The Ubiquitin Ligase Phr1 Regulates Axon Outgrowth through Modulation of Microtubule Dynamics

Neuron

Volumn 56, Issue 4, 2007, Pages 604-620

  Lewcock, Joseph W ^a   Genoud, Nicolas ^a   Lettieri, Karen ^a   Pfaff, Samuel L ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

DEVBIO; MOLNEURO

Indexed keywords

GREEN FLUORESCENT PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; PACLITAXEL; UBIQUITIN PROTEIN LIGASE; UBIQUITIN PROTEIN LIGASE PHR1; UNCLASSIFIED DRUG;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOSKELETON; EMBRYO; ENZYME ACTIVITY; GENE MAPPING; GENE MUTATION; GENETIC SCREENING; GROWTH CONE; MALE; MICROTUBULE; MORPHOLOGY; MOTONEURON; MOUSE; MUTAGENESIS; NERVE FIBER; NERVE FIBER GROWTH; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SENSITIVITY ANALYSIS; SENSORY NERVE CELL;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; EFFERENT PATHWAYS; ENZYME INHIBITORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC SCREENING; GROWTH CONES; MALE; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; MICE, TRANSGENIC; MICROTUBULES; MOTOR NEURONS; MUTATION; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PACLITAXEL; RAL GUANINE NUCLEOTIDE EXCHANGE FACTOR; SPINAL CORD; TUBULIN MODULATORS;

EID: 36048943648     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2007.09.009     Document Type: Article

References (66)

