Skip to main content
SpringerLink
Log in

Ultrastructural morphometry of collagen from lamina propria during experimental oral carcinogenesis and chronic inflammation

  • Original Papers
  • Published:
Journal of Cancer Research and Clinical Oncology Aims and scope Submit manuscript

Summary

Stereological point-counting methods were used to determine the volumetric alterations in collagen from the lamina propria immediately beneath the epithelial-connective tissue junction in hamster check-pouch mucosa treated with the chemical carcinogen DMBA. In addition, a non-neoplastic inflammatory control was evaluated in which a delayed hypersensitivity reaction was induced by the contact-sensitising agent DNCB. DMBA-treated tissues were assigned to histopathologically defined hyperplasia, dysplasia and carcinoma stages. The volume densities of collagen present in unit volume of extracellular lamina propria were found to decrease progressively and significantly in DMBA-treated tissues when compared with values obtained from normal untreated mucosa. Values from the inflammatory control were comparable with those from the dysplasia stage of carcinogenesis. The mechanisms responsible for these decreases in collagen volume density are unknown, but contributory factors might include collagen destruction by enzymes originating in either the epithelium or the cells of the inflammatory infiltrate, dilution of collagen produced by inflammatory oedema or alterations in the synthetic capabilities of fibroblasts.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Alroy J, Gould VE (1980) Epithelial stromal interface in normal and neoplastic human bladder epithelium. Ultrastruct Pathol 1:201–210

    Google Scholar 

  • Birbeck MJC, Wheatley DN (1965) An electron microscopic study of the invasion of ascites tumour cells into the abdominal wall. Cancer Res 25:490–497

    Google Scholar 

  • Birkedal-Hansen H, Cobb CM, Taylor RE (1976) Fibroblastic origin of bovine gingival collagenase. Arch Oral Biol 21:297–305

    Google Scholar 

  • Cimasoni G, Ishikawa I, Jaccard F (1977) Enzymes in the gingival crevice. In: Lehner T (ed). The Borderland between Caries and Periodontal Disease. London, Academic Press, pp 13–41

    Google Scholar 

  • Daniel A, Dupont M (1980) Analyse stereologique du tissu conjonctif gingival humain. Le gencive cliniquement saine. Biol Buccale 8:141–153

    Google Scholar 

  • Dobson RL, Griffin M (1962) The histochemistry of cutaneous carcinogenesis. I. The dermis. J Invest Dermatol 39:597–602

    Google Scholar 

  • Etherington DJ (1977) Collagen degradation. Ann Rheum Dis 36. (Suppl) 2:14–17

    Google Scholar 

  • Etherington DJ, Silver IA, Gibbons R (1979) An in vitro model for the study of collagen degradation during acute inflammation. Life Sci 25:1885–1892

    Google Scholar 

  • Freedman HL, Listgarten MA, Taichman NS (1968) Electron microscopic features of chronically inflamed human gingiva. J Periodont Res 3:313–327

    Google Scholar 

  • Frithiof L (1972) Ultrastructural changes at the epithelial stromal junction in human oral preinvasive and invasive carcinoma. In: Tarin D (ed). Tissue Interaction in Carcinogenesis. New York, Academic Press, pp 161–187

    Google Scholar 

  • Fullmer HM, Gibson WA, Lazarus GS, Bladen HA, Whedon KA (1969) The origin of collagenase in periodontal tissues in man. J Dent Res 48:646–651

    Google Scholar 

  • Garant PR, Mulvihill JE (1971) The ultrastructure of leucocyte emigration through the sulcular epithelium in the beagle dog. J Periodont Res 6:266–277

    Google Scholar 

  • Geiger S, Harper E (1980) Human gingival collagenase in periodontal disease: the release of collagenase and the breakdown of endogenous collagen in gingival explants. J Dent Res 59:11–16

    Google Scholar 

  • Glauert AM, Fell HB, Dingle JT (1969) Endocytosis of sugars in embryonic skeletal tissues in organ culture. II. Effect of sucrose on cellula fine structure. J Cell Sci 4:105–131

    Google Scholar 

  • Gohari K (1978) A quantitative morphological and cytochemical study of the synthetic and metabolic apparatus in hamster cheek pouch epithelium during chemical carcinogenesis. Ph.D. Thesis, University of Sheffield, England

    Google Scholar 

  • Green H, Goldberg B, Todoro J (1966) Differential cell types and the regulation of collagen synthesis. Nature (London) 212:631–633

    Google Scholar 

  • Goss J (1976) Aspects of animal collagenases. In: Ramachandran GN, Reddi AH (eds). Biochemistry of Collagen. New York and London, Plenum Press, pp 275–317

    Google Scholar 

  • Hall BK, Squier CA (1982) Ultrastructural quantitation of connective tissue changes in phenytoin-induced gingival overgrowth in the ferret. J Dent Res 61:942–952

