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, N.; Raimer, A.; Sharp, R.; Spring, A.; Sarachan, K.; Johnson, M.; Van Duyne, G.; Matera, A.

doi:10.1093/nar/gkab508

Assembly of higher-order SMN oligomers is essential for metazoan viability and requires an exposed structural motif present in the YG zipper dimer

Journal Article · 01 January 2022 · Nucleic Acids Research

DOI:https://doi.org/10.1093/nar/gkab508· OSTI ID:1821854

Gupta, K; Wen, Y.; Ninan, N.; Raimer, A.; Sharp, R.; Spring, A.; Sarachan, K.; Johnson, M.; Van Duyne, G.; Matera, A.

Research Organization:: Brookhaven National Lab. (BNL), Upton, NY (United States)

Sponsoring Organization:: ~OTHER

DOE Contract Number:: SC0012704

OSTI ID:: 1821854

Report Number(s):: BNL-222154-2021-JACI

Journal Information:: Nucleic Acids Research, Vol. 49, Issue 13

Country of Publication:: United States

Language:: English

References (73)

3D Complex: A Structural Classification of Protein Complexes Levy, Emmanuel D.; Pereira-Leal, Jose B.; Chothia, Cyrus PLoS Computational Biology, Vol. 2, Issue 11 https://doi.org/10.1371/journal.pcbi.0020155	journal	January 2006
Bioengineering oligomerization and monomerization of enzymes: learning from natural evolution to matching the demands for industrial applications Liu, Hu; Cao, Mingming; Wang, Ying Critical Reviews in Biotechnology, Vol. 40, Issue 2 https://doi.org/10.1080/07388551.2019.1711014	journal	January 2020
Protein oligomerization: How and why Ali, Mayssam H.; Imperiali, Barbara Bioorganic & Medicinal Chemistry, Vol. 13, Issue 17 https://doi.org/10.1016/j.bmc.2005.05.037	journal	September 2005
A day in the life of the spliceosome Matera, A. Gregory; Wang, Zefeng Nature Reviews Molecular Cell Biology, Vol. 15, Issue 2 https://doi.org/10.1038/nrm3742	journal	January 2014
UsnRNP biogenesis: mechanisms and regulation Gruss, Oliver J.; Meduri, Rajyalakshmi; Schilling, Maximilian Chromosoma, Vol. 126, Issue 5 https://doi.org/10.1007/s00412-017-0637-6	journal	August 2017
The SMN Complex: An Assembly Machine for RNPs Battle, D. J.; Kasim, M.; Yong, J. Cold Spring Harbor Symposia on Quantitative Biology, Vol. 71, Issue 0 https://doi.org/10.1101/sqb.2006.71.001	journal	January 2006
SMN - A chaperone for nuclear RNP social occasions? Raimer, Amanda C.; Gray, Kelsey M.; Matera, A. Gregory RNA Biology, Vol. 14, Issue 6 https://doi.org/10.1080/15476286.2016.1236168	journal	November 2016
Diverse role of survival motor neuron protein Singh, Ravindra N.; Howell, Matthew D.; Ottesen, Eric W. Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, Vol. 1860, Issue 3 https://doi.org/10.1016/j.bbagrm.2016.12.008	journal	March 2017
The role of survival motor neuron protein (SMN) in protein homeostasis Chaytow, Helena; Huang, Yu-Ting; Gillingwater, Thomas H. Cellular and Molecular Life Sciences, Vol. 75, Issue 21 https://doi.org/10.1007/s00018-018-2849-1	journal	June 2018
The liquid nucleome – phase transitions in the nucleus at a glance Strom, Amy R.; Brangwynne, Clifford P. Journal of Cell Science, Vol. 132, Issue 22 https://doi.org/10.1242/jcs.235093	journal	November 2019
Identification and characterization of a spinal muscular atrophy-determining gene Lefebvre, Suzie; Bürglen, Lydie; Reboullet, Sophie Cell, Vol. 80, Issue 1 https://doi.org/10.1016/0092-8674(95)90460-3	journal	January 1995
Twenty-Five Years of Spinal Muscular Atrophy Research: From Phenotype to Genotype to Therapy, and What Comes Next Wirth, Brunhilde; Karakaya, Mert; Kye, Min Jeong Annual Review of Genomics and Human Genetics, Vol. 21, Issue 1 https://doi.org/10.1146/annurev-genom-102319-103602	journal	August 2020
