APLP2 regulates neuronal stem cell differentiation during cortical development

Journal of Cell Science

Volumn 126, Issue 5, 2013, Pages 1268-1277

  Shariati, S Ali M ^a,b   Lau, Pierre ^a,b   Hassan, Bassem A ^a,b   Müller, Ulrike ^c   Dotti, Carlos G ^a,b,d   Strooper, Bart De ^a,b   Gä rtner, Annette ^a,b  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

Amyloid precursor protein; Amyloid precursor like protein; Cell cycle exit; Neuron migration; Progenitors

Indexed keywords

AMYLOID PRECURSOR LIKE PROTEIN 1; AMYLOID PRECURSOR LIKE PROTEIN 2; AMYLOID PRECURSOR PROTEIN; EOMESODERMIN; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN DEVELOPMENT; CELL COUNT; CONTROLLED STUDY; DOWN REGULATION; IN VIVO STUDY; MITOSIS; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION;

AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; CELL CYCLE; CELL DIFFERENTIATION; CELL MOVEMENT; CELLS, CULTURED; ELECTROPORATION; FEMALE; IMMUNOHISTOCHEMISTRY; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; NEURAL STEM CELLS; PREGNANCY;

EID: 84877898801     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.122440     Document Type: Article

References (47)

1. Aydin, D., Filippov, M. A., Tschäpe, J. A., Gretz, N., Prinz, M., Eils, R., Brors, B. and Müller, U. C. (2011). Comparative transcriptome profiling of amyloid precursor protein family members in the adult cortex. BMC Genomics 12, 160.
2. Bai, Y., Markham, K., Chen, F., Weerasekera, R., Watts, J., Horne, P., Wakutani, Y., Bagshaw, R., Mathews, P. M., Fraser, P. E. et al. (2008). The in vivo brain interactome of the amyloid precursor protein. Mol. Cell. Proteomics 7, 15-34.
3. Banker, G. and Goslin, K. (1988). Developments in neuronal cell culture. Nature 336, 185-186.
4. Bergmans, B. A., Shariati, S. A., Habets, R. L., Verstreken, P., Schoonjans, L., Müller, U., Dotti, C. G. and De Strooper, B. (2010). Neurons generated from APP/ APLP1/APLP2 triple knockout embryonic stem cells behave normally in vitro and in vivo: lack of evidence for a cell autonomous role of the amyloid precursor protein in neuronal differentiation. Stem Cells 28, 399-406.
5. Calderon de Anda, F., Gärtner, A., Tsai, L. H. and Dotti, C. G. (2008). Pyramidal neuron polarity axis is defined at the bipolar stage. J. Cell Sci. 121, 178-185.
6. Cao, X. and Südhof, T. C. (2001). A transcriptionally [correction of transcriptively] active complex of APP with Fe65 and histone acetyltransferase Tip60. Science 293, 115-120.
7. Chanas-Sacre, G., Rogister, B., Moonen, G. and Leprince, P. (2000). Radial glia phenotype: origin, regulation, and transdifferentiation. J. Neurosci. Res. 61, 357-363.
8. Chenn, A. and Walsh, C. A. (2002). Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 297, 365-369.
9. Coksaygan, T., Magnus, T., Cai, J., Mughal, M., Lepore, A., Xue, H., Fischer, I. and Rao, M. S. (2006). Neurogenesis in Talpha-1 tubulin transgenic mice during development and after injury. Exp. Neurol. 197, 475-485.
10. Deyts, C., Vetrivel, K. S., Das, S., Shepherd, Y. M., Dupré, D. J., Thinakaran, G. and Parent, A. T. (2012). Novel GaS-protein signaling associated with membranetethered amyloid precursor protein intracellular domain. J. Neurosci. 32, 1714-1729.
11. Diez-Roux, G., Banfi, S., Sultan, M., Geffers, L., Anand, S., Rozado, D., Magen, A., Canidio, E., Pagani, M., Peluso, I. et al. (2011). A high-resolution anatomical atlas of the transcriptome in the mouse embryo. PLoS Biol. 9, e1000582.
12. Feng, L., Hatten, M. E. and Heintz, N. (1994). Brain lipid-binding protein (BLBP): a novel signaling system in the developing mammalian CNS. Neuron 12, 895-908.
13. Gloster, A., Wu, W., Speelman, A., Weiss, S., Causing, C., Pozniak, C., Reynolds, B., Chang, E., Toma, J. G. and Miller, F. D. (1994). The T alpha 1 alpha-tubulin promoter specifies gene expression as a function of neuronal growth and regeneration in transgenic mice. J. Neurosci. 14, 7319-7330.
