Skip to main content
Top
Published in: Annals of Surgical Oncology 7/2011

01-07-2011 | Translational Research and Biomarkers

Overexpression of Metastasis-Associated Protein 1 is Significantly Correlated with Tumor Angiogenesis and Poor Survival in Patients with Early-Stage Non-Small Cell Lung Cancer

Authors: Shu-hai Li, MD, Hui Tian, MD, Wei-ming Yue, MD, Lin Li, MD, Wen-jun Li, MD, Zhi-tao Chen, MD, Wen-si Hu, MD, Ying-chao Zhu, MMed, Lei Qi, MMed

Published in: Annals of Surgical Oncology | Issue 7/2011

Login to get access

Abstract

Background

The aims of this work are to detect the expression levels of metastasis-associated protein 1 (MTA1) in patients with early-stage non-small cell lung cancer (NSCLC), and to investigate the relationship of MTA1 protein with clinicopathologic factors, tumor angiogenesis, and prognosis.

Methods

One hundred and two patients with pathologic stage I NSCLC who successfully underwent curative surgical resection were enrolled in this study. Immunohistochemical staining for MTA1 and CD34 was performed using the streptavidin–peroxidase method, and intratumoral microvessel density (MVD) was recorded by counting CD34-positive immunostained endothelial cells. All statistical analyses were performed with SPSS statistical software to determine the effects of MTA1 protein on clinicopathologic factors, tumor angiogenesis, and prognosis.

Results

MTA1 protein overexpression was detected in 41 cases and was significantly associated with MVD (P = 0.008). MTA1 protein overexpression and high MVD were significantly associated with tumor relapse (P = 0.004 and 0.007) and poor 5-year disease-free survival (P = 0.001 and 0.004). Patients with MTA1 protein overexpression and high MVD had significantly poor overall survival (P = 0.005 and 0.043) and disease-specific survival (P = 0.006 and 0.031) at 5 years after operation. Multivariate analysis demonstrated that MTA1 protein overexpression was an independent prognosticator for unfavorable disease-free, overall, and disease-specific survival (P = 0.011, 0.024, and 0.046).

