Skip to main content

Multiple Signaling Pathways Govern Calcium Homeostasis in Photoreceptor Inner Segments

  • Chapter
Visual Transduction and Non-Visual Light Perception

Part of the book series: Ophthalmology Research ((OPHRES))

  • 1384 Accesses

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 119.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 159.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adachi-Akahane S, Cleemann L, Morad M. Cross-signaling between L-type Ca2+ channels and ryanodine receptors in rat ventricular myocytes. J Gen Physiol. 1996;108:435–454.

    PubMed  CAS  Google Scholar 

  • Adamus G, Webb S, Shiraga S and Duvoisin SM. Anti-recoverin antibodies induce an increase in intracellular calcium, leading to apoptosis in retinal cells. J Autoimmun. 2006;26:146–153.

    PubMed  CAS  Google Scholar 

  • Akopian A, Johnson J, Gabriel R, Brecha N, Witkovsky P. Somatostatin modulates voltage-gated K(+) and Ca(2+) currents in rod and cone photoreceptors of the salamander retina. J Neurosci. 2000;20:929–936.

    PubMed  CAS  Google Scholar 

  • Akopian A, Krizaj D, Witkovsky P. Both high- and low voltage-activated calcium currents contribute to the light-evoked responses of luminosity horizontal cells in the Xenopus retina. Brain Res. 1997;762:121–130.

    PubMed  CAS  Google Scholar 

  • Akopian A, Szikra T, Cristofanilli M, Krizaj D. Glutamate-induced Ca2+ influx in third-order neurons of salamander retina is regulated by the actin cytoskeleton. Neuroscience. 2006;138:17–24.

    PubMed  CAS  Google Scholar 

  • Arai J, Katai N, Kuida K, Kikuchi T, Yoshimura N. Decreased retinal neuronal cell death in caspase-1 knockout mice. Jpn J Ophthalmol. 2006;50:417–425.

    PubMed  CAS  Google Scholar 

  • Awatramani GB, Price GD, Trussell LO. Modulation of transmitter release by presynaptic resting potential and background calcium levels. Neuron. 2005;48:109–121.

    PubMed  CAS  Google Scholar 

  • Azarian SM, Williams DS. Calpain activity in the retinas of normal and RCS rats. Curr Eye Res. 1995;14:731–735.

    PubMed  CAS  Google Scholar 

  • Bader CR, Bertrand D, Schwartz EA. Voltage-activated and calcium-activated currents studied in solitary rod inner segments from the salamander retina. J Physiol. 1982;331:2532–2584.

    Google Scholar 

  • Baldridge WH, Kurennyi DE, Barnes S. Calcium-sensitive calcium influx in photoreceptor inner segments. J Neurophysiol. 1998;79:3012–3018.

    PubMed  CAS  Google Scholar 

  • Ball SL, Gregg RG. Using mutant mice to study the role of voltage-gated calcium channels in the retina. Adv Exp Med Biol. 2002;514:439–450.

    PubMed  CAS  Google Scholar 

  • Barnes S. After transduction: response shaping and control of transmission by ion channels of the photoreceptor inner segments. Neuroscience. 1994;58:447–459.

    PubMed  CAS  Google Scholar 

  • Barnes S, B. Hille: Ionic channels of the inner segment of tiger salamander cone photoreceptors. J Gen Physiol. 1989;94:719–743.

    PubMed  CAS  Google Scholar 

  • Barnes S, Merchant V, Mahmud FM. Modulation of transmission gain by protons at the photore-ceptor output synapse. Proc Natl Acad Sci U S A. 1993;90:10081–10085.

    PubMed  CAS  Google Scholar 

  • Baumann L, Gerstner A, Zong X, Biel M, Wahl-Schott C. Functional characterization of the L-type Ca2+ channel Cav1.4alpha1 from mouse retina. Invest Ophthalmol Vis Sci. 2004;45:708–713.

    PubMed  Google Scholar 

  • Bech-Hansen NT, Naylor MJ, Maybaum TA, Pearce WG, Koop B, Fishman GA, Mets M, Musarella MA, Boycott KM. Loss-of-function mutations in a calcium-channel alpha1-subunit gene in Xp11.23 cause incomplete X-linked congenital stationary night blindness. Nat Genet. 1998;19:264–267.

    PubMed  CAS  Google Scholar 

  • Beech DJ, Barnes S. Characterization of a voltage-gated K+ channel that accelerates the rod response to dim light. Neuron. 1989;3:573–581.

    PubMed  CAS  Google Scholar 

  • Belgum JH, Copenhagen DR. Synaptic transfer of rod signals to horizontal and bipolar cells in the retina of the toad (Bufo marinus). J Physiol. 1988;396:225–245.

    PubMed  CAS  Google Scholar 

  • Berliocchi L, Fava E, Leist M, Horvat V, Dinsdale D, Read D, Nicotera P. Botulinum neurotoxin C initiates two different programs for neurite degeneration and neuronal apoptosis. J Cell Biol. 2005;168:607–618.

    PubMed  CAS  Google Scholar 

  • Berntson AK, Morgans CW. Distribution of the presynaptic calcium sensors, synaptotagmin I/II and synaptotagmin III, in the goldfish and rodent retinas. J Vis. 2003;3:274–280.

    PubMed  Google Scholar 

  • Berridge MJ, Bootman MD, Roderick HL. Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol. 2003;4:517–529.

    PubMed  CAS  Google Scholar 

  • Besharse JC, Baker SA, Luby-Phelps K, Pazour GJ. Photoreceptor intersegmental transport and retinal degeneration: a conserved pathway common to motile and sensory cilia. Adv Exp Med Biol. 2003;533:157–164.

    PubMed  CAS  Google Scholar 

  • Bode C, Wolfrum U. Caspase-3 inhibitor reduces apototic photoreceptor cell death during inherited retinal degeneration in tubby mice. Mol Vis. 2003;9:144–150.

    PubMed  CAS  Google Scholar 

  • Bollmann JH, Sakmann B, Borst JG. Calcium sensitivity of glutamate release in a calyx-type terminal. Science. 2000;289:953–957.

    PubMed  CAS  Google Scholar 

  • Breckenridge DG, Germain M, Mathai JP, Nguyen M, Shore GC. Regulation of apoptosis by endoplasmic reticulum pathways. Oncogene. 2003;22:8608–8618.

    PubMed  CAS  Google Scholar 

  • Brostrom MA, Brostrom CO. Calcium dynamics and endoplasmic reticular function in the regulation of protein synthesis: implications for cell growth and adaptability. Cell Calcium. 2003;34:345–363.

    PubMed  CAS  Google Scholar 

  • Bush RA, Kononen L, Machida S, Sieving PA. The effect of calcium channel blocker diltiazem on photoreceptor degeneration in the rhodopsin Pro213His rat. Invest Ophthalmol Vis Sci. 2000;41:2697–2701.

    PubMed  CAS  Google Scholar 

  • Cadetti L, Bryson EJ, Ciccone CA, Rabl K, Thoreson WB. Calcium-induced calcium release in rod photoreceptor terminals boosts synaptic transmission during maintained depolarization. Eur J Neurosci. 2006;23:2983–2990.

