Deletion of the WNT target and cancer stem cell marker CD44 in Apc(Min/+) mice attenuates intestinal tumorigenesis

Cancer Research

Volumn 68, Issue 10, 2008, Pages 3655-3661

  Zeilstra, Jurrit ^a   Joosten, Sander P J ^a   Dokter, Maarten ^a   Verwiel, Eugène ^a   Spaargaren, Marcel ^a   Pals, Steven T ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CELL MARKER; HERMES ANTIGEN; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; BOK GENE; C57BL MOUSE; CANCER INHIBITION; CANCER SUSCEPTIBILITY; CELL PROLIFERATION; CELL SURVIVAL; COLON POLYPOSIS; COLORECTAL CANCER; DR6 GENE; EPITHELIUM CELL; GENE; GENE AMPLIFICATION; GENE DELETION; GENE MUTATION; GENE TARGETING; INTESTINE CANCER; INTESTINE CRYPT; MOUSE; MOUSE STRAIN; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; STRAIN DIFFERENCE; ANIMAL; CYTOLOGY; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; INTESTINE TUMOR; METABOLISM; STEM CELL; TRANSGENIC MOUSE; TUMOR SUPPRESSOR GENE;

ANIMALS; ANTIGENS, CD44; APOPTOSIS; EPITHELIAL CELLS; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, APC; INTESTINAL NEOPLASMS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; STEM CELLS; WNT PROTEINS;

EID: 45549109525     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-07-2940     Document Type: Article

References (50)

