Skip to main content
SpringerLink
Log in

The Implication of mRNA Degradation Disorders on Human DISease: Focus on DIS3 and DIS3-Like Enzymes

  • Chapter
  • First Online:
The mRNA Metabolism in Human Disease

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1157))

Abstract

RNA degradation is considered a critical posttranscriptional regulatory checkpoint, maintaining the correct functioning of organisms. When a specific RNA transcript is no longer required in the cell, it is signaled for degradation through a number of highly regulated steps. Ribonucleases (or simply RNases) are key enzymes involved in the control of RNA stability. These enzymes can perform the RNA degradation alone or cooperate with other proteins in RNA degradation complexes. Important findings over the last years have shed light into eukaryotic RNA degradation by members of the RNase II/RNB family of enzymes. DIS3 enzyme belongs to this family and represents one of the catalytic subunits of the multiprotein complex exosome. This RNase has a diverse range of functions, mainly within nuclear RNA metabolism. Humans encode two other DIS3-like enzymes: DIS3L (DIS3L1) and DIS3L2. DIS3L1 also acts in association with the exosome but is strictly cytoplasmic. In contrast, DIS3L2 acts independently of the exosome and shows a distinctive preference for uridylated RNAs. These enzymes have been shown to be involved in important cellular processes, such as mitotic control, and associated with human disorders like cancer. This review shows how the impairment of function of each of these enzymes is implicated in human disease.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 119.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 159.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 159.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Archer SK et al (2015) Probing the closed-loop model of mRNA translation in living cells. RNA Biol 12(3):248–254

    Article  PubMed  PubMed Central  Google Scholar 

  2. Wells SE et al (1998) Circularization of mRNA by eukaryotic translation initiation factors. Mol Cell 2(1):135–140

    Article  CAS  PubMed  Google Scholar 

  3. Darnell JE Jr (2013) Reflections on the history of pre-mRNA processing and highlights of current knowledge: a unified picture. RNA 19(4):443–460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Kahvejian A et al (2005) Mammalian poly(A)-binding protein is a eukaryotic translation initiation factor, which acts via multiple mechanisms. Genes Dev 19(1):104–113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Mangus DA, Evans MC, Jacobson A (2003) Poly(A)-binding proteins: multifunctional scaffolds for the post-transcriptional control of gene expression. Genome Biol 4(7):223

    Article  PubMed  PubMed Central  Google Scholar 

  6. Barreau C, Paillard L, Osborne HB (2005) AU-rich elements and associated factors: are there unifying principles? Nucleic Acids Res 33(22):7138–7150

    Article  CAS  PubMed  Google Scholar 

  7. Chen CY, Shyu AB (1995) AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem Sci 20(11):465–470

    Article  CAS  PubMed  Google Scholar 

  8. Eulalio A et al (2009) Deadenylation is a widespread effect of miRNA regulation. RNA 15(1):21–32

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Wu L, Fan J, Belasco JG (2006) MicroRNAs direct rapid deadenylation of mRNA. Proc Natl Acad Sci U S A 103(11):4034–4039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Abdelmohsen K, Gorospe M (2010) Posttranscriptional regulation of cancer traits by HuR. Wiley Interdiscip Rev RNA 1(2):214–229

    Article  CAS  PubMed  Google Scholar 

  11. Murray EL, Schoenberg DR (2007) A+U-rich instability elements differentially activate 5′-3′ and 3′-5′ mRNA decay. Mol Cell Biol 27(8):2791–2799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Peng SS et al (1998) RNA stabilization by the AU-rich element binding protein, HuR, an ELAV protein. EMBO J 17(12):3461–3470

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Huntzinger E, Izaurralde E (2011) Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat Rev Genet 12(2):99–110

    Article  CAS  PubMed  Google Scholar 

  14. Oliveto S et al (2017) Role of microRNAs in translation regulation and cancer. World J Biol Chem 8(1):45–56

    Article  PubMed  PubMed Central  Google Scholar 

  15. Valinezhad Orang A, Safaralizadeh R, Kazemzadeh-Bavili M (2014) Mechanisms of miRNA-mediated gene regulation from common downregulation to mRNA-specific upregulation. Int J Genomics 2014:970607

