Indmedica Home | About Indmedica | Medical Jobs | Advertise On Indmedica
Search Indmedica Web
Indmedica - India's premier medical portal

Journal of the Anatomical Society of India

Zinc Iodide Osmium Positive Cells And Dendritic Cells In Stratified Squamous Epithelium of lip, Tongue, And Oesophagus Of BonnetMonkey (Macaca Radiata)

Author(s): Indrasingh, I., Abraham, S. and Vettivel, S.K.

Vol. 50, No. 1 (2001-01 - 2001-06)

Department of Anatomy, Christian Medical College, Vellore. India

For Reprints, request the first author.


Dendritic cells have been demonstrated in human and animal epithelium and subepithelial tissue. The present study hasused Bonnet monkey for the first time and revealed zinc iodide osmium positive cells and dendritic cells in the stratified squamousepithelium in lip, tongue, and oesophagus.

Key words : Bonnet monkey, dendritic cell, stratified squamous epithelium, zinc iodide osmium


Dendritic cells are a distinct and stable subpopulation of cells that appear to be homogenous by cytological features, expression of Ia antigens, and ability to associate with responding T cells. They are bone marrow derived, thymus independent cells (Steinman and Nusenzweig, 1980).

Dendritic cells have been extensively found using zinc-iodide-osmium (ZIO) in lymphoid organs (Niebauer, Krawezyk, Kidd and Wilgram, 1969; Rodriguez and Caorsi, 1978; Crocker and Hopkins, 1984, Chandi, Indrasingh and Sridharan 1988; Chandi, Indrasingh and Chandi, 1989; Degdeviren, Alp and Ors, 1994) and nonlympoid organs such as the epidermis, heart, liver, lung, small intestine, and decidua (Breathnach and Goodwin, 1965; Hart and Fabre, 1981; Sertle, Takemura, Tschachler, Ferrans, Kaliner and Shevach, 1986; Prickett, Mckenzie and Hart, 1988; Steinman, 1991; Pavli, Maxwell, van de Pol and Doe, 1996; Abraham, Indrasingh, Vettivel, and Chandi, 1996; Abraham, Indrainsingh, Vettivel and Chandi, 2000). Dendritic cells have been identified in the stratified squamous epithelium of mouth epidermis (Riley, 1967; Zelickson and Mottax, 1968; Mishima and Miller-Millinska, 1961; Lenz, Heine, Schuler and Romani, 1993), tonsil (Corcker and Hopkins; Chandi et al, 1988, 1989), vagina (Miller, McChensney and Moore, 1992; Hu, Pope, Brown O'Doherty and Miller, 1998) and rat (Muller, 1996).

The present study was to reveal the presence of dendritic cells in the stratified squamous epithelium of lip, tongue, and oesophagus in Bonnet monkey (Macaca radiata) and to describe their location and gross morphology. This animal species has not been so far used for the demonstration of dendritic cell.

Materials and Methods:

Samples of lip, tongue, and oesophagus were collected from Bonnet monkeys (Macaca radiata).

The tissue pieces were immersed in a solution of veronol buffered zinc iodide osmium tetroxide at pH 7.4 (Figueroa and Caorsi, 1980) for 48 hours at 4°C in the dark, washed in distilled water, dehydrated in graded ethanol, cleared in xylene and embedded in paraffin wax, without counter staining (Chandi et al, 1988; Abraham et al. 1996). Serial sections of seven-micron thickness were cut and the sections were transferred to glass slides, deparaffinised, mounted in DPX, and viewed under light microscope. Cellular reactivity to ZIO is attributed to certain reducing substances such as catecholamines and ascorbic acid (Stockinger and Graf, 1965) and to lipid moieties unmasked from lipoprotein (Niebauer et al,. 1969).


  1. lip. ZIO positive cells were located in midepithelium. The cells were polygonal and did not show dendritic processes. These were probably nondendritic accessory antigen presenting cells (Fig. 1).
  2. Tongue. ZIO positive dendritic cells were present in the epithelium of the dorsal surface. The cells were basal and suprabasal and were located in layers at different levels of the epithelium. The processes numbered from one to five. Dendritic cells were not found within the cornified layer of the epithelium (Fig. 2).
  3. Oesophagus. ZIO positive dendritic cells were suprabasal and were located midway. The dendritic processes were thin and numbered two to three (Fig. 3).


