Abstract
Matrix metalloproteinase-1 (MMP-1) is involved in the degradation of interstitial collagen and thus thought to play a role in invasion of carcinoma. We investigated 51 oesophageal carcinoma patients to clarify the significance of MMP-1. MMP-1 mRNA was demonstrated to be expressed exclusively in almost all carcinoma tissue specimens (T) (94.1%) by reverse transcription-polymerase chain reaction, but not found in normal mucosal tissue specimens (N). The mean T/N ratio of MMP-1 was 42.5 and cases with T/N ≥ 10 had a higher incidence of cases involving muscularis propria than those with T/N < 10 which included all the cases involving the submucosa (P< 0.05). MMP-1 mRNA was significantly associated with both 40 kD (putative active MMP-1) and 50 kD (putative latent MMP-1) gelatinolytic bands (n=17). These findings indicated that MMP-1 mRNA reflected the net function of MMP-1 and suggested MMP-1 to be involved in carcinoma invasive process. On the other hand, MMP-1 mRNA was inversely correlated with the patient prognosis (P< 0.01). These results indicated that MMP-1 might therefore play a crucial role in local invasion, but not in systemic dissemination. As a result, MMP-1 might be a novel prognostic factor independent from those previously reported in oesophageal carcinoma. © 2001 Cancer Research Campaign http://www.bjcancer.com
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References
Baba K, Kuwano H, Kitamura K and Sugimachi K (1993) Carcinomatous invasion and lymphocyte infiltration in early esophageal carcinoma with special regard to the basement membrane. An immunohistochemical study. Hepatogastoroenterol 40: 226–231
Brooks P, Silletti S, von Schalscha T, Friendlander M and Cheresh D (1998) Disruption of angiogenesis by PEX, a noncatalytic metalloproteinase fragment with integrin binding activity. Cell 92: 391–400
Brown PD, Levy AT, Margulies IMK, Liotta LA and Stetler-Stevenson WG (1990) Independent expression and cellular processing of Mr 72,000 type IV collagenase and interstitial collagenase in human tumorigenic cell lines. Cancer Res 50: 6184–6191
Burman JF and Carter RL (1985) Lysis of type-I collagen by squamous carcinomas of the head and neck. Int J Cancer 36: 109–116
Fisher E, Paik S, Rockette H, Jones J, Caplan R and Fisher B (1989) Prognostic significance of eosinophils and mast cells in rectal cancer. Hum Pathol 20: 159–163
Gray S, Yun K, Motoori T and Kuys Y (1993) Interstitial collagenase gene expression in colonic neoplasia. Am J Pathol 143: 663–671
Japanese Society for Oesophageal Disease (1976) Guidelines for the clinical and pathologic studies on carcinoma of the oesophagus. Jpn J Surg 6: 69–78
Kim J, Yu W, Kavolski K and Ossowski L (1998) Requirement for specific proteases in cancer cell intravasation as revealed by a novel semiquantitative PCR-based assay. Cell 94: 353–362
Liotta L, Tryggvason K, Garbisa S, Hart I, Foltz C and Shafie S (1980) Metastatic potential correlates with enzymatic degradation of basement membrane collagen. Nature (Lond) 284: 67–68
Liotta L, Steeg P and Stetler-Stevenson W (1991) Cancer metastasis and angiogenesis: an imbalance of positive and negative regulation. Cell 64: 327–336
Lowe D, Jorizzo J and Hutt M (1981) Tumor-associated eosinophilia. A Review J Clin Pathol 34: 1343–1348
Masson R, Lefebvre O, Noel A, Fahime ME, Chenard M-P, Wendling C, Kebers F, LeMeur M, Dierich A, Foidart J-M, Basset P and Rio M-C (1998) In vivo evidence that the stromelysin-3 metalloproteinase contributes in a paracrine manner to epithelial cell malignancy. J Cell Biol 140: 1535–1541
McGinnis M, EL Bradley J, Pretlow T, Ortiz-Reyes R, Bowden C, Stellato T and II TP (1989) Correlation of stromal cells by morphometric analysis with metastatic behavior of human colonic carcinoma. Cancer Res 49: 5989–5993
Migita T, Sato E, Saito K, Mizoi T, Shiiba K, Matsuno S, Nagura H and Ohtani H (1999) Differing expression of MMPs-1 and -9 and urokinase receptor between diffuse-and intestinal-type gastric carcinoma. Int J Cancer 84: 74–79
Mimori K, Mori M, Inoue H, Ueo H, Mafune K, Akiyoshi T and Sugimachi K (1996) Elongation factor 1 gamma mRNA expression in oesophageal carcinoma. Gut 38: 66–70
Mori M, Barnard GF, Raymond J, Sttaniunas JM, Steele GD Jr and Chen LB (1993) Prothymosin-α mRNA expression correlates with that of c-myc in human colon cancer. Oncogene 8: 2821–2826
