Non-coding RNAs as Biomarkers for Survival in Colorectal Cancer Patients


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Abstract

Colorectal cancer (CRC) has a high incidence and fatality rate worldwide. It ranks second concerning death worldwide. Cancer patients are diagnosed with the disease at a later stage due to the absence of early diagnostic methods, which leads to increased death. With the help of recent advancements in the fields of diagnosis and therapy, the development of novel methods using new targets could be helpful for the long-term survival of CRC patients when CRC is detected early. However, the prognosis for the advanced stage of CRC is abysmal. New biomarkers are emerging as promising alternatives since they can be utilized for early detection of CRC, are simple to use, and non-invasive. Non-coding RNAs (ncRNAs) have been seen to have an aberrant expression in the development of many malignancies, including CRC. In the past two decades, much research has been done on non-coding RNAs, which may be valuable as biomarkers and targets for antitumor therapy. Non-coding RNAs can be employed in detecting and treating CRC. Non-coding RNAs play an essential role in regulating gene expression. This article reviews ncRNAs and their expression levels in CRC patients that could be used as potential biomarkers. Various ncRNAs have been associated with CRC, such as microRNAs, long non-coding RNAs, circular RNAs, etc. The expression of these non-coding RNAs may provide insights into the stages of cancer and the prognosis of cancer patients and therefore proper precautionary measures can be taken to decrease cancer-related deaths.

About the authors

Mohammad Andrabi

Department of Genetic Engineering, School of Bio-Engineering, SRM Institute of Science and Technology

Email: info@benthamscience.net

Yasodha Kesavan

Department of Biotechnology, School of Bio-Engineering, SRM Institute of Science and Technology

Email: info@benthamscience.net

Satish Ramalingam

Department of Genetic Engineering, School of Bio-Engineering, SRM Institute of Science and Technology

