Crystal Structure of Bicc1 SAM Polymer and Mapping of Interactions between the Ciliopathy-Associated Proteins Bicc1, ANKS3, and ANKS6

Rothé, Benjamin; Leettola, Catherine N.; Leal-Esteban, Lucia; Cascio, Duilio; Fortier, Simon; Isenschmid, Manuela; Bowie, James U.; Constam, Daniel B.

doi:10.1016/j.str.2017.12.002

Crystal Structure of Bicc1 SAM Polymer and Mapping of Interactions between the Ciliopathy-Associated Proteins Bicc1, ANKS3, and ANKS6

Journal Article · Wed Dec 27 23:00:00 EST 2017 · Structure

DOI:https://doi.org/10.1016/j.str.2017.12.002· OSTI ID:1548878

Rothé, Benjamin; Leettola, Catherine N.; Leal-Esteban, Lucia; Cascio, Duilio; Fortier, Simon; Isenschmid, Manuela; Bowie, James U.; Constam, Daniel B.

Head-to-tail polymers of sterile alpha motifs (SAM) can scaffold large macromolecular complexes. Several SAM-domain proteins that bind each other are mutated in patients with cystic kidneys or laterality defects, including the Ankyrin (ANK) and SAM domain-containing proteins ANKS6 and ANKS3, and the RNA-binding protein Bicc1. To address how their interactions are regulated, we first determined a high-resolution crystal structure of a Bicc1-SAM polymer, revealing a canonical SAM polymer with a high degree of flexibility in the subunit interface orientations. We further mapped interactions between full-length and distinct domains of Bicc1, ANKS3, and ANKS6. Neither ANKS3 nor ANKS6 alone formed macroscopic homopolymers in vivo. However, we report ANKS3 recruited ANKS6 to Bicc1, and the three proteins together cooperatively generated giant macromolecular complexes. Thus, the giant assemblies are shaped by SAM domains, their flanking sequences, and SAM-independent protein-protein and protein-mRNA interactions.

View Journal Article

Sponsoring Organization:: USDOE

Grant/Contract Number:: FC02-02ER63421; AC02-06CH11357

OSTI ID:: 1548878

Journal Information:: Structure, Journal Name: Structure Journal Issue: 2 Vol. 26; ISSN 0969-2126

Publisher:: ElsevierCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (49)

