RPL39L is an example of a recently evolved ribosomal protein paralog that shows highly specific tissue expression patterns and is upregulated in ESCs and HCC tumors

RNA Biology

Volumn 11, Issue 1, 2014, Pages 33-41

  Wong, Queenie Wing Lei ^a   Li, Jia ^b   Ng, Sheng Rong ^a   Lim, Seng Gee ^c   Yang, Henry ^b   Vardy, Leah A ^a,d  

^a INSTITUTE OF MEDICAL BIOLOGY   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c Dept Medicine Endocrinol Diabet   (Singapore)

^d NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

Hepatocellular carcinoma; Ribosomal protein; Ribosomal protein paralogs; RPL39L

Indexed keywords

ALPHA FETOPROTEIN; RIBOSOME PROTEIN;

ADULT; AGED; ALPHA FETOPROTEIN BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CANCER CELL CULTURE; CANCER GRADING; CANCER GROWTH; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYONIC STEM CELL; EUKARYOTE; FEMALE; GENE EXPRESSION; HUMAN; LIVER CELL CARCINOMA; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; MOUSE; NONHUMAN; PARALOGY; PROTEIN EXPRESSION; TISSUE SPECIFICITY; TUMOR INVASION; UPREGULATION;

HEPATOCELLULAR CARCINOMA; RIBOSOMAL PROTEIN; RIBOSOMAL PROTEIN PARALOGS; RPL39L;

AGED; ALPHA-FETOPROTEINS; ANIMALS; CARCINOMA, HEPATOCELLULAR; CELL LINE; CONSERVED SEQUENCE; EMBRYONIC STEM CELLS; EVOLUTION, MOLECULAR; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, NEOPLASTIC; HEP G2 CELLS; HUMANS; LIVER NEOPLASMS; MALE; MICE; MIDDLE AGED; NEOPLASM GRADING; ORGAN SPECIFICITY; PHYLOGENY; RIBOSOMAL PROTEINS;

EID: 84894434971     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.27427     Document Type: Article

References (34)

