Nerve growth factor-induced formation of axonal filopodia and collateral branches involves the intra-axonal synthesis of regulators of the actin-nucleating Arp2/3 complex

Journal of Neuroscience

Volumn 32, Issue 49, 2012, Pages 17671-17689

  Spillane, Mirela ^a   Ketschek, Andrea ^a   Donnelly, Chris J ^b   Pacheco, Almudena ^c   Twiss, Jeffrey L ^c   Gallo, Gianluca ^a  

^a TEMPLE UNIVERSITY   (United States)

^b UNIVERSITY OF DELAWARE   (United States)

^c DREXEL UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN RELATED PROTEIN 2-3 COMPLEX; CORTACTIN; GUANOSINE TRIPHOSPHATASE; MESSENGER RNA; NERVE GROWTH FACTOR; NEUROMODULIN; PHOSPHATIDYLINOSITOL 3 KINASE; RAC1 PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CHICKEN; CONTROLLED STUDY; ELECTROPORATION; EMBRYO; FILOPODIUM; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; IMMUNOCYTOCHEMISTRY; MICROTUBULE; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS INHIBITION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SPINAL CORD;

ACTIN CYTOSKELETON; ACTIN-RELATED PROTEIN 2-3 COMPLEX; ANIMALS; AXONS; CELLS, CULTURED; CHICK EMBRYO; CORTACTIN; GROWTH CONES; MICROTUBULES; NERVE GROWTH FACTOR; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN SYNTHESIS INHIBITORS; PSEUDOPODIA; RAC1 GTP-BINDING PROTEIN; SENSORY RECEPTOR CELLS; SIGNAL TRANSDUCTION; WISKOTT-ALDRICH SYNDROME PROTEIN FAMILY;

EID: 84870551021     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1079-12.2012     Document Type: Article

References (75)