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Eberle AB et al (2009) SMG6 promotes endonucleolytic cleavage of nonsense mRNA in human cells. Nat Struct Mol Biol 16(1):49–55

    Article  CAS  PubMed  Google Scholar 

  17. Huntzinger E et al (2008) SMG6 is the catalytic endonuclease that cleaves mRNAs containing nonsense codons in metazoan. RNA 14(12):2609–2617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Pavlopoulou A et al (2013) A comprehensive phylogenetic analysis of deadenylases. Evol Bioinformatics Online 9:491–497

    CAS  Google Scholar 

  19. Uchida N, Hoshino S, Katada T (2004) Identification of a human cytoplasmic poly(A) nuclease complex stimulated by poly(A)-binding protein. J Biol Chem 279(2):1383–1391

    Article  CAS  PubMed  Google Scholar 

  20. Wahle E, Winkler GS (2013) RNA decay machines: deadenylation by the Ccr4-not and Pan2-Pan3 complexes. Biochim Biophys Acta 1829(6–7):561–570

    Article  CAS  PubMed  Google Scholar 

  21. Wolf J, Passmore LA (2014) mRNA deadenylation by Pan2-Pan3. Biochem Soc Trans 42(1):184–187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Chen CY, Shyu AB (2011) Mechanisms of deadenylation-dependent decay. Wiley Interdiscip Rev RNA 2(2):167–183

    Article  CAS  PubMed  Google Scholar 

  23. Doidge R et al (2012) Deadenylation of cytoplasmic mRNA by the mammalian Ccr4-Not complex. Biochem Soc Trans 40(4):896–901

    Article  CAS  PubMed  Google Scholar 

  24. Lau NC et al (2009) Human Ccr4-Not complexes contain variable deadenylase subunits. Biochem J 422(3):443–453

    Article  CAS  PubMed  Google Scholar 

  25. Temme C, Simonelig M, Wahle E (2014) Deadenylation of mRNA by the CCR4-NOT complex in Drosophila: molecular and developmental aspects. Front Genet 5:143

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Yamashita A et al (2005) Concerted action of poly(A) nucleases and decapping enzyme in mammalian mRNA turnover. Nat Struct Mol Biol 12(12):1054–1063

    Article  CAS  PubMed  Google Scholar 

  27. Coller J, Parker R (2004) Eukaryotic mRNA decapping. Annu Rev Biochem 73:861–890

    Article  CAS  PubMed  Google Scholar 

  28. Franks TM, Lykke-Andersen J (2008) The control of mRNA decapping and P-body formation. Mol Cell 32(5):605–615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Li Y, Kiledjian M (2010) Regulation of mRNA decapping. Wiley Interdiscip Rev RNA 1(2):253–265

    Article  PubMed  CAS  Google Scholar 

  30. Sharif H, Conti E (2013) Architecture of the Lsm1-7-Pat1 complex: a conserved assembly in eukaryotic mRNA turnover. Cell Rep 5(2):283–291

    Article  CAS  PubMed  Google Scholar 

  31. Tharun S (2009) Lsm1-7-Pat1 complex: a link between 3′ and 5′-ends in mRNA decay? RNA Biol 6(3):228–232

    Article  CAS  PubMed  Google Scholar 

  32. Braun JE et al (2012) A direct interaction between DCP1 and XRN1 couples mRNA decapping to 5′ exonucleolytic degradation. Nat Struct Mol Biol 19(12):1324–1331

    Article  CAS  PubMed  Google Scholar 

  33. Nissan T et al (2010) Decapping activators in Saccharomyces cerevisiae act by multiple mechanisms. Mol Cell 39(5):773–783

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Halbach F et al (2013) The yeast ski complex: crystal structure and RNA channeling to the exosome complex. Cell 154(4):814–826

    Article  CAS  PubMed  Google Scholar 

  35. Chen N et al (2005) Crystal structures of human DcpS in ligand-free and m7GDP-bound forms suggest a dynamic mechanism for scavenger mRNA decapping. J Mol Biol 347(4):707–718

