CD44V6 regulates growth of brain tumor stem cells partially through the AKT-mediated pathway

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Jijiwa, Mayumi ^a   Demir, Habibe ^a   Gupta, Snehalata ^a   Leung, Crystal ^b   Joshi, Kaushal ^a   Orozco, Nicholas ^b   Huang, Tiffany ^b   Yildiz, Vedat O ^a   Shibahara, Ichiyo ^b   de Jesus, Jason A ^b   Yong, William H ^b   Mischel, Paul S ^b   Fernandez, Soledad ^a   Kornblum, Harley I ^b   Nakano, Ichiro ^a,c  

^a OHIO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD44V6 ANTIGEN; OSTEOPONTIN; PROTEIN KINASE B; HERMES ANTIGEN; SMALL INTERFERING RNA;

ADULT; AGED; ANTIGEN DETECTION; ARTICLE; CANCER GROWTH; CANCER INHIBITION; CANCER STEM CELL; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; FEMALE; GLIOBLASTOMA; GROWTH REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; INTRACRANIAL TUMOR; MALE; NEURAL STEM CELL; NUCLEOTIDE SEQUENCE; PROGNOSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN VARIANT; ANIMAL; CYTOLOGY; FLOW CYTOMETRY; GENETICS; IMMUNOHISTOCHEMISTRY; METABOLISM; MOUSE; MOUSE MUTANT; NONOBESE DIABETIC MOUSE; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TISSUE MICROARRAY; TUMOR CELL CULTURE; WESTERN BLOTTING;

ANIMALS; ANTIGENS, CD44; BLOTTING, WESTERN; FLOW CYTOMETRY; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED NOD; MICE, SCID; NEOPLASTIC STEM CELLS; OSTEOPONTIN; PROTO-ONCOGENE PROTEINS C-AKT; REAL-TIME POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TISSUE ARRAY ANALYSIS; TUMOR CELLS, CULTURED;

EID: 80052445685     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0024217     Document Type: Article

References (49)

1. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, et al. (2006) Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444: 756-760.
2. Sathornsumetee S, Rich JN, (2006) New treatment strategies for malignant gliomas. Expert Rev Anticancer Ther 6: 1087-1104.
3. Boudreau CR, Yang I, Liau LM, (2005) Gliomas: advances in molecular analysis and characterization. Surg Neurol 64: 286-294; discussion 294.
4. 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.
5. Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, et al. (2004) Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 64: 7011-7021.
6. Nakano I, Saigusa K, Kornblum HI, (2008) BMPing off glioma stem cells. Cancer Cell 13: 3-4.
7. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, et al. (2004) Identification of human brain tumour initiating cells. Nature 432: 396-401.
8. Clement V, Sanchez P, de Tribolet N, Radovanovic I, Ruiz i Altaba A, (2007) HEDGEHOG-GLI1 signaling regulates human glioma growth, cancer stem cell self-renewal, and tumorigenicity. Curr Biol 17: 165-172.
9. Goodison S, Urquidi V, Tarin D, (1999) CD44 cell adhesion molecules. Mol Pathol 52: 189-196.
10. Gotte M, Yip GW, (2006) Heparanase, hyaluronan, and CD44 in cancers: a breast carcinoma perspective. Cancer Res 66: 10233-10237.
11. Marhaba R, Zoller M, (2004) CD44 in cancer progression: adhesion, migration and growth regulation. J Mol Histol 35: 211-231.
12. Gladson CL, (1999) The extracellular matrix of gliomas: modulation of cell function. J Neuropathol Exp Neurol 58: 1029-1040.
13. Xu Y, Stamenkovic I, Yu Q, (2010) CD44 attenuates activation of the hippo signaling pathway and is a prime therapeutic target for glioblastoma. Cancer Res 70: 2455-2464.
14. Anido J, Saez-Borderias A, Gonzalez-Junca A, Rodon L, Folch G, et al. (2010) TGF-beta Receptor Inhibitors Target the CD44(high)/Id1(high) Glioma-Initiating Cell Population in Human Glioblastoma. Cancer Cell 18: 655-668.
15. Naor D, Sionov RV, Ish-Shalom D, (1997) CD44: structure, function, and association with the malignant process. Adv Cancer Res 71: 241-319.
16. Iczkowski KA, Bai S, Pantazis CG, (2003) Prostate cancer overexpresses CD44 variants 7-9 at the messenger RNA and protein level. Anticancer Res 23: 3129-3140.
17. Georgolios A, Batistatou A, Charalabopoulos A, Manolopoulos L, Charalabopoulos K, (2006) The role of CD44 adhesion molecule in oral cavity cancer. Exp Oncol 28: 94-98.
18. Bates RC, Edwards NS, Burns GF, Fisher DE, (2001) A CD44 survival pathway triggers chemoresistance via lyn kinase and phosphoinositide 3-kinase/Akt in colon carcinoma cells. Cancer Res 61: 5275-5283.
19. Hovinga KE, Shimizu F, Wang R, Panagiotakos G, Van Der Heijden M, et al. (2010) Inhibition of notch signaling in glioblastoma targets cancer stem cells via an endothelial cell intermediate. Stem Cells 28: 1019-1029.
20. Khan SA, Cook AC, Kappil M, Gunthert U, Chambers AF, et al. (2005) Enhanced cell surface CD44 variant (v6, v9) expression by osteopontin in breast cancer epithelial cells facilitates tumor cell migration: novel post-transcriptional, post-translational regulation. Clin Exp Metastasis 22: 663-673.
21. Christofori G, (2003): Changing neighbours, changing behaviour: cell adhesion molecule-mediated signalling during tumour progression. EMBO J 22: 2318-2323.
22. Saleh F, Reno W, (2008) Invasive cribriform breast carcinomas in patients with grade 1 and stage IIA (T2 N0 M0) breast cancer strongly express the v3 and v6, but not the v4 isoforms of the metastatic marker CD44. Neoplasma 55: 246-255.
23. Akisik E, Bavbek S, Dalay N, (2002) CD44 variant exons in leukemia and lymphoma. Pathol Oncol Res 8: 36-40.
24. Lee JL, Wang MJ, Sudhir PR, Chen GD, Chi CW, et al. (2007) Osteopontin promotes integrin activation through outside-in and inside-out mechanisms: OPN-CD44V interaction enhances survival in gastrointestinal cancer cells. Cancer Res 67: 2089-2097.
25. Dontu G, Liu S, Wicha MS, (2005) Stem cells in mammary development and carcinogenesis: implications for prevention and treatment. Stem Cell Rev 1: 207-213.