SMN oligomerization defect correlates with spinal muscular atrophy severity Lorson, Christian L.; Strasswimmer, John; Yao, Jun-Mei Nature Genetics, Vol. 19, Issue 1 https://doi.org/10.1038/ng0598-63	journal	May 1998
The Spinal Muscular Atrophy Disease Gene Product, SMN, and Its Associated Protein SIP1 Are in a Complex with Spliceosomal snRNP Proteins Liu, Qing; Fischer, Utz; Wang, Fan Cell, Vol. 90, Issue 6 https://doi.org/10.1016/S0092-8674(00)80367-0	journal	September 1997
The evolution and population diversity of human-specific segmental duplications Dennis, Megan Y.; Harshman, Lana; Nelson, Bradley J. Nature Ecology & Evolution, Vol. 1, Issue 3 https://doi.org/10.1038/s41559-016-0069	journal	February 2017
A Comprehensive Interaction Map of the Human Survival of Motor Neuron (SMN) Complex Otter, Simon; Grimmler, Matthias; Neuenkirchen, Nils Journal of Biological Chemistry, Vol. 282, Issue 8 https://doi.org/10.1074/jbc.M608528200	journal	December 2006
SMN complex localizes to the sarcomeric Z-disc and is a proteolytic target of calpain Walker, Michael P.; Rajendra, T. K.; Saieva, Luciano Human Molecular Genetics, Vol. 17, Issue 21 https://doi.org/10.1093/hmg/ddn234	journal	August 2008
SMA-Causing Missense Mutations in Survival motor neuron (Smn) Display a Wide Range of Phenotypes When Modeled in Drosophila Praveen, Kavita; Wen, Ying; Gray, Kelsey M. PLoS Genetics, Vol. 10, Issue 8 https://doi.org/10.1371/journal.pgen.1004489	journal	August 2014
An update of the mutation spectrum of the survival motor neuron gene (SMN1) in autosomal recessive spinal muscular atrophy (SMA) Wirth, Brunhilde Human Mutation, Vol. 15, Issue 3 https://doi.org/10.1002/(SICI)1098-1004(200003)15:3<228::AID-HUMU3>3.0.CO;2-9	journal	March 2000
A single nucleotide in the SMN gene regulates splicing and is responsible for spinal muscular atrophy Lorson, C. L.; Hahnen, E.; Androphy, E. J. Proceedings of the National Academy of Sciences, Vol. 96, Issue 11 https://doi.org/10.1073/pnas.96.11.6307	journal	May 1999
Oligomeric Properties of Survival Motor Neuron·Gemin2 Complexes Gupta, Kushol; Martin, Renee; Sharp, Robert Journal of Biological Chemistry, Vol. 290, Issue 33 https://doi.org/10.1074/jbc.M115.667279	journal	August 2015
The Survival Motor Neuron Protein Forms Soluble Glycine Zipper Oligomers Martin, Renee; Gupta, Kushol; Ninan, Nisha S. Structure, Vol. 20, Issue 11 https://doi.org/10.1016/j.str.2012.08.024	journal	November 2012
Structural Properties of HIV Integrase·Lens Epithelium-derived Growth Factor Oligomers Gupta, Kushol; Diamond, Tracy; Hwang, Young Journal of Biological Chemistry, Vol. 285, Issue 26 https://doi.org/10.1074/jbc.M110.114413	journal	April 2010
Size-Distribution Analysis of Macromolecules by Sedimentation Velocity Ultracentrifugation and Lamm Equation Modeling Schuck, Peter Biophysical Journal, Vol. 78, Issue 3 https://doi.org/10.1016/S0006-3495(00)76713-0	journal	March 2000
Heterologous modules for efficient and versatile PCR-based gene targeting inSchizosaccharomyces pombe Bähler, Jürg; Wu, Jian-Qiu; Longtine, Mark S. Yeast, Vol. 14, Issue 10 https://doi.org/10.1002/(SICI)1097-0061(199807)14:10<943::AID-YEA292>3.0.CO;2-Y	journal	July 1998
Versatile shuttle vectors and genomic libraries for use with Schizosaccharomyces pombe Barbet, N.; Muriel, W. J.; Carr, A. M. Gene, Vol. 114, Issue 1 https://doi.org/10.1016/0378-1119(92)90707-V	journal	May 1992
Comparison of Schizosaccharomyces pombe expression systems Forsburg, Susan L. Nucleic Acids Research, Vol. 21, Issue 12 https://doi.org/10.1093/nar/21.12.2955	journal	January 1993