    Article  CAS  PubMed  Google Scholar 

  36. Liu H et al (2002) The scavenger mRNA decapping enzyme DcpS is a member of the HIT family of pyrophosphatases. EMBO J 21(17):4699–4708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Milac AL, Bojarska E, Wypijewska del Nogal A (2014) Decapping Scavenger (DcpS) enzyme: advances in its structure, activity and roles in the cap-dependent mRNA metabolism. Biochim Biophys Acta 1839(6):452–462

    Article  CAS  PubMed  Google Scholar 

  38. Shen V et al (2008) DcpS scavenger decapping enzyme can modulate pre-mRNA splicing. RNA 14(6):1132–1142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Bonneau F et al (2009) The yeast exosome functions as a macromolecular cage to channel RNA substrates for degradation. Cell 139(3):547–559

    Article  CAS  PubMed  Google Scholar 

  40. Lebreton A et al (2008) Endonucleolytic RNA cleavage by a eukaryotic exosome. Nature 456(7224):993–996

    Article  CAS  PubMed  Google Scholar 

  41. Mamolen M, Smith A, Andrulis ED (2010) Drosophila melanogaster Dis3 N-terminal domains are required for ribonuclease activities, nuclear localization and exosome interactions. Nucleic Acids Res 38(16):5507–5517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Schaeffer D et al (2009) The exosome contains domains with specific endoribonuclease, exoribonuclease and cytoplasmic mRNA decay activities. Nat Struct Mol Biol 16(1):56–62

    Article  CAS  PubMed  Google Scholar 

  43. Schneider C et al (2009) The N-terminal PIN domain of the exosome subunit Rrp44 harbors endonuclease activity and tethers Rrp44 to the yeast core exosome. Nucleic Acids Res 37(4):1127–1140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Lubas M et al (2013) Exonuclease hDIS3L2 specifies an exosome-independent 3′-5′ degradation pathway of human cytoplasmic mRNA. EMBO J 32(13):1855–1868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Malecki M et al (2013) The exoribonuclease Dis3L2 defines a novel eukaryotic RNA degradation pathway. EMBO J 32(13):1842–1854

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Arribas-Layton M et al (2013) Structural and functional control of the eukaryotic mRNA decapping machinery. Biochim Biophys Acta 1829(6–7):580–589

    Article  CAS  PubMed  Google Scholar 

  47. Chang H et al (2014) TAIL-seq: genome-wide determination of poly(A) tail length and 3′ end modifications. Mol Cell 53(6):1044–1052

    Article  CAS  PubMed  Google Scholar 

  48. Arraiano CM et al (2010) The critical role of RNA processing and degradation in the control of gene expression. FEMS Microbiol Rev 34(5):883–923

    Article  CAS  PubMed  Google Scholar 

  49. Barbas A et al (2008) New insights into the mechanism of RNA degradation by ribonuclease II: identification of the residue responsible for setting the RNase II end product. J Biol Chem 283(19):13070–13076

    Article  CAS  PubMed  Google Scholar 

  50. Barbas A et al (2009) Determination of key residues for catalysis and RNA cleavage specificity: one mutation turns RNase II into a “SUPER-ENZYME”. J Biol Chem 284(31):20486–20498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Frazao C et al (2006) Unravelling the dynamics of RNA degradation by ribonuclease II and its RNA-bound complex. Nature 443(7107):110–114

    Article  CAS  PubMed  Google Scholar 

  52. Robinson SR et al (2018) DIS3 isoforms vary in their endoribonuclease activity and are differentially expressed within haematological cancers. Biochem J 475(12):2091–2105

    Article  CAS  PubMed  Google Scholar 

  53. Viegas SC et al (2015) Surprises in the 3′-end: ‘U’ can decide too! FEBS J 282(18):3489–3499

    Article  CAS  PubMed  Google Scholar 

  54. Matos RG et al (2014) The importance of proteins of the RNase II/RNB-family in pathogenic bacteria. Front Cell Infect Microbiol 4:68

