Characterization of a novel stimulus-induced glial calcium wave in Drosophila larval peripheral segmental nerves and its role in PKG-modulated thermoprotection

References

• Allen, A.M., Anreiter, I., Vesterberg, A., Douglas, S.J., & Sokolowski, M.B. (2018). Pleiotropy of the Drosophila melanogaster foraging gene on larval feeding-related traits. Journal of Neurogenetics, 32(3), 256–266. doi:https://doi.org/10.1080/01677063.2018.1500572
   PubMed Web of Science ®Google Scholar
• Araque, A., & Navarrete, M. (2010). Glial cells in neuronal network function. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 365(1551), 2375–2381. doi:https://doi.org/10.1098/rstb.2009.0313
   PubMed Web of Science ®Google Scholar
• Armstrong, G.A.B., López-Guerrero, J.J., Dawson-Scully, K., Peña, F., & Robertson, R.M. (2010). Inhibition of protein kinase G activity protects neonatal mouse respiratory network from hyperthermic and hypoxic stress. Brain Research, 1311, 64–72. doi:https://doi.org/10.1016/j.brainres.2009.11.038
   PubMed Web of Science ®Google Scholar
• Armstrong, G.A.B., Rodgers, C.I., Money, T.G.A., & Robertson, R.M. (2009). Suppression of spreading depression-like events in Locusts by inhibition of the NO/cGMP/PKG pathway. Journal of Neuroscience, 29(25), 8225–8235. doi:https://doi.org/10.1523/JNEUROSCI.1652-09.2009
   PubMed Web of Science ®Google Scholar
• Armstrong, G.A.B., Xiao, C., Krill, J.L., Seroude, L., Dawson-Scully, K., & Robertson, R.M. (2011). Glial Hsp70 Protects K + Homeostasis in the Drosophila brain during repetitive anoxic depolarization. PLoS One, 6(12), e28994. doi:https://doi.org/10.1371/journal.pone.0028994
   PubMed Web of Science ®Google Scholar
• Arnold, W.P., Mittal, C.K., Katsuki, S., & Murad, F. (1977). Nitric oxide activates guanylate cyclase and increases guanosine 3′:5′-cyclic monophosphate levels in various tissue preparations. Proceedings of the National Academy of Sciences, 74(8), 3203–3207. doi:https://doi.org/10.1073/pnas.74.8.3203
   PubMed Web of Science ®Google Scholar
• Barclay, J.W., & Robertson, R.M. (2000). Heat-shock-induced thermoprotection of hindleg motor control in the locust. Journal of Experimental Biology, 203(5), 941–950. doi:https://doi.org/10.1242/jeb.203.5.941
   PubMed Web of Science ®Google Scholar
• Barclay, J. W., & Robertson, R. M. (2003). Role for calcium in heat shock-mediated synaptic thermoprotection inDrosophila larvae. Journal of Neurobiology, 56(4), 360–371. https://doi.org/https://doi.org/10.1002/neu.10247
   Google Scholar
• Blum, I.D., Keleş, M.F., Baz, E.-S., Han, E., Park, K., Luu, S., … Wu, M.N. (2021). Astroglial calcium signaling encodes sleep need in Drosophila. Current Biology, 31(1), 150–162 e157. doi:https://doi.org/10.1016/j.cub.2020.10.012
   PubMed Web of Science ®Google Scholar
• Brand, A. H., & Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development, 118(2), 401–415. https://www.ncbi.nlm.nih.gov/pubmed/8223268
   PubMed Web of Science ®Google Scholar
• Brink, D.L., Gilbert, M., Xie, X., Petley-Ragan, L., & Auld, V.J. (2012). Glial processes at the Drosophila larval neuromuscular junction match synaptic growth. PLoS One, 7(5), e37876. doi:https://doi.org/10.1371/journal.pone.0037876
   PubMed Web of Science ®Google Scholar