1. Ahmad F.J., Pienkowski T.P., and Baas P.W. Regional differences in microtubule dynamics in the axon. J. Neurosci. 13 (1993) 856-866
2. Aletta J.M., and Greene L.A. Growth cone configuration and advance: a time-lapse study using video-enhanced differential interference contrast microscopy. J. Neurosci. 8 (1988) 1425-1435
3. Bielas S.L., Serneo F.F., Chechlacz M., Deerinck T.J., Perkins G.A., Allen P.B., Ellisman M.H., and Gleeson J.G. Spinophilin facilitates dephosphorylation of doublecortin by PP1 to mediate microtubule bundling at the axonal wrist. Cell 129 (2007) 579-591
4. Briscoe J., and Ericson J. Specification of neuronal fates in the ventral neural tube. Curr. Opin. Neurobiol. 11 (2001) 43-49
5. Brown A., Li Y., Slaughter T., and Black M.M. Composite microtubules of the axon: quantitative analysis of tyrosinated and acetylated tubulin along individual axonal microtubules. J. Cell Sci. 104 (1993) 339-352
6. Buck K.B., and Zheng J.Q. Growth cone turning induced by direct local modification of microtubule dynamics. J. Neurosci. 22 (2002) 9358-9367
7. Burgess R.W., Peterson K.A., Johnson M.J., Roix J.J., Welsh I.C., and O'Brien T.P. Evidence for a conserved function in synapse formation reveals Phr1 as a candidate gene for respiratory failure in newborn mice. Mol. Cell. Biol. 24 (2004) 1096-1105
8. Callahan C.A., Muralidhar M.G., Lundgren S.E., Scully A.L., and Thomas J.B. Control of neuronal pathway selection by a Drosophila receptor protein-tyrosine kinase family member. Nature 376 (1995) 171-174
9. Campbell D.S., and Holt C.E. Apoptotic pathway and MAPKs differentially regulate chemotropic responses of retinal growth cones. Neuron 37 (2003) 939-952
10. Collins C.A., Wairkar Y.P., Johnson S.L., and DiAntonio A. Highwire restrains synaptic growth by attenuating a MAP kinase signal. Neuron 51 (2006) 57-69
11. Concepcion D., Seburn K.L., Wen G., Frankel W.N., and Hamilton B.A. Mutation rate and predicted phenotypic target sizes in ethylnitrosourea-treated mice. Genetics 168 (2004) 953-959
12. D'Souza J., Hendricks M., Le Guyader S., Subburaju S., Grunewald B., Scholich K., and Jesuthasan S. Formation of the retinotectal projection requires Esrom, an ortholog of PAM (protein associated with Myc). Development 132 (2005) 247-256
13. Dasen J.S., Tice B.C., Brenner-Morton S., and Jessell T.M. A Hox regulatory network establishes motor neuron pool identity and target-muscle connectivity. Cell 123 (2005) 477-491
14. Dent E.W., and Gertler F.B. Cytoskeletal dynamics and transport in growth cone motility and axon guidance. Neuron 40 (2003) 209-227
15. Dickson B.J. Molecular mechanisms of axon guidance. Science 298 (2002) 1959-1964
16. Ebens A., Brose K., Leonardo E.D., Hanson Jr. M.G., Bladt F., Birchmeier C., Barres B.A., and Tessier-Lavigne M. Hepatocyte growth factor/scatter factor is an axonal chemoattractant and a neurotrophic factor for spinal motor neurons. Neuron 17 (1996) 1157-1172
17. Eberhart J., Swartz M.E., Koblar S.A., Pasquale E.B., and Krull C.E. EphA4 constitutes a population-specific guidance cue for motor neurons. Dev. Biol. 247 (2002) 89-101
18. Finney M., Ruvkun G., and Horvitz H.R. The C. elegans cell lineage and differentiation gene unc-86 encodes a protein with a homeodomain and extended similarity to transcription factors. Cell 55 (1988) 757-769
19. Gleeson J.G., Lin P.T., Flanagan L.A., and Walsh C.A. Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 23 (1999) 257-271
20. Goldberg D.J., and Burmeister D.W. Stages in axon formation: observations of growth of Aplysia axons in culture using video-enhanced contrast-differential interference contrast microscopy. J. Cell Biol. 103 (1986) 1921-1931
21. Gundersen G.G., and Bulinski J.C. Selective stabilization of microtubules oriented toward the direction of cell migration. Proc. Natl. Acad. Sci. USA 85 (1988) 5946-5950
22. Guo Q., Xie J., Dang C.V., Liu E.T., and Bishop J.M. Identification of a large Myc-binding protein that contains RCC1-like repeats. Proc. Natl. Acad. Sci. USA 95 (1998) 9172-9177
