Research Progress of Esophageal Cancer Stem Cells_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

ZHENGXin-lin , XIAXue-yang ,  ZHANGJian-hua , LiBin

Department of General Thoracic Surgery, Second Affiliated Hospital, Lanzhou University, Lanzhou 730030, P. R. China;

Corresponding author：

ZHANGJian-hua, Email: 972659434@qq.com

Keywords：

Esophageal cancer; Esophageal cancer stem cells; Separation; Indentification

DOI：

10.7507/1007-4848.20160217

Video：

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Abstract Full text Figures/Tables Video References Cited by

Esophageal carcinoma is a kind of common malignant tumor in the digestive tract. Although a lot of basic researches and clinical trials have been carried out all over the world, neither the diagnostic level nor the therapeutic effects have been obviously improved. The 5-year survival rate of esophageal cancer patient is still lower than that of other malignant tumors. Up to now, some frontier researches consider that the reason of the esophageal carcinoma being difficult to cure is related to the stem cells in it. Elimination or suppression of these stem cells may bring new hope for the treatment of esophageal cancer. This article generally introduces the specific markers, separation and indentification methods about the esophageal cancer stem cell. The targeted therapy is also mentioned.

Citation： ZHENGXin-lin, XIAXue-yang, ZHANGJian-hua, LiBin. Research Progress of Esophageal Cancer Stem Cells. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2016, 23(9): 907-911. doi: 10.7507/1007-4848.20160217 Copy

