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2015 | OriginalPaper | Chapter

A Stochastic Model of the Melanopsin Phototransduction Cascade

Authors : R. Lane Brown, Erika Camacho, Evan G. Cameron, Christina Hamlet, Kathleen A. Hoffman, Hye-Won Kang, Phyllis R. Robinson, Katherine S. Williams, Glenn R. Wyrick

Published in: Applications of Dynamical Systems in Biology and Medicine

Publisher: Springer New York

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Abstract

Melanopsin is an unusual vertebrate photopigment that, in mammals, is expressed in a small subset of intrinsically photosensitive retinal ganglion cells (ipRGCs), whose signaling has been implicated in non-image forming vision, regulating such functions as circadian rhythms, pupillary light reflex, and sleep. The biochemical cascade underlying the light response in ipRGCs has not yet been fully elucidated. We developed a stochastic model of the hypothesized melanopsin phototransduction cascade and illustrated that the stochastic model can qualitatively reproduce experimental results under several different conditions. The model allows us to probe various mechanisms in the phototransduction cascade in a way that is not currently experimentally feasible.

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Literature
1.
go back to reference Berson, D.M., Castrucci, A.M., Provencio, I.: Morphology and mosaics of melanopsin-expressing retinal ganglion cell types in mice. Journal of Comparative Neurology 518(13), 2405–2422 (2010) Berson, D.M., Castrucci, A.M., Provencio, I.: Morphology and mosaics of melanopsin-expressing retinal ganglion cell types in mice. Journal of Comparative Neurology 518(13), 2405–2422 (2010)
2.
go back to reference Blasic Jr., J.R., Matos-Cruz, V., Ujla, D., Cameron, E.G., Hattar, S., Halpern, M.E., Robinson, P.R.: Identification of critical phosphorylation sites on the carboxy tail of melanopsin. Biochemistry 53(16), 2644–2649 (2014)CrossRef Blasic Jr., J.R., Matos-Cruz, V., Ujla, D., Cameron, E.G., Hattar, S., Halpern, M.E., Robinson, P.R.: Identification of critical phosphorylation sites on the carboxy tail of melanopsin. Biochemistry 53(16), 2644–2649 (2014)CrossRef
3.
go back to reference Cameron, E.G., Robinson, P.R.: β-arrestin-dependent deactivation of mouse melanopsin. PloS one 9(11) (2014). e113138 Cameron, E.G., Robinson, P.R.: β-arrestin-dependent deactivation of mouse melanopsin. PloS one 9(11) (2014). e113138
4.
go back to reference Caruso, G., Bisegna, P., Andreucci, D., Lenoci, L., Gurevich, V.V., Hamm, H.E., DiBenedetto, E.: Identification of key factors that reduce the variability of the single photon response. Proceedings of the National Academy of Sciences 108(19), 7804–7807 (2011)CrossRef Caruso, G., Bisegna, P., Andreucci, D., Lenoci, L., Gurevich, V.V., Hamm, H.E., DiBenedetto, E.: Identification of key factors that reduce the variability of the single photon response. Proceedings of the National Academy of Sciences 108(19), 7804–7807 (2011)CrossRef
5.
go back to reference Do, M.T.H., Yau, K.W.: Intrinsically photosensitive retinal ganglion cells. Physiological Reviews 90(4), 1547–1581 (2010)CrossRef Do, M.T.H., Yau, K.W.: Intrinsically photosensitive retinal ganglion cells. Physiological Reviews 90(4), 1547–1581 (2010)CrossRef
6.
go back to reference Do, M.T.H., Yau, K.W.: Adaptation to steady light by intrinsically photosensitive retinal ganglion cells. Proceedings of the National Academy of Sciences 110(18), 7470–7475 (2013)CrossRef Do, M.T.H., Yau, K.W.: Adaptation to steady light by intrinsically photosensitive retinal ganglion cells. Proceedings of the National Academy of Sciences 110(18), 7470–7475 (2013)CrossRef
7.
