Home LiteratureArticle Details
PMID: 18299348 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

SAS-4 is recruited to a dynamic structure in newly forming centrioles that is stabilized by the gamma-tubulin-mediated addition of centriolar microtubules.

The Journal of cell biology ·Vol. 180 ·No. 4 ·2008-02-25 ·Pages 771-85

Dammermann A, Maddox PS, Desai A, Oegema K

Abstract

Centrioles are surrounded by pericentriolar material (PCM), which is proposed to promote new centriole assembly by concentrating gamma-tubulin. Here, we quantitatively monitor new centriole assembly in living Caenorhabditis elegans embryos, focusing on the conserved components SAS-4 and SAS-6. We show that SAS-4 and SAS-6 are coordinately recruited to the site of new centriole assembly and reach their maximum levels during S phase. Centriolar SAS-6 is subsequently reduced by a mechanism intrinsic to the early assembly pathway that does not require progression into mitosis. Centriolar SAS-4 remains in dynamic equilibrium with the cytoplasmic pool until late prophase, when it is stably incorporated in a step that requires gamma-tubulin and microtubule assembly. These results indicate that gamma-tubulin in the PCM stabilizes the nascent daughter centriole by promoting microtubule addition to its outer wall. Such a mechanism may help restrict new centriole assembly to the vicinity of preexisting parent centrioles that recruit PCM.