• Caplan, S.L., Milton, S.L., & Dawson-Scully, K. (2013). A cGMP-dependent protein kinase (PKG) controls synaptic transmission tolerance to acute oxidative stress at the Drosophila larval neuromuscular junction. Journal of Neurophysiology, 109(3), 649–658. doi:https://doi.org/10.1152/jn.00784.2011
   PubMed Web of Science ®Google Scholar
• Chen, A., Kramer, E.F., Purpura, L., Krill, J.L., Zars, T., & Dawson-Scully, K. (2011). The influence of natural variation at the foraging gene on thermotolerance in adult Drosophila in a narrow temperature range. Neural, and Behavioral Physiology, 197(12), 1113–1118. doi:https://doi.org/10.1007/s00359-011-0672-3
   Web of Science ®Google Scholar
• Chouhan, A.K., Ivannikov, M.V., Lu, Z., Sugimori, M., Llinas, R.R., & Macleod, G.T. (2012). Cytosolic Calcium coordinates mitochondrial energy metabolism with presynaptic activity. The Journal of Neuroscience, 32(4), 1233–1243. doi:https://doi.org/10.1523/jneurosci.1301-11.2012
   PubMed Web of Science ®Google Scholar
• Chouhan, A.K., Zhang, J., Zinsmaier, K.E., & Macleod, G.T. (2010). Presynaptic mitochondria in functionally different motor neurons exhibit similar affinities for Ca2+ but exert little influence as Ca2+ buffers at nerve firing rates in situ. The Journal of Neuroscience, 30(5), 1869–1881. doi:https://doi.org/10.1523/JNEUROSCI.4701-09.2010
   PubMed Web of Science ®Google Scholar
• Clapham, D.E. (2007). Calcium signaling. Cell, 131(6), 1047–1058. doi:https://doi.org/10.1016/j.cell.2007.11.028
   PubMed Web of Science ®Google Scholar
• Costa, A.D.T., Jakob, R., Costa, C.L., Andrukhiv, K., West, I.C., & Garlid, K.D. (2006). The mechanism by which the mitochondrial ATP-sensitive K + channel opening and H2O2 inhibit the mitochondrial permeability transition. The Journal of Biological Chemistry, 281(30), 20801–20808. doi:https://doi.org/10.1074/jbc.m600959200
   PubMed Web of Science ®Google Scholar
• Dason, J.S., Allen, A.M., Vasquez, O.E., & Sokolowski, M.B. (2019). Distinct functions of a cGMP-dependent protein kinase in nerve terminal growth and synaptic vesicle cycling. Journal of Cell Science, 132(7), doi:https://doi.org/10.1242/jcs.227165
   PubMed Web of Science ®Google Scholar
• Dawson-Scully, K., Armstrong, G.A.B., Kent, C., Robertson, R.M., & Sokolowski, M.B. (2007). Natural variation in the thermotolerance of neural function and behavior due to a cGMP-dependent protein kinase. PLoS One, 2(8), e773. doi:https://doi.org/10.1371/journal.pone.0000773
   PubMed Web of Science ®Google Scholar
• Dawson-Scully, K., Bronk, P., Atwood, H.L., & Zinsmaier, K.E. (2000). Cysteine-string protein increases the calcium sensitivity of neurotransmitter exocytosis in Drosophila. The Journal of Neuroscience, 20(16), 6039–6047. doi:https://doi.org/10.1523/jneurosci.20-16-06039.2000
   PubMed Web of Science ®Google Scholar
• Dawson-Scully, K., Bukvic, D., Chakaborty-Chatterjee, M., Ferreira, R., Milton, S.L., & Sokolowski, M.B. (2010). Controlling anoxic tolerance in adult Drosophila via the cGMP-PKG pathway. The Journal of Experimental Biology, 213(Pt 14), 2410–2416. doi:https://doi.org/10.1242/jeb.041319
   PubMed Web of Science ®Google Scholar
• Dickinson, M.H. (2000). How Animals move: An integrative view. Science , 288(5463), 100–106. doi:https://doi.org/10.1126/science.288.5463.100
