Prognostic and Clinical Value of CD44 and CD133 in Esophageal Cancer: A Systematic Review and Meta-analysis
Abstract
Despite the importance of CD44 and CD133 in various cancers, the clinicopathological and prognostic values of these biomarkers in esophageal cancer remain debated. Hence, in this study, we did a meta-analysis to explore the correlation between overexpression of these markers and some clinicopathological features and their influence on the survival of esophageal cancer patients. A search in PubMed and Web of Science (among all articles published up to January 16, 2018) was done using the following keywords: esophageal cancer, CD44, CD133, prominin-1, AC133. Suitable studies, that were selected based on the criteria listed in the Materials and Methods section, were chosen and hazard ratios with 95% confidence intervals were estimated if available. Heterogeneity and sensitivity were also analyzed. Furthermore, publication bias was assessed using funnel plots, Egger, and Begg tests. The study included 1346 patients from 13 related studies. The median rates of marker expressions by immunohistochemistry were 35.7% (30%-76.6%) from 9 studies for CD44 and 31.9% (21%–44.2%) from 5 studies for CD133. The accumulative 5-year overall survival rates of CD44-positive and CD133-positive were 1.59% (1.22-2.06) and 1.27% (0.93-1.73), respectively. Meta-analysis showed that CD44 expression had a significant correlation with 5-year overall survival. CD44 overexpression showed a correlation with some clinicopathological features such as lymph node metastasis, vascular invasion, and recurrence of the disease, while it was not the case for coexpression of CD44 and CD133. In conclusion, CD44 overexpression was associated with a 5-year overall survival rate and thus this biomarker can be a suitable prognostic tool in esophageal cancer.
1. Rassouli FB, Matin MM, Bahrami AR, Ghaffarzadegan K, Sisakhtnezhad S, Cheshomi H, et al. SOX2 expression in gastrointestinal cancers of Iranian patients. Int J Biol Markers 2015;30: 315–20.
2. Wang D, Plukker JTM, Coppes RP. Cancer stem cells with increased metastatic potential as a therapeutic target for esophageal cancer. Semin Cancer Biol 2017;44:60–6.
3. Arnold M, Laversanne M, Brown LM, Devesa SS, Bray F. Predicting the future burden of esophageal cancer by histological subtype: International trends in incidence up to 2030. Am J Gastroenterol 2017;112:1247–55.
4. Hang D, Dong HC, Ning T, Dong B, Hou DL, Xu WG. Prognostic value of the stem cell markers CD133 and ABCG2 expression in esophageal squamous cell carcinoma. Dis Esophagus 2012;25:638–44.
5. Rassouli FB, Matin MM, Bahrami AR, Ghaffarzadegan K, Cheshomi H, Lari S, et al. Evaluating stem and cancerous biomarkers in CD15+CD44+ KYSE30 cells. Tumor Biol 2013;34:2909–20.
6. Nozoe T, Kohnoe S, Ezaki T, Kabashima A, Maehara Y. Significance of immunohistochemical over-expression of CD44v6 as an indicator of malignant potential in esophageal squamous cell carcinoma. J Cancer Res Clin Oncol. 2004;130: 334–8.
7. Wang C, Xie J, Guo J, Manning HC, Gore JC, Guo N. Evaluation of CD44 and CD133 as cancer stem cell markers for colorectal cancer. Oncol Rep 2012; 28:1301–8.
8. Lu L, Wu M, Sun L, Li W, Fu W, Zhang X, et al. Clinicopathological and prognostic significance of cancer stem cell markers CD44 and CD133 in patients with gastric cancer: A comprehensive meta-analysis with 4729 patients involved. Medicine (Baltimore) 2016;95: e5163.
9. Awad SF, O’Flaherty M, Critchley J, Abu-Raddad LJ. Projecting the Burden of Type 2 Diabetes Mellitus in Qatar: Analytical Insights. In: Qatar Foundation Annual Research Conference Proceedings. HBKU Press Qatar 2018, p HBPD486.
10. Schizas D, Moris D, Kanavidis P, Michalinos A, SioulasIOULAS A, PavlakisAVLAKIS K, et al. The prognostic value of CD44 expression in epithelial–mesenchymal transition: Preliminary data from patients with gastric and esophageal cancer. In Vivo 2016;30:939–44.
11. Okamoto K, Ninomiya I, Ohbatake Y, Hirose A, Tsukada T, Nakanuma S, et al. Expression status of CD44 and CD133 as a prognostic marker in esophageal squamous cell carcinoma treated with neoadjuvant chemotherapy followed by radical esophagectomy. Oncol Rep 2016; 36:3333–42.
12. Zhao J-S, Li W, Ge D, Zhang P-J, Li J, Lu C-L, et al. Tumor initiating cells in esophageal squamous cell carcinomas express high levels of CD44. PLoS One 2011; 6:e21419.
13. Mizukami T, Kamachi H, Mitsuhashi T, Tsuruga Y, Hatanaka Y, Kamiyama T et al. Immunohistochemical analysis of cancer stem cell markers in pancreatic adenocarcinoma patients after neoadjuvant chemoradiotherapy. BMC Cancer 2014;14:687.
