Switching responses: Spatial and temporal regulators of axon guidance

Molecular Neurobiology

Volumn 49, Issue 2, 2014, Pages 1077-1086

  Kaplan, Andrew ^a,b   Kent, Christopher B ^a,b   Charron, Frédéric ^b,c   Fournier, Alyson E ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

Author keywords

14 3 3; Axon guidance; Commissural neuron; Growth cone; Local translation

Indexed keywords

ADAPTOR PROTEIN; CALCIUM; CELL SURFACE RECEPTOR; CYCLIC NUCLEOTIDE; STRATIFIN; PROTEIN 14 3 3;

CALCIUM SIGNALING; CELL FUNCTION; CELL MIGRATION; CELL POLARITY; CELL SURFACE; CELLULAR DISTRIBUTION; ENTROPY; GROWTH CONE; HUMAN; INTRACELLULAR SIGNALING; MEDIATOR RELEASE; NERVE FIBER; NERVE FIBER GROWTH; NERVE INJURY; NERVE REGENERATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PROTEIN DEGRADATION; PROTEIN PROCESSING; REGULATORY MECHANISM; REVIEW; SPATIOTEMPORAL ANALYSIS; TRANSCRIPTION REGULATION; TRANSLATION REGULATION; ANIMAL; CELL MOTION; PHYSIOLOGY; SIGNAL TRANSDUCTION; TIME;

14-3-3 PROTEINS; ANIMALS; AXONS; CELL MOVEMENT; GROWTH CONES; HUMANS; NERVE REGENERATION; NEUROGENESIS; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 84896549731     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-013-8582-8     Document Type: Review

References (86)

