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Journal of the Anatomical Society of India

Demonstration of ZIO positive Langerhans cells in the normal and the postpartum human Fallopian tubes

Author(s): J. Suganthy, I. Indrasingh, J. Lionel

Vol. 55, No. 2 (2006-07 - 2006-12)

J. Suganthy, I. Indrasingh, J. Lionel
C.M.C. Vellore


Langerhans cells in the epithelium play an essential role in antigen presentation in the immunological defense system. The presence of Langerhans cells in the human normal and postpartum fallopian tubes was studied by zinc iodide osmium technique. ZIO positive Langerhans cells could be identified both in normal fallopian tubes and in postpartum fallopian tubes. Langerhans cells in the postpartum fallopian tubes were more in number, densely packed with dendritic morphology when compared to the normal fallopian tubes, where they were few in number with illdefined dendritic morphology. In this study, we had evidence for the migration of the Langerhans cells from the subepithelial tissue to the epithelium. Densely packed Langerhans cells in the postpartum tubes may suggest its major role in the defense of the mucosal immune system.

Key Words: ZIO Positive Cells, Lengerhans Cells, Fallopian tube, increase ZIO Positive Cells.


Dendritic cells (DCs) are a system of antigen presenting cells (APC) that is widely distributed throughout the body. They function to initiate several responses, such as sensitization of major histocompatiblity complex (MHC) restricted T cells, the rejection of organ transplants, formation of the Tdependent antibodies and presentation of antigen to B cells in the germinal center of lymph nodes and the tonsils and adenoids (Bernstein et al. 1992). Langerhans cells (LCs) are the predominant antigen-presenting cells in epithelial tissues. They have been known to be present in the vaginal and uterine cervix. Hagiwara et al (1998) demonstrated the presence of LCs in the human oviduct mucosa by electron microscopy and immunohistochemistry using anti CD1a (CD: cluster of differentiation). The epithelium of the human oviduct also expresses the major histocompatibility complex (MHC) class II as well as intercellular adhesion molecule- 1 (ICAM 1) (Utreras et al.2000).

The fallopian tube has an internal mucosa, an intermediate muscular stratum and an external serosa. The tube is covered by folded simple or pseudostratified ciliated and secretory epithelium. The plicae have cores of connective tissue and are richly supplied by blood vessels and lymphatics. The epithelium is composed of at least four types of cells, the ciliated columnar, secretory, peg (intercalary) and undifferentiated cells. Their ratio varies with hormone levels and position. Ciliated cells are cuboidal with large nucleus. They are much reduced after the menopause. Secretory clls are interspersed among ciliated cells. Peg cells are narrow columnar elements with oval nuclei. They are thought to represent secretory cells in non-secretory phase of their cycle. Undifferentiated cells are small cells restricted to the epithelial base. They are probably mainly stem cells for the ciliated and secretory cell populations, although some may be intraepithelial lymphocytes (Standring et al. 2005).

Many histological techniques have been applied for the demonstration of the Langerhans cells. The zinc iodide-osmium (ZIO) method has been successfully applied for the demonstration of Langerhans cells with both light and electron microscopy (Niebauer 1969 and Figueroa and Caorsi 1980). The aim of the present study is to demonstrate the distribution of ZIO positive Langerhan cells in normal and postpartum fallopian tubes.

Materials and Methods:

Fallopian tube samples were collected from two patients who underwent hysterectomy for fibroid uterus and six patients who had bilateral tubectomy as a family planning procedure between 2 to 5 days postpartum, at the Christian medical college Hospital. The tissue pieces were immersed in a solution of veronal-buffered Zinc Iodide-Osmium tetroxide, pH 7.4 (Figueroa and Caorsi,1980) for 60 hours at 4 C in the dark, washed in distilled water, dehydrated in graded ethanol, cleared in xylene, and embedded in paraffin wax. Serial sections of six micron thickness were cut and the sections were transferred to glass slides, deparaffinised, mounted in DPX without counterstaining (Chandi et al 1988, Abraham et al 1996 and Indrasingh et al 2001) and viewed under light microscope.


