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Published in: International Journal of Colorectal Disease 8/2009

01-08-2009 | Original Article

Elevated expressions of MMP7, TROP2, and survivin are associated with survival, disease recurrence, and liver metastasis of colon cancer

Authors: Y. J. Fang, Z. H. Lu, G. Q. Wang, Z. Z. Pan, Z. W. Zhou, J. P. Yun, M. F. Zhang, D. S. Wan

Published in: International Journal of Colorectal Disease | Issue 8/2009

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Abstract

Purpose

Colorectal cancer is one of the most common cancers worldwide. We tested the hypothesis that differences in the expression of certain molecular markers of colon cancer may account for different clinical outcomes.

Methods

Tissue microarray technology was used to assay the expression of 17 biological markers [β-catenin, CD44v7, c-myc, cyclin D1, estrogen receptor β, mitogen-activated protein kinase/extracellular signal-regulated kinase, maspin, matrix metalloproteinase-7 (MMP7), p53, Pin1, peroxisome proliferators-activated receptor-gamma, survivin, T cell transcription factor 4 (TCF4), transforming growth factor beta receptor II (TGFβR II), TGFβ, TROP2, and Wnt] by immunohistochemistry in 620 colon cancer patients. The Cox proportional hazards regression model was applied to analyze the lifetime data, including time to death, time to recurrence, and time to liver metastasis.

Results

All the markers were present at significantly higher expression levels in tumor specimens than in normal colonic specimens. Kaplan–Meier analysis showed that high expression of TROP2, MMP7, and survivin were related to decreased survival; TCF4 and TROP2 were related to disease recurrence; and CD44v7, cyclin D1, MMP7, p53, survivin, and TCF4 were related to liver metastasis. However, the results of the multivariate analysis only showed that expression of MMP7, survivin, and TROP2 were significant predictors of lower patient survival, while TROP2 and MMP7 were significantly related to disease recurrence and liver metastasis, respectively.

