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Revista chilena de anatomía

versión impresa ISSN 0716-9868

Rev. chil. anat. v.19 n.3 Temuco dic. 2001

http://dx.doi.org/10.4067/S0716-98682001000300013 

MORPHOLOGICAL STUDY OF THE VAS DEFERENS IN THE TUFTED
CAPUCHIN MONKEYS, Cebus apella

ESTUDIO MORFOLÓGICO DEL CONDUCTO DEFERENTE DEL MONO, Cebus apella

Bruno Cesar Schimming

Department of Anatomy, Faculty of Health Sciences, University of Marília, Marília, São Paulo, Brazil.

SUMMARY: The structure of the tufted capuchin monkeys vas deferens was examined by light microscopy. Three main regions (proximal, distal and terminal) were morphologically identified. Each region could be readly distinguished through their gross histological characteristics. The epithelium of the vas consisting of four epithelial cell types: principal, basal, apical and dark cells. The three frequent cell types (principal, apical and basal), seem to be related to a cell cycle, in which the basal cells are the stem cells. The muscular coat comprise three muscular layers: (1) inner longitudinal, (2) middle circular, and (3) outer longitudinal. The muscular coat was relatively thicker than the others, probably in agreement to its peristaltic role, in the spermatic transport.

KEY WORDS: 1. Vas deferens; 2. Monkey; 3. Light microscopy.

INTRODUCTION

According to Popovic et al. (1973), the vas deferens is a tubular structure connecting the tail of the ductus epididymis with the prostatic urethra. Until the 1960s, the vas deferens was usually considered as an inactive tube for passing off sperm, where only accumulation and storage may take place . At this time, Niemi (1965) studied the vas in the rat and postulated that the vas is not a passive tube but an active organ.

The structure of the mammalian ductus deferens has been studied in several species, as rat (Niemi; Hamilton & Cooper, 1978; Kennedy & Heidger, 1979; Clermont & Hermo, 1988; Rodriguez & Bustos-Obregón, 1993), guinea pig (Hoffer & Greenberg, 1978), and man (Popovic et al.; Paniagua et al., 1981; Paniagua et al., 1983 and Nistal et al., 1992).

The morphology of the epithelium of the vas deferens probably show that the vas serves a function more complex than simple conductance of sperm (Niemi). Turner (1995), reported that the vas deferens is one of the major storage sites for sperm. In addition to sperm storage and transport, the vas probably plays other significant roles to maintain sperm viability (Robaire & Hermo, 1988). The epithelial cells lining these vas must, therefore, play important roles in providing sperm with a suitable environment for their survival and protection (Andonian & Hermo, 1999).

Niemi also recognized that the epithelial cells are active in fluid absorption and some in secretion. The principal cells of the vas deferens have been shown to be active in synthesis of proteins destined to be secreted into the lumen (Kennedy & Heidger and  Robaire & Hermo).

Recently, it has been demonstrated the epithelial lining the vas deferens are active in endocytosis and have an abundance of lysosomes (Andonian & Hermo). Therefore, Bergerson et al. (1994) provides morphological evidence for the continuing maturation of bull sperm during their passage through the terminal portion of the deferent duct.

It has been accepted that the role of the vas deferens is relevance, although even less information is available on respect to monkeys (Ramos, 1979; Smithwick & Young, 1997). In view of the current interest in the mammals' ductus deferens, it was the purpose of the present study to describe the morphology of the ductus of the tufted capuchin monkeys, by light microscopy.

MATERIAL AND METHOD

Deferencial tissue from four adult male, sexually mature tufted capuchin monkeys (Cebus apella) were analyzed in this investigation. After its removal, each ductus deferens specimen was fixed in the Bouin's solution, for fixation overnight. Afterwards, each ductus deferens was sectioned into three portions or segments: proximal, distal, and terminal segments.

The three segments from each subject were ethanol-dehydrated, and embedded in histological paraffin. In most of the paraffin-embedded slices, transverse sections (7µm in thickness) were performed and stained with haematoxylin and eosin (H/E), Masson's and Mallory's trichromes. Some paraffin-embedded slices were longitudinally sectioned and stained in the same way. The samples were analyzed by light microscopy and photographed using a Olympus BH-2 microscope.

RESULTS

The defferent duct of tufted capuchin monkey showed three distinct anatomic segments or regions: proximal or adepididymaric, distal or funicular, and terminal or ampular. Starting from the lumen this duct is histologically structured in three distinct layers: mucosa, muscular coat, and adventitia. The mucosa was comprised by a pseudostratified and stereocilated epithelium and a lamina propria. The cellular population of the pseudostratified epithelium  consisting of both columnar and basal cells. Three types of columnar cells were seen in all segments: principal, apical and dark or pencil cells (Figs. 3, 6 and 8). The luminal border of the epithelium showed numerous long  stereocilia protruded into the lumen (Fig. 6). A narrow basal membrane separates the epithelium from the loose lamina propria.

