Structure of the SHOC2?MRAS?PP1C complex provides insights into RAF activation and Noonan syndrome

Bonsor, Daniel A.; Alexander, Patrick; Snead, Kelly; Hartig, Nicole; Drew, Matthew; Messing, Simon; Finci, Lorenzo I.; Nissley, Dwight V.; McCormick, Frank; Esposito, Dominic; Rodriguez-Viciana, Pablo; Stephen, Andrew G.; Simanshu, Dhirendra K.

doi:10.1038/s41594-022-00841-4

Structure of the SHOC2?MRAS?PP1C complex provides insights into RAF activation and Noonan syndrome

Journal Article · 01 September 2022 · Nat. Struct. Mol. Biol.

DOI:https://doi.org/10.1038/s41594-022-00841-4· OSTI ID:1901134

Bonsor, Daniel A.; Alexander, Patrick; Snead, Kelly; Hartig, Nicole; Drew, Matthew; Messing, Simon; Finci, Lorenzo I.; Nissley, Dwight V.; McCormick, Frank; Esposito, Dominic; Rodriguez-Viciana, Pablo; Stephen, Andrew G.; Simanshu, Dhirendra K.

Research Organization:: Advanced Photon Source (APS), Argonne National Laboratory (ANL), Argonne, IL (US)

Sponsoring Organization:: DOE - Office Of Science; NIH

OSTI ID:: 1901134

Journal Information:: Nat. Struct. Mol. Biol., Journal Name: Nat. Struct. Mol. Biol. Vol. 29

Country of Publication:: United States

Language:: ENGLISH

References (77)

