Growth Cone MKK7 mRNA Targeting Regulates MAP1b-Dependent Microtubule Bundling to Control Neurite Elongation

PLoS Biology

Volumn 10, Issue 12, 2012, Pages

  Feltrin, Daniel ^a   Fusco, Ludovico ^a   Witte, Harald ^b   Moretti, Francesca ^a   Martin, Katrin ^a   Letzelter, Michel ^a   Fluri, Erika ^a   Scheiffele, Peter ^b   Pertz, Olivier ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

DUAL LEUCINE ZIPPER KINASE; MESSENGER RNA; MICROTUBULE ASSOCIATED PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 7; PHOSPHOTRANSFERASE; PROTEIN MAP1B; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL ACTIVITY; CONTROLLED STUDY; EMBRYO; ENZYME PHOSPHORYLATION; GENE LOCATION; GENE TARGETING; GROWTH CONE; MICROTUBULE BUNDLING; MKK7 GENE; MOUSE; NERVE FIBER GROWTH; NEURITE ELONGATION; NONHUMAN; REGULATORY MECHANISM; RNA TRANSLATION; SIGNAL TRANSDUCTION;

3' UNTRANSLATED REGIONS; ANIMALS; BASE SEQUENCE; CELL DIFFERENTIATION; CELL LINE; GENOME; GROWTH CONES; HIPPOCAMPUS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE KINASE 7; MAP KINASE SIGNALING SYSTEM; MICE; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MODELS, BIOLOGICAL; NEURITES; PHOSPHORYLATION; PHOSPHOTHREONINE; PROTEIN BIOSYNTHESIS; REPRODUCIBILITY OF RESULTS; RNA TRANSPORT; RNA, MESSENGER; TIME FACTORS;

EID: 84871676498     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001439     Document Type: Article

References (53)

