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The location of the centrosome near the center of the interphase cell, the concentration of various regulatory proteins in it, the organization of the centrosome radial system of microtubules through which intracellular transport is carried out by motor proteins and the involvement of the centrosome in the process of the perception of the external signals and their transmission make this cellular structure a universal regulatory and distribution center, controlling the entire dynamic morphology of an animal cell.
- centrosome
- centriole
- endothelium
1. Introduction
With the light hand of D. Wheatley, who titled his book “The Centriole: a central enigma of cell biology” four decades ago, the centrosome, which includes centrioles in its structure, has been recognized as, and to a large extent still remains, a mysterious structure [1]. There was a good reason for such a definition of the centrosome. By the time of publication, the main details of the chromosome structure and the principles of gene functioning had already been studied in detail. Nevertheless, the mechanism of the centrosome’s functioning, which surprisingly turned out to be a direct participant in many different processes in a living cell, remained mysterious. With the existing variety of functions, the centrosome’s structure practically does not differ in most living organisms. The centrosome’s functional universalism suggests a comparison of this cellular organelle with a computer processor, which, using the information that is stored on the “hard disk” in the nuclear chromosomes, organizes all the work of the cell.
This structure, which is now called the centrosome, was described for the first time in the seventies of the XIX century by several researchers of cell division at once [2][3][4]. It only looked like a dark granule in each of the poles of the mitotic spindle. The size of this organelle is almost at the resolution limit of a light microscope, at that time, it was not possible to study its detailed structure. Initially, two symmetrically arranged structures, having the form of a “radiant radiance”, and which were called centrospheres, were described in dividing cells. Granules, originally called polar corpuscles, were sometimes visible in the focus of each centrosphere [4]. It was found that polar corpuscles do not completely disappear at the end of mitosis but remain in the interphase, often located near the geometric center of the cell [5][6]. For this reason, E. Van Beneden and A. Newt proposed to rename them “central corpuscles” or “central bodies” [5], and T. Boveri proposed to call this structure a centrosome [6] and later a centriole [7].
It should be noted that the numerous names given by different authors to the same structure have created a terminological confusion. Before the era of electron microscopic studies, the terms “centriole” and “centrosome” were often used as synonyms. According to the modern terminology adopted in the literature since the mid-twentieth century, a centriole is a structure that is a part of a centrosome (a specialized zone of the cytoplasm located, as a rule, in the geometric center of the cell).
2. Ultrastructural Features of Endothelial Cell Centrosome
The structure of the centrosome in various endothelial cells began to be actively studied in the 80s of the XX century. Thus, ultrastructural features of human vascular endotheliocytes centriolar complexes in situ were studied in detail in connection with various cardiac pathologies in patients aged 50–60 years [8]. The authors described the structure of “healthy” endotheliocyte centrosomes located in intact zones, as well as in fibrous and atheromatous areas of the artery from human autopsy material in situ.
It was discovered that five types of centrosomes with different structural features can be distinguished [8]. In one of the selected groups, the structure of the centrioles themselves changed: no cartwheel-type structures were found inside the centrioles and one or two microtubules in the triplet were missing. However, in all types of cells, the maternal centriole carried a significant number (from 2 to 12 per centriole) of satellites, as well as distal appendages. The activity of centrosomes in relation to primary cilium formation also differed. Most endotheliocytes from atheromatous regions had a primary cilium, while in fibrous and intact zones such cells were rare. The authors suggested that the observed difference in the centrosome’s structure may be due to functional differences [8].
Studies have shown that in the endothelial cells of the human aorta taken during autopsy in younger patients (14–17 years old), the centrioles that make up one centrosome were variable in length, and in the distal part of the maternal centriole, doublets could be observed instead of microtubule triplets [9]. In the aortic cells of donors who were 30–40 years old, there were centrioles with completely defective walls, consisting of microtubule doublets for the entire length [9]. In endotheliocytes from embryonic material (age 22–24 weeks), the length of the maternal and daughter centriole cylinders was the same (0.5–0.6 microns) [9].
One of the results of the studies described above is the fact that the activity of the endotheliocyte maternal centriole in situ may vary depending on the condition of the vessel. In particular, the number of pericentriolar satellites responsible for the polymerization of microtubules diverging from the centrosome varies significantly. Since ethical standards and the limited human biomaterial availability significantly hindered the research, most of the experiments were carried out on the endotheliocyte culture. This model, which ensures the experimental conditions’ stability and their reproducibility, allowed researchers to make significant progress in understanding how important the centrosome is in ensuring the vital endothelial cell activity.
In endothelial cells in vitro, most of the endotheliocyte microtubules are anchored on the centrosome, which organizes them into a radial system [10][11][12]. The minus ends of the microtubules can be fixed on the head of the subdistal appendage (satellite) or can be located in the pericentriolar material, being capped by the γ-TuRC complex. The plus ends of microtubules progressively grow from the centrosome towards the cell edge, and their growth rate significantly exceeds the growth rate of the plus ends of a few free microtubules.
Studies conducted in vitro on isolated cells of the human aorta and vein indicate that the endotheliocyte centrosome can quickly (on a minute scale) respond to various chemical influences, responding with pronounced biochemical and even morphological changes. It was discovered that the ratio of acetylated and tyrosinylated α-tubulin in the composition of centriolar cylinders can change in response to stimulation by thrombin, which is capable of inducing endothelium barrier dysfunction [13]. The speed with which the response develops is remarkable. Already after 1 min of exposure, a significant increase in the intensity of centrioles staining on acetylated tubulin was observed, and the intensity of staining on tyrosylated tubulin significantly decreased 5 min after exposure [13]. An ultrastructural analysis of human artery endotheliocytes showed that the centrosome morphology changes just as quickly in response to thrombin exposure, and additional pericentriolar satellites are formed on the maternal centriole. After 3 min of thrombin exposure, the number of satellites increased to 5–6 (normally from 1 to 4), and no centrioles with less than 3 satellites were observed. The described effect persisted after 15 min of exposure. Paradoxically, when thrombin was exposed to human vein endotheliocytes, no additional satellites were formed on the maternal centriole, and their number remained close to the control values [13].
An electron microscopy analysis of a human pulmonary artery endothelial cell undertaken by us showed us that centrosomes are very active microtubule-nucleating center: a lot of satellites are located on the maternal centriole and numerous microtubules grow away from both heads of the pericentriolar satellite and centriole walls [14].
Thus, the endotheliocyte centrosome is characterized by the presence of a larger (compared to other cells) number of pericentriolar satellites—structures that provide the active polymerization of microtubules. The endotheliocyte centrosome can respond quickly to external influences that lead to a violation of the barrier function. It stabilizes the structure of centriolar cylinders and increases the number of structures that are responsible for the polymerization of microtubules. It can be assumed that the described changes are a compensatory reaction in response to the depolymerization of microtubules, which is characteristic of the barrier dysfunction caused by thrombin [15].
This entry is adapted from the peer-reviewed paper 10.3390/ijms242015392
References
- Wheatley, D.N. The Centriole: A Central Enigma of Cell Biology; Elsevier Biomedical Press: Amsterdam, The Netherlands; New York, NY, USA, 1982; 232p.
- Flemming, W. Studien in der Entwicklungsgeschichte der Najaden. Sitzungsber Akad. Wissensch Wien 1875, 71, 81–147.
- Hertwig, O. Beitrage zur Kenntniss der Bildung, Befruchtung und Theilung des thierischen Eies. Morphol. Jb. 1875, 1, 347–434.
- Van Beneden, E. Recherches sur les Dicyémides, survivants actuels d’un embranchement des mésozoaires. Bull. Acad. R. Belg. 1876, 41, 1160–1205.
- Van Beneden, E.; Neyt, A. Nouvelles recherches sur la fecondation et la division mitosique ches l’Ascaride megalocephale. Bull. Acad. R. Belg. 1887, 14, 1–110.
- Boveri, T. Die Bildung der Richtungskörper bei Ascaris Megalocephala und Ascaris Lumbricoides; Zellen-studien, 1; Verlag von Gustav Fisher: Jena, Germany, 1887; 93p.
- Boveri, T. Ueber das Verhalten der Centrosomen bei der Befruchtung des Seeigel-Eies, nebst allgemeinen Bemerkungen über Centrosomen und Verwandtes. Verhandl. Phys.-Med. Ges. Würzburg 1895, 29, 1–75.
- Bystrevskaya, V.B.; Lichkun, V.V.; Antonov, A.S.; Perov, N.A. An Ultrastructural Study of Centriolar Complexes in Adult and Embryonic Human Aortic Endothelial Cells. Tissue Cell 1988, 20, 493–503.
- Bystrevskaya, V.B.; Lichkun, V.V.; Krushinsky, A.V.; Smirnov, V.N. Centriole Modification in Human Aortic Endothelial Cells. J. Struct. Biol. 1992, 109, 1–12.
- Shakhov, A.S.; Alieva, I.B. The Centrosome as the Main Integrator of Endothelial Cell Functional Activity. Biochemistry 2017, 82, 663–677.
- Smurova, K.M.; Birukova, A.A.; Verin, A.D.; Alieva, I.B. Microtubule System in Endothelial Barrier Dysfunction: Disassembly of Peripheral Microtubules and Microtubule Reorganization in Internal Cytoplasm. Cell Tissue Biol. 2008, 2, 45–52.
- Alieva, I.B.; Zemskov, E.A.; Kireev, I.I.; Gorshkov, B.A.; Wiseman, D.A.; Black, S.M.; Verin, A.D. Microtubules Growth Rate Alteration in Human Endothelial Cells. J. Biomed. Biotechnol. 2010, 2010, 1–10.
- Vinogradova, T.M.; Balashova, E.E.; Smirnov, V.N.; Bystrevskaya, V.B. Detection of the Centriole Tyr- or Acet-Tubulin Changes in Endothelial Cells Treated with Thrombin Using Microscopic Immunocytochemistry. Cell Motil. Cytoskelet. 2005, 62, 1–12.
- Shakhov, A.S.; Uzbekov, R.E.; Alieva, I.B. Ultrastructural features of the endotheliocyte centrosome and its possible involvement into the functional activity of endothelium. In Proceedings of the EMBO Conference on Centrosome and Spindle Pole Bodies, Heidelberg, Germany, 24–27 September 2017; p. 80.
- Alieva, I.B.; Zemskov, E.A.; Smurova, K.M.; Kaverina, I.N.; Verin, A.D. The Leading Role of Microtubules in Endothelial Barrier Dysfunction: Disassembly of Peripheral Microtubules Leaves behind the Cytoskeletal Reorganization. J. Cell. Biochem. 2013, 114, 2258–2272.
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