The Centrosome and the Primary Cilium: The Yin and Yang of a Hybrid Organelle

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.

Differentiation of ciliated human midbrain-derived LUHMES neurons

“…Prior to cell division the cilium is resorbed to free a pair of centrioles from the ciliary base. During S and G2 phases centrioles are duplicated and mature into functional centrosomes, which organize the formation of the bipolar spindle for sister chromatid separation in M phase (Pletz et al, 2013; Ford et al, 2018; Joukov and De Nicolo, 2019).…”

Nuclear localization of calcium-activated BK channels in skate ampullary electroreceptors

“…Cilia are anchored to basal bodies which operate as microtubule organizing centers, similar to centrioles [62]. Joukov et al [63] describe a physical connection between basal body apparatus and nucleus-associated microtubule organizing center as a means for communication between extracellular and intracellular domains. Our study suggests that BK channel partitioning between plasma membranes, including cilia, and nuclear envelopes may be regulated dynamically through posttranslational modifications within the bipartite NLS.…”

Centrioles and Ciliary Structures during Male Gametogenesis in Hexapoda: Discovery of New Models

“…The dynamics of the CLRs in insect spermatocytes break from the general rule of the primary cilium biology observed in vertebrate cells, where this organelle has a transient life correlated to cell cycle progression and its presence is incompatible with cell division [48,152,153]. On the contrary, in insect spermatocytes, the CLRs do not disassemble at the beginning of the meiotic divisions, but they The dynamics of the CLRs in insect spermatocytes break from the general rule of the primary cilium biology observed in vertebrate cells, where this organelle has a transient life correlated to cell cycle progression and its presence is incompatible with cell division [48,152,153]. On the contrary, in insect spermatocytes, the CLRs do not disassemble at the beginning of the meiotic divisions, but they are internalized, and the centrioles organize the centrosome that drives the assembly of the spindle poles.…”

“…">Centriole Dynamics in Insect Spermatogenesis: Rule or Exception?Centriole duplication must be accurately monitored during the cell cycle to avoid additional centrioles and, therefore, too many centrosomes that may result in multipolar spindles. Multipolar spindles are dangerous to tissue development and homeostasis, since they can lead to apoptosis or chromosomal instability, a hallmark of tumorigenesis [36,[46][47][48][49]. Thus, the centrosome number is tightly regulated in somatic cells and the centrioles duplicate only once during the cell cycle [36].…”