Ephrin-B1 regulates axon guidance by reverse signaling through a PDZ-dependent mechanism

Genes and Development

Volumn 23, Issue 13, 2009, Pages 1586-1599

  Bush, Jeffrey O ^a   Soriano, Philippe ^a  

^a NONE

Author keywords

Corpus callosum; Craniofrontonasal syndrome; Ephrin; Reverse signaling

Indexed keywords

EPHRIN B1; PDZ PROTEIN; TYROSINE KINASE RECEPTOR; EPHRIN RECEPTOR B2; GLIAL FIBRILLARY ASTROCYTIC PROTEIN, MOUSE; NERVE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GENE; CORPUS CALLOSUM; CRANIOFACIAL MALFORMATION; IMMUNOPRECIPITATION; MOUSE; NERVE FIBER; NONHUMAN; PATHOGENESIS; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; AMINO ACID SEQUENCE; ANIMAL; ANIMAL EMBRYO; BONE; CELL CULTURE; CHEMISTRY; FEMALE; GENE EXPRESSION REGULATION; GENE TARGETING; GENETICS; MALE; METABOLISM; MOLECULAR GENETICS; MUTATION; PDZ DOMAIN; PHYSIOLOGY; PRENATAL DEVELOPMENT; SKULL;

MUS;

AMINO ACID SEQUENCE; ANIMALS; AXONS; BONE AND BONES; CELLS, CULTURED; CORPUS CALLOSUM; EMBRYO, MAMMALIAN; EPHRIN-B1; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCK-IN TECHNIQUES; MALE; MICE; MOLECULAR SEQUENCE DATA; MUTATION; NERVE TISSUE PROTEINS; PDZ DOMAINS; RECEPTOR, EPHB2; SIGNAL TRANSDUCTION; SKULL;

EID: 67649649790     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1807209     Document Type: Article

References (54)

