Parcellation of the thalamus into distinct nuclei reflects EphA expression and function

Gene Expression Patterns

Volumn 13, Issue 8, 2013, Pages 454-463

  Lehigh, Kathryn M ^a,b   Leonard, Carrie E ^a,c   Baranoski, Jacob ^a   Donoghue, Maria J ^a  

^a GEORGETOWN UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Development; EphA4; EphA7; Ephrin A5; Nuclei; Segregation; Thalamus

Indexed keywords

EPHRIN A5; EPHRIN RECEPTOR A4; EPHRIN RECEPTOR A7;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN DEVELOPMENT; BRAIN REGION; CELL POPULATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; INTRACELLULAR SIGNALING; LATERAL GENICULATE BODY; MOUSE; NERVE CELL DIFFERENTIATION; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RHOMBENCEPHALON; SUBTHALAMUS; SYNAPSE; THALAMUS; THALAMUS NUCLEUS;

DEVELOPMENT; EPHA4; EPHA7; EPHRIN-A5; NUCLEI; SEGREGATION; THALAMUS;

ANIMALS; GENE EXPRESSION; HEK293 CELLS; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, EPH FAMILY; SIGNAL TRANSDUCTION; THALAMUS;

EID: 84884843603     PISSN: 1567133X     EISSN: 18727298     Source Type: Journal    
DOI: 10.1016/j.gep.2013.08.002     Document Type: Article

References (72)

