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Erschienen in: Journal of Cancer Research and Clinical Oncology 1/2005

01.01.2005 | Original Paper

A single nucleotide polymorphism in the MMP-9 promoter affects tumor progression and invasive phenotype of gastric cancer

verfasst von: Shunji Matsumura, Naohide Oue, Hirofumi Nakayama, Yasuhiko Kitadai, Kazuhiro Yoshida, Yoshiyuki Yamaguchi, Kazue Imai, Kei Nakachi, Keisuke Matsusaki, Kazuaki Chayama, Wataru Yasui

Erschienen in: Journal of Cancer Research and Clinical Oncology | Ausgabe 1/2005

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Abstract

Purpose

Matrix metalloproteinase-9 (MMP-9, gelatinase B) plays a key role in cancer invasion and metastasis by degradating the extracellular matrix (ECM) and basement membrane barriers. A cytosine (C)-thymidine (T) single nucleotide polymorphism (SNP) at position –1562 in the MMP-9 promoter is reported to affect expression of this gene. The purpose of this study was to investigate the relation between the –1562 C/T polymorphism and the development and progression of gastric cancer.

Methods

The study population included 177 gastric cancer patients and 224 healthy control subjects. The SNP in the MMP-9 promoter was analyzed by polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP) and sequencing. Genotype frequencies were compared between patients and controls, and the association of genotypes with clinicopathological features was studied.

Results

Genotype frequencies in gastric cancer patients were similar to those in control subjects (P = 0.223). However, significant association was found between degree of tumor invasion, clinical stage, and lymphatic invasion and the MMP-9 polymorphism in gastric cancer patients (P<0.05, for each).

