Emerging Roles of Nucleolar and Ribosomal Proteins in Cancer, Development, and Aging

Overview

Journal Cell Mol Life Sci

Publisher Springer

Specialty Biology

Date 2015 Jul 25

PMID 26206377

Citations 28

Authors

Hitomi Takada

Akira Kurisaki

Affiliations

Soon will be listed here.

Abstract

Changes in nucleolar morphology and function are tightly associated with cellular activity, such as growth, proliferation, and cell cycle progression. Historically, these relationships have been extensively examined in cancer cells, which frequently exhibit large nucleoli and increased ribosome biogenesis. Recent findings indicate that alteration of nucleolar activity is a key regulator of development and aging. In this review, we have provided evidences that the nucleolus is not just a housekeeping factor but is actively involved in the regulation of cell proliferation, differentiation, and senescence both in vitro and in vivo. In addition, we have discussed how alteration of nucleolar function and nucleolar proteins induces specific physiological effects rather than widespread effects.

Citing Articles

Construction and validation of transcription‑factor‑based prognostic signature for TACE non‑response and characterization of tumor microenvironment infiltration in hepatocellular carcinoma.

Shi J, Wei X, Jiang F, Zhu J, Shen J, Sun Y Oncol Lett. 2024; 29(1):42.

PMID: 39554534 PMC: 11565272. DOI: 10.3892/ol.2024.14788.

CASIN exerts anti-aging effects through RPL4 on the skin of naturally aging mice.

Zhang Y, Wang X, Huang J, Zhang X, Bu L, Zhang Y Aging Cell. 2024; 23(12):e14333.

PMID: 39289787 PMC: 11634736. DOI: 10.1111/acel.14333.

Multi-Omics Analysis Reveals Translational Landscapes and Regulations in Mouse and Human Oocyte Aging.

Huang J, Chen P, Jia L, Li T, Yang X, Liang Q Adv Sci (Weinh). 2023; 10(26):e2301538.

PMID: 37401155 PMC: 10502832. DOI: 10.1002/advs.202301538.

Specific Gain and Loss of Co-Expression Modules in Long-Lived Individuals Indicate a Role of circRNAs in Human Longevity.

Ge M, Jiang J, Yang L, Yang X, He Y, Li G Genes (Basel). 2022; 13(5).

PMID: 35627134 PMC: 9140997. DOI: 10.3390/genes13050749.

Matrix Metalloprotease-7 Mediates Nucleolar Assembly and Intra-nucleolar Cleaving p53 in Gefitinib-Resistant Cancer Stem Cells.

Yu W, Wu E, Li Y, Hou H, Yu S, Huang P iScience. 2020; 23(10):101600.

PMID: 33089100 PMC: 7559243. DOI: 10.1016/j.isci.2020.101600.

References

Hannan K, Sanij E, Hein N, Hannan R, Pearson R . Signaling to the ribosome in cancer--It is more than just mTORC1. IUBMB Life. 2011; 63(2):79-85. DOI: 10.1002/iub.428. View

Derenzini M, Trere D, Pession A, Montanaro L, Sirri V, Ochs R . Nucleolar function and size in cancer cells. Am J Pathol. 1998; 152(5):1291-7. PMC: 1858570. View

Hulbert A, Pamplona R, Buffenstein R, Buttemer W . Life and death: metabolic rate, membrane composition, and life span of animals. Physiol Rev. 2007; 87(4):1175-213. DOI: 10.1152/physrev.00047.2006. View

Smith J, Brachmann C, Pillus L, Boeke J . Distribution of a limited Sir2 protein pool regulates the strength of yeast rDNA silencing and is modulated by Sir4p. Genetics. 1998; 149(3):1205-19. PMC: 1460222. DOI: 10.1093/genetics/149.3.1205. View

Voit R, Schafer K, Grummt I . Mechanism of repression of RNA polymerase I transcription by the retinoblastoma protein. Mol Cell Biol. 1997; 17(8):4230-7. PMC: 232276. DOI: 10.1128/MCB.17.8.4230. View

Yang L, Song T, Chen L, Kabra N, Zheng H, Koomen J . Regulation of SirT1-nucleomethylin binding by rRNA coordinates ribosome biogenesis with nutrient availability. Mol Cell Biol. 2013; 33(19):3835-48. PMC: 3811878. DOI: 10.1128/MCB.00476-13. View

