Tuning Outer Segment Ca2+Homeostasis to Phototransduction in Rods and Cones

Korenbrot, Juan I.; Rebrik, Tatiana I.

doi:10.1007/978-1-4615-0121-3_11

Cited by 56 publications

(51 citation statements)

References 78 publications

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“…6E) at the level of the connecting cilium and the anatomical substrate for this IS staining remains to be determined. Given the canonical view of Ca 2+ regulation in photoreceptor outer segments (Fain et al, 2001;Korenbrot and Rebrik, 2002), the staining of outer segments of cones by the SERCA3 antibody was unexpected. Several lines of evidence suggest that the antigen recognition by N89, the SERCA3 antibody, was specific: (1) Western blots from whole mouse retinas probed with the SERCA3 antibody showed a distinct band at 97 kDa, corresponding to the molecular weight of SERCA3 (Krizaj et al, 2004).…”

Section: Serca3 Signal In Cone Photoreceptorsmentioning

confidence: 98%

“…Ca 2+ extrusion in cone OS is about six-fold faster than in rods (integration time in cones is ~ 50 msec; Nakatani and Yau, 1989; reviewed in Korenbrot and Rebrik, 2002). Ca 2+ decay in cones may be faster than in rods due to greater surface-to-volume ratio of cone OSs or some difference in the properties of NCKX exchangers and/or buffering proteins.…”

Section: Functional Implicationsmentioning

confidence: 99%

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Serca isoform expression in the mammalian retina

Križaj¹

2005

Experimental Eye Research

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The sarcoplasmic-endoplasmic reticulum calcium ATPase (SERCA) is a key intracellular calcium transporter, which regulates cellular calcium concentration [Ca 2+ ] by transporting Ca 2+ ions from the cytosol into the endoplasmic reticulum. SERCA-mediated Ca 2+ sequestration controls proper folding of newly synthesized proteins within the ER as well as the timing and spatial patterning of depolarization-evoked Ca 2+ responses in the cytoplasm. We studied expression and distribution of all three SERCA isoforms in the mouse retina using isoform-specific antibodies. No immunostaining was observed with the SERCA1 antibody. SERCA2 was expressed in photoreceptor inner segments, amacrine and ganglion cells of the mouse retina. Similar SERCA2 localization was observed in adult rat, macaque and ground squirrel retinas. Analysis of distribution of SERCA2 immunofluorescence in the developing mouse retina revealed prominent SERCA2 signals throughout postnatal development. The antibody raised against the SERCA3 isoform labeled inner segments of photoreceptors and cell bodies in the inner nuclear layer of the mouse retina. The SERCA3 signal was detected in the inner plexiform layer of the early postnatal retina, but moved by P10 to the outer retina where it was concentrated in outer segments of cones. These results indicate that SERCA2 represents the dominant SERCA isoform in the mammalian retina. SERCA3 may contribute to calcium regulation in photoreceptors and bipolar cells.

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Section: Serca3 Signal In Cone Photoreceptorsmentioning

confidence: 98%

Section: Functional Implicationsmentioning

confidence: 99%

Serca isoform expression in the mammalian retina

Križaj¹

2005

Experimental Eye Research

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“…With regard to the latter, rod/ cone differences in release kinetics are not explained by the contribution of CICR to synaptic release from rods [136]. Akin to the outer segment in which differences in mechanisms of calcium homeostasis contribute to the ability of cones to respond more rapidly than rods to light [11], differences in intraterminal calcium handling and calcium-dependent enzymes also help to shape differences in the kinetics of release by rods and cones.…”

Section: Conclusion and Future Questionsmentioning

confidence: 99%

“…The light responses of cones are five to ten times faster than those of rods [7][8][9], resulting in a higher flicker fusion frequency for cones than rods [10]. Rod/cone differences in light response kinetics involve rod/cone differences in outer segment Ca 2+ homeostasis as well as faster inactivation of transduction cascade enzymes in cones [11].…”

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confidence: 99%

Kinetics of Synaptic Transmission at Ribbon Synapses of Rods and Cones

Thoreson

2007

Mol Neurobiol

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The ribbon synapse is a specialized structure that allows photoreceptors to sustain the continuous release of vesicles for hours upon hours and years upon years but also respond rapidly to momentary changes in illumination. Light responses of cones are faster than those of rods and, mirroring this difference, synaptic transmission from cones is also faster than transmission from rods. This review evaluates the various factors that regulate synaptic kinetics and contribute to kinetic differences between rod and cone synapses. Presynaptically, the release of glutamate-laden synaptic vesicles is regulated by properties of the synaptic proteins involved in exocytosis, influx of calcium through calcium channels, calcium release from intracellular stores, diffusion of calcium to the release site, calcium buffering, and extrusion of calcium from the cytoplasm. The rate of vesicle replenishment also limits the ability of the synapse to follow changes in release. Post-synaptic factors include properties of glutamate receptors, dynamics of glutamate diffusion through the cleft, and glutamate uptake by glutamate transporters. Thus, multiple synaptic mechanisms help to shape the responses of second-order horizontal and bipolar cells. KeywordsPhotoreceptor; Synaptic transmission; Glutamate; Calcium; Vesicles; Retina Vision begins with the transduction of light into membrane potential changes as the result of an enzymatic cascade occurring in the outer segments of rod and cone photoreceptors [1,2]. Light-evoked membrane potential changes are modified by voltage-dependent currents in the inner segment [3] and transmitted to second order bipolar and horizontal cells by changes in release of the neurotransmitter, L-glutamate, from the synaptic terminals of both rods and cones. Because all of the visual information available to downstream retinal neurons must first pass through the photoreceptor synapse, synaptic transmission from photoreceptors has a considerable impact on visual perception. The focus of this review is on mechanisms that shape the kinetics of synaptic transmission at synapses of rods and cones. Additional information on other physiological and anatomical characteristics of photoreceptor ribbon synapses can be found in recent reviews [4][5][6]. Differences in Rod and Cone KineticsRod and cone photoreceptors are tonically depolarized in darkness with membrane potentials of −35 to −45 mV that allow continuous release of the neurotransmitter, L-glutamate. Light onset causes photoreceptors to hyperpolarize by as much as 30 mV, leading to a reduction in

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“…These differential characteristics can be attributed, in part, to differences in Ca 2+ handling processes and suggest that rods and cones possess different NCKX isoforms (30). The cloning of NCKX2 from chicken retina, which is abundant in cone photoreceptors, suggested a role for this exchanger in cone physiology that was analogous to that of NCKX1 in rod photoreceptors (47).…”

Section: Structure and Functionmentioning

confidence: 99%

K⁺-Dependent Na⁺/Ca²⁺Exchangers: Key Contributors to Ca²⁺Signaling

Visser

Lytton

2007

Physiology

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Ca 2+ acts as a ubiquitous second messenger to control a wide variety of physiological processes by relaying information within mammalian cells (6). For example, Ca 2+ signals trigger fertilization, control development and differentiation, coordinate cellular functions, and even play roles in cell death. The large variety of functional effects are dictated by the spatial and temporal nature of the Ca 2+ signals and by the cellular context in which they occur, that is, the tissue and cell-specific complement of Ca 2+ influx/efflux pathways and downstream targets determine the final outcome. Cytosolic Ca 2+ influx typically occurs when Ca 2+ channels localized to the plasma or endoplasmic reticular membranes open in response to various stimuli such as membrane depolarization or ligand binding (5). Ca 2+ can be subsequently removed from the cytosol by various mechanisms: sarco/endoplasmic reticulum Ca 2+ ATPases (SERCA) and plasma membrane Ca 2+ ATPases (PMCA) utilize the energy from ATP hydrolysis to pump Ca 2+ into the endoplasmic reticulum or outside the cell, respectively, and Na + /Ca 2+ exchangers extrude cytosolic Ca 2+ in exchange for extracellular Na + . In certain cellular contexts, such as localized signals in the dendritic spines of neurons, Ca 2+ flux across the plasma membrane predominates over that from intracellular stores (2, 49). In such cases, PMCA proteins control the resting Ca 2+ concentrations because of their high-affinity/lowcapacity transport properties, whereas Na + /Ca 2+ exchangers display low-affinity/high-capacity transport properties that are ideally suited for cytosolic clearance when Ca 2+ is elevated following a signaling event. Detailed knowledge of the physiological and biochemical properties of calcium channels and transporters is critical to understanding the mechanisms of Ca 2+ signaling in various cellular contexts. This review will focus on recent progress in the understanding of the physiology, function, structure, and regulation of the recently identified family of K + -dependent Na + /Ca 2+ exchangers. K + -Dependent and Independent Na + /Ca 2+ ExchangersThere are two families of Na + /Ca 2+ exchangers in mammalian cells: those that are K + -dependent (NCKX) and those that are K + -independent (NCX). Physiologically, NCX proteins function by extruding cytosolic Ca 2+ in exchange for extracellular Na + ions, whereas NCKX proteins extrude cytosolic Ca 2+ and K + in exchange for Na + ions, which in both cases is referred to as forward mode exchange. In conditions of altered ion gradients and membrane potential, these exchangers can also mediate Ca 2+ entry or so-called reverse mode operation. Three NCX and five NCKX isoforms have been identified by molecular cloning. NCX1 is predominantly expressed in the heart, brain, and kidney, although it is also present in a broad variety of cell types, whereas NCX2 and 3 expression is limited to brain and skeletal muscle (38,42,43). NCKX1 is exclusively expressed in retinal rod outer segments, whereas NCKX2 is expressed in brain and c...

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Tuning Outer Segment Ca2+Homeostasis to Phototransduction in Rods and Cones

Cited by 56 publications

References 78 publications

Serca isoform expression in the mammalian retina

Serca isoform expression in the mammalian retina

Kinetics of Synaptic Transmission at Ribbon Synapses of Rods and Cones

K⁺-Dependent Na⁺/Ca²⁺Exchangers: Key Contributors to Ca²⁺Signaling

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Tuning Outer Segment Ca2+Homeostasis to Phototransduction in Rods and Cones

Cited by 56 publications

References 78 publications

Serca isoform expression in the mammalian retina

Serca isoform expression in the mammalian retina

Kinetics of Synaptic Transmission at Ribbon Synapses of Rods and Cones

K+-Dependent Na+/Ca2+Exchangers: Key Contributors to Ca2+Signaling

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K⁺-Dependent Na⁺/Ca²⁺Exchangers: Key Contributors to Ca²⁺Signaling