The fully linked HTML version of this article has now been published.
Development ePress online publication date 12 Oct 2005
doi: 10.1242/dev.02060
Research article
A conserved RNA-protein complex component involved in physiological germline apoptosis regulation in C. elegans
Peter R. Boag,
Akira Nakamura,
and
T. Keith Blackwell*
* Author for correspondence (e-mail: keith.blackwell{at}joslin.harvard.edu)
Two conserved features of oogenesis are the accumulation of translationally quiescent mRNA, and a high rate of stage-specific apoptosis. Little is understood about the function of this cell death. In C. elegans, apoptosis occurring through a specific 'physiological' pathway normally claims about half of all developing oocytes. The frequency of this germ cell death is dramatically increased by a lack of the RNA helicase CGH-1, orthologs of which are involved in translational control in oocytes and decapping-dependent mRNA degradation in yeast processing (P) bodies. Here, we describe a predicted RNA-binding protein, CAR-1, that associates with CGH-1 and Y-box proteins within a conserved germline RNA-protein (RNP) complex, and in cytoplasmic particles in the gonad and early embryo. The CGH-1/CAR-1 interaction is conserved in Drosophila oocytes. When car-1 expression is depleted by RNA interference (RNAi), physiological apoptosis is increased, brood size is modestly reduced, and early embryonic cytokinesis is abnormal. Surprisingly, if apoptosis is prevented car-1(RNAi) animals are characterized by a progressive oogenesis defect that leads rapidly to gonad failure. Elevated germ cell death similarly compensates for lack of the translational regulator CPB-3 (CPEB), orthologs of which function together with CGH-1 in diverse organisms. We conclude that CAR-1 is of critical importance for oogenesis, that the association between CAR-1 and CGH-1 has been conserved, and that the regulation of physiological germ cell apoptosis is specifically influenced by certain functions of the CGH-1/CAR-1 RNP complex. We propose that this cell death pathway facilitates the formation of functional oocytes, possibly by monitoring specific cytoplasmic events during oogenesis.

CiteULike
Complore
Connotea
Del.icio.us
Digg
Reddit
Technorati
Twitter What's this?
This article has been cited by other articles:

|
 |

|
 |
 
F. Tritschler, A. Eulalio, S. Helms, S. Schmidt, M. Coles, O. Weichenrieder, E. Izaurralde, and V. Truffault
Similar Modes of Interaction Enable Trailer Hitch and EDC3 To Associate with DCP1 and Me31B in Distinct Protein Complexes
Mol. Cell. Biol.,
November 1, 2008;
28(21):
6695 - 6708.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. L. Noble, B. L. Allen, L. K. Goh, K. Nordick, and T. C. Evans
Maternal mRNAs are regulated by diverse P body-related mRNP granules during early Caenorhabditis elegans development
J. Cell Biol.,
August 11, 2008;
182(3):
559 - 572.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. R. Boag, A. Atalay, S. Robida, V. Reinke, and T. K. Blackwell
Protection of specific maternal messenger RNAs by the P body protein CGH-1 (Dhh1/RCK) during Caenorhabditis elegans oogenesis
J. Cell Biol.,
August 11, 2008;
182(3):
543 - 557.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Nykamp, M.-H. Lee, and J. Kimble
C. elegans La-related protein, LARP-1, localizes to germline P bodies and attenuates Ras-MAPK signaling during oogenesis
RNA,
July 1, 2008;
14(7):
1378 - 1389.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. Minshall, M. H. Reiter, D. Weil, and N. Standart
CPEB Interacts with an Ovary-specific eIF4E and 4E-T in Early Xenopus Oocytes
J. Biol. Chem.,
December 28, 2007;
282(52):
37389 - 37401.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Strome and R. Lehmann
Germ Versus Soma Decisions: Lessons from Flies and Worms
Science,
April 20, 2007;
316(5823):
392 - 393.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. E. Pepling, J. E. Wilhelm, A. L. O'Hara, G. W. Gephardt, and A. C. Spradling
Mouse oocytes within germ cell cysts and primordial follicles contain a Balbiani body
PNAS,
January 2, 2007;
104(1):
187 - 192.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. J. Tanaka, K. Ogawa, M. Takagi, N. Imamoto, K. Matsumoto, and M. Tsujimoto
RAP55, a Cytoplasmic mRNP Component, Represses Translation in Xenopus Oocytes
J. Biol. Chem.,
December 29, 2006;
281(52):
40096 - 40106.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. R. DeBella, A. Hayashi, and L. S. Rose
LET-711, the Caenorhabditis elegans NOT1 Ortholog, Is Required for Spindle Positioning and Regulation of Microtubule Length in Embryos
Mol. Biol. Cell,
November 1, 2006;
17(11):
4911 - 4924.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. A. Kritikou, S. Milstein, P.-O. Vidalain, G. Lettre, E. Bogan, K. Doukoumetzidis, P. Gray, T. G. Chappell, M. Vidal, and M. O. Hengartner
C. elegans GLA-3 is a novel component of the MAP kinase MPK-1 signaling pathway required for germ cell survival.
Genes & Dev.,
August 15, 2006;
20(16):
2279 - 2292.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Weston and J. Sommerville
Xp54 and related (DDX6-like) RNA helicases: roles in messenger RNP assembly, translation regulation and RNA degradation
Nucleic Acids Res.,
June 14, 2006;
34(10):
3082 - 3094.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. J. Decker and R. Parker
CAR-1 and Trailer hitch: driving mRNP granule function at the ER?
J. Cell Biol.,
April 24, 2006;
173(2):
159 - 163.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W.-H. YANG, J. H. YU, T. GULICK, K. D. BLOCH, and D. B. BLOCH
RNA-associated protein 55 (RAP55) localizes to mRNA processing bodies and stress granules
RNA,
April 1, 2006;
12(4):
547 - 554.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. M. Squirrell, Z. T. Eggers, N. Luedke, B. Saari, A. Grimson, G. E. Lyons, P. Anderson, and J. G. White
CAR-1, a Protein That Localizes with the mRNA Decapping Component DCAP-1, Is Required for Cytokinesis and ER Organization in Caenorhabditis elegans Embryos
Mol. Biol. Cell,
January 1, 2006;
17(1):
336 - 344.
[Abstract]
[Full Text]
[PDF]
|
 |
|
© The Company of Biologists Ltd 2005