14. Zhao S, He JL, Qiu ZX, Chen NY, Luo Z, Chen BJ, et al. Prognostic value of CD44 variant exon 6 expression in non-small cell lung cancer: a meta-analysis. Asian Pac J Cancer Prev 2014; 15: 6761–6766.
15. Nosrati A, Naghshvar F, Khanari S. Cancer stem cell markers CD44, CD133 in primary gastric adenocarcinoma. Int J Mol Cell Med 2014;3:279.
16. Chen J, Zhou J, Lu J, Xiong H, Shi X, Gong L. Significance of CD44 expression in head and neck cancer: a systemic review and meta-analysis. BMC Cancer 2014;14:15.
17. Wen L, Chen XZ, Yang K, Chen ZX, Zhang B, Chen JP, et al. Prognostic value of cancer stem cell marker CD133 expression in gastric cancer: a systematic review. PLoS One 2013;8:e59154.
18. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, et al. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003;63:5821–8.
19. O’Brien CA, Pollett A, Gallinger S, Dick JE. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature. 2007;445:106–10.
20. Maitland NJ, Collins AT, Bryce S, Sarah M, Berry P, Hyde K, et al. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res 2005;65:591.
21. Yin S, Li J, Hu C, Chen X, Yao M, Yan M, et al. CD133 positive hepatocellular carcinoma cells possess high capacity for tumorigenicity. Int J Cancer 2007;120:1444–50.
22. Eramo A, Lotti F, Sette G, Pilozzi E, Biffoni M, Di Virgilio A, et al. Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ 2008;15:504–14.
23. Florek M, Haase M, Marzesco A-M, Freund D, Ehninger G, Huttner WB, et al. Prominin-1/CD133, a neural and hematopoietic stem cell marker, is expressed in adult human differentiated cells and certain types of kidney cancer. Cell Tissue Res 2005;319:15–26.
24. Ferrandina G, Bonanno G, Pierelli L, Perillo A, Procoli A, Mariotti A, et al. Expression of CD133-1 and CD133-2 in ovarian cancer. Int J Gynecol Cancer 2008;18:506–14.
25. Monzani E, Facchetti F, Galmozzi E, Corsini E, Benetti A, Cavazzin C et al. Melanoma contains CD133 and ABCG2 positive cells with enhanced tumourigenic potential. Eur J Cancer 2007;43:935–46.
26. Karbanová J, Lorico A, Bornhäuser M, Corbeil D, Fargeas CA. Prominin-1/CD133: Lipid raft association, detergent resistance, and immunodetection. Stem Cells Transl Med 2018;7:155–60.
27. Yamaguchi T, Okumura T, Hirano K, Watanabe T, Nagata T, Shimada Y, et al. p75 neurotrophin receptor expression is a characteristic of the mitotically quiescent cancer stem cell population present in esophageal squamous cell carcinoma. Int J Oncol 2016;48:1943–54.
28. Yang Z, Cui Y, Ni W, Kim S, Xuan Y. Gli1, a potential regulator of esophageal cancer stem cell, is identified as an independent adverse prognostic factor in esophageal squamous cell carcinoma. J Cancer Res Clin Oncol 2017;143:243–54.
29. Honing J, Pavlov K V, Meijer C, Smit JK, Boersma-van Ek W, Karrenbeld A, et al. Loss of CD44 and SOX2 expression is correlated with a poor prognosis in esophageal adenocarcinoma patients. Ann Surg Oncol 2014;21:657–64.
30. Turner J, Torres C, Wang H, Shahsafael A, Richards W, Sugarbaker D, et al. Preoperative chemoradiotherapy alters the expression and prognostic significance of adhesion molecules in Barrett’s-associated adenocarcinoma. Hum Pathol 2000; 31:347–53.
31. Gotoda T. Expression of CD44 variants and prognosis in oesophageal squamous cell carcinoma. Gut. 2000;46:14–9.
32. Lagorce-Pages, Paraf, Dubois, Belghiti, FLEjou. Expression of CD44 in premalignant and malignant Barrett’s oesophagus. Histopathology. 1998;32:7–14.
33. Okamoto H, Fujishima F, Nakamura Y, Zuguchi M, Ozawa Y, Takahashi Y, et al. Significance of CD133 expression in esophageal squamous cell carcinoma. World J Surg Oncol 2013;11:1.
34. Lu C, Xu F, Gu J, Yuan Y, Zhao G, Yu X, et al. Clinical and biological significance of stem-like CD133+ CXCR4+ cells in esophageal squamous cell carcinoma. J Thorac Cardiovasc Surg 2015;150:386–95.
35. Nakajima TE, Yoshida H, Okamoto N, Nagashima K, Taniguchi H, Yamada Y, et al. Nucleostemin and TWIST as predictive markers for recurrence after neoadjuvant chemotherapy for esophageal carcinoma. Cancer Sci 2012;103:233–8.
36. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials 1986;7:177–88.