Conclusions

Our results indicate that the T allele in the MMP-9 promoter is associated with the invasive phenotype of gastric cancer.
Literatur
Zurück zum Zitat Baker EA, Leaper DJ (2003) The plasminogen activator and matrix metalloproteinase systems in colorectal cancer: relationship to tumour pathology. Eur J Cancer 39:981–988CrossRefPubMed Baker EA, Leaper DJ (2003) The plasminogen activator and matrix metalloproteinase systems in colorectal cancer: relationship to tumour pathology. Eur J Cancer 39:981–988CrossRefPubMed
Zurück zum Zitat Behrens P, Rothe M, Wellmann A, Krischler J, Wernert N (2001) The Ets-1 transcription factor is up-regulated together with MMP-1 and MMP-9 in the stroma of pre-invasive breast cancer. J Pathol 194:43–50CrossRefPubMed Behrens P, Rothe M, Wellmann A, Krischler J, Wernert N (2001) The Ets-1 transcription factor is up-regulated together with MMP-1 and MMP-9 in the stroma of pre-invasive breast cancer. J Pathol 194:43–50CrossRefPubMed
Zurück zum Zitat Chicoine E, Esteve PO, Robledo O, Van Themsche C, Potworowski EF, St-Pierre Y (2002) Evidence for the role of promoter methylation in the regulation of MMP-9 gene expression. Biochem Biophys Res Commun 297:765–772CrossRefPubMed Chicoine E, Esteve PO, Robledo O, Van Themsche C, Potworowski EF, St-Pierre Y (2002) Evidence for the role of promoter methylation in the regulation of MMP-9 gene expression. Biochem Biophys Res Commun 297:765–772CrossRefPubMed
Zurück zum Zitat Ferrand PE, Parry S, Sammel M, Macones GA, Kuivaniemi H, Romero R, Strauss JF 3rd (2002) A polymorphism in the matrix metalloproteinase-9 promoter is associated with increased risk of preterm premature rupture of membranes in African Americans. Mol Hum Reprod 8:494–501CrossRefPubMed Ferrand PE, Parry S, Sammel M, Macones GA, Kuivaniemi H, Romero R, Strauss JF 3rd (2002) A polymorphism in the matrix metalloproteinase-9 promoter is associated with increased risk of preterm premature rupture of membranes in African Americans. Mol Hum Reprod 8:494–501CrossRefPubMed
Zurück zum Zitat Forget MA, Desrosiers RR, Beliveau R (1999) Physiological roles of matrix metalloproteinases; implications for tumor growth and metastasis. Can J Physiol Pharmacol 77:465–480CrossRefPubMed Forget MA, Desrosiers RR, Beliveau R (1999) Physiological roles of matrix metalloproteinases; implications for tumor growth and metastasis. Can J Physiol Pharmacol 77:465–480CrossRefPubMed
Zurück zum Zitat Gum R, Lengyel E, Juarez J, Chen JH, Sato H, Seiki M, Boyd D (1996) Stimulation of 92-kDa gelatinase B promoter activity by ras is mitogen-activated protein kinase kinase 1-independent and requires multiple transcription factor binding sites including closely spaced PEA3/ets and AP-1 sequences. J Biol Chem 271:10672–10680CrossRefPubMed Gum R, Lengyel E, Juarez J, Chen JH, Sato H, Seiki M, Boyd D (1996) Stimulation of 92-kDa gelatinase B promoter activity by ras is mitogen-activated protein kinase kinase 1-independent and requires multiple transcription factor binding sites including closely spaced PEA3/ets and AP-1 sequences. J Biol Chem 271:10672–10680CrossRefPubMed
Zurück zum Zitat Hujanen ES, Vaisanen A, Zheng A, Tryggvason K, Turpeenniemi-Hujanen T (1994) Modulation of M(r) 72,000 and M(r) 92,000 type-IV collagenase (gelatinase A and B) gene expression by interferons alpha and gamma in human melanoma. Int J Cancer 58:582–586PubMed Hujanen ES, Vaisanen A, Zheng A, Tryggvason K, Turpeenniemi-Hujanen T (1994) Modulation of M(r) 72,000 and M(r) 92,000 type-IV collagenase (gelatinase A and B) gene expression by interferons alpha and gamma in human melanoma. Int J Cancer 58:582–586PubMed