    PubMed  Google Scholar 

  • Cadetti L, Thoreson WB, Piccolino M. Pre- and post-synaptic effects of manipulating surface charge with divalent cations at the photoreceptor synapse. Neuroscience. 2004;129: 791–801.

    PubMed  CAS  Google Scholar 

  • Carafoli E. Calcium signaling: a tale for all seasons. Proc Natl Acad Sci U S A. 2002;99:1115–1122.

    PubMed  CAS  Google Scholar 

  • Chang GQ, Hao Y, Wong F. Apoptosis: final common pathway of photoreceptor death in rd, rds, and rhodopsin mutant mice. Neuron. 1993;11:595–605.

    PubMed  CAS  Google Scholar 

  • Chiarini LB, Leal-Ferreira ML, de Freitas FG, Linden R. Changing sensitivity to cell death during development of retinal photoreceptors. J Neurosci Res 2003;74:875–883.

    PubMed  CAS  Google Scholar 

  • Choi SY, Borghuis BG, Rea R, Levitan ES, Sterling P, Kramer RH. Encoding light intensity by the cone photoreceptor synapse. Neuron. 2005;48:555–562.

    PubMed  CAS  Google Scholar 

  • Cia D, Bordais A, Varela C, Forster V, Sahel JA, Rendon A, Picaud S. Voltage-gated channels and calcium homeostasis in mammalian rod photoreceptors. J Neurophysiol. 2005;93:1468–1475.

    PubMed  CAS  Google Scholar 

  • Corey DP, Dubinsky JM, Schwartz EA. The calcium current in inner segments of rods from the salamander (Ambystoma tigrinum) retina. J Physiol 1984;354:557–575.

    PubMed  CAS  Google Scholar 

  • Cox DH, Dunlap K. Inactivation of N-type calcium current in chick sensory neurons: calcium and voltage dependence. J Gen Physiol. 1994;104:311–336.

    PubMed  CAS  Google Scholar 

  • Cristofanilli M, Akopian A. Calcium channel and glutamate receptor activities regulate actin organization in salamander retinal neurons. J Physiol. 2006;575:543–554.

    PubMed  CAS  Google Scholar 

  • Cusato K, Bosco A, Rozental R, Guimaraes CA, Reese BE, Linden R, Spray DC. Gap junctions mediate bystander cell death in developing retina. J Neurosci. 2003;23:6413–6422.

    PubMed  CAS  Google Scholar 

  • DeBiasi RL, Edelstein CL, Sherry B, Tyler KL. Calpain inhibition protects against virus-induced apoptotic myocardial injury. J Virol. 2001;75:351–361.

    PubMed  CAS  Google Scholar 

  • Dodge FA Jr, Rahamimoff R. Co-operative action a calcium ions in transmitter release at the neuromuscular junction. J Physiol. 1967;193:419–432.

    PubMed  CAS  Google Scholar 

  • Donovan M, Carmody RJ, Cotter TG. Light-induced photoreceptor apoptosis in vivo requires neuronal nitric-oxide synthase and guanylate cyclase activity and is caspase-3-independent. J Biol Chem. 2001;276:23000–23008.

    PubMed  CAS  Google Scholar 

  • Donovan M, Cotter TG. Caspase-independent photoreceptor apoptosis in vivo and differential expression of apoptotic protease activating factor-1 and caspase-3 during retinal development. Cell Death Differ. 2002;9:1220–1231.

    PubMed  CAS  Google Scholar 

  • Doonan F, Donovan M, Cotter TG. Caspase-independent photoreceptor apoptosis in mouse models of retinal degeneration. J Neurosci. 2003;23:5723–5731.

    PubMed  CAS  Google Scholar 

  • Doonan F, Donovan M, Cotter TG. Activation of multiple pathways during photoreceptor apop-tosis in the rd mouse. Invest Ophthalmol Vis Sci. 2005;46:3530–3538.

    PubMed  Google Scholar 

  • Duenker N, Valenciano AI, Franke A, Hernandez-Sanchez C, Dressel R, Behrendt M, De Pablo F, Krieglstein K, de la Rosa EJ. Balance of pro-apoptotic transforming growth factor-beta and anti-apoptotic insulin effects in the control of cell death in the postnatal mouse retina. Eur J Neurosci. 2005;22:28–38.

    PubMed  CAS  Google Scholar 

  • Duncan J, Yang H, Doan T, Silverstein B, Murphy G., Nune G, Liu X, Copenhagen DR, Rieke F, Tempel BL, Krizaj D. Scotopic visual signaling in the mouse retina is modulated by high affinity plasma membrane calcium extrusion J Neurosci. 2006;26:7201–7211.

    PubMed  CAS  Google Scholar 

  • Edward DP, Lam TT, Shahinfar S, Li J, Tso MO. Amelioration of light-induced retinal degeneration by a calcium overload blocker. Flunarizine. Arch Ophthalmol. 1991;109:554–562.

    PubMed  CAS  Google Scholar 

  • Fain GL, Matthews HR, Cornwall MC, Koutalos Y. Adaptation in vertebrate photoreceptors. Physiol Rev. 2001;81:117–151.

    PubMed  CAS  Google Scholar 

  • Fain GL. Why photoreceptors die (and why they don't). Bioessays. 2006;28:344–354.

    PubMed  CAS  Google Scholar 

  • Farber DB. From mice to men: the cyclic GMP phosphodiesterase gene in vision and disease. Invest Ophthalmol Vis Sci. 1995;36:263–275.

    PubMed  CAS  Google Scholar 

  • Firth SI, Morgan IG, Boeken MK, Morgans C. Localization of voltage-sensitive L-type calcium channels in the chicken retina. Clin Experiment Ophthalmol. 2001;29:183–187.

    PubMed  CAS  Google Scholar 

  • Firth SI, Wang CT, Feller MB. Retinal waves: mechanisms and function in visual system development. Cell Calcium. 2005;37:425–432.

    PubMed  CAS  Google Scholar 

  • Fitzgerald KM, Cibis GW, Giambrone SA, Harris DJ. Retinal signal transmission in Duchenne muscular dystrophy: evidence for dysfunction in photoreceptor/depolarizing bipolar cell pathway. J Clin Invest. 1994;93:2425–2430.

    PubMed  CAS  Google Scholar 

  • Fox DA, Poblenz AT, He L, Harris JB, Medrano CJ. Pharmacological strategies to block rod photoreceptor apoptosis caused by calcium overload: a mechanistic target-site approach to neuroprotection. Eur J Ophthalmol. 2003;3:S44–S56.

    Google Scholar 

  • Frasson M, Sahel JA, Fabre M, Simonutti M, Dreyfus H, Picaud S. Retinitis pigmentosa: rod photo-receptor rescue by a calcium-channel blocker in the rd mouse. Nat Med. 1999;5:1183–1187.

    PubMed  CAS  Google Scholar 

  • Geppert M, Sudhof TC. RAB3 and synaptotagmin: the yin and yang of synaptic membrane fusion. Annu Rev Neurosci. 1998;21:75–95.