Modeling Spinal Muscular Atrophy in Drosophila Chang, Howard Chia-Hao; Dimlich, Douglas N.; Yokokura, Takakazu PLoS ONE, Vol. 3, Issue 9 https://doi.org/10.1371/journal.pone.0003209	journal	September 2008
A Drosophila melanogaster model of spinal muscular atrophy reveals a function for SMN in striated muscle Rajendra, T. K.; Gonsalvez, Graydon B.; Walker, Michael P. Journal of Cell Biology, Vol. 176, Issue 6 https://doi.org/10.1083/jcb.200610053	journal	March 2007
Optimization of wrMTrck to monitor Drosophila larval locomotor activity Brooks, David S.; Vishal, Kumar; Kawakami, Jessica Journal of Insect Physiology, Vol. 93-94 https://doi.org/10.1016/j.jinsphys.2016.07.007	journal	October 2016
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
Transmembrane glycine zippers: Physiological and pathological roles in membrane proteins Kim, S.; Jeon, T. -J.; Oberai, A. Proceedings of the National Academy of Sciences, Vol. 102, Issue 40 https://doi.org/10.1073/pnas.0501234102	journal	September 2005
SMN mutants of spinal muscular atrophy patients are defective in binding to snRNP proteins Pellizzoni, L.; Charroux, B.; Dreyfuss, G. Proceedings of the National Academy of Sciences, Vol. 96, Issue 20 https://doi.org/10.1073/pnas.96.20.11167	journal	September 1999
A multiprotein complex mediates the ATP-dependent assembly of spliceosomal U snRNPs Meister, Gunter; Bühler, Dirk; Pillai, Ramesh Nature Cell Biology, Vol. 3, Issue 11 https://doi.org/10.1038/ncb1101-945	journal	September 2001
Evolution of an RNP assembly system: A minimal SMN complex facilitates formation of UsnRNPs in Drosophila melanogaster Kroiss, M.; Schultz, J.; Wiesner, J. Proceedings of the National Academy of Sciences, Vol. 105, Issue 29 https://doi.org/10.1073/pnas.0802287105	journal	July 2008
Quantitative Analysis of Fission Yeast Transcriptomes and Proteomes in Proliferating and Quiescent Cells Marguerat, Samuel; Schmidt, Alexander; Codlin, Sandra Cell, Vol. 151, Issue 3 https://doi.org/10.1016/j.cell.2012.09.019	journal	October 2012
The Schizosaccharomyces pombe protein Yab8p and a novel factor, Yip1p, share structural and functional similarity with the spinal muscular atrophy-associated proteins SMN and SIP1 Hannus, S. Human Molecular Genetics, Vol. 9, Issue 5 https://doi.org/10.1093/hmg/9.5.663	journal	March 2000
Characterization of the Schizosaccharomyces pombe orthologue of the human survival motor neuron (SMN) protein Owen, N. Human Molecular Genetics, Vol. 9, Issue 5 https://doi.org/10.1093/hmg/9.5.675	journal	March 2000
The Survival Motor Neuron Protein of Schizosacharomyces pombe Paushkin, Sergey; Charroux, Bernard; Abel, Linda Journal of Biological Chemistry, Vol. 275, Issue 31 https://doi.org/10.1074/jbc.M001441200	journal	August 2000
Missense mutation clustering in the survival motor neuron gene: a role for a conserved tyrosine and glycine rich region of the protein in RNA metabolism? Talbot, K.; Ponting, C. P.; Theodosiou, A. M. Human Molecular Genetics, Vol. 6, Issue 3 https://doi.org/10.1093/hmg/6.3.497	journal	March 1997
Comprehensive Modeling of Spinal Muscular Atrophy in Drosophila melanogaster Spring, Ashlyn M.; Raimer, Amanda C.; Hamilton, Christine D. Frontiers in Molecular Neuroscience, Vol. 12 https://doi.org/10.3389/fnmol.2019.00113	journal	May 2019
A switch between two-, three-, and four-stranded coiled coils in GCN4 leucine zipper mutants Harbury, P.; Zhang, T; Kim, P. Science, Vol. 262, Issue 5138, p. 1401-1407 https://doi.org/10.1126/science.8248779	journal	November 1993