Mutation of SHOC2 promotes aberrant protein N-myristoylation and causes Noonan-like syndrome with loose anagen hair Cordeddu, Viviana; Di Schiavi, Elia; Pennacchio, Len A. Nature Genetics, Vol. 41, Issue 9 https://doi.org/10.1038/ng.425	journal	August 2009
CRISPR screens in cancer spheroids identify 3D growth-specific vulnerabilities Han, Kyuho; Pierce, Sarah E.; Li, Amy Nature, Vol. 580, Issue 7801 https://doi.org/10.1038/s41586-020-2099-x	journal	March 2020
Towards Dissecting the Mechanism of Protein Phosphatase‐1 Inhibition by Its C ‐Terminal Phosphorylation Salvi, Francesca; Hoermann, Bernhard; Pino García, Javier ChemBioChem, Vol. 22, Issue 5 https://doi.org/10.1002/cbic.202000669	journal	November 2020
Collaboration gets the most out of software Morin, Andrew; Eisenbraun, Ben; Key, Jason eLife, Vol. 2 https://doi.org/10.7554/eLife.01456	journal	September 2013
Microseed matrix screening for optimization in protein crystallization: what have we learned? D'Arcy, Allan; Bergfors, Terese; Cowan-Jacob, Sandra W. Acta Crystallographica Section F Structural Biology Communications, Vol. 70, Issue 9 https://doi.org/10.1107/S2053230X14015507	journal	August 2014
MRAS: A Close but Understudied Member of the RAS Family Young, Lucy C.; Rodriguez-Viciana, Pablo Cold Spring Harbor Perspectives in Medicine, Vol. 8, Issue 12 https://doi.org/10.1101/cshperspect.a033621	journal	January 2018
Architecture of autoinhibited and active BRAF–MEK1–14-3-3 complexes Park, Eunyoung; Rawson, Shaun; Li, Kunhua Nature, Vol. 575, Issue 7783 https://doi.org/10.1038/s41586-019-1660-y	journal	October 2019
M-Ras is Muscle-Ras, Moderate-Ras, Mineral-Ras, Migration-Ras, and Many More-Ras Endo, Takeshi Experimental Cell Research, Vol. 397, Issue 1 https://doi.org/10.1016/j.yexcr.2020.112342	journal	December 2020
Elucidation of MRAS-mediated Noonan syndrome with cardiac hypertrophy Higgins, Erin M.; Bos, J. Martijn; Mason-Suares, Heather JCI Insight, Vol. 2, Issue 5 https://doi.org/10.1172/jci.insight.91225	journal	March 2017
Improvements to the APBS biomolecular solvation software suite: Improvements to the APBS Software Suite Jurrus, Elizabeth; Engel, Dave; Star, Keith Protein Science, Vol. 27, Issue 1 https://doi.org/10.1002/pro.3280	journal	October 2017
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
SUR-8, a Conserved Ras-Binding Protein with Leucine-Rich Repeats, Positively Regulates Ras-Mediated Signaling in C. elegans Sieburth, Derek S.; Sun, Qun; Han, Min Cell, Vol. 94, Issue 1 https://doi.org/10.1016/S0092-8674(00)81227-1	journal	July 1998
Mutation-Specific RAS Oncogenicity Explains NRAS Codon 61 Selection in Melanoma Burd, Christin E.; Liu, Wenjin; Huynh, Minh V. Cancer Discovery, Vol. 4, Issue 12 https://doi.org/10.1158/2159-8290.CD-14-0729	journal	December 2014
The leucine‐rich repeat signaling scaffolds Shoc2 and Erbin: cellular mechanism and role in disease Jang, HyeIn; Stevens, Payton; Gao, Tianyan The FEBS Journal, Vol. 288, Issue 3 https://doi.org/10.1111/febs.15450	journal	July 2020
Structural basis for protein phosphatase 1 recruitment by glycogen‐targeting subunits Yu, Jun; Deng, Tingting; Xiang, Song The FEBS Journal, Vol. 285, Issue 24 https://doi.org/10.1111/febs.14699	journal	November 2018
Biogenesis and activity regulation of protein phosphatase 1 Verbinnen, Iris; Ferreira, Monica; Bollen, Mathieu Biochemical Society Transactions, Vol. 45, Issue 1 https://doi.org/10.1042/BST20160154	journal	February 2017
A novel rasopathy caused by recurrent de novo missense mutations inPPP1CBclosely resembles Noonan syndrome with loose anagen hair Gripp, Karen W.; Aldinger, Kimberly A.; Bennett, James T. American Journal of Medical Genetics Part A, Vol. 170, Issue 9 https://doi.org/10.1002/ajmg.a.37781	journal	June 2016
