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 Table of Contents  
ORIGINAL ARTICLE
Year : 2020  |  Volume : 4  |  Issue : 3  |  Page : 373-382

Histological and immunohistochemical study of telocytes in the heart of male albino rats in different age groups


Department of Histology & Cell Biology, Faculty of Medicine for Girls, Al-Azhar University, Cairo, Egypt

Date of Submission22-Mar-2020
Date of Decision08-Apr-2020
Date of Acceptance14-Apr-2020
Date of Web Publication2-Oct-2020

Correspondence Address:
MD Fatma Al-Zahraa N Al-Shahed
Department of Histology & Cell Biology, Faculty of Medicine for Girls, Al-Azhar University, Cairo, 11754
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/sjamf.sjamf_43_20

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  Abstract 


Background Telocytes (TCs) have been newly discovered as a type of interstitial cells in the heart. They have been suggested to have a role in cardiac renewal and repair.
Aim To study the number and distribution of TCs in the heart of male albino rats and the effect of aging on their numbers.
Materials and methods A total of 24 male albino rats were used in the present study. They were subdivided into four groups: group I included six rats that were 1 week old, group II included six rats that were 1 month old, group III included six rats that were 3 months old, and group IV included six rats that were 1 year old. Specimens were taken from both atria and ventricles and subdivided into two parts: a part processed and examined by light microscope and the other part processed and examined by electron microscope. CD117 and CD34 immunohistochemical stains were used for demonstration of sites, numbers, and distribution of TCs.
Results By CD117 and CD34 immunohistochemical stains, there was a statistically significant increase in the number of TCs in atria more than in ventricles. Moreover, there was a significant decrease in the number of TCs with aging. In Masson’s trichrome-stained sections, there was an increase in collagen fibers between cardiomyocytes and around the blood vessels with age. By electron microscopic examination, TCs appeared as branched spindle, triangular, or cubical cells with long processes (telopodes) arising from the cell body. Telopodes showed variation in diameter, which had a narrow part (podomer) and a dilated part (podom). They showed homocellular junction with another TC’s telopodes and heterocellular junctions between TCs and cardiomyocytes; moreover, multivesicular bodies were also seen.
Conclusion There was a decrease in the number of TCs in the heart together with minimal changes in its shape and structure with aging.

Keywords: aging, electron microscope, heart, immunohistochemistry, telocytes


How to cite this article:
Abdel Gawad SK, Al-Shahed FZN, Abd El-Zaher MH. Histological and immunohistochemical study of telocytes in the heart of male albino rats in different age groups. Sci J Al-Azhar Med Fac Girls 2020;4:373-82

How to cite this URL:
Abdel Gawad SK, Al-Shahed FZN, Abd El-Zaher MH. Histological and immunohistochemical study of telocytes in the heart of male albino rats in different age groups. Sci J Al-Azhar Med Fac Girls [serial online] 2020 [cited 2020 Oct 26];4:373-82. Available from: http://www.sjamf.eg.net/text.asp?2020/4/3/373/296943




  Introduction Top


Telocytes (TCs) were described as a distinct type of interstitial cells in the heart [1]. The presence of another sort of interstitial cells in the heart to be specific, interstitial Cajal-like cells (ICLC), has been portrayed just because by Hinescu and Popescu [2]. Plainly, ICLC are morphologically and practically not the same as the first interstitial Cajal cells in the gut. The expression ‘ICLC’ is excessively long and unfeasible for ordinary practice; therefore, Popescu and Faussone-Pellegrini [3] proposed the new term ‘ TCs.’

By electron microscope, TCs are featured by their small-sized body with several extremely long cellular prolongations (tens to hundreds of µm) termed telopodes. Each telopode is composed of alternating thin segments (podomers) and dilated segments (podoms). The shortest definition of TCs is cells with telopodes [4]. The shape of the cellular body is associated with the number of telopode; it may be piriform, spindle, triangular, or stellate. The nucleus is oval and occupies about 25% of the cell [3]. TCs have been detected in many organs, including the skeletal muscle [5], lung [6], kidney [7], and skin [8].

Cardiac TCs are widely distributed in all layers of the heart and form a network in the endocardium, myocardium, and epicardium [9]. Double-positive immunohistochemistry for CD34/c-kit is considered to be a reliable method for TC visualization [10]. Recently, TCs have been reported to be positive for c-kit/CD117, CD34, vimentin, caveolin-1, platelet-derived growth factor receptor α, vascular endothelial growth factor, inducible nitric oxide synthase, and so on [3]. Yet transmission electron microscopy is the touchstone for identification of TCs [11].

