Academic journal article Genetics

The Centrioles, Centrosomes, Basal Bodies, and Cilia of Drosophila Melanogaster

Academic journal article Genetics

The Centrioles, Centrosomes, Basal Bodies, and Cilia of Drosophila Melanogaster

Article excerpt

CENTROSOMES are the organelles at the poles of the spindle that can persist into interphase as microtubule organizing centers (MTOCs). At their core is a ninefold symmetrical centriole, and their ability to nucleate cytoplasmic microtubules (MTs) is a property of the surrounding pericentriolar material (PCM; Figure 1). The centriole has a dual life, existing not only as the core of the centrosome but also as the basal body, the structure that templates the formation of cilia and flagellae. As a result, the structure and function of the centriole, the centrosome, and the basal body have an impact upon many aspects of development and physiology, resulting in diseases that can readily be modeled in Drosophila. Such diseases include many forms of cancer, where centrosome aberrations have been known for over a century, and a variety of heritable diseases, where developmental disorders characterized by defects in cilia (ciliopathies) or asymmetric cell divisions in the brain (microcephaly) are associated with cilia, centriole, and centrosome defects.

Studies of centriole biology initially depended upon the application of electron microscopy (EM) focused upon the roles of centrioles in critical stages of development. This led, for example, to the discovery that once the nurse cells of the egg chamber begin their endoreduplication cycles, the centrioles migrate to accumulate at the oocyte before ultimately being eliminated so that female meiosis can occur on a centriole-free spindle (Mahowald and Strassheim 1970). EM also gave us the first detailed description of the complex behavior of the centriole in the male germline (Tates 1971), which we will discuss further below. However, progress was greatly accelerated when antibodies became available that recognized centrosomal components, so permitting centrosome behavior to be tracked using immunofluorescence microscopy. Curiously, one of the first centrosomal antigens to be followed in this way, CP190, first identified through a monoclonal antibody, Bx63 (Frasch et al. 1986), may not have its major functions at the centrosome. The Bx63 antigen was later purified as a MT-associated protein (MAP) (Kellogg and Alberts 1992) and indeed does have a MT-binding domain and some function in spindle assembly (Plevock et al. 2015). However, its major role is as a chromatin insulator that is critical to direct the formation of chromosomal loops to organize transcription units in the interphase nucleus [reviewed by Ahanger et al. (2013)]. This highlights the difficulty of many early studies of centrosome proteins to know whether they were taking a "joy ride" on the centrosome or its associated MTs or that they really functioned there (Table 1). Irrespective of its function, CP190 proved to be an invaluable antigen with which to trace centrosome behavior in early cell biological studies, particularly in the rapid nuclear division cycles of the syncytial embryo.

The Parts Catalog

Taking advantage of the fly's life cycle

The identification of key components of the centrosome has been critical to understanding its duplication and function. As a major function of the Drosophila centrosome is as a MTOC in cell division, and because the organelle is essential for syncytial embryo development and male fertility, it is perhaps not surprising that the genes encoding many centrosomal proteins were found in genetic screens for lethality or sterility aimed at identifying cell cycle mutants. One particular class of maternal-effect-lethal (MEL) mutants identify maternallyexpressed genes, required for the first 2 hr of syncytial embryo development when nuclei follow rapid cycles of alternating S- and M-phase, first at 10-min intervals and then gradually lengthening to ~20 min, to allow some zygotic transcription from cycle 10 onward. This massive increase in nuclei during syncytial development requires a dowry of maternally-provided cell cycle regulatory molecules. A mother homozygous for mutations in such genes reaches adulthood because her own heterozygous mother (the grandmother) has provided the wild-type gene product, but she is unable to contribute any wild-type protein to her own offspring. …

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