Association between FOXM1 expression and prognosis of non-small cell lung cancer: a meta-analysis_Chinese Journal of Evidence-Based Medicine

Authors：

TIAN Long , LAI Yutian , WANG Xin , ZHOU Kun ,  CHE Guowei

Department of Thoracic Surgery, West China Hospital of Sichuan University, Chengdu, 610041, P.R.China;

Corresponding author：

CHE Guowei, Email: guowei_che@yahoo.com

Keywords：

FOXM1; Non-small cell lung cancer; Prognosis; Meta-analysis

DOI：

10.7507/1672-2531.201612023

Video：

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Objective To systematically review the prognostic and clinicopathological value of FOXM1 expression in non-small cell lung cancer (NSCLC). Methods Databases including PubMed, EMbase, The Cochrane Library (Issue 1, 2016), CNKI, WanFang Data and CBM were searched to collect cohort studies about the prognostic value of FOXM1 expression in NSCLC from inception to May 30^th 2016. Two reviewers independently screened literature, extracted data and assessed the risk of bias of included studies. Then meta-analysis was performed by using RevMan 5.3 software. Results A total of 8 cohort studies, involving 781 patients were included. The results of meta-analysis showed that FOXM1 expression was higher in tumor stage Ⅲ to Ⅳ than stageⅠtoⅡ(OR=2.24, 95%CI 1.25 to 4.01,P=0.007). Higher FOXM1 expression group had a shorter overall survival (HR=1.77, 95%CI 1.42 to 2.22,P<0.000 01) and disease-free survival (HR=1.96, 95%CI 1.04 to 3.17,P=0.04) than those of the lower FOXM1 expression group. Conclusion Current evidence shows that FOXM1 expression is associated with NSCLC stage. Furthermore, FOXM1 overexpression may be prognosis biomarker for NSCLC patients. Due to the limited quantity and quality of included studies, the above conclusions are needed to be verified by more high quality studies.

Citation： TIAN Long, LAI Yutian, WANG Xin, ZHOU Kun, CHE Guowei. Association between FOXM1 expression and prognosis of non-small cell lung cancer: a meta-analysis. Chinese Journal of Evidence-Based Medicine, 2017, 17(3): 306-311. doi: 10.7507/1672-2531.201612023 Copy

