The role of small nucleolus RNA and its host genes in bladder cancer

doi:10.3877/cma.j.issn.2095-8757.2025.02.006

Abstract

Abstract:

Small nucleolar RNAs (snoRNA) widely exist in the nucleus of eukaryotes. They are a group of non-coding RNA derived from the introns of the primary transcripts of small nucleolar host genes (SNHG), which are mainly involved in the biosynthesis of ribosomes and the post-transcriptional modification of RNA. In recent years, the role of snoRNA in tumorigenesis and development has gained attention. This article provides a comprehensive review of the biological characteristics of snoRNA and their relationship with cancer, focusing on the role of snoRNA and SNHG in bladder cancer, especially the research progress of their expression, regulation, biological function, and clinical applications in bladder cancer, with the aim of providing references for clinical diagnosis and treatment.

Key words: Small nucleolar RNA, Host genes, Bladder cancer

Chunfeng Shi, Xiuyi Lyu, Jun Chen. The role of small nucleolus RNA and its host genes in bladder cancer[J]. Chinese Journal of Geriatrics Research(Electronic Edition), 2025, 12(02): 29-36.

/ / Recommend

Add to citation manager EndNote|Ris|BibTeX

URL: https://zhlnbyjdzzz.cma-cmc.com.cn/EN/10.3877/cma.j.issn.2095-8757.2025.02.006