Conclusions

MTA1 protein overexpression is common in early-stage NSCLC and is significantly associated with tumor angiogenesis and poor survival. These findings suggest that MTA1 may have clinical potential as a promising predictor to identify individuals with poor prognostic potential and as a possible novel target molecule of antiangiogenic therapy for patients with early-stage NSCLC.
Literature
1.
go back to reference Hoffman PC, Mauer AM, Vokes EE. Lung cancer. Lancet. 2000;355:479–85.PubMed Hoffman PC, Mauer AM, Vokes EE. Lung cancer. Lancet. 2000;355:479–85.PubMed
2.
go back to reference Kamangar F, Dores GM, Anderson WF. Patterns of cancer incidence, mortality, and prevalence across five continents: defining priorities to reduce cancer disparities in different geographic regions of the world. J Clin Oncol. 2006;24:2137–50.PubMedCrossRef Kamangar F, Dores GM, Anderson WF. Patterns of cancer incidence, mortality, and prevalence across five continents: defining priorities to reduce cancer disparities in different geographic regions of the world. J Clin Oncol. 2006;24:2137–50.PubMedCrossRef
3.
go back to reference Brognard J, Clark AS, Ni Y, Dennis PA. Akt/protein kinase B is constitutively active in non-small cell lung cancer cells and promotes cellular survival and resistance to chemotherapy and radiation. Cancer Res. 2001;61:3986–97.PubMed Brognard J, Clark AS, Ni Y, Dennis PA. Akt/protein kinase B is constitutively active in non-small cell lung cancer cells and promotes cellular survival and resistance to chemotherapy and radiation. Cancer Res. 2001;61:3986–97.PubMed
4.
go back to reference Ren H, Tang X, Lee JJ, et al. Expression of hepatoma-derived growth factor is a strong prognostic predictor for patients with early-stage non-small-cell lung cancer. J Clin Oncol. 2004;22:3230–7.PubMedCrossRef Ren H, Tang X, Lee JJ, et al. Expression of hepatoma-derived growth factor is a strong prognostic predictor for patients with early-stage non-small-cell lung cancer. J Clin Oncol. 2004;22:3230–7.PubMedCrossRef
6.
go back to reference Fry WA, Philips JL, Menck HR. Ten-year survey of lung cancer treatment and survival in hospitals in the United States: a national cancer data base report. Cancer. 1999;86:1867–76.PubMedCrossRef Fry WA, Philips JL, Menck HR. Ten-year survey of lung cancer treatment and survival in hospitals in the United States: a national cancer data base report. Cancer. 1999;86:1867–76.PubMedCrossRef
7.
go back to reference Kim JH, Bogner PN, Ramnath N, Park Y, Yu J, Park YM. Elevated peroxiredoxin 1, but not NF-E2-related factor 2, is an independent prognostic factor for disease recurrence and reduced survival in stage I non-small cell lung cancer. Clin Cancer Res. 2007;13:3875–82.PubMedCrossRef Kim JH, Bogner PN, Ramnath N, Park Y, Yu J, Park YM. Elevated peroxiredoxin 1, but not NF-E2-related factor 2, is an independent prognostic factor for disease recurrence and reduced survival in stage I non-small cell lung cancer. Clin Cancer Res. 2007;13:3875–82.PubMedCrossRef
8.
go back to reference Arriagada R, Bergman B, Dunant A, Le Chevalier T, Pignon JP, Vansteenkiste J. Cisplatin-based adjuvant chemotherapy in patients with completely resected non- small-cell lung cancer. N Engl J Med. 2004;350:351–60.PubMedCrossRef Arriagada R, Bergman B, Dunant A, Le Chevalier T, Pignon JP, Vansteenkiste J. Cisplatin-based adjuvant chemotherapy in patients with completely resected non- small-cell lung cancer. N Engl J Med. 2004;350:351–60.PubMedCrossRef
9.
