Disruption of snRNP biogenesis factors Tgs1 and pICln induces phenotypes that mirror aspects of SMN-Gemins complex perturbation in Drosophila, providing new insights into spinal muscular atrophy

Neurobiology of Disease

Volumn 94, Issue , 2016, Pages 245-258

  Borg, Rebecca M ^a,b   Fenech Salerno, Benji ^a   Vassallo, Neville ^a   Bordonne, Rémy ^b   Cauchi, Ruben J ^a  

^a UNIVERSITY OF MALTA   (Malta)

^b INSTITUT DE GÉNÉTIQUE MOLÉCULAIRE DE MONTPELLIER   (France)

Author keywords

Gemin2; Gemin3; motor neuron disease; pICln; SMN complex; snRNP assembly; spinal muscular atrophy; Strap; Tgs1; trimethylguanosine synthase 1; Unrip; wmd

Indexed keywords

DEAD BOX PROTEIN 20; GEMIN 2; HELICASE; MEMBRANE PROTEIN; PICLN PROTEIN; SERINE THREONINE KINASE RECEPTOR ASSOCIATED PROTEIN; SMALL NUCLEAR RIBONUCLEOPROTEIN; SURVIVAL MOTOR NEURON PROTEIN; SYNTHETASE; TRIMETHYLGUANOSINE SYNTHASE 1; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOPLASM; DROSOPHILA; GENE OVEREXPRESSION; MOTOR DYSFUNCTION; NERVE CELL; NONHUMAN; ORTHOLOGY; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN INTERACTION; SCHIZOSACCHAROMYCES POMBE; SPINAL MUSCULAR ATROPHY; ANIMAL; DROSOPHILA MELANOGASTER; GENETICS; METABOLISM; MOTONEURON;

ANIMALS; CYTOPLASM; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; MOTOR NEURONS; PHENOTYPE; RIBONUCLEOPROTEINS, SMALL NUCLEAR; SMN COMPLEX PROTEINS;

EID: 84978431864     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2016.06.015     Document Type: Article

References (77)