1.	Chen WQ, Zheng RS, Zhang SW, et al. Esophageal cancer incidence and mortality in China, 2010. Thorac Cancer, 2014, 5(4):343-348.
2.	Makino S. The role of tumor stemcells in regrowth of the tumor following drastic applications. Acta Unio Int Contra Cancrum, 1959, 15(Suppl1):196-198.
3.	Driessens G, Beck B, Caauwe A, et al. Defining the mode of tumour growth by clonal analysis. Nature, 2012, 488(7412):527-530.
4.	Ogawa K, Yoshioka Y, Isohashi F, et al. Radiotherapy targetting cancer stem cells:current views and future perspecti ves. Anticancer Res, 2013, 33(3):747-754.
5.	Sachlos E, Risueno RM, Laronde S, et al. Identification of drugs including a dopamine receptor antagonist that selectively target cancer shem cells. Cell, 2012, 149(6):1284-1297.
6.	Schepers AG, Snippert HJ, Stange DE, et al. Lineage tracing reveals Lgr5+ stem cell activity in mouse intestinal adeNomas. Science, 2012, 337(6095):730-735.
7.	Chen J, Li Y, Yu TS, et al. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature, 2012, 488(7412):522-526.
8.	Yang YM, Chang JW. Current status and issue in cancer stem cell study. Cancer Invest, 2008, 26(7):741-755.
9.	Okumura T, Shimada Y, Imamura M, et al. Neurotrophin receptor p75(NTR) characterizes human esophageal keratinceyte stem cells in vitro. Oneogene, 2003, 22(26):4017-4026.
10.	Huang SD, Yuan Y, Liu XH, et al. Self-renewal and chemotherapy resistance of side of P75NTR positive cells in esophageal squamous cell carcinomas. BMC Cancer, 2009, 9(9):9-17.
11.	张丽荣, 郭长青, 李印, 等.侵袭性及非侵袭性KYSE150细胞的体外分离及P75NTR的表达.郑州大学学报(医学版), 2008, 43(4):631-633.
12.	孙志刚, 黄盛东, 张宝仁, 等.应用P75NTR分选食管肿瘤干细胞并鉴定其生物学特性.第二军医大学学报, 2009, 30(5):480-486.
13.	Shigeishi H, Biddle A, Gammon L, et al. Maintenance of stem cell self renewal in head and neck cancers requires action of GSK3β by CD44 and RHAMM. Stem Cells, 2013, 31(10):2073-2083.
14.	Smit JK, Faber H, Niemantsverdriet M, et al. Prediction of response to radiotherapy in the treatment of esophageal cancer using stem cell markers. Radiother Oncol, 2013, 107(3):434-441.
15.	Zhao JS, Li WJ, Ge D, et al. Tumor initiating cells in esophageal squamous cell carcinomas express high levels of CD44. PLoS One, 2011, 6(6):e21419.
16.	汪建林, 孙志强, 于静萍, 等.食管癌细胞株中肿瘤干细胞样细胞的分离培养及生物鉴定.南京大学学报(自然科学版), 2013, 33(10):1362-1367.
17.	徐兵, 李伟新, 张利.干细胞转录因子Oct4在食管鳞癌中表达的研究.医学动物防治, 2014, 30(3):242-245.
18.	赵生霞, 黄燕燕, 慕晓玲.食管癌Eca109单克隆细胞株的干细胞特性研究.石河子大学学报(医学版), 2013, 31(2):197-201.
19.	黄燕燕, 赵生霞, 李秋霞, 等.人食管鳞癌Eca109细胞株中肿瘤干细胞的分离鉴定.石河子大学学报(医学版), 2014, 32(3):335-339.
20.	He W, Li K, Wang F, et al. Expression of OCT4 in human esophageal squamous cell carcinoma is significantly associated with poorer prognosis. Word J Gastroenterol, 2012, 18(7):712-719.
21.	Zhou X, Huang GR, Hu P. Over-expression of Oct4 in human esophageal squamous cell carcinoma. Mol Cells, 2011, 32(1):39-45.
22.	Rossi DJ, Jamieson CH, Weissman IL. Stem cells and the path-ways to aging and cancer. Cell, 2008, 132(4):681-696.
23.	Silva J, Garcia V, Garcia JM, et al. Circulating Bim-l mRNA as a possible prognostic factor for advanced breast cancer patients. Breast Cancer Res, 2007, 9(4):R55.
24.	Liu JH, Song LB, Zhang X, et al. Bmi-l expression predicts prognosis for patients with gastric carcinoma. J Surg Oncol, 2008, 97(3):267-272.
25.	Wang G, Liu L, Sharma S, et al. Bmi-l confers adaptive radioresistance to KYSE-50R esophaeal carcinoma cells. Biochem Biophys Res Commun, 2012, 425(2):309-314.
26.	Huang DZ, Gao Q, Guo L, et al. Isolaion and identification of cancer stem-like cells in esophageal carcinoma cell lines. Stem Cells Dev, 2009, 18(3):465-473.