go back to reference Gillespie, D.T.: A general method for numerically simulating the stochastic time evolution of coupled chemical reactions. Journal of Computational Physics 22(4), 403–434 (1976)MathSciNetCrossRef Gillespie, D.T.: A general method for numerically simulating the stochastic time evolution of coupled chemical reactions. Journal of Computational Physics 22(4), 403–434 (1976)MathSciNetCrossRef
8.
go back to reference Gillespie, D.T.: Exact stochastic simulation of coupled chemical reactions. Journal of Physical Chemistry 81(25), 2340–2361 (1977)CrossRef Gillespie, D.T.: Exact stochastic simulation of coupled chemical reactions. Journal of Physical Chemistry 81(25), 2340–2361 (1977)CrossRef
9.
go back to reference Gooley, J.J., Lu, J., Fischer, D., Saper, C.B.: A broad role for melanopsin in nonvisual photoreception. Journal of Neuroscience 23(18), 7093–7106 (2003) Gooley, J.J., Lu, J., Fischer, D., Saper, C.B.: A broad role for melanopsin in nonvisual photoreception. Journal of Neuroscience 23(18), 7093–7106 (2003)
10.
go back to reference Graham, D.M., Wong, K.Y., Shapiro, P., Frederick, C., Pattabiraman, K., Berson, D.M.: Melanopsin ganglion cells use a membrane-associated rhabdomeric phototransduction cascade. Journal of Neurophysiology 99(5), 2522–2532 (2008)CrossRef Graham, D.M., Wong, K.Y., Shapiro, P., Frederick, C., Pattabiraman, K., Berson, D.M.: Melanopsin ganglion cells use a membrane-associated rhabdomeric phototransduction cascade. Journal of Neurophysiology 99(5), 2522–2532 (2008)CrossRef
11.
go back to reference Hamer, R.D., Nicholas, S.C., Tranchina, D., Lamb, T.D., Jarvinen, J.L.P.: Toward a unified model of vertebrate rod phototransduction. Visual Neuroscience 22(04), 417–436 (2005)CrossRef Hamer, R.D., Nicholas, S.C., Tranchina, D., Lamb, T.D., Jarvinen, J.L.P.: Toward a unified model of vertebrate rod phototransduction. Visual Neuroscience 22(04), 417–436 (2005)CrossRef
12.
go back to reference Hamer, R.D., Nicholas, S.C., Tranchina, D., Liebman, P.A., Lamb, T.D.: Multiple steps of phosphorylation of activated rhodopsin can account for the reproducibility of vertebrate rod single-photon responses. Journal of General Physiology 122(4), 419–444 (2003)CrossRef Hamer, R.D., Nicholas, S.C., Tranchina, D., Liebman, P.A., Lamb, T.D.: Multiple steps of phosphorylation of activated rhodopsin can account for the reproducibility of vertebrate rod single-photon responses. Journal of General Physiology 122(4), 419–444 (2003)CrossRef
13.
go back to reference Hardie, R.C.: TRP channels and lipids: from Drosophila to mammalian physiology. Journal of Physiology 578(1), 9–24 (2007)CrossRef Hardie, R.C.: TRP channels and lipids: from Drosophila to mammalian physiology. Journal of Physiology 578(1), 9–24 (2007)CrossRef
14.
go back to reference Hattar, S., Kumar, M., Park, A., Tong, P., Tung, J., Yau, K.W., Berson, D.M.: Central projections of melanopsin-expressing retinal ganglion cells in the mouse. Journal of Comparative Neurology 497(3), 326–349 (2006)CrossRef Hattar, S., Kumar, M., Park, A., Tong, P., Tung, J., Yau, K.W., Berson, D.M.: Central projections of melanopsin-expressing retinal ganglion cells in the mouse. Journal of Comparative Neurology 497(3), 326–349 (2006)CrossRef
15.
go back to reference Hofmann, T., Obukhov, A.G., Schaefer, M., Harteneck, C., Gudermann, T., Schultz, G.: Direct activation of human TRPC6 and TRPC3 channels by diacylglycerol. Nature 397(6716), 259–263 (1999)CrossRef Hofmann, T., Obukhov, A.G., Schaefer, M., Harteneck, C., Gudermann, T., Schultz, G.: Direct activation of human TRPC6 and TRPC3 channels by diacylglycerol. Nature 397(6716), 259–263 (1999)CrossRef
16.
