Sentryn and SAD Kinase Link the Guided Transport and Capture of Dense Core Vesicles in <i>Caenorhabditis elegans</i>

Ackley, 2005, The two isoforms of the Caenorhabditis elegans leukocyte-common antigen related receptor tyrosine phosphatase PTP-3 function independently in axon guidance and synapse formation., J. Neurosci., 25, 7517, 10.1523/JNEUROSCI.2010-05.2005

Acuna, 2016, How to make an active zone: unexpected universal functional redundancy between RIMs and RIM-BPs., Neuron, 91, 792, 10.1016/j.neuron.2016.07.042

Arribere, 2014, Efficient marker-free recovery of custom genetic modifications with CRISPR/Cas9 in Caenorhabditis elegans., Genetics, 198, 837, 10.1534/genetics.114.169730

Baas, 2011, Hooks and comets: the story of microtubule polarity orientation in the neuron., Dev. Neurobiol., 71, 403, 10.1002/dneu.20818

Banerjee, 2017, Local neuropeptide signaling modulates serotonergic transmission to shape the temporal organization of C. elegans egg-laying behavior., PLoS Genet., 13, e1006697, 10.1371/journal.pgen.1006697

Bhattacharya, 2015, In the proper context: neuropeptide regulation of behavioral transitions during food searching., Worm, 4, e1062971, 10.1080/21624054.2015.1062971

Bhattacharya, 2014, A conserved dopamine-cholecystokinin signaling pathway shapes context-dependent Caenorhabditis elegans behavior., PLoS Genet., 10, e1004584, 10.1371/journal.pgen.1004584

Brenner, 1974, The genetics of C. elegans., Genetics, 77, 71, 10.1093/genetics/77.1.71

Bulgari, 2014, Vesicle capture, not delivery, scales up neuropeptide storage in neuroendocrine terminals., Proc. Natl. Acad. Sci. USA, 111, 3597, 10.1073/pnas.1322170111

Bulgari, 2017, Loss of Huntingtin stimulates capture of retrograde dense-core vesicles to increase synaptic neuropeptide stores., Eur. J. Cell Biol., 96, 402, 10.1016/j.ejcb.2017.01.001

Burton, 1981, Polarity of axoplasmic microtubules in the olfactory nerve of the frog., Proc. Natl. Acad. Sci. USA, 78, 3269, 10.1073/pnas.78.5.3269

Cavolo, 2015, Mycalolide B dissociates dynactin and abolishes retrograde axonal transport of dense-core vesicles., Mol. Biol. Cell, 26, 2664, 10.1091/mbc.E14-11-1564

Cavolo, 2016, Activity induces Fmr1-sensitive synaptic capture of anterograde circulating neuropeptide vesicles., J. Neurosci., 36, 11781, 10.1523/JNEUROSCI.2212-16.2016

Charlie, 2006, Presynaptic UNC-31 (CAPS) is required to activate the G alpha(s) pathway of the Caenorhabditis elegans synaptic signaling network., Genetics, 172, 943, 10.1534/genetics.105.049577

Chen, 2016, The neuropeptides FLP-2 and PDF-1 act in concert to arouse Caenorhabditis elegans locomotion., Genetics, 204, 1151, 10.1534/genetics.116.192898

Chia, 2012, NAB-1 instructs synapse assembly by linking adhesion molecules and F-actin to active zone proteins., Nat. Neurosci., 15, 234, 10.1038/nn.2991

Choi, 2015, Sensory neurons arouse C. elegans locomotion via both glutamate and neuropeptide release., PLoS Genet., 11, e1005359, 10.1371/journal.pgen.1005359

Cool, 1997, Carboxypeptidase E is a regulated secretory pathway sorting receptor: genetic obliteration leads to endocrine disorders in Cpe(fat) mice., Cell, 88, 73, 10.1016/S0092-8674(00)81860-7

Crump, 2001, The SAD-1 kinase regulates presynaptic vesicle clustering and axon termination., Neuron, 29, 115, 10.1016/S0896-6273(01)00184-2

Dai, 2006, SYD-2 liprin-alpha organizes presynaptic active zone formation through ELKS., Nat. Neurosci., 9, 1479, 10.1038/nn1808

Deken, 2005, Redundant localization mechanisms of RIM and ELKS in Caenorhabditis elegans., J. Neurosci., 25, 5975, 10.1523/JNEUROSCI.0804-05.2005

Dickinson, 2013, Engineering the Caenorhabditis elegans genome using Cas9-triggered homologous recombination., Nat. Methods, 10, 1028, 10.1038/nmeth.2641

