PDE7B is a novel, prognostically significant mediator of glioblastoma growth whose expression is regulated by endothelial cells

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Brooks, Michael D ^a   Jackson, Erin ^a,b   Warrington, Nicole M ^a   Luo, Jingqin ^a   Forys, Jason T ^a   Taylor, Sara ^a   Mao, Diane D ^a   Leonard, Jeffrey R ^a   Kim, Albert H ^a   Piwnica Worms, David ^a,b,c   Mitra, Robi D ^a   Rubin, Joshua B ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP PHOSPHODIESTERASE; PHOSPHODIESTERASE VII;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CARCINOGENICITY; CELL INTERACTION; CELL SUBPOPULATION; CONTROLLED STUDY; ENDOTHELIUM CELL; GENE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; GENE OVEREXPRESSION; GLIOBLASTOMA; HUMAN; HUMAN TISSUE; MOUSE; NONHUMAN; PDE7B GENE; TUMOR MICROENVIRONMENT; UPREGULATION; ANIMAL; CANCER STEM CELL; CELL COMMUNICATION; CELL CULTURE; COCULTURE; METABOLISM; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; STEM CELL NICHE; TUMOR CELL LINE;

ANIMALS; CELL COMMUNICATION; CELL LINE, TUMOR; CELLS, CULTURED; COCULTURE TECHNIQUES; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 7; ENDOTHELIAL CELLS; GLIOBLASTOMA; HUMANS; MICE; MICE, NUDE; NEOPLASTIC STEM CELLS; STEM CELL NICHE;

EID: 84929938841     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0107397     Document Type: Article

References (62)

1. Kocher B, Piwnica-Worms D (2013) Illuminating cancer systems with genetically engineered mouse models and coupled luciferase reporters in vivo. Cancer Discov 3: 616-629.
2. Sottoriva A, Spiteri I, Piccirillo SG, Touloumis A, Collins VP, et al. (2013) Intratumor heterogeneity in human glioblastoma reflects cancer evolutionary dynamics. Proc Natl Acad Sci U S A 110: 4009-4014.
3. Denysenko T, Gennero L, Roos MA, Melcarne A, Juenemann C, et al. (2010) Glioblastoma cancer stem cells: heterogeneity, microenvironment and related therapeutic strategies. Cell Biochem Funct 28: 343-351.
4. Gorin F, Harley W, Schnier J, Lyeth B, Jue T (2004) Perinecrotic glioma proliferation and metabolic profile within an intracerebral tumor xenograft. Acta Neuropathol 107: 235-244.
5. Wang J, Sullenger BA, Rich JN (2012) Notch signaling in cancer stem cells. Adv Exp Med Biol 727: 174-185.
6. Guo P, Imanishi Y, Cackowski FC, Jarzynka MJ, Tao HQ, et al. (2005) Upregulation of angiopoietin-2, matrix metalloprotease-2, membrane type 1 metalloprotease, and laminin 5 gamma 2 correlates with the invasiveness of human glioma. Am J Pathol 166: 877-890.
7. Chekenya M, Enger PO, Thorsen F, Tysnes BB, Al-Sarraj S, et al. (2002) The glial precursor proteoglycan, NG2, is expressed on tumour neovasculature by vascular pericytes in human malignant brain tumours. Neuropathol Appl Neurobiol 28: 367-380.
8. Rath BH, Fair JM, Jamal M, Camphausen K, Tofilon PJ (2013) Astrocytes enhance the invasion potential of glioblastoma stem-like cells. PLoS One 8: e54752.
9. Hussain SF, Yang D, Suki D, Aldape K, Grimm E, et al. (2006) The role of human glioma-infiltrating microglia/macrophages in mediating antitumor immune responses. Neuro Oncol 8: 261-279.
10. Calabrese C, Poppleton H, Kocak M, Hogg TL, Fuller C, et al. (2007) A perivascular niche for brain tumor stem cells. Cancer Cell 11: 69-82.
