Literature DB >> 23798409

Caenorhabditis elegans centriolar protein SAS-6 forms a spiral that is consistent with imparting a ninefold symmetry.

Manuel Hilbert1, Michèle C Erat, Virginie Hachet, Paul Guichard, Iris D Blank, Isabelle Flückiger, Leanne Slater, Edward D Lowe, Georgios N Hatzopoulos, Michel O Steinmetz, Pierre Gönczy, Ioannis Vakonakis.   

Abstract

Centrioles are evolutionary conserved organelles that give rise to cilia and flagella as well as centrosomes. Centrioles display a characteristic ninefold symmetry imposed by the spindle assembly abnormal protein 6 (SAS-6) family. SAS-6 from Chlamydomonas reinhardtii and Danio rerio was shown to form ninefold symmetric, ring-shaped oligomers in vitro that were similar to the cartwheels observed in vivo during early steps of centriole assembly in most species. Here, we report crystallographic and EM analyses showing that, instead, Caenorhabotis elegans SAS-6 self-assembles into a spiral arrangement. Remarkably, we find that this spiral arrangement is also consistent with ninefold symmetry, suggesting that two distinct SAS-6 oligomerization architectures can direct the same output symmetry. Sequence analysis suggests that SAS-6 spirals are restricted to specific nematodes. This oligomeric arrangement may provide a structural basis for the presence of a central tube instead of a cartwheel during centriole assembly in these species.

Entities:  

Keywords:  SAS-5; X-ray crystallography; centriolar architecture; electron microscopy; structure

Mesh:

Substances:

Year:  2013        PMID: 23798409      PMCID: PMC3710844          DOI: 10.1073/pnas.1302721110

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  31 in total

1.  Centriole assembly requires both centriolar and pericentriolar material proteins.

Authors:  Alexander Dammermann; Thomas Müller-Reichert; Laurence Pelletier; Bianca Habermann; Arshad Desai; Karen Oegema
Journal:  Dev Cell       Date:  2004-12       Impact factor: 12.270

Review 2.  Centrosome duplication and nematodes: recent insights from an old relationship.

Authors:  Sebastian Leidel; Pierre Gönczy
Journal:  Dev Cell       Date:  2005-09       Impact factor: 12.270

3.  Mutant sensory cilia in the nematode Caenorhabditis elegans.

Authors:  L A Perkins; E M Hedgecock; J N Thomson; J G Culotti
Journal:  Dev Biol       Date:  1986-10       Impact factor: 3.582

4.  The C. elegans zyg-1 gene encodes a regulator of centrosome duplication with distinct maternal and paternal roles in the embryo.

Authors:  K F O'Connell; C Caron; K R Kopish; D D Hurd; K J Kemphues; Y Li; J G White
Journal:  Cell       Date:  2001-05-18       Impact factor: 41.582

5.  SAS-4 is a C. elegans centriolar protein that controls centrosome size.

Authors:  Matthew Kirkham; Thomas Müller-Reichert; Karen Oegema; Stephan Grill; Anthony A Hyman
Journal:  Cell       Date:  2003-02-21       Impact factor: 41.582

6.  Centriolar SAS-5 is required for centrosome duplication in C. elegans.

Authors:  Marie Delattre; Sebastian Leidel; Khursheed Wani; Karine Baumer; Jeannine Bamat; Heinke Schnabel; Richard Feichtinger; Ralf Schnabel; Pierre Gönczy
Journal:  Nat Cell Biol       Date:  2004-07       Impact factor: 28.824

7.  The Caenorhabditis elegans centrosomal protein SPD-2 is required for both pericentriolar material recruitment and centriole duplication.

Authors:  Laurence Pelletier; Nurhan Ozlü; Eva Hannak; Carrie Cowan; Bianca Habermann; Martine Ruer; Thomas Müller-Reichert; Anthony A Hyman
Journal:  Curr Biol       Date:  2004-05-25       Impact factor: 10.834

8.  Centrosome maturation and duplication in C. elegans require the coiled-coil protein SPD-2.

Authors:  Catherine A Kemp; Kevin R Kopish; Peder Zipperlen; Julie Ahringer; Kevin F O'Connell
Journal:  Dev Cell       Date:  2004-04       Impact factor: 12.270

9.  SAS-4 is essential for centrosome duplication in C elegans and is recruited to daughter centrioles once per cell cycle.

