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SUMO pathway is required for ribosome biogenesis

  • Hong-Yeoul, Ryu (BK21 FOUR KNU Creative BioResearch Group, School of Life Sciences, College of National Sciences, Kyungpook National University)
  • Received : 2022.07.25
  • Accepted : 2022.09.26
  • Published : 2022.11.30

Abstract

Ribosomes, acting as the cellular factories for protein production, are essential for all living organisms. Ribosomes are composed of both proteins and RNAs and are established through the coordination of several steps, including transcription, maturation of ribosomal RNA (rRNA), and assembly of ribosomal proteins. In particular, diverse factors required for ribosome biogenesis, such as transcription factors, small nucleolar RNA (snoRNA)-associated proteins, and assembly factors, are tightly regulated by various post-translational modifications. Among these modifications, small ubiquitin-related modifier (SUMO) targets lots of proteins required for gene expression of ribosomal proteins, rRNA, and snoRNAs, rRNA processing, and ribosome assembly. The tight control of SUMOylation affects functions and locations of substrates. This review summarizes current studies and recent progress of SUMOylation-mediated regulation of ribosome biogenesis.

Keywords

Acknowledgement

This study was supported by a National Research Foundation of Korea (NRF) grant funded by the South Korean government (MSIT) (nos. 2020R1C1C1009367 and 2020R1A4A1018280) and Korean Environment Industry & Technology Institute (KEITI) through Core Technology Development Project for Environmental Diseases Prevention and Management funded by Korean Ministry of Environment (MOE) (no. 2022003310001).