    Google Scholar 

  • Harris ED, Crane SM (1974) Collagenases. N Engl J Med 291:557–563

    Google Scholar 

  • Hashimoto K, Yamanishi Y, Maeyens E, Dabbous MK, Kanzaki T (1973) Collagenolytic activities of squamous cell carcinoma of the skin. Cancer Res 33:2790–2801

    Google Scholar 

  • Karnovsky MJ (1965) A formaldehyde glutaraldehyde fixative of high osmolarity for use in electron microscopy. J Cell Biol 27:137A-138A

    Google Scholar 

  • Kowashi Y, Jaccard F, Cimasoni G (1979) Increase in free collagenase and neutral proteinase activities in the gingival crevice during experimental gingivitis in man. Arch Oral Biol 24:645–650

    Google Scholar 

  • Kramer IRH (1980) Basic histopathological features of oral premalignant lesions. In Mackenzie IC, Dabelsteen E, Squier CA (eds) (1980) Oral Premalignancy: Proceedings of the First Dows Symposium. University of Iowa Press, pp 23–34

  • Lange D, Schroeder HE (1971) Cytochemistry and ultrastructure of gingival sulcular cells. Helv Odontol Acta 15:65–86

    Google Scholar 

  • Lazarus GS, Daniels JR, Brown RS (1968) Degradation of collagen by a human granulocyte collagenolytic system. J Clin Invest 47:262–269

    Google Scholar 

  • Mazzucco K (1972) The role of collagen in tissue interaction during carcinogenesis in mouse skin. In: Tarin D (ed): Tissue Interactions in Carcinogenesis. New York, Academic Press, pp 377–398

    Google Scholar 

  • Machinami R (1973) A study of the invasive growth of malignant tumours. II. Ultrastructural features of the metastatic growth of Yoshida ascites hepatoma 7974 in the rat brain. Acta Pathol Jpn 23:261–278

    Google Scholar 

  • Mohammad AR, Mincer HH (1976) Dinitrochlorobenzene contact hypersensitivity in the hamster cheek pouch. J Oral Pathol 5:169–174

    Google Scholar 

  • Orr JW (1938) The changes antecedent to tumour promotion during the treatment of mouse skin with carcinogenic hydrocarbons. J Pathol Bacteriol 46:495–515

    Google Scholar 

  • Parakkal PF (1969) Involvement of macrophages in collagen resorption. J Cell Biol 41:345–354

    Google Scholar 

  • Perez-Tamayo R (1970) Collagen resorption in carrageenin granulomas. II. Ultrastructure of collagen resorption. Lab Invest 22:142–159

    Google Scholar 

  • Pinto JS, Dobson RL, Bentley JP (1970) Dermal collagen changes during 2-amino-anthracene carcinogenesis in the rat. Cancer Res 30:1168–1173

    Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J Cell Biol 17:208–212

    Google Scholar 

  • Seilern-Aspang F, Mazzucco K, Christian I (1969) Der Einfluß von Methylcholanthren auf Synthese Vernezung und Abbau des Kollagens der Mäusedermis und die mögliche Bedeutung dieses Abbaues für malignes Wachstum. Z Natuforsch [B] 24:894–901

    Google Scholar 

  • Schroeder HE, Lindhe J (1980) Conditions and pathological features of rapidly destructive experimental periodontitis in dogs. J Periodontol 51:7–19

    Google Scholar 

  • Schroeder HE, Lindhe J, Hugoson A, Münzel-Pedrazzoli S (1973a) Structural constituents of clinically normal and slightly inflamed dog gingiva. Helv Odontol Acta 17:70–83

    Google Scholar 

  • Schroeder HE, Münzel-Pedrazzoli S, Page R (1973b) Correlated morphometric and biochemical analysis in gingival tissue in carly chronic gingivitis in man. Arch Oral Biol 18:899–923

    Google Scholar 

  • Smith CJ (1972) The epithelial-connective tissue junction in the pathogenesis of human and experimental oral cancer. In: Tarin D (ed): Tissue Interactions in Carcinogenesis. New York, Academic Press, pp 191–225

    Google Scholar 

  • Smith CJ (1980) Experimental animal models for oral premalignancy. In: Mackenzie IC, Dabelsteen E Squier CA (eds) Oral Premalignancy: Proceedings of the First Dows Symposium. University of Iowa Press, pp 78–100

  • Smith CJ, Pindborg JJ (1969) Histological grading of oral epithelial atypia by the use of photographic standards. W.H.O. International Reference Centre of Oral Precancerous Condition. C. Hamburgers Bogtrykkeri, Copenhagen

    Google Scholar 

  • Squier CA, Kremenak CR (1982) Quantitation of the healing palatal mucoperiosteal wound in the beagle dog. Br J Exp Pathol 63:573–584

