Regulation and misregulation of Eph/ephrin expression

Cell Adhesion and Migration

Volumn 6, Issue 2, 2012, Pages 131-137

  Arvanitis, Dina N ^a   Davy, Alice ^a  

^a UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

Cancer; Development; Eph receptors; Ephrins; Epigenetic; MicroRNA

Indexed keywords

EPHRIN; EPHRIN A1; EPHRIN A2; EPHRIN A3; EPHRIN A4; EPHRIN A5; EPHRIN A6; EPHRIN A7; EPHRIN B1; EPHRIN B2; EPHRIN B3; EPHRIN RECEPTOR; EPHRIN RECEPTOR A1; EPHRIN RECEPTOR A2; EPHRIN RECEPTOR A3; EPHRIN RECEPTOR A4; EPHRIN RECEPTOR A5; EPHRIN RECEPTOR A6; EPHRIN RECEPTOR A7; EPHRIN RECEPTOR A8; EPHRIN RECEPTOR A9; EPHRIN RECEPTOR B1; EPHRIN RECEPTOR B2; EPHRIN RECEPTOR B3; EPHRIN RECEPTOR B4; EPHRIN RECEPTOR B5; EPHRIN RECEPTOR B6; HOMEODOMAIN PROTEIN; MICRORNA; UNCLASSIFIED DRUG;

CANCER CELL; CELL ADHESION; EMBRYO DEVELOPMENT; EPIGENETICS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMAN; NONHUMAN; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

EID: 84863925294     PISSN: 19336918     EISSN: 19336926     Source Type: Journal    
DOI: 10.4161/cam.19690     Document Type: Review

References (99)

1. Kullander K, Klein R. Mechanisms and functions of Eph and ephrin signalling. Nat Rev Mol Cell Biol 2002; 3:475-86; PMID:12094214; http://dx.doi.org/10.1038/nrm856
2. Murai KK, Pasquale EB. 'Eph'ective signaling: forward, reverse and crosstalk. J Cell Sci 2003; 116:2823-32; PMID:12808016; http://dx.doi.org/10. 1242/jcs.00625
3. Pasquale EB. Eph receptor signalling casts a wide net on cell behaviour. Nat Rev Mol Cell Biol 2005; 6:462-75; PMID:15928710; http://dx.doi.org/10.1038/ nrm1662
4. Pasquale EB. The Eph family of receptors. Curr Opin Cell Biol 1997; 9:608-15; PMID:9330863; http://dx.doi.org/10.1016/S0955-0674(97)80113-5
5. Haramis AP, Perrakis A. Selectivity and promiscuity in Eph receptors. Structure 2006; 14:169-71; PMID: 16472735; http://dx.doi.org/10.1016/j.str.2006. 01.005
6. Davy A, Soriano P. Ephrin signaling in vivo: look both ways. Dev Dyn 2005; 232:1-10; PMID:15580616; http://dx.doi.org/10.1002/dvdy.20200
7. Augustin HG, Reiss Y. EphB receptors and ephrinB ligands: regulators of vascular assembly and homeostasis. Cell Tissue Res 2003; 314:25-31; PMID:12905065; http://dx.doi.org/10.1007/s00441-003-0770-9
8. Klein R. Excitatory Eph receptors and adhesive ephrin ligands. Curr Opin Cell Biol 2001; 13:196-203; PMID:11248553; http://dx.doi.org/10.1016/S0955- 0674(00)00197-6
9. Pasquale EB. Eph-ephrin bidirectional signaling in physiology and disease. Cell 2008; 133:38-52; PMID: 18394988; http://dx.doi.org/10.1016/j.cell. 2008.03.011
10. Goldshmit Y, McLenachan S, Turnley A. Roles of Eph receptors and ephrins in the normal and damaged adult CNS. Brain Res Rev 2006; 52:327-45; PMID: 16774788; http://dx.doi.org/10.1016/j.brainresrev.2006.04.006
11. Merlos-Suárez A, Batlle E. Eph-ephrin signalling in adult tissues and cancer. Curr Opin Cell Biol 2008; 20:194-200; PMID:18353626; http://dx.doi.org/10.1016/j.ceb.2008.01.011
12. Kuijper S, Turner CJ, Adams RH. Regulation of angiogenesis by Eph-ephrin interactions. Trends Cardiovasc Med 2007; 17:145-51; PMID:17574121; http://dx.doi.org/10.1016/j.tcm.2007.03.003
13. Pasquale EB. Eph receptors and ephrins in cancer: bidirectional signalling and beyond. Nat Rev Cancer 2010; 10:165-80; PMID:20179713; http://dx.doi.org/10.1038/nrc2806