Two mutations in human BICC1 resulting in Wnt pathway hyperactivity associated with cystic renal dysplasia Kraus, Marine R. -C.; Clauin, Séverine; Pfister, Yvan Human Mutation, Vol. 33, Issue 1 https://doi.org/10.1002/humu.21610	journal	October 2011
Verification of protein structures: Patterns of nonbonded atomic interactions Colovos, Chris; Yeates, Todd O. Protein Science, Vol. 2, Issue 9 https://doi.org/10.1002/pro.5560020916	journal	September 1993
A human sterile alpha motif domain polymerizome Knight, Mary Jane; Leettola, Catherine; Gingery, Mari Protein Science, Vol. 20, Issue 10 https://doi.org/10.1002/pro.703	journal	August 2011
Atomic Structures of the Human Immunophilin FKBP-12 Complexes with FK506 and Rapamycin Van Duyne, Gregory D.; Standaert, Robert F.; Karplus, P. Andrew Journal of Molecular Biology, Vol. 229, Issue 1 https://doi.org/10.1006/jmbi.1993.1012	journal	January 1993
Protein composition and movements of membrane swellings associated with primary cilia Mohieldin, Ashraf M.; Haymour, Hanan S.; Lo, Shao T. Cellular and Molecular Life Sciences, Vol. 72, Issue 12 https://doi.org/10.1007/s00018-015-1838-x	journal	February 2015
Positional cloning of jcpk/bpk locus of the mouse Bryda, Elizabeth C.; Flaherty, Lorraine; Cogswell, Cathy Mammalian Genome, Vol. 14, Issue 4 https://doi.org/10.1007/s00335-002-2241-0	journal	April 2003
ANKS3 is mutated in a family with autosomal recessive laterality defect Shamseldin, Hanan E.; Yakulov, Toma Antonov; Hashem, Amal Human Genetics, Vol. 135, Issue 11 https://doi.org/10.1007/s00439-016-1712-4	journal	July 2016
Role of primary cilia in non-dividing and post-mitotic cells Walz, Gerd Cell and Tissue Research, Vol. 369, Issue 1 https://doi.org/10.1007/s00441-017-2599-7	journal	March 2017
The polycystic kidney disease-related proteins Bicc1 and SamCystin interact Stagner, Emily E.; Bouvrette, Denise J.; Cheng, Jianlin Biochemical and Biophysical Research Communications, Vol. 383, Issue 1 https://doi.org/10.1016/j.bbrc.2009.03.113	journal	May 2009
Anks3 alters the sub-cellular localization of the Nek7 kinase Ramachandran, Haribaskar; Engel, Christina; Müller, Barbara Biochemical and Biophysical Research Communications, Vol. 464, Issue 3 https://doi.org/10.1016/j.bbrc.2015.07.063	journal	August 2015
SAM Domain Polymerization Links Subnuclear Clustering of PRC1 to Gene Silencing Isono, Kyoichi; Endo, Takaho A.; Ku, Manching Developmental Cell, Vol. 26, Issue 6 https://doi.org/10.1016/j.devcel.2013.08.016	journal	September 2013
Inference of Macromolecular Assemblies from Crystalline State Krissinel, Evgeny; Henrick, Kim Journal of Molecular Biology, Vol. 372, Issue 3 https://doi.org/10.1016/j.jmb.2007.05.022	journal	September 2007
Tankyrase Requires SAM Domain-Dependent Polymerization to Support Wnt-β-Catenin Signaling Mariotti, Laura; Templeton, Catherine M.; Ranes, Michael Molecular Cell, Vol. 63, Issue 3 https://doi.org/10.1016/j.molcel.2016.06.019	journal	August 2016
NMR Structure of a Heterodimeric SAM:SAM Complex: Characterization and Manipulation of EphA2 Binding Reveal New Cellular Functions of SHIP2 Lee, Hyeong J.; Hota, Prasanta K.; Chugha, Preeti Structure, Vol. 20, Issue 1 https://doi.org/10.1016/j.str.2011.11.013	journal	January 2012
Tankyrase Sterile α Motif Domain Polymerization Is Required for Its Role in Wnt Signaling Riccio, Amanda A.; McCauley, Michael; Langelier, Marie-France Structure, Vol. 24, Issue 9 https://doi.org/10.1016/j.str.2016.06.022	journal	September 2016
Signalosome assembly by domains undergoing dynamic head-to-tail polymerization Bienz, Mariann Trends in Biochemical Sciences, Vol. 39, Issue 10 https://doi.org/10.1016/j.tibs.2014.08.006	journal	October 2014