    Google Scholar 

  • Strauch L (1972) The role of collagenases in tumour invasion. In: Tarin D (ed): Tissue Interaction in Carcinogenesis. New York, Academic Press, pp 393–433

    Google Scholar 

  • Strauli P, Weiss L (1977) Cell locomotion and tumour penetration. Eur J Cancer 13:1–12

    Google Scholar 

  • Tarin D (1967) Sequential electron microscopic studies of experimental mouse skin carcinogenesis. Int J Cancer 2:195–211

    Google Scholar 

  • Tarin D (1968) Further electron microscopic studies on the mechanisms of carcinogenesis. The specificity of the changes in carcinogen treated mouse skin. Int J Cancer 3:734–742

    Google Scholar 

  • Tarin D (1969) Fine structure of murine mammary tomours: the relationship between epithelium and connective tissue in neoplasms induced by various agents. Br J Cancer 23:417–425

    Google Scholar 

  • Tarin d (1972) Morphological studies on the mechanism of carcinogenesis. In: Tarin D (ed). Tissue Interaction in Carcinogenesis. New York, Academic Press, pp 227–286

    Google Scholar 

  • Taichman NS, Freedman HL, Urihara T (1966) Inflammation and tissue injury. I. The response to intradermal injections of human dentogingival plaque in normal and leukopenic rabbits. Arch Oral Biol 11:1385–1392

    Google Scholar 

  • Urban JL, Unsworth BR (1977) Lysosomal enzyme release associated with the invasion of rat liver by Novikoff hepatoma. Experientia 33:1217–1219

    Google Scholar 

  • Weibel ER (1969) Stereological principles for morphometry in electron microscopic cytology. Int Rev Cytol 26:235–302

    Google Scholar 

  • Weibel ER, Bolender RP (1973) Stereological techniques for electron microscopic morphometry. In: Hayat MA (ed). Principles and Techniques of Electron Microscopy Vol 3. New York, Van Nostrand, Reinhold Co., pp 237–296

    Google Scholar 

  • Werb Z, Gordon S (1975) Secretion of a specific collagenase by stimulated macrophages. J Exp Med 142:346–360

    Google Scholar 

  • White FH, Gohari K (1981a) The ultrastructural morphology of hamster cheek pouch epithelium. Arch Oral Biol 26:563–576

    Google Scholar 

  • White FH, Gohari K (1981b) Variation in nuclear cytoplasmic ratio during epithelial differentiation in experimental oral carcinogenesis. J Oral Pathol 10:164–172

    Google Scholar 

  • White FH, Gohari K (1981c) A quantitative study of lamina densa alterations in hamster cheek pouch carcinogenesis. J Pathol 135:277–294

    Google Scholar 

  • White FH, Gohari K (1981d) Quantitative studies of hemidesmosomes during progressive DMBA carcinogenesis in hamster cheek pouch mucosa. Br J Cancer 44:440–450

    Google Scholar 

  • White FH, Gohari K (1984a) Hemidesmosmal dimensions and frequency in experimetal oral carcinogenesis; a stereological investigation. Virch Arch Cell Pathol [B] 45:1–13

    Google Scholar 

  • White FH, Gohari K (1984b) Alterations in the volume of the intercellular space between epithelial cells of the hamster cheek pouch: quantitative studies of normal and carcinogen treated tissues. J Oral Pathol (in press)

  • White FH, Gohari K, Smith CJ (1981) Histological and ultrastructural morphology of 7, 12 dimethylbenz(α)anthracene carcinogenesis in hamster cheek pouch epithelium. Diagnost Histopathol 4:306–333

    Google Scholar 

  • White FH, Mayhew TM, Gohari K (1980) The application of morphometric methods to investigations of normal and pathological stratified squamous epithelium. Pathol Res Pract 166:323–346

    Google Scholar 

  • Yamanishi Y, Dabbous MK, Hashimoto K (1972) Effect of collagenolytic activity in basal cell epithelioma of the skin on reconstitute collagen and physical properties and kinetics of the crude enzyme. Cancer Res 32:2551–2560

    Google Scholar 

  • Yamanishi Y, Maeyens E, Dabbous MK, Ohyama H, Hashimoto K (1973) Collagenolytic activity in malignant melanoma: physicochemical studies. Cancer Res 33:2507–2512

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy and Cell Biology, University of Sheffield, S10 2TN, Sheffield, England

    S. G. Tarpey & F. H. White

Authors
  1. S. G. Tarpey
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. F. H. White
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tarpey, S.G., White, F.H. Ultrastructural morphometry of collagen from lamina propria during experimental oral carcinogenesis and chronic inflammation. J Cancer Res Clin Oncol 107, 183–194 (1984). https://doi.org/10.1007/BF01032605

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01032605

Key words

Search

Navigation