The cytoskeletal and signaling mechanisms of axon collateral branching

Developmental Neurobiology

Volumn 71, Issue 3, 2011, Pages 201-220

  Gallo, Gianluca ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Actin; Axon sprouting; Disease; Injury; Interstitial branch

Indexed keywords

ACTIN; CYCLIC NUCLEOTIDE; PHOSPHATIDYLINOSITIDE; RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

CALCIUM SIGNALING; CYTOSKELETON; FILOPODIUM; HUMAN; LAMELLIPODIUM; NERVE CELL NETWORK; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; AXONS; CYTOSKELETON; GROWTH CONES; HUMANS; SIGNAL TRANSDUCTION;

EID: 79551693366     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.20852     Document Type: Review

References (134)

1. Ahmad FJ, Echeverri CJ, Vallee RB, Baas PW. 1998. Cytoplasmic dynein and dynactin are required for the transport of microtubules into the axon. J Cell Biol 140: 391-401.
2. Ahmad FJ, He Y, Myers KA, Hasaka TP, Francis F, Black MM, Baas PW. 2006. Effects of dynactin disruption and dynein depletion on axonal microtubules. Traffic 7: 524-537.
3. 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.
4. Albertinazzi C, Gilardelli D, Paris S, Longhi R, de Curtis I. 1998. Overexpression of a neural-specific rho family GTPase, cRac1B, selectively induces enhanced neuritogenesis and neurite branching in primary neurons. J Cell Biol 142: 815-825.
5. Andersen R, Li Y, Resseguie M, Brenman JE. 2005. Calcium/calmodulin-dependent protein kinase II alters structural plasticity and cytoskeletal dynamics in Drosophila. J Neurosci 25: 8878-8888.
6. Applewhite DA, Barzik M, Kojima S, Svitkina TM, Gertler FB, Borisy GG. 2007. Ena/VASP proteins have an anti-capping independent function in filopodia formation. Mol Biol Cell 18: 2579-2591.
7. Bastmeyer M, O'Leary DD. 1996. Dynamics of target recognition by interstitial axon branching along developing cortical axons. J Neurosci 16: 1450-1459.
8. Bohil AB, Robertson BW, Cheney RE. 2006. Myosin-X is a molecular motor that functions in filopodia formation. Proc Natl Acad Sci USA 103: 12411-12416.
9. Bouquet C, Soares S, von Boxberg Y, Ravaille-Veron M, Propst F, Nothias F. 2004. Microtubule-associated protein 1B controls directionality of growth cone migration and axonal branching in regeneration of adult dorsal root ganglia neurons. J Neurosci 24: 7204-7213.
10. Chada SR, Hollenbeck PJ. 2004. Nerve growth factor signaling regulates motility and docking of axonal mitochondria. Curr Biol 14: 1272-1276.
11. Chihara T, Luginbuhl D, Luo L. 2007. Cytoplasmic and mitochondrial protein translation in axonal and dendritic terminal arborization. Nat Neurosci 10: 828-837.
12. Cohen-Cory S, Kidane AH, Shirkey NJ, Marshak S. 2010. Brain-derived neurotrophic factor and the development of structural neuronal connectivity. Dev Neurobiol 70: 271-288.
13. Davenport RW, Thies E, Cohen ML. 1999. Neuronal growth cone collapse triggers lateral extensions along trailing axons. Nat Neurosci 2: 254-259.
14. Davis BM, Frank E, Johnson FA, Scott SA. 1989. Development of central projections of lumbosacral sensory neurons in the chick. J Comp Neurol 279: 556-566.
15. Dehmelt L, Smart FM, Ozer RS, Halpain S. 2003. The role of microtubule-associated protein 2c in the reorganization of microtubules and lamellipodia during neurite initiation. J Neurosci 23: 9479-9490.
16. Dent EW, Barnes AM, Tang F, Kalil K. 2004. Netrin-1 and semaphorin 3A promote or inhibit cortical axon branching, respectively, by reorganization of the cytoskeleton. J Neurosci 24: 3002-3012.
17. Dent EW, Callaway JL, Szebenyi G, Baas PW, Kalil K. 1999. Reorganization and movement of microtubules in axonal growth cones and developing interstitial branches. J Neurosci 19: 8894-8908.
18. Dent EW, Gertler FB. 2003. Cytoskeletal dynamics and transport in growth cone motility and axon guidance. Neuron 40: 209-227.
