4gli › Citations

The survival motor neuron protein forms soluble glycine zipper oligomers.

Martin R, Gupta K, Ninan NS, Perry K, Van Duyne GD
Structure 20 1929-39 (2012)
Cited: 46 times
EuropePMC logo PMID: 23022347

Abstract

The survival motor neuron (SMN) protein forms the oligomeric core of a multiprotein complex that functions in spliceosomal snRNP biogenesis. Loss of function mutations in the SMN gene cause spinal muscular atrophy (SMA), a leading genetic cause of infant mortality. Nearly half of the known SMA patient missense mutations map to the SMN YG-box, a highly conserved oligomerization domain of unknown structure that contains a (YxxG)₃ motif. Here, we report that the SMN YG-box forms helical oligomers similar to the glycine zippers found in transmembrane channel proteins. A network of tyrosine-glycine packing between helices drives formation of soluble YG-box oligomers, providing a structural basis for understanding SMN oligomerization and for relating defects in oligomerization to the mutations found in SMA patients. These results have important implications for advancing our understanding of SMN function and glycine zipper-mediated helix-helix interactions.

Reviews - 4gli mentioned but not cited (1)

  1. Crystal structures of MBP fusion proteins. Waugh DS. Protein Sci 25 559-571 (2016)

Articles - 4gli mentioned but not cited (7)

  1. The survival motor neuron protein forms soluble glycine zipper oligomers. Martin R, Gupta K, Ninan NS, Perry K, Van Duyne GD. Structure 20 1929-1939 (2012)
  2. A novel human-specific splice isoform alters the critical C-terminus of Survival Motor Neuron protein. Seo J, Singh NN, Ottesen EW, Lee BM, Singh RN. Sci Rep 6 30778 (2016)
  3. SMA-causing missense mutations in survival motor neuron (Smn) display a wide range of phenotypes when modeled in Drosophila. Praveen K, Wen Y, Gray KM, Noto JJ, Patlolla AR, Van Duyne GD, Matera AG. PLoS Genet 10 e1004489 (2014)
  4. Functional Segments on Intrinsically Disordered Regions in Disease-Related Proteins. Anbo H, Sato M, Okoshi A, Fukuchi S. Biomolecules 9 E88 (2019)
  5. How do SMA-linked mutations of SMN1 lead to structural/functional deficiency of the SMA protein? Li W. PLoS One 12 e0178519 (2017)
  6. Identification and structural analysis of the Schizosaccharomyces pombe SMN complex. Veepaschit J, Viswanathan A, Bordonné R, Grimm C, Fischer U. Nucleic Acids Res 49 7207-7223 (2021)
  7. Assembly of higher-order SMN oligomers is essential for metazoan viability and requires an exposed structural motif present in the YG zipper dimer. Gupta K, Wen Y, Ninan NS, Raimer AC, Sharp R, Spring AM, Sarachan KL, Johnson MC, Van Duyne GD, Matera AG. Nucleic Acids Res 49 7644-7664 (2021)


Reviews citing this publication (17)

