Ribosome Biogenesis and Cancer: Insights into NOB1 and PNO1 Mechanisms


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Abstract

:Post-transcriptional modifications (PTMs) are pivotal in the regulation of gene expression, and pseudouridylation is emerging as a critical player. This modification, facilitated by enzymes such as NOB1 (PNO1), is integral to ribosome biogenesis. PNO1, in collaboration with the NIN1/RPN12 binding protein 1 homolog (NOB1), is vital for the maturation of ribosomes, transitioning 20S pre-rRNA into functional 18S rRNA. Recent studies have highlighted PNO1's potential involvement in cancer progression; however, its underlying mechanisms remain unclear. Relentless growth characterizing cancer underscores the burgeoning significance of epitranscriptomic modifications, including pseudouridylation, in oncogenesis. Given PNO1's emerging role, it is imperative to delineate its contribution to cancer development to identify novel therapeutic interventions. This review summarizes the current literature regarding the role of PNO1 in cancer progression and its molecular underpinnings in oncogenesis. Overexpression of PNO1 was associated with unfavorable prognosis and increased tumor malignancy. At the molecular level, PNO1 facilitates cancer progression by modulating mRNA stability, alternative splicing, and translation efficiency. Its role in pseudouridylation of oncogenic and tumor-suppressor transcripts further underscores its significance in cancer biology. Although disruption of ribosome biogenesis is known to precipitate oncogenesis, the precise mechanisms by which these alterations contribute to cancer remain unclear. This review elucidates the intricate process of ribosomal small subunit maturation, highlighting the roles of crucial ribosomal proteins (RPs) and RNA-binding proteins (RBPs) as well as the positioning and function of NOB1 and PNO1 within the 40S subunit. The involvement of these components in the maturation of the small subunit (SSU) and their significance in the context of cancer therapeutics has been thoroughly explored. PNO1's burgeoning significance in oncology makes it a potential target for cancer therapies. Strategies aimed at modulating PNO1-mediated pseudouridylation may provide new avenues for cancer treatment. However, further research is essential to unravel the complete spectrum of PNO1 mechanisms in cancer and harness this knowledge for the development of targeted and more efficacious anticancer therapies.

About the authors

Muthu Ragunath

Department of Bioscience and Biotechnology, Konkuk University

Email: info@benthamscience.net

Aling Shen

Fujian Key Laboratory of Integrative Medicine in Geriatrics, Academy of Integrative Medicine, Fujian University of Traditional Chinese Medicine,

Email: info@benthamscience.net

Lin Wei

Fujian Key Laboratory of Integrative Medicine in Geriatrics, Academy of Integrative Medicine,, Fujian University of Traditional Chinese Medicine

Email: info@benthamscience.net

Jun Peng

Fujian Key Laboratory of Integrative Medicine in Geriatrics, Academy of Integrative Medicine, Fujian University of Traditional Chinese Medicine

Author for correspondence.
Email: info@benthamscience.net

Muthu Thiruvengadam

Department of Applied Bioscience, College of Life and Environmental Science, Konkuk University

