Skip to main content
Top
Published in: Journal of Experimental & Clinical Cancer Research 1/2012

Open Access 01-12-2012 | Research

Increased expression of CD133 and reduced dystroglycan expression are strong predictors of poor outcome in colon cancer patients

Authors: Claudio Coco, Gian Franco Zannoni, Emanuele Caredda, Stefano Sioletic, Alma Boninsegna, Mario Migaldi, Gianluca Rizzo, Luca Reggiani Bonetti, Giannicola Genovese, Egidio Stigliano, Achille Cittadini, Alessandro Sgambato

Published in: Journal of Experimental & Clinical Cancer Research | Issue 1/2012

Login to get access

Abstract

Background

Expression levels of CD133, a cancer stem cell marker, and of the α-subunit of the dystroglycan (α-DG) complex, have been previously reported to be altered in colorectal cancers.

Methods

Expression levels of CD133 and α-DG were assessed by immunohistochemistry in a series of colon cancers and their prognostic significance was evaluated.

Results

Scattered cells positive for CD133 were rarely detected at the bases of the crypts in normal colonic mucosa while in cancer cells the median percentage of positive cells was 5% (range 0–80). A significant correlation was observed with pT parameter and tumor stage but not with tumor grade and N status. Recurrence and death from disease were significantly more frequent in CD133-high expressing tumors and Kaplan-Meier curves showed a significant separation between high vs low expressor groups for both disease-free (p = 0.002) and overall (p = 0.008) survival.
Expression of α-DG was reduced in a significant fraction of tumors but low α-DG staining did not correlate with any of the classical clinical-pathological parameters. Recurrence and death from the disease were significantly more frequent in α-DG-low expressing tumors and Kaplan-Meier curves showed a significant separation between high vs low expressor tumors for both disease-free (p = 0.02) and overall (p = 0.02) survival. Increased expression of CD133, but not loss of α-DG, confirmed to be an independent prognostic parameters at a multivariate analysis associated with an increased risk of recurrence (RR = 2.4; p = 0.002) and death (RR = 2.3; p = 0.003).