19. Dent EW, Kalil K. 2001. Axon branching requires interactions between dynamic microtubules and actin filaments. J Neurosci 21: 9757-9769.
20. Dent EW, Kwiatkowski AV, Mebane LM, Philippar U, Barzik M, Rubinson DA, Gupton S, et al. 2007. Filopodia are required for cortical neurite initiation. Nat Cell Biol 9: 1347-1359.
21. Dickson BJ. 2001. Rho GTPases in growth cone guidance. Curr Opin Neurobiol 11: 103-110.
22. 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.
23. Dwivedy A, Gertler FB, Miller J, Holt CE, Lebrand C. 2007. Ena/VASP function in retinal axons is required for terminal arborization but not pathway navigation. Development 134: 2137-2146.
24. Faix J, Breitsprecher D, Stradal TE, Rottner K.Filopodia: 2009. Complex models for simple rods. Int J Biochem Cell Biol 41: 1656-1664.
25. Fath T, Agnes Chan YK, Vrhovski B, Clarke H, Curthoys N, Hook J, Lemckert F, et al. 2010. New aspects of tropomyosin-regulated neuritogenesis revealed by the deletion of Tm5NM1 and 2. Eur J Cell Biol 89: 489-498.
26. Feany MB, Buckley KM. 1993. The synaptic vesicle protein synaptotagmin promotes formation of filopodia in fibroblasts. Nature 364: 537-540.
27. Flynn KC, Pak CW, Shaw AE, Bradke F, Bamburg JR. 2009. Growth cone-like waves transport actin and promote axonogenesis and neurite branching. Dev Neurobiol 69: 761-779.
28. Francisco H, Kollins K, Varghis N, Vocadlo D, Vosseller K, Gallo G. 2009. O-GLcNAc post-translational modifications regulate the entry of neurons into an axon branching program. Dev Neurobiol 69: 162-173.
29. Francisco H, Yellen BB, Halverson DS, Friedman G, Gallo G. 2007. Regulation of axon guidance and extension by three-dimensional constraints. Biomaterials 28: 3398-3407.
30. Gallo G, Letourneau PC. 1998. Localized sources of neurotrophins initiate axon collateral sprouting. J Neurosci 18: 5403-5414.
31. 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.
32. 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.
33. Giuditta A, Kaplan BB, van Minnen J, Alvarez J, Koenig E. 2002. Axonal and presynaptic protein synthesis: New insights into the biology of the neuron. Trends Neurosci 25: 400-404.
34. Goldberg DJ, Schacher S. 1987. Differential growth of the branches of a regenerating bifurcate axon is associated with differential axonal transport of organelles. Dev Biol 124: 35-40.
35. 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. JNeurosci Res 87: 3033-3042.
36. Hagg T. 2006. Collateral sprouting as a target for improved function after spinal cord injury. J Neurotrauma 23: 281-294.
37. Halloran MC, Kalil K. 1994. Dynamic behaviors of growth cones extending in the corpus callosum of living cortical brain slices observed with video microscopy. J Neurosci 14: 2161-2177.
38. Han J, Han L, Tiwari P, Wen Z, Zheng JQ. 2007. Spatial targeting of type II protein kinase A to filopodia mediates the regulation of growth cone guidance by cAMP. J Cell Biol 176: 101-111.
39. 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.
40. Heffner CD, Lumsden AG, O'Leary DD. 1990. Target control of collateral extension and directional axon growth in the mammalian brain. Science 247: 217-220.
41. Hernández-Deviez DJ, Roth MG, Casanova JE, Wilson JM. 2004. ARNO and ARF6 regulate axonal elongation and branching through downstream activation of phosphatidylinositol 4-phosphate 5-kinase alpha. Mol Biol Cell 15: 111-120.
42. Homma N, Takei Y, Tanaka Y, Nakata T, Terada S, Kikkawa M, Noda Y, et al. 2003. Kinesin superfamily protein 2A (KIF2A) functions in suppression of collateral branch extension. Cell 114: 229-239.
43. Hu X, Viesselmann C, Nam S, Merriam E, Dent EW. 2008. Activity-dependent dynamic microtubule invasion of dendritic spines. J Neurosci 28: 13094-13105.
44. Hua JY, Smear MC, Baier H, Smith SJ. 2005. Regulation of axon growth in vivo by activity-based competition. Nature 434: 1022-1026.
45. Hwang YS, Luo T, Xu Y, Sargent TD. 2009. Myosin-X is required for cranial neural crest cell migration in Xenopus laevis. Dev Dyn 238: 2522-2529.
46. Jiménez-Mateos EM, González-Billault C, Dawson HN, Vitek MP, Avila J. 2006. Role of MAP1B in axonal retrograde transport of mitochondria. Biochem J 397: 53-59.
47. Jones DM, Tucker BA, Rahimtula M, Mearow KM. 2003. The synergistic effects of NGF and IGF-1 on neurite growth in adult sensory neurons: Convergence on the PI3-kinase signaling pathway. J Neurochem 86: 1116-1128.
48. Kalil K, Szebenyi G, Dent EW. 2000. Common mechanisms underlying growth cone guidance and axon branching. J Neurobiol 44: 145-158.
49. Ketschek AR, Gallo G. 2010. NGF-induces Axonal Filopodia through Localized Microdomains of Phosphoinositide 3-kinase (PI3K) Activity that Drive the Formation of Cytoskeletal Precursors to Filopodia. J Neurosci 30: 12185-12197.
50. Kim MS, Rådinger M, Gilfillan AM. 2008. The multiple roles of phosphoinositide 3-kinase in mast cell biology. Trends Immunol 29: 493-501.
51. Knobel KM, Davis WS, Jorgensen EM, Bastiani MJ. 2001. UNC-119 suppresses axon branching in C. elegans. Development 128: 4079-4092.
52. Knobel KM, Jorgensen EM, Bastiani MJ. 1999. Growth cones stall and collapse during axon outgrowth in Caenorhabditis elegans. Development 126: 4489-4498.
53. Kollins KM, Hu J, Bridgman PC, Huang YQ, Gallo G. 2009. Myosin-II negatively regulates minor process extension and the temporal development of neuronal polarity. Dev Neurobiol 69: 279-298.
54. Korobova F, Svitkina T. 2008. Arp2/3 complex is important for filopodia formation, growth cone motility, and neuritogenesis in neuronal cells. Mol Biol Cell 19: 1561-1574.
55. Korobova F, Svitkina T. 2010. Molecular architecture of synaptic actin cytoskeleton in hippocampal neurons reveals a mechanism of dendritic spine morphogenesis. Mol Biol Cell 21(1): 165-176.
56. Kwon CH, Luikart BW, Powell CM, Zhou J, Matheny SA, Zhang W, Li Y, et al. 2006. Pten regulates neuronal arborization and social interaction in mice. Neuron 50: 377-388.
57. Larner AJ. 1995a. Axonal sprouting and synaptogenesis in temporal lobe epilepsy: Possible pathogenetic and therapeutic roles of neurite growth inhibitory factors. Seizure 4: 249-258.
58. Larner AJ. 1995b. The cortical neuritic dystrophy of Alzheimer's disease: Nature, significance, and possible pathogenesis. Dementia 6: 218-224.
59. Larsson C. 2006. Protein kinase C and the regulation of the actin cytoskeleton. Cell Signal 18: 276-284.
60. Lau PM, Zucker RS, Bentley D. 1999. Induction of filopodia by direct local elevation of intracellular calcium ion concentration. J Cell Biol 145: 1265-1275.
61. Lebrand C, Dent EW, Strasser GA, Lanier LM, Krause M, Svitkina TM, Borisy GG, et al. 2004. Critical role of Ena/VASP proteins for filopodia formation in neurons and in function downstream of netrin-1. Neuron 42: 37-49.
62. Lee SK, Hollenbeck PJ. 2003. Organization and translation of mRNA in sympathetic axons. J Cell Sci 116: 4467-4478.
63. Letourneau PC. 2009. Actin in axons: Stable scaffolds and dynamic filaments. Results Probl Cell Differ 48: 65-90.
64. Letourneau PC, Shattuck TA, Ressler AH. 1986. Branching of sensory and sympathetic neurites in vitro is inhibited by treatment with taxol. J Neurosci 6: 1912-1917.
65. Leu B, Koch E, Schmidt JT. 2010. GAP43 phosphorylation is critical for growth and branching of retinotectal arbors in zebrafish. Dev Neurobiol 70:897-911.
66. Liu K, Lu Y, Lee JK, Samara R, Willenberg R, Sears-Kraxberger I, Tedeschi A, et al. 2010. PTEN deletion enhances the regenerative ability of adult corticospinal neurons. Nat Neurosci 13: 1075-1081.
67. Liu WS, Heckman CA. 1998. The sevenfold way of PKC regulation. Cell Signal 10: 529-542.
68. Loudon RP, Silver LD, Yee HFJr, 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.
69. Lundquist EA. 2009. The finer points of filopodia. PLoS Biol 7: e1000142.
70. Ma L, Tessier-Lavigne M. 2007. Dual branch-promoting and branch-repelling actions of Slit/Robo signaling on peripheral and central branches of developing sensory axons. J Neurosci 27: 6843-6851.
71. Manitt C, Nikolakopoulou AM, Almario DR, Nguyen SA, Cohen-Cory S. 2009. Netrin participates in the development of retinotectal synaptic connectivity by modulating axon arborization and synapse formation in the developing brain. J Neurosci 29: 11065-11077.
72. Markus A, Zhong J, Snider WD. 2002. Raf and Akt mediate distinct aspects of sensory axon growth. Neuron 35: 65-76.
73. Mattila PK, Lappalainen P. 2008. Filopodia: Molecular architecture and cellular functions. Nat Rev Mol Cell Biol 9: 446-454.
74. Matusek T, Gombos R, Szécsényi A, Sánchez-Soriano N, Czibula A, Pataki C, Gedai A, et al. 2008. Formin proteins of the DAAM subfamily play a role during axon growth. J Neurosci 28: 13310-13319.
75. Menna E, Disanza A, Cagnoli C, Schenk U, Gelsomino G, Frittoli E, Hertzog M, et al. 2009. Eps8 regulates axonal filopodia in hippocampal neurons in response to brain-derived neurotrophic factor (BDNF). PLoS Biol 7: e1000138.
76. 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.
77. Moon MS, Gomez TM. 2010. Balanced Vav2 GEF activity regulates neurite outgrowth and branching in vitro and in vivo. Mol Cell Neurosci 44: 118-128.
78. Murphey RK, Caruccio PC, Getzinger M, Westgate PJ, Phillis RW. 1999. Dynein-dynactin function and sensory axon growth during Drosophila metamorphosis: A role for retrograde motors. Dev Biol 209: 86-97.
79. Myers KA, Baas PW. 2007. Kinesin-5 regulates the growth of the axon by acting as a brake on its microtubule array. J Cell Biol 178: 1081-1091.
80. Nakata T, Terada S, Hirokawa N. 1998. Visualization of the dynamics of synaptic vesicle and plasma membrane proteins in living axons. J Cell Biol 140: 659-674.
81. Ng J, Nardine T, Harms M, Tzu J, Goldstein A, Sun Y, Dietzl G, et al. 2002. Rac GTPases control axon growth, guidance and branching. Nature 416: 442-447.
82. O'Leary DD, Bicknese AR, De Carlos JA, Heffner CD, Koester SE, Kutka LJ, Terashima T. 1990. Target selection by cortical axons: Alternative mechanisms to establish axonal connections in the developing brain. Cold Spring Harb Symp Quant Biol 55: 453-468.
83. O'Leary DD, Stanfield BB, Cowan WM. 1981. Evidence that the early postnatal restriction of the cells of origin of the callosal projection is due to the elimination of axonal collaterals rather than to the death of neurons. Brain Res 227: 607-617.
84. Oakley RA, Tosney KW. 1993. J Neurosci Contact-mediated mechanisms of motor axon segmentation 13: 3773-3792.
85. Ohnami S, Endo M, Hirai S, Uesaka N, Hatanaka Y, Yamashita T, Yamamoto N. 2008. Role of RhoA in activity-dependent cortical axon branching. J Neurosci 28: 9117-9121.
86. Olink-Coux M, Hollenbeck PJ. 1996. Localization and active transport of mRNA in axons of sympathetic neurons in culture. J Neurosci 16: 1346-1358.
87. Orlova I, Silver L, Gallo G. 2007. Regulation of actomyosin contractility by PI3K in sensory axons. Dev Neurobiol 67: 1843-1851.
88. Overly CC, Hollenbeck PJ. 1996. Dynamic organization of endocytic pathways in axons of cultured sympathetic neurons. J Neurosci 16: 6056-6064.
89. Patel TD, Jackman A, Rice FL, Kucera J, Snider WD. 2000. Development of sensory neurons in the absence of NGF/TrkA signaling in vivo. Neuron 25: 345-357.
90. Petruska JC, Mendell LM. 2004. The many functions of nerve growth factor: Multiple actions on nociceptors. Neurosci Lett 361: 168-171.