   PubMed Web of Science ®Google Scholar
• Donlea, J., Leahy, A., Thimgan, M.S., Suzuki, Y., Hughson, B.N., Sokolowski, M.B., & Shaw, P.J. (2012). foraging alters resilience/vulnerability to sleep disruption and starvation in Drosophila. Proceedings of the National Academy of Sciences, 109(7), 2613–2618. doi:https://doi.org/10.1073/pnas.1112623109
   PubMed Web of Science ®Google Scholar
• Duchen, M.R. (2000). Mitochondria and calcium: From cell signalling to cell death. The Journal of Physiology, 529(1), 57–68. doi:https://doi.org/10.1111/j.1469-7793.2000.00057.x
   PubMed Web of Science ®Google Scholar
• Elekonich, M.M. (2009). Extreme thermotolerance and behavioral induction of 70-kDa heat shock proteins and their encoding genes in honey bees. Cell Stress & Chaperones, 14(2), 219–226. doi:https://doi.org/10.1007/s12192-008-0063-z
   PubMed Web of Science ®Google Scholar
• Giorgi, C., Baldassari, F., Bononi, A., Bonora, M., De Marchi, E., Marchi, S., … Pinton, P. (2012). Mitochondrial Ca2+ and apoptosis. Cell Calcium. 52(1), 36–43. doi:https://doi.org/10.1016/j.ceca.2012.02.008
   PubMed Web of Science ®Google Scholar
• Glancy, B., & Balaban, R.S. (2012). Role of mitochondrial Ca2+ in the regulation of cellular energetics. Biochemistry, 51(14), 2959–2973. doi:https://doi.org/10.1021/bi2018909
   PubMed Web of Science ®Google Scholar
• He, H., Lam, M., McCormick, T.S., & Distelhorst, C.W. (1997). Maintenance of Calcium homeostasis in the endoplasmic reticulum by Bcl-2. The Journal of Cell Biology, 138(6), 1219–1228. doi:https://doi.org/10.1083/jcb.138.6.1219
   PubMed Web of Science ®Google Scholar
• Huang, Y.H., & Bergles, D.E. (2004). Glutamate transporters bring competition to the synapse. Current Opinion in Neurobiology, 14(3), 346–352. doi:https://doi.org/10.1016/j.conb.2004.05.007
   PubMed Web of Science ®Google Scholar
• Kalimuthu, S., & Se-Kwon, K. (2013). Cell survival and apoptosis signaling as therapeutic target for cancer: Marine bioactive compounds. International Journal of Molecular Sciences, 14(2), 2334–2354. doi:https://doi.org/10.3390/ijms14022334
   PubMed Web of Science ®Google Scholar
• Keshishian, H., Broadie, K., Chiba, A., & Bate, M. (1996). The Drosophila neuromuscular junction: A model system for studying synaptic development and function. Annual Review of Neuroscience, 19(1), 545–575. doi:https://doi.org/10.1146/annurev.ne.19.030196.002553
   PubMed Web of Science ®Google Scholar
• Kirischuk, S., Scherer, J., Möller, T., Verkhratsky, A., & Kettenmann, H. (1995). Subcellular heterogeneity of voltage-gated Ca2+ channels in cells of the oligodendrocyte lineage. Glia, 13(1), 1–12. doi:https://doi.org/10.1002/glia.440130102
   PubMed Web of Science ®Google Scholar
• Knodel, M.M., Geiger, R., Ge, L., Bucher, D., Grillo, A., Wittum, G., … Queisser, G. (2014). Synaptic bouton properties are tuned to best fit the prevailing firing pattern. Frontiers in Computational Neuroscience, 8, 101. doi:https://doi.org/10.3389/fncom.2014.00101
   PubMed Web of Science ®Google Scholar
• Kofuji, P., & Newman, E.A. (2004). Potassium buffering in the central nervous system. Neuroscience, 129(4), 1043–1054. doi:https://doi.org/10.1016/j.neuroscience.2004.06.008