Conclusions

Loss of α-DG and increased CD133 expression are frequent events in human colon cancer and evaluation of CD133 expression could help to identify high-risk colon cancer patients.
Appendix
Available only for authorised users
Literature
1.
go back to reference 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: 1285-1289. 10.1038/sj.bjc.6604664.PubMedCentralCrossRefPubMed 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: 1285-1289. 10.1038/sj.bjc.6604664.PubMedCentralCrossRefPubMed
2.
go back to reference Kojima M, Ishii G, Atsumi N, Fujii S, Saito N, Ochiai A: Immunohistochemical detection of CD133 expression in colorectal cancer: a clinicopathological study. Cancer Sci. 2008, 99: 1578-1583. 10.1111/j.1349-7006.2008.00849.x.CrossRefPubMed Kojima M, Ishii G, Atsumi N, Fujii S, Saito N, Ochiai A: Immunohistochemical detection of CD133 expression in colorectal cancer: a clinicopathological study. Cancer Sci. 2008, 99: 1578-1583. 10.1111/j.1349-7006.2008.00849.x.CrossRefPubMed
3.
go back to reference Li C, Li B, Liang Y, Peng R, Ding Y, Xu D, et al: Higher percentage of CD133+ cells is associated with poor prognosis in colon carcinoma patients with stage IIIB. J Transl Med. 2009, 7: 56-10.1186/1479-5876-7-56.PubMedCentralCrossRefPubMed Li C, Li B, Liang Y, Peng R, Ding Y, Xu D, et al: Higher percentage of CD133+ cells is associated with poor prognosis in colon carcinoma patients with stage IIIB. J Transl Med. 2009, 7: 56-10.1186/1479-5876-7-56.PubMedCentralCrossRefPubMed
4.
go back to reference Winder SJ: The complexities of dystroglycan. TIBS. 2001, 26: 118-124.PubMed Winder SJ: The complexities of dystroglycan. TIBS. 2001, 26: 118-124.PubMed
5.
go back to reference Muschler J, Levy D, Boudreau R, Henry M, Campbell K, Bissell MJ: A role for dystroglycan in epithelial polarization: loss of function in breast tumor cells. Cancer Res. 2002, 62: 7102-7109.PubMed Muschler J, Levy D, Boudreau R, Henry M, Campbell K, Bissell MJ: A role for dystroglycan in epithelial polarization: loss of function in breast tumor cells. Cancer Res. 2002, 62: 7102-7109.PubMed
6.
go back to reference Sgambato A, Brancaccio A: The dystroglycan complex: from biology to cancer. J Cell Physiol. 2005, 205: 163-169. 10.1002/jcp.20411.CrossRefPubMed Sgambato A, Brancaccio A: The dystroglycan complex: from biology to cancer. J Cell Physiol. 2005, 205: 163-169. 10.1002/jcp.20411.CrossRefPubMed
7.
go back to reference Sgambato A, Di Salvatore M, De Paola B, Rettino A, Faraglia B, Boninsegna A, et al: Analysis of dystroglycan regulation and functions in mouse mammary epithelial cells and implications for mammary tumorigenesis. J Cell Physiol. 2006, 207: 520-529. 10.1002/jcp.20600.CrossRefPubMed Sgambato A, Di Salvatore M, De Paola B, Rettino A, Faraglia B, Boninsegna A, et al: Analysis of dystroglycan regulation and functions in mouse mammary epithelial cells and implications for mammary tumorigenesis. J Cell Physiol. 2006, 207: 520-529. 10.1002/jcp.20600.CrossRefPubMed
8.
go back to reference Calogero A, Pavoni E, Gramaglia T, D'Amati G, Ragona G, Brancaccio A, et al: Altered exression of a-dystroglycan subunit in human gliomas. Cancer Biol Ther. 2006, 5: 441-448. 10.4161/cbt.5.4.2546.CrossRefPubMed Calogero A, Pavoni E, Gramaglia T, D'Amati G, Ragona G, Brancaccio A, et al: Altered exression of a-dystroglycan subunit in human gliomas. Cancer Biol Ther. 2006, 5: 441-448. 10.4161/cbt.5.4.2546.CrossRefPubMed
9.