Conclusions

We conclude that elevated survivin, MMP7, and TROP2 expression levels are related to decreased survival. In addition, elevated MMP7 and TROP2 expression levels are predictors of disease recurrence and liver metastasis, respectively.
Literature
1.
go back to reference Weitz J, Koch M, Debus J, Hohler T, Galle PR, Buchler MW (2005) Colorectal cancer. Lancet 365:153–165PubMedCrossRef Weitz J, Koch M, Debus J, Hohler T, Galle PR, Buchler MW (2005) Colorectal cancer. Lancet 365:153–165PubMedCrossRef
2.
go back to reference Graziano F, Cascinu S (2003) Prognostic molecular markers for planning adjuvant chemotherapy trials in Dukes' B colorectal cancer patients: how much evidence is enough? Ann Oncol 14:1026–1038PubMedCrossRef Graziano F, Cascinu S (2003) Prognostic molecular markers for planning adjuvant chemotherapy trials in Dukes' B colorectal cancer patients: how much evidence is enough? Ann Oncol 14:1026–1038PubMedCrossRef
3.
go back to reference McLeod HL, Murray GI (1999) Tumour markers of prognosis in colorectal cancer. Br J Cancer 79:191–203PubMedCrossRef McLeod HL, Murray GI (1999) Tumour markers of prognosis in colorectal cancer. Br J Cancer 79:191–203PubMedCrossRef
4.
go back to reference Leichman CG (2001) Predictive and prognostic markers in gastrointestinal cancers. Curr Opin Oncol 13:291–299PubMedCrossRef Leichman CG (2001) Predictive and prognostic markers in gastrointestinal cancers. Curr Opin Oncol 13:291–299PubMedCrossRef
5.
go back to reference Eschrich S, Yang I, Bloom G, Kwong KY, Boulware D, Cantor A et al (2005) Molecular staging for survival prediction of colorectal cancer patients. J Clin Oncol 23:3526–3535PubMedCrossRef Eschrich S, Yang I, Bloom G, Kwong KY, Boulware D, Cantor A et al (2005) Molecular staging for survival prediction of colorectal cancer patients. J Clin Oncol 23:3526–3535PubMedCrossRef
6.
go back to reference Kuramochi J, Arai T, Ikeda S, Kumagai J, Uetake H, Sugihara K (2006) High Pin1 expression is associated with tumor progression in colorectal cancer. J Surg Oncol 94:155–160PubMedCrossRef Kuramochi J, Arai T, Ikeda S, Kumagai J, Uetake H, Sugihara K (2006) High Pin1 expression is associated with tumor progression in colorectal cancer. J Surg Oncol 94:155–160PubMedCrossRef
7.
go back to reference Kirimlioglu H, Kirimlioglu V, Yilmaz S, Sagir V, Coban S, Turkmen E et al (2006) Role of matrix metalloproteinase-7 in colorectal adenomas. Dig Dis Sci 51:2068–2072PubMedCrossRef Kirimlioglu H, Kirimlioglu V, Yilmaz S, Sagir V, Coban S, Turkmen E et al (2006) Role of matrix metalloproteinase-7 in colorectal adenomas. Dig Dis Sci 51:2068–2072PubMedCrossRef
8.
go back to reference Ponnelle T, Chapusot C, Martin L, Bouvier AM, Plenchette S, Faivre J et al (2005) Cellular localisation of survivin: impact on the prognosis in colorectal cancer. J Cancer Res Clin Oncol 131:504–510PubMedCrossRef Ponnelle T, Chapusot C, Martin L, Bouvier AM, Plenchette S, Faivre J et al (2005) Cellular localisation of survivin: impact on the prognosis in colorectal cancer. J Cancer Res Clin Oncol 131:504–510PubMedCrossRef
9.
go back to reference Ohmachi T, Tanaka F, Mimori K, Inoue H, Yanaga K, Mori M (2006) Clinical significance of TROP2 expression in colorectal cancer. Clin Cancer Res 12:3057–3063PubMedCrossRef Ohmachi T, Tanaka F, Mimori K, Inoue H, Yanaga K, Mori M (2006) Clinical significance of TROP2 expression in colorectal cancer. Clin Cancer Res 12:3057–3063PubMedCrossRef
10.
go back to reference Horvath L, Henshall S (2001) The application of tissue microarrays to cancer research. Pathology 33:125–129PubMedCrossRef Horvath L, Henshall S (2001) The application of tissue microarrays to cancer research. Pathology 33:125–129PubMedCrossRef
11.
12.
go back to reference Iczkowski KA, Omara-Opyene AL, Kulkarni TR, Pansara M, Shah GV (2005) Paracrine calcitonin in prostate cancer is linked to CD44 variant expression and invasion. Anticancer Res 25:2075–2083PubMed Iczkowski KA, Omara-Opyene AL, Kulkarni TR, Pansara M, Shah GV (2005) Paracrine calcitonin in prostate cancer is linked to CD44 variant expression and invasion. Anticancer Res 25:2075–2083PubMed