37. Higgins JPT, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med 2002;21:1539–58.
38. Smith TC, Spiegelhalter DJ, Thomas A. Bayesian approaches to random-effects meta-analysis: a comparative study. Stat Med 1995;14:2685–99.
39. Batlle E, Clevers H. Cancer stem cells revisited. Nat Med 2017;23:1124.
40. Wang J, Zhang B, Meng J, Xiao G, Li X, Li G, et al. Analysis of risk factors for post‑operative complications and prognostic predictors of disease recurrence following definitive treatment of patients with esophageal cancer from two medical centers in Northwest China. Exp Ther Med 2017;14:2584–94.
41. Clevers H. The cancer stem cell: premises, promises and challenges. Nat Med 2011;17:313.
42. Okumura T, Kojima H, Yamaguchi T, Shimada Y. Clinical application of stem cell biology in esophageal cancer. In: Molecular Diagnosis and Targeting for Thoracic and Gastrointestinal Malignancy. Springer, 2018, pp 49–62.
43. Darlavoix T, Seelentag W, Yan P, Bachmann A, Bosman FT. Altered expression of CD44 and DKK1 in the progression of Barrett’s esophagus to esophageal adenocarcinoma. Virchows Arch 2009;454:629–37.
44. Minato T, Yamamoto Y, Seike J, Yoshida T, Yamai H, Takechi H et al. Aldehyde dehydrogenase 1 expression is associated with poor prognosis in patients with esophageal squamous cell carcinoma. Ann Surg Oncol 2013;20:209–17.
45. Liu L, Yin X, Ding X, Sun X, Gao S. Prognostic effects of the expression of Kruppel-like factor 4 and CD44 in patients with esophageal squamous carcinoma. Chinese J Dig 2018;38:528–34.
46. Okumura T, Yamaguchi T, Hirano K, Watanabe T, Nagata T, Shimada Y, et al. Circulating tumor cells detected by the expression of cancer stem cell marker CD90 and CD44 in patients with esophageal cancer. Int Surg 2017;1.
47. Shiozaki M, Ishiguro H, Kuwabara Y, Kimura M, Mitsui A, Naganawa Y, et al. Expression of CD44v6 is an independent prognostic factor for poor survival in patients with esophageal squamous cell carcinoma. Oncol Lett 2011;2:429–34.
48. Fujiwara Y, Yoshikawa R, Tsujie M, Kato H, Takeyama H, Kitani K, et al. CD44, a cancer stemness marker, to predict poor clinical outcome of esophageal cancer patients after neoadjuvant chemoradiotherapy. J Clin Oncol 2015; 15:15068.
49. Mokrowiecka A, Veits L, Falkeis C, Musial J, Kordek R, Lochowski M, et al. Expression profiles of cancer stem cell markers: CD133, CD44, Musashi-1 and EpCAM in the cardiac mucosa—Barrett’s esophagus—early esophageal adenocarcinoma—advanced esophageal adenocarcinoma sequence. Pathol Res Pract 2017;213:205–9.
50. Pang Y, Liu J, Li X, Zhang Y, Zhang B, Zhang J, et al. Nano Let-7b sensitization of eliminating esophageal cancer stem-like cells is dependent on blockade of Wnt activation of symmetric division. Int J Oncol 2017;51:1077–88.
51. Wang J, Huang S, Zhang L, Liu Z, Liang R, Jiang S, et al. Combined prognostic value of the cancer stem cell markers CD47 and CD133 in esophageal squamous cell carcinoma. Cancer Med 2019;8:1315–25.
52. Rocco A, Liguori E, Pirozzi G, Tirino V, Compare D, Franco R, et al. CD133 and CD44 cell surface markers do not identify cancer stem cells in primary human gastric tumors. J Cell Physiol 2012;227:2686–93.
53. Horst D, Kriegl L, Engel J, Kirchner T, Jung A. Prognostic significance of the cancer stem cell markers CD133, CD44, and CD166 in colorectal cancer. Cancer Invest. 2009;27:844–50.
54. Galizia G, Gemei M, Del Vecchio L, Zamboli A, Di Noto R, Mirabelli P, et al. Combined CD133/CD44 expression as a prognostic indicator of disease-free survival in patients with colorectal cancer. Arch Surg 2012;147:18–24.
55. Dittfeld C, Dietrich A, Peickert S, Hering S, Baumann M, Grade M, et al. CD133 expression is not selective for tumor-initiating or radioresistant cell populations in the CRC cell lines HCT-116. Radiother Oncol 2009; 92:353–61.
56. Choi D, Lee HW, Hur KY, Kim JJ, Park G-S, Jang S-H, et al. Cancer stem cell markers CD133 and CD24 correlate with invasiveness and differentiation in colorectal adenocarcinoma. World J Gastroenterol 2009;15:2258.
57. Takaishi S, Okumura T, Tu S, Wang SSW, Shibata W, Vigneshwaran R, et al. Identification of gastric cancer stem cells using the cell surface marker CD44. Stem Cells. 2009;27:1006–20.