Functions of telocytes in the heart

TCs and their telopodes are involved in intercellular signaling at distance because they are situated very close to cardiomyocytes, blood capillaries, and nerve ending [12]. TCs, attributable to their very long telopodes and their capacity to frame connection plaques interfacing them to the extracellular lattice, are anticipated to work as mechanoreceptors/transducers [13]. TCs are key players in cardiovascular restoration and in heart repair. This capacity depends on a few examinations showing the nearness of TCs in subepicardial specialties in grown-up rat and human hearts. The perceptions that TCs and telopodes are in close contact with youthful cardiomyoblasts offer help for the theory that TCs and their telopodes may ‘guide’ and ‘nurse’ the myocardial antecedents, and in this manner altogether adding to cardiovascular restoration and repair [14].


  Materials and methods Top


Animals

A total of 24 male albino rats were used in the present study. They were divided into four groups: group I contained six rats 1 week old of average weight 25–30 g. Group II contained six rats 1 month old of average weight 70–90 g. Group III contained six rats 3 months old of average weight 120–150 g, and group IV contained six rats 1 year old of average weight 200–250 g.

They were kept in the animal house at the Faculty of Medicine for Girls, Al-Azhar University, in conventional stainless-steel mashed cages at room temperature with strict care and hygienic condition. They were supplied with water and ordinary rat chow ad-libitum and were kept under observation for about 7 days for acclimatization. All animal procedures were performed in accordance with the Guide for the Care and Use of Laboratory Animals and approved by the Animal Ethical Committee at Faculty of Medicine for Girls, Al-Azhar University.

Methods

The experimental animals were killed by ether inhalation. The hearts were dissected out and were divided into two parts: a part was fixed in 10% formol saline, and the other part was fixed in glutaraldehyde.

Formol-fixed specimens were processed for light microscopic examination [15] and alternate serial sections were stained by the following stains:
  1. Hematoxylin and eosin stain, for studying the general structure [16].
  2. Masson’s trichrome stain, for staining the collagen and muscle fibers [17].
  3. Immunohistochemical staining by streptavidin–biotin–immunoperoxidase technique using anti-CD117 and anti-CD34 antibodies in the heart for TCs [17].
    1. Glutaraldehyde-fixed specimens were processed for electron microscopic examination [18].
    2. Morphometric analysis was performed using Leica Quin 500 image analyzer (Leica, 13 Abdel Salam Aref St (Ex Bustan St.) Bab Ellouk, Cairo, Egypt) which is connected to a Leica microscope and is calibrated automatically to convert the measurement units (pixels) produced by image analyzer program into actual micrometer units.


The following parameters were measured:
  1. The mean area percentage of CD117 and CD34-positive immune-stained TCs: it was counted in the atria and ventricles of the heart in all experimental groups in 10 nonoverlapping randomly selected fields per slide. Magnification used was ×200 by light microscopy transferred to the screen.
  2. The mean area percentage of collagen fibers in Masson’s trichrome-stained sections: the collagen area percentage was measured in between the muscle fibers and around the blood vessels in the atria and ventricles of the heart in all experimental groups in 10 nonoverlapping randomly selected fields per slide. Magnification used was ×200 by light microscopy transferred to the screen.


Mean values and SD were obtained from each specimen, and expressed for statistical analysis.

Statistical analysis

All data were collected, revised, and statistically analyzed using one-way analysis of variance test performed by SPSS program (SPSS Inc., Chicago, Illinois, USA), version 21. P value less than or equal to 0.05 is significant.


  Histological results Top


Group I

Examination of hematoxylin and eosin-stained sections in a rat’s heart revealed that it was formed of three layers: inner endocardium, middle thick myocardium, and outer epicardium ([Figure 1]a).
Figure 1 (a) A photomicrograph showing the layers of the left ventricle formed of endocardium, myocardium, and epicardium (hematoxylin and eosin, ×40), (b) showing very thin layer of collagen fibers (green color) in between cardiomyocytes and around blood vessels (yellow arrows) (Masson trichrome, ×200), (c) showing multiple brown CD117-positive cells in cardiac muscle interstitium (arrows) (streptavidin–biotin technique, ×1000), and (d) showing multiple brown CD34-positive cells in cardiac muscle interstitium (arrows) (streptavidin–biotin technique, ×1000). (e) A semithin section showing big number of telocytes (TCs) (arrows) (toluidine blue, ×400). (f, g, h) Electron photomicrographs showing a TC, telopodes (TP), podomere, podom, homocellular junction (square), heterocellular junctions (circle), multivesicular body (MV), cardiomyocytes (CMCs), nucleus (N), and rough endoplasmic reticulum (rER) (uranyl acetate and lead citrate, ×6000, ×10 000, and 10 000, respectively).

