Prognostic impact of the expression of putative cancer stem cell markers CD133, CD166, CD44s, EpCAM, and ALDH1 in colorectal cancer

British Journal of Cancer

Volumn 103, Issue 3, 2010, Pages 382-390

  Lugli, A ^a   Iezzi, G ^a   Hostettler, I ^a   Muraro, M G ^a   Mele, V ^a   Tornillo, L ^a   Carafa, V ^a   Spagnoli, G ^a   Terracciano, L ^a   Zlobec, I ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

cancer stem cell; CD133; CD166; CD44; colorectal cancer; EpCAM

Indexed keywords

ACTIVATED LEUKOCYTE CELL ADHESION MOLECULE; ALDEHYDE DEHYDROGENASE; ALDEHYDE DEHYDROGENASE ISOENZYME 1; CD133 ANTIGEN; CD44V ANTIGEN; EPITHELIAL CELL ADHESION MOLECULE; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; CANCER CELL; CANCER STEM CELL; CELL INVASION; CLINICAL FEATURE; COLORECTAL CANCER; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MALE; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; TISSUE MICROARRAY;

ADULT; AGED; AGED, 80 AND OVER; ALDEHYDE DEHYDROGENASE; ANTIGENS, CD; ANTIGENS, CD44; ANTIGENS, NEOPLASM; CELL ADHESION MOLECULES; CELL ADHESION MOLECULES, NEURONAL; CELL DIVISION; COLORECTAL NEOPLASMS; FEMALE; FETAL PROTEINS; GLYCOPROTEINS; HUMANS; INTESTINAL MUCOSA; ISOENZYMES; LOSS OF HETEROZYGOSITY; MALE; MIDDLE AGED; NEOPLASM INVASIVENESS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PEPTIDES; PROGNOSIS; REFERENCE VALUES; STEM CELLS; SURVIVAL RATE;

EID: 77955051047     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/sj.bjc.6605762     Document Type: Article

References (45)

