Transcriptional regulators that differentially control dendrite and axon development

Abstract

Neurons are the basic units of connectivity in the nervous system. As a signature feature, neurons form polarized structures: dendrites and axons, which integrate either sensory stimuli or inputs from upstream neurons and send outputs to target cells, respectively. The separation of dendritic and axonal compartments is achieved in two steps during development: 1) dendrite and axon specification: how neurites are initially specified as dendrites and axons; and 2) dendrite and axon commitment: how dendrites and axons are committed to distinct compartmental fates and architectures. To understand neural circuit assembly and to correct erroneous dendrite or axon growth in a compartment-specific manner, it is essential to understand the regulatory mechanisms underlying dendrite and axon commitment. Compared to extensive studies on dendrite and axon specification, little is known about the molecular mechanisms exclusively dedicated to dendrite or axon commitment. Recent studies have uncovered the requirement of transcriptional regulation in this process. Here, we review the studies on transcriptional regulators: Dar1, p300-SnoN, NeuroD, which have been shown to separate dendrite- and axon-specific growth of the same neuron type after compartmental fates are specified.

Keywords

dendrite and axon commitment / Dar1 / p300-SnoN / NeuroD

References

[1] Aizawa H, Hu S C, Bobb K, Balakrishnan K, Ince G, Gurevich I, Cowan M, Ghosh A (2004). Dendrite development regulated by CREST, a calcium-regulated transcriptional activator. Science, 303(5655): 197-202

[2] Arimura N, Kaibuchi K (2005). Key regulators in neuronal polarity. Neuron, 48(6): 881-884

[3] Barnes A P, Lilley B N, Pan Y A, Plummer L J, Powell A W, Raines A N, Sanes J R, Polleux F (2007). LKB1 and SAD kinases define a pathway required for the polarization of cortical neurons. Cell, 129(3): 549-563

[4] Barnes A P, Polleux F (2009). Establishment of axon-dendrite polarity in developing neurons. Annu Rev Neurosci, 32(1): 347-381

[5] Bonni S, Wang H R, Causing C G, Kavsak P, Stroschein S L, Luo K, Wrana J L (2001). TGF-beta induces assembly of a Smad2-Smurf2 ubiquitin ligase complex that targets SnoN for degradation. Nat Cell Biol, 3(6): 587-595

[6] Crozatier M, Vincent A (2008). Control of multidendritic neuron differentiation in Drosophila: the role of Collier. Dev Biol, 315(1): 232-242

[7] de la Torre-Ubieta L, Bonni A (2011). Transcriptional regulation of neuronal polarity and morphogenesis in the mammalian brain. Neuron, 72(1): 22-40

[8] Dickson B J (2002). Molecular mechanisms of axon guidance. Science, 298(5600): 1959-1964

[9] Dotti C G, Sullivan C A, Banker G A (1988). The establishment of polarity by hippocampal neurons in culture. J Neurosci, 8(4): 1454-1468

[10] Gao Z, Ure K, Ables J L, Lagace D C, Nave K A, Goebbels S, Eisch A J, Hsieh J (2009). Neurod1 is essential for the survival and maturation of adult-born neurons. Nat Neurosci, 12(9): 1090-1092

[11] Gärtner A, Fornasiero E F, Munck S, Vennekens K, Seuntjens E, Huttner W B, Valtorta F, Dotti C G (2012). N-cadherin specifies first asymmetry in developing neurons. EMBO J, 31(8): 1893-1903

[12] Gaudillière B, Konishi Y, de la Iglesia N, Yao G, Bonni A (2004). A CaMKII-NeuroD signaling pathway specifies dendritic morphogenesis. Neuron, 41(2): 229-241

[13] Ghosh A, Greenberg M E (1995). Calcium signaling in neurons: molecular mechanisms and cellular consequences. Science, 268(5208): 239-247

[14] Goldberg J L (2004). Intrinsic neuronal regulation of axon and dendrite growth. Curr Opin Neurobiol, 14(5): 551-557

[15] Goldberg J L, Klassen M P, Hua Y, Barres B A (2002). Amacrine-signaled loss of intrinsic axon growth ability by retinal ganglion cells. Science, 296(5574): 1860-1864

