Acute inactivation of the serine-threonine kinase Stk25 disrupts neuronal migration

Neural Development

Volumn 8, Issue 1, 2013, Pages

  Matsuki, Tohru ^a,b   Chen, Jianhua ^a   Howell, Brian W ^a  

^a State University of New York Upstate Medical University: College of Medicine   (United States)

^b INSTITUTE FOR DEVELOPMENTAL RESEARCH   (Japan)

Author keywords

Brain development; Dab1; LYK5; Neuronal migration; Reelin; Sok1; Ysk1

Indexed keywords

PROTEIN KINASE LKB1; PROTEIN SERINE THREONINE KINASE; SIGNAL PEPTIDE; STK25 PROTEIN, MOUSE;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROPORATION; EMBRYO; IMMUNODETECTION; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; MOUSE; NEURONAL MIGRATION DISORDER; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; BRAIN; C57BL MOUSE; CELL MOTION; DRUG ANTAGONISM; GENE EXPRESSION; GENETICS; METABOLISM; NERVE CELL; PHYSIOLOGY; PRENATAL DEVELOPMENT;

ANIMALS; BRAIN; CELL MOVEMENT; GENE EXPRESSION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONS; PROTEIN-SERINE-THREONINE KINASES;

EID: 84887323459     PISSN: None     EISSN: 17498104     Source Type: Journal    
DOI: 10.1186/1749-8104-8-21     Document Type: Article

References (48)

