p21-Activated Kinases 1 and 3 Control Brain Size through Coordinating Neuronal Complexity and Synaptic Properties

REFERENCES

• Aizawa, H., et al. 2001. Phosphorylation of cofilin by LIM kinase is necessary for semaphorin 3A-induced growth cone collapse. Nat. Neurosci. 4:367–373.
   PubMed Web of Science ®Google Scholar
• Allen, J. D., et al. 2009. p21-activated kinase regulates mast cell degranulation via effects on calcium mobilization and cytoskeletal dynamics. Blood 113:2695–2705.
   PubMed Web of Science ®Google Scholar
• Allen, K. M., et al. 1998. PAK3 mutation in nonsyndromic X-linked mental retardation. Nat. Genet. 20:25–30.
   PubMed Web of Science ®Google Scholar
• Ang, L., J. Kim, V. Stepensky, and H. Hing. 2003. Dock and Pak regulate olfactory axon pathfinding in Drosophila. Development 130:1307–1316.
   PubMed Web of Science ®Google Scholar
• Arias-Romero, L. E., and J. Chernoff. 2008. A tale of two Paks. Biol. Cell 100:97–108.
   PubMed Web of Science ®Google Scholar
• Armstrong, D. D. 2002. Neuropathology of Rett syndrome. Ment. Retard. Dev. Disabil. Res. Rev. 8:72–76.
   PubMedGoogle Scholar
• Asrar, S., Y. Meng, Z. Zhou, Z. Todorovski, W. W. Huang, and Z. Jia. 2009. Regulation of hippocampal long-term potentiation by p21-activated protein kinase 1 (PAK1). Neuropharmacology 56:73–80.
   PubMedGoogle Scholar
• Ayala, R., T. Shu, and L. H. Tsai. 2007. Trekking across the brain: the journey of neuronal migration. Cell 128:29–43.
   PubMed Web of Science ®Google Scholar
• Boda, B., et al. 2004. The mental retardation protein PAK3 contributes to synapse formation and plasticity in hippocampus. J. Neurosci. 24:10816–10825.
   PubMed Web of Science ®Google Scholar
• Boda, B., L. Jourdain, and D. Muller. 2008. Distinct, but compensatory roles of PAK1 and PAK3 in spine morphogenesis. Hippocampus 18:857–861.
   PubMedGoogle Scholar
• Bokoch, G. M. 2003. Biology of p21-activated kinases. Annu. Rev. Biochem. 72:743–781.
   PubMed Web of Science ®Google Scholar
• Cahana, A., et al. 2001. Targeted mutagenesis of Lis1 disrupts cortical development and LIS1 homodimerization. Proc. Natl. Acad. Sci. U. S. A. 98:6429–6434.
   PubMedGoogle Scholar
• Causeret, F., et al. 2009. The p21-activated kinase is required for neuronal migration in the cerebral cortex. Cereb. Cortex 19:861–875.
   PubMedGoogle Scholar
• Chen, R. Z., S. Akbarian, M. Tudor, and R. Jaenisch. 2001. Deficiency of methyl-CpG binding protein-2 in CNS neurons results in a Rett-like phenotype in mice. Nat. Genet. 27:327–331.
   PubMed Web of Science ®Google Scholar
• Cobos, I., U. Borello, and J. L. R. Rubenstein. 2007. Dlx transcription factors promote migration through repression of axon and dendrite growth. Neuron 54:873–888.
   PubMedGoogle Scholar
• Cox, J., A. P. Jackson, J. Bond, and C. G. Woods. 2006. What primary microcephaly can tell us about brain growth. Trends Mol. Med. 12:358–366.
   PubMed Web of Science ®Google Scholar
• Daniels, R. H., P. S. Hall, and G. M. Bokoch. 1998. Membrane targeting of p21-activated kinase 1 (PAK1) induces neurite outgrowth from PC12 cells. EMBO J. 17:754–764.
   PubMed Web of Science ®Google Scholar
• Depaepe, V., et al. 2005. Ephrin signalling controls brain size by regulating apoptosis of neural progenitors. Nature 435:1244–1250.
   PubMed Web of Science ®Google Scholar
• Dorr, A. E., J. P. Lerch, S. Spring, N. Kabani, and R. M. Henkelman. 2008. High resolution three-dimensional brain atlas using an average magnetic resonance image of 40 adult C57Bl/6J mice. Neuroimage 42:60–69.
   PubMedGoogle Scholar
• Fan, X., J. P. Labrador, H. Hing, and G. J. Bashaw. 2003. Slit stimulation recruits Dock and Pak to the roundabout receptor and increases Rac activity to regulate axon repulsion at the CNS midline. Neuron 40:113–127.
   PubMed Web of Science ®Google Scholar
• Feng, Y., and C. A. Walsh. 2004. Mitotic spindle regulation by NdeI controls cerebral cortical size. Neuron 44:279–293.
