Osteopontin-CD44 signaling in the glioma perivascular niche enhances cancer stem cell phenotypes and promotes aggressive tumor growth

Cell Stem Cell

Volumn 14, Issue 3, 2014, Pages 357-369

  Pietras, Alexander ^a,b,c   Katz, Amanda M ^c   Ekström, Elin J ^c   Wee, Boyoung ^c   Halliday, John J ^c   Pitter, Kenneth L ^c   Werbeck, Jillian L ^c   Amankulor, Nduka M ^d   Huse, Jason T ^c   Holland, Eric C ^a,b  

^a Fred Hutchinson Cancer Research Center   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; E1A ASSOCIATED P300 PROTEIN; GAMMA SECRETASE; HERMES ANTIGEN; HYPOXIA INDUCIBLE FACTOR 2ALPHA; OSTEOPONTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER STEM CELL; CANCER SURVIVAL; CONTROLLED STUDY; CORRELATION ANALYSIS; GENE EXPRESSION; GLIOBLASTOMA; GLIOMA; HUMAN; HUMAN CELL; IN VIVO STUDY; MOLECULAR BIOLOGY; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; RADIOSENSITIVITY; SIGNAL TRANSDUCTION; TUMOR GROWTH; ANIMAL TISSUE; STEM CELL NICHE; SURVIVAL;

ANIMALS; ANTIGENS, CD44; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; E1A-ASSOCIATED P300 PROTEIN; GLIOBLASTOMA; HUMANS; LIGANDS; MICE; NEOPLASM INVASIVENESS; NEOPLASTIC STEM CELLS; OSTEOPONTIN; PHENOTYPE; PLATELET-DERIVED GROWTH FACTOR; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION; STEM CELL NICHE; SURVIVAL ANALYSIS;

ANIMALIA;

EID: 84896107633     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2014.01.005     Document Type: Article

References (48)

1. J. Anido, A. Sáez-Borderías, A. Gonzàlez- Juncà, L. Rodón, G. Folch, M.A. Carmona, R.M. Prieto- Sánchez, I. Barba, E. Martínez-Sáez, and L. Prudkin et al. TGF-β receptor inhibitors target the CD44(high)/Id1(high) glioma-initiating cell population in human glioblastoma Cancer Cell 18 2010 655 668
2. E.E. Bar, A. Lin, V. Mahairaki, W. Matsui, and C.G. Eberhart Hypoxia increases the expression of stem-cell markers and promotes clonogenicity in glioblastoma neurospheres Am. J. Pathol. 177 2010 1491 1502
3. L.E. Barrett, Z. Granot, C. Coker, A. Iavarone, D. Hambardzumyan, E.C. Holland, H.S. Nam, and R. Benezra Self-renewal does not predict tumor growth potential in mouse models of high-grade glioma Cancer Cell 21 2012 11 24
4. A.M. Bleau, D. Hambardzumyan, T. Ozawa, E.I. Fomchenko, J.T. Huse, C.W. Brennan, and E.C. Holland PTEN/PI3K/Akt pathway regulates the side population phenotype and ABCG2 activity in glioma tumor stem-like cells Cell Stem Cell 4 2009 226 235
5. L.Y. Bourguignon, H. Zhu, L. Shao, and Y.W. Chen CD44 interaction with c-Src kinase promotes cortactin-mediated cytoskeleton function and hyaluronic acid-dependent ovarian tumor cell migration J. Biol. Chem. 276 2001 7327 7336
6. C. Calabrese, H. Poppleton, M. Kocak, T.L. Hogg, C. Fuller, B. Hamner, E.Y. Oh, M.W. Gaber, D. Finklestein, and M. Allen et al. A perivascular niche for brain tumor stem cells Cancer Cell 11 2007 69 82
7. Cancer Genome Atlas Research Network Comprehensive genomic characterization defines human glioblastoma genes and core pathways Nature 455 2008 1061 1068
8. N. Charles, T. Ozawa, M. Squatrito, A.M. Bleau, C.W. Brennan, D. Hambardzumyan, and E.C. Holland Perivascular nitric oxide activates notch signaling and promotes stem-like character in PDGF-induced glioma cells Cell Stem Cell 6 2010 141 152
9. K.L. Covello, J. Kehler, H. Yu, J.D. Gordan, A.M. Arsham, C.J. Hu, P.A. Labosky, M.C. Simon, and B. Keith HIF-2alpha regulates Oct-4: effects of hypoxia on stem cell function, embryonic development, and tumor growth Genes Dev. 20 2006 557 570
10. V. De Falco, A. Tamburrino, S. Ventre, M.D. Castellone, M. Malek, S.N. Manié, and M. Santoro CD44 proteolysis increases CREB phosphorylation and sustains proliferation of thyroid cancer cells Cancer Res. 72 2012 1449 1458
11. G.P. Elvidge, L. Glenny, R.J. Appelhoff, P.J. Ratcliffe, J. Ragoussis, and J.M. Gleadle Concordant regulation of gene expression by hypoxia and 2-oxoglutarate-dependent dioxygenase inhibition: the role of HIF-1alpha, HIF-2alpha, and other pathways J. Biol. Chem. 281 2006 15215 15226
12. B.M. Emerling, F. Weinberg, J.L. Liu, T.W. Mak, and N.S. Chandel PTEN regulates p300-dependent hypoxia-inducible factor 1 transcriptional activity through Forkhead transcription factor 3a (FOXO3a) Proc. Natl. Acad. Sci. USA 105 2008 2622 2627
13. X. Fan, W. Matsui, L. Khaki, D. Stearns, J. Chun, Y.M. Li, and C.G. Eberhart Notch pathway inhibition depletes stem-like cells and blocks engraftment in embryonal brain tumors Cancer Res. 66 2006 7445 7452
14. S. Godar, T.A. Ince, G.W. Bell, D. Feldser, J.L. Donaher, J. Bergh, A. Liu, K. Miu, R.S. Watnick, and F. Reinhardt et al. Growth-inhibitory and tumor- suppressive functions of p53 depend on its repression of CD44 expression Cell 134 2008 62 73
15. A. Golebiewska, N.H. Brons, R. Bjerkvig, and S.P. Niclou Critical appraisal of the side population assay in stem cell and cancer stem cell research Cell Stem Cell 8 2011 136 147
16. J.D. Gordan, P. Lal, V.R. Dondeti, R. Letrero, K.N. Parekh, C.E. Oquendo, R.A. Greenberg, K.T. Flaherty, W.K. Rathmell, and B. Keith et al. HIF-alpha effects on c-Myc distinguish two subtypes of sporadic VHL-deficient clear cell renal carcinoma Cancer Cell 14 2008 435 446
17. D. Hambardzumyan, O.J. Becher, M.K. Rosenblum, P.P. Pandolfi, K. Manova-Todorova, and E.C. Holland PI3K pathway regulates survival of cancer stem cells residing in the perivascular niche following radiation in medulloblastoma in vivo Genes Dev. 22 2008 436 448
18. A.L. Harris Hypoxia - a key regulatory factor in tumour growth Nat. Rev. Cancer 2 2002 38 47
19. D.N. Haylock, and S.K. Nilsson Stem cell regulation by the hematopoietic stem cell niche Cell Cycle 4 2005 1353 1355
20. E.C. Holland, W.P. Hively, R.A. DePinho, and H.E. Varmus A constitutively active epidermal growth factor receptor cooperates with disruption of G1 cell-cycle arrest pathways to induce glioma-like lesions in mice Genes Dev. 12 1998 3675 3685
21. K.H. Hsu, H.W. Tsai, P.W. Lin, Y.S. Hsu, Y.S. Shan, and P.J. Lu Clinical implication and mitotic effect of CD44 cleavage in relation to osteopontin/CD44 interaction and dysregulated cell cycle protein in gastrointestinal stromal tumor Ann. Surg. Oncol. 17 2010 2199 2212
22. J.T. Huse, and E.C. Holland Targeting brain cancer: advances in the molecular pathology of malignant glioma and medulloblastoma Nat. Rev. Cancer 10 2010 319 331
23. A. Jögi, I. ∅ra, H. Nilsson, A. Lindeheim, Y. Makino, L. Poellinger, H. Axelson, and S. Påhlman Hypoxia alters gene expression in human neuroblastoma cells toward an immature and neural crest-like phenotype Proc. Natl. Acad. Sci. USA 99 2002 7021 7026