58. Jiang Y, He Y, Li H, Li HN, Zhang L, Hu W, et al. Expressions of putative cancer stem cell markers ABCB1, ABCG2, and CD133 are correlated with the degree of differentiation of gastric cancer. Gastric Cancer 2012;15:440–50.
59. Jang BI, Li Y, Graham DY, Cen P. The role of CD44 in the pathogenesis, diagnosis, and therapy of gastric cancer. Gut Liver. 2011;5:397.
60. Mayer B, Jauch KW, Schildberg FW, Funke I, Günthert U, Figdor CG, et al. De-novo expression of CD44 and survival in gastric cancer. Lancet 1993;342:1019–22.
61. Ishimoto T, Oshima H, Oshima M, Kai K, Torii R, Masuko T, et al. CD44+ slow‐cycling tumor cell expansion is triggered by cooperative actions of Wnt and prostaglandin E2 in gastric tumorigenesis. Cancer Sci 2010;101:673–8.
62. Ishimoto T, Nagano O, Yae T, Tamada M, Motohara T, Oshima H, et al. CD44 variant regulates redox status in cancer cells by stabilizing the xCT subunit of system xc− and thereby promotes tumor growth. Cancer Cell 2011;19:387–400.
63. Zeilstra J, Joosten SPJ, Van Andel H, Tolg C, Berns A, Snoek M, et al. Stem cell CD44v isoforms promote intestinal cancer formation in Apc (min) mice downstream of Wnt signaling. Oncogene 2014;33:665.
64. Lau WM, Teng E, Chong HS, Lopez KAP, Tay AYL, Salto-Tellez M, et al. CD44v8-10 is a cancer-specific marker for gastric cancer stem cells. Cancer Res 2014;74:2630–41.
65. Lv L, Liu H-G, Dong S-Y, Yang F, Wang Q-X, Guo G-L, et al. Upregulation of CD44v6 contributes to acquired chemoresistance via the modulation of autophagy in colon cancer SW480 cells. Tumor Biol 2016;37:8811–24.
66. Chen W, Zhang X, Chu C, Cheung WL, Ng L, Lam S, et al. Identification of CD44+ cancer stem cells in human gastric cancer. Hepato-Gastroenterol 2013;60:949–54.
67. Ishigami S, Ueno S, Arigami T, Uchikado Y, Setoyama T, Arima H, et al. Prognostic impact of CD133 expression in gastric carcinoma. Anticancer Res 2010;30:2453–2457.
68. Hashimoto K, Aoyagi K, Isobe T, Kouhuji K, Shirouzu K. Expression of CD133 in the cytoplasm is associated with cancer progression and poor prognosis in gastric cancer. Gastric Cancer 2014;17:97–106.
69. Leng Z, Xia Q, Chen J, Li Y, Xu J, Zhao E, et al. Lgr5+ CD44+ EpCAM+ strictly defines cancer stem cells in human colorectal cancer. Cell Physiol Biochem 2018;46:860–72.
70. Lugli A, Iezzi G, Hostettler I, Muraro MG, Mele V, Tornillo L, et al. Prognostic impact of the expression of putative cancer stem cell markers CD133, CD166, CD44s, EpCAM, and ALDH1 in colorectal cancer. Br J Cancer 2010; 103: 382.
71. Jing F, Kim HJ, Kim CH, Kim YJ, Lee JH, Kim HR. Colon cancer stem cell markers CD44 and CD133 in patients with colorectal cancer and synchronous hepatic metastases. Int J Oncol 2015;46:1582–8.
72. Finke L, Terpe H-J, Zörb C, Haensch W, et al. Colorectal cancer prognosis and expression of exon-v6-containing CD44 proteins. Lancet 1995;345:583–4.
73. Yamao T, Matsumura Y, Shimada Y, Moriya Y, Sugihara KI, et al. Abnormal expression of CD44 variants in the exfoliated cells in the feces of patients with colorectal cancer. Gastroenterology. 1998;114:1196–1205.
74. Todaro M, Gaggianesi M, Catalano V, Benfante A, Iovino F, et al. CD44v6 is a marker of constitutive and reprogrammed cancer stem cells driving colon cancer metastasis. Cell Stem Cell 2014; 14: 342–356.
75. Huang R, Mo D, Wu J, et al. CD133 expression correlates with clinicopathologic features and poor prognosis of colorectal cancer patients: An updated meta-analysis of 37 studies. Medicine. 2018;97.
76. Horst D, Kriegl L, Engel J, Kirchner T, Jung A. CD133 expression is an independent prognostic marker for low survival in colorectal cancer. Br J Cancer 2008;99:1285.
77. Pradhan T, Padmanabhan K, Prasad M, Chandramohan K, Nair SA. Augmented CD133 expression in distal margin correlates with poor prognosis in colorectal cancer. J Cell Mol Med 2019;23:3984–94.
78. Munakata K, Uemura M, Tanaka S, Kawai K, Kitahara T, Miyo M, et al. Cancer stem-like properties in colorectal cancer cells with low proteasome activity. Clin Cancer Res 2016;22:5277–86.
79. Han S, Huang T, Wu X, Wang X, Liu S, Yang W, et al. Prognostic value of CD133 and SOX2 in advanced cancer. J Oncol 2019;2019:1–12.