   PubMedGoogle Scholar
• Guy, J., B. Hendrich, M. Holmes, J. E. Martin, and A. Bird. 2001. A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nat. Genet. 27:322–326.
   PubMed Web of Science ®Google Scholar
• Hayashi, K., T. Ohshima, and K. Mikoshiba. 2002. Pak1 is involved in dendrite initiation as a downstream effector of Rac1 in cortical neurons. Mol. Cell. Neurosci. 20:579–594.
   PubMedGoogle Scholar
• Hayashi, M. L., et al. 2004. Altered cortical synaptic morphology and impaired memory consolidation in forebrain-specific dominant-negative PAK transgenic mice. Neuron 42:773–787.
   PubMed Web of Science ®Google Scholar
• Hayashi, K., T. Ohshima, M. Hashimoto, and K. Mikoshiba. 2007. Pak1 regulates dendritic branching and spine formation. Dev. Neurobiol. 67:655–669.
   PubMedGoogle Scholar
• Hing, H., J. Xiao, N. Harden, L. Lim, and S. L. Zipursky. 1999. Pak functions downstream of Dock to regulate photoreceptor axon guidance in Drosophila. Cell 97:853–863.
   PubMed Web of Science ®Google Scholar
• Hirotsune, S., et al. 1998. Graded reduction of Pafah1b1 (Lis1) activity results in neuronal migration defects and early embryonic lethality. Nat. Genet. 19:333–339.
   PubMed Web of Science ®Google Scholar
• Hu, H., T. F. Marton, and C. S. Goodman. 2001. Plexin B mediates axon guidance in Drosophila by simultaneously inhibiting active Rac and enhancing RhoA signaling. Neuron 32:39–51.
   PubMed Web of Science ®Google Scholar
• Jacobs, T., et al. 2007. Localized activation of p21-activated kinase controls neuronal polarity and morphology. J. Neurosci. 27:8604–8615.
   PubMed Web of Science ®Google Scholar
• Kreis, P., E. Thévenot, V. Rousseau, B. Boda, D. Muller, and J. V. Barnier. 2007. The p21-activated kinase 3 implicated in mental retardation regulates spine morphogenesis through a Cdc42-dependent pathway. J. Biol. Chem. 282:21497–21506.
   PubMedGoogle Scholar
• Kreis, P., and J. Barnier. 2009. PAK signalling in neuronal physiology. Cell. Signal. 21:384–393.
   PubMed Web of Science ®Google Scholar
• Li, X., and A. Minden. 2003. Targeted disruption of the gene for the PAK5 kinase in mice. Mol. Cell. Biol. 23:7134–7142.
   PubMed Web of Science ®Google Scholar
• Lucanic, M., M. Kiley, N. Ashcroft, N. L'etoile, and H. Cheng. 2006. The Caenorhabditis elegans p21-activated kinases are differentially required for UNC-6/netrin-mediated commissural motor axon guidance. Development 133:4549–4559.
   PubMedGoogle Scholar
• Luo, L. 2000. Rho GTPases in neuronal morphogenesis. Nat. Rev. Neurosci. 1:173–180.
   PubMed Web of Science ®Google Scholar
• Malenka, R. C., and M. F. Bear. 2004. LTP and LTD: an embarrassment of riches. Neuron 44:5–21.
   PubMed Web of Science ®Google Scholar
• Marler, K. J. M., R. Kozma, S. Ahmed, J. Dong, C. Hall, and L. Lim. 2005. Outgrowth of neurites from NIE-115 neuroblastoma cells is prevented on repulsive substrates through the action of PAK. Mol. Cell. Biol. 25:5226–5241.
   PubMedGoogle Scholar
• McPhie, D. L., et al. 2003. DNA synthesis and neuronal apoptosis caused by familial Alzheimer disease mutants of the amyloid precursor protein are mediated by the p21 activated kinase PAK3. J. Neurosci. 23:6914–6927.
   PubMed Web of Science ®Google Scholar
• Meng, Y., et al. 2002. Abnormal spine morphology and enhanced LTP in LIMK-1 knockout mice. Neuron 35:121–133.
   PubMed Web of Science ®Google Scholar
• Meng, J., Y. Meng, A. Hanna, C. Janus, and Z. Jia. 2005. Abnormal long-lasting synaptic plasticity and cognition in mice lacking the mental retardation gene Pak3. J. Neurosci. 25:6641–6650.
   PubMed Web of Science ®Google Scholar
• Mochida, G. H., and C. A. Walsh. 2001. Molecular genetics of human microcephaly. Curr. Opin. Neurol. 14:151–156.
   PubMedGoogle Scholar
• Mochida, G. H. 2009. Genetics and biology of microcephaly and lissencephaly. Semin. Pediatr. Neurol. 16:120–126.