A Drosophila Model of Spinal Muscular Atrophy Uncouples snRNP Biogenesis Functions of Survival Motor Neuron from Locomotion and Viability Defects Praveen, Kavita; Wen, Ying; Matera, A. Gregory Cell Reports, Vol. 1, Issue 6 https://doi.org/10.1016/j.celrep.2012.05.014	journal	June 2012
Detection of novel mutations in the SMN Tudor domain in type I SMA patients Cusco, I.; Barcelo, M. J.; del Rio, E. Neurology, Vol. 63, Issue 1 https://doi.org/10.1212/01.WNL.0000132634.48815.13	journal	July 2004
A novel mutation at the N-terminal of SMN Tudor domain inhibits its interaction with target proteins Kotani, Tomohiro; Sutomo, Retno; Sasongko, Teguh Haryo Journal of Neurology, Vol. 254, Issue 5 https://doi.org/10.1007/s00415-006-0410-x	journal	April 2007
Characterisation of novel point mutations in the survival motor neuron gene SMN , in three patients with SMA Skordis, Leigh; Dunckley, Matthew; Burglen, Lydia Human Genetics, Vol. 108, Issue 4 https://doi.org/10.1007/s004390100497	journal	April 2001
Identification of a novel missense mutation of the SMN T gene in two siblings with spinal muscular atrophy Day, J. Kevin; Wang, C. H.; Papendick, Brett D. neurogenetics, Vol. 1, Issue 4 https://doi.org/10.1007/s100480050040	journal	August 1998
Self-oligomerization regulates stability of survival motor neuron protein isoforms by sequestering an SCF ^Slmb degron Gray, Kelsey M.; Kaifer, Kevin A.; Baillat, David Molecular Biology of the Cell, Vol. 29, Issue 2 https://doi.org/10.1091/mbc.E17-11-0627	journal	January 2018
A degron created by SMN2 exon 7 skipping is a principal contributor to spinal muscular atrophy severity Cho, S.; Dreyfuss, G. Genes & Development, Vol. 24, Issue 5 https://doi.org/10.1101/gad.1884910	journal	March 2010
Gemin3 Is an Essential Gene Required for Larval Motor Function and Pupation in Drosophila Shpargel, Karl B.; Praveen, Kavita; Rajendra, T. K. Molecular Biology of the Cell, Vol. 20, Issue 1 https://doi.org/10.1091/mbc.e08-01-0024	journal	January 2009
Neuromuscular defects in a Drosophila survival motor neuron gene mutant Chan, Y. B. Human Molecular Genetics, Vol. 12, Issue >12 https://doi.org/10.1093/hmg/ddg157	journal	June 2003
Identification and structural analysis of the Schizosaccharomyces pombe SMN complex Veepaschit, Jyotishman; Viswanathan, Aravindan; Bordonné, Rémy Nucleic Acids Research https://doi.org/10.1093/nar/gkab158	journal	March 2021
Comparison of Helix Interactions in Membrane and Soluble α-Bundle Proteins Eilers, Markus; Patel, Ashish B.; Liu, Wei Biophysical Journal, Vol. 82, Issue 5 https://doi.org/10.1016/S0006-3495(02)75613-0	journal	May 2002
α-Helical coiled coils and bundles: How to design an α-helical protein Cohen, Carolyn; Parry, David A. D. Proteins: Structure, Function, and Genetics, Vol. 7, Issue 1 https://doi.org/10.1002/prot.340070102	journal	January 1990
The GxxxG motif: A framework for transmembrane helix-helix association Russ, William P.; Engelman, Donald M. Journal of Molecular Biology, Vol. 296, Issue 3 https://doi.org/10.1006/jmbi.1999.3489	journal	February 2000
Structure of a Glycerol-Conducting Channel and the Basis for Its Selectivity Fu, D. Science, Vol. 290, Issue 5491 https://doi.org/10.1126/science.290.5491.481	journal	October 2000
A Transmembrane Helix Dimer: Structure and Implications MacKenzie, K. R. Science, Vol. 276, Issue 5309 https://doi.org/10.1126/science.276.5309.131	journal	April 1997
Phase separation in biology Alberti, Simon Current Biology, Vol. 27, Issue 20 https://doi.org/10.1016/j.cub.2017.08.069	journal	October 2017