   Web of Science ®Google Scholar
• Kottmeier, R., Bittern, J., Schoofs, A., Scheiwe, F., Matzat, T., Pankratz, M., & Klämbt, C. (2020). Wrapping glia regulates neuronal signaling speed and precision in the peripheral nervous system of Drosophila. Nature Communications, 11(1), 4491. doi:https://doi.org/10.1038/s41467-020-18291-1
   PubMed Web of Science ®Google Scholar
• Krieger, C., & Duchen, M.R. (2002). Mitochondria, Ca2+ and neurodegenerative disease. European Journal of Pharmacology, 447(2–3), 177–188. doi:https://doi.org/10.1016/s0014-2999(02)01842-3
   PubMed Web of Science ®Google Scholar
• Krill, J.L., & Dawson-Scully, K. (2016). cGMP-dependent protein kinase inhibition extends the upper temperature limit of stimulus-evoked calcium responses in motoneuronal boutons of Drosophila melanogaster Larvae. PLoS One, 11(10), e0164114. doi:https://doi.org/10.1371/journal.pone.0164114
   PubMed Web of Science ®Google Scholar
• Leiserson, W.M., & Keshishian, H. (2011). Maintenance and regulation of extracellular volume and the ion environment in Drosophila larval nerves. Glia, 59(9), 1312–1321. doi:https://doi.org/10.1002/glia.21132
   PubMed Web of Science ®Google Scholar
• Lu, Y.F., & Hawkins, R.D. (2002). Ryanodine receptors contribute to cGMP-induced late-phase LTP and CREB phosphorylation in the hippocampus. J Neurophysiol, 88(3), 1270–1278. doi:https://doi.org/10.1152/jn.2002.88.3.1270
   PubMed Web of Science ®Google Scholar
• Lytton, J., Westlin, M., & Hanley, M.R. (1991). Thapsigargin inhibits the sarcoplasmic or endoplasmic reticulum Ca-ATPase family of calcium pumps. The Journal of Biological Chemistry, 266(26), 17067–17071. doi:https://doi.org/10.1016/S0021-9258(19)47340-7
   PubMed Web of Science ®Google Scholar
• Macleod, G.T. (2012). Imaging and analysis of nonratiometric calcium indicators at the Drosophila Larval Neuromuscular junction. Cold Spring Harbor Protocols, 2012(7), pdb.prot070110-p. doi:https://doi.org/10.1101/pdb.prot070110
   PubMedGoogle Scholar
• Macleod, G.T., Hegström-Wojtowicz, M., Charlton, M.P., & Atwood, H.L. (2002). Fast calcium signals in Drosophila motor neuron terminals. Journal of Neurophysiology, 88(5), 2659–2663. doi:https://doi.org/10.1152/jn.00515.2002
   PubMed Web of Science ®Google Scholar
• Macvicar, B. (1984). Voltage-dependent calcium channels in glial cells. Science, 226(4680), 1345–1347. doi:https://doi.org/10.1126/science.6095454
   PubMed Web of Science ®Google Scholar
• McCormack, J.G., Halestrap, A.P., & Denton, R.M. (1990). Role of calcium ions in regulation of mammalian intramitochondrial metabolism. Physiological Reviews, 70(2), 391–425. doi:https://doi.org/10.1152/physrev.1990.70.2.391
   PubMed Web of Science ®Google Scholar
• Melom, J.E., & Littleton, J.T. (2013). Mutation of a NCKX eliminates glial Microdomain Calcium Oscillations and enhances seizure susceptibility. The Journal of Neuroscience, 33(3), 1169–1178. doi:https://doi.org/10.1523/jneurosci.3920-12.2013
   PubMed Web of Science ®Google Scholar
• Milton, S.L., & Dawson-Scully, K. (2013). Alleviating brain stress: What alternative animal models have revealed about therapeutic targets for hypoxia and anoxia. Future Neurology, 8(3), 287–301. doi:https://doi.org/10.2217/fnl.13.12