14. Noren NK, Pasquale EB. Eph receptor-ephrin bidirectional signals that target Ras and Rho proteins. Cell Signal 2004; 16:655-66; PMID:15093606; http://dx.doi.org/10.1016/j.cellsig.2003.10.006
15. Xu Q, Mellitzer G, Wilkinson DG. Roles of Eph receptors and ephrins in segmental patterning. Philos Trans R Soc Lond B Biol Sci 2000; 355:993-1002; PMID:11128993; http://dx.doi.org/10.1098/rstb.2000.0635
16. Wilkinson DG. Eph receptors and ephrins: regulators of guidance and assembly. Int Rev Cytol 2000; 196:177-244; PMID:10730216; http://dx.doi.org/10. 1016/S0074-7696(00)96005-4
17. Feldheim DA, O'Leary DD. Visual map development: bidirectional signaling, bifunctional guidance molecules, and competition. Cold Spring Harb Perspect Biol 2010; 2:a001768; PMID:20880989; http://dx.doi.org/10.1101/cshperspect. a001768
18. Luria V, Krawchuk D, Jessell TM, Laufer E, Kania A. Specification of motor axon trajectory by ephrin-B: EphB signaling: symmetrical control of axonal patterning in the developing limb. Neuron 2008; 60:1039-53; PMID:19109910; http://dx.doi.org/10.1016/j.neuron.2008.11.011
19. Studer M, Gavalas A, Marshall H, Ariza-McNaughton L, Rijli FM, Chambon P, et al. Genetic interactions between Hoxa1 and Hoxb1 reveal new roles in regulation of early hindbrain patterning. Development 1998; 125:1025-36; PMID:9463349
20. Luria V, Laufer E. Lateral motor column axons execute a ternary trajectory choice between limb and body tissues. Neural Dev 2007; 2:13; PMID:17605791; http://dx.doi.org/10.1186/1749-8104-2-13
21. Kania A, Jessell TM. Topographic motor projections in the limb imposed by LIM homeodomain protein regulation of ephrin-A:EphA interactions. Neuron 2003; 38:581-96; PMID:12765610; http://dx.doi.org/10.1016/S0896-6273(03)00292-7
22. Schulte D, Furukawa T, Peters MA, Kozak CA, Cepko CL. Misexpression of the Emx-related homeobox genes cVax and mVax2 ventralizes the retina and perturbs the retinotectal map. Neuron 1999; 24:541-53; PMID: 10595508; http://dx.doi.org/10.1016/S0896-6273(00) 81111-3
23. Schneider-Maunoury S, Seitanidou T, Topilko P, Vesque C, Frain M, Gilardi-Hebenstreit P, et al. [Role of the Krox-20 gene in the development of rhombencephalon]. C R Seances Soc Biol Fil 1997; 191:91-4; PMID:9181130
24. Richmond CA, Breault DT. Regulation of gene expression in the intestinal epithelium. Prog Mol Biol Transl Sci 2010; 96:207-29; PMID:21075346; http://dx.doi.org/10.1016/B978-0-12-381280-3.00009-9
25. Suzuki A, Urushitani H, Sato T, Kobayashi T, Watanabe H, Ohta Y, et al. Gene expression change in the Müllerian duct of the mouse fetus exposed to diethylstilbestrol in utero. Exp Biol Med (Maywood) 2007; 232:503-14; PMID:17392486
26. Hernandez RE, Rikhof HA, Bachmann R, Moens CB. vhnf1 integrates global RA patterning and local FGF signals to direct posterior hindbrain development in zebrafish. Development 2004; 131:4511-20; PMID: 15342476; http://dx.doi.org/10. 1242/dev.01297
27. Bruhl T, Urbich C, Aicher D, Acker-Palmer A, Zeiher AM, Dimmeler S. Homeobox A9 transcriptionally regulates the EphB4 receptor to modulate endothelial cell migration and tube formation. Circ Res 2004; 94:743-51; PMID:14764452; http://dx.doi.org/10.1161/01.RES.0000120861.27064.09