1. Adams RH, Wilkinson GA,Weiss C, Diella F, Gale NW, Deutsch U, RisauW, Klein R. 1999. Roles of ephrinB ligands and EphB receptors in cardiovascular development: Demarcation of arterial/venous domains, vascular morphogenesis, and sprouting angiogenesis. Genes & Dev 13: 295-306. (Pubitemid 29095801)
2. Bagri A, Marin O, Plump AS, Mak J, Pleasure SJ, Rubenstein JL, Tessier-Lavigne M. 2002. Slit proteins prevent midline crossing and determine the dorsoventral position of major axonal pathways in the mammalian forebrain. Neuron 33: 233-248. (Pubitemid 34127756)
3. Birgbauer E, Cowan CA, Sretavan DW, Henkemeyer M. 2000. Kinase independent function of EphB receptors in retinal axon pathfinding to the optic disc from dorsal but not ventral retina. Development 127: 1231-1241. (Pubitemid 30179513)
4. Birgbauer E, Oster SF, Severin CG, Sretavan DW. 2001. Retinal axon growth cones respond to EphB extracellular domains as inhibitory axon guidance cues. Development 128: 3041-3048. Blits-Huizinga CT, Nelersa CM, Malhotra A, Liebl DJ. 2004. Ephrins and their receptors: Binding versus biology. IUBMB Life 56: 257-265. (Pubitemid 32771634)
5. Bong YS, Park YH, Lee HS, Mood K, Ishimura A, Daar IO. 2004. Tyr-298 in ephrinB1 is critical for an interaction with the Grb4 adaptor protein. Biochem J 377: 499-507. (Pubitemid 38142205)
6. Bouzioukh F, Wilkinson GA, Adelmann G, Frotscher M, Stein V, Klein R. 2007. Tyrosine phosphorylation sites in ephrinB2 are required for hippocampal long-term potentiation but not long-term depression. J Neurosci 27: 11279-11288. (Pubitemid 47621306)
7. Bruckner K, Pasquale EB, Klein R. 1997. Tyrosine phosphorylation of transmembrane ligands for Eph receptors. Science 275: 1640-1643. (Pubitemid 27120539)
8. Chalasani SH, Sabelko KA, Sunshine MJ, Littman DR, Raper JA. 2003. A chemokine, SDF-1, reduces the effectiveness of multiple axonal repellents and is required for normal axon pathfinding. J Neurosci 23: 1360-1371. (Pubitemid 36258914)
9. Chong LD, Park EK, Latimer E, Friesel R, Daar IO. 2000. Fibroblast growth factor receptor-mediated rescue of x-ephrin B1-induced cell dissociation in Xenopus embryos. Mol Cell Biol 20: 724-734. (Pubitemid 30023114)
10. Compagni A, Logan M, Klein R, Adams RH. 2003. Control of skeletal patterning by ephrinB1-EphB interactions. Dev Cell 5: 217-230. (Pubitemid 37006467)
11. Cowan CA, Henkemeyer M. 2001. The SH2/SH3 adaptor Grb4 transduces β-ephrin reverse signals. Nature 413: 174-179. (Pubitemid 32867879)
12. Cowan CA, Yokoyama N, Saxena A, Chumley MJ, Silvany RE, Baker LA, Srivastava D, Henkemeyer M. 2004. Ephrin-B2 reverse signaling is required for axon pathfinding and cardiac valve formation but not early vascular development. Dev Biol 271: 263-271. (Pubitemid 38833660)
13. Davy A, Soriano P. 2005. Ephrin signaling in vivo: Look both ways. Dev Dyn 232: 1-10. (Pubitemid 40070853)
14. Davy A, Aubin J, Soriano P. 2004. Ephrin-B1 forward and reverse signaling are required during mouse development. Genes & Dev 18: 572-583. (Pubitemid 38372813)
15. Davy A, Bush JO, Soriano P. 2006. Inhibition of gap junction communication at ectopic Eph/ephrin boundaries underlies craniofrontonasal syndrome. PLoS Biol 4: e315. doi: 10.1371/ journal.pbio.0040315. (Pubitemid 44610095)
16. Dickson BJ. 2002. Molecular mechanisms of axon guidance. Science 298: 1959-1964.
17. Dravis C, Yokoyama N, Chumley MJ, Cowan CA, Silvany RE, Shay J, Baker LA, Henkemeyer M. 2004. Bidirectional signaling mediated by ephrin-B2 and EphB2 controls urorectal development. Dev Biol 271: 272-290. (Pubitemid 38833661)
18. Egea J, Klein R. 2007. Bidirectional Eph-ephrin signaling during axon guidance. Trends Cell Biol 17: 230-238. (Pubitemid 46679245)