SUMO fusions and SUMO-specific protease for efficient expression and purification of proteins Malakhov, Michael P.; Mattern, Michael R.; Malakhova, Oxana A. Journal of Structural and Functional Genomics, Vol. 5, Issue 1/2 https://doi.org/10.1023/B:JSFG.0000029237.70316.52	journal	March 2004
The SAM domain of ANKS6 has different interacting partners and mutations can induce different cystic phenotypes Bakey, Zeineb; Bihoreau, Marie-Thérèse; Piedagnel, Rémi Kidney International, Vol. 88, Issue 2 https://doi.org/10.1038/ki.2015.122	journal	August 2015
Anks3 interacts with nephronophthisis proteins and is required for normal renal development Yakulov, Toma A.; Yasunaga, Takayuki; Ramachandran, Haribaskar Kidney International, Vol. 87, Issue 6 https://doi.org/10.1038/ki.2015.17	journal	June 2015
ANKS6 is the critical activator of NEK8 kinase in embryonic situs determination and organ patterning Czarnecki, Peter G.; Gabriel, George C.; Manning, Danielle K. Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms7023	journal	January 2015
ANKS6 is a central component of a nephronophthisis module linking NEK8 to INVS and NPHP3 Hoff, Sylvia; Halbritter, Jan; Epting, Daniel Nature Genetics, Vol. 45, Issue 8 https://doi.org/10.1038/ng.2681	journal	June 2013
The centrosomal OFD1 protein interacts with the translation machinery and regulates the synthesis of specific targets Iaconis, Daniela; Monti, Maria; Renda, Mario Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-01156-x	journal	April 2017
Ciliopathies Hildebrandt, Friedhelm; Benzing, Thomas; Katsanis, Nicholas New England Journal of Medicine, Vol. 364, Issue 16 https://doi.org/10.1056/NEJMra1010172	journal	April 2011
Electrostatics of nanosystems: Application to microtubules and the ribosome Baker, N. A.; Sept, D.; Joseph, S. Proceedings of the National Academy of Sciences, Vol. 98, Issue 18, p. 10037-10041 https://doi.org/10.1073/pnas.181342398	journal	August 2001
SLP-76 Sterile α Motif (SAM) and Individual H5 α Helix Mediate Oligomer Formation for Microclusters and T-cell Activation Liu, Hebin; Thaker, Youg Raj; Stagg, Loren Journal of Biological Chemistry, Vol. 288, Issue 41 https://doi.org/10.1074/jbc.M112.424846	journal	October 2013
Clustal W and Clustal X version 2.0 Larkin, M. A.; Blackshields, G.; Brown, N. P. Bioinformatics, Vol. 23, Issue 21, p. 2947-2948 https://doi.org/10.1093/bioinformatics/btm404	journal	September 2007
Bicc1 links the regulation of cAMP signaling in polycystic kidneys to microRNA-induced gene silencing Piazzon, Nathalie; Maisonneuve, Charlotte; Guilleret, Isabelle Journal of Molecular Cell Biology, Vol. 4, Issue 6 https://doi.org/10.1093/jmcb/mjs027	journal	May 2012
Characterization of the interaction between protein Snu13p/15.5K and the Rsa1p/NUFIP factor and demonstration of its functional importance for snoRNP assembly Rothé, Benjamin; Back, Régis; Quinternet, Marc Nucleic Acids Research, Vol. 42, Issue 3 https://doi.org/10.1093/nar/gkt1091	journal	November 2013
InterPro in 2017—beyond protein family and domain annotations Finn, Robert D.; Attwood, Teresa K.; Babbitt, Patricia C. Nucleic Acids Research, Vol. 45, Issue D1 https://doi.org/10.1093/nar/gkw1107	journal	November 2016
How do cilia organize signalling cascades? Nachury, Maxence V. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 369, Issue 1650 https://doi.org/10.1098/rstb.2013.0465	journal	September 2014
Molecular basis of PRC1 targeting to Polycomb response elements by PhoRC Frey, Felice; Sheahan, Thomas; Finkl, Katja Genes & Development, Vol. 30, Issue 9 https://doi.org/10.1101/gad.279141.116	journal	May 2016
HKL2MAP : a graphical user interface for macromolecular phasing with SHELX programs Pape, Thomas; Schneider, Thomas R. Journal of Applied Crystallography, Vol. 37, Issue 5 https://doi.org/10.1107/S0021889804018047	journal	September 2004
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
PROCHECK: a program to check the stereochemical quality of protein structures Laskowski, R. A.; MacArthur, M. W.; Moss, D. S. Journal of Applied Crystallography, Vol. 26, Issue 2 https://doi.org/10.1107/S0021889892009944	journal	April 1993
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
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
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
The ankyrin repeat as molecular architecture for protein recognition Mosavi, Leila K.; Cammett, Tobin J.; Desrosiers, Daniel C. Protein Science, Vol. 13, Issue 6 https://doi.org/10.1110/ps.03554604	journal	June 2004
Linking Crystallographic Model and Data Quality Karplus, P. A.; Diederichs, K. Science, Vol. 336, Issue 6084 https://doi.org/10.1126/science.1218231	journal	May 2012
A method to identify protein sequences that fold into a known three-dimensional structure Bowie, J.; Luthy, R.; Eisenberg, D. Science, Vol. 253, Issue 5016 https://doi.org/10.1126/science.1853201	journal	July 1991
The Many Faces of SAM Qiao, F.; Bowie, J. U. Science Signaling, Vol. 2005, Issue 286 https://doi.org/10.1126/stke.2862005re7	journal	May 2005
Bicc1 Polymerization Regulates the Localization and Silencing of Bound mRNA Rothé, Benjamin; Leal-Esteban, Lucia; Bernet, Florian Molecular and Cellular Biology, Vol. 35, Issue 19 https://doi.org/10.1128/MCB.00341-15	journal	October 2015
Characterization of the SAM domain of the PKD-related protein ANKS6 and its interaction with ANKS3 Leettola, Catherine N.; Knight, Mary; Cascio, Duilio BMC Structural Biology, Vol. 14, Issue 1 https://doi.org/10.1186/1472-6807-14-17	journal	January 2014
Bicaudal C, a novel regulator of Dvl signaling abutting RNA-processing bodies, controls cilia orientation and leftward flow Maisonneuve, Charlotte; Guilleret, Isabelle; Vick, Philipp Development, Vol. 136, Issue 17 https://doi.org/10.1242/dev.038174	journal	September 2009
ANKS3 Co-Localises with ANKS6 in Mouse Renal Cilia and Is Associated with Vasopressin Signaling and Apoptosis In Vivo in Mice Delestré, Laure; Bakey, Zeineb; Prado, Cécilia PLOS ONE, Vol. 10, Issue 9 https://doi.org/10.1371/journal.pone.0136781	journal	September 2015
Missense Mutation in Sterile α Motif of Novel Protein SamCystin is Associated with Polycystic Kidney Disease in ( cy /+) Rat Brown, Joanna H.; Bihoreau, Marie-Thérèse; Hoffmann, Sigrid Journal of the American Society of Nephrology, Vol. 16, Issue 12 https://doi.org/10.1681/ASN.2005060601	journal	October 2005
Folate-Conjugated Rapamycin Slows Progression of Polycystic Kidney Disease Shillingford, Jonathan M.; Leamon, Christopher P.; Vlahov, Iontcho R. Journal of the American Society of Nephrology, Vol. 23, Issue 10 https://doi.org/10.1681/ASN.2012040367	journal	August 2012
Mutations in ANKS6 Cause a Nephronophthisis-Like Phenotype with ESRD Taskiran, Ekim Z.; Korkmaz, Emine; Gucer, Safak Journal of the American Society of Nephrology, Vol. 25, Issue 8 https://doi.org/10.1681/ASN.2013060646	journal	March 2014

Similar Records

Tandem SAM Domain Structure of Human Caskin1: A Presynaptic, Self-Assembling Scaffold for CASK

Journal Article · Mon Feb 06 23:00:00 EST 2012 · Structure · OSTI ID:1031389

Anks3 alters the sub-cellular localization of the Nek7 kinase

Journal Article · Fri Aug 28 00:00:00 EDT 2015 · Biochemical and Biophysical Research Communications · OSTI ID:22462230

Crystal Structure of Bicc1 SAM Polymer and Mapping of Interactions between the Ciliopathy-Associated Proteins Bicc1, ANKS3, and ANKS6

Citation Formats

References (49)

Similar Records

Related Subjects