[16] Grueber W B, Jan L Y, Jan Y N (2003). Different levels of the homeodomain protein cut regulate distinct dendrite branching patterns of Drosophila multidendritic neurons. Cell, 112(6): 805-818

[17] Hattori Y, Sugimura K, Uemura T (2007). Selective expression of Knot/Collier, a transcriptional regulator of the EBF/Olf-1 family, endows the Drosophila sensory system with neuronal class-specific elaborated dendritic patterns. Genes Cells, 12(9): 1011-1022

[18] Ikeuchi Y, Stegmüller J, Netherton S, Huynh M A, Masu M, Frank D, Bonni S, Bonni A (2009). A SnoN-Ccd1 pathway promotes axonal morphogenesis in the mammalian brain. J Neurosci, 29(13): 4312-4321

[19] Jacobson C, Schnapp B, Banker G A (2006). A change in the selective translocation of the Kinesin-1 motor domain marks the initial specification of the axon. Neuron, 49(6): 797-804

[20] Jan Y N, Jan L Y (2003). The control of dendrite development. Neuron, 40(2): 229-242

[21] Jan Y N, Jan L Y (2010). Branching out: mechanisms of dendritic arborization. Nat Rev Neurosci, 11(5): 316-328

[22] Jinushi-Nakao S, Arvind R, Amikura R, Kinameri E, Liu A W, Moore A W (2007). Knot/Collier and cut control different aspects of dendrite cytoskeleton and synergize to define final arbor shape. Neuron, 56(6): 963-978

[23] Kollins K M, Hu J, Bridgman P C, Huang Y Q, Gallo G (2009). Myosin-II negatively regulates minor process extension and the temporal development of neuronal polarity. Dev Neurobiol, 69(5): 279-298

[24] Konishi Y, Stegmüller J, Matsuda T, Bonni S, Bonni A (2004). Cdh1-APC controls axonal growth and patterning in the mammalian brain. Science, 303(5660): 1026-1030

[25] Konur S, Ghosh A (2005). Calcium signaling and the control of dendritic development. Neuron, 46(3): 401-405

[26] Li W, Wang F, Menut L, Gao F B (2004). BTB/POZ-zinc finger protein abrupt suppresses dendritic branching in a neuronal subtype-specific and dosage-dependent manner. Neuron, 43(6): 823-834

[27] Ménager C, Arimura N, Fukata Y, Kaibuchi K (2004). PIP3 is involved in neuronal polarization and axon formation. J Neurochem, 89(1): 109-118

[28] Miyata T, Maeda T, Lee J E (1999). NeuroD is required for differentiation of the granule cells in the cerebellum and hippocampus. Genes Dev, 13(13): 1647-1652

[29] Moore D L, Apara A, Goldberg J L (2011). Krüppel-like transcription factors in the nervous system: novel players in neurite outgrowth and axon regeneration. Mol Cell Neurosci, 47(4): 233-243

[30] Moore D L, Goldberg J L (2011). Multiple transcription factor families regulate axon growth and regeneration. Dev Neurobiol, 71(12): 1186-1211

[31] Nishimura T, Kato K, Yamaguchi T, Fukata Y, Ohno S, Kaibuchi K (2004). Role of the PAR-3-KIF3 complex in the establishment of neuronal polarity. Nat Cell Biol, 6(4): 328-334

[32] Pearson R, Fleetwood J, Eaton S, Crossley M, Bao S (2008). Krüppel-like transcription factors: a functional family. Int J Biochem Cell Biol, 40(10): 1996-2001

[33] Pollarolo G, Schulz J G, Munck S, Dotti C G (2011). Cytokinesis remnants define first neuronal asymmetry in vivo. Nat Neurosci, 14(12): 1525-1533

[34] Saneyoshi T, Fortin D A, Soderling T R (2010). Regulation of spine and synapse formation by activity-dependent intracellular signaling pathways. Curr Opin Neurobiol, 20(1): 108-115

[35] Shelly M, Cancedda L, Heilshorn S, Sumbre G, Poo M M (2007). LKB1/STRAD promotes axon initiation during neuronal polarization. Cell, 129(3): 565-577

[36] Shelly M, Lim B K, Cancedda L, Heilshorn S C, Gao H, Poo M M (2010). Local and long-range reciprocal regulation of cAMP and cGMP in axon/dendrite formation. Science, 327(5965): 547-552