1. Komili S, Farny NG, Roth FP, Silver PA. Functional specificity among ribosomal proteins regulates gene expression. Cell 2007; 131:557-71; PMID:17981122; http://dx.doi.org/10.1016/j.cell.2007.08.037
2. Gilbert WV. Functional specialization of ribosomes? Trends Biochem Sci 2011; 36:127-32; PMID:21242088; http://dx.doi.org/10.1016/j.tibs.2010.12.002
3. Kondrashov N, Pusic A, Stumpf CR, Shimizu K, Hsieh AC, Xue S, Ishijima J, Shiroishi T, Barna M. Ribosome-mediated specificity in Hox mRNA translation and vertebrate tissue patterning. Cell 2011; 145:383-97; PMID:21529712; http://dx.doi.org/10.1016/j.cell.2011.03.028
4. Xue S, Barna M. Specialized ribosomes: a new frontier in gene regulation and organismal biology. Nat Rev Mol Cell Biol 2012; 13:355-69; PMID:22617470; http://dx.doi.org/10.1038/nrm3359
5. Ben-Shem A, Jenner L, Yusupova G, Yusupov M. Crystal structure of the eukaryotic ribosome. Science 2010; 330:1203-9; PMID:21109664; http://dx.doi.org/10.1126/science.1194294
6. Klinge S, Voigts-Hoffmann F, Leibundgut M, Ban N. Atomic structures of the eukaryotic ribosome. Trends Biochem Sci 2012; 37:189-98; PMID:22436288; http://dx.doi.org/10.1016/j.tibs.2012.02.007
7. Warner JR, McIntosh KB. How common are extraribosomal functions of ribosomal proteins? Mol Cell 2009; 34:3-11; PMID:19362532; http://dx.doi.org/10. 1016/j.molcel.2009.03.006
8. Marygold SJ, Roote J, Reuter G, Lambertsson A, Ashburner M, Millburn GH, Harrison PM, Yu Z, Kenmochi N, Kaufman TC, et al. The ribosomal protein genes and Minute loci of Drosophila melanogaster. Genome Biol 2007; 8:R216; PMID:17927810; http://dx.doi.org/10.1186/gb-2007-8-10-r216
9. Teng T, Thomas G, Mercer CA. Growth control and ribosomopathies. Curr Opin Genet Dev 2013; 23:63-71; PMID:23490481; http://dx.doi.org/10.1016/j.gde. 2013.02.001
10. Boria I, Garelli E, Gazda HT, Aspesi A, Quarello P, Pavesi E, Ferrante D, Meerpohl JJ, Kartal M, Da Costa L, et al. The ribosomal basis of Diamond-Blackfan Anemia: mutation and database update. Hum Mutat 2010; 31:1269-79; PMID:20960466; http://dx.doi.org/10.1002/humu.21383
11. Horos R, Ijspeert H, Pospisilova D, Sendtner R, Andrieu-Soler C, Taskesen E, Nieradka A, Cmejla R, Sendtner M, Touw IP, et al. Ribosomal deficiencies in Diamond-Blackfan anemia impair translation of transcripts essential for differentiation of murine and human erythroblasts. Blood 2012; 119:262-72; PMID:22058113; http://dx.doi.org/10.1182/blood-2011-06-358200
12. Shenoy N, Kessel R, Bhagat TD, Bhattacharyya S, Yu Y, McMahon C, Verma A. Alterations in the ribosomal machinery in cancer and hematologic disorders. J Hematol Oncol 2012; 5:32; PMID:22709827; http://dx.doi.org/10.1186/1756-8722-5- 32
13. Bee A, Brewer D, Beesley C, Dodson A, Forootan S, Dickinson T, Gerard P, Lane B, Yao S, Cooper CS, et al. siRNA knockdown of ribosomal protein gene RPL19 abrogates the aggressive phenotype of human prostate cancer. PLoS One 2011; 6:e22672; PMID:21799931; http://dx.doi.org/10.1371/journal.pone.0022672
14. MacInnes AW, Amsterdam A, Whittaker CA, Hopkins N, Lees JA. Loss of p53 synthesis in zebrafish tumors with ribosomal protein gene mutations. Proc Natl Acad Sci U S A 2008; 105:10408-13; PMID:18641120; http://dx.doi.org/10.1073/ pnas.0805036105
15. Takagi M, Absalon MJ, McLure KG, Kastan MB. Regulation of p53 translation and induction after DNA damage by ribosomal protein L26 and nucleolin. Cell 2005; 123:49-63; PMID:16213212; http://dx.doi.org/10.1016/j.cell.2005.07.034
16. Zhang Y, Duc AC, Rao S, Sun XL, Bilbee AN, Rhodes M, Li Q, Kappes DJ, Rhodes J, Wiest DL. Control of hematopoietic stem cell emergence by antagonistic functions of ribosomal protein paralogs. Dev Cell 2013; 24:411-25; PMID:23449473; http://dx.doi.org/10.1016/j.devcel.2013.01.018
17. Lopes AM, Miguel RN, Sargent CA, Ellis PJ, Amorim A, Affara NA. The human RPS4 paralogue on Yq11.223 encodes a structurally conserved ribosomal protein and is preferentially expressed during spermatogenesis. BMC Mol Biol 2010; 11:33; PMID:20459660; http://dx.doi.org/10.1186/1471-2199-11-33
