Abstract

Centrioles are microtubule-based cellular structures present in most human cells that build centrosomes and cilia. Proliferating cells have only two centrosomes and this number is stringently maintained through the temporally and spatially controlled processes of centriole assembly and segregation. The assembly of new centrioles begins in early S phase and ends in the third G1 phase from their initiation. This lengthy process of centriole assembly from their initiation to their maturation is characterized by numerous structural and still poorly understood biochemical changes, which occur in synchrony with the progression of cells through three consecutive cell cycles. As a result, proliferating cells contain three structurally, biochemically, and functionally distinct types of centrioles: procentrioles, daughter centrioles, and mother centrioles. This age difference is critical for proper centrosome and cilia function. Here we discuss the centriole assembly process as it occurs in somatic cycling human cells with a focus on the structural, biochemical, and functional characteristics of centrioles of different ages.

Highlights

  • The centrosome is a major microtubule (MT)-nucleating center of vertebrate cells and functions in controlling cell and tissue architecture, cell signaling, cell proliferation, and cell motility [1,2,3,4,5,6]

  • From G12 until the ensuing S phase (S2 ), the daughter centriole accumulates pericentriolar material (PCM) components including those required for the initiation of their own procentriole

  • We will discuss the milestones, as well as the ultrastructural and biochemical changes, that occur on a typical centriole in a cycling somatic human cell, from its procentriole stage until its final transformation into a fully mature centriole

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Summary

Introduction

The centrosome is a major microtubule (MT)-nucleating center of vertebrate cells and functions in controlling cell and tissue architecture, cell signaling, cell proliferation, and cell motility [1,2,3,4,5,6]. Each of the two centrosomes present in a cell is comprised of a core component, a centriole, which is a MT-based cylindrical structure, and a surrounding proteinaceous matrix called pericentriolar material (PCM). Two centrosomes organize the two poles of the mitotic spindle, a transient MT-based structure that mediates chromosome segregation (Figure 1B). A mother centriole (MC, in cross-section) associated with a procentriole (PC, in longitudinal section) from an mIMCD3 (mouse inner medullary collecting duct) cell. STORM and conventional microscopy were performed as described in centrosomal proteins immunolabeled as indicated and superimposed, to illustrate toroidal organization using the antibodies as follows: γ-tubulin: Sigma;STORM. Scale bars: 400 nm in (A and C); 5000 nm in (B); 400 nm in (D)

The Organization of Mature Centrioles and Centrosomes
Assembly
Procentriole Initiation—Ultrastructural Aspect
Procentriole Initiation
Proteins Involved in Procentriole Elongation
Regulation of Procentriole Elongation
Mother Centriole–Procentriole Distancing and Separation
From Daughter Centrioles to Mother Centrioles and Basal Bodies
Assembly of Subdistal and Distal Appendages
Regulation of Centriole Maturation by Plk1
Perspectives
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