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  55. Matos RG et al (2012) The rnb gene of Synechocystis PCC6803 encodes a RNA hydrolase displaying RNase II and not RNase R enzymatic properties. PLoS One 7(3):e32690

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Matos RG et al (2011) Swapping the domains of exoribonucleases RNase II and RNase R: conferring upon RNase II the ability to degrade ds RNA. Proteins 79(6):1853–1867

    Article  CAS  PubMed  Google Scholar 

  57. Astuti D et al (2012) Germline mutations in DIS3L2 cause the Perlman syndrome of overgrowth and Wilms tumor susceptibility. Nat Genet 44(3):277–284

    Article  CAS  PubMed  Google Scholar 

  58. Chapman MA et al (2011) Initial genome sequencing and analysis of multiple myeloma. Nature 471(7339):467–472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Ding L et al (2012) Clonal evolution in relapsed acute myeloid leukaemia revealed by whole-genome sequencing. Nature 481(7382):506–510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Reis FP et al (2013) The RNase II/RNB family of exoribonucleases: putting the ‘Dis’ in disease. Wiley Interdiscip Rev RNA 4(5):607–615

    Article  PubMed  CAS  Google Scholar 

  61. Dziembowski A et al (2007) A single subunit, Dis3, is essentially responsible for yeast exosome core activity. Nat Struct Mol Biol 14(1):15–22

    Article  CAS  PubMed  Google Scholar 

  62. Wasmuth EV, Lima CD (2012) Exo- and endoribonucleolytic activities of yeast cytoplasmic and nuclear RNA exosomes are dependent on the noncatalytic core and central channel. Mol Cell 48(1):133–144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Liu Q, Greimann JC, Lima CD (2006) Reconstitution, activities, and structure of the eukaryotic RNA exosome. Cell 127(6):1223–1237

    Article  CAS  PubMed  Google Scholar 

  64. Makino DL, Baumgartner M, Conti E (2013) Crystal structure of an RNA-bound 11-subunit eukaryotic exosome complex. Nature 495(7439):70–75

    Article  CAS  PubMed  Google Scholar 

  65. Wasmuth EV, Januszyk K, Lima CD (2014) Structure of an Rrp6-RNA exosome complex bound to poly(A) RNA. Nature 511(7510):435–439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Allmang C et al (1999) Functions of the exosome in rRNA, snoRNA and snRNA synthesis. EMBO J 18(19):5399–5410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Bousquet-Antonelli C, Presutti C, Tollervey D (2000) Identification of a regulated pathway for nuclear pre-mRNA turnover. Cell 102(6):765–775

    Article  CAS  PubMed  Google Scholar 

  68. Chen CY et al (2001) AU binding proteins recruit the exosome to degrade ARE-containing mRNAs. Cell 107(4):451–464

    Article  CAS  PubMed  Google Scholar 

  69. Milligan L et al (2005) A nuclear surveillance pathway for mRNAs with defective polyadenylation. Mol Cell Biol 25(22):9996–10004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Mitchell P et al (1997) The exosome: a conserved eukaryotic RNA processing complex containing multiple 3′-->5′ exoribonucleases. Cell 91(4):457–466

    Article  CAS  PubMed  Google Scholar 

  71. Mukherjee D et al (2002) The mammalian exosome mediates the efficient degradation of mRNAs that contain AU-rich elements. EMBO J 21(1–2):165–174

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Tomecki R et al (2010) The human core exosome interacts with differentially localized processive RNases: hDIS3 and hDIS3L. EMBO J 29(14):2342–2357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Schaeffer D et al (2012) The CR3 motif of Rrp44p is important for interaction with the core exosome and exosome function. Nucleic Acids Res 40(18):9298–9307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Schneider C, Anderson JT, Tollervey D (2007) The exosome subunit Rrp44 plays a direct role in RNA substrate recognition. Mol Cell 27(2):324–331

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Wang HW et al (2007) Architecture of the yeast Rrp44 exosome complex suggests routes of RNA recruitment for 3′ end processing. Proc Natl Acad Sci U S A 104(43):16844–16849

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Lorentzen E et al (2008) Structure of the active subunit of the yeast exosome core, Rrp44: diverse modes of substrate recruitment in the RNase II nuclease family. Mol Cell 29(6):717–728

