Abstract
Centrosomes and primary cilia are usually considered as distinct organelles, although both are assembled with the same evolutionary conserved, microtubule-based templates, the centrioles. Centrosomes serve as major microtubule- and actin cytoskeleton-organizing centers and are involved in a variety of intracellular processes, whereas primary cilia receive and transduce environmental signals to elicit cellular and organismal responses. Understanding the functional relationship between centrosomes and primary cilia is important because defects in both structures have been implicated in various diseases, including cancer. Here, we discuss evidence that the animal centrosome evolved, with the transition to complex multicellularity, as a hybrid organelle comprised of the two distinct, but intertwined, structural-functional modules: the centriole/primary cilium module and the pericentriolar material/centrosome module. The evolution of the former module may have been caused by the expanding cellular diversification and intercommunication, whereas that of the latter module may have been driven by the increasing complexity of mitosis and the requirement for maintaining cell polarity, individuation, and adhesion. Through its unique ability to serve both as a plasma membrane-associated primary cilium organizer and a juxtanuclear microtubule-organizing center, the animal centrosome has become an ideal integrator of extracellular and intracellular signals with the cytoskeleton and a switch between the non-cell autonomous and the cell-autonomous signaling modes. In light of this hypothesis, we discuss centrosome dynamics during cell proliferation, migration, and differentiation and propose a model of centrosome-driven microtubule assembly in mitotic and interphase cells. In addition, we outline the evolutionary benefits of the animal centrosome and highlight the hierarchy and modularity of the centrosome biogenesis networks.
Highlights
On the Definition of the CentrosomeThe architecture and motility of eukaryotic cells are underpinned by the dynamic and interconnected networks of actin and microtubule (MT) cytoskeletons [1,2]
The animal centrosome appears to be a composite organelle evolved from a merger between the ancestral nuclear membrane-associated MT-organizing centers (MTOCs) and the plasma membrane-bound basal body apparatus, which were the precursors of the pericentriolar material (PCM) and centrioles, respectively
Unlike the PCNT-CEP215 module, the PCNT-centrosomal protein of 192 kDa (CEP192) module is absolutely dependent on Polo-like kinase 1 (PLK1) activity, because PLK1 phosphorylation of PCNT presumably initiates the recruitment of CEP192 complexes to centrosomes, and because PLK1 docking to and phosphorylation of CEP192 is a prerequisite for NEDD1-γ-tubulin ring complex (γ-TuRC) recruitment and MT
Summary
The architecture and motility of eukaryotic cells are underpinned by the dynamic and interconnected networks of actin and microtubule (MT) cytoskeletons [1,2]. With the discovery of γ-tubulin, a conserved subtype of tubulin and a key MT-nucleating component of animal centrosomes and the acentriolar yeast spindle pole bodies [26,27,28,29,30,31], the term MTOC was often used instead of, or even synonymously to centrosome It was shown, that, besides centrosomes, a number of other cellular structures promote γ-tubulin-mediated MT nucleation and anchoring [32,33,34,35]. The centrosome can be defined as an organelle with three basic properties: i) ability to form an MTOC at the center of the cell through γ-tubulin-dependent nucleation and anchoring of MTs at their minus ends; ii) ability to associate with the nucleus in interphase and spindle poles during mitosis; iii) duplication once during the cell cycle [40,41,42]. A definition oforganizes, MTOC as and/or any structure generates, organizes, and/or anchors MTs
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