Author for correspondence.
Email: info@benthamscience.net

References

  1. Shen A, Chen Y, Liu L, et al. EBF1-mediated upregulation of ribosome assembly factor PNO1 contributes to cancer progression by negatively regulating the p53 signaling pathway. Cancer Res 2019; 79(9): 2257-70. doi: 10.1158/0008-5472.CAN-18-3238 PMID: 30862720
  2. de la Cruz J, Karbstein K, Woolford JL Jr. Functions of ribosomal proteins in assembly of eukaryotic ribosomes in vivo. Annu Rev Biochem 2015; 84(1): 93-129. doi: 10.1146/annurev-biochem-060614-033917 PMID: 25706898
  3. Trerè D, Borzio M, Morabito A, Borzio F, Roncalli M, Derenzini M. Nucleolar hypertrophy correlates with hepatocellular carcinoma development in cirrhosis due to HBV infection. Hepatology 2003; 37(1): 72-8. doi: 10.1053/jhep.2003.50039 PMID: 12500191
  4. Orsolic I, Jurada D, Pullen N, Oren M, Eliopoulos AG, Volarevic S. The relationship between the nucleolus and cancer: Current evidence and emerging paradigms. Semin Cancer Biol 2016; 37-38: 36-50. doi: 10.1016/j.semcancer.2015.12.004 PMID: 26721423
  5. Harold CM, Buhagiar AF, Cheng Y, Baserga SJ. Ribosomal RNA transcription regulation in breast cancer. Genes 2021; 12(4): 502. doi: 10.3390/genes12040502 PMID: 33805424
  6. Pelletier J, Thomas G, Volarević S. Ribosome biogenesis in cancer: New players and therapeutic avenues. Nat Rev Cancer 2018; 18(1): 51-63. doi: 10.1038/nrc.2017.104 PMID: 29192214
  7. Cheng J, Baßler J, Fischer P, et al. Thermophile 90S pre-ribosome structures reveal the reverse order of co-transcriptional 18S rRNA subdomain integration. Mol Cell 2019; 75(6): 1256-1269.e7. doi: 10.1016/j.molcel.2019.06.032 PMID: 31378463
  8. Dragon F, Gallagher JEG, Compagnone-Post PA, et al. A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis. Nature 2002; 417(6892): 967-70. doi: 10.1038/nature00769 PMID: 12068309
  9. Larburu N, Montellese C, O’Donohue MF, Kutay U, Gleizes PE, Plisson-Chastang C. Structure of a human pre-40S particle points to a role for RACK1 in the final steps of 18S rRNA processing. Nucleic Acids Res 2016; 44(17): 8465-78. doi: 10.1093/nar/gkw714 PMID: 27530427
  10. Zorbas C, Nicolas E, Wacheul L, Huvelle E, Heurgué-Hamard V, Lafontaine DLJ. The human 18S rRNA base methyltransferases DIMT1L and WBSCR22-TRMT112 but not rRNA modification are required for ribosome biogenesis. Mol Biol Cell 2015; 26(11): 2080-95. doi: 10.1091/mbc.E15-02-0073 PMID: 25851604
  11. Turowski TW, Lebaron S, Zhang E, et al. Rio1 mediates ATP-dependent final maturation of 40S ribosomal subunits. Nucleic Acids Res 2014; 42(19): 12189-99. doi: 10.1093/nar/gku878 PMID: 25294836
  12. Heuer A, Thomson E, Schmidt C, et al. Cryo-EM structure of a late pre-40S ribosomal subunit from Saccharomyces cerevisiae. eLife 2017; 6: e30189. doi: 10.7554/eLife.30189 PMID: 29155690
  13. Fatica A, Oeffinger M, Dlakić M, Tollervey D. NOB1p is required for cleavage of the 3′ end of 18S rRNA. Mol Cell Biol 2003; 23(5): 1798-807. doi: 10.1128/MCB.23.5.1798-1807.2003 PMID: 12588997
  14. Woolls HA, Lamanna AC, Karbstein K. Roles of Dim2 in ribosome assembly. J Biol Chem 2011; 286(4): 2578-86. doi: 10.1074/jbc.M110.191494 PMID: 21075849
  15. Ameismeier M, Cheng J, Berninghausen O, Beckmann R. Visualizing late states of human 40S ribosomal subunit maturation. Nature 2018; 558(7709): 249-53. doi: 10.1038/s41586-018-0193-0 PMID: 29875412
  16. Zhou GJ, Zhang Y, Wang J, et al. Cloning and characterization of a novel human RNA binding protein gene PNO1. DNA Seq 2004; 15(3): 219-24. doi: 10.1080/10425170410001702159 PMID: 15497447