    Article  CAS  PubMed  Google Scholar 

  77. Amblar M et al (2006) Characterization of the functional domains of Escherichia coli RNase II. J Mol Biol 360(5):921–933

    Article  CAS  PubMed  Google Scholar 

  78. Amblar M et al (2007) The role of the S1 domain in exoribonucleolytic activity: substrate specificity and multimerization. RNA 13(3):317–327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Lee G et al (2012) Elastic coupling between RNA degradation and unwinding by an exoribonuclease. Science 336(6089):1726–1729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Matelska D, Steczkiewicz K, Ginalski K (2017) Comprehensive classification of the PIN domain-like superfamily. Nucleic Acids Res 45(12):6995–7020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Senissar M, Manav MC, Brodersen DE (2017) Structural conservation of the PIN domain active site across all domains of life. Protein Sci 26(8):1474–1492

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Drazkowska K et al (2013) The RNA exosome complex central channel controls both exonuclease and endonuclease Dis3 activities in vivo and in vitro. Nucleic Acids Res 41(6):3845–3858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Schneider C et al (2012) Transcriptome-wide analysis of exosome targets. Mol Cell 48(3):422–433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Malet H et al (2010) RNA channelling by the eukaryotic exosome. EMBO Rep 11(12):936–942

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Tomecki R et al (2014) Multiple myeloma-associated hDIS3 mutations cause perturbations in cellular RNA metabolism and suggest hDIS3 PIN domain as a potential drug target. Nucleic Acids Res 42(2):1270–1290

    Article  CAS  PubMed  Google Scholar 

  86. Hou D, Ruiz M, Andrulis ED (2012) The ribonuclease Dis3 is an essential regulator of the developmental transcriptome. BMC Genomics 13:359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Szczepinska T et al (2015) DIS3 shapes the RNA polymerase II transcriptome in humans by degrading a variety of unwanted transcripts. Genome Res 25(11):1622–1633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Morton DJ et al (2018) The RNA exosome and RNA exosome-linked disease. RNA 24(2):127–142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Robinson SR et al (2015) The 3′ to 5′ exoribonuclease DIS3: from structure and mechanisms to biological functions and role in human disease. Biomol Ther 5(3):1515–1539

    CAS  Google Scholar 

  90. Lionetti M et al (2015) A compendium of DIS3 mutations and associated transcriptional signatures in plasma cell dyscrasias. Oncotarget 6(28):26129–26141

    Article  PubMed  PubMed Central  Google Scholar 

  91. Lohr JG et al (2014) Widespread genetic heterogeneity in multiple myeloma: implications for targeted therapy. Cancer Cell 25(1):91–101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Walker BA et al (2012) Intraclonal heterogeneity and distinct molecular mechanisms characterize the development of t(4;14) and t(11;14) myeloma. Blood 120(5):1077–1086

    Article  CAS  PubMed  Google Scholar 

  93. Weissbach S et al (2015) The molecular spectrum and clinical impact of DIS3 mutations in multiple myeloma. Br J Haematol 169(1):57–70

    Article  CAS  PubMed  Google Scholar 

  94. Laubach J, Richardson P, Anderson K (2011) Multiple myeloma. Annu Rev Med 62:249–264

    Article  CAS  PubMed  Google Scholar 

  95. Preker P et al (2008) RNA exosome depletion reveals transcription upstream of active human promoters. Science 322(5909):1851–1854

    Article  CAS  PubMed  Google Scholar 

  96. Wang Y et al (2015) A novel long non-coding RNA, hypoxia-inducible factor-2alpha promoter upstream transcript, functions as an inhibitor of osteosarcoma stem cells in vitro. Mol Med Rep 11(4):2534–2540

    Article  CAS  PubMed  Google Scholar 

  97. Ng D et al (2007) Identification of a novel chromosome region, 13q21.33-q22.2, for susceptibility genes in familial chronic lymphocytic leukemia. Blood 109(3):916–925