80. Zhao Y, Peng J, Zhang E, Jiang N, Li J, Zhang Q, et al. CD133 expression may be useful as a prognostic indicator in colorectal cancer, a tool for optimizing therapy and supportive evidence for the cancer stem cell hypothesis: a meta-analysis. Oncotarget 2016;7:10023.
81. Li R, Dong H, Zhu J, Yi H, Liu S. Overexpression of CD133 confers poor prognosis in colorectal cancer: a systematic review and meta-analysis. Int J Clin Exp Med 2019;12:1492–1502.
2. Wang D, Plukker JTM, Coppes RP. Cancer stem cells with increased metastatic potential as a therapeutic target for esophageal cancer. Semin Cancer Biol 2017;44:60–6.
3. Arnold M, Laversanne M, Brown LM, Devesa SS, Bray F. Predicting the future burden of esophageal cancer by histological subtype: International trends in incidence up to 2030. Am J Gastroenterol 2017;112:1247–55.
4. Hang D, Dong HC, Ning T, Dong B, Hou DL, Xu WG. Prognostic value of the stem cell markers CD133 and ABCG2 expression in esophageal squamous cell carcinoma. Dis Esophagus 2012;25:638–44.
5. Rassouli FB, Matin MM, Bahrami AR, Ghaffarzadegan K, Cheshomi H, Lari S, et al. Evaluating stem and cancerous biomarkers in CD15+CD44+ KYSE30 cells. Tumor Biol 2013;34:2909–20.
6. Nozoe T, Kohnoe S, Ezaki T, Kabashima A, Maehara Y. Significance of immunohistochemical over-expression of CD44v6 as an indicator of malignant potential in esophageal squamous cell carcinoma. J Cancer Res Clin Oncol. 2004;130: 334–8.
7. Wang C, Xie J, Guo J, Manning HC, Gore JC, Guo N. Evaluation of CD44 and CD133 as cancer stem cell markers for colorectal cancer. Oncol Rep 2012; 28:1301–8.
8. Lu L, Wu M, Sun L, Li W, Fu W, Zhang X, et al. Clinicopathological and prognostic significance of cancer stem cell markers CD44 and CD133 in patients with gastric cancer: A comprehensive meta-analysis with 4729 patients involved. Medicine (Baltimore) 2016;95: e5163.
9. Awad SF, O’Flaherty M, Critchley J, Abu-Raddad LJ. Projecting the Burden of Type 2 Diabetes Mellitus in Qatar: Analytical Insights. In: Qatar Foundation Annual Research Conference Proceedings. HBKU Press Qatar 2018, p HBPD486.
10. Schizas D, Moris D, Kanavidis P, Michalinos A, SioulasIOULAS A, PavlakisAVLAKIS K, et al. The prognostic value of CD44 expression in epithelial–mesenchymal transition: Preliminary data from patients with gastric and esophageal cancer. In Vivo 2016;30:939–44.
11. Okamoto K, Ninomiya I, Ohbatake Y, Hirose A, Tsukada T, Nakanuma S, et al. Expression status of CD44 and CD133 as a prognostic marker in esophageal squamous cell carcinoma treated with neoadjuvant chemotherapy followed by radical esophagectomy. Oncol Rep 2016; 36:3333–42.
12. Zhao J-S, Li W, Ge D, Zhang P-J, Li J, Lu C-L, et al. Tumor initiating cells in esophageal squamous cell carcinomas express high levels of CD44. PLoS One 2011; 6:e21419.
13. Mizukami T, Kamachi H, Mitsuhashi T, Tsuruga Y, Hatanaka Y, Kamiyama T et al. Immunohistochemical analysis of cancer stem cell markers in pancreatic adenocarcinoma patients after neoadjuvant chemoradiotherapy. BMC Cancer 2014;14:687.
14. Zhao S, He JL, Qiu ZX, Chen NY, Luo Z, Chen BJ, et al. Prognostic value of CD44 variant exon 6 expression in non-small cell lung cancer: a meta-analysis. Asian Pac J Cancer Prev 2014; 15: 6761–6766.
15. Nosrati A, Naghshvar F, Khanari S. Cancer stem cell markers CD44, CD133 in primary gastric adenocarcinoma. Int J Mol Cell Med 2014;3:279.
16. Chen J, Zhou J, Lu J, Xiong H, Shi X, Gong L. Significance of CD44 expression in head and neck cancer: a systemic review and meta-analysis. BMC Cancer 2014;14:15.
17. Wen L, Chen XZ, Yang K, Chen ZX, Zhang B, Chen JP, et al. Prognostic value of cancer stem cell marker CD133 expression in gastric cancer: a systematic review. PLoS One 2013;8:e59154.
18. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, et al. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003;63:5821–8.
19. O’Brien CA, Pollett A, Gallinger S, Dick JE. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature. 2007;445:106–10.
20. Maitland NJ, Collins AT, Bryce S, Sarah M, Berry P, Hyde K, et al. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res 2005;65:591.