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Masson trichrome-stained sections revealed few collagen fibers in between muscle fibers and around the blood vessels ([Figure 1]b).

Immunostained sections with anti-CD117 antibody showed big number of strong positive immunostained TCs, which is confirmed by the statistical results ([Figure 1]c).

Immunostained sections with anti-CD34 antibody showed big number of positive immunostained TCs, which is confirmed by statistical results ([Figure 1]d).

In toluidine blue-stained semithin sections, apparent large numbers of TCs were detected ([Figure 1]e).

Electron microscopic sections showed TCs in interstitial space between the cardiomyocytes. They appeared as branched cells with long processes (telopodes) of variable diameter arising from the cell body. Telopodes showed dilated portions (podoms) and narrow portion (podomeres). Multivesicular body was seen released from telopodes. Telopodes showed homocellular junction with neighboring telopodes and heterocellular junction with cardiomyocytes. TCs revealed nuclei with peripheral heterochromatin, and the cytoplasm contained cisternae of rough endoplasmic reticulum ([Figure 1]f–h).

Group II

Masson trichrome-stained sections revealed mild increase in density of collagen fibers in between the muscle fibers and around the blood vessels compared with 1-week group ([Figure 2]a).
Figure 2 (a) A photomicrograph of a section in the left ventricles revealing mild increase in density of collagen fibers (green color) around blood vessel and in between cardiomyocytes (arrows) (Masson trichrome, ×200), (b) showing mild decrease in brown CD117-positive cells in cardiac muscle interstitium (arrows) (streptavidin–biotin technique, ×1000), (c) showing mild decrease in brown CD34-positive cells in cardiac muscle interstitium (arrows) (streptavidin–biotin technique, ×1000). (d) A semithin section showing mild decrease in number of telocytes (TCs) (arrows) (toluidine blue, ×400). (e) An electron photomicrograph showing a TC with long telopodes (TP) extending between the cardiomyocytes. No obvious changes were detected in TCs (uranyl acetate and lead citrate, ×10 000).

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Immunostained sections with anti-CD117 antibody showed mild decrease in immunostained cells compared with 1-week group ([Figure 2]b).

Immunostained sections with anti-CD34 antibody showed mild decrease in immunostained cells compared with 1-week group ([Figure 2]c).

In toluidine blue-stained semithin sections, apparent mild decrease in the number of TCs compared with 1-week group was detected ([Figure 2]d).

In electron microscopic sections, ultrathin sections revealed presence of TCs with long telopodes in interstitial space between cardiomyocytes. No apparent changes were detected in TCs when compared with 1-week group ([Figure 2]e).

Group III

Masson trichrome-stained sections revealed moderate increase in density of collagen fibers in between the muscle fibers and around the blood vessels compared with 1-week group ([Figure 3]a).
Figure 3 (a) A photomicrograph of a section in the left ventricles of the heart revealing thick layer of collagen fibers (green color) around blood vessel and in between cardiomyocytes. (Masson trichrome, ×200), (b) showing minimal brown CD117-positive cells in cardiac muscle interstitium (streptavidin–biotin technique, ×1000), (c) showing minimal brown CD34-positive cells in cardiac muscle interstitium (streptavidin–biotin technique, ×1000). (d) A semithin sections showing moderate decrease in the number of telocytes (TCs) (arrows) (toluidine blue, ×400), and (e) showing a TC with long telopodes (TP) extending between the cardiomyocytes (CMCs), which appeared slightly enlarged in size (uranyl acetate and lead citrate, ×10 000).

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Immunostained sections with anti-CD117 antibody showed moderate decrease in immunostained cells compared with 1-week group ([Figure 3]b).

Immunostained sections with anti-CD34 antibody showed moderate decrease in immunostained cells compared with 1-week group ([Figure 3]c).

Toluidine blue-stained semithin sections showed moderate decrease in the number of TCs compared with 1-week group ([Figure 3]d).

