CD44 upregulation in E-cadherin-negative esophageal cancers results in cell invasion

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  Le Bras, Grégoire F ^a   Allison, Gillian L ^a   Richards, Nicole F ^a   Ansari, Shazia S ^a   Washington, M Kay ^a   Andl, Claudia D ^a  

^a VANDERBILT INGRAM CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN A; GELATINASE B; HERMES ANTIGEN; UVOMORULIN;

ARTICLE; CANCER GROWTH; CANCER INVASION; CELL INVASION; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; EPITHELIAL MESENCHYMAL TRANSITION; ESOPHAGUS CANCER; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; PROCESS MODEL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION;

ANTIGENS, CD44; BLOTTING, WESTERN; CADHERINS; CELL ADHESION; CELL LINE; CELL MOVEMENT; CELL PROLIFERATION; EPITHELIAL CELLS; ESOPHAGEAL NEOPLASMS; ESOPHAGUS; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOENZYME TECHNIQUES; MATRIX METALLOPROTEINASE 9; NEOPLASM INVASIVENESS; UP-REGULATION;

EID: 84858208747     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0027063     Document Type: Article

References (48)

1. Aruffo A, Stamenkovic I, Melnick M, Underhill CB, Seed B, (1990) CD44 is the principal cell surface receptor for hyaluronate. Cell 61: 1303-1313.
2. Legg JW, Lewis CA, Parsons M, Ng T, Isacke CM, (2002) A novel PKC-regulated mechanism controls CD44-ezrin association and directional cell motility. Nat Cell Biol 4: 399-407.
3. Yu Q, Toole BP, Stamenkovic I, (1997) Induction of apoptosis of metastatic mammary carcinoma cells in vivo by disruption of tumor cell surface CD44 function. J. Exp. Med 186: 1985-1996.
4. Bennett KL, Jackson DG, Simon JC, Tanczos E, Peach R, et al. (1995) CD44 isoforms containing exon V3 are responsible for the presentation of heparin-binding growth factor. The Journal of Cell Biology 128: 687-698.
5. Naor D, Nedvetzki S, Golan I, Melnik L, Faitelson Y, (2002) CD44 in cancer. Critical Reviews in Clinical Laboratory Sciences 39: 527-579.
6. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF, (2003) Prospective identification of tumorigenic breast cancer cells. Proceedings of the National Academy of Sciences of the United States of America 100: 3983-3988.
7. Wheatley SC, Isacke CM, (1995) Induction of a hyaluronan receptor, CD44, during embryonal carcinoma and embryonic stem cell differentiation. Cell Adhes. Commun 3: 217-230.
8. Mani SA, Guo W, Liao M-J, Eaton EN, Ayyanan A, et al. (2008) The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133: 704-715 doi:10.1016/j.cell.2008.03.027.
9. Zöller M, (2011) CD44: can a cancer-initiating cell profit from an abundantly expressed molecule? Nat Rev Cancer 11: 254-267 doi:10.1038/nrc3023.
10. Günthert U, Hofmann M, Rudy W, Reber S, Zöller M, et al. (1991) A new variant of glycoprotein CD44 confers metastatic potential to rat carcinoma cells. Cell 65: 13-24.
11. Stappert J, Kemler R, (1994) A short core region of E-cadherin is essential for catenin binding and is highly phosphorylated. Cell Adhes. Commun 2: 319-327.
12. Thoreson MA, Anastasiadis PZ, Daniel JM, Ireton RC, Wheelock MJ, et al. (2000) Selective uncoupling of p120(ctn) from E-cadherin disrupts strong adhesion. J. Cell Biol 148: 189-202.
13. Rimm DL, Koslov ER, Kebriaei P, Cianci CD, Morrow JS, (1995) Alpha 1(E)-catenin is an actin-binding and-bundling protein mediating the attachment of F-actin to the membrane adhesion complex. Proceedings of the National Academy of Sciences 92: 8813-8817.
14. Peinado H, Olmeda D, Cano A, (2007) Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nature Reviews. Cancer 7: 415-428 doi:10.1038/nrc2131.