   PubMedGoogle Scholar
• Niemi, N.M., & MacKeigan, J.P. (2013). Mitochondrial phosphorylation in apoptosis: Flipping the death switch. Antioxidants & Redox Signaling, 19(6), 572–582. doi:https://doi.org/10.1089/ars.2012.4982
   PubMed Web of Science ®Google Scholar
• Park, J.E., Lee, E.J., Kim, J.K., Song, Y., Choi, J.H., & Kang, M.J. (2018). Flightless-I controls fat storage in Drosophila. Molecules and Cells, 41(6), 603–611. doi:https://doi.org/10.14348/molcells.2018.0120
   PubMed Web of Science ®Google Scholar
• Parker, R.J., & Auld, V.J. (2006). Roles of glia in the Drosophila nervous system. Seminars in Cell & Developmental Biology, 17(1), 66–77. doi:https://doi.org/10.1016/j.semcdb.2005.11.012
   PubMed Web of Science ®Google Scholar
• Parton, R.M., Valles, A.M., Dobbie, I.M., & Davis, I. (2010a). Drosophila larval fillet preparation and imaging of neurons. Cold Spring Harbor Protocols, 2010(4), pdb prot5405. doi:https://doi.org/10.1101/pdb.prot5405
   PubMedGoogle Scholar
• Parton, R.M., Valles, A.M., Dobbie, I.M., & Davis, I. (2010b). Live cell imaging in Drosophila melanogaster. Cold Spring Harbor Protocols, 2010(4), pdb top75. doi:https://doi.org/10.1101/pdb.top75
   PubMedGoogle Scholar
• Perea, G., & Araque, A. (2005). Glial calcium signaling and neuron-glia communication. Cell Calcium, 38(3–4), 375–382. doi:https://doi.org/10.1016/j.ceca.2005.06.015
   PubMed Web of Science ®Google Scholar
• Petersen, O.H., Petersen, C.C.H., & Kasai, H. (1994). Calcium and hormone action. Review of Physiology, 56(1), 297–319. doi:https://doi.org/10.1146/annurev.ph.56.030194.001501
   PubMed Web of Science ®Google Scholar
• Petrov, A.M., Giniatullin, A.R., Sitdikova, G.F., & Zefirov, A.L. (2008). The Role of cGMP-Dependent signaling pathway in synaptic vesicle cycle at the frog motor nerve terminals. Journal of Neuroscience, 28(49), 13216–13222. doi:https://doi.org/10.1523/jneurosci.2947-08.2008
   PubMed Web of Science ®Google Scholar
• Pinton, P., Giorgi, C., Siviero, R., Zecchini, E., & Rizzuto, R. (2008). Calcium and apoptosis: ER-mitochondria Ca2+ transfer in the control of apoptosis. Oncogene, 27(50), 6407–6418. doi:https://doi.org/10.1038/onc.2008.308
   PubMed Web of Science ®Google Scholar
• Ramachandran, P., & Budnik, V. (2010). Dissection of Drosophila larval body-wall muscles. Cold Spring Harbor Protocols, 2010(8), pdb.prot5469. doi:https://doi.org/10.1101/pdb.prot5469
   PubMedGoogle Scholar
• Renger, J.J., Yao, W.-D., Sokolowski, M.B., & Wu, C.-F. (1999). Neuronal polymorphism among natural alleles of a cGMP-dependent kinase gene, foraging, in Drosophila. The Journal of Neuroscience, 19(19), RC28–RC28. doi:https://doi.org/10.1523/JNEUROSCI.19-19-j0002.1999
   PubMed Web of Science ®Google Scholar
• Rizzuto, D., Stefani, D., Raffaello, A., & Mammucari, C. (2012). Mitochondria as sensors and regulators of calcium signalling. Nature Reviews. Molecular Cell Biology, 13(9), 566–578. doi:https://doi.org/10.1038/nrm3412
   PubMed Web of Science ®Google Scholar
• Rizzuto , Marchi, S., Bonora, M., Aguiari, P., Bononi, A., De Stefani, D., … Pinton, P. (2009). Ca2+ transfer from the ER to mitochondria: When, how and why. Biochimica et Biophysica Acta (BBA) – Bioenergetics, 1787(11), 1342–1351. doi:https://doi.org/10.1016/j.bbabio.2009.03.015
   PubMed Web of Science ®Google Scholar
• Rizzuto, R., Pinton, P., Carrington, W., Fay, F.S., Fogarty, K.E., Lifshitz, L.M. … (1998). Close Contacts with the Endoplasmic Reticulum as Determinants of Mitochondrial Ca2+ Responses. Science, 280(5370), 1763–1766. doi:https://doi.org/10.1126/science.280.5370.1763
   PubMed Web of Science ®Google Scholar
• Robertson, R.M. (2004). Thermal stress and neural function: Adaptive mechanisms in insect model systems. Journal of Thermal Biology, 29(7–8), 351–358. doi:https://doi.org/10.1016/j.jtherbio.2004.08.073
   Web of Science ®Google Scholar
• Rodgers, C.I., Armstrong, G.A.B., & Robertson, R.M. (2010). Coma in response to environmental stress in the locust: A model for cortical spreading depression. Journal of Insect Physiology, 56(8), 980–990. doi:https://doi.org/10.1016/j.jinsphys.2010.03.030
   PubMed Web of Science ®Google Scholar
• Rodgers, C.I., Armstrong, G.A.B., Shoemaker, K.L., Labrie, J.D., Moyes, C.D., & Robertson, R.M. (2007). Stress preconditioning of spreading depression in the Locust CNS. PLoS One, 2(12), e1366. doi:https://doi.org/10.1371/journal.pone.0001366
   PubMed Web of Science ®Google Scholar
• Ruth, P., Landgraf, W., Keilbach, A., May, B., Egleme, C., & Hofmann, F. (1991). The activation of expressed cGMP-dependent protein kinase isozymes Ialpha and Ibeta is determined by the different amino-termini. European Journal of Biochemistry, 202(3), 1339–1344. doi:https://doi.org/10.1111/j.1432-1033.1991.tb16509.x
   PubMedGoogle Scholar
• Schousboe, A. (2003). Role of astrocytes in the maintenance and modulation of glutamatergic and GABAergic neurotransmission. Neurochemical Research, 28(2), 347–352. doi:https://doi.org/10.1023/A:1022397704922
   PubMed Web of Science ®Google Scholar
• Seifert, G., Schilling, K., & Steinhäuser, C. (2006). Astrocyte dysfunction in neurological disorders: A molecular perspective. Nature Reviews. Neuroscience, 7(3), 194–206. doi:https://doi.org/10.1038/nrn1870
   PubMed Web of Science ®Google Scholar
• Sepp, K.J., Schulte, J., & Auld, V.J. (2000). Developmental dynamics of peripheral glia in Drosophila melanogaster. Glia, 30(2), 122–133. doi:https://doi.org/10.1002/(SICI)1098-1136(200004)30:2<122::AID-GLIA2>3.0.CO;2-B
   PubMed Web of Science ®Google Scholar
• Sheehan, J. P., Swerdlow, R. H., Miller, S. W., Davis, R. E., Parks, J. K., Parker, W. D., & Tuttle, J. B. (1997). Calcium homeostasis and reactive oxygen species production in cells transformed by mitochondria from individuals with sporadic Alzheimer's disease. J Neurosci, 17(12), 4612–4622. https://www.ncbi.nlm.nih.gov/pubmed/9169522
   PubMed Web of Science ®Google Scholar
• Sink, H., & Whitington, P.M. (1991). Location and connectivity of abdominal motoneurons in the embryo and larva of Drosophila melanogaster. Journal of Neurobiology, 22(3), 298–311. doi:https://doi.org/10.1002/neu.480220309
   PubMed Web of Science ®Google Scholar
• Sokolowski, M.B. (1980). Foraging strategies of Drosophila melanogaster: A chromosomal analysis. Behavior Genetics, 10(3), 291–302. doi:https://doi.org/10.1007/BF01067774
   PubMed Web of Science ®Google Scholar