go back to reference Sgambato A, Camerini A, Montanari M, Camerini A, Brancaccio A, Spada D, et al: Increased expression of dystroglycan inhibits the growth and tumorigenicity of human mammary epithelial cells. Cancer Biol Ther. 2004, 3: 849-860.CrossRef Sgambato A, Camerini A, Montanari M, Camerini A, Brancaccio A, Spada D, et al: Increased expression of dystroglycan inhibits the growth and tumorigenicity of human mammary epithelial cells. Cancer Biol Ther. 2004, 3: 849-860.CrossRef
10.
go back to reference Sgambato A, De Paola B, Migaldi M, Di Salvatore M, Rettino A, Rossi G, et al: Dystroglycan expression is reduced during prostate tumorigenesis and is regulated by androgens in prostate cancer cells. J Cell Physiol. 2007, 213: 528-539. 10.1002/jcp.21130.CrossRefPubMed Sgambato A, De Paola B, Migaldi M, Di Salvatore M, Rettino A, Rossi G, et al: Dystroglycan expression is reduced during prostate tumorigenesis and is regulated by androgens in prostate cancer cells. J Cell Physiol. 2007, 213: 528-539. 10.1002/jcp.21130.CrossRefPubMed
11.
go back to reference Compton C, Greene F: The staging of colorectal cancer: 2004 and beyond. CA Cancer J Clin. 2004, 54: 295-308. 10.3322/canjclin.54.6.295.CrossRefPubMed Compton C, Greene F: The staging of colorectal cancer: 2004 and beyond. CA Cancer J Clin. 2004, 54: 295-308. 10.3322/canjclin.54.6.295.CrossRefPubMed
12.
go back to reference Sgambato A, Migaldi M, Montanari M, Camerini A, Brancaccio A, Rossi G, et al: Dystroglycan expression is frequently reduced in human breast and colon cancers and is associated with tumor progression. Am J Pathol. 2003, 162: 849-860. 10.1016/S0002-9440(10)63881-3.PubMedCentralCrossRefPubMed Sgambato A, Migaldi M, Montanari M, Camerini A, Brancaccio A, Rossi G, et al: Dystroglycan expression is frequently reduced in human breast and colon cancers and is associated with tumor progression. Am J Pathol. 2003, 162: 849-860. 10.1016/S0002-9440(10)63881-3.PubMedCentralCrossRefPubMed
13.
go back to reference Zannoni G, Faraglia B, Tarquini E, Camerini A, Vrijens K, Migaldi M, et al: Expression of the CDK inhibitor p27kip1 and oxidative DNA damage in non-neoplastic and neoplastic vulvar epithelial lesions. Mod Pathol. 2006, 19: 504-513. 10.1038/modpathol.3800532.CrossRefPubMed Zannoni G, Faraglia B, Tarquini E, Camerini A, Vrijens K, Migaldi M, et al: Expression of the CDK inhibitor p27kip1 and oxidative DNA damage in non-neoplastic and neoplastic vulvar epithelial lesions. Mod Pathol. 2006, 19: 504-513. 10.1038/modpathol.3800532.CrossRefPubMed
14.
go back to reference Sgambato A, Tarquini E, Resci F, De Paola B, Faraglia B, Camerini A, et al: Aberrant expression of alpha-dystroglycan in cervical and vulvar cancer. Gynecol Oncol. 2006, 103: 397-404. 10.1016/j.ygyno.2006.03.059.CrossRefPubMed Sgambato A, Tarquini E, Resci F, De Paola B, Faraglia B, Camerini A, et al: Aberrant expression of alpha-dystroglycan in cervical and vulvar cancer. Gynecol Oncol. 2006, 103: 397-404. 10.1016/j.ygyno.2006.03.059.CrossRefPubMed
15.
go back to reference Jiang X, Rieder S, Giese N, Friess H, Michalski C, Kleeff J: Reduced alpha-dystroglycan expression correlates with shortened patient survival in pancreatic cancer. J Surg Res. 2011, 171: 120-126. 10.1016/j.jss.2009.11.730.CrossRefPubMed Jiang X, Rieder S, Giese N, Friess H, Michalski C, Kleeff J: Reduced alpha-dystroglycan expression correlates with shortened patient survival in pancreatic cancer. J Surg Res. 2011, 171: 120-126. 10.1016/j.jss.2009.11.730.CrossRefPubMed
16.
go back to reference Shen JG, Xu CY, Li X, Dong M, Jiang ZN, Wang J, et al: Dystroglycan is associated with tumor progression and patient survival in gastric cancer. Pathol Oncol Res. 2012, 18: 79-84. 10.1007/s12253-011-9419-2.CrossRefPubMed Shen JG, Xu CY, Li X, Dong M, Jiang ZN, Wang J, et al: Dystroglycan is associated with tumor progression and patient survival in gastric cancer. Pathol Oncol Res. 2012, 18: 79-84. 10.1007/s12253-011-9419-2.CrossRefPubMed