The proximal segment showed, on section, a uniform lumen and absence of mucosal invaginations, e.g., no exhibited as called, epithelial folds. The others segments (distal and terminal) exhibiting a folded mucosa with portions of the

epithelium and underlying lamina propria projecting into the lumen (Fig. 1, 2 and 3). The longitudinal folds of the epithelium gradually became more complex towards the terminal segment.


Fig. 1 - Proximal region of the vas deferens. A regular lumen (l) packed with spermatozoa (star) is surrounding by epithelium (e), lamina propria (lp) and muscular coat (mc). x200.
Fig. 2 - Cross-section of the distal region of the vas deferens showing lumen (l) packed with spermatozoa (star), folded appearance (arrows) of the epithelium (e), lamina propria (lp) and muscular coat (mc). x200.

 The luminal diameter was greatest in the initial portion of the proximal segment where the muscular wall was the thinnest; the diameter decreased gradually along the length of the vas. Spermatozoa were always found along the whole length of the ductus deferens (Figs. 1, 2 and 3).

Figs. 3-5. Terminal segment of the vas deferens. Note spermatozoa (star), epithelial folds (arrows), principal (p) and dark (d) cells. The fibrous connective tissue (ct) of the lamina propria; and the inner longitudinal (il), middle circular (mc) and outer longitudinal (ol) layers of the muscular coat are also shown. x400.
 
 

The nuclei of columnar cells varied in outline. The principal cells was a major cell type of the epithelium, and extends from the basement membrane to the lumen of the vas. The position and shape of their nuclei are variable along the length of the duct. The apical cells are characterized by a more apically located nucleus, comparatively to principal cells morphology. Some pencil-shaped cells could be observed in all segments. They are similar to principal cells except for a darker cytoplasm and nucleoplasm. The pencil or dark cells only seldom reached through the whole thickness of the epithelium, but were mostly lying in the apical part of it (Figs. 3, 6 and 8).


Fig. 6-8. The epithelium of the vas deferens containing principal (p), basal (b), apical (a) and dark (d) cells. Sperma-tozoa (star) in the lumen, stereocilia (s) in the luminal border of the epithelium (e), and myoid cells (my) in the lamina propria are frequent. Surrounding the lamina propria there is a muscular coat (mc). x400 x400 x1.000.
 
 

The basal cells lie next to the basal lamina, and do not reach the tubular lumen. Their nuclei were ovoid in shape, with longitudinal axis orientated parallel to the basement membrane (Figs. 6 and 8). The lamina propria surrounding the basement membrane of the mucosa contains few muscle cells, myoid cells, many fibrocytes, and is extremely well supplied with collagen (Figs. 1, 2, 3 and 7).

Surrounding the lamina propria there was a thick muscular coat with fascicules with different spacial configurations. It could be divided into three layers: an inner longitudinal,  a middle circular, and an outer longitudinal layer (Figs. 1, 2, 4, 5 and 7). These layers was observed in all regions of the vas. The muscular coat was relatively thicker than the others. The thickness of the muscular coat gradually increased along the length of the vas.

DISCUSSION

In the present study, the vas deferens of the tufted capuchin monkey was divided in three anatomically and histologically well defined segments: proximal, distal and terminal, it was similar to those reported for rat by Hamilton & Cooper and  Rodríguez & Bustos-Obregón. The basic pattern of the three segments, consists of three layers of tissue surrounding the lumen: mucosa, muscular coat and adventitia variations suggest that the adult vas serves a function more complex than simple conductance of sperm. The height of the epithelium and the richness of highly organized cyto-plasmic components speaks rather in favor of an active role (Niemi).

The presence of large numbers of long stereocilia in all the cells of the vas deferens was a constant observation in the present study; similar to rat vas deferens (Niemi). To this author, structurally the stereocilia were microvillus projections of the cell membrane, although their fibrillar content and their roots suggest that they might be capable of movements. Nevertheless, the layer of stereocilia greatly increases the surface area of the duct cells. This together with the numerous invaginations of the plasma membrane suggest that the cell surface is mainly differentiated towards an active engagement in fluid uptake by the mechanism of pinocytosis.

