EphB2 activity plays a pivotal role in pediatric medulloblastoma cell adhesion and invasion

Neuro-Oncology

Volumn 14, Issue 9, 2012, Pages 1125-1135

  Sikkema, Arend H ^a   Den Dunnen, Wilfred F A ^a   Hulleman, Esther ^b   Van Vuurden, Dannis G ^b   Garcia Manero, Guillermo ^c   Yang, Hui ^c   Scherpen, Frank J G ^a   Kampen, Kim R ^a   Hoving, Eelco W ^a   Kamps, Willem A ^a   Diks, Sander H ^a   Peppelenbosch, Maikel P ^d   De Bont, Eveline S J M ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b University of Amsterdam   (Netherlands)

^c UNIVERSITY OF TEXAS   (United States)

^d ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Adhesion; Eph; EphB2; Ephrin B1; Invasion; Medulloblastoma

Indexed keywords

EPHRIN; EPHRIN B1; EPHRIN RECEPTOR A2; EPHRIN RECEPTOR B2; EPHRIN RECEPTOR B4; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; SHORT HAIRPIN RNA;

ARTICLE; CANCER INVASION; CELL ADHESION; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL STIMULATION; CEREBELLUM; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MEDULLOBLASTOMA; PHENOTYPE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

APOPTOSIS; BLOTTING, WESTERN; CELL ADHESION; CELL MOVEMENT; CELL PROLIFERATION; CEREBELLAR NEOPLASMS; CHILD; DNA METHYLATION; EPHRIN-B1; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MEDULLOBLASTOMA; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR, EPHB2; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED;

EID: 84867519695     PISSN: 15228517     EISSN: 15235866     Source Type: Journal    
DOI: 10.1093/neuonc/nos130     Document Type: Article

References (52)

