Signalling mechanisms regulating axonal branching in vivo

BioEssays

Volumn 32, Issue 11, 2010, Pages 977-985

  Schmidt, Hannes ^a   Rathjen, Fritz G ^a  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

Axonal branching; Axonal pathfinding; Brain derived neurotrophic factor; Cyclic guanosine monophosphate signalling; Retinotectal system

Indexed keywords

ACTIN; BRAIN DERIVED NEUROTROPHIC FACTOR; EPHRIN A1; NATRIURETIC PEPTIDE TYPE C; PROTEASOME; TUBULIN; UBIQUITIN;

CYTOSKELETON; HUMAN; IN VIVO STUDY; MICROTUBULE; NERVE CELL; NERVE FIBER GROWTH; POLYMERIZATION; RETINA GANGLION CELL; REVIEW; SIGNAL TRANSDUCTION; SPINAL CORD; SPINAL GANGLION; TOPOGRAPHY; TROPHIC CASCADE;

ANIMALS; AXONS; GROWTH CONES; HUMANS; MICROTUBULES; NERVE NET; SIGNAL TRANSDUCTION; VISUAL PATHWAYS;

EID: 77958180013     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201000054     Document Type: Review

References (101)

1. Arimura N, Kaibuchi K., 2007., Neuronal polarity: from extracellular signals to intracellular mechanisms., Nat Rev Neurosci, 8: 194-205.
2. Tessier-Lavigne M, Goodman CS., 1996., The molecular biology of axon guidance., Science, 274: 1123-33.
3. Nikolaev A, McLaughlin T, O'Leary DD, Tessier-Lavigne M., 2009., APP binds DR6 to trigger axon pruning and neuron death via distinct caspases., Nature, 457: 981-9.
4. Tang F, Kalil K., 2005., Netrin-1 induces axon branching in developing cortical neurons by frequency-dependent calcium signaling pathways., J Neurosci, 25: 6702-15.
5. Dent EW, Barnes AM, Tang F, Kalil K., 2004., Netrin-1 and semaphorin 3A promote or inhibit cortical axon branching, respectively, by reorganisation of the cytoskeleton., J Neurosci, 24: 3002-12.
6. Wang KH, Brose K, Arnott D, Kidd T, et al.1999., Biochemical purification of a mammalian Slit protein as a positive regulator of sensory axon elongation and branching., Cell, 96: 771-84.
7. Cohen-Cory S, Fraser SE., 1995., Effects of brain-derived neurotrophic factor on optic axon branching and remodelling in vivo, Nature, 378: 192-6.
8. Szebenyi G, Dent EW, Callaway JL, Seys C, et al. 2001., Fibroblast growth factor-2 promotes axon branching of cortical neurons by influencing morphology and behaviour of the primary growth cone., J Neurosci, 21: 3932-41.
9. Tang F, Dent EW, Kalil K., 2003., Spontaneous calcium transients in developing cortical neurons regulate axon outgrowth., J Neurosci, 23: 927-36.
10. Hutchins BI, Kalil K., 2008., Differential outgrowth of axons and their branches is regulated by localised calcium transients., J Neurosci, 28: 143-53.
11. Ruthazer ES, Akerman CJ, Cline HT., 2003., Control of axon branch dynamics by correlated activity in vivo, Science, 301: 66-70.
12. Cantallops I, Haas K, Cline HT., 2000., Postsynaptic CPG15 promotes synaptic maturation and presynaptic axon arbor elaboration in vivo, Nat Neurosci, 3: 1004-11.
13. Purro SA, Ciani L, Hoyos-Flight M, Stamatakou E, et al.2008., Wnt regulates axon behaviour through changes in microtubule growth directionality: a new role for adenomatous polyposis coli., J Neurosci, 28: 8644-54.
14. Gong Q, Chen H, Farbman AI., 2009., Olfactory sensory axon growth and branching is influenced by sonic hedgehog., Dev Dyn, 238: 1768-76.
15. Salinas PC, Zou Y., 2008., Wnt signalling in neural circuit assembly., Annu Rev Neurosci, 31: 339-58.
16. Bodmer D, Levine-Wilkinson S, Richmond A, Hirsh S, et al.2009., Wnt5a mediates nerve growth factor-dependent axonal branching and growth in developing sympathetic neurons., J Neurosci, 29: 7569-81.
17. Wickramasinghe SR, Alvania RS, Ramanan N, Wood JN, et al.2008., Serum response factor mediates NGF-dependent target innervation by embryonic DRG sensory neurons., Neuron, 58: 532-45.
18. Barnes SH, Price SR, Wentzel C, Guthrie SC., 2010., Cadherin-7 and cadherin-6B differentially regulate the growth, branching and guidance of cranial motor axons., Development, 137: 805-14.
19. Soussi-Yanicostas N, de Castro F, Julliard AK, Perfettini I, et al.2002., Anosmin-1, defective in the X-linked form of Kallmann syndrome, promotes axonal branch formation from olfactory bulb output neurons., Cell, 109: 217-28.
20. Gianola S, de Castro F, Rossi F., 2009., Anosmin-1 stimulates outgrowth and branching of developing Purkinje axons., Neuroscience, 158: 570-84.
21. Parrish JZ, Emoto K, Kim MD, Jan YN., 2007., Mechanisms that regulate establishment, maintenance, and remodelling of dendritic fields., Annu Rev Neurosci, 30: 399-423.
22. Jan YN, Jan LY., 2010., Branching out: mechanisms of dendritic arborisation., Nat Rev Neurosci, 11: 316-28.
23. Acebes A, Ferrus A., 2000., Cellular and molecular features of axon collaterals and dendrites., Trends Neurosci, 23: 557-65.
24. O'Leary DD, Terashima T., 1988., Cortical axons branch to multiple subcortical targets by interstitial axon budding: implications for target recognition and 'waiting periods'., Neuron, 1: 901-10.
25. Portera-Cailliau C, Weimer RM, De Paola V, Caroni P, et al.2005., Diverse modes of axon elaboration in the developing neocortex., PLoS Biol, 3: e272.
26. Schmidt H, Stonkute A, Juttner R, Schaffer S, et al.2007., The receptor guanylyl cyclase Npr2 is essential for sensory axon bifurcation within the spinal cord., J Cell Biol, 179: 331-40.
27. 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 behaviours., J Neurosci, 18: 7930-40.
28. Altman J., 1975., Postnatal development of the cerebellar cortex in the rat. IV. Spatial organisation of bipolar cells, parallel fibres and glial palisades., J Comp Neurol, 163: 427-47.
29. Matsuda S, Baluk P, Shimizu D, Fujiwara T., 1996., Dorsal root ganglion neuron development in chick and rat., Anat Embryol (Berl), 193: 475-80.
30. Ozaki S, Snider WD., 1997., Initial trajectories of sensory axons toward laminar targets in the developing mouse spinal cord., J Comp Neurol, 380: 215-29.
31. Mirnics K, Koerber HR., 1995., Prenatal development of rat primary afferent fibers: II. Central projections., J Comp Neurol, 355: 601-14.
32. 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: 6843-51.
33. Schmidt H, Werner M, Heppenstall PA, Henning M, et al.2002., cGMP-mediated signalling via cGKIalpha is required for the guidance and connectivity of sensory axons., J Cell Biol, 159: 489-98.
34. Schmidt H, Stonkute A, Juttner R, Koesling D, et al.2009., C-type natriuretic peptide (CNP) is a bifurcation factor for sensory neurons., Proc Natl Acad Sci USA, 106: 16847-52.
35. Zhao Z, Ma L., 2009., Regulation of axonal development by natriuretic peptide hormones., Proc Natl Acad Sci USA, 106: 18016-21.
36. Zhao Z, Wang Z, Gu Y, Feil R, et al.2009., Regulate axon branching by the cyclic GMP pathway via inhibition of glycogen synthase kinase 3 in dorsal root ganglion sensory neurons., J Neurosci, 29: 1350-60.
37. Zhou FQ, Snider WD., 2005., Cell biology. GSK-3beta and microtubule assembly in axons., Science, 308: 211-4.
38. McManus EJ, Sakamoto K, Armit LJ, Ronaldson L, et al.2005., Role that phosphorylation of GSK3 plays in insulin and Wnt signalling defined by knockin analysis., EMBO J, 24: 1571-83.
39. Gartner A, Huang X, Hall A., 2006., Neuronal polarity is regulated by glycogen synthase kinase-3 (GSK-3beta) independently of Akt/PKB serine phosphorylation., J Cell Sci, 119: 3927-34.
40. Huang EJ, Li H, Tang AA, Wiggins AK, et al.2005., Targeted deletion of numb and numblike in sensory neurons reveals their essential functions in axon arborisation., Genes Dev, 19: 138-51.
41. Krylova O, Herreros J, Cleverley KE, Ehler E, et al.2002., WNT-3, expressed by motoneurons, regulates terminal arborisation of neurotrophin-3-responsive spinal sensory neurons., Neuron, 35: 1043-56.
42. O'Leary DD, Heffner CD, Kutka L, Lopez-Mascaraque L, et al.1991., A target-derived chemoattractant controls the development of the corticopontine projection by a novel mechanism of axon targeting., Development, 2 (Suppl): 123-30.
43. Bastmeyer M, O'Leary DD., 1996., Dynamics of target recognition by interstitial axon branching along developing cortical axons., J Neurosci, 16: 1450-9.
44. Zhu Y, Matsumoto T, Mikami S, Nagasawa T, et al.2009., SDF1/CXCR4 signalling regulates two distinct processes of precerebellar neuronal migration and its depletion leads to abnormal pontine nuclei formation., Development, 136: 1919-28.
45. Heffner CD, Lumsden AG, O'Leary DD., 1990., Target control of collateral extension and directional axon growth in the mammalian brain., Science, 247: 217-20.
46. McLaughlin T, O'Leary DD., 2005., Molecular gradients and development of retinotopic maps., Annu Rev Neurosci, 28: 327-55.
47. Stuermer CA., 1988., Retinotopic organisation of the developing retinotectal projection in the zebrafish embryo., J Neurosci, 8: 4513-30.
48. Manitt C, Nikolakopoulou AM, Almario DR, Nguyen SA, et al.2009., Netrin participates in the development of retinotectal synaptic connectivity by modulating axon arborisation and synapse formation in the developing brain., J Neurosci, 29: 11065-77.
49. Marshak S, Nikolakopoulou AM, Dirks R, Martens GJ, et al.2007., Cell-autonomous TrkB signaling in presynaptic retinal ganglion cells mediates axon arbor growth and synapse maturation during the establishment of retinotectal synaptic connectivity., J Neurosci, 27: 2444-56.
50. Campbell DS, Stringham SA, Timm A, Xiao T, et al.2007., Slit1a inhibits retinal ganglion cell arborisation and synaptogenesis via Robo2-dependent and independent pathways., Neuron, 55: 231-45.
51. Drinjakovic J, Jung H, Campbell DS, Strochlic L, et al.2010., E3 ligase Nedd4 promotes axon branching by downregulating PTEN., Neuron, 65: 341-57.
52. Marler KJ, Becker-Barroso E, Martinez A, Llovera M, et al.2008., A TrkB/EphrinA interaction controls retinal axon branching and synaptogenesis., J Neurosci, 28: 12700-12.
53. Rashid T, Upton AL, Blentic A, Ciossek T, et al.2005., Opposing gradients of ephrin-As and EphA7 in the superior colliculus are essential for topographic mapping in the mammalian visual system., Neuron, 47: 57-69.
54. Lim YS, McLaughlin T, Sung TC, Santiago A, et al.2008., p75(NTR) mediates ephrin-A reverse signalling required for axon repulsion and mapping., Neuron, 59: 746-58.
55. Hutchins BI, Li L., 2009., EphrinA and TrkB interact to promote axon branching., J Neurosci, 29: 4329-31.
56. Smear MC, Tao HW, Staub W, Orger MB, et al.2007., Vesicular glutamate transport at a central synapse limits the acuity of visual perception in zebrafish., Neuron, 53: 65-77.
57. Huberman AD, Feller MB, Chapman B., 2008., Mechanisms underlying development of visual maps and receptive fields., Annu Rev Neurosci, 31: 479-509.
58. Blankenship AG, Feller MB., 2010., Mechanisms underlying spontaneous patterned activity in developing neural circuits., Nat Rev Neurosci, 11: 18-29.
59. Datwani A, McConnell MJ, Kanold PO, Micheva KD, et al.2009., Classical MHCI molecules regulate retinogeniculate refinement and limit ocular dominance plasticity., Neuron, 64: 463-70.
60. Shatz CJ., 2009., MHC class I: an unexpected role in neuronal plasticity., Neuron, 64: 40-5.
61. van Horck FP, Weinl C, Holt CE., 2004., Retinal axon guidance: novel mechanisms for steering., Curr Opin Neurobiol, 14: 61-6.
62. DiAntonio A, Haghighi AP, Portman SL, Lee JD, et al.2001., Ubiquitination-dependent mechanisms regulate synaptic growth and function., Nature, 412: 449-52.
63. Myat A, Henry P, McCabe V, Flintoft L, et al.2002., Drosophila Nedd4, a ubiquitin ligase, is recruited by Commissureless to control cell surface levels of the roundabout receptor., Neuron, 35: 447-59.
64. Nakata K, Abrams B, Grill B, Goncharov A, et al.2005., Regulation of a DLK-1 and p38 MAP kinase pathway by the ubiquitin ligase RPM-1 is required for presynaptic development., Cell, 120: 407-20.
65. Zhu S, Perez R, Pan M, Lee T., 2005., Requirement of Cul3 for axonal arborisation and dendritic elaboration in Drosophila mushroom body neurons., J Neurosci, 25: 4189-97.
66. Yang Y, Kim AH, Bonni A., 2010., The dynamic ubiquitin ligase duo: Cdh1-APC and Cdc20-APC regulate neuronal morphogenesis and connectivity., Curr Opin Neurobiol, 20: 92-9.
67. van Roessel P, Elliott DA, Robinson IM, Prokop A, et al.2004., Independent regulation of synaptic size and activity by the anaphase-promoting complex., Cell, 119: 707-18.
68. Kim AH, Puram SV, Bilimoria PM, Ikeuchi Y, et al.2009., A centrosomal Cdc20-APC pathway controls dendrite morphogenesis in postmitotic neurons., Cell, 136: 322-36.
69. Collins CA, Wairkar YP, Johnson SL, DiAntonio A., 2006., Highwire restrains synaptic growth by attenuating a MAP kinase signal., Neuron, 51: 57-69.
70. Cosker KE, Eickholt BJ., 2007., Phosphoinositide 3-kinase signalling events controlling axonal morphogenesis., Biochem Soc Trans, 35: 207-10.
71. D'Souza J, Hendricks M, Le Guyader S, Subburaju S, et al.2005., Formation of the retinotectal projection requires Esrom, an ortholog of PAM (protein associated with Myc)., Development, 132: 247-56.
72. Kawabe H, Neeb A, Dimova K, Young SM Jr, et al.2010., Regulation of Rap2A by the ubiquitin ligase Nedd4-1 controls neurite development., Neuron, 65: 358-72.
73. Dent EW, Kalil K., 2001., Axon branching requires interactions between dynamic microtubules and actin filaments., J Neurosci, 21: 9757-69.
74. Zacharias U, Leuschner R, Norenberg U, Rathjen FG., 2002., Tenascin-R induces actin-rich microprocesses and branches along neurite shafts., Mol Cell Neurosci, 21: 626-33.
75. Conde C, Caceres A., 2009., Microtubule assembly, organisation and dynamics in axons and dendrites., Nat Rev Neurosci, 10: 319-32.
76. Lowery LA, van Vactor D., 2009., The trip of the tip: understanding the growth cone machinery., Nat Rev Mol Cell Biol, 10: 332-43.
77. Pak CW, Flynn KC, Bamburg JR., 2008., Actin-binding proteins take the reins in growth cones., Nat Rev Neurosci, 9: 136-47.
78. Yu W, Ahmad FJ, Baas PW., 1994., Microtubule fragmentation and partitioning in the axon during collateral branch formation., J Neurosci, 14: 5872-84.
79. Qiang L, Yu W, Liu M, Solowska JM, et al.2010., Basic fibroblast growth factor elicits formation of interstitial axonal branches via enhanced severing of microtubules., Mol Biol Cell, 21: 334-44.