28. Durbin L, Sordino P, Barrios A, Gering M, Thisse C, Thisse B, et al. Anteroposterior patterning is required within segments for somite boundary formation in developing zebrafish. Development 2000; 127:1703-13; PMID:10725246
29. Niederreither K, Vermot J, Schuhbaur B, Chambon P, Dollé P. Retinoic acid synthesis and hindbrain patterning in the mouse embryo. Development 2000; 127:75-85; PMID:10654602
30. Manzanares M, Trainor PA, Nonchev S, Ariza-McNaughton L, Brodie J, Gould A, et al. The role of kreisler in segmentation during hindbrain development. Dev Biol 1999; 211:220-37; PMID:10395784; http://dx.doi.org/10.1006/dbio.1999.9318
31. Chen J, Ruley HE. An enhancer element in the EphA2 (Eck) gene sufficient for rhombomere-specific expression is activated by HOXA1 and HOXB1 homeobox proteins. J Biol Chem 1998; 273:24670-5; PMID: 9733765; http://dx.doi.org/10. 1074/jbc.273.38.24670
32. Theil T, Frain M, Gilardi-Hebenstreit P, Flenniken A, Charnay P, Wilkinson DG. Segmental expression of the EphA4 (Sek-1) receptor tyrosine kinase in the hindbrain is under direct transcriptional control of Krox-20. Development 1998; 125:443-52; PMID:9425139
33. Taneja R, Thisse B, Rijli FM, Thisse C, Bouillet P, Dollé P, et al. The expression pattern of the mouse receptor tyrosine kinase gene MDK1 is conserved through evolution and requires Hoxa-2 for rhombomere-specific expression in mouse embryos. Dev Biol 1996; 177:397-412; PMID:8806819; http://dx.doi.org/10.1006/dbio.1996.0173
34. Shashikant CS, Utset MF, Violette SM,Wise TL, Einat P, Einat M, et al. Homeobox genes in mouse development. Crit Rev Eukaryot Gene Expr 1991; 1:207-45; PMID:1686978
35. Salsi V, Zappavigna V. Hoxd13 and Hoxa13 directly control the expression of the EphA7 Ephrin tyrosine kinase receptor in developing limbs. J Biol Chem 2006; 281:1992-9; PMID:16314414; http://dx.doi.org/10.1074/jbc.M510900200
36. Cooke J, Moens C, Roth L, Durbin L, Shiomi K, Brennan C, et al. Eph signalling functions downstream of Val to regulate cell sorting and boundary formation in the caudal hindbrain. Development 2001; 128:571-80; PMID:11171340
37. Rhinn M, Dierich A, Le Meur M, Ang S. Cell autonomous and non-cell autonomous functions of Otx2 in patterning the rostral brain. Development 1999; 126:4295-304; PMID:10477297
38. Ting MC, Wu NL, Roybal PG, Sun J, Liu L, Yen Y, et al. EphA4 as an effector of Twist1 in the guidance of osteogenic precursor cells during calvarial bone growth and in craniosynostosis. Development 2009; 136:855-64; PMID:19201948; http://dx.doi.org/10.1242/dev.028605
39. Merrill AE, Bochukova EG, Brugger SM, Ishii M, Pilz DT, Wall SA, et al. Cell mixing at a neural crestmesoderm boundary and deficient ephrin-Eph signaling in the pathogenesis of craniosynostosis. Hum Mol Genet 2006; 15:1319-28; PMID:16540516; http://dx.doi.org/10.1093/hmg/ddl052
40. Takahashi H, Shintani T, Sakuta H, Noda M. CBF1 controls the retinotectal topographical map along the anteroposterior axis through multiple mechanisms. Development 2003; 130:5203-15; PMID:12954716; http://dx.doi.org/10.1242/dev. 00724
41. Munthe E, Aasheim HC. Characterization of the human ephrin-A4 promoter. Biochem J 2002; 366:447-58; PMID:12030849; http://dx.doi.org/10.1042/BJ20011693
42. Sohl M, Lanner F, Farnebo F. Characterization of the murine Ephrin-B2 promoter. Gene 2009; 437:54-9; PMID:19268698; http://dx.doi.org/10.1016/j.gene. 2009.02.017