13.
go back to reference Chang AJ, Song DH, Wolfe MM (2006) Attenuation of peroxisome proliferator-activated receptor gamma (PPARgamma) mediates gastrin-stimulated colorectal cancer cell proliferation. J Biol Chem 281:14700–14710PubMedCrossRef Chang AJ, Song DH, Wolfe MM (2006) Attenuation of peroxisome proliferator-activated receptor gamma (PPARgamma) mediates gastrin-stimulated colorectal cancer cell proliferation. J Biol Chem 281:14700–14710PubMedCrossRef
14.
go back to reference Ishikawa T, Ichikawa Y, Mitsuhashi M, Momiyama N, Chishima T, Tanaka K et al (1996) Matrilysin is associated with progression of colorectal tumor. Cancer Lett 107:5–10PubMedCrossRef Ishikawa T, Ichikawa Y, Mitsuhashi M, Momiyama N, Chishima T, Tanaka K et al (1996) Matrilysin is associated with progression of colorectal tumor. Cancer Lett 107:5–10PubMedCrossRef
15.
go back to reference Hipfner DR, Cohen SM (2004) Connecting proliferation and apoptosis in development and disease. Nat Rev Mol Cell Biol 5:805–815PubMedCrossRef Hipfner DR, Cohen SM (2004) Connecting proliferation and apoptosis in development and disease. Nat Rev Mol Cell Biol 5:805–815PubMedCrossRef
16.
go back to reference Fu M, Wang C, Li Z, Sakamaki T, Pestell RG (2004) Minireview: cyclin D1: normal and abnormal functions. Endocrinology 145:5439–5447PubMedCrossRef Fu M, Wang C, Li Z, Sakamaki T, Pestell RG (2004) Minireview: cyclin D1: normal and abnormal functions. Endocrinology 145:5439–5447PubMedCrossRef
17.
go back to reference Fornaro M, Dell'Arciprete R, Stella M, Bucci C, Nutini M, Capri MG et al (1995) Cloning of the gene encoding Trop-2, a cell-surface glycoprotein expressed by human carcinomas. Int J Cancer 62:610–618PubMedCrossRef Fornaro M, Dell'Arciprete R, Stella M, Bucci C, Nutini M, Capri MG et al (1995) Cloning of the gene encoding Trop-2, a cell-surface glycoprotein expressed by human carcinomas. Int J Cancer 62:610–618PubMedCrossRef
18.
go back to reference Umekita Y, Souda M, Yoshida H (2006) Expression of maspin in colorectal cancer. In Vivo 20:797–800PubMed Umekita Y, Souda M, Yoshida H (2006) Expression of maspin in colorectal cancer. In Vivo 20:797–800PubMed
19.
go back to reference Boltze C (2005) Loss of maspin is a helpful prognosticator in colorectal cancer: a tissue microarray analysis. Pathol Res Pract 200:783–790PubMedCrossRef Boltze C (2005) Loss of maspin is a helpful prognosticator in colorectal cancer: a tissue microarray analysis. Pathol Res Pract 200:783–790PubMedCrossRef
20.
go back to reference Massague J, Blain SW, Lo RS (2000) TGFb signaling in growth control, cancer, and heritable disorders. Cell 103:295–309PubMedCrossRef Massague J, Blain SW, Lo RS (2000) TGFb signaling in growth control, cancer, and heritable disorders. Cell 103:295–309PubMedCrossRef
22.
go back to reference Campbell-Thompson M, Lynch IJ, Bhardwaj B (2001) Expression of estrogen receptor (ER) subtypes and ERbeta isoforms in colon cancer. Cancer Res 61:632–640PubMed Campbell-Thompson M, Lynch IJ, Bhardwaj B (2001) Expression of estrogen receptor (ER) subtypes and ERbeta isoforms in colon cancer. Cancer Res 61:632–640PubMed
23.
go back to reference Konstantinopoulos PA, Kominea A, Vandoros G, Sykiotis GP, Andricopoulos P, Varakis I et al (2003) Oestrogen receptor β (ERbeta) is abundantly expressed in normal colonic mucosa, but declines in colon denocarcinoma paralleling the tumour’s dedifferentiation. Eur J Cancer 39:1251–1258PubMedCrossRef Konstantinopoulos PA, Kominea A, Vandoros G, Sykiotis GP, Andricopoulos P, Varakis I et al (2003) Oestrogen receptor β (ERbeta) is abundantly expressed in normal colonic mucosa, but declines in colon denocarcinoma paralleling the tumour’s dedifferentiation. Eur J Cancer 39:1251–1258PubMedCrossRef
26.
