Bone morphogenetic protein signaling promotes tumorigenesis in a murine model of high-grade glioma

Neuro-Oncology

Volumn 18, Issue 7, 2016, Pages 928-938

  Hover, Laura D ^a   Owens, Philip ^b   Munden, Alexander L ^a   Wang, Jialiang ^a   Chambless, Lola B ^a   Hopkins, Corey R ^b   Hong, Charles C ^a,b,c   Moses, Harold L ^b   Abel, Ty W ^a  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

BMP; BMPR1a; DMH1; genetically engineered mice; high grade glioma

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN RECEPTOR 1A; SMAD1 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; BMPR1A PROTEIN, MOUSE; BONE MORPHOGENETIC PROTEIN RECEPTOR 1;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BMPR1A GENE; CARCINOGENESIS; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; FEMALE; GENE DELETION; GENE EXPRESSION; GLIOBLASTOMA; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MOUSE; NEWBORN; NONHUMAN; ONCOGENE RAS; SIGNAL TRANSDUCTION; TISSUE MICROARRAY; TUMOR SUPPRESSOR GENE; ANIMAL; CELL TRANSFORMATION; GENE EXPRESSION REGULATION; GENETICS; GLIOMA; METABOLISM; TRANSGENIC MOUSE;

ANIMALS; ASTROCYTES; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; BONE MORPHOGENETIC PROTEINS; CARCINOGENESIS; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; GENE EXPRESSION REGULATION; GLIOMA; MICE, TRANSGENIC; SIGNAL TRANSDUCTION;

EID: 84977483312     PISSN: 15228517     EISSN: 15235866     Source Type: Journal    
DOI: 10.1093/neuonc/nov310     Document Type: Article

References (34)