Development of a Peptide that Selectively Activates Protein Phosphatase-1 in Living Cells Chatterjee, Jayanta; Beullens, Monique; Sukackaite, Rasa Angewandte Chemie International Edition, Vol. 51, Issue 40 https://doi.org/10.1002/anie.201204308	journal	September 2012
SHOC2 and CRAF Mediate ERK1/2 Reactivation in Mutant NRAS-mediated Resistance to RAF Inhibitor Kaplan, Fred M.; Kugel, Curtis H.; Dadpey, Neda Journal of Biological Chemistry, Vol. 287, Issue 50 https://doi.org/10.1074/jbc.M112.390906	journal	December 2012
The recurrent PPP1CB mutation p.Pro49Arg in an additional Noonan-like syndrome individual: Broadening the clinical phenotype Bertola, Débora; Yamamoto, Guilherme; Buscarilli, Michelle American Journal of Medical Genetics Part A, Vol. 173, Issue 3 https://doi.org/10.1002/ajmg.a.38070	journal	February 2017
Degeneracy and Function of the Ubiquitous RV X F Motif That Mediates Binding to Protein Phosphatase-1 Wakula, Paulina; Beullens, Monique; Ceulemans, Hugo Journal of Biological Chemistry, Vol. 278, Issue 21 https://doi.org/10.1074/jbc.M300175200	journal	March 2003
A Structure is Worth a Thousand Words: New Insights for RAS and RAF Regulation Simanshu, Dhirendra K.; Morrison, Deborah K. Cancer Discovery, Vol. 12, Issue 4 https://doi.org/10.1158/2159-8290.CD-21-1494	journal	January 2022
The Molecular Basis for Substrate Specificity of the Nuclear NIPP1:PP1 Holoenzyme O'Connell, Nichole; Nichols, Scott R.; Heroes, Ewald Structure, Vol. 20, Issue 10 https://doi.org/10.1016/j.str.2012.08.003	journal	October 2012
Functions and therapeutic potential of protein phosphatase 1: Insights from mouse genetics Ferreira, Mónica; Beullens, Monique; Bollen, Mathieu Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1866, Issue 1 https://doi.org/10.1016/j.bbamcr.2018.07.019	journal	January 2019
REFMAC 5 for the refinement of macromolecular crystal structures Murshudov, Garib N.; Skubák, Pavol; Lebedev, Andrey A. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444911001314	journal	March 2011
Optimizing Expression and Solubility of Proteins in E. coli Using Modified Media and Induction Parameters Taylor, Troy; Denson, John-Paul; Esposito, Dominic Methods in Molecular Biology https://doi.org/10.1007/978-1-4939-6887-9_5	book	May 2017
An overlapping kinase and phosphatase docking site regulates activity of the retinoblastoma protein Hirschi, Alexander; Cecchini, Matthew; Steinhardt, Rachel C. Nature Structural & Molecular Biology, Vol. 17, Issue 9 https://doi.org/10.1038/nsmb.1868	journal	August 2010
SHOC2 phosphatase-dependent RAF dimerization mediates resistance to MEK inhibition in RAS-mutant cancers Jones, Greg G.; del Río, Isabel Boned; Sari, Sibel Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-10367-x	journal	June 2019
Noonan syndrome with loose anagen hair with variants in the PPP1CB gene: First familial case reported Huckstadt, Victoria; Chinton, Josefina; Gomez, Abel American Journal of Medical Genetics Part A, Vol. 185, Issue 4 https://doi.org/10.1002/ajmg.a.62089	journal	January 2021
Dissecting the sequence determinants for dephosphorylation by the catalytic subunits of phosphatases PP1 and PP2A Hoermann, Bernhard; Kokot, Thomas; Helm, Dominic Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-17334-x	journal	July 2020
Functional Integration of the Conserved Domains of Shoc2 Scaffold Jeoung, Myoungkun; Abdelmoti, Lina; Jang, Eun Ryoung PLoS ONE, Vol. 8, Issue 6 https://doi.org/10.1371/journal.pone.0066067	journal	June 2013