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2.	Spira A, Ettinger DS. Multidisciplinary management of lung cancer. N Engl J Med, 2004, 350(4): 379-392.
3.	Katoh M. Human FOX gene family (Review). Int J Oncol, 2004, 25(5): 1495-1500.
4.	Wonsey DR, Follettie MT. Loss of the forkhead transcription factor FoxM1 causes centrosome amplification and mitotic catastrophe. Cancer Res, 2005, 65(12): 5181-5189.
5.	Wierstra I, Alves J. FOXM1, a typical proliferation-associated transcription factor. Biol Chem, 2007, 388(12): 1257-1274.
6.	Kim IM, Ackerson T, Ramakrishna S,et al. The forkhead box m1 transcription factor stimulates the proliferation of tumor cells during development of lung cancer. Cancer Res, 2006, 66(4): 2153-2161.
7.	Yang DK, Son CH, Lee SK,et al. Forkhead box M1 expression in pulmonary squamous cell carcinoma: correlation with clinicopathologic features and its prognostic significance. Hum Pathol, 2009, 40(4): 464-470.
8.	刘怡茜, 郭人花, 刘连科, 等. 叉头框转录因子 M1 在非小细胞癌中的表达及其与患者病理特征和生存关系. 中华肿瘤杂志, 2011, 33(6): 426-430.
9.	Xu N, Wu SD, Wang H,et a1. Involvement of foxm1 in non-small cell lung cancer recurrence. Asian Pac J Cancer Prev, 2012, 13(9): 4739-4743.
10.	Wang Y, Wen L, Zhao SH,et al. FoxM1 expression is significantly associated with cisplatin-based chemotherapy resistance and poor prognosis in advanced non-small cell lung cancer patients. Lung Cancer, 2013, 79(2): 173-179.
11.	Xu N, Jia D, Chen W,et al. FoxM1 Is Associated with Poor Prognosis of Non-Small Cell Lung Cancer Patients through Promoting Tumor Metastasis. PLoS One, 2013, 8(3): e59412.
12.	陈芸, 梁鸿镖, 吴琼雅, 等. 叉头框转录因子 M1 在非小细胞肺癌中的表达及临床意义. 解放军医药杂志, 2013, 25(5): 48-52.
13.	Chen PM, Cheng YW, Wang YC,et al. Up-regulation of FOXM1 by E6 oncoprotein through the MZF1/NKX2-1 axis is required for human papillomavirus-associated tumorigenesis. Neoplasia (New York, NY), 2014, 16(11): 961-971.
14.	Kong FF, Qu ZQ, Yuan HH,et al. Overexpression of FOXM1 is associated with EMT and is a predictor of poor prognosis in non-small cell lung cancer. Oncol Rep, 2014, 31(6): 2660-2668.
15.	Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol, 2010, 25(9): 603-605.
16.	江峰, 吕赛平, 黄秀珍, 等. 非小细胞肺癌组织表达 FOXM1 与患者临床特征及术后辅助化疗疗效的关系研究. 中国医学创新, 2014, 30: 1-3.
17.	Li X, Qiu W, Liu B,et al. Forkhead box transcription factor 1 expression in gastric cancer: FOXM1 is a poor prognostic factor and mediates resistance to docetaxel. J Transl Med, 2013, 11: 204.
18.	Xia JT, Wang H, Liang LJ,et al. Overexpression of FOXM1 is associated with poor prognosis and clinicopathologic stage of pancreatic ductal adenocarcinoma. Pancreas, 2012, 41(4): 629-635.
19.	Chu XY, Zhu ZM, Chen LB,et al. FOXM1 expression correlates with tumor invasion and a poor prognosis of colorectal cancer. Acta Histochem, 2012, 114(8): 755-762.
20.	Wen N, Wang Y, Wen L,et al. Overexpression of FOXM1 predicts poor prognosis and promotes cancer cell proliferation, migration and invasion in epithelial ovarian cancer. J Transl Med, 2014, 12: 134.
21.	He SY, Shen HW, Xu L,et al. FOXM1 promotes tumor cell invasion and correlates with poor prognosis in early-stage cervical cancer. Gynecol Oncol, 2012, 127(3): 601-610.
22.	Park HJ, Gusarova G, Wang Z,et al. Deregulation of FoxM1b leads to tumour metastasis. EMBO Mol Med, 2011, 3(1): 21-34.
23.	Wang HX, Teh MT, Ji YM,et al. EPS8 upregulates FOXM1 expression, enhancing cell growth and motility. Carcinogenesis, 2010, 31(6): 1132-1141.
24.	Wei P, Zhang N, Wang Y,et al. FOXM1 promotes lung adenocarcinoma invasion and metastasis by upregulating SNAIL. Int J Biol Sci, 2015, 11(2): 186-198.
25.	Dai J, Yang L, Wang J,et al. Prognostic value of FOXM1 in patients with malignant solid tumor: a meta-analysis and systemativ review. Dis Markers, 2015, 2015: 352478.
26.	Laoukili J, Kooistra MRH, Bras A,et al. FoxM1 is required for execution of the mitotic programme and chromosome stability. Nat Cell Biol, 2005, 7(2): 126-134.
27.	Wang IC, Chen YJ, Hughes D,et al. Forkhead box m1 regulates the transcriptional network of genes essential for mitotic progression and genes encoding the SCF (Skp2-Cks1) ubiquitin ligase. Mol Cell Biol, 2005, 25(24): 10875-10894.
28.	Balli D, Ren X, Chou FS,et al. Foxm1 transcription factor is required for macrophage migration during lung inflammation and tumor formation. Oncogene, 2012, 31(34): 3875-3888.
29.	Koo CY, Muir KW, Lam EWF. FOXM1: From cancer initiation to progression and treatment. Biochim Biophys Acta, 2012, 1819(1): 28-37.
30.	Myatt SS, Lam EWF. The emerging roles of forkhead box (Fox) proteins in cancer. Nat Rev Cancer, 2007, 7(11): 847-859.
31.	Wang IC, Meliton L, Ren X,et al. Deletion of Forkhead Box M1 transcription factor from respiratory epithelial cells inhibits pulmonary tumorigenesis. Plos One, 2009, 4(8): e6609.
32.	Balli D, Zhang YF, Snyder J,et al. Endothelial cell-specific deletion of transcription factor FoxM1 increases urethane-induced lung carcinogenesis. Cancer Res, 2011, 71(1): 40-50.
33.	Wang IC, Meliton L, Tretiakova M,et al. Transgenic expression of the forkhead box M1 transcription factor induces formation of lung tumors. Oncogene, 2008, 27(30): 4137-4149.
34.	Li Q, Zhang N, Jia ZL,et al. Critical role and regulation of transcription factor FoxM1 in human gastric cancer angiogenesis and progression. Cancer Res, 2009, 69(8): 3501-3509.
35.	Zhang YJ, Zhang N, Dai BB,et al. FoxM1B transcriptionally regulates vascular endothelial growth factor expression and promotes the angiogenesis and growth of glioma cells. Cancer Res, 2008, 68(21): 8733-8742.
36.	Liu Y, Chen X, Gu Y,et al. FOXM1 overexpression is associated with cisplatin resistance in non-small cell lung cancer and mediates sensitivity to cisplatin in A549 cells via the JNK/mitochondrial pathway. Neoplasma, 2015, 62(1): 61-71.

