Epithelial Mesenchymal Transition Effects and Regulation Mechanism in Astric Carcinoma Metastasis_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

 ZHUDeng-feng ^1,2 ,  JIANGBo-jian ²

1. Department of General Surger, Xinhua Hospital Chongming Branch Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai 202150, China;
2. Department of General Surgery, Shanghai Third People's Hospital affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai 201999, China;

Corresponding author：

JIANGBo-jian, Email: Jiang_md@hotmail.com

Keywords：

Epithelial mesenchymal transition; Gastric cancer; Invasion; Metastasis; Circulating tumor cell

DOI：

10.7507/1007-9424.20150334

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To study the relationship between mesenchymal transition epithelial (EMT) and the occurrence, development, invasion, and metastasis of gastric cancer, and to seek to block the EMT process so as to achieve the purpose of treating tumor. Methods The literatures of EMT, signal pathway, and gastric cancer were analyzed by querying the PubMed. Results The function and regulation mechanism of EMT is closely related to the development of gastric cancer, in the growth and proliferation of gastric cancer, tumor invasion and metastasis through a variety of signaling pathways play a role, with a great clinical application prospects. Conclusions EMT and tumor metastasis is very close, almost involved in every process of metastasis. It is necessary to further study the relationship between EMT and cancer, including gastric carcinoma metastasis. A new way for the treatment of human gastric cancer.

Citation： ZHUDeng-feng, JIANGBo-jian. Epithelial Mesenchymal Transition Effects and Regulation Mechanism in Astric Carcinoma Metastasis. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2015, 22(10): 1284-1288. doi: 10.7507/1007-9424.20150334 Copy