  17. Wong AG, McBurney KL, Thompson KJ, Stickney LM, Mackie GA. S1 and KH domains of polynucleotide phosphorylase determine the efficiency of RNA binding and autoregulation. J Bacteriol 2013; 195(9): 2021-31. doi: 10.1128/JB.00062-13 PMID: 23457244
  18. Yadav M, Singh RS, Hogan D, et al. The KH domain facilitates the substrate specificity and unwinding processivity of DDX43 helicase. J Biol Chem 2021; 296: 100085. doi: 10.1074/jbc.RA120.015824 PMID: 33199368
  19. Ameismeier M, Zemp I, van den Heuvel J, et al. Structural basis for the final steps of human 40S ribosome maturation. Nature 2020; 587(7835): 683-7. doi: 10.1038/s41586-020-2929-x PMID: 33208940
  20. van den Heuvel J, Ashiono C, Gillet LC, et al. Processing of the ribosomal ubiquitin-like fusion protein FUBI-eS30/FAU is required for 40S maturation and depends on USP36. eLife 2021; 10: e70560. doi: 10.7554/eLife.70560 PMID: 34318747
  21. Lamanna AC, Karbstein K. NOB1 binds the single-stranded cleavage site D at the 3′-end of 18S rRNA with its PIN domain. Proc Natl Acad Sci USA 2009; 106(34): 14259-64. doi: 10.1073/pnas.0905403106 PMID: 19706509
  22. Dai H, Zhang S, Ma R, Pan L. Celecoxib inhibits hepatocellular carcinoma cell growth and migration by targeting PNO1. Med Sci Monit 2019; 25: 7351-60. doi: 10.12659/MSM.919218 PMID: 31568401
  23. Nait Slimane S, Marcel V, Fenouil T, et al. Ribosome biogenesis alterations in colorectal cancer. Cells 2020; 9(11): 2361. doi: 10.3390/cells9112361 PMID: 33120992
  24. Plassart L, Shayan R, Montellese C, et al. The final step of 40S ribosomal subunit maturation is controlled by a dual key lock. eLife 2021; 10: e61254. doi: 10.7554/eLife.61254 PMID: 33908345
  25. Li J, Liu L, Chen Y, et al. Ribosome assembly factor PNO1 is associated with progression and promotes tumorigenesis in triple-negative breast cancer. Oncol Rep 2022; 47(6): 108. doi: 10.3892/or.2022.8319 PMID: 35445733
  26. Stepanchick A, Zhi H, Cavanaugh AH, Rothblum K, Schneider DA, Rothblum LI. DNA binding by the ribosomal DNA transcription factor rrn3 is essential for ribosomal DNA transcription. J Biol Chem 2013; 288(13): 9135-44. doi: 10.1074/jbc.M112.444265 PMID: 23393135
  27. Sharma S, Marchand V, Motorin Y, Lafontaine DLJ. Identification of sites of 2′-O-methylation vulnerability in human ribosomal RNAs by systematic mapping. Sci Rep 2017; 7(1): 11490. doi: 10.1038/s41598-017-09734-9 PMID: 28904332
  28. Cerqueira AV, Lemos B. Ribosomal DNA and the nucleolus as keystones in nuclear architecture, organization, and function. Trends Genet 2019; 35(10): 710-23. doi: 10.1016/j.tig.2019.07.011 PMID: 31447250
  29. Montanaro L, Treré D, Derenzini M. Nucleolus, ribosomes, and cancer. Am J Pathol 2008; 173(2): 301-10. doi: 10.2353/ajpath.2008.070752 PMID: 18583314
  30. Narasimha A, Vasavi B, Harendra Kumar ML. Significance of nuclear morphometry in benign and malignant breast aspirates. Int J Appl Basic Med Res 2013; 3(1): 22-6. doi: 10.4103/2229-516X.112237 PMID: 23776836
  31. Penzo M, Montanaro L, Treré D, Derenzini M. The ribosome biogenesis-cancer connection. Cells 2019; 8(1): 55. doi: 10.3390/cells8010055 PMID: 30650663
  32. Derenzini M, Montanaro L, Treré D. What the nucleolus says to a tumour pathologist. Histopathology 2009; 54(6): 753-62. doi: 10.1111/j.1365-2559.2008.03168.x PMID: 19178588
  33. Stępiński D. The nucleolus, an ally, and an enemy of cancer cells. Histochem Cell Biol 2018; 150(6): 607-29. doi: 10.1007/s00418-018-1706-5 PMID: 30105457
