Molecular Basis for Specific Regulation of Neuronal Kinesin-3 Motors by Doublecortin Family Proteins

Molecular Cell

Volumn 47, Issue 5, 2012, Pages 707-721

  Liu, Judy S ^a,b   Schubert, Christian R ^b,f   Fu, Xiaoqin ^a   Fourniol, Franck J ^c,d   Jaiswal, Jyoti K ^a   Houdusse, Anne ^e   Stultz, Collin M ^f   Moores, Carolyn A ^c   Walsh, Christopher A ^b  

^a CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c UNIVERSITY OF LONDON   (United Kingdom)

^d THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^e CNRS   (France)

^f USA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLECORTIN; DOUBLECORTIN LIKE KINASE 1; KIF1A PROTEIN; KINESIN; SYNAPTOBREVIN 2; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CELL MIGRATION; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; IMAGE RECONSTRUCTION; MOUSE; NERVE CELL; NONHUMAN; POINT MUTATION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS REGULATION; PROTEIN TRANSPORT;

ANIMALS; FEMALE; KINESIN; MALE; MICE; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; NEURONS; NEUROPEPTIDES; PROTEIN-SERINE-THREONINE KINASES;

EID: 84866284504     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2012.06.025     Document Type: Article

References (54)

1. Bai J., Ramos R.L., Ackman J.B., Thomas A.M., Lee R.V., LoTurco J.J. RNAi reveals doublecortin is required for radial migration in rat neocortex. Nat. Neurosci. 2003, 6:1277-1283.
2. Bielas S.L., Serneo F.F., Chechlacz M., Deerinck T.J., Perkins G.A., Allen P.B., Ellisman M.H., Gleeson J.G. Spinophilin facilitates dephosphorylation of doublecortin by PP1 to mediate microtubule bundling at the axonal wrist. Cell 2007, 129:579-591.
3. Bilimoria P.M., de la Torre-Ubieta L., Ikeuchi Y., Becker E.B., Reiner O., Bonni A. A JIP3-regulated GSK3beta/DCX signaling pathway restricts axon branching. J. Neurosci. 2010, 30:16766-16776.
4. Binder L.I., Frankfurter A., Rebhun L.I. Differential localization of MAP-2 and tau in mammalian neurons in situ. Ann. N Y Acad. Sci. 1986, 466:145-166.
5. Caviston J.P., Holzbaur E.L. Microtubule motors at the intersection of trafficking and transport. Trends Cell Biol. 2006, 16:530-537.
6. Chae T., Kwon Y.T., Bronson R., Dikkes P., Li E., Tsai L.H. Mice lacking p35, a neuronal specific activator of Cdk5, display cortical lamination defects, seizures, and adult lethality. Neuron 1997, 18:29-42.
7. Cho K.I., Cai Y., Yi H., Yeh A., Aslanukov A., Ferreira P.A. Association of the kinesin-binding domain of RanBP2 to KIF5B and KIF5C determines mitochondria localization and function. Traffic 2007, 8:1722-1735.
8. Cierpicki T., Kim M.H., Cooper D.R., Derewenda U., Bushweller J.H., Derewenda Z.S. The DC-module of doublecortin: dynamics, domain boundaries, and functional implications. Proteins 2006, 64:874-882.
9. Coquelle F.M., Levy T., Bergmann S., Wolf S.G., Bar-El D., Sapir T., Brody Y., Orr I., Barkai N., Eichele G., et al. Common and divergent roles for members of the mouse DCX superfamily. Cell Cycle 2006, 5:976-983.
10. Dehmelt L., Halpain S. The MAP2/Tau family of microtubule-associated proteins. Genome Biol. 2005, 6:204.
11. des Portes V., Francis F., Pinard J.M., Desguerre I., Moutard M.L., Snoeck I., Meiners L.C., Capron F., Cusmai R., Ricci S., et al. Doublecortin is the major gene causing X-linked subcortical laminar heterotopia (SCLH). Hum. Mol. Genet. 1998, 7:1063-1070.
12. Deuel T.A., Liu J.S., Corbo J.C., Yoo S.Y., Rorke-Adams L.B., Walsh C.A. Genetic interactions between doublecortin and doublecortin-like kinase in neuronal migration and axon outgrowth. Neuron 2006, 49:41-53.
13. Duncan J.E., Goldstein L.S. The genetics of axonal transport and axonal transport disorders. PLoS Genet. 2006, 2:e124. 10.1371/journal.pgen.0020124.
14. Feng J., Yan Z., Ferreira A., Tomizawa K., Liauw J.A., Zhuo M., Allen P.B., Ouimet C.C., Greengard P. Spinophilin regulates the formation and function of dendritic spines. Proc. Natl. Acad. Sci. USA 2000, 97:9287-9292.
15. Fourniol F.J., Sindelar C.V., Amigues B., Clare D.K., Thomas G., Perderiset M., Francis F., Houdusse A., Moores C.A. Template-free 13-protofilament microtubule-MAP assembly visualized at 8 A resolution. J. Cell Biol. 2010, 191:463-470.
16. Friocourt G., Marcorelles P., Saugier-Veber P., Quille M.L., Marret S., Laquerriere A. Role of cytoskeletal abnormalities in the neuropathology and pathophysiology of type I lissencephaly. Acta Neuropathol. 2011, 121:149-170.
17. Gdalyahu A., Ghosh I., Levy T., Sapir T., Sapoznik S., Fishler Y., Azoulai D., Reiner O. DCX, a new mediator of the JNK pathway. EMBO J. 2004, 23:823-832.
18. Gilmore E.C., Ohshima T., Goffinet A.M., Kulkarni A.B., Herrup K. Cyclin-dependent kinase 5-deficient mice demonstrate novel developmental arrest in cerebral cortex. J. Neurosci. 1998, 18:6370-6377.
19. Glater E.E., Megeath L.J., Stowers R.S., Schwarz T.L. Axonal transport of mitochondria requires milton to recruit kinesin heavy chain and is light chain independent. J. Cell Biol. 2006, 173:545-557.
20. Gleeson J.G., Allen K.M., Fox J.W., Lamperti E.D., Berkovic S., Scheffer I., Cooper E.C., Dobyns W.B., Minnerath S.R., Ross M.E., et al. Doublecortin, a brain-specific gene mutated in human X-linked lissencephaly and double cortex syndrome, encodes a putative signaling protein. Cell 1998, 92:63-72.
21. Gleeson J.G., Lin P.T., Flanagan L.A., Walsh C.A. Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 1999, 23:257-271.
22. Hammond J.W., Cai D., Verhey K.J. Tubulin modifications and their cellular functions. Curr. Opin. Cell Biol. 2008, 20:71-76.
23. Hammond J.W., Cai D., Blasius T.L., Li Z., Jiang Y., Jih G.T., Meyhofer E., Verhey K.J. Mammalian Kinesin-3 motors are dimeric in vivo and move by processive motility upon release of autoinhibition. PLoS Biol. 2009, 7:e72. 10.1371/journal.pbio.1000072.
24. Hammond J.W., Huang C.F., Kaech S., Jacobson C., Banker G., Verhey K.J. Posttranslational modifications of tubulin and the polarized transport of kinesin-1 in neurons. Mol. Biol. Cell 2010, 21:572-583.
25. Horesh D., Sapir T., Francis F., Wolf S.G., Caspi M., Elbaum M., Chelly J., Reiner O. Doublecortin, a stabilizer of microtubules. Hum. Mol. Genet. 1999, 8:1599-1610.
26. Huang C.F., Banker G. The translocation selectivity of the kinesins that mediate neuronal organelle transport. Traffic 2011, Published online December 28, 2011. 10.1111/j.1600-0854.2011.01325.x.
27. Jacobson C., Schnapp B., Banker G.A. A change in the selective translocation of the Kinesin-1 motor domain marks the initial specification of the axon. Neuron 2006, 49:797-804.
28. Kim M.H., Cierpicki T., Derewenda U., Krowarsch D., Feng Y., Devedjiev Y., Dauter Z., Walsh C.A., Otlewski J., Bushweller J.H., et al. The DCX-domain tandems of doublecortin and doublecortin-like kinase. Nat. Struct. Biol. 2003, 10:324-333.
29. Koizumi H., Tanaka T., Gleeson J.G. Doublecortin-like kinase functions with doublecortin to mediate fiber tract decussation and neuronal migration. Neuron 2006, 49:55-66.
30. Leger P.L., Souville I., Boddaert N., Elie C., Pinard J.M., Plouin P., Moutard M.L., des Portes V., Van Esch H., Joriot S., et al. The location of DCX mutations predicts malformation severity in X-linked lissencephaly. Neurogenetics 2008, 9:277-285.
31. Lin P.T., Gleeson J.G., Corbo J.C., Flanagan L., Walsh C.A. DCAMKL1 encodes a protein kinase with homology to doublecortin that regulates microtubule polymerization. J. Neurosci. 2000, 20:9152-9161.
32. Lo K.Y., Kuzmin A., Unger S.M., Petersen J.D., Silverman M.A. KIF1A is the primary anterograde motor protein required for the axonal transport of dense-core vesicles in cultured hippocampal neurons. Neurosci. Lett. 2011, 491:168-173.