1.	Fock KM. Review article:the epidemiology and prevention of gastric cancer. Aliment Pharmacol Ther, 2014, 40(3):250-260.
2.	Chen W, Zheng R, Zhang S, et al. Report of incidence and mortality in China cancer registries, 2009. Chin J Cancer Res, 2013, 25(1):10-21.
3.	Tirino V, Desiderio V, Paino F, et al. Cancer stem cells in solid tumors:an overview and new approaches for their isolation and characterization. FASEB J, 2013, 27(1):13-24.
4.	Tsai JH, Yang J. Epithelial-mesenchymal plasticity in carcinoma metastasis. Genes Dev, 2013, 27(20):2192-2206.
5.	Lamouille S, Xu J, Derynck R. Molecular mechanisms of epithelialmesenchymal transition. Nat Rev Mol Cell Biol, 2014, 15(3):178-196.
6.	Huang RY, Guilford P, Thiery JP. Early events in cell adhesion and polarity during epithelial-mesenchymal transition. J Cell Sci, 2012, 125(Pt 19):4417-4422.
7.	Bax NA, Pijnappels DA, van Oorschot AA, et al. Epithelial-tomesenchymal transformation alters electrical conductivity of human epicardial cells. J Cell Mol Med, 2011, 15(12):2675-2683.
8.	Jung H, Jun KH, Jung JH, et al. The expression of claudin-1, claudin-2, claudin-3, and claudin-4 in gastric cancer tissue. J Surg Res, 2011, 167(2):e185-e191.
9.	Masuda R, Semba S, Mizuuchi E, et al. Negative regulation of the tight junction protein tricellulin by snail-induced epithelialmesenchymal transition in gastric carcinoma cells. Pathobiology, 2010, 77(2):106-113.
10.	Katoh M. Epithelial-mesenchymal transition in gastric cancer (Review). Int J Oncol, 2005, 27(6):1677-1683.
11.	Berx G, van Roy F. Involvement of members of the cadherin superfamily in cancer. Cold Spring Harb Perspect Biol, 2009, 1(6):a003129.
12.	Guilford P, Hopkins J, Harraway J, et al. E-cadherin germline mutations in familial gastric cancer. Nature, 1998, 392(6674):402-405.
13.	Rosivatz E, Becker I, Specht K, et al. Differential expression of the epithelial-mesenchymal transition regulators snail, SIP1, and twist in gastric cancer. Am J Pathol, 2002, 161(5):1881-1891.
14.	Yoo YA, Kang MH, Lee HJ, et al. Sonic hedgehog pathway promotes metastasis and lymphangiogenesis via activation of Akt, EMT, and MMP-9 pathway in gastric cancer. Cancer Res, 2011, 71(22):7061-7070.
15.	Fanelli MF, Chinen LT, Begnami MD, et al. The influence of transforming growth factor-alpha, cyclooxygenase-2, matrix metalloproteinase (MMP)-7, MMP-9 and CXCR4 proteins involved in epithelial-mesenchymal transition on overall survival of patients with gastric cancer. Histopathology, 2012, 61(2):153-161.
16.	Eckert MA, Lwin TM, Chang AT, et al. Twist1-induced invadopodia formation promotes tumor metastasis. Cancer Cell, 2011, 19(3):372-386.
17.	Murphy DA, Courtneidge SA. The 'ins' and 'outs' of podosomes and invadopodia:characteristics, formation and function. Nat Rev Mol Cell Biol, 2011, 12(7):413-426.
18.	de Paula CA, Coulson-Thomas VJ, Ferreira JG, et al. Enterolobium contortisiliquum trypsin inhibitor (EcTI), a plant proteinase inhibitor, decreases in vitro cell adhesion and invasion by inhibition of Src protein-focal adhesion kinase (FAK) signaling pathways. J Biol Chem, 2012, 287(1):170-182.