18. Sugihara Y, Sadohara E, Yonezawa K, Kugo M, Oshima K, Matsuda T, Nadano D. Identification and expression of an autosomal paralogue of ribosomal protein S4, X-linked, in mice: potential involvement of testis-specific ribosomal proteins in translation and spermatogenesis. Gene 2013; 521:91-9; PMID:23500592; http://dx.doi.org/10.1016/j.gene.2013.02.040
19. Sugihara Y, Honda H, Iida T, Morinaga T, Hino S, Okajima T, Matsuda T, Nadano D. Proteomic analysis of rodent ribosomes revealed heterogeneity including ribosomal proteins L10-like, L22-like 1, and L39-like. J Proteome Res 2010; 9:1351-66; PMID:20063902; http://dx.doi.org/10.1021/pr9008964
20. Yoshihama M, Uechi T, Asakawa S, Kawasaki K, Kato S, Higa S, Maeda N, Minoshima S, Tanaka T, Shimizu N, et al. The human ribosomal protein genes: sequencing and comparative analysis of 73 genes. Genome Res 2002; 12:379-90; PMID:11875025; http://dx.doi.org/10.1101/gr.214202
21. Uechi T, Maeda N, Tanaka T, Kenmochi N. Functional second genes generated by retrotransposition of the X-linked ribosomal protein genes. Nucleic Acids Res 2002; 30:5369-75; PMID:12490704; http://dx.doi.org/10.1093/nar/gkf696
22. Bortoluzzi S, d'Alessi F, Romualdi C, Danieli GA. Differential expression of genes coding for ribosomal proteins in different human tissues. Bioinformatics 2001; 17:1152-7; PMID:11751223; http://dx.doi.org/10.1093/ bioinformatics/17.12.1152
23. Ishii K, Washio T, Uechi T, Yoshihama M, Kenmochi N, Tomita M. Characteristics and clustering of human ribosomal protein genes. BMC Genomics 2006; 7:37; PMID:16504170; http://dx.doi.org/10.1186/1471-2164-7-37
24. Nadano D, Notsu T, Matsuda T, Sato T. A human gene encoding a protein homologous to ribosomal protein L39 is normally expressed in the testis and derepressed in multiple cancer cells. Biochim Biophys Acta 2002; 1577:430-6; PMID:12359333; http://dx.doi.org/10.1016/S0167-4781(02)00445-1
25. Ben-Shem A, Garreau de Loubresse N, Melnikov S, Jenner L, Yusupova G, Yusupov M. The structure of the eukaryotic ribosome at 3.0 Å resolution. Science 2011; 334:1524-9; PMID:22096102; http://dx.doi.org/10.1126/science. 1212642
26. Petrone PM, Snow CD, Lucent D, Pande VS. Side-chain recognition and gating in the ribosome exit tunnel. Proc Natl Acad Sci U S A 2008; 105:16549-54; PMID:18946046; http://dx.doi.org/10.1073/pnas.0801795105
27. Woolhead CA, McCormick PJ, Johnson AE. Nascent membrane and secretory proteins differ in FRET-detected folding far inside the ribosome and in their exposure to ribosomal proteins. Cell 2004; 116:725-36; PMID:15006354; http://dx.doi.org/10.1016/S0092-8674(04)00169-2
28. Schnell DJ, Hebert DN. Protein translocons: multifunctional mediators of protein translocation across membranes. Cell 2003; 112:491-505; PMID:12600313; http://dx.doi.org/10.1016/S0092-8674(03)00110-7
29. Hirsch CA, Hiatt HH. Turnover of liver ribosomes in fed and in fasted rats. J Biol Chem 1966; 241:5936-40; PMID:5954370
30. Dresios J, Derkatch IL, Liebman SW, Synetos D. Yeast ribosomal protein L24 affects the kinetics of protein synthesis and ribosomal protein L39 improves translational accuracy, while mutants lacking both remain viable. Biochemistry 2000; 39:7236-44; PMID:10852723; http://dx.doi.org/10.1021/bi9925266
31. Caldarola S, De Stefano MC, Amaldi F, Loreni F. Synthesis and function of ribosomal proteins - fading models and new perspectives. FEBS J 2009; 276:3199-210; PMID:19438715; http://dx.doi.org/10.1111/j.1742-4658.2009.07036.x
32. He H, Sun Y. Ribosomal protein S27L is a direct p53 target that regulates apoptosis. Oncogene 2007; 26:2707-16; PMID:17057733; http://dx.doi.org/10.1038/ sj.onc.1210073
33. Zhang D, Zhao T, Ang HS, Chong P, Saiki R, Igarashi K, Yang H, Vardy LA. AMD1 is essential for ESC self-renewal and is translationally down-regulated on differentiation to neural precursor cells. Genes Dev 2012; 26:461-73; PMID:22391449; http://dx.doi.org/10.1101/gad.182998.111
34. Ho HK, Pok S, Streit S, Ruhe JE, Hart S, Lim KS, Loo HL, Aung MO, Lim SG, Ullrich A. Fibroblast growth factor receptor 4 regulates proliferation, anti-apoptosis and alpha-fetoprotein secretion during hepatocellular carcinoma progression and represents a potential target for therapeutic intervention. J Hepatol 2009; 50:118-27; PMID:19008009; http://dx.doi.org/10.1016/j.jhep.2008. 08.015