Eph/ephrin signaling: Genetic, phosphoproteomic, and transcriptomic approaches

Seminars in Cell and Developmental Biology

Volumn 23, Issue 1, 2012, Pages 26-34

  Bush, Jeffrey O ^a   Soriano, Philippe ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Eph; Ephrin; Microarray; Mouse; Proteomic

Indexed keywords

BETA GALACTOSIDASE; CHIMERIN; CYCLIN D1; EPHRIN A4; EPHRIN B1; EPHRIN B2; EPHRIN B3; FK 506 BINDING PROTEIN; MICRORNA; MITOGEN ACTIVATED PROTEIN KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NERVE CELL ADHESION MOLECULE; NEUROPSIN; REELIN; STAT3 PROTEIN; TRANSCRIPTION FACTOR SOX2; VASCULOTROPIN RECEPTOR 2; VASCULOTROPIN RECEPTOR 3;

ACTIN FILAMENT; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL FUNCTION; CELL PROLIFERATION; CELL SELECTION; CELL SHAPE; CELL STRESS; CRANIOFACIAL DEVELOPMENT; ENDOCYTOSIS; ENZYME ACTIVATION; GENE EXPRESSION; GENETICS; IMMEDIATE EARLY GENE; IN VIVO STUDY; INTERNALIZATION; LONG TERM DEPRESSION; LONG TERM POTENTIATION; LUNG NON SMALL CELL CANCER; MASS SPECTROMETRY; MESENCHYME CELL; MICROARRAY ANALYSIS; NERVE CELL DIFFERENTIATION; NONHUMAN; POINT MUTATION; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEOMICS; REVIEW; SCHWANN CELL; SIGNAL TRANSDUCTION; STEM CELL; TIME OF FLIGHT MASS SPECTROMETRY; TRANSCRIPTOMICS;

EID: 84857443558     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2011.10.018     Document Type: Review

References (62)