    PubMed  CAS  Google Scholar 

  • Ghosh A, Greenberg ME. Calcium signaling in neurons: molecular mechanisms and cellular consequences. Science. 1995;268:239–247. Review.

    PubMed  CAS  Google Scholar 

  • Giessl A, Trojan P, Rausch S, Pulvermuller A, Wolfrum U. Centrins, gatekeepers for the light-dependent translocation of transducin through the photoreceptor cell connecting cilium. Vision Res. 2006;46:4502–4509.

    PubMed  CAS  Google Scholar 

  • Gilgun-Sherki Y, Rosenbaum Z, Melamed E, Offen D. Antioxidant therapy in acute central nervous system injury: current state. Pharmacol Rev. 2002;54:271–384.

    PubMed  CAS  Google Scholar 

  • Goda Y, Stevens CF. Two components of transmitter release at a central synapse. Proc Natl Acad Sci U S A. 1994;91:12942–12946.

    PubMed  CAS  Google Scholar 

  • Gomez-Vicente V, Donovan M, Cotter TG. Multiple death pathways in retina-derived 661 W cells following growth factor deprivation: crosstalk between caspases and calpains. Cell Death Differ. 2005;12:796–804.

    PubMed  CAS  Google Scholar 

  • Hackam AS, Strom R, Liu D, Qian J, Wang C, Otteson D, Gunatilaka T, Farkas RH, Chowers I, Kageyama M, Leveillard T, Sahel JA, Campochiaro PA, Parmigiani G, Zack DJ. Identification of gene expression changes associated with the progression of retinal degeneration in the rd1 mouse. Invest Ophthalmol Vis Sci. 2004;45:2929–2942.

    PubMed  Google Scholar 

  • Haeseleer F, Imanishi Y, Maeda T, Possin DE, Maeda A, Lee A, Rieke F, Palczewski K. Essential role of Ca2+-binding protein 4, a Cav1.4 channel regulator, in photoreceptor synaptic function. Nat Neurosci. 2004;7:1079–1087.

    PubMed  CAS  Google Scholar 

  • Hajnoczky G, Csordas G, Das S, Garcia-Perez C, Saotome M, Sinha Roy S, Yi M. Mitochondrial calcium signalling and cell death: approaches for assessing the role of mitochondrial Ca2+ uptake in apoptosis. Cell Calcium. 2006;40:553–560. Review.

    PubMed  CAS  Google Scholar 

  • Hajnoczky G, Davies E, Madesh M. Calcium signaling and apoptosis. Biochem Biophys Res Commun. 2003;304:445–454.

    PubMed  CAS  Google Scholar 

  • Hart J, Wilkinson MF, Kelly ME, Barnes S. Inhibitory action of diltiazem on voltage-gated calcium channels in cone photoreceptors. Exp Eye Res. 2003;76:597–604.

    PubMed  CAS  Google Scholar 

  • Haverkamp S, Grunert U, Wassle H. The cone pedicle, a complex synapse in the retina. Neuron. 2000;27:85–95.

    PubMed  CAS  Google Scholar 

  • He L, Perkins GA, Poblenz AT, Harris JB, Hung M, Ellisman MH, Fox DA. Bcl-xL overexpres-sion blocks bax-mediated mitochondrial contact site formation and apoptosis in rod photo-receptors of lead-exposed mice. Proc Natl Acad Sci U S A. 2003;100:1022–1027.

    PubMed  CAS  Google Scholar 

  • He L, Poblenz AT, Medrano CJ, Fox DA. Lead and calcium produce rod photoreceptor cell apoptosis by opening the mitochondrial permeability transition pore. J Biol Chem. 2000;275:12175–12184.

    PubMed  CAS  Google Scholar 

  • Heidelberger R, Heinemann C, Neher E, Matthews G. Calcium dependence of the rate of exocy-tosis in a synaptic terminal. Nature. 1994;371:513–515.

    PubMed  CAS  Google Scholar 

  • Heidelberger R, Thoreson WB, Witkovsky P. Synaptic transmission at retinal ribbon synapses. Prog Retin Eye Res. 2005;24:682–720.

    PubMed  CAS  Google Scholar 

  • Hemara-Wahanui A, Berjukow S, Hope CI, Dearden PK, Wu SB, Wilson-Wheeler J, Sharp DM, Lundon-Treweek P, Clover GM, Hoda JC, Striessnig J, Marksteiner R, Hering S, Maw MA. A CACNA1F mutation identified in an X-linked retinal disorder shifts the voltage dependence of Cav1.4 channel activation. Proc Natl Acad Sci U S A. 2005;102:7553–7558.

    PubMed  CAS  Google Scholar 

  • Hernandez-Guijo JM, Maneu-Flores VE, Ruiz-Nuno A, Villarroya M, Garcia AG, Gandia L. Calcium-dependent inhibition of L, N, and P/Q Ca2+ channels in chromaffin cells: role of mitochondria. J Neurosci. 2001;21:2553–2560.

    PubMed  CAS  Google Scholar 

  • Higgs MH, Lukasiewicz PD. Activation of group II metabotropic glutamate receptors inhibits glutamate release from salamander retinal photoreceptors. Vis Neurosci. 2002;19:275–281.

    PubMed  Google Scholar 

  • Hirasawa H, Kaneko A. pH changes in the invaginating synaptic cleft mediate feedback from horizontal cells to cone photoreceptors by modulating Ca2+ channels. J Gen Physiol. 2003;122:657–671.

    PubMed  CAS  Google Scholar 

  • Hoda JC, Zaghetto F, Singh A, Koschak A, Striessnig J. Effects of congenital stationary night blindness type 2 mutations R508Q and L1364H on Cav1.4 L-type Ca2+ channel function and expression. J Neurochem. 2006;96:1648–1658.

    PubMed  CAS  Google Scholar 

  • Hood JL, Brooks WH, Roszman TL. Differential compartmentalization of the calpain/calpastatin network with the endoplasmic reticulum and Golgi apparatus. J Biol Chem. 2004;279: 43126–43135.

    PubMed  CAS  Google Scholar 

  • Hosoi N, Arai I, Tachibana M. Group III metabotropic glutamate receptors and exocytosed protons inhibit L-type calcium currents in cones but not in rods. J Neurosci. 2005;25:4062–4072.

    PubMed  CAS  Google Scholar 

  • Imredy JP, Yue DT. Submicroscopic Ca2+ diffusion mediates inhibitory coupling between individual Ca2+ channels. Neuron. 1992;9:197–207.

    PubMed  CAS  Google Scholar 

  • Jiang L, Katz BJ, Yang Z, Zhao Y, Faulkner N, Hu J, Baird J, Baehr W, Creel DJ, Zhang K. Auto-somal dominant cone dystrophy caused by a novel mutation in the GCAP1 gene (GUCA1A) Mol Vis. 2005;11:143–151.

    PubMed  CAS  Google Scholar 

  • Katai N, Yoshimura N. Apoptotic retinal neuronal death by ischemia-reperfusion is executed by two distinct caspase family proteases. Invest Ophthalmol Vis Sci. 1999;40:2697–2705.