1. Albini A, Benelli R (2007) The chemoinvasion assay: a method to assess tumor and endothelial cell invasion and its modulation. Nat Protoc 2: 504-511
2. Brabletz T, Hlubek F, Spaderna S, Schmalhofer O, Hiendlmeyer E, Jung A, Kirchner T (2005a) Invasion and metastasis in colorectal cancer: epithelial-mesenchymal transition, mesenchymal-epithelial transition, stem cells and beta-catenin. Cells Tissues Organs 179: 56-65
3. Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T (2005b) Opinion: migrating cancer stem cells-an integrated concept of malignant tumour progression. Nat Rev Cancer 5: 744-749
4. Choi D, Lee HW, Hur KY, Kim JJ, Park GS, Jang SH, Song YS, Jang KS, Paik SS (2009) Cancer stem cell markers CD133 and CD24 correlate with invasiveness and differentiation in colorectal adenocarcinoma. World J Gastroenterol 15: 2258-2264
5. Coppola D, Hyacinthe M, Fu L, Cantor AB, Karl R, Marcet J, Cooper DL, Nicosia SV, Cooper HS (1998) CD44V6 expression in human colorectal carcinoma. Hum Pathol 29: 627-635
6. Dalerba P, Cho RW, Clarke MF (2007a) Cancer stem cells: models and concepts. Annu Rev Med 58: 267-284 (Pubitemid 46706514)
7. 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 (2007b) Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci USA 104: 10158-10163
8. Dean M, Fojo T, Bates S (2005) Tumour stem cells and drug resistance. Nat Rev Cancer 5: 275-284
9. Gastl G, Spizzo G, Obrist P, Dunser M, Mikuz G (2000) Ep-CAM over-expression in breast cancer as a predictor of survival. Lancet 356: 1981-1982
10. Ginestier C, Wicha MS (2007) Mammary stem cell number as a determinate of breast cancer risk. Breast Cancer Res 9: 109
11. Gosens MJ, van Kempen LC, van de Velde CJ, van Krieken JH, Nagtegaal ID (2007) Loss of membranous Ep-CAM in budding colorectal carcinoma cells. Mod Pathol 20: 221-232
12. Herrlich P, Pals S, Ponta H (1995) CD44 in colon cancer. Eur J Cancer 31A:1110-1112
13. Horst D, Kriegl L, Engel J, Kirchner T, Jung A (2008) CD133 expression is an independent prognostic marker for low survival in colorectal cancer. Br J Cancer 99: 1285-1289
14. Horst D, Kriegl L, Engel J, Kirchner T, Jung A (2009) Prognostic significance of the cancer stem cell markers cd133, cd44, and cd166 in colorectal cancer. Cancer Invest 27(8): 844-850
15. Hostettler L, Zlobec I, Terracciano L, Lugli A (2010) ABCG5-positivity in tumor buds is an indicator of poor prognosis in node-negative colorectal cancer patients. World J Gastroenterol 16: 732-739
16. Huang EH, Hynes MJ, Zhang T, Ginestier C, Dontu G, Appelman H, Fields JZ, Wicha MS, Boman BM (2009) Aldehyde dehydrogenase 1 is a marker for normal and malignant human colonic stem cells (SC) and tracks SC overpopulation during colon tumorigenesis. Cancer Res 69: 3382-3389
17. Huh JW, Kim HR, Kim YJ, Lee JH, Park YS, Cho SH, Joo JK (2009) Expression of standard CD44 in human colorectal carcinoma: association with prognosis. Pathol Int 59: 241-246
18. Jass JR, Love SB, Northover JM (1987) A new prognostic classification of rectal cancer. Lancet 1: 1303-1306
19. Kojima M, Ishii G, Atsumi N, Fujii S, Saito N, Ochiai A (2008) Immunohistochemical detection of CD133 expression in colorectal cancer: a clinicopathological study. Cancer Sci 99: 1578-1583
20. Kristiansen G, Pilarsky C, Wissmann C, Stephan C, Weissbach L, Loy V, Loening S, Dietel M, Rosenthal A (2003) ALCAM/CD166 is up-regulated in low-grade prostate cancer and progressively lost in high-grade lesions. Prostate 54: 34-43
21. Li CY, Li BX, Liang Y, Peng RQ, Ding Y, Xu DZ, Zhang X, Pan ZZ, Wan DS, Zeng YX, Zhu XF, Zhang XS (2009) Higher percentage of CD133+ cells is associated with poor prognosis in colon carcinoma patients with stage IIIB. J Transl Med 7: 56
22. Mezzanzanica D, Fabbi M, Bagnoli M, Staurengo S, Losa M, Balladore E, Alberti P, Lusa L, Ditto A, Ferrini S, Pierotti MA, Barbareschi M, Pilotti S, Canevari S (2008) Subcellular localization of activated leukocyte cell adhesion molecule is a molecular predictor of survival in ovarian carcinoma patients. Clin Cancer Res 14: 1726-1733
23. Morrin M, Delaney PV (2002) CD44v6 is not relevant in colorectal tumour progression. Int J Colorectal Dis 17: 30-36
