Ephrin-A2 reverse signaling negatively regulates neural progenitor proliferation and neurogenesis

Genes and Development

Volumn 19, Issue 4, 2005, Pages 462-471

  Holmberg, Johan ^a   Armulik, Annika ^a   Senti, Kirsten André ^a,c   Edoff, Karin ^a   Spalding, Kirsty ^a   Momma, Stefan ^a   Cassidy, Rob ^a   Flanagan, John G ^b   Frisén, Jonas ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b HARVARD MEDICAL SCHOOL   (United States)

^c STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

Adult; Ephrins; Neuronal progenitors; Proliferation; Reverse signaling; SVZ

Indexed keywords

EPHRIN; EPHRIN A2; EPHRIN A7; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CYCLE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MOUSE; MUTANT; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WILD TYPE;

ANIMALS; BRAIN; CELL PROLIFERATION; EPHRIN-A2; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; NERVOUS SYSTEM; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; STEM CELLS;

ANIMALIA;

EID: 13844269325     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.326905     Document Type: Article

References (48)

1. Alvarez-Buylla, A. and Lim, D.A. 2004. For the long run: Maintaining germinal niches in the adult brain. Neuron 41: 683-686.
2. Batlle, E., Henderson, J.T., Beghtel, H., van den Born, M.M.W., Sancho, E., Huls, G., Meeldijk, J., Robertson, J., van de Wetering, M., Pawson, T., et al. 2002. β-Catenin and TCF mediate cell positioning in the intestinal epithelium by controlling the expression of EphB/EphrinB. Cell 111: 251-263.
3. Carlén, M., Cassidy, R.M., Brismar, H., Smith, G.A., Enquist, L.W., and Frisén, J. 2002. Functional integration of adult-born neurons. Curr. Biol. 12: 606-608.
4. Carleton, A., Petreanu, L.T., Lansford, R., Alvarez-Buylla, A., and Lledo, P.M. 2003. Becoming a new neuron in the adult olfactory bulb. Nat. Neurosci. 6: 507-518.
5. Ciossek, T., Millauer, B., and Ullrich, A. 1995. Identification of alternatively spliced mRNAs encoding variants of MDK1, a novel receptor tyrosine kinase expressed in the murine nervous system. Oncogene 10: 97-108.
6. Conover, J.C., Doetsch, F., Garcia-Verdugo, J.M., Gale, N.W., Yancopoulos, G.D., and Alvarez-Buylla, A. 2000. Disruption of Eph/ephrin signaling affects migration and proliferation in the adult subventricular zone. Nat. Neurosci. 3: 1091-1097.
7. Cowan, C.A. and Henkemeyer, M. 2002. Ephrins in reverse, park and drive. Trends Cell Biol. 12: 339-346.
8. Cutforth, T., Moring, L., Mendelsohn, M., Nemes, A., Shah, N.M., Kim, M.M., Frisen, J., and Axel, R. 2003. Axonal ephrin-As and odorant receptors: Coordinate determination of the olfactory sensory map. Cell 114: 311-322.
9. Davis, S., Gale, N.W., Aldrich, T.H., Maisonpierre, P.C., Lhotak, V., Pawson, T., Goldfarb, M., and Yancopoulos, G.D. 1994. Ligands for EPH-related receptor tyrosine kinases that require membrane attachment or clustering for activity. Science 266: 816-819.
10. Davy, A. and Robbins, S.M. 2000. Ephrin-A5 modulates cell adhesion and morphology in an integrin-dependent manner. EMBO J. 19: 5396-5405.
11. Doetsch, F., Caille, I., Lim, D.A., Garcia-Verdugo, J.M., and Alvarez-Buylla, A. 1999. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97: 703-716.
12. Donoghue, M.J. and Rakic, P. 1999. Molecular evidence for the early specification of presumptive functional domains in the embryonic primate cerebral cortex. J. Neurosci. 19: 5967-5979.