In electron microscopic sections, TCs with long telopodes in interstitial space between cardiomyocytes appeared to be slightly enlarged in size as compared to the previous two groups ([Figure 3]e).

Group IV

Masson trichrome-stained sections revealed marked increase in density of collagen fibers in between the muscle fibers and around the blood vessels compared with 1-week group ([Figure 4]a).
Figure 4 (a) A photomicrograph of a section in the left ventricle showing very thick layer of collagen fibers (green color) in between cardiomyocytes and around blood vessels. (Masson trichrome, ×200), (b) showing few brown CD117-positive cells in cardiac muscle interstitium (streptavidin–biotin technique, ×1000), (c) showing few brown CD34 positive cells in cardiac muscle interstitium (streptavidin–biotin technique, ×1000). (d) A semithin section showing marked decrease in the number of TCs (arrows) (toluidine blue, ×400). (e) An electron photomicrograph showing a TC with long telopodes (TP) extending between cardiomyocytes(CMCs), which is apparently decreased in size in relation to other groups (uranyl acetate and lead citrate, ×10 000).

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Immunostained sections with anti-CD117 antibody showed marked decrease in immunostained cells compared with 1-week group ([Figure 4]b).

Immunostained sections with anti-CD34 antibody showed marked decrease in nuclei of immune-stained cells compared with 1-week group ([Figure 4]c).

In toluidine blue-stained semithin sections, apparent marked decrease in the number of TCs compared with 1-week group was detected ([Figure 4]d).

In electron microscopic sections, ultrathin sections revealed presence of TCs with long telopodes in interstitial space between cardiomyocytes, which appeared slightly decreased in size as compared with 3-month group ([Figure 4]e).

Morphometric results

Area percentage of CD117-positive and CD34-positive cells/high power fields

The mean±SD value of positive immunoreactive TCs for CD117 and CD34 in the atria and ventricles of the heart of 1-week, 1-month, 3-month, and 1-year male albino rats was calculated and compared using analysis of variance test. The highest mean value was observed in 1-week group, whereas the lowest mean value was in 1-year group, which was statistically significant as shown in [Table 1] and [Table 2] and [Graph 1] and [Graph 2].
Table 2 Comparison of mean area percentage of CD34 positive cells in atria and ventricles of all groups

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Measurement of collagen area percentage/high power fields

The mean value of collagen area percentage in atria and ventricles of all the experimental groups was calculated. The highest mean value was observed in 1-year group, and the lowest mean value was observed in 1-week group. The difference was statistically significant, as shown in [Table 3] and [Graph 3].
Table 3 Changes of collagen area percentage in the atria and ventricles of all groups

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  Discussion Top


This study aimed to examine the distribution of TCs and the effect of aging on their number in the heart of normal male albino rats.

Hematoxylin and eosin-stained sections were examined to study the general structure of heart, and to select the sections with viable representative areas for subsequent immunohistochemical studies.

TCs could not be identified in routine hematoxylin and eosin-stained sections. This is in agreement with Popescu and Faussone-Pellegrini [3], who found that neither TCs nor its telopodes could be seen by ordinary hematoxylin and eosin stain.

In our study, we used CD117 and CD34 immunohistochemical staining, and TCs were counted by image analyzer in atria and ventricles of all subgroups. This is in agreement with Cretoiu and Popescu [19] who declared that double immunolabeling for CD34 and c-kit/CD117 may also be helpful for identification of TCs from other stromal cells under light microscopy. Moreover, Kajstura et al. [20] mentioned that discovery of CD34 and c-kit played a key role in visualization of TCs and studying their role in normal and pathological states.

In 1-week group, CD117-positive immunoreactions were noticed in between cardiomyocytes. They appeared as long cells with extensions. Moreover, CD34-positive immunoreactions were done, and they appeared as a strong positive brown immunoreaction in between muscle fibers. These results are in agreement with Chang et al. [21] who studied TCs in culture and found that it is positive for marker of embryonic stem cell and myocardial stem cell, and this indicated that it is a pluripotent cell line.

In 1-month group, CD117-positive and CD34-positive immunoreactions were noticed in between cardiomyocytes. They appeared as positive brown immunoreaction in between muscle fibers. TCs decreased in atria and ventricles of 1-month group in comparison with 1-week group. These results were in agreement with Bani et al. [22] who studied TCs’ c-kit marker and found that it decreased throughout the cardiac muscle development.