go back to reference Hu, C., Hill, D.J.D., Wong, K.Y.: Intrinsic physiological properties of the five types of mouse ganglion-cell photoreceptors. Journal of Neurophysiology 109(7), 1876–1889 (2013)CrossRef Hu, C., Hill, D.J.D., Wong, K.Y.: Intrinsic physiological properties of the five types of mouse ganglion-cell photoreceptors. Journal of Neurophysiology 109(7), 1876–1889 (2013)CrossRef
17.
go back to reference Hughes, S., Jagannath, A.,, Hickey, D., Gatti, S., Wood, M., Peirson, S.N., Foster, R.G., Hankins, M.W.: Using siRNA to define functional interactions between melanopsin and multiple G protein partners. Cellular and Molecular Life Sciences (2014). DOI 10.1007/s00018-014-1664-6 Hughes, S., Jagannath, A.,, Hickey, D., Gatti, S., Wood, M., Peirson, S.N., Foster, R.G., Hankins, M.W.: Using siRNA to define functional interactions between melanopsin and multiple G protein partners. Cellular and Molecular Life Sciences (2014). DOI 10.1007/s00018-014-1664-6
18.
go back to reference Hurley, J.B., Spencer, M., Niemi, G.A.: Rhodopsin phosphorylation and its role in photoreceptor function. Vision Research 38(10), 1341–1352 (1998)CrossRef Hurley, J.B., Spencer, M., Niemi, G.A.: Rhodopsin phosphorylation and its role in photoreceptor function. Vision Research 38(10), 1341–1352 (1998)CrossRef
19.
go back to reference Invergo, B.M., Montanucci, L., Koch, K.W., Bertranpetit, J., Dell’Orco, D.: Exploring the rate-limiting steps in visual phototransduction recovery by bottom-up kinetic modeling. Cell Communication and Signaling 11(1), 36 (2013)CrossRef Invergo, B.M., Montanucci, L., Koch, K.W., Bertranpetit, J., Dell’Orco, D.: Exploring the rate-limiting steps in visual phototransduction recovery by bottom-up kinetic modeling. Cell Communication and Signaling 11(1), 36 (2013)CrossRef
20.
go back to reference Kennedy, M.J., Dunn, F.A., Hurley, J.B.: Visual pigment phosphorylation but not transducin translocation can contribute to light adaptation in zebrafish cones. Neuron 41(6), 915–928 (2004)CrossRef Kennedy, M.J., Dunn, F.A., Hurley, J.B.: Visual pigment phosphorylation but not transducin translocation can contribute to light adaptation in zebrafish cones. Neuron 41(6), 915–928 (2004)CrossRef
21.
go back to reference Korenbrot, J.I.: Speed, adaptation, and stability of the response to light in cone photoreceptors: The functional role of Ca-dependent modulation of ligand sensitivity in cGMP-gated ion channels. Journal of General Physiology 139(1), 31–56 (2012)CrossRef Korenbrot, J.I.: Speed, adaptation, and stability of the response to light in cone photoreceptors: The functional role of Ca-dependent modulation of ligand sensitivity in cGMP-gated ion channels. Journal of General Physiology 139(1), 31–56 (2012)CrossRef
22.
go back to reference Kurtz, T.G.: The relationship between stochastic and deterministic models for chemical reactions. Journal of Chemical Physics 57(7), 2976–2978 (1972)CrossRef Kurtz, T.G.: The relationship between stochastic and deterministic models for chemical reactions. Journal of Chemical Physics 57(7), 2976–2978 (1972)CrossRef
23.
go back to reference Lamb, T.D., Pugh Jr., E.N.: A quantitative account of the activation steps involved in phototransduction in amphibian photoreceptors. Journal of Physiology 449(1), 719–758 (1992)CrossRef Lamb, T.D., Pugh Jr., E.N.: A quantitative account of the activation steps involved in phototransduction in amphibian photoreceptors. Journal of Physiology 449(1), 719–758 (1992)CrossRef
24.