    Article  CAS  PubMed  Google Scholar 

  98. Pils D et al (2013) A combined blood based gene expression and plasma protein abundance signature for diagnosis of epithelial ovarian cancer--a study of the OVCAD consortium. BMC Cancer 13:178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Lim J et al (1997) Isolation of murine and human homologues of the fission-yeast dis3+ gene encoding a mitotic-control protein and its overexpression in cancer cells with progressive phenotype. Cancer Res 57(5):921–925

    CAS  PubMed  Google Scholar 

  100. Kinoshita N, Goebl M, Yanagida M (1991) The fission yeast dis3+ gene encodes a 110-kDa essential protein implicated in mitotic control. Mol Cell Biol 11(12):5839–5847

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Ohkura H et al (1988) Cold-sensitive and caffeine-supersensitive mutants of the Schizosaccharomyces pombe dis genes implicated in sister chromatid separation during mitosis. EMBO J 7(5):1465–1473

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Towler BP et al (2015) The 3′-5′ exoribonuclease Dis3 regulates the expression of specific microRNAs in Drosophila wing imaginal discs. RNA Biol 12(7):728–741

    Article  PubMed  PubMed Central  Google Scholar 

  103. Camps J et al (2013) Genetic amplification of the NOTCH modulator LNX2 upregulates the WNT/beta-catenin pathway in colorectal cancer. Cancer Res 73(6):2003–2013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. de Groen FL et al (2014) Gene-dosage dependent overexpression at the 13q amplicon identifies DIS3 as candidate oncogene in colorectal cancer progression. Genes Chromosom Cancer 53(4):339–348

    Article  CAS  PubMed  Google Scholar 

  105. Rose AE et al (2011) Integrative genomics identifies molecular alterations that challenge the linear model of melanoma progression. Cancer Res 71(7):2561–2571

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Liu W, Peng Y, Tobin DJ (2013) A new 12-gene diagnostic biomarker signature of melanoma revealed by integrated microarray analysis. PeerJ 1:e49

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  107. Rozenblum E et al (2002) A genomic map of a 6-Mb region at 13q21-q22 implicated in cancer development: identification and characterization of candidate genes. Hum Genet 110(2):111–121

    Article  CAS  PubMed  Google Scholar 

  108. Hoskins JW et al (2016) Functional characterization of a chr13q22.1 pancreatic cancer risk locus reveals long-range interaction and allele-specific effects on DIS3 expression. Hum Mol Genet 25(21):4726–4738

    CAS  PubMed  PubMed Central  Google Scholar 

  109. Shen L, Shi Q, Wang W (2018) Double agents: genes with both oncogenic and tumor-suppressor functions. Oncogene 7(3):25

    Article  CAS  Google Scholar 

  110. Segalla S et al (2015) The ribonuclease DIS3 promotes let-7 miRNA maturation by degrading the pluripotency factor LIN28B mRNA. Nucleic Acids Res 43(10):5182–5193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Noguchi E et al (1996) Dis3, implicated in mitotic control, binds directly to ran and enhances the GEF activity of RCC1. EMBO J 15(20):5595–5605

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Glavan F et al (2006) Structures of the PIN domains of SMG6 and SMG5 reveal a nuclease within the mRNA surveillance complex. EMBO J 25(21):5117–5125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Bleichert F et al (2006) The PINc domain protein Utp24, a putative nuclease, is required for the early cleavage steps in 18S rRNA maturation. Proc Natl Acad Sci U S A 103(25):9464–9469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Staals RH et al (2010) Dis3-like 1: a novel exoribonuclease associated with the human exosome. EMBO J 29(14):2358–2367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Slomovic S et al (2010) Addition of poly(A) and poly(A)-rich tails during RNA degradation in the cytoplasm of human cells. Proc Natl Acad Sci U S A 107(16):7407–7412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Slomovic S et al (2006) Polyadenylation of ribosomal RNA in human cells. Nucleic Acids Res 34(10):2966–2975

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Lima WF et al (2016) RNA cleavage products generated by antisense oligonucleotides and siRNAs are processed by the RNA surveillance machinery. Nucleic Acids Res 44(7):3351–3363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Kohn M et al (2015) The Y3∗∗ ncRNA promotes the 3′ end processing of histone mRNAs. Genes Dev 29(19):1998–2003