1. Pasquale EB. Eph receptors and ephrins in cancer: bidirectional signalling and beyond. Nat Rev Cancer. 2010;10:165-180.
2. Kullander K, Klein R. Mechanisms and functions of Eph and ephrin signalling. Nat Rev Mol Cell Biol. 2002;3:475-486.
3. Pasquale EB. Eph-ephrin bidirectional signaling in physiology and disease. Cell. 2008;133:38-52.
4. Pasquale EB. Eph-ephrin promiscuity is now crystal clear. Nat Neurosci. 2004;7:417-418.
5. Brantley-Sieders DM, Fang WB, Hicks DJ, Zhuang G, Shyr Y, Chen J. Impaired tumor microenvironment in EphA2-deficient mice inhibits tumor angiogenesis and metastatic progression. FASEB J. 2005;19:1884-1886.
6. Bush JO, Soriano P. Ephrin-B1 regulates axon guidance by reverse signaling through a PDZ-dependent mechanism. Genes Dev. 2009;23:1586-1599.
7. Hafner C, Schmitz G, Meyer S, et al. Differential gene expression of Eph receptors and ephrins in benign human tissues and cancers. Clin Chem. 2004;50:490-499.
8. Branco-Price C, Johnson RS. Tumor vessels are Eph-ing complicated. Cancer Cell. 2010;17:533-534.
9. Sawamiphak S, Seidel S, Essmann CL, et al. Ephrin-B2 regulates VEGFR2 function in developmental and tumour angiogenesis. Nature. 2010;465:487-491.
10. Wang Y, Nakayama M, Pitulescu ME, et al. Ephrin-B2 controls VEGF-induced angiogenesis and lymphangiogenesis. Nature. 2010;465:483-486.
11. Kuang SQ, Bai H, Fang ZH, et al. Aberrant DNA methylation and epigenetic inactivation of Eph receptor tyrosine kinases and ephrin ligands in acute lymphoblastic leukemia. Blood. 2010;115:2412-2419.
12. Nakada M, Niska JA, Tran NL, McDonough WS, Berens ME. EphB2/R-Ras signaling regulates glioma cell adhesion, growth, and invasion. Am J Pathol. 2005;167:565-576.
13. Nakada M, Drake KL, Nakada S, Niska JA, Berens ME. Ephrin-B3 ligand promotes glioma invasion through activation of Rac1. Cancer Res. 2006;66:8492-8500.
14. Zelinski DP, Zantek ND, Stewart JC, Irizarry AR, Kinch MS. EphA2 overexpression causes tumorigenesis of mammary epithelial cells. Cancer Res. 2001;61:2301-2306.
15. Guo DL, Zhang J, Yuen ST, et al. Reduced expression of EphB2 that parallels invasion and metastasis in colorectal tumours. Carcinogenesis. 2006;27:454-464.
16. Li JJ, Liu DP, Liu GT, Xie D. EphrinA5 acts as a tumor suppressor in glioma by negative regulation of epidermal growth factor receptor. Oncogene. 2009;28:1759-1768.
17. Batlle E, Bacani J, Begthel H, et al. EphB receptor activity suppresses colorectal cancer progression. Nature. 2005;435:1126-1130.
18. Noren NK, Foos G, Hauser CA, Pasquale EB. The EphB4 receptor suppresses breast cancer cell tumorigenicity through an Abl-Crk pathway. Nat Cell Biol. 2006;8:815-825.
19. Truitt L, Freywald T, De Coteau J, Sharfe N, Freywald A. The EphB6 receptor cooperates with c-Cbl to regulate the behavior of breast cancer cells. Cancer Res. 2010;70:1141-1153.
20. Davalos V, Dopeso H, Castano J, et al. EPHB4 and survival of colorectal cancer patients. Cancer Res. 2006;66:8943-8948.
21. Noberini R, Pasquale EB. Proliferation and tumor suppression: not mutually exclusive for Eph receptors. Cancer Cell. 2009;16:452-454.
22. Genander M, Halford MM, Xu NJ, et al. Dissociation of EphB2 signaling pathways mediating progenitor cell proliferation and tumor suppression. Cell. 2009;139:679-692.
23. Sikkema AH, Diks SH, Den Dunnen WF, et al. Kinome profiling in pediatric brain tumors as a new approach for target discovery. Cancer Res. 2009;69:5987-5995.
24. Koeller KK, Rushing EJ. From the archives of the AFIP: medulloblastoma: a comprehensive review with radiologic-pathologic correlation. Radiographics. 2003;23:1613-1637.
25. Laerum OD. Local spread of malignant neuroepithelial tumors. Acta Neurochir (Wien). 1997;139:515-522.
26. Ayan I, Kebudi R, Bayindir C, Darendeliler E. Microscopic local leptomeningeal invasion at diagnosis of medulloblastoma. Int J Radiat Oncol Biol Phys. 1997;39:461-466.
27. Louis, DN, Ohgaki, H, Wiestler, OD, Cavenee, WK, eds. WHO Classification of the Central Nervous System. Lyon: IARC Lyon; 2007.
28. Bobola MS, Silber JR, Ellenbogen RG, Geyer JR, Blank A, Goff RD. O6-methylguanine-DNA methyltransferase, O6-benzylguanine, and resistance to clinical alkylators in pediatric primary brain tumor cell lines. Clin Cancer Res. 2005;11:2747-2755.
29. De Bont ES, Fidler V, Meeuwsen T, Scherpen F, Hahlen K, Kamps WA. Vascular endothelial growth factor secretion is an independent prognostic factor for relapse-free survival in pediatric acute myeloid leukemia patients. Clin Cancer Res. 2002;8:2856-2861.