Author for correspondence.
Email: info@benthamscience.net

References

  1. Yamashita R, Long J, Longacre T, et al. Deep learning model for the prediction of microsatellite instability in colorectal cancer: A diagnostic study. Lancet Oncol 2021; 22(1): 132-41. doi: 10.1016/S1470-2045(20)30535-0 PMID: 33387492
  2. Muzny DM, Bainbridge MN, Chang K, et al. Comprehensive molecular characterization of human colon and rectal cancer. Nature 2012; 487(7407): 330-7. doi: 10.1038/nature11252 PMID: 22810696
  3. Zhou XY, Luo B, Jiang ZK, et al. Non-coding RNAS and colorectal cancer liver metastasis. Mol Cell Biochem 2020; 475(1-2): 151-9. doi: 10.1007/s11010-020-03867-8 PMID: 32767228
  4. Ogunwobi OO, Mahmood F, Akingboye A. Biomarkers in colorectal cancer: Current research and future prospects. Int J Mol Sci 2020; 21(15): 5311. doi: 10.3390/ijms21155311 PMID: 32726923
  5. Campos-da-Paz M, Dórea JG, Galdino AS, Lacava ZGM, de Fatima MASM. Carcinoembryonic antigen (CEA) and hepatic metastasis in colorectal cancer: Update on biomarker for clinical and biotechnological approaches. Recent Pat Biotechnol 2018; 12(4): 269-79. doi: 10.2174/1872208312666180731104244 PMID: 30062978
  6. Yang G, Lu X, Yuan L. LncRNA: A link between RNA and cancer. Biochim Biophys Acta Gene Regul Mech 2014; 1839(11): 1097-109. doi: 10.1016/j.bbagrm.2014.08.012 PMID: 25159663
  7. Kung JTY, Colognori D, Lee JT. Long noncoding RNAs: Past, present, and future. Genetics 2013; 193(3): 651-69. doi: 10.1534/genetics.112.146704 PMID: 23463798
  8. Lei B, Tian Z, Fan W, Ni B. Circular RNA: A novel biomarker and therapeutic target for human cancers. Int J Med Sci 2019; 16(2): 292-301. doi: 10.7150/ijms.28047 PMID: 30745810
  9. Statello L, Guo CJ, Chen LL, Huarte M. Gene regulation by long non-coding RNAs and its biological functions. Nat Rev Mol Cell Biol 2021; 22(2): 96-118. doi: 10.1038/s41580-020-00315-9 PMID: 33353982
  10. Rinn JL, Chang HY. Genome regulation by long noncoding RNAs. Annu Rev Biochem 2012; 81(1): 145-66. doi: 10.1146/annurev-biochem-051410-092902 PMID: 22663078
  11. Sati S, Ghosh S, Jain V, Scaria V, Sengupta S. Genome-wide analysis reveals distinct patterns of epigenetic features in long non-coding RNA loci. Nucleic Acids Res 2012; 40(20): 10018-31. doi: 10.1093/nar/gks776 PMID: 22923516
  12. Winkle M, El-Daly SM, Fabbri M, Calin GA. Noncoding RNA therapeutics - challenges and potential solutions. Nat Rev Drug Discov 2021; 20(8): 629-51. doi: 10.1038/s41573-021-00219-z PMID: 34145432
  13. Macfarlane L-A, Murphy PR. MicroRNA: Biogenesis, function and role in cancer. Curr Genomics 2010; 11(7): 537-61. doi: 10.2174/138920210793175895 PMID: 21532838
  14. Liu B, Li J, Cairns MJ. Identifying miRNAs, targets and functions. Brief Bioinform 2014; 15(1): 1-19. doi: 10.1093/bib/bbs075 PMID: 23175680
  15. Tay Y, Rinn J, Pandolfi PP. The multilayered complexity of ceRNA crosstalk and competition. Nature 2014; 505(7483): 344-52. doi: 10.1038/nature12986 PMID: 24429633
  16. Yao R, Zou H, Liao W. Prospect of circular RNA in hepatocellular carcinoma: A novel potential biomarker and therapeutic target. Front Oncol 2018; 8: 332. doi: 10.3389/fonc.2018.00332 PMID: 30191143
  17. Jeck WR, Sorrentino JA, Wang K, et al. Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA 2013; 19(2): 141-57. doi: 10.1261/rna.035667.112 PMID: 23249747
  18. Yin Y, Long J, He Q, et al. Emerging roles of circRNA in formation and progression of cancer. J Cancer 2019; 10(21): 5015-21. doi: 10.7150/jca.30828 PMID: 31602252
  19. Zhang M, Xin Y. Circular RNAs: A new frontier for cancer diagnosis and therapy. J Hematol Oncol 2018; 11(1): 21. doi: 10.1186/s13045-018-0569-5 PMID: 29433541
