G-Protein coupled receptor 64 promotes invasiveness and metastasis in Ewing sarcomas through PGF and MMP1

Journal of Pathology

Volumn 230, Issue 1, 2013, Pages 70-81

  Richter, Günther H S ^a   Fasan, Annette ^a   Hauer, Kristina ^a   Grunewald, Thomas G P ^a   Berns, Colette ^a   Rössler, Sabine ^a   Naumann, Ivonne ^b   Staege, Martin S ^c   Fulda, Simone ^b   Esposito, Irene ^a,d   Burdach, Stefan ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b GOETHE UNIVERSITY   (Germany)

^c MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^d INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

Ewing sarcoma; G protein coupled receptor; invasion; matrix metalloproteinase 1; metastasis; PBX2; placental growth factor, SLIT2

Indexed keywords

G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 64; INTERSTITIAL COLLAGENASE; PLACENTAL GROWTH FACTOR; SLIT2 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CANCER INVASION; COLONY FORMATION; EWING SARCOMA; GENE REPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; LUNG METASTASIS; METASTASIS; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA INTERFERENCE; TRANSCRIPTION REGULATION; UPREGULATION;

ANIMALS; BONE NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; DNA-BINDING PROTEINS; HOMEODOMAIN PROTEINS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MATRIX METALLOPROTEINASE 13; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; NEOPLASM INVASIVENESS; NERVE TISSUE PROTEINS; NEUROBLASTOMA; PREGNANCY PROTEINS; PROTO-ONCOGENE PROTEINS; RECEPTORS, G-PROTEIN-COUPLED; SARCOMA, EWING; TUMOR CELLS, CULTURED; UP-REGULATION;

EID: 84876147713     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4170     Document Type: Article

References (48)