15. Kuo Y-C, Su C-H, Liu C-Y, Chen T-H, Chen C-P, et al. (2009) Transforming growth factor-beta induces CD44 cleavage that promotes migration of MDA-MB-435s cells through the up-regulation of membrane type 1-matrix metalloproteinase. International Journal of Cancer. Journal International Du Cancer 124: 2568-2576 doi:10.1002/ijc.24263.
16. Ito T, Williams JD, Fraser DJ, Phillips AO, (2004) Hyaluronan regulates transforming growth factor-beta1 receptor compartmentalization. J. Biol. Chem 279: 25326-25332 doi:10.1074/jbc.M403135200.
17. Xiao L, Yuan X, Sharkis SJ, (2006) Activin A maintains self-renewal and regulates fibroblast growth factor, Wnt, and bone morphogenic protein pathways in human embryonic stem cells. Stem Cells 24: 1476-1486 doi:10.1634/stemcells.2005-0299.
18. Yu J, Dolter KE, (1997) Production of activin A and its roles in inflammation and hematopoiesis. Cytokines Cell. Mol. Ther 3: 169-177.
19. Larsson J, Karlsson S, (2005) The role of Smad signaling in hematopoiesis. Oncogene 24: 5676-5692 doi:10.1038/sj.onc.1208920.
20. Thisse B, Wright CV, Thisse C, (2000) Activin- and Nodal-related factors control antero-posterior patterning of the zebrafish embryo. Nature 403: 425-428 doi:10.1038/35000200.
21. Wildi S, Kleeff J, Maruyama H, Maurer CA, Büchler MW, et al. (2001) Overexpression of activin A in stage IV colorectal cancer. Gut 49: 409-417.
22. Yoshinaga K, Inoue H, Utsunomiya T, Sonoda H, Masuda T, et al. (2004) N-cadherin is regulated by activin A and associated with tumor aggressiveness in esophageal carcinoma. Clin. Cancer Res 10: 5702-5707 doi:10.1158/1078-0432.CCR-03-0262.
23. Yoshinaga K, Mimori K, Inoue H, Kamohara Y, Yamashita K, et al. (2008) Activin A enhances MMP-7 activity via the transcription factor AP-1 in an esophageal squamous cell carcinoma cell line. Int. J. Oncol 33: 453-459.
24. Yoshinaga K, Yamashita K, Mimori K, Tanaka F, Inoue H, et al. (2008) Activin a causes cancer cell aggressiveness in esophageal squamous cell carcinoma cells. Ann. Surg. Oncol 15: 96-103 doi:10.1245/s10434-007-9631-1.
25. Andl CD, Fargnoli BB, Okawa T, Bowser M, Takaoka M, et al. (2006) Coordinated functions of E-cadherin and transforming growth factor beta receptor II in vitro and in vivo. Cancer Res 66: 9878-9885 doi:10.1158/0008-5472.CAN-05-4157.
26. Gotoda T, Matsumura Y, Kondo H, Ono H, Kanamoto A, et al. (2000) Expression of CD44 variants and prognosis in oesophageal squamous cell carcinoma. Gut 46: 14-19.
27. Nozoe T, Kohnoe S, Ezaki T, Kabashima A, Maehara Y, (2004) Significance of immunohistochemical over-expression of CD44v6 as an indicator of malignant potential in esophageal squamous cell carcinoma. J. Cancer Res. Clin. Oncol 130: 334-338 doi:10.1007/s00432-004-0542-2.
28. Harada H, Nakagawa H, Oyama K, Takaoka M, Andl CD, et al. (2003) Telomerase induces immortalization of human esophageal keratinocytes without p16INK4a inactivation. Mol. Cancer Res 1: 729-738.
29. Altorki N, Schwartz GK, Blundell M, Davis BM, Kelsen DP, et al. (1993) Characterization of cell lines established from human gastric-esophageal adenocarcinomas. Biologic phenotype and invasion potential. Cancer 72: 649-657.
30. Hughes SJ, Nambu Y, Soldes OS, Hamstra D, Rehemtulla A, et al. (1997) Fas/APO-1 (CD95) is not translocated to the cell membrane in esophageal adenocarcinoma. Cancer Res 57: 5571-5578.
31. Rockett JC, Larkin K, Darnton SJ, Morris AG, Matthews HR, (1997) Five newly established oesophageal carcinoma cell lines: phenotypic and immunological characterization. Br. J. Cancer 75: 258-263.