21. Yin S, Li J, Hu C, Chen X, Yao M, Yan M, et al. CD133 positive hepatocellular carcinoma cells possess high capacity for tumorigenicity. Int J Cancer 2007;120:1444–50.
22. Eramo A, Lotti F, Sette G, Pilozzi E, Biffoni M, Di Virgilio A, et al. Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ 2008;15:504–14.
23. Florek M, Haase M, Marzesco A-M, Freund D, Ehninger G, Huttner WB, et al. Prominin-1/CD133, a neural and hematopoietic stem cell marker, is expressed in adult human differentiated cells and certain types of kidney cancer. Cell Tissue Res 2005;319:15–26.
24. Ferrandina G, Bonanno G, Pierelli L, Perillo A, Procoli A, Mariotti A, et al. Expression of CD133-1 and CD133-2 in ovarian cancer. Int J Gynecol Cancer 2008;18:506–14.
25. Monzani E, Facchetti F, Galmozzi E, Corsini E, Benetti A, Cavazzin C et al. Melanoma contains CD133 and ABCG2 positive cells with enhanced tumourigenic potential. Eur J Cancer 2007;43:935–46.
26. Karbanová J, Lorico A, Bornhäuser M, Corbeil D, Fargeas CA. Prominin-1/CD133: Lipid raft association, detergent resistance, and immunodetection. Stem Cells Transl Med 2018;7:155–60.
27. Yamaguchi T, Okumura T, Hirano K, Watanabe T, Nagata T, Shimada Y, et al. p75 neurotrophin receptor expression is a characteristic of the mitotically quiescent cancer stem cell population present in esophageal squamous cell carcinoma. Int J Oncol 2016;48:1943–54.
28. Yang Z, Cui Y, Ni W, Kim S, Xuan Y. Gli1, a potential regulator of esophageal cancer stem cell, is identified as an independent adverse prognostic factor in esophageal squamous cell carcinoma. J Cancer Res Clin Oncol 2017;143:243–54.
29. Honing J, Pavlov K V, Meijer C, Smit JK, Boersma-van Ek W, Karrenbeld A, et al. Loss of CD44 and SOX2 expression is correlated with a poor prognosis in esophageal adenocarcinoma patients. Ann Surg Oncol 2014;21:657–64.
30. Turner J, Torres C, Wang H, Shahsafael A, Richards W, Sugarbaker D, et al. Preoperative chemoradiotherapy alters the expression and prognostic significance of adhesion molecules in Barrett’s-associated adenocarcinoma. Hum Pathol 2000; 31:347–53.
31. Gotoda T. Expression of CD44 variants and prognosis in oesophageal squamous cell carcinoma. Gut. 2000;46:14–9.
32. Lagorce-Pages, Paraf, Dubois, Belghiti, FLEjou. Expression of CD44 in premalignant and malignant Barrett’s oesophagus. Histopathology. 1998;32:7–14.
33. Okamoto H, Fujishima F, Nakamura Y, Zuguchi M, Ozawa Y, Takahashi Y, et al. Significance of CD133 expression in esophageal squamous cell carcinoma. World J Surg Oncol 2013;11:1.
34. Lu C, Xu F, Gu J, Yuan Y, Zhao G, Yu X, et al. Clinical and biological significance of stem-like CD133+ CXCR4+ cells in esophageal squamous cell carcinoma. J Thorac Cardiovasc Surg 2015;150:386–95.
35. Nakajima TE, Yoshida H, Okamoto N, Nagashima K, Taniguchi H, Yamada Y, et al. Nucleostemin and TWIST as predictive markers for recurrence after neoadjuvant chemotherapy for esophageal carcinoma. Cancer Sci 2012;103:233–8.
36. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials 1986;7:177–88.
37. Higgins JPT, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med 2002;21:1539–58.
38. Smith TC, Spiegelhalter DJ, Thomas A. Bayesian approaches to random-effects meta-analysis: a comparative study. Stat Med 1995;14:2685–99.
39. Batlle E, Clevers H. Cancer stem cells revisited. Nat Med 2017;23:1124.
40. Wang J, Zhang B, Meng J, Xiao G, Li X, Li G, et al. Analysis of risk factors for post‑operative complications and prognostic predictors of disease recurrence following definitive treatment of patients with esophageal cancer from two medical centers in Northwest China. Exp Ther Med 2017;14:2584–94.
41. Clevers H. The cancer stem cell: premises, promises and challenges. Nat Med 2011;17:313.
42. Okumura T, Kojima H, Yamaguchi T, Shimada Y. Clinical application of stem cell biology in esophageal cancer. In: Molecular Diagnosis and Targeting for Thoracic and Gastrointestinal Malignancy. Springer, 2018, pp 49–62.
43. Darlavoix T, Seelentag W, Yan P, Bachmann A, Bosman FT. Altered expression of CD44 and DKK1 in the progression of Barrett’s esophagus to esophageal adenocarcinoma. Virchows Arch 2009;454:629–37.
