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Relationships between telocytes and cardiomyocytes during pre- and post-natal life.

Faussone-Pellegrini MS, Bani D - J. Cell. Mol. Med. (2010)

Bottom Line: In our opinion, investigating the occurrence and morphology of telocytes during heart histogenesis may shed further light on this issue.These cells closely embrace the growing cardiomyocytes with their long, slender cytoplasmic processes.Hence, in the developing myocardium, telocytes may play nursing and guiding roles for myocardial precursors to form the correct three-dimensional tissue architectural pattern, as previously suggested.

View Article: PubMed Central - PubMed

Affiliation: Department of Anatomy, Histology and Forensic Medicine, University of Florence, Florence, Italy.

ABSTRACT
Evidence has been given that the adult heart contains a specific population of stromal cells lying in close spatial relationship with cardiomyocytes and with cardiac stem cells in sub-epicardial cardiogenic niches. Recently termed 'telocytes' because of their long cytoplasmic processes embracing the parenchymal cells, these cells have been postulated to be involved in heart morphogenesis. In our opinion, investigating the occurrence and morphology of telocytes during heart histogenesis may shed further light on this issue. Our findings show that typical telocytes are present in the mouse heart by early embryonic to adult life. These cells closely embrace the growing cardiomyocytes with their long, slender cytoplasmic processes. Hence, in the developing myocardium, telocytes may play nursing and guiding roles for myocardial precursors to form the correct three-dimensional tissue architectural pattern, as previously suggested.

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Immunohistochemistry. A–C: c-kit-immunolabelling. In (A), at E14 the lining epicardial cells and the immature cardiomyocytes are intensely c-kit+. Intermingled with these cells and towards the ventricular lumen there are several c-kit-negative stellate cells featuring the telocytes (arrows). In (B), at E17, and in (C), at P6, both immature and mature cardiomyocytes are c-kit+. The lining epicardial cells are still c-kit+ (upper part of B) and the putative telocytes (arrows) are c-kit–. These latter cells closely border the cardiomyocyte columns. D–F: CD34-immunolabelling. In (D), at E17, the lining epicardial cells and several sub-epicardial cells identifiable as endothelial cells are C34+. In (E), at P0, most of the endothelial cells as well as few interstitial cells (arrows), likely identifiable as telocytes, are CD34+. In (F), adult mouse heart, a typical telocyte (arrow) is CD34+. Bar: A, B, D= 40 μm; C, E= 20 μm; F= 15 μm.
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fig01: Immunohistochemistry. A–C: c-kit-immunolabelling. In (A), at E14 the lining epicardial cells and the immature cardiomyocytes are intensely c-kit+. Intermingled with these cells and towards the ventricular lumen there are several c-kit-negative stellate cells featuring the telocytes (arrows). In (B), at E17, and in (C), at P6, both immature and mature cardiomyocytes are c-kit+. The lining epicardial cells are still c-kit+ (upper part of B) and the putative telocytes (arrows) are c-kit–. These latter cells closely border the cardiomyocyte columns. D–F: CD34-immunolabelling. In (D), at E17, the lining epicardial cells and several sub-epicardial cells identifiable as endothelial cells are C34+. In (E), at P0, most of the endothelial cells as well as few interstitial cells (arrows), likely identifiable as telocytes, are CD34+. In (F), adult mouse heart, a typical telocyte (arrow) is CD34+. Bar: A, B, D= 40 μm; C, E= 20 μm; F= 15 μm.