19. Henkemeyer M, Orioli D, Henderson JT, Saxton TM, Roder J, Pawson T, Klein R. 1996. Nuk controls pathfinding of commissural axons in the mammalian central nervous system. Cell 86: 35-46. (Pubitemid 26256576)
20. Holland SJ, GaleNW,Mbamalu G, Yancopoulos GD, Henkemeyer M, Pawson T. 1996. Bidirectional signalling through the EPHfamily receptor Nuk and its transmembrane ligands. Nature 383: 722-725. (Pubitemid 26360649)
21. Hu Z, Yue X, Shi G, Yue Y, Crockett DP, Blair-Flynn J, Reuhl K, Tessarollo L, Zhou R. 2003. Corpus callosum deficiency in transgenic mice expressing a truncated ephrin-A receptor. J Neurosci 23: 10963-10970. (Pubitemid 37499706)
22. Kalo MS, Yu HH, Pasquale EB. 2001. In vivo tyrosine phosphorylation sites of activated ephrin-B1 and ephB2 from neural tissue. J Biol Chem 276: 38940-38948.
23. Kapfhammer JP, Xu H, Raper JA. 2007. The detection and quantification of growth cone collapsing activities. Nat Protocols 2: 2005-2011. (Pubitemid 47308139)
24. Knoll B, Weinl C, Nordheim A, Bonhoeffer F. 2007. Stripe assay to examine axonal guidance and cell migration. Nat Protocols 2: 1216-1224. (Pubitemid 46901301)
25. Lee HS, Mood K, Battu G, Ji YJ, Singh A, Daar IO. 2009. Fibroblast growth factor receptor-induced phosphorylation of ephrinB1 modulates its interaction with Dishevelled. Mol Biol Cell 20: 124-133.
26. Lin D, Gish GD, Songyang Z, Pawson T. 1999. The carboxyl terminus of B class ephrins constitutes a PDZ domain binding motif. J Biol Chem 274: 3726-3733. (Pubitemid 29077220)
27. Lu Q, Sun EE, Klein RS, Flanagan JG. 2001. Ephrin-B reverse signaling is mediated by a novel PDZ-RGS protein and selectively inhibits G protein-coupled chemoattraction. Cell 105: 69-79. (Pubitemid 32323917)
28. Makinen T, Adams RH, Bailey J, Lu Q, Ziemiecki A, Alitalo K, Klein R, Wilkinson GA. 2005. PDZ interaction site in ephrinB2 is required for the remodeling of lymphatic vasculature. Genes & Dev 19: 397-410. (Pubitemid 40189302)
29. Mann F, Miranda E, Weinl C, Harmer E, Holt CE. 2003. β-type Eph receptors and ephrins induce growth cone collapse through distinct intracellular pathways. J Neurobiol 57: 323-336. (Pubitemid 37433466)
30. Martin JF, Bradley A, Olson EN. 1995. The paired-like homeo box gene MHox is required for early events of skeletogenesis in multiple lineages. Genes & Dev 9: 1237-1249.
31. Mendes SW, Henkemeyer M, Liebl DJ. 2006. Multiple Eph receptors and B-class ephrins regulate midline crossing of corpus callosum fibers in the developing mouse forebrain. J Neurosci 26: 882-892. (Pubitemid 43237081)
32. Orioli D, Henkemeyer M, Lemke G, Klein R, Pawson T. 1996. Sek4 and Nuk receptors cooperate in guidance of commissural axons and in palate formation. EMBO J 15: 6035-6049. (Pubitemid 26397876)
33. Palmer A, Zimmer M, Erdmann KS, Eulenburg V, Porthin A, Heumann R, Deutsch U, Klein R. 2002. EphrinB phosphorylation and reverse signaling: Regulation by Src kinases and PTP-BL phosphatase. Mol Cell 9: 725-737. (Pubitemid 34454885)
34. Paul LK, Brown WS, Adolphs R, Tyszka JM, Richards LJ, Mukherjee P, Sherr EH. 2007. Agenesis of the corpus callosum: Genetic, developmental and functional aspects of connectivity. Nat Rev Neurosci 8: 287-299. (Pubitemid 46452323)
35. Richards LJ. 2002. Surrounded by Slit - How forebrain commissural axons can be led astray. Neuron 33: 153-155. (Pubitemid 34127746)
36. Richards LJ, Plachez C, Ren T. 2004. Mechanisms regulating the development of the corpus callosum and its agenesis in mouse and human. Clin Genet 66: 276-289. (Pubitemid 39317630)
37. Risley M, Garrod D, Henkemeyer M, McLean W. 2008. EphB2 and EphB3 forward signalling are required for palate development. Mech Dev 126: 230-239.
