Prognostic impact of CD44-positive cancer stem-like cells at the invasive front of gastric cancer

British Journal of Cancer

Volumn 116, Issue 2, 2017, Pages 186-194

  Kodama, Hirokazu ^a   Murata, Satoshi ^a   Ishida, Mitsuaki ^a,b   Yamamoto, Hiroshi ^a   Yamaguchi, Tsuyoshi ^a   Kaida, Sachiko ^a   Miyake, Tohru ^a   Takebayashi, Katsushi ^a   Kushima, Ryoji ^a   Tani, Masaji ^a  

^a SHIGA UNIVERSITY OF MEDICAL SCIENCE   (Japan)

^b KANSAI MEDICAL UNIVERSITY   (Japan)

Author keywords

cancer stem cells; CD44; gastrectomy; prognosis; recurrence; survival

Indexed keywords

CD44V6 ANTIGEN; CD44V9 ANTIGEN; HERMES ANTIGEN; LYMPHOCYTE ANTIGEN; UNCLASSIFIED DRUG; CD44 PROTEIN, HUMAN; TUMOR MARKER;

ADULT; AGED; ANTIGEN EXPRESSION; ARTICLE; CANCER PROGNOSIS; CANCER RECURRENCE; CANCER STEM CELL; CANCER SURVIVAL; DISEASE SPECIFIC SURVIVAL; FEMALE; HISTOPATHOLOGY; HUMAN; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; RISK ASSESSMENT; STOMACH CANCER; TREATMENT OUTCOME; TUMOR INVASION; ADENOCARCINOMA; FOLLOW UP; METABOLISM; MIDDLE AGED; MORTALITY; PATHOLOGY; PROGNOSIS; RECURRENT DISEASE; STOMACH NEOPLASMS; SURVIVAL ANALYSIS; VERY ELDERLY;

ADENOCARCINOMA; ADULT; AGED; AGED, 80 AND OVER; ANTIGENS, CD44; BIOMARKERS, TUMOR; FEMALE; FOLLOW-UP STUDIES; HUMANS; MALE; MIDDLE AGED; NEOPLASM INVASIVENESS; NEOPLASTIC STEM CELLS; PROGNOSIS; RECURRENCE; STOMACH NEOPLASMS; SURVIVAL ANALYSIS;

EID: 85001790619     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2016.401     Document Type: Article

References (35)

1. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 100(7): 3983-3988.
2. Bankfalvi A, Piffko J (2000) Prognostic and predictive factors in oral cancer: The role of the invasive tumour front. J Oral Pathol Med 29(7): 291-298.
3. Brown RL, Reinke LM, Damerow MS, Perez D, Chodosh LA, Yang J, Cheng C (2011) CD44 splice isoform switching in human and mouse epithelium is essential for epithelial-mesenchymal transition and breast cancer progression. J Clin Invest 121(3): 1064-1074.
4. Cao X, Cao D, Jin M, Jia Z, Kong F, Ma H, Wang Y, Jiang J (2014) CD44 but not CD24 expression is related to poor prognosis in non-cardia adenocarcinoma of the stomach. BMC Gastroenterol 14: 157.
5. Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ (2005) Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res 65(23): 10946-10951.
6. Dalerba P, Dylla SJ, Park IK, Liu R, Wang X, Cho RW, Hoey T, Gurney A, Huang EH, Simeone DM, Shelton AA, Parmiani G, Castelli C, Clarke MF (2007) Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci USA 104(24): 10158-10163.
7. Ishigami S, Ueno S, Arigami T, Uchikado Y, Setoyama T, Arima H, Kita Y, Kurahara H, Okumura H, Matsumoto M, Kijima Y, Natsugoe S (2010) Prognostic impact of CD133 expression in gastric carcinoma. Anticancer Res 30(6): 2453-2457.
8. Ishimoto T, Nagano O, Yae T, Tamada M, Motohara T, Oshima H, Oshima M, Ikeda T, Asaba R, Yagi H, Masuko T, Shimizu T, Ishikawa T, Kai K, Takahashi E, Imamura Y, Baba Y, Ohmura M, Suematsu M, Baba H, Saya H (2011) CD44 variant regulates redox status in cancer cells by stabilizing the xCT subunit of system xc(-) and thereby promotes tumor growth. Cancer Cell 19(3): 387-400.
9. Ishimoto T, Oshima H, Oshima M, Kai K, Torii R, Masuko T, Baba H, Saya H, Nagano O (2010) CD44 slow-cycling tumor cell expansion is triggered by cooperative actions of Wnt and prostaglandin E2 in gastric tumorigenesis. Cancer Sci 101(3): 673-678.
10. Jackson DG, Buckley J, Bell JI (1992) Multiple variants of the human lymphocyte homing receptor CD44 generated by insertions at a single site in the extracellular domain. J Biol Chem 267(7): 4732-4739.
11. Japanese Gastric Cancer Association (2011) Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer 14(2): 101-112.
12. Khanh do T, Mekata E, Mukaisho K, Sugihara H, Shimizu T, Shiomi H, Murata S, Naka S, Yamamoto H, Endo Y, Tani T (2011) Prognostic role of CD10() myeloid cells in association with tumor budding at the invasion front of colorectal cancer. Cancer Sci 102(9): 1724-1733.
13. Klonisch T, Wiechec E, Hombach-Klonisch S, Ande SR, Wesselborg S, Schulze-Osthoff K, Los M (2008) Cancer stem cell markers in common cancers-Therapeutic implications. Trends Mol Med 14(10): 450-460.
14. Mashita N, Yamada S, Nakayama G, Tanaka C, Iwata N, Kanda M, Kobayashi D, Fujii T, Sugimoto H, Koike M, Nomoto S, Fujiwara M, Kodera Y (2014) Epithelial to mesenchymal transition might be induced via CD44 isoform switching in colorectal cancer. J Surg Oncol 110(6): 745-751.
15. Murata S, Yamamoto H, Yamaguchi T, Kaida S, Ishida M, Kodama H, Takebayashi K, Shimizu T, Miyake T, Tani T, Kushima R, Tani M (2016) Viable cancer cells in the remnant stomach are a potential source of peritoneal metastasis after curative distal gastrectomy for gastric cancer. Ann Surg Oncol 23(9): 2920-2927.
16. Okayama H, Kumamoto K, Saitou K, Hayase S, Kofunato Y, Sato Y, Miyamoto K, Nakamura I, Ohki S, Sekikawa K, Takenoshita S (2009) CD44v6, MMP-7 and nuclear Cdx2 are significant biomarkers for prediction of lymph node metastasis in primary gastric cancer. Oncol Rep 22(4): 745-755.
17. Rowe RG, Weiss SJ (2009) Navigating ECM barriers at the invasive front: The cancer cell-stroma interface. Annu Rev Cell Dev Biol 25: 567-595.
18. Ryu HS, Park DJ, Kim HH, Kim WH, Lee HS (2012) Combination of epithelial-mesenchymal transition and cancer stem cell-like phenotypes has independent prognostic value in gastric cancer. Hum Pathol 43(4): 520-528.