References

  1. Thomson E, Ferreira-Cerca S and Hurt E (2013) Eukaryotic ribosome biogenesis at a glance. J Cell Sci 126, 4815-4821 https://doi.org/10.1242/jcs.111948
  2. Bassler J and Hurt E (2019) Eukaryotic ribosome assembly. Annu Rev Biochem 88, 281-306 https://doi.org/10.1146/annurev-biochem-013118-110817
  3. Kressler D, Hurt E and Bassler J (2010) Driving ribosome assembly. Biochim Biophys Acta 1803, 673-683 https://doi.org/10.1016/j.bbamcr.2009.10.009
  4. Henras AK, Soudet J, Gerus M et al (2008) The post-transcriptional steps of eukaryotic ribosome biogenesis. Cell Mol Life Sci 65, 2334-2359
  5. Diwakarla C, Hannan K, Hein N and Yip D (2017) Advanced pancreatic ductal adenocarcinoma - complexities of treatment and emerging therapeutic options. World J Gastroenterol 23, 2276-2285 https://doi.org/10.3748/wjg.v23.i13.2276
  6. Nosrati N, Kapoor NR and Kumar V (2014) Combinatorial action of transcription factors orchestrates cell cycle-dependent expression of the ribosomal protein genes and ribosome biogenesis. FEBS J 281, 2339-2352 https://doi.org/10.1111/febs.12786
  7. Martin DE, Soulard A and Hall MN (2004) TOR regulates ribosomal protein gene expression via PKA and the forkhead transcription factor FHL1. Cell 119, 969-979 https://doi.org/10.1016/j.cell.2004.11.047
  8. Neumansilberberg FS, Bhattacharya S and Broach JR (1995) Nutrient availability and the ras/cyclic amp path-way both induce expression of ribosomal-protein genes in saccharomyces-cerevisiae but by different mechanisms. Mol Cell Biol 15, 3187-3196
  9. Simsek D and Barna M (2017) An emerging role for the ribosome as a nexus for post-translational modifications. Curr Opin Cell Biol 45, 92-101 https://doi.org/10.1016/j.ceb.2017.02.010
  10. Flotho A and Melchior F (2013) Sumoylation: a regulatory protein modification in health and disease. Annu Rev Biochem 82, 357-385 https://doi.org/10.1146/annurev-biochem-061909-093311
  11. Ryu HY (2021) SUMO: a novel target for anti-coronavirus therapy. Pathog Glob Health 115, 292-299 https://doi.org/10.1080/20477724.2021.1906562
  12. Ryu HY, Ahn SH and Hochstrasser M (2020) SUMO and cellular adaptive mechanisms. Exp Mol Med 52, 931-939 https://doi.org/10.1038/s12276-020-0457-2
  13. Chaikam V and Karlson DT (2010) Response and transcriptional regulation of rice SUMOylation system during development and stress conditions. BMB Rep 43, 103-109 https://doi.org/10.5483/BMBRep.2010.43.2.103
  14. Ryu HY, Wilson NR, Mehta S, Hwang SS and Hochstrasser M (2016) Loss of the SUMO protease Ulp2 triggers a specific multichromosome aneuploidy. Genes Dev 30, 1881-1894 https://doi.org/10.1101/gad.282194.116
  15. Huang WC, Ko TP, Li SS and Wang AH (2004) Crystal structures of the human SUMO-2 protein at 1.6 A and 1.2 A resolution: implication on the functional differences of SUMO proteins. Eur J Biochem 271, 4114-4122 https://doi.org/10.1111/j.1432-1033.2004.04349.x
  16. Liang YC, Lee CC, Yao YL, Lai CC, Schmitz ML and Yang WM (2016) SUMO5, a novel poly-SUMO isoform, regulates PML nuclear bodies. Sci Rep 6, 26509 https://doi.org/10.1038/srep26509
  17. Muller S, Hoege C, Pyrowolakis G and Jentsch S (2001) SUMO, ubiquitin's mysterious cousin. Nat Rev Mol Cell Biol 2, 202-210 https://doi.org/10.1038/35056591
  18. Hickey CM, Wilson NR and Hochstrasser M (2012) Function and regulation of SUMO proteases. Nat Rev Mol Cell Biol 13, 755-766 https://doi.org/10.1038/nrm3478
  19. Owerbach D, McKay EM, Yeh ETH, Gabbay KH and Bohren KM (2005) A proline-90 residue unique to SUMO-4 prevents maturation and sumoylation. Biochem Biophys Res Commun 337, 517-520 https://doi.org/10.1016/j.bbrc.2005.09.090
  20. Hendriks IA and Vertegaal AC (2016) A comprehensive compilation of SUMO proteomics. Nat Rev Mol Cell Biol 17, 581-595 https://doi.org/10.1038/nrm.2016.81
  21. Song J, Durrin LK, Wilkinson TA, Krontiris TG and Chen YA (2004) Identification of a SUMO-binding motif that recognizes SUMO-modified proteins. Proc Natl Acad Sci U S A 101, 14373-14378 https://doi.org/10.1073/pnas.0403498101
  22. Wohlschlegel JA, Johnson ES, Reed SI and Yates JR (2004) Global analysis of protein sumoylation in Saccharomyces cerevisiae. J Biol Chem 279, 45662-45668 https://doi.org/10.1074/jbc.M409203200
  23. Hannich JT, Lewis A, Kroetz MB et al (2005) Defining the SUMO-modified proteome by multiple approaches in Saccharomyces cerevisiae. J Biol Chem 280, 4102-4110 https://doi.org/10.1074/jbc.M413209200