27.	于茜颖. miR-203调控食管癌干细胞自我更新及食管癌相关基因ECRC1转录调控的研究.北京:北京协和医学院, 2010.博士学位论文.
28.	叶仕新, 曾志勇, 黄盛东, 等. p75NTR阳性人食管鳞癌细胞的干细胞特性研究.山东医药, 2012, 52(7):41-43.
29.	Zhao Y, Bao Q, Schwarz B, et al. Stem cell like side populations in esophagealcancer:a source of chemotherapy resistence and metastases. Stem Cells Dev, 2014, 23(2):180-192.
30.	李步强, 慕晓玲.食管肿瘤干细胞的研究进展.中国现代医药杂志, 2011, 13(3):124-125.
31.	Wang JL, Yu JP, Sun ZQ, et al. Radiobiological characteristics of cancer stem cells from esophageal cancer cell lines. World J Gastroenterol, 2014, 28(48):18296-18305.
32.	Li JC, Liu D, Yang Y, et al. Growth clonability and radiation resistance of esopheal carcinoma-derived stem-like cells. Asian Pac J Cancer Prev, 2013, 14(8):4891-4896.
33.	Zhang X, Komaki R, Wang L, et al. Treatment of radioresistant stem-like esophageal cancer cells by an apoptotic gene-armed, telomerase-specific oncolytic adenovirus. Clin Cancer Res, 2008, 14(9):2813-2823.
34.	Che SM, Zhang XZ, Liu XL, et al. The radiosensitization effect of NS398 on esophaeal cancer stem cell-like radioresistant cells. Dis Esophagus, 2011, 24(4):265-273.
35.	许健.食管癌干细胞的分选与鉴定.石河子:石河子大学, 2011.
36.	Wong R, Malthaner R. Combined chemotherapy and radiotherapy (without surgery) compared with radiotherapy alone in localized caicinoma of the esophague. Cochrance Database Syst Rev, 2010, (1):CD002092.
37.	Guzman ML, Rossi RM, Karnischky L, et al. The sesquiterpene lactone parthenolide induces apoptosis of human acute myelogenous leukemia stem and progenitor cells. Blood, 2005, 105(11):4163-4169.
38.	Ulla M, Cavadas D, Muñoz I, et al. Esophageal cancer:pneumo-64-MDCT. Abdom Imaging, 2010, 35(4):383-389.
39.	Jensen AD, Grehn C, Nikoghosyan A, et al. Catch me if you can use the image guidance in the radiotherapy of an unusual case of esophageal cancer. Srahlenther Onkol, 2009, 185(7):469-473.
40.	李珂, 龙辉, 王洁莲, 等.钼对人食管癌细胞ECA-109的化疗增敏作用及对食管癌干细胞P75NTR的影响.世界华人杂志, 2012, 20(11):959-963.
41.	Huang JX, Chen WC, Lin M, et al. Clinicopathological significance of cyclooxygenase-2 and cell cycle-regulatory proteins expression in patients with esophageal squamous cell carcinoma. Dis Esophagus, 2011, 15(10):1442-2050.
42.	Yoon MS, Nam TK, Lee JS, et al. VEGF as a predictor for response to definitive chemoradiotherapy and COX-2 as a prognosticator for survival in esophageal squamous cell carcinoma. J Korean Med Sci, 2011, 26(4):513-520.
43.	朱兆峰, 卢鑫, 肖宝荣, 等. COX-2和VEGF在食管癌中的表达及其与放射敏感性的关系.临床肿瘤学杂志, 2011, 16(1):27-30.
44.	龙辉, 李欢, 王洁莲, 等. NS-398对人食管癌细胞放射增敏机制的研究.胃肠病学和肝病学杂志, 2011, 20(12):1102-1104.
45.	郑娇娇, 吴清明, 陈建华, 等. P162对食管癌细胞株Eca109的放射增敏作用及其对P75NTR表达的影响.中国病理生理杂志, 2013, 29(1):103-107.
46.	陈琦, 吴清明, 程静, 等.冬凌草甲素对食管癌干细胞放射增敏作用的研究.中国现代医学杂志, 2012, 22(29):57-60.
47.	Ma XY, Zheng RL, Meng XQ. The antitumor activity of clostridium difficile toxin A. Chinese Pharm acological Bulletin, 2003, 19(4):458-461.
48.	张建华, 宋铁牛, 李斌, 等.艰难梭菌A毒素对食管癌干细胞损伤的研究.中国现代医学杂志, 2013, 23(25):16-18.
49.	Mori Y, Ishiguro H, Kuwabara Y, et al. MicroRNA-21 induces cell proliferation and invasion in esophageal squamous cell carcinoma.Mol Med Report, 2009, 2(2):235-239.
50.	Huang S, Li XQ, Chen X, et al. Inhibition of microRNA-21 increases radiosensitivity of esophageal cancer cells through phosphatase and tensin homolog deleted on chromosome 10 activation. Dis Esophagus, 2013, 26(8):823-831.
51.	Guo GH, Chen SZ, Zhang J, et al. Antitumor activity of a fusion of esophageal carcinoma cells with dendritic cells derived from cord blood. Vaccine, 2005, 23(45):5225-5230.