  20. Mannoor K, Liao J, Jiang F. Small nucleolar RNAs in cancer. Biochim Biophys Acta Rev Cancer 2012; 1826(1): 121-8. doi: 10.1016/j.bbcan.2012.03.005 PMID: 22498252
  21. Dhamodharan S, Rose MM, Chakkarappan SR, et al. Genetic variant rs10251977 (G > A) in EGFR-AS1 modulates the expression of EGFR isoforms A and D. Sci Rep 2021; 11(1): 8808. doi: 10.1038/s41598-021-88161-3 PMID: 33888812
  22. Huang L, Liang XZ, Deng Y, et al. Prognostic value of small nucleolar RNAs (snoRNAs) for colon adenocarcinoma based on RNA sequencing data. Pathol Res Pract 2020; 216(6): 152937. doi: 10.1016/j.prp.2020.152937 PMID: 32312483
  23. Iwasaki YW, Siomi MC, Siomi H. PIWI-interacting RNA: Its biogenesis and functions. Annu Rev Biochem 2015; 84(1): 405-33. doi: 10.1146/annurev-biochem-060614-034258 PMID: 25747396
  24. Chalbatani GM, Dana H, Memari F, et al. Biological function and molecular mechanism of piRNA in cancer. Pract Lab Med 2019; 13: e00113. doi: 10.1016/j.plabm.2018.e00113 PMID: 30705933
  25. Chu H, Hui G, Yuan L, et al. Identification of novel piRNAs in bladder cancer. Cancer Lett 2015; 356(2): 561-7. doi: 10.1016/j.canlet.2014.10.004 PMID: 25305452
  26. Peng L, Song L, Liu C, et al. piR-55490 inhibits the growth of lung carcinoma by suppressing mTOR signaling. Tumour Biol 2016; 37(2): 2749-56. doi: 10.1007/s13277-015-4056-0 PMID: 26408181
  27. Ji Q, Zhang L, Liu X, et al. Long non-coding RNA MALAT1 promotes tumour growth and metastasis in colorectal cancer through binding to SFPQ and releasing oncogene PTBP2 from SFPQ/PTBP2 complex. Br J Cancer 2014; 111(4): 736-48. doi: 10.1038/bjc.2014.383 PMID: 25025966
  28. Zheng HT, Shi DB, Wang YW, et al. High expression of lncRNA MALAT1 suggests a biomarker of poor prognosis in colorectal cancer. Int J Clin Exp Pathol 2014; 7(6): 3174-81. PMID: 25031737
  29. Jin L, Pan YL, Zhang J, Cao PG. LncRNA HOTAIR recruits SNAIL to inhibit the transcription of HNF4α and promote the viability, migration, invasion and EMT of colorectal cancer. Transl Oncol 2021; 14(4): 101036. doi: 10.1016/j.tranon.2021.101036 PMID: 33588137
  30. Zhang Z, Zhou C, Chang Y, et al. Long non-coding RNA CASC11 interacts with hnRNP-K and activates the WNT/β-catenin pathway to promote growth and metastasis in colorectal cancer. Cancer Lett 2016; 376(1): 62-73. doi: 10.1016/j.canlet.2016.03.022 PMID: 27012187
  31. Nissan A, Stojadinovic A, Mitrani-Rosenbaum S, et al. Colon cancer associated transcript-1: A novel RNA expressed in malignant and pre-malignant human tissues. Int J Cancer 2012; 130(7): 1598-606. doi: 10.1002/ijc.26170 PMID: 21547902
  32. Yang C, Pan Y, Deng SP. Downregulation of lncRNA CCAT1 enhances 5-fluorouracil sensitivity in human colon cancer cells. BMC Mol Cell Biol 2019; 20(1): 9. doi: 10.1186/s12860-019-0188-1 PMID: 31039730
  33. Zhang Y, Sun J, Qi Y, et al. Long non-coding RNA TPT1-AS1 promotes angiogenesis and metastasis of colorectal cancer through TPT1-AS1/NF90/VEGFA signaling pathway. Aging 2020; 12(7): 6191-205. doi: 10.18632/aging.103016 PMID: 32248186
  34. Han D, Gao X, Wang M, et al. Long noncoding RNA H19 indicates a poor prognosis of colorectal cancer and promotes tumor growth by recruiting and binding to eIF4A3. Oncotarget 2016; 7(16): 22159-73. doi: 10.18632/oncotarget.8063 PMID: 26989025
  35. Chen R, Zhou S, Chen J, Lin S, Ye F, Jiang P. Lncrna blacat1/mir-519d-3p/creb1 axis mediates proliferation, apoptosis, migration, invasion, and drug-resistance in colorectal cancer progression. Cancer Manag Res 2020; 12: 13137-48. doi: 10.2147/CMAR.S274447 PMID: 33376405
  36. Fan H, Zhu J, Yao X. Long non-coding RNA PVT1 as a novel potential biomarker for predicting the prognosis of colorectal cancer. Int J Biol Markers 2018; 33(4): 415-22. doi: 10.1177/1724600818777242 PMID: 29888675