[37] Shi S H, Jan L Y, Jan Y N (2003). Hippocampal neuronal polarity specified by spatially localized mPar3/mPar6 and PI 3-kinase activity. Cell, 112(1): 63-75

[38] Stegmüller J, Huynh M A, Yuan Z, Konishi Y, Bonni A (2008). TGFbeta-Smad2 signaling regulates the Cdh1-APC/SnoN pathway of axonal morphogenesis. J Neurosci, 28(8): 1961-1969

[39] Stegmüller J, Konishi Y, Huynh M A, Yuan Z, Dibacco S, Bonni A (2006). Cell-intrinsic regulation of axonal morphogenesis by the Cdh1-APC target SnoN. Neuron, 50(3): 389-400

[40] Stroschein S L, Bonni S, Wrana J L, Luo K (2001). Smad3 recruits the anaphase-promoting complex for ubiquitination and degradation of SnoN. Genes Dev, 15(21): 2822-2836

[41] Sugimura K, Satoh D, Estes P, Crews S, Uemura T (2004). Development of morphological diversity of dendrites in Drosophila by the BTB-zinc finger protein abrupt. Neuron, 43(6): 809-822

[42] Tahirovic S, Bradke F (2009). Neuronal polarity. Cold Spring Harb Perspect Biol, 1(3): a001644

[43] Wan Y, Liu X, Kirschner M W (2001). The anaphase-promoting complex mediates TGF-beta signaling by targeting SnoN for destruction. Mol Cell, 8(5): 1027-1039

[44] Wang T, Liu Y, Xu X H, Deng C Y, Wu K Y, Zhu J, Fu X Q, He M, Luo Z G (2011). Lgl1 activation of rab10 promotes axonal membrane trafficking underlying neuronal polarization. Dev Cell, 21(3): 431-444

[45] Wang X, Zheng L, Zeng Z, Zhou G, Chien J, Qian C, Vasmatzis G, Shridhar V, Chen L, Liu W (2006). DIXDC1 isoform, l-DIXDC1, is a novel filamentous actin-binding protein. Biochem Biophys Res Commun, 347(1): 22-30

[46] West A E, Greenberg M E (2011). Neuronal activity-regulated gene transcription in synapse development and cognitive function. Cold Spring Harb Perspect Biol, 3(6): 3

[47] Whitford K L, Dijkhuizen P, Polleux F, Ghosh A (2002). Molecular control of cortical dendrite development. Annu Rev Neurosci, 25(1): 127-149

[48] Wong R O L, Ghosh A (2002). Activity-dependent regulation of dendritic growth and patterning. Nat Rev Neurosci, 3(10): 803-812

[49] Yan D, Guo L, Wang Y (2006). Requirement of dendritic Akt degradation by the ubiquitin-proteasome system for neuronal polarity. J Cell Biol, 174(3): 415-424

[50] Ye B, Kim J H, Yang L, McLachlan I, Younger S, Jan L Y, Jan Y N (2011). Differential regulation of dendritic and axonal development by the novel Krüppel-like factor Dar1. J Neurosci, 31(9): 3309-3319

[51] Ye B, Zhang Y, Song W, Younger S H, Jan L Y, Jan Y N (2007). Growing dendrites and axons differ in their reliance on the secretory pathway. Cell, 130(4): 717-729

[52] Yuan Q, Xiang Y, Yan Z, Han C, Jan L Y, Jan Y N (2011). Light-induced structural and functional plasticity in Drosophila larval visual system. Science, 333(6048): 1458-1462

[53] Zheng Y, Wildonger J, Ye B, Zhang Y, Kita A, Younger S H, Zimmerman S, Jan L Y, Jan Y N (2008). Dynein is required for polarized dendritic transport and uniform microtubule orientation in axons. Nat Cell Biol, 10(10): 1172-1180

Acknowledgments

We thank Lindsey Cregan and the anonymous reviewer for constructivesuggestions on the manuscript.Research in Ye laboratory is supported by grants from NIH (R00MH080599 and R01MH091186), the Whitehall foundation, and the Pew Charitable Trusts.

RIGHTS & PERMISSIONS

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg