Thermal Properties of Rhodopsin: Insight into Molecular Mechanism of Dim-Light Vision

Liu, Jian; Liu, Monica; Nguyen, Jennifer B.; Bhagat, Aditi; Mooney, Victoria; Yan, Elsa C. Y.

doi:10.1016/j.bpj.2010.12.1881

Cited by 12 publications

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“…Fig. 2 E and F shows the Arrhenius plots for thermal isomerization and hydrolysis of the PSB, which are the two competing reactions responsible for thermal decay (12,13) (Fig. 2D).…”

Section: Resultsmentioning

confidence: 99%

“…In addition, the mutant S186A where the H-bonds in the retinyl binding site are disrupted (Fig. 4A) has rates increased by one to two orders of magnitude (11,13). It is, therefore, natural to consider that thermal decay at 52.0-64.6°C, close to T m , might involve breaking or at least weakening H-bonds associated with internal water molecules.…”

Section: Resultsmentioning

confidence: 99%

“…The procedures of preparing rhodopsin were described in detail elsewhere (13). The stable cell line of HEK293S expressing WT bovine opsin was made as previously described (32).…”

Section: Methodsmentioning

confidence: 99%

“…Fig. 2A shows the time-dependent UV-visible spectra of our expressed and purified bovine rhodopsin in 0.1% n-dodecyl-β-Dmaltoside (DDM) after being added to a preheated buffer that initiates the thermal decay, as in previous studies (12,13). The optical density at 500 nm (OD 500 ) decreases, whereas absorption at 380 nm (OD 380 ) increases, due to formation of all-trans retinyl Significance For vertebrates to have sensitive vision in dim light, any background signals in the dark must be minimal, i.e., thermal reactions of the visual pigment rhodopsin must be very slow.…”

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confidence: 93%

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Unusual kinetics of thermal decay of dim-light photoreceptors in vertebrate vision

Guo

Sekharan

Liu

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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We present measurements of rate constants for thermal-induced reactions of the 11-cis retinyl chromophore in vertebrate visual pigment rhodopsin, a process that produces noise and limits the sensitivity of vision in dim light. At temperatures of 52.0-64.6°C, the rate constants fit well to an Arrhenius straight line with, however, an unexpectedly large activation energy of 114 ± 8 kcal/mol, which is much larger than the 60-kcal/mol photoactivation energy at 500 nm. Moreover, we obtain an unprecedentedly large prefactor of 10 72±5 s −1 , which is roughly 60 orders of magnitude larger than typical frequencies of molecular motions! At lower temperatures, the measured Arrhenius parameters become more normal: E a = 22 ± 2 kcal/mol and A pref = 10 9±1 s −1 in the range of 37.0-44.5°C. We present a theoretical framework and supporting calculations that attribute this unusual temperature-dependent kinetics of rhodopsin to a lowering of the reaction barrier at higher temperatures due to entropy-driven partial breakup of the rigid hydrogen-bonding network that hinders the reaction at lower temperatures.non-Arrhenius | dim-light vision | transition state theory | isomerization rate R hodopsin is a vertebrate dim-light photoreceptor. Molecular studies of rhodopsin in recent decades have largely focused on its photochemistry and photoactivation (1-3). However, complete understanding of rhodopsin's function requires characterization of its thermal properties because thermal isomerization of the 11-cis retinyl chromophore can trigger the same physiological response as photo-isomerization, generating false visual signals as dark noise that jeopardizes photosensitivity (4-6). To enhance dim-light vision, rhodopsin has evolved to acquire remarkable thermal stability with a half-life of 420 y as determined by electrophysiological experiments using the outer segments of rod cells at 36°C (4). However, the molecular mechanism for the thermal stability has remained unclear. Here, we have addressed this by exploring the temperature dependence of thermal decay rate constants k(T) associated with isomerization of the retinyl chromophore and hydrolysis of the chromophore protonated Schiff-base (PSB) linkage, for temperatures ranging from the physiological temperature of 37.0°C to 64.6°C. In the upper range of temperatures from 52.0°C to 64.6°C, we find that the rate constants determined by UV-visible spectroscopy follow a linear Arrhenius model, k(T) = A pref exp(−E a /k B T), where k B is the Boltzmann constant (Fig. 1A). The slope, however, is very steep, giving an elevated activation energy, E a = 114 ± 8 kcal/mol. Surprisingly, this value is much higher than the photoactivation energy at visible wavelengths (60 kcal/mol at 500 nm). E a is also much higher than the reaction enthalpy change (32-35 kcal/mol) (7, 8) (Fig. 1B). In the lower temperature range of our rate constant measurements, 37.0-44.5°C, the slope of the Arrhenius plot decreases abruptly, as shown in Fig. 1A. Fitting a straight line through the low temperature points prod...

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“…Fig. 2 E and F shows the Arrhenius plots for thermal isomerization and hydrolysis of the PSB, which are the two competing reactions responsible for thermal decay (12,13) (Fig. 2D).…”

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

“…The procedures of preparing rhodopsin were described in detail elsewhere (13). The stable cell line of HEK293S expressing WT bovine opsin was made as previously described (32).…”

Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 93%

See 2 more Smart Citations

Unusual kinetics of thermal decay of dim-light photoreceptors in vertebrate vision

Guo

Sekharan

Liu

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

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show abstract

“…A sequence of conformational rearrangements causes the dark-adapted rhodopsin to undergo metarhodopsin II (Meta II) transition (Sakmar, 1997;Gelasco et al, 2000;Burns and Baylor, 2001;Okada et al, 2001;Isin et al, 2006). Given that Meta II comprises all-trans-retinal and opsin that bind together by a deprotonated Schiff base linkage, the absorbance of this light-activated intermediate is at 380 nm, reflecting around 120-nm blue shift relative to the maximal absorbance (λ max ) value of native rhodopsin (500 nm) (Borhan et al, 2000;Liu et al, 2011). A hydrolysis of Meta II results in the release of a free all-trans-retinal, followed by a reduction in the latter to all-trans-retinol under the action of all-trans-retinol dehydrogenases (atRDHs).…”

Section: Introductionmentioning

confidence: 99%

Structures and biogenetic analysis of lipofuscin bis-retinoids

Yao

2013

J. Zhejiang Univ. Sci. B

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Age-related macular degeneration (AMD) is still an incurable blinding eye disease because of complex pathogenic mechanisms and unusual diseased regions. With the use of chemical biology tools, great progress has been achieved in improving the understanding of AMD pathogenesis. The severity of AMD is, at least in part, linked to the non-degradable lipofuscin bis-retinoids in retinal pigment epithelial (RPE). This material is thought to result from the lifelong accumulation of lysosomal residual bodies containing the end products derived from the daily phagocytosis of rod outer segments by RPE cells. Here, we present previously recognized bis-retinoids with focus on structures and biosynthetic pathways. In addition to a brief discussion on the mutual conversion relationships of bis-retinoids, future perspectives and the medical relevance of such studies on these lipofuscin constituents are also highlighted.

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Biophotons Contribute to Retinal Dark Noise

Dai

2016

Neurosci. Bull.

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The discovery of dark noise in retinal photoreceptors resulted in a long-lasting controversy over its origin and the underlying mechanisms. Here, we used a novel ultra-weak biophoton imaging system (UBIS) to detect biophotonic activity (emission) under dark conditions in rat and bullfrog (Rana catesbeiana) retinas in vitro. We found a significant temperature-dependent increase in biophotonic activity that was completely blocked either by removing intracellular and extracellular Ca(2+) together or inhibiting phosphodiesterase 6. These findings suggest that the photon-like component of discrete dark noise may not be caused by a direct contribution of the thermal activation of rhodopsin, but rather by an indirect thermal induction of biophotonic activity, which then activates the retinal chromophore of rhodopsin. Therefore, this study suggests a possible solution regarding the thermal activation energy barrier for discrete dark noise, which has been debated for almost half a century.

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Thermal Properties of Rhodopsin: Insight into Molecular Mechanism of Dim-Light Vision

Cited by 12 publications

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Unusual kinetics of thermal decay of dim-light photoreceptors in vertebrate vision

Unusual kinetics of thermal decay of dim-light photoreceptors in vertebrate vision

Structures and biogenetic analysis of lipofuscin bis-retinoids

Biophotons Contribute to Retinal Dark Noise

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