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1 Chapter 51 Sensory Transduction Copyright © 2012, American Society for Neurochemistry. Published by Elsevier Inc. All rights reserved.
2 FIGURE 51-1: The vertebrate retina: A, amacrine cell; B, bipolar cell; BM, Bruchs membrane; C, ciliary process (cilium); CIS, cone inner segment; COS, cone outer segment; G, ganglion cell; H, horizontal cell; I, inner limiting membrane; M, Müller cell (glial cell); Me, melanin granule; MC, mitochondrion; N, nucleus; PE, retinal pigmented epithelium; RIS, rod inner segment; ROS, rod outer segment. (from H. Shichi, 2006). Copyright © 2012, American Society for Neurochemistry. Published by Elsevier Inc. All rights reserved.
3 FIGURE 51-2: The layers of the retina. Scanning electron micrograph of a mouse retina. OS, photoreceptor outer segments; IS, photoreceptor inner segments; ONL, outer nuclear layer, containing photoreceptor nuclei; OPL, outer plexiform layer, containing axonal termini of rods and cones, dendrites of bipolar cells and horizontal cells, and the synapses formed between them. INL, inner nuclear layer, containing nuclei of bipolar cells, horizontal cells, most amacrine cells, and Müller glial cells. Courtesy of Drs. Ivan Anastassov and Alecia K. Gross and the 2010 class of the Fundamental Issues in Vision Research course of the Marine Biological Laboratory, Woods Hole, MA. Copyright © 2012, American Society for Neurochemistry. Published by Elsevier Inc. All rights reserved.
4 FIGURE 51-3: Membrane organization of rod outer segments. Electron micrograph of an isolated mouse rod outer segment, flashfrozen in liquid ethane and imaged in vitreous ice, without stains or fixatives. The outer segment is suspended over a hole in a carbon film. The highly regular arrangement of the stacked disks and their relationship to the plasma membrane can be seen clearly. Courtesy of Drs. Jared C. Gilliam and Juan T. Chang and the National Center for Macromolecular Imaging. Copyright © 2012, American Society for Neurochemistry. Published by Elsevier Inc. All rights reserved.
5 FIGURE 51-4: Molecular transformations of retinoids in photoreceptors during the primary events of vision and the photoreceptor portion of the visual cycle. Rhodopsin is formed when the aldehyde moiety of 11-cis-retinal forms a protonated Schiffs base with lysine 296 of the apo-receptor opsin. Its absorbance spectrum shifts dramatically to the red, from a maximum absorbance in the ultraviolet (380 nm) to the visible (500 nm). Absorption by rhodopsin leads to a photoisomerization from all-trans to 11-cis, forming bathorhodopsin. In a series of protein conformational changes and deprotonation and protonation steps, bathorhodopsin relaxes to the form responsible for activating the G protein, metarhodopsin II. Ultimately, metarhodopsin II decays to metarhodopsin III, from which all-trans-retinal is hydrolyzed, generating a transient pool of free all- trans -retinal and opsin. Free all-trans -retinal is converted to all-trans-retinol by the action of a class of enzymes known as retinol de-hydrogenases (RDH), which use NADPH as the reductant. The all-trans-retinol can diffuse through the cell membrane and make its way to retinal pigmented epithelium, where further transformations of the visual cycle take place (see Fig. 51-10), eventually regenerating 11-cis-retinal. Copyright © 2012, American Society for Neurochemistry. Published by Elsevier Inc. All rights reserved.
6 FIGURE 51-5: Conformational activation of rhodopsin. Ribbon diagram of structure of dark, inactive state of rhodopsin (cyan ribbons) with the covalently coupled chromophore, 11-cis retinaldehyde shown in space-filling mode (cyan) (pdb file 1U19, Okada et al., 2004) superimposed on the structure of an active conformation of opsin (orange ribbons; pdb file 3DQB; Scheerer et al., 2008) with a C-terminal peptide from the visual G protein Gat bound (orange space-filling model) at its cytoplasmic face. All molecular graphics in this chapter were rendered with UCSF Chimera (Pettersen et al., 2004). Copyright © 2012, American Society for Neurochemistry. Published by Elsevier Inc. All rights reserved.
7 FIGURE 51-6: G protein activation by metarhodopsin II. In the dark, the visual G protein transducin exists primarily as a heterotrimer, Gαβ, with GDP bound to the Gαt subunit. This is the inactive state of the G protein, and it interacts only weakly with rhodopsin. GDP dissociation is extremely slow, occurring with a time constant of 10,000s. Upon light activation and formation of metarhodopsin II (MII), the heterotrimer binds MII, which induces a conformational change that allows rapid GDP dissociation. In the absence of GTP, this complex of MII (shown here as a dimer of MII and rhodopsin), and nucleotide-free Gαβ is very stable. Within the rod outer segment GTP concentration is on the order of 10 –3 mol/L, so that GDP binds very rapidly to the nucleotide-free Gαt subunit. GTP binding induces a conformational change (see Fig. 51-7) that causes Gαt–GTP to dissociate both from Gαβ and MII. Structures are based on the following pdb files: 1GOT (Lambright et al., 1996); 3DQ (Pettersen et al., 2004); and 1TND (Noel et al., 1993). Copyright © 2012, American Society for Neurochemistry. Published by Elsevier Inc. All rights reserved.