1. Holt CE, Bullock SL, (2009) Subcellular mRNA localization in animal cells and why it matters. Science 326: 1212-1216.
2. Wu KY, Hengst U, Cox LJ, Macosko EZ, Jeromin A, et al. (2005) Local translation of RhoA regulates growth cone collapse. Nature 436: 1020-1024.
3. Barrett LE, Sul JY, Takano H, Van Bockstaele EJ, Haydon PG, et al. (2006) Region-directed phototransfection reveals the functional significance of a dendritically synthesized transcription factor. Nat Methods 3: 455-460.
4. Cox LJ, Hengst U, Gurskaya NG, Lukyanov KA, Jaffrey SR, (2008) Intra-axonal translation and retrograde trafficking of CREB promotes neuronal survival. Nat Cell Biol 10: 149-159.
5. Ben-Yaakov K, Dagan SY, Segal-Ruder Y, Shalem O, Vuppalanchi D, et al. (2012) Axonal transcription factors signal retrogradely in lesioned peripheral nerve. EMBO J 31: 1350-1363.
6. Jung H, O'Hare CM, Holt CE, (2011) Translational regulation in growth cones. Curr Opin Genet Dev 21: 458-464.
7. Martin KC, Zukin RS, (2006) RNA trafficking and local protein synthesis in dendrites: an overview. J Neurosci 26: 7131-7134.
8. Taylor AM, Berchtold NC, Perreau VM, Tu CH, Li Jeon N, et al. (2009) Axonal mRNA in uninjured and regenerating cortical mammalian axons. J Neurosci 29: 4697-4707.
9. Cajigas IJ, Tushev G, Will TJ, tom Dieck S, Fuerst N, et al. (2012) The local transcriptome in the synaptic neuropil revealed by deep sequencing and high-resolution imaging. Neuron 74: 453-466.
10. Zivraj KH, Tung YC, Piper M, Gumy L, Fawcett JW, et al. (2010) Subcellular profiling reveals distinct and developmentally regulated repertoire of growth cone mRNAs. J Neurosci 30: 15464-15478.
11. Gumy LF, Yeo GS, Tung YC, Zivraj KH, Willis D, et al. (2011) Transcriptome analysis of embryonic and adult sensory axons reveals changes in mRNA repertoire localization. RNA 17: 85-98.
12. Weston CR, Davis RJ, (2007) The JNK signal transduction pathway. Curr Opin Cell Biol 19: 142-149.
13. Coffey ET, Hongisto V, Dickens M, Davis RJ, Courtney MJ, (2000) Dual roles for c-Jun N-terminal kinase in developmental and stress responses in cerebellar granule neurons. J Neurosci 20: 7602-7613.
14. Waetzig V, Zhao Y, Herdegen T, (2006) The bright side of JNKs-Multitalented mediators in neuronal sprouting, brain development and nerve fiber regeneration. Prog Neurobiol 80: 84-97.
15. Chang L, Jones Y, Ellisman MH, Goldstein LS, Karin M, (2003) JNK1 is required for maintenance of neuronal microtubules and controls phosphorylation of microtubule-associated proteins. Dev Cell 4: 521-533.
16. Ng DC, Zhao TT, Yeap YY, Ngoei KR, Bogoyevitch MA, (2010) c-Jun N-terminal kinase phosphorylation of stathmin confers protection against cellular stress. J Biol Chem 285: 29001-29013.
17. Tararuk T, Ostman N, Li W, Bjorkblom B, Padzik A, et al. (2006) JNK1 phosphorylation of SCG10 determines microtubule dynamics and axodendritic length. J Cell Biol 173: 265-277.
18. Gdalyahu A, Ghosh I, Levy T, Sapir T, Sapoznik S, et al. (2004) DCX, a new mediator of the JNK pathway. EMBO J 23: 823-832.
19. Oliva AA Jr, Atkins CM, Copenagle L, Banker GA, (2006) Activated c-Jun N-terminal kinase is required for axon formation. J Neurosci 26: 9462-9470.
20. Dajas-Bailador F, Jones EV, Whitmarsh AJ, (2008) The JIP1 scaffold protein regulates axonal development in cortical neurons. Curr Biol 18: 221-226.
21. Haeusgen W, Herdegen T, Waetzig V, (2011) The bottleneck of JNK signaling: molecular and functional characteristics of MKK4 and MKK7. Eur J Cell Biol 90: 536-544.
22. Gallo KA, Johnson GL, (2002) Mixed-lineage kinase control of JNK and p38 MAPK pathways. Nat Rev Mol Cell Biol 3: 663-672.
23. Pertz OC, Wang Y, Yang F, Wang W, Gay LJ, et al. (2008) Spatial mapping of the neurite and soma proteomes reveals a functional Cdc42/Rac regulatory network. Proc Natl Acad Sci U S A 105: 1931-1936.
24. Torre ER, Steward O, (1992) Demonstration of local protein synthesis within dendrites using a new cell culture system that permits the isolation of living axons and dendrites from their cell bodies. J Neurosci 12: 762-772.
25. Kiebler MA, Bassell GJ, (2006) Neuronal RNA granules: movers and makers. Neuron 51: 685-690.
26. Fosbrink M, Aye-Han NN, Cheong R, Levchenko A, Zhang J, (2010) Visualization of JNK activity dynamics with a genetically encoded fluorescent biosensor. Proc Natl Acad Sci U S A 107: 5459-5464.
27. Hirai S, Banba Y, Satake T, Ohno S, (2011) Axon formation in neocortical neurons depends on stage-specific regulation of microtubule stability by the dual leucine zipper kinase-c-Jun N-terminal kinase pathway. J Neurosci 31: 6468-6480.
28. Riedl J, Crevenna AH, Kessenbrock K, Yu JH, Neukirchen D, et al. (2008) Lifeact: a versatile marker to visualize F-actin. Nat Methods 5: 605-607.
29. Dehmelt L, Halpain S, (2004) Actin and microtubules in neurite initiation: are MAPs the missing link? J Neurobiol 58: 18-33.
30. Tournier C, Whitmarsh AJ, Cavanagh J, Barrett T, Davis RJ, (1999) The MKK7 gene encodes a group of c-Jun NH2-terminal kinase kinases. Mol Cell Biol 19: 1569-1581.
31. Mili S, Moissoglu K, Macara IG, (2008) Genome-wide screen reveals APC-associated RNAs enriched in cell protrusions. Nature 453: 115-119.
32. Takahashi S, Ebihara A, Kajiho H, Kontani K, Nishina H, et al. (2011) RASSF7 negatively regulates pro-apoptotic JNK signaling by inhibiting the activity of phosphorylated-MKK7. Cell Death Differ 18: 645-655.
33. Welshhans K, Bassell GJ, (2011) Netrin-1-induced local beta-actin synthesis and growth cone guidance requires zipcode binding protein 1. J Neurosci 31: 9800-9813.
34. Fivaz M, Meyer T, (2003) Specific localization and timing in neuronal signal transduction mediated by protein-lipid interactions. Neuron 40: 319-330.
35. Yudin D, Hanz S, Yoo S, Iavnilovitch E, Willis D, et al. (2008) Localized regulation of axonal RanGTPase controls retrograde injury signaling in peripheral nerve. Neuron 59: 241-252.
36. Dotti CG, Sullivan CA, Banker GA, (1988) The establishment of polarity by hippocampal neurons in culture. J Neurosci 8: 1454-1468.
37. Condeelis J, Singer RH, (2005) How and why does beta-actin mRNA target? Biol Cell 97: 97-110.
38. Eng H, Lund K, Campenot RB, (1999) Synthesis of beta-tubulin, actin, and other proteins in axons of sympathetic neurons in compartmented cultures. J Neurosci 19: 1-9.
39. Taylor AM, Blurton-Jones M, Rhee SW, Cribbs DH, Cotman CW, et al. (2005) A microfluidic culture platform for CNS axonal injury, regeneration and transport. Nat Methods 2: 599-605.
40. Dieterich DC, Hodas JJ, Gouzer G, Shadrin IY, Ngo JT, et al. (2010) In situ visualization and dynamics of newly synthesized proteins in rat hippocampal neurons. Nat Neurosci 13: 897-905.
41. Chicurel ME, Singer RH, Meyer CJ, Ingber DE, (1998) Integrin binding and mechanical tension induce movement of mRNA and ribosomes to focal adhesions. Nature 392: 730-733.
42. de Hoog CL, Foster LJ, Mann M, (2004) RNA and RNA binding proteins participate in early stages of cell spreading through spreading initiation centers. Cell 117: 649-662.
43. Huttelmaier S, Zenklusen D, Lederer M, Dictenberg J, Lorenz M, et al. (2005) Spatial regulation of beta-actin translation by Src-dependent phosphorylation of ZBP1. Nature 438: 512-515.
44. Antar LN, Li C, Zhang H, Carroll RC, Bassell GJ, (2006) Local functions for FMRP in axon growth cone motility and activity-dependent regulation of filopodia and spine synapses. Mol Cell Neurosci 32: 37-48.
45. Buckley PT, Lee MT, Sul JY, Miyashiro KY, Bell TJ, et al. (2011) Cytoplasmic intron sequence-retaining transcripts can be dendritically targeted via ID element retrotransposons. Neuron 69: 877-884.
46. Donnelly CJ, Willis DE, Xu M, Tep C, Jiang C, et al. (2011) Limited availability of ZBP1 restricts axonal mRNA localization and nerve regeneration capacity. EMBO J 30: 4665-4677.
47. Merritt SE, Mata M, Nihalani D, Zhu C, Hu X, et al. (1999) The mixed lineage kinase DLK utilizes MKK7 and not MKK4 as substrate. J Biol Chem 274: 10195-10202.
48. Fleming Y, Armstrong CG, Morrice N, Paterson A, Goedert M, et al. (2000) Synergistic activation of stress-activated protein kinase 1/c-Jun N-terminal kinase (SAPK1/JNK) isoforms by mitogen-activated protein kinase kinase 4 (MKK4) and MKK7. Biochem J 352 Pt 1: 145-154.
49. Yamasaki T, Kawasaki H, Arakawa S, Shimizu K, Shimizu S, et al. (2011) Stress-activated protein kinase MKK7 regulates axon elongation in the developing cerebral cortex. J Neurosci 31: 16872-16883.
50. Hirai S, Cui de F, Miyata T, Ogawa M, Kiyonari H, et al. (2006) The c-Jun N-terminal kinase activator dual leucine zipper kinase regulates axon growth and neuronal migration in the developing cerebral cortex. J Neurosci 26: 11992-12002.
51. Chong KW, Lee AY, Koay ES, Seet SJ, Cheung NS, (2006) pH dependent high transfection efficiency of mouse neuroblastomas using TransFectin. J Neurosci Methods 158: 56-63.
52. Vessey JP, Macchi P, Stein JM, Mikl M, Hawker KN, et al. (2008) A loss of function allele for murine Staufen1 leads to impairment of dendritic Staufen1-RNP delivery and dendritic spine morphogenesis. Proc Natl Acad Sci U S A 105: 16374-16379.
53. Hodgson L, Pertz O, Hahn KM, (2008) Design and optimization of genetically encoded fluorescent biosensors: GTPase biosensors. Methods Cell Biol 85: 63-81.