Mentions: Myocardial samples obtained from embryonic (E14, E17), newborn (P0, P6) and adult (2 months) CD1 mice were examined by immunohistochemistry and transmission electron microscopy. It was observed that, during cardiac development, stellate-shaped stromal cells featuring bona fide telocytes were present since the early developmental stages (Fig. 1A–F). They accompanied the proliferating myocardial buds moving from the epicardium towards the ventricular lumen and closely bordered the cardiomyocyte trabeculae for their entire length. At E14, short, thin columns of immature cardiomyocytes amidst stromal cells protruded from the sub-epicardial area towards the heart lumen (Fig. 1A). By E17 up to P6, the trabecular organization of the heart was maintained and the columns of cardiomyocytes were thick, interconnected and clearly bordered by telocytes (Fig. 1B, C, E). During the embryonic life, the putative telocytes were negative for c-kit, a marker for myocardial precursors [7], and CD34, a marker for adult telocytes [4] (Fig. 1A–E). During post-natal life, CD34 was expressed by a few putative telocytes at P0 and P6 (Fig. 1E), and by most of them in the adult hearts (Fig. 1F). By E17 to post-natal life, the epicardial lining cells and cells identifiable as endothelial cells also were CD34+ (Fig. 1D, E). In turn, c-kit-positivity was intense in both the epicardial lining cells and the cardiomyocytes of embryos and newborns (Fig. 1A–C), whereas it tended to decrease with age, being very faint in the cardiomyocytes and absent in the epicardium of the adult hearts. By transmission electron microscopy analysis, in the E14 and E17 hearts, cells featuring telocytes, i.e. provided with a small, oval-shaped body and long, thin processes, were observed in the sub-epicardial layer amidst the immature cardiomyocytes and in the myocardial trabeculae closely bordering the cardiomyocyte columns (Fig. 2A, B). In the early embryonic hearts, telocytes had immature features, as they had many free polyribosomes, and were surrounded by an electron-lucent matrix (Fig. 2A). In the newborn hearts, telocytes showed a more differentiated phenotype, with several rough endoplasmic cisternae located both in the cell body and processes (Fig. 2C), and were immersed in a loose extracellular matrix. Moreover, these cells established numerous interactions with the adjacent cardiomyocytes, in the form of focal plasma membrane contacts and intercellular bridges of flocculent, basal lamina-like material (Fig. 2D), similar to those observed in the cardiogenic niches of the adult heart [7].


Relationships between telocytes and cardiomyocytes during pre- and post-natal life.

Faussone-Pellegrini MS, Bani D - J. Cell. Mol. Med. (2010)

Immunohistochemistry. A–C: c-kit-immunolabelling. In (A), at E14 the lining epicardial cells and the immature cardiomyocytes are intensely c-kit+. Intermingled with these cells and towards the ventricular lumen there are several c-kit-negative stellate cells featuring the telocytes (arrows). In (B), at E17, and in (C), at P6, both immature and mature cardiomyocytes are c-kit+. The lining epicardial cells are still c-kit+ (upper part of B) and the putative telocytes (arrows) are c-kit–. These latter cells closely border the cardiomyocyte columns. D–F: CD34-immunolabelling. In (D), at E17, the lining epicardial cells and several sub-epicardial cells identifiable as endothelial cells are C34+. In (E), at P0, most of the endothelial cells as well as few interstitial cells (arrows), likely identifiable as telocytes, are CD34+. In (F), adult mouse heart, a typical telocyte (arrow) is CD34+. Bar: A, B, D= 40 μm; C, E= 20 μm; F= 15 μm.
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Related In: Results  -  Collection