23. Haase G., Dessaud E., Garces A., de Bovis B., Birling M., Filippi P., Schmalbruch H., Arber S., and deLapeyriere O. GDNF acts through PEA3 to regulate cell body positioning and muscle innervation of specific motor neuron pools. Neuron 35 (2002) 893-905
24. Harris W.A., Holt C.E., and Bonhoeffer F. Retinal axons with and without their somata, growing to and arborizing in the tectum of Xenopus embryos: a time-lapse video study of single fibres in vivo. Development 101 (1987) 123-133
25. Helmbacher F., Schneider-Maunoury S., Topilko P., Tiret L., and Charnay P. Targeting of the EphA4 tyrosine kinase receptor affects dorsal/ventral pathfinding of limb motor axons. Development 127 (2000) 3313-3324
26. Helmbacher F., Dessaud E., Arber S., deLapeyriere O., Henderson C.E., Klein R., and Maina F. Met signaling is required for recruitment of motor neurons to PEA3-positive motor pools. Neuron 39 (2003) 767-777
27. Henderson C.E., Camu W., Mettling C., Gouin A., Poulsen K., Karihaloo M., Rullamas J., Evans T., McMahon S.B., Armanini M.P., et al. Neurotrophins promote motor neuron survival and are present in embryonic limb bud. Nature 363 (1993) 266-270
28. Huber A.B., Kania A., Tran T.S., Gu C., De Marco Garcia N., Lieberam I., Johnson D., Jessell T.M., Ginty D.D., and Kolodkin A.L. Distinct roles for secreted semaphorin signaling in spinal motor axon guidance. Neuron 48 (2005) 949-964
29. Jessell T.M., and Sanes J.R. Development. The decade of the developing brain. Curr. Opin. Neurobiol. 10 (2000) 599-611
30. Kalil K., Szebenyi G., and Dent E.W. Common mechanisms underlying growth cone guidance and axon branching. J. Neurobiol. 44 (2000) 145-158
31. Kania A., and Jessell T.M. Topographic motor projections in the limb imposed by LIM homeodomain protein regulation of ephrin-A:EphA interactions. Neuron 38 (2003) 581-596
32. Kasarskis A., Manova K., and Anderson K.V. A phenotype-based screen for embryonic lethal mutations in the mouse. Proc. Natl. Acad. Sci. USA 95 (1998) 7485-7490
33. Kolodkin A.L., Matthes D.J., and Goodman C.S. The semaphorin genes encode a family of transmembrane and secreted growth cone guidance molecules. Cell 75 (1993) 1389-1399
34. Kramer E.R., Knott L., Su F., Dessaud E., Krull C.E., Helmbacher F., and Klein R. Cooperation between GDNF/Ret and ephrinA/EphA4 signals for motor-axon pathway selection in the limb. Neuron 50 (2006) 35-47
35. Landmesser L. The development of motor projection patterns in the chick hind limb. J. Physiol. 284 (1978) 391-414
36. Landmesser L.T. The generation of neuromuscular specificity. Annu. Rev. Neurosci. 3 (1980) 279-302
37. Lee S.K., Jurata L.W., Funahashi J., Ruiz E.C., and Pfaff S.L. Analysis of embryonic motoneuron gene regulation: derepression of general activators function in concert with enhancer factors. Development 131 (2004) 3295-3306
38. Lieberam I., Agalliu D., Nagasawa T., Ericson J., and Jessell T.M. A Cxcl12-CXCR4 chemokine signaling pathway defines the initial trajectory of mammalian motor axons. Neuron 47 (2005) 667-679
39. Marquardt T., Shirasaki R., Ghosh S., Andrews S.E., Carter N., Hunter T., and Pfaff S.L. Coexpressed EphA receptors and ephrin-A ligands mediate opposing actions on growth cone navigation from distinct membrane domains. Cell 121 (2005) 127-139
40. Matus A. Stiff microtubules and neuronal morphology. Trends Neurosci. 17 (1994) 19-22
41. McLaughlin T., and O'Leary D.D. Molecular gradients and development of retinotopic maps. Annu. Rev. Neurosci. 28 (2005) 327-355
42. Myers C.P., Lewcock J.W., Hanson M.G., Gosgnach S., Aimone J.B., Gage F.H., Lee K.F., Landmesser L.T., and Pfaff S.L. Cholinergic input is required during embryonic development to mediate proper assembly of spinal locomotor circuits. Neuron 46 (2005) 37-49
43. Nakata K., Abrams B., Grill B., Goncharov A., Huang X., Chisholm A.D., and Jin Y. Regulation of a DLK-1 and p38 MAP kinase pathway by the ubiquitin ligase RPM-1 is required for presynaptic development. Cell 120 (2005) 407-420
44. Novak K.D., Prevette D., Wang S., Gould T.W., and Oppenheim R.W. Hepatocyte growth factor/scatter factor is a neurotrophic survival factor for lumbar but not for other somatic motoneurons in the chick embryo. J. Neurosci. 20 (2000) 326-337