91. Portera-Cailliau C, Weimer RM, De Paola V, Caroni P, Svoboda K. 2005. Diverse modes of axon elaboration in the developing neocortex. PLo S Biol 3: e272.
92. Qiang L, Yu W, Andreadis A, Luo M, Baas PW. 2006. Tau protects microtubules in the axon from severing by katanin. J Neurosci 26: 3120-3129.
93. Qiang L, Yu W, Liu M, Solowska JM, Baas PW. 2010. Basic fibroblast growth factor elicits formation of interstitial axonal branches via enhanced severing of microtubules. Mol Biol Cell 21: 334-344.
94. Reed NA, Cai D, Blasius TL, Jih GT, Meyhofer E, Gaertig J, Verhey KJ. 2006. Microtubule acetylation promotes kinesin-1 binding and transport. Curr Biol 16: 2166-2172.
95. Rico B, Beggs HE, Schahin-Reed D, Kimes N, Schmidt A, Reichardt LF. 2004. Control of axonal branching and synapse formation by focal adhesion kinase. Nat Neurosci 7: 1059-1069.
96. Ruthel G, Banker G. 1998. Actin-dependent anterograde movement of growth-cone-like structures along growing hippocampal axons: A novel form of axonal transport? Cell Motil Cytoskeleton 40: 160-173.
97. Ruthel G, Banker G. 1999. Role of moving growth cone-like "wave" structures in the outgrowth of cultured hippocampal axons and dendrites. J Neurobiol 39: 97-106.
98. Ruthel G, Hollenbeck PJ. 2003. Response of mitochondrial traffic to axon determination and differential branch growth. J Neurosci 23: 8618-8624.
99. Sato M, Lopez-Mascaraque L, Heffner CD, O'Leary DD. 1994. Action of a diffusible target-derived chemoattractant on cortical axon branch induction and directed growth. Neuron 13: 791-803.
100. Sato T, Sato-Harada R, Takano M, Kato S, Saburi S, Harada A. 2002. Localization of cAMP-dependent protein kinase in the actin and microtubule cytoskeletons in mouse hippocampal neurons. Neurosci Lett 325: 83-86.
101. Schmidt H, Stonkute A, Jüttner R, Schäffer S, Buttgereit J, Feil R, Hofmann F, et al. 2007. The receptor guanylyl cyclase Npr2 is essential for sensory axon bifurcation within the spinal cord. J Cell Biol 179: 331-340.
102. Schmidt JT, Fleming MR, Leu B. 2004. Presynaptic protein kinase C controls maturation and branch dynamics of developing retinotectal arbors: Possible role in activity-driven sharpening. J Neurobiol 58: 328-340.
103. Sirotkin V, Berro J, Macmillan K, Zhao L, Pollard TD. 2010. Quantitative Analysis of the Mechanism of Endocytic Actin Patch Assembly and Disassembly in Fission Yeast. Mol Biol Cell 21:2894-2904.
104. Smith A, Gervasi C, Szaro BG. 2006. Neurofilament content is correlated with branch length in developing collateral branches of Xenopus spinal cord neurons. Neurosci Lett 403: 283-287.
105. Snider J, Pillai A, Stevens CF. 2010. A universal property of axonal and dendritic arbors. Neuron 66: 45-56.
106. Song HJ, Ming GL, Poo MM. 1997. cAMP-induced switching in turning direction of nerve growth cones. Nature 388: 275-279.
107. Sousa AD, Berg JS, Robertson BW, Meeker RB, Cheney RE. 2006. Myo10 in brain: Developmental regulation, identification of a headless isoform and dynamics in neurons. J Cell Sci 119: 184-194.
108. Stanfield BB, O'Leary DD, Fricks C. 1982. Selective collateral elimination in early postnatal development restricts cortical distribution of rat pyramidal tract neurones. Nature 298: 371-373.
109. Steketee M, Balazovich K, Tosney KW. 2001. Filopodial initiation and a novel filament-organizing center, the focal ring. Mol Biol Cell 12: 2378-2395.
110. 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.
111. Struckhoff EC, Lundquist EA. 2003. The actin-binding protein UNC-115 is an effector of Rac signaling during axon pathfinding in C. elegans. Development 130: 693-704.
112. Svitkina T. 2007. Electron microscopic analysis of the leading edge in migrating cells. Methods Cell Biol 79: 295-319.