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fig01: Immunohistochemistry. A–C: c-kit-immunolabelling. In (A), at E14 the lining epicardial cells and the immature cardiomyocytes are intensely c-kit+. Intermingled with these cells and towards the ventricular lumen there are several c-kit-negative stellate cells featuring the telocytes (arrows). In (B), at E17, and in (C), at P6, both immature and mature cardiomyocytes are c-kit+. The lining epicardial cells are still c-kit+ (upper part of B) and the putative telocytes (arrows) are c-kit–. These latter cells closely border the cardiomyocyte columns. D–F: CD34-immunolabelling. In (D), at E17, the lining epicardial cells and several sub-epicardial cells identifiable as endothelial cells are C34+. In (E), at P0, most of the endothelial cells as well as few interstitial cells (arrows), likely identifiable as telocytes, are CD34+. In (F), adult mouse heart, a typical telocyte (arrow) is CD34+. Bar: A, B, D= 40 μm; C, E= 20 μm; F= 15 μm.
Mentions: Myocardial samples obtained from embryonic (E14, E17), newborn (P0, P6) and adult (2 months) CD1 mice were examined by immunohistochemistry and transmission electron microscopy. It was observed that, during cardiac development, stellate-shaped stromal cells featuring bona fide telocytes were present since the early developmental stages (Fig. 1A–F). They accompanied the proliferating myocardial buds moving from the epicardium towards the ventricular lumen and closely bordered the cardiomyocyte trabeculae for their entire length. At E14, short, thin columns of immature cardiomyocytes amidst stromal cells protruded from the sub-epicardial area towards the heart lumen (Fig. 1A). By E17 up to P6, the trabecular organization of the heart was maintained and the columns of cardiomyocytes were thick, interconnected and clearly bordered by telocytes (Fig. 1B, C, E). During the embryonic life, the putative telocytes were negative for c-kit, a marker for myocardial precursors [7], and CD34, a marker for adult telocytes [4] (Fig. 1A–E). During post-natal life, CD34 was expressed by a few putative telocytes at P0 and P6 (Fig. 1E), and by most of them in the adult hearts (Fig. 1F). By E17 to post-natal life, the epicardial lining cells and cells identifiable as endothelial cells also were CD34+ (Fig. 1D, E). In turn, c-kit-positivity was intense in both the epicardial lining cells and the cardiomyocytes of embryos and newborns (Fig. 1A–C), whereas it tended to decrease with age, being very faint in the cardiomyocytes and absent in the epicardium of the adult hearts. By transmission electron microscopy analysis, in the E14 and E17 hearts, cells featuring telocytes, i.e. provided with a small, oval-shaped body and long, thin processes, were observed in the sub-epicardial layer amidst the immature cardiomyocytes and in the myocardial trabeculae closely bordering the cardiomyocyte columns (Fig. 2A, B). In the early embryonic hearts, telocytes had immature features, as they had many free polyribosomes, and were surrounded by an electron-lucent matrix (Fig. 2A). In the newborn hearts, telocytes showed a more differentiated phenotype, with several rough endoplasmic cisternae located both in the cell body and processes (Fig. 2C), and were immersed in a loose extracellular matrix. Moreover, these cells established numerous interactions with the adjacent cardiomyocytes, in the form of focal plasma membrane contacts and intercellular bridges of flocculent, basal lamina-like material (Fig. 2D), similar to those observed in the cardiogenic niches of the adult heart [7].

Bottom Line: In our opinion, investigating the occurrence and morphology of telocytes during heart histogenesis may shed further light on this issue.These cells closely embrace the growing cardiomyocytes with their long, slender cytoplasmic processes.Hence, in the developing myocardium, telocytes may play nursing and guiding roles for myocardial precursors to form the correct three-dimensional tissue architectural pattern, as previously suggested.

View Article: PubMed Central - PubMed

Affiliation: Department of Anatomy, Histology and Forensic Medicine, University of Florence, Florence, Italy.

ABSTRACT
Evidence has been given that the adult heart contains a specific population of stromal cells lying in close spatial relationship with cardiomyocytes and with cardiac stem cells in sub-epicardial cardiogenic niches. Recently termed 'telocytes' because of their long cytoplasmic processes embracing the parenchymal cells, these cells have been postulated to be involved in heart morphogenesis. In our opinion, investigating the occurrence and morphology of telocytes during heart histogenesis may shed further light on this issue. Our findings show that typical telocytes are present in the mouse heart by early embryonic to adult life. These cells closely embrace the growing cardiomyocytes with their long, slender cytoplasmic processes. Hence, in the developing myocardium, telocytes may play nursing and guiding roles for myocardial precursors to form the correct three-dimensional tissue architectural pattern, as previously suggested.

Show MeSH