Three-dimensional visualization of perlecan-rich neoplastic stroma induced concurrently with the invasion of oral squamous cell carcinoma

J Oral Pathol Med. 2014 Sep;43(8):627-36. doi: 10.1111/jop.12184. Epub 2014 Apr 4.

Abstract

Background: We have demonstrated the induction of perlecan-rich stroma of oral squamous cell carcinoma (SCC) on and after its start of invasion. However, it remains unknown how such a neoplastic stroma is actually arranged in tumor tissues.

Methods: To this end, tissue microarray samples, in which keratin and perlecan were contrastively labeled by immunohistochemistry, were three-dimensionally analyzed using digital images and image analysis software to demonstrate the relationship between SCC foci and the perlecan-positive stromal space or that between carcinoma in situ (CIS) and invasive SCC foci.

Results: The three-dimensional (3D) reconstruction demonstrated three kinds of perlecan profiles for inside (I) and outside (O) areas of the carcinoma cell focus: mode 1, I(+)/O(-) ; mode 2, I(+)/O(+) ; and mode 3, I(-)/O(+). Mode 1 was seen in CIS as well as SCC tumor massifs in the surface part. Mode 2 was seen in small SCC foci, which seemed isolated in 2D sections but were mostly continuous with the tumor massif in 3D reconstructions. Mode 3 was limited to small SCC foci, which were truly segregated from the tumor massif.

Conclusions: The results indicated that the 2D SCC focus isolation could not be regarded as invasion but that the SCC foci surrounded by perlecan-positive stroma (modes 2 and 3) could be regarded as a more objective measure for invasion of SCC. This is the first 3D tissue-level demonstration of the neoplastic stroma space induced with oral SCC invasion, the presence of which we have predicted based on our previous 2D and tissue culture evidence.

Keywords: invasion judgment; neoplastic stroma; oral squamous cell carcinoma; perlecan; three-dimensional visualization.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aged
  • Aged, 80 and over
  • Carcinoma in Situ / chemistry
  • Carcinoma in Situ / pathology
  • Carcinoma, Squamous Cell / chemistry*
  • Carcinoma, Squamous Cell / pathology
  • Connective Tissue / chemistry
  • Connective Tissue / pathology
  • Epithelium / chemistry
  • Epithelium / pathology
  • Female
  • Heparan Sulfate Proteoglycans / chemistry*
  • Humans
  • Image Processing, Computer-Assisted / methods*
  • Imaging, Three-Dimensional / methods*
  • Immunohistochemistry
  • Keratin-13 / analysis
  • Keratin-17 / analysis
  • Keratin-19 / analysis
  • Ki-67 Antigen / analysis
  • Male
  • Middle Aged
  • Neoplasm Invasiveness
  • Precancerous Conditions / chemistry
  • Precancerous Conditions / pathology
  • Tissue Array Analysis
  • Tongue Neoplasms / chemistry*
  • Tongue Neoplasms / pathology

Substances

  • Heparan Sulfate Proteoglycans
  • KRT13 protein, human
  • Keratin-13
  • Keratin-17
  • Keratin-19
  • Ki-67 Antigen
  • perlecan