44. Minato T, Yamamoto Y, Seike J, Yoshida T, Yamai H, Takechi H et al. Aldehyde dehydrogenase 1 expression is associated with poor prognosis in patients with esophageal squamous cell carcinoma. Ann Surg Oncol 2013;20:209–17.
45. Liu L, Yin X, Ding X, Sun X, Gao S. Prognostic effects of the expression of Kruppel-like factor 4 and CD44 in patients with esophageal squamous carcinoma. Chinese J Dig 2018;38:528–34.
46. Okumura T, Yamaguchi T, Hirano K, Watanabe T, Nagata T, Shimada Y, et al. Circulating tumor cells detected by the expression of cancer stem cell marker CD90 and CD44 in patients with esophageal cancer. Int Surg 2017;1.
47. Shiozaki M, Ishiguro H, Kuwabara Y, Kimura M, Mitsui A, Naganawa Y, et al. Expression of CD44v6 is an independent prognostic factor for poor survival in patients with esophageal squamous cell carcinoma. Oncol Lett 2011;2:429–34.
48. Fujiwara Y, Yoshikawa R, Tsujie M, Kato H, Takeyama H, Kitani K, et al. CD44, a cancer stemness marker, to predict poor clinical outcome of esophageal cancer patients after neoadjuvant chemoradiotherapy. J Clin Oncol 2015; 15:15068.
49. Mokrowiecka A, Veits L, Falkeis C, Musial J, Kordek R, Lochowski M, et al. Expression profiles of cancer stem cell markers: CD133, CD44, Musashi-1 and EpCAM in the cardiac mucosa—Barrett’s esophagus—early esophageal adenocarcinoma—advanced esophageal adenocarcinoma sequence. Pathol Res Pract 2017;213:205–9.
50. Pang Y, Liu J, Li X, Zhang Y, Zhang B, Zhang J, et al. Nano Let-7b sensitization of eliminating esophageal cancer stem-like cells is dependent on blockade of Wnt activation of symmetric division. Int J Oncol 2017;51:1077–88.
51. Wang J, Huang S, Zhang L, Liu Z, Liang R, Jiang S, et al. Combined prognostic value of the cancer stem cell markers CD47 and CD133 in esophageal squamous cell carcinoma. Cancer Med 2019;8:1315–25.
52. Rocco A, Liguori E, Pirozzi G, Tirino V, Compare D, Franco R, et al. CD133 and CD44 cell surface markers do not identify cancer stem cells in primary human gastric tumors. J Cell Physiol 2012;227:2686–93.
53. Horst D, Kriegl L, Engel J, Kirchner T, Jung A. Prognostic significance of the cancer stem cell markers CD133, CD44, and CD166 in colorectal cancer. Cancer Invest. 2009;27:844–50.
54. Galizia G, Gemei M, Del Vecchio L, Zamboli A, Di Noto R, Mirabelli P, et al. Combined CD133/CD44 expression as a prognostic indicator of disease-free survival in patients with colorectal cancer. Arch Surg 2012;147:18–24.
55. Dittfeld C, Dietrich A, Peickert S, Hering S, Baumann M, Grade M, et al. CD133 expression is not selective for tumor-initiating or radioresistant cell populations in the CRC cell lines HCT-116. Radiother Oncol 2009; 92:353–61.
56. Choi D, Lee HW, Hur KY, Kim JJ, Park G-S, Jang S-H, et al. Cancer stem cell markers CD133 and CD24 correlate with invasiveness and differentiation in colorectal adenocarcinoma. World J Gastroenterol 2009;15:2258.
57. Takaishi S, Okumura T, Tu S, Wang SSW, Shibata W, Vigneshwaran R, et al. Identification of gastric cancer stem cells using the cell surface marker CD44. Stem Cells. 2009;27:1006–20.
58. Jiang Y, He Y, Li H, Li HN, Zhang L, Hu W, et al. Expressions of putative cancer stem cell markers ABCB1, ABCG2, and CD133 are correlated with the degree of differentiation of gastric cancer. Gastric Cancer 2012;15:440–50.
59. Jang BI, Li Y, Graham DY, Cen P. The role of CD44 in the pathogenesis, diagnosis, and therapy of gastric cancer. Gut Liver. 2011;5:397.
60. Mayer B, Jauch KW, Schildberg FW, Funke I, Günthert U, Figdor CG, et al. De-novo expression of CD44 and survival in gastric cancer. Lancet 1993;342:1019–22.
61. Ishimoto T, Oshima H, Oshima M, Kai K, Torii R, Masuko T, et al. CD44+ slow‐cycling tumor cell expansion is triggered by cooperative actions of Wnt and prostaglandin E2 in gastric tumorigenesis. Cancer Sci 2010;101:673–8.
62. Ishimoto T, Nagano O, Yae T, Tamada M, Motohara T, Oshima H, et al. CD44 variant regulates redox status in cancer cells by stabilizing the xCT subunit of system xc− and thereby promotes tumor growth. Cancer Cell 2011;19:387–400.
63. Zeilstra J, Joosten SPJ, Van Andel H, Tolg C, Berns A, Snoek M, et al. Stem cell CD44v isoforms promote intestinal cancer formation in Apc (min) mice downstream of Wnt signaling. Oncogene 2014;33:665.
