Babashah S. Non-coding RNAs underlying chemoresistance in gastric cancer. Cellular oncology 2020; 43(6): 961-988. [DOI:10.1007/s13402-020-00528-2]
14. Razmara E, Bitaraf A, Yousefi H, Nguyen TH, Garshasbi M, Chi-Shing Cho W, Babashah S. Non-coding RNAs in cartilage development: An updated review. International journal of molecular sciences 2019; 20(18): 4475. [DOI:10.3390/ijms20184475]
15. Razmara E, Salehi M, Aslani S, Bitaraf A, Yousefi H, Rosario Colón J, Mahmoudi M. Graves' disease: introducing new genetic and epigenetic contributors. Journal of molecular endocrinology 2021; 66(2): R33-R55. [DOI:10.1530/JME-20-0078]
16. Razmara E, Bitaraf A, Karimi B, Babashah S. Functions of the SNAI family in chondrocyte‐to‐osteocyte development. Annals of the New York Academy of Sciences 2021; 1503(1):5-22. [DOI:10.1111/nyas.14668]
17. Elham O. Mahgoub ER, Amirreza Bitaraf, Fahimeh-Sadat Norouzi, Maryam Montazeri, Roudabeh Behzadi-Andouhjerdi, Mojtaba Falahati, Ke Cheng, Yousif Haik, Anwarul Hasan, Babashah S. Advances of exosome isolation techniques in lung cancer. Molecular biology reports 2020; 47(9):7229-7251. [DOI:10.1007/s11033-020-05715-w]
18. Zhao B, Bian EB, Li J, Li J. New advances of microRNAs in glioma stem cells, with special emphasis on aberrant methylation of microRNAs. Journal of cellular physiology 2014; 229(9): 1141-1147. [DOI:10.1002/jcp.24540]
19. Azzopardi J, Chepick O, Hartmann W. The World Health Organization histological typing of breast tumors-Second edition. American journal of clinical pathology 1982; 78(6): 806-816. [DOI:10.1093/ajcp/78.6.806]
20. Moslemi M, Sohrabi E, Azadi N, Zekri A, Razmara E. Expression analysis of EEPD1 and MUS81 genes in breast Cancer. Biomedical journalof scientificand tecnical research 2020; 29: 22556-22564. [DOI:10.26717/BJSTR.2020.29.004821]
21. Razmara E, Bitarafan F, Esmaeilzadeh-Gharehdaghi E, Almadani N, Garshasbi M. The first case of NSHL by direct impression on EYA1 gene and identification of one novel mutation in MYO7A in the Iranian families. Iranian journal of basic medical sciences 2018; 21(3): 333.
22. Tahmouresi F, Razmara E, Pakravan K, Mossahebi-Mohammadi M, Rouhollah F, Montazeri M, Sarrafzadeh A, Fahimi H. Upregulation of the long noncoding RNAs DSCAM‐AS1 and MANCR is a potential diagnostic marker for breast carcinoma. Biotechnology and applied biochemistry 2020; 68(6):1250-1256. [DOI:10.1002/bab.2048]
23. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C(T)) method. Methods 2001; 25(4): 402-408. [DOI:10.1006/meth.2001.1262]
24. Vlachos IS, Zagganas K, Paraskevopoulou MD, Georgakilas G, Karagkouni D, Vergoulis T, Dalamagas T, Hatzigeorgiou V. DIANA-miRPath v3. 0: deciphering microRNA function with experimental support. Nucleic acids research 2015; 43: W460-W466. [DOI:10.1093/nar/gkv403]
25. Kern F, Aparicio-Puerta E, Li Y, Fehlmann T, Kehl T, Wagner V, Ray K, Ludwig N, Lenhof H-P, Meese E. miRTargetLink 2.0-interactive miRNA target gene and target pathway networks. Nucleic Acids research 2021; 49(W1): W409-W416. [DOI:10.1093/nar/gkab297]
26. Sticht C, De La Torre C, Parveen A, Gretz N. miRWalk: An online resource for prediction of microRNA binding sites. PLoS One 2018; 13: e0206239. [DOI:10.1371/journal.pone.0206239]
27. Clough E, Barrett T. The gene expression omnibus database. Methods in molecular biology 2016; 1418: 93-110. [DOI:10.1007/978-1-4939-3578-9_5]
