Promotion of Esophageal Squamous Cell Carcinoma Metastasis by GOLPH3 via Up-regulation of Epithelial-mesenchymal Transition_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

 WANGJian-hua ¹ , YUANLin-jing ² , ZHONGZhi-min ¹ , LIANGRong-xin ¹ , LIBo-hai ¹ , WENZhe-sheng ³

1. Cardiovascular Surgery Department, Second People's Hospital of Guangdong Province, Guangzhou 510317, P. R. China;
2. Department of Gynecology, Sun Yat-sen University Cancer Center, Guangzhou 510060, P. R. China;
3. Department of Chest, Sun Yat-sen University Cancer Center, Guangzhou 510060, P. R. China;

Corresponding author：

WANGJian-hua, Email: wangjh296@163.com

Keywords：

Esophageal carcinoma; GOLPH3; Epithelial-mesenchymal transition

DOI：

10.7507/1007-4848.20150171

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To investigate the role of GOLPH3 in esophageal squamous cell carcinoma (ESCC). Methods Wound healing assays, transwell invasion assays and 3D culture were carried out to analyze the cell migration and invasion ability of GOLPH3 overexpression and knockdown KYSE-140 cells. The relationship between GOLPH3 expression and CYR61, CD44 and Snail mRNA expression was further examined through qRT-PCR, to identify the mechanisms involved. Results GOLPH3-promoted ESCC cell migration and invasion. CYR61, CD44 and Snail mRNA expression levels were correlated with GOLPH3 protein expression level. Conclusion GOLPH3 overexpression promotes ESCC metastasis through epithelial-mesenchymal transition (EMT), and plays an oncogenesis role in ESCC.

Citation： WANGJian-hua, YUANLin-jing, ZHONGZhi-min, LIANGRong-xin, LIBo-hai, WENZhe-sheng. Promotion of Esophageal Squamous Cell Carcinoma Metastasis by GOLPH3 via Up-regulation of Epithelial-mesenchymal Transition. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2015, 22(7): 672-676. doi: 10.7507/1007-4848.20150171 Copy

