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PMID: 8686751 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Expression of most matrix metalloproteinase family members in breast cancer represents a tumor-induced host response.

The American journal of pathology ·Vol. 149 ·No. 1 ·1996-07-00 ·Pages 273-82

Heppner KJ, Matrisian LM, Jensen RA, Rodgers WH

Abstract

Matrix metalloproteinase (MMP) family members have been associated with advanced-stage cancer and contribute to tumor progression, invasion, and metastasis as determined by inhibitor studies. In situ hybridization was performed to analyze the expression and localization of all known MMPs in a series of human breast cancer biopsy specimens. Most MMPs were localized to tumor stroma, and all MMPs had very distinct expression patterns. Matrilysin was expressed by morphologically normal epithelial ducts within tumors and in tissue from reduction mammoplasties, and by epithelial-derived tumor cells. Many family members, including stromelysin-3, gelatinase A, MT-MMP, interstitial collagenase, and stromelysin-1 were localized to fibroblasts of tumor stroma of invasive cancers but in quite distinct, and generally widespread, patterns. Gelatinase B, collagenase-3, and metalloelastase expression were more focal; gelatinase B was primarily localized to endothelial cells, collagenase-3 to isolated tumor cells, and metalloelastase to cytokeratin-negative, macrophage-like cells. The MMP inhibitor, TIMP-1, was expressed in both stromal and tumor components in most tumors, and neither stromelysin-2 nor neutrophil collagenase were detected in any of the tumors. These results indicate that there is very tight and complex regulation in the expression of MMP family members in breast cancer that generally represents a host response to the tumor and emphasize the need to further evaluate differential functions for MMP family members in breast tumor progression.

MeSH Terms
Antisense Elements (Genetics) Breast Neoplasms/chemistry,physiopathology Carcinoma in Situ/chemistry,physiopathology Carcinoma, Ductal, Breast/chemistry,physiopathology Endothelium/chemistry Epithelium/chemistry Female Fibroblasts/chemistry Humans In Situ Hybridization Metalloendopeptidases/analysis,genetics RNA, Messenger/analysis
Chemicals
Antisense Elements (Genetics) RNA, Messenger Metalloendopeptidases
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Heppner K J
Department of Cell Biology, Vanderbilt University, Nashville, Tennessee, USA.
Matrisian L M
Jensen R A
Rodgers W H
References (46)
46 references, click to expand
  1. SV40-transformed human lung fibroblasts secrete a 92-kDa type IV collagenase which is identical to that secreted by normal human macrophages.
    J Biol Chem. 1989 Oct 15;264(29):17213-21 PMID: 2551898
  2. The collagenase gene family in humans consists of at least four members.
    Biochem J. 1988 Jul 1;253(1):187-92 PMID: 2844164
  3. Antitumor promotion and antiinflammation: down-modulation of AP-1 (Fos/Jun) activity by glucocorticoid hormone.
    Cell. 1990 Sep 21;62(6):1189-204 PMID: 2169351
  4. Transcriptional interference between c-Jun and the glucocorticoid receptor: mutual inhibition of DNA binding due to direct protein-protein interaction.
    Cell. 1990 Sep 21;62(6):1205-15 PMID: 2169352
  5. Concanavalin A produces a matrix-degradative phenotype in human fibroblasts. Induction and endogenous activation of collagenase, 72-kDa gelatinase, and Pump-1 is accompanied by the suppression of the tissue inhibitor of matrix metalloproteinases.
    J Biol Chem. 1990 Dec 5;265(34):21141-51 PMID: 2174435
  6. Contributions of tumor and stromal matrix metalloproteinases to tumor progression, invasion and metastasis.
    Cancer Metastasis Rev. 1995 Dec;14(4):351-62 PMID: 8821095
  7. A novel metalloproteinase gene specifically expressed in stromal cells of breast carcinomas.
    Nature. 1990 Dec 20-27;348(6303):699-704 PMID: 1701851
  8. Expression of metalloproteinase genes in human prostate cancer.
    J Cancer Res Clin Oncol. 1991;117(2):144-50 PMID: 1848860
  9. Structure and expression of the cDNA encoding human neutrophil collagenase.
    Blood. 1991 Jun 15;77(12):2731-8 PMID: 1646048
  10. Expression of collagenase-related metalloproteinase genes in human lung or head and neck tumours.
    Int J Cancer. 1991 Jun 19;48(4):550-6 PMID: 1646178
  11. Metalloproteinases and their inhibitors in matrix remodeling.
    Trends Genet. 1990 Apr;6(4):121-5 PMID: 2132731
  12. Expression and localization of the matrix metalloproteinase pump-1 (MMP-7) in human gastric and colon carcinomas.
    Mol Carcinog. 1991;4(6):527-33 PMID: 1793490
  13. Immunolocalization of matrix metallo-proteinases and their tissue inhibitor in human mammary pathology.
    Bull Cancer. 1992;79(3):261-70 PMID: 1392165
  14. Expression of the stromelysin-3 gene in fibroblastic cells of invasive carcinomas of the breast and other human tissues: a review.
    Breast Cancer Res Treat. 1993;24(3):185-93 PMID: 8435474
  15. Stromelysin 3 belongs to a subgroup of proteinases expressed in breast carcinoma fibroblastic cells and possibly implicated in tumor progression.
    Proc Natl Acad Sci U S A. 1993 Mar 1;90(5):1843-7 PMID: 8446598
  16. Urokinase and urokinase receptor: a paracrine/autocrine system regulating cell migration and invasiveness.
    Bioessays. 1993 Feb;15(2):105-11 PMID: 8385942
  17. A synthetic matrix metalloproteinase inhibitor decreases tumor burden and prolongs survival of mice bearing human ovarian carcinoma xenografts.
    Cancer Res. 1993 May 1;53(9):2087-91 PMID: 8347186
  18. Activity of type IV collagenases in benign and malignant breast disease.
    Br J Cancer. 1993 May;67(5):1126-31 PMID: 8494711
  19. The basic region of AP-1 specifies glucocorticoid receptor activity at a composite response element.
    Genes Dev. 1992 Dec;6(12B):2491-501 PMID: 1340464
  20. Cloning and characterization of a unique elastolytic metalloproteinase produced by human alveolar macrophages.
    J Biol Chem. 1993 Nov 15;268(32):23824-9 PMID: 8226919
  21. Stromelysin-3 expression in breast cancer biopsies: clinico-pathological correlations.
    Int J Cancer. 1993 Nov 11;55(5):771-4 PMID: 8244574
  22. Structure and expression in breast tumors of human TIMP-3, a new member of the metalloproteinase inhibitor family.
    Cancer Res. 1994 Apr 15;54(8):2091-4 PMID: 8174111
  23. Molecular cloning and expression of collagenase-3, a novel human matrix metalloproteinase produced by breast carcinomas.
    J Biol Chem. 1994 Jun 17;269(24):16766-73 PMID: 8207000
  24. Expression of matrilysin mRNA in colorectal adenomas and its induction by truncated fibronectin.
    Biochem Biophys Res Commun. 1994 Jun 15;201(2):657-64 PMID: 8002999
  25. 72 KD and 92 KD type IV collagenase, type IV collagen, and laminin mRNAs in breast cancer: a study by in situ hybridization.
    J Histochem Cytochem. 1994 Jul;42(7):945-51 PMID: 8014478
  26. A matrix metalloproteinase expressed on the surface of invasive tumour cells.
    Nature. 1994 Jul 7;370(6484):61-5 PMID: 8015608
  27. Gelatinase A expression and localization in human breast cancers. An in situ hybridization study and immunohistochemical detection using confocal microscopy.
    Virchows Arch. 1994;424(6):641-5 PMID: 8055158
  28. Modulation of matrilysin levels in colon carcinoma cell lines affects tumorigenicity in vivo.
    Cancer Res. 1994 Sep 1;54(17):4805-12 PMID: 8062282
  29. Expression and localization of matrix-degrading metalloproteinases during colorectal tumorigenesis.
    Mol Carcinog. 1994 Aug;10(4):199-206 PMID: 8068180
  30. Patterns of matrix metalloproteinase expression in cycling endometrium imply differential functions and regulation by steroid hormones.
    J Clin Invest. 1994 Sep;94(3):946-53 PMID: 8083380
  31. Correlation between stromelysin-3 mRNA level and outcome of human breast cancer.
    Int J Cancer. 1994 Sep 15;58(6):830-5 PMID: 7927875
  32. Enhanced expression of tissue inhibitor of metalloproteinase-2 (TIMP-2) in the stroma of breast carcinomas correlates with tumor recurrence.
    Int J Cancer. 1994 Nov 1;59(3):339-44 PMID: 7927938
  33. Inhibition of angiogenesis and murine hemangioma growth by batimastat, a synthetic inhibitor of matrix metalloproteinases.
    J Natl Cancer Inst. 1995 Feb 15;87(4):293-8 PMID: 7535861
  34. Membrane-type matrix metalloproteinase (MT-MMP) gene is expressed in stromal cells of human colon, breast, and head and neck carcinomas.
    Proc Natl Acad Sci U S A. 1995 Mar 28;92(7):2730-4 PMID: 7708715
  35. Inhibition of bone resorption in vitro by selective inhibitors of gelatinase and collagenase.
    Biochem J. 1995 May 15;308 ( Pt 1):167-75 PMID: 7755562
  36. Human macrophage metalloelastase. Genomic organization, chromosomal location, gene linkage, and tissue-specific expression.
    J Biol Chem. 1995 Jun 16;270(24):14568-75 PMID: 7782320
  37. Inhibition of organ invasion by the matrix metalloproteinase inhibitor batimastat (BB-94) in two human colon carcinoma metastasis models.
    Cancer Res. 1995 Aug 15;55(16):3629-33 PMID: 7627972
  38. Matrix metalloproteinase matrilysin is constitutively expressed in adult human exocrine epithelium.
    J Invest Dermatol. 1995 Aug;105(2):190-6 PMID: 7636300
  39. Transforming growth factor beta mediates the progesterone suppression of an epithelial metalloproteinase by adjacent stroma in the human endometrium.
    Proc Natl Acad Sci U S A. 1995 Aug 1;92(16):7362-6 PMID: 7638197
  40. cDNA sequence and mRNA tissue distribution of a novel human matrix metalloproteinase with a potential transmembrane segment.
    Eur J Biochem. 1995 Aug 1;231(3):602-8 PMID: 7649159
  41. The metalloproteinase matrilysin is preferentially expressed by epithelial cells in a tissue-restricted pattern in the mouse.
    Mol Biol Cell. 1995 Jul;6(7):851-69 PMID: 7579699
  42. Matrilysin: an epithelial matrix metalloproteinase with potentially novel functions.
    Int J Biochem Cell Biol. 1996 Feb;28(2):123-36 PMID: 8729000
  43. Primary structure and cDNA cloning of human fibroblast collagenase inhibitor.
    Proc Natl Acad Sci U S A. 1986 Apr;83(8):2407-11 PMID: 3010309
  44. Tumor invasion through the human amniotic membrane: requirement for a proteinase cascade.
    Cell. 1986 Nov 21;47(4):487-98 PMID: 3022933
  45. H-ras oncogene-transformed human bronchial epithelial cells (TBE-1) secrete a single metalloprotease capable of degrading basement membrane collagen.
    J Biol Chem. 1988 May 15;263(14):6579-87 PMID: 2834383
  46. Immunohistochemical distribution of type IV collagenase in normal, benign, and malignant breast tissue.
    Am J Pathol. 1990 Mar;136(3):585-92 PMID: 2156430
Article Info
Journal
The American journal of pathology
Abbr.
Am J Pathol
ISSN
0002-9440
Published
1996-07-00
Pages
273-82
Language
English
Region
United States
NLM ID
0370502
PMCID
PMC1865221
Subset
IM
Grants
NCI NIH HHS · R01 CA50468 · United States
NICHD NIH HHS · R01 HD30472 · United States
NCI NIH HHS · R03 CA54942 · United States
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