The duct epithelium of the vas deferens as shown in the present report consists of tall columnar epithelial cells and basal cells. These same epithelial cell type were observed in vas of the man (Paniagua et al., 1981; Nistal et al.). The principal cell, a major cell type found in the vas, possess nuclei variable in the position and shape, along the length of the duct of the tufted capuchin monkeys. It was also observed in rat (Kennedy & Heidger) and man (Paniagua et al., 1981).

The vas deferens may not be considered as a simple passive duct for transport of sperm (Hoffer, 1976). The varied morphology of its epithelium as well as the regional

The cytologic characteristics of principal cells, as stereocilia, apical blebblings, primary and secondary lysosomes, seem to indicate that these cells are mainly responsible for the resorptive function (Paniagua et al., 1981). Therefore, Hermo & de Melo (1987) reported that the principal cells in addition to sequestering the endocytosed tracers within secondary lysosomes where they are presumably degraded also appear to be involved in the transcytosis of material from the lumen of the vas deferens to the underlying lamina propria. Many cytologic features of principal cells, as development of both rough endoplasmic reticulum and Golgi complex; and prominent nucleolus, are evidence for a secretory role from principal cells of the vas deferens (Hoffer and Paniagua et al., 1981).

The apical cell are similar to mitochondrion-rich cells described in rat (Kennedy & Heidger) and man (Hoffer; Paniagua et al., 1981 and Nistal et al.). Their function is unclear. According to Nistal et al., they might represent old or "exhausted" columnar secretory cells that have undergone mitochondrial hyperplasia and loss of organelles involved in glycoprotein synthesis. It has been suggested that these cells might be involved in the acidification of the seminal plasma or transport of electrolytes, hydrogen ions and water across the mucosa.

The origin and physiological role of dark or pencil cells observed in vas of the tufted capuchin monkey and in others mammals as rat (Rodríguez & Bustos-Obregón), have been the subject of controversy. They have been considered as: cell similar to those of gallbladder epithelium (Popovic et al.), holocrine secretory cells (Martan et al., 1964), dead or dying columnar cells (Hoffer). Paniagua et al. (1981) reported that the latter theory seems the most problable. It is suggested by the observation of several transitional steps from the principal cell to the dark cell, showing lysosomes with an electrondense content, intermingled with other vacuoles containing both elec-trondense and nonosmiophilic (lipids) subs-tances. In as much as the vas deferens mainly resorbs proteins from the lumen, the presence of lipid vacuoles in the cytoplasm of dark cells suggests that they problaby correspond to autophagic vacuoles.

The other cell type observed in this report, it was basal cells. Their morphology was like those reported in man epithelia. They are probably undiffe-rentiated cells that are capable of differentiation into columnar cells, repla-cing the dead sloughing cells (Paniagua et al., 1981; Nistal et al.). Thus, we could suggest that the principal, apical, and basal cells seem to be related to a cell cycle, in which the basal cells are the stem cells.

The vas has been classically described as exhibiting a folded mucosa with portions of the epithelium and underlying lamina propria projection into the lumen, this description in the monkey appears in the middle and distal segment of duct. Kennedy & Heidger observed a folded mucosa only in the terminal segment of vasa. Nistal et al. described a uniform lumen and absence of mucosal invaginations only in the proximal segment.

The tufted capuchin monkey vas has the usual three layered muscular envelope with the central circular muscle layer somewhat thinner than either of the longitudinal layers. The human vas has the same structure (Popovic et al.). Although, the middle coat was oblique in the proximal and distal portions, and only became circular in the terminal portions of the vas deferens in the man (Paniagua et al., 1981). The muscular coat was always more thicker than the mucosa and adventitia. It is probably in agreement to its peristaltic role, in the spermatic transport.

RESUMEN: Se efectuó, bajo microscopio de luz, un estudio morfológico del conducto deferente de mono. El conducto deferente está constituido por tres regiones morfológicamente distintas: proximal, distal y terminal. Cada región puede distinguirse fácilmente por variaciones en sus características morfológicas. Fueron observados cuatro tipos de células en el epitelio de revestimiento: principal, basal, apical y parda. Las tres primeras células podrían estar involucradas en el desencadenamiento del desarrollo del ciclo celular. La túnica muscular está formada de tres láminas: longitudinal interna, circular media y longitudinal externa. La túnica muscular es de mayor espesor que las túnicas mucosa y adventicia.

PALABRAS CLAVE: 1. Conducto deferente; 2. Mono; 3. Microscopía de luz.

Correspondence to:
Prof. Dr. Bruno Cesar Schimming
Department of Anatomy
Faculty of Health Sciences
University of Marília
Av. Hygino Muzzy Filho, 1001
Marília - São Paulo
Cep 17525-902
BRAZIL

E-mail: brunoidish@uol.com.br
00000 schimmin-fcs@unimar.br

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