Authors:  Sebastian Leidel; Pierre Gönczy
Journal:  Dev Cell       Date:  2003-03       Impact factor: 12.270

10.  Caenorhabditis elegans spermatozoan locomotion: amoeboid movement with almost no actin.

Authors:  G A Nelson; T M Roberts; S Ward
Journal:  J Cell Biol       Date:  1982-01       Impact factor: 10.539

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  28 in total

Review 1.  Centrosome function and assembly in animal cells.

Authors:  Paul T Conduit; Alan Wainman; Jordan W Raff
Journal:  Nat Rev Mol Cell Biol       Date:  2015-09-16       Impact factor: 94.444

2.  Quantitative immunofluorescence assay to measure the variation in protein levels at centrosomes.

Authors:  Shubhra Majumder; Harold A Fisk
Journal:  J Vis Exp       Date:  2014-12-20       Impact factor: 1.355

Review 3.  Centriole structure.

Authors:  Mark Winey; Eileen O'Toole
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2014-09-05       Impact factor: 6.237

4.  SAS-6 engineering reveals interdependence between cartwheel and microtubules in determining centriole architecture.

Authors:  Manuel Hilbert; Akira Noga; Daniel Frey; Virginie Hamel; Paul Guichard; Sebastian H W Kraatz; Moritz Pfreundschuh; Sarah Hosner; Isabelle Flückiger; Rolf Jaussi; Mara M Wieser; Katherine M Thieltges; Xavier Deupi; Daniel J Müller; Richard A Kammerer; Pierre Gönczy; Masafumi Hirono; Michel O Steinmetz
Journal:  Nat Cell Biol       Date:  2016-03-21       Impact factor: 28.824

5.  The ubiquitin ligase FBXW7 targets the centriolar assembly protein HsSAS-6 for degradation and thereby regulates centriole duplication.

Authors:  Binshad Badarudeen; Ria Gupta; Sreeja V Nair; Aneesh Chandrasekharan; Tapas K Manna
Journal:  J Biol Chem       Date:  2020-02-21       Impact factor: 5.157

6.  The mechanism of dynein light chain LC8-mediated oligomerization of the Ana2 centriole duplication factor.

Authors:  Lauren K Slevin; Erin M Romes; Mary G Dandulakis; Kevin C Slep
Journal:  J Biol Chem       Date:  2014-06-11       Impact factor: 5.157

Review 7.  The centrosome and its duplication cycle.

Authors:  Jingyan Fu; Iain M Hagan; David M Glover
Journal:  Cold Spring Harb Perspect Biol       Date:  2015-02-02       Impact factor: 10.005

8.  The homo-oligomerisation of both Sas-6 and Ana2 is required for efficient centriole assembly in flies.

Authors:  Matthew A Cottee; Nadine Muschalik; Steven Johnson; Joanna Leveson; Jordan W Raff; Susan M Lea
Journal:  Elife       Date:  2015-05-23       Impact factor: 8.140

9.  Gorab is a Golgi protein required for structure and duplication of Drosophila centrioles.

Authors:  Levente Kovacs; Jennifer Chao-Chu; Sandra Schneider; Marco Gottardo; George Tzolovsky; Nikola S Dzhindzhev; Maria Giovanna Riparbelli; Giuliano Callaini; David M Glover
Journal:  Nat Genet       Date:  2018-06-11       Impact factor: 38.330

10.  Tuning SAS-6 architecture with monobodies impairs distinct steps of centriole assembly.

Authors:  Georgios N Hatzopoulos; Tim Kükenshöner; Niccolò Banterle; Tatiana Favez; Isabelle Flückiger; Virginie Hamel; Santiago Andany; Georg E Fantner; Oliver Hantschel; Pierre Gönczy
Journal:  Nat Commun       Date:  2021-06-21       Impact factor: 14.919

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