  24. Zhou WD, Ryan JJ and Zhou HL (2004) Global analyses of sumoylated proteins in Saccharomyces cerevisiae - induction of protein sumoylation by cellular stresses. J Biol Chem 279, 32262-32268 https://doi.org/10.1074/jbc.M404173200
  25. Esteras M, Liu IC, Snijders AP, Jarmuz A and Aragon L (2017) Identification of SUMO conjugation sites in the budding yeast proteome. Microb Cell 4, 331-341 https://doi.org/10.15698/mic2017.10.593
  26. Wykoff DD and O'Shea EK (2005) Identification of sumoylated proteins by systematic immunoprecipitation of the budding yeast proteome. Mol Cell Proteomics 4, 73-83 https://doi.org/10.1074/mcp.M400166-MCP200
  27. Mojsa B, Tatham MH, Davidson L, Liczmanska M, Branigan E and Hay RT (2021) Identification of SUMO targets associated with the pluripotent state in human stem cells. Mol Cell Proteomics 20, 100164 https://doi.org/10.1016/j.mcpro.2021.100164
  28. Hendriks IA, D'Souza RC, Yang B, Verlaan-de Vries M, Mann M and Vertegaal AC (2014) Uncovering global SUMOylation signaling networks in a site-specific manner. Nat Struct Mol Biol 21, 927-936 https://doi.org/10.1038/nsmb.2890
  29. Tammsalu T, Matic I, Jaffray EG, Ibrahim AFM, Tatham MH and Hay RT (2014) Proteome-wide identification of SUMO2 modification sites. Sci Signal 7, rs2 https://doi.org/10.1126/scisignal.2005146
  30. Xiao Z, Chang JG, Hendriks IA, Sigurethsson JO, Olsen JV and Vertegaal AC (2015) System-wide analysis of SUMOylation dynamics in response to replication stress reveals novel small ubiquitin-like modified target proteins and acceptor lysines relevant for genome stability. Mol Cell Proteomics 14, 1419-1434
  31. Hendriks IA, Treffers LW, Verlaan-de Vries M, Olsen JV and Vertegaal ACO (2015) SUMO-2 orchestrates chromatin modifiers in response to DNA damage. Cell Rep 10, 1778-1791 https://doi.org/10.1016/j.celrep.2015.02.033
  32. Impens F, Radoshevich L, Cossart P and Ribet D (2014) Mapping of SUMO sites and analysis of SUMOylation changes induced by external stimuli. Proc Natl Acad Sci U S A 111, 12432-12437 https://doi.org/10.1073/pnas.1413825111
  33. Lamoliatte F, Caron D, Durette C et al (2014) Large-scale analysis of lysine SUMOylation by SUMO remnant immunoaffinity profiling. Nat Commun 5, 5409 https://doi.org/10.1038/ncomms6409
  34. Hendriks IA, D'Souza RC, Chang JG, Mann M and Vertegaal AC (2015) System-wide identification of wild-type SUMO-2 conjugation sites. Nat Commun 6, 7289 https://doi.org/10.1038/ncomms8289
  35. Verger A, Perdomo J and Crossley M (2003) Modification with SUMO. A role in transcriptional regulation. EMBO Rep 4, 137-142
  36. Choi J, Ryoo ZY, Cho DH, Lee HS and Ryu HY (2021) Trans-tail regulation-mediated suppression of cryptic transcription. Exp Mol Med 53, 1683-1688 https://doi.org/10.1038/s12276-021-00711-x
  37. Ouyang J and Gill G (2009) SUMO engages multiple corepressors to regulate chromatin structure and transcription. Epigenetics 4, 440-444 https://doi.org/10.4161/epi.4.7.9807
  38. Neyret-Kahn H, Benhamed M, Ye T et al (2013) Sumoylation at chromatin governs coordinated repression of a transcriptional program essential for cell growth and proliferation. Genome Res 23, 1563-1579 https://doi.org/10.1101/gr.154872.113
  39. Peng Y, Wang Z, Wang Z, Yu F, Li J and Wong J (2019) SUMOylation down-regulates rDNA transcription by repressing expression of upstream-binding factor and proto-oncogene c-Myc. J Biol Chem 294, 19155-19166 https://doi.org/10.1074/jbc.RA119.010624
  40. Chymkowitch P, Nguea AP, Aanes H et al (2015) Sumoylation of Rap1 mediates the recruitment of TFIID to promote transcription of ribosomal protein genes. Genome Res 25, 897-906
  41. Ryu HY, Su D, Wilson-Eisele NR, Zhao DJ, LopezGiraldez F and Hochstrasser M (2019) The Ulp2 SUMO protease promotes transcription elongation through regulation of histone sumoylation. Embo J 38, e102003 https://doi.org/10.15252/embj.2019102003
  42. Ryu HY, Lopez-Giraldez F, Knight J et al (2018) Distinct adaptive mechanisms drive recovery from aneuploidy caused by loss of the Ulp2 SUMO protease. Nat Commun 9, 5417 https://doi.org/10.1038/s41467-018-07836-0
  43. Gillies J, Hickey CM, Su D, Wu Z, Peng J and Hochstrasser M (2016) SUMO pathway modulation of regulatory protein binding at the ribosomal DNA locus in Saccharomyces cerevisiae. Genetics 202, 1377-1394 https://doi.org/10.1534/genetics.116.187252