19.	Frisch SM, Schaller M, Cieply B. Mechanisms that link the oncogenic epithelial-mesenchymal transition to suppression of anoikis. J Cell Sci, 2013, 126(Pt 1):21-29.
20.	Chaabane W, User SD, El-Gazzah M, et al. Autophagy, apoptosis, mitoptosis and necrosis:interdependence between those pathways and effects on cancer. Arch Immunol Ther Exp (Warsz), 2013, 61(1):43-58.
21.	Kim YJ, Choi WI, Jeon BN, et al. Stereospecific effects of ginsenoside 20-Rg3 inhibits TGF-beta1-induced epithelial-mesenchymal transition and suppresses lung cancer migration, invasion and anoikis resistance. Toxicology, 2014, 322:23-33.
22.	Sakai H, Ohuchida K, Mizumoto K, et al. Inhibition of p600 expression suppresses both invasiveness and anoikis resistance of gastric cancer. Ann Surg Oncol, 2011, 18(7):2057-2065.
23.	Kumar S, Park SH, Cieply B, et al. A pathway for the control of anoikis sensitivity by E-cadherin and epithelial-to-mesenchymal transition. Mol Cell Biol, 2011, 31(19):4036-4051.
24.	Medici D, Nawshad A. TypeⅠcollagen promotes epithelial-mesenchymal transition through ILK-dependent activation of NF-kappaB and LEF-1. Matrix Biol, 2010, 29(3):161-165.
25.	Cicchini C, Laudadio I, Citarella F, et al. TGFbeta-induced EMT requires focal adhesion kinase (FAK) signaling. Exp Cell Res, 2008, 314(1):143-152.
26.	Serrano I, McDonald PC, Lock FE, et al. Role of the integrin-linked kinase (ILK)/Rictor complex in TGFbeta-1-induced epithelialmesenchymal transition (EMT). Oncogene, 2013, 32(1):50-60.
27.	Luo BH, Xiong F, Wang JP, et al. Epidermal growth factor-like domain-containing protein 7(EGFL7) enhances EGF receptor-AKT signaling, epithelial-mesenchymal transition, and metastasis of gastric cancer cells. PloS One, 2014, 9(6):e99922.
28.	Zhang L, Wang X, Chen P. MiR-204 down regulates SIRT1 and reverts SIRT1-induced epithelial-mesenchymal transition, anoikis resistance and invasion in gastric cancer cells. BMC Cancer, 2013, 13:290.
29.	Miles FL, Pruitt FL, van Golen KL, et al. Stepping out of the flow:capillary extravasation in cancer metastasis. Clin Exp Metastasis, 2008, 25(4):305-324.
30.	Drake JM, Strohbehn G, Bair TB, et al. ZEB1 enhances transendothelial migration and represses the epithelial phenotype of prostate cancer cells. Mol Biol Cell, 2009, 20(8):2207-2217.
31.	Ota I, Li XY, Hu Y, et al. Induction of a MT1-MMP and MT2-MMP-dependent basement membrane transmigration program in cancer cells by Snail1. Proc Natl Acad Sci U S A, 2009, 106(48):20318-20323.
32.	Lin BR, Chang CC, Chen LR, et al. Cysteine-rich 61(CCN1) enhances chemotactic migration, transendothelial cell migration, and intravasation by concomitantly up-regulating chemokine receptor 1 and 2. Mol Cancer Res, 2007, 5(11):1111-1123.
33.	Sarela AI, Turnbull AD, Coit DG, et al. Accurate lymph node staging is of greater prognostic importance than subclassification of the T2 category for gastric adenocarcinoma. Ann Surg Oncol, 2003, 10(7):783-791.
34.	Li H, Xu L, Li C, et al. Ubiquitin ligase Cbl-b represses IGF-I-induced epithelial mesenchymal transition via ZEB2 and microRNA-200c regulation in gastric cancer cells. Mol Cancer, 2014, 13:136.
35.	Wang ZS, Shen Y, Li X, et al. Significance and prognostic value of Gli-1 and Snail/E-cadherin expression in progressive gastric cancer. Tumour Biol, 2014, 35(2):1357-1363.