14. Goto, H., Tomono, Y., Ajiro, K., Kosako, H., Fujita, M., Sakurai, M., Okawa, K., Iwamatsu, A., Okigaki, T., Takahashi, T. et al. (1999). Identification of a novel phosphorylation site on histone H3 coupled with mitotic chromosome condensation. J. Biol. Chem. 274, 25543-25549.
15. Hashimoto-Torii, K., Torii, M., Sarkisian, M. R., Bartley, C. M., Shen, J., Radtke, F., Gridley, T., Sestan, N. and Rakic, P. (2008). Interaction between Reelin and Notch signaling regulates neuronal migration in the cerebral cortex. Neuron 60, 273- 284.
16. Haubensak, W., Attardo, A., Denk, W. and Huttner, W. B. (2004). Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc. Natl. Acad. Sci. USA 101, 3196-3201.
17. Heber, S., Herms, J., Gajic, V., Hainfellner, J., Aguzzi, A., Rülicke, T., von Kretzschmar, H., von Koch, C., Sisodia, S., Tremml, P. et al. (2000). Mice with combined gene knock-outs reveal essential and partially redundant functions of amyloid precursor protein family members. J. Neurosci. 20, 7951-7963.
18. Hébert, S. S., Serneels, L., Tolia, A., Craessaerts, K., Derks, C., Filippov, M. A., Müller, U. and De Strooper, B. (2006). Regulated intramembrane proteolysis of amyloid precursor protein and regulation of expression of putative target genes. EMBO Rep. 7, 739-745.
19. Herms, J., Anliker, B., Heber, S., Ring, S., Fuhrmann, M., Kretzschmar, H., Sisodia, S. and Müller, U. (2004). Cortical dysplasia resembling human type 2 lissencephaly in mice lacking all three APP family members. EMBO J. 23, 4106- 4115.
20. Homayouni, R., Rice, D. S., Sheldon, M. and Curran, T. (1999). Disabled-1 binds to the cytoplasmic domain of amyloid precursor-like protein 1. J. Neurosci. 19, 7507- 7515.
21. Lakomá , J., Garcia-Alonso, L. and Luque, J. M. (2011). Reelin sets the pace of neocortical neurogenesis. Development 138, 5223-5234.
22. Leyssen, M., Ayaz, D., Hébert, S. S., Reeve, S., De Strooper, B. and Hassan, B. A. (2005). Amyloid precursor protein promotes post-developmental neurite arborization in the Drosophila brain. EMBO J. 24, 2944-2955.
23. López-Sánchez, N., Müller, U. and Frade, J. M. (2005). Lengthening of G2/mitosis in cortical precursors from mice lacking beta-amyloid precursor protein. Neuroscience 130, 51-60.
24. Lorent, K., Overbergh, L., Moechars, D., De Strooper, B., Van Leuven, F. and Van den Berghe, H. (1995). Expression in mouse embryos and in adult mouse brain of three members of the amyloid precursor protein family, of the alpha-2-macroglobulin receptor/low density lipoprotein receptor-related protein and of its ligands apolipoprotein E, lipoprotein lipase, alpha-2-macroglobulin and the 40,000 molecular weight receptor-associated protein. Neuroscience 65, 1009-1025.
25. Ma, Q.-H., Futagawa, T., Yang, W.-L., Jiang, X.-D., Zeng, L., Takeda, Y., Xu, R.-X., Bagnard, D., Schachner, M., Furley, A. J. et al. (2008). A TAG1-APP signalling pathway through Fe65 negatively modulates neurogenesis. Nat. Cell Biol. 10, 283-294.
26. McConnell, S. K. and Kaznowski, C. E. (1991). Cell cycle dependence of laminar determination in developing neocortex. Science 254, 282-285.
27. Molyneaux, B. J., Arlotta, P., Menezes, J. R. and Macklis, J. D. (2007). Neuronal subtype specification in the cerebral cortex. Nat. Rev. Neurosci. 8, 427-437.
28. Müller, U. C. and Zheng, H. (2012). Physiological functions of APP family proteins. Cold Spring Harb Perspect Med 2, a006288.
29. Müller, U. C., Pietrzik, C. U. and Deller, T. (2012). The physiological functions of the b-amyloid precursor protein APP. Exp. Brain Res. 217, 325-329.
30. Nikolaev, A., McLaughlin, T., O'Leary, D. D. and Tessier-Lavigne, M. (2009). APP binds DR6 to trigger axon pruning and neuron death via distinct caspases. Nature 457, 981-989.