The Ki-67 and RepoMan mitotic phosphatases assemble via an identical, yet novel mechanism Kumar, Ganesan Senthil; Gokhan, Ezgi; De Munter, Sofie eLife, Vol. 5 https://doi.org/10.7554/eLife.16539	journal	August 2016
A Phosphatase Holoenzyme Comprised of Shoc2/Sur8 and the Catalytic Subunit of PP1 Functions as an M-Ras Effector to Modulate Raf Activity Rodriguez-Viciana, Pablo; Oses-Prieto, Juan; Burlingame, Alma Molecular Cell, Vol. 22, Issue 2 https://doi.org/10.1016/j.molcel.2006.03.027	journal	April 2006
Stabilization of Sur8 via PKCα/δ degradation promotes transformation and migration of colorectal cancer cells Lee, Kug Hwa; Jeong, Woo-Jeong; Cha, Pu-Hyeon Oncotarget, Vol. 8, Issue 70 https://doi.org/10.18632/oncotarget.23313	journal	December 2017
Endothelial SUR-8 acts in an ERK-independent pathway during atrioventricular cushion development Yi, Jing; Chen, Muyun; Wu, Xiaohui Developmental Dynamics, Vol. 239, Issue 7 https://doi.org/10.1002/dvdy.22343	journal	June 2010
Macromolecular structure determination using X-rays, neutrons and electrons: recent developments in Phenix Liebschner, Dorothee; Afonine, Pavel V.; Baker, Matthew L. Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 10 https://doi.org/10.1107/S2059798319011471	journal	October 2019
Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910045749	journal	March 2011
Structural basis of protein phosphatase 1 regulation Terrak, Mohammed; Kerff, Frederic; Langsetmo, Knut Nature, Vol. 429, Issue 6993 https://doi.org/10.1038/nature02582	journal	May 2004
Classical RAS proteins are not essential for paradoxical ERK activation induced by RAF inhibitors Lai, Lick Pui; Fer, Nicole; Burgan, William Proceedings of the National Academy of Sciences, Vol. 119, Issue 5 https://doi.org/10.1073/pnas.2113491119	journal	January 2022
A Leucine-Rich Repeat Protein Provides a SHOC2 the RAS Circuit: a Structure-Function Perspective Kwon, Jason J.; Hahn, William C. Molecular and Cellular Biology, Vol. 41, Issue 4 https://doi.org/10.1128/MCB.00627-20	journal	March 2021
Homogeneous Dual-Parametric-Coupled Assay for Simultaneous Nucleotide Exchange and KRAS/RAF-RBD Interaction Monitoring Kopra, Kari; Vuorinen, Emmiliisa; Abreu-Blanco, Maria Analytical Chemistry, Vol. 92, Issue 7 https://doi.org/10.1021/acs.analchem.9b05126	journal	February 2020
SHOC2 Is a Critical Modulator of Sensitivity to EGFR–TKIs in Non–Small Cell Lung Cancer Cells Terai, Hideki; Hamamoto, Junko; Emoto, Katsura Molecular Cancer Research, Vol. 19, Issue 2 https://doi.org/10.1158/1541-7786.MCR-20-0664	journal	February 2021
Ras and relatives—job sharing and networking keep an old family together Ehrhardt, Annette; Ehrhardt, Götz R. A.; Guo, Xuecui Experimental Hematology, Vol. 30, Issue 10 https://doi.org/10.1016/S0301-472X(02)00904-9	journal	October 2002
Molecular basis for substrate specificity of the Phactr1/PP1 phosphatase holoenzyme Fedoryshchak, Roman O.; Přechová, Magdalena; Butler, Abbey M. eLife, Vol. 9 https://doi.org/10.7554/eLife.61509	journal	September 2020
SHOC2–MRAS–PP1 complex positively regulates RAF activity and contributes to Noonan syndrome pathogenesis Young, Lucy C.; Hartig, Nicole; Boned del Río, Isabel Proceedings of the National Academy of Sciences, Vol. 115, Issue 45 https://doi.org/10.1073/pnas.1720352115	journal	October 2018
Targeting Alterations in the RAF–MEK Pathway Yaeger, Rona; Corcoran, Ryan B. Cancer Discovery, Vol. 9, Issue 3 https://doi.org/10.1158/2159-8290.CD-18-1321	journal	February 2019
Polycistronic baculovirus expression of SUGT1 enables high-yield production of recombinant leucine-rich repeat proteins and protein complexes Snead, Kelly; Wall, Vanessa; Ambrose, Hannah Protein Expression and Purification, Vol. 193 https://doi.org/10.1016/j.pep.2022.106061	journal	May 2022