11. Eyler CE, Wu Q, Yan K, MacSwords JM, Chandler-Militello D, et al. (2011) Glioma stem cell proliferation and tumor growth are promoted by nitric oxide synthase-2. Cell 146: 53-66.
12. Charalambous C, Hofman FM, Chen TC (2005) Functional and phenotypic differences between glioblastoma multiforme-derived and normal human brain endothelial cells. J Neurosurg 102: 699-705.
13. Rao S, Sengupta R, Choe EJ, Woerner BM, Jackson E, et al. (2012) CXCL12 mediates trophic interactions between endothelial and tumor cells in glioblastoma. PLoS One 7: e33005.
14. Arnaoutova I, Kleinman HK (2010) In vitro angiogenesis: endothelial cell tube formation on gelled basement membrane extract. Nat Protoc 5: 628-635.
15. Morrison C, Mancini S, Cipollone J, Kappelhoff R, Roskelley C, et al. (2011) Microarray and proteomic analysis of breast cancer cell and osteoblast cocultures: role of osteoblast matrix metalloproteinase (MMP)-13 in bone metastasis. The Journal of biological chemistry 286: 34271-34285.
16. Santos RP, Benvenuti TT, Honda ST, Del Valle PR, Katayama ML, et al. (2011) Influence of the interaction between nodal fibroblast and breast cancer cells on gene expression. Tumour biology: the journal of the International Society for Oncodevelopmental Biology and Medicine 32: 145-157.
17. Lawler J (2002) Thrombospondin-1 as an endogenous inhibitor of angiogenesis and tumor growth. J Cell Mol Med 6: 1-12.
18. Tang KH, Ma S, Lee TK, Chan YP, Kwan PS, et al. (2012) CD133(+) liver tumor-initiating cells promote tumor angiogenesis, growth, and self-renewal through neurotensin/interleukin-8/CXCL1 signaling. Hepatology 55: 807-820.
19. Yamamoto S, Nishimura O, Misaki K, Nishita M, Minami Y, et al. (2008) Cthrc1 selectively activates the planar cell polarity pathway of Wnt signaling by stabilizing the Wnt-receptor complex. Dev Cell 15: 23-36.
20. Zhang Z, Schittenhelm J, Guo K, Buhring HJ, Trautmann K, et al. (2006) Upregulation of frizzled 9 in astrocytomas. Neuropathol Appl Neurobiol 32: 615-624.
21. Fodde R, Brabletz T (2007) Wnt/beta-catenin signaling in cancer stemness and malignant behavior. Curr Opin Cell Biol 19: 150-158.
22. Hetman JM, Soderling SH, Glavas NA, Beavo JA (2000) Cloning and characterization of PDE7B, a cAMP-specific phosphodiesterase. Proc Natl Acad Sci U S A 97: 472-476.
23. Warrington NM, Gianino SM, Jackson E, Goldhoff P, Garbow JR, et al. (2010) Cyclic AMP suppression is sufficient to induce gliomagenesis in a mouse model of neurofibromatosis-1. Cancer Res 70: 5717-5727.
24. Goldhoff P, Warrington NM, Limbrick DD Jr, Hope A, Woerner BM, et al. (2008) Targeted inhibition of cyclic AMP phosphodiesterase-4 promotes brain tumor regression. Clin Cancer Res 14: 7717-7725.
25. Sengupta R, Sun T, Warrington NM, Rubin JB (2011) Treating brain tumors with PDE4 inhibitors. Trends in pharmacological sciences 32: 337-344.
26. Yang L, Jackson E, Woerner BM, Perry A, Piwnica-Worms D, et al. (2007) Blocking CXCR4-Mediated Cyclic AMP Suppression Inhibits Brain Tumor Growth In vivo. Cancer Res 67: 651-658.
27. Yue XS, Fujishiro M, Nishioka C, Arai T, Takahashi E, et al. (2012) Feeder cells support the culture of induced pluripotent stem cells even after chemical fixation. PLoS One 7: e32707.