  34. Prakash V, Carson BB, Feenstra JM, et al. Ribosome biogenesis during cell cycle arrest fuels EMT in development and disease. Nat Commun 2019; 10(1): 2110. doi: 10.1038/s41467-019-10100-8 PMID: 31068593
  35. Derenzini M, Montanaro L, Chillà A, et al. Key role of the achievement of an appropriate ribosomal RNA complement for G1-S phase transition in H4-II-E-C3 rat hepatoma cells. J Cell Physiol 2005; 202(2): 483-91. doi: 10.1002/jcp.20144 PMID: 15389582
  36. Coussens LM, Werb Z. Inflammation and cancer. Nature 2002; 420(6917): 860-7. doi: 10.1038/nature01322 PMID: 12490959
  37. Brighenti E, Calabrese C, Liguori G, et al. Interleukin 6 downregulates p53 expression and activity by stimulating ribosome biogenesis: A new pathway connecting inflammation to cancer. Oncogene 2014; 33(35): 4396-406. doi: 10.1038/onc.2014.1 PMID: 24531714
  38. Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell 2010; 140(6): 883-99. doi: 10.1016/j.cell.2010.01.025 PMID: 20303878
  39. Narla A, Ebert BL. Ribosomopathies: Human disorders of ribosome dysfunction. Blood 2010; 115(16): 3196-205. doi: 10.1182/blood-2009-10-178129 PMID: 20194897
  40. Zhang C, Comai L, Johnson DL. Expression of PTEN in PTEN-deficient cells represses Pol I transcription by disrupting the SL1 complex. Mol Cell Biol 2005; 25: 6899-911. doi: 10.1128/MCB.25.16.6899-6911.2005 PMID: 16055704
  41. Goudarzi KM, Lindström MS. Role of ribosomal protein mutations in tumor development (Review). Int J Oncol 2016; 48(4): 1313-24. doi: 10.3892/ijo.2016.3387 PMID: 26892688
  42. Gregory B, Rahman N, Bommakanti A, et al. The small and large ribosomal subunits depend on each other for stability and accumulation. Life Sci Alliance 2019; 2(2): e201800150. doi: 10.26508/lsa.201800150 PMID: 30837296
  43. Naiyer S, Singh SS, Kaur D, et al. Transcriptomic analysis of ribosome biogenesis and pre-rRNA processing during growth stress in Entamoeba histolytica. Exp Parasitol 2022; 239: 108308. doi: 10.1016/j.exppara.2022.108308 PMID: 35718007
  44. Catalanotto C, Barbato C, Cogoni C, Benelli D. The RNA-binding function of ribosomal proteins and ribosome biogenesis factors in human health and disease. Biomedicines 2023; 11(11): 2969. doi: 10.3390/biomedicines11112969 PMID: 38001969
  45. Schneider DA. RNA polymerase I activity is regulated at multiple steps in the transcription cycle: Recent insights into factors that influence transcription elongation. Gene 2012; 493(2): 176-84. doi: 10.1016/j.gene.2011.08.006 PMID: 21893173
  46. Chen J, Zhang L, Ye K. Functional regions in the 5′ external transcribed spacer of yeast pre-rRNA. RNA 2020; 26(7): 866-77. doi: 10.1261/rna.074807.120 PMID: 32213618
  47. Lin J, Lu J, Feng Y, Sun M, Ye K. An RNA-binding complex involved in ribosome biogenesis contains a protein with homology to tRNA CCA-adding enzyme. PLoS Biol 2013; 11(10): e1001669. doi: 10.1371/journal.pbio.1001669 PMID: 24130456
  48. Barandun J, Hunziker M, Klinge S. Assembly and structure of the SSU processome - a nucleolar precursor of the small ribosomal subunit. Curr Opin Struct Biol 2018; 49: 85-93. doi: 10.1016/j.sbi.2018.01.008 PMID: 29414516
  49. Hunziker M, Barandun J, Petfalski E, et al. UtpA and UtpB chaperone nascent pre-ribosomal RNA and U3 snoRNA to initiate eukaryotic ribosome assembly. Nat Commun 2016; 7(1): 12090. doi: 10.1038/ncomms12090 PMID: 27354316
  50. Marmier-Gourrier N, Cléry A, Schlotter F, Senty-Ségault V, Branlant C. A second base pair interaction between U3 small nucleolar RNA and the 5′-ETS region is required for early cleavage of the yeast pre-ribosomal RNA. Nucleic Acids Res 2011; 39(22): 9731-45. doi: 10.1093/nar/gkr675 PMID: 21890904