19. Schwitalla S (2014) Tumor cell plasticity: The challenge to catch a moving target. J Gastroenterol 49(4): 618-627.
20. Sentani K, Matsuda M, Oue N, Uraoka N, Naito Y, Sakamoto N, Yasui W (2014) Clinicopathological significance of MMP-7, laminin gamma2 and EGFR expression at the invasive front of gastric carcinoma. Gastric Cancer 17(3): 412-422.
21. Sharma M, Sah P, Sharma SS, Radhakrishnan R (2013) Molecular changes in invasive front of oral cancer. J Oral Maxillofac Pathol 17(2): 240-247.
22. Sneath RJ, Mangham DC (1998) The normal structure and function of CD44 and its role in neoplasia. Mol Pathol 51(4): 191-200.
23. Takaishi S, Okumura T, Tu S, Wang SS, Shibata W, Vigneshwaran R, Gordon SA, Shimada Y, Wang TC (2009) Identification of gastric cancer stem cells using the cell surface marker CD44. Stem Cells 27(5): 1006-1020.
24. Takebayashi K, Murata S, Yamamoto H, Ishida M, Yamaguchi T, Kojima M, Shimizu T, Shiomi H, Sonoda H, Naka S, Mekata E, Okabe H, Tani T (2014) Surgery-induced peritoneal cancer cells in patients who have undergone curative gastrectomy for gastric cancer. Ann Surg Oncol 21(6): 1991-1997.
25. Tanaka K, Shimura T, Kitajima T, Kondo S, Ide S, Okugawa Y, Saigusa S, Toiyama Y, Inoue Y, Araki T, Uchida K, Mohri Y, Kusunoki M (2014) Tropomyosin-related receptor kinase B at the invasive front and tumour cell dedifferentiation in gastric cancer. Br J Cancer 110(12): 2923-2934.
26. Tsugawa H, Suzuki H, Saya H, Hatakeyama M, Hirayama T, Hirata K, Nagano O, Matsuzaki J, Hibi T (2012) Reactive oxygen species-induced autophagic degradation of Helicobacter pylori CagA is specifically suppressed in cancer stem-like cells. Cell Host Microbe 12(6): 764-777.
27. Voulgari A, Pintzas A (2009) Epithelial-mesenchymal transition in cancer metastasis: mechanisms, markers and strategies to overcome drug resistance in the clinic. Biochim Biophys Acta 1796(2): 75-90.
28. Wakamatsu Y, Sakamoto N, Oo HZ, Naito Y, Uraoka N, Anami K, Sentani K, Oue N, Yasui W (2012) Expression of cancer stem cell markers ALDH1, CD44 and CD133 in primary tumor and lymph node metastasis of gastric cancer. Pathol Int 62(2): 112-119.
29. Wang T, Ong CW, Shi J, Srivastava S, Yan B, Cheng CL, Yong WP, Chan SL, Yeoh KG, Iacopetta B, Salto-Tellez M (2011) Sequential expression of putative stem cell markers in gastric carcinogenesis. Br J Cancer 105(5): 658-665.
30. Wu Y, Li Z, Zhang C, Yu K, Teng Z, Zheng G, Wang S, Liu Y, Cui L, Yu X (2015) CD44 family proteins in gastric cancer: A meta-Analysis and narrative review. Int J Clin Exp Med 8(3): 3595-3606.
31. Wu Y, Zhou BP (2008) New insights of epithelial-mesenchymal transition in cancer metastasis. Acta Biochim Biophys Sin 40(7): 643-650.
32. Xie JW, Chen PC, Zheng CH, Li P, Wang JB, Lin JX, Lu J, Chen QY, Cao LL, Lin M, Lin Y, Huang CM (2015) Evaluation of the prognostic value and functional roles of CD44v6 in gastric cancer. J Cancer Res Clin Oncol 141(10): 1809-1817.
33. Yae T, Tsuchihashi K, Ishimoto T, Motohara T, Yoshikawa M, Yoshida GJ, Wada T, Masuko T, Mogushi K, Tanaka H, Osawa T, Kanki Y, Minami T, Aburatani H, Ohmura M, Kubo A, Suematsu M, Takahashi K, Saya H, Nagano O (2012) Alternative splicing of CD44 mRNA by ESRP1 enhances lung colonization of metastatic cancer cell. Nat Commun 3: 883.
34. Yamaguchi A, Goi T, Yu J, Hirono Y, Ishida M, Iida A, Kimura T, Takeuchi K, Katayama K, Hirose K (2002) Expression of CD44v6 in advanced gastric cancer and its relationship to hematogenous metastasis and long-Term prognosis. J Surg Oncol 79(4): 230-235.
35. Yasui W, Kudo Y, Naka K, Fujimoto J, Ue T, Yokozaki H, Tahara E (1998) Expression of CD44 containing variant exon 9 (CD44v9) in gastric adenomas and adenocarcinomas: relation to the proliferation and progression. Int J Oncol 12(6): 1253-1258.