17.
go back to reference Bao X, Fukuda M: A tumor suppressor function of laminin-binding alpha-dystroglycan. Methods Enzymol. 2010, 479: 387-396.CrossRefPubMed Bao X, Fukuda M: A tumor suppressor function of laminin-binding alpha-dystroglycan. Methods Enzymol. 2010, 479: 387-396.CrossRefPubMed
18.
go back to reference Brennan P, Jing J, Ethunandan M, Gorecki D: Dystroglycan complex in cancer. Eur J Surg Oncol. 2004, 30: 589-592. 10.1016/j.ejso.2004.03.014.CrossRefPubMed Brennan P, Jing J, Ethunandan M, Gorecki D: Dystroglycan complex in cancer. Eur J Surg Oncol. 2004, 30: 589-592. 10.1016/j.ejso.2004.03.014.CrossRefPubMed
19.
go back to reference Henry MD, Cohen MB, Campbell KP: Reduced expression of dystroglycan in breast and prostate cancer. Hum Pathol. 2001, 32: 791-795. 10.1053/hupa.2001.26468.CrossRefPubMed Henry MD, Cohen MB, Campbell KP: Reduced expression of dystroglycan in breast and prostate cancer. Hum Pathol. 2001, 32: 791-795. 10.1053/hupa.2001.26468.CrossRefPubMed
20.
go back to reference Cross S, Lippitt J, Mitchell A, Hollingsbury F, Balasubramanian S, Reed M, et al: Expression of beta-dystroglycan is reduced or absent in many human carcinomas. Histopathology. 2008, 53: 561-566. 10.1111/j.1365-2559.2008.03157.x.CrossRefPubMed Cross S, Lippitt J, Mitchell A, Hollingsbury F, Balasubramanian S, Reed M, et al: Expression of beta-dystroglycan is reduced or absent in many human carcinomas. Histopathology. 2008, 53: 561-566. 10.1111/j.1365-2559.2008.03157.x.CrossRefPubMed
21.
go back to reference Losasso C, Di Tommaso F, Sgambato A, Ardito R, Cittadini A, Giardina B, et al: Anomalous dystroglycan in carcinoma cell lines. FEBS Lett. 2000, 484: 194-198. 10.1016/S0014-5793(00)02157-8.CrossRefPubMed Losasso C, Di Tommaso F, Sgambato A, Ardito R, Cittadini A, Giardina B, et al: Anomalous dystroglycan in carcinoma cell lines. FEBS Lett. 2000, 484: 194-198. 10.1016/S0014-5793(00)02157-8.CrossRefPubMed
22.
go back to reference Herzog C, Has C, Franzke C-W, Echtermeyer F, Schlotzer-Schrehardt U, Kroger S, et al: Dystroglycan in skin and cutaneous cells: ß-subunit is shed from the cell surface. J Invest Dermatol. 2004, 122: 1372-1380. 10.1111/j.0022-202X.2004.22605.x.CrossRefPubMed Herzog C, Has C, Franzke C-W, Echtermeyer F, Schlotzer-Schrehardt U, Kroger S, et al: Dystroglycan in skin and cutaneous cells: ß-subunit is shed from the cell surface. J Invest Dermatol. 2004, 122: 1372-1380. 10.1111/j.0022-202X.2004.22605.x.CrossRefPubMed
23.
go back to reference Jing J, Lien CF, Sharma S, Rice J, Brennan PA, Gorecki DC: Aberrant expression, processing and degradation of dystroglycan in squamous cell carcinomas. European J Cancer. 2004, 40: 2143-2151. 10.1016/j.ejca.2004.05.018.CrossRef Jing J, Lien CF, Sharma S, Rice J, Brennan PA, Gorecki DC: Aberrant expression, processing and degradation of dystroglycan in squamous cell carcinomas. European J Cancer. 2004, 40: 2143-2151. 10.1016/j.ejca.2004.05.018.CrossRef
24.
go back to reference Singh J, Itahana Y, Knight-Krajewski S, Kanagawa M, Campbell KP, Bissell MJ, et al: Proteolytic enzymes and altered glycosylation modulate dystroglycan function in carcinoma cells. Cancer Res. 2004, 64: 6152-6159. 10.1158/0008-5472.CAN-04-1638.CrossRefPubMed Singh J, Itahana Y, Knight-Krajewski S, Kanagawa M, Campbell KP, Bissell MJ, et al: Proteolytic enzymes and altered glycosylation modulate dystroglycan function in carcinoma cells. Cancer Res. 2004, 64: 6152-6159. 10.1158/0008-5472.CAN-04-1638.CrossRefPubMed