  51. Chaker-Margot M, Hunziker M, Barandun J, Dill BD, Klinge S. Stage-specific assembly events of the 6-MDa small-subunit processome initiate eukaryotic ribosome biogenesis. Nat Struct Mol Biol 2015; 22(11): 920-3. doi: 10.1038/nsmb.3111 PMID: 26479197
  52. Phipps KR, Charette JM, Baserga SJ. The small subunit processome in ribosome biogenesis-progress and prospects. Wiley Interdiscip Rev RNA 2011; 2(1): 1-21. doi: 10.1002/wrna.57 PMID: 21318072
  53. Barandun J, Chaker-Margot M, Hunziker M, Molloy KR, Chait BT, Klinge S. The complete structure of the small-subunit processome. Nat Struct Mol Biol 2017; 24(11): 944-53. doi: 10.1038/nsmb.3472 PMID: 28945246
  54. Linnemann J, Pöll G, Jakob S, et al. Impact of two neighbouring ribosomal protein clusters on biogenesis factor binding and assembly of yeast late small ribosomal subunit precursors. PLoS One 2019; 14(1): e0203415. doi: 10.1371/journal.pone.0203415 PMID: 30653518
  55. Bleichert F, Granneman S, Osheim YN, Beyer AL, Baserga SJ. The PINc domain protein Utp24, a putative nuclease, is required for the early cleavage steps in 18S rRNA maturation. Proc Natl Acad Sci USA 2006; 103(25): 9464-9. doi: 10.1073/pnas.0603673103 PMID: 16769905
  56. Koš M, Tollervey D. Yeast pre-rRNA processing and modification occur cotranscriptionally. Mol Cell 2010; 37(6): 809-20. doi: 10.1016/j.molcel.2010.02.024 PMID: 20347423
  57. Schäfer T, Strauss D, Petfalski E, Tollervey D, Hurt E. The path from nucleolar 90S to cytoplasmic 40S pre-ribosomes. EMBO J 2003; 22(6): 1370-80. doi: 10.1093/emboj/cdg121 PMID: 12628929
  58. Schäfer T, Maco B, Petfalski E, et al. Hrr25-dependent phosphorylation state regulates organization of the pre-40S subunit. Nature 2006; 441(7093): 651-5. doi: 10.1038/nature04840 PMID: 16738661
  59. Johnson MC, Ghalei H, Doxtader KA, Karbstein K, Stroupe ME. Structural heterogeneity in pre-40S ribosomes. Structure 2017; 25(2): 329-40. doi: 10.1016/j.str.2016.12.011 PMID: 28111018
  60. Cheng J, Lau B, Thoms M, et al. The nucleoplasmic phase of pre-40S formation prior to nuclear export. Nucleic Acids Res 2022; 50(20): 11924-37. doi: 10.1093/nar/gkac961 PMID: 36321656
  61. Johnson AG, Lapointe CP, Wang J, et al. RACK1 on and off the ribosome. RNA 2019; 25(7): 881-95. doi: 10.1261/rna.071217.119 PMID: 31023766
  62. Woolford JL Jr, Baserga SJ. Ribosome biogenesis in the yeast Saccharomyces cerevisiae. Genetics 2013; 195(3): 643-81. doi: 10.1534/genetics.113.153197 PMID: 24190922
  63. Aspden JL, Eyre-Walker YC, Phillips RJ, et al. Extensive translation of small open reading frames revealed by poly-ribo-seq. eLife 2014; 3: e03528. doi: 10.7554/eLife.03528 PMID: 25144939
  64. Haskell D, Zinovyeva A. KH domain containing RNA-binding proteins coordinate with microRNAs to regulate Caenorhabditis elegans development. G3 (Bethesda) 2021; 11(2): jkab013. doi: 10.1093/g3journal/jkab013 PMID: 33585875
  65. Granneman S, Petfalski E, Swiatkowska A, Tollervey D. Cracking pre-40S ribosomal subunit structure by systematic analyses of RNA–protein cross-linking. EMBO J 2010; 29(12): 2026-36. doi: 10.1038/emboj.2010.86 PMID: 20453830
  66. Landry-Voyer AM, Mir Hassani Z, Avino M, Bachand F. Ribosomal protein uS5 and friends: Protein–protein interactions involved in ribosome assembly and beyond. Biomolecules 2023; 13(5): 853. doi: 10.3390/biom13050853 PMID: 37238722