1. Ostrom QT, Gittleman H, Liao P, et al. CBTRUS statistical report: Primary brain and central nervous system tumors diagnosed in the United States in 2007-2011. Neuro Oncol. 2014;16 (suppl 4):iv1-iv63.
2. Miyazono K, Kamiya Y, Morikawa M. Bone morphogenetic protein receptors and signal transduction. J Biochem. 2010;147(1):35-51.
3. Chen H-L, Panchision DM. Concise review: bone morphogenetic protein pleiotropism in neural stem cells and their derivativesalternative pathways, convergent signals. Stem Cells. 2007; 25(1):63-68.
4. Massague J. TGFbeta in Cancer. Cell. 2008;134(2):215-230.
5. Ehata S, Yokoyama Y, Takahashi K, et al. Bi-directional roles of bone morphogenetic proteins in cancer: Another molecular Jekyll and Hyde? Pathol Int. 2013;63(6):287-296.
6. Yamada N, Kato M, Dijkel P, et al. Bone morphogenetic protein type IB receptor is progressively expressed in malignant glioma tumours. Br J Cancer. 1996;73(5):624-629.
7. Liu C, Tian G, Tu Y, et al. Expression pattern and clinical prognostic relevance of bone morphogenetic protein-2 in human gliomas. Jpn J Clin Oncol. 2009;39(10):625-631.
8. Bao Z, Zhang C, Yan W, et al. BMP4, a strong better prognosis predictor, has a subtype preference and cell development association in gliomas. J Transl Med. 2013;11:1-7.
9. Guo M, Jiang Z, Zhang X, et al. miR-656 inhibits glioma tumorigenesis through repression of BMPR1A. Carcinogenesis. 2014;35(8):1698-1706.
10. Piccirillo SGM, Reynolds BA, Zanetti N, et al. Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature. 2006;444(7120):761-765.
11. Lee J, Son MJ, Woolard K, et al. Epigenetic-mediated dysfunction of the bone morphogenetic protein developmental pathway inhibits differentiation of human glioblastoma tumor initiating cells. Cancer Cell. 2008;13(1):69-80.
12. Ghazi SO, Stark M, Zhao Z, et al. Cell of origin determines tumor phenotype in an oncogenic Ras/p53 knockout transgenic model of high-grade glioma. J Neuropathol Exp Neurol. 2012;71(8):1-12.
13. Mishina Y, Hanks MC, Miura S, et al. Generation of Bmpr/Alk3 conditional knockout mice. Genesis 2002;32(2):69-72.
14. Muzumdar MD, Tasic B, Miyamichi K, et al. A global doublefluorescent cre reporter mouse. Genesis. 2007;45(9):593-605.
15. Carlson BL, Pokorny JL, Schroeder MA, et al. Establishment, maintenance and in vitro and in vivo applications of primary human glioblastoma multiforme (GBM) xenograft models for translational biology studies and drug discovery. Curr Protoc Pharmacol. 2012;52(14):1-14.
16. Pickup MW, Hover LD, Guo Y, et al. Deletion of the BMP receptor BMPR1a impairs mammary tumor formation and metastasis. Oncotarget. 2015;6(26):22890-22904.
17. Bierie B, Chung CH, Parker JS, et al. Abrogation of TGF-beta signaling enhances chemokine production and correlates with prognosis in human breast cancer. J Clin Invest. 2009;119(6): 1571-1582.
18. Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science. 1992;255(5052):1707-1710.
19. Schildge S, Bohrer C, Beck K, et al. Isolation and culture of mouse cortical astrocytes. J Vis Exp. 2013;19(71):50079.
20. Hao J, Ho JN, Lewis JA, et al. In vivo structure activity relationship study of dorsomorphin analogues identifies selective VEGF and BMP inhibitors. ACS Chem Biol. 2010;5(2):245-253.
21. Singh SK, Hawkins CC, Clarke ID, et al. Identification of human brain tumour initiating cells. Nature. 2004;432(7015):396-400.
22. Clément V, Dutoit V, Marino D, et al. Limits of CD133 as a marker of glioma self-renewing cells. Int J Cancer 2009;125(1):244-248.
23. McLendon R, Friedman A, Bigner D, et al. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature. 2008;455(7216):1061-1068.
24. Jeuken J, van den Broecke C, Gijsen S, et al. RAS/RAF pathway activation in gliomas: The result of copy number gains rather than activating mutations. Acta Neuropathol. 2007;114(2): 121-133.
25. Abel TW, Clark C, Bierie B, et al. GFAP-Cre-mediated activation of oncogenic K-ras results in expansion of the subventricular zone and infiltrating glioma. Mol Cancer Res 2009;7(5):645-.
26. Holland EC, Celestino J, Dai C, et al. Combined activation of Ras and Akt in neural progenitors induces glioblastoma formation in mice. Nat Genet. 2000;25(1):55-57.
27. Ding H, Roncari L, Shannon P, et al. Astrocyte-specific expression of activated p21-ras results in malignant astrocytoma formation in a transgenic mouse model of human gliomas astrocyte-specific expression of activated p21-ras results in malignant astrocytoma formation in a transgenic mouse. Cancer Res. 2001; 61(9):3826-3836.
28. Samanta J, Burke GM, McGuire T, et al. BMPR1a signaling determines numbers of oligodendrocytes and calbindin-expressing interneurons in the cortex. J Neurosci. 2007;27(28):7397-7407.
29. Louis DN, Ohgaki H, Wiestler OD, et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol. 2007;114(2):97-109.
30. Hao J, Lee R, Chang A, et al. DMH1, a small molecule inhibitor of BMP type i receptors, suppresses growth and invasion of lung cancer. PLoS One. 2014;9(6):e90748.
31. Owens P, PickupMW, Novitskiy SV, et al. Inhibition of BMP signaling suppresses metastasis in mammary cancer. Oncogene. 2015; 34(19):2437-2449.
32. Virtanen S, Alarmo E-L, Sandström S, et al. Bone morphogenetic protein-4 and-5 in pancreatic cancer-novel bidirectional players. Exp Cell Res. 2011;317(15):2136-2146.
33. Hu Y, Ylivinkka I, Chen P, et al. Netrin-4 promotes glioblastoma cell proliferation through integrin b4 signaling. Neoplasia. 2012;14(3): 219-227.
34. Bao S, Wu Q, McLendon R, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 2006;444(7120):756-760.