80. Yu W, Qiang L, Solowska JM, Karabay A, et al.2008., The microtubule-severing proteins spastin and katanin participate differently in the formation of axonal branches., Mol Biol Cell, 19: 1485-98.
81. Yu W, Solowska JM, Qiang L, Karabay A, et al.2005., Regulation of microtubule severing by katanin subunits during neuronal development., J Neurosci, 25: 5573-83.
82. Qiang L, Yu W, Andreadis A, Luo M, et al.2006., Tau protects microtubules in the axon from severing by katanin., J Neurosci, 26: 3120-9.
83. Ng J, Nardine T, Harms M, Tzu J, et al.2002., Rac GTPases control axon growth, guidance and branching., Nature, 416: 442-7.
84. Struckhoff EC, Lundquist EA., 2003., The actin-binding protein UNC-115 is an effector of Rac signalling during axon pathfinding in C. elegans., Development, 130: 693-704.
85. Rico B, Beggs HE, Schahin-Reed D, Kimes N, et al.2004., Control of axonal branching and synapse formation by focal adhesion kinase., Nat Neurosci, 7: 1059-69.
86. Riederer BM., 2007., Microtubule-associated protein 1B, a growth-associated and phosphorylated scaffold protein., Brain Res Bull, 71: 541-58.
87. Salinas PC., 2007., Modulation of the microtubule cytoskeleton: a role for a divergent canonical Wnt pathway., Trends Cell Biol, 17: 333-42.
88. Trivedi N, Marsh P, Goold RG, Wood-Kaczmar A, et al.2005., Glycogen synthase kinase-3beta phosphorylation of MAP1B at Ser1260 and Thr1265 is spatially restricted to growing axons., J Cell Sci, 118: 993-1005.
89. Bouquet C, Soares S, von Boxberg Y, Ravaille-Veron M, et al.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: 7204-13.
90. Creppe C, Malinouskaya L, Volvert ML, Gillard M, et al.2009., Elongator controls the migration and differentiation of cortical neurons through acetylation of alpha-tubulin., Cell, 136: 551-64.
91. Homma N, Takei Y, Tanaka Y, Nakata T, et al.2003., Kinesin superfamily protein 2A (KIF2A) functions in suppression of collateral branch extension., Cell, 114: 229-39.
92. Kim WY, Zhou FQ, Zhou J, Yokota Y, et al.2006., Essential roles for GSK-3s and GSK-3-primed substrates in neurotrophin-induced and hippocampal axon growth., Neuron, 52: 981-96.
93. Poulain FE, Sobel A., 2007., The 'SCG10-LIke Protein' SCLIP is a novel regulator of axonal branching in hippocampal neurons, unlike SCG10., Mol Cell Neurosci, 34: 137-46.
94. Dancause N, Barbay S, Frost SB, Plautz EJ, et al.2005., Extensive cortical rewiring after brain injury., J Neurosci, 25: 10167-79.
95. Helmstaedter M, Sakmann B, Feldmeyer D., 2009., Neuronal correlates of local, lateral, and translaminar inhibition with reference to cortical columns., Cereb Cortex, 19: 926-37.
96. Honig MG, Hume RI., 1989., Dil and diO: versatile fluorescent dyes for neuronal labelling and pathway tracing., Trends Neurosci, 12: 333-1.
97. Feng G, Mellor RH, Bernstein M, Keller-Peck C, et al.2000., Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP., Neuron, 28: 41-51.
98. Livet J, Weissman TA, Kang H, Draft RW, et al.2007., Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system., Nature, 450: 56-62.
99. Luo L., 2007., Fly MARCM and mouse MADM: genetic methods of labeling and manipulating single neurons., Brain Res Rev, 55: 220-7.
100. Javaherian A, Cline HT., 2005., Coordinated motor neuron axon growth and neuromuscular synaptogenesis are promoted by CPG15 in vivo., Neuron, 45: 505-12.
101. Alsina B, Vu T, Cohen-Cory S., 2001., Visualising synapse formation in arborising optic axons in vivo: dynamics and modulation by BDNF., Nat Neurosci, 4: 1093-101.