Zurück zum Zitat Japanese Gastric Cancer Association (1998) Japanese classification of gastric carcinoma. 2nd English Edition. Gastric Cancer 1:10–24CrossRefPubMed Japanese Gastric Cancer Association (1998) Japanese classification of gastric carcinoma. 2nd English Edition. Gastric Cancer 1:10–24CrossRefPubMed
Zurück zum Zitat Jones JL, Glynn P, Walker RA (1999) Expression of MMP-2 and MMP-9, their inhibitors, and the activator MT1-MMP in primary breast carcinomas. J Pathol 189:161–168CrossRefPubMed Jones JL, Glynn P, Walker RA (1999) Expression of MMP-2 and MMP-9, their inhibitors, and the activator MT1-MMP in primary breast carcinomas. J Pathol 189:161–168CrossRefPubMed
Zurück zum Zitat Kallakury BV, Karikehalli S, Haholu A, Sheehan CE, Azumi N, Ross JS (2001) Increased expression of matrix metalloproteinases 2 and 9 and tissue inhibitors of metalloproteinases 1 and 2 correlate with poor prognostic variables in renal cell carcinoma. Clin Cancer Res 7:3113–3119PubMed Kallakury BV, Karikehalli S, Haholu A, Sheehan CE, Azumi N, Ross JS (2001) Increased expression of matrix metalloproteinases 2 and 9 and tissue inhibitors of metalloproteinases 1 and 2 correlate with poor prognostic variables in renal cell carcinoma. Clin Cancer Res 7:3113–3119PubMed
Zurück zum Zitat Kohn EC, Liotta LA (1995) Molecular insights into cancer invasion: strategies for prevention and intervention. Cancer Res 55:1856–1862PubMed Kohn EC, Liotta LA (1995) Molecular insights into cancer invasion: strategies for prevention and intervention. Cancer Res 55:1856–1862PubMed
Zurück zum Zitat Kuraoka K, Matsumura S, Hamai Y, Nakachi K, Imai K, Matsusaki K, Oue N, Ito R, Nakayama H, Yasui W (2003) A single nucleotide polymorphism in the transmenbrane domain coding region of HER-2 is associated with development and malignant phenotype of gastric cancer. Int J Cancer 107:593–596CrossRefPubMed Kuraoka K, Matsumura S, Hamai Y, Nakachi K, Imai K, Matsusaki K, Oue N, Ito R, Nakayama H, Yasui W (2003) A single nucleotide polymorphism in the transmenbrane domain coding region of HER-2 is associated with development and malignant phenotype of gastric cancer. Int J Cancer 107:593–596CrossRefPubMed
Zurück zum Zitat Lauren P (1965) The two histological main types of gastric carcinoma. Diffuse and so-called intestinal type carcinoma: an attempt at histological classification. Acta Pathol Microbiol Scand 64:31–49PubMed Lauren P (1965) The two histological main types of gastric carcinoma. Diffuse and so-called intestinal type carcinoma: an attempt at histological classification. Acta Pathol Microbiol Scand 64:31–49PubMed
Zurück zum Zitat Liotta LA, Steeg PS, Stetler-Stevenson WG (1991) Cancer metastasis and angiogenesis: an imbalance of positive and negative regulation. Cell 64:327–336CrossRefPubMed Liotta LA, Steeg PS, Stetler-Stevenson WG (1991) Cancer metastasis and angiogenesis: an imbalance of positive and negative regulation. Cell 64:327–336CrossRefPubMed
Zurück zum Zitat Matsumura S, Oue N, Kitadai Y, Chayama K, Yoshida K, Yamaguchi Y, Toge T, Imai K, Nakachi K, Yasui W (2004) A single nucleotide polymorphism in the MMP-1 promoter is correlated with histological differentiation of gastric cancer. J Cancer Res Clin Oncol 130:259–265CrossRef Matsumura S, Oue N, Kitadai Y, Chayama K, Yoshida K, Yamaguchi Y, Toge T, Imai K, Nakachi K, Yasui W (2004) A single nucleotide polymorphism in the MMP-1 promoter is correlated with histological differentiation of gastric cancer. J Cancer Res Clin Oncol 130:259–265CrossRef
Zurück zum Zitat McDonnell S, Matrisian LM (1990) Stromelysin in tumor progression and metastasis. Cancer Metastasis Rev 9:305–319PubMed McDonnell S, Matrisian LM (1990) Stromelysin in tumor progression and metastasis. Cancer Metastasis Rev 9:305–319PubMed