30. Roorda BD, Ter Elst A, Diks SH, Meeuwsen-De Boer TG, Kamps WA, De Bont ES. PTK787/ZK 222584 inhibits tumor growth promoting mesenchymal stem cells: kinase activity profiling as powerful tool in functional studies. Cancer Biol Ther. 2009;8:1239-1248.
31. Van Dongen JJ, Langerak AW, Bruggemann M, et al. Design and standardization of PCR primers and protocols for detection of clonal immunoglobulin and T-cell receptor gene recombinations in suspect lymphoproliferations: report of the BIOMED-2 Concerted Action BMH4-CT98-3936. Leukemia. 2003;17:2257-2317.
32. Kool M, Koster J, Bunt J, et al. Integrated genomics identifies five medulloblastoma subtypes with distinct genetic profiles, pathway signatures and clinicopathological features. PLoS One. 2008;3:e3088.
33. Larsen AB, Pedersen MW, Stockhausen MT, Grandal MV, Van Deurs B, Poulsen HS. Activation of the EGFR gene target EphA2 inhibits epidermal growth factor-induced cancer cell motility. Mol Cancer Res. 2007;5:283-293.
34. Himanen JP, Chumley MJ, Lackmann M, et al. Repelling class discrimination: ephrin-A5 binds to and activates EphB2 receptor signaling. Nat Neurosci. 2004;7:501-509.
35. Larsen AB, Stockhausen MT, Poulsen HS. Cell adhesion and EGFR activation regulate EphA2 expression in cancer. Cell Signal. 2010;22:636-644.
36. Yang NY, Fernandez C, Richter M, et al. Crosstalk of the EphA2 receptor with a serine/threonine phosphatase suppresses the Akt-mTORC1 pathway in cancer cells. Cell Signal. 2011;23:201-212.
37. MacDonald TJ, Brown KM, La Fleur B, et al. Expression profiling of medulloblastoma: PDGFRA and the RAS/MAPK pathway as therapeutic targets for metastatic disease. Nat Genet. 2001;29:143-152.
38. Zou JX, Wang B, Kalo MS, Zisch AH, Pasquale EB, Ruoslahti E. An Eph receptor regulates integrin activity through R-Ras. Proc Natl Acad Sci USA. 1999;96:13813-13818.
39. Lai KO, Chen Y, Po HM, Lok KC, Gong K, Ip NY. Identification of the Jak/Stat proteins as novel downstream targets of EphA4 signaling in muscle: implications in the regulation of acetylcholinesterase expression. J Biol Chem. 2004;279:13383-13392.
40. Larrea MD, Wander SA, Slingerland JM. p27 as Jekyll and Hyde: regulation of cell cycle and cell motility. Cell Cycle. 2009;8:3455-3461.
41. Roorda BD, Ter Elst A, Scherpen FJ, Meeuwsen-De Boer TG, Kamps WA, De Bont ES. VEGF-A promotes lymphoma tumour growth by activation of STAT proteins and inhibition of p27 (KIP1) via paracrine mechanisms. Eur J Cancer. 2010;46:974-982.
42. Wander SA, Zhao D, Slingerland JM. p27: a barometer of signaling deregulation and potential predictor of response to targeted therapies. Clin Cancer Res. 2011;17:12-18.
43. Crowe DL, Ohannessian A. Recruitment of focal adhesion kinase and paxillin to beta1 integrin promotes cancer cell migration via mitogen activated protein kinase activation. BMC Cancer. 2004;4:18.
44. Azuma K, Tanaka M, Uekita T, et al. Tyrosine phosphorylation of paxillin affects the metastatic potential of human osteosarcoma. Oncogene. 2005;24:4754-4764.
45. Vindis C, Teli T, Cerretti DP, Turner CE, Huynh-Do U. EphB1-mediated cell migration requires the phosphorylation of paxillin at Tyr-31/Tyr-118. J Biol Chem. 2004;279:27965-27970.
46. Nalla AK, Asuthkar S, Bhoopathi P, Gujrati M, Dinh DH, Rao JS. Suppression of uPAR retards radiation-induced invasion and migration mediated by integrin beta1/FAK signaling in medulloblastoma. PLoS One. 2010;5:e13006.
47. Bhatia B, Malik A, Fernandez L, Kenney AM. p27 (Kip1), a doubleedged sword in Shh-mediated medulloblastoma: tumor accelerator and suppressor. Cell Cycle. 2010;9:4307-4314.
48. Cheng N, Brantley DM, Liu H, et al. Blockade of EphA receptor tyrosine kinase activation inhibits vascular endothelial cell growth factor-induced angiogenesis. Mol Cancer Res. 2002;1:2-11.
49. Pandey A, Shao H, Marks RM, Polverini PJ, Dixit VM. Role of B61, the ligand for the Eck receptor tyrosine kinase, in TNF-alpha-induced angiogenesis. Science. 1995;268:567-569.
50. Ireton RC, Chen J. EphA2 receptor tyrosine kinase as a promising target for cancer therapeutics. Curr Cancer Drug Targets. 2005;5:149-157.
51. Wykosky J, Debinski W. The EphA2 receptor and ephrinA1 ligand in solid tumors: function and therapeutic targeting. Mol Cancer Res. 2008;6:1795-1806.
52. Sikkema AH, De Bont ES, Molema G, et al. VEGFR-2 signalling activity in paediatric pilocytic astrocytoma is restricted to tumour endothelial cells. Neuropathol Appl Neurobiol. 2011;37:538-548.