1. K.K. Bluske, T.Y. Vue, Y. Kawakami, M.M. Taketo, K. Yoshikawa, J.E. Johnson, and Y. Nakagawa Beta-catenin signaling specifies progenitor cell identity in parallel with Shh signaling in the developing mammalian thalamus Development 139 2012 2692 2702
2. A. Brown, P.A. Yates, P. Burrola, D. Ortuno, A. Vaidya, T.M. Jessell, S.L. Pfaff, D.D. O'Leary, and G. Lemke Topographic mapping from the retina to the midbrain is controlled by relative but not absolute levels of EphA receptor signaling Cell 102 2000 77 88
3. J. Cang, M. Kaneko, J. Yamada, G. Woods, M.P. Stryker, and D.A. Feldheim Ephrin-as guide the formation of functional maps in the visual cortex Neuron 48 2005 577 589 (Pubitemid 41654680)
4. R.F. Carvalho, M. Beutler, K.J. Marler, B. Knoll, E. Becker-Barroso, R. Heintzmann, T. Ng, and U. Drescher Silencing of EphA3 through a cis interaction with ephrinA5 Nat. Neurosci. 9 2006 322 330 (Pubitemid 43290961)
5. L. Chen, Q. Guo, and J.Y. Li Transcription factor Gbx2 acts cell-nonautonomously to regulate the formation of lineage-restriction boundaries of the thalamus Development 136 2009 1317 1326
6. H.J. Cheng, M. Nakamoto, A.D. Bergemann, and J.G. Flanagan Complementary gradients in expression and binding of ELF-1 and Mek4 in development of the topographic retinotectal projection map Cell 82 1995 371 381
7. E.N. Committee Unified nomenclature for Eph family receptors and their ligands, the ephrins. Eph nomenclature committee [letter] Cell 90 1997 403 404
8. J.E. Cooke, H.A. Kemp, and C.B. Moens EphA4 is required for cell adhesion and rhombomere-boundary formation in the zebrafish Curr. Biol. 15 2005 536 542 (Pubitemid 40413392)
9. V. Depaepe, N. Suarez-Gonzalez, A. Dufour, L. Passante, J.A. Gorski, K.R. Jones, C. Ledent, and P. Vanderhaeghen Ephrin signalling controls brain size by regulating apoptosis of neural progenitors Nature 435 2005 1244 1250 (Pubitemid 40943090)
10. A. Dufour, J. Seibt, L. Passante, V. Depaepe, T. Ciossek, J. Frisen, K. Kullander, J.G. Flanagan, F. Polleux, and P. Vanderhaeghen Area specificity and topography of thalamocortical projections are controlled by ephrin/Eph genes Neuron 39 2003 453 465 (Pubitemid 36937047)
11. J. Eberhart, J. Barr, S. O'Connell, A. Flagg, M.E. Swartz, K.S. Cramer, K.W. Tosney, E.B. Pasquale, and C.E. Krull Ephrin-A5 exerts positive or inhibitory effects on distinct subsets of EphA4-positive motor neurons J. Neurosci. 24 2004 1070 1078 (Pubitemid 38177014)
12. D.A. Feldheim, Y.I. Kim, A.D. Bergemann, J. Frisen, M. Barbacid, and J.G. Flanagan Genetic analysis of ephrin-A2 and ephrin-A5 shows their requirement in multiple aspects of retinocollicular mapping [see comments] Neuron 25 2000 563 574
13. D.A. Feldheim, M. Nakamoto, M. Osterfield, N.W. Gale, T.M. DeChiara, R. Rohatgi, G.D. Yancopoulos, and J.G. Flanagan Loss-of-function analysis of EphA receptors in retinotectal mapping J. Neurosci. 24 2004 2542 2550 (Pubitemid 38327967)
14. W.Y. Fu, Y. Chen, M. Sahin, X.S. Zhao, L. Shi, J.B. Bikoff, K.O. Lai, W.H. Yung, A.K. Fu, M.E. Greenberg, and N.Y. Ip Cdk5 regulates EphA4-mediated dendritic spine retraction through an ephexin1-dependent mechanism Nat. Neurosci. 10 2007 67 76 (Pubitemid 46026529)
15. N.W. Gale, S.J. Holland, D.M. Valenzuela, A. Flenniken, L. Pan, T.E. Ryan, M. Henkemeyer, K. Strebhardt, H. Hirai, D.G. Wilkinson, T. Pawson, S. Davis, and G.D. Yancopoulos Eph receptors and ligands comprise two major specificity subclasses and are reciprocally compartmentalized during embryogenesis Neuron 17 1996 9 19 (Pubitemid 26251587)
16. P.P. Gao, Y. Yue, J.H. Zhang, D.P. Cerretti, P. Levitt, and R. Zhou Regulation of thalamic neurite outgrowth by the Eph ligand ephrin-A5: implications in the development of thalamocortical projections Proc. Natl. Acad. Sci. USA 95 1998 5329 5334 (Pubitemid 28208597)
