Dissecting the determinants of light sensitivity in amphioxus microvillar photoreceptors: Possible evolutionary implications for melanopsin signaling

Journal of Neuroscience

Volumn 32, Issue 50, 2012, Pages 17977-17987

  Ferrer, Camilo ^a   Malagón, Gerardo ^a   Gomez, María del Pilar ^a,b   Nasi, Enrico ^a,b  

^a UNIVERSIDAD NACIONAL DE COLOMBIA   (Colombia)

^b MARINE BIOLOGICAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEGLUMINE; MELANOPSIN;

ANIMAL CELL; ARTICLE; BRANCHIOSTOMA; CONDUCTANCE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; FEMALE; ISOMERIZATION; LIGHT DARK CYCLE; LIGHT EMITTING DIODE; LIGHT INTENSITY; MALE; MICROVILLAR PHOTORECEPTOR; NONHUMAN; PHOTORECEPTOR; PHOTOSENSITIVITY; PHOTOSTIMULATION; PHOTOTRANSDUCTION; PRIORITY JOURNAL; SIGNAL NOISE RATIO; SIGNAL TRANSDUCTION;

ANIMALS; BIOLOGICAL EVOLUTION; CHORDATA, NONVERTEBRATE; FEMALE; LIGHT SIGNAL TRANSDUCTION; MALE; PATCH-CLAMP TECHNIQUES; PHOTIC STIMULATION; PHOTORECEPTOR CELLS; ROD OPSINS;

EID: 84870994746     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3069-12.2012     Document Type: Article

References (45)