  1. A day in the life of the spliceosome. Matera AG, Wang Z. Nat Rev Mol Cell Biol 15 108-121 (2014)
  2. Diverse role of survival motor neuron protein. Singh RN, Howell MD, Ottesen EW, Singh NN. Biochim Biophys Acta Gene Regul Mech 1860 299-315 (2017)
  3. SMN control of RNP assembly: from post-transcriptional gene regulation to motor neuron disease. Li DK, Tisdale S, Lotti F, Pellizzoni L. Semin Cell Dev Biol 32 22-29 (2014)
  4. The role of survival motor neuron protein (SMN) in protein homeostasis. Chaytow H, Huang YT, Gillingwater TH, Faller KME. Cell Mol Life Sci 75 3877-3894 (2018)
  5. Assays for the identification and prioritization of drug candidates for spinal muscular atrophy. Cherry JJ, Kobayashi DT, Lynes MM, Naryshkin NN, Tiziano FD, Zaworski PG, Rubin LL, Jarecki J. Assay Drug Dev Technol 12 315-341 (2014)
  6. UsnRNP biogenesis: mechanisms and regulation. Gruss OJ, Meduri R, Schilling M, Fischer U. Chromosoma 126 577-593 (2017)
  7. SMN - A chaperone for nuclear RNP social occasions? Raimer AC, Gray KM, Matera AG. RNA Biol 14 701-711 (2017)
  8. Specific genomic cues regulate Cajal body assembly. Sawyer IA, Hager GL, Dundr M. RNA Biol 14 791-803 (2017)
  9. Emerging Roles of Gemin5: From snRNPs Assembly to Translation Control. Martinez-Salas E, Embarc-Buh A, Francisco-Velilla R. Int J Mol Sci 21 E3868 (2020)
  10. Characteristics of circular RNAs generated by human Survival Motor Neuron genes. Ottesen EW, Singh RN. Cell Signal 73 109696 (2020)
  11. A survey of transcripts generated by spinal muscular atrophy genes. Singh NN, Ottesen EW, Singh RN. Biochim Biophys Acta Gene Regul Mech 1863 194562 (2020)
  12. Therapeutic Modulation of RNA Splicing in Malignant and Non-Malignant Disease. El Marabti E, Abdel-Wahab O. Trends Mol Med 27 643-659 (2021)
  13. Drug Discovery of Spinal Muscular Atrophy (SMA) from the Computational Perspective: A Comprehensive Review. Chong LC, Gandhi G, Lee JM, Yeo WWY, Choi SB. Int J Mol Sci 22 8962 (2021)
  14. The phospho-landscape of the survival of motoneuron protein (SMN) protein: relevance for spinal muscular atrophy (SMA). Detering NT, Schüning T, Hensel N, Claus P. Cell Mol Life Sci 79 497 (2022)
  15. The SMN Complex at the Crossroad between RNA Metabolism and Neurodegeneration. Faravelli I, Riboldi GM, Rinchetti P, Lotti F. Int J Mol Sci 24 2247 (2023)
  16. SMN post-translational modifications in spinal muscular atrophy. Riboldi GM, Faravelli I, Rinchetti P, Lotti F. Front Cell Neurosci 17 1092488 (2023)
  17. Spinal Muscular Atrophy: The Past, Present, and Future of Diagnosis and Treatment. Nishio H, Niba ETE, Saito T, Okamoto K, Takeshima Y, Awano H. Int J Mol Sci 24 11939 (2023)

Articles citing this publication (21)