43. Batlle E, Henderson JT, Beghtel H, van den Born MM, Sancho E, Huls G, et al. Beta-catenin and TCF mediate cell positioning in the intestinal epithelium by controlling the expression of EphB/ephrinB. Cell 2002; 111:251-63; PMID:12408869; http://dx.doi.org/10.1016/S0092-8674(02)01015-2
44. García-Frigola C, Carreres MI, Vegar C, Mason C, Herrera E. Zic2 promotes axonal divergence at the optic chiasm midline by EphB1-dependent and -independent mechanisms. Development 2008; 135:1833-41; PMID: 18417618; http://dx.doi.org/10.1242/dev.020693
45. Xing W, Baylink D, Kesavan C, Hu Y, Kapoor S, Chadwick RB, et al. Global gene expression analysis in the bones reveals involvement of several novel genes and pathways in mediating an anabolic response of mechanical loading in mice. J Cell Biochem 2005; 96:1049-60; PMID:16149068; http://dx.doi.org/10.1002/jcb. 20606
46. Diercke K, Sen S, Kohl A, Lux CJ, Erber R. Compression-dependent up-regulation of ephrin-A2 in PDL fibroblasts attenuates osteogenesis. J Dent Res 2011; 90:1108-15; PMID:21724962; http://dx.doi.org/10.1177/0022034511413926
47. Obi S, Yamamoto K, Shimizu N, Kumagaya S, Masumura T, Sokabe T, et al. Fluid shear stress induces arterial differentiation of endothelial progenitor cells. J Appl Physiol 2009; 106:203-11; PMID: 18988767; http://dx.doi.org/10. 1152/japplphysiol.00197.2008
48. Sohl M, Lanner F, Farnebo F. Sp1 mediate hypoxia induced ephrinB2 expression via a hypoxia-inducible factor independent mechanism. Biochem Biophys Res Commun 2010; 391:24-7; PMID:19883626; http://dx.doi.org/10.1016/j.bbrc. 2009.10.146
49. Lugli A, Spichtin H, Maurer R, Mirlacher M, Kiefer J, Huusko P, et al. EphB2 expression across 138 human tumor types in a tissue microarray: high levels of expression in gastrointestinal cancers. Clin Cancer Res 2005; 11:6450-8; PMID:16166419; http://dx.doi.org/10.1158/1078-0432.CCR-04-2458
50. Wu Q, Suo Z, Risberg B, Karlsson MG, Villman K, Nesland JM. Expression of Ephb2 and Ephb4 in breast carcinoma. Pathol Oncol Res 2004; 10:26-33; PMID: 15029258; http://dx.doi.org/10.1007/BF02893405
51. Jubb AM, Zhong F, Bheddah S, Grabsch HI, Frantz GD, Mueller W, et al. EphB2 is a prognostic factor in colorectal cancer. Clin Cancer Res 2005; 11:5181-7; PMID:16033834; http://dx.doi.org/10.1158/1078-0432.CCR-05-0143
52. Fu T, Li P, Wang H, He Y, Luo D, Zhang A, et al. c-Rel is a transcriptional repressor of EPHB2 in colorectal cancer. J Pathol 2009; 219:103-13; PMID: 19621336; http://dx.doi.org/10.1002/path.2590
53. Guo DL, Zhang J, Yuen ST, Tsui WY, Chan AS, Ho C, et al. Reduced expression of EphB2 that parallels invasion and metastasis in colorectal tumours. Carcinogenesis 2006; 27:454-64; PMID:16272170; http://dx.doi.org/10. 1093/carcin/bgi259
54. Senior PV, Zhang BX, Chan ST. Loss of cell-surface receptor EphB2 is important for the growth, migration, and invasiveness of a colon cancer cell line. Int J Colorectal Dis 2010; 25:687-94; PMID:20339854; http://dx.doi.org/10. 1007/s00384-010-0916-7
55. Kusumawidjaja G, Kayed H, Giese N, Bauer A, Erkan M, Giese T, et al. Basic transcription factor 3 (BTF3) regulates transcription of tumor-associated genes in pancreatic cancer cells. Cancer Biol Ther 2007; 6:367-76; PMID:17312387; http://dx.doi.org/10.4161/cbt.6.3.3704
56. Kataoka H, Igarashi H, Kanamori M, Ihara M, Wang JD, Wang YJ, et al. Correlation of EPHA2 overexpression with high microvessel count in human primary colorectal cancer. Cancer Sci 2004; 95:136-41; PMID:14965363; http://dx.doi.org/10.1111/j.1349-7006.2004.tb03194.x
57. Brannan JM, Sen B, Saigal B, Prudkin L, Behrens C, Solis L, et al. EphA2 in the early pathogenesis and progression of non-small cell lung cancer. Cancer Prev Res (Phila) 2009; 2:1039-49; PMID:19934338; http://dx.doi.org/10.1158/1940- 6207.CAPR-09-0212
58. Menges CW, McCance DJ. Constitutive activation of the Raf-MAPK pathway causes negative feedback inhibition of Ras-PI3K-AKT and cellular arrest through the EphA2 receptor. Oncogene 2008; 27:2934-40; PMID: 18059341; http://dx.doi.org/10.1038/sj.onc.1210957
59. Macrae M, Neve RM, Rodriguez-Viciana P, Haqq C, Yeh J, Chen C, et al. A conditional feedback loop regulates Ras activity through EphA2. Cancer Cell 2005; 8:111-8; PMID:16098464; http://dx.doi.org/10.1016/j.ccr.2005.07.005
60. Zhang G, Njauw CN, Park JM, Naruse C, Asano M, Tsao H. EphA2 is an essential mediator of UV radiation-induced apoptosis. Cancer Res 2008; 68: 1691-6; PMID:18339848; http://dx.doi.org/10.1158/0008-5472.CAN-07-2372
61. Nakao M. Epigenetics: interaction of DNA methylation and chromatin. Gene 2001; 278:25-31; PMID: 11707319; http://dx.doi.org/10.1016/S0378-1119(01)00721-1
62. Novik KL, Nimmrich I, Genc B, Maier S, Piepenbrock C, Olek A, et al. Epigenomics: genome-wide study of methylation phenomena. Curr Issues Mol Biol 2002; 4:111-28; PMID:12432963
63. Duthie SJ. Epigenetic modifications and human pathologies: cancer and CVD. Proc Nutr Soc 2011; 70:47-56; PMID:21067630; http://dx.doi.org/10.1017/ S0029665110003952
64. Delgado MD, León J. Gene expression regulation and cancer. Clin Transl Oncol 2006; 8:780-7; PMID: 17134965; http://dx.doi.org/10.1007/s12094- 006-0132-7
65. Grønbaek K, Hother C, Jones PA. Epigenetic changes in cancer. APMIS 2007; 115:1039-59; PMID:18042143; http://dx.doi.org/10.1111/j.1600-0463. 2007.apm-636.xml.x
66. Strathdee G, Sim A, Brown R. Control of gene expression by CpG island methylation in normal cells. Biochem Soc Trans 2004; 32:913-5; PMID:15506922; http://dx.doi.org/10.1042/BST0320913
67. Zhou R. Regulation of topographic projection by the Eph family receptor Bsk (EphA5) and its ligands. Cell Tissue Res 1997; 290:251-9; PMID:9321686; http://dx.doi.org/10.1007/s004410050929
68. Petkova TD, Seigel GM, Otteson DC. A role for DNA methylation in regulation of EphA5 receptor expression in the mouse retina. Vision Res 2011; 51:260-8; PMID:20875442; http://dx.doi.org/10.1016/j.visres.2010.09.022
69. Davalos V, Dopeso H, Castaño J, Wilson AJ, Vilardell F, Romero-Gimenez J, et al. EPHB4 and survival of colorectal cancer patients. Cancer Res 2006; 66:8943-8; PMID:16982731; http://dx.doi.org/10.1158/0008-5472. CAN-05-4640
70. Ogino S, Hazra A, Tranah GJ, Kirkner GJ, Kawasaki T, Nosho K, et al. MGMT germline polymorphism is associated with somatic MGMT promoter methylation and gene silencing in colorectal cancer. Carcinogenesis 2007; 28:1985-90; PMID:17621591; http://dx.doi.org/10.1093/carcin/bgm160
71. Wang J, Kataoka H, Suzuki M, Sato N, Nakamura R, Tao H, et al. Downregulation of EphA7 by hypermethylation in colorectal cancer. Oncogene 2005; 24:5637-47; PMID:16007213; http://dx.doi.org/10.1038/sj.onc.1208720