go back to reference Thompson N, Lyons J (2005) Recent progress in targeting the Raf/MEK/ERK pathway with inhibitors in cancer drug discovery. Curr Opin Pharmacol 5:350–356PubMedCrossRef Thompson N, Lyons J (2005) Recent progress in targeting the Raf/MEK/ERK pathway with inhibitors in cancer drug discovery. Curr Opin Pharmacol 5:350–356PubMedCrossRef
27.
go back to reference Greene FL, Page DL, Fleming ID et al (2002) AJCC: cancer staging handbook: from the AJCC cancer staging manual, 6th edn. Springer, New York Greene FL, Page DL, Fleming ID et al (2002) AJCC: cancer staging handbook: from the AJCC cancer staging manual, 6th edn. Springer, New York
28.
go back to reference Sobin LH, Wittekind C (eds) (2002) UICC: TNM classification of malignant tumours. Wiley, London Sobin LH, Wittekind C (eds) (2002) UICC: TNM classification of malignant tumours. Wiley, London
29.
go back to reference Schraml P, Kononen J, Bubendorf L, Moch H, Bissig H, Nocito A et al (1999) Tissue microarrays for gene amplification surveys in many different tumor types. Clin Cancer Res 5:1966–1975PubMed Schraml P, Kononen J, Bubendorf L, Moch H, Bissig H, Nocito A et al (1999) Tissue microarrays for gene amplification surveys in many different tumor types. Clin Cancer Res 5:1966–1975PubMed
30.
go back to reference Mucci NR, Akdas G, Manely S, Rubin MA (2000) Neuroendocrine expression in metastatic prostate cancer: evaluation of high throughput tissue microarrays to detect heterogeneous protein expression. Hum Pathol 31:406–414PubMedCrossRef Mucci NR, Akdas G, Manely S, Rubin MA (2000) Neuroendocrine expression in metastatic prostate cancer: evaluation of high throughput tissue microarrays to detect heterogeneous protein expression. Hum Pathol 31:406–414PubMedCrossRef
31.
go back to reference Richter J, Wagner U, Kononen J, Fijan A, Bruderer J, Schmid U et al (2000) High-throughput tissue microarray analysis of cyclin E gene amplification and overexpression in urinary bladder cancer. Am J Pathol 157:787–794PubMed Richter J, Wagner U, Kononen J, Fijan A, Bruderer J, Schmid U et al (2000) High-throughput tissue microarray analysis of cyclin E gene amplification and overexpression in urinary bladder cancer. Am J Pathol 157:787–794PubMed
32.
go back to reference Benson AB 3rd, Schrag D, Somerfield MR, Cohen AM, Figueredo AT, Flynn PJ et al (2004) American Society of Clinical Oncology recommendations on adjuvant chemotherapy for stage II colon cancer. J Clin Oncol 22:3408–3419PubMedCrossRef Benson AB 3rd, Schrag D, Somerfield MR, Cohen AM, Figueredo AT, Flynn PJ et al (2004) American Society of Clinical Oncology recommendations on adjuvant chemotherapy for stage II colon cancer. J Clin Oncol 22:3408–3419PubMedCrossRef
33.
go back to reference Johnson PM, Porter GA, Ricciardi R, Baxter NN (2006) Increasing negative lymph node count is independently associated with improved long-term survival in stage IIIB and IIIC colon cancer. J Clin Oncol 24:3570–3575PubMedCrossRef Johnson PM, Porter GA, Ricciardi R, Baxter NN (2006) Increasing negative lymph node count is independently associated with improved long-term survival in stage IIIB and IIIC colon cancer. J Clin Oncol 24:3570–3575PubMedCrossRef
34.
go back to reference Nakashima K, Shimada H, Ochiai T, Kuboshima M, Kuroiwa N, Okazumi S et al (2004) Serological identification of TROP2 by recombinant cDNA expression cloning using sera of patients with esophageal squamous cell carcinoma. Int J Cancer 112:1029–1035PubMedCrossRef Nakashima K, Shimada H, Ochiai T, Kuboshima M, Kuroiwa N, Okazumi S et al (2004) Serological identification of TROP2 by recombinant cDNA expression cloning using sera of patients with esophageal squamous cell carcinoma. Int J Cancer 112:1029–1035PubMedCrossRef
35.
go back to reference Kanai Y, Ushijima S, Saito Y, Nakanishi Y, Sakamoto M, Hirohashi S (2001) MRNA expression of genes altered by 5-azacytidine treatment in cancer cell lines is associated with clinicopathological parameters of human cancers. J Cancer Res Clin Oncol 127:697–706PubMed Kanai Y, Ushijima S, Saito Y, Nakanishi Y, Sakamoto M, Hirohashi S (2001) MRNA expression of genes altered by 5-azacytidine treatment in cancer cell lines is associated with clinicopathological parameters of human cancers. J Cancer Res Clin Oncol 127:697–706PubMed
36.
go back to reference Alberti S, Miotti S, Stella M, Klein CE, Fornaro M, Menard S et al (1992) Biochemical characterization of Trop-2, a cell surface molecule expressed by human carcinomas: formal proof that the monoclonal antibodies T16 and MOv-16 recognize Trop-2. Hybridoma 11:539–545PubMedCrossRef Alberti S, Miotti S, Stella M, Klein CE, Fornaro M, Menard S et al (1992) Biochemical characterization of Trop-2, a cell surface molecule expressed by human carcinomas: formal proof that the monoclonal antibodies T16 and MOv-16 recognize Trop-2. Hybridoma 11:539–545PubMedCrossRef
37.
go back to reference Miotti S, Canevari S, Menard S, Mezzanzanica D, Porro G, Pupa SM et al (1987) Characterization of human ovarian carcinoma-associated antigens defined by novel monoclonal antibodies with tumor-restricted specificity. Int J Cancer 39:297–303PubMedCrossRef Miotti S, Canevari S, Menard S, Mezzanzanica D, Porro G, Pupa SM et al (1987) Characterization of human ovarian carcinoma-associated antigens defined by novel monoclonal antibodies with tumor-restricted specificity. Int J Cancer 39:297–303PubMedCrossRef
38.
go back to reference Fradet Y, Cordon-Cardo C, Thomson T, Daly ME, Whitmore WF Jr, Lloyd KO et al (1984) Cell surface antigens of human bladder cancer defined by mouse monoclonal antibodies. Proc Natl Acad Sci U S A 81:224–228PubMedCrossRef Fradet Y, Cordon-Cardo C, Thomson T, Daly ME, Whitmore WF Jr, Lloyd KO et al (1984) Cell surface antigens of human bladder cancer defined by mouse monoclonal antibodies. Proc Natl Acad Sci U S A 81:224–228PubMedCrossRef
39.
go back to reference Lipinski M, Parks DR, Rouse RV, Herzenberg LA (1981) Human trophoblast cell-surface antigens defined by monoclonal antibodies. Proc Natl Acad Sci U S A 78:5147–5150PubMedCrossRef Lipinski M, Parks DR, Rouse RV, Herzenberg LA (1981) Human trophoblast cell-surface antigens defined by monoclonal antibodies. Proc Natl Acad Sci U S A 78:5147–5150PubMedCrossRef
40.
go back to reference White PS, Forus A, Matise TC, Schutte BC, Spieker N, Stanier P et al (1999) Report of the fifth international workshop on human chromosome 1 mapping 1999. Cytogenet Cell Genet 87:143–171PubMedCrossRef White PS, Forus A, Matise TC, Schutte BC, Spieker N, Stanier P et al (1999) Report of the fifth international workshop on human chromosome 1 mapping 1999. Cytogenet Cell Genet 87:143–171PubMedCrossRef
41.
go back to reference El Sewedy T, Fornaro M, Alberti S (1998) Cloning of the murine TROP2 gene: conservation of a PIP2-binding sequence in the cytoplasmic domain of TROP-2. Int J Cancer 75:324–330PubMedCrossRef El Sewedy T, Fornaro M, Alberti S (1998) Cloning of the murine TROP2 gene: conservation of a PIP2-binding sequence in the cytoplasmic domain of TROP-2. Int J Cancer 75:324–330PubMedCrossRef
42.
go back to reference Suzuki A, Hayashida M, Ito T, Kawasaki H, Nakano T, Miura M et al (2000) Survivin initiates cell cycle entry by the competitive interaction with Cdk4/p16(INK4a) and Cdk2/cyclin E complex activation. Oncogene 19:3225–3234PubMedCrossRef Suzuki A, Hayashida M, Ito T, Kawasaki H, Nakano T, Miura M et al (2000) Survivin initiates cell cycle entry by the competitive interaction with Cdk4/p16(INK4a) and Cdk2/cyclin E complex activation. Oncogene 19:3225–3234PubMedCrossRef
43.
go back to reference Sarela AI, Macadam RC, Farmery SM, Markham AF, Guillou PJ (2000) Expression of the antiapoptosis gene, survivin, predicts death from recurrent colorectal carcinoma. Gut 46:645–650PubMedCrossRef Sarela AI, Macadam RC, Farmery SM, Markham AF, Guillou PJ (2000) Expression of the antiapoptosis gene, survivin, predicts death from recurrent colorectal carcinoma. Gut 46:645–650PubMedCrossRef
44.