    PubMed  CAS  Google Scholar 

  • Kawai F, Horiguchi M, Ichinose H, Ohkuma M, Isobe R, Miyachi E. Suppression by an h current of spontaneous Na+ action potentials in human cone and rod photoreceptors. Invest Ophthalmol Vis Sci. 2005;46:390–397.

    PubMed  Google Scholar 

  • Khimich D, Nouvian R, Pujol R, Tom Dieck S, Egner A, Gundelfinger ED, Moser T. Hair cell synaptic ribbons are essential for synchronous auditory signalling. Nature. 2005;434:889–894.

    PubMed  CAS  Google Scholar 

  • Khodair MA, Zarbin MA, Townes-Anderson E. Synaptic plasticity in mammalian photo-receptors prepared as sheets for retinal transplantation. Invest Ophthalmol Vis Sci. 2003;44:4976–4988.

    PubMed  Google Scholar 

  • Kleinschmidt J. Signal transmission at the photoreceptor synapse. Role of calcium ions and protons. Ann N Y Acad Sci. 1991;635:468–470.

    PubMed  CAS  Google Scholar 

  • Korenbrot JI, Rebrik TI. Tuning outer segment Ca2+ homeostasis to phototransduction in rods and cones. Adv Exp Med Biol. 2002;514:179–203.

    PubMed  CAS  Google Scholar 

  • Koschak A, Reimer D, Walter D, Hoda JC, Heinzle T, Grabner M, Striessnig J. Cav1.4alpha1 subunits can form slowly inactivating dihydropyridine-sensitive L-type Ca2+ channels lacking Ca2+-dependent inactivation. J Neurosci. 2003;23:6041–6049.

    PubMed  CAS  Google Scholar 

  • Koulen P, Liu J, Nixon E, Madry C. Interaction between mGluR8 and calcium channels in photo-receptors is sensitive to pertussis toxin and occurs via G protein betagamma subunit signaling Invest Ophthalmol Vis Sci. 2005;46:287–291.

    PubMed  Google Scholar 

  • Kourennyi DE, Barnes S. Depolarization-induced calcium channel facilitation in rod photo-receptors is independent of G proteins and phosphorylation. J Neurophysiol. 2000;84:133–138.

    PubMed  CAS  Google Scholar 

  • Kourennyi DE, Liu XD, Hart J, Mahmud F, Baldridge WH, Barnes S. Reciprocal modulation of calcium dynamics at rod and cone photoreceptor synapses by nitric oxide. J Neurophysiol. 2004;92:477–483.

    PubMed  CAS  Google Scholar 

  • Kreft M, Krizaj D, Grilc S, Zorec R. Properties of exocytotic response in vertebrate photorecep-tors. J Neurophysiol. 2003;90:218–225.

    PubMed  CAS  Google Scholar 

  • Krizaj D. Mesopic state: cellular mechanisms involved in pre- and post-synaptic mixing of rod and cone signals. Microsc Res Tech. 2000;50:347–359. Review.

    PubMed  CAS  Google Scholar 

  • Krizaj D. Compartmentalization of calcium entry pathways in mouse rods. Eur J Neurosci. 2005a;22:3292–3296.

    Google Scholar 

  • Krizaj D. Serca isoform expression in the mammalian retina. Exp Eye Res. 2005b;81:690–699.

    CAS  Google Scholar 

  • Krizaj D, Bao JX, Schmitz Y, Witkovsky P, Copenhagen DR. Caffeine-sensitive calcium stores regulate synaptic transmission from retinal rod photoreceptors. J Neurosci. 1999;19:7249–7261.

    PubMed  CAS  Google Scholar 

  • Krizaj D, Copenhagen DR. Compartmentalization of calcium extrusion mechanisms in the outer and inner segments of photoreceptors. Neuron 1998;21:249–256.

    PubMed  CAS  Google Scholar 

  • Krizaj D, Copenhagen DR. Calcium regulation in photoreceptors. Front Biosci. 2002;7:d2023–d2044.

    PubMed  CAS  Google Scholar 

  • Krizaj D, Demarco SJ, Johnson J, Strehler EE, Copenhagen DR. Cell-specific expression of plasma membrane calcium ATPase isoforms in retinal neurons. J Comp Neurol. 2002;451:1–21.

    PubMed  CAS  Google Scholar 

  • Krizaj D, Lai FA, Copenhagen DR. Ryanodine stores and calcium regulation in the inner segments of salamander rods and cones. J Physiol. 2003;547:761–774.

    PubMed  CAS  Google Scholar 

  • Krizaj D, Liu XL, Copenhagen DR. Expression of calcium transporters in the retina of the tiger salamander (Ambystoma tigrinum). J Comp Neurol. 2004;475:463–480.

    PubMed  CAS  Google Scholar 

  • Krizaj D, Witkovsky P. Effects of submicromolar concentrations of dopamine on photoreceptor to horizontal cell communication. Brain Res. 1993;627:122–128.

    PubMed  CAS  Google Scholar 

  • Lamb TD, Pugh EN Jr. Phototransduction, dark adaptation, and rhodopsin regeneration the proctor lecture. Invest Ophthalmol Vis Sci. 2006;47:5137–5152.

    PubMed  Google Scholar 

  • Lasansky A. Organization of the outer synaptic layer in the retina of the larval tiger salamander. Philos Trans R Soc Lond B Biol Sci. 1973;265:471–489.

    PubMed  CAS  Google Scholar 

  • Lasater EM, Witkovsky P. The calcium current of turtle cone photoreceptor axon terminals. Neurosci Res Suppl. 1991;15:S165–S173.

    PubMed  CAS  Google Scholar 

  • Lazzell DR, Belizaire R, Thakur P, Sherry DM, Janz R. SV2B regulates synaptotagmin 1 by direct interaction. J Biol Chem. 2004;279:52124–52131.

    PubMed  CAS  Google Scholar 

  • Leconte L, Barnstable CJ. Impairment of rod cGMP-gated channel alpha-subunit expression leads to photoreceptor and bipolar cell degeneration. Invest Ophthalmol Vis Sci. 2000;41:917–926.

    PubMed  CAS  Google Scholar 

  • Leist M, Volbracht C, Fava E, Nicotera P. 1-Methyl-4-phenylpyridinium induces autocrine exci-totoxicity, protease activation, and neuronal apoptosis. Mol Pharmacol. 1998;54:789–801.

    PubMed  CAS  Google Scholar 

  • Linden R, Rehen SK, Chiarini LB. Apoptosis in developing retinal tissue. Prog Retinal Eye Res. 1999;18:133–165.

    CAS  Google Scholar 

  • Llinas R, Sugimori M, Silver RB. Microdomains of high calcium concentration in a presynaptic terminal. Science. 1992a;256:677–679.

    CAS  Google Scholar 

  • Llinas R, Sugimori M, Silver RB. Presynaptic calcium concentration microdomains and transmitter release. J Physiol Paris. 1992b;86:135–138.

    CAS  Google Scholar 

  • Lohr HR, Kuntchithapautham K, Sharma AK, Rohrer B. Multiple, parallel cellular suicide mechanisms participate in photoreceptor cell death. Exp Eye Res. 2006;83:380–389.