  67. Konikkat S, Woolford JL Jr. Principles of 60S ribosomal subunit assembly emerging from recent studies in yeast. Biochem J 2017; 474(2): 195-214. doi: 10.1042/BCJ20160516 PMID: 28062837
  68. Ghalei H, Schaub FX, Doherty JR, et al. Hrr25/CK1δ-directed release of LTV1 from pre-40S ribosomes is necessary for ribosome assembly and cell growth. J Cell Biol 2015; 208(6): 745-59. doi: 10.1083/jcb.201409056 PMID: 25778921
  69. Ferreira-Cerca S, Kiburu I, Thomson E, LaRonde N, Hurt E. Dominant Rio1 kinase/ATPase catalytic mutant induces trapping of late pre-40S biogenesis factors in 80S-like ribosomes. Nucleic Acids Res 2014; 42(13): 8635-47. doi: 10.1093/nar/gku542 PMID: 24948609
  70. Parker MD, Collins JC, Korona B, Ghalei H, Karbstein K. A kinase-dependent checkpoint prevents escape of immature ribosomes into the translating pool. PLoS Biol 2019; 17(12): e3000329. doi: 10.1371/journal.pbio.3000329 PMID: 31834877
  71. Weisser M, Ban N. Extensions, extra factors, and extreme complexity: Ribosomal structures provide insights into eukaryotic translation. Cold Spring Harb Perspect Biol 2019; 11(9): a032367. doi: 10.1101/cshperspect.a032367 PMID: 31481454
  72. McCaughan UM, Jayachandran U, Shchepachev V, et al. Pre-40S ribosome biogenesis factor TSR1 is an inactive structural mimic of translational GTPases. Nat Commun 2016; 7(1): 11789. doi: 10.1038/ncomms11789 PMID: 27250689
  73. Lebaron S, Schneider C, van Nues RW, et al. Proofreading of pre-40S ribosome maturation by a translation initiation factor and 60S subunits. Nat Struct Mol Biol 2012; 19(8): 744-53. doi: 10.1038/nsmb.2308 PMID: 22751017
  74. García-Gómez JJ, Fernández-Pevida A, Lebaron S, et al. Final pre-40S maturation depends on the functional integrity of the 60S subunit ribosomal protein L3. PLoS Genet 2014; 10(3): e1004205. doi: 10.1371/journal.pgen.1004205 PMID: 24603549
  75. Rolfe MD, Rice CJ, Lucchini S, et al. Lag phase is a distinct growth phase that prepares bacteria for exponential growth and involves transient metal accumulation. J Bacteriol 2012; 194(3): 686-701. doi: 10.1128/JB.06112-11 PMID: 22139505
  76. Vanrobays E, Leplus A, Osheim YN, Beyer AL, Wacheul L, Lafontaine DLJ. TOR regulates the subcellular distribution of Dim2, a KH domain protein required for cotranscriptional ribosome assembly and pre-40S ribosome export. RNA 2008; 14(10): 2061-73. doi: 10.1261/rna.1176708 PMID: 18755838
  77. Zhao D, Yang J, Yang L. Insights for oxidative stress and mTOR signaling in myocardial ischemia/reperfusion injury under diabetes. Oxid Med Cell Longev 2017; 2017: 1-12. doi: 10.1155/2017/6437467 PMID: 28298952
  78. Wang X, Wu T, Hu Y, et al. PNO1 tissue-specific expression and its functions related to the immune responses and proteasome activities. PLoS One 2012; 7(9): e46093. doi: 10.1371/journal.pone.0046093 PMID: 23029399
  79. Verkhratsky A, Parpura V. Neurological and psychiatric disorders as a neuroglial failure. Period Biol 2014; 116(2): 115-24. PMID: 25544781
  80. Obeng EA, Carlson LM, Gutman DM, Harrington WJ Jr, Lee KP, Boise LH. Proteasome inhibitors induce a terminal unfolded protein response in multiple myeloma cells. Blood 2006; 107(12): 4907-16. doi: 10.1182/blood-2005-08-3531 PMID: 16507771
  81. Tschochner H, Hurt E. Pre-ribosomes on the road from the nucleolus to the cytoplasm. Trends Cell Biol 2003; 13(5): 255-63. doi: 10.1016/S0962-8924(03)00054-0 PMID: 12742169
  82. Rössler I, Weigl S, Fernández-Fernández J, et al. The C-terminal tail of ribosomal protein Rps15 is engaged in cytoplasmic pre-40S maturation. RNA Biol 2022; 19(1): 560-74. doi: 10.1080/15476286.2022.2064073 PMID: 35438042