Mechanisms for Active Regulation of Biomolecular Condensates Söding, Johannes; Zwicker, David; Sohrabi-Jahromi, Salma Trends in Cell Biology, Vol. 30, Issue 1 https://doi.org/10.1016/j.tcb.2019.10.006	journal	January 2020
Genetic Analysis of Nuclear Bodies: From Nondeterministic Chaos to Deterministic Order Rajendra, T. K.; Praveen, K.; Matera, A. G. Cold Spring Harbor Symposia on Quantitative Biology, Vol. 75, Issue 0 https://doi.org/10.1101/sqb.2010.75.043	journal	January 2010
Protein Misfolding Diseases Hartl, F. Ulrich Annual Review of Biochemistry, Vol. 86, Issue 1 https://doi.org/10.1146/annurev-biochem-061516-044518	journal	June 2017
ER stress and the unfolded protein response in neurodegeneration Hetz, Claudio; Saxena, Smita Nature Reviews Neurology, Vol. 13, Issue 8 https://doi.org/10.1038/nrneurol.2017.99	journal	July 2017
Protein Misfolding, Signaling Abnormalities and Altered Fast Axonal Transport: Implications for Alzheimer and Prion Diseases Zamponi, Emiliano; Pigino, Gustavo F. Frontiers in Cellular Neuroscience, Vol. 13 https://doi.org/10.3389/fncel.2019.00350	journal	July 2019
Molecular Mechanisms of TDP-43 Misfolding and Pathology in Amyotrophic Lateral Sclerosis Prasad, Archana; Bharathi, Vidhya; Sivalingam, Vishwanath Frontiers in Molecular Neuroscience, Vol. 12 https://doi.org/10.3389/fnmol.2019.00025	journal	February 2019
Considerations and Challenges in Studying Liquid-Liquid Phase Separation and Biomolecular Condensates Alberti, Simon; Gladfelter, Amy; Mittag, Tanja Cell, Vol. 176, Issue 3 https://doi.org/10.1016/j.cell.2018.12.035	journal	January 2019
Droplet organelles? Courchaine, Edward M.; Lu, Alice; Neugebauer, Karla M. The EMBO Journal, Vol. 35, Issue 15 https://doi.org/10.15252/embj.201593517	journal	June 2016
Sedimentation equilibrium analysis of protein interactions with global implicit mass conservation constraints and systematic noise decomposition Vistica, Jennifer; Dam, Julie; Balbo, Andrea Analytical Biochemistry, Vol. 326, Issue 2 https://doi.org/10.1016/j.ab.2003.12.014	journal	March 2004
Characterizing flexible and intrinsically unstructured biological macromolecules by SAS using the Porod-Debye law Rambo, Robert P.; Tainer, John A. Biopolymers, Vol. 95, Issue 8 https://doi.org/10.1002/bip.21638	journal	April 2011
Accurate assessment of mass, models and resolution by small-angle scattering Rambo, Robert P.; Tainer, John A. Nature, Vol. 496, Issue 7446 https://doi.org/10.1038/nature12070	journal	April 2013
BioXTAS RAW : improvements to a free open-source program for small-angle X-ray scattering data reduction and analysis Hopkins, Jesse Bennett; Gillilan, Richard E.; Skou, Soren Journal of Applied Crystallography, Vol. 50, Issue 5 https://doi.org/10.1107/S1600576717011438	journal	September 2017
Domain Movements upon Activation of Phenylalanine Hydroxylase Characterized by Crystallography and Chromatography-Coupled Small-Angle X-ray Scattering Meisburger, Steve P.; Taylor, Alexander B.; Khan, Crystal A. Journal of the American Chemical Society, Vol. 138, Issue 20 https://doi.org/10.1021/jacs.6b01563	journal	May 2016
GNOM – a program package for small-angle scattering data processing Semenyuk, A. V.; Svergun, D. I. Journal of Applied Crystallography, Vol. 24, Issue 5 https://doi.org/10.1107/S002188989100081X	journal	October 1991
FoXS: a web server for rapid computation and fitting of SAXS profiles Schneidman-Duhovny, D.; Hammel, M.; Sali, A. Nucleic Acids Research, Vol. 38, Issue Web Server https://doi.org/10.1093/nar/gkq461	journal	May 2010

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