28. Murat A, Migliavacca E, Gorlia T, Lambiv WL, Shay T, et al. (2008) Stem cellrelated ''self-renewal'' signature and high epidermal growth factor receptor expression associated with resistance to concomitant chemoradiotherapy in glioblastoma. J Clin Oncol. 26(18): 3015-24. doi:10.1200/JCO.2007.15.7164.
29. Sun L, Hui AM, Su Q, Vortmeyer A, Kotliarov Y, et al. (2006) Neuronal and glioma-derived stem cell factor induces angiogenesis within the brain. Cancer Cell. 9(4): 287-300.
30. Woerner BM, Luo J, Brown KR, Jackson E, Dahiya SM, et al. (2012) Suppression of G-protein-coupled receptor kinase 3 expression is a feature of classical GBM that is required for maximal growth. Mol Cancer Res 10: 156-166.
31. Murat A, Migliavacca E, Gorlia T, Lambiv WL, Shay T, et al. (2008) Stem cellrelated ''self-renewal'' signature and high epidermal growth factor receptor expression associated with resistance to concomitant chemoradiotherapy in glioblastoma. J Clin Oncol 26: 3015-3024.
32. Baillie GS, Sood A, McPhee I, Gall I, Perry SJ, et al. (2003) beta-Arrestinmediated PDE4 cAMP phosphodiesterase recruitment regulates beta-adrenoceptor switching from Gs to Gi. Proc Natl Acad Sci U S A 100: 940-945.
33. Zhao Y, Xiao A, diPierro CG, Carpenter JE, Abdel-Fattah R, et al. (2010) An extensive invasive intracranial human glioblastoma xenograft model: role of high level matrix metalloproteinase 9. Am J Pathol 176: 3032-3049.
34. Xu CP, Zhang HR, Chen FL, Yao XH, Liang ZQ, et al. (2010) Human malignant glioma cells expressing functional formylpeptide receptor recruit endothelial progenitor cells for neovascularization. Int Immunopharmacol 10: 1602-1607.
35. Bao S, Wu Q, Sathornsumetee S, Hao Y, Li Z, et al. (2006) Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res 66: 7843-7848.
36. Delort L, Lequeux C, Dubois V, Dubouloz A, Billard H, et al. (2013) Reciprocal interactions between breast tumor and its adipose microenvironment based on a 3D adipose equivalent model. PLoS One 8: e66284.
37. Zhu TS, Costello MA, Talsma CE, Flack CG, Crowley JG, et al. (2011) Endothelial cells create a stem cell niche in glioblastoma by providing NOTCH ligands that nurture self-renewal of cancer stem-like cells. Cancer Res 71: 6061-6072.
38. Keunen O, Johansson M, Oudin A, Sanzey M, Rahim SA, et al. (2011) Anti- VEGF treatment reduces blood supply and increases tumor cell invasion in glioblastoma. Proc Natl Acad Sci U S A 108: 3749-3754.
39. Lu P, Nakorchevskiy A, Marcotte EM (2003) Expression deconvolution: a reinterpretation of DNA microarray data reveals dynamic changes in cell populations. Proc Natl Acad Sci U S A 100: 10370-10375.
40. Gong T, Hartmann N, Kohane IS, Brinkmann V, Staedtler F, et al. (2011) Optimal deconvolution of transcriptional profiling data using quadratic programming with application to complex clinical blood samples. PLoS One 6: e27156.
41. Ahn J, Yuan Y, Parmigiani G, Suraokar MB, Diao L, et al. (2013) DeMix: deconvolution for mixed cancer transcriptomes using raw measured data. Bioinformatics 29: 1865-1871.
42. Furman MA, Shulman K (1977) Cyclic AMP and adenyl cyclase in brain tumors. J Neurosurg 46: 477-483.
43. Stork PJ, Schmitt JM (2002) Crosstalk between cAMP and MAP kinase signaling in the regulation of cell proliferation. Trends Cell Biol 12: 258-266.
44. Prasad KN, Kumar S (1975) Role of cyclic AMP in differentiation of human neuroblastoma cells in culture. Cancer 36: 1338-1343.
45. Houslay MD (2010) Underpinning compartmentalised cAMP signalling through targeted cAMP breakdown. Trends Biochem Sci 35: 91-100.