   PubMedGoogle Scholar
• Nekrasova, T., M. L. Jobes, J. H. Ting, G. C. Wagner, and A. Minden. 2008. Targeted disruption of the Pak5 and Pak6 genes in mice leads to deficits in learning and locomotion. Dev. Biol. 322:95–108.
   PubMed Web of Science ®Google Scholar
• Nikolić, M. 2008. The Pak1 kinase: an important regulator of neuronal morphology and function in the developing forebrain. Mol. Neurobiol. 37:187–202.
   PubMed Web of Science ®Google Scholar
• Ong, W. Y., X. S. Wang, and E. Manser. 2002. Differential distribution of alpha and beta isoforms of p21-activated kinase in the monkey cerebral neocortex and hippocampus. Exp. Brain Res. 144:189–199.
   PubMedGoogle Scholar
• Pang, T., R. Atefy, and V. Sheen. 2008. Malformations of cortical development. Neurologist 14:181–191.
   PubMed Web of Science ®Google Scholar
• Peippo, M., A. M. Koivisto, T. Särkämö, M. Sipponen, H. von Koskull, T. Ylisaukko-oja, K. Rehnström, G. Froyen, J. Ignatius, and I. Järvelä. 2007. PAK3 related mental disability: further characterization of the phenotype. Am. J. Med. Genet. A 143A:2406–2416.
   PubMedGoogle Scholar
• Peng, Y. R., et al. 2009. Coordinated changes in dendritic arborization and synaptic strength during neural circuit development. Neuron 61:71–84.
   PubMedGoogle Scholar
• Qu, J., et al. 2003. PAK4 kinase is essential for embryonic viability and for proper neuronal development. Mol. Cell. Biol. 23:7122–7133.
   PubMed Web of Science ®Google Scholar
• Rosenberg, M. J., et al. 2002. Mutant deoxynucleotide carrier is associated with congenital microcephaly. Nat. Genet. 32:175–179.
   PubMed Web of Science ®Google Scholar
• Sakakibara, A., and A. F. Horwitz. 2006. Mechanism of polarized protrusion formation on neuronal precursors migrating in the developing chicken cerebellum. J. Cell Sci. 119:3583–3592.
   PubMedGoogle Scholar
• Sandig, V., et al. 2000. Optimization of the helper-dependent adenovirus system for production and potency in vivo. Proc. Natl. Acad. Sci. U. S. A. 97:1002–1007.
   PubMed Web of Science ®Google Scholar
• Silver, D. L., et al. 2010. The exon junction complex component Magoh controls brain size by regulating neural stem cell division. Nat. Neurosci. 13:551–558.
   PubMedGoogle Scholar
• Souopgui, J., M. Sölter, and T. Pieler. 2002. XPak3 promotes cell cycle withdrawal during primary neurogenesis in Xenopus laevis. EMBO J. 21:6429–6439.
   PubMedGoogle Scholar
• Urbanska, M., M. Blazejczyk, and J. Jaworski. 2008. Molecular basis of dendritic arborization. Acta Neurobiol. Exp. 68:264–288.
   PubMedGoogle Scholar
• Vadlamudi, R. K., B. Manavathi, R. R. Singh, D. Nguyen, F. Li, and R. Kumar. 2005. An essential role of Pak1 phosphorylation of SHARP in Notch signaling. Oncogene 24:4591–4596.
   PubMedGoogle Scholar
• van Galen, E. J., and G. J. Ramakers. 2005. Rho proteins, mental retardation and the neurobiological basis of intelligence. Prog. Brain Res. 147:295–317.
   PubMedGoogle Scholar
• Walf, A. A., and C. A. Frye. 2007. The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat. Protoc. 2:322–328.
   PubMed Web of Science ®Google Scholar
• Woods, C. G. 2004. Human microcephaly. Curr. Opin. Neurobiol. 14:112–117.
   PubMed Web of Science ®Google Scholar
• Zhang, H., D. J. Webb, H. Asmussen, S. Niu, and A. F. Horwitz. 2005. A GIT1/PIX/Rac/PAK signaling module regulates spine morphogenesis and synapse formation through MLC. J. Neurosci. 25:3379–3388.
   PubMed Web of Science ®Google Scholar
• Zhao, Z. S., and E. Manser. 2005. PAK and other Rho-associated kinases—effectors with surprisingly diverse mechanisms of regulation. Biochem. J. 386:201–214.
   PubMed Web of Science ®Google Scholar
• Zhong, J. L., M. D. Banerjee, and M. Nikolic. 2003. Pak1 and its T212 phosphorylated form accumulate in neurones and epithelial cells of the developing rodent. Dev. Dyn. 228:121–127.
   PubMedGoogle Scholar
• Zhou, Q., K. J. Homma, and M. M. Poo. 2004. Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44:749–757.
   PubMed Web of Science ®Google Scholar