Yang A, Shi G, Zhou C, Lu R, Li H, Sun L . Nucleolin maintains embryonic stem cell self-renewal by suppression of p53 protein-dependent pathway. J Biol Chem. 2011; 286(50):43370-82. PMC: 3234871. DOI: 10.1074/jbc.M111.225185. View

Dai M, Lu H . Crosstalk between c-Myc and ribosome in ribosomal biogenesis and cancer. J Cell Biochem. 2008; 105(3):670-7. PMC: 2569974. DOI: 10.1002/jcb.21895. View

Matheu A, Maraver A, Klatt P, Flores I, Garcia-Cao I, Borras C . Delayed ageing through damage protection by the Arf/p53 pathway. Nature. 2007; 448(7151):375-9. DOI: 10.1038/nature05949. View

10.

Fichelson P, Moch C, Ivanovitch K, Martin C, Sidor C, Lepesant J . Live-imaging of single stem cells within their niche reveals that a U3snoRNP component segregates asymmetrically and is required for self-renewal in Drosophila. Nat Cell Biol. 2009; 11(6):685-93. DOI: 10.1038/ncb1874. View

11.

Gomez-Roman N, Grandori C, Eisenman R, White R . Direct activation of RNA polymerase III transcription by c-Myc. Nature. 2003; 421(6920):290-4. DOI: 10.1038/nature01327. View

12.

Komili S, Farny N, Roth F, Silver P . Functional specificity among ribosomal proteins regulates gene expression. Cell. 2007; 131(3):557-71. PMC: 2443060. DOI: 10.1016/j.cell.2007.08.037. View

13.

Ali S, Zaidi S, Dacwag C, Salma N, Young D, Shakoori A . Phenotypic transcription factors epigenetically mediate cell growth control. Proc Natl Acad Sci U S A. 2008; 105(18):6632-7. PMC: 2373311. DOI: 10.1073/pnas.0800970105. View

14.

Tang Y, Wade J . Sexually dimorphic expression of the genes encoding ribosomal proteins L17 and L37 in the song control nuclei of juvenile zebra finches. Brain Res. 2006; 1126(1):102-8. PMC: 2878125. DOI: 10.1016/j.brainres.2006.08.002. View

15.

Grewal S, Evans J, Edgar B . Drosophila TIF-IA is required for ribosome synthesis and cell growth and is regulated by the TOR pathway. J Cell Biol. 2007; 179(6):1105-13. PMC: 2140016. DOI: 10.1083/jcb.200709044. View

16.

Hein N, Hannan K, George A, Sanij E, Hannan R . The nucleolus: an emerging target for cancer therapy. Trends Mol Med. 2013; 19(11):643-54. DOI: 10.1016/j.molmed.2013.07.005. View

17.

James A, Cindass Jr R, Mayer D, Terhoeve S, Mumphrey C, DiMario P . Nucleolar stress in Drosophila melanogaster: RNAi-mediated depletion of Nopp140. Nucleus. 2013; 4(2):123-33. PMC: 3621744. DOI: 10.4161/nucl.23944. View

18.

Wang Q, Yang C, Zhou J, Wang X, Wu M, Liu Z . Cloning and characterization of full-length human ribosomal protein L15 cDNA which was overexpressed in esophageal cancer. Gene. 2001; 263(1-2):205-9. DOI: 10.1016/s0378-1119(00)00570-9. View

19.

Kondo T, Minamino N, Nagamura-Inoue T, Matsumoto M, Taniguchi T, Tanaka N . Identification and characterization of nucleophosmin/B23/numatrin which binds the anti-oncogenic transcription factor IRF-1 and manifests oncogenic activity. Oncogene. 1997; 15(11):1275-81. DOI: 10.1038/sj.onc.1201286. View

20.

Zhang Y, Duc A, Rao S, Sun X, Bilbee A, Rhodes M . Control of hematopoietic stem cell emergence by antagonistic functions of ribosomal protein paralogs. Dev Cell. 2013; 24(4):411-25. PMC: 3586312. DOI: 10.1016/j.devcel.2013.01.018. View