1. Barbarossa, A., et al. Characterization and in vivo functional analysis of the Schizosaccharomyces pombe ICLN gene. Mol. Cell. Biol. 34 (2014), 595–605.
2. Battle, D.J., et al. The Gemin5 protein of the SMN complex identifies snRNAs. Mol. Cell 23 (2006), 273–279.
3. Bellen, H.J., Yamamoto, S., Morgan's legacy: fruit flies and the functional annotation of conserved genes. Cell 163 (2015), 12–14.
4. Bischof, J., et al. A versatile platform for creating a comprehensive UAS-ORFeome library in Drosophila. Development 140 (2013), 2434–2442.
5. Boon, K.L., et al. Self-association of Trimethylguanosine Synthase Tgs1 is required for efficient snRNA/snoRNA trimethylation and pre-rRNA processing. Sci. Rep., 5, 2015, 11282.
6. Bordonne, R., Functional characterization of nuclear localization signals in yeast Sm proteins. Mol. Cell. Biol. 20 (2000), 7943–7954.
7. Borg, R., Cauchi, R.J., The gemin associates of survival motor neuron are required for motor function in Drosophila. PLoS One, 8, 2013, e83878.
8. Borg, R., Cauchi, R.J., GEMINs: potential therapeutic targets for spinal muscular atrophy?. Front. Neurosci., 8, 2014, 325.
9. Borg, R.M., et al. Genetic Interactions between the members of the SMN-gemins complex in Drosophila. PLoS One, 10, 2015, e0130974.
10. Burghes, A.H., Beattie, C.E., Spinal muscular atrophy: why do low levels of survival motor neuron protein make motor neurons sick?. Nat. Rev. Neurosci. 10 (2009), 597–609.
11. Campion, Y., et al. Specific splicing defects in S. pombe carrying a degron allele of the survival of motor neuron gene. EMBO J. 29 (2010), 1817–1829.
12. Cappell, K.M., et al. Multiple cancer testis antigens function to support tumor cell mitotic fidelity. Mol. Cell. Biol. 32 (2012), 4131–4140.
13. Carissimi, C., et al. Unrip is a component of SMN complexes active in snRNP assembly. FEBS Lett. 579 (2005), 2348–2354.
14. Cauchi, R.J., SMN and Gemins: 'we are family' … or are we? Insights into the partnership between Gemins and the spinal muscular atrophy disease protein SMN. BioEssays 32 (2010), 1077–1089.
15. Cauchi, R.J., Gem depletion: amyotrophic lateral sclerosis and spinal muscular atrophy crossover. CNS Neurosci. Ther. 20 (2014), 574–581.
16. Cauchi, R.J., van den Heuvel, M., The fly as a model for neurodegenerative diseases: is it worth the jump?. Neurodegener. Dis. 3 (2006), 338–356.
17. Cauchi, R.J., et al. A motor function for the DEAD-box RNA helicase, Gemin3, in Drosophila. PLoS Genet., 4, 2008, e1000265.
18. Cauchi, R.J., et al. Drosophila SMN complex proteins Gemin2, Gemin3, and Gemin5 are components of U bodies. Exp. Cell Res. 316 (2010), 2354–2364.
19. Chang, H.C., et al. Modeling spinal muscular atrophy in Drosophila. PLoS One, 3, 2008, e3209.
20. Chari, A., et al. An assembly chaperone collaborates with the SMN complex to generate spliceosomal SnRNPs. Cell 135 (2008), 497–509.
21. Charroux, B., et al. Gemin3: a novel DEAD box protein that interacts with SMN, the spinal muscular atrophy gene product, and is a component of Gems. J. Cell Biol. 147 (1999), 1181–1193.
22. Chiu, J.C., et al. Assaying locomotor activity to study circadian rhythms and sleep parameters in Drosophila. J. Vis. Exp., 2010.
23. Craven, R.A., et al. Vectors for the expression of tagged proteins in Schizosaccharomyces pombe. Gene 221 (1998), 59–68.
24. Datta, P.K., et al. Identification of STRAP, a novel WD domain protein in transforming growth factor-beta signaling. J. Biol. Chem. 273 (1998), 34671–34674.
25. Dietzl, G., et al. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448 (2007), 151–156.
26. Dworkin, I., Gibson, G., Epidermal growth factor receptor and transforming growth factor-beta signaling contributes to variation for wing shape in Drosophila melanogaster. Genetics 173 (2006), 1417–1431.
27. Fallini, C., et al. Spinal muscular atrophy: the role of SMN in axonal mRNA regulation. Brain Res. 1462 (2012), 81–92.