https://zhlnbyjdzzz.cma-cmc.com.cn/EN/Y2025/V12/I02/29

References 91

[1]	Webster SF, Ghalei H. Maturation of small nucleolar RNAs: From production to function[J]. RNA Biol, 2023, 20(1):715-736.
[2]	Stepanov GA, Filippova JA, Komissarov AB, et al. Regulatory role of small nucleolar rnas in human diseases[J]. Biomed Res Int, 2015, 2015:206849.
[3]	Schubert T, Pusch MC, Diermeier S, et al. Df31 protein and snornas maintain accessible higher-order structures of chromatin[J]. Mol Cell, 2012, 48(3):434-444.
[4]	Holley CL, Li MW, Scruggs BS, et al. Cytosolic accumulation of small nucleolar rnas (snornas) is dynamically regulated by nadph oxidase[J]. J Biol Chem, 2015, 290(18):11741-11748.
[5]	Chabronova A, Holmes TL, Hoang DM, et al. Snornas in cardiovascular development, function, and disease[J]. Trends Mol Med, 2024, 30(6):562-578.
[6]	Liu Y, Zhao C, Wang G, et al. SNORD1C maintains stemness and 5-FU resistance by activation of Wnt signaling pathway in colorectal cancer[J]. Cell Death Discov, 2022, 8(1):200.
[7]	Xu G, Yang F, Ding CL, et al. Small nucleolar RNA 113-1 suppresses tumorigenesis in hepatocellular carcinoma[J]. Mol Cancer, 2014, 13:216.
[8]	Xia C, Dong X, Li H, et al. Cancer statistics in China and United States, 2022: profiles, trends, and determinants[J]. Chin Med J (Engl), 2022, 135(5):584-590.
[9]	Li K, Lin T, Xue W, et al. Current status of diagnosis and treatment of bladder cancer in China - Analyses of Chinese Bladder Cancer Consortium database[J]. Asian J Urol, 2015, 2(2):63-69.
[10]	Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: Globocan estimates of incidence and mortality worldwide for 36 cancers in 185 countries[J]. CA Cancer J Clin, 2021, 71(3):209-249.
[11]	Hussain SA, Lester JF, Jackson R, et al. Addition of nintedanib or placebo to neoadjuvant gemcitabine and cisplatin in locally advanced muscle-invasive bladder cancer (neoblade): A double-blind, randomised, phase 2 trial[J]. Lancet Oncol, 2022, 23(5):650-658.
[12]	Motzer RJ, McDermott DF, Escudier B, et al. Conditional survival and long-term efficacy with nivolumab plus ipilimumab versus sunitinib in patients with advanced renal cell carcinoma[J]. Cancer, 2022, 128(11):2085-2097.
[13]	Becker REN, Meyer AR, Brant A, et al. Clinical restaging and tumor sequencing are inaccurate indicators of response to neoadjuvant chemotherapy for muscle-invasive bladder cancer[J]. Eur Urol, 2021, 79(3):364-371.
[14]	Witjes JA, Bruins HM, Cathomas R, et al. European association of urology guidelines on muscle-invasive and metastatic bladder cancer: Summary of the 2020 guidelines[J]. Eur Urol, 2021, 79(1):82-104.
[15]	Bratkovič T, Božič J, Rogelj B. Functional diversity of small nucleolar RNAs[J]. Nucleic Acids Res, 2020, 48(4):1627-1651.
[16]	Dsouza VL, Adiga D, Sriharikrishnaa S, et al. Small nucleolar rna and its potential role in breast cancer - a comprehensive review[J]. Biochim Biophys Acta Rev Cancer, 2021, 1875(1):188501.
[17]	Zimta AA, Tigu AB, Braicu C, et al. An emerging class of long non-coding rna with oncogenic role arises from the snorna host genes[J]. Front Oncol, 2020, 10:389.
[18]	Bergeron D, Paraqindes H, Fafard-Couture E, et al. Snodb 2.0: An enhanced interactive database, specializing in human snornas[J]. Nucleic Acids Res, 2023, 51(D1):D291-D296.
[19]	Bouchard-Bourelle P, Desjardins-Henri C, Mathurin-St-Pierre D, et al. Snodb: An interactive database of human snorna sequences, abundance and interactions[J]. Nucleic Acids Res, 2020, 48(D1):D220-D225.
[20]	Tollervey D, Kiss T. Function and synthesis of small nucleolar rnas[J]. Curr Opin Cell Biol, 1997, 9(3):337-342.
[21]	Dennis PP, Omer A. Small non-coding rnas in archaea[J]. Curr Opin Microbiol, 2005, 8(6):685-694.
[22]	Nahkuri S, Taft RJ, Korbie DJ, et al. Molecular evolution of the hbii-52 snorna cluster[J]. J Mol Biol, 2008, 381(4):810-815.
[23]	Luo Y, Li S. Genome-wide analyses of retrogenes derived from the human box h/aca snornas[J]. Nucleic Acids Res, 2007, 35(2):559-571.