In 3-month group, CD117-positive and CD34-positive immunoreactions were noticed in interstitial tissue between cardiomyocytes. They appeared as faint positive brown immunoreaction in between muscle fibers. TCs decreased in atria and ventricles of 3-month group in comparison with 1-month group. These results were consistent with the results of Popescu et al. [23].

In 1-year group, CD117-positive and CD34-positive immunoreactions were noticed in between cardiomyocytes. They appeared as almost undetectable positive brown immunoreactions in between muscle fibers; TCs decreased in atria and ventricles of 1-year group in comparison with TC in 3 months group, which was in agreement with Richter and Kostin [24].

In all groups, TCs were not distributed uniformly in the heart, and the number of TCs had been found to be higher in atria than ventricles. These findings were in agreement with Kostin [25] and Kucybala et al. [26].

From the previous data, the TCs are present in the rat heart in different ages. The number of TC was highest in the 1-week group and lowest in 1-year group in both atria and ventricles of the heart. There was a decrease in number of TCs with aging. The highest number of TCs was present in 1 week and then in 1 month, but there was a significant decrease in 3-month and 1-year groups. These results were consistent with the results of Diaz-Flores et al. [10], Lakatta [27], Kwon et al. [28], and Solan and Niklason [29].

In 1-month group, TCs were detected by electron microscope as spindle or triangular cell body with multiple long telopodes emerging from it in between cardiomyocytes, and no obvious changes were detected in TCs as compared with 1-week group. TCs indicated homocell intersections between two neighboring TCs and heterocell intersections among TCs and cardiomyocytes. These discoveries were steady with the findings of Zhou et al. [30] and Zhou et al. [31].

In the 3-month group, TCs were detected by electron microscope with long telopodes in interstitial space between cardiomyocytes, and they appeared slightly enlarged in size as compared with the previous two groups. It additionally indicated homocell intersections and heterocell intersections, a finding which was steady with Popescu et al. [9] who found that central grips of the plasma film and intercellular extensions of basal lamina-like material were increasingly seen in the grown-up heart.

In 1-year group, TCs with long telopodes were detected by electron microscope in interstitial space between cardiomyocytes. They were decreased in size as compared with TCs in the 3-month group. This was in accordance with Luo and Feng [32] and Enciu and Popescu [33] who found that TC morphology can be changed by ageing, and the formation of telopodes increases about 50% more than young TCs.

In the present work, the area percentage of collagen fibers in both atria and ventricles of the heart was measured. Masson’s trichrome-stained layers of green collagen fibers appeared surrounding blood vessels and in between muscle bundles. The thickness of collagen layers increases with age; in the 1-year group, it was more than that of the 3-month group, which was more than that of 1-month group, which also was more than that of 1-week group. This indicates that proliferation of interstitial cells, primarily fibroblasts, increased with aging.

These results are in agreement with Nong et al. [34] who postulated that aging proceeds in both cellular and extracellular compartments, so aging of collagen fibrils might affect aging of cardiomyocytes and may cause atherosclerosis. Moreover, Vafaie et al. [35] reported that the age-related stabilization of collagen entails increasing intermolecular and interfibrillar cross-links and a concomitant decline in the susceptibility of collagen to collagenase digestion. Popescu et al. [23] stated that interstitial area (noncardiomyocytic space) increased more and more with age, presumably because of accumulation of extracellular matrix and proliferation of interstitial cells, chiefly fibroblasts and macrophages; the interstitial compartment expanded in adult human versus infants with about 10%. Additionally, the amount of blood capillaries increased moreover.


  Conclusion Top


Finally, we stated that TCs and fibroblasts, both located in the interstitial spaces, have different functions. Fibroblasts are chiefly answerable for the generation of collagen and some other extracellular framework, whereas TCs are all the more practically associated with intercellular correspondence by means of 3D organize and microvesicles.

TCs may assume a significant job in the heart advancement conceivably comprising in nursing and controlling cardiovascular muscle forerunner cells. These outcomes recommend that preconditioning of heart undeveloped cells with TCs could be helpful previously or during cell transplantation. The number of TCs decreased with aging in both atria and ventricles in all layers of the heart, and there were minimal changes in the shape and structure of TCs with aging. On the contrary, collagen fibers between the muscle bundles and around blood vessels of the heart were increased with aging in both atria and ventricles.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]



 

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