25.
go back to reference de Bernabé D, Inamori K, Yoshida-Moriguchi T, Weydert C, Harper H, Willer T, et al: Loss of alpha-dystroglycan laminin binding in epithelium-derived cancers is caused by silencing of LARGE. J Biol Chem. 2009, 284: 11279-11284.PubMedCentralCrossRefPubMed de Bernabé D, Inamori K, Yoshida-Moriguchi T, Weydert C, Harper H, Willer T, et al: Loss of alpha-dystroglycan laminin binding in epithelium-derived cancers is caused by silencing of LARGE. J Biol Chem. 2009, 284: 11279-11284.PubMedCentralCrossRefPubMed
26.
go back to reference Holt KH, Crosbie RH, Venzke DP, Campbell KP: Biosynthesis of dystroglycan: processing of a precursor peptide. FEBS Lett. 2000, 468: 79-83. 10.1016/S0014-5793(00)01195-9.CrossRefPubMed Holt KH, Crosbie RH, Venzke DP, Campbell KP: Biosynthesis of dystroglycan: processing of a precursor peptide. FEBS Lett. 2000, 468: 79-83. 10.1016/S0014-5793(00)01195-9.CrossRefPubMed
27.
go back to reference O’Brien C, Pollett A, Gallinger S, Dick J: A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature. 2007, 445: 106-110. 10.1038/nature05372.CrossRefPubMed O’Brien C, Pollett A, Gallinger S, Dick J: A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature. 2007, 445: 106-110. 10.1038/nature05372.CrossRefPubMed
28.
go back to reference Ricci-Vitiani L, Lombardi D, Signore M, Biffoni M, Pallini R, Parati E, et al: Identification and expansion of human colon-cancer-initiating cells. Nature. 2007, 445: 111-115. 10.1038/nature05384.CrossRefPubMed Ricci-Vitiani L, Lombardi D, Signore M, Biffoni M, Pallini R, Parati E, et al: Identification and expansion of human colon-cancer-initiating cells. Nature. 2007, 445: 111-115. 10.1038/nature05384.CrossRefPubMed
29.
go back to reference Shmelkov S, Butler J, Hooper A, Hormigo A, Kushner J, Milde T, et al: CD133 expression is not restricted to stem cells, and both CD133+ and CD133- metastatic colon cancer cells initiate tumors. J Clin Invest. 2008, 118: 2111-2120.PubMedCentralPubMed Shmelkov S, Butler J, Hooper A, Hormigo A, Kushner J, Milde T, et al: CD133 expression is not restricted to stem cells, and both CD133+ and CD133- metastatic colon cancer cells initiate tumors. J Clin Invest. 2008, 118: 2111-2120.PubMedCentralPubMed
30.
go back to reference Horst D, Kriegl L, Engel J, Kirchner T: A J. Prognostic significance of the cancer stem cell markers CD133, CD44, and CD166 in colorectal cancer. Cancer Invest. 2009, 27: 844-850. 10.1080/07357900902744502.CrossRefPubMed Horst D, Kriegl L, Engel J, Kirchner T: A J. Prognostic significance of the cancer stem cell markers CD133, CD44, and CD166 in colorectal cancer. Cancer Invest. 2009, 27: 844-850. 10.1080/07357900902744502.CrossRefPubMed
31.
go back to reference Horst D, Scheel S, Liebmann S, Neumann J, Maatz S, Kirchner T, et al: The cancer stem cell marker CD133 has high prognostic impact but unknown functional relevance for the metastasis of human colon cancer. J Pathol. 2009, 219: 427-434. 10.1002/path.2597.CrossRefPubMed Horst D, Scheel S, Liebmann S, Neumann J, Maatz S, Kirchner T, et al: The cancer stem cell marker CD133 has high prognostic impact but unknown functional relevance for the metastasis of human colon cancer. J Pathol. 2009, 219: 427-434. 10.1002/path.2597.CrossRefPubMed
32.
go back to reference Puglisi M, Barba M, Corbi M, Errico M, Giorda E, Saulnier N, et al: Identification of Endothelin-1 and NR4A2 as CD133-regulated genes in colon cancer cells. J Pathol. 2011, 225: 305-314. 10.1002/path.2954.CrossRefPubMed Puglisi M, Barba M, Corbi M, Errico M, Giorda E, Saulnier N, et al: Identification of Endothelin-1 and NR4A2 as CD133-regulated genes in colon cancer cells. J Pathol. 2011, 225: 305-314. 10.1002/path.2954.CrossRefPubMed