24. A.M. Katz, N.M. Amankulor, K. Pitter, K. Helmy, M. Squatrito, and E.C. Holland Astrocyte-specific expression patterns associated with the PDGF-induced glioma microenvironment PLoS ONE 7 2012 e32453
25. B. Keith, and M.C. Simon Hypoxia-inducible factors, stem cells, and cancer Cell 129 2007 465 472
26. Z. Li, S. Bao, Q. Wu, H. Wang, C. Eyler, S. Sathornsumetee, Q. Shi, Y. Cao, J. Lathia, and R.E. McLendon et al. Hypoxia-inducible factors regulate tumorigenic capacity of glioma stem cells Cancer Cell 15 2009 501 513
27. D.J. Manalo, A. Rowan, T. Lavoie, L. Natarajan, B.D. Kelly, S.Q. Ye, J.G. Garcia, and G.L. Semenza Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1 Blood 105 2005 659 669
28. J. Mathieu, Z. Zhang, W. Zhou, A.J. Wang, J.M. Heddleston, C.M. Pinna, A. Hubaud, B. Stadler, M. Choi, and M. Bar et al. HIF induces human embryonic stem cell markers in cancer cells Cancer Res. 71 2011 4640 4652
29. K.E. Miletti-González, K. Murphy, M.N. Kumaran, A.K. Ravindranath, R.P. Wernyj, S. Kaur, G.D. Miles, E. Lim, R. Chan, and M. Chekmareva et al. Identification of function for CD44 intracytoplasmic domain (CD44-ICD): modulation of matrix metalloproteinase 9 (MMP-9) transcription via novel promoter response element J. Biol. Chem. 287 2012 18995 19007
30. D. Murakami, I. Okamoto, O. Nagano, Y. Kawano, T. Tomita, T. Iwatsubo, B. De Strooper, E. Yumoto, and H. Saya Presenilin-dependent gamma-secretase activity mediates the intramembranous cleavage of CD44 Oncogene 22 2003 1511 1516
31. O. Nagano, and H. Saya Mechanism and biological significance of CD44 cleavage Cancer Sci. 95 2004 930 935
32. O. Nagano, D. Murakami, D. Hartmann, B. De Strooper, P. Saftig, T. Iwatsubo, M. Nakajima, M. Shinohara, and H. Saya Cell-matrix interaction via CD44 is independently regulated by different metalloproteinases activated in response to extracellular Ca(2+) influx and PKC activation J. Cell Biol. 165 2004 893 902
33. I. Okamoto, Y. Kawano, D. Murakami, T. Sasayama, N. Araki, T. Miki, A.J. Wong, and H. Saya Proteolytic release of CD44 intracellular domain and its role in the CD44 signaling pathway J. Cell Biol. 155 2001 755 762
34. L. Pelletier, P. Guillaumot, B. Frêche, C. Luquain, D. Christiansen, S. Brugière, J. Garin, and S.N. Manié Gamma-secretase-dependent proteolysis of CD44 promotes neoplastic transformation of rat fibroblastic cells Cancer Res. 66 2006 3681 3687
35. H.S. Phillips, S. Kharbanda, R. Chen, W.F. Forrest, R.H. Soriano, T.D. Wu, A. Misra, J.M. Nigro, H. Colman, and L. Soroceanu et al. Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis Cancer Cell 9 2006 157 173
36. A. Pietras Cancer stem cells in tumor heterogeneity Adv. Cancer Res. 112 2011 255 281
37. A. Pietras, D. Gisselsson, I. Ora, R. Noguera, S. Beckman, S. Navarro, and S. Påhlman High levels of HIF-2alpha highlight an immature neural crest-like neuroblastoma cell cohort located in a perivascular niche J. Pathol. 214 2008 482 488
38. A. Pietras, A.S. Johnsson, and S. Påhlman The HIF-2α-driven pseudo-hypoxic phenotype in tumor aggressiveness, differentiation, and vascularization Curr. Top. Microbiol. Immunol. 345 2010 1 20
39. G.L. Semenza Hypoxia-inducible factor 1 (HIF-1) pathway Sci. STKE 2007 2007 cm8
40. S.K. Singh, I.D. Clarke, M. Terasaki, V.E. Bonn, C. Hawkins, J. Squire, and P.B. Dirks Identification of a cancer stem cell in human brain tumors Cancer Res. 63 2003 5821 5828
41. A. Soeda, M. Park, D. Lee, A. Mintz, A. Androutsellis-Theotokis, R.D. McKay, J. Engh, T. Iwama, T. Kunisada, and A.B. Kassam et al. Hypoxia promotes expansion of the CD133-positive glioma stem cells through activation of HIF-1alpha Oncogene 28 2009 3949 3959
42. Y.J. Su, H.M. Lai, Y.W. Chang, G.Y. Chen, and J.L. Lee Direct reprogramming of stem cell properties in colon cancer cells by CD44 EMBO J. 30 2011 3186 3199
43. J. Vandesompele, K. De Preter, F. Pattyn, B. Poppe, N. Van Roy, A. De Paepe, and F. Speleman Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes Genome Biol 3 2002 RESEARCH0034
44. R.G. Verhaak, K.A. Hoadley, E. Purdom, V. Wang, Y. Qi, M.D. Wilkerson, C.R. Miller, L. Ding, T. Golub, J.P. Mesirov Cancer Genome Atlas Research Network Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1 Cancer Cell 17 2010 98 110
45. J.M. Weiss, A.C. Renkl, C.S. Maier, M. Kimmig, L. Liaw, T. Ahrens, S. Kon, M. Maeda, H. Hotta, T. Uede, and J.C. Simon Osteopontin is involved in the initiation of cutaneous contact hypersensitivity by inducing Langerhans and dendritic cell migration to lymph nodes J. Exp. Med. 194 2001 1219 1229
46. S.C. Winter, F.M. Buffa, P. Silva, C. Miller, H.R. Valentine, H. Turley, K.A. Shah, G.J. Cox, R.J. Corbridge, and J.J. Homer et al. Relation of a hypoxia metagene derived from head and neck cancer to prognosis of multiple cancers Cancer Res. 67 2007 3441 3449
47. Q. Yan, S. Bartz, M. Mao, L. Li, and W.G. Kaelin Jr. The hypoxia-inducible factor 2alpha N-terminal and C-terminal transactivation domains cooperate to promote renal tumorigenesis in vivo Mol. Cell. Biol. 27 2007 2092 2102
48. M. Zöller CD44: can a cancer-initiating cell profit from an abundantly expressed molecule? Nat. Rev. Cancer 11 2011 254 267