1. Henkemeyer M., Orioli D., Henderson J.T., Saxton T.M., Roder J., Pawson T., et al. Nuk controls pathfinding of commissural axons in the mammalian central nervous system. Cell 1996, 86:35-46.
2. Orioli D., Henkemeyer M., Lemke G., Klein R., Pawson T. Sek4 and Nuk receptors cooperate in guidance of commissural axons and in palate formation. Embo J 1996, 15:6035-6049.
3. Davy A., Soriano P. Ephrin signaling in vivo: look both ways. Dev Dyn 2005, 232:1-10.
4. Risley M., Garrod D., Henkemeyer M., McLean W. EphB2 and EphB3 forward signalling are required for palate development. Mech Dev 2009, 126:230-239.
5. Bush J.O., Soriano P. Ephrin-B1 regulates axon guidance by reverse signaling through a PDZ-dependent mechanism. Genes Dev 2009, 23:1586-1599.
6. Compagni A., Logan M., Klein R., Adams R.H. Control of skeletal patterning by ephrinB1-EphB interactions. Dev Cell 2003, 5:217-230.
7. Davy A., Aubin J., Soriano P. Ephrin-B1 forward and reverse signaling are required during mouse development. Genes Dev 2004, 18:572-583.
8. Dottori M., Hartley L., Galea M., Paxinos G., Polizzotto M., Kilpatrick T., et al. EphA4 (Sek1) receptor tyrosine kinase is required for the development of the corticospinal tract. Proc Natl Acad Sci USA 1998, 95:13248-13253.
9. Kullander K., Butt S.J., Lebret J.M., Lundfald L., Restrepo C.E., Rydstrom A., et al. Role of EphA4 and EphrinB3 in local neuronal circuits that control walking. Science 2003, 299:1889-1892.
10. Kullander K., Croll S.D., Zimmer M., Pan L., McClain J., Hughes V., et al. Ephrin-B3 is the midline barrier that prevents corticospinal tract axons from recrossing, allowing for unilateral motor control. Genes Dev 2001, 15:877-888.
11. Kullander K., Mather N.K., Diella F., Dottori M., Boyd A.W., Klein R. Kinase-dependent and kinase-independent functions of EphA4 receptors in major axon tract formation in vivo. Neuron 2001, 29:73-84.
12. Yokoyama N., Romero M.I., Cowan C.A., Galvan P., Helmbacher F., Charnay P., et al. Forward signaling mediated by ephrin-B3 prevents contralateral corticospinal axons from recrossing the spinal cord midline. Neuron 2001, 29:85-97.
13. Egea J., Nissen U.V., Dufour A., Sahin M., Greer P., Kullander K., et al. Regulation of EphA 4 kinase activity is required for a subset of axon guidance decisions suggesting a key role for receptor clustering in Eph function. Neuron 2005, 47:515-528.
14. Beg A.A., Sommer J.E., Martin J.H., Scheiffele P. alpha2-Chimaerin is an essential EphA4 effector in the assembly of neuronal locomotor circuits. Neuron 2007, 55:768-778.
15. Wegmeyer H., Egea J., Rabe N., Gezelius H., Filosa A., Enjin A., et al. EphA4-dependent axon guidance is mediated by the RacGAP alpha2-chimaerin. Neuron 2007, 55:756-767.
16. Shi L., Fu W.Y., Hung K.W., Porchetta C., Hall C., Fu A.K., et al. Alpha2-chimaerin interacts with EphA4 and regulates EphA4-dependent growth cone collapse. Proc Natl Acad Sci USA 2007, 104:16347-16352.
17. Fawcett J.P., Georgiou J., Ruston J., Bladt F., Sherman A., Warner N., et al. Nck adaptor proteins control the organization of neuronal circuits important for walking. Proc Natl Acad Sci USA 2007, 104:20973-20978.
18. Cowan C.A., Henkemeyer M. Ephrins in reverse, park and drive. Trends Cell Biol 2002, 12:339-346.
19. Mendes S.W., Henkemeyer M., Liebl D.J. Multiple Eph receptors and B-class ephrins regulate midline crossing of corpus callosum fibers in the developing mouse forebrain. J Neurosci 2006, 26:882-892.
20. Gerety S.S., Wang H.U., Chen Z.F., Anderson D.J. Symmetrical mutant phenotypes of the receptor EphB4 and its specific transmembrane ligand ephrin-B2 in cardiovascular development. Mol Cell 1999, 4:403-414.
21. Wang H.U., Chen Z.F., Anderson D.J. Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell 1998, 93:741-753.