1. Angueyra JM, Pulido C, Malagón G, Nasi E, Gomez MP(2012) Melanopsinexpressing amphioxus hotoreceptors transduce light via a phospholipase C signaling cascade. PLoS One 7:e29813. CrossRef Medline
2. Arendt D (2003) Evolution of eyes and photoreceptor cell types. Int J Dev Biol 47:563-571. Medline
3. Arendt D, Tessmar K, de Campos-Baptista MI, Dorresteijn A, Wittbrodt J (2002) Development of pigment-cup eyes in the polychaete Platynereis dumerilii and evolutionary conservation of larval eyes in Bilateria. Development 129:1143-1154. Medline
4. Bacigalupo J, Lisman JE (1983) Single channel currents activated by light in Limulus ventral photoreceptors. Nature 304:268-270. CrossRef Medline
5. Baylor DA, Lamb TD, Yau KW (1979) Responses of retinal rods to single photons. J Physiol 288:613-634. Medline
6. Berson DM (2003) Strange vision: ganglion cells as circadian photoreceptors. Trends Neurosci 26:314-320. CrossRef Medline
7. Berson DM, Dunn FA, Takao M (2002) Phototransduction by retinal ganglion cells that set the circadian clock. Science 295:1070-1073. CrossRef Medline
8. Brown JE, Coles JA (1979) Saturation of the response to light in Limulus ventral photoreceptor. J Physiol 296:373-392. Medline
9. Cone RA (1967) Early receptor potential: photoreversible charge displacement in rhodopsin. Science 155:1128-1131. CrossRef Medline
10. Do MT, Kang SH, Xue T, Zhong H, Liao HW, Bergles DE, Yau KW (2009) Photon capture and signalling by melanopsin retinal ganglion cells. Nature 457:281-287. CrossRef Medline
11. Eakin RM, Westfall JA (1962) Fine structure of photoreceptors in Amphioxus. J Ultra Res 6:531-539. CrossRef Medline
12. Ertel EA (1990) Excised patches of plasma membrane from vertebrate rod outer segments retain a functional phototransduction enzymatic cascade. Proc Natl Acad Sci U S A 87:4226-4230. CrossRef Medline
13. Fuortes MG, Yeandle S (1964) Probability of occurrence of discrete potential waves in the eye of Limulus. J Gen Physiol 47:443-463. CrossRef Medline
14. Gomez MP, Nasi E (1994) The light-sensitive conductance of hyperpolarizing invertebrate photoreceptors: a patch-clamp study. J Gen Physiol 103: 939-956. CrossRef Medline
15. Gomez MP, Nasi E (1997) Light adaptation in Pecten hyperpolarizing photoreceptors: insensitivity to Ca manipulations. J Gen Physiol 109:371-384. CrossRef Medline
16. del Gomez M P, Angueyra JM, Nasi E (2009) Light-transduction in melanopsin-expressing photoreceptors of Amphioxus. Proc Natl Acad Sci U S A 106:9081-9086. CrossRef Medline
17. Graham DM, Wong KY, Shapiro P, Frederick C, Pattabiraman K, Berson DM (2008) Melanopsin ganglion cells use a membrane associated rhabdomeric phototransduction cascade. J Neurophysiol 99:2522-2532. CrossRef Medline
18. Hardie RC (1991) Whole-cell recordings of the light induced current in dissociated Drosophila photoreceptors: evidence for feedback by calcium permeating the light-sensitive channels. Proc R Soc Lond B 245:203-210. CrossRef
19. 2+. J Physiol 524:179-194. CrossRef Medline
20. Hestrin S, Korenbrot JI (1990) Activation kinetics of retinal cones and rods: response to intense flashes of light. J Neurosci 10:1967-1973. Medline
21. Hochstrate P, Lindau M, Rüppel H (1982) On the origin and the signalshaping mechanism of the fast photosignal in the vertebrate retina. Biophys J 38:53-61. CrossRef Medline
22. Hodgkin AL, O'Bryan PM (1977) Internal recording of the early receptor potential in turtle cones. J Physiol 267:737-766. Medline
23. Kirkwood A, Lisman JE (1994) Determinants of single photon response variability. J Gen Physiol 103:679-690. CrossRef Medline
24. Koyanagi M, Terakita A (2008) Gq-coupled rhodopsin subfamily composed of invertebrate visual pigment and melanopsin. Photochem Photobiol 84:1024-1030. CrossRef Medline
25. Koyanagi M, Kubokawa K, Tsukamoto H, Shichida Y, Terakita A (2005) Cephalochordate melanopsin: evolutionary linkage between invertebrate visual cells and vertebrate photosensitive retinal ganglion cells. Curr Biol 15:1065-1069. CrossRef Medline
26. Laughlin SB, Weckström M (1993) Fast and slow photoreceptors-a comparative study of the functional diversity of coding and conductances in the Diptera. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 172:593-609. CrossRef
27. Lisman JE, Bering H (1977) Electrophysiological measurement of the number of rhodopsin molecules in single Limulus photoreceptors. J Gen Physiol 70:621-633. CrossRef Medline
28. Lyubarsky AL, Daniele LL, Pugh EN Jr (2004) From candelas to photoisomerizations in the mouse eye by rhodopsin bleaching in situ and the light-rearing dependence of the major components of the mouse ERG. Vis Res 44:3235-3251. CrossRef Medline
29. Makino CL, Taylor WR, Baylor DA (1991) Rapid charge movements and photosensitivity of visual pigments in salamander rods and cones. J Physiol 442:761-780. Medline
30. Nagy K, Stieve H (1990) Light activated single channels currents in Limulus ventral nerve photoreceptors. Eur Biophys J 18:221-224.
31. Nakao T (1964) On the fine structure of the amphioxus photoreceptor. Tohoku J Exp Med 82:349-363. CrossRef Medline
32. Nasi E (1991a) Electrophysiological properties of isolated photoreceptors from the eye of Lima scabra. J Gen Physiol 97:17-34. CrossRef Medline
33. Nasi E (1991b) Two light-dependent conductances in the membrane of Lima photoreceptor cells. J Gen Physiol 97:55-72. CrossRef Medline
34. Nasi E, Gomez MP (1992) Light-activated ion channels in solitary photoreceptors from the eye of the scallop Pecten irradians. J Gen Physiol 99:747-769. CrossRef Medline
35. Nasi E, Gomez MP (2009) Melanopsin-mediated light-sensing in amphioxus: a glimpse of the microvillar photoreceptor lineage within the deuterostomia. Commun Integr Biol 2:441-443. CrossRef
36. Peirson S, Foster RG (2006) Melanopsin: another way of signaling light. Neuron 49:331-339. CrossRef Medline
37. Provencio I, Jiang G, De Grip WJ, Hayes WP, Rollag MD (1998) Melanopsin: an opsin in melanophores, brain and eye. Proc Natl Acad Sci U S A 95:340-345. CrossRef Medline
38. Pulido C, Malagón G, Ferrer C, Chen JK, Angueyra JM, Nasi E, Gomez Mdel P (2012) The light-sensitive conductance of melanopsin-expressing Joseph and Hesse cells in amphioxus. J Gen Physiol 139:19-30. CrossRef Medline
39. Putnam NH, Butts T, Ferrier DE, Furlong RF, Hellsten U, Kawashima T, Robinson-Rechavi M, Shoguchi E, Terry A, Yu JK, Benito-Gutiérrez EL, Dubchak I, Garcia-Fernàndez J, Gibson-Brown JJ, Grigoriev IV, Horton AC, de Jong PJ, Jurka J, Kapitonov VV, Kohara Y, Kuroki Y, et al. (2008) The amphioxus genome and the evolution of chordate karyotype. Nature 453:1064-1072. CrossRef Medline
40. Ruiz MS, Anadon R (1991) Some considerations on the fine structure of rhabdomeric photoreceptors in the amphioxus, Branchiostoma lanceolatum (Cephalochordata). J Hirnforsch 32:159-164. Medline
41. Schubert M, Escriva H, Xavier-Neto J, Laudet V (2006) Amphioxus and tunicates as evolutionary model systems. Trends Ecol Evol 21:269-277. CrossRef Medline
42. Sokabe M, Sachs F, Jing ZQ (1991) Quantitative video microscopy of patch clamped membranes: stress, strain, capacitance, and stretch channel activation. Biophys J 59:722-728. CrossRef Medline
43. Terakita A (2005) The opsins. Genome Biol 6:213. CrossRef Medline
44. Watanabe S, Matthews G (1988) Regional distribution of cGMP-activated ion channels in the plasma membrane of the rod photoreceptor. J Neurosci 8:2334-2337. Medline
45. Wong F, Knight BW, Dodge FA (1980) Dispersion of latencies in photoreceptors of Limulus and the adapting-bump model. J Gen Physiol 76:517-537. CrossRef Medline