IGF-I promotes neuronal migration and positioning in the olfactory bulb and the exit of neuroblasts from the subventricular zone

European Journal of Neuroscience

Volumn 30, Issue 5, 2009, Pages 742-755

  Hurtado Chong, Anahí ^a   Yusta Boyo, María J ^b   Vergaño Vera, Eva ^a,c   Bulfone, Alessandro ^d   De Pablo, Flora ^b   Vicario Abejón, Carlos ^a,c  

^a INSTITUTO CAJAL   (Spain)

^b CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^c CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

^d Polaris Scientific Park ^*  (Italy)

Author keywords

IGF I; Neuronal migration and positioning; Olfactory bulb; Phosphoinositide 3 kinase (PI3K); Src family kinases (SFK); Subventricular zone

Indexed keywords

ADAPTOR PROTEIN; PROTEIN DISABLED 1; SOMATOMEDIN C; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; EMBRYO; INTERNEURON; MITRAL CELL; MOUSE; NERVE CELL; NEUROBLAST; NEWBORN; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SUBVENTRICULAR ZONE;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL COUNT; CELL MOVEMENT; CELLS, CULTURED; FLUORESCENT ANTIBODY TECHNIQUE; GLUTAMIC ACID; IN SITU HYBRIDIZATION; INSULIN-LIKE GROWTH FACTOR I; INTERNEURONS; MICE; MICE, KNOCKOUT; NEUROEPITHELIAL CELLS; NEUROGENESIS; NEURONS; OLFACTORY BULB; ORGAN CULTURE TECHNIQUES; PHOSPHORYLATION; PROSENCEPHALON; SIGNAL TRANSDUCTION; STEM CELLS; TYROSINE 3-MONOOXYGENASE;

EID: 69549116345     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2009.06870.x     Document Type: Article

References (48)