22. Makinen T., Adams R.H., Bailey J., Lu Q., Ziemiecki A., Alitalo K., et al. PDZ interaction site in ephrinB2 is required for the remodeling of lymphatic vasculature. Genes Dev 2005, 19:397-410.
23. Sawamiphak S., Seidel S., Essmann C.L., Wilkinson G.A., Pitulescu M.E., Acker T., et al. Ephrin-B2 regulates VEGFR2 function in developmental and tumour angiogenesis. Nature 2010, 465:487-491.
24. Wang Y., Nakayama M., Pitulescu M.E., Schmidt T.S., Bochenek M.L., Sakakibara A., et al. Ephrin-B2 controls VEGF-induced angiogenesis and lymphangiogenesis. Nature 2010, 465:483-486.
25. Davy A., Soriano P. Ephrin-B2 forward signaling regulates somite patterning and neural crest cell development. Dev Biol 2007, 304:182-193.
26. Bouzioukh F., Wilkinson G.A., Adelmann G., Frotscher M., Stein V., Klein R. Tyrosine phosphorylation sites in ephrinB2 are required for hippocampal long-term potentiation but not long-term depression. J Neurosci 2007, 27:11279-11288.
27. Xu N.J., Henkemeyer M. Ephrin-B3 reverse signaling through Grb4 and cytoskeletal regulators mediates axon pruning. Nat Neurosci 2009, 12:268-276.
28. Senturk A., Pfennig S., Weiss A., Burk K., Acker-Palmer A. Ephrin Bs are essential components of the Reelin pathway to regulate neuronal migration. Nature 2011.
29. Palmer A., Zimmer M., Erdmann K.S., Eulenburg V., Porthin A., Heumann R., et al. EphrinB phosphorylation and reverse signaling: regulation by Src kinases and PTP-BL phosphatase. Mol Cell 2002, 9:725-737.
30. Cowan C.A., Yokoyama N., Saxena A., Chumley M.J., Silvany R.E., Baker L.A., et al. Ephrin-B2 reverse signaling is required for axon pathfinding and cardiac valve formation but not early vascular development. Dev Biol 2004, 271:263-271.
31. Dravis C., Yokoyama N., Chumley M.J., Cowan C.A., Silvany R.E., Shay J., et al. Bidirectional signaling mediated by ephrin-B2 and EphB2 controls urorectal development. Dev Biol 2004, 271:272-290.
32. Essmann C.L., Martinez E., Geiger J.C., Zimmer M., Traut M.H., Stein V., et al. Serine phosphorylation of ephrinB2 regulates trafficking of synaptic AMPA receptors. Nat Neurosci 2008, 11:1035-1043.
33. Nita-Lazar A., Saito-Benz H., White F.M. Quantitative phosphoproteomics by mass spectrometry: past, present, and future. Proteomics 2008, 8:4433-4443.
34. Macek B., Mann M., Olsen J.V. Global and site-specific quantitative phosphoproteomics: principles and applications. Annu Rev Pharmacol Toxicol 2009, 49:199-221.
35. Zhang G., Fenyo D., Neubert T.A. Screening for EphB signaling effectors using SILAC with a linear ion trap-orbitrap mass spectrometer. J Proteome Res 2008, 7:4715-4726.
36. Zhang G., Spellman D.S., Skolnik E.Y., Neubert T.A. Quantitative phosphotyrosine proteomics of EphB2 signaling by stable isotope labeling with amino acids in cell culture (SILAC). J Proteome Res 2006, 5:581-588.
37. Stahl S., Mm Branca R., Efazat G., Ruzzene M., Zhivotovsky B., Lewensohn R., et al. Phosphoproteomic profiling of NSCLC cells reveals that ephrin B3 regulates pro-survival signaling through Akt1-mediated phosphorylation of the EphA2 receptor. J Proteome Res 2011.
38. 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, 128:571-580.
39. Davy A., Bush J.O., Soriano P. Inhibition of gap junction communication at ectopic Eph/ephrin boundaries underlies craniofrontonasal syndrome. PLoS Biol 2006, 4:e315.
40. Xu Q., Mellitzer G., Robinson V., Wilkinson D.G. In vivo cell sorting in complementary segmental domains mediated by Eph receptors and ephrins. Nature 1999, 399:267-271.
41. Parrinello S., Napoli I., Ribeiro S., Digby P.W., Fedorova M., Parkinson D.B., et al. EphB signaling directs peripheral nerve regeneration through Sox2-dependent Schwann cell sorting. Cell 2010, 143:145-155.
42. Cortina C., Palomo-Ponce S., Iglesias M., Fernandez-Masip J.L., Vivancos A., Whissell G., et al. EphB-ephrin-B interactions suppress colorectal cancer progression by compartmentalizing tumor cells. Nat Genet 2007, 39:1376-1383.