Dendritic cells, which belong to mononuclear phagocyte family, initiate immune reactions in lymphocytes and have a critical role in antigen handling (Nossal, Abbot, Mitchell and Lummus, 1968; Veerman and van Rooijen, 1975.)

Dendritic cells have been observed in human epidermis (Mackenzie & Squire 1975), cervical epithelium (Figueroa and Caorlsi, 1980), tonsillar epithelium (Chandi et al. 1988), and oesophagus epithelium (Al Yassin and Toner, 1976).

Dendritic cells are revealed in human and animal epidermis (Mishima and Miller-Milinska, 1961) and in pigmented and unpigmented human, guinea pig and mouse skin (Riley, 1967). Information on epithelial dendritic cells has been derived mostly from epidermis (Prunieras, 1969; Fitzpatrick et al. 1967).

Oral epithelial dendritic cells are present with the epithelium of vestibular gingiva, hard palate, tongue, cheek mucosa, and skin of the external lip of the Rhesus monkey; the presence of dendrites easily distinguished such cells from keratinocytes; in no incident were dendritic cells found within the epithelial cornified layer (Hutchens et al. 1971).

Chimpanzee dendritic cells can be tested as immunotherapeutic agents for cancer, and be studied in relation to the pathogenesis of human immunodeficiency virus (HIV) infection (Barratt-Boyes, Henderson, and Finn, 1996). Dendritic cells can stimulate protective antitumour responses (Morse and Lyerly, 1998). Immunotherapy using autologous dendritic cells loaded with unfractionated tumour-derived antigens in the form of RNA is a powerful & useful vaccination strategy for cancer (Gilboa, Nair and Lyerly, 1998). Dendritic cells have an emerging role in novel cancer therapies (Hermans, Rawson, Ronchese and Richeie, 1998). Dendritic cells have the capacity to induce responses and are used as potent adjuvant for the treatment of human cancer (Nestle and Burge, 1999). Dendritic cell tumour vaccines for cancer immunotherapy reverse T cell energy and result in tumour rejection (Avigan, 1999). Efficient capture and presentation of antigens by dendritic cells is central to the induction of an immune response (Colaco, 1999). Human tumours express a number of protein antigens recognized by T cells. Dendritic cells are potent to present antigens to T cells. The dendritic cells are applied to cancer vaccines (Timmerman and Levy, 1999). Presence of dendritic cells in monkey suggests that these animal models may be used for vaccine and other experiments.

The location of the palatine tonsils at the gateway to the respiratory and digestive tracts suggests a functional role in generating an immune response to inhaled or swallowed antigens (Chandi et al. 1989). Similarly, to respond to inhaled or swallowed antigens, presence of the dendritic cells in the lip, tongue, and oesophagus is possible.

The distribution of ZIO positive dendritic cells in tongue and oesophagus and probably similar cells in lip in this study is important because of the antigens that enter through mouth. Dendritic cells are potent stimulators of primary T cell responses (Steiman, 1991). They reside in the interstitium of many tissues and epithelium of mucoa, where they take up and process both soluble and particulate antigens. Following exposure to antigens, dendritic cells mature and develop potent immunostimulatory activity whilst migrating to draining lymph nodes; there they interact with T cells to initiate T cell responses (Pavli et al. 1996). The distribution of dendritic cells in mucosal (luminal) epithelium suggests that these dendritic cells act as immune adjuvants by recruiting T cell responses when foreign luminal antigens enter the mucosa.

Acknowledgements :

The authors thank Dr. Gunasekaran Vaz for permitting us to take the tissues from the monkeys used for his experiments and fluid Research Committee of Christian Medical College, Vellore for funding this study.