1. Barker N, van Es JH, Kuipers J, et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007;449:1003-7.
2. Radtke F, Clevers H. Self-renewal and cancer of the gut: two sides of a coin. Science 2005;307:1904-9.
3. Wielenga VJ, Smits R, Korinek V, et al. Expression of CD44 in Apc and Tcf mutant mice implies regulation by the WNT pathway. Am J Pathol 1999;154:515-23.
4. Wielenga VJ, van der Neut R, Offerhaus GJ, Pals ST. CD44 glycoproteins in colorectal cancer: expression, function, and prognostic value. Adv Cancer Res 2000;77:169-87.
5. Pals ST, Hogervorst F, Keizer GD, Thepen T, Horst E, Figdor CC. Identification of a widely distributed 90-kDa glycoprotein that is homologous to the Hermes-1 human lymphocyte homing receptor. J Immunol 1989;143:851-7.
6. Screaton GR, Bell MV, Jackson DG, Cornelis FB, Gerth U, Bell JI. Genomic structure of DNA encoding the lymphocyte homing receptor CD44 reveals at least 12 alternatively spliced exons. Proc Natl Acad Sci U S A 1992;89:12160-4.
7. Jalkanen S, Bargatze RF, de los Toyos J, Butcher EC. Lymphocyte recognition of high endothelium: antibodies to distinct epitopes of an 85-95-kD glycoprotein antigen differentially inhibit lymphocyte binding to lymph node, mucosal, or synovial endothelial cells. J Cell Biol 1987;105:983-90.
8. Herrlich P, Zoller M, Pals ST, Ponta H. CD44 splice variants: metastases meet lymphocytes. Immunol Today 1993;14:395-9.
9. Ayroldi E, Cannarile L, Migliorati G, Bartoli A, Nicoletti I, Riccardi C. CD44 (Pgp-1) inhibits CD3 and dexamethasone-induced apoptosis. Blood 1995;86:2672-8.
10. Ponta H, Sherman L, Herrlich PA. CD44: from adhesion molecules to signalling regulators. Nat Rev Mol Cell Biol 2003;4:33-45.
11. Hauptschein RS, Sloan KE, Torella C, et al. Functional proteomic screen identifies a modulating role for CD44 in death receptor-mediated apoptosis. Cancer Res 2005;65:1887-96.
12. Mielgo A, van Driel M, Bloem A, Landmann L, Gunthert U. A novel antiapoptotic mechanism based on interference of Fas signaling by CD44 variant isoforms. Cell Death Differ 2006;13:465-77.
13. Jackson DG, Bell JI, Dickinson R, Timans J, Shields J, Whittle N. Proteoglycan forms of the lymphocyte homing receptor CD44 are alternatively spliced variants containing the v3 exon. J Cell Biol 1995;128:673-85.
14. van der Voort R, Taher TE, Wielenga VJ, et al. Heparan sulfate-modified CD44 promotes hepatocyte growth factor/scatter factor-induced signal transduction through the receptor tyrosine kinase c-Met. J Biol Chem 1999;274:6499-506.
15. van de Wetering M, Sancho E, Verweij C, et al. The β-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell 2002;111:241-50.
16. Batlle E, Henderson JT, Beghtel H, et al. β-Catenin and TCF mediate cell positioning in the intestinal epithelium by controlling the expression of EphB/ ephrinB. Cell 2002;111:251-63.
17. Filali M, Cheng N, Abbott D, Leontiev V, Engelhardt JF. Wnt-3A/β-catenin signaling induces transcription from the LEF-1 promoter. J Biol Chem 2002;277:33398-410.
18. Jho EH, Zhang T, Domon C, Joo CK, Freund JN, Costantini F. Wnt/β-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol Cell Biol 2002;22:1172-83.
19. Sansom OJ, Meniel VS, Muncan V, et al. Myc deletion rescues Apc deficiency in the small intestine. Nature 2007;446:676-9.
20. Dalerba P, Dylla SJ, Park IK, et al. Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci U S A 2007;104:10158-63.
21. Mulder JW, Kruyt PM, Sewnath M, et al. Colorectal cancer prognosis and expression of exon-v6-containing CD44 proteins. Lancet 1994;344:1470-2.
22. Schmits R, Filmus J, Gerwin N, et al. CD44 regulates hematopoietic progenitor distribution, granuloma formation, and tumorigenicity. Blood 1997;90:2217-33.
23. Moser AR, Pitot HC, Dove WF. A dominant mutation that predisposes to multiple intestinal neoplasia in the mouse. Science 1990;247:322-4.
24. Boivin GP, Washington K, Yang K, et al. Pathology of mouse models of intestinal cancer: consensus report and recommendations. Gastroenterology 2003;124:762-77.
25. Ashburner M, Ball CA, Blake JA, et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nature Genet 2000;25:25-9.
26. Ramakers C, Ruijter JM, Deprez RH, Moorman AF. Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 2003;339:62-6.
27. Moorman AF, Houweling AC, de Boer PA, Christoffels VM. Sensitive nonradioactive detection of mRNA in tissue sections: novel application of the whole-mount in situ hybridization protocol. J Histochem Cytochem 2001;49:1-8.
28. Su LK, Kinzler KW, Vogelstein B, et al. Multiple intestinal neoplasia caused by a mutation in the murine homolog of the APC gene. Science 1992;256:668-70.
29. Bates RC, Edwards NS, Burns GF, Fisher DE. A CD44 survival pathway triggers chemoresistance via lyn kinase and phosphoinositide 3-kinase/Akt in colon carcinoma cells. Cancer Res 2001;61:5275-83.
30. Charrad RS, Gadhoum Z, Qi J, et al. Effects of anti-CD44 monoclonal antibodies on differentiation and apoptosis of human myeloid leukemia cell lines. Blood 2002;99:290-9.
31. Crosnier C, Stamataki D, Lewis J. Organizing cell renewal in the intestine: stem cells, signals and combinatorial control. Nat Rev Genet 2006;7:349-59.
32. Sansom OJ, Reed KR, Hayes AJ, et al. Loss of Apc in vivo immediately perturbs Wnt signaling, differentiation, and migration. Genes Dev 2004;18:1385-90.
33. Merritt AJ, Potten CS, Kemp CJ, et al. The role of p53 in spontaneous and radiation-induced apoptosis in the gastrointestinal tract of normal and p53-deficient mice. Cancer Res 1994;54:614-7.
34. Merritt AJ, Potten CS, Watson AJ, et al. Differential expression of bcl-2 in intestinal epithelia. Correlation with attenuation of apoptosis in colonic crypts and the incidence of colonic neoplasia. J Cell Sci 1995;108: 2261-71.
35. Booth C, Potten CS. Gut instincts: thoughts on intestinal epithelial stem cells. J Clin Invest 2000;105: 1493-9.
36. Salvesen GS, Dixit VM. Caspases: intracellular signaling by proteolysis. Cell 1997;91:443-6.
37. Ghatak S, Misra S, Toole BP. Hyaluronan oligosaccharides inhibit anchorage-independent growth of tumor cells by suppressing the phosphoinositide 3-kinase/Akt cell survival pathway. J Biol Chem 2002; 277:38013-20.
38. Bourguignon LY, Zhu H, Chu A, Iida N, Zhang L, Hung MC. Interaction between the adhesion receptor, CD44, and the oncogene product, p185HER2, promotes human ovarian tumor cell activation. J Biol Chem 1997; 272:27913-8.
39. Yu WH, Woessner JF, Jr., McNeish JD, Stamenkovic I. CD44 anchors the assembly of matrilysin/MMP-7 with heparin-binding epidermal growth factor precursor and ErbB4 and regulates female reproductive organ remodeling. Genes Dev 2002;16:307-23.
40. Taher TE, Smit L, Griffioen AW, Schilder-Tol EJ, Borst J, Pals ST. Signaling through CD44 is mediated by tyrosine kinases. Association with p56lck in T lymphocytes. J Biol Chem 1996;271:2863-7.
41. Tsukita S, Oishi K, Sato N, Sagara J, Kawai A, Tsukita S. ERM family members as molecular linkers between the cell surface glycoprotein CD44 and actin-based cytoskeletons. J Cell Biol 1994;126:391-401.
42. Legg JW, Lewis CA, Parsons M, Ng T, Isacke CM. A novel PKC-regulated mechanism controls CD44 ezrin association and directional cell motility. Nat Cell Biol 2002;4:399-407.
43. Yasuda M, Tanaka Y, Fujii K, Yasumoto K. CD44 stimulation down-regulates Fas expression and Fas-mediated apoptosis of lung cancer cells. Int Immunol 2001;13:1309-19.
44. Lakshman M, Subramaniam V, Rubenthiran U, Jothy S. CD44 promotes resistance to apoptosis in human colon cancer cells. Exp Mol Pathol 2004;77:18-25.
45. Lakshman M, Subramaniam V, Wong S, Jothy S. CD44 promotes resistance to apoptosis in murine colonic epithelium. J Cell Physiol 2005;203:583-8.
46. Rodriguez JM, Glozak MA, Ma Y, Cress WD. Bok, Bcl-2-related ovarian killer, is cell cycle-regulated and sensitizes to stress-induced apoptosis. J Biol Chem 2006;281:22729-35.
47. Pan G, Bauer JH, Haridas V, et al. Identification and functional characterization of DR6, a novel death domain-containing TNF receptor. FEBS Lett 1998;431:351-6.
48. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 2003;100: 3983-8.
49. Li C, Heidt DG, Dalerba P, et al. Identification of pancreatic cancer stem cells. Cancer Res 2007;67:1030-7.
50. Jin L, Hope KJ, Zhai Q, Smadja-Joffe F, Dick JE. Targeting of CD44 eradicates human acute myeloid leukemic stem cells. Nat Med 2006;12:1167-74.