[24]	Scott MS, Ono M. From snorna to mirna: Dual function regulatory non-coding rnas[J]. Biochimie, 2011, 93(11):1987-1992.
[25]	Weber MJ. Mammalian small nucleolar rnas are mobile genetic elements[J]. PLoS Genet, 2006, 2(12):e205.
[26]	Jorjani H, Kehr S, Jedlinski DJ, et al. An updated human snornaome[J]. Nucleic Acids Res, 2016, 44(11):5068-5082.
[27]	Grzechnik P, Szczepaniak SA, Dhir S, et al. Nuclear fate of yeast snorna is determined by co-transcriptional rnt1 cleavage[J]. Nat Commun, 2018, 9(1):1783.
[28]	Khoshnevis S, Dreggors RE, Hoffmann TFR, et al. A conserved bcd1 interaction essential for box c/d snornp biogenesis[J]. J Biol Chem, 2019, 294(48):18360-18371.
[29]	Dupuis-Sandoval F, Poirier M, Scott MS. The emerging landscape of small nucleolar rnas in cell biology[J]. Wiley Interdiscip Rev RNA, 2015, 6(4):381-397.
[30]	Meier UT. RNA modification in Cajal bodies[J]. RNA Biol, 2017, 14(6):693-700.
[31]	Rajan KS, Doniger T, Cohen-Chalamish S, et al. Pseudouridines on trypanosoma brucei spliceosomal small nuclear RNAs and their implication for RNA and protein interactions[J]. Nucleic Acids Res, 2019, 47(14):7633-7647.
[32]	Kiss T. Biogenesis of small nuclear rnps[J]. J Cell Sci, 2004, 117(Pt 25):5949-5951.
[33]	Marnef A, Richard P, Pinzon N, et al. Targeting vertebrate intron-encoded box c/d 2'-o-methylation guide rnas into the cajal body[J]. Nucleic Acids Res, 2014, 42(10):6616-6629.
[34]	McMahon M, Contreras A, Ruggero D. Small rnas with big implications: New insights into h/aca snorna function and their role in human disease[J]. Wiley Interdiscip Rev RNA, 2015, 6(2):173-189.
[35]	Liu B, Ni J, Fournier MJ. Probing rna in vivo with methylation guide small nucleolar rnas[J]. Methods, 2001, 23(3):276-286.
[36]	Brameier M, Herwig A, Reinhardt R, et al. Human box c/d snornas with mirna like functions: Expanding the range of regulatory rnas[J]. Nucleic Acids Res, 2011, 39(2):675-686.
[37]	Michel CI, Holley CL, Scruggs BS, et al. Small nucleolar rnas u32a, u33, and u35a are critical mediators of metabolic stress[J]. Cell Metab, 2011, 14(1):33-44.
[38]	Huang C, Shi J, Guo Y, et al. A snorna modulates mrna 3' end processing and regulates the expression of a subset of mrnas[J]. Nucleic Acids Res, 2017, 45(15):8647-8660.
[39]	Schubert T, Langst G. Changes in higher order structures of chromatin by rnp complexes[J]. RNA Biol, 2013, 10(2):175-179.
[40]	Deogharia M, Majumder M. Guide snornas: Drivers or passengers in human disease?[J]. Biology (Basel), 2018, 8(1):1.
[41]	Abel Y, Rederstorff M. Snornas and the emerging class of sdrnas: Multifaceted players in oncogenesis[J]. Biochimie, 2019, 164:17-21.
[42]	Siprashvili Z, Webster DE, Johnston D, et al. The noncoding rnas snord50a and snord50b bind k-ras and are recurrently deleted in human cancer[J]. Nat Genet, 2016, 48(1):53-58.
[43]	Nogueira Jorge NA, Wajnberg G, Ferreira CG, et al. Snorna and pirna expression levels modified by tobacco use in women with lung adenocarcinoma[J]. PLoS One, 2017, 12(8):e0183410.
[44]	Wang K, Wang S, Zhang Y, et al. SNORD88C guided 2'-O-methylation of 28S rRNA regulates SCD1 translation to inhibit autophagy and promote growth and metastasis in non-small cell lung cancer[J]. Cell Death Differ, 2023, 30(2):341-355.
[45]	Chu L, Su MY, Maggi LB, et al. Multiple myeloma-associated chromosomal translocation activates orphan snorna aca11 to suppress oxidative stress[J]. J Clin Invest, 2012, 122(8):2793-2806.
[46]	Cao P, Yang A, Wang R, et al. Germline duplication of snora18l5 increases risk for hbv-related hepatocellular carcinoma by altering localization of ribosomal proteins and decreasing levels of p53[J]. Gastroenterology, 2018, 155(2):542-556.
[47]	Langhendries JL, Nicolas E, Doumont G, et al. The human box c/d snornas u3 and u8 are required for pre-rrna processing and tumorigenesis[J]. Oncotarget, 2016, 7(37):59519-59534.
[48]	Chen L, Han L, Wei J, et al. Snord76, a box c/d snorna, acts as a tumor suppressor in glioblastoma[J]. Sci Rep, 2015, 5:8588.
[49]	Xu B, Ye MH, Lv SG, et al. Snord47, a box c/d snorna, suppresses tumorigenesis in glioblastoma[J]. Oncotarget, 2017, 8(27):43953-43966.
[50]	Dong XY, Rodriguez C, Guo P, et al. Snorna u50 is a candidate tumor-suppressor gene at 6q14.3 with a mutation associated with clinically significant prostate cancer[J]. Hum Mol Genet, 2008, 17(7):1031-1042.
[51]	Liao J, Yu L, Mei Y, et al. Small nucleolar rna signatures as biomarkers for non-small-cell lung cancer[J]. Mol Cancer, 2010, 9:198.
[52]	Cui L, Nakano K, Obchoei S, et al. Small nucleolar noncoding rna snora23, up-regulated in human pancreatic ductal adenocarcinoma, regulates expression of spectrin repeat-containing nuclear envelope 2 to promote growth and metastasis of xenograft tumors in mice[J]. Gastroenterology, 2017, 153(1):292-306.e2.
[53]	Yuan S, Wu Y, Wang Y, et al. An oncolytic adenovirus expressing snord44 and gas5 exhibits antitumor effect in colorectal cancer cells[J]. Hum Gene Ther, 2017, 28(8):690-700.
[54]	Sun Y, Chen E, Li Y, et al. H/aca box small nucleolar rna 7b acts as an oncogene and a potential prognostic biomarker in breast cancer[J]. Cancer Cell Int, 2019, 19:125.
[55]	Gee HE, Buffa FM, Camps C, et al. The small-nucleolar rnas commonly used for microrna normalisation correlate with tumour pathology and prognosis[J]. Br J Cancer, 2011, 104(7):1168-1177.
[56]	Mei YP, Liao JP, Shen J, et al. Small nucleolar rna 42 acts as an oncogene in lung tumorigenesis[J]. Oncogene, 2012, 31(22):2794-804.
[57]	Okugawa Y, Toiyama Y, Toden S, et al. Clinical significance of SNORA42 as an oncogene and a prognostic biomarker in colorectal cancer[J]. Gut, 2017, 66(1):107-117.
[58]	Yoshida K, Toden S, Weng W, et al. Snora21 - an oncogenic small nucleolar rna, with a prognostic biomarker potential in human colorectal cancer[J]. EBioMedicine, 2017, 22:68-77.
[59]	Williams GT, Farzaneh F. Are snornas and snorna host genes new players in cancer? [J]. Nat Rev Cancer, 2012, 12(2):84-88.
[60]	Li T, Huang M, Sun N, et al. Tumorigenesis of basal muscle invasive bladder cancer was mediated by pten protein degradation resulting from snhg1 upregulation[J]. J Exp Clin Cancer Res, 2024, 43(1):50.
[61]	Wang M, Guo C, Wang L, Luo G, et al. Long noncoding rna gas5 promotes bladder cancer cells apoptosis through inhibiting ezh2 transcription[J]. Cell Death Dis, 2018, 9(2):238.
[62]	Chen D, Guo Y, Chen Y, et al. Lncrna growth arrest-specific transcript 5 targets mir-21 gene and regulates bladder cancer cell proliferation and apoptosis through pten[J]. Cancer Med, 2020, 9(8):2846-2858.
[63]	Liu Z, Wang W, Jiang J, et al. Downregulation of gas5 promotes bladder cancer cell proliferation, partly by regulating cdk6[J]. PLoS One, 2013, 8(9):e73991.
[64]	Zhang H, Guo Y, Song Y, et al. Long noncoding rna gas5 inhibits malignant proliferation and chemotherapy resistance to doxorubicin in bladder transitional cell carcinoma[J]. Cancer Chemother Pharmacol, 2017, 79(1):49-55.
[65]	Xie J, Ni J, Shi H, et al. Lncrna snhg3 enhances bmi1 mrna stability by binding and regulating c-myc: Implications for the carcinogenic role of snhg3 in bladder cancer[J]. Cancer Med, 2023, 12(5):5718-5735.
[66]	Dai G, Huang C, Yang J, et al. Lncrna snhg3 promotes bladder cancer proliferation and metastasis through mir-515-5p/gins2 axis[J]. J Cell Mol Med, 2020, 24(16):9231-9243.
[67]	Zhou Y, Tian B, Tang J, et al. Snhg7: A novel vital oncogenic lncrna in human cancers[J]. Biomed Pharmacother, 2020, 124:109921.
[68]	Zhao Q, Gao S, Du Q, et al. Long non-coding rna snhg20 promotes bladder cancer via activating the wnt/beta-catenin signalling pathway[J]. Int J Mol Med, 2018, 42(5):2839-2848.
[69]	Wang W, Chen S, Song X, et al. Elk1/lncrna-snhg7/mir-2682-5p feedback loop enhances bladder cancer cell growth[J]. Life Sci, 2020, 262:118386.
[70]	Ping Q, Shi Y, Yang M, et al. Lncrna dancr regulates lymphatic metastasis of bladder cancer via the mir-335/vegf-c axis[J]. Transl Androl Urol, 2021, 10(4):1743-1753.
[71]	Zhan Y, Chen Z, Li Y, et al. Long non-coding rna dancr promotes malignant phenotypes of bladder cancer cells by modulating the mir-149/msi2 axis as a cerna[J]. J Exp Clin Cancer Res, 2018, 37(1):273.
[72]	Li YH, Hu YQ, Wang SC, et al. Lncrna snhg5: A new budding star in human cancers[J]. Gene, 2020, 749:144724.
[73]	Wang C, Tao W, Ni S, et al. Upregulation of lncrna snorna host gene 6 regulates nuak family snf1-like kinase-1 expression by competitively binding microrna-125b and interacting with snail1/2 in bladder cancer[J]. J Cell Biochem, 2019, 120(1):357-367.
[74]	Ma Z, Xue S, Zeng B, et al. Lncrna snhg5 is associated with poor prognosis of bladder cancer and promotes bladder cancer cell proliferation through targeting p27[J]. Oncol Lett, 2018, 15(2):1924-1930.
[75]	Jiang B, Hailong S, Yuan J, et al. Identification of oncogenic long noncoding rna snhg12 and duxap8 in human bladder cancer through a comprehensive profiling analysis[J]. Biomed Pharmacother, 2018, 108:500-507.
[76]	Li J, Wang AS, Wang S, et al. Lncsnhg14 promotes the development and progression of bladder cancer by targeting mirna-150-5p[J]. Eur Rev Med Pharmacol Sci, 2019, 23(3):1022-1029.
[77]	Wang H, Feng Y, Zheng X, et al. The diagnostic and therapeutic role of snorna and lincrna in bladder cancer[J]. Cancers (Basel), 2023, 15(4):1007.
[78]	Hu Y, Ma Z, He Y, et al. Lncrna-snhg1 contributes to gastric cancer cell proliferation by regulating dnmt1[J]. Biochem Biophys Res Commun, 2017, 491(4):926-931.
[79]	Liu Y, Yang Y, Li L, et al. Lncrna snhg1 enhances cell proliferation, migration, and invasion in cervical cancer[J]. Biochem Cell Biol, 2018, 96(1):38-43.
[80]	Du Q, Chen J. Snhg1 promotes proliferation, migration and invasion of bladder cancer cells via the pi3k/akt signaling pathway[J]. Exp Ther Med, 2020, 20(5):110.
[81]	Min J, Ma J, Wang Q, et al. Long non-coding rna snhg1 promotes bladder cancer progression by upregulating ezh2 and repressing klf2 transcription[J]. Clinics (Sao Paulo), 2022, 77:100081.
[82]	Feng R, Li Z, Wang X, et al. Silenced lncrna snhg14 restrains the biological behaviors of bladder cancer cells via regulating microrna-211-3p/esm1 axis[J]. Cancer Cell Int, 2021, 21(1):67.
[83]	Mokhtar A, Kong C, Zhang Z, et al. Down-regulation lncrna-snhg15 contributes to proliferation and invasion of bladder cancer cells[J]. BMC Urol, 2021, 21(1):83.
[84]	Chen W, Jiang T, Mao H, et al. Snhg16 regulates invasion and migration of bladder cancer through induction of epithelial-to-mesenchymal transition[J]. Hum Cell, 2020, 33(3):737-749.
[85]	Cao X, Xu J, Yue D. Lncrna-snhg16 predicts poor prognosis and promotes tumor proliferation through epigenetically silencing p21 in bladder cancer[J]. Cancer Gene Ther, 2018, 25(1-2):10-17.
[86]	Ke M, Sun N, Lin Z, et al. Snhg18 inhibits bladder cancer cell proliferation by increasing p21 transcription through destabilizing c-myc protein[J]. Cancer Cell Int, 2023, 23(1):48.
[87]	Chamorro-Petronacci C, Perez-Sayans M, Padin-Iruegas ME, et al. Differential expression of snornas in oral squamous cell carcinomas: New potential diagnostic markers[J]. J Enzyme Inhib Med Chem, 2018, 33(1):424-427.
[88]	Umu SU, Langseth H, Bucher-Johannessen C, et al. A comprehensive profile of circulating rnas in human serum[J]. RNA Biol, 2018, 15(2):242-250.
[89]	Cao R, Ma B, Yuan L, et al. Small nucleolar rnas signature (snors) identified clinical outcome and prognosis of bladder cancer (blca)[J]. Cancer Cell Int, 2020, 20:299.
[90]	He RQ, Huang ZG, Zhai GQ, et al. Small nucleolar rnas (snornas)-based risk score classifier predicts overall survival in bladder carcinoma[J]. Med Sci Monit, 2020, 26:e926273.
[91]	Lu Q, Wang J, Tao Y, et al. Small cajal body-specific rna12 promotes carcinogenesis through modulating extracellular matrix signaling in bladder cancer[J]. Cancers (Basel), 2024, 16(3):483.

Please choose a citation manager

Content to export