References :

  1. Abraham, S., Indrasingh, I., Vettivel, S. and Chandi, G. (1996): Zinc iodide-osmium positive decidual and dendritic cells in normal human decidua. Journal of the Anatomical Society of India 45: 97-100.
  2. Abraham, S., Indrasingh, I., Vettivel, S. and Chandi, G. (2000): Groos morphology and ultrastructure of dendritic cells in the normal human decidua. Clinical Anatomy 13: 177-180.
  3. Al Yasin, T. and Toner, P.G. (1976): Langerhans cells in the human oesophagus. Journal of Anatomy 122: 435-445.
  4. Avigan, D. (1999): Dendritic cells: development, function and potential use for cancer immunotherapy Blood Review 13: 53-64.
  5. Barratt-Boyes, S.M., Henderson, R.A. and Finn, O.J. (1996): Chimpanzee dendritic cells with potent immunostimulatory function can be propagated from peripheral blood. Immunology 87: 528:534.
  6. Breathnach, A.S. and Goodwin, D. (1965): Electron microscopy of guinea-pig epidermis stained by the osmium-iodide technique. Journal of Anatomy 100: 159:172.
  7. Chandi, G., Indrasingh, I. And Sridharan, G. (1988): Dendritic cells in tonsillar epithelium. Journal of the Anatomical Society of India 37: 181-185.
  8. Chandi, G., Indrasingh, I. and Chandi, S.M. (1989): Electron microscopic demonstration of langerhans cells in human tonsillar epithelium. Clinical Anatomy 2: 271-276.
  9. Colaco, C.A. (1999): Why are dendritic cells central to cancer immunotherapy ? Molecular Medicine Today 5: 1417.
  10. Crocker, J. and Hopkins, M. (1984): Histiocytes and dendritic reticulum cells shown by a zinc iodide-osmium technique. Journal of Clinical Pathology 37: 620-627.
  11. Dagdevire, A., Alp, H. and Ors, U. (1994): New application for the zinc iodide-osmium tetroxide technique. Journal of Anatomy 184: 83-91.
  12. Figueroa, C.D. and Caoirsi, I. (1980): Ultrastructural and morphometric study of the langerhans cell in the normal human exocervix. Journal of Anatomy 131: 669-682.
  13. Fitzpatrick, T.B., Miyamoto, M. and Ishikawa, K. (1967): The evolution of concepts of melanin biology. Archives of Dermatology 96: 305.
  14. Gilboa, E., Nair, S.K. and Lyerly, H.K. (1998): Immunotherapy of cancer with dendritic-cell-based vaccines. Cancer Immunology and Immunotherapy 46: 82-87.
  15. Hart, D.N.J. and Fabre, J.W. (1981): Demonstration and characterization of Ia-positive dendritic cells in the interstitial connective tissue of the rat heart and other tissues, but not brain. Journal of Experimental Medicine 153: 347-361.
  16. Hermans, I.F., Rawson, M.P., Ronchese, F. and Ritchie, D.S. (1998): The emerging role of the dendritic cell in noval cancer therapies. New Zealand Medical Journal 111: 111113.
  17. Hu, J., Pope, M., Brown, C., O'Doetry, U. and Miller, J.(1998): Immunophenotypic characterization of simian immunodeficiency virus infected dendritic cells in cervix, vagina, and draining lymph nodes in rhesus monkeys Laboratory Investigation 78: 435-451.
  18. Hutchens, L.H., Sagebiel, R.W. and Clarke, M.A. (1971): Oral epithelial dendritic cells of the rhesus monkey - histologic demonstration, fine structure and quantitative distribution. The Journal of Investigative Dermatology 56: 325-336.
  19. Lenz, A., Heine, M., Schuler, G. and Romani, N. (1993): Human and murine dermis contains dendritic cells : Isolation by means of a novel method and phenotypical and functional characterization. Journal of Clinical Investigation 92: 25872596.
  20. Mackenzie, I.C. and Squiere, C.A (1975): Cytochemical identification of ATPase positive langerhans cells in EDTA separated sheets of mouse epidermis. British Journal of Dermatology. 92: 523-533.
  21. Miller, C.J., McChesney, M.B. and Moore, P.F. (1992) Langerhans cells, macrophages and lymphocyte subsets in the cervix and vagina of rhesus macaques. Laboratory Investigation 67: 628-634.