24. Mulder JW, Kruyt PM, Sewnath M, Oosting J, Seldenrijk CA, Weidema WF, Offerhaus GJ, Pals ST (1994) Colorectal cancer prognosis and expression of exon-v6-containing CD44 proteins. Lancet 344: 1470-1472
25. Ngan CY, Yamamoto H, Seshimo I, Ezumi K, Terayama M, Hemmi H, Takemasa I, Ikeda M, Sekimoto M, Monden M (2007) A multivariate analysis of adhesion molecules expression in assessment of colorectal cancer. J Surg Oncol 95: 652-662
26. O'Brien CA, Pollett A, Gallinger S, Dick JE (2007) A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445: 106-110
27. Pardal R, Clarke MF, Morrison SJ (2003) Applying the principles of stem-cell biology to cancer. Nat Rev Cancer 3: 895-902
28. Patel BB, Yu Y, Du J, Levi E, Phillip PA, Majumdar AP (2009) Age-related increase in colorectal cancer stem cells in macroscopically normal mucosa of patients with adenomas: a risk factor for colon cancer. Biochem Biophys Res Commun 378: 344-347
29. Prall F (2007) Tumour budding in colorectal carcinoma. Histopathology 50: 151-162
30. Prince S, Zeidman A, Dekel Y, Ram E, Koren R (2008) Expression of epithelial cell adhesion molecule in gallbladder carcinoma and its correlation with clinicopathologic variables. Am J Clin Pathol 129: 424-429
31. Reya T, Morrison SJ, Clarke MF, Weissman IL (2001) Stem cells, cancer, and cancer stem cells. Nature 414: 105-111
32. Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C, De Maria R (2007) Identification and expansion of human colon-cancer-initiating cells. Nature 445: 111-115
33. Scheunemann P, Stoecklein NH, Rehders A, Bidde M, Metz S, Peiper M, Eisenberger C, Schulte Am Esch J, Knoefel WT, Hosch SB (2007) Frequency and prognostic significance of occult tumor cells in lymph nodes in patients with adenocarcinoma of the papilla of Vater. HPB (Oxford) 9: 135-139
34. Shmelkov SV, Butler JM, Hooper AT, Hormigo A, Kushner J, Milde T, St Clair R, Baljevic M, White I, Jin DK, Chadburn A, Murphy AJ, Valenzuela DM, Gale NW, Thurston G, Yancopoulos GD, D'Angelica M, Kemeny N, Lyden D, Rafii S (2008) CD133 expression is not restricted to stem cells, and both CD133+ and CD133-metastatic colon cancer cells initiate tumors. J Clin Invest 118: 2111-2120
35. Trzpis M, McLaughlin PM, de Leij LM, Harmsen MC (2007) Epithelial cell adhesion molecule: more than a carcinoma marker and adhesion molecule. Am J Pathol 171: 386-395
36. Visvader JE, Lindeman GJ (2008) Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 8: 755-768
37. Weg-Remers S, Anders M, von Lampe B, Riecken EO, Schuder G, Feifel G, Zeitz M, Stallmach A (1998) Decreased expression of CD44 splicing variants in advanced colorectal carcinomas. Eur J Cancer 34: 1607-1611
38. Weichert W, Knosel T, Bellach J, Dietel M, Kristiansen G (2004) ALCAM/CD166 is overexpressed in colorectal carcinoma and correlates with shortened patient survival. J Clin Pathol 57: 1160-1164
39. Wielenga VJ, van der Voort R, Mulder JW, Kruyt PM, Weidema WF, Oosting J, Seldenrijk CA, van Krimpen C, Offerhaus GJ, Pals ST (1998) CD44 splice variants as prognostic markers in colorectal cancer. Scand J Gastroenterol 33: 82-87
40. Woodhouse EC, Chuaqui RF, Liotta LA (1997) General mechanisms of metastasis. Cancer 80: 1529-1537
41. Zhou BB, Zhang H, Damelin M, Geles KG, Grindley JC, Dirks PB (2009) Tumour-initiating cells: challenges and opportunities for anticancer drug discovery. Nat Rev Drug Discov 8: 806-823
42. Zlobec I, Gunthert U, Tornillo L, Iezzi G, Baumhoer D, Terracciano L, Lugli A (2009) Systematic assessment of the prognostic impact of membranous CD44v6 protein expression in colorectal cancer. Histopathology 55: 564-575
43. Zlobec I, Lugli A, Baker K, Roth S, Minoo P, Hayashi S, Terracciano L, Jass JR (2007a) Role of APAF-1, E-cadherin and peritumoral lymphocytic infiltration in tumour budding in colorectal cancer. J Pathol 212: 260-268
44. Zlobec I, Steele R, Terracciano L, Jass JR, Lugli A (2007b) Selecting immunohistochemical cut-off scores for novel biomarkers of progression and survival in colorectal cancer. J Clin Pathol 60: 1112-1116
45. Haier J, Nasralla M, Nicolson GL 2000 Cell surface molecules and their prognostic values in assessing colorectal carcinomas. Ann Surg 231: 11-24 (Pubitemid 30043934)