28. Fischer, U., et al. Biogenesis of spliceosomal small nuclear ribonucleoproteins. Wiley interdisciplinary reviews. RNA 2 (2011), 718–731.
29. Foust, K.D., et al. Rescue of the spinal muscular atrophy phenotype in a mouse model by early postnatal delivery of SMN. Nat. Biotechnol. 28 (2010), 271–274.
30. Fromont-Racine, M., et al. Building protein-protein networks by two-hybrid mating strategy. Methods Enzymol. 350 (2002), 513–524.
31. Gabanella, F., et al. The activity of the spinal muscular atrophy protein is regulated during development and cellular differentiation. Hum. Mol. Genet. 14 (2005), 3629–3642.
32. Gabanella, F., et al. Ribonucleoprotein assembly defects correlate with spinal muscular atrophy severity and preferentially affect a subset of spliceosomal snRNPs. PLoS One, 2, 2007, e921.
33. Gerbino, V., et al. Mislocalised FUS mutants stall spliceosomal snRNPs in the cytoplasm. Neurobiol. Dis. 55 (2013), 120–128.
34. Grice, S.J., Liu, J.L., Survival motor neuron protein regulates stem cell division, proliferation, and differentiation in Drosophila. PLoS Genet., 7, 2011, e1002030.
35. Grimm, C., et al. Structural basis of assembly chaperone-mediated snRNP formation. Mol. Cell 49 (2013), 692–703.
36. Grimmler, M., et al. Unrip, a factor implicated in cap-independent translation, associates with the cytosolic SMN complex and influences its intracellular localization. Hum. Mol. Genet. 14 (2005), 3099–3111.
37. Guarente, L., Yeast promoters and lacZ fusions designed to study expression of cloned genes in yeast. Methods Enzymol. 101 (1983), 181–191.
38. Guruharsha, K.G., et al. A protein complex network of Drosophila melanogaster. Cell 147 (2011), 690–703.
39. Imlach, W.L., et al. SMN is required for sensory-motor circuit function in Drosophila. Cell 151 (2012), 427–439.
40. Jia, Y., et al. Early embryonic lethality of mice with disrupted transcription cofactor PIMT/NCOA6IP/Tgs1 gene. Mech. Dev. 129 (2012), 193–207.
41. Kariya, S., et al. Requirement of enhanced Survival Motoneuron protein imposed during neuromuscular junction maturation. J. Clin. Invest. 124 (2014), 785–800.
42. Komonyi, O., et al. DTL, the Drosophila homolog of PIMT/Tgs1 nuclear receptor coactivator-interacting protein/RNA methyltransferase, has an essential role in development. J. Biol. Chem. 280 (2005), 12397–12404.
43. Kroiss, M., et al. Evolution of an RNP assembly system: a minimal SMN complex facilitates formation of UsnRNPs in Drosophila melanogaster. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 10045–10050.
44. Lau, C.K., et al. Gemin5-snRNA interaction reveals an RNA binding function for WD repeat domains. Nat. Struct. Mol. Biol. 16 (2009), 486–491.
45. Le, T.T., et al. Temporal requirement for high SMN expression in SMA mice. Hum. Mol. Genet. 20 (2011), 3578–3591.
46. Lemm, I., et al. Ongoing U snRNP biogenesis is required for the integrity of Cajal bodies. Mol. Biol. Cell 17 (2006), 3221–3231.
47. Li, D.K., et al. SMN control of RNP assembly: from post-transcriptional gene regulation to motor neuron disease. Semin. Cell Dev. Biol. 32C (2014), 22–29.
48. Lotti, F., et al. An SMN-dependent U12 splicing event essential for motor circuit function. Cell 151 (2012), 440–454.
49. Lutz, C.M., et al. Postsymptomatic restoration of SMN rescues the disease phenotype in a mouse model of severe spinal muscular atrophy. J. Clin. Invest. 121 (2011), 3029–3041.
50. Ma, Y., et al. The Gemin6–Gemin7 heterodimer from the survival of motor neurons complex has an Sm protein-like structure. Structure 13 (2005), 883–892.
51. Maundrell, K., Thiamine-repressible expression vectors pREP and pRIP for fission yeast. Gene 123 (1993), 127–130.
52. Monani, U.R., De Vivo, D.C., Neurodegeneration in spinal muscular atrophy: from disease phenotype and animal models to therapeutic strategies and beyond. Future Neurol. 9 (2014), 49–65.
53. Moreno, S., et al. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194 (1991), 795–823.