  83. Pertschy B, Schneider C, Gnädig M, Schäfer T, Tollervey D, Hurt E. RNA helicase Prp43 and its co-factor Pfa1 promote 20 to 18S rRNA processing catalyzed by the endonuclease NOB1. J Biol Chem 2009; 284(50): 35079-91. doi: 10.1074/jbc.M109.040774 PMID: 19801658
  84. Campbell MG, Karbstein K. Protein-protein interactions within late pre-40S ribosomes. PLoS One 2011; 6(1): e16194. doi: 10.1371/journal.pone.0016194 PMID: 21283762
  85. Koizumi S, Hamazaki J, Murata S. Transcriptional regulation of the 26S proteasome by Nrf1. Proc Jpn Acad, Ser B, Phys Biol Sci 2018; 94(8): 325-36. doi: 10.2183/pjab.94.021 PMID: 30305478
  86. Catalanotto C, Cogoni C, Zardo G. MicroRNA in control of gene expression: An overview of nuclear functions. Int J Mol Sci 2016; 17(10): 1712. doi: 10.3390/ijms17101712 PMID: 27754357
  87. Akbari Moqadam F, Lange-Turenhout EAM, Ariës IM, Pieters R, den Boer ML. MiR-125b, miR-100 and miR-99a co-regulate vincristine resistance in childhood acute lymphoblastic leukemia. Leuk Res 2013; 37(10): 1315-21. doi: 10.1016/j.leukres.2013.06.027 PMID: 23915977
  88. Lin CKE, Kaptein JS, Sheikh J. Differential expression of microRNAs and their possible roles in patients with chronic idiopathic urticaria and active hives. Allergy Rhinol (Providence) 2017; 8(2): ar.2017.8.0199. doi: 10.2500/ar.2017.8.0199 PMID: 28583230
  89. Dai H, Hou K, Cai Z, Zhou Q, Zhu S. Low-level miR-646 in colorectal cancer inhibits cell proliferation and migration by targeting NOB1 expression. Oncol Lett 2017; 14(6): 6708-14. doi: 10.3892/ol.2017.7032 PMID: 29391877
  90. Ke W, Lu Z, Zhao X. NOB1: A potential biomarker or target in cancer. Curr Drug Targets 2019; 20(10): 1081-9. doi: 10.2174/1389450120666190308145346 PMID: 30854959
  91. Dong S, Xue S, Sun Y, et al. MicroRNA-363-3p downregulation in papillary thyroid cancer inhibits tumor progression by targeting NOB1. J Investig Med 2021; 69(1): 66-74. doi: 10.1136/jim-2020-001562 PMID: 33077486
  92. Elhamamsy AR, Metge BJ, Alsheikh HA, Shevde LA, Samant RS. Ribosome biogenesis: A central player in cancer metastasis and therapeutic resistance. Cancer Res 2022; 82(13): 2344-53. doi: 10.1158/0008-5472.CAN-21-4087 PMID: 35303060
  93. Jiao L, Liu Y, Yu XY, et al. Ribosome biogenesis in disease: New players and therapeutic targets. Signal Transduct Target Ther 2023; 8(1): 15. doi: 10.1038/s41392-022-01285-4 PMID: 36617563
  94. Rawla P, Sunkara T, Barsouk A. Epidemiology of colorectal cancer: Incidence, mortality, survival, and risk factors. Prz Gastroenterol 2019; 14(2): 89-103. doi: 10.5114/pg.2018.81072 PMID: 31616522
  95. Li X, Han YR, Xuefeng X, et al. Lentivirus-mediated short hairpin RNA interference of CENPK inhibits growth of colorectal cancer cells with overexpression of Cullin 4A. World J Gastroenterol 2022; 28(37): 5420-43. doi: 10.3748/wjg.v28.i37.5420 PMID: 36312839
  96. Liu L, Chen Y, Lin X, et al. Upregulation of SNTB1 correlates with poor prognosis and promotes cell growth by negative regulating PKN2 in colorectal cancer. Cancer Cell Int 2021; 21(1): 547. PMID: 34663329
  97. Saito A, Kamikawa Y, Ito T, et al. p53-independent tumor suppression by cell-cycle arrest via CREB/ATF transcription factor OASIS. Cell Rep 2023; 42(5): 112479. doi: 10.1016/j.celrep.2023.112479 PMID: 37178686
  98. Bang S, Kaur S, Kurokawa M. Regulation of the p53 family proteins by the ubiquitin proteasomal pathway. Int J Mol Sci 2019; 21(1): 261. doi: 10.3390/ijms21010261 PMID: 31905981

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