33.
go back to reference Sgambato A, Puglisi M, Errico F, Rafanelli F, Boninsegna A, Rettino A, et al: Post-translational modulation of CD133 expression during sodium butyrate-induced differentiation of HT29 human colon cancer cells: implications for its detection. J Cell Physiol. 2010, 224: 234-241.PubMed Sgambato A, Puglisi M, Errico F, Rafanelli F, Boninsegna A, Rettino A, et al: Post-translational modulation of CD133 expression during sodium butyrate-induced differentiation of HT29 human colon cancer cells: implications for its detection. J Cell Physiol. 2010, 224: 234-241.PubMed
34.
go back to reference Sgambato A, Errico F, Caredda E, Puglisi M, Cittadini A: Divergent expression of CD133 in different studies: the need for a consensus panel?. Int J Cancer. 2010, 128: 2247-2249.CrossRef Sgambato A, Errico F, Caredda E, Puglisi M, Cittadini A: Divergent expression of CD133 in different studies: the need for a consensus panel?. Int J Cancer. 2010, 128: 2247-2249.CrossRef
35.
go back to reference Hermansen S, Christensen K, Jensen S, Kristensen B: Inconsistent immunohistochemical expression patterns of four different CD133 antibody clones in glioblastoma. J Histochem Cytochem. 2011, 59: 391-407. 10.1369/0022155411400867.PubMedCentralCrossRefPubMed Hermansen S, Christensen K, Jensen S, Kristensen B: Inconsistent immunohistochemical expression patterns of four different CD133 antibody clones in glioblastoma. J Histochem Cytochem. 2011, 59: 391-407. 10.1369/0022155411400867.PubMedCentralCrossRefPubMed
36.
go back to reference Mak A, Blakely K, Williams R, Penttila P, Shukalyuk A, Osman K, et al: CD133 N-glycosylation processing contributes to cell-surface recognition of the primitive cell marker AC133. J Biol Chem. 2011, 31: 4273-4275. Mak A, Blakely K, Williams R, Penttila P, Shukalyuk A, Osman K, et al: CD133 N-glycosylation processing contributes to cell-surface recognition of the primitive cell marker AC133. J Biol Chem. 2011, 31: 4273-4275.
37.
go back to reference Xi H, Zhao P: Clinicopathological significance and prognostic value of EphA3 and CD133 expression in colorectal carcinoma. J Clin Pathol. 2011, 64: 498-503. 10.1136/jcp.2010.087213.CrossRefPubMed Xi H, Zhao P: Clinicopathological significance and prognostic value of EphA3 and CD133 expression in colorectal carcinoma. J Clin Pathol. 2011, 64: 498-503. 10.1136/jcp.2010.087213.CrossRefPubMed
38.
go back to reference Arena V, Caredda V, Cufino V, Stigliano E, Scaldaferri F, Gasbarrini A, et al: Differential CD133 expression pattern during mouse colon tumorigenesis. Anticancer Res. 2011, 31: 4273-4275.PubMed Arena V, Caredda V, Cufino V, Stigliano E, Scaldaferri F, Gasbarrini A, et al: Differential CD133 expression pattern during mouse colon tumorigenesis. Anticancer Res. 2011, 31: 4273-4275.PubMed
39.
go back to reference Hibi K, Sakata M, Sakuraba K, Shirahata A, Goto T, Mizukami H, et al: CD133 gene overexpression is frequently observed in early colo-rectal carcinoma. Hepatogastroenterology. 2009, 56: 995-997.PubMed Hibi K, Sakata M, Sakuraba K, Shirahata A, Goto T, Mizukami H, et al: CD133 gene overexpression is frequently observed in early colo-rectal carcinoma. Hepatogastroenterology. 2009, 56: 995-997.PubMed
40.
go back to reference Keysar S, Jimeno A: More than markers: biological significance of cancer stem cell-defining molecules. Mol Cancer Ther. 2010, 9: 2450-2457. 10.1158/1535-7163.MCT-10-0530.PubMedCentralCrossRefPubMed Keysar S, Jimeno A: More than markers: biological significance of cancer stem cell-defining molecules. Mol Cancer Ther. 2010, 9: 2450-2457. 10.1158/1535-7163.MCT-10-0530.PubMedCentralCrossRefPubMed