  37. Duan W, Kong X, Li J, et al. LncRNA AC010789.1 promotes colorectal cancer progression by targeting microrna-432-3p/zeb1 axis and the wnt/β-catenin signaling pathway. Front Cell Dev Biol 2020; 8: 565355. doi: 10.3389/fcell.2020.565355 PMID: 33178684
  38. Yang P, Li J, Peng C, et al. TCONS_00012883 promotes proliferation and metastasis via DDX3/YY1/MMP1/PI3KAKT axis in colorectal cancer. Clin Transl Med 2020; 10(6): e211. doi: 10.1002/ctm2.211 PMID: 33135346
  39. Tang Y, Tang R, Tang M, et al. LncRNA DNAJC3-AS1 regulates fatty acid synthase via the egfr pathway to promote the progression of colorectal cancer. Front Oncol 2021; 10: 604534. doi: 10.3389/fonc.2020.604534 PMID: 33604287
  40. Silva-Fisher JM, Dang HX, White NM, et al. Long non-coding RNA RAMS11 promotes metastatic colorectal cancer progression. Nat Commun 2020; 11(1): 2156. doi: 10.1038/s41467-020-15547-8 PMID: 32358485
  41. Khan MZI, Law HKW. RAMS11 promotes CRC through mTOR-dependent inhibition of autophagy, suppression of apoptosis, and promotion of epithelial-mesenchymal transition. Cancer Cell Int 2021; 21(1): 321. doi: 10.1186/s12935-021-02023-6 PMID: 34174900
  42. Li C, Wang P, Du J, Chen J, Liu W, Ye K. LncRNA RAD51AS1/miR29b/c3p/NDRG2 crosstalk repressed proliferation, invasion and glycolysis of colorectal cancer. IUBMB Life 2021; 73(1): 286-98. doi: 10.1002/iub.2427 PMID: 33314669
  43. Liu L, Wang HJ, Meng T, et al. RETRACTED: lncRNA GAS5 inhibits cell migration and invasion and promotes autophagy by targeting mir-222-3p via the gas5/pten-signaling pathway in CRC. Mol Ther Nucleic Acids 2019; 17: 644-56. doi: 10.1016/j.omtn.2019.06.009 PMID: 31400607
  44. Zhuang L, Ding W, Ding W, Zhang Q, Xu X, Xi D. lncRNA ZNF667AS1 (NR_036521.1) inhibits the progression of colorectal cancer via regulating ANK2/JAK2 expression. J Cell Physiol 2021; 236(3): 2178-93. doi: 10.1002/jcp.30004 PMID: 32853419
  45. Balacescu O, Sur D, Cainap C, et al. The impact of miRNA in colorectal cancer progression and its liver metastases. Int J Mol Sci 2018; 19(12): 3711. doi: 10.3390/ijms19123711 PMID: 30469518
  46. Deng S, Wang H, Fan H, et al. Over-expressed miRNA-200b ameliorates ulcerative colitis-related colorectal cancer in mice through orchestrating epithelial-mesenchymal transition and inflammatory responses by channel of AKT2. Int Immunopharmacol 2018; 61: 346-54. doi: 10.1016/j.intimp.2018.06.024 PMID: 29933193
  47. Michael MZ, O’ Connor SM, van Holst PNG, Young GP, James RJ. Reduced accumulation of specific microRNAs in colorectal neoplasia. Mol Cancer Res 2003; 1(12): 882-91. PMID: 14573789
  48. Li C, Yan G, Yin L, Liu T, Li C, Wang L. Prognostic roles of microRNA 143 and microRNA 145 in colorectal cancer: A meta-analysis. Int J Biol Markers 2019; 34(1): 6-14. doi: 10.1177/1724600818807492 PMID: 30854930
  49. Yuan W, Sui C, Liu Q, Tang W, An H, Ma J. Up-regulation of microRNA-145 associates with lymph node metastasis in colorectal cancer. PLoS One 2014; 9(7): e102017. doi: 10.1371/journal.pone.0102017 PMID: 25019299
  50. Zeng Z, Li Y, Pan Y, et al. Cancer-derived exosomal miR-25-3p promotes pre-metastatic niche formation by inducing vascular permeability and angiogenesis. Nat Commun 2018; 9(1): 5395. doi: 10.1038/s41467-018-07810-w PMID: 30568162
  51. Lai X, Friedman A. Exosomal microRNA concentrations in colorectal cancer: A mathematical model. J Theor Biol 2017; 415: 70-83. doi: 10.1016/j.jtbi.2016.12.006 PMID: 27993628
  52. Zhang G, Zhou H, Xiao H, Liu Z, Tian H, Zhou T. MicroRNA-92a functions as an oncogene in colorectal cancer by targeting PTEN. Dig Dis Sci 2014; 59(1): 98-107. doi: 10.1007/s10620-013-2858-8 PMID: 24026406