1. Alcantara, S., Ruiz, M., D'Arcangelo, G., Ezan, F., de Lecea, L., Curran, T., Sotelo, C. Soriano, E. (1998) Regional and cellular patterns of reelin mRNA expression in the forebrain of the developing and adult mouse. J. Neurosci., 18, 7779 7799.
2. Andrade, N., Komnenovic, V., Blake, S.M., Jossin, Y., Howell, B., Goffinet, A., Schneider, W.J. Nimpf, J. (2007) ApoER2/VLDL receptor and Dab1 in the rostral migratory stream function in postnatal neuronal migration independently of Reelin. Proc. Natl. Acad. Sci. U S A, 104, 8508 8513.
3. Ayala, R., Shu, T. Tsai, L.H. (2007) Trekking across the brain: the journey of neuronal migration. Cell, 128, 29 43.
4. Ballif, B.A., Arnaud, L. Cooper, J.A. (2003) Tyrosine phosphorylation of Disabled-1 is essential for Reelin-stimulated activation of Akt and Src family kinases. Brain Res. Mol. Brain Res., 117, 152 159.
5. Bartlett, W.P., Li, X.S., Williams, M. Benkovic, S. (1991) Localization of insulin-like growth factor-1 mRNA in murine central nervous system during postnatal development. Dev. Biol., 147, 239 250.
6. Bateman, J.M. McNeill, H. (2006) Insulin/IGF signalling in neurogenesis. Cell. Mol. Life Sci., 63, 1701 1705.
7. Beck, K.D., Powell-Braxton, L., Widmer, H.R., Valverde, J. Hefti, F. (1995) Igf1 gene disruption results in reduced brain size, CNS hypomyelination, and loss of hippocampal granule and striatal parvalbumin-containing neurons. Neuron, 14, 717 730.
8. Blake, S.M., Strasser, V., Andrade, N., Duit, S., Hofbauer, R., Schneider, W.J. Nimpf, J. (2008) Thrombospondin-1 binds to ApoER2 and VLDL receptor and functions in postnatal neuronal migration. EMBO J, 27, 3069 3080.
9. Blanchart, A., De Carlos, J.A. Lopez-Mascaraque, L. (2006) Time frame of mitral cell development in the mice olfactory bulb. J. Comp. Neurol., 496, 529 543.
10. Bock, H.H. Herz, J. (2003) Reelin activates SRC family tyrosine kinases in neurons. Curr. Biol., 13, 18 26.
11. Bock, H.H., Jossin, Y., Liu, P., Forster, E., May, P., Goffinet, A.M. Herz, J. (2003) Phosphatidylinositol 3-kinase interacts with the adaptor protein Dab1 in response to Reelin signaling and is required for normal cortical lamination. J. Biol. Chem., 278, 38772 38779.
12. Bondy, C.A. Cheng, C.M. (2004) Signaling by insulin-like growth factor 1 in brain. Eur. J. Pharmacol., 490, 25 31.
13. Bondy, C., Werner, H., Roberts, C.T. Jr. LeRoith, D. (1992) Cellular pattern of type-I insulin-like growth factor receptor gene expression during maturation of the rat brain: comparison with insulin-like growth factors I and II. Neuroscience, 46, 909 923.
14. Bulfone, A., Smiga, S.M., Shimamura, K., Peterson, A., Puelles, L. Rubenstein, J.L. (1995) T-brain-1: a homolog of Brachyury whose expression defines molecularly distinct domains within the cerebral cortex. Neuron, 15, 63 78.
15. Bulfone, A., Wang, F., Hevner, R., Anderson, S., Cutforth, T., Chen, S., Meneses, J., Pedersen, R., Axel, R. Rubenstein, J.L. (1998) An olfactory sensory map develops in the absence of normal projection neurons or GABAergic interneurons. Neuron, 21, 1273 1282.
16. Cheng, C.M., Joncas, G., Reinhardt, R.R., Farrer, R., Quarles, R., Janssen, J., McDonald, M.P., Crawley, J.N., Powell-Braxton, L. Bondy, C.A. (1998) Biochemical and morphometric analyses show that myelination in the insulin-like growth factor 1 null brain is proportionate to its neuronal composition. J. Neurosci., 18, 5673 5681.
17. Del Rio, J.A., Heimrich, B., Borrell, V., Forster, E., Drakew, A., Alcantara, S., Nakajima, K., Miyata, T., Ogawa, M., Mikoshiba, K., Derer, P., Frotscher, M. Soriano, E. (1997) A role for Cajal-Retzius cells and reelin in the development of hippocampal connections. Nature, 385, 70 74. (Pubitemid 27024555)
18. Delcourt, N., Thouvenot, E., Chanrion, B., Galeotti, N., Jouin, P., Bockaert, J. Marin, P. (2007) PACAP type I receptor transactivation is essential for IGF-1 receptor signalling and antiapoptotic activity in neurons. EMBO J, 26, 1542 1551.
19. Doetsch, F., Caille, I., Lim, D.A., Garcia-Verdugo, J.M. Alvarez-Buylla, A. (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell, 97, 703 716.
20. Gupta, A., Sanada, K., Miyamoto, D.T., Rovelstad, S., Nadarajah, B., Pearlman, A.L., Brunstrom, J. Tsai, L.H. (2003) Layering defect in p35 deficiency is linked to improper neuronal-glial interaction in radial migration. Nat. Neurosci., 6, 1284 1291.
21. Hack, I., Bancila, M., Loulier, K., Carroll, P. Cremer, H. (2002) Reelin is a detachment signal in tangential chain-migration during postnatal neurogenesis. Nat. Neurosci., 5, 939 945.
22. Hack, M.A., Saghatelyan, A., de Chevigny, A., Pfeifer, A., Ashery-Padan, R., Lledo, P.M. Gotz, M. (2005) Neuronal fate determinants of adult olfactory bulb neurogenesis. Nat. Neurosci., 8, 865 872.
23. Hinds, J.W. (1968) Autoradiographic study of histogenesis in the mouse olfactory bulb. I. Time of origin of neurons and neuroglia. The Journal of comparative neurology, 134, 287 304.