Further evidence that variants in PPP1CB cause a rasopathy similar to Noonan syndrome with loose anagen hair Zambrano, Regina M.; Marble, Michael; Chalew, Stuart A. American Journal of Medical Genetics Part A, Vol. 173, Issue 2 https://doi.org/10.1002/ajmg.a.38056	journal	November 2016
Synthetic Lethal Interaction of SHOC2 Depletion with MEK Inhibition in RAS-Driven Cancers Sulahian, Rita; Kwon, Jason J.; Walsh, Katherine H. Cell Reports, Vol. 29, Issue 1 https://doi.org/10.1016/j.celrep.2019.08.090	journal	October 2019
SHOC2 complex-driven RAF dimerization selectively contributes to ERK pathway dynamics Boned del Río, Isabel; Young, Lucy C.; Sari, Sibel Proceedings of the National Academy of Sciences, Vol. 116, Issue 27 https://doi.org/10.1073/pnas.1902658116	journal	June 2019
Characterization of R-Ras3/M-Ras Null Mice Reveals a Potential Role in Trophic Factor Signaling Nuñez Rodriguez, Nelson; Lee, Ivy N. L.; Banno, Asoka Molecular and Cellular Biology, Vol. 26, Issue 19 https://doi.org/10.1128/MCB.00476-06	journal	October 2006
Impaired Binding of 14-3-3 to C-RAF in Noonan Syndrome Suggests New Approaches in Diseases with Increased Ras Signaling Molzan, Manuela; Schumacher, Benjamin; Ottmann, Corinna Molecular and Cellular Biology, Vol. 30, Issue 19 https://doi.org/10.1128/MCB.01636-09	journal	October 2010
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
Crystal Structure of M-Ras Reveals a GTP-bound “Off” State Conformation of Ras Family Small GTPases Ye, Min; Shima, Fumi; Muraoka, Shin Journal of Biological Chemistry, Vol. 280, Issue 35 https://doi.org/10.1074/jbc.M505503200	journal	June 2005
SDS22 selectively recognizes and traps metal-deficient inactive PP1 Choy, Meng S.; Moon, Thomas M.; Ravindran, Rini Proceedings of the National Academy of Sciences, Vol. 116, Issue 41 https://doi.org/10.1073/pnas.1908718116	journal	September 2019
Disease model discovery from 3,328 gene knockouts by The International Mouse Phenotyping Consortium Meehan, Terrence F.; Conte, Nathalie; West, David B. Nature Genetics, Vol. 49, Issue 8 https://doi.org/10.1038/ng.3901	journal	June 2017
How good are my data and what is the resolution? Evans, Philip R.; Murshudov, Garib N. Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 7 https://doi.org/10.1107/S0907444913000061	journal	June 2013
KRAS interaction with RAF1 RAS-binding domain and cysteine-rich domain provides insights into RAS-mediated RAF activation Tran, Timothy H.; Chan, Albert H.; Young, Lucy C. Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-21422-x	journal	February 2021
Structural and Functional Analysis of the GADD34:PP1 eIF2α Phosphatase Choy, Meng S.; Yusoff, Permeen; Lee, Irene C. Cell Reports, Vol. 11, Issue 12 https://doi.org/10.1016/j.celrep.2015.05.043	journal	June 2015
An MRAS, SHOC2, and SCRIB Complex Coordinates ERK Pathway Activation with Polarity and Tumorigenic Growth Young, Lucy C.; Hartig, Nicole; Muñoz-Alegre, Marta Molecular Cell, Vol. 52, Issue 5 https://doi.org/10.1016/j.molcel.2013.10.004	journal	December 2013
Structural insights into the BRAF monomer-to-dimer transition mediated by RAS binding Martinez Fiesco, Juliana A.; Durrant, David E.; Morrison, Deborah K. Nature Communications, Vol. 13, Issue 1 https://doi.org/10.1038/s41467-022-28084-3	journal	January 2022
Flexible docking of peptides to proteins using CABS‐dock Kurcinski, Mateusz; Badaczewska‐Dawid, Aleksandra; Kolinski, Michal Protein Science, Vol. 29, Issue 1 https://doi.org/10.1002/pro.3771	journal	November 2019