  44. Ryu HY and Hochstrasser M (2021) Histone sumoylation and chromatin dynamics. Nucleic Acids Res 49, 6043-6052 https://doi.org/10.1093/nar/gkab280
  45. Ryu HY, Zhao D, Li J, Su D and Hochstrasser M (2020) Histone sumoylation promotes Set3 histone-deacetylase complex-mediated transcriptional regulation. Nucleic Acids Res 48, 12151-12168 https://doi.org/10.1093/nar/gkaa1093
  46. Watkins NJ and Bohnsack MT (2012) The box C/D and H/ACA snoRNPs: key players in the modification, processing and the dynamic folding of ribosomal RNA. Wiley Interdiscip Rev RNA 3, 397-414 https://doi.org/10.1002/wrna.117
  47. Westman BJ, Verheggen C, Hutten S, Lam YW, Bertrand E and Lamond AI (2010) A proteomic screen for nucleolar SUMO targets shows SUMOylation modulates the function of Nop5/Nop58. Mol Cell 39, 618-631 https://doi.org/10.1016/j.molcel.2010.07.025
  48. Haindl M, Harasim T, Eick D and Muller S (2008) The nucleolar SUMO-specific protease SENP3 reverses SUMO modification of nucleophosmin and is required for rRNA processing. EMBO Rep 9, 273-279 https://doi.org/10.1038/embor.2008.3
  49. Yun C, Wang Y, Mukhopadhyay D et al (2008) Nucleolar protein B23/nucleophosmin regulates the vertebrate SUMO pathway through SENP3 and SENP5 proteases. J Cell Biol 183, 589-595 https://doi.org/10.1083/jcb.200807185
  50. Ryu H, Sun XX, Chen Y et al (2021) The deubiquitinase USP36 promotes snoRNP group SUMOylation and is essential for ribosome biogenesis. EMBO Rep 22, e50684 https://doi.org/10.15252/embr.202050684
  51. Knight JR, Bastide A, Peretti D et al (2016) Cooling-induced SUMOylation of EXOSC10 down-regulates ribosome biogenesis. RNA 22, 623-635 https://doi.org/10.1261/rna.054411.115
  52. Johnson AW, Lund E and Dahlberg J (2002) Nuclear export of ribosomal subunits. Trends Biochem Sci 27, 580-585 https://doi.org/10.1016/S0968-0004(02)02208-9
  53. Finkbeiner E, Haindl M and Muller S (2011) The SUMO system controls nucleolar partitioning of a novel mammalian ribosome biogenesis complex. EMBO J 30, 1067-1078 https://doi.org/10.1038/emboj.2011.33
  54. Castle CD, Cassimere EK and Denicourt C (2012) LAS1L interacts with the mammalian Rix1 complex to regulate ribosome biogenesis. Mol Biol Cell 23, 716-728 https://doi.org/10.1091/mbc.E11-06-0530
  55. Finkbeiner E, Haindl M, Raman N and Muller S (2011) SUMO routes ribosome maturation. Nucleus 2, 527-532 https://doi.org/10.4161/nucl.2.6.17604
  56. El Motiam A, Vidal S, de la Cruz-Herrera CF et al (2019) Interplay between SUMOylation and NEDDylation regulates RPL11 localization and function. FASEB J 33, 643-651 https://doi.org/10.1096/fj.201800341rr
  57. Jang CY, Shin HS, Kim HD, Kim JW, Choi SY and Kim J (2011) Ribosomal protein S3 is stabilized by sumoylation. Biochem Biophys Res Commun 414, 523-527 https://doi.org/10.1016/j.bbrc.2011.09.099
  58. Kearse MG, Ireland JA, Prem SM, Chen AS and Ware VC (2013) RpL22e, but not RpL22e-like-PA, is SUMOylated and localizes to the nucleoplasm of Drosophila meiotic spermatocytes. Nucleus 4, 241-258 https://doi.org/10.4161/nucl.25261
  59. Lin YL, Chung CL, Chen MH, Chen CH and Fang SC (2020) SUMO protease SMT7 modulates ribosomal protein L30 and regulates cell-size checkpoint function. Plant Cell 32, 1285-1307 https://doi.org/10.1105/tpc.19.00301
  60. Panse VG, Kressler D, Pauli A et al (2006) Formation and nuclear export of preribosomes are functionally linked to the small-ubiquitin-related modifier pathway. Traffic 7, 1311-1321 https://doi.org/10.1111/j.1600-0854.2006.00471.x
  61. Venturi G and Montanaro L (2020) How altered ribosome production can cause or contribute to human disease: the spectrum of ribosomopathies. Cells 9, 2300 https://doi.org/10.3390/cells9102300
  62. Park J, Park J, Lee J and Lim C (2021) The trinity of ribosome-associated quality control and stress signaling for proteostasis and neuronal physiology. BMB Rep 54, 439-450 https://doi.org/10.5483/BMBRep.2021.54.9.097
  63. Heiss NS, Knight SW, Vulliamy TJ et al (1998) X-linked dyskeratosis congenita is caused by mutations in a highly conserved gene with putative nucleolar functions. Nat Genet 19, 32-38
  64. Boocock GR, Morrison JA, Popovic M et al (2003) Mutations in SBDS are associated with Shwachman-Diamond syndrome. Nat Genet 33, 97-101 https://doi.org/10.1038/ng1062