SAD kinases control the maturation of nerve terminals in the mammalian peripheral and central nervous systems

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 3, 2014, Pages 1138-1143

  Lilley, Brendan N ^a   Krishnaswamy, Arjun ^a   Wang, Zhi ^b   Kishi, Masashi ^c   Frank, Eric ^b   Sanes, Joshua R ^a  

^a HARVARD UNIVERSITY   (United States)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

Author keywords

Calyx of held; Ia synapse; Neuromuscular junction; Spinal cord; Sympathetic ganglion

Indexed keywords

PHOSPHOTRANSFERASE; SAD A KINASE; SAD B KINASE; UNCLASSIFIED DRUG; VESICULAR GLUTAMATE TRANSPORTER 1;

ACTION POTENTIAL; ANIMAL CELL; ARTICLE; AUTONOMIC GANGLION; CELL MATURATION; CELL ULTRASTRUCTURE; CENTRAL NERVOUS SYSTEM; CHOLINERGIC SYNAPSE; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENZYME LOCALIZATION; EXCITATORY POSTSYNAPTIC POTENTIAL; IMMUNOHISTOCHEMISTRY; MOTONEURON; MOUSE; NERVE CELL DIFFERENTIATION; NERVE ENDING; NERVE FIBER; NERVE FIBER GROWTH; NEUROFILAMENT; NEUROMUSCULAR SYNAPSE; NEUROTRANSMITTER RELEASE; NONHUMAN; PERIPHERAL NERVE; PERIPHERAL NERVOUS SYSTEM; POSTGANGLIONIC NERVE; POSTSYNAPTIC MEMBRANE; PREGANGLIONIC NERVE; PRESYNAPTIC MEMBRANE; PRESYNAPTIC NERVE; PRIORITY JOURNAL; SENSORY NERVE CELL; SYMPATHETIC NERVE CELL; SYNAPSE VESICLE; VENTRAL COCHLEAR NUCLEUS;

CALYX OF HELD; IA SYNAPSE; NEUROMUSCULAR JUNCTION; SPINAL CORD; SYMPATHETIC GANGLION;

ALLELES; ANIMALS; AXONS; CELL DIFFERENTIATION; CENTRAL NERVOUS SYSTEM; ELECTROPHYSIOLOGY; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MICE; MICE, TRANSGENIC; MOTOR NEURONS; NERVE ENDINGS; NEUROMUSCULAR JUNCTION; PRESYNAPTIC TERMINALS; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; SPINAL CORD; SYNAPSES;

EID: 84892944241     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1321990111     Document Type: Article

References (48)

1. Barnes AP, Polleux F (2009) Establishment of axon-dendrite polarity in developing neurons. Annu Rev Neurosci 32:347-381.
2. Gibson DA, Ma L (2011) Developmental regulation of axon branching in the vertebrate nervous system. Development 138(2):183-195.
3. Jin Y, Garner CC (2008) Molecular mechanisms of presynaptic differentiation. Annu Rev Cell Dev Biol 24:237-262.
4. Südhof TC (2012) The presynaptic active zone. Neuron 75(1):11-25.
5. Ahmari SE, Buchanan J, Smith SJ (2000) Assembly of presynaptic active zones from cytoplasmic transport packets. Nat Neurosci 3(5):445-451.
6. Wu YE, Huo L, Maeder CI, Feng W, Shen K (2013) The balance between capture and dissociation of presynaptic proteins controls the spatial distribution of synapses. Neuron 78(6):994-1011.
7. Patel MR, et al. (2006) Hierarchical assembly of presynaptic components in defined C. elegans synapses. Nat Neurosci 9(12):1488-1498.
8. Goldstein A Y N, Wang X, Schwarz TL (2008) Axonal transport and the delivery of presynaptic components. Curr Opin Neurobiol 18(5):495-503.
9. Gundelfinger ED, Fejtova A (2012) Molecular organization and plasticity of the cytomatrix at the active zone. Curr Opin Neurobiol 22(3):423-430.
10. McMahon SA, Díaz E (2011) Mechanisms of excitatory synapse maturation by transsynaptic organizing complexes. Curr Opin Neurobiol 21(2):221-227.
11. Shi L, Fu A K Y, Ip NY (2012) Molecular mechanisms underlying maturation and maintenance of the vertebrate neuromuscular junction. Trends Neurosci 35(7):441-453.
12. Hall AC, Lucas FR, Salinas PC (2000) Axonal remodeling and synaptic differentiation in the cerebellum is regulated by WNT-7a signaling. Cell 100(5):525-535.
13. Umemori H, Linhoff MW, Ornitz DM, Sanes JR (2004) FGF22 and its close relatives are presynaptic organizing molecules in the mammalian brain. Cell 118(2):257-270.
14. Linhoff MW, et al. (2009) An unbiased expression screen for synaptogenic proteins identifies the LRRTM protein family as synaptic organizers. Neuron 61(5):734-749.
15. Siddiqui TJ, Craig AM (2011) Synaptic organizing complexes. Curr Opin Neurobiol 21(1):132-143.
16. Crump JG, Zhen M, Jin Y, Bargmann CI (2001) The SAD-1 kinase regulates presynaptic vesicle clustering and axon termination. Neuron 29(1):115-129.
17. Kishi M, Pan YA, Crump JG, Sanes JR (2005) Mammalian SAD kinases are required for neuronal polarization. Science 307(5711):929-932.
18. Lilley BN, Pan YA, Sanes JR (2013) SAD kinases sculpt axonal arbors of sensory neurons through long- and short-term responses to neurotrophin signals. Neuron 79(1):39-53.
19. Kim J S M, et al. (2008) A chemical-genetic strategy reveals distinct temporal requirements for SAD-1 kinase in neuronal polarization and synapse formation. Neural Dev 3:23.
20. Barnes AP, et al. (2007) LKB1 and SAD kinases define a pathway required for the polarization of cortical neurons. Cell 129(3):549-563.
21. Sanes JR, Lichtman JW (1999) Development of the vertebrate neuromuscular junction. Annu Rev Neurosci 22:389-442.
22. Wu H, Xiong WC, Mei L (2010) To build a synapse: Signaling pathways in neuromuscular junction assembly. Development 137(7):1017-1033.
23. Hagiwara A, Harada K, Hida Y, Kitajima I, Ohtsuka T (2011) Distribution of serine/threonine kinase SAD-B in mouse peripheral nerve synapse. Neuroreport 22(7):319-325.
24. Srinivas S, et al. (2001) Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol 1:4.
25. Rossi J, et al. (2011) Melanocortin-4 receptors expressed by cholinergic neurons regulate energy balance and glucose homeostasis. Cell Metab 13(2):195-204.
26. Tapia JC, et al. (2012) Pervasive synaptic branch removal in the mammalian neuromuscular system at birth. Neuron 74(5):816-829.
27. Parker MJ, Zhao S, Bredt DS, Sanes JR, Feng G (2004) PSD93 regulates synaptic stability at neuronal cholinergic synapses. J Neurosci 24(2):378-388.
28. Krishnaswamy A, Cooper E (2009) An activity-dependent retrograde signal induces the expression of the high-affinity choline transporter in cholinergic neurons. Neuron 61(2):272-286.
29. Schneggenburger R, Forsythe ID (2006) The calyx of Held. Cell Tissue Res 326(2):311-337.
30. Borst J G G, Soria van Hoeve J (2012) The calyx of held synapse: From model synapse to auditory relay. Annu Rev Physiol 74:199-224.
31. Fox MA, Sanes JR (2007) Synaptotagmin I and II are present in distinct subsets of central synapses. J Comp Neurol 503(2):280-296.
32. Solbach S, Celio MR (1991) Ontogeny of the calcium binding protein parvalbumin in the rat nervous system. Anat Embryol (Berl) 184(2):103-124.
33. Hippenmeyer S, et al. (2005) A developmental switch in the response of DRG neurons to ETS transcription factor signaling. PLoS Biol 3(5):e159.
34. Betley JN, et al. (2009) Stringent specificity in the construction of a GABAergic presynaptic inhibitory circuit. Cell 139(1):161-174.
35. Kuba K, Koketsu K (1978) Synaptic events in sympathetic ganglia. Prog Neurobiol 11(2):77-169.
36. Mears SC, Frank E (1997) Formation of specific monosynaptic connections between muscle spindle afferents and motoneurons in the mouse. J Neurosci 17(9):3128-3135.
37. Baas S, et al. (2011) Sugar-free frosting, a homolog of SAD kinase, drives neuralspecific glycan expression in the Drosophila embryo. Development 138(3):553-563.
38. Alvarado-Kristensson M, Rodríguez MJ, Silió V, Valpuesta JM, Carrera AC (2009) SADB phosphorylation of gamma-tubulin regulates centrosome duplication. Nat Cell Biol 11(9):1081-1092.
39. Kneussel M, Wagner W (2013) Myosin motors at neuronal synapses: Drivers of membrane transport and actin dynamics. Nat Rev Neurosci 14(4):233-247.
40. Chi P, Greengard P, Ryan TA (2003) Synaptic vesicle mobilization is regulated by distinct synapsin I phosphorylation pathways at different frequencies. Neuron 38(1):69-78.
41. Inoue E, et al. (2006) SAD: A presynaptic kinase associated with synaptic vesicles and the active zone cytomatrix that regulates neurotransmitter release. Neuron 50(2):261-275.
42. Lewis TL, Jr., Courchet J, Polleux F (2013) Cell biology in neuroscience: Cellular and molecular mechanisms underlying axon formation, growth, and branching. J Cell Biol 202(6):837-848.
43. Hung W, Hwang C, Po MD, Zhen M (2007) Neuronal polarity is regulated by a direct interaction between a scaffolding protein, Neurabin, and a presynaptic SAD-1 kinase in Caenorhabditis elegans. Development 134(2):237-249.
44. Sapir T, et al. (2008) Antagonistic effects of doublecortin and MARK2/Par-1 in the developing cerebral cortex. J Neurosci 28(48):13008-13013.
45. Courchet J, et al. (2013) Terminal axon branching is regulated by the LKB1-NUAK1 kinase pathway via presynaptic mitochondrial capture. Cell 153(7):1510-1525.
46. Fioravante D, Regehr WG (2011) Short-term forms of presynaptic plasticity. Curr Opin Neurobiol 21(2):269-274.
47. Purcell P, et al. (2009) Temporomandibular joint formation requires two distinct hedgehog-dependent steps. Proc Natl Acad Sci USA 106(43):18297-18302.
48. Madisen L, et al. (2010) A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci 13(1):133-140.