RAS Proteins and Their Regulators in Human Disease Simanshu, Dhirendra K.; Nissley, Dwight V.; McCormick, Frank Cell, Vol. 170, Issue 1 https://doi.org/10.1016/j.cell.2017.06.009	journal	June 2017
Protein phosphatase 1 catalytic isoforms: specificity toward interacting proteins Korrodi-Gregório, Luís; Esteves, Sara L. C.; Fardilha, Margarida Translational Research, Vol. 164, Issue 5 https://doi.org/10.1016/j.trsl.2014.07.001	journal	November 2014
Docking Motif-Guided Mapping of the Interactome of Protein Phosphatase-1 Hendrickx, Annick; Beullens, Monique; Ceulemans, Hugo Chemistry & Biology, Vol. 16, Issue 4 https://doi.org/10.1016/j.chembiol.2009.02.012	journal	April 2009
Genome Assembly and Annotation of the Trichoplusia ni Tni-FNL Insect Cell Line Enabled by Long-Read Technologies Talsania, Keyur; Mehta, Monika; Raley, Castle Genes, Vol. 10, Issue 2 https://doi.org/10.3390/genes10020079	journal	January 2019
PDE6D Inhibitors with a New Design Principle Selectively Block K-Ras Activity Siddiqui, Farid A.; Alam, Catharina; Rosenqvist, Petja ACS Omega, Vol. 5, Issue 1 https://doi.org/10.1021/acsomega.9b03639	journal	December 2019
Structural Basis for Regulation of Protein Phosphatase 1 by Inhibitor-2 Hurley, Thomas D.; Yang, Jie; Zhang, Lili Journal of Biological Chemistry, Vol. 282, Issue 39 https://doi.org/10.1074/jbc.M703472200	journal	September 2007
Spinophilin directs protein phosphatase 1 specificity by blocking substrate binding sites Ragusa, Michael J.; Dancheck, Barbara; Critton, David A. Nature Structural & Molecular Biology, Vol. 17, Issue 4 https://doi.org/10.1038/nsmb.1786	journal	March 2010
Regulation of RAF protein kinases in ERK signalling Lavoie, Hugo; Therrien, Marc Nature Reviews Molecular Cell Biology, Vol. 16, Issue 5 https://doi.org/10.1038/nrm3979	journal	April 2015
Structural basis for protein phosphatase 1 regulation and specificity: Protein phosphatase 1 regulation and specificity Peti, Wolfgang; Nairn, Angus C.; Page, Rebecca FEBS Journal, Vol. 280, Issue 2 https://doi.org/10.1111/j.1742-4658.2012.08509.x	journal	February 2012
M-Ras/Shoc2 signaling modulates E-cadherin turnover and cell–cell adhesion during collective cell migration Kota, Pradeep; Terrell, Elizabeth M.; Ritt, Daniel A. Proceedings of the National Academy of Sciences, Vol. 116, Issue 9 https://doi.org/10.1073/pnas.1805919116	journal	February 2019
Identification of the substrate recruitment mechanism of the muscle glycogen protein phosphatase 1 holoenzyme Kumar, Ganesan Senthil; Choy, Meng S.; Koveal, Dorothy M. Science Advances, Vol. 4, Issue 11 https://doi.org/10.1126/sciadv.aau6044	journal	November 2018
Three-dimensional structure of the catalytic subunit of protein serine/threonine phosphatase-1 Goldberg, Jonathan; Huang, Hsien-bin; Kwon, Young-guen Nature, Vol. 376, Issue 6543 https://doi.org/10.1038/376745a0	journal	August 1995
Crystal Structure Reveals the Full Ras–Raf Interface and Advances Mechanistic Understanding of Raf Activation Cookis, Trinity; Mattos, Carla Biomolecules, Vol. 11, Issue 7 https://doi.org/10.3390/biom11070996	journal	July 2021
soc-2 encodes a leucine-rich repeat protein implicated in fibroblast growth factor receptor signaling Selfors, Laura M.; Schutzman, Jennifer L.; Borland, Christina Z. Proceedings of the National Academy of Sciences, Vol. 95, Issue 12 https://doi.org/10.1073/pnas.95.12.6903	journal	June 1998
Understanding the antagonism of retinoblastoma protein dephosphorylation by PNUTS provides insights into the PP1 regulatory code Choy, M. S.; Hieke, M.; Kumar, G. S. Proceedings of the National Academy of Sciences, Vol. 111, Issue 11 https://doi.org/10.1073/pnas.1317395111	journal	March 2014

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