54. Mouaikel, J., et al. Hypermethylation of the cap structure of both yeast snRNAs and snoRNAs requires a conserved methyltransferase that is localized to the nucleolus. Mol. Cell 9 (2002), 891–901.
55. Mouaikel, J., et al. Interaction between the small-nuclear-RNA cap hypermethylase and the spinal muscular atrophy protein, survival of motor neuron. EMBO Rep. 4 (2003), 616–622.
56. Ogawa, C., et al. Role of survival motor neuron complex components in small nuclear ribonucleoprotein assembly. J. Biol. Chem. 284 (2009), 14609–14617.
57. Otter, S., et al. A comprehensive interaction map of the human survival of motor neuron (SMN) complex. J. Biol. Chem. 282 (2007), 5825–5833.
58. Pellizzoni, L., et al. A novel function for SMN, the Spinal Muscular Atrophy disease gene product, in pre-mRNA splicing. Cell 95 (1998), 615–624.
59. Pu, W.T., et al. pICln inhibits snRNP biogenesis by binding core spliceosomal proteins. Mol. Cell. Biol. 19 (1999), 4113–4120.
60. Pu, W.T., et al. ICln is essential for cellular and early embryonic viability. J. Biol. Chem. 275 (2000), 12363–12366.
61. Rajendra, T.K., et al. A Drosophila melanogaster model of spinal muscular atrophy reveals a function for SMN in striated muscle. J. Cell Biol. 176 (2007), 831–841.
62. Reiner, J.E., Datta, P.K., TGF-beta-dependent and -independent roles of STRAP in cancer. Front. Biosci. 16 (2011), 105–115.
63. Sen, A., et al. Genetic circuitry of Survival motor neuron, the gene underlying spinal muscular atrophy. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), E2371–E2380.
64. Shpargel, K.B., et al. Gemin3 is an essential gene required for larval motor function and pupation in Drosophila. Mol. Biol. Cell 20 (2009), 90–101.
65. Simossis, V.A., Heringa, J., PRALINE: a multiple sequence alignment toolbox that integrates homology-extended and secondary structure information. Nucleic Acids Res. 33 (2005), W289–W294.
66. So, B.R., et al. A U1 snRNP-specific assembly pathway reveals the SMN complex as a versatile hub for RNP exchange. Nat. Struct. Mol. Biol. 23 (2016), 225–230.
67. Timmerman, C., Sanyal, S., Behavioral and electrophysiological outcomes of tissue-specific Smn knockdown in Drosophila melanogaster. Brain Res. 1489 (2012), 66–80.
68. Vojtek, A.B., et al. Mammalian Ras interacts directly with the serine/threonine kinase Raf. Cell 74 (1993), 205–214.
69. Wan, L., et al. The survival of motor neurons protein determines the capacity for snRNP assembly: biochemical deficiency in spinal muscular atrophy. Mol. Cell. Biol. 25 (2005), 5543–5551.
70. Winkler, C., et al. Reduced U snRNP assembly causes motor axon degeneration in an animal model for spinal muscular atrophy. Genes Dev. 19 (2005), 2320–2330.
71. Workman, E., et al. A SMN missense mutation complements SMN2 restoring snRNPs and rescuing SMA mice. Hum. Mol. Genet. 18 (2009), 2215–2229.
72. Workman, E., et al. Spliceosomal small nuclear ribonucleoprotein biogenesis defects and motor neuron selectivity in spinal muscular atrophy. Brain Res. 1462 (2012), 93–99.
73. Yan, X., et al. A novel domain within the DEAD-box protein DP103 is essential for transcriptional repression and helicase activity. Mol. Cell. Biol. 23 (2003), 414–423.
74. Yong, J., et al. Gemin5 delivers snRNA precursors to the SMN complex for snRNP biogenesis. Mol. Cell 38 (2010), 551–562.
75. Yu, Y., et al. U1 snRNP is mislocalized in ALS patient fibroblasts bearing NLS mutations in FUS and is required for motor neuron outgrowth in zebrafish. Nucleic Acids Res. 43 (2015), 3208–3218.
76. Zhang, R., et al. Structure of a key intermediate of the SMN complex reveals Gemin2's crucial function in snRNP assembly. Cell 146 (2011), 384–395.
77. Zhang, Z., et al. Dysregulation of synaptogenesis genes antecedes motor neuron pathology in spinal muscular atrophy. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 19348–19353.