  22. Mishima, Y. and Miller-Miniska, A. (1961): Junctional and high level dendritic cells revealed with osmium iodide reaction in human and animal epidermis under conditions of hyperpigmentation and depigmentation. The Journal of Investigative Dermatology 37: 107.
  23. Morse, M.A. and Lyerly, H.K. (1998): Immunotherapy of cancer using dendritic cells. Cytokines Cell Molecular Therapy 4: 35-44.
  24. Muller, T. (1996): The different morphological types of dendritic cells and their innervation in stratified squamous epithelia of the rat as revealed by methylene blue staning. Biomedical Research 7: 149-157.
  25. Nestle, F.O. and Burge, G. (1999): Dendritic cells: Role in skin diseases and therapeutic applications. Clinical Experimental Dermatology 24: 204-207.
  26. Niebauer, G., Krawczyk, W.S., Kidd, R.L. and Wilgram, G.F. (1969): Osmium zinc iodide reactive sites in the epidermal langerhans cell. Journal of Cell Biology 43: 80-89.
  27. Nossal, G.J.V., Abbot, A., Mitchell, J. and Lummus, Z. (1968): Antigens in immunity. XV. ultrastractural features of antigen capture in primary and secondary lymphoid follicles. Journal of Experimental Medicine 127: 277-290.
  28. Pavli, P., Maxwell, L., Van De Pol, E. and Doe, W.F. (1996): Distribution of human colonic dendritic cells and macr
  29. Prickett, T.C.R., McKenzie, J.L. and Hard, D.N.J. (1988): Characterization of interstitial dendritic cells in human liver. Transplantation 46: 754-761.
  30. Purnieras, M. (1969): Interactions between keratinocytes and dendritic cells. The Journal of Investigative Dermatology 52: 1.
  31. Reley, P.A. (1967): A study of the distribution of epidermal dendritic cells in pigmented and unpigmented skin. The Journal of Investigative dermatology 48: 29-38.
  32. Rodriguez, E.M. and Caorsi, I. (1978): A second look at the ultrastructure of the langerhans cell of the human epidermis. Journal of Ultrastructure Research 65: 279-295.
  33. Sertle, K; Takemura, T; Tschachler, E; Ferrans, V.J., Kaliner, M.A. and Shevach, E.M. (1986): Dendritic cells with antigen-presenting capability reside in airway epithelium, lung parenchyma, and visceral pleura. Journal of Experimental Medicine 163: 436-451.
  34. Steinman, R.M. (1991): The dendritic cell system and its role in immunogenecity. Annual Review of Immunology 9: 271-296.
  35. Steinman, R.M. and Nussenzweig, M.C. (1980): Dendritic cells: Features and functions. Immunological Review 53: 127-147.
  36. Stockinger, I. and Graf, J. (1965): Electronenmikro- skopische analyse der osmium-zinkiodid methode. Milkroskopie 20: 16-35.
  37. Timmerman, J.M. and Levy, R. (1999): Dendritic cell vaccines for cancer immunotherapy. Annual Review of Medicine 50: 507-529.
  38. Veerman, A.J.P. and Van Rooijen, N. (1975): Lymphocyte capping and lymphocyte migration as associated events in the in vivo antigen tapping process. An electron microscopic autoradiographic study in the spleen of mice. Cell and Tissue Research 161: 211-217.
  39. Zelickson, A.S. and Mottax, J.H. (1968): Epidermal dendritic cells. A quantitative study. Archives of Dermatology 98: 652.

Opp. 34 Z.I.O. Positive Cells In Stratified Squamous Epithelium

Missing Image

Fig.1. Lip. ZIO positive cell (arrow):
E – Stratified squamous epithelium;
S – Subepithelial tissue ; 230x.

Missing Image

Fig.2. Tongue. ZIO positive dendritic cell (arrow) ;E - Stratified squamous epithelium;S - Subepithelial tissue; 550x.

Missing Image

Fig.3. Oesophagus. ZIO positive dendritic cell (arrow);E - Stratified Squamous epithelium;S - Subepithelial tissue; 165x.

J. Anat. Soc. India 50(1) 34-36 (2001)

Access free medical resources from Wiley-Blackwell now!

About Indmedica - Conditions of Usage - Advertise On Indmedica - Contact Us

Copyright © 2005 Indmedica