  1. Pilot study of population-based newborn screening for spinal muscular atrophy in New York state. Kraszewski JN, Kay DM, Stevens CF, Koval C, Haser B, Ortiz V, Albertorio A, Cohen LL, Jain R, Andrew SP, Young SD, LaMarca NM, De Vivo DC, Caggana M, Chung WK. Genet Med 20 608-613 (2018)
  2. Reconstitution of the human U snRNP assembly machinery reveals stepwise Sm protein organization. Neuenkirchen N, Englbrecht C, Ohmer J, Ziegenhals T, Chari A, Fischer U. EMBO J 34 1925-1941 (2015)
  3. High-affinity RNA targets of the Survival Motor Neuron protein reveal diverse preferences for sequence and structural motifs. Ottesen EW, Singh NN, Luo D, Singh RN. Nucleic Acids Res 46 10983-11001 (2018)
  4. Oligomeric Properties of Survival Motor Neuron·Gemin2 Complexes. Gupta K, Martin R, Sharp R, Sarachan KL, Ninan NS, Van Duyne GD. J Biol Chem 290 20185-20199 (2015)
  5. Self-oligomerization regulates stability of survival motor neuron protein isoforms by sequestering an SCFSlmb degron. Gray KM, Kaifer KA, Baillat D, Wen Y, Bonacci TR, Ebert AD, Raimer AC, Spring AM, Have ST, Glascock JJ, Gupta K, Van Duyne GD, Emanuele MJ, Lamond AI, Wagner EJ, Lorson CL, Matera AG. Mol Biol Cell 29 96-110 (2018)
  6. Composition of the Survival Motor Neuron (SMN) Complex in Drosophila melanogaster. Matera AG, Raimer AC, Schmidt CA, Kelly JA, Droby GN, Baillat D, Ten Have S, Lamond AI, Wagner EJ, Gray KM. G3 (Bethesda) 9 491-503 (2019)
  7. Conditional deletion of SMN in cell culture identifies functional SMN alleles. Blatnik AJ, McGovern VL, Le TT, Iyer CC, Kaspar BK, Burghes AHM. Hum Mol Genet 29 3477-3492 (2020)
  8. Mild SMN missense alleles are only functional in the presence of SMN2 in mammals. Iyer CC, Corlett KM, Massoni-Laporte A, Duque SI, Madabusi N, Tisdale S, McGovern VL, Le TT, Zaworski PG, Arnold WD, Pellizzoni L, Burghes AHM. Hum Mol Genet 27 3404-3416 (2018)
  9. The SMN structure reveals its crucial role in snRNP assembly. Seng CO, Magee C, Young PJ, Lorson CL, Allen JP. Hum Mol Genet 24 2138-2146 (2015)
  10. Functional characterization of SMN evolution in mouse models of SMA. Osman EY, Bolding MR, Villalón E, Kaifer KA, Lorson ZC, Tisdale S, Hao Y, Conant GC, Pires JC, Pellizzoni L, Lorson CL. Sci Rep 9 9472 (2019)
  11. SMA mutations in SMN Tudor and C-terminal domains destabilize the protein. Takarada T, Ar Rochmah M, Harahap NIF, Shinohara M, Saito T, Saito K, Lai PS, Bouike Y, Takeshima Y, Awano H, Morioka I, Iijima K, Nishio H, Takeuchi A. Brain Dev 39 606-612 (2017)
  12. A Single Amino Acid Residue Regulates PTEN-Binding and Stability of the Spinal Muscular Atrophy Protein SMN. Rademacher S, Detering NT, Schüning T, Lindner R, Santonicola P, Wefel IM, Dehus J, Walter LM, Brinkmann H, Niewienda A, Janek K, Varela MA, Bowerman M, Di Schiavi E, Claus P. Cells 9 E2405 (2020)
  13. Interaction modulation through arrays of clustered methyl-arginine protein modifications. Woodsmith J, Casado-Medrano V, Benlasfer N, Eccles RL, Hutten S, Heine CL, Thormann V, Abou-Ajram C, Rocks O, Dormann D, Stelzl U. Life Sci Alliance 1 e201800178 (2018)
  14. Intragenic complementation of amino and carboxy terminal SMN missense mutations can rescue Smn null mice. McGovern VL, Kray KM, Arnold WD, Duque SI, Iyer CC, Massoni-Laporte A, Workman E, Patel A, Battle DJ, Burghes AHM. Hum Mol Genet 29 3493-3503 (2020)
  15. SMA-linked SMN mutants prevent phase separation properties and SMN interactions with FMRP family members. Binda O, Juillard F, Ducassou JN, Kleijwegt C, Paris G, Didillon A, Baklouti F, Corpet A, Couté Y, Côté J, Lomonte P. Life Sci Alliance 6 e202201429 (2023)
  16. What Genetics Has Told Us and How It Can Inform Future Experiments for Spinal Muscular Atrophy, a Perspective. Blatnik AJ, McGovern VL, Burghes AHM. Int J Mol Sci 22 8494 (2021)
  17. Stability and Oligomerization of Mutated SMN Protein Determine Clinical Severity of Spinal Muscular Atrophy. Niba ETE, Nishio H, Wijaya YOS, Ar Rochmah M, Takarada T, Takeuchi A, Kimizu T, Okamoto K, Saito T, Awano H, Takeshima Y, Shinohara M. Genes (Basel) 13 205 (2022)
  18. Structure of a HIV-1 IN-Allosteric inhibitor complex at 2.93 Å resolution: Routes to inhibitor optimization. Eilers G, Gupta K, Allen A, Montermoso S, Murali H, Sharp R, Hwang Y, Bushman FD, Van Duyne G. PLoS Pathog 19 e1011097 (2023)
  19. Case Reports A homozygous missense variant in the YG box domain in an individual with severe spinal muscular atrophy: a case report and variant characterization. Li L, Perera L, Varghese SA, Shiloh-Malawsky Y, Hunter SE, Sneddon TP, Powell CM, Matera AG, Fan Z. Front Cell Neurosci 17 1259380 (2023)
  20. Mechanism of assembly of snRNP cores assisted by ICln and the SMN complex in fission yeast. Hu Y, Hou Y, Zhou S, Wang Y, Shen C, Mu L, Su D, Zhang R. iScience 26 107604 (2023)
  21. NRF2 has a splicing regulatory function involving the survival of motor neuron (SMN) in non-small cell lung cancer. Cui Q, Wang W, Namani A, Wang H, Hammad A, Huang P, Gao Y, Elshaer M, Wu Y, Wang XJ, Tang X. Oncogene 42 2751-2763 (2023)


Quick links