1. Matsuki T, Matthews RT, Cooper JA, van der Brug MP, Cookson MR, Hardy JA, Olson EC, Howell BW. Reelin and stk25 have opposing roles in neuronal polarization and dendritic Golgi deployment. Cell 2010, 143:826-836.
2. Rice DS, Curran T. Role of the reelin signaling pathway in central nervous system development. Annu Rev Neurosci 2001, 24:1005-1039.
3. Crino PB. mTOR: A pathogenic signaling pathway in developmental brain malformations. Trends Mol Med 2011, 17:734-742.
4. Orlova KA, Parker WE, Heuer GG, Tsai V, Yoon J, Baybis M, Fenning RS, Strauss K, Crino PB. STRADalpha deficiency results in aberrant mTORC1 signaling during corticogenesis in humans and mice. J Clin Invest 2010, 120:1591-1602.
5. D'Arcangelo G, Miao GG, Chen SC, Soares HD, Morgan JI, Curran T. A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 1995, 374:719-723.
6. Howell BW, Hawkes R, Soriano P, Cooper JA. Neuronal position in the developing brain is regulated by mouse disabled-1. Nature 1997, 389:733-737.
7. Ogawa M, Miyata T, Nakajima K, Yagyu K, Seike M, Ikenaka K, Yamamoto H, Mikoshiba K. The reeler gene-associated antigen on Cajal-Retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron 1995, 14:899-912.
8. Sheldon M, Rice DS, D'Arcangelo G, Yoneshima H, Nakajima K, Mikoshiba K, Howell BW, Cooper JA, Goldowitz D, Curran T. Scrambler and yotari disrupt the disabled gene and produce a reeler-like phenotype in mice. Nature 1997, 389:730-733.
9. Trommsdorff M, Gotthardt M, Hiesberger T, Shelton J, Stockinger W, Nimpf J, Hammer RE, Richardson JA, Herz J. Reeler/Disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor-2. Cell 1999, 97:689-701.
10. D'Arcangelo G, Homayouni R, Keshvara L, Rice DS, Sheldon M, Curran T. Reelin is a ligand for lipoprotein receptors. Neuron 1999, 24:471-479.
11. Hiesberger T, Trommsdorff M, Howell BW, Goffinet A, Mumby MC, Cooper JA, Herz J. Direct binding of Reelin to VLDL receptor and ApoE receptor 2 induces tyrosine phosphorylation of disabled-1 and modulates tau phosphorylation. Neuron 1999, 24:481-489.
12. Ballif BA, Arnaud L, Arthur WT, Guris D, Imamoto A, Cooper JA. Activation of a Dab1/CrkL/C3G/Rap1 pathway in Reelin-stimulated neurons. Curr Biol 2004, 14:606-610.
13. Chen K, Ochalski PG, Tran TS, Sahir N, Schubert M, Pramatarova A, Howell BW. Interaction between Dab1 and CrkII is promoted by Reelin signaling. J Cell Sci 2004, 117:4527-4536.
14. Franco SJ, Martinez-Garay I, Gil-Sanz C, Harkins-Perry SR, Muller U. Reelin regulates cadherin function via Dab1/Rap1 to control neuronal migration and lamination in the neocortex. Neuron 2011, 69:482-497.
15. Jossin Y, Cooper JA. Reelin, Rap1 and N-cadherin orient the migration of multipolar neurons in the developing neocortex. Nat Neurosci 2011, 14:697-703.
16. Baas AF, Smit L, Clevers H. LKB1 tumor suppressor protein: PARtaker in cell polarity. Trends Cell Biol 2004, 14:312-319.
17. Lizcano JM, Goransson O, Toth R, Deak M, Morrice NA, Boudeau J, Hawley SA, Udd L, Makela TP, Hardie DG, Alessi DR. LKB1 is a master kinase that activates 13 kinases of the AMPK subfamily, including MARK/PAR-1. EMBO J 2004, 23:833-843.
18. Alessi DR, Sakamoto K, Bayascas JR. LKB1-dependent signaling pathways. Annu Rev Biochem 2006, 75:137-163.
19. Puffenberger EG, Strauss KA, Ramsey KE, Craig DW, Stephan DA, Robinson DL, Hendrickson CL, Gottlieb S, Ramsay DA, Siu VM, Heuer GG, Crino PB, Morton DH. Polyhydramnios, megalencephaly and symptomatic epilepsy caused by a homozygous 7-kilobase deletion in LYK5. Brain 2007, 130:1929-1941.
20. Preisinger C, Short B, De Corte V, Bruyneel E, Haas A, Kopajtich R, Gettemans J, Barr FA. YSK1 is activated by the Golgi matrix protein GM130 and plays a role in cell migration through its substrate 14-3-3zeta. J Cell Biol 2004, 164:1009-1020.
21. Marra P, Salvatore L, Mironov A, Di Campli A, Di Tullio G, Trucco A, Beznoussenko G, Mironov A, De Matteis MA. The biogenesis of the Golgi ribbon: the roles of membrane input from the ER and of GM130. Mol Biol Cell 2007, 18:1595-1608.
22. Puthenveedu MA, Bachert C, Puri S, Lanni F, Linstedt AD. GM130 and GRASP65-dependent lateral cisternal fusion allows uniform Golgi-enzyme distribution. Nat Cell Biol 2006, 8:238-248.
23. Bradke F, Dotti CG. Neuronal polarity: vectorial cytoplasmic flow precedes axon formation. Neuron 1997, 19:1175-1186.
24. de Anda FC, Pollarolo G, Da Silva JS, Camoletto PG, Feiguin F, Dotti CG. Centrosome localization determines neuronal polarity. Nature 2005, 436:704-708.
25. Sutterlin C, Colanzi A. The Golgi and the centrosome: building a functional partnership. J Cell Biol 2010, 188:621-628.
26. Barnes AP, Lilley BN, Pan YA, Plummer LJ, Powell AW, Raines AN, Sanes JR, Polleux F. LKB1 and SAD kinases define a pathway required for the polarization of cortical neurons. Cell 2007, 129:549-563.
27. Asada N, Sanada K, Fukada Y. LKB1 regulates neuronal migration and neuronal differentiation in the developing neocortex through centrosomal positioning. J Neurosci 2007, 27:11769-11775.
28. Bai J, Ramos RL, Paramasivam M, Siddiqi F, Ackman JB, LoTurco JJ. The role of DCX and LIS1 in migration through the lateral cortical stream of developing forebrain. Dev Neurosci 2008, 30:144-156.
29. Corbo JC, Deuel TA, Long JM, LaPorte P, Tsai E, Wynshaw-Boris A, Walsh CA. Doublecortin is required in mice for lamination of the hippocampus but not the neocortex. J Neurosci 2002, 22:7548-7557.
30. Deuel TA, Liu JS, Corbo JC, Yoo SY, Rorke-Adams LB, Walsh CA. Genetic interactions between doublecortin and doublecortin-like kinase in neuronal migration and axon outgrowth. Neuron 2006, 49:41-53.
31. Koizumi H, Tanaka T, Gleeson JG. Doublecortin-like kinase functions with doublecortin to mediate fiber tract decussation and neuronal migration. Neuron 2006, 49:55-66.
32. Zheng H, Jiang M, Trumbauer ME, Sirinathsinghji DJS, Hopkins R, Smith DW, Heavens RP, Dawson GR, Boyce S, Conner MW, Stevens KA, Slunt HH, Sisodia SS, Chen HY, van der Ploeg LHT. Beta-amyloid precursor protein-deficient mice show reactive gliosis and decreased locomotor activity. Cell 1995, 81:525-531.
33. Young-Pearse TL, Bai J, Chang R, Zheng JB, LoTurco JJ, Selkoe DJ. A critical function for beta-amyloid precursor protein in neuronal migration revealed by in utero RNA interference. J Neurosci 2007, 27:14459-14469.
34. Chou WH, Choi DS, Zhang H, Mu D, McMahon T, Kharazia VN, Lowell CA, Ferriero DM, Messing RO. Neutrophil protein kinase Cdelta as a mediator of stroke-reperfusion injury. J Clin Invest 2004, 114:49-56.
35. Zhao CT, Li K, Li JT, Zheng W, Liang XJ, Geng AQ, Li N, Yuan XB. PKCdelta regulates cortical radial migration by stabilizing the Cdk5 activator p35. Proc Natl Acad Sci USA 2009, 106:21353-21358.
36. Olson EC, Kim S, Walsh CA. Impaired neuronal positioning and dendritogenesis in the neocortex after cell-autonomous Dab1 suppression. J Neurosci 2006, 26:1767-1775.
37. Sapir T, Sapoznik S, Levy T, Finkelshtein D, Shmueli A, Timm T, Mandelkow EM, Reiner O. Accurate balance of the polarity kinase MARK2/Par-1 is required for proper cortical neuronal migration. J Neurosci 2008, 28:5710-5720.
38. Shelly M, Cancedda L, Heilshorn S, Sumbre G, Poo MM. LKB1/STRAD promotes axon initiation during neuronal polarization. Cell 2007, 129:565-577.
39. Williams T, Courchet J, Viollet B, Brenman JE, Polleux F. AMP-activated protein kinase (AMPK) activity is not required for neuronal development but regulates axogenesis during metabolic stress. Proc Natl Acad Sci USA 2011, 108:5849-5854.
40. Altomare DA, Testa JR. Perturbations of the AKT signaling pathway in human cancer. Oncogene 2005, 24:7455-7464.
41. Beffert U, Morfini G, Bock HH, Reyna H, Brady ST, Herz J. Reelin-mediated signaling locally regulates protein kinase B/Akt and glycogen synthase kinase 3beta. J Biol Chem 2002, 277:49958-49964.
42. Horton AC, Ehlers MD. Neuronal polarity and trafficking. Neuron 2003, 40:277-295.
43. Ye B, Zhang Y, Song W, Younger SH, Jan LY, Jan YN. Growing dendrites and axons differ in their reliance on the secretory pathway. Cell 2007, 130:717-729.
44. O'Dell RS, Ustine CJ, Cameron DA, Lawless SM, Williams RM, Zipfel WR, Olson EC. Layer 6 cortical neurons require Reelin-Dab1 signaling for cellular orientation, Golgi deployment, and directed neurite growth into the marginal zone. Neural Dev 2012, 7:25.
45. de Anda FC, Meletis K, Ge X, Rei D, Tsai LH. Centrosome motility is essential for initial axon formation in the neocortex. J Neurosci 2010, 30:10391-10406.
46. Noctor SC, Martinez-Cerdeno V, Ivic L, Kriegstein AR. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 2004, 7:136-144.
47. Matsuda T, Cepko CL. Controlled expression of transgenes introduced by in vivo electroporation. Proc Natl Acad Sci USA 2007, 104:1027-1032.
48. Matsuki T, Zaka M, Guerreiro R, van der Brug MP, Cooper JA, Cookson MR, Hardy JA, Howell BW. Identification of Stk25 as a genetic modifier of Tau phosphorylation in Dab1-mutant mice. PLoS One 2012, 7:e31152.