CD44 Staining of Cancer Stem-Like Cells Is Influenced by Down-Regulation of CD44 Variant Isoforms and Up-Regulation of the Standard CD44 Isoform in the Population of Cells That Have Undergone Epithelial-to-Mesenchymal Transition

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Biddle, Adrian ^a   Gammon, Luke ^a,b   Fazil, Bilal ^a   Mackenzie, Ian C ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY OF BERGEN   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

HERMES ANTIGEN;

ARTICLE; CANCER STEM CELL; CELL CULTURE; CELL ISOLATION; CELL POPULATION; CELL SURFACE; CONTROLLED STUDY; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; EXON; PHENOTYPE; PROTEIN EXPRESSION; UPREGULATION;

ALTERNATIVE SPLICING; ANTIGENS, CD44; ARTIFACTS; CARCINOMA, SQUAMOUS CELL; CELL LINE; EPITHELIAL-MESENCHYMAL TRANSITION; EXONS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MOUTH NEOPLASMS; NEOPLASTIC STEM CELLS; PROGNOSIS; PROTEIN ISOFORMS; SPECIMEN HANDLING; STAINING AND LABELING;

EID: 84874275555     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0057314     Document Type: Article

References (41)

1. Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH, et al. (2006) Cancer stem cells-perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res 66: 9339-9344.
2. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF, (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 100: 3983-3988.
3. Prince ME, Sivanandan R, Kaczorowski A, Wolf GT, Kaplan MJ, et al. (2007) Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proc Natl Acad Sci U S A 104: 973-978.
4. Bonnet D, Dick JE, (1997) Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 3: 730-737.
5. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, et al. (2003) Identification of a cancer stem cell in human brain tumors. Cancer Res 63: 5821-5828.
6. Charafe-Jauffret E, Ginestier C, Iovino F, Tarpin C, Diebel M, et al. (2010) Aldehyde dehydrogenase 1-positive cancer stem cells mediate metastasis and poor clinical outcome in inflammatory breast cancer. Clin Cancer Res 16: 45-55.
7. Gupta PB, Onder TT, Jiang G, Tao K, Kuperwasser C, et al. (2009) Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 138: 645-659.
8. Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW, et al. (2007) Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 1: 313-323.
9. Li X, Lewis MT, Huang J, Gutierrez C, Osborne CK, et al. (2008) Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J Natl Cancer Inst 100: 672-679.
10. Quintana E, Shackleton M, Sabel MS, Fullen DR, Johnson TM, et al. (2008) Efficient tumour formation by single human melanoma cells. Nature 456: 593-598.
11. Ishizawa K, Rasheed ZA, Karisch R, Wang Q, Kowalski J, et al. (2010) Tumor-initiating cells are rare in many human tumors. Cell Stem Cell 7: 279-282.
12. Joshua B, Kaplan MJ, Doweck I, Pai R, Weissman IL, et al. (2012) Frequency of cells expressing CD44, a head and neck cancer stem cell marker: correlation with tumor aggressiveness. Head Neck 34: 42-49.
13. Pang R, Law WL, Chu AC, Poon JT, Lam CS, et al. (2010) A subpopulation of CD26+ cancer stem cells with metastatic capacity in human colorectal cancer. Cell Stem Cell 6: 603-615.
14. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, et al. (2007) ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 1: 555-567.
15. Schatton T, Murphy GF, Frank NY, Yamaura K, Waaga-Gasser AM, et al. (2008) Identification of cells initiating human melanomas. Nature 451: 345-349.
16. Quintana E, Shackleton M, Foster HR, Fullen DR, Sabel MS, et al. (2010) Phenotypic heterogeneity among tumorigenic melanoma cells from patients that is reversible and not hierarchically organized. Cancer Cell 18: 510-523.
17. Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, et al. (2007) Identification of pancreatic cancer stem cells. Cancer Res 67: 1030-1037.
18. Dalerba P, Dylla SJ, Park IK, Liu R, Wang X, et al. (2007) Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci U S A 104: 10158-10163.
19. Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ, (2005) Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res 65: 10946-10951.
20. Wang SJ, Bourguignon LY, (2011) Role of hyaluronan-mediated CD44 signaling in head and neck squamous cell carcinoma progression and chemoresistance. Am J Pathol 178: 956-963.
21. Zoller M, (2011) CD44: can a cancer-initiating cell profit from an abundantly expressed molecule? Nat Rev Cancer 11: 254-267.
22. Bourguignon LY, Spevak CC, Wong G, Xia W, Gilad E, (2009) Hyaluronan-CD44 interaction with protein kinase C(epsilon) promotes oncogenic signaling by the stem cell marker Nanog and the Production of microRNA-21, leading to down-regulation of the tumor suppressor protein PDCD4, anti-apoptosis, and chemotherapy resistance in breast tumor cells. J Biol Chem 284: 26533-26546.
23. Lee JL, Wang MJ, Chen JY, (2009) Acetylation and activation of STAT3 mediated by nuclear translocation of CD44. J Cell Biol 185: 949-957.
24. Tijink BM, Buter J, de Bree R, Giaccone G, Lang MS, et al. (2006) A phase I dose escalation study with anti-CD44v6 bivatuzumab mertansine in patients with incurable squamous cell carcinoma of the head and neck or esophagus. Clin Cancer Res 12: 6064-6072.
25. Wang SJ, Bourguignon LY, (2006) Hyaluronan and the interaction between CD44 and epidermal growth factor receptor in oncogenic signaling and chemotherapy resistance in head and neck cancer. Arch Otolaryngol Head Neck Surg 132: 771-778.
26. 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. J Clin Invest 121: 1064-1074.
27. Hay ED, (2005) The mesenchymal cell, its role in the embryo, and the remarkable signaling mechanisms that create it. Dev Dyn 233: 706-720.
28. Yang MH, Wu MZ, Chiou SH, Chen PM, Chang SY, et al. (2008) Direct regulation of TWIST by HIF-1alpha promotes metastasis. Nat Cell Biol 10: 295-305.
29. Gjerdrum C, Tiron C, Hoiby T, Stefansson I, Haugen H, et al. (2010) Axl is an essential epithelial-to-mesenchymal transition-induced regulator of breast cancer metastasis and patient survival. Proc Natl Acad Sci U S A 107: 1124-1129.
30. Skvortsova I, Skvortsov S, Raju U, Stasyk T, Riesterer O, et al. (2010) Epithelial-to-mesenchymal transition and c-myc expression are the determinants of cetuximab-induced enhancement of squamous cell carcinoma radioresponse. Radiother Oncol 96: 108-115.
31. Bandyopadhyay A, Wang L, Agyin J, Tang Y, Lin S, et al. (2010) Doxorubicin in combination with a small TGFbeta inhibitor: a potential novel therapy for metastatic breast cancer in mouse models. PLoS One 5: e10365.
32. Biddle A, Liang X, Gammon L, Fazil B, Harper LJ, et al. (2011) Cancer stem cells in squamous cell carcinoma switch between two distinct phenotypes that are preferentially migratory or proliferative. Cancer Res 71: 5317-5326.
33. Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T, (2005) Opinion: migrating cancer stem cells- an integrated concept of malignant tumour progression. Nat Rev Cancer 5: 744-749.
34. Cao C, Chen Y, Masood R, Sinha UK, Kobielak A, (2012) alpha-Catulin Marks the Invasion Front of Squamous Cell Carcinoma and Is Important for Tumor Cell Metastasis. Mol Cancer Res 10: 892-903.
35. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, et al. (2008) The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133: 704-715.
36. Anstee DJ, Gardner B, Spring FA, Holmes CH, Simpson KL, et al. (1991) New monoclonal antibodies in CD44 and CD58: their use to quantify CD44 and CD58 on normal human erythrocytes and to compare the distribution of CD44 and CD58 in human tissues. Immunology 74: 197-205.
37. Mackenzie IC, (2004) Growth of malignant oral epithelial stem cells after seeding into organotypical cultures of normal mucosa. J Oral Pathol Med 33: 71-78.
38. Proby CM, Purdie KJ, Sexton CJ, Purkis P, Navsaria HA, et al. (2000) Spontaneous keratinocyte cell lines representing early and advanced stages of malignant transformation of the epidermis. Exp Dermatol 9: 104-117.
39. Locke M, Heywood M, Fawell S, Mackenzie IC, (2005) Retention of intrinsic stem cell hierarchies in carcinoma-derived cell lines. Cancer Res 65: 8944-8950.
40. Friedrichs K, Franke F, Lisboa BW, Kugler G, Gille I, et al. (1995) CD44 isoforms correlate with cellular differentiation but not with prognosis in human breast cancer. Cancer Res 55: 5424-5433.
41. Herold-Mende C, Seiter S, Born AI, Patzelt E, Schupp M, et al. (1996) Expression of CD44 splice variants in squamous epithelia and squamous cell carcinomas of the head and neck. J Pathol 179: 66-73.