64. Lau WM, Teng E, Chong HS, Lopez KAP, Tay AYL, Salto-Tellez M, et al. CD44v8-10 is a cancer-specific marker for gastric cancer stem cells. Cancer Res 2014;74:2630–41.
65. Lv L, Liu H-G, Dong S-Y, Yang F, Wang Q-X, Guo G-L, et al. Upregulation of CD44v6 contributes to acquired chemoresistance via the modulation of autophagy in colon cancer SW480 cells. Tumor Biol 2016;37:8811–24.
66. Chen W, Zhang X, Chu C, Cheung WL, Ng L, Lam S, et al. Identification of CD44+ cancer stem cells in human gastric cancer. Hepato-Gastroenterol 2013;60:949–54.
67. Ishigami S, Ueno S, Arigami T, Uchikado Y, Setoyama T, Arima H, et al. Prognostic impact of CD133 expression in gastric carcinoma. Anticancer Res 2010;30:2453–2457.
68. Hashimoto K, Aoyagi K, Isobe T, Kouhuji K, Shirouzu K. Expression of CD133 in the cytoplasm is associated with cancer progression and poor prognosis in gastric cancer. Gastric Cancer 2014;17:97–106.
69. Leng Z, Xia Q, Chen J, Li Y, Xu J, Zhao E, et al. Lgr5+ CD44+ EpCAM+ strictly defines cancer stem cells in human colorectal cancer. Cell Physiol Biochem 2018;46:860–72.
70. Lugli A, Iezzi G, Hostettler I, Muraro MG, Mele V, Tornillo L, et al. Prognostic impact of the expression of putative cancer stem cell markers CD133, CD166, CD44s, EpCAM, and ALDH1 in colorectal cancer. Br J Cancer 2010; 103: 382.
71. Jing F, Kim HJ, Kim CH, Kim YJ, Lee JH, Kim HR. Colon cancer stem cell markers CD44 and CD133 in patients with colorectal cancer and synchronous hepatic metastases. Int J Oncol 2015;46:1582–8.
72. Finke L, Terpe H-J, Zörb C, Haensch W, et al. Colorectal cancer prognosis and expression of exon-v6-containing CD44 proteins. Lancet 1995;345:583–4.
73. Yamao T, Matsumura Y, Shimada Y, Moriya Y, Sugihara KI, et al. Abnormal expression of CD44 variants in the exfoliated cells in the feces of patients with colorectal cancer. Gastroenterology. 1998;114:1196–1205.
74. Todaro M, Gaggianesi M, Catalano V, Benfante A, Iovino F, et al. CD44v6 is a marker of constitutive and reprogrammed cancer stem cells driving colon cancer metastasis. Cell Stem Cell 2014; 14: 342–356.
75. Huang R, Mo D, Wu J, et al. CD133 expression correlates with clinicopathologic features and poor prognosis of colorectal cancer patients: An updated meta-analysis of 37 studies. Medicine. 2018;97.
76. Horst D, Kriegl L, Engel J, Kirchner T, Jung A. CD133 expression is an independent prognostic marker for low survival in colorectal cancer. Br J Cancer 2008;99:1285.
77. Pradhan T, Padmanabhan K, Prasad M, Chandramohan K, Nair SA. Augmented CD133 expression in distal margin correlates with poor prognosis in colorectal cancer. J Cell Mol Med 2019;23:3984–94.
78. Munakata K, Uemura M, Tanaka S, Kawai K, Kitahara T, Miyo M, et al. Cancer stem-like properties in colorectal cancer cells with low proteasome activity. Clin Cancer Res 2016;22:5277–86.
79. Han S, Huang T, Wu X, Wang X, Liu S, Yang W, et al. Prognostic value of CD133 and SOX2 in advanced cancer. J Oncol 2019;2019:1–12.
80. Zhao Y, Peng J, Zhang E, Jiang N, Li J, Zhang Q, et al. CD133 expression may be useful as a prognostic indicator in colorectal cancer, a tool for optimizing therapy and supportive evidence for the cancer stem cell hypothesis: a meta-analysis. Oncotarget 2016;7:10023.
81. Li R, Dong H, Zhu J, Yi H, Liu S. Overexpression of CD133 confers poor prognosis in colorectal cancer: a systematic review and meta-analysis. Int J Clin Exp Med 2019;12:1492–1502.
| Files | ||
| Issue | Vol 19, No 2 (2020) | |
| Section | Review Article(s) | |
| DOI | https://doi.org/10.18502/ijaai.v19i2.2756 | |
| PMID | 32372624 | |
| Keywords | ||
| CD133 CD44 Clinicopathological features Esophageal cancer Meta-analysis Prognosis | ||
| Rights and permissions | |
|
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Kamil Mohammed Al-mosawi A, Cheshomi H, Hosseinzadeh A, M. Matin M. Prognostic and Clinical Value of CD44 and CD133 in Esophageal Cancer: A Systematic Review and Meta-analysis. Iran J Allergy Asthma Immunol. 2020;19(2):105-116.