17. M.J. Hansen, G.E. Dallal, and J.G. Flanagan Retinal axon response to ephrin-as shows a graded, concentration-dependent transition from growth promotion to inhibition Neuron 42 2004 717 730 (Pubitemid 38748787)
18. K.F. Heintzelman, H.M. Phillips, and G.S. Davis Liquid-tissue behavior and differential cohesiveness during chick limb budding J. Embryol. Exp. Morphol. 47 1978 1 15 (Pubitemid 9037412)
19. F. Helmbacher, S. Schneider-Maunoury, P. Topilko, L. Tiret, and P. Charnay Targeting of the EphA4 tyrosine kinase receptor affects dorsal/ventral pathfinding of limb motor axons Development 127 2000 3313 3324 (Pubitemid 30649543)
20. J.P. Himanen, M.J. Chumley, M. Lackmann, C. Li, W.A. Barton, P.D. Jeffrey, C. Vearing, D. Geleick, D.A. Feldheim, A.W. Boyd, M. Henkemeyer, and D.B. Nikolov Repelling class discrimination: ephrin-A5 binds to and activates EphB2 receptor signaling Nat. Neurosci. 7 2004 501 509 (Pubitemid 38544589)
21. J.P. Himanen, and D.B. Nikolov Eph signaling: a structural view Trends Neurosci. 26 2003 46 51 (Pubitemid 35463373)
22. J.P. Himanen, K.R. Rajashankar, M. Lackmann, C.A. Cowan, M. Henkemeyer, and D.B. Nikolov Crystal structure of an Eph receptor-ephrin complex Nature 414 2001 933 938 (Pubitemid 34024747)
23. S.J. Holland, N.W. Gale, G. Mbamalu, G.D. Yancopoulos, M. Henkemeyer, and T. Pawson Bidirectional signalling through the Eph-family receptor Nuk and its transmembrane ligands Nature 383 1996 722
24. J. Holmberg, D.L. Clarke, and J. Frisen Regulation of repulsion versus adhesion by different splice forms of an Eph receptor Nature 408 2000 203 206
25. M. Hruska, and M.B. Dalva Ephrin regulation of synapse formation, function and plasticity Mol. Cell. Neurosci. 50 2012 35 44
26. A.D. Huberman, K.D. Murray, D.K. Warland, D.A. Feldheim, and B. Chapman Ephrin-As mediate targeting of eye-specific projections to the lateral geniculate nucleus Nat. Neurosci. 8 2005 1013 1021 (Pubitemid 41061511)
27. D.M. Jacobowitz, and L.C. Abbott Chemoarchitectonic Atlas of the Developing Mouse Brain 1998 CRC Press Boca Raton
28. B. Knoll, and U. Drescher Src family kinases are involved in EphA receptor-mediated retinal axon guidance J. Neurosci. 24 2004 6248 6257 (Pubitemid 38944214)
29. K. Kullander, S.J. Butt, J.M. Lebret, L. Lundfald, C.E. Restrepo, A. Rydstrom, R. Klein, and O. Kiehn Role of EphA4 and EphrinB3 in local neuronal circuits that control walking Science 299 2003 1889 1892 (Pubitemid 36358203)
30. K. Kullander, S.D. Croll, M. Zimmer, L. Pan, J. McClain, V. Hughes, S. Zabski, T.M. DeChiara, R. Klein, G.D. Yancopoulos, and N.W. Gale Ephrin-B3 is the midline barrier that prevents corticospinal tract axons from recrossing, allowing for unilateral motor control Genes Dev. 15 2001 877 888 (Pubitemid 32295068)
31. K. Kullander, and R. Klein Mechanisms and functions of Eph and ephrin signalling Nat. Rev. Mol. Cell Biol. 3 2002 475 486 (Pubitemid 34733429)
32. K. Kullander, N.K. Mather, F. Diella, M. Dottori, A.W. Boyd, and R. Klein Kinase-dependent and kinase-independent functions of EphA4 receptors in major axon tract formation in vivo Neuron 29 2001 73 84 (Pubitemid 32108723)
33. K. Mackarehtschian, C.K. Lau, I. Caras, and S.K. McConnell Regional differences in the developing cerebral cortex revealed by ephrin-A5 expression Cereb. Cortex 9 1999 601 610 (Pubitemid 29441501)
34. S.S. Margolis, J. Salogiannis, D.M. Lipton, C. Mandel-Brehm, Z.P. Wills, A.R. Mardinly, L. Hu, P.L. Greer, J.B. Bikoff, H.Y. Ho, M.J. Soskis, M. Sahin, and M.E. Greenberg EphB-mediated degradation of the RhoA GEF Ephexin5 relieves a developmental brake on excitatory synapse formation Cell 143 2010 442 455