  53. Tsukamoto M, Iinuma H, Yagi T, Matsuda K, Hashiguchi Y. Circulating exosomal MicroRNA-21 as a biomarker in each tumor stage of colorectal cancer. Oncol 2017; 92: 360-70. doi: 10.1159/000463387
  54. Xu K, Liang X, Cui D, Wu Y, Shi W, Liu J. miR-1915 inhibits Bcl-2 to modulate multidrug resistance by increasing drug-sensitivity in human colorectal carcinoma cells. Mol Carcinog 2013; 52(1): 70-8. doi: 10.1002/mc.21832 PMID: 22121083
  55. Yang Y, Weng W, Peng J, et al. Fusobacterium nucleatum increases proliferation of colorectal cancer cells and tumor development in mice by activating toll-like receptor 4 signaling to nuclear factor−κb and up-regulating expression of microRNA-21. Gastroenterology 2017; 152(4): 851-866.e24. doi: 10.1053/j.gastro.2016.11.018 PMID: 27876571
  56. Wu CW, Ng SSM, Dong YJ, et al. Detection of miR-92a and miR-21 in stool samples as potential screening biomarkers for colorectal cancer and polyps. Gut 2012; 61(5): 739-45. doi: 10.1136/gut.2011.239236 PMID: 21930727
  57. Wu CW, Ng SC, Dong Y, et al. Identification of microRNA-135b in stool as a potential noninvasive biomarker for colorectal cancer and adenoma. Clin Cancer Res 2014; 20(11): 2994-3002. doi: 10.1158/1078-0432.CCR-13-1750 PMID: 24691020
  58. Ahmed FE, Ahmed NC, Vos PW, et al. Diagnostic microRNA markers to screen for sporadic human colon cancer in stool: I. Proof of principle. Cancer Genomics Proteomics 2013; 10(3): 93-113. PMID: 23741026
  59. Shahmohamadnejad S, et al. Aberrant methylation of miR-124 upregulates DNMT3B in colorectal cancer to accelerate invasion and migration. Arch Physiol Biochem 2020; 128(6): 1503-9. doi: 10.1080/13813455.2020.1779311 PMID: 32552060
  60. Sun L, Fang Y, Wang X, et al. miR-302a inhibits metastasis and cetuximab resistance in colorectal cancer by targeting NFIB and CD44. Theranostics 2019; 9(26): 8409-25. doi: 10.7150/thno.36605 PMID: 31754405
  61. Qiao PF, Yao L, Zeng ZL. Catalpol mediated microRNA 34a suppresses autophagy and malignancy by regulating SIRT1 in colorectal cancer. Oncol Rep 2020; 43(4): 1053-66. doi: 10.3892/or.2020.7494 PMID: 32323786
  62. Fan M, Ma X, Wang F, et al. MicroRNA-30b-5p functions as a metastasis suppressor in colorectal cancer by targeting Rap1b. Cancer Lett 2020; 477: 144-56. doi: 10.1016/j.canlet.2020.02.021 PMID: 32112903
  63. Bleau AM, Redrado M, Nistal-Villan E, et al. miR-146a targets c-met and abolishes colorectal cancer liver metastasis. Cancer Lett 2018; 414: 257-67. doi: 10.1016/j.canlet.2017.11.008 PMID: 29133238
  64. Zhou Z, Wu L, Liu Z, et al. MicroRNA-214-3p targets the PLAGL2-MYH9 axis to suppress tumor proliferation and metastasis in human colorectal cancer. Aging 2020; 12(10): 9633-57. doi: 10.18632/aging.103233 PMID: 32413870
  65. Ma Z, Shuai Y, Gao X, Wen X, Ji J. Circular RNAs in the tumour microenvironment. Mol Cancer 2020; 19(1): 8. doi: 10.1186/s12943-019-1113-0 PMID: 31937318
  66. Guo L, Yang G, Kang Y, et al. Construction and analysis of a cerna network reveals potential prognostic markers in colorectal cancer. Front Genet 2020; 11: 418. doi: 10.3389/fgene.2020.00418 PMID: 32457800
  67. He C, Huang C, Zhou R, Yu H. CircLMNB1 promotes colorectal cancer by regulating cell proliferation, apoptosis and epithelial-mesenchymal transition. OncoTargets Ther 2019; 12: 6349-59. doi: 10.2147/OTT.S204741 PMID: 31496737
  68. Chen LY, Wang L, Ren YX, et al. The circular RNA circ-ERBIN promotes growth and metastasis of colorectal cancer by miR-125a-5p and miR-138-5p/4EBP-1 mediated cap-independent HIF-1α translation. Mol Cancer 2020; 19(1): 164. doi: 10.1186/s12943-020-01272-9 PMID: 33225938