go back to reference Pignon JP, Tribodet H, Scagliotti GV, Douillard JY, Shepherd FA, Stephens RJ, et al., on behalf of the LACE Collaborative Group. Lung Adjuvant Cisplatin Evaluation (LACE): a pooled analysis of five randomized clinical trials including 4,584 patients. J Clin Oncol. 2006;24(18 suppl):366s (abstract 7008). Pignon JP, Tribodet H, Scagliotti GV, Douillard JY, Shepherd FA, Stephens RJ, et al., on behalf of the LACE Collaborative Group. Lung Adjuvant Cisplatin Evaluation (LACE): a pooled analysis of five randomized clinical trials including 4,584 patients. J Clin Oncol. 2006;24(18 suppl):366s (abstract 7008).
10.
go back to reference Winton T, Livingston R, Johnson D, et al. Vinorelbine plus cisplatin vs. observation in resected non-small-cell lung cancer. N Engl J Med. 2005;352:2589–97.PubMedCrossRef Winton T, Livingston R, Johnson D, et al. Vinorelbine plus cisplatin vs. observation in resected non-small-cell lung cancer. N Engl J Med. 2005;352:2589–97.PubMedCrossRef
11.
go back to reference Dango S, Sienel W, Schreiber M, Stremmel C, Kirschbaum A, Pantel K, et al. Elevated expression of carcinoembryonic antigen-related cell adhesion molecule 1 (CEACAM-1) is associated with increased angiogenic potential in non-small-cell lung cancer. Lung Cancer. 2008;60:426–33.PubMedCrossRef Dango S, Sienel W, Schreiber M, Stremmel C, Kirschbaum A, Pantel K, et al. Elevated expression of carcinoembryonic antigen-related cell adhesion molecule 1 (CEACAM-1) is associated with increased angiogenic potential in non-small-cell lung cancer. Lung Cancer. 2008;60:426–33.PubMedCrossRef
12.
go back to reference Raz DJ, Ray MR, Kim JY, et al. A multigene assay is prognostic of survival in patients with early-stage lung adenocarcinoma. Clin Cancer Res. 2008;14:5565–70.PubMedCrossRef Raz DJ, Ray MR, Kim JY, et al. A multigene assay is prognostic of survival in patients with early-stage lung adenocarcinoma. Clin Cancer Res. 2008;14:5565–70.PubMedCrossRef
14.
go back to reference Toh Y, Nicolson GL. The role of the MTA family and their encoded proteins in human cancers: molecular functions and clinical implications. Clin Exp Metastasis. 2009;26:215–27.PubMedCrossRef Toh Y, Nicolson GL. The role of the MTA family and their encoded proteins in human cancers: molecular functions and clinical implications. Clin Exp Metastasis. 2009;26:215–27.PubMedCrossRef
15.
go back to reference Nicolson GL, Nawa A, Toh Y, Taniguchi S, Nishimori K, Moustafa A. Tumor metastasis-associated human MTA1 gene and its MTA1 protein product: role in epithelial cancer cell invasion, proliferation and nuclear regulation. Clin Exp Metastasis. 2003;20:19–24.PubMedCrossRef Nicolson GL, Nawa A, Toh Y, Taniguchi S, Nishimori K, Moustafa A. Tumor metastasis-associated human MTA1 gene and its MTA1 protein product: role in epithelial cancer cell invasion, proliferation and nuclear regulation. Clin Exp Metastasis. 2003;20:19–24.PubMedCrossRef
16.
go back to reference Kumar R, Wang RA, Bagheri-Yarmand R. Emerging roles of MTA family members in human cancers. Semin Oncol. 2003;30:30–7.PubMedCrossRef Kumar R, Wang RA, Bagheri-Yarmand R. Emerging roles of MTA family members in human cancers. Semin Oncol. 2003;30:30–7.PubMedCrossRef
17.
go back to reference Mazumdar A, Wang RA, Mishra SK, et al. Transcriptional repression of oestrogen receptor by metastasis-associated protein 1 corepressor. Nat Cell Biol. 2001;3:30–7.PubMedCrossRef Mazumdar A, Wang RA, Mishra SK, et al. Transcriptional repression of oestrogen receptor by metastasis-associated protein 1 corepressor. Nat Cell Biol. 2001;3:30–7.PubMedCrossRef
18.
go back to reference Yan C, Wang H, Toh Y, Boyd DD. Repression of 92-kDa type IV collagenase expression by MTA1 is mediated through direct interactions with the promoter via a mechanism, which is both dependent on and independent of histone deacetylation. J Biol Chem. 2003;278:2309–16.PubMedCrossRef Yan C, Wang H, Toh Y, Boyd DD. Repression of 92-kDa type IV collagenase expression by MTA1 is mediated through direct interactions with the promoter via a mechanism, which is both dependent on and independent of histone deacetylation. J Biol Chem. 2003;278:2309–16.PubMedCrossRef
19.
go back to reference Jang KS, Paik SS, Chung H, Oh YH, Kong G. MTA1 overexpression correlates significantly with tumor grade and angiogenesis in human breast cancers. Cancer Sci. 2006;97:374–9.PubMedCrossRef Jang KS, Paik SS, Chung H, Oh YH, Kong G. MTA1 overexpression correlates significantly with tumor grade and angiogenesis in human breast cancers. Cancer Sci. 2006;97:374–9.PubMedCrossRef
20.
go back to reference Martin MD, Hilsenbeck SG, Mohsin SK, et al. Breast tumors that overexpress nuclear metastasis-associated 1 (MTA1) protein have high recurrence risks but enhanced responses to systemic therapies. Breast Cancer Res Treat. 2006;95:7–12.PubMedCrossRef Martin MD, Hilsenbeck SG, Mohsin SK, et al. Breast tumors that overexpress nuclear metastasis-associated 1 (MTA1) protein have high recurrence risks but enhanced responses to systemic therapies. Breast Cancer Res Treat. 2006;95:7–12.PubMedCrossRef
21.
go back to reference Hofer MD, Kuefer R, Varambally S, et al. The role of metastasis-associated protein 1 in prostate cancer progression. Cancer Res. 2004;64:825–9.PubMedCrossRef Hofer MD, Kuefer R, Varambally S, et al. The role of metastasis-associated protein 1 in prostate cancer progression. Cancer Res. 2004;64:825–9.PubMedCrossRef
22.
go back to reference Balasenthil S, Broaddus RR, Kumar R. Expression of metastasis-associate protein 1 (MTA1) in benign endometrium and endometrial adenocarcinomas. Hum Pathol. 2006;37:656–61.PubMedCrossRef Balasenthil S, Broaddus RR, Kumar R. Expression of metastasis-associate protein 1 (MTA1) in benign endometrium and endometrial adenocarcinomas. Hum Pathol. 2006;37:656–61.PubMedCrossRef
23.
go back to reference Ryu SH, Chung YH, Lee H, et al. Metastatic tumor antigen 1 is closely associated with frequent postoperative recurrence and poor survival in patients with hepatocellular carcinoma. Hepatology. 2008;47:929–36.PubMedCrossRef Ryu SH, Chung YH, Lee H, et al. Metastatic tumor antigen 1 is closely associated with frequent postoperative recurrence and poor survival in patients with hepatocellular carcinoma. Hepatology. 2008;47:929–36.PubMedCrossRef
24.
go back to reference Mahoney MG, Simpson A, Jost M, et al. Metastasis-associated protein (MTA) 1 enhances migration, invasion and anchorage-independent survival of immortalized human keratinocytes. Oncogene. 2002;21:2161–70.PubMedCrossRef Mahoney MG, Simpson A, Jost M, et al. Metastasis-associated protein (MTA) 1 enhances migration, invasion and anchorage-independent survival of immortalized human keratinocytes. Oncogene. 2002;21:2161–70.PubMedCrossRef
25.
go back to reference Hofer MD, Menke A, Genze F, Gierschik P, Giehl K. Expression of MTA1 promotes motility and invasiveness of PANC-1 pancreatic carcinoma cells. Br J Cancer. 2004;90:455–62.PubMedCrossRef Hofer MD, Menke A, Genze F, Gierschik P, Giehl K. Expression of MTA1 promotes motility and invasiveness of PANC-1 pancreatic carcinoma cells. Br J Cancer. 2004;90:455–62.PubMedCrossRef
26.
go back to reference Toh Y, Ohga T, Endo K, et al. Expression of the metastasis-associated MTA1 protein and its relationship to deacetylation of the histone H4 in esophageal squamous cell carcinomas. Int J Cancer. 2004;110:362–7.PubMedCrossRef Toh Y, Ohga T, Endo K, et al. Expression of the metastasis-associated MTA1 protein and its relationship to deacetylation of the histone H4 in esophageal squamous cell carcinomas. Int J Cancer. 2004;110:362–7.PubMedCrossRef
27.