1. Kolodkin AL, Tessier-Lavigne M (2011) Mechanisms andmolecules of neuronal wiring: a primer. Cold Spring Harb Perspect Biol 3 (6). doi: 10.1101/cshperspect.a001727
2. Dent EW, Gupton SL, Gertler FB (2011) The growth cone cytoskeleton in axon outgrowth and guidance. Cold Spring Harb Perspect Biol 3 (3). doi: 10.1101/cshperspect.a001800
3. Vitriol Eric A, Zheng James Q (2012) Growth cone travel in space and time: the cellular ensemble of cytoskeleton, adhesion, and membrane. Neuron 73(6):1068-1081. doi:10.1016/j.neuron.2012.03.005
4. Tessier-Lavigne M, Goodman CS (1996) The molecular biology of axon guidance. Science 274(5290):1123-1133 (Pubitemid 26389268)
5. Bashaw GJ, Klein R (2010) Signaling from axon guidance receptors. Cold Spring Harb Perspect Biol 2(5):a001941. doi:10.1101/cshperspect.a001941
6. Dudanova I, Klein R (2013) Integration of guidance cues: parallel signaling and crosstalk. Trends Neurosci 36(5):295-304. doi:10.1016/j.tins.2013. 01.007
7. Castellani V (2013) Building spinal and brain commissures: axon guidance at the midline. ISRN Cell Biol. doi:10.1155/2013/315387
8. Hornberg H, Holt C (2013) RNA-binding proteins and translational regulation in axons and growth cones. Front Neurosci 7:81. doi:10.3389/fnins. 2013.00081
9. Yang T, Terman JR (2013) Regulating small G protein signaling to coordinate axon adhesion and repulsion. Small GTPases 4(1):34-41. doi:10.4161/sgtp.22765
10. Serafini T, Kennedy TE, Galko MJ, Mirzayan C, Jessell TM, Tessier-Lavigne M (1994) The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6. Cell 78(3):409-424 (Pubitemid 24250806)
11. Keino-Masu K, Masu M, Hinck L, Leonardo ED, Chan SS, Culotti JG, Tessier-Lavigne M (1996) Deleted in Colorectal Cancer (DCC) encodes a netrin receptor. Cell 87(2):175-185 (Pubitemid 26358997)
12. Stein E, Tessier-Lavigne M (2001) Hierarchical organization of guidance receptors: silencing of netrin attraction by slit through a Robo/DCC receptor complex. Science 291(5510):1928-1938. doi:10.1126/science.1058445 (Pubitemid 32216987)
13. Sabatier C, Plump AS, Le M, Brose K, Tamada A, Murakami F, Lee EY, Tessier-Lavigne M (2004) The divergent Robo family protein rig-1/Robo3 is a negative regulator of slit responsiveness required for midline crossing by commissural axons. Cell 117(2):157-169 (Pubitemid 38496237)
14. Chen Z, Gore BB, Long H, Ma L, Tessier-Lavigne M (2008) Alternative splicing of the Robo3 axon guidance receptor governs the midline switch from attraction to repulsion. Neuron 58(3):325-332. doi:10.1016/j.neuron.2008.02.016 (Pubitemid 351615180)
15. Leonardo ED, Hinck L, Masu M, Keino-Masu K, Ackerman SL, Tessier-Lavigne M (1997) Vertebrate homologues of C. elegans UNC-5 are candidate netrin receptors. Nature 386(6627):833-838. doi:10.1038/386833a0 (Pubitemid 27181257)
16. Burgess RW, Jucius TJ, Ackerman SL (2006) Motor axon guidance of the mammalian trochlear and phrenic nerves: dependence on the netrin receptor Unc5c and modifier loci. J Neurosci 26(21):5756-5766. doi:10.1523/JNEUROSCI.0736-06. 2006 (Pubitemid 44315268)
17. Hong K, Hinck L, Nishiyama M, Poo MM, Tessier-Lavigne M, Stein E (1999) A ligand-gated association between cytoplasmic domains of UNC5 and DCC family receptors converts netrin-induced growth cone attraction to repulsion. Cell 97(7):927-941 (Pubitemid 29375051)
18. Keleman K, Dickson BJ (2001) Short- and long-range repulsion by the Drosophila Unc5 netrin receptor. Neuron 32(4):605-617 (Pubitemid 33145195)
19. Zarin AA, Asadzadeh J, Labrador JP (2013) Transcriptional regulation of guidance at the midline and in motor circuits. Cell Mol Life Sci. doi:10.1007/s00018-013-1434-x
20. Polleux F, Ince-Dunn G, Ghosh A (2007) Transcriptional regulation of vertebrate axon guidance and synapse formation. Nat Rev Neurosci 8(5):331-340. doi:10.1038/nrn2118 (Pubitemid 46652466)
21. Brittis PA, Lu Q, Flanagan JG (2002) Axonal protein synthesis provides a mechanism for localized regulation at an intermediate target. Cell 110(2):223-235 (Pubitemid 34876550)
22. Colak D, Ji SJ, Porse BT, Jaffrey SR (2013) Regulation of axon guidance by compartmentalized nonsense-mediated mRNA decay. Cell 153(6):1252-1265. doi:10.1016/j.cell.2013.04.056
23. Kuwako K, Kakumoto K, Imai T, Igarashi M, Hamakubo T, Sakakibara S, Tessier-Lavigne M, Okano HJ, Okano H (2010) Neural RNA-binding protein Musashi1 controls midline crossing of precerebellar neurons through posttranscriptional regulation of Robo3/Rig-1 expression. Neuron 67(3):407-421. doi:10.1016/j. neuron.2010.07.005
24. 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(46):15464-15478. doi:10.1523/JNEUROSCI.1800- 10.2010
25. Fambrough D, Pan D, Rubin GM, Goodman CS (1996) The cell surface metalloprotease/disintegrin Kuzbanian is required for axonal extension in Drosophila. Proc Natl Acad Sci U S A 93(23):13233-13238 (Pubitemid 26382799)
26. Hattori M, Osterfield M, Flanagan JG (2000) Regulated cleavage of a contact-mediated axon repellent. Science 289(5483):1360-1365 (Pubitemid 30656055)
27. Janes PW, Saha N, Barton WA, Kolev MV, Wimmer-Kleikamp SH, Nievergall E, Blobel CP, Himanen JP, Lackmann M, Nikolov DB (2005) Adam meets Eph: an ADAM substrate recognition module acts as a molecular switch for ephrin cleavage in trans. Cell 123(2):291-304. doi:10.1016/j.cell.2005.08.014 (Pubitemid 41457218)
28. Galko MJ, Tessier-Lavigne M (2000) Function of an axonal chemoattractant modulated by metalloprotease activity. Science 289(5483):1365-1367 (Pubitemid 30656056)
29. Nawabi H, Briancon-Marjollet A, Clark C, Sanyas I, Takamatsu H, Okuno T, Kumanogoh A, Bozon M, Takeshima K, Yoshida Y, Moret F, Abouzid K, Castellani V (2010) A midline switch of receptor processing regulates commissural axon guidance in vertebrates. Genes Dev 24(4):396-410. doi:10.1101/gad.542510
30. Charoy C, Nawabi H, Reynaud F, Derrington E, Bozon M, Wright K, Falk J, Helmbacher F, Kindbeiter K, Castellani V (2012) gdnf activates midline repulsion by Semaphorin3B via NCAM during commissural axon guidance. Neuron 75(6):1051-1066. doi:10.1016/j.neuron.2012.08.021
31. Fournier AE, Nakamura F, Kawamoto S, Goshima Y, Kalb RG, Strittmatter SM (2000) Semaphorin3A enhances endocytosis at sites of receptor-F-actin colocalization during growth cone collapse. J Cell Biol 149(2):411-422
32. Castellani V, Falk J, Rougon G (2004) Semaphorin3A-induced receptor endocytosis during axon guidance responses is mediated by L1 CAM. Mol Cell Neurosci 26(1):89-100. doi:10.1016/j.mcn.2004.01.010 (Pubitemid 38581025)
33. Bechara A, Falk J, Moret F, Castellani V (2007) Modulation of semaphorin signaling by Ig superfamily cell adhesion molecules. Adv Exp Med Biol 600:61-72. doi:10.1007/978-0-387-70956-7-6
34. Williams ME, Wu SC, McKenna WL, Hinck L (2003) Surface expression of the netrin receptor UNC5H1 is regulated through a protein kinase C-interacting protein/protein kinase-dependent mechanism. J Neurosci 23(36):11279-11288 (Pubitemid 37549683)
35. Gomez TM, Spitzer NC (1999) In vivo regulation of axon extension and pathfinding by growth-cone calcium transients. Nature 397(6717):350-355. doi:10.1038/16927
36. Hong K, Nishiyama M, Henley J, Tessier-Lavigne M, Poo M (2000) Calcium signalling in the guidance of nerve growth by netrin-1. Nature 403(6765):93-98. doi:10.1038/47507 (Pubitemid 30038528)
37. Zheng JQ (2000) Turning of nerve growth cones induced by localized increases in intracellular calcium ions. Nature 403(6765):89-93. doi:10.1038/47501
38. Gomez TM, Robles E, Poo M, Spitzer NC (2001) Filopodial calcium transients promote substrate-dependent growth cone turning. Science 291(5510):1983-1987. doi:10.1126/science.1056490 (Pubitemid 32217001)
39. Henley JR, Huang K-H, Wang D, Poo M-M (2004) Calcium mediates bidirectional growth cone turning induced by myelin-associated glycoprotein. Neuron 44(6):909-916 (Pubitemid 39643087)
40. Wen Z, Guirland C, Ming GL, Zheng JQ (2004) A CaMKII/calcineurin switch controls the direction of Ca(2+)-dependent growth cone guidance. Neuron 43(6):835-846. doi:10.1016/j.neuron.2004.08.037 (Pubitemid 39215014)
41. Tojima T, Hines JH, Henley JR, Kamiguchi H (2011) Second messengers and membrane trafficking direct and organize growth cone steering. Nat Rev Neurosci 12(4):191-203. doi:10.1038/nrn2996
42. Song HJ, Ming GL, Poo MM (1997) cAMP-induced switching in turning direction of nerve growth cones. Nature 388(6639):275-279. doi:10.1038/40864
43. Ming G-L, Song H-J, Berninger B, Holt CE, Tessier-Lavigne M, Poo M-M (1997) cAMP-dependent growth cone guidance by Netrin-1. Neuron 19(6):1225-1235 (Pubitemid 28030542)
44. Song H, Ming G, He Z, Lehmann M, McKerracher L, Tessier-Lavigne M, Poo M (1998) Conversion of neuronal growth cone responses from repulsion to attraction by cyclic nucleotides. Science 281(5382):1515-1518 (Pubitemid 28425577)
45. Ming G, Henley J, Tessier-Lavigne M, Song H, Poo M (2001) Electrical activity modulates growth cone guidance by diffusible factors. Neuron 29(2):441-452 (Pubitemid 32206482)
46. Dontchev VD, Letourneau PC (2002) Nerve growth factor and semaphorin 3A signaling pathways interact in regulating sensory neuronal growth cone motility. J Neurosci 22(15):6659-6669 (Pubitemid 35386422)
47. Shewan D, Dwivedy A, Anderson R, Holt CE (2002) Age-related changes underlie switch in netrin-1 responsiveness as growth cones advance along visual pathway. Nat Neurosci 5(10):955-962. doi:10.1038/nn919
48. Hopker VH, Shewan D, Tessier-Lavigne M, Poo M, Holt C (1999) Growth-cone attraction to netrin-1 is converted to repulsion by laminin-1. Nature 401(6748):69-73. doi:10.1038/43441
49. 2+ channels sets the polarity of nerve growth-cone turning. Nature 423(6943):990-995. doi:10.1038/nature01751
50. 2+-mediated steering of growth cones via cyclic AMP and ryanodine receptor type 3. J Cell Biol 170(7):1159-1167. doi:10.1083/jcb.200503157
51. 2+ signals. J Neurosci 29(24):7886-7897. doi:10.1523/JNEUROSCI.0087-09.2009
52. Nishiyama M, von Schimmelmann MJ, Togashi K, Findley WM, Hong K (2008) Membrane potential shifts caused by diffusible guidance signals direct growth-cone turning. Nat Neurosci 11(7):762-771. doi:10.1038/nn.2130 (Pubitemid 351896672)
53. Togashi K, von Schimmelmann MJ, Nishiyama M, Lim CS, Yoshida N, Yun B, Molday RS, Goshima Y, Hong K (2008) Cyclic GMP-gated CNG channels function in Sema3A-induced growth cone repulsion. Neuron 58(5):694-707. doi:10.1016/j. neuron.2008.03.017 (Pubitemid 351778462)
54. Shelly M, Lim BK, Cancedda L, Heilshorn SC, Gao H, Poo MM (2010) Local and long-range reciprocal regulation of cAMP and cGMP in axon/dendrite formation. Science 327(5965):547-552. doi:10.1126/science.1179735
55. Nicol X, Hong KP, Spitzer NC (2011) Spatial and temporal second messenger codes for growth cone turning. Proc Natl Acad Sci U S A 108(33):13776-13781. doi:10.1073/pnas.1100247108
56. Qiu J, Cai D, Dai H, McAtee M, Hoffman PN, Bregman BS, Filbin MT (2002) Spinal axon regeneration induced by elevation of cyclic AMP. Neuron 34(6):895-903 (Pubitemid 34722280)
57. Neumann S, Bradke F, Tessier-Lavigne M, Basbaum AI (2002) Regeneration of sensory axons within the injured spinal cord induced by intraganglionic cAMP elevation. Neuron 34(6):885-893 (Pubitemid 34722279)
58. Pearse DD, Pereira FC, Marcillo AE, Bates ML, Berrocal YA, Filbin MT, Bunge MB (2004) cAMP and Schwann cells promote axonal growth and functional recovery after spinal cord injury. Nat Med 10(6):610-616. doi:10.1038/nm1056 (Pubitemid 38796852)
59. Mackintosh C (2004) Dynamic interactions between 14-3-3 proteins and phosphoproteins regulate diverse cellular processes. Biochem J 381(Pt 2):329-342
60. Rosenquist M, Sehnke P, Ferl RJ, Sommarin M, Larsson C (2000) Evolution of the 14-3-3 Pprotein family: does the large number of isoforms in multicellular organisms reflect functional specificity? J Mol Evol 51:446-458
61. Aitken A (2006) 14-3-3 proteins: a historic overview. Semin Cancer Biol 16(3):162-172
62. Liu D, Bienkowska J, Petosa C, Collier RJ, Fu H, Liddington R (1995) Crystal structure of the zeta isoform of the 14-3-3 protein. Nature 376(6536):191-194
63. Xiao B, Smerdon SJ, Jones DH, Dodson GG, Soneji Y, Aitken A, Gamblin SJ (1995) Structure of a 14-3-3 protein and implications for coordination of multiple signalling pathways. Nature 376(6536):188-191
64. Yang X, Lee WH, Sobott F, Papagrigoriou E, Robinson CV, Grossmann JG, Sundstrom M, Doyle DA, Elkins JM (2006) Structural basis for protein-protein interactions in the 14-3-3 protein family. Proc Natl Acad Sci U S A 103(46):17237-17242 (Pubitemid 44788953)
65. Bridges D, Moorhead GBG (2005) 14-3-3 Proteins: a number of functions for a numbered protein. Sci STKE 2005 (296):re10. doi:10.1126/stke.2962005re10
66. Rittinger K, Budman J, Xu J, Volinia S, Cantley LC, Smerdon SJ, Gamblin SJ, Yaffe MB (1999) Structural analysis of 14-3-3 phosphopeptide complexes identifies a dual role for the nuclear export signal of 14-3-3 in ligand binding. Mol Cell 4(2):153-166 (Pubitemid 29456884)
67. Aitken A, Baxter H, Dubois T, Clokie S, Mackie S, Mitchell K, Peden A, Zemlickova E (2002) Specificity of 14-3-3 isoform dimer interactions and phosphorylation. Biochem Soc Trans 30(4):351-360. doi:10.1042/
68. Toyo-oka K, Shionoya A, Gambello MJ, Cardoso C, Leventer R, Ward HL, Ayala R, Tsai L-H, Dobyns W, Ledbetter D, Hirotsune S, Wynshaw-Boris A (2003) 14-3-3 [epsi] is important for neuronal migration by binding to NUDEL: a molecular explanation for Miller-Dieker syndrome. Nat Genet 34(3):274-285 (Pubitemid 36792859)
69. Yingling J, Toyo-oka K, Wynshaw-Boris A (2003) Miller-Dieker syndrome: analysis of a human contiguous gene syndrome in the mouse. Am J Hum Genet 73:475-488 (Pubitemid 37076263)
70. Cheah PS, Ramshaw HS, Thomas PQ, Toyo-Oka K, Xu X, Martin S, Coyle P, Guthridge MA, Stomski F, van den Buuse M, Wynshaw-Boris A, Lopez AF, Schwarz QP (2012) Neurodevelopmental and neuropsychiatric behaviour defects arise from 14-3-3zeta deficiency. Mol Psychiatry 17(4):451-466. doi:10.1038/mp.2011.158
71. Estrada-Bernal A, Sanford SD, Sosa LJ, Simon GC, Hansen KC, Pfenninger KH (2012) Functional complexity of the axonal growth cone: a proteomic analysis. PLoS One 7(2):e31858. doi:10.1371/journal.pone.0031858
72. Kent CB, Shimada T, Ferraro GB, Ritter B, Yam PT, McPherson PS, Charron F, Kennedy TE, Fournier AE (2010) 14-3-3 proteins regulate protein kinase a activity tomodulate growth cone turning responses. J Neurosci 30(42):14059-14067. doi:10.1523/JNEUROSCI.3883-10.2010
73. Nozumi M, Togano T, Takahashi-Niki K, Lu J, Honda A, Taoka M, Shinkawa T, Koga H, Takeuchi K, Isobe T, Igarashi M (2009) Identification of functionalmarker proteins in themammalian growth cone. Proc Natl Acad Sci U S A 106(40):17211-17216. doi:10.1073/pnas.0904092106
74. 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(1):85-98. doi:10.1261/rna.2386111
75. Wang B, Yang H, Liu YC, Jelinek T, Zhang L, Ruoslahti E, Fu H (1999) Isolation of high-affinity peptide antagonists of 14-3-3 proteins by phage display. Biochemistry 38(38):12499-12504
76. Yam PT, Kent CB, Morin S, Farmer WT, Alchini R, Lepelletier L, Colman DR, Tessier-Lavigne M, Fournier AE, Charron F (2012) 14-3-3 proteins regulate a cell-intrinsic switch from sonic hedgehog-mediated commissural axon attraction to repulsion after midline crossing. Neuron 76(4):735-749. doi:10.1016/j.neuron. 2012.09.017
77. Yoon BC, Zivraj KH, Strochlic L, Holt CE (2011) 14-3-3 proteins regulate retinal axon growth by modulating ADF/cofilin activity. Dev Neurobiol. doi:10.1002/dneu.20955
78. Gohla A, Bokoch GM (2002) 14-3-3 regulates actin dynamics by stabilizing phosphorylated cofilin. Curr Biol 12(19):1704-1710 (Pubitemid 35161927)
79. Yang T, Terman JR (2012) 14-3-3epsilon couples protein kinase A to semaphorin signaling and silences plexin RasGAP-mediated axonal repulsion. Neuron 74(1):108-121. doi:10.1016/j.neuron.2011.12.034
80. Ramser EM, Buck F, Schachner M, Tilling T (2010) Binding of alphaII spectrin to 14-3-3beta is involved in NCAM-dependent neurite outgrowth. Mol Cell Neurosci 45(1):66-74. doi:10.1016/j.mcn.2010.05.013
81. Ramser EM, Wolters G, Dityateva G, Dityatev A, Schachner M, Tilling T (2010) The 14-3-3zeta protein binds to the cell adhesion molecule L1, promotes L1 phosphorylation by CKII and influences L1-dependent neurite outgrowth. PLoS One 5(10):e13462. doi:10.1371/journal.pone.0013462
82. Deakin NO, Bass MD, Warwood S, Schoelermann J, Mostafavi-Pour Z, Knight D, Ballestrem C, Humphries MJ (2009) An integrin-alpha4-14-3-3zeta-paxillin ternary complex mediates localised Cdc42 activity and accelerates cell migration. J Cell Sci 122(Pt 10): 1654-1664. doi:10.1242/jcs.049130
83. Kobayashi H, Ogura Y, Sawada M, Nakayama R, Takano K, Minato Y, Takemoto Y, Tashiro E, Watanabe H, Imoto M (2011) Involvement of 14-3-3 proteins in the second epidermal growth factor-induced wave of Rac1 activation in the process of cell migration. J Biol Chem 286(45):39259-39268. doi:10.1074/jbc.M111.255489
84. O'Toole TE, Bialkowska K, Li X, Fox JE (2011) Tiam1 is recruited to beta1-integrin complexes by 14-3-3zeta where it mediates integrin-induced Rac1 activation and motility. J Cell Physiol 226(11):2965-2978. doi:10.1002/jcp.22644
85. Leto D, Uhm M, Williams A, Chen XW, Saltiel AR (2013) Negative regulation of the RalGAP complex by 14-3-3. J Biol Chem 288(13):9272-9283. doi:10.1074/jbc.M112.426106
86. Riou P, Kjaer S, Garg R, Purkiss A, George R, Cain RJ, Bineva G, Reymond N, McColl B, Thompson AJ, O'Reilly N, McDonald NQ, Parker PJ, Ridley AJ (2013) 14-3-3 proteins interact with a hybrid prenyl-phosphorylation motif to inhibit g proteins. Cell 153(3):640-653. doi:10.1016/j.cell.2013.03.044