113. Svitkina TM, Bulanova EA, Chaga OY, Vignjevic DM, Kojima S, Vasiliev JM, Borisy GG. 2003. Mechanism of filopodia initiation by reorganization of a dendritic network. J Cell Biol 160: 409-421.
114. Szaro BG, Strong MJ. 2010. Post-transcriptional control of neurofilaments: New roles in development, regeneration and neurodegenerative disease. Trends Neurosci 33: 27-37.
115. Szebenyi G, Callaway JL, Dent EW, Kalil K. 1998. Interstitial branches develop from active regions of the axon demarcated by the primary growth cone during pausing behaviors. J Neurosci 18: 7930-7940.
116. Tang F, Dent EW, Kalil K. 2003. Spontaneous calcium transients in developing cortical neurons regulate axon outgrowth. J Neurosci 23: 927-936.
117. Tang F, Kalil K. 2005. Netrin-1 induces axon branching in developing cortical neurons by frequency-dependent calcium signaling pathways. J Neurosci 25: 6702-6715.
118. Tint I, Jean D, Baas PW, Black MM. 2009. Doublecortin associates with microtubules preferentially in regions of the axon displaying actin-rich protrusive structures. J Neurosci 29: 10995-11010.
119. Tsukada M, Prokscha A, Ungewickell E, Eichele G. 2005. Doublecortin association with actin filaments is regulated by neurabin II. J Biol Chem 280: 11361-11368.
120. Uesaka N, Ruthazer ES, Yamamoto N. 2006. The role of neural activity in cortical axon branching. Neuroscientist 12: 102-106.
121. Undamatla J, Szaro BG. 2001. Differential expression and localization of neuronal intermediate filament proteins within newly developing neurites in dissociated cultures of Xenopus laevis embryonic spinal cord. Cell Motil Cytoskeleton 49: 16-32.
122. Verburg J, Hollenbeck PJ. 2008. Mitochondrial membrane potential in axons increases with local nerve growth factor or semaphorin signaling. J Neurosci 28: 8306-8315.
123. Vuppalanchi D, Willis DE, Twiss JL. 2009. Regulation of mRNA transport and translation in axons. Results Probl Cell Differ 48: 193-224.
124. Walker KL, Yoo HK, Undamatla J, Szaro BG. 2001. Loss of neurofilaments alters axonal growth dynamics. J Neurosci 21: 9655-9666.
125. Wang W, van Niekerk E, Willis DE, Twiss JL. 2007. RNA transport and localized protein synthesis in neurological disorders and neural repair. Dev Neurobiol 67: 1166-1182.
126. Watanabe TM, Tokuo H, Gonda K, Higuchi H, Ikebe M. 2010. Myosin-X induces filopodia by multiple elongation mechanism. J Biol Chem 285: 19605-19614.
127. Wessells NK, Nuttall RP. 1978. Normal branching, induced branching, and steering of cultured parasympathetic motor neurons. Exp Cell Res 115: 111-122.
128. Willis DE, van Niekerk EA, Sasaki Y, Mesngon M, Merianda TT, Williams GG, Kendall M, et al. 2007. Extracellular stimuli specifically regulate localized levels of individual neuronal mRNAs. J Cell Biol 178: 965-980.
129. Withers GS, James CD, Kingman CE, Craighead HG, Banker GA. 2006. Effects of substrate geometry on growth cone behavior and axon branching. J Neurobiol 66: 1183-1194.
130. Yang C, Hoelzle M, Disanza A, Scita G, Svitkina T. 2009. Coordination of membrane and actin cytoskeleton dynamics during filopodia protrusion. PLo S One 4: e5678.
131. Yu W, Ahmad FJ, Baas PW. 1994. Microtubule fragmentation and partitioning in the axon during collateral branch formation. J Neurosci 14: 5872-5884.
132. Yu W, Qiang L, Solowska JM, Karabay A, Korulu S, Baas PW. 2008. The microtubule-severing proteins spastin and katanin participate differently in the formation of axonal branches. Mol Biol Cell 19: 1485-1498.
133. Zhou FQ, Snider WD. 2006. Intracellular control of developmental and regenerative axon growth. Philos Trans R Soc Lond B Biol Sci 361: 1575-1592.
134. Zhu XJ, Wang CZ, Dai PG, Xie Y, Song NN, Liu Y, Du QS, et al. 2007. Myosin X regulates netrin receptors and functions in axonal path-finding. Nat Cell Biol 9: 184-192.