Edwards, 2008, A novel molecular solution for ultraviolet light detection in Caenorhabditis elegans., PLoS Biol., 6, e198, 10.1371/journal.pbio.0060198

Edwards, 2015, UNC-16 (JIP3) acts through synapse-assembly proteins to inhibit the active transport of cell soma organelles to Caenorhabditis elegans motor neuron axons., Genetics, 201, 117, 10.1534/genetics.115.177345

Edwards, 2015, Synapse-assembly proteins maintain synaptic vesicle cluster stability and regulate synaptic vesicle transport in Caenorhabditis elegans., Genetics, 201, 91, 10.1534/genetics.115.177337

Edwards, 2018, Sentryn acts with a subset of active zone proteins to optimize the localization of synaptic vesicles in Caenorhabditis elegans., Genetics, 210, 947, 10.1534/genetics.118.301466

Fouquet, 2009, Maturation of active zone assembly by Drosophila Bruchpilot., J. Cell Biol., 186, 129, 10.1083/jcb.200812150

Fricker, 1988, Carboxypeptidase E., Annu. Rev. Physiol., 50, 309, 10.1146/annurev.ph.50.030188.001521

Goodwin, 2013, The scaffolding protein SYD-2/liprin-alpha regulates the mobility and polarized distribution of dense-core vesicles in C. elegans motor neurons., PLoS One, 8, e54763, 10.1371/journal.pone.0054763

Goodwin, 2012, Cyclin-dependent kinase 5 regulates the polarized trafficking of neuropeptide-containing dense-core vesicles in Caenorhabditis elegans motor neurons., J. Neurosci., 32, 8158, 10.1523/JNEUROSCI.0251-12.2012

Greenwald, 1980, unc-93 (e1500): a behavioral mutant of Caenorhabditis elegans that defines a gene with a wild type null phenotype., Genetics, 96, 147, 10.1093/genetics/96.1.147

Hall, 1991, Kinesin-related gene unc-104 is required for axonal transport of synaptic vesicles in C. elegans., Cell, 65, 837, 10.1016/0092-8674(91)90391-B

Hammarlund, 2008, CAPS and syntaxin dock dense core vesicles to the plasma membrane in neurons., J. Cell Biol., 180, 483, 10.1083/jcb.200708018

Heidemann, 1981, Polarity orientation of axonal microtubules., J. Cell Biol., 91, 661, 10.1083/jcb.91.3.661

Hoover, 2014, A novel CaM kinase II pathway controls the location of neuropeptide release from Caenorhabditis elegans motor neurons., Genetics, 196, 745, 10.1534/genetics.113.158568

Hu, 2011, A neuropeptide-mediated stretch response links muscle contraction to changes in neurotransmitter release., Neuron, 71, 92, 10.1016/j.neuron.2011.04.021

Hu, 2015, NLP-12 engages different UNC-13 proteins to potentiate tonic and evoked release., J. Neurosci., 35, 1038, 10.1523/JNEUROSCI.2825-14.2015

Hung, 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, 237, 10.1242/dev.02725

Inoue, 2006, SAD: a presynaptic kinase associated with synaptic vesicles and the active zone cytomatrix that regulates neurotransmitter release., Neuron, 50, 261, 10.1016/j.neuron.2006.03.018

Kim, 2008, A chemical-genetic strategy reveals distinct temporal requirements for SAD-1 kinase in neuronal polarization and synapse formation., Neural Dev., 3, 23, 10.1186/1749-8104-3-23

Kim, 2010, C. elegans STRADalpha and SAD cooperatively regulate neuronal polarity and synaptic organization., Development, 137, 93, 10.1242/dev.041459

Kim, 2003, The GIT family of proteins forms multimers and associates with the presynaptic cytomatrix protein Piccolo., J. Biol. Chem., 278, 6291, 10.1074/jbc.M212287200

Kittelmann, 2013, Liprin-alpha/SYD-2 determines the size of dense projections in presynaptic active zones in C. elegans., J. Cell Biol., 203, 849, 10.1083/jcb.201302022

Klassen, 2010, An Arf-like small G protein, ARL-8, promotes the axonal transport of presynaptic cargoes by suppressing vesicle aggregation., Neuron, 66, 710, 10.1016/j.neuron.2010.04.033

Ko, 2003, Interaction between liprin-alpha and GIT1 is required for AMPA receptor targeting., J. Neurosci., 23, 1667, 10.1523/JNEUROSCI.23-05-01667.2003

Ko, 2003, Interaction of the ERC family of RIM-binding proteins with the liprin-alpha family of multidomain proteins., J. Biol. Chem., 278, 42377, 10.1074/jbc.M307561200

Koushika, 2001, A post-docking role for active zone protein Rim., Nat. Neurosci., 4, 997, 10.1038/nn732