26. Beier D, Rohrl S, Pillai DR, Schwarz S, Kunz-Schughart LA, et al. (2008) Temozolomide preferentially depletes cancer stem cells in glioblastoma. Cancer Res 68: 5706-5715.
27. Lee CJ, Dosch J, Simeone DM, (2008) Pancreatic cancer stem cells. J Clin Oncol 26: 2806-2812.
28. Yang YM, Chang JW, (2008) Bladder cancer initiating cells (BCICs) are among EMA-CD44v6+ subset: novel methods for isolating undetermined cancer stem (initiating) cells. Cancer Invest 26: 725-733.
29. Nakano I, Masterman-Smith M, Saigusa K, Paucar AA, Horvath S, et al. (2008) Maternal embryonic leucine zipper kinase is a key regulator of the proliferation of malignant brain tumors, including brain tumor stem cells. J Neurosci Res 86: 48-60.
30. Nakano I, Paucar AA, Bajpai R, Dougherty JD, Zewail A, et al. (2005) Maternal embryonic leucine zipper kinase (MELK) regulates multipotent neural progenitor proliferation. J Cell Biol 170: 413-427.
31. Ylagan LR, Quinn B, (1997) CD44 expression in astrocytic tumors. Mod Pathol 10: 1239-1246.
32. Ranuncolo SM, Ladeda V, Specterman S, Varela M, Lastiri J, et al. (2002) CD44 expression in human gliomas. J Surg Oncol 79: 30-35; discussion 35-36.
33. Nakano I, Joshi K, Visneyi K, Hu B, Watanabe M, et al. (2011) Siomycin A targets brain tumor stem cells partially through a MELK-mediated pathway. Neuro Oncology pp. 622-34.
34. Vescovi AL, Galli R, Reynolds BA, (2006) Brain tumour stem cells. Nat Rev Cancer 6: 425-436.
35. Jin L, Hope KJ, Zhai Q, Smadja-Joffe F, Dick JE, (2006) Targeting of CD44 eradicates human acute myeloid leukemic stem cells. Nat Med 12: 1167-1174.
36. Xu Y, Stamenkovic I, Yu Q, (2010) CD44 attenuates activation of the hippo signaling pathway and is a prime therapeutic target for glioblastoma. Cancer Res 70: 2455-2464.
37. Wiranowska M, Ladd S, Moscinski LC, Hill B, Haller E, et al. (2010) Modulation of hyaluronan production by CD44 positive glioma cells. Int J Cancer 127: 532-542.
38. Katoh S, Matsumoto N, Kawakita K, Tominaga A, Kincade PW, et al. (2003) A role for CD44 in an antigen-induced murine model of pulmonary eosinophilia. J Clin Invest 111: 1563-1570.
39. Lee J, Kotliarova S, Kotliarov Y, Li A, Su Q, et al. (2006) Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell 9: 391-403.
40. Laks DR, Masterman-Smith M, Visnyei K, Angenieux B, Orozco NM, et al. (2009) Neurosphere formation is an independent predictor of clinical outcome in malignant glioma. Stem Cells 27: 980-987.
41. Lin YH, Yang-Yen HF, (2001) The osteopontin-CD44 survival signal involves activation of the phosphatidylinositol 3-kinase/Akt signaling pathway. J Biol Chem 276: 46024-46030.
42. Dirks PB, Brain tumor stem cells (2010): the cancer stem cell hypothesis writ large. Mol Oncol 4: 420-430.
43. Dirks P, Cancer stem cells (2010): Invitation to a second round. Nature 466: 40-41.
44. Diamandis P, Wildenhain J, Clarke ID, Sacher AG, Graham J, et al. (2007) Chemical genetics reveals a complex functional ground state of neural stem cells. Nat Chem Biol 3: 268-273.
45. Sonoda Y, Ozawa T, Aldape KD, Deen DF, Berger MS, et al. (2001) Akt pathway activation converts anaplastic astrocytoma to glioblastoma multiforme in a human astrocyte model of glioma. Cancer Res 61: 6674-6678.
46. Lagadec C, Vlashi E, Della Donna L, Meng Y, Dekmezian C, et al. (2010) Survival and self-renewing capacity of breast cancer initiating cells during fractionated radiation treatment. Breast Cancer Res 12: R13.
47. Chakravarti A, Zhai G, Suzuki Y, Sarkesh S, Black PM, et al. (2004) The prognostic significance of phosphatidylinositol 3-kinase pathway activation in human gliomas. J Clin Oncol 22: 1926-1933.
48. Gallia GL, Tyler BM, Hann CL, Siu IM, Giranda VL, et al. (2009) Inhibition of Akt inhibits growth of glioblastoma and glioblastoma stem-like cells. Mol Cancer Ther 8: 386-393.
49. Eyler CE, Foo WC, LaFiura KM, McLendon RE, Hjelmeland AB, et al. (2008) Brain cancer stem cells display preferential sensitivity to Akt inhibition. Stem Cells 26: 3027-3036.