36.	Zhao L, Li W, Zang W, et al. JMJD2B promotes epithelial-mesenchymal transition by cooperating with beta-catenin and enhances gastric cancer metastasis. Clin Cancer Res, 2013, 19(23):6419-6429.
37.	Kurashige J, Kamohara H, Watanabe M, et al. MicroRNA-200b regulates cell proliferation, invasion, and migration by directly targeting ZEB2 in gastric carcinoma. Ann Surg Oncol, 2012, 19 Suppl 3:S656-S664.
38.	Wang SH, Li X, Zhou LS, et al. microRNA-148a suppresses human gastric cancer cell metastasis by reversing epithelial-to-mesenchymal transition. Tumour Biol, 2013, 34(6):3705-3712.
39.	Williams SC. Circulating tumor cells. Proc Natl Acad Sci U S A, 2013, 110(13):4861.
40.	Tseng JY, Yang CY, Liang SC, et al. Interleukin-17A modulates circulating tumor cells in tumor draining vein of colorectal cancers and affects metastases. Clin Cancer Res, 2014, 20(11):2885-2897.
41.	Kallergi G, Papadaki MA, Politaki E, et al. Epithelial to mesenchymal transition markers expressed in circulating tumour cells of early and metastatic breast cancer patients. Breast Cancer Res, 2011, 13(3):R59.
42.	Raimondi C, Gradilone A, Naso G, et al. Epithelial-mesenchymal transition and stemness features in circulating tumor cells from breast cancer patients. Breast Cancer Res Treat, 2011, 130(2):449-455.
43.	Yu M, Bardia A, Wittner BS, et al. Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science, 2013, 339(6119):580-584.
44.	Tsai JH, Donaher JL, Murphy DA, et al. Spatiotemporal regulation of epithelial-mesenchymal transition is essential for squamous cell carcinoma metastasis. Cancer Cell, 2012, 22(6):725-736.
45.	Labelle M, Begum S, Hynes RO. Direct signaling between platelets and cancer cells induces an epithelial-mesenchymal-like transition and promotes metastasis. Cancer Cell, 2011, 20(5):576-590.
46.	Li Y, Zhang X, Ge S, et al. Clinical significance of phenotyping and karyotyping of circulating tumor cells in patients with advanced gastric cancer. Oncotarget, 2014, 5(16):6594-6602.
47.	Li M, Zhang B, Zhang Z, et al. Stem cell-like circulating tumor cells indicate poor prognosis in gastric cancer. Biomed Res Int, 2014, 2014:981261.
48.	Mendoza A, Hong SH, Osborne T, et al. Modeling metastasis biology and therapy in real time in the mouse lung. J Clin Invest, 2010, 120(8):2979-2988.
49.	Stoletov K, Kato H, Zardouzian E, et al. Visualizing extravasation dynamics of metastatic tumor cells. J Cell Sci, 2010, 123(Pt 13):2332-2341.
50.	Vega S, Morales AV, Ocana OH, et al. Snail blocks the cell cycle and confers resistance to cell death. Genes Dev, 2004, 18(10):1131-1143.
51.	Gao D, Joshi N, Choi H, et al. Myeloid progenitor cells in the premetastatic lung promote metastases by inducing mesenchymal to epithelial transition. Cancer Res, 2012, 72(6):1384-1394.
52.	Siemens H, Jackstadt R, Hunten S, et al. miR-34 and SNAIL form a double-negative feedback loop to regulate epithelial-mesenchymal transitions. Cell Cycle, 2011, 10(24):4256-4271.
53.	Kanzawa M, Semba S, Hara S, et al. WNT5A is a key regulator of the epithelial-mesenchymal transition and cancer stem cell properties in human gastric carcinoma cells. Pathobiology, 2013, 80(5):235-244.

1. Fock KM. Review article:the epidemiology and prevention of gastric cancer. Aliment Pharmacol Ther, 2014, 40(3):250-260.
2. Chen W, Zheng R, Zhang S, et al. Report of incidence and mortality in China cancer registries, 2009. Chin J Cancer Res, 2013, 25(1):10-21.
3. Tirino V, Desiderio V, Paino F, et al. Cancer stem cells in solid tumors:an overview and new approaches for their isolation and characterization. FASEB J, 2013, 27(1):13-24.
4. Tsai JH, Yang J. Epithelial-mesenchymal plasticity in carcinoma metastasis. Genes Dev, 2013, 27(20):2192-2206.
5. Lamouille S, Xu J, Derynck R. Molecular mechanisms of epithelialmesenchymal transition. Nat Rev Mol Cell Biol, 2014, 15(3):178-196.
6. Huang RY, Guilford P, Thiery JP. Early events in cell adhesion and polarity during epithelial-mesenchymal transition. J Cell Sci, 2012, 125(Pt 19):4417-4422.
7. Bax NA, Pijnappels DA, van Oorschot AA, et al. Epithelial-tomesenchymal transformation alters electrical conductivity of human epicardial cells. J Cell Mol Med, 2011, 15(12):2675-2683.
8. Jung H, Jun KH, Jung JH, et al. The expression of claudin-1, claudin-2, claudin-3, and claudin-4 in gastric cancer tissue. J Surg Res, 2011, 167(2):e185-e191.
9. Masuda R, Semba S, Mizuuchi E, et al. Negative regulation of the tight junction protein tricellulin by snail-induced epithelialmesenchymal transition in gastric carcinoma cells. Pathobiology, 2010, 77(2):106-113.
10. Katoh M. Epithelial-mesenchymal transition in gastric cancer (Review). Int J Oncol, 2005, 27(6):1677-1683.
11. Berx G, van Roy F. Involvement of members of the cadherin superfamily in cancer. Cold Spring Harb Perspect Biol, 2009, 1(6):a003129.
12. Guilford P, Hopkins J, Harraway J, et al. E-cadherin germline mutations in familial gastric cancer. Nature, 1998, 392(6674):402-405.
13. Rosivatz E, Becker I, Specht K, et al. Differential expression of the epithelial-mesenchymal transition regulators snail, SIP1, and twist in gastric cancer. Am J Pathol, 2002, 161(5):1881-1891.
14. Yoo YA, Kang MH, Lee HJ, et al. Sonic hedgehog pathway promotes metastasis and lymphangiogenesis via activation of Akt, EMT, and MMP-9 pathway in gastric cancer. Cancer Res, 2011, 71(22):7061-7070.
15. Fanelli MF, Chinen LT, Begnami MD, et al. The influence of transforming growth factor-alpha, cyclooxygenase-2, matrix metalloproteinase (MMP)-7, MMP-9 and CXCR4 proteins involved in epithelial-mesenchymal transition on overall survival of patients with gastric cancer. Histopathology, 2012, 61(2):153-161.
16. Eckert MA, Lwin TM, Chang AT, et al. Twist1-induced invadopodia formation promotes tumor metastasis. Cancer Cell, 2011, 19(3):372-386.
17. Murphy DA, Courtneidge SA. The 'ins' and 'outs' of podosomes and invadopodia:characteristics, formation and function. Nat Rev Mol Cell Biol, 2011, 12(7):413-426.
18. de Paula CA, Coulson-Thomas VJ, Ferreira JG, et al. Enterolobium contortisiliquum trypsin inhibitor (EcTI), a plant proteinase inhibitor, decreases in vitro cell adhesion and invasion by inhibition of Src protein-focal adhesion kinase (FAK) signaling pathways. J Biol Chem, 2012, 287(1):170-182.
19. Frisch SM, Schaller M, Cieply B. Mechanisms that link the oncogenic epithelial-mesenchymal transition to suppression of anoikis. J Cell Sci, 2013, 126(Pt 1):21-29.
20. Chaabane W, User SD, El-Gazzah M, et al. Autophagy, apoptosis, mitoptosis and necrosis:interdependence between those pathways and effects on cancer. Arch Immunol Ther Exp (Warsz), 2013, 61(1):43-58.
21. Kim YJ, Choi WI, Jeon BN, et al. Stereospecific effects of ginsenoside 20-Rg3 inhibits TGF-beta1-induced epithelial-mesenchymal transition and suppresses lung cancer migration, invasion and anoikis resistance. Toxicology, 2014, 322:23-33.
22. Sakai H, Ohuchida K, Mizumoto K, et al. Inhibition of p600 expression suppresses both invasiveness and anoikis resistance of gastric cancer. Ann Surg Oncol, 2011, 18(7):2057-2065.
23. Kumar S, Park SH, Cieply B, et al. A pathway for the control of anoikis sensitivity by E-cadherin and epithelial-to-mesenchymal transition. Mol Cell Biol, 2011, 31(19):4036-4051.
24. Medici D, Nawshad A. TypeⅠcollagen promotes epithelial-mesenchymal transition through ILK-dependent activation of NF-kappaB and LEF-1. Matrix Biol, 2010, 29(3):161-165.
25. Cicchini C, Laudadio I, Citarella F, et al. TGFbeta-induced EMT requires focal adhesion kinase (FAK) signaling. Exp Cell Res, 2008, 314(1):143-152.
26. Serrano I, McDonald PC, Lock FE, et al. Role of the integrin-linked kinase (ILK)/Rictor complex in TGFbeta-1-induced epithelialmesenchymal transition (EMT). Oncogene, 2013, 32(1):50-60.
27. Luo BH, Xiong F, Wang JP, et al. Epidermal growth factor-like domain-containing protein 7(EGFL7) enhances EGF receptor-AKT signaling, epithelial-mesenchymal transition, and metastasis of gastric cancer cells. PloS One, 2014, 9(6):e99922.
28. Zhang L, Wang X, Chen P. MiR-204 down regulates SIRT1 and reverts SIRT1-induced epithelial-mesenchymal transition, anoikis resistance and invasion in gastric cancer cells. BMC Cancer, 2013, 13:290.
29. Miles FL, Pruitt FL, van Golen KL, et al. Stepping out of the flow:capillary extravasation in cancer metastasis. Clin Exp Metastasis, 2008, 25(4):305-324.
30. Drake JM, Strohbehn G, Bair TB, et al. ZEB1 enhances transendothelial migration and represses the epithelial phenotype of prostate cancer cells. Mol Biol Cell, 2009, 20(8):2207-2217.
31. Ota I, Li XY, Hu Y, et al. Induction of a MT1-MMP and MT2-MMP-dependent basement membrane transmigration program in cancer cells by Snail1. Proc Natl Acad Sci U S A, 2009, 106(48):20318-20323.
32. Lin BR, Chang CC, Chen LR, et al. Cysteine-rich 61(CCN1) enhances chemotactic migration, transendothelial cell migration, and intravasation by concomitantly up-regulating chemokine receptor 1 and 2. Mol Cancer Res, 2007, 5(11):1111-1123.
33. Sarela AI, Turnbull AD, Coit DG, et al. Accurate lymph node staging is of greater prognostic importance than subclassification of the T2 category for gastric adenocarcinoma. Ann Surg Oncol, 2003, 10(7):783-791.
34. Li H, Xu L, Li C, et al. Ubiquitin ligase Cbl-b represses IGF-I-induced epithelial mesenchymal transition via ZEB2 and microRNA-200c regulation in gastric cancer cells. Mol Cancer, 2014, 13:136.
35. Wang ZS, Shen Y, Li X, et al. Significance and prognostic value of Gli-1 and Snail/E-cadherin expression in progressive gastric cancer. Tumour Biol, 2014, 35(2):1357-1363.
36. Zhao L, Li W, Zang W, et al. JMJD2B promotes epithelial-mesenchymal transition by cooperating with beta-catenin and enhances gastric cancer metastasis. Clin Cancer Res, 2013, 19(23):6419-6429.
37. Kurashige J, Kamohara H, Watanabe M, et al. MicroRNA-200b regulates cell proliferation, invasion, and migration by directly targeting ZEB2 in gastric carcinoma. Ann Surg Oncol, 2012, 19 Suppl 3:S656-S664.
38. Wang SH, Li X, Zhou LS, et al. microRNA-148a suppresses human gastric cancer cell metastasis by reversing epithelial-to-mesenchymal transition. Tumour Biol, 2013, 34(6):3705-3712.
39. Williams SC. Circulating tumor cells. Proc Natl Acad Sci U S A, 2013, 110(13):4861.
40. Tseng JY, Yang CY, Liang SC, et al. Interleukin-17A modulates circulating tumor cells in tumor draining vein of colorectal cancers and affects metastases. Clin Cancer Res, 2014, 20(11):2885-2897.
41. Kallergi G, Papadaki MA, Politaki E, et al. Epithelial to mesenchymal transition markers expressed in circulating tumour cells of early and metastatic breast cancer patients. Breast Cancer Res, 2011, 13(3):R59.
42. Raimondi C, Gradilone A, Naso G, et al. Epithelial-mesenchymal transition and stemness features in circulating tumor cells from breast cancer patients. Breast Cancer Res Treat, 2011, 130(2):449-455.
43. Yu M, Bardia A, Wittner BS, et al. Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science, 2013, 339(6119):580-584.
44. Tsai JH, Donaher JL, Murphy DA, et al. Spatiotemporal regulation of epithelial-mesenchymal transition is essential for squamous cell carcinoma metastasis. Cancer Cell, 2012, 22(6):725-736.
45. Labelle M, Begum S, Hynes RO. Direct signaling between platelets and cancer cells induces an epithelial-mesenchymal-like transition and promotes metastasis. Cancer Cell, 2011, 20(5):576-590.
46. Li Y, Zhang X, Ge S, et al. Clinical significance of phenotyping and karyotyping of circulating tumor cells in patients with advanced gastric cancer. Oncotarget, 2014, 5(16):6594-6602.
47. Li M, Zhang B, Zhang Z, et al. Stem cell-like circulating tumor cells indicate poor prognosis in gastric cancer. Biomed Res Int, 2014, 2014:981261.
48. Mendoza A, Hong SH, Osborne T, et al. Modeling metastasis biology and therapy in real time in the mouse lung. J Clin Invest, 2010, 120(8):2979-2988.
49. Stoletov K, Kato H, Zardouzian E, et al. Visualizing extravasation dynamics of metastatic tumor cells. J Cell Sci, 2010, 123(Pt 13):2332-2341.
50. Vega S, Morales AV, Ocana OH, et al. Snail blocks the cell cycle and confers resistance to cell death. Genes Dev, 2004, 18(10):1131-1143.
51. Gao D, Joshi N, Choi H, et al. Myeloid progenitor cells in the premetastatic lung promote metastases by inducing mesenchymal to epithelial transition. Cancer Res, 2012, 72(6):1384-1394.
52. Siemens H, Jackstadt R, Hunten S, et al. miR-34 and SNAIL form a double-negative feedback loop to regulate epithelial-mesenchymal transitions. Cell Cycle, 2011, 10(24):4256-4271.
53. Kanzawa M, Semba S, Hara S, et al. WNT5A is a key regulator of the epithelial-mesenchymal transition and cancer stem cell properties in human gastric carcinoma cells. Pathobiology, 2013, 80(5):235-244.

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Epithelial Mesenchymal Transition Effects and Regulation Mechanism in Astric Carcinoma Metastasis

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