41.
go back to reference Huang X, Sheng Y, Guan M: Co-expression of stem cell genes CD133 and CD44 in colorectal cancers with early liver metastasis. Surg Oncol. 2012, 21: 103-107. 10.1016/j.suronc.2011.06.001.CrossRefPubMed Huang X, Sheng Y, Guan M: Co-expression of stem cell genes CD133 and CD44 in colorectal cancers with early liver metastasis. Surg Oncol. 2012, 21: 103-107. 10.1016/j.suronc.2011.06.001.CrossRefPubMed
42.
go back to reference Puglisi M, Sgambato A, Saulnier N, Rafanelli F, Barba M, Boninsegna A, et al: Isolation and characterization of CD133+ population within human primary and metastatic colon cancer. Eur Rev Med Pharmacol Sci. 2009, 13 (Suppl 1): 55-62.PubMed Puglisi M, Sgambato A, Saulnier N, Rafanelli F, Barba M, Boninsegna A, et al: Isolation and characterization of CD133+ population within human primary and metastatic colon cancer. Eur Rev Med Pharmacol Sci. 2009, 13 (Suppl 1): 55-62.PubMed
43.
go back to reference Deng W, Schneider M, Frock R, Castillejo-Lopez C, Gaman E, Baumgartner S, et al: Dystroglycan is required for polarizing the epithelial cells and the oocyte in Drosophila. Development. 2003, 130: 173-184. 10.1242/dev.00199.CrossRefPubMed Deng W, Schneider M, Frock R, Castillejo-Lopez C, Gaman E, Baumgartner S, et al: Dystroglycan is required for polarizing the epithelial cells and the oocyte in Drosophila. Development. 2003, 130: 173-184. 10.1242/dev.00199.CrossRefPubMed
44.
go back to reference Feng H, Liu Y, Yang L, Bian X, Yang Z, Gu B, et al: Expression of CD133 correlates with differentiation of human colon cancer cells. Cancer Biol Ther. 2010, 9: 215-222.CrossRef Feng H, Liu Y, Yang L, Bian X, Yang Z, Gu B, et al: Expression of CD133 correlates with differentiation of human colon cancer cells. Cancer Biol Ther. 2010, 9: 215-222.CrossRef
45.
go back to reference Kemper K, Sprick M, de Bree M, Scopelliti A, Vermeulen L, Hoek M, et al: The AC133 epitope, but not the CD133 protein, is lost upon cancer stem cell differentiation. Cancer Res. 2010, 70: 719-729. 10.1158/0008-5472.CAN-09-1820.CrossRefPubMed Kemper K, Sprick M, de Bree M, Scopelliti A, Vermeulen L, Hoek M, et al: The AC133 epitope, but not the CD133 protein, is lost upon cancer stem cell differentiation. Cancer Res. 2010, 70: 719-729. 10.1158/0008-5472.CAN-09-1820.CrossRefPubMed
46.
go back to reference Yang K, Chen X, Zhang B, Yang C, Chen H, Chen Z, et al: Is CD133 a biomarker for cancer stem cells of colorectal cancer and brain tumors? A meta-analysis. Int J Biol Markers. 2011, 26: 173-180. 10.5301/JBM.2011.8551.CrossRefPubMed Yang K, Chen X, Zhang B, Yang C, Chen H, Chen Z, et al: Is CD133 a biomarker for cancer stem cells of colorectal cancer and brain tumors? A meta-analysis. Int J Biol Markers. 2011, 26: 173-180. 10.5301/JBM.2011.8551.CrossRefPubMed
Metadata
Title
Increased expression of CD133 and reduced dystroglycan expression are strong predictors of poor outcome in colon cancer patients
Authors
Claudio Coco
Gian Franco Zannoni
Emanuele Caredda
Stefano Sioletic
Alma Boninsegna
Mario Migaldi
Gianluca Rizzo
Luca Reggiani Bonetti
Giannicola Genovese
Egidio Stigliano
Achille Cittadini
Alessandro Sgambato
Publication date
01-12-2012
Publisher
BioMed Central
Published in
Journal of Experimental & Clinical Cancer Research / Issue 1/2012
Electronic ISSN: 1756-9966
DOI
https://doi.org/10.1186/1756-9966-31-71

Other articles of this Issue 1/2012

Journal of Experimental & Clinical Cancer Research 1/2012 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine