A kinetic analysis of mouse rod and cone photoreceptor responses.
cone
mathematical model
photoreceptor
retina
rod
vision
Journal
The Journal of physiology
ISSN: 1469-7793
Titre abrégé: J Physiol
Pays: England
ID NLM: 0266262
Informations de publication
Date de publication:
09 2020
09 2020
Historique:
received:
03
01
2020
accepted:
08
06
2020
pubmed:
20
6
2020
medline:
16
2
2021
entrez:
20
6
2020
Statut:
ppublish
Résumé
Most vertebrate eyes have rods for dim-light vision and cones for brighter light and higher temporal sensitivity. Rods evolved from cone-like precursors through expression of different transduction genes or the same genes at different expression levels, but we do not know which molecular differences were most important. We approached this problem by analysing rod and cone responses with the same model but with different values for model parameters. We showed that, in addition to outer-segment volume, the most important differences between rods and cones are: (1) decreased transduction gain, reflecting smaller amplification in the G-protein cascade; (2) a faster rate of turnover of the second messenger cGMP in darkness; and (3) an accelerated rate of decay of the effector enzyme phosphodiesterase and perhaps also of activated visual pigment. We believe our analysis has identified the principal alterations during evolution responsible for the duplex retina. Most vertebrates have rod and cone photoreceptors, which differ in their sensitivity and response kinetics. We know that rods evolved from cone-like precursors through the expression of different transduction genes or the same genes at different levels, but we do not know which molecular differences were most important. We have approached this problem in mouse retina by analysing the kinetic differences between rod flash responses and recent voltage-clamp recordings of cone flash responses, using a model incorporating the principal features of photoreceptor transduction. We apply a novel method of analysis using the log-transform of the current, and we ask which of the model's dynamic parameters need be changed to transform the flash response of a rod into that of a cone. The most important changes are a decrease in the gain of the response, reflecting a reduction in amplification of the transduction cascade; an increase in the rate of turnover of cGMP in darkness; and an increase in the rate of decay of activated phosphodiesterase, with perhaps also an increase in the rate of decay of light-activated visual pigment. Although we cannot exclude other differences, and in particular alterations in the Ca
Identifiants
pubmed: 32557629
doi: 10.1113/JP279524
pmc: PMC7484371
mid: NIHMS1617265
doi:
Substances chimiques
Retinal Pigments
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
3747-3763Subventions
Organisme : NEI NIH HHS
ID : P30 EY000331
Pays : United States
Organisme : NEI NIH HHS
ID : R01 EY001844
Pays : United States
Informations de copyright
© 2020 The Authors. The Journal of Physiology © 2020 The Physiological Society.
Références
Vis Neurosci. 2005 Jul-Aug;22(4):417-36
pubmed: 16212700
J Biol Chem. 2013 Feb 22;288(8):5257-67
pubmed: 23288843
Proc Natl Acad Sci U S A. 2000 Dec 5;97(25):13913-8
pubmed: 11095744
J Gen Physiol. 2007 Jul;130(1):21-40
pubmed: 17591985
Open Biol. 2018 Aug;8(8):
pubmed: 30068566
J Physiol. 2010 Sep 1;588(Pt 17):3231-41
pubmed: 20603337
Neuron. 2002 May 30;34(5):773-85
pubmed: 12062023
J Neurosci. 2010 Dec 1;30(48):16232-40
pubmed: 21123569
Philos Trans R Soc Lond B Biol Sci. 2017 Apr 5;372(1717):
pubmed: 28193819
Proc Natl Acad Sci U S A. 2014 Feb 18;111(7):2752-7
pubmed: 24550304
Nature. 1986 May 1-7;321(6065):70-2
pubmed: 2422559
Elife. 2015 Jun 22;4:
pubmed: 26095697
J Biol Chem. 2015 Apr 3;290(14):9239-50
pubmed: 25673692
J Physiol. 1991 Feb;433:561-87
pubmed: 1841958
Curr Biol. 2015 Feb 16;25(4):484-7
pubmed: 25660538
Proc Natl Acad Sci U S A. 2001 Aug 14;98(17):9948-53
pubmed: 11493703
J Neurosci. 2003 Feb 15;23(4):1287-97
pubmed: 12598617
J Neurosci. 2015 Jun 17;35(24):9225-35
pubmed: 26085644
Biophys J. 1996 Nov;71(5):2553-72
pubmed: 8913594
J Physiol. 2015 Jun 15;593(12):2547-9
pubmed: 26095019
Biophys J. 2012 Apr 18;102(8):1775-84
pubmed: 22768933
J Physiol. 1990 Oct;429:451-81
pubmed: 1703573
J Gen Physiol. 2012 Jan;139(1):31-56
pubmed: 22200947
J Neurosci. 2013 Jul 17;33(29):11745-53
pubmed: 23864662
Vis Neurosci. 2017 Jan;34:E006
pubmed: 28965521
Nat Neurosci. 2008 May;11(5):565-71
pubmed: 18425122
J Gen Physiol. 2003 Oct;122(4):419-44
pubmed: 12975449
J Biol Chem. 2018 Oct 5;293(40):15332-15346
pubmed: 30126843
Bioinformatics. 2015 Nov 1;31(21):3558-60
pubmed: 26142188
Neuron. 2019 Jun 19;102(6):1172-1183.e5
pubmed: 31056353
Proc Natl Acad Sci U S A. 2009 Oct 20;106(42):17681-6
pubmed: 19815523
J Neurosci. 2011 Mar 9;31(10):3670-82
pubmed: 21389222
J Gen Physiol. 2005 Mar;125(3):287-304
pubmed: 15738050
Nat Commun. 2017 May 4;8(1):16
pubmed: 28473692
PLoS One. 2013 Sep 30;8(9):e74335
pubmed: 24098642
Prog Retin Eye Res. 2020 May;76:100823
pubmed: 31790748
J Neurosci. 2007 Sep 19;27(38):10084-93
pubmed: 17881515
Proc Natl Acad Sci U S A. 2013 Nov 26;110(48):19378-83
pubmed: 24214653
F1000Res. 2018 May 23;7:
pubmed: 29899971
PLoS One. 2019 Jul 25;14(7):e0219848
pubmed: 31344066
Bioinformatics. 2009 Aug 1;25(15):1923-9
pubmed: 19505944
Biochim Biophys Acta. 1993 Mar 1;1141(2-3):111-49
pubmed: 8382952
Annu Rev Neurosci. 1989;12:289-327
pubmed: 2467600
J Gen Physiol. 2006 Apr;127(4):359-74
pubmed: 16567464
J Neurosci. 2010 Jan 27;30(4):1213-20
pubmed: 20107049
Biophys J. 2008 Mar 15;94(6):1954-70
pubmed: 18065454
Neuron. 2012 Oct 18;76(2):370-82
pubmed: 23083739
Nature. 1985 Sep 5-11;317(6032):61-4
pubmed: 2993914
J Physiol. 2016 Oct 1;594(19):5415-26
pubmed: 27218707
Proc Natl Acad Sci U S A. 2009 Jul 14;106(28):11788-93
pubmed: 19556550
Proc Natl Acad Sci U S A. 1998 Apr 28;95(9):5351-6
pubmed: 9560279
J Neurosci. 2011 Jun 1;31(22):7991-8000
pubmed: 21632921
J Neurosci. 2006 Apr 26;26(17):4472-80
pubmed: 16641226
J Gen Physiol. 1999 Feb;113(2):267-77
pubmed: 9925824
Neuron. 2005 May 5;46(3):413-20
pubmed: 15882641
J Gen Physiol. 2019 Nov 4;151(11):1287-1299
pubmed: 31562185
Phys Rev E Stat Nonlin Soft Matter Phys. 2009 Mar;79(3 Pt 1):030904
pubmed: 19391893
J Neurosci. 2010 Mar 3;30(9):3450-7
pubmed: 20203204
J Gen Physiol. 1995 Sep;106(3):543-57
pubmed: 8786347
Biophys J. 2003 Sep;85(3):1358-76
pubmed: 12944255
Neuron. 2006 Aug 17;51(4):409-16
pubmed: 16908407
Curr Biol. 2010 Feb 9;20(3):R114-24
pubmed: 20144772