Mori M, Mimori K, Shiraishi T, Fujie T, Baba K, Kusumoto H, Haraguchi M, Ueo H and Akiyoshi T (1997) Analysis of MT1-MMP and MMP2 expression in human gastric cancers. Int J Cancer 74: 316–321
Murray GI, Duncan ME, O'Neil P, Melvin WT and Fothergill JE (1996) Matrix metalloproteinase-1 is associated with poor prognosis in colorectal cancer. Nat Med 2: 461–462
Murray GI, Duncan ME, Arbuckle E, Melvin WT and Fothergill JE (1998a) Matrix metalloproteinases and their inhibitors in gastric cancer. Gut 43: 791–797
Murray GI, Duncan ME, O'Neil P, Mckay JA, Melvin WT and Fothergill JE (1998b) Matrix metalloproteinase-1 is associated with poor prognosis in oesophageal cancer. J Pathol 185: 256–261
Okada A, Bellocq J-P, Rouyer N, Chenard M-P, Rio M-C, Chambon P and Basset P (1995) Membrane-type matrix metalloproteinase (MT-MMP) gene is expressed in stromal cells of human colon, breast, and head and neck carcinoma. Proc Natl Acad Sci USA 92: 2730–2734
Ono Y, Fujii M, Kameyama K, Otani Y, Sakurai Y and Kanzai J (1997) Expression of matrix metalloproteinase-1 mRNA related to eosinophilia and interleukin-5 gene expression in head and neck tumor tissues. Virchows Arch 431: 305–310
Ossowski L (1992) Invasion of connective tissue by human carcinoma cell lines: Requirement for urokinase, urokinase receptor, and interstitial collagenase. Cancer Res 52: 6754–6760
Otani Y, Okazaki I, Arai M, Kameyama K, Wada N, Maruyama K, Yoshino K, Kitajima M, Hosoda Y and Tsuchiya M (1994) Gene expression of interstitial collagenase (matrix metalloproteinase 1) in gastrointestinal tract cancers. J Gastroenterol 29: 391–397
Pretlow T, Keith E, Cryar K, Bartolucci A, Pitts A, Pretlow TI, Kimball P and Boohaker E (1983) Eosinophilic infiltration of human colonic carcinoma as a prognostic indicator. Cancer Res 43: 2997–3000
Remacle A, Noel A, Duggan C, McRermott E, O'higgins N, Foidart J and Duffy M (1996) Assay of matrix metalloproteinases type 1, 2, 3 and 9 in breast cancer. Br J Cancer 77: 925–931
Shima I, Sasaguri Y, Kusukawa J, Yamana H, Fujita H, Kakegawa T and Morimatsu M (1992) Production of matrix metalloproteinase-2 and metalloproteinase-3 related to malignant behavior of esophageal carcinoma. A clinicopathologic study Cancer 70: 2747–2753
Sier C, Kubben F, Ganesh S, Heerding M, Griffioen G, Hanemaaijer R, Krieken JV, Lamers C and Verspaget H (1996) Tissue levels matrix metalloproteinases MMP2 and MMP9 are related to the overall survival of patients with gastric carcinoma. Br J Cancer 74: 413–417
Sugimachi K, Ohno S, Matsumoto H, Mori M, Matsuoka H and Kuwano H (1989) Clinicopathologic study of early stage esophageal carcinoma. Surgery 105: 706–710
Takeha S, Fujiyama Y, Bamba T, Sorsa T, Nagura H and Ohtani H (1997) Stromal expression of MMP-9 and urokinase receptor is inversely associated with liver metastasis and with infiltrating growth in human colorectal cancer: a novel approach from immune/inflammatory aspect. Jpn J Cancer Res 88: 72–81
van der Stappen JF Jr, Hendriks J and Wobbes T (1990) Correlation between collagenolytic activity and grade of histological differentiation in colorectal tumors. Int J Cancer 45: 1071–1078
Wilson CL, Heppner KJ, Labosky PA, Hogan BLM and Matrisian LM (1997) Intestinal tumorigenesis is suppressed in mice lacking the metalloproteinase matrilysin. Proc Natl Acad Sci USA 94: 1402–1407
Woessner JE Jr (1991) Matrix metalloproteinases and their inhibitors in connective tissue remodeling. FASEB J 5: 2145–2154
Yamashita K, Mori M, Shiraishi T, Shibuta K and Sugimachi K (2000) Clinical significance of matrix metalloproteinase-7 (MMP-7) in esophageal carcinoma. Clin Cancer Res 6: 1169–1174
Yoshizaki T, Sato T, Maruyama Y, Murono S, Furukawa M, Park C and Seiki M (1997) Increased expression of membrane type 1-matrix metelloproteinase in head and neck carcinoma. Cancer 79: 139–144
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Yamashita, K., Mori, M., Kataoka, A. et al. The clinical significance of MMP-1 expression in oesophageal carcinoma. Br J Cancer 84, 276–282 (2001). https://doi.org/10.1054/bjoc.2000.1568
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DOI: https://doi.org/10.1054/bjoc.2000.1568
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