1. Paulussen M, Ahrens S, Burdach S, et al,. Primary metastatic (stage IV) Ewing tumor: survival analysis of 171 patients from the EICESS studies. European Intergroup Cooperative Ewing Sarcoma Studies. Ann Oncol 1998; 9: 275-281.
2. Schmidt D, Harms D, Burdach S,. Malignant peripheral neuroectodermal tumours of childhood and adolescence. Virchows Arch A Pathol Anat Histopathol 1985; 406: 351-365.
3. Richter GH, Plehm S, Fasan A, et al,. EZH2 is a mediator of EWS/FLI1 driven tumor growth and metastasis blocking endothelial and neuro-ectodermal differentiation. Proc Natl Acad Sci (USA) 2009; 106: 5324-5329.
4. Burdach S, Plehm S, Unland R, et al,. Epigenetic maintenance of stemness and malignancy in peripheral neuroectodermal tumors by EZH2. Cell Cycle 2009; 8: 1991-1996.
5. Hauer K, Calzada-Wack J, Steiger K, et al,. DKK2 mediates osteolysis, invasiveness and metastatic spread in Ewing sarcoma. Cancer Res 2013; 73: 967-977.
6. Cotterill SJ, Ahrens S, Paulussen M, et al,. Prognostic factors in Ewing's tumor of bone: analysis of 975 patients from the European Intergroup Cooperative Ewing's Sarcoma Study Group. J Clin Oncol 2000; 18: 3108-3114.
7. Burdach S, Meyer-Bahlburg A, Laws HJ, et al,. High-dose therapy for patients with primary multifocal and early relapsed Ewing's tumors: results of two consecutive regimens assessing the role of total-body irradiation. J Clin Oncol 2003; 21: 3072-3078.
8. Burdach S, Thiel U, Schoniger M, et al,. Total body MRI-governed involved compartment irradiation combined with high-dose chemotherapy and stem cell rescue improves long-term survival in Ewing tumor patients with multiple primary bone metastases. Bone Marrow Transplant 2010; 45: 483-489.
9. Thiel U, Wawer A, Wolf P, et al,. No improvement of survival with reduced- versus high-intensity conditioning for allogeneic stem cell transplants in Ewing tumor patients. Ann Oncol 2011; 22: 1614-1621.
10. Staege MS, Hutter C, Neumann I, et al,. DNA microarrays reveal relationship of Ewing family tumors to both endothelial and fetal neural crest-derived cells and define novel targets. Cancer Res 2004; 64: 8213-8221.
11. Staege MS, Hattenhorst UE, Neumann UE, et al,. DNA-microarrays as tools for the identification of tumor specific gene expression profiles: applications in tumor biology, diagnosis and therapy. Klin Padiatr 2003; 215: 135-139.
12. Osterhoff C, Ivell R, Kirchhoff C,. Cloning of a human epididymis-specific mRNA, HE6, encoding a novel member of the seven transmembrane-domain receptor superfamily. DNA Cell Biol 1997; 16: 379-389.
13. Whitehead IP, Zohn IE, Der CJ,. Rho GTPase-dependent transformation by G protein-coupled receptors. Oncogene 2001; 20: 1547-1555.
14. Li S, Huang S, Peng SB,. Overexpression of G protein-coupled receptors in cancer cells: involvement in tumor progression. Int J Oncol 2005; 27: 1329-1339.
15. Fredriksson R, Lagerstrom MC, Hoglund PJ, et al,. Novel human G protein-coupled receptors with long N-terminals containing GPS domains and Ser/Thr-rich regions. FEBS Lett 2002; 531: 407-414.
16. Fredriksson R, Lagerstrom MC, Lundin LG, et al,. The G-protein-coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints. Mol Pharmacol 2003; 63: 1256-1272.
17. Yona S, Lin HH, Siu WO, et al,. Adhesion-GPCRs: emerging roles for novel receptors. Trends Biochem Sci 2008; 33: 491-500.
18. Gupta GP, Nguyen DX, Chiang AC, et al,. Mediators of vascular remodelling co-opted for sequential steps in lung metastasis. Nature 2007; 446: 765-770.
19. Boire A, Covic L, Agarwal A, et al,. PAR1 is a matrix metalloprotease-1 receptor that promotes invasion and tumorigenesis of breast cancer cells. Cell 2005; 120: 303-313.
20. Fuchs B, Inwards CY, Janknecht R,. Upregulation of the matrix metalloproteinase-1 gene by the Ewing's sarcoma associated EWS-ER81 and EWS-Fli-1 oncoproteins, c-Jun and p300. FEBS Lett 2003; 553: 104-108.
21. Moosmann S, Hutter J, Moser C, et al,. Milieu-adopted in vitro and in vivo differentiation of mesenchymal tissues derived from different adult human CD34-negative progenitor cell clones. Cells Tissues Organs 2005; 179: 91-101.
22. Baird K, Davis S, Antonescu CR, et al,. Gene expression profiling of human sarcomas: insights into sarcoma biology. Cancer Res 2005; 65: 9226-9235.
23. Wu W, Wong K, Chen J, et al,. Directional guidance of neuronal migration in the olfactory system by the protein Slit. Nature 1999; 400: 331-336.