Zurück zum Zitat Murray GI, Duncan ME, Arbuckle E, Melvin WT, Fothergill JE (1998) Matrix metalloproteinases and their inhibitors in gastric cancer. Gut 43:791–797PubMed Murray GI, Duncan ME, Arbuckle E, Melvin WT, Fothergill JE (1998) Matrix metalloproteinases and their inhibitors in gastric cancer. Gut 43:791–797PubMed
Zurück zum Zitat Nakayama T, Ito M, Ohtsuru A, Naito S, Nakashima M, Fagin JA, Yamashita S, Sekine I (1996) Expression of the Ets-1 proto-oncogene in human gastric carcinoma: correlation with tumor invasion. Am J Pathol 149:1931–1939PubMed Nakayama T, Ito M, Ohtsuru A, Naito S, Nakashima M, Fagin JA, Yamashita S, Sekine I (1996) Expression of the Ets-1 proto-oncogene in human gastric carcinoma: correlation with tumor invasion. Am J Pathol 149:1931–1939PubMed
Zurück zum Zitat Oue N, Motoshita J, Yokozaki H, Hayashi K, Tahara E, Taniyama K, Matsusaki K, Yasui W (2002) Distinct promoter hypermethylation of p16INK4a, CDH1, and RAR-ß in intestinal, diffuse-adherent, and diffuse-scattered type gastric carcinomas. J Pathol 198:55–59CrossRefPubMed Oue N, Motoshita J, Yokozaki H, Hayashi K, Tahara E, Taniyama K, Matsusaki K, Yasui W (2002) Distinct promoter hypermethylation of p16INK4a, CDH1, and RAR-ß in intestinal, diffuse-adherent, and diffuse-scattered type gastric carcinomas. J Pathol 198:55–59CrossRefPubMed
Zurück zum Zitat Oue N, Oshimo Y, Nakayama H, Ito R, Yoshida K, Matsusaki K, Yasui W (2003) DNA methylation of multiple genes in gastric carcinoma: association with histological type and CpG island methylator phenotype. Cancer Sci 94:901–905PubMed Oue N, Oshimo Y, Nakayama H, Ito R, Yoshida K, Matsusaki K, Yasui W (2003) DNA methylation of multiple genes in gastric carcinoma: association with histological type and CpG island methylator phenotype. Cancer Sci 94:901–905PubMed
Zurück zum Zitat Ozalp S, Tanir HM, Yalcin OT, Kabukcuoglu S, Oner U, Uray M (2003) Prognostic value of matrix metalloproteinase-9 (gelatinase-B) expression in epithelial ovarian tumors. Eur J Gynaecol Oncol 24:417–420PubMed Ozalp S, Tanir HM, Yalcin OT, Kabukcuoglu S, Oner U, Uray M (2003) Prognostic value of matrix metalloproteinase-9 (gelatinase-B) expression in epithelial ovarian tumors. Eur J Gynaecol Oncol 24:417–420PubMed
Zurück zum Zitat Park CC, Bissell MJ, Barcellos-Hoff MH (2000) The influence of the microenvironment on the malignant phenotype. Mol Med Today 6:324–329CrossRefPubMed Park CC, Bissell MJ, Barcellos-Hoff MH (2000) The influence of the microenvironment on the malignant phenotype. Mol Med Today 6:324–329CrossRefPubMed
Zurück zum Zitat Rao JS, Steck PA, Mohanam S, Stetler-Stevenson WG, Liotta LA, Sawaya R (1993) Elevated levels of M(r) 92,000 type IV collagenase in human brain tumors. Cancer Res 53:2208–2211PubMed Rao JS, Steck PA, Mohanam S, Stetler-Stevenson WG, Liotta LA, Sawaya R (1993) Elevated levels of M(r) 92,000 type IV collagenase in human brain tumors. Cancer Res 53:2208–2211PubMed
Zurück zum Zitat Sakata K, Satoh M, Someya M, Asanuma H, Nagakura H, Oouchi A, Nakata K, Kogawa K, Koito K, Hareyama M, Himi T (2004) Expression of matrix metalloproteinase 9 is a prognostic factor in patients with non-Hodgkin lymphoma. Cancer 100:356–365CrossRefPubMed Sakata K, Satoh M, Someya M, Asanuma H, Nagakura H, Oouchi A, Nakata K, Kogawa K, Koito K, Hareyama M, Himi T (2004) Expression of matrix metalloproteinase 9 is a prognostic factor in patients with non-Hodgkin lymphoma. Cancer 100:356–365CrossRefPubMed