28. Bauman GS, Gaspar LE, Fisher BJ, Halperin EC, Macdonald DR, Cairncross JG. A prospective study of short-course radiotherapy in poor prognosis glioblastoma multiforme. International Journal of Radiation Oncology, Biology, Physics 1994; 29: 835-839. [DOI:10.1016/0360-3016(94)90573-8]
29. Petterson SA, Dahlrot RH, Hermansen SK, Munthe SKA, Tveden Gundesen M, Wohlleben H, Rasmussen T, Patrick BeierC, HansenS, Winther Kristensen B. High levels of c-Met is associated with poor prognosis in glioblastoma. Journal of neuro-oncology 2015; 122(3): 517-527. [DOI:10.1007/s11060-015-1723-3]
30. Nagy Á, Munkácsy G, Győrffy B. Pancancer survival analysis of cancer hallmark genes. Scientific reports 2021; 11(1): 1-10. [DOI:10.1038/s41598-021-84787-5]
31. Von Ahlfen S, Missel A, Bendrat K, Schlumpberger M. Determinants of RNA quality from FFPE samples. PLoS One 2007; 2: e1261. [DOI:10.1371/journal.pone.0001261]
32. Sreekanthreddy P, Srinivasan H, Kumar DM, Bangalore Nijaguna M, Sridevi S, Vrinda M, Arivazhagan A, Balasubramaniam A, Sathyaranjandas Hegde A, Chandramouli B, Santosh V, Rao, Paturu Kondaiah MRS, Somasundaram K. Identification of potential serum biomarkers of glioblastoma: serum osteopontin levels correlate with poor prognosis. Cancer epidemiology and prevention biomarkers 2010; 19(6): 1409-1422. [DOI:10.1158/1055-9965.EPI-09-1077]
33. Bitaraf A, Babashah S, Garshasbi M. Aberrant expression of a five‐microRNA signature in breast carcinoma as a promising biomarker for diagnosis. Journal of clinical laboratory analysis 2020; 34(2): e23063. [DOI:10.1002/jcla.23063]
34. Luo J, Wang X, Yang Y, Mao Q. Role of micro-RNA (miRNA) in pathogenesis of glioblastoma. European review for medical and pharmacological sciences 2015; 19(9): 1630-1639.
35. Li XF, Shen WZ, Jin X, Ren P, Zhang J. Let-7c regulated epithelial-mesenchymal transition leads to osimertinib resistance in NSCLC cells with EGFR T790M mutations. Scientific reports 2020; 10(1): 1-9. [DOI:10.1038/s41598-020-67908-4]
36. Luo K, Qin Y, Ouyang T, Wang X, Zhang A, Luo P, Pan X. let-7c-5p regulates CyclinD1 in fluoride-mediated osteoblast proliferation and activation. Toxicological sciences 2021; 182(2):275-287. [DOI:10.1093/toxsci/kfab054]
37. Bo L, Wei B, Li Z, Wang Z, Gao Z, Miao Z. Bioinformatics analysis of miRNA expression profile between primary and recurrent glioblastoma. European review for medical and pharmacological sciences 2015; 19(19): 3579-3586.
38. Han HB, Gu J, Zuo HJ, Chen ZG, Zhao W, Li M, Ji DB, Lu YY, Zhang ZQ. Let‐7c functions as a metastasis suppressor by targeting MMP11 and PBX3 in colorectal cancer. The Journal of pathology 2012; 226(3): 544-555. [DOI:10.1002/path.3014]
39. Morgan R, Pandha HS. PBX3 in Cancer. Cancers (Basel) 2020; 12(2): 431. [DOI:10.3390/cancers12020431]
40. Zhang L, Liu X, Jin H, Guo X, Xia L, Chen Z, Bai M, Liu J, Shang X, Wu K, Pan Y, Fan D. miR-206 inhibits gastric cancer proliferation in part by repressing cyclinD2. Cancer letters 2013; 332(1): 94-101. [DOI:10.1016/j.canlet.2013.01.023]
41. Kondo N, Toyama T, Sugiura H, Fujii Y, Yamashita H. MiR-206 expression is down-regulated in estrogen receptor α-positive human breast cancer. Cancer research 2008; 68(13): 5004-5008. [DOI:10.1158/0008-5472.CAN-08-0180]
42. Zhang T, Liu M, Wang C, Lin C, Sun Y, Jin D. Down-regulation of miR-206 promotes proliferation and invasion of laryngeal cancer by regulating VEGF expression. Anticancer research 2011; 31(11): 3859-3863.
43. Taulli R, Bersani F, Foglizzo V, Linari A, Vigna E, Ladanyi M, Tuschl T, Ponzetto C. The muscle-specific microRNA miR-206 blocks human rhabdomyosarcoma growth in xenotransplanted mice by promoting myogenic differentiation. The Journal of clinical investigation 2009; 119(8): 2366-2378. [DOI:10.1172/JCI38075]
44. Dong X, Yang Z, Yang H, Li D, Qiu X. Long non-coding RNA MIR4435-2HG promotes colorectal cancer proliferation and metastasis through miR-206/YAP1 axis. Frontiers in oncology 2020; 10: 160. [DOI:10.3389/fonc.2020.00160]
45. Wang Y, Xu H, Si L, Li Q, Zhu X, Yu T, Gang X. MiR‐206 inhibits proliferation and migration of prostate cancer cells by targeting CXCL11. The prostate 2018; 78(7): 479-490. [DOI:10.1002/pros.23468]
46. Song G, Zhang Y, Wang L. MicroRNA-206 targets notch3, activates apoptosis, and inhibits tumor cell migration and focus formation. The Journal of biological chemistry 2009; 284(46): 31921-31927. [DOI:10.1074/jbc.M109.046862]
47. Singh A, Happel C, Manna SK, Acquaah-Mensah G, Carrerero J, Kumar S, Nasipuri P, Krausz KW, Wakabayashi N, Dewi R, Boros LG, Gonzalez FJ, Gabrielson E, Wong K, Girnun G, Biswa S. Transcription factor NRF2 regulates miR-1 and miR-206 to drive tumorigenesis. The Journal of clinical investigation 2013; 123(7): 2921-2934. [DOI:10.1172/JCI66353]
48. Hao W, Luo W, Bai M, Li J, Bai X, Guo J, Wu J, Wang M. MicroRNA-206 inhibited the progression of glioblastoma through BCL-2. Journal of molecular neuroscience 2016; 60(4): 531-538. [DOI:10.1007/s12031-016-0824-6]
49. Braoudaki M, Lambrou G, Papadodima S, Stefanaki K, Prodromou N, Kanavakis E. MicroRNA expression profiles in pediatric dysembryoplastic neuroepithelial tumors. Medical oncology 2016; 33(1): 5. [DOI:10.1007/s12032-015-0719-3]
50. Scarpati GDV, Falcetta F, Carlomagno C, Ubezio S, Marchini S, De Stefano A, Kumar Singh V, D'Incalci M, De Placido S, Pepe S. A specific miRNA signature correlates with complete pathological response to neoadjuvant chemoradiotherapy in locally advanced rectal cancer. International journal of radiation oncology, biology, physics 2012; 83(4): 1113-1119. [DOI:10.1016/j.ijrobp.2011.09.030]
51. Bibi F, Naseer MI, Alvi SA, Yasir M, Jiman-Fatani AA, Sawan A, Abuzenadah AM, Al-Qahtani MH, Azhar EI. microRNA analysis of gastric cancer patients from Saudi Arabian population. BMC Genomics 2016; 17(suppl 9): 51-60. [DOI:10.1186/s12864-016-3090-7]
52. Li KKW, Zhang RQ, Chan AKY, Ng HK. HG-07 aberrantly expressed microRNAs in BRAF mutated young adult GBM. Neuro-oncology 2016; 18(suppl 3): iii49. [DOI:10.1093/neuonc/now073.06]
53. Rivera-Díaz M, Miranda-Román MA, Soto D, Quintero-Aguilo M, Ortiz-Zuazaga H, Marcos-Martinez MJ, Vivas-Mejía PE. MicroRNA-27a distinguishes glioblastoma multiforme from diffuse and anaplastic astrocytomas and has prognostic value. American journal of cancer research 2015; 5(1): 201.
54. Sulaiman SA, Ainaa Muhsin NI, Arshad AR, Rasyadan A, Mohamad Nazarie W, Fahmi W; Rahman J, Norlinah Mohamed I, Nor Azian AM. Differential expression of circulating miRNAs in Parkinson's disease patients: Potential early biomarker? Neurology Asia 2020; 25(3): 319-329.

Add your comments about this article : Your username or Email:
CAPTCHA

Send email to the article author


Rights and permissions
Creative Commons License This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

© 2022 CC BY-NC 4.0 | Iranian Biomedical Journal

Designed & Developed by : Yektaweb