1. Aakalu G, Smith WB, Nguyen N, Jiang C, Schuman EM (2001) Dynamic visualization of local protein synthesis in hippocampal neurons. Neuron 30:489-502. CrossRef Medline
2. Ahuja R, Pinyol R, Reichenbach N, Custer L, Klingensmith J, Kessels MM, Qualmann B (2007) Cordon-bleu is an actin nucleation factor and controls neuronal morphology. Cell 131:337-350. CrossRef Medline
3. Alvarez J, Giuditta A, Koenig E (2000) Protein synthesis in axons and terminals: significance for maintenance, plasticity and regulation of phenotype. With a critique of slow transport theory. Prog Neurobiol 62:1-62. CrossRef Medline
4. Andersen EF, Asuri NS, Halloran MC (2011) In vivo imaging of cell behaviors and F-actin reveals LIM-HD transcription factor regulation of peripheral versus central sensory axon development. Neural Dev 6:27. CrossRef Medline
5. 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. CrossRef Medline
6. Brittis PA, Lu Q, Flanagan JG (2002) Axonal protein synthesis provides a mechanism for localized regulation at an intermediate target. Cell 110: 223-235. CrossRef Medline
7. Brown MD, Cornejo BJ, Kuhn TB, Bamburg JR (2000) Cdc42 stimulates neurite outgrowth and formation of growth cone filopodia and lamellipodia. J Neurobiol 43:352-364. CrossRef Medline
8. Buckmaster PS, Lew FH (2011) Rapamycin suppresses mossy fiber sprouting but not seizure frequency in a mouse model of temporal lobe epilepsy. J Neurosci 31:2337-2347. CrossRef Medline
9. Buckmaster PS, Wen X (2011) Rapamycin suppresses axon sprouting by somatostatin interneurons in a mouse model of temporal lobe epilepsy. Epilepsia 52:2057-2064. CrossRef Medline
10. Campbell DS, Holt CE (2001) Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron 32:1013-1026. CrossRef Medline
11. Chadborn NH, Ahmed AI, Holt MR, Prinjha R, Dunn GA, Jones GE, Eickholt BJ (2006) PTEN couples Sema3A signalling to growth cone collapse. J Cell Sci 119:951-957. CrossRef Medline
12. Chen TJ, Gehler S, Shaw AE, Bamburg JR, Letourneau PC (2006) Cdc42 participates in the regulation of ADF/cofilin and retinal growth cone filopodia by brain derived neurotrophic factor. J Neurobiol 66:103-114. CrossRef Medline
13. Cheng Y, Leung S, Mangoura D (2000) Transient suppression of cortactin ectopically induces large telencephalic neurons towards a GABAergic phenotype. J Cell Sci 113:3161-3172. Medline
14. Cox LJ, Hengst U, Gurskaya NG, Lukyanov KA, Jaffrey SR (2008) Intraaxonal translation and retrograde trafficking of CREB promotes neuronal survival. Nat Cell Biol 10:149-159. CrossRef Medline
15. Derivery E, Gautreau A (2010) Generation of branched actin networks: assembly and regulation of the N-WASP and WAVE molecular machines. Bioessays 32:119-131. CrossRef Medline
16. Donnelly CJ, Fainzilber M, Twiss JL (2010) Subcellular communication through RNA transport and localized protein synthesis. Traffic 11: 1498-1505. CrossRef Medline
17. Donnelly CJ, Willis DE, Xu M, Tep C, Jiang C, Yoo S, Schanen NC, Kirn- Safran CB, van Minnen J, English A, Yoon SO, Bassell GJ, Twiss JL (2011) Limited availability of ZBP1 restricts axonalmRNAlocalization and nerve regeneration capacity. EMBO J 30:4665-4677. CrossRef Medline
18. Drinjakovic J, Jung H, Campbell DS, Strochlic L, Dwivedy A, Holt CE (2010) E3 ligase Nedd4 promotes axon branching by downregulating PTEN. Neuron 65:341-357. CrossRef Medline
19. Gallo G (2003) Making proteins into drugs: assisted delivery of proteins and peptides into living neurons. Methods Cell Biol 71:325-338. CrossRef Medline
20. Gallo G (2006) RhoA-kinase coordinates F-actin organization and myosin II activity during semaphorin-3A-induced axon retraction. J Cell Sci 119: 3413-3423. CrossRef Medline
21. Gallo G (2008) Semaphorin 3A inhibits ERM protein phosphorylation in growth cone filopodia through inactivation of PI3K. Dev Neurobiol 68: 926-933. CrossRef Medline
22. Gallo G (2011) The cytoskeletal and signaling mechanisms of axon collateral branching. Dev Neurobiol 71:201-220. CrossRef Medline
23. Gallo G, Letourneau PC (1999) Different contributions of microtubule dynamics and transport to the growth of axons and collateral sprouts. J Neurosci 19:3860-3873. Medline
24. Gibson DA, Ma L (2011) Developmental regulation of axon branching in the vertebrate nervous system. Development 138:183-195. CrossRef Medline
25. Grider MH, Park D, Spencer DM, Shine HD (2009) Lipid raft-targeted Akt promotes axonal branching and growth cone expansion via mTOR and Rac1, respectively. J Neurosci Res 87:3033-3042, 2009 Nov 1. Medline
26. Gu J, Firestein BL, Zheng JQ (2008) Microtubules in dendritic spine development. J Neurosci 28:12120-12124CrossRef Medline
27. Gumy LF, Yeo GS, Tung YC, Zivraj KH, Willis D, Coppola G, Lam BY, Twiss JL, Holt CE, Fawcett JW (2011) Transcriptome analysis of embryonic and adult sensory axons reveals changes in mRNA repertoire localization. RNA 17:85-98. CrossRef Medline
28. Hanz S, Perlson E, Willis D, Zheng JQ, Massarwa R, Huerta JJ, Koltzenburg M, Kohler M, van-Minnen J, Twiss JL, Fainzilber M (2003) Axoplasmic importins enable retrograde injury signaling in lesioned nerve. Neuron 40:1095-1104. CrossRef Medline
29. Harris WA, Holt CE, Bonhoeffer F (1987) 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 101:123-133. Medline
30. Hu X, Ballo L, Pietila L, Viesselmann C, Ballweg J, Lumbard D, Stevenson M, Merriam E, Dent EW (2011) BDNF-induced increase of PSD-95 in dendritic spines requires dynamic microtubule invasions. J Neurosci 31: 15597-15603. CrossRef Medline
31. Jones SL, Selzer ME, Gallo G (2006) Developmental regulation of sensory axon regeneration in the absence of growth cones. J Neurobiol 66:1630-1645. CrossRef Medline
32. Jung H, Holt CE (2011) Local translation of mRNAs in neural development. Wiley Interdiscip Rev RNA 2:153-165. CrossRef Medline
33. Ketschek A, Gallo G (2010) Nerve growth factor induces axonal filopodia through localized microdomains of phosphoinositide 3-kinase activity that drive the formation of cytoskeletal precursors to filopodia. J Neurosci 30:12185-12197. CrossRef Medline
34. Kuhn TB, Brown MD, Bamburg JR (1998) Rac1-dependent actin filament organization in growth cones is necessary for beta1-integrin-mediated advance but not for growth on poly-D-lysine. J Neurobiol 37:524-540. CrossRef Medline
35. Lee SK, Hollenbeck PJ (2003) Organization and translation of mRNA in sympathetic axons. J Cell Sci 116:4467-4478. CrossRef Medline
36. Leemhuis J, Bouché E, Frotscher M, Henle F, Hein L, Herz J, Meyer DK, Pichler M, Roth G, Schwan C, Bock HH (2010) Reelin signals through apolipoprotein E receptor 2 and Cdc42 to increase growth cone motility and filopodia formation. J Neurosci 30:14759-14772. CrossRef Medline
37. Lelkes PI, Unsworth BR, Saporta S, Cameron DF, Gallo G (2006) Culture of neuroendocrine and neuronal cells for tissue engineering. In: Culture of cells for tissue engineering, Chap 14 (Vunjak-Novakovic G. and Freshney, R.I., eds). Wiley-Liss.
38. Li PP, Chen C, Lee CW, Madhavan R, Peng HB (2011) Axonal filopodial asymmetry induced by synaptic target. Mol Biol Cell 22:2480-2490. CrossRef Medline
39. Lin AC, Holt CE (2007) Local translation and directional steering in axons. EMBO J 26:3729-3736. CrossRef Medline
40. Loudon RP, Silver LD, Yee HF Jr, Gallo G (2006) RhoA-kinase and myosin II are required for the maintenance of growth cone polarity and guidance by nerve growth factor. J Neurobiol 66:847-867. CrossRef Medline