1. Chen WQ, Zheng RS, Zhang SW, et al. Esophageal cancer incidence and mortality in China, 2010. Thorac Cancer, 2014, 5(4):343-348.
2. Makino S. The role of tumor stemcells in regrowth of the tumor following drastic applications. Acta Unio Int Contra Cancrum, 1959, 15(Suppl1):196-198.
3. Driessens G, Beck B, Caauwe A, et al. Defining the mode of tumour growth by clonal analysis. Nature, 2012, 488(7412):527-530.
4. Ogawa K, Yoshioka Y, Isohashi F, et al. Radiotherapy targetting cancer stem cells:current views and future perspecti ves. Anticancer Res, 2013, 33(3):747-754.
5. Sachlos E, Risueno RM, Laronde S, et al. Identification of drugs including a dopamine receptor antagonist that selectively target cancer shem cells. Cell, 2012, 149(6):1284-1297.
6. Schepers AG, Snippert HJ, Stange DE, et al. Lineage tracing reveals Lgr5+ stem cell activity in mouse intestinal adeNomas. Science, 2012, 337(6095):730-735.
7. Chen J, Li Y, Yu TS, et al. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature, 2012, 488(7412):522-526.
8. Yang YM, Chang JW. Current status and issue in cancer stem cell study. Cancer Invest, 2008, 26(7):741-755.
9. Okumura T, Shimada Y, Imamura M, et al. Neurotrophin receptor p75(NTR) characterizes human esophageal keratinceyte stem cells in vitro. Oneogene, 2003, 22(26):4017-4026.
10. Huang SD, Yuan Y, Liu XH, et al. Self-renewal and chemotherapy resistance of side of P75NTR positive cells in esophageal squamous cell carcinomas. BMC Cancer, 2009, 9(9):9-17.
11. 张丽荣, 郭长青, 李印, 等.侵袭性及非侵袭性KYSE150细胞的体外分离及P75NTR的表达.郑州大学学报(医学版), 2008, 43(4):631-633.
12. 孙志刚, 黄盛东, 张宝仁, 等.应用P75NTR分选食管肿瘤干细胞并鉴定其生物学特性.第二军医大学学报, 2009, 30(5):480-486.
13. Shigeishi H, Biddle A, Gammon L, et al. Maintenance of stem cell self renewal in head and neck cancers requires action of GSK3β by CD44 and RHAMM. Stem Cells, 2013, 31(10):2073-2083.
14. Smit JK, Faber H, Niemantsverdriet M, et al. Prediction of response to radiotherapy in the treatment of esophageal cancer using stem cell markers. Radiother Oncol, 2013, 107(3):434-441.
15. Zhao JS, Li WJ, Ge D, et al. Tumor initiating cells in esophageal squamous cell carcinomas express high levels of CD44. PLoS One, 2011, 6(6):e21419.
16. 汪建林, 孙志强, 于静萍, 等.食管癌细胞株中肿瘤干细胞样细胞的分离培养及生物鉴定.南京大学学报(自然科学版), 2013, 33(10):1362-1367.
17. 徐兵, 李伟新, 张利.干细胞转录因子Oct4在食管鳞癌中表达的研究.医学动物防治, 2014, 30(3):242-245.
18. 赵生霞, 黄燕燕, 慕晓玲.食管癌Eca109单克隆细胞株的干细胞特性研究.石河子大学学报(医学版), 2013, 31(2):197-201.
19. 黄燕燕, 赵生霞, 李秋霞, 等.人食管鳞癌Eca109细胞株中肿瘤干细胞的分离鉴定.石河子大学学报(医学版), 2014, 32(3):335-339.
20. He W, Li K, Wang F, et al. Expression of OCT4 in human esophageal squamous cell carcinoma is significantly associated with poorer prognosis. Word J Gastroenterol, 2012, 18(7):712-719.
21. Zhou X, Huang GR, Hu P. Over-expression of Oct4 in human esophageal squamous cell carcinoma. Mol Cells, 2011, 32(1):39-45.
22. Rossi DJ, Jamieson CH, Weissman IL. Stem cells and the path-ways to aging and cancer. Cell, 2008, 132(4):681-696.
23. Silva J, Garcia V, Garcia JM, et al. Circulating Bim-l mRNA as a possible prognostic factor for advanced breast cancer patients. Breast Cancer Res, 2007, 9(4):R55.
24. Liu JH, Song LB, Zhang X, et al. Bmi-l expression predicts prognosis for patients with gastric carcinoma. J Surg Oncol, 2008, 97(3):267-272.
25. Wang G, Liu L, Sharma S, et al. Bmi-l confers adaptive radioresistance to KYSE-50R esophaeal carcinoma cells. Biochem Biophys Res Commun, 2012, 425(2):309-314.
26. Huang DZ, Gao Q, Guo L, et al. Isolaion and identification of cancer stem-like cells in esophageal carcinoma cell lines. Stem Cells Dev, 2009, 18(3):465-473.