1. Siegel R, DeSantis C, Virgo K,et al. Cancer treatment and survivorship statistics, 2012. CA Cancer J Clin, 2012, 62(4): 220-241.
2. Spira A, Ettinger DS. Multidisciplinary management of lung cancer. N Engl J Med, 2004, 350(4): 379-392.
3. Katoh M. Human FOX gene family (Review). Int J Oncol, 2004, 25(5): 1495-1500.
4. Wonsey DR, Follettie MT. Loss of the forkhead transcription factor FoxM1 causes centrosome amplification and mitotic catastrophe. Cancer Res, 2005, 65(12): 5181-5189.
5. Wierstra I, Alves J. FOXM1, a typical proliferation-associated transcription factor. Biol Chem, 2007, 388(12): 1257-1274.
6. Kim IM, Ackerson T, Ramakrishna S,et al. The forkhead box m1 transcription factor stimulates the proliferation of tumor cells during development of lung cancer. Cancer Res, 2006, 66(4): 2153-2161.
7. Yang DK, Son CH, Lee SK,et al. Forkhead box M1 expression in pulmonary squamous cell carcinoma: correlation with clinicopathologic features and its prognostic significance. Hum Pathol, 2009, 40(4): 464-470.
8. 刘怡茜, 郭人花, 刘连科, 等. 叉头框转录因子 M1 在非小细胞癌中的表达及其与患者病理特征和生存关系. 中华肿瘤杂志, 2011, 33(6): 426-430.
9. Xu N, Wu SD, Wang H,et a1. Involvement of foxm1 in non-small cell lung cancer recurrence. Asian Pac J Cancer Prev, 2012, 13(9): 4739-4743.
10. Wang Y, Wen L, Zhao SH,et al. FoxM1 expression is significantly associated with cisplatin-based chemotherapy resistance and poor prognosis in advanced non-small cell lung cancer patients. Lung Cancer, 2013, 79(2): 173-179.
11. Xu N, Jia D, Chen W,et al. FoxM1 Is Associated with Poor Prognosis of Non-Small Cell Lung Cancer Patients through Promoting Tumor Metastasis. PLoS One, 2013, 8(3): e59412.
12. 陈芸, 梁鸿镖, 吴琼雅, 等. 叉头框转录因子 M1 在非小细胞肺癌中的表达及临床意义. 解放军医药杂志, 2013, 25(5): 48-52.
13. Chen PM, Cheng YW, Wang YC,et al. Up-regulation of FOXM1 by E6 oncoprotein through the MZF1/NKX2-1 axis is required for human papillomavirus-associated tumorigenesis. Neoplasia (New York, NY), 2014, 16(11): 961-971.
14. Kong FF, Qu ZQ, Yuan HH,et al. Overexpression of FOXM1 is associated with EMT and is a predictor of poor prognosis in non-small cell lung cancer. Oncol Rep, 2014, 31(6): 2660-2668.
15. Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol, 2010, 25(9): 603-605.
16. 江峰, 吕赛平, 黄秀珍, 等. 非小细胞肺癌组织表达 FOXM1 与患者临床特征及术后辅助化疗疗效的关系研究. 中国医学创新, 2014, 30: 1-3.
17. Li X, Qiu W, Liu B,et al. Forkhead box transcription factor 1 expression in gastric cancer: FOXM1 is a poor prognostic factor and mediates resistance to docetaxel. J Transl Med, 2013, 11: 204.
18. Xia JT, Wang H, Liang LJ,et al. Overexpression of FOXM1 is associated with poor prognosis and clinicopathologic stage of pancreatic ductal adenocarcinoma. Pancreas, 2012, 41(4): 629-635.
19. Chu XY, Zhu ZM, Chen LB,et al. FOXM1 expression correlates with tumor invasion and a poor prognosis of colorectal cancer. Acta Histochem, 2012, 114(8): 755-762.
20. Wen N, Wang Y, Wen L,et al. Overexpression of FOXM1 predicts poor prognosis and promotes cancer cell proliferation, migration and invasion in epithelial ovarian cancer. J Transl Med, 2014, 12: 134.
21. He SY, Shen HW, Xu L,et al. FOXM1 promotes tumor cell invasion and correlates with poor prognosis in early-stage cervical cancer. Gynecol Oncol, 2012, 127(3): 601-610.
22. Park HJ, Gusarova G, Wang Z,et al. Deregulation of FoxM1b leads to tumour metastasis. EMBO Mol Med, 2011, 3(1): 21-34.
23. Wang HX, Teh MT, Ji YM,et al. EPS8 upregulates FOXM1 expression, enhancing cell growth and motility. Carcinogenesis, 2010, 31(6): 1132-1141.
24. Wei P, Zhang N, Wang Y,et al. FOXM1 promotes lung adenocarcinoma invasion and metastasis by upregulating SNAIL. Int J Biol Sci, 2015, 11(2): 186-198.
25. Dai J, Yang L, Wang J,et al. Prognostic value of FOXM1 in patients with malignant solid tumor: a meta-analysis and systemativ review. Dis Markers, 2015, 2015: 352478.
26. Laoukili J, Kooistra MRH, Bras A,et al. FoxM1 is required for execution of the mitotic programme and chromosome stability. Nat Cell Biol, 2005, 7(2): 126-134.
27. Wang IC, Chen YJ, Hughes D,et al. Forkhead box m1 regulates the transcriptional network of genes essential for mitotic progression and genes encoding the SCF (Skp2-Cks1) ubiquitin ligase. Mol Cell Biol, 2005, 25(24): 10875-10894.
28. Balli D, Ren X, Chou FS,et al. Foxm1 transcription factor is required for macrophage migration during lung inflammation and tumor formation. Oncogene, 2012, 31(34): 3875-3888.
29. Koo CY, Muir KW, Lam EWF. FOXM1: From cancer initiation to progression and treatment. Biochim Biophys Acta, 2012, 1819(1): 28-37.
30. Myatt SS, Lam EWF. The emerging roles of forkhead box (Fox) proteins in cancer. Nat Rev Cancer, 2007, 7(11): 847-859.
31. Wang IC, Meliton L, Ren X,et al. Deletion of Forkhead Box M1 transcription factor from respiratory epithelial cells inhibits pulmonary tumorigenesis. Plos One, 2009, 4(8): e6609.
32. Balli D, Zhang YF, Snyder J,et al. Endothelial cell-specific deletion of transcription factor FoxM1 increases urethane-induced lung carcinogenesis. Cancer Res, 2011, 71(1): 40-50.
33. Wang IC, Meliton L, Tretiakova M,et al. Transgenic expression of the forkhead box M1 transcription factor induces formation of lung tumors. Oncogene, 2008, 27(30): 4137-4149.
34. Li Q, Zhang N, Jia ZL,et al. Critical role and regulation of transcription factor FoxM1 in human gastric cancer angiogenesis and progression. Cancer Res, 2009, 69(8): 3501-3509.
35. Zhang YJ, Zhang N, Dai BB,et al. FoxM1B transcriptionally regulates vascular endothelial growth factor expression and promotes the angiogenesis and growth of glioma cells. Cancer Res, 2008, 68(21): 8733-8742.
36. Liu Y, Chen X, Gu Y,et al. FOXM1 overexpression is associated with cisplatin resistance in non-small cell lung cancer and mediates sensitivity to cisplatin in A549 cells via the JNK/mitochondrial pathway. Neoplasma, 2015, 62(1): 61-71.

Chinese Journal of Evidence-Based Medicine

Association between FOXM1 expression and prognosis of non-small cell lung cancer: a meta-analysis

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