• Stewart, B.A., Atwood, H.L., Renger, J.J., Wang, J., & Wu, C.F. (1994). Improved stability of Drosophila larval neuromuscular preparations in haemolymph-like physiological solutions. Journal of Comparative Physiology., 175(2), 179–191. doi:https://doi.org/10.1007/BF00215114
   Web of Science ®Google Scholar
• Tian, L., Hires, S.A., Mao, T., Huber, D., Chiappe, M.E., Chalasani, S.H., … Looger, L.L. (2009). Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nature Methods, 6(12), 875–881. doi:https://doi.org/10.1038/nmeth.1398
   PubMed Web of Science ®Google Scholar
• Tzingounis, A.V., & Wadiche, J.I. (2007). Glutamate transporters: Confining runaway excitation by shaping synaptic transmission. Nature Reviews. Neuroscience, 8(12), 935–947. doi:https://doi.org/10.1038/nrn2274
   PubMed Web of Science ®Google Scholar
• Verkhratsky, A., & Kettenmann, H. (1996). Calcium signalling in glial cells. Trends in Neurosciences., 19(8), 346–352. doi:https://doi.org/10.1016/0166-2236(96)10048-5
   PubMed Web of Science ®Google Scholar
• Verkhratsky, A., Orkand, R.K., & Kettenmann, H. (1998). Glial calcium: Homeostasis and signaling function. Physiological Reviews, 78(1), 99–141. doi:https://doi.org/10.1152/physrev.1998.78.1.99
   PubMed Web of Science ®Google Scholar
• Waldman, S.A., & Murad, F. (1988). Biochemical mechanisms underlying vascular smooth muscle relaxation: The guanylate cyclase-cyclic GMP system. Journal of Cardiovascular Pharmacology., 12 (Suppl 5), 115–118. doi:https://doi.org/10.1097/00005344-198806125-00020
   PubMed Web of Science ®Google Scholar
• Wallraff, A. (2006). The impact of astrocytic gap junctional coupling on potassium buffering in the hippocampus. Journal of Neuroscience, 26(20), 5438–5447. doi:https://doi.org/10.1523/JNEUROSCI.0037-06.2006
   PubMed Web of Science ®Google Scholar
• Wei, J.-Y., Cohen, E.D., Yan, Y.-Y., Genieser, H.-G., & Barnstable, C.J. (1996). Identification of competitive antagonists of the rod photoreceptor cGMP-Gated cation channel: β-Phenyl-1,N2-etheno-substituted cGMP analogues as probes of the cGMP-binding site. Biochemistry, 35(51), 16815–16823. doi:https://doi.org/10.1021/bi961763v
   PubMed Web of Science ®Google Scholar
• Weiss, S., Clamon, L.C., Manoim, J.E., Ormerod, K.G., Parnas, M., & Littleton, J.T. (2020). Disruption of Glial Ca2+ oscillations at the Drosophila blood-brain barrier predisposes to seizure-like behavior. bioRxiv, 2020.2009.2016.285841. doi:https://doi.org/10.1101/2020.09.16.285841
   Google Scholar
• Williams, G.S.B., Boyman, L., Chikando, A.C., Khairallah, R.J., & Lederer, W.J. (2013). Mitochondrial calcium uptake. Proceedings of the National Academy of Sciences, 110(26), 10479–10486. doi:https://doi.org/10.1073/pnas.1300410110
   PubMed Web of Science ®Google Scholar
• Willmott, N. J., Wong, K., & Strong, A. J. (2000). A fundamental role for the nitric oxide-G-kinase signaling pathway in mediating intercellular Ca(2+) waves in glia. J Neurosci, 20(5), 1767–1779. https://www.ncbi.nlm.nih.gov/pubmed/10684878
   PubMed Web of Science ®Google Scholar
• Xie, X., & Auld, V.J. (2011). Integrins are necessary for the development and maintenance of the glial layers in the Drosophila peripheral nerve. Development (Cambridge, England), 138(17), 3813–3822. doi:https://doi.org/10.1242/dev.064816
   PubMed Web of Science ®Google Scholar