  69. Wu M, Kong C, Cai M, et al. Hsa_circRNA_002144 promotes growth and metastasis of colorectal cancer through regulating miR-615-5p/LARP1/mTOR pathway. Carcinogenesis 2021; 42(4): 601-10. doi: 10.1093/carcin/bgaa140 PMID: 33347535
  70. Wang X, Zhang Y, Huang L, et al. Decreased expression of hsa_circ_001988 in colorectal cancer and its clinical significances. Int J Clin Exp Pathol 2015; 8(12): 16020-5. PMID: 26884878
  71. Li C, Zhou H. Circular RNA hsa_circRNA_102209 promotes the growth and metastasis of colorectal cancer through mir761-mediated ras and rab interactor 1 signaling. Cancer Med 2020; 9(18): 6710-25. doi: 10.1002/cam4.3332 PMID: 32706154
  72. Du J, Xu J, Chen J, Liu W, Wang P, Ye K. circRAE1 promotes colorectal cancer cell migration and invasion by modulating miR-338-3p/TYRO3 axis. Cancer Cell Int 2020; 20(1): 430. doi: 10.1186/s12935-020-01519-x PMID: 32908453
  73. Fang G, Ye BL, Hu BR, Ruan XJ, Shi YX. circRNA_100290 promotes colorectal cancer progression through miR-516b-induced downregulation of FZD4 expression and Wnt/β-catenin signaling. Biochem Biophys Res Commun 2018; 504(1): 184-9. doi: 10.1016/j.bbrc.2018.08.152 PMID: 30173892
  74. Pan B, Qin J, Liu X, et al. Identification of serum exosomal hsa-circ-0004771 as a novel diagnostic biomarker of colorectal cancer. Front Genet 2019; 10: 1096. doi: 10.3389/fgene.2019.01096 PMID: 31737058
  75. Zhang L, Dong X, Yan B, Yu W, Shan L. circAGFG1 drives metastasis and stemness in colorectal cancer by modulating YY1/CTNNB1. Cell Death Dis 2020; 11(7): 542. doi: 10.1038/s41419-020-2707-6 PMID: 32681092
  76. Wang X, Ren Y, Ma S, Wang S. Circular rna 0060745, a novel circrna, promotes colorectal cancer cell proliferation and metastasis through mir-4736 sponging. OncoTargets Ther 2020; 13: 1941-51. doi: 10.2147/OTT.S240642 PMID: 32273712
  77. Zeng W, Liu Y, Li WT, Li Y, Zhu JF. circFNDC3B sequestrates miR9375p to derepress TIMP3 and inhibit colorectal cancer progression. Mol Oncol 2020; 14(11): 2960-84. doi: 10.1002/1878-0261.12796 PMID: 32896063
  78. Yuan Y, Liu W, Zhang Y, Zhang Y, Sun S. CircRNA circ_0026344 as a prognostic biomarker suppresses colorectal cancer progression via microRNA-21 and microRNA-31. Biochem Biophys Res Commun 2018; 503(2): 870-5. doi: 10.1016/j.bbrc.2018.06.089 PMID: 29928882
  79. Zhang X, Zhao Y, Kong P, Han M, Li B. Expression of circZNF609 is down-regulated in colorectal cancer tissue and promotes apoptosis in colorectal cancer cells by upregulating p53. Med Sci Monit 2019; 25: 5977-85. doi: 10.12659/MSM.915926 PMID: 31401644
  80. Mai D, Ding P, Tan L, et al. PIWI-interacting RNA-54265 is oncogenic and a potential therapeutic target in colorectal adenocarcinoma. Theranostics 2018; 8(19): 5213-30. doi: 10.7150/thno.28001 PMID: 30555542
  81. Weng W, Liu N, Toiyama Y, et al. Novel evidence for a PIWI-interacting RNA (piRNA) as an oncogenic mediator of disease progression, and a potential prognostic biomarker in colorectal cancer. Mol Cancer 2018; 17(1): 16. doi: 10.1186/s12943-018-0767-3 PMID: 29382334
  82. Qu A, Wang W, Yang Y, et al. A serum piRNA signature as promising non-invasive diagnostic and prognostic biomarkers for colorectal cancer. Cancer Manag Res 2019; 11: 3703-20. doi: 10.2147/CMAR.S193266 PMID: 31118791
  83. Yoshida K, Toden S, Weng W, et al. SNORA21 - An oncogenic small nucleolar RNA, with a prognostic biomarker potential in human colorectal cancer. EBioMedicine 2017; 22: 68-77. doi: 10.1016/j.ebiom.2017.07.009 PMID: 28734806
  84. Okugawa Y, Toiyama Y, Toden S, et al. Clinical significance of SNORA42 as an oncogene and a prognostic biomarker in colorectal cancer. Gut 2017; 66(1): 107-17. doi: 10.1136/gutjnl-2015-309359 PMID: 26475630

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