go back to reference Eskens FA. Angiogenesis inhibitors in clinical development; where are we now and where are we going? Br J Cancer. 2004;90:1–7.PubMedCrossRef Eskens FA. Angiogenesis inhibitors in clinical development; where are we now and where are we going? Br J Cancer. 2004;90:1–7.PubMedCrossRef
28.
go back to reference Steeg PS. Tumor metastasis: mechanistic insights and clinical challenges. Nat Med. 2006;12:895–904.PubMedCrossRef Steeg PS. Tumor metastasis: mechanistic insights and clinical challenges. Nat Med. 2006;12:895–904.PubMedCrossRef
29.
go back to reference Bremnes RM, Camps C, Sirera R. Angiogenesis in non-small cell lung cancer: the prognostic impact of neoangiogenesis and the cytokines VEGF and bFGF in tumours and blood. Lung Cancer. 2006;51:143–58.PubMedCrossRef Bremnes RM, Camps C, Sirera R. Angiogenesis in non-small cell lung cancer: the prognostic impact of neoangiogenesis and the cytokines VEGF and bFGF in tumours and blood. Lung Cancer. 2006;51:143–58.PubMedCrossRef
30.
go back to reference Kerbel R, Folkman J. Clinical translation of angiogenesis inhibitors. Nat Rev Cancer. 2002;2:727–39.PubMedCrossRef Kerbel R, Folkman J. Clinical translation of angiogenesis inhibitors. Nat Rev Cancer. 2002;2:727–39.PubMedCrossRef
31.
go back to reference Moon HE, Cheon H, Chun KH, et al. Metastasis-associated protein 1 enhances angiogenesis by stabilization of HIF-1alpha. Oncol Rep. 2006;16:929–35.PubMed Moon HE, Cheon H, Chun KH, et al. Metastasis-associated protein 1 enhances angiogenesis by stabilization of HIF-1alpha. Oncol Rep. 2006;16:929–35.PubMed
32.
go back to reference Naruke T, Suematu K, Ishikawa S. Lymph node mapping and curability at various levels of metastasis in resected lung cancer. J Thorac Cardiovasc Surg. 1978;76:832–9.PubMed Naruke T, Suematu K, Ishikawa S. Lymph node mapping and curability at various levels of metastasis in resected lung cancer. J Thorac Cardiovasc Surg. 1978;76:832–9.PubMed
33.
go back to reference Travis WD, Brambilla E, Muller-Hermelink HK, Harris CC. Pathology and genetics of tumours of the lung, pleura, thymus and heart. Lyon: IARC Press; 2004. Travis WD, Brambilla E, Muller-Hermelink HK, Harris CC. Pathology and genetics of tumours of the lung, pleura, thymus and heart. Lyon: IARC Press; 2004.
34.
go back to reference Mountain CF. Revision in the international system for staging lung cancer. Chest. 1997;111:1710–7.PubMedCrossRef Mountain CF. Revision in the international system for staging lung cancer. Chest. 1997;111:1710–7.PubMedCrossRef
35.
go back to reference Yuan A, Yu CJ, Shun CT, Luh KT, Kuo SH, Lee YC, et al. Total cyclooxygenase-2 mRNA levels correlate with vascular endothelial growth factor mRNA levels, tumor angiogenesis and prognosis in non-small cell lung cancer patients. Int J Cancer. 2005;115:545–55.PubMedCrossRef Yuan A, Yu CJ, Shun CT, Luh KT, Kuo SH, Lee YC, et al. Total cyclooxygenase-2 mRNA levels correlate with vascular endothelial growth factor mRNA levels, tumor angiogenesis and prognosis in non-small cell lung cancer patients. Int J Cancer. 2005;115:545–55.PubMedCrossRef
36.
go back to reference Li SH, Wang Z, Liu XY. Metastasis-associated protein 1 (MTA1) overexpression is closely associated with shorter disease-free interval after complete resection of histologically node-negative esophageal cancer. World J Surg. 2009;33:1876–81.PubMedCrossRef Li SH, Wang Z, Liu XY. Metastasis-associated protein 1 (MTA1) overexpression is closely associated with shorter disease-free interval after complete resection of histologically node-negative esophageal cancer. World J Surg. 2009;33:1876–81.PubMedCrossRef
37.
go back to reference Vermeulen PB, Gasparini G, Fox SB, et al. Second international consensus on the methodology and criteria of evaluation of angiogenesis quantification in solid human tumours. Eur J Cancer. 2002;38:1564–79.PubMedCrossRef Vermeulen PB, Gasparini G, Fox SB, et al. Second international consensus on the methodology and criteria of evaluation of angiogenesis quantification in solid human tumours. Eur J Cancer. 2002;38:1564–79.PubMedCrossRef
38.
go back to reference Yuan A, Yu CJ, Chen WJ, Lin FY, Kuo SH, Luh KT, et al. Correlation of total VEGF mRNA and protein expression with histologic type, tumor angiogenesis, patient survival and timing of relapse in non-small-cell lung cancer. Int J Cancer. 2000;89:475–83.PubMedCrossRef Yuan A, Yu CJ, Chen WJ, Lin FY, Kuo SH, Luh KT, et al. Correlation of total VEGF mRNA and protein expression with histologic type, tumor angiogenesis, patient survival and timing of relapse in non-small-cell lung cancer. Int J Cancer. 2000;89:475–83.PubMedCrossRef
39.
go back to reference Masuya D, Huang C, Liu D, et al. The intratumoral expression of vascular endothelial growth factor and interleukin-8 associated with angiogenesis in nonsmall cell lung carcinoma patients. Cancer. 2001;92:2628–38.PubMedCrossRef Masuya D, Huang C, Liu D, et al. The intratumoral expression of vascular endothelial growth factor and interleukin-8 associated with angiogenesis in nonsmall cell lung carcinoma patients. Cancer. 2001;92:2628–38.PubMedCrossRef
40.
go back to reference Huang C, Liu D, Masuya D, et al. Clinical application of biological markers for treatments of resectable non-small-cell lung cancers. Br J Cancer. 2005;92:1231–9.PubMedCrossRef Huang C, Liu D, Masuya D, et al. Clinical application of biological markers for treatments of resectable non-small-cell lung cancers. Br J Cancer. 2005;92:1231–9.PubMedCrossRef
41.
go back to reference Kadota K, Huang CL, Liu D, Ueno M, Kushida Y, Haba R, et al. The clinical significance of lymphangiogenesis and angiogenesis in non-small cell lung cancer patients. Eur J Cancer. 2008;44:1057–67.PubMedCrossRef Kadota K, Huang CL, Liu D, Ueno M, Kushida Y, Haba R, et al. The clinical significance of lymphangiogenesis and angiogenesis in non-small cell lung cancer patients. Eur J Cancer. 2008;44:1057–67.PubMedCrossRef
42.
go back to reference Guo NL, Wan YW, Tosun K, et al. Confirmation of gene expression-based prediction of survival in non-small cell lung cancer. Clin Cancer Res. 2008;14:8213–20.PubMedCrossRef Guo NL, Wan YW, Tosun K, et al. Confirmation of gene expression-based prediction of survival in non-small cell lung cancer. Clin Cancer Res. 2008;14:8213–20.PubMedCrossRef
43.
go back to reference D’Amico TA. Angiogenesis in non-small cell lung cancer. Semin Thorac Cardiovasc Surg. 2004;16:13–8.PubMedCrossRef D’Amico TA. Angiogenesis in non-small cell lung cancer. Semin Thorac Cardiovasc Surg. 2004;16:13–8.PubMedCrossRef
44.
go back to reference Kim HS, Youm HR, Lee JS, Min KW, Chung JH, Park CS. Correlation between cyclooxygenase-2 and tumor angiogenesis in non-small cell lung cancer. Lung Cancer. 2003;42:163–70.PubMedCrossRef Kim HS, Youm HR, Lee JS, Min KW, Chung JH, Park CS. Correlation between cyclooxygenase-2 and tumor angiogenesis in non-small cell lung cancer. Lung Cancer. 2003;42:163–70.PubMedCrossRef
45.
go back to reference Chen HY, Yu SL, Chen CH, et al. A five-gene signature and clinical outcome in non-small-cell lung cancer. N Engl J Med. 2007;356:11–20.PubMedCrossRef Chen HY, Yu SL, Chen CH, et al. A five-gene signature and clinical outcome in non-small-cell lung cancer. N Engl J Med. 2007;356:11–20.PubMedCrossRef
46.
go back to reference Sasaki H, Moriyama S, Nakashima Y, et al. Expression of the MTA1 mRNA in advanced lung cancer. Lung Cancer. 2002;35:149–54.PubMedCrossRef Sasaki H, Moriyama S, Nakashima Y, et al. Expression of the MTA1 mRNA in advanced lung cancer. Lung Cancer. 2002;35:149–54.PubMedCrossRef
47.
go back to reference Li D, Qian J, Hong Z. Expression and clinical significance of MTA1 in non-small cell lung cancer. Zhongguo Fei Ai Za Zhi. 2008;11:775–9.PubMed Li D, Qian J, Hong Z. Expression and clinical significance of MTA1 in non-small cell lung cancer. Zhongguo Fei Ai Za Zhi. 2008;11:775–9.PubMed
48.
go back to reference Zhu XX, Guo Y, Chen LH, Ding YQ. Expressions of metastatic tumor antigen 1 and hypoxia-inducible-factor l alpha in lung cancer and their clinical significance. Nan Fang Yi Ke Da Xue Xue Bao. 2009;29:642–4.PubMed Zhu XX, Guo Y, Chen LH, Ding YQ. Expressions of metastatic tumor antigen 1 and hypoxia-inducible-factor l alpha in lung cancer and their clinical significance. Nan Fang Yi Ke Da Xue Xue Bao. 2009;29:642–4.PubMed
49.
go back to reference Zhu X, Guo Y, Li X, Ding Y, Chen L. Metastasis-associated protein 1 nuclear expression is associated with tumor progression and clinical outcome in patients with non-small cell lung cancer. J Thorac Oncol. 2010;5:1159–66.PubMedCrossRef Zhu X, Guo Y, Li X, Ding Y, Chen L. Metastasis-associated protein 1 nuclear expression is associated with tumor progression and clinical outcome in patients with non-small cell lung cancer. J Thorac Oncol. 2010;5:1159–66.PubMedCrossRef
50.
go back to reference Shijubo N, Kojima H, Nagata M, Ohchi T, Suzuki A, Abe S, et al. Tumor angiogenesis of non-small cell lung cancer. Microsc Res Tech. 2003;60:186–98.PubMedCrossRef Shijubo N, Kojima H, Nagata M, Ohchi T, Suzuki A, Abe S, et al. Tumor angiogenesis of non-small cell lung cancer. Microsc Res Tech. 2003;60:186–98.PubMedCrossRef
51.
go back to reference Meert AP, Paesmans M, Martin B, et al. The role of microvessel density on the survival of patients with lung cancer: a systematic review of the literature with meta-analysis. Br J Cancer. 2002;87:694–701.PubMedCrossRef Meert AP, Paesmans M, Martin B, et al. The role of microvessel density on the survival of patients with lung cancer: a systematic review of the literature with meta-analysis. Br J Cancer. 2002;87:694–701.PubMedCrossRef
52.
go back to reference Marrogi AJ, Travis WD, Welsh JA, et al. Nitric oxide synthase, cyclooxygenase 2, and vascular endothelial growth factor in the angiogenesis of non-small cell lung carcinoma. Clin Cancer Res. 2000;6:4739–44.PubMed Marrogi AJ, Travis WD, Welsh JA, et al. Nitric oxide synthase, cyclooxygenase 2, and vascular endothelial growth factor in the angiogenesis of non-small cell lung carcinoma. Clin Cancer Res. 2000;6:4739–44.PubMed
53.
go back to reference Han H, Silverman JF, Santucci TS, et al. Vascular endothelial growth factor expression in stage I non-small cell lung cancer correlates with neoangiogenesis and a poor prognosis. Ann Surg Oncol. 2001;8:72–9.PubMedCrossRef Han H, Silverman JF, Santucci TS, et al. Vascular endothelial growth factor expression in stage I non-small cell lung cancer correlates with neoangiogenesis and a poor prognosis. Ann Surg Oncol. 2001;8:72–9.PubMedCrossRef
Metadata
Title
Overexpression of Metastasis-Associated Protein 1 is Significantly Correlated with Tumor Angiogenesis and Poor Survival in Patients with Early-Stage Non-Small Cell Lung Cancer
Authors
Shu-hai Li, MD
Hui Tian, MD
Wei-ming Yue, MD
Lin Li, MD
Wen-jun Li, MD
Zhi-tao Chen, MD
Wen-si Hu, MD
Ying-chao Zhu, MMed
Lei Qi, MMed
Publication date
01-07-2011
Publisher
Springer-Verlag
Published in
Annals of Surgical Oncology / Issue 7/2011
Print ISSN: 1068-9265
Electronic ISSN: 1534-4681
DOI
https://doi.org/10.1245/s10434-010-1510-5

Other articles of this Issue 7/2011

Annals of Surgical Oncology 7/2011 Go to the issue