A multicomponent assembly pathway contributes to the formation of acentrosomal microtubule arrays in interphase Drosophila cells

In animal cells, centrosomes nucleate microtubules that form polarized arrays to organize the cytoplasm. Drosophila presents an interesting paradox however, as centrosome-deficient mutant animals develop into viable adults. To understand this discrepancy, we analyzed behaviors of centrosomes and mic...

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Bibliographic Details
Published in:Molecular biology of the cell 2008-07, Vol.19 (7), p.3163-3178
Main Authors: Rogers, Gregory C, Rusan, Nasser M, Peifer, Mark, Rogers, Stephen L
Format: Article
Language:English
Subjects:
Animals
Centrioles - metabolism
Centrosome - ultrastructure
Drosophila melanogaster
Dyneins - metabolism
Gene Expression Regulation
Green Fluorescent Proteins - metabolism
Interphase
Microscopy, Electron, Transmission
Microscopy, Fluorescence
Mitosis
Models, Biological
RNA Interference
Spindle Apparatus
Tubulin - metabolism
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Summary:In animal cells, centrosomes nucleate microtubules that form polarized arrays to organize the cytoplasm. Drosophila presents an interesting paradox however, as centrosome-deficient mutant animals develop into viable adults. To understand this discrepancy, we analyzed behaviors of centrosomes and microtubules in Drosophila cells, in culture and in vivo, using a combination of live-cell imaging, electron microscopy, and RNAi. The canonical model of the cycle of centrosome function in animal cells states that centrosomes act as microtubule-organizing centers throughout the cell cycle. Unexpectedly, we found that many Drosophila cell-types display an altered cycle, in which functional centrosomes are only present during cell division. On mitotic exit, centrosomes disassemble producing interphase cells containing centrioles that lack microtubule-nucleating activity. Furthermore, steady-state interphase microtubule levels are not changed by codepleting both gamma-tubulins. However, gamma-tubulin RNAi delays microtubule regrowth after depolymerization, suggesting that it may function partially redundantly with another pathway. Therefore, we examined additional microtubule nucleating factors and found that Mini-spindles, CLIP-190, EB1, or dynein RNAi also delayed microtubule regrowth; surprisingly, this was not further prolonged when we codepleted gamma-tubulins. Taken together, these results modify our view of the cycle of centrosome function and reveal a multi-component acentrosomal microtubule assembly pathway to establish interphase microtubule arrays in Drosophila.
ISSN:1059-1524
1939-4586
DOI:10.1091/mbc.E07-10-1069