8 FIGURE 51-7: Conformational activation of transducin, Gαt. Ribbon diagram of structure of dark, inactive state of Gαt (cyan ribbons) with bound GDP shown in space-filling mode (cyan) (pdb file 1TAG, (Lambright et al., 1994) superimposed on the structure of an active conformation of Gαt (orange ribbons; pdb file 1TNDb (Noel et al., 1993); with a non-hydrolyzable GTP analogue bound (orange space- filling model; coordinated Mg 2+ in black). Copyright © 2012, American Society for Neurochemistry. Published by Elsevier Inc. All rights reserved.
9 FIGURE 51-8: Activation of PDE6 by activated transducin, Gαt-GTP. PDE6 is kept at a very low level of activity (PDE6i) in the dark by its inhibitory PDE6 subunits. In its GTP-bound form, Gαt binds tightly to PDE6 and relieves the inhibitory constraint imposed by PDE6, forming the active form PDE6*, and allowing rapid catalysis of cGMP hydrolysis. Structures taken from pdb file 1FQJ, Slep et al., 2001 (Gαt and C-terminal fragment of PDE6 ), and from unpublished electron microscopy data, courtesy of Dr. Zhixian Zhang (PDE6). Copyright © 2012, American Society for Neurochemistry. Published by Elsevier Inc. All rights reserved.
10 Copyright © 2012, American Society for Neurochemistry. Published by Elsevier Inc. All rights reserved. FIGURE 51-9: cGMP and CNG channel activity are regulated by PDE6, guanylate cyclase, GCAP and Ca 2+ feedback. cGMP is synthesized from GTP in a reaction that is catalyzed by guanylate cyclase, GCyclase, and releases inorganic pyrophosphate (PPi). PPi is rapidly hydrolyzed by inorganic pyrophosphatase (PPase), which drives the equilibrium toward cGMP formation. GCyclase is a transmembrane enzyme, bound constitutively to Ca 2+ sensors known as guanylate cyclase activating proteins (GCAP), which inhibit its activity in the moderate concentrations of intracellular Ca 2+ found in the dark. Thus GCyclase activity is low in the dark. Basal GCyclase activity in the dark is balanced by relatively low dark activity of PDE6, a cGMP-specific phosphodiesterase, which catalyzes hydrolysis of cGMP. A steady state [cGMP] of a few micromolar is established, and maintains enough CNG channels in the open state to produce a dark current of 10–20 pA, and a resting membrane potential near –40 mV. When PDE6 is converted to its active form, PDE6*, by binding Gαt-GTP generated by light activation of R*, PDE6* rapidly hydrolyzes cGMP leading to channel closure, blockage of the dark current, and membrane hyperpolarization. CNG channel closure also blocks Ca 2+ from leaking into the outer segment, whereas the Na + /K + /Ca 2+ exchanger continues to extrude Ca 2+ from the cytoplasm. Thus, in the light, cytoplasmic [Ca 2+ ] falls to very low levels, and the lowered Ca 2+ concentration leads to stimulation of the GCyclase/GCAP complex. Homeostasis is restored as cGMP is synthesized to balance its hydrolysis by PDE6*, and a new steady state is achieved. This Ca 2 + feedback mechanism ensures rapid recovery from light stimulation, and provides a mechanism contributing to light adaptation.
11 Copyright © 2012, American Society for Neurochemistry. Published by Elsevier Inc. All rights reserved. FIGURE 51-10: Recycling of retinoids by the enzymes of the visual cycle in the retinal pigmented epithelium (RPE). The alcohol all-trans-retinol moves from the photoreceptors to the RPE, where it is conjugated to fatty acids to produce retinyl esters in a reaction catalyzed by lecithin:retinol acyl transferase (LRAT), which transfers the fatty acyl group from phosphatidylcholine (lecithin). The retinyl esters then serve as substrates for a reaction catalyzed by an isomerohydrolase enzyme known as RPE65, in which the energy released by ester hydrolysis is harnessed to effect a trans-to-cis isomerization at the 11-position to form 11-cis -retinol. The 11-cis retinol is then oxidized in a reaction catalyzed by another retinol dehydrogenase (RDH) enzyme to form the aldehyde 11-cis -retinal, which returns to photoreceptors for regeneration of rhodopsin and cone pigments.
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