A FOXO-Pak1 transcriptional pathway controls neuronal polarity

Genes and Development

Volumn 24, Issue 8, 2010, Pages 799-813

  De La Torre Ubieta, Luis ^a   Gaudillière, Brice ^a   Yang, Yue ^a   Ikeuchi, Yoshiho ^a   Yamada, Tomoko ^a   Dibacco, Sara ^a   Stegmüller, Judith ^a,c   Schüller, Ulrich ^a,d   Salih, Dervis A ^b   Rowitch, David ^a,e   Brunet, Anne ^b   Bonni, Azad ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b STANFORD UNIVERSITY   (United States)

^c MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^d UNIVERSITY OF MUNICH   (Germany)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Axons; Dendrites; FOXO; Neuronal polarity; Pak1; Transcription

Indexed keywords

P21 ACTIVATED KINASE 1; TRANSCRIPTION FACTOR FOXO; FORKHEAD TRANSCRIPTION FACTOR; P21 ACTIVATED KINASE; PAK1 PROTEIN, RAT;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL DIFFERENTIATION; CELL POLARITY; CELL STRUCTURE; CEREBELLUM CORTEX; HIPPOCAMPUS; IN VIVO STUDY; NEURITE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RAT; ANIMAL; CELL CULTURE; CYTOLOGY; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; METABOLISM; NERVE CELL; PHYSIOLOGY; RNA INTERFERENCE;

RATTUS;

ANIMALS; CELL POLARITY; CELLS, CULTURED; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCKDOWN TECHNIQUES; HIPPOCAMPUS; NEURONS; P21-ACTIVATED KINASES; RATS; RNA INTERFERENCE;

EID: 77950933448     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1880510     Document Type: Article

References (58)

1. Accili D, Arden KC. 2004. FoxOs at the crossroads of cellular metabolism, differentiation, and transformation. Cell 117: 421-426. (Pubitemid 38610228)
2. Aizawa H, Hu SC, Bobb K, Balakrishnan K, Ince G, Gurevich I, Cowan M, Ghosh A. 2004. Dendrite development regulated by CREST, a calcium-regulated transcriptional activator. Science 303: 197-202. (Pubitemid 38057563)
3. Altman J, Bayer S.A. 1997. Development of the cerebellar system: In relation to its evolution, structure, and functions. CRC Press, Boca Raton, FL.
4. Alvarez B, Martinez AC, Burgering BM, Carrera AC. 2001. Forkhead transcription factors contribute to execution of the mitotic programme in mammals. Nature 413: 744-747. (Pubitemid 33009953)
5. Arden KC. 2004. FoxO: Linking new signaling pathways. Mol Cell 14: 416-418.
6. Arias-Romero LE, Chernoff J. 2008. A tale of two Paks. Biol Cell 100: 97-108.
7. Arimura N, Kaibuchi K. 2007. Neuronal polarity: From extracellular signals to intracellular mechanisms. Nat Rev Neurosci 8: 194-205. (Pubitemid 46294662)
8. Barnes AP, Lilley BN, Pan YA, Plummer LJ, Powell AW, Raines AN, Sanes JR, Polleux F. 2007. LKB1 and SAD kinases define a pathway required for the polarization of cortical neurons. Cell 129: 549-563. (Pubitemid 46660970)
9. Barthel A, Schmoll D, Unterman TG. 2005. FoxO proteins in insulin action and metabolism. Trends Endocrinol Metab 16: 183-189. (Pubitemid 40603098)
10. Bokoch GM. 2003. Biology of the p21-activated kinases. Annu Rev Biochem 72: 743-781.
11. Brewer GJ, Torricelli JR, Evege EK, Price PJ. 1993. Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J Neurosci Res 35: 567-576.
12. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME. 1999. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96: 857-868. (Pubitemid 29165088)
13. Burgering BM, Kops GJ. 2002. Cell cycle and death control: Long live Forkheads. Trends Biochem Sci 27: 352-360.
14. Carter ME, Brunet A. 2007. FOXO transcription factors. Curr Biol 17: R113-R114. doi: 10.1016/j.cub.2007.01.008.
15. Causeret F, Terao M, Jacobs T, Nishimura YV, Yanagawa Y, Obata K, Hoshino M, Nikolic M. 2009. The p21-activated kinase is required for neuronal migration in the cerebral cortex. Cereb Cortex 19: 861-875.
16. Coffer PJ, Burgering BM. 2004. Forkhead-box transcription factors and their role in the immune system. Nat Rev Immunol 4: 889-899. (Pubitemid 39490764)
17. Craig AM, Banker G. 1994. Neuronal polarity. Annu Rev Neurosci 17: 267-310.
18. de Anda FC, Pollarolo G, Da Silva JS, Camoletto PG, Feiguin F, Dotti CG. 2005. Centrosome localization determines neuronal polarity. Nature 436: 704-708. (Pubitemid 41117273)
19. Edwards DC, Sanders LC, Bokoch GM, Gill GN. 1999. Activation of LIM-kinase by Pak1 couples Rac/Cdc42 GTPase signalling to actin cytoskeletal dynamics. Nat Cell Biol 1: 253-259.
20. Gaudillière B, Shi Y, Bonni A. 2002. RNA interference reveals a requirement for myocyte enhancer factor 2A in activity-dependent neuronal survival. J Biol Chem 277: 46442-46446. (Pubitemid 35417639)
21. Gaudillière B, Konishi Y, de la Iglesia N, Yao G, Bonni A. 2004. A CaMKII-NeuroD signaling pathway specifies dendritic morphogenesis. Neuron 41: 229-241. (Pubitemid 38125184)
22. Goldberg JL. 2004. Intrinsic neuronal regulation of axon and dendrite growth. Curr Opin Neurobiol 14: 551-557. (Pubitemid 39349615)
23. Grueber WB, Jan LY, Jan YN. 2003. Different levels of the homeodomain protein cut regulate distinct dendrite branching patterns of Drosophila multidendritic neurons. Cell 112: 805-818.
24. Hand R, Bortone D, Mattar P, Nguyen L, Heng JI, Guerrier S, Boutt E, Peters E, Barnes AP, Parras C, et al. 2005. Phosphorylation of Neurogenin2 specifies the migration properties and the dendritic morphology of pyramidal neurons in the neocortex. Neuron 48: 45-62. (Pubitemid 41384165)
25. Hayashi ML, Choi SY, Rao BS, Jung HY, Lee HK, Zhang D, Chattarji S, Kirkwood A, Tonegawa S. 2004. Altered cortical synaptic morphology and impaired memory consolidation in forebrain-specific dominant-negative PAK transgenic mice. Neuron 42: 773-787. (Pubitemid 38748791)
26. Hayashi ML, Rao BS, Seo JS, Choi HS, Dolan BM, Choi SY, Chattarji S, Tonegawa S. 2007. Inhibition of p21-activated kinase rescues symptoms of fragile X syndrome in mice. Proc Natl Acad Sci 104: 11489-11494. (Pubitemid 47175167)
27. Hoekman MF, Jacobs FM, Smidt MP, Burbach JP. 2006. Spatial and temporal expression of FoxO transcription factors in the developing and adult murine brain. Gene Expr Patterns 6: 134-140.
28. Jacobs FM, van der Heide LP, Wijchers PJ, Burbach JP, Hoekman MF, Smidt MP. 2003. FoxO6, a novel member of the FoxO class of transcription factors with distinct shuttling dynamics. J Biol Chem 278: 35959-35967.
29. Jacobs T, Causeret F, Nishimura YV, Terao M, Norman A, Hoshino M, Nikolic M. 2007. Localized activation of p21-activated kinase controls neuronal polarity and morphology. J Neurosci 27: 8604-8615. (Pubitemid 47254258)
30. Jacobson C, Schnapp B, Banker GA. 2006. A change in the selective translocation of the Kinesin-1 motor domain marks the initial specification of the axon. Neuron 49: 797-804. (Pubitemid 43376077)
31. Jan YN, Jan LY. 2003. The control of dendrite development. Neuron 40: 229-242.
32. Jiang H, Guo W, Liang X, Rao Y. 2005. Both the establishment and the maintenance of neuronal polarity require active mechanisms: Critical roles of GSK-3b and its upstream regulators. Cell 120: 123-135. (Pubitemid 40094608)
33. Kandel ER, Schwartz JH, Jessell TM. 2000. Principles of neural science. McGraw-Hill, Health Professions Division, New York.
34. Kim AH, Bonni A. 2007. Thinking within the D box: Initial identification of Cdh1-APC substrates in the nervous system. Mol Cell Neurosci 34: 281-287. (Pubitemid 46350721)
35. Kishi M, Pan YA, Crump JG, Sanes JR. 2005. Mammalian SAD kinases are required for neuronal polarization. Science 307: 929-932. (Pubitemid 40229230)
36. Konishi Y, Lehtinen M, Donovan N, Bonni A. 2002. Cdc2 phosphorylation of BAD links the cell cycle to the cell death machinery. Mol Cell 9: 1005-1016. (Pubitemid 34626670)
37. Konishi Y, Stegmüller J, Matsuda T, Bonni S, Bonni A. 2004. Cdh1-APC controls axonal growth and patterning in the mammalian brain. Science 303: 1026-1030. (Pubitemid 38209709)
38. Kumar R, Gururaj AE, Barnes CJ. 2006. p21-activated kinases in cancer. Natl Rev 6: 459-471.
39. Lehtinen MK, Yuan Z, Boag PR, Yang Y, Villen J, Becker EB, DiBacco S, de la Iglesia N, Gygi S, Blackwell TK, et al. 2006. A conserved MST-FOXO signaling pathway mediates oxidative-stress responses and extends life span. Cell 125: 987-1001. (Pubitemid 43795191)
40. Nikolic M. 2008. The pak1 kinase: An important regulator of neuronal morphology and function in the developing forebrain. Mol Neurobiol 37: 187-202.
41. Paik JH, Kollipara R, Chu G, Ji H, Xiao Y, Ding Z, Miao L, Tothova Z, Horner JW, Carrasco DR, et al. 2007. FoxOs are lineage-restricted redundant tumor suppressors and regulate endothelial cell homeostasis. Cell 128: 309-323. (Pubitemid 46123514)
42. Polleux F, Ince-Dunn G, Ghosh A. 2007. Transcriptional regulation of vertebrate axon guidance and synapse formation. Nat Rev Neurosci 8: 331-340. (Pubitemid 46652466)
43. Powell SK, Rivas RJ, Rodriguez-Boulan E, Hatten ME. 1997. Development of polarity in cerebellar granule neurons. J Neurobiol 32: 223-236. (Pubitemid 27058704)
44. Ramón y Cajal S. 1995. Histology of the nervous system of man and vertebrates. Oxford University Press, New York, NY.
45. Ramos B, Gaudillière B, Bonni A, Gill G. 2007. Transcription factor Sp4 regulates dendritic patterning during cerebellar maturation. Proc Natl Acad Sci 104: 9882-9887. (Pubitemid 47175360)
46. Schwamborn JC, Puschel AW. 2004. The sequential activity of the GTPases Rap1B and Cdc42 determines neuronal polarity. Nat Neurosci 7: 923-929.
47. Shalizi A, Gaudillière B, Yuan Z, Stegmüller J, Shirogane T, Ge Q, Tan Y, Schulman B, Harper JW, Bonni A. 2006. A calcium-regulated MEF2 sumoylation switch controls postsynaptic differentiation. Science 311: 1012-1017. (Pubitemid 43271730)
48. Shelly M, Cancedda L, Heilshorn S, Sumbre G, Poo MM. 2007. LKB1/STRAD promotes axon initiation during neuronal polarization. Cell 129: 565-577. (Pubitemid 46660974)
49. Shi SH, Jan LY, Jan YN. 2003. Hippocampal neuronal polarity specified by spatially localized mPar3/mPar6 and PI 3-kinase activity. Cell 112: 63-75.
50. Stegmüller J, Bonni A. 2005. Moving past proliferation: New roles for Cdh1-APC in postmitotic neurons. Trends Neurosci 28: 596-601. (Pubitemid 41476690)
51. Stegmüller J, Konishi Y, Huynh MA, Yuan Z, Dibacco S, Bonni A. 2006. Cell-intrinsic regulation of axonal morphogenesis by the Cdh1-APC target SnoN. Neuron 50: 389-400.
52. Tran H, Brunet A, Griffith EC, Greenberg ME. 2003. The many forks in FOXO's road. Sci STKE 2003: RE5. doi: 10.1126/stke.2003.172.re5.
53. Van Der Heide LP, Hoekman MF, Smidt MP. 2004. The ins and outs of FoxO shuttling: Mechanisms of FoxO translocation and transcriptional regulation. Biochem J 380: 297-309. (Pubitemid 38788101)
54. van der Heide LP, Jacobs FM, Burbach JP, Hoekman MM, Smidt MP. 2005. FoxO6 transcriptional activity is regulated by Thr26 and Ser184, independent of nucleo-cytoplasmic shuttling. Biochem J 391: 623-628.
55. Wittmann T, Bokoch GM, Waterman-Storer CM. 2004. Regulation of microtubule destabilizing activity of Op18/stathmin downstream of Rac1. J Biol Chem 279: 6196-6203. (Pubitemid 38220653)
56. Yoshimura T, Kawano Y, Arimura N, Kawabata S, Kikuchi A, Kaibuchi K. 2005. GSK-3b regulates phosphorylation of CRMP-2 and neuronal polarity. Cell 120: 137-149. (Pubitemid 40094609)
57. Yuan Z, Becker EB, Merlo P, Yamada T, DiBacco S, Konishi Y, Schaefer EM, Bonni A. 2008. Activation of FOXO1 by Cdk1 in cycling cells and postmitotic neurons. Science 319: 1665-1668. (Pubitemid 351432504)
58. Zhou FQ, Zhou J, Dedhar S, Wu YH, Snider WD. 2004. NGF-induced axon growth is mediated by localized inactivation of GSK-3b and functions of the microtubule plus end binding protein APC. Neuron 42: 897-912. (Pubitemid 38798229)