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  119. Kowalski MP, Krude T (2015) Functional roles of non-coding Y RNAs. Int J Biochem Cell Biol 66:20–29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Savage SA (1993) Dyskeratosis congenita. In: Adam MP et al (eds) GeneReviews((R)). University of Washington, Seattle

    Google Scholar 

  121. Shukla S, Parker R (2017) PARN modulates Y RNA stability and its 3′-end formation. Mol Cell Biol 37(20):e00264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Shukla S et al (2019) The RNase PARN controls the levels of specific miRNAs that contribute to p53 regulation. Mol Cell 73:1204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Palmer CJ et al (2014) Zfx facilitates tumorigenesis caused by activation of the hedgehog pathway. Cancer Res 74(20):5914–5924

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Lee JY et al (2017) Genome-based exome sequencing analysis identifies GYG1, DIS3L and DDRGK1 are associated with myocardial infarction in Koreans. J Genet 96(6):1041–1046

    Article  CAS  PubMed  Google Scholar 

  125. Oates CP et al (2018) Novel polymorphisms associated with hyperalphalipoproteinemia and apparent cardioprotection. J Clin Lipidol 12(1):110–115

    Article  PubMed  Google Scholar 

  126. Labno A et al (2016) Perlman syndrome nuclease DIS3L2 controls cytoplasmic non-coding RNAs and provides surveillance pathway for maturing snRNAs. Nucleic Acids Res 44(21):10437–10453

    CAS  PubMed  PubMed Central  Google Scholar 

  127. Pirouz M et al (2016) Dis3l2-mediated decay is a quality control pathway for noncoding RNAs. Cell Rep 16(7):1861–1873

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Ustianenko D et al (2013) Mammalian DIS3L2 exoribonuclease targets the uridylated precursors of let-7 miRNAs. RNA 19(12):1632–1638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Ustianenko D et al (2016) TUT-DIS3L2 is a mammalian surveillance pathway for aberrant structured non-coding RNAs. EMBO J 35(20):2179–2191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Lim J et al (2014) Uridylation by TUT4 and TUT7 marks mRNA for degradation. Cell 159(6):1365–1376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Chang HM et al (2013) A role for the Perlman syndrome exonuclease Dis3l2 in the Lin28-let-7 pathway. Nature 497(7448):244–248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Faehnle CR, Walleshauser J, Joshua-Tor L (2014) Mechanism of Dis3l2 substrate recognition in the Lin28-let-7 pathway. Nature 514(7521):252–256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Rissland OS, Mikulasova A, Norbury CJ (2007) Efficient RNA polyuridylation by noncanonical poly(A) polymerases. Mol Cell Biol 27(10):3612–3624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Mullen TE, Marzluff WF (2008) Degradation of histone mRNA requires oligouridylation followed by decapping and simultaneous degradation of the mRNA both 5′ to 3′ and 3′ to 5′. Genes Dev 22(1):50–65

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Song MG, Kiledjian M (2007) 3′ terminal oligo U-tract-mediated stimulation of decapping. RNA 13(12):2356–2365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Tomecki R et al (2004) Identification of a novel human nuclear-encoded mitochondrial poly(A) polymerase. Nucleic Acids Res 32(20):6001–6014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Shimizu S et al (2014) Autophagic cell death and cancer. Int J Mol Sci 15(2):3145–3153

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  138. Thomas MP et al (2015) Apoptosis triggers specific, rapid, and global mRNA decay with 3′ uridylated intermediates degraded by DIS3L2. Cell Rep 11(7):1079–1089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Liu X et al (2018) PNPT1 release from mitochondria during apoptosis triggers decay of Poly(A) RNAs. Cell 174(1):187–201.e12

    Article  CAS  PubMed  Google Scholar 

  140. Briani F, Carzaniga T, Deho G (2016) Regulation and functions of bacterial PNPase. Wiley Interdiscip Rev RNA 7(2):241–258

