Revisiting the Role of the Mother Centriole in Centriole Biogenesis

Centrioles duplicate once in each cell division cycle through so-called templated or canonical duplication. SAK, also called PLK4 (SAK/PLK4), a kinase implicated in tumor development, is an upstream regulator of canonical biogenesis necessary for centriole formation. We found that overexpression of SAK/PLK4 could induce amplification of centrioles in Drosophila embryos and their de novo formation in unfertilized eggs. Both processes required the activity of DSAS-6 and DSAS-4, two molecules required for canonical duplication. Thus, centriole biogenesis is a template-free self-assembly process triggered and regulated by molecules that ordinarily associate with the existing centriole. The mother centriole is not a bona fide template but a platform for a set of regulatory molecules that catalyzes and regulates daughter centriole assembly.

[1]  K. Kemphues,et al.  The C. elegans zyg-1 Gene Encodes a Regulator of Centrosome Duplication with Distinct Maternal and Paternal Roles in the Embryo , 2001, Cell.

[2]  C. Mollinari,et al.  Centrosomes and microtubule organisation during Drosophila development. , 1998, Journal of cell science.

[3]  AC Tose.  Cell , 1993, Cell.

[4]  M. Bornens,et al.  The centrosome-nucleus complex and microtubule organization in the Drosophila oocyte , 2006, Development.

[5]  C. Sunkel,et al.  Maternal expression of the checkpoint protein BubR1 is required for synchrony of syncytial nuclear divisions and polar body arrest in Drosophila melanogaster , 2005, Development.

[6]  W. Marshall,et al.  Kinetics and regulation of de novo centriole assembly Implications for the mechanism of centriole duplication , 2001, Current Biology.

[7]  L. Lehmann,et al.  SAK/PLK4 Is Required for Centriole Duplication and Flagella Development , 2005, Current Biology.

[8]  Dominant-negative mutant dynein allows spontaneous centrosome assembly, uncouples chromosome and centrosome cycles , 2001, Current Biology.

[9]  A. Mahowald,et al.  INTERCELLULAR MIGRATION OF CENTRIOLES IN THE GERMARIUM OF DROSOPHILA MELANOGASTER , 1970, The Journal of cell biology.

[10]  Christopher J. Wilkinson,et al.  The Polo kinase Plk4 functions in centriole duplication , 2005, Nature Cell Biology.

[11]  A. Hyman,et al.  Centriole assembly in Caenorhabditis elegans , 2006, Nature.

[12]  Eric Karsenti,et al.  Gradients in the self-organization of the mitotic spindle. , 2006, Trends in cell biology.

[13]  Sebastian A. Leidel,et al.  SAS-4 is essential for centrosome duplication in C elegans and is recruited to daughter centrioles once per cell cycle. , 2003, Developmental cell.

[14]  R. Rosenfeld.  Nature , 2009, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[15]  D. Glover,et al.  The gnu mutation of Drosophila causes inappropriate DNA synthesis in unfertilized and fertilized eggs. , 1987, Genes & development.

[16]  W. Marshall,et al.  What is the function of centrioles? , 2007, Journal of cellular biochemistry.

[17]  P. Gönczy,et al.  The arithmetic of centrosome biogenesis , 2004, Journal of Cell Science.

[18]  T. Orr-Weaver,et al.  The Drosophila plutonium and pan gu genes regulate entry into S phase at fertilization , 1991, Cell.

[19]  T. Date,et al.  Distribution of PCNA in Drosophila embryo during nuclear division cycles. , 1991, Journal of cell science.

[20]  B. McEwen,et al.  The de novo centriole assembly pathway in HeLa cells: cell cycle progression and centriole assembly/maturation. , 2005, The Journal of cell biology.

[21]  G. Borisy,et al.  Mode of centriole duplication and distribution , 1990, The Journal of cell biology.

[22]  M. Riparbelli,et al.  Drosophila parthenogenesis: a model for de novo centrosome assembly. , 2003, Developmental biology.

[23]  Anthony A. Hyman,et al.  SAS-4 Is a C. elegans Centriolar Protein that Controls Centrosome Size , 2003, Cell.

[24]  Sebastian A. Leidel,et al.  SAS-6 defines a protein family required for centrosome duplication in C. elegans and in human cells , 2005, Nature Cell Biology.

[25]  J. Dennis,et al.  Sak, a murine protein-serine/threonine kinase that is related to the Drosophila polo kinase and involved in cell proliferation. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[26]  J. Dennis,et al.  Plk4 haploinsufficiency causes mitotic infidelity and carcinogenesis , 2005, Nature Genetics.

[27]  Tien Hsu,et al.  RNA-dependent integrin α3 protein localization regulated by the Muscleblind-like protein MLP1 , 2005, Nature Cell Biology.

[28]  J. Raff,et al.  Flies without Centrioles , 2006, Cell.

[29]  R. Wollman,et al.  Genes Required for Mitotic Spindle Assembly in Drosophila S2 Cells , 2007, Science.

[30]  M. Martinez-Campos,et al.  The Drosophila pericentrin-like protein is essential for cilia/flagella function, but appears to be dispensable for mitosis , 2004, The Journal of cell biology.

[31]  Bianca Habermann,et al.  Centriole assembly requires both centriolar and pericentriolar material proteins. , 2004, Developmental cell.

[32]  P. Gönczy,et al.  Sequential Protein Recruitment in C. elegans Centriole Formation , 2006, Current Biology.