Kupfermann, 1991, Functional studies of cotransmission., Physiol. Rev., 71, 683, 10.1152/physrev.1991.71.3.683

Levitan, 2008, Signaling for vesicle mobilization and synaptic plasticity., Mol. Neurobiol., 37, 39, 10.1007/s12035-008-8014-3

Li, 2014, Drosophila Syd-1, liprin-alpha, and protein phosphatase 2A B’ subunit Wrd function in a linear pathway to prevent ectopic accumulation of synaptic materials in distal axons., J. Neurosci., 34, 8474, 10.1523/JNEUROSCI.0409-14.2014

Lim, 2017, Two kinesins drive anterograde neuropeptide transport., Mol. Biol. Cell, 28, 3542, 10.1091/mbc.E16-12-0820

Lim, 2016, Neuroendocrine modulation sustains the C. elegans forward motor state., eLife, 5, 10.7554/eLife.19887

Liu, 2011, RIM-binding protein, a central part of the active zone, is essential for neurotransmitter release., Science, 334, 1565, 10.1126/science.1212991

Liu, 2007, FMRFamide-like neuropeptides and mechanosensory touch receptor neurons regulate male sexual turning behavior in Caenorhabditis elegans., J. Neurosci., 27, 7174, 10.1523/JNEUROSCI.1405-07.2007

Mello, 1991, Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences., EMBO J., 10, 3959, 10.1002/j.1460-2075.1991.tb04966.x

Miller, 2005, Direct observation demonstrates that liprin-alpha is required for trafficking of synaptic vesicles., Curr. Biol., 15, 684, 10.1016/j.cub.2005.02.061

Miller, 1999, Goalpha and diacylglycerol kinase negatively regulate the Gqalpha pathway in C. elegans., Neuron, 24, 323, 10.1016/S0896-6273(00)80847-8

Ohtsuka, 2002, Cast: a novel protein of the cytomatrix at the active zone of synapses that forms a ternary complex with RIM1 and munc13–1., J. Cell Biol., 158, 577, 10.1083/jcb.200202083

Olsen, 2005, Neurotransmitter release regulated by a MALS-liprin-alpha presynaptic complex., J. Cell Biol., 170, 1127, 10.1083/jcb.200503011

Ou, 2010, Two cyclin-dependent kinase pathways are essential for polarized trafficking of presynaptic components., Cell, 141, 846, 10.1016/j.cell.2010.04.011

Owald, 2010, A Syd-1 homologue regulates pre- and postsynaptic maturation in Drosophila., J. Cell Biol., 188, 565, 10.1083/jcb.200908055

Pack-Chung, 2007, A Drosophila kinesin required for synaptic bouton formation and synaptic vesicle transport., Nat. Neurosci., 10, 980, 10.1038/nn1936

Paix, 2014, Scalable and versatile genome editing using linear DNAs with microhomology to Cas9 sites in Caenorhabditis elegans., Genetics, 1347, 10.1534/genetics.114.170423

Patel, 2006, Hierarchical assembly of presynaptic components in defined C. elegans synapses., Nat. Neurosci., 9, 1488, 10.1038/nn1806

Reynolds, 2005, Convergent, RIC-8-dependent Galpha signaling pathways in the Caenorhabditis elegans synaptic signaling network., Genetics, 169, 651, 10.1534/genetics.104.031286

Richmond, 2002, The synaptic vesicle cycle: exocytosis and endocytosis in Drosophila and C. elegans., Curr. Opin. Neurobiol., 12, 499, 10.1016/S0959-4388(02)00360-4

Rindler, 1998, Carboxypeptidase E, a peripheral membrane protein implicated in the targeting of hormones to secretory granules, co-aggregates with granule content proteins at acidic pH., J. Biol. Chem., 273, 31180, 10.1074/jbc.273.47.31180

Schade, 2005, Mutations that rescue the paralysis of Caenorhabditis elegans ric-8 (synembryn) mutants activate the G alpha(s) pathway and define a third major branch of the synaptic signaling network., Genetics, 169, 631, 10.1534/genetics.104.032334

Schoch, 2002, RIM1alpha forms a protein scaffold for regulating neurotransmitter release at the active zone., Nature, 415, 321, 10.1038/415321a

Serra-Pages, 1998, Liprins, a family of LAR transmembrane protein-tyrosine phosphatase-interacting proteins., J. Biol. Chem., 273, 15611, 10.1074/jbc.273.25.15611

Shakiryanova, 2006, Activity-dependent synaptic capture of transiting peptidergic vesicles., Nat. Neurosci., 9, 896, 10.1038/nn1719

Shin, 2003, Association of the kinesin motor KIF1A with the multimodular protein liprin-alpha., J. Biol. Chem., 278, 11393, 10.1074/jbc.M211874200

Sieburth, 2007, PKC-1 regulates secretion of neuropeptides., Nat. Neurosci., 10, 49, 10.1038/nn1810

Sossin, 1991, Biosynthesis and sorting of neuropeptides., Curr. Opin. Neurobiol., 1, 79, 10.1016/0959-4388(91)90013-W

Stefanakis, 2015, Regulatory logic of Pan-neuronal gene expression in C. elegans., Neuron, 87, 733, 10.1016/j.neuron.2015.07.031

Stiernagle, 2006, Maintenance of C. elegans, 10.1895/wormbook.1.101.1

Stigloher, 2011, The presynaptic dense projection of the Caenorhabditis elegans cholinergic neuromuscular junction localizes synaptic vesicles at the active zone through SYD-2/liprin and UNC-10/RIM-dependent interactions., J. Neurosci., 31, 4388, 10.1523/JNEUROSCI.6164-10.2011

Sudhof, 2004, The synaptic vesicle cycle., Annu. Rev. Neurosci., 27, 509, 10.1146/annurev.neuro.26.041002.131412

Sudhof, 2012, The presynaptic active zone., Neuron, 75, 11, 10.1016/j.neuron.2012.06.012

Sulston, 1988, Methods, The Nematode Caenorhabditis elegans, 596

Von Stetina, 2007, Cell-specific microarray profiling experiments reveal a comprehensive picture of gene expression in the C. elegans nervous system., Genome Biol., 8, R135, 10.1186/gb-2007-8-7-r135

Wagh, 2006, Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila., Neuron, 49, 833, 10.1016/j.neuron.2006.02.008

Wagner, 2009, Synaptic scaffolding protein SYD-2 clusters and activates kinesin-3 UNC-104 in C. elegans., Proc. Natl. Acad. Sci. USA, 106, 19605, 10.1073/pnas.0902949106

Wang, 2016, Fusion competent synaptic vesicles persist upon active zone disruption and loss of vesicle docking., Neuron, 91, 777, 10.1016/j.neuron.2016.07.005

Wang, 1997, Rim is a putative Rab3 effector in regulating synaptic-vesicle fusion., Nature, 388, 593, 10.1038/41580

Wang, 2000, The RIM/NIM family of neuronal C2 domain proteins. Interactions with Rab3 and a new class of Src homology 3 domain proteins., J. Biol. Chem., 275, 20033, 10.1074/jbc.M909008199

Wang, 2002, A family of RIM-binding proteins regulated by alternative splicing: implications for the genesis of synaptic active zones., Proc. Natl. Acad. Sci. USA, 99, 14464, 10.1073/pnas.182532999

Weimer, 2006, Preservation of C. elegans tissue via high-pressure freezing and freeze-substitution for ultrastructural analysis and immunocytochemistry., Methods Mol. Biol., 351, 203

Weimer, 2006, UNC-13 and UNC-10/rim localize synaptic vesicles to specific membrane domains., J. Neurosci., 26, 8040, 10.1523/JNEUROSCI.2350-06.2006

White, 1986, The structure of the nervous system of the nematode Caenorhabditis elegans., Philos. Trans. R. Soc. Lond. B Biol. Sci., 314, 1, 10.1098/rstb.1986.0056

Wong, 2012, Neuropeptide delivery to synapses by long-range vesicle circulation and sporadic capture., Cell, 148, 1029, 10.1016/j.cell.2011.12.036

Wu, 2013, The balance between capture and dissociation of presynaptic proteins controls the spatial distribution of synapses., Neuron, 78, 994, 10.1016/j.neuron.2013.04.035

Wyszynski, 2002, Interaction between GRIP and liprin-alpha/SYD2 is required for AMPA receptor targeting., Neuron, 34, 39, 10.1016/S0896-6273(02)00640-2

Xuan, 2017, Clarinet (CLA-1), a novel active zone protein required for synaptic vesicle clustering and release., eLife, 6, e29276, 10.7554/eLife.29276

Yeh, 2005, Identification of genes involved in synaptogenesis using a fluorescent active zone marker in Caenorhabditis elegans., J. Neurosci., 25, 3833, 10.1523/JNEUROSCI.4978-04.2005

Zhen, 1999, The liprin protein SYD-2 regulates the differentiation of presynaptic termini in C. elegans., Nature, 401, 371, 10.1038/43886

Zheng, 2014, The vesicle protein SAM-4 regulates the processivity of synaptic vesicle transport., PLoS Genet., 10, e1004644, 10.1371/journal.pgen.1004644