    PubMed  CAS  Google Scholar 

  • Lolley RN. The rd gene defect triggers programmed rod cell death. The Proctor Lecture. Invest Ophthalmol Vis Sci. 1994;35:4182–4191.

    PubMed  CAS  Google Scholar 

  • Lolley RN, Farber DB, Rayborn ME, Hollyfield JG. Cyclic GMP accumulation causes degeneration of photoreceptor cells: simulation of an inherited disease. Science. 1977;196:664–666.

    PubMed  CAS  Google Scholar 

  • Maeda T, Lem J, Palczewski K, Haeseleer F. A critical role of CaBP4 in the cone synapse. Invest Ophthalmol Vis Sci. 2005;46:4320–4327.

    PubMed  Google Scholar 

  • Mansergh F, Orton NC, Vessey JP, Lalonde MR, Stell WK, Tremblay F, Barnes S, Rancourt DE, Bech-Hansen NT. Mutation of the calcium channel gene Cacna1f disrupts calcium signaling, synaptic transmission and cellular organization in mouse retina. Hum Mol Genet. 2005 Oct 14:3035–3046.

    PubMed  CAS  Google Scholar 

  • Maricq AV, Korenbrot JI. Calcium and calcium-dependent chloride currents generate action potentials in solitary cone photoreceptors. Neuron. 1988;1:503–515.

    PubMed  CAS  Google Scholar 

  • Mattson MP, Chan SL. Calcium orchestrates apoptosis. Nat Cell Biol. 2003;5:1041–1043.

    PubMed  CAS  Google Scholar 

  • Maximov A, Shin OH, Liu X, Sudhof TC. Synaptotagmin-12, a synaptic vesicle phosphoprotein that modulates spontaneous neurotransmitter release. J Cell Biol. 2007;176:113–124.

    PubMed  CAS  Google Scholar 

  • Maximov A, Sudhof TC. Autonomous function of synaptotagmin 1 in triggering synchronous release independent of asynchronous release. Neuron. 2005;48:547–554.

    PubMed  CAS  Google Scholar 

  • McGinnis JF, Matsumoto B, Whelan JP, Cao W. Cytoskeleton participation in subcellular trafficking of signal transduction proteins in rod photoreceptor cells. J Neurosci Res. 2002;67:290–297.

    PubMed  CAS  Google Scholar 

  • McRory JE, Hamid J, Doering CJ, Garcia E, Parker R, Hamming K, Chen L, Hildebrand M, Beedle AM, Feldcamp L, Zamponi GW, Snutch TP. The CACNA1F gene encodes an L-type calcium channel with unique biophysical properties and tissue distribution. J Neurosci. 2004;24:1707–1718.

    PubMed  CAS  Google Scholar 

  • Mervin K, Stone J. Developmental death of photoreceptors in the C57BL/6J mouse: association with retinal function and self-protection. Exp Eye Res. 2002;75:703–713.

    PubMed  CAS  Google Scholar 

  • Metea MR, Newman EA. Calcium signaling in specialized glial cells. Glia. 2006;54:650–655.

    PubMed  Google Scholar 

  • Minke B, Agam K. TRP gating is linked to the metabolic state and maintenance of the Drosophila photoreceptor cells. Cell Calcium. 2003;33:395–408.

    PubMed  CAS  Google Scholar 

  • Missler M, Zhang W, Rohlmann A, Kattenstroth G, Hammer RE, Gottmann K, Sudhof TC. Alpha-neurexins couple Ca2+ channels to synaptic vesicle exocytosis. Nature. 2003;423:939–948.

    PubMed  CAS  Google Scholar 

  • Miyake Y, Yagasaki K, Horiguchi M, Kawase Y, Kanda T. Congenital stationary night blindness with negative electroretinogram. A new classification. Arch Ophthalmol. 1986;104:1013–1020.

    PubMed  CAS  Google Scholar 

  • Morgans CW, El Far O, Bernstson A, Wassle H, Taylor WR. Calcium extrusion from mammalian photoreceptor terminals. J Neurosci 1998;18:2467–2474.

    PubMed  CAS  Google Scholar 

  • Nachman-Clewner M, St Jules R, Townes-Anderson E. L-type calcium channels in the photo-receptor ribbon synapse: localization and role in plasticity. J Comp Neurol. 1999;415:1–16.

    PubMed  CAS  Google Scholar 

  • Nakatani K, Chen C, Koutalos Y. Calcium diffusion coefficient in rod photoreceptor outer segments. Biophys J. 2002;82:728–739.

    PubMed  CAS  Google Scholar 

  • Nakatani K, Chen C, Yau KW, Koutalos Y. Calcium and phototransduction. Adv Exp Med Biol. 2002;514:1–20.

    PubMed  CAS  Google Scholar 

  • Neher E. The use of fura-2 for estimating Ca buffers and Ca fluxes. Neuropharmacology. 1995;34:1423–1442.

    PubMed  CAS  Google Scholar 

  • Neher E. Vesicle pools and Ca2+ microdomains: new tools for understanding their roles in neuro-transmitter release. Neuron. 1998;20:389–399.

    PubMed  CAS  Google Scholar 

  • Nicotera P, Orrenius S. The role of calcium in apoptosis. Cell Calcium. 1998;23:173–180.

    PubMed  CAS  Google Scholar 

  • Ohkuma M, Kawai F, Horiguchi M, Miyachi EI. Patch-clamp recording of human retinal photo-receptors and bipolar cells. Photochem Photobiol. 2007;83:317–322.

    PubMed  CAS  Google Scholar 

  • Osborne NN, Wood JPM, Cupido A, Melena J, Chidlow G. Topical flunarizine reduces IOP and protects the retina against ischemia-excitotoxicity. Invest Ophthalmol Vis Sci. 2002;43: 1456–1464.

    PubMed  Google Scholar 

  • Paillart C, Zhang K, Rebrik TI, Baehr W, Korenbrot JI. Cloning and molecular characterization of cGMP-gated ion channels from rod and cone photoreceptors of striped bass (M. saxatilis) retina. Vis Neurosci. 2006;23:99–113.

    PubMed  Google Scholar 

  • Palczewski K, Sokal I, Baehr W. Guanylate cyclase-activating proteins: structure, function, and diversity. Biochem Biophys Res Commun. 2004;322:1123–1130. Review.

    PubMed  CAS  Google Scholar 

  • Paquet-Durand F, Azadi D, Hauck SM, Uefong M, Veen T, Ekstrom P. Calpain is activated in degenerating photoreceptors in the rd1 mouse. J Neurochem. 2006;96:802–814.

    PubMed  CAS  Google Scholar 

  • Paquet-Durand F, Johnson L, Ekstrom P. Calpain activity in retinal degeneration. J Neurosci Res. 2007;85:693–702.

    PubMed  CAS  Google Scholar 

  • Paschen W. Mechanisms of neuronal cell death: diverse roles of calcium in the various subcel-lular compartments. Cell Calcium. 2003;34:305–310.