72. Alazzouzi H, Davalos V, Kokko A, Domingo E, Woerner SM, Wilson AJ, et al. Mechanisms of inactivation of the receptor tyrosine kinase EPHB2 in colorectal tumors. Cancer Res 2005; 65:10170-3; PMID:16288001; http://dx.doi.org/10.1158/ 0008-5472.CAN-05-2580
73. Herath NI, Doecke J, Spanevello MD, Leggett BA, Boyd AW. Epigenetic silencing of EphA1 expression in colorectal cancer is correlated with poor survival. Br J Cancer 2009; 100:1095-102; PMID:19277044; http://dx.doi.org/10. 1038/sj.bjc.6604970
74. Dottori M, Down M, Hüttmann A, Fitzpatrick DR, Boyd AW. Cloning and characterization of EphA3 (Hek) gene promoter: DNA methylation regulates expression in hematopoietic tumor cells. Blood 1999; 94:2477-86; PMID:10498621
75. Kuang SQ, Bai H, Fang ZH, Lopez G, Yang H, Tong W, et al. Aberrant DNA methylation and epigenetic inactivation of Eph receptor tyrosine kinases and ephrin ligands in acute lymphoblastic leukemia. Blood 2010; 115:2412-9; PMID:20061560; http://dx.doi.org/10.1182/blood-2009-05-222208
76. Kitamura T, Kabuyama Y, Kamataki A, Homma MK, Kobayashi H, Aota S, et al. Enhancement of lymphocyte migration and cytokine production by ephrinB1 system in rheumatoid arthritis. Am J Physiol Cell Physiol 2008; 294:C189-96; PMID:17942634; http://dx.doi.org/10.1152/ajpcell.00314.2007
77. Arvanitis DN, Jungas T, Behar A, Davy A. Ephrin-B1 reverse signaling controls a posttranscriptional feedback mechanism via miR-124. Mol Cell Biol 2010; 30:2508-17; PMID:20308325; http://dx.doi.org/10.1128/MCB.01620-09
78. Winter J, Roepcke S, Krause S, Müller EC, Otto A, Vingron M, et al. Comparative 3'UTR analysis allows identification of regulatory clusters that drive Eph/ephrin expression in cancer cell lines. PLoS One 2008; 3:e2780; PMID:18648668; http://dx.doi.org/10.1371/journal.pone.0002780
79. Kokko A, Laiho P, Lehtonen R, Korja S, Carvajal-Carmona LG, Järvinen H, et al. EPHB2 germline variants in patients with colorectal cancer or hyperplastic polyposis. BMC Cancer 2006; 6:145; PMID:16740153; http://dx.doi.org/10.1186/1471-2407-6-145
80. Huusko P, Ponciano-Jackson D, Wolf M, Kiefer JA, Azorsa DO, Tuzmen S, et al. Nonsense-mediated decay microarray analysis identifies mutations of EPHB2 in human prostate cancer. Nat Genet 2004; 36:979-83; PMID:15300251; http://dx.doi.org/10.1038/ng1408
81. Wieland I, Makarov R, Reardon W, Tinschert S, Goldenberg A, Thierry P, et al. Dissecting the molecular mechanisms in craniofrontonasal syndrome: differential mRNA expression of mutant EFNB1 and the cellular mosaic. Eur J Hum Genet 2008; 16:184-91; PMID:18043713; http://dx.doi.org/10.1038/sj.ejhg.5201968
82. Ambros V. The functions of animal microRNAs. Nature 2004; 431:350-5; PMID:15372042; http://dx.doi.org/10.1038/nature02871
83. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004; 116:281-97; PMID: 14744438; http://dx.doi.org/10.1016/S0092-8674(04) 00045-5
84. Filipowicz W, Bhattacharyya SN, Sonenberg N. Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet 2008; 9:102-14; PMID:18197166; http://dx.doi.org/10.1038/nrg2290
85. Yu CH, Xu CF, Li YM. Association of MicroRNA-223 expression with hepatic ischemia/reperfusion injury in mice. Dig Dis Sci 2009; 54:2362-6; PMID:19104939; http://dx.doi.org/10.1007/s10620-008-0629-8
86. Alisi A, Da Sacco L, Bruscalupi G, Piemonte F, Panera N, De Vito R, et al. Mirnome analysis reveals novel molecular determinants in the pathogenesis of diet-induced nonalcoholic fatty liver disease. Lab Invest 2011; 91:283-93; PMID:20956972; http://dx.doi.org/10.1038/labinvest.2010.166
87. Fasanaro P, D'Alessandra Y, Di Stefano V, Melchionna R, Romani S, Pompilio G, et al. MicroRNA-210 modulates endothelial cell response to hypoxia and inhibits the receptor tyrosine kinase ligand Ephrin-A3. J Biol Chem 2008; 283:15878-83; PMID:18417479; http://dx.doi.org/10.1074/jbc.M800731200
88. Zhang Y, Fei M, Xue G, Zhou Q, Jia Y, Li L, et al. Elevated levels of hypoxia-inducible microRNA-210 in pre-eclampsia: new insights into molecular mechanisms for the disease. J Cell Mol Med 2012; 16:249-59; PMID:21388517; http://dx.doi.org/10.1111/j.1582-4934.2011.01291.x
89. Wu N, Zhao X, Liu M, Liu H, Yao W, Zhang Y, et al. Role of microRNA-26b in glioma development and its mediated regulation on EphA2. PLoS One 2011; 6: e16264; PMID:21264258; http://dx.doi.org/10.1371/journal.pone.0016264
90. Walker-Daniels J, Riese DJ, 2nd, Kinch MS. c-Cbldependent EphA2 protein degradation is induced by ligand binding. Mol Cancer Res 2002; 1:79-87; PMID: 12496371
91. Walker-Daniels J, Hess AR, Hendrix MJ, Kinch MS. Differential regulation of EphA2 in normal and malignant cells. Am J Pathol 2003; 162:1037-42; PMID:12651595; http://dx.doi.org/10.1016/S0002-9440(10)63899-0
92. Vihanto MM, Plock J, Erni D, Frey BM, Frey FJ, Huynh-Do U. Hypoxia up-regulates expression of Eph receptors and ephrins in mouse skin. FASEB J 2005; 19:1689-91; PMID:16081502
93. Bush JO, Soriano P. Ephrin-B1 forward signaling regulates craniofacial morphogenesis by controlling cell proliferation across Eph-ephrin boundaries. Genes Dev 2010; 24:2068-80; PMID:20844017; http://dx.doi.org/10.1101/gad.1963210
94. Carvalho RF, Beutler M, Marler KJ, Knöll B, Becker-Barroso E, Heintzmann R, et al. Silencing of EphA3 through a cis interaction with ephrinA5. Nat Neurosci 2006; 9:322-30; PMID:16491080; http://dx.doi.org/10.1038/nn1655
95. Kao TJ, Kania A. Ephrin-mediated cis-attenuation of Eph receptor signaling is essential for spinal motor axon guidance. Neuron 2011; 71:76-91; PMID:21745639; http://dx.doi.org/10.1016/j.neuron.2011.05.031
96. Hatano M, Eguchi J, Tatsumi T, Kuwashima N, Dusak JE, Kinch MS, et al. EphA2 as a glioma-associated antigen: a novel target for glioma vaccines. Neoplasia 2005; 7:717-22; PMID:16207473; http://dx.doi.org/10.1593/neo.05277
97. Oricchio E, Nanjangud G, Wolfe AL, Schatz JH, Mavrakis KJ, Jiang M, et al. The Eph-receptor A7 is a soluble tumor suppressor for follicular lymphoma. Cell 2011; 147:554-64; PMID:22036564; http://dx.doi.org/10.1016/j.cell.2011.09. 035
98. Lee JW, Han HD, Shahzad MM, Kim SW, Mangala LS, Nick AM, et al. EphA2 immunoconjugate as molecularly targeted chemotherapy for ovarian carcinoma. J Natl Cancer Inst 2009; 101:1193-205; PMID: 19641174; http://dx.doi.org/10.1093/ jnci/djp231
99. Kiewlich D, Zhang J, Gross C, Xia W, Larsen B, Cobb RR, et al. Anti-EphA2 antibodies decrease EphA2 protein levels in murine CT26 colorectal and human MDA-231 breast tumors but do not inhibit tumor growth. Neoplasia 2006; 8:18-30; PMID:16533422; http://dx.doi.org/10.1593/neo.05544