32. Lee JJ, Natsuizaka M, Ohashi S, Wong GS, Takaoka M, et al. (2010) Hypoxia activates the cyclooxygenase-2-prostaglandin E synthase axis. Carcinogenesis 31: 427-434 doi:10.1093/carcin/bgp326.
33. Peng DF, Razvi M, Chen H, Washington K, Roessner A, et al. (2009) DNA hypermethylation regulates the expression of members of the Mu-class glutathione S-transferases and glutathione peroxidases in Barrett's adenocarcinoma. Gut 58: 5-15 doi:10.1136/gut.2007.146290.
34. Schlemper RJ, Kato Y, Stolte M, (2000) Diagnostic criteria for gastrointestinal carcinomas in Japan and Western countries: proposal for a new classification system of gastrointestinal epithelial neoplasia. J. Gastroenterol. Hepatol 15 (Suppl): G49-57.
35. Andl CD, McCowan KM, Allison GL, Rustgi AK, (2010) Cathepsin B is the driving force of esophageal cell invasion in a fibroblast-dependent manner. Neoplasia 12: 485-498.
36. Klingbeil P, Isacke CM, (2011) The "alternative" EMT switch. Breast Cancer Research: BCR 13: 313 doi:10.1186/bcr2915.
37. Bourguignon LYW, Singleton PA, Diedrich F, Stern R, Gilad E, (2004) CD44 interaction with Na+-H+ exchanger (NHE1) creates acidic microenvironments leading to hyaluronidase-2 and cathepsin B activation and breast tumor cell invasion. The Journal of Biological Chemistry 279: 26991-27007.
38. Yu Q, Stamenkovic I, (1999) Localization of matrix metalloproteinase 9 to the cell surface provides a mechanism for CD44-mediated tumor invasion. Genes Dev 13: 35-48.
39. Konig H, Ponta H, Herrlich P, (1998) Coupling of signal transduction to alternative pre-mRNA splicing by a composite splice regulator. EMBO J 17: 2904-2913 doi:10.1093/emboj/17.10.2904.
40. Warzecha CC, Sato TK, Nabet B, Hogenesch JB, Carstens RP, (2009) ESRP1 and ESRP2 are epithelial cell-type-specific regulators of FGFR2 splicing. Molecular Cell 33: 591-601.
41. Brown RL, Reinke LM, Damerow MS, Perez D, Chodosh LA, et al. (2011) CD44 splice isoform switching in human and mouse epithelium is essential for epithelial-mesenchymal transition and breast cancer progression. The Journal of Clinical Investigation 121: 1064-1074.
42. Warzecha CC, Jiang P, Amirikian K, Dittmar KA, Lu H, et al. (2010) An ESRP-regulated splicing programme is abrogated during the epithelial-mesenchymal transition. The EMBO Journal 29: 3286-3300.
43. Warzecha CC, Shen S, Xing Y, Carstens RP, (2009) The epithelial splicing factors ESRP1 and ESRP2 positively and negatively regulate diverse types of alternative splicing events. RNA biology 6: 546.
44. Shapiro IM, Cheng AW, Flytzanis NC, Balsamo M, Condeelis JS, et al. (2011) An EMT-Driven Alternative Splicing Program Occurs in Human Breast Cancer and Modulates Cellular Phenotype. PLoS Genet 7: e1002218 doi:10.1371/journal.pgen.1002218.
45. Fang X, Cai Y, Liu J, Wang Z, Wu Q, et al. (2011) Twist2 contributes to breast cancer progression by promoting an epithelial-mesenchymal transition and cancer stem-like cell self-renewal. Oncogene Available: http://www.ncbi.nlm.nih.gov/pubmed/21602879. Accessed 27 Sep 2011.
46. Xu Y, Yu Q, (2003) E-cadherin negatively regulates CD44-hyaluronan interaction and CD44-mediated tumor invasion and branching morphogenesis. J. Biol. Chem 278: 8661-8668 doi:10.1074/jbc.M208181200.
47. Yu Q, Stamenkovic I, (2000) Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-beta and promotes tumor invasion and angiogenesis. Genes Dev 14: 163-176.
48. Noma K, Smalley KSM, Lioni M, Naomoto Y, Tanaka N, et al. (2008) The essential role of fibroblasts in esophageal squamous cell carcinoma-induced angiogenesis. Gastroenterology 134: 1981-1993 doi:10.1053/j.gastro.2008.02.061.