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3.	曾红梅, 郑荣寿, 张思维, 等. 中国食管癌发病趋势分析和预测. 中华预防医学杂志, 2012, 46(7):593.
4.	方文涛, 陈文虎. 食管癌手术治疗原则和淋巴结清扫. 中国癌症杂志, 2011(7):522.
5.	赫捷, 邵康. 中国食管癌流行病学现状、诊疗现状及担任中华未来对策. 中国癌症杂志, 2011, 21(7):501.
6.	Mohamed A, El-Rayes B, Khuri FR, et al. Targeted therapies in metastatic esophageal cancer:Advances over the past decade.Crit Rev Oncol Hematol, 2014, 91(2):186.
7.	Wu CC, Taylor RS, Lane DR, et al.GMx33:a novel family of trans-Golgi proteins identified by proteomics.Traffic, 2000, 1(12):963.
8.	Dippold HC, Ng MM, Farber-Katz SE, et al. GOLPH3 bridges phosphatidylinositol-4-phosphate and actomyosin to stretch and shape the Golgi to promote budding. Cell, 2009, 139(2):337.
9.	Scott KL, Kabbarah O, Liang MC, et al. GOLPH3 modulates mTOR signalling and rapamycin sensitivity in cancer. Nature, 2009, 459(7250):1085.
10.	Wood CS, Schmitz KR, Bessman NJ, et al. PtdIns4P recognition by Vps74/GOLPH3 links PtdIns 4-kinase signaling to retrograde Golgi trafficking. J Cell Biol, 2009, 187(7):967.
11.	Scott KL, Chin L. Signaling from the Golgi:mechanisms and models for Golgi phosphoprotein 3-mediated oncogenesis. Clin Cancer Res, 2010, 16(8):2229.
12.	Bugarcic A, Zhe Y, Kerr MC, et al. Vps26A and Vps26B subunits define distinct retromer complexes.Traffic, 2011, 12(12):1759.
13.	Graham TR, Burd CG. Coordination of Golgi functions by phosphatidylinositol 4-kinases.Trends Cell Biol, 2011, 21(2):113.
14.	Taft MH, Behrmann E, Munske-Weidemann LC, et al. Functional characterization of human myosin-18A and its interaction with F-actin and GOLPH3. J Biol Chem, 2013, 288(42):30029.
15.	Li XY, Liu W, Chen SF, et al. Expression of the Golgi phosphoprotein-3 gene in human gliomas:a pilot study. J Neurooncol, 2011, 105(2):159.
16.	Hua X, Yu L, Pan W, et al. Increased expression of Golgi phosphoprotein-3 is associated with tumor aggressiveness and poor prognosis of prostate cancer.Diagn Pathol, 2012, 7:127.
17.	Li H, Guo L, Chen SW, et al. GOLPH3 overexpression correlates with tumor progression and poor prognosis in patients with clinically N0 oral tongue cancer.J Transl Med, 2012, 10:168.
18.	Sotgia F, Whitaker-Menezes D, Martinez-Outschoorn UE, et al. Mitochondria "fuel" breast cancer metabolism:fifteen markers of mitochondrial biogenesis label epithelial cancer cells, but are excluded from adjacent stromal cells. Cell Cycle, 2012, 11(23):4390.
19.	Hu BS, Hu H, Zhu CY, et al. Overexpression of GOLPH3 is associated with poor clinical outcome in gastric cancer. Tumour Biol, 2013, 34(1):515.
20.	Hu GS, Li YQ, Yang YM, et al. High expression of Golgi phosphoprotein-3 is associated with poor survival in patients with hepatocellular carcinoma.Tumour Biol, 2014, 35(9):8625-8632.
21.	Ma Y, Ren Y, Zhang X, et al. High GOLPH3 expression is associated with a more aggressive behavior of epithelial ovarian carcinoma. Virchows Arch, 2014, 464(4):443.
22.	Wang JH, Chen XT, Wen ZS, et al. High expression of GOLPH3 in esophageal squamous cell carcinoma correlates with poor prognosis.PLoS One, 2012, 7(10):e45622.
23.	Shimada Y, Imamura M, Wagata T, et al. Characterization of 21 newly established esophageal cancer cell lines. Cancer, 1992, 69(2):277.
24.	Tu L, Chen L, Banfield DK. A conserved N-terminal arginine-motif in GOLPH3-family proteins mediates binding to coatomer. Traffic, 2012, 13(11):1496.