31. Pechnick, R. N., Zonis, S., Wawrowsky, K., Pourmorady, J. and Chesnokova, V. (2008). p21Cip1 restricts neuronal proliferation in the subgranular zone of the dentate gyrus of the hippocampus. Proc. Natl. Acad. Sci. USA 105, 1358-1363.
32. Reinhard, C., Hébert, S. S. and De Strooper, B. (2005). The amyloid-beta precursor protein: integrating structure with biological function. EMBO J. 24, 3996-4006.
33. Roncarati, R., Sestan, N., Scheinfeld, M. H., Berechid, B. E., Lopez, P. A., Meucci, O., McGlade, J. C., Rakic, P. and D'Adamio, L. (2002). The c-secretase-generated intracellular domain of b-amyloid precursor protein binds Numb and inhibits Notch signaling. Proc. Natl. Acad. Sci. USA 99, 7102-7107.
34. Soba, P., Eggert, S., Wagner, K., Zentgraf, H., Siehl, K., Kreger, S., Löwer, A., Langer, A., Merdes, G., Paro, R. et al. (2005). Homo- and heterodimerization of APP family members promotes intercellular adhesion. EMBO J. 24, 3624-3634.
35. Suzuki, T., Ando, K., Isohara, T., Oishi, M., Lim, G. S., Satoh, Y., Wasco, W., Tanzi, R. E., Nairn, A. C., Greengard, P. et al. (1997). Phosphorylation of Alzheimer beta-amyloid precursor-like proteins. Biochemistry 36, 4643-4649.
36. Tabata, H. and Nakajima, K. (2001). Efficient in utero gene transfer system to the developing mouse brain using electroporation: visualization of neuronal migration in the developing cortex. Neuroscience 103, 865-872.
37. Tabata, H. and Nakajima, K. (2008). Labeling embryonic mouse central nervous system cells by in utero electroporation. Dev. Growth Differ. 50, 507-511.
38. Tamayev, R., Zhou, D. and D'Adamio, L. (2009). The interactome of the amyloid beta precursor protein family members is shaped by phosphorylation of their intracellular domains. Mol. Neurodegener. 4, 28.
39. Temple, S. and Davis, A. A. (1994). Isolated rat cortical progenitor cells are maintained in division in vitro by membrane-associated factors. Development 120, 999-1008.
40. Vidaki, M., Tivodar, S., Doulgeraki, K., Tybulewicz, V., Kessaris, N., Pachnis, V. and Karagogeos, D. (2012). Rac1-dependent cell cycle exit of MGE precursors and GABAergic interneuron migration to the cortex. Cereb. Cortex 22, 680-692.
41. Visel, A., Thaller, C. and Eichele, G. (2004). GenePaint.org: an atlas of gene expression patterns in the mouse embryo. Nucleic Acids Res. 32 Database issue, D552-D556.
42. Wang, Z., Wang, B., Yang, L., Guo, Q., Aithmitti, N., Songyang, Z. and Zheng, H. (2009). Presynaptic and postsynaptic interaction of the amyloid precursor protein promotes peripheral and central synaptogenesis. J. Neurosci. 29, 10788- 10801.
43. Weyer, S. W., Klevanski, M., Delekate, A., Voikar, V., Aydin, D., Hick, M., Filippov, M., Drost, N., Schaller, K. L., Saar, M. et al. (2011). APP and APLP2 are essential at PNS and CNS synapses for transmission, spatial learning and LTP. EMBO J. 30, 2266-2280.
44. Yang, Y. T., Wang, C. L. and Van Aelst, L. (2012). DOCK7 interacts with TACC3 to regulate interkinetic nuclear migration and cortical neurogenesis. Nat. Neurosci. 15, 1201-1210.
45. Yoon, K., Nery, S., Rutlin, M. L., Radtke, F., Fishell, G. and Gaiano, N. (2004). Fibroblast growth factor receptor signaling promotes radial glial identity and interacts with Notch1 signaling in telencephalic progenitors. J. Neurosci. 24, 9497- 9506.
46. Young-Pearse, T. L., Bai, J., Chang, R., Zheng, J. B., LoTurco, J. J. and Selkoe, D. J. (2007). A critical function for beta-amyloid precursor protein in neuronal migration revealed by in utero RNA interference. J. Neurosci. 27, 14459-14469.
47. Young-Pearse, T. L., Chen, A. C., Chang, R., Marquez, C. and Selkoe, D. J. (2008). Secreted APP regulates the function of full-length APP in neurite outgrowth through interaction with integrin beta1. Neural Dev. 3, 15.