33. Moores C.A., Perderiset M., Francis F., Chelly J., Houdusse A., Milligan R.A. Mechanism of microtubule stabilization by doublecortin. Mol. Cell 2004, 14:833-839.
34. Nadarajah B., Parnavelas J.G. Modes of neuronal migration in the developing cerebral cortex. Nat. Rev. Neurosci. 2002, 3:423-432.
35. Nangaku M., Sato-Yoshitake R., Okada Y., Noda Y., Takemura R., Yamazaki H., Hirokawa N. KIF1B, a novel microtubule plus end-directed monomeric motor protein for transport of mitochondria. Cell 1994, 79:1209-1220.
36. Nitta R., Kikkawa M., Okada Y., Hirokawa N. KIF1A alternately uses two loops to bind microtubules. Science 2004, 305:678-683.
37. Noctor S.C., Martinez-Cerdeno V., Ivic L., Kriegstein A.R. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci. 2004, 7:136-144.
38. Okada Y., Hirokawa N. A processive single-headed motor: kinesin superfamily protein KIF1A. Science 1999, 283:1152-1157.
39. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., Ferrin T.E. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 2004, 25:1605-1612.
40. Reiner O., Coquelle F.M., Peter B., Levy T., Kaplan A., Sapir T., Orr I., Barkai N., Eichele G., Bergmann S. The evolving doublecortin (DCX) superfamily. BMC Genomics 2006, 7:188. 10.1186/1471-2164-7-188.
41. Sapir T., Horesh D., Caspi M., Atlas R., Burgess H.A., Wolf S.G., Francis F., Chelly J., Elbaum M., Pietrokovski S., et al. Doublecortin mutations cluster in evolutionarily conserved functional domains. Hum. Mol. Genet. 2000, 9:703-712.
42. Shahpasand K., Ahmadian S., Riazi G.H. A possible mechanism for controlling processive transport by microtubule-associated proteins. Neurosci. Res. 2008, 61:347-350.
43. Sindelar C.V., Downing K.H. An atomic-level mechanism for activation of the kinesin molecular motors. Proc. Natl. Acad. Sci. USA 2010, 107:4111-4116.
44. Solecki D.J., Govek E.E., Tomoda T., Hatten M.E. Neuronal polarity in CNS development. Genes Dev. 2006, 20:2639-2647.
45. Song A.H., Wang D., Chen G., Li Y., Luo J., Duan S., Poo M.M. A selective filter for cytoplasmic transport at the axon initial segment. Cell 2009, 136:1148-1160.
46. Tanaka T., Serneo F.F., Tseng H.C., Kulkarni A.B., Tsai L.H., Gleeson J.G. Cdk5 phosphorylation of doublecortin ser297 regulates its effect on neuronal migration. Neuron 2004, 41:215-227.
47. Taylor K.R., Holzer A.K., Bazan J.F., Walsh C.A., Gleeson J.G. Patient mutations in doublecortin define a repeated tubulin-binding domain. J. Biol. Chem. 2000, 275:34442-34450.
48. Tint I., Jean D., Baas P.W., Black M.M. Doublecortin associates with microtubules preferentially in regions of the axon displaying actin-rich protrusive structures. J. Neurosci. 2009, 29:10995-11010.
49. Topf M., Lasker K., Webb B., Wolfson H., Chiu W., Sali A. Protein structure fitting and refinement guided by cryo-EM density. Structure 2008, 16:295-307.
50. Tsai J.W., Lian W.N., Kemal S., Kriegstein A.R., Vallee R.B. Kinesin 3 and cytoplasmic dynein mediate interkinetic nuclear migration in neural stem cells. Nat. Neurosci. 2010, 13:1463-1471.
51. Verhey K.J., Hammond J.W. Traffic control: regulation of kinesin motors. Nat. Rev. Mol. Cell Biol. 2009, 10:765-777.
52. Wozniak M.J., Melzer M., Dorner C., Haring H.U., Lammers R. The novel protein KBP regulates mitochondria localization by interaction with a kinesin-like protein. BMC Cell Biol. 2005, 6:35. 10.1186/1471-2121-6-35.
53. Xue X., Jaulin F., Espenel C., Kreitzer G. PH-domain-dependent selective transport of p75 by kinesin-3 family motors in non-polarized MDCK cells. J. Cell Sci. 2010, 123:1732-1741.
54. Yonekawa Y., Harada A., Okada Y., Funakoshi T., Kanai Y., Takei Y., Terada S., Noda T., Hirokawa N. Defect in synaptic vesicle precursor transport and neuronal cell death in KIF1A motor protein-deficient mice. J. Cell Biol. 1998, 141:431-441.