24. Hinds, J.W. (1972) Early neuron differentiation in the mouse of olfactory bulb. I. Light microscopy. J Comp Neurol, 146, 233 252.
25. Howell, B.W., Gertler, F.B. Cooper, J.A. (1997a) Mouse disabled (mDab1): a Src binding protein implicated in neuronal development. EMBO J, 16, 121 132.
26. Howell, B.W., Hawkes, R., Soriano, P. Cooper, J.A. (1997b) Neuronal position in the developing brain is regulated by mouse disabled-1. Nature, 389, 733 737.
27. Howell, B.W., Herrick, T.M., Hildebrand, J.D., Zhang, Y. Cooper, J.A. (2000) Dab1 tyrosine phosphorylation sites relay positional signals during mouse brain development. Curr. Biol., 10, 877 885.
28. Jossin, Y. Goffinet, A.M. (2007) Reelin signals through phosphatidylinositol 3-kinase and Akt to control cortical development and through mTor to regulate dendritic growth. Mol. Cell. Biol., 27, 7113 7124.
29. Keshvara, L., Magdaleno, S., Benhayon, D. Curran, T. (2002) Cyclin-dependent kinase 5 phosphorylates disabled 1 independently of Reelin signaling. J. Neurosci., 22, 4869 4877.
30. Kuo, G., Arnaud, L., Kronstad-O'Brien, P. Cooper, J.A. (2005) Absence of Fyn and Src causes a reeler-like phenotype. J. Neurosci., 25, 8578 8586.
31. Liu, J.P., Baker, J., Perkins, A.S., Robertson, E.J. Efstratiadis, A. (1993) Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igf1r). Cell, 75, 59 72.
32. Lois, C. Alvarez-Buylla, A. (1994) Long-distance neuronal migration in the adult mammalian brain. Science (New York, N.Y.), 264, 1145 1148.
33. Luque, J.M., Morante-Oria, J. Fairen, A. (2003) Localization of ApoER2, VLDLR and Dab1 in radial glia: groundwork for a new model of reelin action during cortical development. Brain Res. Dev. Brain Res., 140, 195 203.
34. Martinez-Cerdeno, V., Galazo, M.J. Clasca, F. (2003) Reelin- immunoreactive neurons, axons, and neuropil in the adult ferret brain: evidence for axonal secretion of reelin in long axonal pathways. J. Comp. Neurol., 463, 92 116.
35. Merkle, F.T., Mirzadeh, Z. Alvarez-Buylla, A. (2007) Mosaic organization of neural stem cells in the adult brain. Science, 317, 381 384.
36. Ng, K.L., Li, J.D., Cheng, M.Y., Leslie, F.M., Lee, A.G. Zhou, Q.Y. (2005) Dependence of olfactory bulb neurogenesis on prokineticin 2 signaling. Science (New York, N.Y.), 308, 1923 1927.
37. Nomura, T. Osumi, N. (2004) Misrouting of mitral cell progenitors in the Pax6/small eye rat telencephalon. Development, 131, 787 796.
38. Otaegi, G., Yusta-Boyo, M.J., Vergano-Vera, E., Mendez-Gomez, H.R., Carrera, A.C., Abad, J.L., Gonzalez, M., de la Rosa, E.J., Vicario-Abejon, C. de Pablo, F. (2006) Modulation of the PI 3-kinase-Akt signalling pathway by IGF-I and PTEN regulates the differentiation of neural stem/precursor cells. J. Cell Sci., 119, 2739 2748.
39. Pichel, J.G., Fernandez-Moreno, C., Vicario-Abejon, C., Testillano, P.S., Patterson, P.H. de Pablo, F. (2003) Developmental cooperation of leukemia inhibitory factor and insulin-like growth factor I in mice is tissue-specific and essential for lung maturation involving the transcription factors Sp3 and TTF-1. Mech. Dev., 120, 349 361.
40. Russo, V.C., Gluckman, P.D., Feldman, E.L. Werther, G.A. (2005) The insulin-like growth factor system and its pleiotropic functions in brain. Endocr. Rev., 26, 916 943.
41. Simo, S., Pujadas, L., Segura, M.F., La Torre, A., Del Rio, J.A., Urena, J.M., Comella, J.X. Soriano, E. (2007) Reelin induces the detachment of postnatal subventricular zone cells and the expression of the Egr-1 through Erk1/2 activation. Cereb. Cortex, 17, 294 303.
42. Tissir, F. Goffinet, A.M. (2003) Reelin and brain development. Nat Rev Neurosci, 4, 496 505.
43. Varela-Nieto, I., de la Rosa, E.J., Valenciano, A.I. Leon, Y. (2003) Cell death in the nervous system: lessons from insulin and insulin-like growth factors. Mol. Neurobiol., 28, 23 50.
44. Vergano-Vera, E., Yusta-Boyo, M.J., de Castro, F., Bernad, A., de Pablo, F. Vicario-Abejon, C. (2006) Generation of GABAergic and dopaminergic interneurons from endogenous embryonic olfactory bulb precursor cells. Development, 133, 4367 4379.
45. Vicario-Abejón, C., Yusta-Boyo, M.J., Fernandez-Moreno, C. de Pablo, F. (2003) Locally born olfactory bulb stem cells proliferate in response to insulin-related factors and require endogenous insulin-like growth factor-I for differentiation into neurons and glia. J. Neurosci., 23, 895 906.
46. Wyss, J.M., Stanfield, B.B. Cowan, W.M. (1980) Structural abnormalities in the olfactory bulb of the Reeler mouse. Brain Res., 188, 566 571.
47. Yang, Z. (2008) Postnatal subventricular zone progenitors give rise not only to granular and periglomerular interneurons but also to interneurons in the external plexiform layer of the rat olfactory bulb. J. Comp. Neurol., 506, 347 358.
48. Young, K.M., Fogarty, M., Kessaris, N. Richardson, W.D. (2007) Subventricular zone stem cells are heterogeneous with respect to their embryonic origins and neurogenic fates in the adult olfactory bulb. J. Neurosci., 27, 8286 8296.