45. Ozdinler P.H., and Macklis J.D. IGF-I specifically enhances axon outgrowth of corticospinal motor neurons. Nat. Neurosci. 9 (2006) 1371-1381
46. Santos T.M., Han S., Bowser M., Sazani K., Beauchamp R.L., Murthy V., Bhide P.G., and Ramesh V. Alternative splicing in protein associated with Myc (Pam) influences its binding to c-Myc. J. Neurosci. Res. 83 (2006) 222-232
47. Schaefer A.M., Hadwiger G.D., and Nonet M.L. rpm-1, a conserved neuronal gene that regulates targeting and synaptogenesis in C. elegans. Neuron 26 (2000) 345-356
48. Sharma K., Leonard A.E., Lettieri K., and Pfaff S.L. Genetic and epigenetic mechanisms contribute to motor neuron pathfinding. Nature 406 (2000) 515-519
49. Shirasaki R., and Pfaff S.L. Transcriptional codes and the control of neuronal identity. Annu. Rev. Neurosci. 25 (2002) 251-281
50. Shirasaki R., Lewcock J.W., Lettieri K., and Pfaff S.L. FGF as a target-derived chemoattractant for developing motor axons genetically programmed by the LIM Code. Neuron 50 (2006) 841-853
51. Song M.R., Shirasaki R., Cai C.L., Ruiz E.C., Evans S.M., Lee S.K., and Pfaff S.L. T-Box transcription factor Tbx20 regulates a genetic program for cranial motor neuron cell body migration. Development 133 (2006) 4945-4955
52. Suter D.M., Schaefer A.W., and Forscher P. Microtubule dynamics are necessary for SRC family kinase-dependent growth cone steering. Curr. Biol. 14 (2004) 1194-1199
53. Tessier-Lavigne M., and Goodman C.S. The molecular biology of axon guidance. Science 274 (1996) 1123-1133
54. Thaler J.P., Koo S.J., Kania A., Lettieri K., Andrews S., Cox C., Jessell T.M., and Pfaff S.L. A postmitotic role for Isl-class LIM homeodomain proteins in the assignment of visceral spinal motor neuron identity. Neuron 41 (2004) 337-350
55. Uemura O., Okada Y., Ando H., Guedj M., Higashijima S., Shimazaki T., Chino N., Okano H., and Okamoto H. Comparative functional genomics revealed conservation and diversification of three enhancers of the isl1 gene for motor and sensory neuron-specific expression. Dev. Biol. 278 (2005) 587-606
56. Van Vactor D. Adhesion and signaling in axonal fasciculation. Curr. Opin. Neurobiol. 8 (1998) 80-86
57. Varela-Echavarria A., Tucker A., Puschel A.W., and Guthrie S. Motor axon subpopulations respond differentially to the chemorepellents netrin-1 and semaphorin D. Neuron 18 (1997) 193-207
58. Vrieseling E., and Arber S. Target-induced transcriptional control of dendritic patterning and connectivity in motor neurons by the ETS gene Pea3. Cell 127 (2006) 1439-1452
59. Wan H.I., DiAntonio A., Fetter R.D., Bergstrom K., Strauss R., and Goodman C.S. Highwire regulates synaptic growth in Drosophila. Neuron 26 (2000) 313-329
60. West A.G., Gaszner M., and Felsenfeld G. Insulators: many functions, many mechanisms. Genes Dev. 16 (2002) 271-288
61. Williamson T., Gordon-Weeks P.R., Schachner M., and Taylor J. Microtubule reorganization is obligatory for growth cone turning. Proc. Natl. Acad. Sci. USA 93 (1996) 15221-15226
62. Wu C., Wairkar Y.P., Collins C.A., and DiAntonio A. Highwire function at the Drosophila neuromuscular junction: spatial, structural, and temporal requirements. J. Neurosci. 25 (2005) 9557-9566
63. Yamamoto Y., Livet J., Pollock R.A., Garces A., Arce V., deLapeyriere O., and Henderson C.E. Hepatocyte growth factor (HGF/SF) is a muscle-derived survival factor for a subpopulation of embryonic motoneurons. Development 124 (1997) 2903-2913
64. Zallen J.A., Yi B.A., and Bargmann C.I. The conserved immunoglobulin superfamily member SAX-3/Robo directs multiple aspects of axon guidance in C. elegans. Cell 92 (1998) 217-227
65. Zhen M., Huang X., Bamber B., and Jin Y. Regulation of presynaptic terminal organization by C. elegans RPM-1, a putative guanine nucleotide exchanger with a RING-H2 finger domain. Neuron 26 (2000) 331-343
66. Zhou F.Q., and Cohan C.S. How actin filaments and microtubules steer growth cones to their targets. J. Neurobiol. 58 (2004) 84-91