27. 于茜颖. miR-203调控食管癌干细胞自我更新及食管癌相关基因ECRC1转录调控的研究.北京:北京协和医学院, 2010.博士学位论文.
28. 叶仕新, 曾志勇, 黄盛东, 等. p75NTR阳性人食管鳞癌细胞的干细胞特性研究.山东医药, 2012, 52(7):41-43.
29. Zhao Y, Bao Q, Schwarz B, et al. Stem cell like side populations in esophagealcancer:a source of chemotherapy resistence and metastases. Stem Cells Dev, 2014, 23(2):180-192.
30. 李步强, 慕晓玲.食管肿瘤干细胞的研究进展.中国现代医药杂志, 2011, 13(3):124-125.
31. Wang JL, Yu JP, Sun ZQ, et al. Radiobiological characteristics of cancer stem cells from esophageal cancer cell lines. World J Gastroenterol, 2014, 28(48):18296-18305.
32. Li JC, Liu D, Yang Y, et al. Growth clonability and radiation resistance of esopheal carcinoma-derived stem-like cells. Asian Pac J Cancer Prev, 2013, 14(8):4891-4896.
33. Zhang X, Komaki R, Wang L, et al. Treatment of radioresistant stem-like esophageal cancer cells by an apoptotic gene-armed, telomerase-specific oncolytic adenovirus. Clin Cancer Res, 2008, 14(9):2813-2823.
34. Che SM, Zhang XZ, Liu XL, et al. The radiosensitization effect of NS398 on esophaeal cancer stem cell-like radioresistant cells. Dis Esophagus, 2011, 24(4):265-273.
35. 许健.食管癌干细胞的分选与鉴定.石河子:石河子大学, 2011.
36. Wong R, Malthaner R. Combined chemotherapy and radiotherapy (without surgery) compared with radiotherapy alone in localized caicinoma of the esophague. Cochrance Database Syst Rev, 2010, (1):CD002092.
37. Guzman ML, Rossi RM, Karnischky L, et al. The sesquiterpene lactone parthenolide induces apoptosis of human acute myelogenous leukemia stem and progenitor cells. Blood, 2005, 105(11):4163-4169.
38. Ulla M, Cavadas D, Muñoz I, et al. Esophageal cancer:pneumo-64-MDCT. Abdom Imaging, 2010, 35(4):383-389.
39. Jensen AD, Grehn C, Nikoghosyan A, et al. Catch me if you can use the image guidance in the radiotherapy of an unusual case of esophageal cancer. Srahlenther Onkol, 2009, 185(7):469-473.
40. 李珂, 龙辉, 王洁莲, 等.钼对人食管癌细胞ECA-109的化疗增敏作用及对食管癌干细胞P75NTR的影响.世界华人杂志, 2012, 20(11):959-963.
41. Huang JX, Chen WC, Lin M, et al. Clinicopathological significance of cyclooxygenase-2 and cell cycle-regulatory proteins expression in patients with esophageal squamous cell carcinoma. Dis Esophagus, 2011, 15(10):1442-2050.
42. Yoon MS, Nam TK, Lee JS, et al. VEGF as a predictor for response to definitive chemoradiotherapy and COX-2 as a prognosticator for survival in esophageal squamous cell carcinoma. J Korean Med Sci, 2011, 26(4):513-520.
43. 朱兆峰, 卢鑫, 肖宝荣, 等. COX-2和VEGF在食管癌中的表达及其与放射敏感性的关系.临床肿瘤学杂志, 2011, 16(1):27-30.
44. 龙辉, 李欢, 王洁莲, 等. NS-398对人食管癌细胞放射增敏机制的研究.胃肠病学和肝病学杂志, 2011, 20(12):1102-1104.
45. 郑娇娇, 吴清明, 陈建华, 等. P162对食管癌细胞株Eca109的放射增敏作用及其对P75NTR表达的影响.中国病理生理杂志, 2013, 29(1):103-107.
46. 陈琦, 吴清明, 程静, 等.冬凌草甲素对食管癌干细胞放射增敏作用的研究.中国现代医学杂志, 2012, 22(29):57-60.
47. Ma XY, Zheng RL, Meng XQ. The antitumor activity of clostridium difficile toxin A. Chinese Pharm acological Bulletin, 2003, 19(4):458-461.
48. 张建华, 宋铁牛, 李斌, 等.艰难梭菌A毒素对食管癌干细胞损伤的研究.中国现代医学杂志, 2013, 23(25):16-18.
49. Mori Y, Ishiguro H, Kuwabara Y, et al. MicroRNA-21 induces cell proliferation and invasion in esophageal squamous cell carcinoma.Mol Med Report, 2009, 2(2):235-239.
50. Huang S, Li XQ, Chen X, et al. Inhibition of microRNA-21 increases radiosensitivity of esophageal cancer cells through phosphatase and tensin homolog deleted on chromosome 10 activation. Dis Esophagus, 2013, 26(8):823-831.
51. Guo GH, Chen SZ, Zhang J, et al. Antitumor activity of a fusion of esophageal carcinoma cells with dendritic cells derived from cord blood. Vaccine, 2005, 23(45):5225-5230.

Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Research Progress of Esophageal Cancer Stem Cells

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