go back to reference Rodel F, Hoffmann J, Grabenbauer GG, Papadopoulos T, Weiss C, Gunther K et al (2002) High survivin expression is associated with reduced apoptosis in rectal cancer and may predict disease-free survival after preoperative radiochemotherapy and surgical resection. Strahlenther Onkol 178:426–435PubMedCrossRef Rodel F, Hoffmann J, Grabenbauer GG, Papadopoulos T, Weiss C, Gunther K et al (2002) High survivin expression is associated with reduced apoptosis in rectal cancer and may predict disease-free survival after preoperative radiochemotherapy and surgical resection. Strahlenther Onkol 178:426–435PubMedCrossRef
45.
go back to reference Rodel F, Hoffmann J, Distel L, Herrmann M, Noisternig T, Papadopoulos T et al (2005) Survivin as a radioresistance factor, and prognostic and therapeutic target for radiotherapy in rectal cancer. Cancer Res 65:4881–4887PubMedCrossRef Rodel F, Hoffmann J, Distel L, Herrmann M, Noisternig T, Papadopoulos T et al (2005) Survivin as a radioresistance factor, and prognostic and therapeutic target for radiotherapy in rectal cancer. Cancer Res 65:4881–4887PubMedCrossRef
46.
go back to reference Ryan BM, Konecny GE, Kahlert S, Wang HJ, Untch M, Meng G et al (2006) Survivin expression in breast cancer predicts clinical outcome and is associated with HER2, VEGF, urokinase plasminogen activator and PAI-1. Ann Oncol 17:597–604PubMedCrossRef Ryan BM, Konecny GE, Kahlert S, Wang HJ, Untch M, Meng G et al (2006) Survivin expression in breast cancer predicts clinical outcome and is associated with HER2, VEGF, urokinase plasminogen activator and PAI-1. Ann Oncol 17:597–604PubMedCrossRef
47.
go back to reference Kato J, Kuwabara Y, Mitani M, Shinoda N, Sato A, Toyama T et al (2001) Expression of survivin in esophageal cancer: correlation with the prognosis and response to chemotherapy. Int J Cancer 95:92–95PubMedCrossRef Kato J, Kuwabara Y, Mitani M, Shinoda N, Sato A, Toyama T et al (2001) Expression of survivin in esophageal cancer: correlation with the prognosis and response to chemotherapy. Int J Cancer 95:92–95PubMedCrossRef
48.
go back to reference Takai N, Miyazaki T, Nishida M, Nasu K, Miyakawa I (2002) Survivin expression correlates with clinical stage, histological grade, invasive behavior and survival rate in endometrial carcinoma. Cancer Lett 184:105–116PubMedCrossRef Takai N, Miyazaki T, Nishida M, Nasu K, Miyakawa I (2002) Survivin expression correlates with clinical stage, histological grade, invasive behavior and survival rate in endometrial carcinoma. Cancer Lett 184:105–116PubMedCrossRef
49.
51.
go back to reference Yang D, Welm A, Bishop JM (2004) Cell survival in the absence of survivin. Proc Natl Acad Sci U S A 101:15100–15105PubMedCrossRef Yang D, Welm A, Bishop JM (2004) Cell survival in the absence of survivin. Proc Natl Acad Sci U S A 101:15100–15105PubMedCrossRef
52.
go back to reference Okada H, Mak TW (2004) Pathways of apoptotic and nonapoptotic death in tumour cells. Nat. Rev. Cancer 4:592–603PubMedCrossRef Okada H, Mak TW (2004) Pathways of apoptotic and nonapoptotic death in tumour cells. Nat. Rev. Cancer 4:592–603PubMedCrossRef
53.
go back to reference Kawasaki H, Toyoda M, Shinohara H, Okuda J, Watanabe I, Yamamoto T et al (2001) Expression of survivin correlates with apoptosis, proliferation and angiogenesis during human colorectal carcinogenesis. Cancer 91:2026–2032PubMedCrossRef Kawasaki H, Toyoda M, Shinohara H, Okuda J, Watanabe I, Yamamoto T et al (2001) Expression of survivin correlates with apoptosis, proliferation and angiogenesis during human colorectal carcinogenesis. Cancer 91:2026–2032PubMedCrossRef
54.
go back to reference Blanc-Brude OP, Mesri M, Wall NR, Plescia J, Dohi T, Altieri DC (2003) Therapeutic targeting of the survivin pathway in cancer: initiation of mitochondrial apoptosis and suppression of tumor-associated angiogenesis. Cancer Res 9:2683–2692 Blanc-Brude OP, Mesri M, Wall NR, Plescia J, Dohi T, Altieri DC (2003) Therapeutic targeting of the survivin pathway in cancer: initiation of mitochondrial apoptosis and suppression of tumor-associated angiogenesis. Cancer Res 9:2683–2692
55.