24. Monica K, Galili N, Nourse J, et al,. PBX2 and PBX3, new homeobox genes with extensive homology to the human proto-oncogene PBX1. Mol Cell Biol 1991; 11: 6149-6157.
25. Hendrich B, Bird A,. Identification and characterization of a family of mammalian methyl-CpG binding proteins. Mol Cell Biol 1998; 18: 6538-6547.
26. Luttun A, Tjwa M, Moons L, et al,. Revascularization of ischemic tissues by PlGF treatment, and inhibition of tumor angiogenesis, arthritis and atherosclerosis by anti-Flt1. Nat Med 2002; 8: 831-840.
27. Maes C, Coenegrachts L, Stockmans I, et al,. Placental growth factor mediates mesenchymal cell development, cartilage turnover, and bone remodeling during fracture repair. J Clin Invest 2006; 116: 1230-1242.
28. Adini A, Kornaga T, Firoozbakht F, et al,. Placental growth factor is a survival factor for tumor endothelial cells and macrophages. Cancer Res 2002; 62: 2749-2752.
29. Odorisio T, Schietroma C, Zaccaria ML, et al,. Mice overexpressing placenta growth factor exhibit increased vascularization and vessel permeability. J Cell Sci 2002; 115: 2559-2567.
30. Luttun A, Tjwa M, Carmeliet P,. Placental growth factor (PlGF) and its receptor Flt-1 (VEGFR-1): novel therapeutic targets for angiogenic disorders. Ann N Y Acad Sci 2002; 979: 80-93.
31. Fischer C, Jonckx B, Mazzone M, et al,. Anti-PlGF inhibits growth of VEGF(R)-inhibitor-resistant tumors without affecting healthy vessels. Cell 2007; 131: 463-475.
32. Aird WC,. Phenotypic heterogeneity of the endothelium: II. Representative vascular beds. Circ Res 2007; 100: 174-190.
33. Ewing J., Classics in oncology. Diffuse endothelioma of bone. James Ewing. Proceedings of the New York Pathological Society, 1921. CA Cancer J Clin 1972; 22: 95-98.
34. Fanjul-Fernandez M, Folgueras AR, Cabrera S, et al,. Matrix metalloproteinases: evolution, gene regulation and functional analysis in mouse models. Biochim Biophys Acta 2010; 1803: 3-19.
35. Davies B, Baumann C, Kirchhoff C, et al,. Targeted deletion of the epididymal receptor HE6 results in fluid dysregulation and male infertility. Mol Cell Biol 2004; 24: 8642-8648.
36. Bjarnadottir TK, Fredriksson R, Schioth HB,. The adhesion GPCRs: a unique family of G protein-coupled receptors with important roles in both central and peripheral tissues. Cell Mol Life Sci 2007; 64: 2104-2119.
37. Kirchhoff C, Obermann H, Behnen M, et al,. Role of epididymal receptor HE6 in the regulation of sperm microenvironment. Mol Cell Endocrinol 2006; 250: 43-48.
38. Bhattacharya SK, Ramchandani S, Cervoni N, et al,. A mammalian protein with specific demethylase activity for mCpG DNA. Nature 1999; 397: 579-583.
39. Shi J, Liu Y, Zheng Y, et al,. Therapeutic expression of an anti-death receptor 5 single-chain fixed-variable region prevents tumor growth in mice. Cancer Res 2006; 66: 11946-11953.
40. Carmeliet P, Moons L, Luttun A, et al,. Synergism between vascular endothelial growth factor and placental growth factor contributes to angiogenesis and plasma extravasation in pathological conditions. Nat Med 2001; 7: 575-583.
41. Zhou Y, Bellingard V, Feng KT, et al,. Human cytotrophoblasts promote endothelial survival and vascular remodeling through secretion of Ang2, PlGF, and VEGF-C. Dev Biol 2003; 263: 114-125.
42. DuBois S, Demetri G,. Markers of angiogenesis and clinical features in patients with sarcoma. Cancer 2007; 109: 813-819.
43. Nagase H, Barrett AJ, Woessner JF, Jr., Nomenclature and glossary of the matrix metalloproteinases. Matrix Suppl 1992; 1: 421-424.
44. Shukunami C, Hiraki Y,. Chondromodulin-I and tenomodulin: the negative control of angiogenesis in connective tissue. Curr Pharm Des 2007; 13: 2101-2112.
45. Blackburn JS, Liu I, Coon CI, et al,. A matrix metalloproteinase-1/ protease activated receptor-1 signaling axis promotes melanoma invasion and metastasis. Oncogene 2009; 28: 4237-4248.
46. Blackburn JS, Rhodes CH, Coon CI, et al,. RNA interference inhibition of matrix metalloproteinase-1 prevents melanoma metastasis by reducing tumor collagenase activity and angiogenesis. Cancer Res 2007; 67: 10849-10858.
47. Grunewald TG, Diebold I, Esposito I, et al,. STEAP1 is associated with the invasive and oxidative stress phenotype of Ewing tumors. Mol Cancer Res 2012; 10: 52-65.
48. McCawley LJ, Matrisian LM,. Matrix metalloproteinases: they're not just for matrix anymore! Curr Opin Cell Biol 2001; 13: 534-540.