13. Feldheim, D.A., Kim, Y.I., Bergemann, A.D., Frisen, J., Barbacid, M., and Flanagan, J.G. 2000. Genetic analysis of ephrin-A2 and ephrin-A5 shows their requirement in multiple aspects of retinocollicular mapping. Neuron 25: 563-574.
14. Gage, F.H. 2002. Neurogenesis in the adult brain. J. Neurosci. 22: 612-613.
15. Gale, N.W., Holland, S.J., Valenzuela, D.M., Flenniken, A., Pan, L., Ryan, T.E., Henkemeyer, M., Strebhardt, K., Hirai, H., Wilkinson, D.G., et al. 1996. Eph receptors and ligands comprise two major specificity subclasses and are reciprocally compartmentalized during embryogenesis. Neuron 17: 9-19.
16. Henkemeyer, M., Orioli, D., Henderson, J.T., Saxton, T.M., Roder, J., Pawson, T., and Klein, R. 1996. Nuk controls path-finding of commissural axons in the mammalian central nervous system. Cell 86: 35-46.
17. Himanen, J.P., Chumley, M.J., Lackmann, M., Li, C., Barton, W.A., Jeffrey, P.D., Vearing, C., Geleick, D., Feldheim, D.A., Boyd, A.W., et al. 2004. Repelling class discrimination: Ephrin-A5 binds to and activates EphB2 receptor signaling. Nat. Neurosci. 7: 501-509.
18. Holmberg, J. and Frisén, J. 2002. Ephrins are not only unattractive. Trends Neurosci. 25: 239-243.
19. Holmberg, J., Clarke, D.L., and Frisén, J. 2000. Regulation of repulsion versus adhesion by different splice forms of an Eph receptor. Nature 408: 203-206.
20. Horner, P.J., Power, A.E., Kempermann, G., Kuhn, H.G., Palmer, T.D., Winkler, J., Thal, L.J., and Gage, F.H. 2000. Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord. J. Neurosci. 20: 2218-2228.
21. Huai, J. and Drescher, U. 2001. An ephrin-A-dependent signaling pathway controls integrin function and is linked to the tyrosine phosphorylation of a 120-kDa protein. J. Biol. Chem. 276: 6689-6694.
22. Ivanova, N.B., Dimos, J.T., Schaniel, C., Hackney, J.A., Moore, K.A., and Lemischka, I.R. 2002. A stem cell molecular signature. Science 298: 601-604.
23. Johansson, C.B., Momma, S., Clarke, D.L., Risling, M., Lendahl, U., and Frisén, J. 1999. Identification of a neural stem cell in the adult mammalian central nervous system. Cell 96: 25-34.
24. Knoll, B., Zarbalis, K., Wurst, W., and Drescher, U. 2001. A role for the EphA family in the topographic targeting of vomero-nasal axons. Development 128: 895-906.
25. Kuhn, H.G., Winkler, J., Kempermann, G., Thal, L.J., and Gage, F.H. 1997. Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J. Neurosci. 17: 5820-5829.
26. Lendahl, U., Zimmerman, L., and McKay, R. 1990. CNS stem cells express a new class of intermediate filament protein. Cell 60: 585-595.
27. Lie, D.C., Song, H., Colamarino, S.A., Ming, G.L., and Gage, F.H. 2004. Neurogenesis in the adult brain: New strategies for central nervous system diseases. Annu. Rev. Pharmacol. Toxicol. 44: 399-421.
28. Liu, W., Ahmad, S.A., Jung, Y.D., Reinmuth, N., Fan, F., Bucana, C.D., and Ellis, L.M. 2002. Coexpression of ephrin-Bs and their receptors in colon carcinoma. Cancer 94: 934-939.
29. Martens, D.J., Seaberg, R.M., and van der Kooy, D. 2002. In vivo infusions of exogenous growth factors into the fourth ventricle of the adult mouse brain increase the proliferation of neural progenitors around the fourth ventricle and the central canal of the spinal cord. Eur. J. Neurosci. 16: 1045-1057.
30. Mellitzer, G., Xu, Q., and Wilkinson, D.G. 1999. Eph receptors and ephrins restrict cell intermingling and communication. Nature 400: 77-81.
31. Miller, M.A., Ruest, P.J., Kosinski, M., Hanks, S.K., and Greenstein, D. 2003. An Eph receptor sperm-sensing control mechanism for oocyte meiotic maturation in Caenorhabditis elegans. Genes and Dev. 17: 187-200.
32. Palmer, A. and Klein, R. 2003. Multiple roles of ephrins in morphogenesis, neuronal networking, and brain function. Genes & Dev. 17: 1429-1450.
33. Palmer, T.D., Markakis, E.A., Willhoite, A.R., Safar, F., and Gage, F.H. 1999. Fibroblast growth factor-2 activates a latent neurogenic program in neural stem cells from diverse regions of the adult CNS. J. Neurosci. 19: 8487-8497.
34. Pardal, R., Clarke, M.F., and Morrison, S.J. 2003. Applying the principles of stem cell biology to cancer. Nature Rev. Cancer 3: 895-902.
35. Ramalho-Santos, M., Yoon, S., Matsuzaki, Y., Mulligan, R.C., and Melton, D.A. 2002. 'Stemness': Transcriptional profiling of embryonic and adult stem cells. Science 298: 597-600.
36. Rogers, J.H., Ciossek, T., Ullrich, A., West, E., Hoare, M., and Muir, E.M. 1999. Distribution of the receptor EphA7 and its ligands in the development of the mouse nervous system. Mol. Brain Res. 74: 225-230.
37. Schänzer, A., Wachs, F.P., Wilhelm, D., Acker, T., Cooper-Kuhn, C., Beck, H., Winkler, J., Aigner, L., Plate, K.H., and Kuhn, H.G. 2004. Direct stimulation of adult neural stem cells in vitro and neurogenesis in vivo by vascular endothelial growth factor. Brain Pathol. 14: 237-248.
38. Schmal, W. 1983. Developmental gradient of cell cycle in the telencephalic roof of the fetal NMRI-mouse. Anat. Embryol. 167: 355-364.
39. Stephenson, S.A., Slomka, S., Douglas, E.L., Hewett, P.J., and Hardingham, J.E. 2001. Receptor protein tyrosine kinase EphB4 is up-regulated in colon cancer. BMC Mol. Biol. 2: 15.
40. Tang, X.X., Evans, A.E., Zhao, H., Cnaan, A., London, W., Cohn, S.L., Brodeur, G.M., and Ikegaki, N. 1999. High-level expression of EPHB6, EFNB2, and EFNB3 is associated with low tumor stage and high TrkA expression in human neuroblastomas. Clin. Cancer Res. 5: 1491-1496.
41. Tang, X.X., Zhao, H., Robinson, M.E., Cohen, B., Cnaan, A., London, W., Cohn, S.L., Cheung, N.K., Brodeur, G.M., Evans, A.E., et al. 2000. Implications of EPHB6, EFNB2, and EFNB3 expressions in human neuroblastoma. Proc. Natl. Acad. Sci. 97: 10936-10941.
42. Tumbar, T., Guasch, G., Greco, V., Blanpain, C., Lowry, W.E., Rendl, M., and Fuchs, E. 2004. Defining the epithelial stem cell niche in skin. Science 303: 359-363.
43. van Praag, H., Schinder, A.F., Christie, B.R., Toni, N. Palmer, T.D., and Gage, F.H. 2002. Functional neurogenesis in the adult hippocampus. Nature 415: 1030-1034.
44. Weiss, S., Dunne, C., Hewson, J., Wohl, C., Wheatley, M., Peterson, A.C., and Reynolds, B.R. 1996. Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J. Neurosci. 16: 7599-7609.
45. Wilkinson, D.G. 2001. Multiple roles of EPH receptors and ephrins in neural development. Nat. Rev. Neurosci. 2: 155-164.
46. Xu, Q., Mellitzer, G., Robinson, V., and Wilkinson, D.G. 1999. In vivo cell sorting in complementary segmental domains mediated by Eph receptors and ephrins. Nature 399: 267-271.
47. Yamamoto, S., Nagao, M., Sugimori, M., Kosako, H., Nakatomi, H., Yamamoto, N., Takebayashi, H., Nabeshima, Y., Kitamura, T., Weinmaster, G., et al. 2001. Transcription factor expression and Notch-dependent regulation of neural progenitors in the adult rat spinal cord. J. Neurosci. 21: 9814-9823.
48. Zhang, J.H., Cerretti, D.P., Yu, T., Flanagan, J.G., and Zhou, R. 1996. Detection of ligands in regions anatomically connected to neurons expressing the Eph receptor Bsk: Potential roles in neuron-target interaction. J. Neurosci. 16: 7182-7192.