43. Jorgensen C., Sherman A., Chen G.I., Pasculescu A., Poliakov A., Hsiung M., et al. Cell-specific information processing in segregating populations of Eph receptor ephrin-expressing cells. Science 2009, 326:1502-1509.
44. Poliakov A., Cotrina M.L., Pasini A., Wilkinson D.G. Regulation of EphB2 activation and cell repulsion by feedback control of the MAPK pathway. J Cell Biol 2008, 183:933-947.
45. Bush J.O., Soriano P. Ephrin-B1 forward signaling regulates craniofacial morphogenesis by controlling cell proliferation across Eph-ephrin boundaries. Genes Dev 2010, 24:2068-2080.
46. Kong C., Su X., Chen P.I., Stahl P.D. Rin1 interacts with signal-transducing adaptor molecule (STAM) and mediates epidermal growth factor receptor trafficking and degradation. J Biol Chem 2007, 282:15294-15301.
47. Deininger K., Eder M., Kramer E.R., Zieglgansberger W., Dodt H.U., Dornmair K., et al. The Rab5 guanylate exchange factor Rin1 regulates endocytosis of the EphA4 receptor in mature excitatory neurons. Proc Natl Acad Sci USA 2008, 105:12539-12544.
48. Attwood B.K., Bourgognon J.M., Patel S., Mucha M., Schiavon E., Skrzypiec A.E., et al. Neuropsin cleaves EphB2 in the amygdala to control anxiety. Nature 2011.
49. Dalva M.B., Takasu M.A., Lin M.Z., Shamah S.M., Hu L., Gale N.W., et al. EphB receptors interact with NMDA receptors and regulate excitatory synapse formation. Cell 2000, 103:945-956.
50. Takasu M.A., Dalva M.B., Zigmond R.E., Greenberg M.E. Modulation of NMDA receptor-dependent calcium influx and gene expression through EphB receptors. Science 2002, 295:491-495.
51. Batlle E., Henderson J.T., Beghtel H., van den Born M.M., 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, 111:251-263.
52. Holmberg J., Genander M., Halford M.M., Anneren C., Sondell M., Chumley M.J., et al. EphB receptors coordinate migration and proliferation in the intestinal stem cell niche. Cell 2006, 125:1151-1163.
53. Genander M., Halford M.M., Xu N.J., Eriksson M., Yu Z., Qiu Z., et al. Dissociation of EphB2 signaling pathways mediating progenitor cell proliferation and tumor suppression. Cell 2009, 139:679-692.
54. Georgakopoulos A., Litterst C., Ghersi E., Baki L., Xu C., Serban G., et al. Metalloproteinase/Presenilin1 processing of ephrinB regulates EphB-induced Src phosphorylation and signaling. Embo J 2006, 25:1242-1252.
55. Tomita T., Tanaka S., Morohashi Y., Iwatsubo T. Presenilin-dependent intramembrane cleavage of ephrin-B1. Mol Neurodegener 2006, 1:2.
56. Wu C., Qiu R., Wang J., Zhang H., Murai K., Lu Q. ZHX2 Interacts with Ephrin-B and regulates neural progenitor maintenance in the developing cerebral cortex. J Neurosci 2009, 29:7404-7412.
57. Arvanitis D.N., Jungas T., Behar A., Davy A. Ephrin-B1 reverse signaling controls a posttranscriptional feedback mechanism via miR-124. Mol Cell Biol 2010, 30:2508-2517.
58. Adams R.H., Wilkinson G.A., Weiss C., Diella F., Gale N.W., Deutsch U., et al. Roles of ephrinB ligands and EphB receptors in cardiovascular development: demarcation of arterial/venous domains, vascular morphogenesis, and sprouting angiogenesis. Genes Dev 1999, 13:295-306.
59. Grunwald I.C., Korte M., Adelmann G., Plueck A., Kullander K., Adams R.H., et al. Hippocampal plasticity requires postsynaptic ephrinBs. Nat Neurosci 2004, 7:33-40.
60. Grunwald I.C., Korte M., Wolfer D., Wilkinson G.A., Unsicker K., Lipp H.P., et al. Kinase-independent requirement of EphB2 receptors in hippocampal synaptic plasticity. Neuron 2001, 32:1027-1040.
61. Wilkinson G.A., Schittny J.C., Reinhardt D.P., Klein R. Role for ephrinB2 in postnatal lung alveolar development and elastic matrix integrity. Dev Dyn 2008, 237:2220-2234.
62. Hsieh C.Y., Nakamura P.A., Luk S.O., Miko I.J., Henkemeyer M., Cramer K.S. Ephrin-B reverse signaling is required for formation of strictly contralateral auditory brainstem pathways. J Neurosci 2010, 30:9840-9849.