35. A. Martinez, R. Otal, and E. Soriano Garcia Ephrins, neuronal development and plasticity Rev. Neurol. 38 2004 647 655 (Pubitemid 38788531)
36. G. Mellitzer, Q. Xu, and D.G. Wilkinson Eph receptors and ephrins restrict cell intermingling and communication Nature 400 1999 77 81 (Pubitemid 29315114)
37. K. Miller, S.M. Kolk, and M.J. Donoghue EphA7-ephrin-A5 signaling in mouse somatosensory cortex: developmental restriction of molecular domains and postnatal maintenance of functional compartments J. Comp. Neurol. 496 2006 627 642
38. K.K. Murai, L.N. Nguyen, F. Irie, Y. Yamaguchi, and E.B. Pasquale Control of hippocampal dendritic spine morphology through ephrin-A3/EphA4 signaling Nat. Neurosci. 6 2003 153 160 (Pubitemid 36182784)
39. Y. Nakagawa, J.E. Johnson, and D.D.M. O'Leary Graded and areal expression patterns of regulatory genes and cadherins in embryonic neocortex independent of thalamocortical input J. Neurosci. 19 1999 10877 10885 (Pubitemid 30235732)
40. Y. Nakagawa, and D.D. O'Leary Combinatorial expression patterns of LIM-homeodomain and other regulatory genes parcellate developing thalamus J. Neurosci. 21 2001 2711 2725 (Pubitemid 32298213)
41. Y. Nakagawa, and D.D. O'Leary Dynamic patterned expression of orphan nuclear receptor genes RORalpha and RORbeta in developing mouse forebrain Dev. Neurosci. 25 2003 234 244 (Pubitemid 37100216)
42. Y. Nakagawa, and T. Shimogori Diversity of thalamic progenitor cells and postmitotic neurons Eur. J. Neurosci. 35 2012 1554 1562
43. D. Nie, A. Di Nardo, J.M. Han, H. Baharanyi, I. Kramvis, T. Huynh, S. Dabora, S. Codeluppi, P.P. Pandolfi, E.B. Pasquale, and M. Sahin Tsc2-Rheb signaling regulates EphA-mediated axon guidance Nat. Neurosci. 13 2010 163 172
44. N.K. Noren, and E.B. Pasquale Eph receptor-ephrin bidirectional signals that target Ras and Rho proteins Cell Signal. 16 2004 655 666 (Pubitemid 38490547)
45. H.A. North, M.A. Clifford, and M.J. Donoghue 'Til Eph Do Us Part': Intercellular signaling via eph receptors and ephrin ligands guides cerebral cortical development from birth through maturation Cereb. Cortex 23 2013 1765 1773
46. H.A. North, A. Karim, M.F. Jacquin, and M.J. Donoghue EphA4 is necessary for spatially selective peripheral somatosensory topography Dev. Dyn. 239 2010 630 638
47. H.A. North, X. Zhao, S.M. Kolk, M.A. Clifford, D.M. Ziskind, and M.J. Donoghue Promotion of proliferation in the developing cerebral cortex by EphA4 forward signaling Development 136 2009 2467 2476
48. E. Oricchio, G. Nanjangud, A.L. Wolfe, J.H. Schatz, K.J. Mavrakis, M. Jiang, X. Liu, J. Bruno, A. Heguy, A.B. Olshen, N.D. Socci, J. Teruya-Feldstein, F. Weis-Garcia, W. Tam, R. Shaknovich, A. Melnick, J.P. Himanen, R.S. Chaganti, and H.G. Wendel The Eph-receptor A7 is a soluble tumor suppressor for follicular lymphoma Cell 147 2011 554 564
49. E.B. Pasquale Eph receptor signalling casts a wide net on cell behaviour Nat. Rev. Mol. Cell Biol. 6 2005 462 475 (Pubitemid 40780558)
50. E.B. Pasquale Eph-ephrin bidirectional signaling in physiology and disease Cell 133 2008 38 52 (Pubitemid 351442996)
51. D.B. Polley, E. Kvasnak, and R.D. Frostig Naturalistic experience transforms sensory maps in the adult cortex of caged animals Nature 429 2004 67 71 (Pubitemid 38620551)
52. N. Prakash, P. Vanderhaeghen, S. Cohen-Cory, J. Frisen, J. Flanagan, and R. Frostig Malformation of the functional organization of somatosensory cortex in adult ephrin-A5 knock-out mice revealed by in vivo functional imaging J. Neurosci. 20 2000 5841 5847 (Pubitemid 30636914)
53. L. Puelles, and J.L. Rubenstein Forebrain gene expression domains and the evolving prosomeric model Trends Neurosci. 26 2003 469 476 (Pubitemid 37025784)