In the post partum tubes vascularisation is more than in normal tubes and the ZIO positive Langerhans cells are more in number and their dendritic morphology is well defined (Fig.1a). ZIO positive Langerhans cells are found both in the epithelium and sub-epithelial tissue of the postpartum fallopian tubes (Fig.1b). Langerhans cells are arranged in rows in postpartum tubes near the basement membrane (Fig. 1c). In one specimen we could demonstrate the row of ZIO positive cells, may be they are secretory cells in the epithelium (Fig.1d). In another postpartum tube, the epithelium has Langerhans cells as well as few ZIO positive columnar cells (Fig 1e). In some areas there are evidences that the Langerhans cells are migrated to the epithelium from the sub-epithelial tissue (Fig. 1f). In the normal tubes we could demonstrate the ZIO positive cells in the epithelium. But they are not dendritic in nature. They are triangular with a single long process directed towards the base of the epithelium (Fig. 2). In normal tubes the sub-epithelial tissue has very few ZIO positive cells.


Fig. 1: (a). Cross section of normal fallopian tube (192x) Arrow indicates the ZIO positive cell in the epithelium E-Epithelium, S-Subepithelia tissue, (b). Cross section of postpartum fallopian tube (175 x) EEpithelium, S-Subepithelia tissue, B-Blood vessel, (c). Arrow indicates ZIO positive Langerhan cell which is polygonal in shape in subepithelium (100x), (d). Arrow indicates row of ZIO positive cells in the subepithelial tissue (450 x), (e). Arrow indicates row of ZIO positive secretory cells in the epithelium (175 x) E-Epithelium, (f). Arrow indicates the ZIO positive columnar cells in the epithelium (175x).

Fig. 2: Arrows indicate the migration of Langerhans cells towards surface epithelium (450 x) E-Epithelium, S-Subepithelia tissue, B-Blood vessel,


Dendritic cells possess the ability to present foreign antigen peptides complexed with MHC class II molecules expressed on their surfaces to active and resting T cells. There are number of “molecular couples” that influence DC and T lymphocyte interaction during antigen presentation: CD/1/CD18 integrins, intercellular adhesion molecules (ICAMs), lymphocyte function associated antigen 3 (LFA-3), CD 40, CD80/ B7-1, CD86/B7-2, and heat-stable antigen. The “molecular couples” are involved in adhesive or costimulatory regulations, mediating an effective binding of DCs to T lymphocyes and the stimulation of specific intercellular communications. DCs also provide all of the known co-stimulatory signals required for activation of unprimed T lymphocytes (Bodey et al. 1997).

Mucosal Associated Lymphoid Tissue (MALT) exists in the fallopian tube and epithelial cells form an integral part of this system (Morris et al. 1986). CD1a-positive LCs in the fallopian tube epithelium were more common in women at the age of 40 to 59 ( Hagiwara et al. 1998). The presence of ICAM-1 and MHC class II antigens in the oviduct epithelium supports the role of oviductal epithelium in antigen presentation. Binding of lymphoid cells to the surface of the oviductal epithelium may help to retain these immune cells that are required for the clearance of pathogens (Utreras et al. 2000). The effects of age and gonadal steroids on the antigen presenting cells in the chicken oviduct revealed that local immunity in the chicken oviduct is enhanced during sexual maturation and possibly decreased during ageing (Zheng et al. 1998).

In the present study, the epithelium of the fallopian tubes has Langerhans cells as well as few ZIO positive colummar cells. The ZIO positive cells in the normal tubes have single dendritic process directed towards the base of the epithelium as described by Hagiwara et al. (1998). Their morphology is similar to the ZIO positive cells seen in the human ileum and the human colon (Koshy et al.2003 and Indrasingh et al. 2003). The ZIO positive Langerhans cells are densely packed in the postpartum fallopian tubes than in the normal tubes. Their dendritic morphology differs from the normal tubes to postpartum tubes. In the sub-epithelial tissue ZIO positive cells are polygonal, as well as dendritic in nature. We also have evidence of LCs migration from the sub-epithelial tissue to the epithelium. The presence of densely packed LCs in the postpartum tubes, their dendritic morphology and their migratory nature indicates that these antigen presenting cells (APC) are needed for proper presentation of antigen to immunocompentent cells. Tew et al (1989) have shown in the ageing mouse, that in the absence of APC, immunological recognition and appropriate maturation of B cells into both memory as well as into immunoglobulin secreting cells do not occur.

Our study suggests that the ZIO positive Langerhans cells in the sub-epithelium and epithelium of fallopian tube may alter the epithelial microenvironment and thus increase the immunocompetence to restrain pathogens. The densely packed Langerhans cells in the human postpartum fallopian tubes indicate that they function as gatekeeper of the mucosal immune system.


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