Zurück zum Zitat Sehgal I, Baley PA, Thompson TC (1996) Transforming growth factor beta1 stimulates contrasting responses in metastatic versus primary mouse prostate cancer-derived cell lines in vitro. Cancer Res 56:3359–3365PubMed Sehgal I, Baley PA, Thompson TC (1996) Transforming growth factor beta1 stimulates contrasting responses in metastatic versus primary mouse prostate cancer-derived cell lines in vitro. Cancer Res 56:3359–3365PubMed
Zurück zum Zitat Sobin LH, Wittekind CH (eds) (2002) TNM classification of malignant tumors, 6th edn. Wiley-Liss, New York, pp 65–68 Sobin LH, Wittekind CH (eds) (2002) TNM classification of malignant tumors, 6th edn. Wiley-Liss, New York, pp 65–68
Zurück zum Zitat Tanioka Y, Yoshida T, Yagawa T, Saiki Y, Takeo S, Harada T, Okazawa T, Yanai H, Okita K (2003) Matrix metalloproteinase-7 and matrix metalloproteinase-9 are associated with unfavourable prognosis in superficial oesophageal cancer. Br J Cancer 89:2116–2121CrossRefPubMed Tanioka Y, Yoshida T, Yagawa T, Saiki Y, Takeo S, Harada T, Okazawa T, Yanai H, Okita K (2003) Matrix metalloproteinase-7 and matrix metalloproteinase-9 are associated with unfavourable prognosis in superficial oesophageal cancer. Br J Cancer 89:2116–2121CrossRefPubMed
Zurück zum Zitat Wroblewski LE, Pritchard DM, Carter S, Varro A (2002) Gastrin-stimulated gastric epithelial cell invasion: the role and mechanism of increased matrix metalloproteinase 9 expression. Biochem J 365:873–879PubMed Wroblewski LE, Pritchard DM, Carter S, Varro A (2002) Gastrin-stimulated gastric epithelial cell invasion: the role and mechanism of increased matrix metalloproteinase 9 expression. Biochem J 365:873–879PubMed
Zurück zum Zitat Yasui W, Yokozaki H, Fujimoto J, Naka K, Kuniyasu H, Tahara E (2000) Genetic and epigenetic alterations in multistep carcinogenesis of the stomach. J Gastroenterol 35:111–115PubMed Yasui W, Yokozaki H, Fujimoto J, Naka K, Kuniyasu H, Tahara E (2000) Genetic and epigenetic alterations in multistep carcinogenesis of the stomach. J Gastroenterol 35:111–115PubMed
Zurück zum Zitat Zhang B, Ye S, Hermann SM, Eriksson P, de Maat M, Evans A, Arveiler D, Luc G, Cambien F, Hamsten A, Watkins H, Henney AM (1999) Functional polymorphism in the regulatory region of gelatinase B gene in relation to severity of coronary atherosclerosis. Circulation 99:1788–794PubMed Zhang B, Ye S, Hermann SM, Eriksson P, de Maat M, Evans A, Arveiler D, Luc G, Cambien F, Hamsten A, Watkins H, Henney AM (1999) Functional polymorphism in the regulatory region of gelatinase B gene in relation to severity of coronary atherosclerosis. Circulation 99:1788–794PubMed
Zurück zum Zitat Zhang S, Li L, Lin JY, Lin H (2003) Imbalance between expression of matrix metalloproteinase-9 and tissue inhibitor of metalloproteinase-1 in invasiveness and metastasis of human gastric carcinoma. World J Gastroenterol 9:899–904PubMed Zhang S, Li L, Lin JY, Lin H (2003) Imbalance between expression of matrix metalloproteinase-9 and tissue inhibitor of metalloproteinase-1 in invasiveness and metastasis of human gastric carcinoma. World J Gastroenterol 9:899–904PubMed
Metadaten
Titel
A single nucleotide polymorphism in the MMP-9 promoter affects tumor progression and invasive phenotype of gastric cancer
verfasst von
Shunji Matsumura
Naohide Oue
Hirofumi Nakayama
Yasuhiko Kitadai
Kazuhiro Yoshida
Yoshiyuki Yamaguchi
Kazue Imai
Kei Nakachi
Keisuke Matsusaki
Kazuaki Chayama
Wataru Yasui
Publikationsdatum
01.01.2005
Verlag
Springer-Verlag
Erschienen in
Journal of Cancer Research and Clinical Oncology / Ausgabe 1/2005
Print ISSN: 0171-5216
Elektronische ISSN: 1432-1335
DOI
https://doi.org/10.1007/s00432-004-0621-4

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