54. T. Rashid, A.L. Upton, A. Blentic, T. Ciossek, B. Knoll, I.D. Thompson, and U. Drescher Opposing gradients of Ephrin-As and EphA7 in the superior colliculus are essential for topographic mapping in the mammalian visual system Neuron 47 2005 57 69
55. M. Richter, K.K. Murai, C. Bourgin, D.T. Pak, and E.B. Pasquale The EphA4 receptor regulates neuronal morphology through SPAR-mediated inactivation of Rap GTPases J. Neurosci. 27 2007 14205 14215 (Pubitemid 351377865)
56. M. Sahin, P.L. Greer, M.Z. Lin, H. Poucher, J. Eberhart, S. Schmidt, T.M. Wright, S.M. Shamah, S. O'Connell, C.W. Cowan, L. Hu, J.L. Goldberg, A. Debant, G. Corfas, C.E. Krull, and M.E. Greenberg Eph-dependent tyrosine phosphorylation of ephexin1 modulates growth cone collapse Neuron 46 2005 191 204 (Pubitemid 40545776)
57. Schambra, U.B., Lauder, J.M., Silver, J., 1992. Atlas of the Prenatal Mouse Brain, Academic Press, San Diego, xxix, p. 327.
58. N. Sestan, P. Rakic, and M.J. Donoghue Independent parcellation of the embryonic visual cortex and thalamus revealed by combinatorial Eph/ephrin gene expression Curr. Biol. 11 2001 39 43 (Pubitemid 32062714)
59. S.M. Sherman, and R.W. Guillery The role of the thalamus in the flow of information to the cortex Philos. Trans. R. Soc. Lond. B Biol. Sci. 357 2002 1695 1708 (Pubitemid 36080517)
60. A.M. Sillito, and H.E. Jones Corticothalamic interactions in the transfer of visual information Philos. Trans. R. Soc. Lond. B Biol. Sci. 357 2002 1739 1752 (Pubitemid 36080521)
61. W.A. Thomas, and J. Yancey Can retinal adhesion mechanisms determine cell-sorting patterns: a test of the differential adhesion hypothesis Development 103 1988 37 48
62. M. Torii, and P. Levitt Dissociation of corticothalamic and thalamocortical axon targeting by an EphA7-mediated mechanism Neuron 48 2005 563 575 (Pubitemid 41654679)
63. M. Torii, P. Rakic, and P. Levitt Role of EphA/ephrin - a signaling in the development of topographic maps in mouse corticothalamic projections J. Comp. Neurol. 521 2013 626 637
64. D. Uziel, P. Garcez, R. Lent, C. Peuckert, R. Niehage, F. Weth, and J. Bolz Connecting thalamus and cortex: the role of ephrins Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 288 2006 135 142 (Pubitemid 43208624)
65. P. Vanderhaeghen, Q. Lu, N. Prakash, J. Frisen, C.A. Walsh, R.D. Frostig, and J.G. Flanagan A mapping label required for normal scale of body representation in the cortex Nat. Neurosci. 3 2000 358 365 (Pubitemid 30185486)
66. T.Y. Vue, J. Aaker, A. Taniguchi, C. Kazemzadeh, and J.M. Skidmore Characterization of progenitor domains in the developing mouse thalamus J. Comp Neurol. 505 2007 73 91 (Pubitemid 350068231)
67. T.Y. Vue, K. Bluske, A. Alishahi, L.L. Yang, N. Koyano-Nakagawa, B. Novitch, and Y. Nakagawa Sonic hedgehog signaling controls thalamic progenitor identity and nuclei specification in mice J. Neurosci. 29 2009 4484 4497
68. L. Wang, K.K. Bluske, L.K. Dickel, and Y. Nakagawa Basal progenitor cells in the embryonic mouse thalamus-their molecular characterization and the role of neurogenins and Pax6 Neural Dev. 6 2011 35
69. Q. Xu, G. Mellitzer, V. Robinson, and D. Wilkinson In vivo cell sorting in complementary segmental domains by Eph receptors and ephrins Nature 399 1999
70. Q. Xu, G. Mellitzer, and D.G. Wilkinson Roles of Eph receptors and ephrins in segmental patterning Philos. Trans. R. Soc. Lond. B Biol. Sci. 355 2000 993 1002 (Pubitemid 30613324)
71. K. Yun, S. Potter, and J.L. Rubenstein Gsh2 and Pax6 play complementary roles in dorsoventral patterning of the mammalian telencephalon Development 128 2001 193 205 (Pubitemid 32124145)
72. M.E. Yun, R.R. Johnson, A. Antic, and M.J. Donoghue EphA family gene expression in the developing mouse neocortex: regional patterns reveal intrinsic programs and extrinsic influence J. Comp. Neurol. 456 2003 203 216 (Pubitemid 36110244)