    PubMed  CAS  Google Scholar 

  • Pawlyk BS, Li T, Scimeca MS, Sandberg MA, Berson EL. Absence of photoreceptor rescue with D-cis-diltiazem in the rd mouse. Invest Ophthalmol Vis Sci. 2002;43:1912–1915.

    PubMed  Google Scholar 

  • Pearce-Kelling SE, Aleman TS, Nickle A, Laties AM, Aguirre GD, Jacobson SG, Acland GM. Calcium channel blocker D-cis-diltiazem does not slow retinal degeneration in the PDE6B mutant rcd1 canine model of retinitis pigmentosa. Mol Vis. 2001;25:42–47.

    Google Scholar 

  • Pearson RA, Catsicas M, Becker DL, Bayley P, Luneborg NL, Mobbs P. Ca(2+) signalling and gap junction coupling within and between pigment epithelium and neural retina in the developing chick. Eur J Neurosci. 2004;19:2435–2445.

    PubMed  Google Scholar 

  • Pearson R, Catsicas M, Becker D, Mobbs P. Purinergic and muscarinic modulation of the cell cycle and calcium signaling in the chick retinal ventricular zone. J Neurosci. 2002;22:7569–7579.

    PubMed  CAS  Google Scholar 

  • Pearson RA, Luneborg NL, Becker DL, Mobbs P. Gap junctions modulate interkinetic nuclear movement in retinal progenitor cells. J Neurosci. 2005;16:10803–10814.

    Google Scholar 

  • Peng YW, Sharp AH, Snyder SH, Yau KW. Localization of the inositol 1,4,5-trisphosphate receptor in synaptic terminals in the vertebrate retina. Neuron. 1991;6:525–531.

    PubMed  CAS  Google Scholar 

  • Piccolino M, Vellani V, Rakotobe LA, Pignatelli A, Barnes S, McNaughton P. Manipulation of synaptic sign and strength with divalent cations in the vertebrate retina: pushing the limits of tonic, chemical neurotransmission. Eur J Neurosci. 1999;11:4134–4138.

    PubMed  CAS  Google Scholar 

  • Pörn-Ares MI, Samali A, Orrenius S. Cleavage of the calpain inhibitor, calpastatin, during apop-tosis. Cell Death Differ. 1998;5:1028–1033.

    PubMed  Google Scholar 

  • Rabl K, Bryson EJ, Thoreson WB. Activation of glutamate transporters in rods inhibits presyn-aptic calcium currents. Vis Neurosci. 2003;20:557–566.

    PubMed  Google Scholar 

  • Rabl K, Thoreson WB. Calcium-dependent inactivation and depletion of synaptic cleft calcium ions combine to regulate rod calcium currents under physiological conditions. Eur J Neuro-sci. 2002;16:2070–2077.

    Google Scholar 

  • Raviola E, Gilula NB. Intramembrane organization of specialized contacts in the outer plexiform layer of the retina. A freeze-fracture study in monkeys and rabbits. J Cell Biol. 1975;65:192–222.

    PubMed  CAS  Google Scholar 

  • Ray SK, Wilford GG, Matzelle DC, Hogan EL, Banik NL. Calpeptin and methylprednisolone inhibit apoptosis in rat spinal cord injury. Ann N Y Acad Sci. 1999;890:261–269.

    PubMed  CAS  Google Scholar 

  • Read DS, McCal MA and Gregg RG. Absence of voltage-dependent calcium channels delays photoreceptor degeneration in rd mice Exp. Eye Res. 2002;75:415–420.

    CAS  Google Scholar 

  • Renterĺa RC, Strehler EE, Copenhagen DR, Krizaj D. Ontogeny of plasma membrane Ca2+ ATPase isoforms in the neural retina of the postnatal rat. Vis Neurosci. 2005;22:263–274.

    PubMed  Google Scholar 

  • Rieke F, Schwartz EA. A cGMP-gated current can control exocytosis at cone synapses. Neuron. 1994;13:863–873.

    PubMed  CAS  Google Scholar 

  • Rieke F, Schwartz EA. Asynchronous transmitter release: control of exocytosis and endocytosis at the salamander rod synapse. J Physiol. 1996;493:1–8.

    PubMed  CAS  Google Scholar 

  • Roberts WM. Localization of calcium signals by a mobile calcium buffer in frog saccular hair cells. J Neurosci. 1994;14:3246–3262.

    PubMed  CAS  Google Scholar 

  • Rohrer B, Pinto FR, Hulse KE, Lohr HR, Zhang L, Almeida JS. Multidestructive pathways triggered in photoreceptor cell death of the rd mouse as determined through gene expression profiling. J Biol Chem. 2004;279:41903–41910.

    PubMed  CAS  Google Scholar 

  • Rosenbaum EE, Hardie RC, Colley NJ. Calnexin is essential for rhodopsin maturation, Ca2+ regulation, and photoreceptor cell survival. Neuron. 2006;49:229–241.

    PubMed  CAS  Google Scholar 

  • Sakamoto YR, Nakajima TR, Fukiage CR, Sakai OR, Yoshida YR, Azuma MR, Shearer TR. Involvement of calpain isoforms in ischemia-reperfusion injury in rat retina. Curr Eye Res. 2000;21:571–580.

    PubMed  CAS  Google Scholar 

  • Samardzija M, Wenzel A, Thiersch M, Frigg R, Reme C, Grimm C. Caspase-1 ablation protects photoreceptors in a model of autosomal dominant retinitis pigmentosa. Invest Ophthalmol Vis Sci. 2006;47:5181–5190.

    PubMed  Google Scholar 

  • Sato M, Ohguro H, Ohguro I, Mamiya K, Takano Y, Yamazaki H, Metoki T, Miyagawa Y, Ishikawa F, Nakazawa M. Study of pharmacological effects of nilvadipine on RCS rat retinal degeneration by microarray analysis. Biochem Biophys Res Commun. 2003;306:826–831.

    PubMed  CAS  Google Scholar 

  • Schaeffer SF, Raviola E. Ultrastructural analysis of functional changes in the synaptic endings of turtle cone cells. Cold Spring Harb Symp Quant Biol. 1976;40:521–528.

    PubMed  CAS  Google Scholar 

  • Schmitz Y, Witkovsky P. Dependence of photoreceptor glutamate release on a dihydropyridine-sensitive calcium channel. Neuroscience. 1997;78:1209–1216.

    PubMed  CAS  Google Scholar 

  • Scorrano L, Oakes SA, Opferman JT, Cheng EH, Sorcinelli MD, Pozzan T, Korsmeyer SJ. BAX and BAK regulation of endoplasmic reticulum Ca2+: a control point for apoptosis. Science. 2003;300:135–139.

    PubMed  CAS  Google Scholar 

  • Sharma AK, Rohrer B. Calcium-induced calpain mediates apoptosis via caspase-3 in a mouse photoreceptor cell line. J Biol Chem. 2004;279:35564–35572.

    PubMed  CAS  Google Scholar 

  • Shoshan-Barmatz V, Orr I, Martin C, Vardi N. Novel ryanodine-binding properties in mammalian retina. Int J Biochem Cell Biol. 2005;37:1681–1695.

    PubMed  CAS  Google Scholar 

  • Singh A, Hamedinger D, Hoda JC, Gebhart M, Koschak A, Romanin C, Striessnig J. C-terminal modulator controls Ca2+-dependent gating of Ca(v)1.4 L-type Ca2+ channels. Nat Neurosci. 2006;9:1108–1116.

    PubMed  CAS  Google Scholar 

  • Sinha SR, Wu LG, Saggau P. Presynaptic calcium dynamics and transmitter release evoked by single action potentials at mammalian central synapses. Biophys J. 1997;72:637–651.

    PubMed  CAS  Google Scholar 

  • Sokal I, Li N, Verlinde CLMJ, Haeseleer F, Baehr W, Palczewski K. Ca-binding proteins in the retina: from discovery to etiology of human disease. Biochim Biophys Acta. 2000;1498: 233–251.

    PubMed  CAS  Google Scholar 

  • Sokolov M, Lyubarsky AL, Strissel KJ, Savchenko AB, Govardovskii VI, Pugh EN Jr, Arshavsky VY. Massive light-driven translocation of transducin between the two major compartments of rod cells: a novel mechanism of light adaptation. Neuron. 2002;34:95–106.

    PubMed  CAS  Google Scholar 

  • Song JY, Ichtchenko K, Sudhof TC, Brose N. Neuroligin 1 is a postsynaptic cell-adhesion molecule of excitatory synapses. Proc Natl Acad Sci U S A. 1999;96:1100–1105.

    PubMed  CAS  Google Scholar 

  • Steele EC, Chen X, Iuvone PM, MacLeish PR. Imaging of Ca2+ dynamics within the presynaptic terminals of salamander rod photoreceptors. J Neurophysiol. 2005;94:4544–4553.

    PubMed  CAS  Google Scholar 

  • Stella SL Jr, Bryson EJ, Thoreson WB. Insulin inhibits voltage-dependent calcium influx into rod photoreceptors. Neuroreport. 2001;12:947–951.

    PubMed  CAS  Google Scholar 

  • Stella SL, Bryson EJ, Thoreson WB. A2 adenosine receptors inhibit calcium influx through L-type calcium channels in rod photoreceptors of the salamander retina. J Neurophysiol. 2002;87:351–360.

    PubMed  CAS  Google Scholar 

  • Stella SL Jr, Thoreson WB. Differential modulation of rod and cone calcium currents in tiger salamander retina by D2 dopamine receptors and cAMP. Eur J Neurosci. 2000;12:3537–3548.

    PubMed  Google Scholar 

  • Strissel KJ, Lishko P V, Trieu LH, Kennedy MJ, Hurley JB, Arshavsky V Y. Recoverin undergoes light-dependent intracellular translocation in rod photoreceptors. J Biol Chem. 2005;280:29250–29255.

    PubMed  CAS  Google Scholar 

  • Strom TM, Nyakatura G, Apfelstedt-Sylla E, Hellebrand H, Lorenz B, Weber BH, Wutz K, Gutwillinger N, Ruther K, Drescher B, Sauer C, Zrenner E, Meitinger T, Rosenthal A, Meindl A. An L-type calcium-channel gene mutated in incomplete X-linked congenital stationary night blindness. Nat Genet. 1998;19:260–263.

    PubMed  CAS  Google Scholar 

  • Subramanian L, Polans AS. Cancer-related diseases of the eye: the role of calcium and calcium-binding proteins. Biochem Biophys Res Commun. 2004;322:1153–1165.

    PubMed  CAS  Google Scholar 

  • Sugioka M, Yamashita M. Calcium signaling to nucleus via store-operated system during cell cycle in retinal neuroepithelium. Neurosci Res. 2003;45:447–458.

    PubMed  CAS  Google Scholar 

  • Sugioka M, Zhou WL, Hofmann HD, Yamashita M. Ca2+ mobilization and capacitative Ca2+ entry regulate DNA synthesis in cultured chick retinal neuroepithelial cells. Int J Dev Neu-rosci. 1999;17:163–172.

    CAS  Google Scholar 

  • Suryanarayanan A, Slaughter MM. Synaptic transmission mediated by internal calcium stores in rod photoreceptors. J Neurosci. 2006;26:1759–1766.

    PubMed  CAS  Google Scholar 

  • Syed MM, Lee S, He S, Zhou ZJ. Spontaneous waves in the ventricular zone of developing mammalian retina. J Neurophysiol. 2004;91:1999–2009.

    PubMed  Google Scholar 

  • Szikra T, Cusato K, Krizaj D. Store-operated channels regulate baseline Ca in light-adapted pho-toreceptors. IOVS Abstr 2006, Ft. Lauderdale, FL.

    Google Scholar 

  • Szikra T, Krizaj D. The dynamic range and domain-specific signals of intracellular calcium in photoreceptors. Neuroscience. 2006;141:143–155.

    PubMed  CAS  Google Scholar 

  • Takano Y, Ohguro H, Dezawa M, Ishikawa H, Yamazaki H, Ohguro I, Mamiya K, Metoki T, Ishikawa F, Nakazawa M. Study of drug effects of calcium channel blockers on retinal degeneration of rd mouse. Biochem Biophys Res Commun. 2004;313:1015–1022.

    PubMed  CAS  Google Scholar 

  • Tatsukawa T, Hirasawa H, Kaneko A, Kaneda M. GABA-mediated component in the feedback response of turtle retinal cones. Vis Neurosci. 2005;22:317–324.

    PubMed  CAS  Google Scholar 

  • Thoreson WB, Bryson EJ, Rabl K. Reciprocal interactions between calcium and chloride in rod photoreceptors. J Neurophysiol. 2003;90:1747–1753.

    PubMed  CAS  Google Scholar 

  • Thoreson WB, Rabl K, Townes-Anderson E, Heidelberger R. A highly Ca2+-sensitive pool of vesicles contributes to linearity at the rod photoreceptor ribbon synapse. Neuron. 2004;42:595–605.

    PubMed  CAS  Google Scholar 

  • Thoreson WB, Stella SL Jr, Bryson EI, Clements J, Witkovsky P. D2-like dopamine receptors promote interactions between calcium and chloride channels that diminish rod synaptic transfer in the salamander retina. Vis Neurosci. 2002;19:235–247.

    PubMed  Google Scholar 

  • Toescu EC. Hypoxia sensing and pathways of cytosolic Ca2+ increases. Cell Calcium. 2004;36:187–199.

    PubMed  CAS  Google Scholar 

  • tom Dieck S, Altrock WD, Kessels MM, Qualmann B, Regus H, Brauner D, Fejtová A, Barcko O, Gundelfinger ED, Brandstätter JH. Molecular dissection of the photoreceptor ribbon synapse: physical interaction of Bassoon and RIBEYE is essential for the assembly of the ribbon complex. J Cell Biol. 2005;168:825–836.

    PubMed  Google Scholar 

  • Tremblay F, Laroche RG, De Becker I. The electroretinographic diagnosis of the incomplete form of congenital stationary night blindness. Vision Res. 1995;35:2383–2393.

    PubMed  CAS  Google Scholar 

  • Vallazza-Deschamps G, Fuchs C, Cia D, Tessier LH, Sahel JA, Dreyfus H, Picaud S. Diltiazem-induced neuroprotection in glutamate excitotoxicity and ischemic insult of retinal neurons. Doc Ophthalmol. 2005;110:25–35.

    PubMed  Google Scholar 

  • Verweij J, Hornstein EP, Schnapf JL. Surround antagonism in macaque cone photoreceptors. J Neurosci. 2003;23:10249–10257.

    PubMed  CAS  Google Scholar 

  • Verweij J, Kamermans M, Spekreijse H. Horizontal cells feed back to cones by shifting the cone calcium-current activation range. Vision Res. 1996;36:3943–3953.

    PubMed  CAS  Google Scholar 

  • Vessey JP, Stratis AK, Daniels BA, Da Silva N, Jonz MG, Lalonde MR, Baldridge WH, Barnes S. Proton-mediated feedback inhibition of presynaptic calcium channels at the cone photo-receptor synapse. J Neurosci. 2005;25:4108–4117.

    PubMed  CAS  Google Scholar 

  • von Gersdorff H, Matthews G. Calcium-dependent inactivation of calcium current in synaptic terminals of retinal bipolar neurons. J Neurosci. 1996;16:115–122.

    Google Scholar 

  • von Kriegstein K, Schmitz F, Lonk E, Sudhof T. Distribution of synaptic vesicle proteins in the mammalian retina identifies obligatory and facultative components of ribbon synapses. Eur J Neurosci. 1999;11:1335–1348.

    Google Scholar 

  • Wang TL, Sterling P, Vardi N. Localization of type I inositol 1,4,5-triphosphate receptor in the outer segments of mammalian cones. J Neurosci. 1999;19:4221–4228.

    PubMed  CAS  Google Scholar 

  • Wenzel A, Grimm C, Samardzija M, Reme CE. Molecular mechanisms of light-induced photo-receptor apoptosis and neuroprotection for retinal degeneration. Prog Retinal Eye Res. 2005;24:275–306.

    CAS  Google Scholar 

  • Wersinger E, Schwab Y, Sahel JA, Rendon A, Pow DV, Picaud S, Roux MJ. The glutamate transporter EAAT5 works as a presynaptic receptor in mouse rod bipolar cells. J Physiol. 2006;577:221–234.

    PubMed  CAS  Google Scholar 

  • Wilkinson MF, Barnes S. The dihydropyridine-sensitive calcium channel subtype in cone photo-receptors. J Gen Physiol. 1996;107:621–630.

    PubMed  CAS  Google Scholar 

  • Witkovsky P, Schmitz Y, Akopian A, Krizaj D, Tranchina D. Gain of rod to horizontal cell syn-aptic transfer: relation to glutamate release and a dihydropyridine-sensitive calcium current. J Neurosci. 1997;17:7297–7306.

    PubMed  CAS  Google Scholar 

  • Xu JW, Slaughter MM. Large-conductance calcium-activated potassium channels facilitate transmitter release in salamander rod synapse. J Neurosci. 2005;25:7660–7668.

    PubMed  CAS  Google Scholar 

  • Yagi T, MacLeish PR. Ionic conductances of monkey solitary cone inner segments. J Neurophysiol. 1994;71:656–665.

    PubMed  CAS  Google Scholar 

  • Yamazaki H, Ohguro H, Maeda T, Maruyama I, Takano Y, Metoki T, Nakazawa M, Sawada H, Dezawa M. Preservation of retinal morphology and functions in royal college surgeons rat by nilvadipine, a Ca(2+) antagonist. Invest Ophthalmol Vis Sci. 2002;43:919–926.

    PubMed  Google Scholar 

  • Yoon J, Ben-Ami HC, Hong YS, Park S, Strong LL, Bowman J, Geng C, Baek K, Minke B, Pak WL. Novel mechanism of massive photoreceptor degeneration caused by mutations in the trp gene of Drosophila. J Neurosci. 2000;20:649–659.

    PubMed  CAS  Google Scholar 

  • Yoshizawa K, Kiuchi K, Nambu H, Yang J, Senzaki H, Kiyozuka Y, Shikata N, Tsubura A. Caspase-3 inhibitor transiently delays inherited retinal degeneration in C3H mice carrying the rd gene. Graefes Arch Clin Exp Ophthalmol. 2002;240:214–219.

    PubMed  CAS  Google Scholar 

  • Zador A, Koch C. Linearized models of calcium dynamics: formal equivalence to the cable equation. J Neurosci. 1994;14:4705–4715.

    PubMed  CAS  Google Scholar 

  • Zeiss CJ, Neal J, Johnson EA. Caspase-3 in postnatal retinal development and degeneration. Invest Ophthalmol Vis Sci. 2004;45:964–970.

    PubMed  Google Scholar 

  • Zhang N, Beuve A, Townes-Anderson E. The nitric oxide-cGMP signaling pathway differentially regulates presynaptic structural plasticity in cone and rod cells. J Neurosci. 2005;25:2761–2770.

    PubMed  CAS  Google Scholar 

  • Zhou Z Y, Wan QF, Thakur P, Heidelberger R. Capacitance measurements in the mouse rod bipolar cell identify a pool of releasable synaptic vesicles. J Neurophysiol. 2006;96:2539–2548.

    PubMed  CAS  Google Scholar 

  • Zimov S, Yazulla S. Localization of vanilloid receptor 1 (TRPV1/VR1)-like immunoreactivity in goldfish and zebrafish retinas: restriction to photoreceptor synaptic ribbons. J Neurocytol. 2004;33:441–452.

    PubMed  CAS  Google Scholar 

  • Zufall F, Leinders-Zufall T. The cellular and molecular basis of odor adaptation. Chem Senses. 2000;25:473–481.

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Tamas Szikra is presently at the Friedrich Miescher Institute for Biomedical Research, Basel, Switzerland. We thank Prof. Paul Witkovsky (New York School of Medicine) for comments on the manuscript. The work was supported by a grant from the Hungarian Eötvös Fellowship and the Knights Templar Foundation (T.S.), by the National Institutes of Health (EY13870), and That Man May See Foundation to D.K. and an unrestricted grant from Research to Prevent Blindness to the University of Utah's Department of Ophthalmology. Also, Dr. Krizaj is a recipient of a Research to Prevent Blindness James S. Adams Award.

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2008 Humana Press, a part of Springer Science + Business Media, LLC

About this chapter

Cite this chapter

Szikra, T., Krizaj, D. (2008). Multiple Signaling Pathways Govern Calcium Homeostasis in Photoreceptor Inner Segments. In: Tombran-Tink, J., Barnstable, C.J. (eds) Visual Transduction and Non-Visual Light Perception. Ophthalmology Research. Humana Press. https://doi.org/10.1007/978-1-59745-374-5_9

Download citation

  • DOI: https://doi.org/10.1007/978-1-59745-374-5_9

  • Publisher Name: Humana Press

  • Print ISBN: 978-1-58829-957-4

  • Online ISBN: 978-1-59745-374-5

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics