@article{hodorovich_harris_burton_neese_bieler_chudasama_marsden_2024, title={Effects of 4 Testing Arena Sizes and 11 Types of Embryo Media on Sensorimotor Behaviors in Wild-Type and <i>chd7</i> Mutant Zebrafish Larvae}, volume={2}, ISSN={["1557-8542"]}, url={https://doi.org/10.1089/zeb.2023.0052}, DOI={10.1089/zeb.2023.0052}, abstractNote={The larval zebrafish is a highly versatile model across research disciplines, and the expanding use of behavioral analysis has contributed to many advances in neuropsychiatric, developmental, and toxicological studies, often through large-scale chemical and genetic screens. In the absence of standardized approaches to larval zebrafish behavior analysis, however, it is critical to understand the impact on behavior of experimental variables such as the size of testing arenas and the choice of embryo medium. Using a custom-built, modular high-throughput testing system, we examined the effects of 4 testing arena sizes and 11 types of embryo media on conserved sensorimotor behaviors in zebrafish larvae. Our data show that testing arena size impacts acoustic startle sensitivity and kinematics, as well as spontaneous locomotion and thigmotaxis, with fish tested in larger arenas displaying reduced startle sensitivity and increased locomotion. We also find that embryo media can dramatically affect startle sensitivity, kinematics, habituation, and prepulse inhibition, as well as spontaneous swimming, turning, and overall activity. Common medium components such as methylene blue and high calcium concentration consistently reduced startle sensitivity and locomotion. To further address how the choice of embryo medium can impact phenotype expression in zebrafish models of disease, we reared chd7 mutant larvae, a model of CHARGE syndrome with previously characterized morphological and behavioral phenotypes, in five different types of media and observed impacts on all phenotypes. By defining the effects of these key extrinsic factors on larval zebrafish behavior, these data can help researchers select the most appropriate conditions for their specific research questions, particularly for genetic and chemical screens.}, journal={ZEBRAFISH}, author={Hodorovich, Dana R. and Harris, Tiara Fryer and Burton, Derek F. and Neese, Katie M. and Bieler, Rachael A. and Chudasama, Vimal and Marsden, Kurt C.}, year={2024}, month={Feb} }
 @article{green_wall_weeks_mattingly_marsden_planchart_2023, title={Developmental cadmium exposure disrupts zebrafish vestibular calcium channels interfering with otolith formation and inner ear function}, volume={96}, ISSN={["1872-9711"]}, DOI={10.1016/j.neuro.2023.04.006}, abstractNote={Dizziness or balance problems are estimated to affect approximately 3.3 million children aged three to 17 years. These disorders develop from a breakdown in the balance control system and can be caused by anything that affects the inner ear or the brain, including exposure to environmental toxicants. One potential environmental toxicant linked to balance disorders is cadmium, an extremely toxic metal that occurs naturally in the earth's crust and is released as a byproduct of industrial processes. Cadmium is associated with balance and vestibular dysfunction in adults exposed occupationally, but little is known about the developmental effects of low-concentration cadmium exposure. Our findings indicate that zebrafish exposed to 10-60 parts per billion (ppb) cadmium from four hours post-fertilization (hpf) to seven days post-fertilization (dpf) exhibit abnormal behaviors, including pronounced increases in auditory sensitivity and circling behavior, both of which are linked to reductions in otolith growth and are rescued by the addition of calcium to the media. Pharmacological intervention shows that agonist-induced activation of the P2X calcium ion channel in the presence of cadmium restores otolith size. In conclusion, cadmium-induced ototoxicity is linked to vestibular-based behavioral abnormalities and auditory sensitivity following developmental exposure, and calcium ion channel function is associated with these defects.}, journal={NEUROTOXICOLOGY}, author={Green, Adrian J. and Wall, Alex R. and Weeks, Ryan D. and Mattingly, Carolyn J. and Marsden, Kurt C. and Planchart, Antonio}, year={2023}, month={May}, pages={129–139} }
 @article{hodorovich_harris_burton_neese_bieler_chudasama_marsden_2023, title={Effects of 4 testing arena sizes and 11 types of embryo media on sensorimotor behaviors in wild-type andchd7mutant zebrafish larvae}, url={https://doi.org/10.1101/2023.07.31.551330}, DOI={10.1101/2023.07.31.551330}, abstractNote={Abstract}, author={Hodorovich, Dana R. and Harris, Tiara Fryer and Burton, Derek and Neese, Katie and Bieler, Rachael and Chudasama, Vimal and Marsden, Kurt. C}, year={2023}, month={Aug} }
 @article{hodorovich_lindsley_berry_burton_marsden_2023, title={Morphological and sensorimotor phenotypes in a zebrafish CHARGE syndrome model are domain-dependent}, volume={1}, ISSN={["1601-183X"]}, url={https://doi.org/10.1111/gbb.12839}, DOI={10.1111/gbb.12839}, abstractNote={Abstract}, journal={GENES BRAIN AND BEHAVIOR}, author={Hodorovich, Dana R. R. and Lindsley, Patrick M. M. and Berry, Austen A. A. and Burton, Derek F. F. and Marsden, Kurt C. C.}, year={2023}, month={Jan} }
 @article{hodorovich_lindsley_berry_burton_marsden_2022, title={Morphological and sensorimotor phenotypes in a zebrafish CHARGE syndrome model are domain-dependent}, url={https://doi.org/10.1101/2022.07.14.499979}, DOI={10.1101/2022.07.14.499979}, abstractNote={Abstract}, author={Hodorovich, Dana R. and Lindsley, Patrick M. and Berry, Austen A. and Burton, Derek F. and Marsden, Kurt C.}, year={2022}, month={Jul} }
 @article{martin_bereman_marsden_2022, title={The Cyanotoxin 2,4-DAB Reduces Viability and Causes Behavioral and Molecular Dysfunctions Associated with Neurodegeneration in Larval Zebrafish}, volume={40}, ISSN={["1476-3524"]}, url={https://doi.org/10.1007/s12640-021-00465-4}, DOI={10.1007/s12640-021-00465-4}, abstractNote={Abstract}, number={2}, journal={NEUROTOXICITY RESEARCH}, publisher={Springer Science and Business Media LLC}, author={Martin, Rubia M. and Bereman, Michael S. and Marsden, Kurt C.}, year={2022}, month={Jan} }
 @article{meserve_nelson_marsden_hsu_echeverry_jain_wolman_pereda_granato_2021, title={A forward genetic screen identifies Dolk as a regulator of startle magnitude through the potassium channel subunit Kv1.1}, volume={17}, ISSN={["1553-7404"]}, url={https://doi.org/10.1371/journal.pgen.1008943}, DOI={10.1371/journal.pgen.1008943}, abstractNote={The acoustic startle response is an evolutionarily conserved avoidance behavior. Disruptions in startle behavior, particularly startle magnitude, are a hallmark of several human neurological disorders. While the neural circuitry underlying startle behavior has been studied extensively, the repertoire of genes and genetic pathways that regulate this locomotor behavior has not been explored using an unbiased genetic approach. To identify such genes, we took advantage of the stereotypic startle behavior in zebrafish larvae and performed a forward genetic screen coupled with whole genome analysis. We uncovered mutations in eight genes critical for startle behavior, including two genes encoding proteins associated with human neurological disorders, Dolichol kinase (Dolk), a broadly expressed regulator of the glycoprotein biosynthesis pathway, and the potassium Shaker-like channel subunit Kv1.1. We demonstrate that Kv1.1 and Dolk play critical roles in the spinal cord to regulate movement magnitude during the startle response and spontaneous swim movements. Moreover, we show that Kv1.1 protein is mislocalized in dolk mutants, suggesting they act in a common genetic pathway. Combined, our results identify a diverse set of eight genes, all associated with human disorders, that regulate zebrafish startle behavior and reveal a previously unappreciated role for Dolk and Kv1.1 in regulating movement magnitude via a common genetic pathway.}, number={6}, journal={PLOS GENETICS}, publisher={Public Library of Science (PLoS)}, author={Meserve, Joy H. and Nelson, Jessica C. and Marsden, Kurt C. and Hsu, Jerry and Echeverry, Fabio A. and Jain, Roshan A. and Wolman, Marc A. and Pereda, Alberto E. and Granato, Michael}, editor={Moens, CeciliaEditor}, year={2021}, month={Jun} }
 @article{martin_bereman_marsden_2021, title={BMAA and MCLR Interact to Modulate Behavior and Exacerbate Molecular Changes Related to Neurodegeneration in Larval Zebrafish}, volume={179}, ISSN={["1096-0929"]}, url={https://doi.org/10.1093/toxsci/kfaa178}, DOI={10.1093/toxsci/kfaa178}, abstractNote={Abstract}, number={2}, journal={TOXICOLOGICAL SCIENCES}, publisher={Oxford University Press (OUP)}, author={Martin, Rubia M. and Bereman, Michael S. and Marsden, Kurt C.}, year={2021}, month={Feb}, pages={251–261} }
 @article{lasseigne_echeverry_ijaz_michel_martin_marsh_trujillo_marsden_pereda_miller_2021, title={Electrical synaptic transmission requires a postsynaptic scaffolding protein}, volume={10}, ISSN={["2050-084X"]}, url={https://doi.org/10.7554/eLife.66898}, DOI={10.7554/eLife.66898}, abstractNote={Electrical synaptic transmission relies on neuronal gap junctions containing channels constructed by Connexins. While at chemical synapses neurotransmitter-gated ion channels are critically supported by scaffolding proteins, it is unknown if channels at electrical synapses require similar scaffold support. Here, we investigated the functional relationship between neuronal Connexins and Zonula Occludens 1 (ZO1), an intracellular scaffolding protein localized to electrical synapses. Using model electrical synapses in zebrafish Mauthner cells, we demonstrated that ZO1 is required for robust synaptic Connexin localization, but Connexins are dispensable for ZO1 localization. Disrupting this hierarchical ZO1/Connexin relationship abolishes electrical transmission and disrupts Mauthner cell-initiated escape responses. We found that ZO1 is asymmetrically localized exclusively postsynaptically at neuronal contacts where it functions to assemble intercellular channels. Thus, forming functional neuronal gap junctions requires a postsynaptic scaffolding protein. The critical function of a scaffolding molecule reveals an unanticipated complexity of molecular and functional organization at electrical synapses.}, journal={ELIFE}, author={Lasseigne, Abagael M. and Echeverry, Fabio A. and Ijaz, Sundas and Michel, Jennifer Carlisle and Martin, E. Anne and Marsh, Audrey J. and Trujillo, Elisa and Marsden, Kurt C. and Pereda, Alberto E. and Miller, Adam C.}, year={2021}, month={Apr} }
 @article{kikel-coury_green_nichols_zellmer_pai_hedlund_marsden_smith_2021, title={Pioneer Axons Utilize a Dcc Signaling-Mediated Invasion Brake to Precisely Complete Their Pathfinding Odyssey}, volume={41}, ISSN={["1529-2401"]}, DOI={10.1523/JNEUROSCI.0212-21.2021}, abstractNote={Axons navigate through the embryo to construct a functional nervous system. A missing part of the axon navigation puzzle is how a single axon traverses distinct anatomic choice points through its navigation. The dorsal root ganglia (DRG) neurons experience such choice points. First, they navigate to the dorsal root entry zone (DREZ), then halt navigation in the peripheral nervous system to invade the spinal cord, and then reinitiate navigation inside the CNS. Here, we used time-lapse super-resolution imaging in zebrafish DRG pioneer neurons to investigate how embryonic axons control their cytoskeleton to navigate to and invade at the correct anatomic position. We found that invadopodia components form in the growth cone even during filopodia-based navigation, but only stabilize when the axon is at the spinal cord entry location. Further, we show that intermediate levels of DCC and cAMP, as well as Rac1 activation, subsequently engage an axon invasion brake. Our results indicate that actin-based invadopodia components form in the growth cone and disruption of the invasion brake causes axon entry defects and results in failed behavioral responses, thereby demonstrating the importance of regulating distinct actin populations during navigational challenges. SIGNIFICANCE STATEMENT Correct spatiotemporal navigation of neuronal growth cones is dependent on extracellular navigational cues and growth cone dynamics. Here, we link dcc-mediated signaling to actin-based invadopodia and filopodia dynamics during pathfinding and entry into the spinal cord using an in vivo model of dorsal root ganglia (DRG) sensory axons. We reveal a molecularly-controlled brake on invadopodia stabilization until the sensory neuron growth cone is present at the dorsal root entry zone (DREZ), which is ultimately essential for growth cone entry into the spinal cord and behavioral response.}, number={31}, journal={JOURNAL OF NEUROSCIENCE}, author={Kikel-Coury, Nina L. and Green, Lauren A. and Nichols, Evan L. and Zellmer, Abigail M. and Pai, Sanjana and Hedlund, Sam A. and Marsden, Kurt C. and Smith, Cody J.}, year={2021}, month={Aug}, pages={6617–6636} }
 @article{martin_bereman_marsden_2021, title={The cyanotoxin 2,4-DAB enhances mortality and causes behavioral and molecular dysfunctions associated with neurodegeneration in larval zebrafish}, volume={10}, url={https://doi.org/10.1101/2021.10.13.464292}, DOI={10.1101/2021.10.13.464292}, abstractNote={Abstract}, publisher={Cold Spring Harbor Laboratory}, author={Martin, Rubia M. and Bereman, Michael S. and Marsden, Kurt C.}, year={2021}, month={Oct} }
 @article{meserve_nelson_marsden_hsu_echeverry_jain_wolman_pereda_granato_2020, title={A forward genetic screen identifies Dolk as a regulator of startle magnitude through the potassium channel subunit Kv1.1}, volume={6}, url={https://doi.org/10.1101/2020.06.19.161240}, DOI={10.1101/2020.06.19.161240}, abstractNote={Abstract}, publisher={Cold Spring Harbor Laboratory}, author={Meserve, Joy H. and Nelson, Jessica C. and Marsden, Kurt C. and Hsu, Jerry and Echeverry, Fabio A. and Jain, Roshan A. and Wolman, Marc A. and Pereda, Alberto E. and Granato, Michael}, year={2020}, month={Jun} }
 @article{martin_bereman_marsden_2020, title={Exposure to a mixture of BMAA and MCLR synergistically modulates behavior in larval zebrafish while exacerbating molecular changes related to neurodegeneration}, volume={7}, url={https://doi.org/10.1101/2020.07.15.205617}, DOI={10.1101/2020.07.15.205617}, abstractNote={Abstract}, publisher={Cold Spring Harbor Laboratory}, author={Martin, Rubia M. and Bereman, Michael S. and Marsden, Kurt C.}, year={2020}, month={Jul} }
 @article{bremer_marsden_miller_granato_2019, title={The ubiquitin ligase PHR promotes directional regrowth of spinal zebrafish axons}, volume={2}, ISSN={["2399-3642"]}, url={https://doi.org/10.1038/s42003-019-0434-2}, DOI={10.1038/s42003-019-0434-2}, abstractNote={Abstract}, number={1}, journal={COMMUNICATIONS BIOLOGY}, publisher={Springer Science and Business Media LLC}, author={Bremer, Juliane and Marsden, Kurt C. and Miller, Adam and Granato, Michael}, year={2019}, month={May} }
 @article{marsden_jain_wolman_echeverry_nelson_hayer_miltenberg_pereda_granato_2018, title={A Cyfip2-Dependent Excitatory Interneuron Pathway Establishes the Innate Startle Threshold}, volume={23}, ISSN={["2211-1247"]}, url={http://europepmc.org/articles/PMC6642828}, DOI={10.1016/j.celrep.2018.03.095}, abstractNote={Sensory experiences dynamically modify whether animals respond to a given stimulus, but it is unclear how innate behavioral thresholds are established. Here, we identify molecular and circuit-level mechanisms underlying the innate threshold of the zebrafish startle response. From a forward genetic screen, we isolated five mutant lines with reduced innate startle thresholds. Using whole-genome sequencing, we identify the causative mutation for one line to be in the fragile X mental retardation protein (FMRP)-interacting protein cyfip2. We show that cyfip2 acts independently of FMRP and that reactivation of cyfip2 restores the baseline threshold after phenotype onset. Finally, we show that cyfip2 regulates the innate startle threshold by reducing neural activity in a small group of excitatory hindbrain interneurons. Thus, we identify a selective set of genes critical to establishing an innate behavioral threshold and uncover a circuit-level role for cyfip2 in this process.}, number={3}, journal={CELL REPORTS}, author={Marsden, Kurt C. and Jain, Roshan A. and Wolman, Marc A. and Echeverry, Fabio A. and Nelson, Jessica C. and Hayer, Katharina E. and Miltenberg, Ben and Pereda, Alberto E. and Granato, Michael}, year={2018}, month={Apr}, pages={878–887} }
 @article{jain_wolman_marsden_nelson_shoenhard_echeverry_szi_bell_skinner_cobbs_et al._2018, title={A Forward Genetic Screen in Zebrafish Identifies the G-Protein-Coupled Receptor CaSR as a Modulator of Sensorimotor Decision Making}, volume={28}, ISSN={["1879-0445"]}, url={http://europepmc.org/articles/PMC5940496}, DOI={10.1016/j.cub.2018.03.025}, abstractNote={<h2>Summary</h2> Animals continuously integrate sensory information and select contextually appropriate responses. Here, we show that zebrafish larvae select a behavioral response to acoustic stimuli from a pre-existing choice repertoire in a context-dependent manner. We demonstrate that this sensorimotor choice is modulated by stimulus quality and history, as well as by neuromodulatory systems—all hallmarks of more complex decision making. Moreover, from a genetic screen coupled with whole-genome sequencing, we identified eight mutants with deficits in this sensorimotor choice, including mutants of the vertebrate-specific G-protein-coupled extracellular calcium-sensing receptor (<i>CaSR</i>), whose function in the nervous system is not well understood. We demonstrate that <i>CaSR</i> promotes sensorimotor decision making acutely through Gα<sub>i/o</sub> and Gα<sub>q/11</sub> signaling, modulated by clathrin-mediated endocytosis. Combined, our results identify the first set of genes critical for behavioral choice modulation in a vertebrate and reveal an unexpected critical role for <i>CaSR</i> in sensorimotor decision making.}, number={9}, journal={CURRENT BIOLOGY}, author={Jain, Roshan A. and Wolman, Marc A. and Marsden, Kurt C. and Nelson, Jessica C. and Shoenhard, Hannah and Echeverry, Fabio A. and Szi, Christina and Bell, Hannah and Skinner, Julianne and Cobbs, Emilia N. and et al.}, year={2018}, month={May}, pages={1357-+} }
 @article{miller_whitebirch_shah_marsden_granato_o'brien_moens_2017, title={A genetic basis for molecular asymmetry at vertebrate electrical synapses}, volume={1}, DOI={10.1101/102319}, abstractNote={Abstract}, publisher={Cold Spring Harbor Laboratory}, author={Miller, Adam C and Whitebirch, Alex C and Shah, Arish N and Marsden, Kurt C and Granato, Michael and O'Brien, John and Moens, Cecilia B}, year={2017}, month={Jan} }
 @article{wolman_jain_marsden_bell_skinner_hayer_hogenesch_granato_2015, title={A Genome-wide Screen Identifies PAPP-AA-Mediated IGFR Signaling as a Novel Regulator of Habituation Learning}, volume={85}, DOI={10.1016/j.neuron.2015.02.025}, abstractNote={Habituation represents a fundamental form of learning, yet the underlying molecular genetic mechanisms are not well defined. Here we report on a genome-wide genetic screen, coupled with whole-genome sequencing, that identified 14 zebrafish startle habituation mutants including mutants of the vertebrate-specific gene pregnancy-associated plasma protein-aa (pappaa). PAPP-AA encodes an extracellular metalloprotease known to increase IGF bioavailability, thereby enhancing IGF receptor signaling. We find that pappaa is expressed by startle circuit neurons, and expression of wild-type but not a metalloprotease-inactive version of pappaa restores habituation in pappaa mutants. Furthermore, acutely inhibiting IGF1R function in wild-type reduces habituation, while activation of IGF1R downstream effectors in pappaa mutants restores habituation, demonstrating that pappaa promotes learning by acutely and locally increasing IGF bioavailability. In sum, our results define the first functional gene set for habituation learning in a vertebrate and identify PAPPAA-regulated IGF signaling as a novel mechanism regulating habituation learning.}, number={6}, journal={Neuron}, publisher={Elsevier BV}, author={Wolman, Marc A. and Jain, Roshan A. and Marsden, Kurt C. and Bell, Hannah and Skinner, Julianne and Hayer, Katharina E. and Hogenesch, John B. and Granato, Michael}, year={2015}, month={Mar}, pages={1200–1211} }
 @article{wolman_jain_marsden_bell_skinner_hayer_hogenesch_granato_2015, title={A Genome-wide Screen Identifies PAPP-AA-Mediated IGFR Signaling as a Novel Regulator of Habituation Learning}, volume={87}, DOI={10.1016/j.neuron.2015.08.009}, abstractNote={(Neuron 85, 1200–1211; March 18, 2015) In the original publication, Figure 6 did not accurately reflect the pappaap170 genotypes analyzed for habituation. The corrected version of the figure is shown below, and this has now been corrected in the article online. A Genome-wide Screen Identifies PAPP-AA-Mediated IGFR Signaling as a Novel Regulator of Habituation LearningWolman et al.NeuronMarch 5, 2015In BriefThrough a forward genetic screen in zebrafish, Wolman et al. isolate the first functional vertebrate gene set for habituation learning and identify pregnancy-associated plasma protein aa (PAPP-AA)-regulated IGF signaling as a novel mechanism underlying habituation learning. Full-Text PDF Open Archive}, number={4}, journal={Neuron}, publisher={Elsevier BV}, author={Wolman, Marc A. and Jain, Roshan A. and Marsden, Kurt C. and Bell, Hannah and Skinner, Julianne and Hayer, Katharina E. and Hogenesch, John B. and Granato, Michael}, year={2015}, month={Aug}, pages={906–907} }
 @article{marsden_granato_2015, title={In Vivo Ca2+ Imaging Reveals that Decreased Dendritic Excitability Drives Startle Habituation}, volume={13}, DOI={10.1016/j.celrep.2015.10.060}, abstractNote={Exposure to repetitive startling stimuli induces habitation, a simple form of learning. Despite its simplicity, the precise cellular mechanisms by which repeated stimulation converts a robust behavioral response to behavioral indifference are unclear. Here, we use head-restrained zebrafish larvae to monitor subcellular Ca(2+) dynamics in Mauthner neurons, the startle command neurons, during startle habituation in vivo. Using the Ca(2+) reporter GCaMP6s, we find that the amplitude of Ca(2+) signals in the lateral dendrite of the Mauthner neuron determines startle probability and that depression of this dendritic activity rather than downstream inhibition mediates glycine and N-methyl-D-aspartate (NMDA)-receptor-dependent short-term habituation. Combined, our results suggest a model for habituation learning in which increased inhibitory drive from feedforward inhibitory neurons combined with decreased excitatory input from auditory afferents decreases dendritic and Mauthner neuron excitability.}, number={9}, journal={Cell Reports}, publisher={Elsevier BV}, author={Marsden, Kurt C. and Granato, Michael}, year={2015}, pages={1733–1740} }
 @article{butler_iben_marsden_epstein_granato_weinstein_2015, title={SNPfisher: tools for probing genetic variation in laboratory-reared zebrafish}, volume={142}, DOI={10.1242/dev.118786}, abstractNote={Single nucleotide polymorphisms (SNPs) are the benchmark molecular markers for modern genomics. Until recently, relatively few SNPs were known in the zebrafish genome. The use of next-generation sequencing for the positional cloning of zebrafish mutations has increased the number of known SNP positions dramatically. Still, the identified SNP variants remain under-utilized, owing to scant annotation of strain specificity and allele frequency. To address these limitations, we surveyed SNP variation in three common laboratory zebrafish strains using whole-genome sequencing. This survey identified an average of 5.04 million SNPs per strain compared with the Zv9 reference genome sequence. By comparing the three strains, 2.7 million variants were found to be strain specific, whereas the remaining variants were