38. Sciavolino PJ, Abrams EW, Yang L, Austenberg LP, Shen MM, Abate-Shen C. 1997. Tissue-specific expression of murine Nkx3.1 in the male urogenital system. Dev Dyn 209: 127-138. (Pubitemid 27188345)
39. Segura I, Essmann CL, Weinges S, Acker-Palmer A. 2007. Grb4 and GIT1 transduce ephrinB reverse signals modulating spine morphogenesis and synapse formation. Nat Neurosci 10: 301-310. (Pubitemid 46310476)
40. Shu T, Richards LJ. 2001. Cortical axon guidance by the glial wedge during the development of the corpus callosum. J Neurosci 21: 2749-2758. (Pubitemid 32298216)
41. Shu T, Puche AC, Richards LJ. 2003. Development of midline glial populations at the corticoseptal boundary. J Neurobiol 57: 81-94. (Pubitemid 37087788)
42. Smith KM, Ohkubo Y, Maragnoli ME, Rasin MR, Schwartz ML, Sestan N, Vaccarino FM. 2006. Midline radial glia translocation and corpus callosum formation require FGF signaling. Nat Neurosci 9: 787-797.
43. Stumm RK, Zhou C, Ara T, Lazarini F, Dubois-Dalcq M, Nagasawa T, Hollt V, Schulz S. 2003. CXCR4 regulates interneuron migration in the developing neocortex. J Neurosci 23: 5123-5130. (Pubitemid 36793240)
44. Su Z, Xu P, Ni F. 2004. Single phosphorylation of Tyr304 in the cytoplasmic tail of ephrin B2 confers high-affinity and bifunctional binding to both the SH2 domain of Grb4 and the PDZ domain of the PDZ-RGS3 protein. Eur J Biochem 271: 1725-1736. (Pubitemid 38586304)
45. Tallquist MD, Klinghoffer RA, Heuchel R, Mueting-Nelsen PF, Corrin PD, Heldin CH, Johnson RJ, Soriano P. 2000. Retention of PDGFR-β function in mice in the absence of phosphatidylinositol 3′-kinase and phospholipase Cg signaling pathways. Genes & Dev 14: 3179-3190. (Pubitemid 32015135)
46. Tanaka M, Kamata R, Takigahira M, Yanagihara K, Sakai R. 2007. Phosphorylation of ephrin-B1 regulates dissemination of gastric scirrhous carcinoma. Am J Pathol 171: 68-78. (Pubitemid 47339227)
47. Thelemann A, Petti F, Griffin G, Iwata K, Hunt T, Settinari T, Fenyo D, Gibson N, Haley JD. 2005. Phosphotyrosine signaling networks in epidermal growth factor receptor overexpressing squamous carcinoma cells. Mol Cell Proteomics 4: 356-376. (Pubitemid 40590556)
48. Torres R, Firestein BL, Dong H, Staudinger J, Olson EN, Huganir RL, Bredt DS, Gale NW, Yancopoulos GD. 1998. PDZ proteins bind, cluster, and synaptically colocalize with Eph receptors and their ephrin ligands. Neuron 21: 1453-1463. (Pubitemid 29022546)
49. Twigg SR, Kan R, Babbs C, Bochukova EG, Robertson SP, Wall SA, Morriss-Kay GM, Wilkie AO. 2004. Mutations of ephrin- B1 (EFNB1), a marker of tissue boundary formation, cause craniofrontonasal syndrome. Proc Natl Acad Sci 101: 8652-8657. (Pubitemid 38745826)
50. Wahlsten D, Bishop KM, Ozaki HS. 2006. Recombinant inbreeding in mice reveals thresholds in embryonic corpus callosum development. Genes Brain Behav 5: 170-188. (Pubitemid 43344967)
51. Wieland I, Jakubiczka S, Muschke P, Cohen M, Thiele H, Gerlach KL, Adams RH, Wieacker P. 2004. Mutations of the ephrin-B1 gene cause craniofrontonasal syndrome. Am J Hum Genet 74: 1209-1215. (Pubitemid 38669319)
52. Wieland I, Reardon W, Jakubiczka S, Franco B, KressW, Vincent- Delorme C, Thierry P, Edwards M, Konig R, Rusu C, et al. 2005. Twenty-six novel EFNB1 mutations in familial and sporadic craniofrontonasal syndrome (CFNS). Hum Mutat 26: 113-118. (Pubitemid 41040679)
53. Xu NJ, Henkemeyer M. 2009. Ephrin-B3 reverse signaling through Grb4 and cytoskeletal regulators mediates axon pruning. Nat Neurosci 12: 268-276.
54. Yokoyama N, Romero MI, Cowan CA, Galvan P, Helmbacher F, Charnay P, Parada LF, Henkemeyer M. 2001. Forward signaling mediated by ephrin-B3 prevents contralateral corticospinal axons from recrossing the spinal cord midline. Neuron 29: 85-97. (Pubitemid 32108724)