25.	Zeng Z, Lin H, Zhao X,et al. Overexpression of GOLPH3 promotes proliferation and tumorigenicity in breast cancer via suppression of the FOXO1 transcription factor. Clin Cancer Res, 2012, 18(15):4059.
26.	Zhou J, Xu T, Qin R, et al. Overexpression of Golgi phosphoprotein-3 (GOLPH3) in glioblastoma multiforme is associated with worse prognosis. J Neurooncol, 2012, 110(2):195.
27.	Zhou X, Zhan W, Bian W, et al. GOLPH3 regulates the migration and invasion of glioma cells though RhoA.Biochem Biophys Res Commun, 2013, 433(3):338.
28.	Alemany-Ribes M, Semino CE. Bioengineering 3D environments for cancer models. Adv Drug Deliv Rev, 2014, 79-80:40-49.
29.	Lim SH, Becker TM, Chua W, et al. Circulating tumour cells and the epithelial mesenchymal transition in colorectal cancer. J Clin Pathol, 2014, 67(10):848-853.
30.	Diaz-Lopez A, Moreno-Bueno G, Cano A. Role of microRNA in epithelial to mesenchymal transition and metastasis and clinical perspectives. Cancer Manag Res, 2014, 6:205.
31.	Kim S, Lee JW.Membrane Proteins involved in epithelial-mesenchymal transition and tumor invasion:Studies on TMPRSS4 and TM4SF5.Genomics Inform, 2014, 12(1):12.
32.	Geng SQ, Alexandrou AT, Li JJ.Breast cancer stem cells:Multiple capacities in tumor metastasis. Cancer Lett, 2014, 349(1):1.
33.	Monnier Y, Farmer P, Bieler G, et al.CYR61 and alphaVbeta5 integrin cooperate to promote invasion and metastasis of tumors growing in preirradiated stroma.Cancer Res, 2008, 68(18):7323.
34.	Sun ZJ, Wang Y, Cai Z, et al. Involvement of Cyr61 in growth, migration, and metastasis of prostate cancer cells.Br J Cancer, 2008, 99(10):1656.
35.	Haque I, Mehta S, Majumder M, et al. Cyr61/CCN1 signaling is critical for epithelial-mesenchymal transition and stemness and promotes pancreatic carcinogenesis. Mol Cancer, 2011, 10:8.
36.	Kaufhold S, Bonavida B. Central role of Snail1 in the regulation of EMT and resistance in cancer:a target for therapeutic intervention. J Exp Clin Cancer Res, 2014, 33(1):62.
37.	Grass GD, Dai L, Qin Z, et al. CD147:Regulator of hyaluronan signaling in invasiveness and chemoresistance. Adv Cancer Res, 2014, 123:351.
38.	Kim Y, Kumar S. CD44-mediated adhesion to hyaluronic acid contributes to mechanosensing and invasive motility. Mol Cancer Res, 2014, 12(10):1416-1429.
39.	Takahashi H, Takizawa T, Matsubara S, et al. Extravillous trophoblast cell invasion is promoted by the CD44-hyaluronic acid interaction. Placenta, 2014, 35(3):163.
40.	Ouhtit A, Madani S, Gupta I, et al. TGF-beta2:a novel target ofCD44-Promoted breast cancer invasion. J Cancer, 2013, 4(7):566.
41.	Gudadze M, Kankava K, Mariamidze A, et al. Distribution of cancer stem cells in ductal invasive carcinoma of breast (review). Georgian Med News, 2013, 222:44.
42.	Sinha N, Mukhopadhyay S, Das DN, et al. Relevance of cancer initiating/stem cells in carcinogenesis and therapy resistance in oral cancer. Oral Oncol, 2013, 49(9):854.
43.	Lopez J, Valdez-Morales FJ, Benitez-Bribiesca L, et al. Normal and cancer stem cells of the human female reproductive system. Reprod Biol Endocrinol, 2013, 11:53.
44.	Xu L. Cancer stem cell in the progression and therapy of pancreatic cancer. Front Biosci (Landmark Ed), 2013, 18:795.

1. Jemal A, Bray F, Center MM, et al. Global cancer statistics. CA Cancer J Clin, 2011, 61(2):69.
2. 陈万青, 主编. 2013中国肿瘤登记年报. 北京:军事医学科学出版社. 2014.
3. 曾红梅, 郑荣寿, 张思维, 等. 中国食管癌发病趋势分析和预测. 中华预防医学杂志, 2012, 46(7):593.
4. 方文涛, 陈文虎. 食管癌手术治疗原则和淋巴结清扫. 中国癌症杂志, 2011(7):522.
5. 赫捷, 邵康. 中国食管癌流行病学现状、诊疗现状及担任中华未来对策. 中国癌症杂志, 2011, 21(7):501.
6. Mohamed A, El-Rayes B, Khuri FR, et al. Targeted therapies in metastatic esophageal cancer:Advances over the past decade.Crit Rev Oncol Hematol, 2014, 91(2):186.
7. Wu CC, Taylor RS, Lane DR, et al.GMx33:a novel family of trans-Golgi proteins identified by proteomics.Traffic, 2000, 1(12):963.
8. Dippold HC, Ng MM, Farber-Katz SE, et al. GOLPH3 bridges phosphatidylinositol-4-phosphate and actomyosin to stretch and shape the Golgi to promote budding. Cell, 2009, 139(2):337.
9. Scott KL, Kabbarah O, Liang MC, et al. GOLPH3 modulates mTOR signalling and rapamycin sensitivity in cancer. Nature, 2009, 459(7250):1085.
10. Wood CS, Schmitz KR, Bessman NJ, et al. PtdIns4P recognition by Vps74/GOLPH3 links PtdIns 4-kinase signaling to retrograde Golgi trafficking. J Cell Biol, 2009, 187(7):967.
11. Scott KL, Chin L. Signaling from the Golgi:mechanisms and models for Golgi phosphoprotein 3-mediated oncogenesis. Clin Cancer Res, 2010, 16(8):2229.
12. Bugarcic A, Zhe Y, Kerr MC, et al. Vps26A and Vps26B subunits define distinct retromer complexes.Traffic, 2011, 12(12):1759.
13. Graham TR, Burd CG. Coordination of Golgi functions by phosphatidylinositol 4-kinases.Trends Cell Biol, 2011, 21(2):113.
14. Taft MH, Behrmann E, Munske-Weidemann LC, et al. Functional characterization of human myosin-18A and its interaction with F-actin and GOLPH3. J Biol Chem, 2013, 288(42):30029.
15. Li XY, Liu W, Chen SF, et al. Expression of the Golgi phosphoprotein-3 gene in human gliomas:a pilot study. J Neurooncol, 2011, 105(2):159.
16. Hua X, Yu L, Pan W, et al. Increased expression of Golgi phosphoprotein-3 is associated with tumor aggressiveness and poor prognosis of prostate cancer.Diagn Pathol, 2012, 7:127.
17. Li H, Guo L, Chen SW, et al. GOLPH3 overexpression correlates with tumor progression and poor prognosis in patients with clinically N0 oral tongue cancer.J Transl Med, 2012, 10:168.
18. Sotgia F, Whitaker-Menezes D, Martinez-Outschoorn UE, et al. Mitochondria "fuel" breast cancer metabolism:fifteen markers of mitochondrial biogenesis label epithelial cancer cells, but are excluded from adjacent stromal cells. Cell Cycle, 2012, 11(23):4390.
19. Hu BS, Hu H, Zhu CY, et al. Overexpression of GOLPH3 is associated with poor clinical outcome in gastric cancer. Tumour Biol, 2013, 34(1):515.
20. Hu GS, Li YQ, Yang YM, et al. High expression of Golgi phosphoprotein-3 is associated with poor survival in patients with hepatocellular carcinoma.Tumour Biol, 2014, 35(9):8625-8632.
21. Ma Y, Ren Y, Zhang X, et al. High GOLPH3 expression is associated with a more aggressive behavior of epithelial ovarian carcinoma. Virchows Arch, 2014, 464(4):443.
22. Wang JH, Chen XT, Wen ZS, et al. High expression of GOLPH3 in esophageal squamous cell carcinoma correlates with poor prognosis.PLoS One, 2012, 7(10):e45622.
23. Shimada Y, Imamura M, Wagata T, et al. Characterization of 21 newly established esophageal cancer cell lines. Cancer, 1992, 69(2):277.
24. Tu L, Chen L, Banfield DK. A conserved N-terminal arginine-motif in GOLPH3-family proteins mediates binding to coatomer. Traffic, 2012, 13(11):1496.
25. Zeng Z, Lin H, Zhao X,et al. Overexpression of GOLPH3 promotes proliferation and tumorigenicity in breast cancer via suppression of the FOXO1 transcription factor. Clin Cancer Res, 2012, 18(15):4059.
26. Zhou J, Xu T, Qin R, et al. Overexpression of Golgi phosphoprotein-3 (GOLPH3) in glioblastoma multiforme is associated with worse prognosis. J Neurooncol, 2012, 110(2):195.
27. Zhou X, Zhan W, Bian W, et al. GOLPH3 regulates the migration and invasion of glioma cells though RhoA.Biochem Biophys Res Commun, 2013, 433(3):338.
28. Alemany-Ribes M, Semino CE. Bioengineering 3D environments for cancer models. Adv Drug Deliv Rev, 2014, 79-80:40-49.
29. Lim SH, Becker TM, Chua W, et al. Circulating tumour cells and the epithelial mesenchymal transition in colorectal cancer. J Clin Pathol, 2014, 67(10):848-853.
30. Diaz-Lopez A, Moreno-Bueno G, Cano A. Role of microRNA in epithelial to mesenchymal transition and metastasis and clinical perspectives. Cancer Manag Res, 2014, 6:205.
31. Kim S, Lee JW.Membrane Proteins involved in epithelial-mesenchymal transition and tumor invasion:Studies on TMPRSS4 and TM4SF5.Genomics Inform, 2014, 12(1):12.
32. Geng SQ, Alexandrou AT, Li JJ.Breast cancer stem cells:Multiple capacities in tumor metastasis. Cancer Lett, 2014, 349(1):1.
33. Monnier Y, Farmer P, Bieler G, et al.CYR61 and alphaVbeta5 integrin cooperate to promote invasion and metastasis of tumors growing in preirradiated stroma.Cancer Res, 2008, 68(18):7323.
34. Sun ZJ, Wang Y, Cai Z, et al. Involvement of Cyr61 in growth, migration, and metastasis of prostate cancer cells.Br J Cancer, 2008, 99(10):1656.
35. Haque I, Mehta S, Majumder M, et al. Cyr61/CCN1 signaling is critical for epithelial-mesenchymal transition and stemness and promotes pancreatic carcinogenesis. Mol Cancer, 2011, 10:8.
36. Kaufhold S, Bonavida B. Central role of Snail1 in the regulation of EMT and resistance in cancer:a target for therapeutic intervention. J Exp Clin Cancer Res, 2014, 33(1):62.
37. Grass GD, Dai L, Qin Z, et al. CD147:Regulator of hyaluronan signaling in invasiveness and chemoresistance. Adv Cancer Res, 2014, 123:351.
38. Kim Y, Kumar S. CD44-mediated adhesion to hyaluronic acid contributes to mechanosensing and invasive motility. Mol Cancer Res, 2014, 12(10):1416-1429.
39. Takahashi H, Takizawa T, Matsubara S, et al. Extravillous trophoblast cell invasion is promoted by the CD44-hyaluronic acid interaction. Placenta, 2014, 35(3):163.
40. Ouhtit A, Madani S, Gupta I, et al. TGF-beta2:a novel target ofCD44-Promoted breast cancer invasion. J Cancer, 2013, 4(7):566.
41. Gudadze M, Kankava K, Mariamidze A, et al. Distribution of cancer stem cells in ductal invasive carcinoma of breast (review). Georgian Med News, 2013, 222:44.
42. Sinha N, Mukhopadhyay S, Das DN, et al. Relevance of cancer initiating/stem cells in carcinogenesis and therapy resistance in oral cancer. Oral Oncol, 2013, 49(9):854.
43. Lopez J, Valdez-Morales FJ, Benitez-Bribiesca L, et al. Normal and cancer stem cells of the human female reproductive system. Reprod Biol Endocrinol, 2013, 11:53.
44. Xu L. Cancer stem cell in the progression and therapy of pancreatic cancer. Front Biosci (Landmark Ed), 2013, 18:795.

Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Promotion of Esophageal Squamous Cell Carcinoma Metastasis by GOLPH3 via Up-regulation of Epithelial-mesenchymal Transition

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