41. Marsick BM, San Miguel-Ruiz JE, Letourneau PC (2012) Activation of ezrin/ radixin/moesin mediates attractive growth cone guidance through regulation of growth cone actin and adhesion receptors. J Neurosci 32: 282-296, 2012 Jan 4. CrossRef Medline
42. Martelli AM, Evangelisti C, Chappell W, Abrams SL, Bäsecke J, Stivala F, Donia M, Fagone P, Nicoletti F, Libra M, Ruvolo V, Ruvolo P, Kempf CR, Steelman LS, McCubrey JA (2011) Targeting the translational apparatus to improve leukemia therapy: roles of the PI3K/PTEN/Akt/mTOR pathway. Leukemia 25:1064-1079. CrossRef Medline
43. Meberg PJ, Bamburg JR (2000) Increase in neurite outgrowth mediated by overexpression of actin depolymerizing factor. J Neurosci 20:2459-2469. Medline
44. Mendelson B, Koerber HR, Frank E (1992) Development of cutaneous and proprioceptive afferent projections in the chick spinal cord. Neurosci Lett 138:72-76. CrossRef Medline
45. Mingorance-Le Meur A, O'Connor TP (2009) Neurite consolidation is an active process requiring constant repression of protrusive activity. EMBO J 28:248-260. CrossRef Medline
46. Olink-Coux M, Hollenbeck PJ (1996) Localization and active transport of mRNA in axons of sympathetic neurons in culture. J Neurosci 16:1346-1358. Medline
47. Pan J, Kao YL, Joshi S, Jeetendran S, Dipette D, Singh US (2005) Activation of Rac1 by phosphatidylinositol 3-kinase in vivo: role in activation of mitogen-activated protein kinase (MAPK) pathways and retinoic acidinduced neuronal differentiation of SH-SY5Y cells. J Neurochem 93:571-583. CrossRef
48. Pan L, Zhang YQ, Woodruff E, Broadie K (2004) The Drosophila fragile X gene negatively regulates neuronal elaboration and synaptic differentiation. Curr Biol 14:1863-1870. CrossRef Medline
49. Park HS, Lee SH, Park D, Lee JS, Ryu SH, Lee WJ, Rhee SG, Bae YS (2004) Sequential activation of phosphatidylinositol 3-kinase, beta Pix, Rac1, and Nox1 in growth factor-induced production of H2O2. Mol Cell Biol 24:4384-4394. CrossRef Medline
50. Petruska JC, Mendell LM (2004) The many functions of nerve growth factor: multiple actions on nociceptors. Neurosci Lett 361:168-171. CrossRef Medline
51. Qian Y, Zhong X, Flynn DC, Zheng JZ, Qiao M, Wu C, Dedhar S, Shi X, Jiang BH (2005) ILK mediates actin filament rearrangements and cell migration and invasion through PI3K/Akt/Rac1 signaling. Oncogene 24:3154-3165. CrossRef Medline
52. Rajnicek AM, Foubister LE, McCaig CD (2006) Growth cone steering by a physiological electric field requires dynamic microtubules, microfilaments and Rac-mediated filopodial symmetry. J Cell Sci 119:1736-1745. CrossRef Medline
53. Ren G, Crampton MS, Yap AS (2009) Cortactin: coordinating adhesion and the actin cytoskeleton at cellular protrusions. Cell Motil Cytoskeleton 66:865-873. CrossRef Medline
54. Ridley AJ (2006) Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol 16:522-529. CrossRef Medline
55. Roche FK, Marsick BM, Letourneau PC (2009) Protein synthesis in distal axons is not required for growth cone responses to guidance cues. J Neurosci 29:638-652. CrossRef Medline
56. Spillane M, Ketschek A, Jones SL, Korobova F, Marsick B, Lanier L, Svitkina T, Gallo G (2011) The actin nucleating Arp2/3 complex contributes to the formation of axonal filopodia and branches through the regulation of actin patch precursors to filopodia. Dev Neurobiol 71:747-758. CrossRef Medline
57. Strasser GA, Rahim NA, VanderWaal KE, Gertler FB, Lanier LM (2004) Arp2/3 is a negative regulator of growth cone translocation. Neuron 43: 81-94. CrossRef Medline
58. Tang MC, Chan LC, Yeh YC, Chen CY, Chou TY, Wang WS, Su Y (2011) Thymosin beta 4 induces colon cancer cell migration and clinical metastasis via enhancing ILK/IQGAP1/Rac1 signal transduction pathway. Cancer Lett 308:162-171. CrossRef Medline
59. Teeter CM, Stevens CF (2011) A general principle of neural arbor branch density. Curr Biol 21:2105-2108. CrossRef Medline
60. Thies E, Davenport RW (2003) Independent roles of Rho-GTPases in growth cone and axonal behavior. J Neurobiol 54:358-369, 2003Feb 5. CrossRef Medline
61. Tucker B, Richards RI, Lardelli M (2006) Contribution of mGluR and Fmr1 functional pathways to neurite morphogenesis, craniofacial development and fragile X syndrome. Hum Mol Genet 15:3446-3458. CrossRef Medline
62. Verma P, Chierzi S, Codd AM, Campbell DS, Meyer RL, Holt CE, Fawcett JW (2005) Axonal protein synthesis and degradation are necessary for efficient growth cone regeneration. J Neurosci 25:331-342, 2005 Jan 12. CrossRef Medline
63. Vuppalanchi D, Coleman J, Yoo S, Merianda TT, Yadhati AG, Hossain J, Blesch A, Willis DE, Twiss JL (2010) Conserved 3'-untranslated region sequences direct subcellular localization of chaperone protein mRNAs in neurons. J Biol Chem 285:18025-18038. CrossRef Medline
64. Welshhans K, Bassell GJ (2011) Netrin-1-induced local β-actin synthesis and growth cone guidance requires zipcode binding protein 1. J Neurosci 31:9800-9813. CrossRef Medline
65. Williams EJ, Doherty P (1999) Evidence for and against a pivotal role of PI 3-kinase in a neuronal cell survival pathway. Mol Cell Neurosci 13:272-280. CrossRef Medline
66. Willis DE, van Niekerk EA, Sasaki Y, Mesngon M, Merianda TT, Williams GG, Kendall M, Smith DS, Bassell GJ, Twiss JL (2007) Extracellular stimuli specifically regulate localized levels of individual neuronal mRNAs. J Cell Biol 178:965-980. CrossRef Medline
67. Willis DE, Xu M, Donnelly CJ, Tep C, Kendall M, Erenstheyn M, English AW, Schanen NC, Kirn-Safran CB, Yoon SO, Bassell GJ, Twiss JL (2011) Axonal Localization of transgene mRNA in mature PNS and CNS neurons. J Neurosci 31:14481-14487. CrossRef Medline
68. Willis D, Li KW, Zheng JQ, Chang JH, Smit A, Kelly T, Merianda TT, Sylvester J, van Minnen J, Twiss JL (2005) Differential transport and local translation of cytoskeletal, injury-response, and neurodegeneration protein mRNAs in axons. J Neurosci 25:778-791. CrossRef
69. Yang C, Svitkina T (2011) Filopodia initiation: focus on the Arp2/3 complex and formins. Cell Adh Migr 5:402-408. CrossRef Medline
70. +-dependent growth cone guidance. Nat Neurosci 9:1265-1273. CrossRef Medline
71. Yoo S, van Niekerk EA, Merianda TT, Twiss JL (2010) Dynamics of axonal mRNA transport and implications for peripheral nerve regeneration. Exp Neurol 223:19-27. CrossRef Medline
72. Yudin D, Hanz S, Yoo S, Iavnilovitch E, Willis D, Gradus T, Vuppalanchi D, Segal-Ruder Y, Ben-Yaakov K, Hieda M, Yoneda Y, Twiss JL, Fainzilber M (2008) Localized regulation of axonal RanGTPase controls retrograde injury signaling in peripheral nerve. Neuron 59:241-252. CrossRef Medline
73. Zhang HL, Eom T, Oleynikov Y, Shenoy SM, Liebelt DA, Dictenberg JB, Singer RH, Bassell GJ (2001) Neurotrophin-induced transport of a betaactin mRNP complex increases beta-actin levels and stimulates growth cone motility. Neuron 31:261-275. CrossRef Medline
74. Zheng JQ, Kelly TK, Chang B, Ryazantsev S, Rajasekaran AK, Martin KC, Twiss JL (2001) A functional role for intra-axonal protein synthesis during axonal regeneration from adult sensory neurons. J Neurosci 21:9291-9303. Medline
75. Zivraj KH, Tung YC, Piper M, Gumy L, Fawcett JW, Yeo GS, Holt CE (2010) Subcellular profiling reveals distinct and developmentally regulated repertoire of growth cone mRNAs. J Neurosci 30:15464-15478. CrossRef Medline