MeSH Terms
Animals Caenorhabditis elegans/metabolism,ultrastructure Caenorhabditis elegans Proteins/metabolism Cell Cycle Proteins/metabolism Cell Differentiation/physiology Centrioles/metabolism,ultrastructure Embryo, Nonmammalian/cytology,metabolism Macromolecular Substances/metabolism Microtubules/metabolism,ultrastructure Protein Transport/physiology Species Specificity Spindle Apparatus/metabolism,ultrastructure Tubulin/metabolism
Chemicals
Caenorhabditis elegans Proteins Cell Cycle Proteins Macromolecular Substances SAS-4 protein, C elegans SAS-6 protein, C elegans Tubulin
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Dammermann Alexander
Department of Cellular and Molecular Medicine, Ludwig Institute for Cancer Research, University of California, San Diego, La Jolla, CA 92093, USA. adammermann@ucsd.edu
Maddox Paul S
Desai Arshad
Oegema Karen
References (41)
41 references, click to expand
  1. Overexpressing centriole-replication proteins in vivo induces centriole overduplication and de novo formation.
    Curr Biol. 2007 May 15;17(10):834-43 PMID: 17475495
  2. Cell division.
    WormBook. 2006 Jan 19;:1-40 PMID: 18050484
  3. DSAS-6 organizes a tube-like centriole precursor, and its absence suggests modularity in centriole assembly.
    Curr Biol. 2007 Sep 4;17(17):1465-72 PMID: 17689959
  4. Gamma-tubulin complexes and microtubule nucleation.
    Curr Opin Struct Biol. 2001 Apr;11(2):174-81 PMID: 11297925
  5. SAS-6 defines a protein family required for centrosome duplication in C. elegans and in human cells.
    Nat Cell Biol. 2005 Feb;7(2):115-25 PMID: 15665853
  6. Elongation of centriolar microtubule triplets contributes to the formation of the mitotic spindle in gamma-tubulin-depleted cells.
    J Cell Sci. 2004 Nov 1;117(Pt 23):5497-507 PMID: 15479719
  7. Checkpoint silencing during the DNA damage response in Caenorhabditis elegans embryos.
    J Cell Biol. 2006 Mar 27;172(7):999-1008 PMID: 16549501
  8. Centriolar SAS-5 is required for centrosome duplication in C. elegans.
    Nat Cell Biol. 2004 Jul;6(7):656-64 PMID: 15232593
  9. Differential role of CENP-A in the segregation of holocentric C. elegans chromosomes during meiosis and mitosis.
    Nat Cell Biol. 2005 Dec;7(12):1248-55 PMID: 16273096
  10. Katanin controls mitotic and meiotic spindle length.
    J Cell Biol. 2006 Dec 18;175(6):881-91 PMID: 17178907
  11. Plk4-induced centriole biogenesis in human cells.
    Dev Cell. 2007 Aug;13(2):190-202 PMID: 17681131
  12. DNA synthesis and the control of embryonic gene expression in C. elegans.
    Cell. 1988 May 20;53(4):589-99 PMID: 3131016
  13. Centriole disassembly in vivo and its effect on centrosome structure and function in vertebrate cells.
    J Cell Biol. 1998 Dec 14;143(6):1575-89 PMID: 9852152
  14. Aurora-A kinase is required for centrosome maturation in Caenorhabditis elegans.
    J Cell Biol. 2001 Dec 24;155(7):1109-16 PMID: 11748251
  15. The formation of basal bodies (centrioles) in the Rhesus monkey oviduct.
    J Cell Biol. 1971 Jul;50(1):10-34 PMID: 4998200
  16. SAS-4 is essential for centrosome duplication in C elegans and is recruited to daughter centrioles once per cell cycle.
    Dev Cell. 2003 Mar;4(3):431-9 PMID: 12636923
  17. Molecular analysis of mitotic chromosome condensation using a quantitative time-resolved fluorescence microscopy assay.
    Proc Natl Acad Sci U S A. 2006 Oct 10;103(41):15097-102 PMID: 17005720
  18. Myosin domain evolution and the primary divergence of eukaryotes.
    Nature. 2005 Aug 25;436(7054):1113-8 PMID: 16121172
  19. Basal body duplication in Paramecium requires gamma-tubulin.
    Curr Biol. 1999 Jan 14;9(1):43-6 PMID: 9889124
  20. Mode of centriole duplication and distribution.
    J Cell Biol. 1990 May;110(5):1599-605 PMID: 2335566
  21. NEDD1-dependent recruitment of the gamma-tubulin ring complex to the centrosome is necessary for centriole duplication and spindle assembly.
    J Cell Biol. 2006 Feb 13;172(4):505-15 PMID: 16461362
  22. SAS-4 is a C. elegans centriolar protein that controls centrosome size.
    Cell. 2003 Feb 21;112(4):575-87 PMID: 12600319
  23. Tetrahymena thermophila contains a conventional gamma-tubulin that is differentially required for the maintenance of different microtubule-organizing centers.
    J Cell Biol. 2002 Sep 30;158(7):1195-206 PMID: 12356864
  24. Functional analysis of kinetochore assembly in Caenorhabditis elegans.
    J Cell Biol. 2001 Jun 11;153(6):1209-26 PMID: 11402065
  25. Centrosome biogenesis and function: centrosomics brings new understanding.
    Nat Rev Mol Cell Biol. 2007 Jun;8(6):451-63 PMID: 17505520
  26. The C. elegans zyg-1 gene encodes a regulator of centrosome duplication with distinct maternal and paternal roles in the embryo.
    Cell. 2001 May 18;105(4):547-58 PMID: 11371350
  27. Centriole assembly requires both centriolar and pericentriolar material proteins.
    Dev Cell. 2004 Dec;7(6):815-29 PMID: 15572125
  28. A microtubule-independent role for centrosomes and aurora a in nuclear envelope breakdown.
    Dev Cell. 2007 Apr;12(4):515-29 PMID: 17419991
  29. Long-lost relatives reappear: identification of new members of the tubulin superfamily.
    Curr Opin Microbiol. 2003 Dec;6(6):634-40 PMID: 14662361
  30. The kinetically dominant assembly pathway for centrosomal asters in Caenorhabditis elegans is gamma-tubulin dependent.
    J Cell Biol. 2002 May 13;157(4):591-602 PMID: 12011109
  31. Sequential protein recruitment in C. elegans centriole formation.
    Curr Biol. 2006 Sep 19;16(18):1844-9 PMID: 16979563
  32. SAK/PLK4 is required for centriole duplication and flagella development.
    Curr Biol. 2005 Dec 20;15(24):2199-207 PMID: 16326102
  33. A combined approach for the localization and tandem affinity purification of protein complexes from metazoans.
    Sci STKE. 2005 Jan 11;2005(266):pl1 PMID: 15644491
  34. Molecular characterization of centriole assembly in ciliated epithelial cells.
    J Cell Biol. 2007 Jul 2;178(1):31-42 PMID: 17606865
  35. Flies without centrioles.
    Cell. 2006 Jun 30;125(7):1375-86 PMID: 16814722
  36. Centriole assembly in Caenorhabditis elegans.
    Nature. 2006 Nov 30;444(7119):619-23 PMID: 17136092
  37. What is the function of centrioles?
    J Cell Biochem. 2007 Mar 1;100(4):916-22 PMID: 17115414
  38. Centrosome maturation and mitotic spindle assembly in C. elegans require SPD-5, a protein with multiple coiled-coil domains.
    Dev Cell. 2002 Nov;3(5):673-84 PMID: 12431374
  39. Regulated HsSAS-6 levels ensure formation of a single procentriole per centriole during the centrosome duplication cycle.
    Dev Cell. 2007 Aug;13(2):203-13 PMID: 17681132
  40. Revisiting the role of the mother centriole in centriole biogenesis.
    Science. 2007 May 18;316(5827):1046-50 PMID: 17463247
  41. The Polo kinase Plk4 functions in centriole duplication.
    Nat Cell Biol. 2005 Nov;7(11):1140-6 PMID: 16244668
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
1540-8140
DOI
10.1083/jcb.200709102
Email
adammermann@ucsd.edu
Published
2008-02-25
Pages
771-85
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2265562
Subset
IM
Grants
NIGMS NIH HHS · R01 GM074207 · United States
NIGMS NIH HHS · R01-GM074207 · United States
External Links
PubMed source DOI: 10.1083/jcb.200709102 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2