    Article  CAS  PubMed  Google Scholar 

  141. Bussing I, Slack FJ, Grosshans H (2008) let-7 microRNAs in development, stem cells and cancer. Trends Mol Med 14(9):400–409

    Article  PubMed  CAS  Google Scholar 

  142. Thornton JE, Gregory RI (2012) How does Lin28 let-7 control development and disease? Trends Cell Biol 22(9):474–482

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Kurosaki T et al (2018) NMD-degradome sequencing reveals ribosome-bound intermediates with 3′-end non-templated nucleotides. Nat Struct Mol Biol 25(10):940–950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Schilke K et al (2000) A case of Perlman syndrome: fetal gigantism, renal dysplasia, and severe neurological deficits. Am J Med Genet 91(1):29–33

    Article  CAS  PubMed  Google Scholar 

  145. Hunter RW et al (2018) Loss of Dis3l2 partially phenocopies Perlman syndrome in mice and results in up-regulation of Igf2 in nephron progenitor cells. Genes Dev 32(13–14):903–908

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Morris MR, Astuti D, Maher ER (2013) Perlman syndrome: overgrowth, Wilms tumor predisposition and DIS3L2. Am J Med Genet C: Semin Med Genet 163C(2):106–113

    Article  CAS  Google Scholar 

  147. Tassano E et al (2013) Genotype-phenotype correlation of 2q37 deletions including NPPC gene associated with skeletal malformations. PLoS One 8(6):e66048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. von Kodolitsch Y et al (2010) Marfan syndrome and the evolving spectrum of heritable thoracic aortic disease: do we need genetics for clinical decisions? Vasa 39(1):17–32

    Article  Google Scholar 

  149. Bocciardi R et al (2007) Overexpression of the C-type natriuretic peptide (CNP) is associated with overgrowth and bone anomalies in an individual with balanced t(2;7) translocation. Hum Mutat 28(7):724–731

    Article  CAS  PubMed  Google Scholar 

  150. Moncla A et al (2007) A cluster of translocation breakpoints in 2q37 is associated with overexpression of NPPC in patients with a similar overgrowth phenotype. Hum Mutat 28(12):1183–1188

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by project LISBOA-01-0145-FEDER-007660 (Microbiologia Molecular, Estrutural e Celular) funded by FEDER funds through COMPETE2020 – Programa Operacional Competitividade e Internacionalização (POCI) and by national funds from FCT (Fundação para a Ciência e a Tecnologia); project PTDC/BIA-MIC/1399/2014 to CMA and project PTDC/BIM-MEC/3749/2014 to SCV. In addition, FCT provides postdoctoral grant ref. SFRH/BPD/109464/2015 to MS. SCV was financed by program IF of FCT (ref IF/00217/2015).

Author information

Authors and Affiliations

  1. Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, Oeiras, Portugal

    Margarida Saramago, Sandra C. Viegas & Cecília M. Arraiano

  2. Department of Human Genetics, National Institute of Health Doutor Ricardo Jorge, Lisboa, Portugal

    Paulo J. da Costa

  3. Faculty of Sciences, BioISI – Biosystems & Integrative Sciences Institute, University of Lisbon, Lisboa, Portugal

    Paulo J. da Costa

Authors
  1. Margarida Saramago
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paulo J. da Costa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sandra C. Viegas
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Cecília M. Arraiano
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Sandra C. Viegas or Cecília M. Arraiano .

Editor information

Editors and Affiliations

  1. Department of Human Genetics, National Institute of Health Doutor Ricardo Jorge, Lisboa, Portugal, Faculty of Sciences, BioISI – Biosystems & Integrative Sciences Institute, University of Lisbon, Lisboa, Portugal

    Luísa Romão

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Saramago, M., da Costa, P.J., Viegas, S.C., Arraiano, C.M. (2019). The Implication of mRNA Degradation Disorders on Human DISease: Focus on DIS3 and DIS3-Like Enzymes. In: Romão, L. (eds) The mRNA Metabolism in Human Disease. Advances in Experimental Medicine and Biology, vol 1157. Springer, Cham. https://doi.org/10.1007/978-3-030-19966-1_4

Download citation

Publish with us

Policies and ethics

Search

Navigation