46. Conti M, Beavo J (2007) Biochemistry and physiology of cyclic nucleotide phosphodiesterases: essential components in cyclic nucleotide signaling. Annu Rev Biochem 76: 481-511.
47. Ponsioen B, Zhao J, Riedl J, Zwartkruis F, van der Krogt G, et al. (2004) Detecting cAMP-induced Epac activation by fluorescence resonance energy transfer: Epac as a novel cAMP indicator. EMBO Rep 5: 1176-1180.
48. Bolger GB, Baillie GS, Li X, Lynch MJ, Herzyk P, et al. (2006) Scanning peptide array analyses identify overlapping binding sites for the signalling scaffold proteins, beta-arrestin and RACK1, in cAMP-specific phosphodiesterase PDE4D5. Biochem J 398: 23-36.
49. Perry SJ, Baillie GS, Kohout TA, McPhee I, Magiera MM, et al. (2002) Targeting of cyclic AMP degradation to beta 2-adrenergic receptors by betaarrestins. Science 298: 834-836.
50. Shakur Y, Pryde JG, Houslay MD (1993) Engineered deletion of the unique Nterminal domain of the cyclic AMP-specific phosphodiesterase RD1 prevents plasma membrane association and the attainment of enhanced thermostability without altering its sensitivity to inhibition by rolipram. Biochem J 292 (Pt 3): 677-686.
51. Yarwood SJ, Steele MR, Scotland G, Houslay MD, Bolger GB (1999) The RACK1 signaling scaffold protein selectively interacts with the cAMP-specific phosphodiesterase PDE4D5 isoform. J Biol Chem 274: 14909-14917.
52. Mantamadiotis T, Papalexis N, Dworkin S (2012) CREB signalling in neural stem/progenitor cells: recent developments and the implications for brain tumour biology. Bioessays 34: 293-300.
53. Gonzalez-Garcia C, Bravo B, Ballester A, Gomez-Perez R, Eguiluz C, et al. (2013) Comparative assessment of phosphodiesterase 4 and 7 inhibitors as therapeutic agents in Experimental Autoimmune Encephalomyelitis. Br J Pharmacol.
54. Safavi M, Baeeri M, Abdollahi M (2013) New methods for the discovery and synthesis of PDE7 inhibitors as new drugs for neurological and inflammatory disorders. Expert Opin Drug Discov 8: 733-751.
55. Pollard SM, Yoshikawa K, Clarke ID, Danovi D, Stricker S, et al. (2009) Glioma stem cell lines expanded in adherent culture have tumor-specific phenotypes and are suitable for chemical and genetic screens. Cell Stem Cell 4: 568-580.
56. Edgar R, Domrachev M, Lash AE (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30: 207-210.
57. Mitra RD, Butty VL, Shendure J, Williams BR, Housman DE, et al. (2003) Digital genotyping and haplotyping with polymerase colonies. Proc Natl Acad Sci U S A 100: 5926-5931.
58. Ding S, Wu X, Li G, Han M, Zhuang Y, et al. (2005) Efficient transposition of the piggyBac (PB) transposon in mammalian cells and mice. Cell 122: 473-483.
59. Hu Y, Smyth GK (2009) ELDA: extreme limiting dilution analysis for comparing depleted and enriched populations in stem cell and other assays. J Immunol Methods 347: 70-78.
60. Warrington NM, Woerner BM, Daginakatte GC, Dasgupta B, Perry A, et al. (2007) Spatiotemporal differences in CXCL12 expression and cyclic AMP underlie the unique pattern of optic glioma growth in neurofibromatosis type 1. Cancer Res 67: 8588-8595.
61. Gravendeel LA, Kouwenhoven MC, Gevaert O, de Rooi JJ, Stubbs AP, et al. (2009) Intrinsic gene expression profiles of gliomas are a better predictor of survival than histology. Cancer Res 69: 9065-9072.
62. Verhaak RG, Hoadley KA, Purdom E, Wang V, Qi Y, et al. (2010) Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 17: 98-110.