shared among all (2.3 million) or some of the strains. We also demonstrate the broad usefulness of our identified variants by validating most in independent populations of the same laboratory strains. We have made all of the identified SNPs accessible through ‘SNPfisher’, a searchable online database (snpfisher.nichd.nih.gov). The SNPfisher website includes the SNPfisher Variant Reporter tool, which provides the genomic position, alternate allele read frequency, strain specificity, restriction enzyme recognition site changes and flanking primers for all SNPs and Indels in a user-defined gene or region of the zebrafish genome. The SNPfisher site also contains links to display our SNP data in the UCSC genome browser. The SNPfisher tools will facilitate the use of SNP variation in zebrafish research as well as vertebrate genome evolution.}, number={8}, journal={Development}, publisher={The Company of Biologists}, author={Butler, M. G. and Iben, J. R. and Marsden, K. C. and Epstein, J. A. and Granato, M. and Weinstein, B. M.}, year={2015}, month={Mar}, pages={1542–1552} }
 @article{perni_marsden_escobar_hollingworth_baylor_franzini-armstrong_2015, title={Structural and functional properties of ryanodine receptor type 3 in zebrafish tail muscle}, volume={145}, DOI={10.1085/jgp.201411303}, abstractNote={The ryanodine receptor (RyR)1 isoform of the sarcoplasmic reticulum (SR) Ca2+ release channel is an essential component of all skeletal muscle fibers. RyR1s are detectable as “junctional feet” (JF) in the gap between the SR and the plasmalemma or T-tubules, and they are required for excitation–contraction (EC) coupling and differentiation. A second isoform, RyR3, does not sustain EC coupling and differentiation in the absence of RyR1 and is expressed at highly variable levels. Anatomically, RyR3 expression correlates with the presence of parajunctional feet (PJF), which are located on the sides of the SR junctional cisternae in an arrangement found only in fibers expressing RyR3. In frog muscle fibers, the presence of RyR3 and PJF correlates with the occurrence of Ca2+ sparks, which are elementary SR Ca2+ release events of the EC coupling machinery. Here, we explored the structural and functional roles of RyR3 by injecting zebrafish (Danio rerio) one-cell stage embryos with a morpholino designed to specifically silence RyR3 expression. In zebrafish larvae at 72 h postfertilization, fast-twitch fibers from wild-type (WT) tail muscles had abundant PJF. Silencing resulted in a drop of the PJF/JF ratio, from 0.79 in WT fibers to 0.03 in the morphants. The frequency with which Ca2+ sparks were detected dropped correspondingly, from 0.083 to 0.001 sarcomere−1 s−1. The few Ca2+ sparks detected in morphant fibers were smaller in amplitude, duration, and spatial extent compared with those in WT fibers. Despite the almost complete disappearance of PJF and Ca2+ sparks in morphant fibers, these fibers looked structurally normal and the swimming behavior of the larvae was not affected. This paper provides important evidence that RyR3 is the main constituent of the PJF and is the main contributor to the SR Ca2+ flux underlying Ca2+ sparks detected in fully differentiated frog and fish fibers.}, number={3}, journal={The Journal of General Physiology}, publisher={Rockefeller University Press}, author={Perni, Stefano and Marsden, Kurt C. and Escobar, Matias and Hollingworth, Stephen and Baylor, Stephen M. and Franzini-Armstrong, Clara}, year={2015}, month={Feb}, pages={173–184} }
 @article{perni_marsden_escobar_hollingworth_baylor_franzini-armstrong_2015, title={Structural and functional properties of ryanodine receptor type 3 in zebrafish tail muscle}, volume={145}, DOI={10.1085/jgp.20141130302112015c}, abstractNote={The ryanodine receptor (RyR)1 isoform of the sarcoplasmic reticulum (SR) Ca2+ release channel is an essential component of all skeletal muscle fibers. RyR1s are detectable as “junctional feet” (JF) in the gap between the SR and the plasmalemma or T-tubules, and they are required for excitation–contraction (EC) coupling and differentiation. A second isoform, RyR3, does not sustain EC coupling and differentiation in the absence of RyR1 and is expressed at highly variable levels. Anatomically, RyR3 expression correlates with the presence of parajunctional feet (PJF), which are located on the sides of the SR junctional cisternae in an arrangement found only in fibers expressing RyR3. In frog muscle fibers, the presence of RyR3 and PJF correlates with the occurrence of Ca2+ sparks, which are elementary SR Ca2+ release events of the EC coupling machinery. Here, we explored the structural and functional roles of RyR3 by injecting zebrafish (Danio rerio) one-cell stage embryos with a morpholino designed to specifically silence RyR3 expression. In zebrafish larvae at 72 h postfertilization, fast-twitch fibers from wild-type (WT) tail muscles had abundant PJF. Silencing resulted in a drop of the PJF/JF ratio, from 0.79 in WT fibers to 0.03 in the morphants. The frequency with which Ca2+ sparks were detected dropped correspondingly, from 0.083 to 0.001 sarcomere−1 s−1. The few Ca2+ sparks detected in morphant fibers were smaller in amplitude, duration, and spatial extent compared with those in WT fibers. Despite the almost complete disappearance of PJF and Ca2+ sparks in morphant fibers, these fibers looked structurally normal and the swimming behavior of the larvae was not affected. This paper provides important evidence that RyR3 is the main constituent of the PJF and is the main contributor to the SR Ca2+ flux underlying Ca2+ sparks detected in fully differentiated frog and fish fibers.}, number={3}, journal={The Journal of General Physiology}, publisher={Rockefeller University Press}, author={Perni, Stefano and Marsden, Kurt C. and Escobar, Matias and Hollingworth, Stephen and Baylor, Stephen M. and Franzini-Armstrong, Clara}, year={2015}, month={Feb}, pages={253–253} }
 @article{casimiro_sossa_uzunova_beattie_marsden_carroll_2011, title={mGluR and NMDAR activation internalize distinct populations of AMPARs}, volume={48}, DOI={10.1016/j.mcn.2011.07.007}, abstractNote={Activation of metabotropic- (mGluRs) or NMDA-type glutamate receptors (NMDARs) each can induce long-term depression (LTD) of synaptic transmission in CA1 hippocampal neurons. These two forms of LTD are triggered by diverse signaling pathways yet both are expressed by the internalization of AMPA-type glutamate receptors (AMPARs). An unanswered question remains as to whether the convergence of the mGluR and NMDAR signaling pathways on AMPAR endocytosis renders these two forms of plasticity functionally equivalent, with both pathways inducing endocytosis of the same population of synaptic AMPARs. We now report evidence that these pathways couple to the endocytosis of distinct populations of AMPARs defined by their mobility in the membrane surface. NMDAR activation enhances removal of surface AMPARs that rapidly cycle into and out of the membrane surface, while activation of mGluRs with DHPG results in the internalization of a non-mobile population of AMPARs. Glutamate Receptor Interacting Proteins 1 and 2 (GRIP1/2) play a key role in defining the non-cycling receptor population. GRIP1/2 knockdown with siRNA increases the proportion of rapidly cycling surface AMPARs and inhibits mGluR- but not NMDAR-mediated AMPAR internalization. Additionally, we find that mGluR activation dissociates surface AMPARs from GRIP1/2 while stimulation of NMDARs elicits the loss of membrane receptors not bound to GRIP1/2. We propose that these two receptor pathways can drive the endocytosis of distinct populations of AMPARs: NMDARs activation induces the endocytosis of rapidly cycling surface AMPARs not directly associated with GRIP1/2 while mGluR activation induces the endocytosis of non-cycling GRIP-bound surface AMPARs.}, number={2}, journal={Molecular and Cellular Neuroscience}, publisher={Elsevier BV}, author={Casimiro, Tanya M. and Sossa, Kenneth G. and Uzunova, Genoveva and Beattie, Jennifer B. and Marsden, Kurt C. and Carroll, Reed C.}, year={2011}, month={Oct}, pages={161–170} }
 @article{marsden_shemesh_bayer_carroll_2010, title={Selective translocation of Ca2+/calmodulin protein kinase II  (CaMKII ) to inhibitory synapses}, volume={107}, DOI={10.1073/pnas.1010346107}, abstractNote={
            Ca
            2+
            /Calmodulin protein kinase IIα (CaMKIIα) has a central role in regulating neuronal excitability. It is well established that CaMKIIα translocates to excitatory synapses following strong glutamatergic stimuli that induce NMDA-receptor (NMDAR)-dependent long-term potentiation in CA1 hippocampal neurons. We now show that CaMKIIα translocates to inhibitory but not excitatory synapses in response to more moderate NMDAR-activating stimuli that trigger GABA
            A
            -receptor (GABA
            A
            R) insertion and enhance inhibitory transmission. Such moderate NMDAR activation causes Thr286 autophosphorylation of CaMKIIα, which our results demonstrate is necessary and sufficient, under basal conditions, to localize CaMKIIα at inhibitory synapses and enhance surface GABA
            A
            R expression. Although stronger glutamatergic stimulation coupled to AMPA receptor insertion also elicits Thr286 autophosphorylation, accumulation of CaMKIIα at inhibitory synapses is prevented under these conditions by the phosphatase calcineurin. This preferential targeting of CaMKIIα to glutamatergic or GABAergic synapses provides neurons with a mechanism whereby activity can selectively potentiate excitation or inhibition through a single kinase mediator.
          }, number={47}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Marsden, K. C. and Shemesh, A. and Bayer, K. U. and Carroll, R. C.}, year={2010}, month={Nov}, pages={20559–20564} }
 @article{weinger_omari_marsden_raine_shafit-zagardo_2009, title={Up-Regulation of Soluble Axl and Mer Receptor Tyrosine Kinases Negatively Correlates with Gas6 in Established Multiple Sclerosis Lesions}, volume={175}, DOI={10.2353/ajpath.2009.080807}, abstractNote={Multiple sclerosis is a disease that is characterized by inflammation, demyelination, and axonal damage; it ultimately forms gliotic scars and lesions that severely compromise the function of the central nervous system. Evidence has shown previously that altered growth factor receptor signaling contributes to lesion formation, impedes recovery, and plays a role in disease progression. Growth arrest-specific protein 6 (Gas6), the ligand for the TAM receptor tyrosine kinase family, consisting of Tyro3, Axl, and Mer, is important for cell growth, survival, and clearance of debris. In this study, we show that levels of membrane-bound Mer (205 kd), soluble Mer ( approximately 150 kd), and soluble Axl (80 kd) were all significantly elevated in homogenates from established multiple sclerosis lesions comprised of both chronic active and chronic silent lesions. Whereas in normal tissue Gas6 positively correlated with soluble Axl and Mer, there was a negative correlation between Gas6 and soluble Axl and Mer in established multiple sclerosis lesions. In addition, increased levels of soluble Axl and Mer were associated with increased levels of mature ADAM17, mature ADAM10, and Furin, proteins that are associated with Axl and Mer solubilization. Soluble Axl and Mer are both known to act as decoy receptors and block Gas6 binding to membrane-bound receptors. These data suggest that in multiple sclerosis lesions, dysregulation of protective Gas6 receptor signaling may prolong lesion activity.}, number={1}, journal={The American Journal of Pathology}, publisher={Elsevier BV}, author={Weinger, Jason G. and Omari, Kakuri M. and Marsden, Kurt and Raine, Cedric S. and Shafit-Zagardo, Bridget}, year={2009}, month={Jul}, pages={283–293} }
 @article{marsden_beattie_friedenthal_carroll_2007, title={NMDA Receptor Activation Potentiates Inhibitory Transmission through GABA Receptor-Associated Protein-Dependent Exocytosis of GABAA Receptors}, volume={27}, DOI={10.1523/jneurosci.4433-07.2007}, abstractNote={The trafficking of postsynaptic AMPA receptors (AMPARs) is a powerful mechanism for regulating the strength of excitatory synapses. It has become clear that the surface levels of inhibitory GABAAreceptors (GABAARs) are also subject to regulation and that GABAAR trafficking may contribute to inhibitory plasticity, although the underlying mechanisms are not fully understood. Here, we report that NMDA receptor activation, which has been shown to drive excitatory long-term depression through AMPAR endocytosis, simultaneously increases expression of GABAARs at the dendritic surface of hippocampal neurons. This NMDA stimulus increases miniature IPSC amplitudes and requires the activity of Ca2+calmodulin-dependent kinase II and the trafficking proteinsN-ethylmaleimide-sensitive factor, GABA receptor-associated protein (GABARAP), and glutamate receptor interacting protein (GRIP). These data demonstrate for the first time that endogenous GABARAP and GRIP contribute to the regulated trafficking of GABAARs. In addition, they reveal that the bidirectional trafficking of AMPA and GABAAreceptors can be driven by a single glutamatergic stimulus, providing a potent postsynaptic mechanism for modulating neuronal excitability.}, number={52}, journal={Journal of Neuroscience}, publisher={Society for Neuroscience}, author={Marsden, K. C. and Beattie, J. B. and Friedenthal, J. and Carroll, R. C.}, year={2007}, pages={14326–14337} }
 @article{clarke_buskey_marsden_2004, title={Effects of water motion and prey behavior on zooplankton capture by two coral reef fishes}, volume={146}, DOI={10.1007/s00227-004-1528-y}, number={6}, journal={Marine Biology}, publisher={Springer Nature}, author={Clarke, R. D. and Buskey, E. J. and Marsden, K. C.}, year={2004}, pages={1145–1155} }