go back to reference Liu, W., Wen, W., Wei, Z., Yu, J., Ye, F., Liu, C.H., Hardie, R.C., Zhang, M.: The INAD scaffold is a dynamic, redox-regulated modulator of signaling in the Drosophila eye. Cell 145(7), 1088–1101 (2011)CrossRef Liu, W., Wen, W., Wei, Z., Yu, J., Ye, F., Liu, C.H., Hardie, R.C., Zhang, M.: The INAD scaffold is a dynamic, redox-regulated modulator of signaling in the Drosophila eye. Cell 145(7), 1088–1101 (2011)CrossRef
25.
go back to reference Lucas, R.J.: Mammalian inner retinal photoreception. Current Biology 23(3) (2013). R125-133CrossRef Lucas, R.J.: Mammalian inner retinal photoreception. Current Biology 23(3) (2013). R125-133CrossRef
26.
go back to reference Marino, S., Hogue, I.B., Ray, C.J., Kirschner, D.E.: A methodology for performing global uncertainty and sensitivity analysis in systems biology. Journal of Theoretical Biology 254(1), 178–196 (2008)MathSciNetCrossRef Marino, S., Hogue, I.B., Ray, C.J., Kirschner, D.E.: A methodology for performing global uncertainty and sensitivity analysis in systems biology. Journal of Theoretical Biology 254(1), 178–196 (2008)MathSciNetCrossRef
27.
go back to reference Mendez, A., Burns, M.E., Roca, A., Lem, J., Wu, L.W., Simon, M.I., Baylor, D.A., Chen, J.: Rapid and reproducible deactivation of rhodopsin requires multiple phosphorylation sites. Neuron 28(1), 153–164 (2000)CrossRef Mendez, A., Burns, M.E., Roca, A., Lem, J., Wu, L.W., Simon, M.I., Baylor, D.A., Chen, J.: Rapid and reproducible deactivation of rhodopsin requires multiple phosphorylation sites. Neuron 28(1), 153–164 (2000)CrossRef
28.
go back to reference Palczewski, K.: Chemistry and biology of vision. Journal of Biological Chemistry 287(3), 1612–1619 (2012)CrossRef Palczewski, K.: Chemistry and biology of vision. Journal of Biological Chemistry 287(3), 1612–1619 (2012)CrossRef
29.
go back to reference Porter, M.L., Blasic, J.R., Bok, M.J., Cameron, E.G., Pringle, T., Cronin, T.W., Robinson, P.R.: Shedding new light on opsin evolution. Proceedings of the Royal Society B: Biological Sciences (2011). Rspb.2011.1819 Porter, M.L., Blasic, J.R., Bok, M.J., Cameron, E.G., Pringle, T., Cronin, T.W., Robinson, P.R.: Shedding new light on opsin evolution. Proceedings of the Royal Society B: Biological Sciences (2011). Rspb.2011.1819
30.
go back to reference Rao, C.V., Arkin, A.P.: Stochastic chemical kinetics and the quasi-steady-state assumption: Application to the Gillespie algorithm. Journal of Chemical Physics 118(11), 4999–5010 (2003)CrossRef Rao, C.V., Arkin, A.P.: Stochastic chemical kinetics and the quasi-steady-state assumption: Application to the Gillespie algorithm. Journal of Chemical Physics 118(11), 4999–5010 (2003)CrossRef
31.
go back to reference Reingruber, J., Pahlberg, J., Woodruff, M.L., Sampath, A.P., Fain, G.L., Holcman, D.: Detection of single photons by toad and mouse rods. Proceedings of the National Academy of Sciences 110(48), 19,378–19,383 (2013) Reingruber, J., Pahlberg, J., Woodruff, M.L., Sampath, A.P., Fain, G.L., Holcman, D.: Detection of single photons by toad and mouse rods. Proceedings of the National Academy of Sciences 110(48), 19,378–19,383 (2013)
32.
go back to reference Schmidt, T.M., Do, M.T.H., Dacey, D., Lucas, R., Hattar, S., Matynia, A.: Melanopsin-positive intrinsically photosensitive retinal ganglion cells: From form to function. Journal of Neuroscience 31(45), 16,094–16,101 (2011)CrossRef Schmidt, T.M., Do, M.T.H., Dacey, D., Lucas, R., Hattar, S., Matynia, A.: Melanopsin-positive intrinsically photosensitive retinal ganglion cells: From form to function. Journal of Neuroscience 31(45), 16,094–16,101 (2011)CrossRef
33.
go back to reference Shen, L., Caruso, G., Bisegna, P., Andreucci, D., Gurevich, V.V., Hamm, H.E., DiBenedetto, E.: Dynamics of mouse rod phototransduction and its sensitivity to variation of key parameters. IET Systems Biology 4(1), 12–32 (2010)CrossRef Shen, L., Caruso, G., Bisegna, P., Andreucci, D., Gurevich, V.V., Hamm, H.E., DiBenedetto, E.: Dynamics of mouse rod phototransduction and its sensitivity to variation of key parameters. IET Systems Biology 4(1), 12–32 (2010)CrossRef
34.
go back to reference Shieh, B.H., Zhu, M.Y.: Regulation of the TRP Ca2+ channel by INAD in Drosophila photoreceptors. Neuron 16(5), 991–998 (1996)CrossRef Shieh, B.H., Zhu, M.Y.: Regulation of the TRP Ca2+ channel by INAD in Drosophila photoreceptors. Neuron 16(5), 991–998 (1996)CrossRef
35.
go back to reference Vishnivetskiy, S.A., Raman, D., Wei, J., Kennedy, M.J., Hurley, J.B., Gurevich, V.V.: Regulation of arrestin binding by rhodopsin phosphorylation level. Journal of Biological Chemistry 282(44), 32,075–32,083 (2007)CrossRef Vishnivetskiy, S.A., Raman, D., Wei, J., Kennedy, M.J., Hurley, J.B., Gurevich, V.V.: Regulation of arrestin binding by rhodopsin phosphorylation level. Journal of Biological Chemistry 282(44), 32,075–32,083 (2007)CrossRef
36.
go back to reference Warren, E.J., Allen, C.N., Brown, R.L., Robinson, D.W.: Intrinsic light responses of retinal ganglion cells projecting to the circadian system. European Journal of Neuroscience 17(9), 1727–1735 (2003)CrossRef Warren, E.J., Allen, C.N., Brown, R.L., Robinson, D.W.: Intrinsic light responses of retinal ganglion cells projecting to the circadian system. European Journal of Neuroscience 17(9), 1727–1735 (2003)CrossRef
37.
go back to reference Wong, K.Y., Dunn, F.A., Berson, D.M.: Photoreceptor adaptation in intrinsically photosensitive retinal ganglion cells. Neuron 48(6), 1001–1010 (2005)CrossRef Wong, K.Y., Dunn, F.A., Berson, D.M.: Photoreceptor adaptation in intrinsically photosensitive retinal ganglion cells. Neuron 48(6), 1001–1010 (2005)CrossRef
38.
go back to reference Xue, T., Do, M.T.H., Riccio, A., Jiang, Z., Hsieh, J., Wang, H.C., Merbs, S.L., Welsbie, D.S., Yoshioka, T., Weissgerber, P., Stolz, S., Flockerzi, V., Freichel, M., Simon, M.I., Clapham, D.E., Yau, K.W.: Melanopsin signalling in mammalian iris and retina. Nature 479(7371), 67–73 (2011)CrossRef Xue, T., Do, M.T.H., Riccio, A., Jiang, Z., Hsieh, J., Wang, H.C., Merbs, S.L., Welsbie, D.S., Yoshioka, T., Weissgerber, P., Stolz, S., Flockerzi, V., Freichel, M., Simon, M.I., Clapham, D.E., Yau, K.W.: Melanopsin signalling in mammalian iris and retina. Nature 479(7371), 67–73 (2011)CrossRef
Metadata
Title
A Stochastic Model of the Melanopsin Phototransduction Cascade
Authors
R. Lane Brown
Erika Camacho
Evan G. Cameron
Christina Hamlet
Kathleen A. Hoffman
Hye-Won Kang
Phyllis R. Robinson
Katherine S. Williams
Glenn R. Wyrick
Copyright Year
2015
Publisher
Springer New York
DOI
https://doi.org/10.1007/978-1-4939-2782-1_8

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