go back to reference Ambrosini G, Adida C, Altieri DC (1997) A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nat Med 3:917–921PubMedCrossRef Ambrosini G, Adida C, Altieri DC (1997) A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nat Med 3:917–921PubMedCrossRef
56.
go back to reference Sternlicht MD, Werb Z (2001) How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 17:463–516PubMedCrossRef Sternlicht MD, Werb Z (2001) How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 17:463–516PubMedCrossRef
57.
go back to reference Vihinen P, Kahari VM (2002) Matrix metalloproteinases in cancer: prognostic markers and therapeutic targets. Int J Cancer 99:157–166PubMedCrossRef Vihinen P, Kahari VM (2002) Matrix metalloproteinases in cancer: prognostic markers and therapeutic targets. Int J Cancer 99:157–166PubMedCrossRef
58.
go back to reference Gu ZD, Li JY, Li M, Gu J, Shi XT, Ke Y et al (2005) Matrix metalloproteinases expression correlates with survival in patients with esophageal squamous cell carcinoma. Am J Gastroenterol 100:1835–1843PubMedCrossRef Gu ZD, Li JY, Li M, Gu J, Shi XT, Ke Y et al (2005) Matrix metalloproteinases expression correlates with survival in patients with esophageal squamous cell carcinoma. Am J Gastroenterol 100:1835–1843PubMedCrossRef
59.
go back to reference Yamamoto H, Itoh F, Adachi Y, Fukushima H, Itoh H, Sasaki S et al (1999) Messenger RNA expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in human hepatocellular carcinoma. Jpn J Clin Oncol 29:58–62PubMedCrossRef Yamamoto H, Itoh F, Adachi Y, Fukushima H, Itoh H, Sasaki S et al (1999) Messenger RNA expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in human hepatocellular carcinoma. Jpn J Clin Oncol 29:58–62PubMedCrossRef
60.
go back to reference Yamashita K, Azumano I, Mai M, Okada Y (1998) Expression and tissue localization of matrix metalloproteinase 7 (matrilysin) in human gastric carcinomas. Implications for vessel invasion and metastasis. Int J Cancer 79:187–194PubMedCrossRef Yamashita K, Azumano I, Mai M, Okada Y (1998) Expression and tissue localization of matrix metalloproteinase 7 (matrilysin) in human gastric carcinomas. Implications for vessel invasion and metastasis. Int J Cancer 79:187–194PubMedCrossRef
61.
go back to reference Leeman MF, Curran S, Murray GI (2003) New insights into the roles of matrix metalloproteinases in colorectal cancer development and progression. J Pathol 201:528–534PubMedCrossRef Leeman MF, Curran S, Murray GI (2003) New insights into the roles of matrix metalloproteinases in colorectal cancer development and progression. J Pathol 201:528–534PubMedCrossRef
62.
go back to reference Crawford HC, Fingleton BM, Rudolph-Owen LA, Goss KJ, Rubinfeld B, Polakis P et al (1999) The metalloproteinase matrilysin is a target of beta-catenin transactivation in intestinal tumors. Oncogene 18:2883–2891PubMedCrossRef Crawford HC, Fingleton BM, Rudolph-Owen LA, Goss KJ, Rubinfeld B, Polakis P et al (1999) The metalloproteinase matrilysin is a target of beta-catenin transactivation in intestinal tumors. Oncogene 18:2883–2891PubMedCrossRef
63.
go back to reference Zeng ZS, Shu WP, Cohen AM, Guillem JG (2002) Matrix metalloproteinase-7 expression in colorectal cancer liver metastases: evidence for involvement of MMP-7 activation in human cancer metastases. Clin Cancer Res 8:144–148PubMed Zeng ZS, Shu WP, Cohen AM, Guillem JG (2002) Matrix metalloproteinase-7 expression in colorectal cancer liver metastases: evidence for involvement of MMP-7 activation in human cancer metastases. Clin Cancer Res 8:144–148PubMed
Metadata
Title
Elevated expressions of MMP7, TROP2, and survivin are associated with survival, disease recurrence, and liver metastasis of colon cancer
Authors
Y. J. Fang
Z. H. Lu
G. Q. Wang
Z. Z. Pan
Z. W. Zhou
J. P. Yun
M. F. Zhang
D. S. Wan
Publication date
01-08-2009
Publisher
Springer-Verlag
Published in
International Journal of Colorectal Disease / Issue 8/2009
Print ISSN: 0179-1958
Electronic ISSN: 1432-1262
DOI
https://doi.org/10.1007/s00384-009-0725-z

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